Wound healing in embryos: A review

Anatomy and Embryology

Volumn 195, Issue 3, 1997, Pages 215-228

  Nodder, Sue ^a   Martin, Paul ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Cell movement; Embryos; Epidermal cells; Growth factors; Skin; Wound healing

Indexed keywords

GROWTH FACTOR;

CELL MOTION; CONNECTIVE TISSUE; EMBRYO; EPIDERMIS CELL; EPITHELIZATION; GASTRULATION; MYOFIBROBLAST; NEURULATION; PRIORITY JOURNAL; REVIEW; SCAR FORMATION; SKIN INJURY; WOUND HEALING;

ACTINS; ANIMALS; CELL MOVEMENT; CONNECTIVE TISSUE; EMBRYO; EXTRACELLULAR MATRIX; GRANULATION TISSUE; GROWTH SUBSTANCES; INFLAMMATION; MICROSCOPY, ELECTRON; MICROSCOPY, ELECTRON, SCANNING; TIME FACTORS; WOUND HEALING;

EID: 0031050923     PISSN: 03402061     EISSN: None     Source Type: Journal    
DOI: 10.1007/s004290050041     Document Type: Review

References (87)

1. Abercrombie M, Flint MH, James DW (1954) Collagen formation and wound contraction during repair of small excised wounds in the skin of rats. J Embryol Exp Morph 2: 264-274
2. Adzick NS, Harrison MR (1994a) Fetal surgical therapy. Lancet. 343: 897-902
3. Adzick NS, Harrison MR (1994b) The unborn surgical patient. Curr Probl Surg 31: 1-68
4. Adzick NS, Harrison MR, Glick PL, Beckstaed JH, Villa RL, Scheuenstuhl H, Goodson WH III (1985) Comparison of fetal, newborn, and adult wound healing by histologic, enzyme-histochemical, and hydroxyproline determinations. J Pediatr Surg 20: 315-319
5. al-Qattan MM, Posnick JC, Lin KY, Thorner P (1993) Fetal tendon healing: development of an experimental model. Plast Reconstr Surg 92: 1155-1160
6. Armstrong JR, Ferguson MW (1995) Ontogeny of the skin and the transition from scar-free to scarring phenotype during wound healing in the pouch young of a marsupial, Monodelphis domestica. Dev Biol 169: 242-60
7. Austyn JM, Gordon S (1981) F4/80, a monoclonal antibody directed specifically against the mouse macrophage. Eur J Immunol 11: 805-815
8. Bard JBL (1990a) Morphogenesis: the cellular and molecular processes of developmental anatomy. Cambridge University Press, Cambridge
9. Bard JBL (1990b) Traction and the formation of mesenchymal condensations in vivo. Bioessays 12: 389-395
10. Bement WM, Forscher P, Mooseker MS (1993) A novel cytoskeletal structure involved in purse-string wound closure and cell polarity maintenance. J Cell Biol 121: 565-578
11. Blewett CJ, Cilley RE, Ehrlich HP, Dillon PW, Blackburn JH III, Krummel TM (1995) Regenerative healing of incisional wounds in murine fetal lungs maintained in organ culture. J Pediatr Surg 30: 945-948
12. Brock J, Midwinter K, Lewis J, Martin P (1996) Healing of incisional wounds in the embryonic chick wing bud: characterisation of the actin purse-string and demonstration of a requirement for Rho activation. J Cell Biol 135: 1097-1107
13. Bruess JM, Gallo J, DeLisser HM, Klimanskaya IV, Folkesson HG, Pittet JF, Nishimura SL, Aldape K, Landers DV, Carpenter W, Gillett N, Sheppard D, Mathay MA, Albelda SM, Kramer RH, Pytela R (1995) Expression of the beta 6 integrin subunit in development, neoplasia and tissue repair suggests a role in epithelial remodelling. J Cell Sci 108: 2241-2251
14. Buck RC (1979) Cell migration in repair of the mouse corneal epithelium. Invest Opthalmol Vis Sci 18: 767-784
15. Burgess LPA, Morin GV, Rand M, Vossoughi J, Hollinger JO (1990) Wound healing: relationship of wound closing tension to scar width in rats. Arch Otolaryngol Head Neck Surg 116: 798-802
16. Cavani A, Zambruno G, Marconi A, Maneca V, Marchetti M, Giannetti A (1993) Distinctive integrin expression in the newly forming epidermis during wound healing in humans. J Invest Dermatol 101: 600-604
17. Clark RAF (1996) Molecular and cellular biology of wound repair, 2nd edn. Plenum Press, New York
18. Dale L, Bownes M (1980) Is regeneration in Drosophila the result of epimorphic regulation? Wilhelm Roux Arch Dev Biol 198: 91-96
19. Darby I, Gabbiani G (1990) α-smooth muscle actin is transiently expressed by myofibroblasts during experimental wound healing. Lab Invest 63: 21-29
20. Desmouliere A, Geinoz A, Gabbiani F, Gabbiani G (1993) 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: 103-111
21. Dixon JB (1960) Inflammation in the fetal and neonatal rat. The local reactions to skin burns. J Pathol Bacteriol 80: 73-82
22. England MA, Cowper SV (1977) Wound healing in the early chick embryo studied by scanning electron microscopy. Anal Embryol 152: 1-14
23. Estes JM, Adzick NS, Harrison MR, Longaker MT, Stern R (1993) Hyaluronate metabolism undergoes an ontogenic transition during fetal development: implications for scar-free wound healing. J Pediatr Surg 28: 1227-31
24. Estes JM, Van De Berg JS, Adzick NS, MacGillivray TE, Desmouliere A, Gabbiani G (1994) Phenotypic and functional features of myofibroblasts in sheep fetal wounds. Differentiation 56: 173-181
25. ffrench-Constant C, Van De Water L, Dvorak HF, Hynes RO (1989) Reappearance of an embryonic pattern of fibronectin splicing during wound healing in the adult rat. J Cell Biol 109: 903-914
26. Freund RM, Siebert JW, Cabrera RC, Longaker MT, Eidelman Y, Adzick NS, Garg HG (1993) Serial quantitation of hyaluronan and sulfated glycosaminoglycans in fetal sheep skin. Biochem Mol Biol Int 29: 773-83
27. Grinnell F (1992) Wound repair, keratinocyte activation and integrin modulation. J Cell Sci 101: 1-5
28. Grinnell F (1994) Fibroblasts, myofibroblasts, and wound contraction. J Cell Biol 124: 401-404
29. Haynes JH, Johnson DE, Mast BA, Dieglemann RF, Salzberg DA, Kohen IK, Krummel TM (1994) Platelet-derived growth factor induces fetal fibrosis. J Pediat Surg 29: 1405-1408
30. Heath JP (1996) Epithelial cell migration in the intestine. Cell Biol Int 20: 139-146
31. Hopkinson-Woolley J, Hughes D, Gordon S, Martin P (1994) Macrophage recruitment during limb development and wound healing in the embryonic and fetal mouse. J Cell Sci 107: 1159-1167
32. Ihara S, Motobayashi Y (1992) Wound closure in fetal rat skin. Development 114: 573-582
33. Kolega J (1986) Effects of mechanical tension on protrusive activity and microfilament and intermediate filament organisation in an epidermal epithelium moving in culture. J Cell Biol 102: 1400-1411
34. Krummel TM, Michna BA, Thomas BL, Sporn MB, Nelson JM, Saltzberg AM, Cohen IK, Diegelmann RF (1988) Transforming growth factor beta (TGF-β) induces fibrosis in fetal wound model. J Pediatr Surg 23: 647-652
35. Krummel TM, Erlich HP, Nelson JM, Michna BA, Thomas BL, Haynes JM, Cohen IK, Diegelmann RF (1989) Fetal wounds do not contract in utero. Surg Forum 40: 613-614
36. Leibovich SJ, Ross R (1975) The role of the macrophage in wound repair. A study with hydrocortisone and antimacrophage serum. Am J Pathol 78: 71-92
37. Lin RY, Sullivan KM, Argenta PA, Meuli M, Lorenz HP, Adzick NS (1995) Exogenous transforming growth factor-beta amplifies its own expression and induces scar formation in a model of human fetal skin repair. Ann Surg 222: 146-154
38. Longaker MT, Whitby DJ, Adzick NS, Crombleholme TM, Langer JC, Duncan BW, Bradley SM, Stern R, Ferguson MWJ, Harrison MR (1990) Studies in fetal wound healing VI. Second and early third trimester fetal wounds demonstrate rapid collagen deposition without scar formation. J Pediatr Surg 25: 63-69
39. Longaker MT, Burd DAR, Gown AM, Yen TSB, Jennings RW, Duncan BW, Harrison MR, Adzick NS (1991a) Midgestational excisional fetal lamb wounds contract in utero. J Pediatr Surg 26: 942-948
40. Longaker MT, Chui ES, Adzick NS, Stem M, Harrison MR, Stern R (1991b) Studies in fetal wound healing V. A prolonged presence of hyaluronic acid characterises fetal wound fluid. Ann Surg 213: 292-6
41. Longaker MT, Moelleken BR, Cheng JC, Jennings RW, Adzick NS, Mintorovich J, Levinsohn DG, Gordon L, Harrison MR, Simmons DJ (1992) Fetal fracture healing in a lamb model. Plast Reconstr Surg 90: 161-71
42. Lorenz HP, Longaker MT, Perkocha LA, Jennings RW, Harrison MR, Adzick NS (1992) Scarless wound repair: A human fetal skin model. Development 114: 253-259
43. Lorenz HP, Whitby DJ, Longaker MT, Adzick NS (1993) Fetal wound healing. The ontogeny of scar formation in the non-human primate. Ann Surg 217: 319-398
44. Madri JA, Pratt BM (1988) Angiogenesis. In: Clark RAF, Henson PM (eds) The molecular and cellular biology of wound repair. Plenum Press, New York
45. Martin P, Lewis J (1991) The mechanics of embryonic skin wound healing: limb bud lesions in mouse and chick embryos. In: Adzick NS, Longaker MT (eds) Fetal Wound Healing. Elsevier, New York
46. Martin P, Lewis J (1992) Actin cables and epidermal movement in embryonic wound healing. Nature 360: 179-182
47. Martin P, Nobes CD (1992) 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: 209-216
48. Martin P, Hopkinson-Woolley J, McCluskey J (1992) Growth factors and cutaneous wound repair. Prog Growth Factor Res 4: 25-44
49. Martin P, Dickson MC, Millan FA, Akhurst RJ (1993) Rapid induction and clearance of TGFβ1 in response to wounding in the mouse embryo. Dev Genet 14: 225-238
50. Mast BA, Haynes JH, Krummel TM, Diegelmann RF, Cohen IK (1992) In vivo degradation of fetal wound hyaluronic acid results in increased fibroplasia, collagen deposition, and neovascularisation. Plast Reconstr Surg 89: 503-9
51. McCluskey J, Martin P (1995) Analysis of the tissue movements of embryonic wound healing - DiI studies in the limb bud stage mouse embryo. Dev Biol 170: 102-114
52. McCluskey J, Hopkinson-Woolley J, Luke B, Martin P (1993) A study of wound healing in the E11.5 mouse embryo by light and electron microscopy. Tissue Cell 25: 173-181
53. McCullagh JJ, Gill P, Wilson DJ (1990) Repair of cartilaginous fractures during chick limb development. J Orthop Research 8: 127-131
54. Meuli M, Lorenz HP, Hedrick MH, Sullivan KM, Harrison MR, Adzick NS (1995) Scar formation in the fetal alimentary canal. J Pediatr Surg 30: 392-395
55. Moelleken BRW, Longaker MT, Cheng JC, Simmons DJ (1991) Fetal fracture healing. In: Adzick NS, Longaker MT (eds) Fetal wound healing. Elsevier, New York
56. Montesano R, Orci L (1988) Transforming growth factor β stimulates collagen-matrix contraction by fibroblasts: implications for wound healing. Proc Natl Acad Sci USA 85: 4894-4897
57. Morris L, Graham CF, Gordon S (1991) Macrophages in haemopoetic and other tissues of the developing mouse detected by the monoclonal antibody F4/80. Development 112: 517-526
58. Oster GF, Murray JD, Harris AK (1983) Mechanical aspects of mesenchymal morphogenesis. J Embryol Exp Morphol 78: 83-125
59. Piscatelli SJ, Michaels BM, Gregory P, Jennings RW, Longaker MT, Harrison MR, Siebert JW (1994) Fetal fibroblast contraction of collagen matrices in vitro: the effects of epidermal growth factor and transforming growth factor beta. Ann Plast Surg 33: 38-4
60. Ridley AJ, Hall A (1992) The small GTP-binding protein Rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell 70: 389-399
61. Romer J, Bugge TH, Pyke C, Lund LR, Flick MJ, Degen JL, Dano K (1996) Impaired wound healing in mice with a disrupted plasminogen gene. Nature Med 2: 287-292
62. Rugh R (1990) The mouse: its reproduction and development. Oxford University Press, Oxford
63. Saarialho-Kere UK, Kovacs SO, Pentland AP, Olerud JE, Welgus HG, Parks WC (1993) Cell-matrix interactions modulate interstitial collagenase expression by human keratinocytes actively involved in wound healing. J Clin Invest 92: 2858-2866
64. Saarialho-Kere UK, Pentland AP, Birkedal-Hansen H, Parks WC, Welgus HG (1994) Distinct populations of basal keratinocytes express stromelysin-1 and stromelsin-2 in chronic wounds. J Clin Invest 94: 79-88
65. Schafer BM, Maier K, Eickhoff U, Todd RF, Kramer MD (1994) Plasminogen activation in healing human wounds. Am J Pathol 144: 1269-1280
66. Sengel P (1976) Morphogenesis of skin. Cambridge University Press, Cambridge
67. Shah M, Foreman DM, Ferguson MW (1992) Control of scarring in adult wounds by neutralising antibody to transforming growth factor beta. Lancet 25: 213-4
68. Shah M, Foreman DM, Ferguson MWJ (1994) Neutralising antibody to TGFβ1, 2 reduces cutaneous scarring in adult rodents. J Cell Sci 107: 1137-1157
69. Shah M, Foreman DM, Ferguson MW (1995) Neutralisation of TGF beta-1 and TGF beta-2 or exogenous addition of TGF beta-3 to cutaneous rat wounds reduces scarring. J Cell Sci 108: 985-1002
70. Shigeno Y, Ashton BA (1995) Human bone-cell proliferation in vitro decreases with human donor age. J Bone Joint Surg 77: 139-142
71. Simpson DM, Ross R (1972) The neutrophilic leucocyte in wound repair: a study with antineutrophil serum. J Clin Invest 51: 2009-2023
72. Skalli O, Gabbiani G (1988) The biology of the myofibroblast. Relationship to wound contraction and fibrocontractive diseases. In: Clark RAF, Henson PM (eds) The molecular and cellular biology of wound repair. Plenum Press, New York
73. Somasunderam K, Prathrap K (1970) Intra-uterine healing of skin wounds in rabbit foetuses. J Pathol 100: 81-86
74. Somasunderam K, Prathrap K (1972) The effect of exclusion of amniotic fluid on intra-uterine healing of skin in rabbit foetuses. J Pathol 107: 127-130
75. Stannistreet M, Wakely J, England MA (1980) Scanning electron microscopy of wound healing in Xenopus and chicken embryos. J Embryol Exp Morph 59: 341-353
76. Stenn KS, DePalma L (1988) Re-epithelialisation. In: Clark RAF, Henson PM (eds) The molecular and cellular biology of wound repair. Plenum Press, New York, pp 321-335
77. Stopak D, Harris AK (1982) Connective tissue morphogenesis by fibroblast traction. Dev Biol 90: 383-398
78. Sullivan KM, Lorenz HP, Meuli M, Lin RY, Adzick NS (1995) A model of scarless fetal wound repair is deficient in transforming growth factor beta. J Pediatr Surg 30: 198-202
79. Thevenet A (1981) Wound healing of the integument in the 5-day chick embryo. Arch Anat Microsc Morphol Exp 70: 227-244
80. Thevenet A (1984) Proliferation cellulaire au cours de la cicatrisation du tegument d'embryon de poulet de 5 jours. Arch Anat Microsc Morphol Exp 73: 121-132
81. Toole BP (1981) Glycosaminoglycans in morphogenesis. In: Hay ED (ed) Cell biology of the extracellular matrix. Plenum Press, New York
82. Welch MP, Odland GF, Clark RA (1990) Temporal relationships of F-actin bundle formation, collagen and fibronectin matrix assembly, and fibronectin receptor expression to wound contraction. J Cell Biol 110: 133-45
83. Wells MD, Posnick JC, Goldstein J, Slate RK, Keeley FW, Thorner PS (1993) Fetal hone cap healing in utero. J Oral Maxillofac Surg 51: 1235-42
84. Whithy DJ, Ferguson MWJ (1991a) The extracellular matrix of lip wounds in fetal, neonatal and adult mice. Development 112: 651-668
85. Whithy DJ, Ferguson MWJ (1991b) Immunohistochemical localisation of growth factors in fetal wound healing. Dev Biol 147: 207-215
86. Wild AE (1965) Protein composition of the rabbit fetal fluids. Proc R Soc Lond Biol Sci 163: 90-115
87. Young PE, Richman AM, Ketchum AS, Kiehart DP (1993) Morphogenesis in Drosophila requires non-muscle myosin heavy chain function. Genes Dev 7: 29-41