Animal models of skin disease for drug discovery

Avci, Pinar; Sadasivam, Magesh; Gupta, Asheesh; De Melo, Wanessa CMA; Huang, Ying-Ying; Yin, Rui; Chandran, Rakkiyappan; Kumar, Raj; Otufowora, Ayodeji; Nyame, Theodore; Hamblin, Michael R

doi:10.1517/17460441.2013.761202

Cited by 130Dermatology and Skin DiseasesAdvancements in Transdermal Drug DeliveryHair Growth and Disorders

Animal models of skin disease for drug discovery

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Avci, Pinar, Sadasivam, Magesh, Gupta, Asheesh, De Melo, Wanessa CMA, Huang, Ying-Ying, Yin, Rui, Chandran, Rakkiyappan, Kumar, Raj +3 more·2013·Expert Opinion on Drug Discovery

DOI 10.1517/17460441.2013.761202PMC PMC3580014

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Abstract

INTRODUCTION: Discovery of novel drugs, treatments, and testing of consumer products in the field of dermatology is a multi-billion dollar business. Due to the distressing nature of many dermatological diseases, and the enormous consumer demand for products to reverse the effects of skin photodamage, aging, and hair loss, this is a very active field. AREAS COVERED: In this paper, we will cover the use of animal models that have been reported to recapitulate to a greater or lesser extent the features of human dermatological disease. There has been a remarkable increase in the number and variety of transgenic mouse models in recent years, and the basic strategy for constructing them is outlined. EXPERT OPINION: Inflammatory and autoimmune skin diseases are all represented by a range of mouse models both transgenic and normal. Skin cancer is mainly studied in mice and fish. Wound healing is studied in a wider range of animal species, and skin infections such as acne and leprosy also have been studied in animal models. Moving to the more consumer-oriented area of dermatology, there are models for studying the harmful effect of sunlight on the skin, and testing of sunscreens, and several different animal models of hair loss or alopecia.

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Animal models remain constrained by interspecies differences in cytokine networks, immune repertoires and epidermal structure, thereby limiting translational relevance.
“Animal models, though valuable for systemic analyses, remain constrained by interspecies differences in cytokine networks, immune repertoires and epidermal structure, thereby limiting translational relevance 10 .”
From Vascularized human skin assembloids model compartmental skin organization and immune responsiveness in vitro (2026) · cites this paper as [10]

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Background
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Background
Pathogenesis of Foreign Body Infection: Description and Characteristics of an Animal Model
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Method
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Background
Psoriasis-like skin disease and arthritis caused by inducible epidermal deletion of Jun proteins
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Background
From keratinocyte to cancer: the pathogenesis and modeling of cutaneous squamous cell carcinoma
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BackgroundInfluential
New perspectives on epidermal barrier dysfunction in atopic dermatitis: Gene–environment interactions
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Method
Skin Permeability In Vivo: Comparison in Rat, Rabbit, Pig and Man
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Background
Animal Models of Atopic Dermatitis
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Background
TNF-mediated inflammatory skin disease in mice with epidermis-specific deletion of IKK2
Pasparakis, M., Courtois, G., Hafner, M., Schmidt‐Supprian, M., Nenci, A., Toksoy, A., Krampert, M., Goebeler, M., Gillitzer, R., Israël, A., et al. (2002) · Nature · doi:10.1038/nature00820 · Cited by 471 · cited 1× · see citing works
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Background
Simian Virus 40 DNA Sequences in DNA of Healthy Adult Mice Derived from Preimplantation Blastocysts Injected with Viral DNA
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Background
Site- and Time-Specific Gene Targeting in the Mouse
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Method
Targeted Disruption of the Pemphigus Vulgaris Antigen (Desmoglein 3) Gene in Mice Causes Loss of Keratinocyte Cell Adhesion with a Phenotype Similar to Pemphigus Vulgaris
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Background
Transgenic mice provide new insights into the role of TGF-alpha during epidermal development and differentiation.Preprint
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“These include the transgenic and knockout models, such as human leukocyte antigen B27 (HLA-B27) transgenic rats [74], CD18 hypomorphic mice [75], K14/VEGF and Tie2 mice [76,77], K14/TGF-a, K5/TGF-b1, K14/KGF and K14/IL-20 transgenic mice [78-80], IKK2 [81] and JunB/c-Jun transgenic mice [82], K5.”
Background
Overproduction of Th2-specific chemokines in NC/Nga mice exhibiting atopic dermatitis–like lesions
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Background
Sunlight and skin cancer: another link revealed
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“Excessive exposure to solar UVR causes severe acute damages to the skin, which include erythema, sunburn, immunosuppressant, and also long-term effects such as photoaging and skin cancer [150-154].”
Background
Sunlight and sunburn in human skin cancer: p53, apoptosis, and tumor promotion.
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Background
Human Molecular Genetics
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Murine Models of Systemic Lupus Erythematosus
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“Themain examples of SLE-pronemice areNewZealand Black (NZB), F1 hybrids of NZB New Zealand White (NZW) (B/W F1), MRL/Mp-lpr/lpr, and BXSB mice (Table 1) [100-102].”
BackgroundInfluential
Transgenic delivery of VEGF to mouse skin leads to an inflammatory condition resembling human psoriasis
Xia, Y.-P., Li, B., Hylton, D., Detmar, M., Yancopoulos, G. D., & Rudge, J. S. (2003) · Blood · doi:10.1182/blood-2002-12-3793 · Cited by 367 · cited 1× · see citing works
“These include the transgenic and knockout models, such as human leukocyte antigen B27 (HLA-B27) transgenic rats [74], CD18 hypomorphic mice [75], K14/VEGF and Tie2 mice [76,77], K14/TGF-a, K5/TGF-b1, K14/KGF and K14/IL-20 transgenic mice [78-80], IKK2 [81] and JunB/c-Jun transgenic mice [82], K5.”
Background
“Outside-to-Inside” (and Now Back to “Outside”) Pathogenic Mechanisms in Atopic Dermatitis
Elias, P. M., & Steinhoff, M. S. (2008) · Journal of Investigative Dermatology · doi:10.1038/jid.2008.88 · Cited by 344 · see citing works
Humanization of autoantigen
Nishie, W., Sawamura, D., Goto, M., Ito, K., Shibaki, A., McMillan, J. R., Sakai, K., Nakamura, H., Olasz, E. B., Yancey, K. B., et al. (2007) · Nature Medicine · doi:10.1038/nm1496 · Cited by 316 · see citing works
Induction of cutaneous delayed-type hypersensitivity reactions in VEGF-A transgenic mice results in chronic skin inflammation associated with persistent lymphatic hyperplasia
Kunstfeld, R., Hirakawa, S., Hong, Y.-K., Schacht, V., Lange‐Asschenfeldt, B., Velasco, P., Lin, C. P., Fiebiger, E., Wei, X., Wu, Y. L., et al. (2004) · Blood · doi:10.1182/blood-2003-08-2964 · Cited by 309 · cited 1× · see citing works
“These include the transgenic and knockout models, such as human leukocyte antigen B27 (HLA-B27) transgenic rats [74], CD18 hypomorphic mice [75], K14/VEGF and Tie2 mice [76,77], K14/TGF-a, K5/TGF-b1, K14/KGF and K14/IL-20 transgenic mice [78-80], IKK2 [81] and JunB/c-Jun transgenic mice [82], K5.”
Background
Expression of Interleukin-4 in the Epidermis of Transgenic Mice Results in a Pruritic Inflammatory Skin Disease: An Experimental Animal Model to Study Atopic Dermatitis
Chan, L. S., Robinson, N. D., & Xu, L. (2001) · Journal of Investigative Dermatology · doi:10.1046/j.0022-202x.2001.01484.x · Cited by 306 · cited 1× · see citing works
“4 IL-4 transgenic mice Transgenic mice overexpressing IL-4 in the skin develop spontaneous pruritus and chronic dermatitis at the age of 4 months [61].”
Background
How atopic is atopic dermatitis?
Flohr, C., Johansson, S. G. O., Wahlgren, C., & Williams, H. C. (2004) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2004.04.027 · Cited by 296 · cited 1× · see citing works
“in AD might be related to epidermal barrier dysfunction and the introduction of environmental antigens, rather than intrinsic immune hypersensitivity [46,47].”
Background
Animal model of human disease.
Lofland, H. B. (1975) · PubMed · Cited by 289 · see citing works
Scleroderma: from cell and molecular mechanisms to disease models
Abraham, D., & Varga, J. (2005) · Trends in Immunology · doi:10.1016/j.it.2005.09.004 · Cited by 282 · cited 2× · see citing works
“Animal models of SSc can be divided into three groups (Table 2) [105,106].”
Background
Tamoxifen-inducible glia-specific Cre mice for somatic mutagenesis in oligodendrocytes and Schwann cells
Leone, D. P., Genoud, S., Atanasoski, S., Grausenburger, R., Berger, P., METZGER, D., Macklin, W. B., Chambon, P., & Suter, U. (2003) · Molecular and Cellular Neuroscience · doi:10.1016/s1044-7431(03)00029-0 · Cited by 270 · cited 1× · see citing works
“Controlled gene expression in mouse models is studied based on the tamoxifen-inducible Cre recombinase system [33,34], Cre-loxP and the tetracycline (Tet)-inducible systems [35], and tet-operon/repressor bi-transgenic system, the estrogen receptor (ER) ligand-binding domain, the cell-specific activation and inactivati…”
Method
Targeting expression of keratinocyte growth factor to keratinocytes elicits striking changes in epithelial differentiation in transgenic mice.
Guo, L., Yu, Q. C., & Fuchs, E. V. (1993) · The EMBO Journal · doi:10.1002/j.1460-2075.1993.tb05738.x · Cited by 268 · cited 1× · see citing works
“These include the transgenic and knockout models, such as human leukocyte antigen B27 (HLA-B27) transgenic rats [74], CD18 hypomorphic mice [75], K14/VEGF and Tie2 mice [76,77], K14/TGF-a, K5/TGF-b1, K14/KGF and K14/IL-20 transgenic mice [78-80], IKK2 [81] and JunB/c-Jun transgenic mice [82], K5.”
Background
IL-18 contributes to the spontaneous development of atopic dermatitis-like inflammatory skin lesion independently of IgE/stat6 under specific pathogen-free conditions
Konishi, H., Tsutsui, H., Murakami, T., Futatsugi‐Yumikura, S., Yamanaka, K.-I., Tanaka, M., Iwakura, Y., 昇, 鈴., Takeda, K., Akira, S., et al. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.152337799 · Cited by 268 · cited 1× · see citing works
“IL-1b-deficient CASP1 and IL-18 transgenic mice exhibited similar dermatitis [66].”
Background
Photocarcinogenesis: an overview
Black, H. S., deGruijl, F. R., Forbes, P. D., Cleaver, J. E., Ananthaswamy, H. N., DeFabo, E. C., Ullrich, S. E., & Tyrrell, R. M. (1997) · Journal of Photochemistry and Photobiology B Biology · doi:10.1016/s1011-1344(97)00021-3 · Cited by 258 · see citing works
Autoimmune hair loss (alopecia areata) transferred by T lymphocytes to human scalp explants on SCID mice.
Gilhar, A., Ullmann, Y., Berkutzki, T., Assy, B., & Kalish, R. S. (1998) · Journal of Clinical Investigation · doi:10.1172/jci551 · Cited by 254 · cited 2× · see citing works
“These workers transplanted samples of involved scalp tissue from AA patients into subcutaneous tissue of SCID mice and the graft tissue was then injected with autologous T lymphocytes which had been isolated from affected scalp [175].”
Method
Filaggrin-deficient mice exhibit TH17-dominated skin inflammation and permissiveness to epicutaneous sensitization with protein antigen
Oyoshi, M. K., Murphy, G. F., & Geha, R. S. (2009) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2009.05.042 · Cited by 245 · cited 1× · see citing works
“These findings indicated that flaky tail mice demonstrate Th17-dominated skin inflammation and eczematous dermatitis with advancing age change [56].”
Background
Psoriasis genetics: breaking the barrier
Roberson, E. D. O., & Bowcock, A. M. (2010) · Trends in Genetics · doi:10.1016/j.tig.2010.06.006 · Cited by 240 · cited 7× · see citing works
“infection and dehydration (Figure 5) [69].”
BackgroundInfluential
Fifty years of skin aging
Yaar, M., Eller, M. S., & Gilchrest, B. A. (2002) · Journal of Investigative Dermatology Symposium Proceedings · doi:10.1046/j.1523-1747.2002.19636.x · Cited by 233 · cited 1× · see citing works
“Although both photoaging and chronological aging are associated with wrinkles, photoaging-induced wrinkles are regarded as deeper and more coarse, whereas those associated with chronological aging are generally more superficial and delicate [156].”
Background
Andrews' Diseases of the Skin: Clinical Dermatology
Wechsler, H. L. (1982) · Archives of Dermatology · doi:10.1001/archderm.1982.01650180082029 · Cited by 231 · see citing works
Interleukin 6: insights to its function in skin by overexpression in transgenic mice.
Turksen, K., Kupper, T. S., Degenstein, L., Williams, I. R., & Fuchs, E. V. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.11.5068 · Cited by 225 · cited 1× · see citing works
“Stat3C mice [83], and K14/IL-6 and K14/IL-1atransgenic mice [84].”
Background
The filaggrin story: novel insights into skin-barrier function and disease
McGrath, J. A., & Uitto, J. (2007) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2007.10.006 · Cited by 224 · cited 1× · see citing works
“Unlike the common belief that was widely accepted for a very long time, there is now little support for the view that AD is the result of allergies [43,44].”
Background
Latent TGFβ1 overexpression in keratinocytes results in a severe psoriasis‐like skin disorder
Li, A. G., Wang, D., Feng, X., & Wang, X. (2004) · The EMBO Journal · doi:10.1038/sj.emboj.7600183 · Cited by 224 · cited 1× · see citing works
“These include the transgenic and knockout models, such as human leukocyte antigen B27 (HLA-B27) transgenic rats [74], CD18 hypomorphic mice [75], K14/VEGF and Tie2 mice [76,77], K14/TGF-a, K5/TGF-b1, K14/KGF and K14/IL-20 transgenic mice [78-80], IKK2 [81] and JunB/c-Jun transgenic mice [82], K5.”
Background
A hypomorphic mouse model of dystrophic epidermolysis bullosa reveals mechanisms of disease and response to fibroblast therapy
Fritsch, A., Loeckermann, S., Kern, J. S., Braun, A., Bösl, M. R., Bley, T. A., Schumann, H., von Elverfeldt, D., Paul, D., Erlacher, M., et al. (2008) · Journal of Clinical Investigation · doi:10.1172/jci34292 · Cited by 220 · cited 1× · see citing works
“It has been used as a mouse model for generalized non-Herlitz junctional epidermolysis bullosa (JEB) [23] and generalized non-Herlitz JEB to find out the response to fibroblast therapy [24].”
Method
Photodynamic therapy for methicillin‐resistant Staphylococcus aureus infection in a mouse skin abrasion model
Dai, T., Tegos, G. P., Zhiyentayev, T., Mylonakis, E. E., & Hamblin, M. R. (2010) · Lasers in Surgery and Medicine · doi:10.1002/lsm.20887 · Cited by 208 · cited 2× · see citing works
“aureus infection in a partial-thickness skin abrasion [130] and Acinetobacter baumanii infection in a third-degree burn [131].”
BackgroundSelf-citation
Models for use in wound healing research: A survey focusing on in vitro and in vivo adult soft tissue
Gottrup, F., Ågren, M. S., & Karlsmark, T. (2000) · Wound Repair and Regeneration · doi:10.1046/j.1524-475x.2000.00083.x · Cited by 199 · cited 3× · see citing works
“Recently, efficacy of different novel pharmacotherapeutic agents and tissue-engineered wound dressings have been evaluated for augmenting nonhealing diabetic and burn wounds [118].”
BackgroundMethodInfluential
Role of Mitochondria in Photoaging of Human Skin: The Defective Powerhouse Model
Krutmann, J., & Schröeder, P. (2009) · Journal of Investigative Dermatology Symposium Proceedings · doi:10.1038/jidsymp.2009.1 · Cited by 198 · cited 1× · see citing works
“Solar-induced damage to mitochondria in skin fibroblasts is proposed to be one of the key factors in premature photoaging of human skin, and the defective powerhouse model (mtDNA mutator mice) has been used in order to demonstrate this phenomenon [161].”
Method
Fitzpatrick's Color Atlas & Synopsis of Clinical Dermatology
Wolff, K. D., & Johnson, R. A. (2005) · Medical Entomology and Zoology · Cited by 196 · see citing works
DC ablation in mice: promises, pitfalls, and challenges
Bennett, C. L., & Clausen, B. E. (2007) · Trends in Immunology · doi:10.1016/j.it.2007.08.011 · Cited by 181 · cited 1× · see citing works
“An example of the former is the diphtheria toxin receptor [39], and an example of the later is viral TK that can produce a lethal toxin from gancyclovir [40].”
Background
Wound healing in adult skin: aiming for perfect regeneration
Heng, M. C. Y. (2011) · International Journal of Dermatology · doi:10.1111/j.1365-4632.2011.04940.x · Cited by 180 · cited 1× · see citing works
“targets in the form of novel pharmaceutical molecules, which markedly improve or completely prevent scarring during adult wound healing in experimental animals [126,127].”
Background
Epidermal Overexpression of Stratum Corneum Chymotryptic Enzyme in Mice: A Model for Chronic Itchy Dermatitis
Bäckman, A., Ny, A., Edlund, M., Ekholm, E., Hammarström, B., Törnell, J., Wallbrandt, P., Egelrud, T., Hansson, L., & Wennbo, H. (2002) · Journal of Investigative Dermatology · doi:10.1046/j.0022-202x.2001.01684.x · Cited by 180 · cited 2× · see citing works
“6 SC chymotryptic enzyme transgenic mice Overexpression of a human SC chymotryptic enzyme transgene in suprabasal epidermal keratinocytes of mice led to the development of AD-like skin starting at the age of 7 -- 8 weeks or older [63].”
Background
Non-germline genetically engineered mouse models for translational cancer research
Heyer, J., Kwong, L. N., Lowe, S. W., & Chin, L. (2010) · Nature reviews. Cancer · doi:10.1038/nrc2877 · Cited by 179 · cited 1× · see citing works
“In this approach, a tissue-specific promoter is used to direct expression of one of the site-specific recombinases to limit gene inactivation to only those cells expressing the recombinase [31].”
Background
A spontaneous mutation characterized by chronic proliferative dermatitis in C57BL mice.
HogenEsch, H., Gijbels, M. J., Offerman, E. H., van der Hooft, J. J. J., van Bekkum, D. W., & ZURCHER, C. (1993) · PubMed Central · Cited by 176 · see citing works
Animal models of external traumatic wound infections
Dai, T., Kharkwal, G. B., Tanaka, M., Huang, Y., de Arce, V. J. B., & Hamblin, M. R. (2011) · Virulence · doi:10.4161/viru.2.4.16840 · Cited by 176 · cited 2× · see citing works
“6 External traumatic wound infection models The external traumatic wound has been studied with experimental infections in animal models of surgical site wounds, burns, skin abrasions, lacerations, excisional wounds, and open fractures [128].”
BackgroundSelf-citation
Making waves in cancer research: new models in the zebrafish.
Berghmans, S., Jette, C. A., Langenau, D. M., Hsu, K., Stewart, R., Look, T., & Kanki, J. P. (2005) · BioTechniques · doi:10.2144/05392rv02 · Cited by 170 · cited 4× · see citing works
“Each female is capable of laying 200 -- 300 eggs per week, external fertilization allows manipulation of embryos ex utero, and rapid development of optically clear embryos allows the direct observation of developing internal organs and tissues in vivo [113].”
BackgroundInfluential
Amelioration of epidermolysis bullosa by transfer of wild-type bone marrow cells
Tolar, J., Ishida‐Yamamoto, A., Riddle, M. J., McElmurry, R. T., Osborn, M. J., Xia, L., Lund, T. C., Slattery, C., Uitto, J., Christiano, A. M., et al. (2008) · Blood · doi:10.1182/blood-2008-06-161299 · Cited by 168 · cited 1× · see citing works
“The collagen VII knockout mouse has been used for pilot studies of protein replacement- and cell-based treatments [93], but the short life span of the mouse has prevented long-term follow-up and limited the interpretation of results [94-96].”
Method
Chemotherapy-induced alopecia in mice. Induction by cyclophosphamide, inhibition by cyclosporine A, and modulation by dexamethasone.
Paus, R., Handjiski, B., Eichmüller, S. B., & Czarnetzki, B. M. (1994) · PubMed Central · Cited by 168 · see citing works
Molecular Biology of Aging
Balcells, F. S. (1986) · Journal of Gerontology · doi:10.1093/geronj/41.5.685b · Cited by 167 · see citing works
Targeted inactivation of the type VII collagen gene (Col7a1) in mice results in severe blistering phenotype: a model for recessive dystrophic epidermolysis bullosa
Heinonen, S. T., Männikkö, M., Klement, J. F., et al. (1999) · Journal of Cell Science · doi:10.1242/jcs.112.21.3641 · Cited by 159 · see citing works
Transgenic Animal Technology: A Laboratory Handbook
Pinkert, C. A. (2014) · doi:10.1016/b978-0-12-410490-7.00026-8 · Cited by 158 · see citing works
Desmoglein 3 anchors telogen hair in the follicle
Koch, P. J., Mahoney, M. G., Cotsarelis, G., Rothenberger, K., Lavker, R. M., & Stanley, J. R. (1998) · Journal of Cell Science · doi:10.1242/jcs.111.17.2529 · Cited by 156 · see citing works
Sonic hedgehog signaling in basal cell carcinomas
Daya–Grosjean, L., & Couvé, S. (2004) · Cancer Letters · doi:10.1016/j.canlet.2004.10.003 · Cited by 153 · cited 8× · see citing works
“Targeted inactivation of the Shh, Ptch, Smo, and Gli genes, which are all involved in sonic hedgehog signaling (SHH) pathway, has enabled important insights into BCC development, proliferation, and oncogenesis [115].”
BackgroundInfluential
Molecular mechanisms of photocarcinogenesis
Matsumura, Y. (2002) · Frontiers in bioscience · doi:10.2741/matsumur · Cited by 143 · cited 1× · see citing works
“Excessive exposure to solar UVR causes severe acute damages to the skin, which include erythema, sunburn, immunosuppressant, and also long-term effects such as photoaging and skin cancer [150-154].”
Background
Injection of Recombinant Human Type VII Collagen Corrects the Disease Phenotype in a Murine Model of Dystrophic Epidermolysis Bullosa
Remington, J., Wang, X., Hou, Y., Zhou, H., Burnett, J., Muirhead, T., Uitto, J., Keene, D. R., Woodley, D. T., & Chen, M. (2008) · Molecular Therapy · doi:10.1038/mt.2008.234 · Cited by 143 · cited 1× · see citing works
“The collagen VII knockout mouse has been used for pilot studies of protein replacement- and cell-based treatments [93], but the short life span of the mouse has prevented long-term follow-up and limited the interpretation of results [94-96].”
Method
Photodynamic Therapy for Acinetobacter baumannii Burn Infections in Mice
Dai, T., Tegos, G. P., Lu, Z., Huang, L., Zhiyentayev, T., Franklin, M. J., Baer, D. G., & Hamblin, M. R. (2009) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.00027-09 · Cited by 141 · cited 1× · see citing works
“aureus infection in a partial-thickness skin abrasion [130] and Acinetobacter baumanii infection in a third-degree burn [131].”
BackgroundSelf-citation
Prevention of Ultraviolet-B Radiation Damage by Resveratrol in Mouse Skin Is Mediated via Modulation in Survivin¶
Aziz, M. H., Afaq, F., & Ahmad, N. (2004) · Photochemistry and Photobiology · doi:10.1562/2004-08-13-ra-274.1 · Cited by 139 · see citing works
Adenoviral mediated gene transfer of PDGF‐B enhances wound healing in type I and type II diabetic wounds
Keswani, S. G., Katz, A. B., Lim, F. Y., Zoltick, P. W., Radu, A. P., Alaee, D., Herlyn, M., & Crombleholme, T. M. (2004) · Wound Repair and Regeneration · doi:10.1111/j.1067-1927.2004.12501.x · Cited by 136 · cited 1× · see citing works
“, the leptin receptor defect, the streptozotocin, or the immunologic defect of the NOD mouse [134].”
Background
Skin-Specific Caspase-1-Transgenic Mice Show Cutaneous Apoptosis and Pre-Endotoxin Shock Condition with a High Serum Level of IL-18
Yamanaka, K., Tanaka, M., Tsutsui, H., Kupper, T. S., Asahi, K., Okamura, H., Nakanishi, K., Suzuki, M., Kayagaki, N., Black, R. A., et al. (2000) · The Journal of Immunology · doi:10.4049/jimmunol.165.2.997 · Cited by 135 · see citing works
Glucocorticoids drive human CD8+ T cell differentiation towards a phenotype with high IL-10 and reduced IL-4, IL-5 and IL-13 production
Richards, D. F., Fernandez, M., Caulfield, J., & Hawrylowicz, C. M. (2000) · European Journal of Immunology · doi:10.1002/1521-4141(2000)30:8 · Cited by 133 · see citing works
Epicutaneous sensitization with superantigen induces allergic skin inflammation
Laouini, D., Kawamoto, S., Yalçindağ, A., et al. (2003) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2003.07.007 · Cited by 131 · cited 1× · see citing works
“Application of SEB instead of OVA by repeated EC sensitization to tapestripped skin was able to elicit Th2-dominated allergic skin inflammation accompanied by a systemic Th2 response to the superantigen [53].”
Background
Andrews' Diseases of the Skin
James, W. D., Berger, T. G., & Elston, D. M. (2015) · Cited by 128 · see citing works
Protection Against Chemotherapy-Induced Alopecia
Wang, J., Lu, Z., & Au, J. L. ‐. (2006) · Pharmaceutical Research · doi:10.1007/s11095-006-9105-3 · Cited by 122 · cited 7× · see citing works
“In wave pattern, the entry of hair follicles begins from the head and moves toward the tail, which is a pattern seen in neonatal rats and hair loss in CIA [182].”
BackgroundMethodInfluential
Filaggrin's Fuller Figure: A Glimpse into the Genetic Architecture of Atopic Dermatitis
Sandilands, A., Smith, F. J. D., Irvine, A. D., & McLean, W. H. I. (2007) · Journal of Investigative Dermatology · doi:10.1038/sj.jid.5700876 · Cited by 119 · cited 1× · see citing works
“Unlike the common belief that was widely accepted for a very long time, there is now little support for the view that AD is the result of allergies [43,44].”
Background
Murine model of atopic dermatitis associated with food hypersensitivity
Li, X.-M., Kleiner, G., Huang, C.-K., et al. (2001) · Journal of Allergy and Clinical Immunology · doi:10.1067/mai.2001.114110 · Cited by 116 · cited 1× · see citing works
“lesions in up to 35% mice, accompanied by elevated serum levels of specific IgE and blood eosinophilia [55].”
Background
Impairment of skin barrier function in NC/Nga Tnd mice as a possible model for atopic dermatitis
Aioi, A., Tonogaito, H., Suto, H., et al. (2001) · British Journal of Dermatology · doi:10.1046/j.1365-2133.2001.03946.x · Cited by 116 · cited 1× · see citing works
“The content of ceramide in the skin is remarkably decreased in NC/Tnd mice before dermatitis, and it became clear that transepidermal water loss was promoted in the affected skin as a result [60].”
Background
Wound healing in embryos: a review
Nodder, S., & Martin, P. B. (1997) · Anatomy and Embryology · doi:10.1007/s004290050041 · Cited by 113 · cited 1× · see citing works
“5 Embryonic wound models Unlike in adult skin, wound healing in early gestational stage mammalian embryos involves repair processes that result in the essentially perfect regeneration of damaged tissue [124].”
Background
Pharmacokinetic–Pharmacodynamic Analysis of Vismodegib in Preclinical Models of Mutational and Ligand-Dependent Hedgehog Pathway Activation
Wong, H., Alicke, B., West, K. A., Pacheco, P., La, H., Januario, T., Yauch, R. L., de Sauvage, F. J., & Gould, S. E. (2011) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-11-0975 · Cited by 113 · cited 1× · see citing works
“Vismodegib [187] is a potent and selective inhibitor of the Hedgehog (Hh) pathway that showed antitumor activity in patient-derived colorectal cancer xenograft tumor models and medulloblastoma allograft tumors driven by mutational or ligand-dependent activation of the Hh pathway.”
Background
Effect of body weight on the pharmacokinetics of cyclophosphamide in breast cancer patients
Powis, G., Reece, P. A., Ahmann, D. L., & Ingle, J. N. (1987) · Cancer Chemotherapy and Pharmacology · doi:10.1007/bf00570489 · Cited by 112 · see citing works
Application of a partial-thickness human ex vivo skin culture model in cutaneous wound healing study
Xu, W., Hong, S. J., Jia, S., Zhao, Y., Galiano, R. D., & Mustoe, T. A. (2012) · Laboratory Investigation · doi:10.1038/labinvest.2011.184 · Cited by 108 · cited 1× · see citing works
“For example, the host’s vascular and immune systems, as well as the external environment, influence animal models like humans [119].”
Background
From UVs to Metastases: Modeling Melanoma Initiation and Progression in the Mouse
Zaidi, M. R., Day, C., & Merlino, G. T. (2008) · Journal of Investigative Dermatology · doi:10.1038/jid.2008.177 · Cited by 106 · cited 9× · see citing works
“These events are initiated by UVR of certain wavelengths, and include formation of DNA damage products, DNA repair, and mutation of proto-oncogenes and tumor suppressor genes [162].”
BackgroundInfluential
Monitoring photodynamic therapy of localized infections by bioluminescence imaging of genetically engineered bacteria
Demidova, T. N., Gad, F., Zahra, T., et al. (2005) · Journal of Photochemistry and Photobiology B Biology · doi:10.1016/j.jphotobiol.2005.05.007 · Cited by 106 · cited 1× · see citing works
“An innovative technique has been developed employing bioluminescent (glow-in-the-dark) bacteria and low-light imaging cameras to noninvasively monitor the progress of the infection in real time in the same animal [129].”
MethodSelf-citation
Bone Marrow Cell Transfer into Fetal Circulation Can Ameliorate Genetic Skin Diseases by Providing Fibroblasts to the Skin and Inducing Immune Tolerance
Chino, T., Tamai, K., Yamazaki, T., Otsuru, S., Kikuchi, Y., Nimura, K., Endo, M., Nagai, M., Uitto, J., Kitajima, Y., et al. (2008) · American Journal Of Pathology · doi:10.2353/ajpath.2008.070977 · Cited by 103 · see citing works
Transgenic Animal Models in Toxicology: Historical Perspectives and Future Outlook
Boverhof, D. R., Chamberlain, M. P., Elcombe, C. R., Gonzalez, F. J., Heflich, R. H., Soeteman‐Hernández, L. G., Jacobs, A. C., Jacobson‐Kram, D., Luijten, M., Maggi, A. C., et al. (2011) · Toxicological Sciences · doi:10.1093/toxsci/kfr075 · Cited by 103 · cited 2× · see citing works
“Microinjection (Figure 2) exposes the fertilized egg to the transgene before the embryo forms, thus allowing the gene to be present in the embryo before development [28].”
Background
Percutaneous absorption in the rhesus monkey compared to man
Wester, R. C., & Maïbach, H. I. (1975) · Toxicology and Applied Pharmacology · doi:10.1016/0041-008x(75)90230-6 · Cited by 101 · cited 1× · see citing works
“Rhesus monkey was found to be similar to human in terms of percutaneous absorption studies of hydrocortisone, testosterone, and benzoic acid [5].”
Background
Models of Wound Healing
Greenhalgh, D. G. (2005) · Journal of Burn Care & Rehabilitation · doi:10.1097/01.bcr.0000169885.66639.b5 · Cited by 99 · see citing works
Tetracycline-inducible Expression Systems: New Strategies and Practices in the Transgenic Mouse Modeling
Sun, Y., Chen, X., & Xiao, D. (2007) · Acta Biochimica et Biophysica Sinica · doi:10.1111/j.1745-7270.2007.00258.x · Cited by 94 · cited 3× · see citing works
“Controlled gene expression in mouse models is studied based on the tamoxifen-inducible Cre recombinase system [33,34], Cre-loxP and the tetracycline (Tet)-inducible systems [35], and tet-operon/repressor bi-transgenic system, the estrogen receptor (ER) ligand-binding domain, the cell-specific activation and inactivati…”
Method
Association of Cathepsin E Deficiency with Development of Atopic Dermatitis
Tsukuba, T. (2003) · The Journal of Biochemistry · doi:10.1093/jb/mvg216 · Cited by 90 · cited 1× · see citing works
“aureus was identified [67].”
Animal models of psoriasis: a critical appraisal
Schön, M. P. (2008) · Experimental Dermatology · doi:10.1111/j.1600-0625.2008.00751.x · Cited by 90 · cited 2× · see citing works
“Spontaneous mutation mouse models, such as homozygous asebia (Scd1ab/Scd1ab) mutant mice [71], Flaky skin mice (Ttcfsn/Ttcfsn) [72], spontaneous chronic proliferative dermatitis mutation mice [73] and so on, do not closely mimic the disease enough to be considered as good models of psoriasis.”
Background
Mouse models for melanoma: a personal perspective
Becker, J. C., Houben, R., Schrama, D., Voigt, H., Ugurel, S., & Reisfeld, R. A. (2009) · Experimental Dermatology · doi:10.1111/j.1600-0625.2009.00986.x · Cited by 90 · cited 1× · see citing works
“, during embryogenesis or postnatal) [11].”
A polygenic mouse model of psoriasiform skin disease in CD18-deficient mice.
Bullard, D. C., Scharffetter‐Kochanek, K., McArthur, M. J., Chosay, J. G., McBride, M. E., Montgomery, C. A., & Beaudet, A. L. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.5.2116 · Cited by 87 · cited 1× · see citing works
“These include the transgenic and knockout models, such as human leukocyte antigen B27 (HLA-B27) transgenic rats [74], CD18 hypomorphic mice [75], K14/VEGF and Tie2 mice [76,77], K14/TGF-a, K5/TGF-b1, K14/KGF and K14/IL-20 transgenic mice [78-80], IKK2 [81] and JunB/c-Jun transgenic mice [82], K5.”
Background
Establishment of an atopic dermatitis‐like skin model in a hairless mouse by repeated elicitation of contact hypersensitivity that enables to conduct functional analyses of the stratum corneum with various non‐invasive biophysical instruments
Matsumoto, K., Mizukoshi, K., Oyobikawa, M., et al. (2004) · Skin Research and Technology · doi:10.1111/j.1600-0846.2004.00062.x · Cited by 80 · cited 2× · see citing works
“However, it has been reported that multiple challenges with haptens of the skin over an extended period cause the skin inflammation to shift from Th1-dominated responses to chronic Th2-dominated inflammatory responses that are similar to those in human AD patients [52].”
Background
Transgenic zebrafish produced by retroviral infection of in vitro -cultured sperm
Kurita, K., Burgess, S. M., & Sakai, N. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0304265101 · Cited by 74 · cited 1× · see citing works
“, gene gun, electroporation, laser irradiation), chemical (calcium phosphate precipitation, diethylaminoethanol (DEAE)-dextran), and biological (lipids, virus, plasmids), and currently, transgenic animals can be constructed in several ways such as microinjection [15], embryonic stem cell (ESC) injection [16], retrovir…”
Background
Alopecia areata − animal models
McElwee, K. J., & Hoffmann, R. (2002) · Clinical and Experimental Dermatology · doi:10.1046/j.1365-2230.2002.01075.x · Cited by 72 · cited 3× · see citing works
“Table 3 shows a brief summary of commonly used mouse strains with histologically confirmed AA-like diseases [172].”
Background
Sinclair miniature swine: an animal model of human melanoma
Misfeldt, M. L., & Grimm, D. R. (1994) · Veterinary Immunology and Immunopathology · doi:10.1016/0165-2427(94)90133-3 · Cited by 71 · cited 1× · see citing works
“Swine (Duroc-Jersey swine, Sinclair miniature swine, Munich Troll miniature swine) [110] and Camargue horses develop melanoma; however, neither of these develop melanoma with a sunlightbased etiology [10].”
Background
Mouse models for human hair loss disorders
Porter, R. M. (2003) · Journal of Anatomy · doi:10.1046/j.1469-7580.2003.00140.x · Cited by 71 · cited 3× · see citing works
“This short synchronized hair cycle allows hair follicles to be harvested and examined at specific time points in the cycle very easily [14].”
BackgroundInfluential
The C3H/HeJ mouse and DEBR rat models for alopecia areata: review of preclinical drug screening approaches and results
Sun, J., Silva, K. A., McElwee, K. J., et al. (2008) · Experimental Dermatology · doi:10.1111/j.1600-0625.2008.00773.x · Cited by 71 · cited 2× · see citing works
“The DEBR model develops spontaneous AA at a higher frequency than in the mouse model; however, the disadvantage of this model is that they are more expensive to use in drug studies owing to their larger size [173].”
Background
Genetic and environmental melanoma models in fish
Patton, E. E., Mitchell, D. L., & Nairn, R. S. (2010) · Pigment Cell & Melanoma Research · doi:10.1111/j.1755-148x.2010.00693.x · Cited by 70 · see citing works
Comparison of bovine udder skin with human and porcine skin in percutaneous permeation experiments.
Netzlaff, F., Schaefer, U. F., Lehr, C., Meiers, P., Stahl, J., Kietzmann, M., & Niedorf, F. (2006) · PubMed · Cited by 69 · see citing works
Mite Allergen Induces Allergic Dermatitis with Concomitant Neurogenic Inflammation in Mouse
Huang, C. H., Kuo, I.-C., Xu, H., et al. (2003) · Journal of Investigative Dermatology · doi:10.1046/j.1523-1747.2003.12356.x · Cited by 68 · cited 1× · see citing works
“On the other hand, mice-sensitized features by the recombinant house dust mite allergen were similar to those observed with EC sensitization models with OVA, and manifested epidermal hyperplasia and spongiosis (intracellular swelling within the epidermis), infiltration of CD4 and CD8 cells, and a skewed Th2 response l…”
Method
Ultraviolet B Irradiation Induces Expansion of Intraepithelial Tumor Cells in a Tissue Model of Early Cancer Progression
Fusenig, N. E., Mudgil, A. V., Segal, N., Andriani, F., Wang, Y., & Garlick, J. A. (2003) · Journal of Investigative Dermatology · doi:10.1046/j.1523-1747.2003.12320.x · Cited by 62 · cited 1× · see citing works
“Excessive exposure to solar UVR causes severe acute damages to the skin, which include erythema, sunburn, immunosuppressant, and also long-term effects such as photoaging and skin cancer [150-154].”
Background
Animal models of spontaneous and drug-induced cutaneous lupus erythematosus
Furukawa, F., & Yoshimasu, T. (2005) · Autoimmunity Reviews · doi:10.1016/j.autrev.2005.01.006 · Cited by 59 · cited 4× · see citing works
“An alternative way to induce cutaneous lesions is through TCR alpha -/- mice that are treated with fluorouracil and UVB light irradiation [104].”
BackgroundInfluential
Mouse Models of Human Autoimmune Diseases: Essential Tools That Require the Proper Controls
Morel, L. M. (2004) · PLoS Biology · doi:10.1371/journal.pbio.0020241 · Cited by 58 · cited 4× · see citing works
“Recent discoveries have shown that genetic susceptibility to autoimmune diseases involves a large number of genes with small individual contributions, but in spite of this great complexity, significant advances have been made and a small but growing number of susceptibility genes have been identified [99].”
BackgroundInfluential
The Site ofLeishmania majorInfection Determines Disease Severity andImmuneResponses
Baldwin, T. M., Elso, C. M., Curtis, J., et al. (2003) · Infection and Immunity · doi:10.1128/iai.71.12.6830-6834.2003 · Cited by 58 · see citing works
Animal Models of Acute Photodamage: Comparisons of Anatomic, Cellular and Molecular Responses in C57BL/6J, SKH1 and Balb/c Mice
Sharma, M. R., Werth, B. B., & Werth, V. P. (2011) · Photochemistry and Photobiology · doi:10.1111/j.1751-1097.2011.00911.x · Cited by 56 · cited 1× · see citing works
“C57BL/6J, SKH1, and BALB/c mice are the three main strains used for photoaging and photocarcinogenesis studies [157-159].”
Background
Inducible Transgenic Mouse Models
Saunders, T. L. (2010) · Methods in molecular biology · doi:10.1007/978-1-60761-974-1_7 · Cited by 55 · cited 2× · see citing works
“Thus, the Tet-regulated and Cre-ER systems are complementary in animal models, through utility in the cell-specific activation and inactivation of gene expression [37].”
BackgroundMethod
Spontaneous Alopecia Areata-Like Hair Loss in One Congenic and Seven Inbred Laboratory Mouse Strains
McElwee, K. J., Boggess, D., Miller, J. V., et al. (1999) · Journal of Investigative Dermatology Symposium Proceedings · doi:10.1038/sj.jidsp.5640211 · Cited by 53 · cited 1× · see citing works
“1 Alopecia areata Alopecia areata (AA) like hair loss has been observed in several species, including monkeys, dogs, cats, horses, cattle, poultry, and non-human primates [171,172].”
Background
Varicella-Zoster Virus Immunizes Patas Monkeys against Simian Varicella-like Disease
FELSENFELD, A. D., & Schmidt, N. J. (1979) · Journal of General Virology · doi:10.1099/0022-1317-42-1-171 · Cited by 53 · see citing works
Correlation of Propionibacterium acnes Populations with the Presence of Triglycerides on Nonhuman Skin
WEBSTER, G. F., Ruggieri, M. R., & McGinley, K. J. (1981) · Applied and Environmental Microbiology · doi:10.1128/aem.41.5.1269-1270.1981 · Cited by 52 · cited 1× · see citing works
“The list of animal models that have been used in the study of acne include the rabbit ear model, rhino mouse model [138], Mexican hairless dog model [138,139], Golden Hamster model, swine, and guinea pig [140].”
Method
Recent advances in inducible expression in transgenic mice
Albanese, C., Hulit, J., Sakamaki, T., & Pestell, R. G. (2002) · Seminars in Cell and Developmental Biology · doi:10.1016/s1084-9521(02)00021-6 · Cited by 52 · cited 1× · see citing works
“Controlled gene expression in mouse models is studied based on the tamoxifen-inducible Cre recombinase system [33,34], Cre-loxP and the tetracycline (Tet)-inducible systems [35], and tet-operon/repressor bi-transgenic system, the estrogen receptor (ER) ligand-binding domain, the cell-specific activation and inactivati…”
Method
Phosphocreatine protects ATP from a fructose load in transgenic mouse liver expressing creatine kinase
Brosnan, M. J., Chen, L. H., Wheeler, C. E., Dyke, T. A. V., & Koretsky, A. P. (1991) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.1991.260.6.c1191 · Cited by 52 · cited 1× · see citing works
“, gene gun, electroporation, laser irradiation), chemical (calcium phosphate precipitation, diethylaminoethanol (DEAE)-dextran), and biological (lipids, virus, plasmids), and currently, transgenic animals can be constructed in several ways such as microinjection [15], embryonic stem cell (ESC) injection [16], retrovir…”
Background
Inherited Mouse Mutations as Models of Human Adnexal, Cornification, and Papulosquamous Dermatoses
Sundberg, J. P., Beamer, W. G., Shultz, L. D., & Dunstan, R. W. (1990) · Journal of Investigative Dermatology · doi:10.1111/1523-1747.ep12505816 · Cited by 51 · cited 1× · see citing works
“Spontaneous mutation mouse models, such as homozygous asebia (Scd1ab/Scd1ab) mutant mice [71], Flaky skin mice (Ttcfsn/Ttcfsn) [72], spontaneous chronic proliferative dermatitis mutation mice [73] and so on, do not closely mimic the disease enough to be considered as good models of psoriasis.”
Background
Animal Models of Epidermolysis Bullosa: Update 2010
Bruckner‐Tuderman, L., McGrath, J. A., Robinson, E. C., et al. (2010) · Journal of Investigative Dermatology · doi:10.1038/jid.2010.75 · Cited by 50 · cited 1× · see citing works
“Transgenic mice have been developed as models for different forms of EB [89].”
Background
Cytokines as genetic modifiers in K5��/��mice and in human epidermolysis bullosa simplex
Roth, W., Reuter, U., Wohlenberg, C., Bruckner‐Tuderman, L., & Magin, T. M. (2009) · Human Mutation · doi:10.1002/humu.20981 · Cited by 48 · cited 1× · see citing works
“Examples include the transforming growth factor-b-induced, myofibroblastmediated contractile fibrosis in severe DEB [90] and the Langerhans cell-mediated inflammatory processes described in keratin 5-deficient mice [91].”
Background
Melanoma Biology and the Promise of Zebrafish
Ceol, C. J., Houvras, Y. J., White, R. M., & Zon, L. I. (2008) · Zebrafish · doi:10.1089/zeb.2008.0544 · Cited by 46 · cited 2× · see citing works
“Furthermore, the development of melanocytes from the embryonic neural crest is well characterized [114].”
Background
A fibre-free alginate dressing in the treatment of split thickness skin graft donor sites
Steenfos, H. H., & Ågren, M. S. (1998) · Journal of the European Academy of Dermatology and Venereology · doi:10.1016/s0926-9959(98)00078-6 · Cited by 42 · see citing works
Animal models of melanoma: Recent advances and future prospects
Bardeesy, N. M., Wong, K., DePinho, R. A., & Chin, L. (2000) · Advances in cancer research · doi:10.1016/s0065-230x(00)79004-x · Cited by 42 · cited 1× · see citing works
“Transgenic models are also in use both in mouse [112] [e.”
Method
Alopecia Areata and Universalis in the Smyth Chicken Model for Spontaneous Autoimmune Vitiligo
Smyth, J. R., & McNeil, M. (1999) · Journal of Investigative Dermatology Symposium Proceedings · doi:10.1038/sj.jidsp.5640213 · Cited by 42 · cited 1× · see citing works
“The Smyth line chicken model is not yet widely used; however, it also shows promising results for future use, both in alopecia areata and alopecia universalis [176].”
Background
A Mouse Model of Generalized Non-Herlitz Junctional Epidermolysis Bullosa
Bubier, J. A., Sproule, T. J., Alley, L. M., et al. (2010) · Journal of Investigative Dermatology · doi:10.1038/jid.2010.46 · Cited by 40 · cited 2× · see citing works
“It is classified according to the site of blister formation, and the main three groups are epidermolytic or EB simplex (EBS), JEB, and dermolytic or dystrophic EB (DEB) [85].”
Method
Strategies of Conditional Gene Expression in Myocardium
Heine, H. L., Leong, H. S., Rossi, F. M. V., McManus, B. M., & Podor, T. J. (2005) · Methods in molecular medicine · doi:10.1007/978-1-59259-879-3_8 · Cited by 40 · see citing works
Naturally Occurring Dermatitis Associated with Staphylococcus aureus in DS-Nh Mice.
Haraguchi, M., Hino, M., Tanaka, H., et al. (1997) · EXPERIMENTAL ANIMALS · doi:10.1538/expanim.46.225 · Cited by 38 · cited 1× · see citing works
“aureus-associated AD [68].”
Ultrastructural Changes in Cells of the Mouse Footpad Infected with Mycobacterium leprae
Evans, M. J., & Lévy, L. (1972) · Infection and Immunity · doi:10.1128/iai.5.2.238-247.1972 · Cited by 38 · cited 1× · see citing works
“Footpad was the preferred site of inoculation since it is a cooler site (30 C), which mirrors the preferred cooler sites in human leprosy, permits serial sampling of the tissue as the infection progresses, and there is a minimum of inflammatory response in the footpad tissues [135,136].”
Background
Naturally Acquired Simian Varicella Virus Infection in African Green Monkeys
Mahalingam, R., Traina‐Dorge, V., Wellish, M., et al. (2002) · Journal of Virology · doi:10.1128/jvi.76.17.8548-8550.2002 · Cited by 37 · cited 4× · see citing works
“Varicella-zoster virus (VZV) infection is commonly seen as a benign disease of children causing fever and vesicular skin lesions [143].”
BackgroundMethodInfluential
Chemotherapy of Leishmaniasis
Beveridge, E. (1963) · Elsevier eBooks · doi:10.1016/b978-1-4832-3178-5.50011-3 · Cited by 37 · cited 1× · see citing works
“braziliensis, although other types of hamsters have been used as well [148].”
Method
The Translational Basis of Human Cutaneous Photoaging
Laga, A. C., & Murphy, G. F. (2009) · American Journal Of Pathology · doi:10.2353/ajpath.2009.081029 · Cited by 34 · cited 7× · see citing works
“These events are initiated by UVR of certain wavelengths, and include formation of DNA damage products, DNA repair, and mutation of proto-oncogenes and tumor suppressor genes [162].”
BackgroundInfluential
Passive drug diffusion via standardized skin mini-erosion; methodological aspects and clinical findings with new device.
Svedman, P., Lundin, S., Höglund, P., et al. (1996) · Pharmaceutical Research · doi:10.1023/a:1016021900286 · Cited by 34 · cited 1× · see citing works
“The model can be used both in animals and in humans for evaluation of epidermal regeneration and the influence of different compounds and drugs [121].”
Background
Animal Models of Melanoma
Ha, L., Noonan, F. P., Fabo, E. C. D., & Merlino, G. T. (2005) · Journal of Investigative Dermatology Symposium Proceedings · doi:10.1111/j.1087-0024.2005.200409.x · Cited by 33 · see citing works
Human Delayed-Type Hypersensitivity Reaction in a SCID Mouse Engrafted with Human T Cells and Autologous Skin
Petzelbauer, P., Gröger, M., Kunstfeld, R., et al. (1996) · Journal of Investigative Dermatology · doi:10.1111/1523-1747.ep12582823 · Cited by 33 · cited 1× · see citing works
“Drug discovery for dermatitis has been less well developed, although there is a skin xenotransplantation model “Trans in vivo delayed hypersensitivity model” using an antigen-specific immune response that is relevant for both psoriasis and AD [185].”
Background
In Vivo Assessment of Acute UVB Responses in Normal and Xeroderma Pigmentosum (XP-C) Skin-Humanized Mouse Models
García, M., Llames, S. G., García, E., Meana, Á., Cuadrado‐Corrales, N., Recasens, M., Puig, S., Nagore, E., Illera, N., Jorcano, J. L., et al. (2010) · American Journal Of Pathology · doi:10.2353/ajpath.2010.091096 · Cited by 33 · see citing works
An experimental model of "dermatomyositis" induced by calciphylaxis.
Selye, H., Gentile, G., & Jean, P. (1961) · PubMed · Cited by 32 · see citing works
Development of Atopic Dermatitis in Mice Transgenic for Human Apolipoprotein C1
Nagelkerken, L. M., Verzaal, P., Lagerweij, T., et al. (2007) · Journal of Investigative Dermatology · doi:10.1038/sj.jid.5701182 · Cited by 32 · cited 1× · see citing works
“APOC1Tg mice spontaneously develop age-severe dermatitis with moderate epidermal hyperplasia, hyperkeratosis and parakeratosis, scaling, lichenification, dermal infiltration of inflammatory cells, and pruritus [57].”
Background
Evaluation of sunscreens with various sun protection factors in a new transgenic mouse model of cutaneous photoaging that measures elastin promoter activation
Bernstein, E. F., Brown, D. B., Takeuchi, T., et al. (1997) · Journal of the American Academy of Dermatology · doi:10.1016/s0190-9622(97)70108-7 · Cited by 32 · cited 10× · see citing works
“This transgenic mouse can be used to measure the response to single exposures of UV emitted from a fluorescent source, and since promoter induction is one of the primary events causing elastin production in skin, this model provides a precise measurement of one of the earliest events leading to photoaging [160].”
BackgroundMethodInfluential
Laser photobiostimulation of wound healing: Defining a dose response for splinted wounds in diabetic mice
Chung, T., Peplow, P. V., & Baxter, D. G. (2010) · Lasers in Surgery and Medicine · doi:10.1002/lsm.20981 · Cited by 30 · cited 2× · see citing works
“Laser photobiomodulation that stimulated healing in splinted wounds in diabetic mice has been reported [123].”
Background
A novel rat model for chemotherapy-induced alopecia: A rat model for chemotherapy-induced alopecia
Wikramanayake, T. C., Amini, S., Simon, J., Mauro, L. M., Elgart, G., Schachner, L. A., & Jimenez, J. J. (2012) · Clinical and Experimental Dermatology · doi:10.1111/j.1365-2230.2011.04239.x · Cited by 30 · cited 1× · see citing works
“Mice, rats, and rabbits are the animal models that have been studied so far (Table 5) [178-182].”
Background
Radiation Sensitivity of Human Hair Follicles in SCID-hu Mice
Kyoizumi, S., Suzuki, T., Teraoka, S., & Seyama, T. (1998) · Radiation Research · doi:10.2307/3579676 · Cited by 30 · cited 1× · see citing works
“Human scalp explants on SCID mice is another experimental model reported by Kyoizumi and colleagues [174] and later adapted by Gilhar and colleagues [175].”
Method
Transgenic mice: a decade of progress in technology and research
Wight, D. C., & Wagner, T. E. (1994) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/0027-5107(94)90254-2 · Cited by 30 · cited 1× · see citing works
“, gene gun, electroporation, laser irradiation), chemical (calcium phosphate precipitation, diethylaminoethanol (DEAE)-dextran), and biological (lipids, virus, plasmids), and currently, transgenic animals can be constructed in several ways such as microinjection [15], embryonic stem cell (ESC) injection [16], retrovir…”
Background
Progress in Heritable Skin Diseases: Translational Implications of Mutation Analysis and Prospects of Molecular Therapies*
Uitto, J. (2009) · Acta Dermato Venereologica · doi:10.2340/00015555-0648 · Cited by 30 · cited 1× · see citing works
“Of particular interest was the suitability of EB mouse models for preclinical testing of gene-, protein-, and cell-based therapies [92,93].”
Background
Animal Models for SLE
Cohen, P. L., & Maldonado, M. A. (2002) · Current Protocols in Immunology · doi:10.1002/0471142735.im1520s52 · Cited by 29 · cited 2× · see citing works
“Characteristics of well-studied SLE-prone mouse strains [100-102].”
Background
Animal models of cutaneous lupus erythematosus and lupus erythematosus photosensitivity
Furukawa, F. (1997) · Lupus · doi:10.1177/096120339700600215 · Cited by 29 · cited 7× · see citing works
“Themain examples of SLE-pronemice areNewZealand Black (NZB), F1 hybrids of NZB New Zealand White (NZW) (B/W F1), MRL/Mp-lpr/lpr, and BXSB mice (Table 1) [100-102].”
BackgroundInfluential
Protective effects of sunscreening agents on photocarcinogenesis, photoaging, and DNA damage in XPA gene knockout mice
Horiki, S., Miyauchi‐Hashimoto, H., Tanaka, K., Nikaido, O., & Horio, T. (2000) · Archives of Dermatological Research · doi:10.1007/s004030000164 · Cited by 29 · cited 1× · see citing works
“The xeroderma pigmentosum (XPA) mice model, on the other hand, is XPA gene deficient and therefore is defective in NER and consequently shows high incidence of skin tumors and severe acute inflammation in response to UVB irradiation [168].”
Background
Familial canine dermatomyositis
Hargis, A. M., & Mundell, A. C. (1986) · Journal of the American Veterinary Medical Association · doi:10.2460/javma.1986.188.04.386 · Cited by 29 · see citing works
Atopic Dermatitis in 2008
Chan, L. S. (2008) · KARGER eBooks · doi:10.1159/000131450 · Cited by 28 · see citing works
Directed Expression of Transgenes to Alveolar Type I Cells in the Mouse
Vanderbilt, J. N., Allen, L., Gonzalez, R. F., et al. (2008) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2008-0049oc · Cited by 28 · cited 1× · see citing works
“A second method is by using retroviruses which are more efficient in integrating foreign DNA, even though the integration site for retroviruses is most often random [29].”
Method
IL-12 and IL-23 Affect Photocarcinogenesis Differently
Jantschitsch, C., Weichenthal, M., Proksch, E., Schwarz, T., & Schwarz, A. (2012) · Journal of Investigative Dermatology · doi:10.1038/jid.2011.469 · Cited by 27 · cited 1× · see citing works
“C57BL/6J, SKH1, and BALB/c mice are the three main strains used for photoaging and photocarcinogenesis studies [157-159].”
Background
Prevention of chemotherapy-induced alopecia by the anti-death FNK protein
Nakashima-Kamimura, N., Nishimaki, K., Mori, T., et al. (2007) · Life Sciences · doi:10.1016/j.lfs.2007.11.011 · Cited by 25 · cited 1× · see citing works
“Mice, rats, and rabbits are the animal models that have been studied so far (Table 5) [178-182].”
Background
Animal models for male pattern (androgenetic) alopecia.
Sundberg, J. P., King, L. E., & Bascom, C. C. (2001) · PubMed · Cited by 24 · see citing works
Dermatomyositis
Dourmishev, L., & Dourmishev, A. L. (2009) · Springer eBooks · doi:10.1007/978-3-540-79313-7 · Cited by 23 · see citing works
Genetically engineered T-cells expressing a ganciclovir-sensitive HSV-tk suicide gene for the prevention of GvHD.
Mailly, L., Leboeuf, C., Tiberghien, P., et al. (2010) · PubMed · Cited by 23 · see citing works
Genetically engineered mouse models for skin research: Taking the next step
Jiang, C., & Roop, D. R. (2008) · Journal of Dermatological Science · doi:10.1016/j.jdermsci.2008.03.012 · Cited by 22 · cited 7× · see citing works
“Some of the resulting progeny will harbor both the floxed region and express the Cre recombinase in specific cell types [20,32].”
BackgroundInfluential
Effect of immunization with herpes simplex virus type-1 (HSV-1) glycoprotein D (gD) plus the immune enhancer GPI-0100 on infection with HSV-1 or HSV-2
Quenelle, D. C., COLLINS, D., Marciani, D. J., et al. (2005) · Vaccine · doi:10.1016/j.vaccine.2005.10.017 · Cited by 21 · cited 1× · see citing works
“Commonly used animal models for herpes simplex are the albino guinea pig and the hairless guinea pig [141,142].”
Background
The Psoriasis SCID Mouse Model: A Tool for Drug Discovery?
Boehncke, W. (2006) · Springer eBooks · doi:10.1007/3-540-26811-1_12 · Cited by 19 · cited 1× · see citing works
“Drug discovery efforts in animal models for skin disease have been most notable in the psoriasis SCID mouse model where efalizumab (Raptiva ) [183] and infliximab (Remicade ) [184] were both discovered.”
Background
Correlation of murine anti-dinitrophenyl antibody content as determined by ELISA, passive cutaneous anaphylaxis and passive hemolysis
Maekawa, S., & Óváry, Z. (1984) · Journal of Immunological Methods · doi:10.1016/0022-1759(84)90069-3 · Cited by 19 · cited 1× · see citing works
“1 Passive sensitization model This model shows IgE-mediated cutaneous inflammation reaction which is carried out by intravenous injection of murine monoclonal IgE anti-hapten antibodies [48].”
Background
A monoclonal antibody against kininogen reduces inflammation in the HLA-B27 transgenic rat
Keith, J. C., Sáinz, I. M., Isordia‐Salas, I., et al. (2005) · Arthritis Research & Therapy · doi:10.1186/ar1728 · Cited by 19 · cited 1× · see citing works
“These include the transgenic and knockout models, such as human leukocyte antigen B27 (HLA-B27) transgenic rats [74], CD18 hypomorphic mice [75], K14/VEGF and Tie2 mice [76,77], K14/TGF-a, K5/TGF-b1, K14/KGF and K14/IL-20 transgenic mice [78-80], IKK2 [81] and JunB/c-Jun transgenic mice [82], K5.”
Background
Cutaneous lupus erythematosus: recent lessons from animal models
Ghoreishi, M., & Dutz, J. (2010) · Lupus · doi:10.1177/0961203310370045 · Cited by 18 · cited 2× · see citing works
“In this model, lpr mutation causes an alteration in the Fas gene and a defect of apoptosis, which in turn result in abnormal lymphocyte proliferation with abnormal function and autoantibody production [103].”
Background
Doxorubicin-induced hair loss in the Angora rabbit: a study of treatments to protect against the hair loss
Powis, G., & Kooistra, K. L. (1987) · Cancer Chemotherapy and Pharmacology · doi:10.1007/bf00262579 · Cited by 18 · cited 4× · see citing works
“Animal models of androgenetic alopecia are summarized in Table 4 [177,178].”
BackgroundMethodInfluential
Pyrimidine Dimer Formation and Oxidative Damage in M13 Bacteriophage Inactivation by Ultraviolet C Irradiation¶
Kurosaki, Y., Abe, H., Morioka, H., Hirayama, J., Ikebuchi, K., Kamo, N., Nikaido, O., Azuma, H., & Ikeda, H. (2003) · Photochemistry and Photobiology · doi:10.1562/0031-8655(2003)078 · Cited by 18 · see citing works
Real-TimeReflectance Confocal Microscopy, a Noninvasive Tool for in vivo Quantitative Evaluation of Comedolysis in the Rhino Mouse Model
Nakano, K., Kiyokane, K., Benvenuto-Andrade, C., et al. (2006) · Skin Pharmacology and Physiology · doi:10.1159/000096169 · Cited by 16 · cited 1× · see citing works
“The list of animal models that have been used in the study of acne include the rabbit ear model, rhino mouse model [138], Mexican hairless dog model [138,139], Golden Hamster model, swine, and guinea pig [140].”
Method
Advantages of Using Hairless Mice Versus Haired Mice to Test Sunscreen Efficacy Against Photoimmune Suppression¶
Kim, T.-H., Ananthaswamy, H. N., Kripke, M. L., et al. (2003) · Photochemistry and Photobiology · doi:10.1562/0031-8655(2003)0780037aouhmv2.0.co2 · Cited by 16 · see citing works
Nitric Oxide Donor Exisulind Is an Effective Inhibitor of Murine Photocarcinogenesis†
Singh, T., Chaudhary, S. C., Kapur, P., Weng, Z., Elmets, C. A., Kopelovich, L., & Athar, M. (2012) · Photochemistry and Photobiology · doi:10.1111/j.1751-1097.2012.01093.x · Cited by 15 · cited 1× · see citing works
“Recently, in SKH-1 hairless mice the effects of NO-exisulind on the growth of UVBinduced skin tumor development have been investigated [163].”
Background
An Animal Model for Evaluation of Topical Photoprotection Against Ultraviolet A (320–380 nm) Radiation
Chew, S., DeLeo, V. A., & Harber, L. C. (1987) · Journal of Investigative Dermatology · doi:10.1111/1523-1747.ep12471776 · Cited by 15 · cited 1× · see citing works
“The guinea pig (Hartley strain) is a reliable test model for protection against UVA-induced erythema with a solar-simulated source and is convenient and relatively inexpensive for testing photoprotection agents [169,170].”
Background
Mouse Models for Blistering Skin Disorders
Ganeshan, R., Chen, J., & Koch, P. J. (2010) · Dermatology Research and Practice · doi:10.1155/2010/584353 · Cited by 13 · cited 2× · see citing works
“Note that the forestomach is a characteristic feature of the mouse which is not present in humans [88].”
Background
Sunscreen testing using the mouse ear model.
Cole, C. A., Forbes, P. D., & Ludwigsen, K. (1989) · PubMed · Cited by 13 · see citing works
Gene expression of retinoic acid receptors and cellular retinoic acid-binding proteins in rhino and hairless mouse skin
Beehler, B. C., Chen, S., & Tramposch, K. M. (1995) · Archives of Dermatological Research · doi:10.1007/bf00373433 · Cited by 12 · cited 1× · see citing works
“The rhino mouse comedolytic model and the hairless mouse photoaging model are established animal models for screening the in vivo activity of retinoids [186].”
Method
Animal model of human disease. Dermatomyositis. Familial canine dermatomyositis.
Hargis, A. M., Haupt, K. H., Prieur, D. J., et al. (1985) · PubMed · Cited by 11 · see citing works
Animal models in leprosy
Rees, R. J. W. (1988) · British Medical Bulletin · doi:10.1093/oxfordjournals.bmb.a072274 · Cited by 10 · cited 3× · see citing works
“Footpad was the preferred site of inoculation since it is a cooler site (30 C), which mirrors the preferred cooler sites in human leprosy, permits serial sampling of the tissue as the infection progresses, and there is a minimum of inflammatory response in the footpad tissues [135,136].”
BackgroundMethod
Animal Models of Scleroderma: From Cellular and Molecular Mechanisms to Novel Antifibrotic Strategies
Manetti, M., Neumann, E., Distler, O., & Müller‐Ladner, U. (2009) · Springer eBooks · doi:10.1007/978-1-84882-637-3_3 · Cited by 4 · cited 2× · see citing works
“Animal models of SSc can be divided into three groups (Table 2) [105,106].”
Background
Animal model of human disease: lepromatous leprosy.
Storrs, E. E., Binford, C. H., & MIGAKI, G. (1978) · PubMed · Cited by 4 · see citing works
Treatment of Cutaneous Herpesvirus hominis Type 2 Infection with 8-Methoxypsoralen and Long-Wave Ultraviolet Light in Guinea Pigs
Oill, P. A., Galpin, J. E., Fox, M. A., et al. (1978) · The Journal of Infectious Diseases · doi:10.1093/infdis/137.6.715 · Cited by 4 · cited 1× · see citing works
“Commonly used animal models for herpes simplex are the albino guinea pig and the hairless guinea pig [141,142].”
Background
The Utility of Transgenic Mouse Models in the Study of Cutaneous Immunology and Inflammation
Kupper, T. S. (1996) · The Journal of Dermatology · doi:10.1111/j.1346-8138.1996.tb02695.x · Cited by 4 · cited 4× · see citing works
“It also enables the analysis of the function of a protein produced from a specific gene in vivo [21].”
BackgroundInfluential
Evaluation of ultraviolet-A protection by sunscreen agents using a mouse model of contact photoallergy
TOKURA, Y., Yagi, H., Ihda, H., et al. (1994) · Journal of Dermatological Science · doi:10.1016/0923-1811(94)90020-5 · Cited by 4 · cited 5× · see citing works
“5 days later, sun screen agents were applied to the earlobes and subsequently challenged with TCSA/UVA [167].”
BackgroundMethodInfluential
A Comparison of Sun Protective Factor (SPF) Determinations in Guinea Pigs and Humans Utilizing Artificial Light
Loudin, B. A., & Drake, K. D. (1985) · Journal of Toxicology Cutaneous and Ocular Toxicology · doi:10.3109/15569529509033541 · Cited by 2 · cited 1× · see citing works
“The guinea pig (Hartley strain) is a reliable test model for protection against UVA-induced erythema with a solar-simulated source and is convenient and relatively inexpensive for testing photoprotection agents [169,170].”
Background
Hypomorphic Mice
Baker, D. J. (2010) · Methods in molecular biology · doi:10.1007/978-1-60761-974-1_13 · Cited by 2 · cited 1× · see citing works
“This approach facilitates the selection genetic function of interest to be expressed without compromising cell viability [22].”
Background
Novel animal models for bullous pemphigoid utilized by "humanization of autoantigen"
Nishie, W., & Shimizu, H. (2009) · Japanese Journal of Clinical Immunology · doi:10.2177/jsci.32.472 · Cited by 1 · cited 2× · see citing works
“To overcome this challenge, a novel molecular method has been established which is through ‘humanization of autoantigen’ by genetic manipulation [98].”
BackgroundMethod
[Transgenic mice in basic research].
Gassmann, M., Hennet, T., & Bauer, C. (1998) · PubMed · Cited by 1 · see citing works

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Skin models for the testing of transdermal drugs
Abd, E., Yousuf, S. A., Pastore, M. N., Telaprolu, K. C., Mohammed, Y., Namjoshi, S., Grice, J. E., & Roberts, M. S. (2016) · Clinical Pharmacology Advances and Applications · doi:10.2147/cpaa.s64788 · Cited by 418 · see citing works
“106 An overview of animal models for a wide range of skin conditions, with an emphasis on their application to drug discovery, has been published by Avci et al. 107 Of particular interest are the chimeric models, in which living human skin is grafted on to the skin of severe combined immunodeficient (SCID) mice.”
Advances in the Biofabrication of 3D Skin in vitro: Healthy and Pathological Models
Randall, M. J., Jüngel, A., Rimann, M., & Wuertz‐Kozak, K. (2018) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2018.00154 · Cited by 193 · see citing works
“Currently, the primary means of identifying therapeutics for these diseases require the use of animal models (Avci et al., 2013), increasing not only the cost of drug development, but also the cost for consumers.”
Background
Histological and functional comparisons of four anatomical regions of porcine skin with human abdominal skin
In, M. K., Richardson, K. C., Löwa, A., Hedtrich, S., Kaessmeyer, S., & Plendl, J. (2019) · Anatomia Histologia Embryologia · doi:10.1111/ahe.12425 · Cited by 154 · see citing works
“…primates, pigs, dogs, cats, rodents, rabbits and fish, for use in medical research including studies on skin xenotransplan‐ tation, has been a major focus over the past decade (Abdullahi et al., 2014; Avci et al., 2013; Badyal & Desai, 2014; Boneva, Folks, & Chapman, 2001; Ge, Zheng, & Wei, 2009).”
Background
Models in the Research Process of Psoriasis
Bocheńska, K., Smolińska, E., Moskot, M., Jakóbkiewicz‐Banecka, J., & Gabig‐Cimińska, M. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18122514 · Cited by 135 · see citing works
“Nevertheless, mouse in vivo models have been used to greatly expand our current knowledge of the causes, pathogenesis, and treatment of Ps [21,60].”
Background
Modelling the Complexity of Human Skin In Vitro
Hofmann, E., Schwarz, A., Fink, J., Kamolz, L.-P., & Kotzbeck, P. (2023) · Biomedicines · doi:10.3390/biomedicines11030794 · Cited by 129 · see citing works
New insights into acne pathogenesis: Exploring the role of acne-associated microbial populations
Kumar, B. D., Pathak, R., Mary, P. B., Jha, D., Sardana, K., & Gautam, H. K. (2016) · Dermatologica Sinica · doi:10.1016/j.dsi.2015.12.004 · Cited by 119 · see citing works
Human In Vitro Skin Models for Wound Healing and Wound Healing Disorders
Hofmann, E., Fink, J., Pignet, A.-L., Schwarz, A., Schellnegger, M., Nischwitz, S. P., Holzer-Geissler, J. C. J., Kamolz, L.-P., & Kotzbeck, P. (2023) · Biomedicines · doi:10.3390/biomedicines11041056 · Cited by 104 · see citing works
Next generation human skin constructs as advanced tools for drug development
Abaci, H., Guo, Z., Doucet, Y., Jacków, J., & Christiano, A. (2017) · Experimental Biology and Medicine · doi:10.1177/1535370217712690 · Cited by 104 · see citing works
“mice, pigs) are widely used to perform drug screening for skin disease, they are not representative of the physiology or structure of the human skin, resulting in high drug attrition rates at later stages of drug development.(13) Clearly, there is a need for human skin disease models that allow for reliable and highth…”
Background
Activation of Nrf2 reduces UVA-mediated MMP-1 upregulation via MAPK/AP-1 signaling cascades: the photoprotective effects of sulforaphane and hispidulin
Chaiprasongsuk, A., Lohakul, J., Soontrapa, K., Sampattavanich, S., Akarasereenont, P., & Panich, U. (2017) · The Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.116.238048 · Cited by 101 · see citing works
“BALB/c mice were used in this study because they have been shown to preserve the expression of glycosaminoglycans in the dermis, which are critical for structural integrity of the skin similarly to that observed in the human physiology (Avci et al., 2013).”
Method
Microfluidic skin chip with vasculature for recapitulating the immune response of the skin tissue
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Strategies to apply 3Rs in preclinical testing
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Review of Major Theories of Skin Aging
Gragnani, A., Cornick, S. M., Chominski, V., de Noronha, S. M. R., de Noronha, S. A. A. C., & Ferreira, L. M. (2014) · Advances in Aging Research · doi:10.4236/aar.2014.34036 · Cited by 75 · see citing works
“The effects of skin photodamage and aging are studied by the use of animal models [38].”
Background
The biology of Acanthamoeba keratitis
Niederkorn, J. Y. (2020) · Experimental Eye Research · doi:10.1016/j.exer.2020.108365 · Cited by 68 · see citing works
“By contrast, Mycobacterium leprae, the bacterium that causes leprosy, is exquisitely host-specific (Adams et al., 2012; Avci et al., 2013).”
Background
The regional-dependent biaxial behavior of young and aged mouse skin: A detailed histomechanical characterization, residual strain analysis, and constitutive model
Meador, W. D., Sugerman, G. P., Story, H. M., Seifert, A. W., Bersi, M. R., Tepole, A. B., & Rausch, M. K. (2019) · Acta Biomaterialia · doi:10.1016/j.actbio.2019.10.020 · Cited by 60 · see citing works
Size dependent skin penetration of nanoparticles in murine and porcine dermatitis models
Try, C., Moulari, B., Béduneau, A., Fantini, O., Pin, D., Pellequer, Y., & Lamprecht, A. (2016) · European Journal of Pharmaceutics and Biopharmaceutics · doi:10.1016/j.ejpb.2016.01.002 · Cited by 60 · see citing works
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“However, only few animal models have been used for studying host–microbiome interactions in the oral cavity 30 , vagina 31 or skin 32 .”
Non-animal models in dermatological research
Dellambra, E. (2018) · ALTEX · doi:10.14573/altex.1808022 · Cited by 47 · see citing works
Advancements in Extracellular Matrix-Based Biomaterials and Biofabrication of 3D Organotypic Skin Models
Phang, S. J., Basak, S., Teh, H. X., Packirisamy, G., Fauzi, M. B., Kuppusamy, U. R., Neo, Y. P., & Looi, M. L. (2022) · ACS Biomaterials Science & Engineering · doi:10.1021/acsbiomaterials.2c00342 · Cited by 45 · see citing works
Topical Application of Oleuropein Induces Anagen Hair Growth in Telogen Mouse Skin
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“For example, the hair follicle density in mice is much greater than that in humans making the resulting interfollicular region of skin thinner, potentially increasing the rate of chemical absorption [47].”
Background
Assessment of skin barrier function and biochemical changes of ex vivo human skin in response to physical and chemical barrier disruption
Döge, N., Avetisyan, A., Hadam, S., Pfannes, E. K. B., Rancan, F., Blume‐Peytavi, U., & Vogt, A. (2016) · European Journal of Pharmaceutics and Biopharmaceutics · doi:10.1016/j.ejpb.2016.12.012 · Cited by 39 · see citing works
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“Several animal models including rabbit ear model, rhino mouse model, Mexican hairless dog model, hamster model, swine, and guinea pig have been used in the study of acne (Avci et al., 2013).”
MethodSelf-citation
Antivirulence and wound healing effects of royal jelly and garlic extract for the control of MRSA skin infections
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3D Human Skin Bioprinting: A View from the Bio Side
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Promises and challenges of senolytics in skin regeneration, pathology and ageing
Pils, V., Ring, N., Valdivieso, K., Lämmermann, I., Грубер, Ф., Schosserer, M., Grillari, J., & Ogrodnik, M. B. (2021) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2021.111588 · Cited by 32 · see citing works
Modeling of solar UV-induced photodamage on the hair follicles in human skin organoids
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“8 Since the European Union banned the use of animals in cosmetic testing in 2013, the need to develop physiologically similar skin models and three-dimensional human skin models has rapidly increased.”
Background
In vivo characterization of minipig skin as a model for dermatological research using multiphoton microscopy
Alex, A., Chaney, E. J., Žurauskas, M., Criley, J. M., Spillman, D. R., Hutchison, P. B., Li, J., Marjanović, M., Frey, S., Arp, Z. A., et al. (2020) · Experimental Dermatology · doi:10.1111/exd.14152 · Cited by 29 · see citing works
Is Tretinoin Still a Key Agent for Photoaging Management?
Ascenso, A., Ribeiro, H. M., Cabral-Marques, H. M., Oliveira, H., Santos, C., & Simões, S. (2014) · Mini-Reviews in Medicinal Chemistry · doi:10.2174/1389557514666140820102735 · Cited by 25 · see citing works
“These mechanisms may include accumulation of genome mutations and toxic metabolites, hormonal deprivation, increased ROS, and cross-linking of macromolecules by glycation [11].”
Background
Adipose Stem Cells with Conditioned Media for Treatment of Acne Vulgaris Scar
Shan, X., Choi, J. H., Kim, K. J., et al. (2018) · Tissue Engineering and Regenerative Medicine · doi:10.1007/s13770-017-0105-7 · Cited by 25 · see citing works
Antioxidant Potential-Rich Betel Leaves (Piper betle L.) Exert Depigmenting Action by Triggering Autophagy and Downregulating MITF/Tyrosinase In Vitro and In Vivo
Alam, M. B., Park, N. H., Song, B., & Lee, S. (2023) · Antioxidants · doi:10.3390/antiox12020374 · Cited by 24 · see citing works
“However, the use of animals in dermatological research has increased dramatically in recent years, allowing scientists to understand better the pathophysiological mechanisms underlying skin dis-ease and test potential preclinical therapies [59].”
Background
Macroenvironment-gene-microenvironment interactions in ultraviolet radiation-induced melanomagenesis
Mo, X., Preston, S., & Zaidi, M. R. (2019) · Advances in cancer research · doi:10.1016/bs.acr.2019.03.008 · Cited by 25 · see citing works
A 3D In Vitro Model for Burn Wounds: Monitoring of Regeneration on the Epidermal Level
Schneider, V., Kruse, D., de Mattos, I. B., et al. (2021) · Biomedicines · doi:10.3390/biomedicines9091153 · Cited by 23 · see citing works
“For example, in rodents the primary wound-healing mechanism is wound contraction, while in humans the primary process is reepithelialization and granulation [3,8,9].”
Background
Biomimetic Full-Thickness Skin-on-a-Chip Based on a Fibroblast-Derived Matrix
Zoio, P., Lopes‐Ventura, S., & Oliva, A. (2022) · Micro · doi:10.3390/micro2010013 · Cited by 23 · see citing works
The importance of immunity in the development of reliable animal models for psoriasis and atopic dermatitis
Guerrero‐Aspizua, S., Carretero, M., Conti, C. J., & Río, M. D. (2020) · Immunology and Cell Biology · doi:10.1111/imcb.12365 · Cited by 22 · see citing works
“Ovalbumin(68) and house dust mite(69,79) have been widely used to generate the disease in mice presenting a barrier defect phenotype, which is induced by different physical or targeted gene approaches.(28) Epicutaneous sensitization elicits the induction of antigen-specific IgE and a systemic Th2-skewed immune respons…”
BackgroundInfluential
The Experimental Animal Models in Psoriasis Research: A Comprehensive Review
Parab, S. B., & Doshi, G. (2023) · International Immunopharmacology · doi:10.1016/j.intimp.2023.109897 · Cited by 22 · see citing works
Beyond the MHC: A canine model of dermatomyositis shows a complex pattern of genetic risk involving novel loci
Evans, J. M., Noorai, R. E., Tsai, K. L., et al. (2017) · PLoS Genetics · doi:10.1371/journal.pgen.1006604 · Cited by 21 · see citing works
Bioconjugated Plasmonic Nanoparticles for Enhanced Skin Penetration
Alba-Molina, D., Giner-Casares, J. J., & Cano, M. (2019) · Topics in Current Chemistry · doi:10.1007/s41061-019-0273-0 · Cited by 21 · see citing works
Anti-bacterial, anti-fungal, and anti-inflammatory activities of wood vinegar: a potential remedy for major plant diseases and inflammatory reactions
Yıldızlı, G., Coral, G., & Ayaz, F. (2022) · Biomass Conversion and Biorefinery · doi:10.1007/s13399-022-02482-5 · Cited by 20 · see citing works
“Therefore, its topical application to the animals might suppress inflammatory skin diseases on the animals as well as on the humans [4, 42].”
A curated catalog of canine and equine keratin genes
Balmer, P., Bauer, A., Pujar, S., McGarvey, K. M., Welle, M. M., Galichet, A., Müller, E. J., Pruitt, K. D., Leeb, T., & Jagannathan, V. (2017) · PLoS ONE · doi:10.1371/journal.pone.0180359 · Cited by 20 · see citing works
The Development of Human Ex Vivo Models of Inflammatory Skin Conditions
Wang, E. H. C., Barresi‐Thornton, R., Chen, L.-C., Senna, M. M., Liao, I., Chen, Y., Zheng, Q., & Bouez, C. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms242417255 · Cited by 19 · see citing works
“These models serve as pre-clinical models for comprehending disease mechanisms and facilitating drug discovery [8–10].”
Method
A sustainable strategy for generating highly stable human skin equivalents based on fish collagen
Tan, S. H., Liu, S., Teoh, S. H., Bonnard, C., Leavesley, D. I., & Liang, K. (2024) · Biomaterials Advances · doi:10.1016/j.bioadv.2024.213780 · Cited by 20 · see citing works
Human pluripotent stem cells: An alternative for 3D in vitro modelling of skin disease
Khurana, P., Kolundžić, N., Flohr, C., & Ilić, D. (2021) · Experimental Dermatology · doi:10.1111/exd.14358 · Cited by 17 · see citing works
“Animal, in particular mouse models have been useful in aiding the development of therapies for skin diseases.[10] However, the physiological differences between animal and human skin have hindered the extrapolation of these advances to humans.”
Background
Self-Assembled Protein Vesicles as Vaccine Delivery Platform to Enhance Antigen-Specific Immune Responses
Li, Y., Rodriguez-Otero, M. R., & Champion, J. A. (2024) · Biomaterials · doi:10.1016/j.biomaterials.2024.122666 · Cited by 17 · see citing works
Recent advances in cutaneous drug delivery by iontophoresis
Gross, I. P., Lima, A. L., Barreto, L. C. L. D. S., et al. (2025) · Expert Opinion on Drug Delivery · doi:10.1080/17425247.2025.2490267 · Cited by 16 · see citing works
“As a result, these models may not fully capture the complex interactions between iontophoresis and physiological skin structures, leading to an oversim-plified assessment of drug penetration [77,78].”
Influential
Advances in tissue engineering and biofabrication for in vitro skin modeling
Wistner, S. C., Rashad, L., & Slaughter, G. E. (2023) · Bioprinting · doi:10.1016/j.bprint.2023.e00306 · Cited by 15 · see citing works
Exploring the efficacy of AHA–BHA infused nanofiber skin masks as a topical treatment for acne vulgaris
Tören, E., Mazari, A., & Buzgo, M. (2024) · Journal of Applied Polymer Science · doi:10.1002/app.55203 · Cited by 15 · see citing works
Poly (ɛ‐caprolactone)–chitosan–poly (vinyl alcohol) nanofibrous scaffolds for skin excisional and burn wounds in a canine model
Gholipour‐Kanani, A., Mohsenzadegan, M., Fayyazi, M., et al. (2018) · IET Nanobiotechnology · doi:10.1049/iet-nbt.2017.0115 · Cited by 15 · see citing works
Quantitative Photothermal Characterization with Bioprinted 3D Complex Tissue Constructs for Early‐Stage Breast Cancer Therapy Using Gold Nanorods
Nam, K., Jeong, C. B., Kim, H., Ahn, M., Ahn, S., Hur, H., Kim, D. U., Jang, J., Gwon, H., Lim, Y., et al. (2021) · Advanced Healthcare Materials · doi:10.1002/adhm.202100636 · Cited by 14 · see citing works
Whole-mount Confocal Microscopy for Adult Ear Skin: A Model System to Study Neuro-vascular Branching Morphogenesis and Immune Cell Distribution
Yamazaki, T., Li, W., & Mukouyama, Y. (2018) · Journal of Visualized Experiments · doi:10.3791/57406 · Cited by 14 · see citing works
Animal Models of Skin Disorders
Zhang, J. Y. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-809468-6.00015-2 · Cited by 13 · see citing works
Generation of a Simplified Three-Dimensional Skin-on-a-chip Model in a Micromachined Microfluidic Platform
Risueño, I., Valencia, L., Holgado, M., et al. (2021) · Journal of Visualized Experiments · doi:10.3791/62353 · Cited by 13 · see citing works
Nutraceuticals and skin appearance: Is there any evidence to support this growing trend?
Spiro, A., & Lockyer, S. (2018) · Nutrition Bulletin · doi:10.1111/nbu.12304 · Cited by 13 · see citing works
“…mouse model is also used extensively to study the mechanisms related to prevention and treatment of age-related skin changes, although it is recognised that human and murine skin have some fundamental differences (e.g. in thickness and responses to radiation) (Holzer et al. 2010; Avci et al. 2013).”
Background
Development of solid lipid microparticles (SLMs) containing asiatic acid for topical treatment of acne: Characterization, stability, in vitro and in vivo anti-acne assessment
Chutoprapat, R., Witarat, J., Jongpanyangarm, P., Mang Sung Thluai, L., Khankaew, P., & Wah Chan, L. (2024) · International Journal of Pharmaceutics · doi:10.1016/j.ijpharm.2024.123980 · Cited by 11 · see citing works
Advances in skin-mimetic platforms: A comprehensive review of drug permeation models
Suthar, D., Raut, R., & Bajaj, A. (2024) · Journal of Drug Delivery Science and Technology · doi:10.1016/j.jddst.2024.105887 · Cited by 11 · see citing works
Reconnoitring signaling pathways and exploiting innovative approaches tailoring multifaceted therapies for skin cancer
Datta, D., Sulthana, S., Strauss, J., Puri, A., Bandi, S. P., & Singh, S. K. (2024) · International Journal of Pharmaceutics · doi:10.1016/j.ijpharm.2024.124719 · Cited by 11 · see citing works
Persimmon leaf extract protects mice from atopic dermatitis by inhibiting T cell activation via regulation of the JNK pathway
Lee, H., Kim, E., Kim, G., & Jeong, G. (2021) · Phytotherapy Research · doi:10.1002/ptr.6985 · Cited by 11 · see citing works
“The most widely used animal models for studying dermatitis are AD, psoriasis, and contact hypersensitivity (Avci et al., 2013) models.”
Method
Anti-inflammatory activities of Dangyuja (Citrus grandis Osbeck) in concanavalin A stimulated murine splenocytes and 12-O-tetradecanoylphorbol-13-acetate-induced murine skin edema
Herath, K. H. I. N. M., Bing, S. J., Cho, J., Kim, A., Shin, S., Kim, G., Lee, J.-C., & Jee, Y. (2016) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2016.08.042 · Cited by 11 · see citing works
Dual-crosslinked injectable polysaccharide-based hydrogel with synergistic photothermal-controlled release of black phosphorus-baicalein for accelerating wound healing
Han, H., Wang, Z., Wu, T., et al. (2025) · Carbohydrate Polymers · doi:10.1016/j.carbpol.2025.124532 · Cited by 10 · see citing works
Establishment and translational evaluation of animal models for skin wound healing: a systematic review
Zhang, Y., Leng, K., Dong, M., Wu, J., Wang, Z., Zhu, Q., Gao, X., & Sun, Y. (2026) · Frontiers in Physiology · doi:10.3389/fphys.2026.1800001 · Cited by 11 · see citing works
Experimental Animal Models: Tools to Investigate Antidiabetic Activity
Jain, A. K., Madhariya, R., Dixena, B., Ram, A., & Vyas, A. (2022) · Current Pharmaceutical Design · doi:10.2174/1381612829666221220115649 · Cited by 10 · see citing works
Antipsoriatic effect of fatty acid enriched fraction of Vernonia anthelmintica Willd. fruits
Dogra, N. K., Kumar, S., Thakur, K., & Kumar, D. (2018) · Journal of Ethnopharmacology · doi:10.1016/j.jep.2018.05.038 · Cited by 10 · see citing works
Estimation of Biological Parameters of Cutaneous Ulcers Caused by Leishmaniasis in an Animal Model Using Diffuse Reflectance Spectroscopy
Botina-Monsalve, D. J., Franco, R., Murillo, J. D., et al. (2019) · Sensors · doi:10.3390/s19214674 · Cited by 10 · see citing works
“The golden hamster is recommended for CL studies, due to the similarity of the structure of its skin with respect to human skin [30,31].”
Background
Polysaccharide-based skin scaffolds with enhanced mechanical compatibility with native human skin
Malhotra, D., Pan, S., Rüther, L., Schlippe, G., Voss, W., & Germann, N. (2021) · Journal of the mechanical behavior of biomedical materials/Journal of mechanical behavior of biomedical materials · doi:10.1016/j.jmbbm.2021.104607 · Cited by 10 · see citing works
The First Cut Is the Deepest
Hobson, D. W., Schuh, J. C. L., Zurawski, D. V., et al. (2016) · International Journal of Toxicology · doi:10.1177/1091581816656804 · Cited by 10 · see citing works
“There are numerous small and large animal models of wound healing, and careful consideration of the pros and cons of each model or induction method needs to be understood to select the best wounding model for investigative or therapeutic studies.(9,10) Once the model or models are selected, the study must be designed…”
Method
Recent Trends in Nanocarriers for the Management of Atopic Dermatitis
Kumar, P., Ashawat, M. S., Pandit, V. R., et al. (2023) · Pharmaceutical Nanotechnology · doi:10.2174/2211738511666230330115229 · Cited by 9 · see citing works
Impetigo Animal Models: A Review of Their Feasibility and Clinical Utility for Therapeutic Appraisal of Investigational Drug Candidates
Abrha, S., Bartholomaeus, A., Tesfaye, W. H., & Thomas, J. (2020) · Antibiotics · doi:10.3390/antibiotics9100694 · Cited by 9 · see citing works
“There has been a preference for mice (Mus musculus) as a model for SSTIs in recent years and mice are currently the most widely employed animal to model skin and other infectious diseases [24,36,67], not only because of their relative genomic similarity with humans, but also because of their availability, ease of hand…”
Background
Barrier lipid composition and response to plasma lipids: A direct comparison of mouse dorsal back and ear skin
Cardoso, R. M., Absalah, S., Eck, M. V., & Bouwstra, J. A. (2020) · Experimental Dermatology · doi:10.1111/exd.14106 · Cited by 9 · see citing works
IFN-gamma role in granuloma formation in experimental subcutaneous cysticercosis
Freitas, A. A., Moura, V. B. L., Irusta, V. R. C., et al. (2016) · Experimental Parasitology · doi:10.1016/j.exppara.2016.06.004 · Cited by 8 · see citing works
Evaluation of lyophilized royal jelly and garlic extract emulgels using a murine model infected with methicillin-resistant Staphylococcus aureus
El-Gayar, M. H., Ishak, R. A. H., Esmat, A., et al. (2022) · AMB Express · doi:10.1186/s13568-022-01378-x · Cited by 8 · see citing works
“Many studies in the literature concerned with superficial skin infection in mice/rats (Aguiar et al. 2009; Kugelberg et al. 2005; Masson-Meyers et al. 2020; Guay 2003; Avci et al. 2013).”
Background
Preclinical techniques for drug discovery in psoriasis
Gujarathi, P. P., Korat, R., & Gujarathi, P. S. (2024) · International Immunopharmacology · doi:10.1016/j.intimp.2024.112378 · Cited by 8 · see citing works
Augmented Transcutaneous Stimulation Using an Injectable Electrode: A Computational Study
Verma, N., Graham, R., Mudge, J., et al. (2021) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2021.796042 · Cited by 8 · see citing works
“The domestic swine is a good model for human skin, with similar histological and biochemical properties, such as epidermal turnover time, subdermal adipose tissue, vasculature, and collagen structure, and arrangement in the dermis (Avci et al., 2013).”
BackgroundInfluential
Radiation dermatitis in the hairless mouse model mimics human radiation dermatitis
Lawrence, J., Seelig, D. M., Demos-Davies, K. M., Ferreira, C., Ren, Y., Wang, L., Alam, S. K., Yang, R., Guedes, A. G. P., Craig, A., et al. (2024) · Scientific Reports · doi:10.1038/s41598-024-76021-9 · Cited by 7 · see citing works
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Background
Treatment of experimentally induced partial-thickness burns in rats with different silver-impregnated dressings
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BackgroundInfluential
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Background
Topical ozonated virgin coconut oil improves wound healing and increases HSP90α, VEGF-A, EGF, bFGF and CD34 in diabetic ulcer mouse model of wound healing
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Authors: Avci, P., Sadasivam, M., Gupta, A., De Melo, W. C., Huang, Y.-Y., Yin, R., Chandran, R., Kumar, R., Otufowora, A., Nyame, T., & Hamblin, M. R.
Affiliations: Harvard University (US)
Amity University (IN)
Massachusetts General Hospital (US)
ORCID: Sadasivam, Magesh
Gupta, Asheesh
Huang, Ying-Ying
Yin, Rui
Chandran, Rakkiyappan
Kumar, Raj
Otufowora, Ayodeji
Hamblin, Michael R
Venue: Expert Opinion on Drug Discovery
Publisher: Informa UK Limited
Published: 2013-01-08
Volume: 8
Issue: 3
Pages: 331-355
ISSN: 1746-0441 (ISSN-L)
1746-045X
DOI: 10.1517/17460441.2013.761202
PMC: PMC3580014
OpenAlex: W2102728708
Cited by: 130
References: 190
Citations by year: 2026: 6 · 2025: 11 · 2024: 18 · 2023: 13 · 2022: 10 · 2021: 19 · 2020: 9 · 2019: 11 · 2018: 8 · 2017: 10 · 2016: 9 · 2015: 3 · 2014: 3
FWCI: 0.83
Type: journal article
Language: en
Open access: green
europepmc.org
Locations: Expert Opinion on Drug Discovery (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
UNIFESP Institutional Repository (Universidade Federal de São Paulo) (submittedVersion)
Funders: National Institute of Allergy and Infectious Diseases (R01AI050875)
Topics: Health Sciences › Medicine › Dermatology › Dermatology and Skin Diseases
Life Sciences › Pharmacology, Toxicology and Pharmaceutics › Pharmaceutical Science › Advancements in Transdermal Drug Delivery
Health Sciences › Medicine › Urology › Hair Growth and Disorders
Keywords: transgenic mouse model, inflammatory skin diseases, autoimmune skin disease, wound healing model, acne, leprosy, sunburn, sunscreen testing, hair loss
MeSH terms: Animals, Autoimmune Diseases, Disease Models, Animal, Inflammation, Skin Diseases, Drug Discovery

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