Extracellular Matrix and Dermal Fibroblast Function in the Healing Wound

Advances in Wound Care

Volumn 5, Issue 3, 2016, Pages 119-136

  Tracy, Lauren E ^a   Minasian, Raquel A ^a   Caterson, E J ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGGRECAN; BIGLYCAN; CHONDROITIN SULFATE; COLLAGEN; COLLAGEN TYPE 1; COLLAGEN TYPE 3; COLLAGEN TYPE 4; COLLAGEN TYPE 5; COLLAGEN TYPE 6; COLLAGEN TYPE 7; DECORIN; DERMATAN SULFATE; ELASTIN; FIBRILLAR COLLAGEN; FIBRILLIN 1; FIBRILLIN 2; FIBRIN; FIBRONECTIN; FIBULIN 5; GLYCOSAMINOGLYCAN; HYALURONIC ACID; KALININ; LUMICAN; NONFIBRILLAR COLLAGEN; OSTEOPONTIN; PROTEOGLYCAN; STRUCTURAL PROTEIN; TENASCIN; VERSICAN; VITRONECTIN;

CELL METABOLISM; CELL MIGRATION; CELL SURVIVAL; CHRONOLOGY; EX VIVO STUDY; EXTRACELLULAR MATRIX; HUMAN; PRIORITY JOURNAL; REVIEW; SKIN FIBROBLAST; TENSION; TISSUE CULTURE; TISSUE ENGINEERING; TISSUE SCAFFOLD; WOUND DRESSING; WOUND HEALING;

EID: 84988586157     PISSN: 21621918     EISSN: 21621934     Source Type: Journal    
DOI: 10.1089/wound.2014.0561     Document Type: Review

References (188)

1. Stoker M, O'Neill C, Berryman S, Waxman V. Anchorage and growth regulation in normal and virus-transformed cells. Int J Cancer 1968;3: 683-693.
2. Alberts J, Johnson B, Lewis A. The Extracellular Matrix of Animals. New York: Garland Science, 2002.
3. Majno G, Gabbiani G, Hirschel BJ, Ryan GB, Statkov PR. Contraction of granulation tissue in vitro: similarity to smooth muscle. Science 1971;173:548-550.
4. Schultz GS, Wysocki A. Interactions between extracellular matrix and growth factors in wound healing. Wound Repair Regen 2009;17:153-162.
5. Sorrell JM, Baber MA, Caplan AI. Clonal characterization of fibroblasts in the superficial layer of the adult human dermis. Cell Tissue Res 2007;327:499-510.
6. Sorrell JM, Baber MA, Caplan AI. Site-matched papillary and reticular human dermal fibroblasts differ in their release of specific growth factors/cytokines and in their interaction with keratinocytes. J Cell Physiol 2004;200:134-145.
7. Nolte SV, Xu W, Rennekampff H-O, Rodemann HP. Diversity of fibroblasts - a review on implications for skin tissue engineering. Cells Tissues Organs 2008;187:165-176.
8. Sorrell JM, Caplan AI. Fibroblast heterogeneity: more than skin deep. J Cell Sci 2004;117:667-675.
9. Ali-Bahar M, Bauer B, Tredget EE, Ghahary A. Dermal fibroblasts from different layers of human skin are heterogeneous in expression of collagenase and types I and III procollagen mRNA. Wound Repair Regen 2004;12:175-182.
10. Andrade ZA, de-Oliveira-Filho J, Fernandes AL. Interrelationship between adipocytes and fibroblasts during acute damage to the subcutaneous adipose tissue of rats: an ultrastructural study. Braz J Med Biol Res 1998;31:659-664.
11. Matsumoto T, et al. Mature adipocyte-derived dedifferentiated fat cells exhibit multilineage potential. J Cell Physiol 2008;215:210-222.
12. Tholpady SS, et al. The cellular plasticity of human adipocytes. Ann Plast Surg 2005;54:651-656.
13. Schrimpf C, Duffield JS. Mechanisms of fibrosis: the role of the pericyte. Curr Opin Nephrol Hypertens 2011;20:297-305.
14. Karén J, et al. Effects of the histone deacetylase inhibitor valproic acid on human pericytes in vitro. PLoS One 2011;6:e24954.
15. Piera-Velazquez S, Li Z, Jimenez SA. Role of endothelial-mesenchymal transition (EndoMT) in the pathogenesis of fibrotic disorders. Am J Pathol 2011;179:1074-1080.
16. Lee JG, Ko MK, Kay EP. Endothelial mesenchymal transformation mediated by IL-1b-induced FGF-2 in corneal endothelial cells. Exp Eye Res 2012;95:35-39.
17. Lin F, Wang N, Zhang T-C. The role of endothelial-mesenchymal transition in development and pathological process. IUBMB Life 2012;64: 717-723.
18. Slukvin II, Vodyanik M. Endothelial origin of mesenchymal stem cells. Cell Cycle 2011;10: 1370-1373.
19. Takahashi K, Yamanaka, S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006;126:663-676.
20. Takahashi K, et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007;131:861-872.
21. Yu, J. et al. Induced pluripotent stem cell lines derived from human somatic cells. Science 2007;318:1917-1920.
22. Kiwanuka E, Junker J, Eriksson, E. Harnessing growth factors to influence wound healing. Clin Plast Surg 2012;39:239-248.
23. Barrientos S, Stojadinovic O, Golinko MS, Brem H, Tomic-Canic M. Growth factors and cytokines in wound healing. Wound Repair Regen 2008;16: 585-601.
24. Bainbridge P. Wound healing and the role of fibroblasts. J Wound Care 2013;22:407-408, 410-412.
25. Donovan J, Abraham D, Norman, J. Plateletderived growth factor signaling in mesenchymal cells. Front Biosci (Landmark Ed) 2013;18:106-119.
26. Järveläinen H, Sainio A, Koulu M, Wight TN, Penttinen R. Extracellular matrix molecules: potential targets in pharmacotherapy. Pharmacol Rev 2009;61:198-223.
27. Weinstein G, Boucek, R. Collagen and elastin of human dermis. J Invest Dermatol 1960;35:227-229.
28. Frantz C, Stewart KM, Weaver VM. The extracellular matrix at a glance. J Cell Sci 2010;123: 4195-4200.
29. Carrino DA, Sorrell JM, Caplan AI. Age-related changes in the proteoglycans of human skin. Arch Biochem Biophys 2000;373:91-101.
30. Okamoto O, Fujiwara S. Dermatopontin, a novel player in the biology of the extracellular matrix. Connect Tissue Res 2006;47:177-189.
31. Bornstein P, Sage EH. Matricellular proteins: extracellular modulators of cell function. Curr Opin Cell Biol 2002;14:608-616.
32. Eyre DR. Collagen: molecular diversity in the body's protein scaffold. Science 1980;207:1315-1322.
33. Smith LT, Holbrook KA, Madri JA. Collagen types I, III, and V in human embryonic and fetal skin. Am J Anat 1986;175:507-521.
34. Cox HT. The cleavage lines of the skin. Br J Surg 1941;29:234-240.
35. KRAISSL CJ. The selection of appropriate lines for elective surgical incisions. Plast Reconstr Surg (1946) 1951;8:1-28.
36. Piérard GE, Lapière CM. Microanatomy of the dermis in relation to relaxed skin tension lines and Langer's lines. Am J Dermatopathol 1987; 9:219-224.
37. Ridge MD, Wright V. The directional effects of skin. A bio-engineering study of skin with particular reference to Langer's lines. J Invest Dermatol 1966;46:341-346.
38. Sakai S, Yamanari M, Lim Y, Nakagawa N, Yasuno Y. In vivo evaluation of human skin anisotropy by polarization-sensitive optical coherence tomography. Biomed Opt Express 2011;2:2623-2631.
39. Baur PS, Larson DL, Stacey TR. The observation of myofibroblasts in hypertrophic scars. Surg Gynecol Obstet 1975;141:22-26.
40. Junker JPE, Kratz C, Tollbäck A, Kratz G. Mechanical tension stimulates the transdifferentiation of fibroblasts into myofibroblasts in human burn scars. Burns 2008;34:942-946.
41. Varani J, et al. Decreased collagen production in chronologically aged skin: roles of age-dependent alteration in fibroblast function and defective mechanical stimulation. Am J Pathol 2006;168:1861-1868.
42. Liu F, et al. Feedback amplification of fibrosis through matrix stiffening and COX-2 suppression. J Cell Biol 2010;190:693-706.
43. Prager-Khoutorsky, M. et al. Fibroblast polarization is a matrix-rigidity-dependent process controlled by focal adhesion mechanosensing. Nat Cell Biol 2011;13:1457-1465.
44. Huang X, et al. Matrix stiffness-induced myofibroblast differentiation is mediated by intrinsic mechanotransduction. Am J Respir Cell Mol Biol 2012;47:340-348.
45. Marinković A, Mih JD, Park J-A, Liu F, Tschumperlin DJ. Improved throughput traction microscopy reveals pivotal role for matrix stiffness in fibroblast contractility and TGF-b responsiveness. Am J Physiol Lung Cell Mol Physiol 2012;303:L169-L180.
46. Leight JL, Wozniak MA, Chen S, Lynch ML, Chen CS. Matrix rigidity regulates a switch between TGF-b1-induced apoptosis and epithelial-mesenchymal transition 2012; Mol Biol Cell 23:781-791.
47. Karamichos D, Brown RA, Mudera V. Collagen stiffness regulates cellular contraction and matrix remodeling gene expression. J Biomed Mater Res 2007;A 83:887-894.
48. Derderian CA, et al. Mechanical strain alters gene expression in an in vitro model of hypertrophic scarring. Ann Plast Surg 2005;55:69-75; discussion 75.
49. Wen H, Blume PA, Sumpio BE. Role of integrins and focal adhesion kinase in the orientation of dermal fibroblasts exposed to cyclic strain. Int Wound J 2009;6:149-158.
50. Jones C, Ehrlich HP. Fibroblast expression of asmooth muscle actin, a2b1 integrin and avb3 integrin: influence of surface rigidity. Exp Mol Pathol 2011;91:394-399.
51. Ziade M, et al. Use of botulinum toxin type A to improve treatment of facial wounds: a prospective randomised study. J Plast Reconstr Aesthet Surg 2013;66:209-214.
52. Gauglitz GG, et al. Botulinum toxin A for the treatment of keloids. Skin Pharmacol Physiol 2012;25:313-318.
53. Lygoe KA, Wall I, Stephens P, Lewis MP. Role of vitronectin and fibronectin receptors in oral mucosal and dermal myofibroblast differentiation. Biol Cell 2007;99:601-614.
54. Nakamoto T, et al. Analysis of gene expression profile in p130(Cas)-deficient fibroblasts. Biochem Biophys Res Commun 2002;294:635-641.
55. Zouq NK, et al. FAK engages multiple pathways to maintain survival of fibroblasts and epithelia: differential roles for paxillin and p130Cas. J Cell Sci 2009;122:357-367.
56. Wong VW, Longaker MT, Gurtner GC. Soft tissue mechanotransduction in wound healing and fibrosis. Semin Cell Dev Biol 2012;23:981-986.
57. Wong VW, et al. Focal adhesion kinase links mechanical force to skin fibrosis via inflammatory signaling. Nat Med 2012;18:148-152.
58. Paterno J, et al. Akt-mediated mechanotransduction in murine fibroblasts during hypertrophic scar formation. Wound Repair Regen 2011;19:49-58.
59. Xia H, Nho RS, Kahm J, Kleidon J, Henke CA. Focal adhesion kinase is upstream of phosphatidylinositol 3-kinase/Akt in regulating fibroblast survival in response to contraction of type I collagen matrices via a beta 1 integrin viability signaling pathway. J Biol Chem 2004;279: 33024-33034.
60. Davis J, Burr AR, Davis GF, Birnbaumer L, Molkentin JD. A TRPC6-dependent pathway for myofibroblast transdifferentiation and wound healing in vivo. Dev Cell 2012;23:705-715.
61. Volk SW, Wang Y, Mauldin EA, Liechty KW, Adams SL. Diminished type III collagen promotes myofibroblast differentiation and increases scar deposition in cutaneous wound healing. Cells Tissues Organs 2011;194:25-37.
62. Liu X, Wu H, Byrne M, Krane S, Jaenisch R. Type III collagen is crucial for collagen I fibrillogenesis and for normal cardiovascular development. Proc Natl Acad Sci U S A 1997;94:1852-1856.
63. Merkel JR, DiPaolo BR, Hallock GG, Rice DC. Type I and type III collagen content of healing wounds in fetal and adult rats. Proc Soc Exp Biol Med 1988;187:493-497.
64. Carter R, Jain K, Sykes V, Lanning D. Differential expression of procollagen genes between midand late-gestational fetal fibroblasts. J Surg Res 2009;156:90-94.
65. Cuttle L, et al. Collagen in the scarless fetal skin wound: detection with picrosirius-polarization. Wound Repair Regen 2005;13:198-204.
66. Burd DA, Longaker MT, Adzick NS, Harrison MR, Ehrlich HP. Foetal wound healing in a large animal model: the deposition of collagen is confirmed. Br J Plast Surg 1990;43:571-577.
67. Wenstrup RJ, et al. Type V collagen controls the initiation of collagen fibril assembly. J Biol Chem 2004;279:53331-53337.
68. Zoppi N, Gardella R, De Paepe A, Barlati S, Colombi M. Human fibroblasts with mutations in COL5A1 and COL3A1 genes do not organize collagens and fibronectin in the extracellular matrix, down-regulate alpha2beta1 integrin, and recruit alphavbeta3 Instead of alpha5beta1 integrin. J Biol Chem 2004;279:18157-18168.
69. Chanut-Delalande H, et al. Development of a functional skin matrix requires deposition of collagen V heterotrimers. Mol Cell Biol 2004;24: 6049-6057.
70. Martin P, et al. Abnormal collagen V deposition in dermis correlates with skin thickening and disease activity in systemic sclerosis. Autoimmun Rev 2012;11:827-835.
71. Viglio S, et al. Rescue of migratory defects of Ehlers-Danlos syndrome fibroblasts in vitro by type V collagen but not insulin-like binding protein-1. J Invest Dermatol 2008;128:1915-1919.
72. Donaghue VM, et al. Evaluation of a collagenalginate wound dressing in the management of diabetic foot ulcers. Adv Wound Care 11:114-119.
73. Becker GD, Adams LA, Hackett J. Collagen-assisted healing of facial wounds after Mohs surgery. Laryngoscope 1994;104:1267-1270.
74. Graumlich JF, et al. Healing pressure ulcers with collagen or hydrocolloid: a randomized, controlled trial. J Am Geriatr Soc 2003;51:147-154.
75. Rühl M, et al. Soluble collagen VI drives serumstarved fibroblasts through S phase and prevents apoptosis via down-regulation of Bax. J Biol Chem 1999;274:34361-34368.
76. Betz P, et al. Time-dependent pericellular expression of collagen type IV, laminin, and heparan sulfate proteoglycan in myofibroblasts. Int J Legal Med 1992;105:169-172.
77. Jongewaard IN, Lauer RM, Behrendt DA, Patil S, Klewer SE. Beta 1 integrin activation mediates adhesive differences between trisomy 21 and non-trisomic fibroblasts on type VI collagen. Am J Med Genet 2002;109:298-305.
78. Karousou E, et al. New insights into the pathobiology of Down syndrome - hyaluronan synthase-2 overexpression is regulated by collagen VI a2 chain. FEBS J 2013;280:2418-2430.
79. Mik G, Gholve PA, Scher DM, Widmann RF, Green DW. Down syndrome: orthopedic issues. Curr Opin Pediatr 2008;20:30-36.
80. Nyström A, et al. Collagen VII plays a dual role in wound healing. J Clin Invest 2013;123:3498-3509.
81. Wang X, et al. Topical application of recombinant type VII collagen incorporates into the dermal-epidermal junction and promotes wound closure. Mol Ther 2013;21:1335-1344.
82. Woodley DT, et al. Intravenously injected human fibroblasts home to skin wounds, deliver type VII collagen, and promote wound healing. Mol Ther 2007;15:628-635.
83. Ruehl M, et al. The elongated first fibronectin type III domain of collagen XIV is an inducer of quiescence and differentiation in fibroblasts and preadipocytes. J Biol Chem 2005;280:38537-38543.
84. Ansorge HL, et al. Type XIV Collagen Regulates Fibrillogenesis: PREMATURE COLLAGEN FIBRIL GROWTH AND TISSUE DYSFUNCTION IN NULL MICE. J Biol Chem 2009;284:8427-8438.
85. Pereira M, et al. The incorporation of fibrinogen into extracellular matrix is dependent on active assembly of a fibronectin matrix. J Cell Sci 2002;115:609-617.
86. Tuan TL, Song A, Chang S, Younai S, Nimni ME. In vitro fibroplasia: matrix contraction, cell growth, and collagen production of fibroblasts cultured in fibrin gels. Exp Cell Res 1996;223: 127-134.
87. Coustry F, Gillery P, Maquart FX, Borel JP. Effect of transforming growth factor beta on fibroblasts in three-dimensional lattice cultures. FEBS Lett 1990;262:339-341.
88. Sander EA, Barocas VH, Tranquillo RT. Initial fiber alignment pattern alters extracellular matrix synthesis in fibroblast-populated fibrin gel cruciforms and correlates with predicted tension. Ann Biomed Eng 2011;39:714-729.
89. Gildner CD, Roy DC, Farrar CS, Hocking DC. Opposing effects of collagen I and vitronectin on fibronectin fibril structure and function. Matrix Biol 2014;34:33-45.
90. Corbett SA, Lee L, Wilson CL, Schwarzbauer JE. Covalent cross-linking of fibronectin to fibrin is required for maximal cell adhesion to a fibronectin-fibrin matrix. J Biol Chem 1997;272: 24999-25005.
91. Sottile J, Hocking DC. Fibronectin polymerization regulates the composition and stability of extracellular matrix fibrils and cell-matrix adhesions. Mol Biol Cell 2002;13:3546-3559.
92. Sethi KK, et al. Evidence for sequential utilization of fibronectin, vitronectin, and collagen during fibroblast-mediated collagen contraction. Wound Repair Regen 2002;10:397-408.
93. Obara M, Yoshizato K. A novel domain of fibronectin revealed by epitope mapping of a monoclonal antibody which inhibits fibroblastsmediated collagen gel contraction. FEBS Lett 1997;412:48-52.
94. Kwon A-H, Qiu Z, Hirao Y. Topical application of plasma fibronectin in full-thickness skin wound healing in rats. Exp Biol Med (Maywood) 2007; 232:935-941.
95. Schvartz I, Seger D, Shaltiel S. Vitronectin. Int J Biochem Cell Biol 1999;31:539-544.
96. Nissen NN, Shankar R, Gamelli RL, Singh A, Di-Pietro LA. Heparin and heparan sulphate protect basic fibroblast growth factor from non-enzymic glycosylation. Biochem J 1999;338:637-642.
97. Antonicelli F, Bellon G, Lorimier S, Hornebeck W. Role of the elastin receptor complex (S-Gal/Cath-A/Neu-1) in skin repair and regeneration. Wound Repair Regen 2009;17:631-638.
98. Almine JF, et al. Elastin sequences trigger transient proinflammatory responses by human dermal fibroblasts. FASEB J 2013;27:3455-3465.
99. Meran S, et al. Involvement of hyaluronan in regulation of fibroblast phenotype. J Biol Chem 2007;282:25687-25697.
100. DePalma RL, et al. Characterization and quantitation of wound matrix in the fetal rabbit. Matrix 1989;9:224-231.
101. Nyman E, Huss F, Nyman T, Junker J, Kratz G. Hyaluronic acid, an important factor in the wound healing properties of amniotic fluid: in vitro studies of re-epithelialisation in human skin wounds. J Plast Surg Hand Surg 2013;47:89-92.
102. Sidgwick GP, Iqbal SA, Bayat A. Altered expression of hyaluronan synthase and hyaluronidase mRNA may affect hyaluronic acid distribution in keloid disease compared with normal skin. Exp Dermatol 2013;22:377-379.
103. Tolg C, et al. A RHAMM mimetic peptide blocks hyaluronan signaling and reduces inflammation and fibrogenesis in excisional skin wounds. Am J Pathol 2012;181:1250-1270.
104. David-Raoudi M, et al. Differential effects of hyaluronan and its fragments on fibroblasts: relation to wound healing. Wound Repair Regen 2008;16:274-287.
105. Tolg C, Telmer P, Turley E. Specific sizes of hyaluronan oligosaccharides stimulate fibroblast migration and excisional wound repair. PLoS One 2014;9:e88479.
106. Webber J, Jenkins RH, Meran S, Phillips A, Steadman R. Modulation of TGFbeta1-dependent myofibroblast differentiation by hyaluronan. Am J Pathol 2009;175:148-160.
107. Webber J, Meran S, Steadman R, Phillips A. Hyaluronan orchestrates transforming growth factor-beta1-dependent maintenance of myofibroblast phenotype. J Biol Chem 2009;284:9083-9092.
108. Simpson RML, et al. Aging fibroblasts resist phenotypic maturation because of impaired hyaluronan-dependent CD44/epidermal growth factor receptor signaling. Am J Pathol 2010;176:1215-1228.
109. Müller SA, et al. Quantitative proteomics reveals altered expression of extracellular matrix related proteins of human primary dermal fibroblasts in response to sulfated hyaluronan and collagen applied as artificial extracellular matrix. J Mater Sci Mater Med 2012;23:3053-3065.
110. Hintze V, et al. Sulfated hyaluronan and chondroitin sulfate derivatives interact differently with human transforming growth factor-b1 (TGFb1). Acta Biomater 2012;8:2144-2152.
111. Kosir MA, Quinn CC, Wang W, Tromp G. Matrix glycosaminoglycans in the growth phase of fibroblasts: more of the story in wound healing. J Surg Res 2000;92:45-52.
112. Penc SF, et al. Dermatan sulfate released after injury is a potent promoter of fibroblast growth factor-2 function. J Biol Chem 1998;273:28116-28121.
113. Radek KA, Taylor KR, Gallo RL. FGF-10 and specific structural elements of dermatan sulfate size and sulfation promote maximal keratinocyte migration and cellular proliferation. Wound Repair Regen 2009;17:118-126.
114. Hildebrand A, et al. Interaction of the small interstitial proteoglycans biglycan, decorin and fibromodulin with transforming growth factor beta. Biochem J 1994;302:527-534.
115. Mohan RR, Gupta R, Mehan MK, Cowden JW, Sinha S. Decorin transfection suppresses profibrogenic genes and myofibroblast formation in human corneal fibroblasts. Exp Eye Res 2010;91: 238-245.
116. Meenakshi J, et al. Low decorin expression along with inherent activation of ERK1,2 in ear lobe keloids. Burns 2009;35:519-526.
117. Scott PG, Dodd CM, Tredget EE, Ghahary A, Rahemtulla F. Immunohistochemical localization of the proteoglycans decorin, biglycan and versican and transforming growth factor-beta in human post-burn hypertrophic and mature scars. Histopathology 1995;26:423-431.
118. Sayani K, et al. Delayed appearance of decorin in healing burn scars. Histopathology 2000;36:262-272.
119. Järveläinen H, et al. A role for decorin in cutaneous wound healing and angiogenesis. Wound Repair Regen 2006;14:443-452.
120. Ferdous Z, et al. A role for decorin in controlling proliferation, adhesion, and migration of murine embryonic fibroblasts. J Biomed Mater Res A 2010;93:419-428.
121. Li H, Nahas Z, Feng F, Elisseeff JH, Boahene K. Tissue engineering for in vitro analysis of matrix metalloproteinases in the pathogenesis of keloid lesions. JAMA Facial Plast Surg 15:448-456
122. Wang J, Dodd C, Shankowsky HA, Scott PG, Tredget EE. Deep dermal fibroblasts contribute to hypertrophic scarring. Lab Invest 2008;88: 1278-1290.
123. Varkey M, Ding J, Tredget EE. Fibrotic remodeling of tissue-engineered skin with deep dermal fibroblasts is reduced by keratinocytes. Tissue Eng Part A 2014;20:716-727.
124. Feng M, Yang G, Wu J. Versican targeting by RNA interference suppresses aggregative growth of dermal papilla cells. Clin Exp Dermatol 2011;36:77-84.
125. Liu X-J, et al. Lumican accelerates wound healing by enhancing a2b1 integrin-mediated fibroblast contractility. PLoS One 2013;8:e67124.
126. Vij N, Roberts L, Joyce S, Chakravarti S. Lumican suppresses cell proliferation and aids Fas-Fas ligand mediated apoptosis: implications in the cornea. Exp Eye Res 2004;78:957-971.
127. Takeda U, et al. Targeted disruption of dermatopontin causes abnormal collagen fibrillogenesis. J Invest Dermatol 2002;119:678-683.
128. Kuroda K, Okamoto O, Shinkai H. Dermatopontin expression is decreased in hypertrophic scar and systemic sclerosis skin fibroblasts and is regulated by transforming growth factor-beta1, interleukin-4, and matrix collagen. J Invest Dermatol 1999;112: 706-710.
129. Kato A, et al. Dermatopontin interacts with fibronectin, promotes fibronectin fibril formation, and enhances cell adhesion. J Biol Chem 2011; 286:14861-14869.
130. Hunzelmann N, Anders S, Sollberg S, Schönherr E, Krieg T. Co-ordinate induction of collagen type I and biglycan expression in keloids. Br J Dermatol 1996;135:394-399.
131. Wu M, et al. Osteopontin in systemic sclerosis and its role in dermal fibrosis. J Invest Dermatol 2012;132:1605-1614.
132. Hunter C, Bond J, Kuo PC, Selim MA, Levinson H. The role of osteopontin and osteopontin aptamer (OPN-R3) in fibroblast activity. J Surg Res 2012; 176:348-358.
133. Lenga Y, et al. Osteopontin expression is required for myofibroblast differentiation. Circ Res 2008;102:319-327.
134. Mori R, Shaw TJ, Martin P. Molecular mechanisms linking wound inflammation and fibrosis: knockdown of osteopontin leads to rapid repair and reduced scarring. J Exp Med 2008;205:43-51.
135. Wang J-C, et al. Attenuation of fibrosis in vitro and in vivo with SPARC siRNA. Arthritis Res Ther 2010;12:R60.
136. Rentz TJ, Poobalarahi F, Bornstein P, Sage EH, Bradshaw AD. SPARC regulates processing of procollagen I and collagen fibrillogenesis in dermal fibroblasts. J Biol Chem 2007;282:22062-22071.
137. Zhou X, Tan FK, Guo X, Arnett FC. Attenuation of collagen production with small interfering RNA of SPARC in cultured fibroblasts from the skin of patients with scleroderma. Arthritis Rheum 2006; 54:2626-2631.
138. Bradshaw AD, Reed MJ, Sage EH. SPARC-null mice exhibit accelerated cutaneous wound closure. J Histochem Cytochem 2002;50:1-10.
139. Wang JF, Olson ME, Ball DK, Brigstock DR, Hart DA. Recombinant connective tissue growth factor modulates porcine skin fibroblast gene expression. Wound Repair Regen 2003;11: 220-229.
140. Lee CH, Shah B, Moioli EK, Mao JJ. CTGF directs fibroblast differentiation from human mesenchymal stem/stromal cells and defines connective tissue healing in a rodent injury model. J Clin Invest 2010;120:3340-3349.
141. Liu S, Thompson K, Leask A. CCN2 expression by fibroblasts is not required for cutaneous tissue repair. Wound Repair Regen 2014;22:119-124.
142. Leask A. Transcriptional profiling of the scleroderma fibroblast reveals a potential role for connective tissue growth factor (CTGF) in pathological fibrosis. Keio J Med 2004;53:74-77.
143. Xia W, et al. Increased CCN2 transcription in keloid fibroblasts requires cooperativity between AP-1 and SMAD binding sites. Ann Surg 2007; 246:886-895.
144. Kiwanuka E, et al. CCN2 promotes keratinocyte adhesion and migration via integrin a5b1. Exp Cell Res 2013;319:2938-2946.
145. Hu X, et al. The role of ERK and JNK signaling in connective tissue growth factor induced extracellular matrix protein production and scar formation. Arch Dermatol Res 2013;305:433-445.
146. Dalkowski A, Schuppan D, Orfanos CE, Zouboulis CC. Increased expression of tenascin C by keloids in vivo and in vitro. Br J Dermatol 1999; 141:50-56.
147. Filsell W, Rudman S, Jenkins G, Green MR. Coordinate upregulation of tenascin C expression with degree of photodamage in human skin. Br J Dermatol 1999;140:592-599.
148. Orend G, Huang W, Olayioye MA, Hynes NE, Chiquet-Ehrismann R. Tenascin-C blocks cell-cycle progression of anchorage-dependent fibroblasts on fibronectin through inhibition of syndecan-4. Oncogene 2003;22:3917-3926.
149. Trebaul A, Chan EK, Midwood KS. Regulation of fibroblast migration by tenascin-C. Biochem Soc Trans 2007;35:695-697.
150. Lee MJ, Roy NK, Mogford JE, Schiemann WP, Mustoe TA. Fibulin-5 promotes wound healing in vivo. J Am Coll Surg 2004;199:403-410.
151. Zheng Q, et al. Normal wound healing in mice deficient for fibulin-5, an elastin binding protein essential for dermal elastic fiber assembly. J Invest Dermatol 2006;126:2707-2714.
152. Rittié L, Berton A, Monboisse JC, Hornebeck W, Gillery P. Decreased contraction of glycated collagen lattices coincides with impaired matrix metalloproteinase production. Biochem Biophys Res Commun 1999;264:488-492.
153. Niu Y, Xie T, Ge K, Lin Y, Lu S. Effects of extracellular matrix glycosylation on proliferation and apoptosis of human dermal fibroblasts via the receptor for advanced glycosylated end products. Am J Dermatopathol 2008;30:344-351.
154. Okano Y, Masaki H, Sakurai H. Dysfunction of dermal fibroblasts induced by advanced glycation end-products (AGEs) and the contribution of a nonspecific interaction with cell membrane and AGEs. J Dermatol Sci 2002;29:171-180.
155. Reihsner R, Melling M, Pfeiler W, Menzel EJ. Alterations of biochemical and two-dimensional biomechanical properties of human skin in diabetes mellitus as compared to effects of in vitro non-enzymatic glycation. Clin Biomech (Bristol, Avon) 2000;15:379-386.
156. Kuzuya M, et al. Inhibition of angiogenesis on glycated collagen lattices. Diabetologia 1998;41: 491-499.
157. Goova MT, et al. Blockade of receptor for advanced glycation end-products restores effective wound healing in diabetic mice. Am J Pathol 2001; 159:513-525.
158. Sidgwick GP, Bayat A. Extracellular matrix molecules implicated in hypertrophic and keloid scarring. J Eur Acad Dermatol Venereol 2012; 26:141-152.
159. End P, Panayotou G, Entwistle A, Waterfield MD, Chiquet M. Tenascin: a modulator of cell growth. Eur J Biochem 1992;209:1041-1051.
160. Kubo H, et al. Temporal expression of wound healing-related genes in skin burn injury. Leg Med (Tokyo) 2014;16:8-13.
161. Betz P. Immunohistochemical parameters for the age estimation of human skin wounds. A review. Am J Forensic Med Pathol 1995;16:203-209.
162. Betz P, et al. Time-dependent appearance of myofibroblasts in granulation tissue of human skin wounds. Int J Legal Med 1992;105:99-103.
163. Betz P, et al. Comparison of the solophenyl-red polarization method and the immunohistochemical analysis for collagen type III. Int J Legal Med 1992;105:27-29.
164. Betz P, et al. Immunohistochemical localization of fibronectin as a tool for the age determination of human skin wounds. Int J Legal Med 1992; 105:21-26.
165. Oono T, et al. Expression of type VI collagen mRNA during wound healing. J Invest Dermatol 1993;100:329-334.
166. McGrath JA, Leigh IM, Eady RA. Intracellular expression of type VII collagen during wound healing in severe recessive dystrophic epidermolysis bullosa and normal human skin. Br J Dermatol 1992;127:312-317.
167. Wester J, Sixma JJ, Geuze JJ, van der Veen J. Morphology of the early hemostasis in human skin wounds: influence of acetylsalicylic acid. Lab Invest 1978;39:298-311.
168. Olczyk P, et al. Propolis modulates vitronectin, laminin, and heparan sulfate/heparin expression during experimental burn healing. J Zhejiang Univ Sci B 2012;13:932-941.
169. Olczyk P, et al. Propolis induces chondroitin/dermatan sulphate and hyaluronic Acid accumulation in the skin of burned wound. Evid Based Complement Alternat Med 2013;2013: 290675.
170. Ashcroft GS, Kielty CM, Horan MA, Ferguson MW. Age-related changes in the temporal and spatial distributions of fibrillin and elastin mRNAs and proteins in acute cutaneous wounds of healthy humans. J Pathol 1997;183:80-89.
171. Oksala O, et al. Expression of proteoglycans and hyaluronan during wound healing. J Histochem Cytochem 1995;43:125-135.
172. Tammi R, Pasonen-Seppänen S, Kolehmainen E, Tammi M. Hyaluronan synthase induction and hyaluronan accumulation in mouse epidermis following skin injury. J Invest Dermatol 2005; 124:898-905.
173. Siméon A, Wegrowski Y, Bontemps Y, Maquart FX. Expression of glycosaminoglycans and small proteoglycans in wounds: modulation by the tripeptide-copper complex glycyl-L-histidyl-L-lysine-Cu(2 + ). J Invest Dermatol 2000;115:962-968.
174. Yeo TK, Brown L, Dvorak HF. Alterations in proteoglycan synthesis common to healing wounds and tumors. Am J Pathol 1991;138:1437-1450.
175. Honardoust D, Eslami A, Larjava H, Häkkinen L. Localization of small leucine-rich proteoglycans and transforming growth factor-beta in human oral mucosal wound healing. Wound Repair Regen 2008;16:814-823.
176. Geary RL, et al. Wound healing: a paradigm for lumen narrowing after arterial reconstruction. J Vasc Surg 1998;27:96-106; discussion 106-108.
177. Zimmermann DR, Dours-Zimmermann MT, Schubert M, Bruckner-Tuderman L. Versican is expressed in the proliferating zone in the epidermis and in association with the elastic network of the dermis. J Cell Biol 1994;124:817-825.
178. Wick G, Glanville RW, Timpl R. Characterization of antibodies to basement membrane (type IV) collagen in immunohistological studies. Immunobiology 1980;156:372-381.
179. Sharma A, Singh AK, Warren J, Thangapazham RL, Maheshwari RK. Differential regulation of angiogenic genes in diabetic wound healing. J Invest Dermatol 2006;126:2323-2331.
180. Reed MJ, et al. Differential expression of SPARC and thrombospondin 1 in wound repair: immunolocalization and in situ hybridization. J Histochem Cytochem 1993;41:1467-1477.
181. Wu RX, et al. Fibroblast migration after myocardial infarction is regulated by transient SPARC expression. J Mol Med (Berl) 2006;84:241-252.
182. Mackie EJ, Halfter W, Liverani D. Induction of tenascin in healing wounds. J Cell Biol 1988; 107:2757-2767.
183. Ishida Y, Kimura A, Takayasu T, Eisenmenger W, Kondo T. Detection of fibrocytes in human skin wounds and its application for wound age determination. Int J Legal Med 2009;123:299-304.
184. Wu YJ, La Pierre DP, Wu J, Yee AJ, Yang BB. The interaction of versican with its binding partners. Cell Res 2005;15:483-494.
185. Betz P, et al. The time-dependent rearrangement of the epithelial basement membrane in human skin wounds - immunohistochemical localization of collagen IV and VII. Int J Legal Med 1992;105:93-97.
186. Huang-Lee LL, Wu JH, Nimni ME. Effects of hyaluronan on collagen fibrillar matrix contraction by fibroblasts. J Biomed Mater Res 1994; 28:123-132.
187. Clark RAF, Lin F, Greiling D, An J, Couchman JR. Fibroblast invasive migration into fibronectin/fibrin gels requires a previously uncharacterized dermatan sulfate-CD44 proteoglycan. J Invest Dermatol 2004;122:266-277.
188. Zou XH, et al. Chondroitin sulfate in palatal wound healing. J Dent Res 2004;83:880-885.