Scarless integumentary wound healing in the mammalian fetus: Molecular basis and therapeutic implications

Birth Defects Research Part C - Embryo Today: Reviews

Volumn 96, Issue 3, 2012, Pages 223-236

  Kathju, Sandeep ^a   Gallo, Phillip H ^a   Satish, Latha ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Chaperonins; Collagen; Expressome; Fetal scarless wounds; Growth factors

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; ANTISENSE OLIGONUCLEOTIDE; AVOTERMIN; BASIC FIBROBLAST GROWTH FACTOR RECEPTOR; BECLAPERMIN; COLLAGEN; CYTOKINE; DERMATOLOGICAL AGENT; FIBROBLAST GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 2; FIBROBLAST GROWTH FACTOR 9; GROWTH FACTOR; MANNOSE 6 PHOSPHATE; MATRIX METALLOPROTEINASE; MATRIX METALLOPROTEINASE INHIBITOR; MESSENGER RNA; MICRORNA; PLACEBO; PLATELET DERIVED GROWTH FACTOR; RECOMBINANT FIBROBLAST GROWTH FACTOR; RECOMBINANT PLATELET DERIVED GROWTH FACTOR; RECOMBINANT TRANSFORMING GROWTH FACTOR BETA; RECOMBINANT TRANSFORMING GROWTH FACTOR BETA1; RECOMBINANT VASCULOTROPIN; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA1; TRANSFORMING GROWTH FACTOR BETA2; TRANSFORMING GROWTH FACTOR BETA3; UNCLASSIFIED DRUG; UNINDEXED DRUG; VASCULOTROPIN;

ANGIOGENESIS; ANTISENSE THERAPY; ARTICLE; CELL DEDIFFERENTIATION; CELL DIFFERENTIATION; CELL REGENERATION; CLINICAL TRIAL (TOPIC); CYTOKINE PRODUCTION; DIABETIC FOOT; DRUG EFFICACY; DRUG FORMULATION; DRUG SAFETY; EXTRACELLULAR MATRIX; FETUS; GENE DELIVERY SYSTEM; GENE EXPRESSION; GESTATIONAL AGE; GUINEA PIG; HAPLORHINI; HISTOPATHOLOGY; HUMAN; HYPERTROPHIC SCAR; IMMUNOHISTOCHEMISTRY; INTEGUMENTARY SYSTEM; KERATINOCYTE; MAMMAL; MOLECULAR BIOLOGY; MOLECULARLY TARGETED THERAPY; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; RABBIT; SCAR; SCAR FORMATION; SCARLESS FETAL WOUND HEALING; SHEEP; SKIN; SKIN BIOPSY; SKIN FIBROBLAST; SKIN INJURY; SKIN ULCER; SWINE; TISSUE REPAIR; TREATMENT RESPONSE; WOUND HEALING;

ANIMALS; CHAPERONIN CONTAINING TCP-1; CICATRIX; EXTRACELLULAR MATRIX; FETUS; FIBROBLAST GROWTH FACTORS; GENE EXPRESSION PROFILING; GENES, HOMEOBOX; HUMANS; INTERLEUKIN-10; MAMMALS; PLATELET-DERIVED GROWTH FACTOR; REGENERATION; SKIN PHYSIOLOGICAL PHENOMENA; TRANSFORMING GROWTH FACTOR BETA; VASCULAR ENDOTHELIAL GROWTH FACTOR A; WOUND HEALING;

MAMMALIA;

EID: 84868093263     PISSN: 1542975X     EISSN: 15429768     Source Type: Journal    
DOI: 10.1002/bdrc.21015     Document Type: Article

References (96)

1. Aarabi S, Longaker MT, Gurtner GC. 2007. Hypertrophic scar formation following burns and trauma: new approaches to treatment. PLoS Med 4: e234.
2. Abraham JA, Klagsbrun M. 1996. Modulation of wound repair by members of the fibroblast growth factor family. In: Clark RAF, editor. The molecular and cellular biology of wound repair.2nd ed. New York: Plenum. pp. 195-248.
3. Adzick NS, Longaker MT. 1991. Animal models for the study of fetal tissue repair. J Surg Res 51: 216-222.
4. Antony AK, Kong W, Lorenz HP. 2010. Upregulation of neurodevelopmental genes during scarless healing. Ann Plast Surg 64: 247-250.
5. 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.
6. Bayat A, McGrouther DA, Ferguson MWJ. 2003. Skin Scarring. BMJ 326: 88-92.
7. Beer HD, Longaker MT, Werner S. 1997. Reduced expression of PDGF and PDGF receptors during impaired wound healing. J Invest Dermatol 109: 132-138.
8. Brown BC, McKenna SP, Siddhi K, et al. 2008. The hidden cost of skin scars: quality of life after skin scarring. J Plast Reconstr Aesthet Surg 61: 1049-1058.
9. Brown LF, Yeo KT, Berse B, et al. 1992. Expression of vascular permeability factor (vascular endothelial growth factor) by epidermal keratinocytes during wound healing. J Exp Med 176: 1375-1379.
10. 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.
11. Chen W, Fu X, Ge S, et al. 2007. Profiling of genes differentially expressed in a rat of early and later gestational ages with high-density oligonucleotide DNA array. Wound Repair Regen 15: 147-155.
12. Chen W, Fu XB, Ge SL, et al. 2005. Ontogeny of expression of basic fibroblast growth factor and its receptors in human fetal skin. Chin J Traumatol 8: 332-338.
13. Chen W, Fu X, Ge S, et al. 2005. Ontogeny of expression of transforming growth factor-beta and its receptors and their possible relationship with scarless healing in human fetal skin. Wound Repair Regen 13: 68-75.
14. Cheng J, Yu H, Deng S, et al. 2010. MicroRNA profiling in mid-and late-gestational fetal skin: implication for scarless wound healing. Tohoku J Exp Med 221: 203-209.
15. Choi BM, Kwak HJ, Jun CD, et al. 1996. Control of scarring in adult wounds using antisense transforming growth factor-beta 1 oligodeoxynucleotides. Immunol Cell Biol 74: 144-150.
16. Colwell AS, Beanes SR, Soo C, et al. 2005. Increased angiogenesis and expression of vascular endothelial growth factor during scarless repair. Plast Reconstr Surg 115: 204-212.
17. Colwell AS, Krummel TM, Longaker MT, et al. 2006. Early-gestation fetal scarless wounds have less lysyl oxidase expression. Plast Reconstr Surg 118: 1125-1129.
18. Colwell AS, Longaker MT, Lorenz HP. 2008. Identification of differentially regulated genes in fetal wounds during regenerative repair. Wound Repair Regen 16: 450-459.
19. 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.
20. Dang CM, Beanes SR, Soo C, et al. 2003. Decreased expression of fibroblast and keratinocyte growth factor isoforms and receptors during scarless repair. Plast Reconstr Surg 111: 1969-1979.
21. Darden DL, Hu FZ, Ehrlich MD, et al. 2000. RNA differential display of scarless wound healing in fetal rabbit indicates downregulation of a CCT chaperonin subunit and upregulation of a glycophorin-like gene transcript. J Pediatr Surg 35: 406-419.
22. Dennis PA, Rifkin DB. 1991. Cellular activation of latent transforming growth factor beta requires binding to the cation-independent mannose 6-phosphate/insulin-like growth factor type II receptor. Proc Natl Acad Sci USA 88: 580-584.
23. Dohar JE, Klein EC, Betsch JL, et al. 1998. Fetal airway wound repair: a new frontier. Arch Otolaryngol Head Neck Surg 124: 25.
24. Duncan BW, Qian J, Liu X, et al. 1992. Regulation of prolyl hydroxylase activity in fetal and adult fibroblasts. In: Adzick NS, Longaker MT, editors. Fetal wound healing. New York, NY: Elsevier Scientific Press. pp. 303-323, Chapter 20.
25. Ferguson MW, Duncan J, Bond J, et al. 2009. Prophylactic administration of avotermin for improvement of skin scarring: three double-blind, placebo-controlled, phase I/II studies. Lancet 373: 1264-1274.
26. Frantz FW, Bettinger DA, Haynes JH, et al. 1993. Biology of fetal repair: the presence of bacteria in fetal wounds induces an adult-like healing response. J Pediatr Surg 28: 428-433.
27. Freund RM, Siebert JW, Cabrera RC, et al. 1993. Serial quantitation of hyaluronan and sulfated glycosaminoglycans in fetal sheep skin. Biochem Mol Biol Int 29: 773-783.
28. Fricke NB, Omnell ML, Dutcher KD, et al. 1996. Skeletal and dental disturbances after facial burns and pressure garments. J Burn Care Rehabil 17: 338-345.
29. Galiano RD, Tepper OM, Pelo CR, et al. 2004. Topical vascular endothelial growth factor accelerates diabetic wound healing through increased angiogenesis and by mobilizing and recruiting bone marrow-derived cells. Am J Pathol 164: 1935-1947.
30. Gallo PH, Satish L, Johnson S, et al. 2011. Increased expression of Ero1L-alpha in healing fetal wounds. BMC Res Notes 4: 175.
31. Gelbard M, Lindner A, Chvapil M, et al. 1983. Topical beta-aminopropionitrile in the treatment of Peyronie's disease. J Urol 129: 746-748.
32. Gordon A, Kozin ED, Keswani SG, et al. 2008. Permissive environment in postnatal wounds induced by adenoviral-mediated overexpression of the anti-inflammatory cytokine IL-10 prevents scar formation. Wound Repair Regen 16: 70-79.
33. Haynes JH, Johnson DE, Mast BA, et al. 1994. Platelet-derived growth factor induces fetal wound fibrosis. J Pediatr Surg 29: 1405-1408.
34. Hess A. Reactions of mammalian fetal tissues to injury. II. Skin. 1954. Anat Rec 119: 435-447.
35. Heyborne KD, McGregor JA, Henry G, et al. 1994. Interleukin-10 in amniotic fluid at midtrimester: immune activation and suppression in relation to fetal growth. Am J Obstet Gynecol 171: 55-59.
36. Hsu M, Peled ZM, Chin GS, et al. 2001. Ontogeny of expression of transforming growth factor-beta 1 (TGF-beta 1), TGF-beta 3, and TGF-beta receptors I and II in fetal rat fibroblasts and skin. Plast Reconstr Surg 107: 1787-1794.
37. 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.
38. Jain K, Sykes V, Kordula T, et al. 2008. Homoebox genes Hoxd3 and Hoxd8 are differentially expressed in fetal mouse excisional wounds. J Surg Res 148: 45-48.
39. 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 Regen 14: 413-420.
40. Krummel TM, Michna BA, Thomas BL, et al. 1988. Transforming growth factor beta (TGF_beta) induces fibrosis in a fetal wound model. J Pediatr Surg 23: 647-652.
41. Kumar S, Wong PF, Leaper DJ. 2009. Intra-peritoneal prophylactic agents for preventing adhesions and adhesive intestinal obstruction after non-gynaecological abdominal surgery. Cochrane Database Syst Rev 1: CD005080.
42. Kwon MJ, An S, Choi S, et al. 2012. Effective healing of diabetic skin wounds by using nonviral gene therapy based on minicircle vascular endothelial growth factor DNA and a cationic dendrimer. J Gene Med 14: 272-278.
43. La Trenta GS, Grant RT, Haworth RD, et al. 1992. Functional reconstruction for severe postburn microstomia. Ann Plast Surg 29: 178-181.
44. Lauer G, Sollberg G, Cole M, et al. 2000. Expression and proteolysis of vascular endothelial growth factor is increased in chronic wounds. J Invest Dermatol 115: 12-18.
45. Li HS, Hebda PA, Kelly LA, et al. 2000. Differential display identifying higher levels of EP4 in fetal skin wounds. Arch Otolaryngol Head Neck Surg 126: 1337-1443.
46. Li Z, Hassan MQ, Jafferji M, et al. 2009. Biological functions of miR-29b contribute to positive regulation of osteoblast differentiation. J Biol Chem 284: 15676-15684.
47. Liechty KW, Kim HB, Adzick NS, et al. 2000. Fetal wound repair results in scar formation in interleukin-10 deficient mice in a syngeneic murine model of scarless fetal wound repair. J Pediatr Surg 35: 866-872.
48. Liechty KW, Adzick NS, Crombleholme TM. 2000. Diminished IL-6 production during scarless human fetal wound repair. Cytokine 12: 671-676.
49. Liechty KW, Crombleholme TM, Cass DL, et al. 1998. Diminished IL-8 production in the fetal wound healing response. J Surg Res 77: 80-84.
50. 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.
51. 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.
52. Longaker MT, Whitby DJ, Jennings RW, et al. 1991. Fetal diaphragmatic wounds heal with scar formation. J Surg Res 50: 375-385.
53. Lorenz HP, Longaker MT, Perkocha LA, et al. 1992. Scarless wound repair: a human fetal skin model. Development 114: 253-259.
54. 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.
55. Maragakis GM, Garcia-Tempone M. 1998. Microstomia following facial burns. J Clin Pediatr Dent 23: 69-74.
56. Mast BA, Haynes JH, Krummel TM, et al. 1992. In vivo degradation of fetal wound hyaluronic acid results in increased fibroplasia, collagen deposition, and neovascularization. Plast Reconstr Surg 89: 503-509.
57. Meuli M, Lorenz HP, Hedrick MH, et al. 1995. Scar formation in the fetal alimentary tract. J Pediatr Surg 30: 392-395.
58. Mignatti P, Rifkin DB, Welgus HG, et al. 1996. Proteinases and tissue remodeling. In: Clark RAF, editor. The molecular and cellular biology of wound repair. New York: Plenum Press. pp. 427-474.
59. Mustoe TA, Cutler NR, Allman RM, et al. 1994. A phase II study to evaluate recombinant platelet-derived growth factor-BB in the treatment of stage 3 and 4 pressure ulcers. Arch Surg 129: 213-219.
60. Occleston NL, O'Kane S, Laverty HG, et al. 2011. Discovery and development of avotermin (recombinant human transforming growth factor beta 3): a new class of prophylactic therapeutic for the improvement of scarring. Wound Repair Regen 19( Suppl 1): s38--s48.
61. Peacock EEJr. 1981. Pharmacologic control of surface scarring in human beings. Ann Surg 193: 592-597.
62. Peacock EEJr. 1981. Control of wound healing and scar formation in surgical patients. Arch Surg 116: 1325-1329.
63. Peacock EE, Madden JW. 1978. Administration of beta-aminopropionitrile to human beings with urethral strictures: a preliminary report. Am J Surg 136: 600-605.
64. Peranteau WH, Zhang L, Muvarak N, et al. 2008. IL-10 overexpression decreases inflammatory mediators and promotes regenerative healing in an adult models of scar formation. J Invest Dermatol 128: 1852-1860.
65. Peters KG, deVries C, Williams LT. 1993. Vascular endothelial growth factor receptor expression during embryogenesis and tissue repair suggests a role in endothelial differentiation and blood vessel growth. Proc Natl Acad Sci USA 90: 8915-8919.
66. Pierce GF, Tarpley JE, Tseng J, et al. 1995. Detection of platelet-derived growth factor (PDGF)-AA in actively healing human wounds treated with recombinant PDGF-BB and absence of PDGF in chronic nonhealing wounds. J Clin Invest 96: 1336-1350.
67. Rankin M, Borah GL. 2003. Perceived functional impact of abnormal facial appearance. Plast Reconstr Surg 111: 2140-2146.
68. Roberts AB, Sporn MB. 1996. Transforming growth factor-beta. In: Clark RAF, editor. The molecular and cellular biology of wound repair. New York: Plenum Press. pp. 275-308.
69. Rowlatt U. 1979. Intrauterine wound healing in a 20 week human fetus. Virchows Arch A Pathol Anat Histol 381: 353-361.
70. Satish L, Abdulally A, Oswald D, et al. 2008. Differential expression of chaperonin containing T-complex polypeptide (CCT) subunits during fetal and adult skin wound healing. Cell Stress Chaperones 13: 527-533.
71. Satish L, Johnson S, Abdulally A, et al. 2010a. Cloning and expression of rabbit CCT subunits eta and beta in healing cutaneous wounds. Cell Stress Chaperones 15: 819-826.
72. Satish L, Johnson S, Wang JH, et al. 2010b. Chaperonin containing T-complex polypeptide subunit eta (CCT-eta) is a specific regulator of fibroblast motility and contractility. PLoS One 5: e10063.
73. Shah M, Foreman DM, Ferguson MW. 1994. Neutralising antibody to TGF-beta 1, 2 reduces cutaneous scarring in adult rodents. J Cell Sci 107: 1137-1157.
74. Shah M, Foreman DM, Ferguson MWJ. 1992. Control of scarring in adult wounds by neutralizing antibody to transforming growth factor β. Lancet 339: 213-214.
75. 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.
76. Shilo S, Roy S, Khanna S, et al. 2007. MicroRNA in cutaneous wound healing: a new paradigm. DNA Cell Biol 26: 227-237.
77. Somasundaram K, Prathap K. 1970. Intra-uterine healing of skin wounds in rabbit fetuses. J Pathol 100: 81-86.
78. Somasundaram K, Prathap K. 1972. The effect of exclusion of amniotic fluid on intra-uterine healing of skin wounds in rabbit fetuses. J Pathol 107: 127-130.
79. Staley M, Richard R, Billmire D, et al. 1997. Head/face/neck burns: therapist considerations for the pediatric patient. J Burn Care Rehabil 18: 164-171.
80. Steed DL. 1995. Clinical evaluation of recombinant human platelet-derived growth factor for the treatment of lower extremity diabetic ulcers. Diabetic Ulcer Study Group. J Vasc Surg 21: 71-78.
81. Stelnicki EJ, KÖmÜves 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 andadult skin. Differentiation 62: 33-41.
82. Stelnicki EJ, KÖmÜves LG, Kwong AO, et al. 1998. Differential HOX homeobox gene expression during human skin development. J Invest Dermatol 110: 110-115.
83. Stelnicki EJ, Arbeit J, Cass DL, et al. 1998. Modulation of the human homeobox genes PRX-2 and HOXB13 in scarless fetal wounds. J Invest Dermatol 111: 57-63.
84. Swift ME, Kleinman HK, DiPietro LA. 1999. Impaired wound repair and delayed angiogenesis in aged mice. Lab Invest 79: 1479-1487.
85. Teusner JT, Goddard C, Belford DA, et al. 2006. Identification of novel FCgammaRIII-X expression was identified during scarless healing. Wound Repair Regen 14: 405-412.
86. Tower I, Lasko LA, Kathju S. 2010. Secondary surgery for cicatricial complications of facial injury. J Oral Maxillofac Surg 68: 751-755.
87. Uygur F, Sever C, Tuncer S, et al. 2009. Reconstruction of postburn antebrachial contractures using pedicled thoracodorsal artery perforator flaps. Plast Reconstr Surg 123: 1544-1552.
88. van der Wal JB, Iordens GI, Vrijland WW, et al. 2011. Adhesion prevention during laparotomy: long-term follow-up of a randomized clinical trial. Ann Surg 253: 1118-1121.
89. van Rooij E, Sutherland LB, Thatcher JE, et al. 2008. Dysregulation of microRNAs after myocardial infarction reveals a role of miR-29 in cardiac fibrosis. Proc Natl Acad Sci USA 105: 13027-13032.
90. Wang XQ, Hayes MT, Kempf M, et al. 2008. Fetuin-A: a major fetal serum protein that promotes "wound closure" and scarless healing. J Invest Dermatol 128: 753-757.
91. Werner S, Grose R. 2003. Regulation of wound healing by growth factors and cytokines. Physiol Rev 83: 835-870.
92. Whitby DJ, Ferguson MW. 1991. Immunohistochemical localization of growth factors in fetal wound healing. Dev Biol 147: 207-215.
93. Whitby DJ, Ferguson MWJ. 1991. The extracellular matrix of lip wounds in fetal, neonatal and adult mice. Development 112: 651-668.
94. Wilgus TA, Ferreira AM, Oberyszyn TM, et al. 2008. Regulation of scar formation by vascular endothelial growth factor. Lab Invest 88: 579-590.
95. White P, Thomas DW, Fong S, et al. 2003. Deletion of the homeobox gene PRX-2 affects fetal but not adult fibroblast wound healing responses. J Invest Dermatol 120: 135-144.
96. Yang Y, Ge S. 1995. [Effect of hyaluronic acid-stimulating factor on scar formation in wound healing process of deep partial thickness burns] Zhonghua Zheng Xing Shao Shang Wai Ke Za Zhi 11: 339-342.