Mechanisms of wound healing in the embryo and fetus

Current Topics in Developmental Biology

Volumn 32, Issue , 1996, Pages 175-203

  Martin, P ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 0030050590     PISSN: 00702153     EISSN: None     Source Type: Journal    
DOI: 10.1016/s0070-2153(08)60428-7     Document Type: Review

References (95)

1. B.C. Adelmann-Grill F. Wach Z. Cully R. Hein T. Krieg Chemotactic migration of normal dermal fibroblasts towards epidermal growth factor and its modulation by platelet-derived growth factor and transforming growth factor beta Eur. J. Cell Biol. 51 1990 322 326
2. N.S. Adzick M.R. Harrison The fetal surgery experience N.S. Adzick M.T. Longaker “Fetal Wound Healing” 1991 Elsevier New York 1 23
3. N.S. Adzick M.R. Harrison P.L. Click J.H. Beckstead R.L. Villa H. Scheuenstuhl W.H. Goodson III Comparison of fetal, newborn, and adult wound healing by histologic, enzyme-histochemical, and hydroxyproline determinations J. Pediatr. Surg. 20 1985 315 319
4. R.A. Assoian M.B. Sporn Type-beta transforming growth factor in human platelets: Release during platelet degranulation and action on vascular smooth muscle cells J. Cell Biol. 102 1986 1712 1733
5. R.K. Assoian B.E. Fleurdelys H.C. Stevenson P.J. Miller D.K. Madtes E.W. Raines R. Ross M.B. Sporn Expression and secretion of type β transforming growth factor by activated human macrophages Proc. Natl. Acad. Sci. U.S.A. 84 1987 6020 6024
6. J.M. Austyn S. Gordon F4/80, a monoclonal antibody directed specifically against the mouse macrophage Eur. J. Immunol. 11 1981 805 815
7. P.C. Baker T.E. Schroeder Cytoplasmic filaments and morphogenetic movement in the amphibian neural tube Dev. Biol. 15 1967 432 450
8. S. Bard P. Sengel Reconstitution of the epidermal basement membrane after enzymatic dermal-epidermal separation of embryonic mouse skin Arch. Anat. Microsc. Morphol. Exp. 73 1984 239 257
9. Y. Barrandon H. Green Cell migration is essential for sustained growth of ker-atinocyte colonies: The roles of transforming growth factor a and epidermal growth factor Cell (Cambridge, Mass.) 50 1987 1131 1137
10. W.M. Bement P. Forscher M.S. Mooseker A novel cytoskeletal structure involved in purse-string wound closure and cell polarity maintenance J. Cell Biol. 121 1993 565 578
11. M. Block Wound healing in the newborn opossum Nature (London) 187 1960 340 341
12. J. Brock, K. Midwinter, and J. Lewis, P. Martin, Healing of incisional wounds in the embryonic chick wing bud: Characterisation of the actin purse-string. In preparation.
13. R.C. Buck Cell migration in repair of mouse corneal epithelium Invest. Ophthalmol. Visual Sci. 18 1979 767 784
14. L.P.A. Burgess G.V. Morin M. Rand J. Vossoughi Hollinger J.O. Wound healing: Relationship of wound closing tension to scar width in rats Arch. Otolaryngol., Head & Neck Surg. 116 1990 798 802
15. B. Burnside Microtubules and microfilaments in amphibian neurulation Am. Zool. 13 1971 989 1006
16. R.A. Clarke J.M. Lanigan P. DellaPelle E. Manseau H.F. Dvorak R.B. Colvin Fibronectin and fibrin provide a provisional matrix for epidermal cell migration during wound re-epithelialisation J. Invest. Dermatol. 79 1982 264 269
17. J.N. Clore I.K. Cohen R.F. Diegelmann Quantitation of collagen types I and III during wound healing in rat skin Proc. Soc. Exp. Biol. Med. 161 1979 337 340
18. R.J. Coffey C.C. Bascom N.J. Sipes R. Graves-Deal B.E. Weissman H.L. Moses Selective growth inhibition of growth-related gene expression in murine ker-atinocytes by transforming growth factor β Mol. Cell. Biol. 8 1988 3088 3093
19. L. Dale M. Bownes Is regeneration in Drosophila the result of epimorphic regulation? Wilhelm Roux's Arch. Dev. Biol. 189 1980 91 96
20. I. Darby G. Gabbiani α-smooth muscle actin is transiently expressed by myofibroblasts during experimental wound healing Lab. Invest. 63 1990 21 29
21. A. Desmouliere A. Geinoz F. Gabbiani G. Gabbiani Transforming growth factor-β1 induces α-smooth muscle actin expression in granulation tissue myofibroblasts and in quiescent and growing cultured fibroblasts J. Cell Biol. 122 1993 103 111
22. J.B. Dixon Inflammation in the fetal and neonatal rat. The local reactions to skin burns. J. Pathol. Bacterial. 80 1960 73 82
23. D.R. Edwards G. Murphy J.J. Reynolds S.E. Whitman A.J.P. Docherty P. Angel J.K. Heath Transforming growth factor beta modulates the expression of collagenase and metalloproteinase inhibitor EMBO J. 6 1987 1899 1904
24. M.A. England S.V. Cowper Wound healing in the early chick embryo studied by scanning electron microscopy Anat. Embryol. 152 1977 1 14
25. J.M. Estes J.S. BergVande N.S. Adzick T.E. MacGillivray A. Desmouliere G. Gabbiani Phenotypic and functional features of myofibroblasts in sheep fetal wounds Differentiation (Berlin) 56 1994 173 181
26. M.W.J. Ferguson G.F. Howarth Marsupial models of scarless fetal wound healing N.S. Adzick M.T. Longaker “Fetal Wound Healing” 1991 Elsevier New York 95 124
27. C. ffrench-Constant L. WaterVan De H.F. Dvorak R.O. Hynes Reappearance of an embryonic pattern of fibronectin splicing during wound healing in the adult rat J. Cell Biol. 109 1989 903 914
28. R.D. Fink J.P. Trinkaus Fundulus deep cells: Directional migration in response to epithelial wounding Dev. Biol. 129 1988 179 190
29. I.K. Gipson S.J. Spurr-Michaud A.S. Tisdale Hemidesmosomes and anchoring fibril collagen appear synchronously during development and wound healing Dev. Biol. 126 1988 253 262
30. F. Grinnell Wound repair, keratinocyte activation and integrin modulation J. Cell Sci. 101 1992 1 5
31. F. Grinnell Fibroblasts, myofibroblasts, and wound contraction J. Cell Biol. 124 1994 401 404
32. V. Hamburger H.L. Hamilton A series of normal stages in the development of the chick embryo J. Morphol. 88 1951 49 92
33. A. Hammacher U. Hellman A. Johnson A. Ostman K. Gunnarsson B. Westerman A. Wasteson C.H. Heldin A major part of PDGF purified from human platelets is a heterodimer of one A chain and one B chain J. Biol. Chem. 263 1986 16493 16498
34. J. Hopkinson-Woolley D. Hughes S. Gordon P. Martin Macrophage recruitment during limb development and wound healing in the embryonic and fetal mouse J. Cell Sci. 107 1994 1159 1167
35. R. Ignotz T. Endo J. Massague Regulation of fibronectin and type I collagen mRNA levels by transforming growth factor-β J. Biol. Chem. 262 1987 6443 6446
36. S. Ihara Y. Motobayashi Wound closure in fetal rat skin Development (Cambridge, UK) 114 1992 573 582
37. S. Ihara Y. Motobayashi E. Nagao A. Kistler Ontogenetic transition of wound healing pattern in rat skin occurring at the fetal stage Development (Cambridge, UK) 110 1990 671 680
38. S.-J. Kim P. Angel R. Lafyatis K. Hattori K.Y. Kim M. Sporn M. Karin A.B. Roberts Autoinduction of transforming growth factor β1 is mediated by the AP-1 complex Mol. Cell. Biol. 10 1990 1492 1497
39. J. Kolega Effects of mechanical tension on protrusive activity and microfilament and intermediate filament organisation in an epidermal epithelium moving in culture J. Cell Biol. 102 1986 1400 1411
40. T.M. Krummel B.A. Michna B.L. Thomas M.B. Sporn J.M. Nelson A.M. Salzberg I.K. Cohen R.F. Diegelmann Transforming growth factor beta (TGF-β) induces fibrosis in a fetal wound model J. Pediatr. Surg. 23 1988 647 652
41. T.M. Krummel H.P. Erlich J.M. Nelson B.A. Michna B.L. Thomas J.M. Haynes I.K. Cohen R.F. Diegelmann Fetal wounds do not contract in utero Surg. Forum. 40 1989 613 614
42. S.J. Leibovich R. Ross The role of the macrophage in wound repair. A study with hydrocortisone and antimacrophage serum. Am. J. Pathol. 78 1975 71 92
43. M.T. Longaker D.J. Whitby M.W.J. Ferguson M.R. Harrison T.M. Crombleholme J.C. Langer J.C. Cochrum E.D. Verrier R. Stern Studies in fetal healing: III Early deposition of fibronectin distinguishes fetal from adult wound healing J. Pediatr. Surg. 24 1989 799 805
44. M.T. Longaker D.J. Whitby R.W. Jennings B.W. Duncan T.M. Cromblholme M.R. Harrison M.W.J. Ferguson N.S. Adzick Adult skin in the fetal environment heals with scar formation Surg. Forum. 41 1990 639 641
45. M.T. Longaker D.J. Whitby N.S. Adzick T.M. Crombleholme J.C. Langer B.W. Duncan S.M. Bradley R. Stern M.W.J. Ferguson M.R. Harrison Studies in fetal wound healing VI. Second and early third trimester fetal wounds demonstrate rapid collagen deposition without scar formation. J. Pediatr. Surg. 25 1990 63 69
46. M.T. Longaker D.A.R. Burd A.M. Gown T.S.B. Yen R.W. Jennings B.W. Duncan M.R. Harrison N.S. Adzick Midgestation fetal lamb wounds contract in utero J. Pediatr. Surg. 26 1991 942 948
47. M.T. Longaker E.S. Chiu N.S. Adzick M. Stern M.R. Harrison R. Stern Studies in fetal healing: V A prolonged presence of hyaluronic acid characterises fetal wound fluid Ann. Surg. 213 1991 292 296
48. Longaker M.T. Whitby D.J. Jennings R.W. Duncan B.W. Ferguson M.W.J. Harrison M.R. Adzick N.S. Fetal diaphragmatic wounds heal with scar formation J. Surg. Res. 50 1991 375 385
49. H.P. Lorenz M.T. Longaker L.A. Perkocha R.W. Jennings M.R. Harrison N.S. Adzick Scarless wound repair: A human fetal skin model Development (Cambridge, UK) 114 1992 253 259
50. H.P. Lorenz D.J. Whitby M.T. Longaker N.S. Adzick Fetal wound healing: The ontogeny of scar formation in the non-human primate Ann. Surg. 217 1993 391 396
51. E.J. Mackie W. Halfter D. Liverani Induction of tenascin in healing wounds J. Cell Biol. 107 1988 2757 2767
52. P. Martin J. Lewis Actin cables and epidermal movement in embryonic wound healing Nature (London) 360 1992 179 183
53. P. Martin C.D. Nobes 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. 38 1992 209 216
54. P. Martin J. Hopkinson-Woolley J. McCluskey Growth factors and cutaneous wound repair Prog. Growth Factor Res. 4 1992 25 44
55. P. Martin M.C. Dickson F.A. Millan R.J. Akhurst Rapid induction and clearance of TGFβl is an early response to wounding in the mouse embryo Dev. Genet. 14 1993 225 238
56. J. McCluskey, P. Martin, (1995). Analysis of the tissue movements of embryonic wound healing-Dil studies in the limb bud stage mouse embryo. Dev. Biol. (in press).
57. J. McCluskey J. Hopkinson-Woolley B. Luke P. Martin A study of wound healing in the E11.5 mouse embryo by light and electron microscopy Tissue Cell 25 1993 173 181
58. J.J. McCullagh P. Gill D.J. Wilson Repair of cartilaginous fractures during chick limb development J. Orthop. Res. 8 1990 127 131
59. J.M. McPherson K.A. Piez Collagen in dermal wound repair R.A.F. Clark P.M. Henson “The Molecular and Cellular Biology of Wound Repair” 1988 Plenum New York 471 496
60. J.R. Merkel B.R. DiPaulo G.G. Hallock D. Rice Type I and type III collagen content of healing wounds in fetal and adult rats Proc. Soc. Exp. Biol. Med. 187 1988 493 497
61. B.R.W. Moelleken M.T. Longaker J.C. Cheng D.J. Simmons Fetal fracture healing N.S. Adzick M.T. Longaker “Fetal Wound Healing” 1991 Elsevier New York
62. R. Montesano L. Orci Transforming growth factor (3 stimulates collagen matrix contraction by fibroblasts; Implications for wound healing Proc. Natl. Acad. Sci. U.S.A. 85 1988 4894 4897
63. L. Morris C.F. Graham S. Gordon Macrophages in haemopoetic and other tissues of the developing mouse detected by the monoclonal antibody F4/80 Development (Cambridge, UK) 112 1991 517 526
64. G. Morriss-Kay F. Tuckett The role of microfilaments in cranial neurulation in rat embryos: Effects of short term exposure to cyochalasin D J. Embryol. Exp, Morphol. 88 1985 333 348
65. S.L. Newman J.E. Henson P.M. Henson Phagocytosis of senescent neutrophils by human monocyte-derived macrophages and rabbit inflammatory macrophages J. Exp. Med. 156 1982 430 442
66. G. Odland R. Ross Human wound repair. I. Epidermal regeneration. J. Cell Biol. 39 1968 1135 1151
67. Y. Oka D.N. Orth Human plasma epidermal growth factor/b-urogastrone is associated with blood platelets J. Clin. Invest. 72 1983 249 259
68. G.F. Pierce T.A. Mustoe J. Lingelbach V.R. Masakowski G.L. Griffen R.M. Senior T.F. Deuel Platelet derived growth factor and transforming growth factor-beta enhance tissue repair activities by unique mechanisms J. Cell Biol. 109 1989 429 440
69. G.P. Radice The spreading of epithelial cells during wound closure in Xenopus larvae Dev. Biol. 76 1980 26 46
70. D.A. Rappolee D. Mark M.J. Banda Z. Werb Wound macrophages express TGFβ and other growth factors in vivo: Analysis by mRNA phenotyping Science 241 1988 708 712
71. A.J. Ridley A. Hall The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors Cell (Cambridge, Mass.) 70 1992 389 399
72. A.B. Roberts S.-J. Kim P. Kondaiah S.B. Jakowlew F. Denhez A.B. Click A.G. Geiser S. Watanabe T. Noma R. Lechleider M.B. Sporn Transcriptional control of expression of the TGFβs Ann. N. Y. Acad. Sci. 593 1991 43 90
73. Rugh R. “The Mouse: Its Reproduction and Development” 1990 Oxford Univ. Press Oxford
74. Seppa H. Grotendorst G.R. Seppa S. Schiffman E. Martin G.R. Platelet-derived growth factor is chemotactic for fibroblasts J. Cell Biol. 92 1982 584 588
75. M. Shah D.M. Foreman M.W.J. Ferguson Control of scarring in adult wounds by neutralising antibody to transforming growth factor (3 Lancet 339 1992 213 214
76. M. Shah D.M. Foreman M.W.J. Ferguson Neutralising antibody to TGFβ1,2 reduces cutaneous scarring in adult rodents J. Cell Sci. 107 1994 1137 1157
77. D.M. Simpson R. Ross The neutrophilic leukocyte in wound repair: A study with antineutrophil serum J. Clin. Invest. 51 1972 2009 2023
78. M.J. Smedley M. Stanisstreet Scanning electron microscopy of wound healing in rat embryos J. Embryol. Exp. Morphol. 83 1984 109 117
79. L.T. Smith K.A. Holbrook J.A. Madri Collagen types I, III and V in human embryonic and fetal skin Am. J. Anat. 175 1986 507 521
80. K. Somasunderam K. Prathrap Intra-uterine healing of skin wounds in rabbit foetuses J. Pathol. 100 1970 81 86
81. K. Somasunderam K. Prathrap The effect of exclusion of amniotic fluid on intrauterine healing of skin in rabbit foetuses J. Pathol. 107 1972 127 130
82. M. Stanisstreet Calcium and wound healing in Xenopus early embryos J. Embryol. Exp. Morphol. 67 1982 195 205
83. M. Stanisstreet M. Panayi Effects of colchicine, cytochalasin-B and papaverine on wound healing in Xenopus early embryos Experientia 36 1980 1110 1111
84. M. Stanisstreet J. Wakely M.A. England Scanning electron microscopy of wound healing in Xenopus and chicken embryos J. Embryol. Exp. Morphol. 59 1980 341 353
85. R.A. Terkeltaub M.H. Ginsberg Platelets and response to injury R.A.F. Clark P.M. Henson “The Molecular and Cellular Biology of Wound Repair” 1988 Plenum New York 35 48
86. A. Thevenet Wound healing of the integument of the 5 day chick embryo Arch. Anat. Microsc. Morphol. Exp. 70 1981 227 244
87. A. Thevenet Proliferation cellulaire au cours de la cicatrisation du tegument d'embryon de poulet de 5 jours Arch. Anat. Microsc. Morphol. Exp. 73 1984 121 132
88. B.P. Toole Glycosaminoglycans in morphogenesis E.D. Hay “Cell Biology of the Extracellular Matrix” 1981 Plenum New York
89. N. Torpey C.C. Wylie J. Heasman Function of maternal cytokeratin in Xenopus development Nature (London) 357 1992 413 415
90. P. Weiss G. Matoltsy Wound healing in chick embryos in vivo and in vitro Dev. Biol. 1 1959 302 326
91. D.J. Whitby M.W.J. Ferguson The extracellular matrix of lip wounds in fetal, neonatal and adult mice Development (Cambridge, UK) 112 1991 651 668
92. D.J. Whitby M.W.J. Ferguson Immunohistochemical localization of growth factors in fetal wound healing Dev. Biol. 147 1991 207 215
93. D.J. Whitby M.T. Longaker M.R. Harrison N.S. Adzick M.W.J. Ferguson Rapid epithelialisation of fetal wounds is associated with the early deposition of tenascin J. Cell Sci. 99 1991 583 586
94. A.E. Wild Protein composition of the rabbit fetal fluids Proc. R. Soc. London, Ser. B. 163 1965 90 115
95. P.E. Young A.M. Richman A.S. Ketchum D.P. Kiehart Morphogenesis in Drosophila requires nonmuscle myosin heavy chain function Genes Develop 7 1993 29 41