Scarless fetal skin wound healing update

Birth Defects Research Part C - Embryo Today: Reviews

Volumn 96, Issue 3, 2012, Pages 237-247

  Lo, David D ^a,b   Zimmermann, Andrew S ^a   Nauta, Allison ^a,c   Longaker, Michael T ^a   Lorenz, H Peter ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

^c OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Fetal skin; Scar formation; Scarless wound healing

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; CHONDROITIN SULFATE; COLLAGEN TYPE 5; CONNECTIVE TISSUE GROWTH FACTOR; CYTOKINE; DECORIN; ELASTIN; GELATINASE A; GELATINASE B; GROWTH FACTOR; HEPARAN SULFATE; HYALURONIC ACID; HYPOXIA INDUCIBLE FACTOR 1ALPHA; INTERLEUKIN 1; INTERLEUKIN 10; INTERLEUKIN 6; INTERLEUKIN 8; TRANSFORMING GROWTH FACTOR BETA1; TRANSFORMING GROWTH FACTOR BETA2; TRANSFORMING GROWTH FACTOR BETA3; UVOMORULIN; VASCULOTROPIN;

ARTICLE; EXTRACELLULAR MATRIX; FETUS CELL; FIBROBLAST; GENE EXPRESSION; GESTATIONAL AGE; HUMAN; MACROPHAGE; MAST CELL; MESENCHYMAL STEM CELL; NEUTROPHIL; PHENOTYPE; PRIORITY JOURNAL; SCAR; SKIN INJURY; WOUND HEALING;

ADULT; CICATRIX; CYTOKINES; EXTRACELLULAR MATRIX; FETUS; GENE EXPRESSION REGULATION; HUMANS; INFLAMMATION; MACROPHAGES; MAST CELLS; NEUTROPHILS; SKIN PHYSIOLOGICAL PHENOMENA; WOUND HEALING;

EID: 84868102866     PISSN: 1542975X     EISSN: 15429768     Source Type: Journal    
DOI: 10.1002/bdrc.21018     Document Type: Article

References (73)

1. Adzick NS, Longaker MT. 1991. Animal models for the study of fetal tissue repair. J Surg Res 51: 216-222.
2. Adzick NS, Longaker MT. 1992. Scarless fetal healing. Therapeutic implications. Ann Surg 215: 3-7.
3. Adzick NS, Lorenz HP. 1994. Cells, matrix, growth factors, and the surgeon. The biology of scarless fetal wound repair. Ann Surg 220: 10-18.
4. Alaish SM, Yager D, Diegelmann RF, et al. 1994. Biology of fetal wound healing: hyaluronate receptor expression in fetal fibroblasts. J Pediatr Surg 29: 1040-1043.
5. Antony AK, Kong W, Lorenz HP. 2010. Upregulation of neurodevelopmental genes during scarless healing. Ann Plast Surg 64: 247-250.
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: 242-260.
7. Arnardottir HH, Freysdottir J, Hardardottir I. 2012. Two circulating neutrophil populations in acute inflammation in mice. Inflamm Res 61: 931-939.
8. Barrientos S, Stojadinovic O, Golinko MS, et al. 2008. Growth factors and cytokines in wound healing. Wound Repair Regen 16: 585-601.
9. Beanes SR, Dang C, Soo C, et al. 2001. Down-regulation of decorin, a transforming growth factor-beta modulator, is associated with scarless fetal wound healing. J Pediatr Surg 36: 1666-1671.
10. Bouabe H, Liu Y, Moser M, et al. 2011. Novel highly sensitive IL-10-beta-lactamase reporter mouse reveals cells of the innate immune system as a substantial source of IL-10 in vivo. J Immunol 187: 3165-3176.
11. Bullard KM, Longaker MT, Lorenz HP. 2003. Fetal wound healing: current biology. World J Surg 27: 54-61.
12. Burd DA, Longaker MT, Adzick NS, et al. 1990. Foetal wound healing in a large animal model: the deposition of collagen is confirmed. Br J Plast Surg 43: 571-577.
13. Caniggia I, Mostachfi H, Winter J, et al. 2000. Hypoxia-inducible factor-1 mediates the biological effects of oxygen on human trophoblast differentiation through TGFbeta(3). J Clin Invest 105: 577-587.
14. Carter R, Jain K, Sykes V, Lanning D. 2009. Differential expression of procollagen genes between mid- and late-gestational fetal fibroblasts. J Sur Res 156: 90-94.
15. Cass DL, Bullard KM, Sylvester KG, et al. 1997. Wound size and gestational age modulate scar formation in fetal wound repair. J Pediatr Surg 32: 411-415.
16. Cass DL, Bullard KM, Sylvester KG, et al. 1998. Epidermal integrin expression is upregulated rapidly in human fetal wound repair. J Pediatr Surg 33: 312-316.
17. Chin GS, Lee S, Hsu M, et al. 2001. Discoidin domain receptors and their ligand, collagen, are temporally regulated in fetal rat fibroblasts in vitro. Plast Reconstr Surg 107: 769-776.
18. Colwell AS, Krummel TM, Longaker MT, et al. 2006. An in vivo mouse excisional wound model of scarless healing. Plast Reconstr Surg 117: 2292-2296.
19. Colwell AS, Longaker MT, Peter Lorenz H. 2008. Identification of differentially regulated genes in fetal wounds during regenerative repair. Wound Repair Regen 16: 450-459.
20. Couper KN, Blount DG, Riley EM. 2008. IL-10: the master regulator of immunity to infection. J Immunol 180: 5771-5777.
21. Cuttle L, Nataatmadja M, Fraser JF, et al. 2005. Collagen in the scarless fetal skin wound: detection with picrosirius-polarization. Wound Repair Regen 13: 198-204.
22. Dang CM, Beanes SR, Lee H, et al. 2003. Scarless fetal wounds are associated with an increased matrix metalloproteinase-to-tissue-derived inhibitor of metalloproteinase ratio. Plast Reconstr Surg 111: 2273-2285.
23. Ellis IR, Schor SL. 1996. Differential effects of TGF-beta1 on hyaluronan synthesis by fetal and adult skin fibroblasts: implications for cell migration and wound healing. Exp Cell Res 228: 326-333.
24. Estes JM, Vande Berg JS, Adzick NS, et al. 1994. Phenotypic and functional features of myofibroblasts in sheep fetal wounds. Differentiation 56: 173-181.
25. Gurtner GC, Werner S, Barrandon Y, et al. 2008. Wound repair and regeneration. Nature 453: 314-321.
26. Ihara S, Motobayashi Y, Nagao E, et al. 1990. Ontogenetic transition of wound healing pattern in rat skin occurring at the fetal stage. Development 110: 671-680.
27. Jain K, Sykes V, Kordula T, et al. 2008. Homeobox genes Hoxd3 and Hoxd8 are differentially expressed in fetal mouse excisional wounds. J Surg Res 148: 45-48.
28. Kathju S, Satish L, Rabik C, et al. 2006. Identification of differentially expressed genes in scarless wound healing utilizing polymerase chain reaction-suppression subtractive hybridization. Wound repair and regeneration: official publication of the Wound Healing Society [and] the European Tissue Repair Society 14: 413-420.
29. Kennedy CI, Diegelmann RF, Haynes JH, et al. 2000. Proinflammatory cytokines differentially regulate hyaluronan synthase isoforms in fetal and adult fibroblasts. J Pediatr Surg 35: 874-879.
30. Kishi K, Ohyama K, Satoh H, et al. 2006. Mutual dependence of murine fetal cutaneous regeneration and peripheral nerve regeneration. Wound Repair Regen 14: 91-99.
31. Klein JD, Turner CG, Steigman SA, et al. 2011. Amniotic mesenchymal stem cells enhance normal fetal wound healing. Stem Cells Dev 20: 969-976.
32. Kong W, Li S, Longaker MT, et al. 2008. Blood-derived small Dot cells reduce scar in wound healing. Exp Cell Res 314: 1529-1539.
33. Kong W, Li S, Lorenz HP. 2010. Germ plasm-like Dot cells maintain their wound regenerative function after in vitro expansion. Clin Exp Pharmacol Physiol 37: e136-144.
34. Krummel TM, Nelson JM, Diegelmann RF, et al. 1987. Fetal response to injury in the rabbit. J Pediatr Surg 22: 640-644.
35. Larson BJ, Longaker MT, Lorenz HP. 2010. Scarless fetal wound healing: a basic science review. Plastic Reconstr Surg 126: 1172-1180.
36. Laskin DL, Sunil VR, Gardner CR, et al. 2011. Macrophages and tissue injury: agents of defense or destruction? Annu Rev Pharmacol Toxicol 51: 267-288.
37. Liechty KW, Adzick NS, Crombleholme TM. 2000. Diminished interleukin 6 (IL-6) production during scarless human fetal wound repair. Cytokine 12: 671-676.
38. Longaker MT, Chiu ES, Adzick NS, et al. 1991a. Studies in fetal wound healing. V. A prolonged presence of hyaluronic acid characterizes fetal wound fluid. Ann Surg 213: 292-296.
39. Longaker MT, Whitby DJ, Adzick NS, et al. 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: 63-68; discussion 68-69.
40. Longaker MT, Whitby DJ, Ferguson MW, et al. 1994. Adult skin wounds in the fetal environment heal with scar formation. Ann Surg 219: 65-72.
41. Longaker MT, Whitby DJ, Jennings RW, et al. 1991b. Fetal diaphragmatic wounds heal with scar formation. J Surg Res 50: 375-385.
42. Lorenz HP, Longaker MT, Perkocha LA, et al. 1992. Scarless wound repair: a human fetal skin model. Development 114: 253-259.
43. Lorenz HP, Whitby DJ, Longaker MT, et al. 1993. Fetal wound healing. The ontogeny of scar formation in the non-human primate. Ann Surg 217: 391-396.
44. Lovvorn HNIII, Cheung DT, Nimni ME, et al. 1999. Relative distribution and crosslinking of collagen distinguish fetal from adult sheep wound repair. J Pediatr Surg 34: 218-223.
45. Lunderius-Andersson C, Enoksson M, Nilsson G. 2012. Mast Cells Respond to Cell Injury through the Recognition of IL-33. Front Immunol 3: 82.
46. Madlener M. 1998. Differential expression of matrix metalloproteinases and their physiological inhibitors in acute murine skin wounds. Arch Dermatol Res 290 Suppl: S24-29.
47. Mast BA, Diegelmann RF, Krummel TM, et al. 1993. Hyaluronic acid modulates proliferation, collagen and protein synthesis of cultured fetal fibroblasts. Matrix 13: 441-446.
48. Mast BA, Flood LC, Haynes JH, et al. 1991. Hyaluronic acid is a major component of the matrix of fetal rabbit skin and wounds: implications for healing by regeneration. Matrix 11: 63-68.
49. Merkel JR, DiPaolo BR, Hallock GG, et al. 1988. Type I and type III collagen content of healing wounds in fetal and adult rats. Proc Soc Exp Biol Med 187: 493-497.
50. Naik-Mathuria B, Gay AN, Zhu X, et al. 2007. Age-dependent recruitment of neutrophils by fetal endothelial cells: implications in scarless wound healing. J Pediatr Surg 42: 166-171.
51. Olutoye OO, Zhu X, Cass DL, et al. 2005. Neutrophil recruitment by fetal porcine endothelial cells: implications in scarless fetal wound healing. Pediatr Res 58: 1290-1294.
52. Parks WC. 1999. Matrix metalloproteinases in repair. Wound Repair Regen 7: 423-432.
53. Peranteau WH, Zhang L, Muvarak N, et al. 2008. IL-10 overexpression decreases inflammatory mediators and promotes regenerative healing in an adult model of scar formation. J Invest Dermatol 128: 1852-1860.
54. Prockop DJ, Oh JY. 2012. Mesenchymal stem/stromal cells (MSCs): role as guardians of inflammation. Mol Ther 20: 14-20.
55. Rennekampff HO, Hansbrough JF, Kiessig V, et al. 2000. Bioactive interleukin-8 is expressed in wounds and enhances wound healing. J Surg Res 93: 41-54.
56. Rowlatt U. 1979. Intrauterine wound healing in a 20 week human fetus. Virchows Arch A Pathol Anat Histol 381: 353-361.
57. Saed GM, Zhang W, Chegini N, et al. 1999. Alteration of type I and III collagen expression in human peritoneal mesothelial cells in response to hypoxia and transforming growth factor-beta1. Wound Repair Regen 7: 504-510.
58. Satish L, Kathju S. 2010. Cellular and molecular characteristics of scarless versus fibrotic wound healing. Dermatol Res Pract 2010: 790234.
59. Scheid A, Wenger RH, Schaffer L, et al. 2002. Physiologically low oxygen concentrations in fetal skin regulate hypoxia-inducible factor 1 and transforming growth factor-beta3. FASEB J 16: 411-413.
60. Shih B, Garside E, McGrouther DA, et al. 2010. Molecular dissection of abnormal wound healing processes resulting in keloid disease. Wound Repair Regen 18: 139-153.
61. Singer AJ, Clark RA. 1999. Cutaneous wound healing. N Engl J Med 341: 738-746.
62. Soo C, Hu FY, Zhang X, et al. 2000. Differential expression of fibromodulin, a transforming growth factor-beta modulator, in fetal skin development and scarless repair. Am J Pathol 157: 423-433.
63. Stelnicki EJ, Arbeit J, Cass DL, et al. 1998a. Modulation of the human homeobox genes PRX-2 and HOXB13 in scarless fetal wounds. J Invest Dermatol 111: 57-63.
64. Stelnicki EJ, Komuves LG, Holmes D, et al. 1997. The human homeobox genes MSX-1, MSX-2, and MOX-1 are differentially expressed in the dermis and epidermis in fetal and adult skin. Differentiation 62: 33-41.
65. Stelnicki EJ, Komuves LG, Kwong AO, et al. 1998b. HOX homeobox genes exhibit spatial and temporal changes in expression during human skin development. J Invest Dermatol 110: 110-115.
66. Thomas BL, Krummel TM, Melany M, et al. 1998. Collagen synthesis and type expression by fetal fibroblasts invitro. Surg Forum 39: 642-644.
67. Uyeno LA, Newman-Keagle JA, Cheung I, et al. 2001. Hox D3 expression in normal and impaired wound healing. J Surg Res 100: 46-56.
68. Wang S, Qu X, Zhao RC. 2011. Mesenchymal stem cells hold promise for regenerative medicine. Front Med 5: 372-378.
69. Weller K, Foitzik K, Paus R, et al. 2006. Mast cells are required for normal healing of skin wounds in mice. FASEB J 20: 2366-2368.
70. Whitby DJ, Ferguson MW. 1991. The extracellular matrix of lip wounds in fetal, neonatal and adult mice. Development 112: 651-668.
71. Whitby DJ, Longaker MT, Harrison MR, et al. 1991. Rapid epithelialisation of fetal wounds is associated with the early deposition of tenascin. J Cell Sci 99 (Pt 3): 583-586.
72. Wilgus TA, Ferreira AM, Oberyszyn TM, et al. 2008. Regulation of scar formation by vascular endothelial growth factor. Lab Invest 88: 579-590.
73. Wulff BC, Parent AE, Meleski MA, et al. 2012. Mast cells contribute to scar formation during fetal wound healing. J Invest Dermatol 132: 458-465.