Cellular and molecular mechanisms of repair in acute and chronic wound healing

British Journal of Dermatology

Volumn 173, Issue 2, 2015, Pages 370-378

  Martin, P ^a   Nunan, R ^b  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b CARDIFF UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACUTE WOUND; ANGIOGENESIS; CHRONIC WOUND; CYTOLOGY; DECUBITUS; DERMIS; DIABETIC FOOT; DROSOPHILA; EPITHELIZATION; GRANULATION TISSUE; HUMAN; IMMUNE RESPONSE; INFLAMMATION; INNERVATION; KELOID; LEG ULCER; MEDICAL RESEARCH; MOLECULAR GENETICS; NONHUMAN; PRIORITY JOURNAL; REVIEW; SCAR FORMATION; SKIN INJURY; SKIN REPAIR; TISSUE REPAIR; WOUND; WOUND HEALING; WOUND HEALING IMPAIRMENT; ZEBRA FISH; ACUTE DISEASE; ANIMAL; CELLULAR IMMUNITY; CHRONIC DISEASE; CICATRIX; DISEASE MODEL; IMMUNOLOGY; NERVE REGENERATION; PATHOPHYSIOLOGY; PHYSIOLOGY; WOUND INFECTION;

ACUTE DISEASE; ANIMALS; CHRONIC DISEASE; CICATRIX; DISEASE MODELS, ANIMAL; DROSOPHILA; GRANULATION TISSUE; HUMANS; IMMUNITY, CELLULAR; INFLAMMATION; NEOVASCULARIZATION, PHYSIOLOGIC; NERVE REGENERATION; RE-EPITHELIALIZATION; WOUND HEALING; WOUND INFECTION; ZEBRAFISH;

EID: 84941073722     PISSN: 00070963     EISSN: 13652133     Source Type: Journal    
DOI: 10.1111/bjd.13954     Document Type: Review

References (77)

1. Schultz GS, White M, Mitchell R, et al,. Epithelial wound healing enhanced by transforming growth factor-alpha and vaccinia growth factor. Science 1987; 235: 350-2.
2. Grose R, Werner S,. Wound-healing studies in transgenic and knockout mice. Mol Biotechnol 2004; 28: 147-66.
3. Cooper L, Johnson C, Burslem F, Martin P,. Wound healing and inflammation genes revealed by array analysis of 'macrophageless' PU.1 null mice. Genome Biol 2005; 6: R5.
4. Pedersen TX, Leethanakul C, Patel V, et al,. Laser capture microdissection-based in vivo genomic profiling of wound keratinocytes identifies similarities and differences to squamous cell carcinoma. Oncogene 2003; 22: 3964-76.
5. Paladini RD, Takahashi K, Bravo NS, Coulombe PA,. Onset of re-epithelialization after skin injury correlates with a reorganization of keratin filaments in wound edge keratinocytes: defining a potential role for keratin 16. J Cell Biol 1996; 132: 381-97.
6. Martin P, Nobes CD,. An early molecular component of the wound healing response in rat embryos-induction of c-fos protein in cells at the epidermal wound margin. Mech Dev 1992; 38: 209-15.
7. Grose R, Harris BS, Cooper L, et al,. Immediate early genes krox-24 and krox-20 are rapidly up-regulated after wounding in the embryonic and adult mouse. Dev Dyn 2002; 223: 371-8.
8. Shaw T, Martin P,. Epigenetic reprogramming during wound healing: loss of polycomb-mediated silencing may enable upregulation of repair genes. EMBO Rep 2009; 10: 881-6.
9. Grose R, Hutter C, Bloch W, et al,. A crucial role of β1 integrins for keratinocyte migration in vitro and during cutaneous wound repair. Development 2002; 129: 2303-15.
10. Thomason HA, Cooper NH, Ansell DM, et al,. Direct evidence that PKCα positively regulates wound re-epithelialization: correlation with changes in desmosomal adhesiveness. J Pathol 2012; 227: 346-56.
11. Gill SE, Parks WC,. Metalloproteinases and their inhibitors: regulators of wound healing. Int J Biochem Cell Biol 2008; 40: 1334-47.
12. Chmielowiec J, Borowiak M, Morkel M, et al,. c-Met is essential for wound healing in the skin. J Cell Biol 2007; 177: 151-62.
13. Meyer M, Müller AK, Yang J, et al,. FGF receptors 1 and 2 are key regulators of keratinocyte migration in vitro and in wounded skin. J Cell Sci 2012; 125: 5690-701.
14. Repertinger SK, Campagnaro E, Fuhrman J, et al,. EGFR enhances early healing after cutaneous incisional wounding. J Invest Dermatol 2004; 123: 982-9.
15. Werner S, Smola H, Liao X, et al,. The function of KGF in morphogenesis of epithelium and reepithelialization of wounds. Science 1994; 266: 819-22.
16. Ito M, Liu Y, Yang Z, et al,. Stem cells in the hair follicle bulge contribute to wound repair but not to homeostasis of the epidermis. Nat Med 2005; 11: 1351-4.
17. Levy V, Lindon C, Zheng Y, et al,. Epidermal stem cells arise from the hair follicle after wounding. FASEB J 2007; 21: 1358-66.
18. Ito M, Yang Z, Andl T, et al,. Wnt-dependent de novo hair follicle regeneration in adult mouse skin after wounding. Nature 2007; 447: 316-20.
19. Desmouliere A, Geinoz A, Gabbiani F, Gabbiani G,. Transforming growth factor-β1 induces α-smooth muscle actin expression in granulation tissue myofibroblasts and in quiescent and growing cultured fibroblasts. J Cell Biol 1993; 122: 103-11.
20. Fathke C, Wilson L, Hutter J, et al,. Contribution of bone marrow-derived cells to skin: collagen deposition and wound repair. Stem Cells 2004; 22: 812-22.
21. Ishii G, Sangai T, Sugiyama K, et al,. In vivo characterization of bone marrow-derived fibroblasts recruited into fibrotic lesions. Stem Cells 2005; 23: 699-706.
22. Sasaki M, Abe R, Fujita Y, et al,. Mesenchymal stem cells are recruited into wounded skin and contribute to wound repair by transdifferentiation into multiple skin cell type. J Immunol 2008; 180: 2581-7.
23. Driskell RR, Lichtenberger BM, Hoste E, et al,. Distinct fibroblast lineages determine dermal architecture in skin development and repair. Nature 2013; 504: 277-81.
24. Hopkinson-Woolley J, Hughes D, Gordon S, Martin P,. Macrophage recruitment during limb development and wound healing in the embryonic and foetal mouse. J Cell Sci 1994; 107: 1159-67.
25. Adzick NS, Harrison MR, Glick PL, et al,. Comparison of fetal, newborn, and adult wound healing by histologic, enzyme-histochemical, and hydroxyproline determinations. J Pediatr Surg 1985; 20: 315-19.
26. Martin P, D'Souza D, Martin J, et al,. Wound healing in the PU.1 null mouse-tissue repair is not dependent on inflammatory cells. Curr Biol 2003; 13: 1122-8.
27. Dovi JV, He LK, DiPietro LA,. Accelerated wound closure in neutrophil-depleted mice. J Leukoc Biol 2003; 73: 448-55.
28. Lucas T, Waisman A, Ranjan R, et al,. Differential roles of macrophages in diverse phases of skin repair. J Immunol 2010; 184: 3964-77.
29. Antsiferova M, Martin C, Huber M, et al,. Mast cells are dispensable for normal and activin-promoted wound healing and skin carcinogenesis. J Immunol 2013; 191: 6147-55.
30. Willenborg S, Eckes B, Brinckmann J, et al,. Genetic ablation of mast cells redefines the role of mast cells in skin wound healing and bleomycin-induced fibrosis. J Invest Dermatol 2014; 134: 2005-15.
31. Jameson J, Ugarte K, Chen N, et al,. A role for skin γδ T cells in wound repair. Science 2002; 296: 747-9.
32. Deppermann C, Cherpokova D, Nurden P, et al,. Gray platelet syndrome and defective thrombo-inflammation in Nbeal2-deficient mice. J Clin Invest 2015; doi: 10.1172/JCI69210.
33. Bianchi ME, Manfredi AA,. Immunology. Dangers in and out. Science 2009; 323: 1683-4.
34. Wong VW, Rustad KC, Akaishi S, et al,. Focal adhesion kinase links mechanical force to skin fibrosis via inflammatory signaling. Nat Med 2012; 18: 148-52.
35. Cash JL, Bass MD, Campbell J, et al,. Resolution mediator chemerin15 reprograms the wound microenvironment to promote repair and reduce scarring. Curr Biol 2014; 24: 1406-14.
36. Ferguson MW, O'Kane S,. Scar-free healing: from embryonic mechanisms to adult therapeutic intervention. Philos Trans R Soc Lond B Biol Sci 2004; 359: 839-50.
37. Mori R, Shaw TJ, Martin P,. Molecular mechanisms linking wound inflammation and fibrosis: knockdown of osteopontin leads to rapid repair and reduced scarring. J Exp Med 2008; 205: 43-51.
38. Gerhardt H, Golding M, Fruttiger M, et al,. VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J Cell Biol 2003; 161: 1163-77.
39. Rossiter H, Barresi C, Pammer J, et al,. Loss of vascular endothelial growth factor A activity in murine epidermal keratinocytes delays wound healing and inhibits tumor formation. Cancer Res 2004; 64: 3508-16.
40. Fantin A, Vieira JM, Gestri G, et al,. Tissue macrophages act as cellular chaperones for vascular anastomosis downstream of VEGF-mediated endothelial tip cell induction. Blood 2010; 116: 829-40.
41. Wallace H,. The response of denervated axolotl arms to delayed amputation. J Embryol Exp Morphol 1984; 84: 303-7.
42. Kumar A, Brockes JP,. Nerve dependence in tissue, organ, and appendage regeneration. Trends Neurosci 2012; 35: 691-9.
43. Harsum S, Clarke JD, Martin P,. A reciprocal relationship between cutaneous nerves and repairing skin wounds in the developing chick embryo. Dev Biol 2001; 238: 27-39.
44. Razzell W, Wood W, Martin P,. Swatting flies: modelling wound healing and inflammation in Drosophila. Dis Model Mech 2011; 4: 569-74.
45. Henry KM, Loynes CA, Whyte MK, Renshaw SA,. Zebrafish as a model for the study of neutrophil biology. J Leukoc Biol 2013; 94: 633-42.
46. Stramer B, Wood W, Galko MJ, et al,. Live imaging of wound inflammation in Drosophila embryos reveals key roles for small GTPases during in vivo cell migration. J Cell Biol 2005; 168: 567-73.
47. Wood W, Jacinto A, Grose R, et al,. Wound healing recapitulates morphogenesis in Drosophila embryos. Nat Cell Biol 2002; 4: 907-12.
48. Razzell W, Wood W, Martin P,. Recapitulation of morphogenetic cell shape changes enables wound re-epithelialisation. Development 2014; 141: 1814-20.
49. Lesch C, Jo J, Wu Y, et al,. A targeted UAS-RNAi screen in Drosophila larvae identifies wound closure genes regulating distinct cellular processes. Genetics 2010; 186: 943-57.
50. Campos I, Geiger JA, Santos AC, et al,. Genetic screen in Drosophila melanogaster uncovers a novel set of genes required for embryonic epithelial repair. Genetics 2010; 184: 129-40.
51. Mace KA, Pearson JC, McGinnis W,. An epidermal barrier wound repair pathway in Drosophila is mediated by grainy head. Science 2005; 308: 381-5.
52. Ting SB, Caddy J, Hislop N, et al,. A homolog of Drosophila grainy head is essential for epidermal integrity in mice. Science 2005; 308: 411-13.
53. Caddy J, Wilanowski T, Darido C, et al,. Epidermal wound repair is regulated by the planar cell polarity signaling pathway. Dev Cell 2010; 19: 138-47.
54. Niethammer P, Grabher C, Look AT, Mitchison TJ,. A tissue-scale gradient of hydrogen peroxide mediates rapid wound detection in zebrafish. Nature 2009; 459: 996-9.
55. Pase L, Layton JE, Wittmann C, et al,. Neutrophil-delivered myeloperoxidase dampens the hydrogen peroxide burst after tissue wounding in zebrafish. Curr Biol 2012; 22: 1818-24.
56. Richardson R, Slanchev K, Kraus C, et al,. Adult zebrafish as a model system for cutaneous wound-healing research. J Invest Dermatol 2013; 133: 1655-65.
57. Herrick SE, Sloan P, McGurk M, et al,. Sequential changes in histologic pattern and extracellular matrix deposition during the healing of chronic venous ulcers. Am J Pathol 1992; 141: 1085-95.
58. Stojadinovic O, Pastar I, Vukelic S, et al,. Deregulation of keratinocyte differentiation and activation: a hallmark of venous ulcers. J Cell Mol Med 2008; 12: 2675-90.
59. Brem H, Stojadinovic O, Diegelmann RF, et al,. Molecular markers in patients with chronic wounds to guide surgical debridement. Mol Med 2007; 13: 30-9.
60. Pastar I, Stojadinovic O, Krzyzanowska A, et al,. Attenuation of the transforming growth factor β-signaling pathway in chronic venous ulcers. Mol Med 2010; 16: 92-101.
61. Trengove NJ, Stacey MC, MacAuley S, et al,. Analysis of the acute and chronic wound environments: the role of proteases and their inhibitors. Wound Repair Regen 1999; 7: 442-52.
62. Charles CA, Tomic-Canic M, Vincek V, et al,. A gene signature of nonhealing venous ulcers: potential diagnostic markers. J Am Acad Dermatol 2008; 59: 758-71.
63. Loots MA, Lamme EN, Zeegelaar J, et al,. Differences in cellular infiltrate and extracellular matrix of chronic diabetic and venous ulcers versus acute wounds. J Invest Dermatol 1998; 111: 850-7.
64. Stojadinovic O, Yin N, Lehmann J, et al,. Increased number of Langerhans cells in the epidermis of diabetic foot ulcers correlates with healing outcome. Immunol Res 2013; 57: 222-8.
65. Naghibi M, Smith RP, Baltch AL, et al,. The effect of diabetes mellitus on chemotactic and bactericidal activity of human polymorphonuclear leukocytes. Diabetes Res Clin Pract 1987; 4: 27-35.
66. Gottrup F, Jorgensen B,. Maggot debridement: an alternative method for debridement. Eplasty 2011; 11: e33.
67. Smith C, Kavar B,. Extensive spinal epidural abscess as a complication of Crohn's disease. J Clin Neurosci 2010; 17: 144-6.
68. Grice EA, Segre JA,. Interaction of the microbiome with the innate immune response in chronic wounds. Adv Exp Med Biol 2012; 946: 55-68.
69. Nunan R, Harding KG, Martin P,. Clinical challenges of chronic wounds: searching for an optimal animal model to recapitulate their complexity. Dis Model Mech 2014; 7: 1205-13.
70. Lorenz HP, Longaker MT, Perkocha LA, et al,. Scarless wound repair: a human fetal skin model. Development 1992; 114: 253-9.
71. Shih B, Bayat A,. Genetics of keloid scarring. Arch Dermatol Res 2010; 302: 319-39.
72. Mogili NS, Krishnaswamy VR, Jayaraman M, et al,. Altered angiogenic balance in keloids: a key to therapeutic intervention. Transl Res 2012; 159: 182-9.
73. Canady J, Karrer S, Fleck M, Bosserhoff AK,. Fibrosing connective tissue disorders of the skin: molecular similarities and distinctions. J Dermatol Sci 2013; 70: 151-8.
74. Reish RG, Eriksson E,. Scars: a review of emerging and currently available therapies. Plast Reconstr Surg 2008; 122: 1068-78.
75. Wynn TA, Ramalingam TR,. Mechanisms of fibrosis: therapeutic translation for fibrotic disease. Nat Med 2012; 18: 1028-40.
76. Friedman SL, Sheppard D, Duffield JS, Violette S,. Therapy for fibrotic diseases: nearing the starting line. Sci Transl Med 2013; 5: 167sr1.
77. Bosanquet DC, Harding KG,. Wound duration and healing rates: cause or effect? Wound Repair Regen 2014; 22: 143-50.