Cutaneous wound healing

New England Journal of Medicine

Volumn 341, Issue 10, 1999, Pages 738-746

  Singer, Adam J ^a,b   Clark, Richard A F ^a  

^a STONY BROOK UNIVERSITY   (United States)

^b STONY BROOK UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GROWTH FACTOR;

ANGIOGENESIS; CYTOKINE PRODUCTION; EPIDERMIS; EPITHELIZATION; EXTRACELLULAR MATRIX; GRANULATION TISSUE; HUMAN; NONHUMAN; PRIORITY JOURNAL; REVIEW; SKIN EPITHELIUM; SKIN GRAFT; SKIN INJURY; WOUND CLOSURE; WOUND CONTRACTION; WOUND HEALING;

GRANULATION TISSUE; HUMANS; INFLAMMATION; NEOVASCULARIZATION, PHYSIOLOGIC; SKIN; SKIN PHYSIOLOGY; SKIN, ARTIFICIAL; WOUND HEALING;

EID: 0033517356     PISSN: 00284793     EISSN: None     Source Type: Journal    
DOI: 10.1056/NEJM199909023411006     Document Type: Review

References (86)

1. Brigham PA, McLoughlin E. Burn incidence and medical care use in the United States: estimate, trends, and data sources. J Burn Care Rehabil 1996;17:95-107.
2. U.S. markets for wound management products. Irvine, Calif.: Medical Data International, August 1997.
3. Clark RAF, ed. The molecular and cellular biology of wound repair. 2nd ed. New York: Plenum Press, 1996.
4. Heldin C-H, Westermark B. Role of platelet-derived growth factor in vivo. In: Clark RAF, ed. The molecular and cellular biology of wound repair. 2nd ed. New York: Plenum Press, 1996:249-73.
5. Brown EJ. Phagocytosis. Bioessays 1995;17:109-17.
6. Rappolee DA, Mark D, Banda MJ, Werb Z. Wound macrophages express TGF-α and other growth factors in vivo: analysis by mRNA phenotyping. Science 1988;241:708-12.
7. Leibovich SJ, Ross R. The role of the macrophage in wound repair: a study with hydrocortisone and antimacrophage serum. Am J Pathol 1975; 78:71-100.
8. Riches DWH. Macrophage involvement in wound repair, remodeling, and fibrosis. In: Clark RAF, ed. The molecular and cellular biology of wound repair. 2nd ed. New York: Plenum Press, 1996:95-141.
9. 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.
10. Goliger JA, Paul DL. Wounding alters epidermal connexin expression and gap junction-mediated intercellular communication. Mol Biol Cell 1995;6:1491-501.
11. Gabbiani G, Chaponnier C, Hurtner I. Cytoplasmic filaments and gap junctions in epithelial cells and myofibroblasts during wound healing. J Cell Biol 1978;76:561-8.
12. Clark RAF. Fibronectin matrix deposition and fibronectin receptor expression in healing and normal skin. J Invest Dermatol 1990;94:Suppl: 128S-134S.
13. Larjava H, Salo T, Haapasalmi K, Kramer RH, Heino J. Expression of integrins and basement membrane components by wound keratinoctyes. J Clin Invest 1993;92:1425-35.
14. Clark RAF, Ashcroft GS, Spencer M-J, Larjava H, Ferguson MWJ. Reepithelialization of normal human excisional wounds is associated with a switch from αvβ5 to αvβ6 integrins. Br J Dermatol 1996;135:46-51.
15. Pilcher BK, Dumin JA, Sudbeck BD, Krane SM, Welgus HG, Parks WC. The activity of collagenase-1 is required for keratinocyte migration on a type I collagen matrix. J Cell Biol 1997;137:1445-57.
16. Bugge TH, Kombrinck KW, Flick MJ, Daugherty CC, Danton MJS, Degen JL. Loss of fibrinogen rescues mice from the pleiotropic effects of plasminogcn deficiency. Cell 1996;87:709-19.
17. Mignatti P, Rifkin DB, Welgus HG, Parks WC. Proteinases and tissue remodeling. In: Clark RAF, ed. The molecular and cellular biology of wound repair. 2nd ed. New York: Plenum Press, 1996:427-74.
18. Nanney LB, King LE Jr. Epidermal growth factor and transforming growth factor-α. In: Clark RAF, ed. The molecular and cellular biology of wound repair. 2nd ed. New York: Plenum Press, 1996:171-94.
19. 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.
20. Abraham JA, Klagsbrun M. Modulation of wound repair by members of the fibroblast growth factor family. In: Clark RAF, ed. The molecular and cellular biology of wound repair. 2nd ed. New York: Plenum Press, 1996:195-248.
21. Clark RAF, Lanigan JM, DellaPelle P, Manseau E, Dvorak HF, Colvin RB. Fibronectin and fibrin provide a provisional matrix for epidermal cell migration during wound reepithelialization. J Invest Dermatol 1982;79:264-9.
22. Hunt TK, ed. Wound healing and wound infection: theory and surgical practice. New York: Appleton-Century-Crofts, 1980.
23. Roberts AB, Sporn MB. Transforming growth factor-β. In: Clark RAF, ed. The molecular and cellular biology of wound repair. 2nd ed. New York: Plenum Press, 1996:275-308.
24. Gray AJ, Bishop JE, Reeves JT, Laurent GJ. Aα and Bβ chains of fibrinogen stimulate proliferation of human fibroblasts. J Cell Sci 1993;104: 409-13.
25. Xu J, Clark RAF. Extracellular matrix alters PDGF regulation of fibroblast integrins. J Cell Biol 1996;132:239-49.
26. Robson MC, Phillips LG, Thomason A, Robson LE, Pierce GF. Platelet-derived growth factor BB for the treatment of chronic pressure ulcers. Lancet 1992;339:23-5.
27. Steed DL. Clinical evaluation of recombinant human platelet-derived growth factor for the treatment of lower extremity diabetic ulcers. J Vasc Surg 1995;21:71-8.
28. Robson MC, Phillips LG, Lawrence WT, et al. The safety and effect of topically applied recombinant basic fibroblast growth factor on the healing of chronic pressure sores. Ann Surg 1992;216:401-6.
29. Greiling D, Clark RAF. Fibronectin provides a conduit for fibroblast transmigration from collagenous stroma into fibrin clot provisional matrix. J Cell Sci 1997;110:861-70.
30. Toole BP. Proteoglycans and hyaluronan in morphogenesis and differentiation. In: Hay ED, ed. Cell biology of extracellular matrix. 2nd ed. New York: Plenum Press, 1991:305-41.
31. McClain SA, Simon M, Jones E, et al. Mesenchymal cell activation is the rate-limiting step of granulation tissue induction. Am J Pathol 1996; 149:1257-70.
32. Clark RAF, Nielsen LD, Welch MP, McPherson JM. Collagen matrices attenuate the collagen-synthetic response of cultured fibroblasts to TGF-β. J Cell Sci 1995;108:1251-61.
33. Vaalamo M, Mattila L, Johansson N, et al. Distinct populations of stromal cells express collagenase-3 (MMP-13) and collagenase-1 (MMP-1) in chronic ulcers but not in normally healing wounds. J Invest Dermatol 1997;109:96-101.
34. Welch MP, Odland GF, Clark RAF. Temporal relationships of F-actin bundle formation, collagen and fibronectin matrix assembly, and fibronectin receptor expression to wound contraction. J Cell Biol 1990;110:133-45.
35. Desmouliere A, Redard M, Darby I, Gabbiani G. Apoptosis mediates the decrease in cellularity during the transition between granulation tissue and scar. Am J Pathol 1995;146:56-66.
36. Madri JA, Sankar S, Romanic AM. Angiogenesis. In: Clark RAF, ed. The molecular and cellular biology of wound repair. 2nd ed. New York: Plenum Press, 1996:355-71.
37. Folkman J, D'Amore PA. Blood vessel formation: what is its molecular basis? Cell 1996;87:1153-5.
38. Iruela-Arispe ML, Dvorak HF. Angiogenesis: a dynamic balance of stimulators and inhibitors. Thromb Haemost 1997;78:672-7.
39. Risau W. Mechanisms of angiogenesis. Nature 1997;386:671-4.
40. Detmar M, Brown LF, Berse B, et al. Hypoxia regulates the expression of vascular permeability factor/vascular endothelial growth factor (VPF/VEGF) and its receptors in human skin. J Invest Dermatol 1997;108:263-8.
41. Brown LF, Yeo K-T, Berse B, et al. Expression of vascular permeability factor (vascular endothelial growth factor) by epidermal keratinocytes during wound healing. J Exp Med 1992;176:1375-9.
42. Nissen NN, Polverini PJ, Koch AE, Volin MV, Gamelli RL, DiPietro LA. Vascular endothelial growth factor mediates angiogenic activity during the proliferative phase of wound healing. Am J Pathol 1998;152:1445-52.
43. Clark RAF, Quinn JH, Winn HJ, Lanigan JM, Dellepelle P, Colvin RB. Fibronectin is produced by blood vessels in response to injury. J Exp Med 1982;156:646-51.
44. Brooks PC, Clark RAF, Cheresh DA. Requirement of vascular integrin αvβ3 for angiogenesis. Science 1994;264:569-71.
45. Pintucci G, Bikfalvi A, Klein S, Rifkin DB. Angiogenesis and the fibrinolytic system. Semin Thromb Hemost 1996;22:517-24.
46. Ilan N, Mahooti S, Madri JA. Distinct signal transduction pathways are utilized during the tube formation and survival phases of in vitro angiogenesis. J Cell Sci 1998;111:3621-31.
47. Guo N, Krutzsch HC, Inman JK, Roberts DD. Thrombospondin 1 and type I repeat peptides of thrombospondin 1 specifically induce apoptosis of endothelial cells. Cancer Res 1997;57:1735-42.
48. Folkman J. Angiogenesis and angiogenesis inhibition: an overview. EXS 1997;79:1-8.
49. Desmoulière A, Gabbiani G. The role of the myofibroblast in wound healing and fibrocontractive diseases. In: Clark RAF, ed. The molecular and cellular biology of wound repair. 2nd ed. New York: Plenum Press, 1996:391-423.
50. Montesano R, Orci L. Transforming growth factor-β stimulates collagen-matrix contraction by fibroblasts: implications for wound healing. Proc Natl Acad Sci U S A 1988;85:4894-7.
51. Clark RAF, Folkvord JM, Hart CE, Murray MJ, McPherson JM. Platelet isoforms of platelet-derived growth factor stimulate fibroblasts to contract collagen matrices. J Clin Invest 1989;84:1036-40.
52. Schiro JA, Chan BMC, Roswit WT, et al. Integrin α2β1 (VLA-2) mediates reorganization and contraction of collagen matrices by human cells. Cell 1991;67:403-10.
53. Woodley DT, Yamauchi M, Wynn KC, Mechanic G, Briggaman RA. Collagen telopeptides (cross-linking sites) play a role in collagen gel lattice contraction. J Invest Dermatol 1991;97:580-5.
54. Madlener M, Parks WC, Werner S. Matrix metalloproteinases (MMPs) and their physiological inhibitors (TIMPs) are differentially expressed during excisional skin wound repair. Exp Cell Res 1998;242:201-10.
55. Bailey AJ, Bazin S, Sims TJ, Le Lous M, Nicholetis C, Delaunay A. Characterization of the collagen of human hypertrophic and normal scars. Biochim Biophys Acta 1975;405:412-21.
56. Levenson SM, Geever EF, Crowley LV, Oates JF III, Berard CW, Rosen H. The healing of rat skin wounds. Ann Surg 1965;161:293-308.
57. Nolan CM, Beaty HN, Bagdade JD. Further characterization of the impaired bactericidal function of granulocytes in patients with poorly controlled diabetes. Diabetes 1978;27:889-94.
58. Fahey TJ III, Sadaty A, Jones WG II, Barber A, Smoller B, Shires GT. Diabetes impairs the late inflammatory response to wound healing. J Surg Res 1991;50:308-13.
59. Loots MA. Differences in cellular infiltrate and extracellular matrix of chronic diabetic and venous ulcers versus acute wounds. J Invest Dermatol 1998;111:850-7.
60. Tredget EF, Nedelec B, Scott PG, Ghahary A. Hypertrophic scars, keloids, and contractures: the cellular and molecular basis for therapy. Surg Clin North Am 1997;77:701-30.
61. Babu M, Diegelmann R, Oliver N. Keloid fibroblasts exhibit an altered response to TGF-beta. J Invest Dermatol 1992;99:650-5.
62. Zhang K, Garner W, Cohen L, Rodriguez J, Phan S. Increased types I and III collagen and transforming growth factor-beta 1 mRNA and protein in hypertrophic burn scar. J Invest Dermatol 1995;104:750-4.
63. Saed GM, Ladin D, Olson J. Analysis of p53 gene mutations in keloids using polymerase chain reaction-based single-strand conformational polymorphism and DNA sequencing. Arch Dermatol 1998;134:963-7.
64. Machesney M, Tidman N, Waseem A, Kirby L, Leigh I. Activated keratinocytes in the epidermis of hypertrophic scars. Am J Pathol 1998;152: 1133-41.
65. Pierce GF, Mustoe TA. Pharmacologic enhancement of wound healing. Annu Rev Med 1995;46:467-81.
66. Martin P, Lewis J. Actin cables and epidermal movement in embryonic wound healing. Nature 1992;360:179-83.
67. Sullivan KM, Lorenz HP, Meuli M, Lin RY, Adzick NS. A model of scarless human fetal wound repair is deficient in transforming growth factor beta. J Pediatr Surg 1995;30:198-203.
68. Bullard KM, Cass DL, Banda MJ, Adzick NS. Transforming growth factor beta-1 decreases interstitial collagenase in healing human fetal skin. J Pediatr Surg 1997;32:1023-7.
69. Shah M, Foreman DM, Ferguson MWJ. Neutralisation of TGF-β1 and TGF-β2 or exogenous addition of TGF-β3 to cutaneous rat wounds reduces scarring. J Cell Sci 1995;108:985-1002.
70. Rheinwald JG, Green H. Serial cultivation of strains of human epidermal keratinocytes: the formation of keratinizing colonies from single cells. Cell 1975;6:331-43.
71. Grafting of burns with cultured epithelium prepared from autologous epidermal cells. Lancet 1981;1:75-8.
72. Hefton JM, Caldwell D, Biozes DG, Balin AK, Carter DM. Grafting of skin ulcers with cultured autologous epidermal cells. J Am Acad Dermatol 1986;14:399-405.
73. Rue LW III, Cioffi WG, McManus WF, Pruitt BA Jr. Wound closure and outcome in extensively burned patients treated with cultured autologous keratinocytes. J Trauma 1993;34:662-8.
74. Hefton JM, Madden MR, Finkelstein JL, Shires GT. Grafting of burn patients with allografts of cultured epidermal cells. Lancet 1983;2:428-30.
75. Madden MR, Finkelstein JL, Staiano-Coico L, et al. Grafting of cultured allogeneic epidermis on second- and third-degree burn wounds on 26 patients. J Trauma 1986;26:955-62.
76. Thivolet J, Faure M, Demidem A, Mauduit G. Long-term survival and immunological tolerance of human epidermal allografts produced in culture. Transplantation 1986;42:274-80.
77. Leigh IM, Purkis PE, Navsaria HA, Phillips TJ. Treatment of chronic venous ulcers with sheets of cultured allogenic keratinocytes. Br J Dermatol 1987;117:591-7.
78. Gilchrest BA, Karassik RL, Wilkins LM, Vrabel MA, Maciag T. Autocrine and paracrine growth stimulation of cells derived from human skin. J Cell Physiol 1983;117:235-40.
79. Phillips TJ, Kehinde O, Green H, Gilchrest BA. Treatment of skin ulcers with cultured epidermal allografts. J Am Acad Dermatol 1989;21:191-9.
80. Teepe RGC, Koebrugge EJ, Ponec M, Vermeer BJ. Fresh versus cryopreserved cultured allografts for the treatment of chronic skin ulcers. Br J Dermatol 1990;122:81-9.
81. Cuono C, Langdon R, McGuire J. Use of cultured epidermal autografts and dermal allografts as skin replacement after burn injury. Lancet 1986;1:1123-4.
82. Heimbach D, Luterman A, Burke J, et al. Artificial dermis for major burns: a multi-center randomized clinical trial. Ann Surg 1988;208:313-20.
83. Boyce ST, Glatter R, Kitzmiller WJ. Treatment of chronic wounds with cultured skin substitutes: a pilot study. Wounds 1995;7:24-9.
84. Purdue GF. Dermagraft-TC pivotal efficacy and safety study. J Burn Care Rehabil 1997;18:S13-S14.
85. Eaglstein WH, Iriondo M, Laszlo K. A composite skin substitute (graftskin) for surgical wounds: a clinical experience. Dermatol Surg 1995; 21:839-43.
86. Falanga V, Margolis D, Alvarez O, et al. Rapid healing of venous ulcers and lack of clinical rejection with an allogeneic cultured human skin equivalent. Arch Dermatol 1998;134:293-300.