The molecular biology of chronic wounds and delayed healing in diabetes

Blakytny, R.; Jude, E.

doi:10.1111/j.1464-5491.2006.01773.x

Cited by 632Wound Healing and TreatmentsDiabetic Foot Ulcer Assessment and ManagementSkin Diseases and Diabetes

The molecular biology of chronic wounds and delayed healing in diabetes

Blakytny, R., Jude, E.·2006·Diabetic Medicine

DOI 10.1111/j.1464-5491.2006.01773.x

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Abstract

Wound healing is a complicated and integrated process. Although there is some tolerance in terms of redundancy and interrelated control mechanisms, pushing beyond such limits may contribute to delayed wound healing, and in extreme cases lead to chronic wounds/ulcers and thus potentially to lower extremity amputation. Diabetes is associated with such disruption in wound healing. Research in humans and in animal models has identified a large number of changes associated with diabetes at the molecular level in delayed wound healing and to a lesser extent in chronic diabetic ulcers. Better overall understanding of these changes and how they are interrelated would allow for specifically targeted treatment, thus ensuring improved quality of life for patients and providing savings to the high costs that are associated with all aspects of chronic diabetic ulcers. This review examines the work done at the molecular level on chronic diabetic ulcers, as well as considering changes seen in diabetes in general, both in humans and animal models, that may in turn contribute to ulcer formation.

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Diabetics typically have delayed and diminished wound healing.
“Diabetics typically suffer from delayed and diminished wound healing.127”
From Biocompatible Materials for Continuous Glucose Monitoring Devices (2013) · cites this paper as [127]
During impaired healing associated with diabetes, wounds exhibit prolonged accumulation of Mp associated with elevated levels of proinflammatory cytokines and proteases and reduced levels of various growth factors.
“During impaired healing associated with diabetes, wounds exhibit prolonged accumulation of Mp associated with elevated levels of proinflammatory cytokines and proteases and reduced levels of various growth factors (2,12,13).”
From Sustained Inflammasome Activity in Macrophages Impairs Wound Healing in Type 2 Diabetic Humans and Mice (2014) · cites this paper as [2]

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The Role of Macrophages in Acute and Chronic Wound Healing and Interventions to Promote Pro-wound Healing Phenotypes
Krzyszczyk, P., Schloss, R. S., Palmer, A. F., & Francois Berthiaume, B. (2018) · Frontiers in Physiology · doi:10.3389/fphys.2018.00419 · Cited by 1,562 · see citing works
Inflammation in Chronic Wounds
Zhao, R., Liang, H. H., Clarke, E., Jackson, C., & Xue, M. (2016) · International Journal of Molecular Sciences · doi:10.3390/ijms17122085 · Cited by 1,201 · see citing works
Pathogenesis and Treatment of Impaired Wound Healing in Diabetes Mellitus: New Insights
Baltzis, D., Eleftheriadou, I., & Veves, A. (2014) · Advances in Therapy · doi:10.1007/s12325-014-0140-x · Cited by 730 · see citing works
Curcumin as a wound healing agent
Akbik, D., Ghadiri, M., Chrzanowski, W., & Rohanizadeh, R. (2014) · Life Sciences · doi:10.1016/j.lfs.2014.08.016 · Cited by 710 · see citing works
Exosomes derived from human adipose mensenchymal stem cells accelerates cutaneous wound healing via optimizing the characteristics of fibroblasts
Hu, L., Wang, J., Zhou, X., Xiong, Z., Zhao, J., Yu, R., Huang, F., Zhang, H., & Chen, L. (2016) · Scientific Reports · doi:10.1038/srep32993 · Cited by 678 · see citing works
Nitric Oxide Therapy for Diabetic Wound Healing
Malone‐Povolny, M. J., Maloney, S. E., & Schoenfisch, M. H. (2019) · Advanced Healthcare Materials · doi:10.1002/adhm.201801210 · Cited by 509 · see citing works
The pathology of the foreign body reaction against biomaterials
Klopfleisch, R., & Jung, F. (2017) · Journal of Biomedical Materials Research Part A · doi:10.1002/jbm.a.35958 · Cited by 524 · see citing works
The Role of Chemokines in Wound Healing
Ridiandries, A., Tan, J. T. M., & Bursill, C. A. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19103217 · Cited by 479 · see citing works
Exosomes from adipose‐derived stem cells and application to skin wound healing
An, Y., Lin, S., Tan, X.-J., Zhu, S., Nie, F., Zhen, Y., Gu, L., Zhang, C., Wang, B., Wei, W., et al. (2021) · Cell Proliferation · doi:10.1111/cpr.12993 · Cited by 473 · see citing works
Blocking Interleukin-1β Induces a Healing-Associated Wound Macrophage Phenotype and Improves Healing in Type 2 Diabetes
Mirza, R. E., Fang, M. M., Ennis, W. J., & Koh, T. J. (2013) · Diabetes · doi:10.2337/db12-1450 · Cited by 459 · see citing works
Advanced Growth Factor Delivery Systems in Wound Management and Skin Regeneration
Park, J. K., Hwang, S. Y., & Yoon, I. (2017) · Molecules · doi:10.3390/molecules22081259 · Cited by 415 · see citing works
Curcumin loaded chitosan nanoparticles impregnated into collagen-alginate scaffolds for diabetic wound healing
Karri, V. V. S. R., Kuppusamy, G., Talluri, S. V., Mannemala, S. S., Kollipara, R., Wadhwani, A. D., Mulukutla, S., Raju, K. R. S., & Malayandi, R. (2016) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2016.05.038 · Cited by 393 · see citing works
Promotion of skin regeneration in diabetic rats by electrospun core-sheath fibers loaded with basic fibroblast growth factor
Yang, Y., Xia, T., Zhi, W., Li, W., Weng, J., Zhang, C., & Li, X. (2011) · Biomaterials · doi:10.1016/j.biomaterials.2011.02.042 · Cited by 349 · see citing works
Biocompatible Materials for Continuous Glucose Monitoring Devices
Nichols, S. P., Koh, A., Storm, W. L., Shin, J. H., & Schoenfisch, M. H. (2013) · Chemical Reviews · doi:10.1021/cr300387j · Cited by 347 · see citing works
Dysregulation of monocyte/macrophage phenotype in wounds of diabetic mice
Mirza, R., & Koh, T. J. (2011) · Cytokine · doi:10.1016/j.cyto.2011.06.016 · Cited by 342 · see citing works
Fibrin-based scaffold incorporating VEGF- and bFGF-loaded nanoparticles stimulates wound healing in diabetic mice
Losi, P., Briganti, E., Errico, C., Lisella, A., Sanguinetti, E., Chiellini, E., & Soldani, G. (2013) · Acta Biomaterialia · doi:10.1016/j.actbio.2013.04.019 · Cited by 335 · see citing works
Sustained Inflammasome Activity in Macrophages Impairs Wound Healing in Type 2 Diabetic Humans and Mice
Mirza, R. E., Fang, M. M., Weinheimer-Haus, E. M., Ennis, W. J., & Koh, T. J. (2014) · Diabetes · doi:10.2337/db13-0927 · Cited by 319 · see citing works
“During impaired healing associated with diabetes, wounds exhibit prolonged accumulation of Mp associated with elevated levels of proinflammatory cytokines and proteases and reduced levels of various growth factors (2,12,13).”
Background
Fibronectin in development and wound healing
Patten, J., & Wang, K. (2020) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2020.09.005 · Cited by 303 · see citing works
Macrophage Related Chronic Inflammation in Non-Healing Wounds
Li, M., Hou, Q., Zhong, L., Zhao, Y., & Fu, X. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.681710 · Cited by 299 · see citing works
Inflammation and neuropeptides: the connection in diabetic wound healing
Pradhan, L., Nabzdyk, C. S., Andersen, N. D., LoGerfo, F. W., & Veves, A. (2009) · Expert Reviews in Molecular Medicine · doi:10.1017/s1462399409000945 · Cited by 286 · see citing works
An Essential Role of NRF2 in Diabetic Wound Healing
Long, M., de la Vega, M. R., Wen, Q., Bharara, M., Jiang, T., Zhang, R., Zhou, S., Wong, P. K., Wondrak, G. T., Zheng, H., et al. (2015) · Diabetes · doi:10.2337/db15-0564 · Cited by 268 · see citing works
Nitric Oxide: A Key Mediator of Biofilm Dispersal with Applications in Infectious Diseases
Barraud, N., Kelso, M. J., Rice, S., & Kjelleberg, S. J. (2014) · Current Pharmaceutical Design · doi:10.2174/1381612820666140905112822 · Cited by 255 · see citing works
Self‐Assembled Wound Dressings Silence MMP‐9 and Improve Diabetic Wound Healing In Vivo
Castleberry, S. A., Almquist, B. D., Li, W., Reis, T. C., Chow, J., Mayner, S., & Hammond, P. T. (2015) · Advanced Materials · doi:10.1002/adma.201503565 · Cited by 253 · see citing works
Biofilm-Innate Immune Interface: Contribution to Chronic Wound Formation
Versey, Z., Nizer, W. S. D. C., Russell, E., Zigic, S., DeZeeuw, K. G., Marek, J. E., Overhage, J., & Cassol, E. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.648554 · Cited by 268 · see citing works
Pro-Inflammatory Chemokine CCL2 (MCP-1) Promotes Healing in Diabetic Wounds by Restoring the Macrophage Response
Wood, S. J., Jayaraman, V., Huelsmann, E., Bonish, B., Burgad, D., Sivaramakrishnan, G., Qin, S., DiPietro, L., Zloza, A., Zhang, C., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0091574 · Cited by 252 · see citing works
‘See-saw’ expression of microRNA-198 and FSTL1 from a single transcript in wound healing
Sundaram, G. M., Common, J. E. A., Gopal, F. E., Srikanta, S., Lakshman, K., Lunny, D. P., Lim, T. C., Tanavde, V., Lane, E. B., & Sampath, P. (2013) · Nature · doi:10.1038/nature11890 · Cited by 231 · see citing works
Abnormal Cell Responses and Role of TNF- α in Impaired Diabetic Wound Healing
Xu, F., Zhang, C., & Graves, D. T. (2013) · BioMed Research International · doi:10.1155/2013/754802 · Cited by 231 · see citing works
Transdermal deferoxamine prevents pressure-induced diabetic ulcers
Duscher, D., Neofytou, E. A., Wong, V., Maan, Z. N., Rennert, R. C., Inayathullah, M., Januszyk, M., Rodrigues, M., Malkovskiy, A. V., Whitmore, A. J., et al. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1413445112 · Cited by 227 · see citing works
The Role of MicroRNA-146a in the Pathogenesis of the Diabetic Wound-Healing Impairment
Xu, J., Wu, W., Zhang, L., Dorset-Martin, W., Morris, M. W., Mitchell, M. E., & Liechty, K. W. (2012) · Diabetes · doi:10.2337/db12-0145 · Cited by 225 · see citing works
Physiological role of reactive oxygen species as promoters of natural defenses
Roy, J., Galano, J., Durand, T., Guennec, J. L., & Lee, J. C. (2017) · The FASEB Journal · doi:10.1096/fj.201700170r · Cited by 223 · see citing works
Mesenchymal stem cells induce dermal fibroblast responses to injury
Smith, A. N., Willis, E., Chan, V. T., Muffley, L. A., Isik, F. F., Gibran, N. S., & Hocking, A. M. (2009) · Experimental Cell Research · doi:10.1016/j.yexcr.2009.08.001 · Cited by 219 · see citing works
Chitosan–hyaluronic acid/VEGF loaded fibrin nanoparticles composite sponges for enhancing angiogenesis in wounds
Mohandas, A., Anisha, B. S., Chennazhi, K. P., & Jayakumar, R. (2015) · Colloids and Surfaces B Biointerfaces · doi:10.1016/j.colsurfb.2015.01.024 · Cited by 218 · see citing works
Pharmacological Activity and Clinical Use of PDRN
Squadrito, F., Bitto, A., Irrera, N., Pizzino, G., Pallio, G., Minutoli, L., & Altavilla, D. (2017) · Frontiers in Pharmacology · doi:10.3389/fphar.2017.00224 · Cited by 215 · see citing works
From Inflammation to Current and Alternative Therapies Involved in Wound Healing
Serra, M. B., Barroso, W. A., da Silva, N. N., Silva, S. D. N., Borges, A. C. R., Abreu, I. C., & Borges, M. O. D. R. (2017) · International Journal of Inflammation · doi:10.1155/2017/3406215 · Cited by 202 · see citing works
Antimicrobial properties of nitric oxide and its application in antimicrobial formulations and medical devices
Jones, M. L., Ganopolsky, J. G., Labbé, A., Wahl, C., & Prakash, S. (2010) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-010-2733-x · Cited by 196 · see citing works
The biology of chronic foot ulcers in persons with diabetes
Sibbald, R. G., & Woo, K. Y. (2008) · Diabetes/Metabolism Research and Reviews · doi:10.1002/dmrr.847 · Cited by 197 · see citing works
The Electrical Response to Injury: Molecular Mechanisms and Wound Healing
Reid, B., & Zhao, M. (2013) · Advances in Wound Care · doi:10.1089/wound.2013.0442 · Cited by 195 · see citing works
Engineered Biopolymeric Scaffolds for Chronic Wound Healing
Dickinson, L. E., & Gerecht, S. (2016) · Frontiers in Physiology · doi:10.3389/fphys.2016.00341 · Cited by 195 · see citing works
Curcumin nanofibers for the purpose of wound healing
Fereydouni, N., Darroudi, M., Movaffagh, J., Shahroodi, A., Butler, A. E., Ganjali, S., & Sahebkar, A. (2018) · Journal of Cellular Physiology · doi:10.1002/jcp.27362 · Cited by 197 · see citing works
Hyperglycaemic conditions decrease cultured keratinocyte mobility: implications for impaired wound healing in patients with diabetes
Lan, C.-C. E., Liu, I.-H., Fang, A.-H., Wen, C.-H., & Wu, C.-S. (2008) · British Journal of Dermatology · doi:10.1111/j.1365-2133.2008.08789.x · Cited by 183 · see citing works
Angiogenic properties of dehydrated human amnion/chorion allografts: therapeutic potential for soft tissue repair and regeneration
Koob, T. J., Lim, J. J., Massee, M., Zabek, N., Rennert, R. C., Gurtner, G. C., & Li, W. W. (2014) · Vascular Cell · doi:10.1186/2045-824x-6-10 · Cited by 180 · see citing works
Macrophage PPARγ and impaired wound healing in type 2 diabetes
Mirza, R. E., Fang, M. M., Novak, M. L., Urao, N., Sui, A., Ennis, W. J., & Koh, T. J. (2015) · The Journal of Pathology · doi:10.1002/path.4548 · Cited by 177 · see citing works
Early detection and monitoring of chronic wounds using low-cost, omniphobic paper-based smart bandages
Pal, A., Goswami, D., Cuellar, H. E., Castro, B., Kuang, S., & Martínez, R. V. (2018) · Biosensors and Bioelectronics · doi:10.1016/j.bios.2018.06.060 · Cited by 175 · see citing works
Low Cost Inkjet Printed Smart Bandage for Wireless Monitoring of Chronic Wounds
Farooqui, M. F., & Shamim, A. (2016) · Scientific Reports · doi:10.1038/srep28949 · Cited by 173 · see citing works
Stimuli‐Responsive Delivery of Growth Factors for Tissue Engineering
Qu, M., Jiang, X., Zhou, X., Wang, C., Wu, Q., Ren, L. M., Zhu, J., Zhu, S., Tebon, P. J., Sun, W., et al. (2020) · Advanced Healthcare Materials · doi:10.1002/adhm.201901714 · Cited by 178 · see citing works
The Role of Phytochemicals in the Inflammatory Phase of Wound Healing
Shah, A., & Amini‐Nik, S. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18051068 · Cited by 172 · see citing works
MicroRNA signature in diabetic wound healing: promotive role of miR‐21 in fibroblast migration
Madhyastha, R., Madhyastha, H., Nakajima, Y., Omura, S., & Maruyama, M. (2012) · International Wound Journal · doi:10.1111/j.1742-481x.2011.00890.x · Cited by 168 · see citing works
Acceleration of diabetic wound healing with chitosan-crosslinked collagen sponge containing recombinant human acidic fibroblast growth factor in healing-impaired STZ diabetic rats
Wang, W., Lin, S., Xiao, Y., Huang, Y., Tan, Y., Cai, L., & Li, X. (2007) · Life Sciences · doi:10.1016/j.lfs.2007.11.009 · Cited by 167 · see citing works
Enhanced susceptibility to infections in a diabetic wound healing model
Hirsch, T., Spielmann, M., Zuhaili, B., Koehler, T., Fossum, M., Steinau, H., Yao, F., Steinstraesser, L., Onderdonk, A. B., & Eriksson, E. K. (2008) · BMC Surgery · doi:10.1186/1471-2482-8-5 · Cited by 166 · see citing works
Antioxidant Therapy and Antioxidant-Related Bionanomaterials in Diabetic Wound Healing
Zhang, W., Chen, L., Xiong, Y., Panayi, A. C., Abududilibaier, A., Hu, Y., Yu, C., Zhou, W., Sun, Y., Liu, M., et al. (2021) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2021.707479 · Cited by 163 · see citing works
Topical gel-based biomaterials for the treatment of diabetic foot ulcers
Bardill, J. R., Laughter, M. R., Stager, M. A., Liechty, K. W., Krebs, M. D., & Zgheib, C. (2021) · Acta Biomaterialia · doi:10.1016/j.actbio.2021.10.045 · Cited by 168 · see citing works
In Vivo Assessment of Printed Microvasculature in a Bilayer Skin Graft to Treat Full-Thickness Wounds
Yanez, M., Rincon, J. E., Dones, A., Maria, C. D., Gonzales, R., & Boland, T. (2014) · Tissue Engineering Part A · doi:10.1089/ten.tea.2013.0561 · Cited by 159 · see citing works
Evidence-based Management of PAD & the Diabetic Foot
Brownrigg, J. R. W., Apelqvist, J., Bakker, K., Schaper, N. C., & Hinchliffe, R. J. (2013) · European Journal of Vascular and Endovascular Surgery · doi:10.1016/j.ejvs.2013.02.014 · Cited by 162 · see citing works
Porous Hyaluronic Acid Hydrogels for Localized Nonviral DNA Delivery in a Diabetic Wound Healing Model
Tokatlian, T., Cam, C., & Segura, T. (2015) · Advanced Healthcare Materials · doi:10.1002/adhm.201400783 · Cited by 145 · see citing works
Characterization of Self-Assembled Polyelectrolyte Complex Nanoparticles Formed from Chitosan and Pectin
Birch, N. P., & Schiffman, J. D. (2014) · Langmuir · doi:10.1021/la500491c · Cited by 145 · see citing works
Wound Chronicity, Impaired Immunity and Infection in Diabetic Patients
Rodríguez-Rodríguez, N., Martínez-Jiménez, I., Ojalvo, A. G., Mendoza‐Marí, Y., Guillén, G. E., Armstrong, D. G., & Berlanga‐Acosta, J. (2021) · MEDICC Review · doi:10.37757/mr2021.v23.n3.8 · Cited by 147 · see citing works
Enhanced wound healing properties of guar gum/curcumin-stabilized silver nanoparticle hydrogels
Bhubhanil, S., Talodthaisong, C., Khongkow, M., Namdee, K., Wongchitrat, P., Yingmema, W., Hutchison, J. A., Lapmanee, S., & Kulchat, S. (2021) · Scientific Reports · doi:10.1038/s41598-021-01262-x · Cited by 145 · see citing works
Heat Shock Proteins in Diabetes and Wound Healing
Atalay, M., Oksala, N., Lappalainen, J., Laaksonen, D. E., Sen, C. K., & Roy, S. (2009) · Current Protein and Peptide Science · doi:10.2174/138920309787315202 · Cited by 144 · see citing works
Electrospun Fibers with Plasmid bFGF Polyplex Loadings Promote Skin Wound Healing in Diabetic Rats
Yang, Y., Xia, T., Chen, F., Wei, W., Liu, C., He, S., & Li, X. (2011) · Molecular Pharmaceutics · doi:10.1021/mp200246b · Cited by 143 · see citing works
Neurotensin-loaded collagen dressings reduce inflammation and improve wound healing in diabetic mice
Moura, L. I. F., Dias, A. M. A., Suesca, E., Casadiegos, S., Leal, E. C., Fontanilla, M. R., Carvalho, L., de Sousa, H. C., & Carvalho, E. (2013) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2013.10.009 · Cited by 135 · see citing works
Effects of structurally stabilized EGF and bFGF on wound healing in type I and type II diabetic mice
Choi, S. M., Lee, K.-M., Kim, H. J., Park, I. K., Kang, H. J., Shin, H., Baek, D., Choi, Y., Park, K. H., & Lee, J. W. (2017) · Acta Biomaterialia · doi:10.1016/j.actbio.2017.11.045 · Cited by 134 · see citing works
Exosomal PD‐L1 functions as an immunosuppressant to promote wound healing
Su, D., Tsai, H., Xu, Z., Yan, F., Wu, Y., Xiao, Y., Liu, X., Wu, Y., Parvanian, S., Zhu, W., et al. (2019) · Journal of Extracellular Vesicles · doi:10.1080/20013078.2019.1709262 · Cited by 129 · see citing works
Regulation of impaired angiogenesis in diabetic dermal wound healing by microRNA-26a
Icli, B., Nabzdyk, C., Lujan-Hernandez, J., Cahill, M., Auster, M., Wara, A., Sun, X., Ozdemir, D., Giatsidis, G., Orgill, D., et al. (2016) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2016.01.007 · Cited by 116 · see citing works
Benefit-Risk Assessment of Becaplermin in the Treatment of Diabetic Foot Ulcers
Παπάνας, Ν., & Maltezos, E. S. (2010) · Drug Safety · doi:10.2165/11534570-000000000-00000 · Cited by 125 · see citing works
Proteome analysis reveals antiangiogenic environments in chronic wounds of diabetes mellitus type 2 patients
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Authors: Blakytny, R., & Jude, E.
Affiliations: Fachklinik Hornheide (DE)
Tameside Hospital (GB)
Corresponding author: Jude, E.
ORCID: Jude, E.
Venue: Diabetic Medicine
Publisher: Wiley
Published: 2006-02-13
Volume: 23
Issue: 6
Pages: 594-608
ISSN: 0742-3071 (ISSN-L)
1464-5491
DOI: 10.1111/j.1464-5491.2006.01773.x
OpenAlex: W1967162280
Cited by: 632
References: 224
Citations by year: 2026: 13 · 2025: 32 · 2024: 34 · 2023: 50 · 2022: 38 · 2021: 65 · 2020: 41 · 2019: 36 · 2018: 32 · 2017: 38 · 2016: 43 · 2015: 37 · 2014: 40 · 2013: 31 · 2012: 22
FWCI: 2.23
Type: journal article
Language: en
Open access: closed
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations: Diabetic Medicine (publishedVersion)
PubMed (publishedVersion)
Funders: Deutsche Forschungsgemeinschaft
Topics: Health Sciences › Medicine › Rehabilitation › Wound Healing and Treatments
Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Diabetic Foot Ulcer Assessment and Management
Health Sciences › Medicine › Dermatology › Skin Diseases and Diabetes
Keywords: chronic wounds, diabetic ulcers, delayed wound healing, diabetes mellitus, molecular mechanisms, lower limb amputation, animal models of diabetes
MeSH terms: Animals, Diabetes Mellitus, Experimental, Extracellular Matrix, Glucose, Humans, Nitric Oxide, Oxidation-Reduction, Skin, Wound Healing, Cytokines, Intercellular Signaling Peptides and Proteins, Diabetes Complications

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The molecular biology of chronic wounds and delayed healing in diabetes

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