Exploring the “Hair Growth–Wound Healing Connection”: Anagen Phase Promotes Wound Re-Epithelialization
Open accessAbstract
When the skin is damaged, a variety of cell types must migrate, proliferate, and differentiate to reform a functional barrier to the external environment. Recent studies have shown that progenitor cells residing in hair follicles (HFs) are able to contribute to this re-epithelialization of wounds in vivo. However, the influence of the hair cycle on wound healing has not previously been addressed. Here, we have exploited spontaneous postnatal hair-cycle synchronicity in mice to systematically examine the influence of the different hair-cycle stages on murine skin wound healing. We report significant acceleration of healing during the anagen phase of HF cycling in vivo, associated with alterations in epithelial, endothelial, and inflammatory cell types. Intriguingly, gene profiling data reveal a clear correlation between the transcription of genes beneficial for wound healing and those upregulated during the anagen phase of the hair cycle in unwounded skin. These findings, which demonstrate a previously unappreciated association between HF cycling and wound healing, reveal numerous molecular correlates for further investigation.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The pattern and stage of hair growth in different regions of mouse skin can significantly affect rates of skin healing in mouse tissue.
“Indeed, the pattern and stage of hair growth in different regions of the mouse skin can significantly affect rates of skin healing in mouse tissue (114).”
From Wound repair and regeneration: Mechanisms, signaling, and translation (2014) · cites this paper as [114]
Cites
Junqueira, L. C. U., Bignolas, G., & Brentani, H. (1979) · The Histochemical Journal · doi:10.1007/bf01002772 · Cited by 2,570 · see citing works
Defining the Epithelial Stem Cell Niche in Skin
Tumbar, T., Guasch, G., Greco, V., Blanpain, C., Lowry, W. E., Rendl, M., & Fuchs, E. (2004) · Science · doi:10.1126/science.1092436 · Cited by 2,031 · see citing works
Identifying biological themes within lists of genes with EASE
Hosack, D. A., Dennis, G., Sherman, B. T., Lane, H. C., & Lempicki, R. A. (2003) · Genome biology · doi:10.1186/gb-2003-4-10-r70 · Cited by 1,950 · see citing works
Controls of Hair Follicle Cycling
Stenn, K. S., & Paus, R. (2001) · Physiological Reviews · doi:10.1152/physrev.2001.81.1.449 · Cited by 1,520 · see citing works
Self-citationMüller-Röver, S., Foitzik, K., Paus, R., Handjiski, B., van der Veen, C., Eichmüller, S., McKay, I. A., & Stenn, K. S. (2001) · Journal of Investigative Dermatology · doi:10.1046/j.0022-202x.2001.01377.x · Cited by 1,375 · see citing works
Self-citationIto, M., Liu, Y., Yang, Z., Nguyen, J., Liang, F., Morris, R. J., & Cotsarelis, G. (2005) · Nature Medicine · doi:10.1038/nm1328 · Cited by 1,317 · see citing works
MIF Signal Transduction Initiated by Binding to CD74
Leng, L., Metz, C. N., Fang, Y., Xu, J., Donnelly, S., Baugh, J., Delohery, T., Chen, Y., Mitchell, R. A., & Bucala, R. (2003) · The Journal of Experimental Medicine · doi:10.1084/jem.20030286 · Cited by 1,154 · see citing works
The Hair Follicle as a Dynamic Miniorgan
Schneider, M. R., Schmidt-Ullrich, R., & Paus, R. (2009) · Current Biology · doi:10.1016/j.cub.2008.12.005 · Cited by 1,119 · see citing works
Self-citationDominant role of the niche in melanocyte stem-cell fate determination
Nishimura, E. K., Jordan, S. A., Oshima, H., Yoshida, H., Osawa, M., Moriyama, M., Jackson, I. J., Barrandon, Y., Miyachi, Y., & Nishikawa, S. (2002) · Nature · doi:10.1038/416854a · Cited by 900 · see citing works
Horak, E., Klenk, N., Leek, R., LeJeune, S., Smith, K. J., Stuart, N. S. A., Harris, A. L., Greenall, M. J., & Stepniewska, K. (1992) · The Lancet · doi:10.1016/0140-6736(92)93150-l · Cited by 800 · see citing works
<i>Lgr6</i> Marks Stem Cells in the Hair Follicle That Generate All Cell Lineages of the Skin
Snippert, H. J., Haegebarth, A., Kasper, M., Jaks, V., van Es, J. H., Barker, N., van de Wetering, M., van den Born, M., Begthel, H., Vries, R. G., et al. (2010) · Science · doi:10.1126/science.1184733 · Cited by 751 · see citing works
Control of hair growth and follicle size by VEGF-mediated angiogenesis
Yano, K., Brown, L. F., & Detmar, M. (2001) · Journal of Clinical Investigation · doi:10.1172/jci11317 · Cited by 710 · see citing works
CD44 Is the Signaling Component of the Macrophage Migration Inhibitory Factor-CD74 Receptor Complex
Shi, X., Leng, L., Wang, T., Wang, W., Du, X., Li, J., McDonald, C., Chen, Z., Murphy, J. W., Lolis, E., et al. (2006) · Immunity · doi:10.1016/j.immuni.2006.08.020 · Cited by 679 · see citing works
Couffinhal, T., Silver, M., Zheng, L., Kearney, M., Witzenbichler, B., & Isner, J. M. (1998) · Europe PMC (PubMed Central) · Cited by 672 · see citing works
Estrogen accelerates cutaneous wound healing associated with an increase in TGF-β1 levels
Ashcroft, G. S., Dodsworth, J., Boxtel, E. V., Tarnuzzer, R. W., Horan, M. A., Schultz, G. S., & Ferguson, M. W. J. (1997) · Nature Medicine · doi:10.1038/nm1197-1209 · Cited by 573 · see citing works
Chase, H. B. (1954) · Physiological Reviews · doi:10.1152/physrev.1954.34.1.113 · Cited by 553 · see citing works
Distinct Stem Cell Populations Regenerate the Follicle and Interfollicular Epidermis
Levy, V., Lindon, C., Harfe, B. D., & Morgan, B. A. (2005) · Developmental Cell · doi:10.1016/j.devcel.2005.11.003 · Cited by 419 · see citing works
Epidermal stem cells arise from the hair follicle after wounding
Levy, V., Lindon, C., Zheng, Y., Harfe, B. D., & Morgan, B. A. (2007) · The FASEB Journal · doi:10.1096/fj.06-6926com · Cited by 386 · see citing works
Paus, R., Nickoloff, B. J., & ITO, T. (2004) · Trends in Immunology · doi:10.1016/j.it.2004.09.014 · Cited by 325 · see citing works
Self-citationTargeting Connexin43 Expression Accelerates the Rate of Wound Repair
Qiu, C. X., Coutinho, P., Frank, S., Franke, S., Law, L. Y., Martin, P. B., Green, C. R., & Becker, D. L. (2003) · Current Biology · doi:10.1016/j.cub.2003.09.007 · Cited by 284 · see citing works
Exploring the role of stem cells in cutaneous wound healing
Lau, K., Paus, R., Tiede, S., Day, P., & Bayat, A. (2009) · Experimental Dermatology · doi:10.1111/j.1600-0625.2009.00942.x · Cited by 279 · see citing works
Self-citationHair follicle dermal cells differentiate into adipogenic and osteogenic lineages
Jahoda, C. A. B., Whitehouse, C. J., Reynolds, A. J., & Hole, N. (2003) · Experimental Dermatology · doi:10.1111/j.0906-6705.2003.00161.x · Cited by 267 · see citing works
Active Hair Growth (Anagen) is Associated with Angiogenesis
Mecklenburg, L., Tobin, D. J., Müller‐Röver, S., Handjiski, B., Wendt, G., Peters, E. M. J., Pohl, S., Moll, I., & Paus, R. (2000) · Journal of Investigative Dermatology · doi:10.1046/j.1523-1747.2000.00954.x · Cited by 265 · see citing works
Self-citationCritical Stages of Hair Development and Pigmentation in the Mouse
Chase, H. B., Rauch, H., & Smith, V. W. (1951) · Physiological Zoology · doi:10.1086/physzool.24.1.30152098 · Cited by 254 · see citing works
Hair follicle dermal sheath cells: unsung participants in wound healing
Jahoda, C. A. B., & Reynolds, A. J. (2001) · The Lancet · doi:10.1016/s0140-6736(01)06532-1 · Cited by 248 · see citing works
Plasticity of hair follicle dermal cells in wound healing and induction
Gharzi, A., Reynolds, A. J., & Jahoda, C. A. B. (2003) · Experimental Dermatology · doi:10.1034/j.1600-0625.2003.00106.x · Cited by 236 · see citing works
Telogen skin contains an inhibitor of hair growth
Paus, R., Stenn, K. S., & LINK, R. E. (1990) · British Journal of Dermatology · doi:10.1111/j.1365-2133.1990.tb06266.x · Cited by 236 · see citing works
Self-citationKloepper, J. E., Tiede, S., Brinckmann, J., Reinhardt, D. P., Meyer, W., Faessler, R., & Paus, R. (2008) · Experimental Dermatology · doi:10.1111/j.1600-0625.2008.00720.x · Cited by 197 · see citing works
Self-citationLangton, A. K., Herrick, S. E., & Headon, D. J. (2007) · Journal of Investigative Dermatology · doi:10.1038/sj.jid.5701178 · Cited by 186 · see citing works
Hair follicle stem cells: Walking the maze
Tiede, S., Kloepper, J. E., Bodó, E., Tiwari, S., Kruse, C., & Paus, R. (2007) · European Journal of Cell Biology · doi:10.1016/j.ejcb.2007.03.006 · Cited by 176 · see citing works
Self-citationMolecular biology of hair morphogenesis: Development and cycling
Botchkarev, V. A., & Paus, R. (2003) · Journal of Experimental Zoology Part B Molecular and Developmental Evolution · doi:10.1002/jez.b.33 · Cited by 168 · see citing works
Self-citationThélu, J., Rossio, P., & Favier, B. (2002) · BMC Dermatology · doi:10.1186/1471-5945-2-7 · Cited by 164 · see citing works
Ellison, T. I., Smith, M. K., Gilliam, A. C., & MacDonald, P. N. (2008) · Journal of Investigative Dermatology · doi:10.1038/jid.2008.131 · Cited by 159 · see citing works
Estrogen, not intrinsic aging, is the major regulator of delayed human wound healing in the elderly
Hardman, M. J., & Ashcroft, G. S. (2008) · Genome Biology · doi:10.1186/gb-2008-9-5-r80 · Cited by 157 · see citing works
Self-citationAbnormal Connexin Expression Underlies Delayed Wound Healing in Diabetic Skin
Wang, C. M., Lincoln, J., Cook, J. E., & Becker, D. L. (2007) · Diabetes · doi:10.2337/db07-0613 · Cited by 156 · see citing works
Notch1 is essential for postnatal hair follicle development and homeostasis
Vauclair, S., Nicolas, M., Barrandon, Y., & Radtke, F. (2005) · Developmental Biology · doi:10.1016/j.ydbio.2005.05.018 · Cited by 145 · see citing works
Ligand-Independent Actions of the Vitamin D Receptor Maintain Hair Follicle Homeostasis
Skorija, K., Cox, M. K., Sisk, J. M., Dowd, D. R., MacDonald, P. N., Thompson, C. C., & Demay, M. B. (2004) · Molecular Endocrinology · doi:10.1210/me.2004-0415 · Cited by 143 · see citing works
Generation and Cyclic Remodeling of the Hair Follicle Immune System in Mice
Paus, R., van der Veen, C., Eichmüller, S. B., Kopp, T., Hagen, E., Müller‐Röver, S., & Hofmann, U. (1998) · Journal of Investigative Dermatology · doi:10.1046/j.1523-1747.1998.00243.x · Cited by 141 · see citing works
Self-citationPremature aging in vitamin D receptor mutant mice
Keisala, T., Minasyan, A., Lou, Y., Zou, J., Kalueff, A. V., Pyykkö, I. V., & Tuohimaa, P. (2009) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2009.03.007 · Cited by 132 · see citing works
Defective Epidermal Barrier in Neonatal Mice Lacking the C-Terminal Region of Connexin43
Maass, K., Ghanem, A., Kim, J.-S., Saathoff, M., Urschel, S., Kirfel, G., Grümmer, R., Kretz, M., Lewalter, T., Tiemann, K., et al. (2004) · Molecular Biology of the Cell · doi:10.1091/mbc.e04-04-0324 · Cited by 129 · see citing works
Growth and differentiation of hair follicles between periods of activity and quiescence
Straile, W. E., Chase, H. B., & Arsenault, C. T. (1961) · Journal of Experimental Zoology · doi:10.1002/jez.1401480304 · Cited by 118 · see citing works
Macrophage Migration Inhibitory Factor
Hardman, M. J., Waite, A., Zeef, L. A. H., Burow, M. E., Nakayama, T., & Ashcroft, G. S. (2005) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)61241-2 · Cited by 101 · see citing works
Self-citationTseng, H., & Green, H. (1994) · The Journal of Cell Biology · doi:10.1083/jcb.126.2.495 · Cited by 99 · see citing works
Lin, K., Chudova, D. I., Hatfield, G. W., Smyth, P., & D, B. A. M. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0407114101 · Cited by 92 · see citing works
Regeneration after experimental removal of skin in man
Bishop, G. H. (1945) · American Journal of Anatomy · doi:10.1002/aja.1000760202 · Cited by 87 · see citing works
Wnt signaling in skin organogenesis
Widelitz, R. B. (2008) · Organogenesis · doi:10.4161/org.4.2.5859 · Cited by 85 · see citing works
Delayed Wound Healing and Epidermal Hyperproliferation in Mice Lacking JunB in the Skin
Florin, L., Knebel, J., Zigrino, P., Vonderstrass, B., Mauch, C., Schorpp-Kistner, M., Szabowski, A., & Angel, P. (2006) · Journal of Investigative Dermatology · doi:10.1038/sj.jid.5700123 · Cited by 79 · see citing works
Expression and Activity of Arginase Isoenzymes During Normal and Diabetes-Impaired Skin Repair
Kämpfer, H., Pfeilschifter, J. M., & Frank, S. (2003) · Journal of Investigative Dermatology · doi:10.1046/j.1523-1747.2003.12610.x · Cited by 75 · see citing works
Lee, J., Basak, J. M., Demehri, S., & Kopan, R. (2007) · Development · doi:10.1242/dev.02868 · Cited by 72 · see citing works
Ohnemus, U. G., Paus, R., Ünalan, M., & Handjiski, B. (2004) · Journal of Investigative Dermatology · doi:10.1046/j.0022-202x.2003.22120.x · Cited by 70 · see citing works
Self-citationTiede, S., Kloepper, J. E., Ernst, N., Poeggeler, B., Kruse, C., & Paus, R. (2009) · Journal of Investigative Dermatology · doi:10.1038/jid.2009.148 · Cited by 66 · see citing works
Self-citationEpidermal JunB represses G-CSF transcription and affects haematopoiesis and bone formation
Meixner, A., Zenz, R., Schönthaler, H. B., Kenner, L., Scheuch, H., Penninger, J. M., & Wagner, E. F. (2008) · Nature Cell Biology · doi:10.1038/ncb1761 · Cited by 50 · see citing works
Standard depth burns in the rat: The importance of the hair growth cycle
Zawacki, B. E., & Jones, R. J. (1967) · British Journal of Plastic Surgery · doi:10.1016/s0007-1226(67)80065-1 · Cited by 45 · see citing works
Basonuclin-Null Mutation Impairs Homeostasis and Wound Repair in Mouse Corneal Epithelium
Zhang, X., & Tseng, H. (2007) · PLoS ONE · doi:10.1371/journal.pone.0001087 · Cited by 34 · see citing works
Pepper, F. J. (1954) · Journal of Morphology · doi:10.1002/jmor.1050950305 · Cited by 28 · see citing works
The Anagen Hair Cycle Induces Systemic Immunosuppression of Contact Hypersensitivity in Mice
Hofmann, U., TOKURA, Y., Rückert, R., & Paus, R. (1998) · Cellular Immunology · doi:10.1006/cimm.1998.1258 · Cited by 20 · see citing works
Self-citationEpidemiology and Economic Impact of Foot Ulcers
LeMaster, J. W., & Reiber, G. E. (2006) · doi:10.1002/0470029374.ch1 · Cited by 14 · see citing works
Delayed wound healing in elderly people
Thomason, H. A., & Hardman, M. J. (2009) · Reviews in Clinical Gerontology · doi:10.1017/s095925980999027x · Cited by 13 · see citing works
Self-citationPlucking during telogen induces apoptosis in the lower part of hair follicles
Matsuo, K., Mori, O., & Hashimoto, T. (2003) · Archives of Dermatological Research · doi:10.1007/s00403-003-0384-9 · Cited by 12 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Wound repair and regeneration: Mechanisms, signaling, and translation
Eming, S. A., Martin, P., & Tomic-Canic, M. (2014) · Science Translational Medicine · doi:10.1126/scitranslmed.3009337 · Cited by 3,562 · see citing works
Epithelialization in Wound Healing: A Comprehensive Review
Pastar, I., Stojadinović, O., Yin, N. C., Ramirez, H. A., Nusbaum, A. G., Sawaya, A. P., Patel, S. B., Khalid, L., Isseroff, R. R., & Tomic‐Canic, M. (2014) · Advances in Wound Care · doi:10.1089/wound.2013.0473 · Cited by 1,549 · see citing works
Wound Healing and Skin RegenerationPreprint
Takeo, M., Lee, W., & Ito, M. (2015) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a023267 · Cited by 681 · see citing works
Smart Bandage for Monitoring and Treatment of Chronic Wounds
Mostafalu, P., Tamayol, A., Rahimi, R., Ochoa, M., Khalilpour, A., Kiaee, G., Yazdi, I. K., Bagherifard, S., Dokmeci, M. R., Ziaie, B., et al. (2018) · Small · doi:10.1002/smll.201703509 · Cited by 482 · see citing works
How UV Light Touches the Brain and Endocrine System Through Skin, and Why
Slominski, A. T., Zmijewski, M. A., Plonka, P. M., Szaflarski, J. P., & Paus, R. (2018) · Endocrinology · doi:10.1210/en.2017-03230 · Cited by 452 · see citing works
Self-citationSkin and Its Regenerative Powers: An Alliance between Stem Cells and Their Niche
Gonzales, K. A. U., & Fuchs, E. (2017) · Developmental Cell · doi:10.1016/j.devcel.2017.10.001 · Cited by 414 · see citing works
Bian, D., Wu, Y., Song, G., Azizi, R., & Zamani, A. (2022) · Stem Cell Research & Therapy · doi:10.1186/s13287-021-02697-9 · Cited by 383 · see citing works
Research Techniques Made Simple: Animal Models of Wound Healing
Grada, A. A., Mervis, J. S., & Falanga, V. (2018) · Journal of Investigative Dermatology · doi:10.1016/j.jid.2018.08.005 · Cited by 342 · see citing works
Microbial symbionts accelerate wound healing via the neuropeptide hormone oxytocin
Poutahidis, T., Kearney, S. M., Levkovich, T., Qi, P., Varian, B. J., Lakritz, J. R., Ibrahim, Y. M., Chatzigiagkos, A., Alm, E. J., & Erdman, S. E. (2013) · PLoS ONE · doi:10.1371/journal.pone.0078898 · Cited by 310 · see citing works
Organ-Level Quorum Sensing Directs Regeneration in Hair Stem Cell Populations
Chen, C., Wang, L., Plikus, M. V., Jiang, T. X., Murray, P. J., Ramos, R., Guerrero‐Juarez, C. F., Hughes, M. W., Lee, O. K., Shi, S., et al. (2015) · Cell · doi:10.1016/j.cell.2015.02.016 · Cited by 245 · see citing works
Zhou, W., Qiao, Z., Zare, E. N., Huang, J., Zheng, X.-Q., Sun, X., Shao, M., Wang, H., Wang, X., Chen, D., et al. (2020) · Journal of Medicinal Chemistry · doi:10.1021/acs.jmedchem.9b02115 · Cited by 212 · see citing works
Luo, Z., & Zhang, S. (2012) · Chemical Society Reviews · doi:10.1039/c2cs15360b · Cited by 207 · see citing works
Wang, X.-S., Chen, H.-Y., Tian, R.-Y., Zhang, Y., Drutskaya, M., Wang, C., Ge, J.-F., Fan, Z., Kong, D., Wang, X.-X., et al. (2017) · Nature Communications · doi:10.1038/ncomms14091 · Cited by 208 · see citing works
Epithelial stem cells and implications for wound repair
Plikus, M. V., Gay, D. L., Treffeisen, E. R., Wang, A., Supapannachart, R. J., & Cotsarelis, G. (2012) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2012.10.001 · Cited by 199 · see citing works
Macrophages Contribute to the Cyclic Activation of Adult Hair Follicle Stem Cells
Castellana, D., Paus, R., & Pérez‐Moreno, M. (2014) · PLoS Biology · doi:10.1371/journal.pbio.1002002 · Cited by 189 · see citing works
Self-citationProinflammatory cytokines regulate epidermal stem cells in wound epithelialization
Xiao, T., Yan, Z., Xiao, S., & Xia, Y. (2020) · Stem Cell Research & Therapy · doi:10.1186/s13287-020-01755-y · Cited by 196 · see citing works
Resting no more: re‐defining telogen, the maintenance stage of the hair growth cycle
Geyfman, M., Plikus, M. V., Treffeisen, E. R., D, B. A. M., & Paus, R. (2014) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/brv.12151 · Cited by 173 · see citing works
Self-citationLef1 expression in fibroblasts maintains developmental potential in adult skin to regenerate wounds
Phan, Q. M., Fine, G. M., Salz, L., Herrera, G. G., Wildman, B., Driskell, I. M., & Driskell, R. R. (2020) · eLife · doi:10.7554/elife.60066 · Cited by 170 · see citing works
Hair transplantation: Basic overview
Jiménez, F., Alam, M. A., Vogel, J. E., & Avram, M. R. (2021) · Journal of the American Academy of Dermatology · doi:10.1016/j.jaad.2021.03.124 · Cited by 141 · see citing works
Olfactory receptor OR2AT4 regulates human hair growth
Chéret, J., Bertolini, M., Ponce, L., Lehmann, J., Tsai, T., Alam, M. A., Hatt, H. H., & Paus, R. (2018) · Nature Communications · doi:10.1038/s41467-018-05973-0 · Cited by 135 · see citing works
Self-citationMardaryev, A. N., Meier, N. T., Poterlowicz, K., Sharov, A. A., Sharova, T. Y., Ahmed, M. I., Rapisarda, V., Lewis, C. J., Fessing, M. Y., Rünger, T. M., et al. (2011) · Development · doi:10.1242/dev.070284 · Cited by 129 · see citing works
Self-citationNeuroendocrinology of the hair follicle: principles and clinical perspectives
Paus, R., Langan, E. A., Vidali, S., Ramot, Y., & D, B. A. M. (2014) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2014.06.002 · Cited by 122 · see citing works
Self-citationRepeated Microneedle Stimulation Induces Enhanced Hair Growth in a Murine Model
Kim, Y., Jeong, K. H., Kim, J. E., Woo, Y. J., Kim, B. J., & Kang, H. (2016) · Annals of Dermatology · doi:10.5021/ad.2016.28.5.586 · Cited by 116 · see citing works
Wound healing related agents: Ongoing research and perspectives
Kaplani, K., Koutsi, S., Armenis, V., Skondra, F. G., Karantzelis, N., Tsaniras, S. C., & Taraviras, S. L. (2018) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2018.02.007 · Cited by 105 · see citing works
MicroRNA-132 with Therapeutic Potential in Chronic Wounds
Li, X., Li, D., Wang, A., Chu, T., Lohcharoenkal, W., Zheng, X., Grünler, J., Narayanan, S., Eliasson, S., Herter, E. K., et al. (2017) · Journal of Investigative Dermatology · doi:10.1016/j.jid.2017.08.003 · Cited by 103 · see citing works
Notch Regulates Macrophage-Mediated Inflammation in Diabetic Wound Healing
Kimball, A., Joshi, A., Boniakowski, A. E., Schaller, M. A., Chung, J., Allen, R., Bermick, J., Carson, W. F., Henke, P. K., Maillard, I. P., et al. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.00635 · Cited by 101 · see citing works
Flynn, K., Mahmoud, N. N., Sharifi, S., Gould, L. J., & Mahmoudi, M. (2023) · ACS Pharmacology & Translational Science · doi:10.1021/acsptsci.3c00030 · Cited by 101 · see citing works
A statistical analysis of murine incisional and excisional acute wound models
Ansell, D. M., Campbell, L., Thomason, H. A., Brass, A., & Hardman, M. J. (2014) · Wound Repair and Regeneration · doi:10.1111/wrr.12148 · Cited by 93 · see citing works
Self-citationThe histone methyltransferase Setd8 acts in concert with c-Myc and is required to maintain skin
Driskell, I., Oda, H., Blanco, S., Nascimento, E. M., Humphreys, P., & Frye, M. (2011) · EMBO Journal · doi:10.1038/emboj.2011.421 · Cited by 93 · see citing works
A Beginner’s Introduction to Skin Stem Cells and Wound Healing
Garcia, D. D., Filipová, A., Veloz, I. G., & Martínez‐Fierro, M. L. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222011030 · Cited by 92 · see citing works
A matter of life and death: stem cell survival in tissue regeneration and tumour formation
Soteriou, D., & Fuchs, Y. (2018) · Nature Reviews Cancer · doi:10.1038/nrc.2017.122 · Cited by 87 · see citing works
Martínez, M. L. M., Escario, E., Poblet, E., Sánchez, D., Buchón, F.-F., Izeta, A., & Jiménez, F. (2016) · Journal of the American Academy of Dermatology · doi:10.1016/j.jaad.2016.02.1161 · Cited by 84 · see citing works
TRPV1: Role in Skin and Skin Diseases and Potential Target for Improving Wound Healing
Bagood, M. D., & Isseroff, R. R. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22116135 · Cited by 82 · see citing works
From frog integument to human skin: dermatological perspectives from frog skin biology
Haslam, I. S., Roubos, E. W., Mangoni, M. L., Yoshizato, K., Vaudry, H., Kloepper, J. E., Pattwell, D. M., MADERSON, P. F. A., & Paus, R. (2013) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/brv.12072 · Cited by 82 · see citing works
Self-citationMSCs and their exosomes: a rapidly evolving approach in the context of cutaneous wounds therapy
Marofi, F., Alexandrovna, K. I., Margiana, R., Bahramali, M., Suksatan, W., Abdelbasset, W. K., Chupradit, S., Nasimi, M., & Maashi, M. S. (2021) · Stem Cell Research & Therapy · doi:10.1186/s13287-021-02662-6 · Cited by 78 · see citing works
Reproducible strategy for excisional skin-wound-healing studies in mice
Yampolsky, M., Bachelet, I., & Fuchs, Y. (2023) · Nature Protocols · doi:10.1038/s41596-023-00899-4 · Cited by 77 · see citing works
Ahmadi, H., Amini, A., Fathabady, F. F., Mostafavinia, A., Zare, F., Ebrahimpour‐Malekshah, R., Ghalibaf, M. N., Abrisham, M., Rezaei, F., Albright, R., et al. (2020) · Stem Cell Research & Therapy · doi:10.1186/s13287-020-01967-2 · Cited by 67 · see citing works
Endogenous retinoids in the hair follicle and sebaceous gland
Everts, H. B. (2011) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2011.08.017 · Cited by 66 · see citing works
Bae, J. M., Jung, H. M., Goo, B., & Park, Y. M. (2015) · Lasers in Surgery and Medicine · doi:10.1002/lsm.22358 · Cited by 65 · see citing works
A pilot clinical study of hair grafting in chronic leg ulcers
Jiménez, F., Garde, C., Poblet, E., Jimeno, B., Ortiz, J., Martínez, M. L., Gutiérrez‐Rivera, A., Pérez‐López, V., Etxaniz, U., Naveda, C., et al. (2012) · Wound Repair and Regeneration · doi:10.1111/j.1524-475x.2012.00846.x · Cited by 65 · see citing works
Jiménez, F., Poblet, E., & Izeta, A. (2014) · Experimental Dermatology · doi:10.1111/exd.12521 · Cited by 64 · see citing works
Liang, X., Bhattacharya, S., Bajaj, G., Guha, G., Wang, Z., Jang, H. S., Leid, M. E., Indra, A. K., & Ganguli‐Indra, G. (2012) · PLoS ONE · doi:10.1371/journal.pone.0029999 · Cited by 62 · see citing works
Macrophage ferroportin is essential for stromal cell proliferation in wound healing
Recalcati, S., Gammella, E., Buratti, P., Doni, A., Anselmo, A., Locati, M., & Cairo, G. (2018) · Haematologica · doi:10.3324/haematol.2018.197517 · Cited by 57 · see citing works
Cutaneous Wound Healing in Diabetic Mice Is Improved by Topical Mineralocorticoid Receptor Blockade
Nguyen, V. T., Farman, N., Palacios, R., Sbeih, M., Béhar‐Cohen, F., Aractingi, S., & Jaisser, F. (2019) · Journal of Investigative Dermatology · doi:10.1016/j.jid.2019.04.030 · Cited by 60 · see citing works
Augmenting Endogenous Wnt Signaling Improves Skin Wound Healing
Whyte, J. L., Smith, A. A., Liu, B., Manzano, W., Evans, N. D., Dhamdhere, G. R., Fang, M. Y., Chang, H. Y., Oro, A. E., & Helms, J. A. (2013) · PLoS ONE · doi:10.1371/journal.pone.0076883 · Cited by 61 · see citing works
Vagnozzi, A. N., Reiter, J. F., & Wong, S. Y. (2015) · Cell Cycle · doi:10.1080/15384101.2015.1090062 · Cited by 61 · see citing works
Kruglikov, I. L., & Scherer, P. E. (2016) · Experimental Dermatology · doi:10.1111/exd.12941 · Cited by 61 · see citing works
Jing, Y., Huang, T., Zhao, B., Zhao, L., Zhang, N., Zhang, K., Wang, K., Wang, J., Hua, J., & Tu, Q. (2024) · Chemical Engineering Journal · doi:10.1016/j.cej.2024.150561 · Cited by 60 · see citing works
Restoration of skin pigmentation after deep partial or full-thickness burn injury
Dai, N., Chang, H., Wang, Y.-W., Fu, K., Huang, T., Huang, N.-C., Li, J.-K., Hsieh, P., Dai, L., Hsu, C.-K., et al. (2017) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2017.10.010 · Cited by 58 · see citing works
Morgun, E. I., & Vorotelyak, E. A. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.581697 · Cited by 56 · see citing works
Probiotic ‘glow of health’: it's more than skin deep
Erdman, S. E., & Poutahidis, T. (2014) · Beneficial Microbes · doi:10.3920/bm2013.0042 · Cited by 56 · see citing works
Dermal Fibroblast Heterogeneity and Its Contribution to the Skin Repair and Regeneration
Xue, M., Zhao, R., MARCH, L. M., & Jackson, C. (2021) · Advances in Wound Care · doi:10.1089/wound.2020.1287 · Cited by 55 · see citing works
Thyrotropin-Releasing Hormone (TRH) Promotes Wound Re-Epithelialisation in Frog and Human Skin
Meier, N. T., Haslam, I. S., Pattwell, D. M., Zhang, G.-Y., Emelianov, V. U., Paredes, R., Debus, E. S., Augustin, M., Funk, W., Amaya, E., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0073596 · Cited by 55 · see citing works
Self-citationHair Follicle Bulge Stem Cells Appear Dispensable for the Acute Phase of Wound Re-epithelialization
Garcin, C. L., Ansell, D. M., Headon, D. J., Paus, R., & Hardman, M. J. (2016) · Stem Cells · doi:10.1002/stem.2289 · Cited by 54 · see citing works
Self-citationStudying Hair Growth Cycle and its Effects on Mouse Skin
Wang, W., Ramos, R., Tai, K., Wu, Y.-S., Chang, T.-Y., Yan, J.-Y., Plikus, M. V., Oh, J. W., & Lin, S. (2023) · Journal of Investigative Dermatology · doi:10.1016/j.jid.2023.04.015 · Cited by 54 · see citing works
Zhu, D., Hu, Y., Kong, X., Luo, Y., Zhang, Y., Wu, Y., Tan, J., Chen, J., Xu, T., & Zhu, L. (2024) · Regenerative Biomaterials · doi:10.1093/rb/rbae035 · Cited by 53 · see citing works
Hair Restoration Surgery: The State of the Art
Vogel, J. E., Jiménez, F., Cole, J. P., Keene, S. A., Harris, J. A., Barrera, A., & Rose, P. T. (2012) · Aesthetic Surgery Journal · doi:10.1177/1090820x12468314 · Cited by 53 · see citing works
The Hair Follicle: An Underutilized Source of Cells and Materials for Regenerative Medicine
Kiani, M. T., Higgins, C. A., & Almquist, B. D. (2017) · ACS Biomaterials Science & Engineering · doi:10.1021/acsbiomaterials.7b00072 · Cited by 51 · see citing works
Poblet, E., Jiménez, F., Escario-Travesedo, E., Hardman, J. A., Hernández, I., Agudo-Mena, J. L., Cabrera, J. J., Nicu, C., & Paus, R. (2018) · British Journal of Dermatology · doi:10.1111/bjd.16436 · Cited by 48 · see citing works
Self-citationMultifaceted role of hair follicle dermal cells in bioengineered skins
Higgins, C. A., Roger, M., Hill, R. P., Ali-Khan, A. S., Garlick, J. A., Christiano, A. M., & Jahoda, C. A. B. (2016) · British Journal of Dermatology · doi:10.1111/bjd.15087 · Cited by 42 · see citing works
Studying Wound Repair in the Mouse
Tan, N. S., & Wahli, W. (2013) · Current Protocols in Mouse Biology · doi:10.1002/9780470942390.mo130135 · Cited by 42 · see citing works
Oda, Y., Hu, L., Nguyen, T., Fong, C., Tu, C., & Bikle, D. D. (2017) · Endocrinology · doi:10.1210/en.2017-00061 · Cited by 40 · see citing works
Loss of epidermal MMP-14 expression interferes with angiogenesis but not with re-epithelialization
Zigrino, P., Ayachi, O., Schild, A., Kaltenberg, J., Zamek, J., Nischt, R., Koch, M., & Mauch, C. (2012) · European Journal of Cell Biology · doi:10.1016/j.ejcb.2012.05.003 · Cited by 39 · see citing works
A Multimodal Assessment of Melanin and Melanocyte Activity in Abnormally Pigmented Hypertrophic Scar
Travis, T. E., Ghassemi, P., Ramella‐Roman, J. C., Prindeze, N. J., Paul, D. W., Moffatt, L. T., Jordan, M. H., & Shupp, J. W. (2014) · Journal of Burn Care & Research · doi:10.1097/bcr.0000000000000154 · Cited by 38 · see citing works
Shikimic acid, a mannose bioisostere, promotes hair growth with the induction of anagen hair cycle
Choi, M., Choi, S., Jang, S., Choi, H., Kang, B., Hwang, S., & Kwon, O. (2019) · Scientific Reports · doi:10.1038/s41598-019-53612-5 · Cited by 38 · see citing works
Johansson, J. A., & Headon, D. J. (2013) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2013.12.007 · Cited by 37 · see citing works
Preclinical models for wound-healing studies
Pastar, I., Liang, L., Sawaya, A. P., Wikramanayake, T. C., Glinos, G. D., Drakulich, S., Chen, V., Stojadinović, O., Davis, S. C., & Tomic‐Canic, M. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-810545-0.00010-3 · Cited by 39 · see citing works
Exploring the “brain-skin connection”: Leads and lessons from the hair follicle
Paus, R. (2016) · Current Research in Translational Medicine · doi:10.1016/j.retram.2016.10.003 · Cited by 36 · see citing works
Self-citationTopical α‐gal nanoparticles accelerate diabetic wound healing
Kaymakcalan, O. E., Abadeer, A. I., Goldufsky, J. W., Galili, U., Karinja, S. J., Dong, X., Jin, J., Samadi, A., & Spector, J. A. (2020) · Experimental Dermatology · doi:10.1111/exd.14084 · Cited by 37 · see citing works
Zhang, C., Tan, C. K., McFarlane, C., Sharma, M., Tan, N. S., & Kambadur, R. (2012) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00179.2011 · Cited by 32 · see citing works
The Wound Reporting in Animal and Human Preclinical Studies (WRAHPS) Guidelines
Ojeh, N. O., Vecin, N. M., Pastar, I., Volk, S. W., Wilgus, T. A., Griffiths, S., Ramey-Ward, A. N., Driver, V. R., DiPietro, L. A., Gould, L. J., et al. (2024) · Wound Repair and Regeneration · doi:10.1111/wrr.13232 · Cited by 32 · see citing works
Are hair follicle stem cells promising candidates for wound healing?
Li, B., Hu, W., Ma, K., Zhang, C., & Fu, X. (2018) · Expert Opinion on Biological Therapy · doi:10.1080/14712598.2019.1559290 · Cited by 31 · see citing works
Chen, F., Zhang, Q., Wu, P., Zhao, Y., Suo, X., Xiao, A., Ke, M., He, X., Tong, Z., & Chen, Y. (2020) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2020.11.154 · Cited by 31 · see citing works
Lim, Y. Y., Kim, S. Y., Kim, H. M., Li, K., Kim, M. N., Park, K.-C., & Kim, B. J. (2014) · Clinical and Experimental Dermatology · doi:10.1111/ced.12241 · Cited by 31 · see citing works
Thyroxine (T4) may promote re-epithelialisation and angiogenesis in wounded human skin ex vivo
Zhang, G.-Y., Langan, E. A., Meier, N. T., Funk, W., Siemers, F., & Paus, R. (2019) · PLoS ONE · doi:10.1371/journal.pone.0212659 · Cited by 31 · see citing works
Self-citationVazquez-Ayala, L., del Angel-Olarte, C., Escobar‐García, D. M., Rosales‐Mendoza, S., Solis-Andrade, I., Pozos‐Guillén, A., & Palestino, G. (2023) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2023.127691 · Cited by 30 · see citing works
Morus alba Root Extract Induces the Anagen Phase in the Human Hair Follicle Dermal Papilla Cells
Hyun, J., Im, J., Kim, S., Kim, H. Y., Seo, I., & Bhang, S. H. (2021) · Pharmaceutics · doi:10.3390/pharmaceutics13081155 · Cited by 29 · see citing works
Choi, H., Kim, D. Y., Choi, S., Shin, C.-Y., Hwang, S., Kim, K. H., & Kwon, O. (2018) · Journal of Dermatological Science · doi:10.1016/j.jdermsci.2018.04.005 · Cited by 29 · see citing works
Foster, A. R., Nicu, C., Schneider, M. R., Hinde, E., & Paus, R. (2018) · Archives of Dermatological Research · doi:10.1007/s00403-018-1831-y · Cited by 28 · see citing works
Self-citationLoss of γδ T Cells Results in Hair Cycling Defects
Kloepper, J. E., Kawai, K., Bertolini, M., Kanekura, T., & Paus, R. (2013) · Journal of Investigative Dermatology · doi:10.1038/jid.2013.17 · Cited by 28 · see citing works
Self-citationSilver oxysalts promote cutaneous wound healing independent of infection
Thomason, H. A., Lovett, J. M., Spina, C. J., Stephenson, C., McBain, A. J., & Hardman, M. J. (2018) · Wound Repair and Regeneration · doi:10.1111/wrr.12627 · Cited by 28 · see citing works
Self-citationMigrating melanocyte stem cells: masters of disaster?
Paus, R. (2013) · Nature Medicine · doi:10.1038/nm.3264 · Cited by 25 · see citing works
Self-citationOzonated Oils and Cutaneous Wound Healing
Lim, Y., Lee, H., Woodby, B. L., & Valacchi, G. (2019) · Current Pharmaceutical Design · doi:10.2174/1381612825666190702100504 · Cited by 24 · see citing works
Alam, M. A., Bertolini, M., Gherardini, J., Keren, A., Ponce, L., Chéret, J., Alenfall, J., Dunér, P., Nilsson, A. H., Gilhar, A., et al. (2019) · British Journal of Dermatology · doi:10.1111/bjd.18479 · Cited by 22 · see citing works
Self-citationHematopoietic Stem Cells in Wound Healing Response
Urao, N., Liu, J., Takahashi, K., & Ganesh, G. (2021) · Advances in Wound Care · doi:10.1089/wound.2021.0065 · Cited by 22 · see citing works
Biçer, M. (2024) · Archives of Dermatological Research · doi:10.1007/s00403-024-03055-4 · Cited by 21 · see citing works
Injury modifies the fate of hair follicle dermal stem cell progeny in a hair cycle‐dependent manner
Abbasi, S., & Biernaskie, J. A. (2019) · Experimental Dermatology · doi:10.1111/exd.13924 · Cited by 21 · see citing works
Tomaszewski, K. L., Blanchard, M., Olaniyi, R., Brenton, H. R., Hayes, S., Fatma, F., Amarasinghe, G. K., Cho, B.-K., Goo, Y. A., DeDent, A. C., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-52714-7 · Cited by 20 · see citing works
MSC-EVs and UCB-EVs promote skin wound healing and spatial transcriptome analysis
Li, R., Wang, H., Wang, X., Yang, Y., Zhong, K., Zhang, X., & Li, H. (2025) · Scientific Reports · doi:10.1038/s41598-025-87592-6 · Cited by 20 · see citing works
Potential effects of shift work on skin autoimmune diseases
Stenger, S., Graßhoff, H., Hundt, J. E., & Lange, T. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2022.1000951 · Cited by 21 · see citing works
Immune-mediated alopecias and their mechanobiological aspects
Watson, V. E., Faniel, M. L., Kamili, N. A., Krueger, L. D., & Zhu, C. (2022) · Cells and Development · doi:10.1016/j.cdev.2022.203793 · Cited by 19 · see citing works
Evaluating STZ-Induced Impaired Wound Healing in Rats
Ansell, D. M., Marsh, C., Walker, L., Hardman, M. J., & Holden, K. A. (2017) · Journal of Investigative Dermatology · doi:10.1016/j.jid.2017.10.020 · Cited by 19 · see citing works
Self-citationIn vitro models to study hair follicle generation
Korosec, A., & Lichtenberger, B. M. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-810545-0.00012-7 · Cited by 18 · see citing works
Advances in engineered organoid models of skin for biomedical research
Zeng, D., Li, S., Du, F., Xia, Y., Zhang, J., Yu, S., & Qin, J. (2025) · Burns & Trauma · doi:10.1093/burnst/tkaf016 · Cited by 20 · see citing works
Frontiers in the physiology of male pattern androgenetic alopecia: beyond the androgen horizon
Altendorf, S., Bertolini, M., Riche, A. L., Tosti, A., & Paus, R. (2025) · Physiological Reviews · doi:10.1152/physrev.00005.2024 · Cited by 17 · see citing works
Self-citationEctodysplasin A Pathway Contributes to Human and Murine Skin Repair
Garcin, C. L., Huttner, K. M., Kirby, N., Schneider, P., & Hardman, M. J. (2016) · Journal of Investigative Dermatology · doi:10.1016/j.jid.2015.09.002 · Cited by 17 · see citing works
Self-citationPhysiology and Pathophysiology of Wound Healing in Diabetes
Stojadinović, O., Pastar, I., Gordon, K. A., & Tomic‐Canic, M. (2012) · Humana Press eBooks · doi:10.1007/978-1-61779-791-0_7 · Cited by 16 · see citing works
Post, H., Hundt, J. E., Zhang, G., Depping, R., Rosé, C., Langan, E. A., & Paus, R. (2020) · Archives of Dermatological Research · doi:10.1007/s00403-020-02092-z · Cited by 15 · see citing works
Self-citationAlam, M. A., Cooley, J. E., Plotczyk, M., Martínez-Martin, M. S., Izeta, A., Paus, R., & Jiménez, F. (2019) · Dermatologic Surgery · doi:10.1097/dss.0000000000001748 · Cited by 14 · see citing works
Self-citationEffects of CO2 fractional laser on hair growth in C57BL/6 mice and potential underlying mechanisms
Zhuo, F., Li, L., Cai, L., & Huang, Y. M. (2019) · Chinese Medical Journal · doi:10.1097/cm9.0000000000000220 · Cited by 14 · see citing works
- Authors
- Ansell, D. M., Kloepper, J. E., Thomason, H. A., Paus, R., & Hardman, M. J.
- Affiliations
- University of Manchester (GB)
- University of Lübeck (DE)
- Corresponding author
- Hardman, Matthew J.
- Venue
- Journal of Investigative Dermatology
- Publisher
- Elsevier BV
- Published
- 2011-02
- Volume
- 131
- Issue
- 2
- Pages
- 518-528
- ISSN
- 0022-202X (ISSN-L)
- OpenAlex
- W2109605961
- Cited by
- 171
- References
- 59
- Citations by year
- 2026: 8 · 2025: 13 · 2024: 11 · 2023: 9 · 2022: 11 · 2021: 11 · 2020: 14 · 2019: 16 · 2018: 16 · 2017: 15 · 2016: 11 · 2015: 5 · 2014: 10 · 2013: 8 · 2012: 8
- FWCI
- 9.15
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Journal of Investigative Dermatology (publishedVersion)
- PubMed (publishedVersion)
- Research Explorer (The University of Manchester) (submittedVersion)
- Funders
- Manchester Biomedical Research Centre
- Biotechnology and Biological Sciences Research Council
- Topics
- Health Sciences › Medicine › Urology › Hair Growth and Disorders
- Health Sciences › Medicine › Rehabilitation › Wound Healing and Treatments
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Skin and Cellular Biology Research
- Keywords
- hair cycle, anagen phase, wound healing, re-epithelialization, skin wound healing, gene expression profiling, inflammatory cells, endothelial cells
- MeSH terms
- Animals, Cell Cycle, Cell Movement, Epithelial Cells, Female, Mice, Inbred C57BL, Regeneration, Skin, Skin Physiological Phenomena, Wound Healing, Hair Follicle, Neovascularization, Physiologic, Models, Animal, Mice
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review