Deconstructing fibrosis research: Do pro-fibrotic signals point the way for chronic dermal wound regeneration?

Journal of Cell Communication and Signaling

Volumn 5, Issue 4, 2011, Pages 301-315

  Elliott, Christopher G ^a   Hamilton, Douglas W ^a,b  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

^b WESTERN UNIVERSITY   (Canada)

Author keywords

Chronic dermal wounds; Dermal fibroblast; Fibrosis; Matricellular proteins; Periostin; Transforming growth factor beta

Indexed keywords

BECAPLERMIN; CELL PROTEIN; DASATINIB; IMATINIB; NILOTINIB; PLACEBO; PLATELET DERIVED GROWTH FACTOR BB; RECOMBINANT PLATELET DERIVED GROWTH FACTOR BB; RECOMBINANT TRANSFORMING GROWTH FACTOR BETA; TRANSCRIPTION FACTOR RUNX2; TRANSFORMING GROWTH FACTOR BETA;

CHRONIC WOUND; DEBRIDEMENT; DECUBITUS; DIABETIC FOOT; EXTRACELLULAR MATRIX; HUMAN; NONHUMAN; PRIORITY JOURNAL; REVIEW; SKIN DISEASE; SKIN FIBROSIS; THROMBOCYTE RELEASE REACTION; THROMBOCYTE RICH PLASMA; ULCER; WOUND CLOSURE; WOUND HEALING;

EID: 85027919851     PISSN: 18739601     EISSN: 1873961X     Source Type: Journal    
DOI: 10.1007/s12079-011-0131-5     Document Type: Review

References (171)

1. Abergel RP, Pizzurro D, Meeker CA et al (1985) Biochemical composition of the connective tissue in keloids and analysis of collagen metabolism in keloid fibroblast cultures. J Invest Dermatol 84:384-390 (Pubitemid 15056660)
2. Abraham DJ, Varga J (2005) Scleroderma: from cell and molecular mechanisms to disease models. Trends Immunol 26:587-595 (Pubitemid 41726446)
3. Akhmetshina A, Dees C, Pileckyte M et al (2008) Dual inhibition of c-abl and PDGF receptor signaling by dasatinib and nilotinib for the treatment of dermal fibrosis. FASEB J 22:2214-2222 (Pubitemid 351948641)
4. Aragon-Sanchez J, Hernandez-Herrero MJ, Lazaro-Martinez JL et al (2010) In-hospital complications and mortality following major lower extremity amputations in a series of predominantly diabetic patients. Int J Low Extrem Wounds 9:16-23
5. Armstrong DG, Wrobel J, Robbins JM (2007) Guest Editorial: are diabetes-related wounds and amputations worse than cancer? Int Wound J 4:286-287 (Pubitemid 350264806)
6. Bao S, Ouyang G, Bai X et al (2004) Periostin potently promotes metastatic growth of colon cancer by augmenting cell survival via the Akt/PKB pathway. Cancer Cell 5:329-339 (Pubitemid 38482069)
7. Baril P, Gangeswaran R, Mahon PC et al (2007) Periostin promotes invasiveness and resistance of pancreatic cancer cells to hypoxiainduced cell death: role of the beta4 integrin and the PI3k pathway. Oncogene 26:2082-2094 (Pubitemid 46514745)
8. Barrientos S, Stojadinovic O, Golinko MS et al (2008) Growth factors and cytokines in wound healing. Wound Repair Regen 16:585-601
9. Beck LS, Chen TL, Hirabayashi SE et al (1990) Accelerated healing of ulcer wounds in the rabbit ear by recombinant human transforming growth factor-beta 1. Growth Factors 2:273-282 (Pubitemid 20105851)
10. Bennett SP, Griffiths GD, Schor AM et al (2003) Growth factors in the treatment of diabetic foot ulcers. Br J Surg 90:133-146 (Pubitemid 36237887)
11. Beyer C, Distler JH, Distler O (2010) Are tyrosine kinase inhibitors promising for the treatment of systemic sclerosis and other fibrotic diseases? Swiss Med Wkly 140:w13050
12. Bornstein P (1995) Diversity of function is inherent in matricellular proteins: an appraisal of thrombospondin 1. J Cell Biol 130:503-506
13. Bostrom H, Willetts K, Pekny M et al (1996) PDGF-A signaling is a critical event in lung alveolar myofibroblast development and alveogenesis. Cell 85:863-873 (Pubitemid 26192137)
14. Butcher JT, Norris RA, Hoffman S et al (2007) Periostin promotes atrioventricular mesenchyme matrix invasion and remodeling mediated by integrin signaling through Rho/PI 3-kinase. Dev Biol 302:256-266 (Pubitemid 46099041)
15. Cavanagh PR, Lipsky BA, Bradbury AW et al (2005) Treatment for diabetic foot ulcers. Lancet 366:1725-1735 (Pubitemid 41587453)
16. Chaby G, Senet P, Vaneau M et al (2007) Dressings for acute and chronic wounds: a systematic review. Arch Dermatol 143:1297-1304 (Pubitemid 47607683)
17. Chen SM, Ward SI, Olutoye OO et al (1997) Ability of chronic wound fluids to degrade peptide growth factors is associated with increased levels of elastase activity and diminished levels of proteinase inhibitors. Wound Repair Regen 5:23-32 (Pubitemid 127686717)
18. Chen Y, Shi-Wen X, van Beek J et al (2005) Matrix contraction by dermal fibroblasts requires transforming growth factor-beta/activin-linked kinase 5, heparan sulfate-containing proteoglycans, and MEK/ERK: insights into pathological scarring in chronic fibrotic disease. Am J Pathol 167:1699-1711 (Pubitemid 41713321)
19. Clark R (1996) The molecular and cellular biology of wound repair, 2nd edn. Plenum Publishing Corporation, New York
20. Cochrane CG (1977) Role of granulocytes in immune complexinduced tissue injuries. Inflammation 2:319-333
21. Cowin AJ, Hatzirodos N, Holding CA et al (2001) Effect of healing on the expression of transforming growth factor beta (s) and their receptors in chronic venous leg ulcers. J Invest Dermatol 117:1282-1289 (Pubitemid 34205930)
22. Daniels CE, Wilkes MC, Edens M et al (2004) Imatinib mesylate inhibits the profibrogenic activity of TGF-beta and prevents bleomycin-mediated lung fibrosis. J Clin Invest 114:1308-1316 (Pubitemid 40385302)
23. Denhardt DT, Giachelli CM, Rittling SR (2001) Role of osteopontin in cellular signaling and toxicant injury. Annu Rev Pharmacol Toxicol 41:723-749 (Pubitemid 32385904)
24. Denton CP, Merkel PA, Furst de et al (2007) Recombinant human anti-transforming growth factor beta1 antibody therapy in systemic sclerosis: a multicenter, randomized, placebocontrolled phase I/II trial of CAT-192. Arthritis Rheum 56:323-333 (Pubitemid 46106206)
25. Desmouliere A, Geinoz A, Gabbiani F et al (1993) Transforming growth factor-beta 1 induces alpha-smooth muscle actin expression in granulation tissue myofibroblasts and in quiescent and growing cultured fibroblasts. J Cell Biol 122:103-111 (Pubitemid 23188802)
26. Desmouliere A, Chaponnier C, Gabbiani G (2005) Tissue repair, contraction, and the myofibroblast. Wound Repair Regen 13:7-12 (Pubitemid 40250424)
27. Deuel TF, Senior RM, Huang JS et al (1982) Chemotaxis of monocytes and neutrophils to platelet-derived growth factor. J Clin Invest 69:1046-1049 (Pubitemid 12149184)
28. Diegelmann RF, Evans MC (2004) Wound healing: an overview of acute, fibrotic and delayed healing. Front Biosci 9:283-289 (Pubitemid 38925460)
29. Distler JH, Jungel A, Huber LC et al (2007) Imatinib mesylate reduces production of extracellular matrix and prevents development of experimental dermal fibrosis. Arthritis Rheum 56:311-322 (Pubitemid 46106205)
30. Donaghue VM, Chrzan JS, Rosenblum BI et al (1998) Evaluation of a collagen-alginate wound dressing in the management of diabetic foot ulcers. Adv Wound Care 11:114-119
31. Driver VR, Hanft J, Fylling CP et al (2006) A prospective, randomized, controlled trial of autologous platelet-rich plasma gel for the treatment of diabetic foot ulcers. Ostomy/Wound Management 52:68-70, 2, 4 passim
32. Driver VR, Fabbi M, Lavery la et al (2010) The costs of diabetic foot: the economic case for the limb salvage team. J Vasc Surg 52:17S-22S
33. Edwards DR, Murphy G, Reynolds JJ et al (1987) Transforming growth factor beta modulates the expression of collagenase and metalloproteinase inhibitor. EMBO J 6:1899-1904
34. Erkan M, Kleeff J, Gorbachevski A et al (2007) Periostin creates a tumorsupportive microenvironment in the pancreas by sustaining fibrogenic stellate cell activity. Gastroenterology 132:1447-1464 (Pubitemid 46627568)
35. Galkowska H, Wojewodzka U, Olszewski WL (2006) Chemokines, cytokines, and growth factors in keratinocytes and dermal endothelial cells in the margin of chronic diabetic foot ulcers. Wound Repair Regen 14:558-565 (Pubitemid 44470072)
36. Gao Z, Sasaoka T, Fujimori T et al (2005) Deletion of the PDGFR-beta gene affects key fibroblast functions important for wound healing. J Biol Chem 280:9375-9389 (Pubitemid 40409631)
37. Gillan L, Matei D, Fishman DA et al (2002) Periostin secreted by epithelial ovarian carcinoma is a ligand for alpha (V) beta (3) and alpha (V) beta (5) integrins and promotes cell motility. Cancer Res 62:5358-5364 (Pubitemid 35024613)
38. Greiling D, Clark RA (1997) Fibronectin provides a conduit for fibroblast transmigration from collagenous stroma into fibrin clot provisional matrix. J Cell Sci 110 (Pt 7):861-870 (Pubitemid 27196785)
39. Hambleton IR, Jonnalagadda R, Davis CR et al (2009) All-cause mortality after diabetes-related amputation in Barbados: a prospective case-control study. Diabetes Care 32:306-307
40. Hamilton DW (2008) Functional role of periostin in development and wound repair: implications for connective tissue disease. J Cell Commun Signal 2:9-17
41. Harding K, Queen D (2010) Chronic wounds and their management and prevention is a significiant public health issue. Int Wound J 7:125-126
42. Harding KG, Morris HL, Patel GK (2002) Science, medicine and the future: healing chronic wounds. BMJ 324:160-163 (Pubitemid 34084511)
43. Hasan A, Murata H, Falabella A et al (1997) Dermal fibroblasts from venous ulcers are unresponsive to the action of transforming growth factor-beta 1. J Dermatol Sci 16:59-66 (Pubitemid 28004775)
44. Hehenberger K, Heilborn JD, Brismar K et al (1998) Inhibited proliferation of fibroblasts derived from chronic diabetic wounds and normal dermal fibroblasts treated with high glucose is associated with increased formation of l-lactate. Wound Repair Regen 6:135-141 (Pubitemid 128659189)
45. Heldin CH, Westermark B (1999) Mechanism of action and in vivo role of platelet-derived growth factor. Physiol Rev 79:1283-1316 (Pubitemid 29473317)
46. Holmes A, Abraham DJ, Sa S et al (2001) CTGF and SMADs, maintenance of scleroderma phenotype is independent of SMAD signaling. J Biol Chem 276:10594-10601 (Pubitemid 38089227)
47. Horiuchi K, Amizuka N, Takeshita S et al (1999) Identification and characterization of a novel protein, periostin, with restricted expression to periosteum and periodontal ligament and increased expression by transforming growth factor beta. J Bone Miner Res 14:1239-1249 (Pubitemid 29314070)
48. Igarashi A, Okochi H, Bradham DM et al (1993) Regulation of connective tissue growth factor gene expression in human skin fibroblasts and during wound repair. Mol Biol Cell 4:637-645 (Pubitemid 23183611)
49. Ignotz RA, Massague J (1986) Transforming growth factor-beta stimulates the expression of fibronectin and collagen and their incorporation into the extracellular matrix. J Biol Chem 261:4337-4345 (Pubitemid 17198877)
50. Jackson-Boeters L, Wen W, Hamilton DW (2009) Periostin localizes to cells in normal skin, but is associated with the extracellular matrix during wound repair. J Cell Commun Signal 3:125-133
51. Jinnin M, Ihn H, Mimura y et al (2005) Regulation of fibrogenic/ fibrolytic genes by platelet-derived growth factor C, a novel growth factor, in human dermal fibroblasts. J Cell Physiol 202:510-517 (Pubitemid 40041322)
52. Jude EB, Blakytny R, Bulmer J et al (2002) Transforming growth factor-beta 1, 2, 3 and receptor type I and II in diabetic foot ulcers. Diabet Med 19:440-447 (Pubitemid 34639153)
53. Jun. JI, Lau LF (2010) Cellular senescence controls fibrosis in wound healing. Aging (Albany NY) 2:627-631
54. Katsuragi N, Morishita R, Nakamura N et al (2004) Periostin as a novel factor responsible for ventricular dilation. Circulation 110:1806-1813 (Pubitemid 39299222)
55. Kawakami T, Ihn H, Xu W et al (1998) Increased expression of TGF-beta receptors by scleroderma fibroblasts: evidence for contribution of autocrine TGF-beta signaling to scleroderma phenotype. J Invest Dermatol 110:47-51 (Pubitemid 28086062)
56. Kennedy L, Liu S, Shi-Wen X et al (2007) CCN2 is necessary for the function of mouse embryonic fibroblasts. Exp Cell Res 313:952-964
57. Kii I, Amizuka N, Minqi L et al (2006) Periostin is an extracellular matrix protein required for eruption of incisors in mice. Biochem Biophys Res Commun 342:766-772 (Pubitemid 43320464)
58. Kii I, Nishiyama T, Li M et al (2009) Incorporation of tenascin-C into the extracellular matrix by periostin underlies an extracellular meshwork architecture. J Biol Chem 285:2028-2039
59. Kim JE, Jeong HW, Nam JO et al (2002) Identification of motifs in the fasciclin domains of the transforming growth factor-betainduced matrix protein betaig-h3 that interact with the alphavbeta5 integrin. J Biol Chem 277:46159-46165
60. Kirshen C, Woo K, Ayello EA et al (2006) Debridement: a vital component of wound bed preparation. Adv Skin Wound Care 19:506-517, quiz 17-9
61. Klareskog L, Gustafsson R, Scheynius A et al (1990) Increased expression of platelet-derived growth factor type B receptors in the skin of patients with systemic sclerosis. Arthritis Rheum 33:1534-1541 (Pubitemid 20362097)
62. Kocher O, Madri JA (1989) Modulation of actin mRNAs in cultured vascular cells by matrix components and TGF-beta 1. In Vitro Cell Dev Biol 25:424-434 (Pubitemid 19158902)
63. Kraling BM, Maul GG, Jimenez sa (1995) Mononuclear cellular infiltrates in clinically involved skin from patients with systemic sclerosis of recent onset predominantly consist of monocytes/macrophages. Pathobiology 63:48-56
64. Kubo M, Ihn H, Yamane K et al (2002) Upregulated expression of transforming growth factor-beta receptors in dermal fibroblasts of skin sections from patients with systemic sclerosis. J Rheumatol 29:2558-2564 (Pubitemid 35416962)
65. Leask A (2008) Targeting the TGFbeta, endothelin-1 and CCN2 axis to combat fibrosis in scleroderma. Cell Signal 20:1409-1414
66. Leask A (2010) Potential therapeutic targets for cardiac fibrosis: TGFbeta, angiotensin, endothelin, CCN2, and PDGF, partners in fibroblast activation. Circ Res 106:1675-1680
67. Leask A, Abraham DJ (2004) TGF-beta signaling and the fibrotic response. FASEB J 18:816-827
68. Leibovich SJ, Ross R (1975) The role of the macrophage in wound repair. A study with hydrocortisone and antimacrophage serum. Am J Pathol 78:71-100
69. Lenga Y, Koh A, Perera as et al (2008) Osteopontin expression is required for myofibroblast differentiation. Circ Res 102:319-327 (Pubitemid 351271652)
70. Levenson SM, Geever EF, Crowley LV et al (1965) The healing of rat skin wounds. Ann Surg 161:293-308
71. Li G, Oparil S, Sanders JM et al (2006) Phosphatidylinositol-3-kinase signaling mediates vascular smooth muscle cell expression of periostin in vivo and in vitro. Atherosclerosis 188:292-300 (Pubitemid 44301134)
72. Li G, Jin R, Norris RA et al (2010) Periostin mediates vascular smooth muscle cell migration through the integrins alphavbeta3 and alphavbeta5 and focal adhesion kinase (FAK) pathway. Atherosclerosis 208:358-365
73. Lin H, Chen B, Sun W et al (2006) The effect of collagen-targeting platelet-derived growth factor on cellularization and vascularization of collagen scaffolds. Biomaterials 27:5708-5714 (Pubitemid 44294823)
74. Lindner V, Wang Q, Conley BA et al (2005) Vascular injury induces expression of periostin: implications for vascular cell differentiation and migration. Arterioscler Thromb Vasc Biol 25:77-83 (Pubitemid 40054257)
75. Litvin J, Selim AH, Montgomery MO et al (2004) Expression and function of periostin-isoforms in bone. J Cell Biochem 92:1044-1061 (Pubitemid 44264252)
76. Liu S, Xu SW, Kennedy L et al (2007) FAK is required for TGFbetainduced JNK phosphorylation in fibroblasts: implications for acquisition of a matrix-remodeling phenotype. Mol Biol Cell 18:2169-2178 (Pubitemid 46911368)
77. Liu Y, Min D, Bolton T et al (2009) Increased matrix metalloproteinase-9 predicts poor wound healing in diabetic foot ulcers. Diabetes Care 32:117-119
78. Loot MA, Kenter SB, Au FL et al (2002) Fibroblasts derived from chronic diabetic ulcers differ in their response to stimulation with EGF, IGF-I, bFGF and PDGF-AB compared to controls. Eur J Cell Biol 81:153-160 (Pubitemid 34308679)
79. Ludwicka A, Ohba T, Trojanowska M et al (1995) Elevated levels of platelet derived growth factor and transforming growth factorbeta 1 in bronchoalveolar lavage fluid from patients with scleroderma. J Rheumatol 22:1876-1883
80. Margolis DJ, Kantor J, Santanna J et al (2001) Effectiveness of platelet releasate for the treatment of diabetic neuropathic foot ulcers. Diabetes Care 24:483-488 (Pubitemid 32198417)
81. Maruhashi T, Kii I, Saito M et al (2010) Interaction between periostin and BMP-1 promotes proteolytic activation of lysyl oxidase. J Biol Chem 285:13294-13303
82. Massague J, Wotton D (2000) Transcriptional control by the TGF-beta/Smad signaling system. EMBO J 19:1745-1754 (Pubitemid 30204386)
83. Matsuda A, Yoshiki A, Tagawa y et al (1999) Corneal wound healing in tenascin knockout mouse. Invest Ophthalmol Vis Sci 40:1071-1080 (Pubitemid 29211444)
84. Mendez MV, Stanley A, Phillips T et al (1998) Fibroblasts cultured from distal lower extremities in patients with venous reflux display cellular characteristics of senescence. J Vasc Surg 28:1040-1050 (Pubitemid 28562708)
85. Midwood KS, Williams LV, Schwarzbauer JE (2004) Tissue repair and the dynamics of the extracellular matrix. Int J Biochem Cell Biol 36:1031-1037 (Pubitemid 38501555)
86. Moiseeva EP, Williams B, Samani NJ (2003) Galectin 1 inhibits incorporation of vitronectin and chondroitin sulfate B into the extracellular matrix of human vascular smooth muscle cells. Biochim Biophys Acta 1619:125-132 (Pubitemid 36078348)
87. Morbach S, Groblinghoff U, Schulze H et al (2009) All-cause mortality after diabetes-related amputation in Barbados: a prospective case-control study: response to Hambleton et al. Diabetes Care 32:e100, author reply e1
88. Mori Y, Chen SJ, Varga J (2003) Expression and regulation of intracellular SMAD signaling in scleroderma skin fibroblasts. Arthritis Rheum 48:1964-1978 (Pubitemid 36828692)
89. Mosesson MW (2005) Fibrinogen and fibrin structure and functions. J Thromb Haemost 3:1894-1904 (Pubitemid 41716577)
90. Mostow EN, Haraway GD, Dalsing M et al (2005) Effectiveness of an extracellular matrix graft (OASIS Wound Matrix) in the treatment of chronic leg ulcers: a randomized clinical trial. J Vasc Surg 41:837-843 (Pubitemid 40693807)
91. Moxey PW, Hofman D, Hinchliffe RJ et al (2010) Epidemiological study of lower limb amputation in England between 2003 and 2008. Br J Surg 97:1348-1353
92. Murakami K, Aoki H, Nakamura S et al (2010) Hydrogel blends of chitin/chitosan, fucoidan and alginate as healing-impaired wound dressings. Biomaterials 31:83-90
93. Mustoe TA, Purdy J, Gramates P et al (1989) Reversal of impaired wound healing in irradiated rats by platelet-derived growth factor-BB. Am J Surg 158:345-350 (Pubitemid 19246238)
94. Mustoe TA, Landes A, Cromack DT et al (1990) Differential acceleration of healing of surgical incisions in the rabbit gastrointestinal tract by platelet-derived growth factor and transforming growth factor, type beta. Surgery 108:324-329, discussion 9-30
95. Mustoe TA, Pierce GF, Morishima C et al (1991) Growth factorinduced acceleration of tissue repair through direct and inductive activities in a rabbit dermal ulcer model. J Clin Invest 87:694-703
96. 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 (Pubitemid 24056078)
97. Naitoh M, Kubota H, Ikeda M et al (2005) Gene expression in human keloids is altered from dermal to chondrocytic and osteogenic lineage. Genes Cells 10:1081-1091 (Pubitemid 41556076)
98. Nakazawa T, Nakajima A, Seki N et al (2004) Gene expression of periostin in the early stage of fracture healing detected by cDNA microarray analysis. J Orthop Res 22:520-525 (Pubitemid 38489728)
99. Niezgoda JA, Van Gils CC, Frykberg RG et al (2005) Randomized clinical trial comparing OASIS Wound Matrix to Regranex Gel for diabetic ulcers. Adv Skin Wound Care 18:258-266
100. Norris RA, Damon B, Mironov V et al (2007) Periostin regulates collagen fibrillogenesis and the biomechanical properties of connective tissues. J Cell Biochem 101:695-711 (Pubitemid 46698854)
101. Oka T, Xu J, Kaiser RA et al (2007) Genetic manipulation of periostin expression reveals a role in cardiac hypertrophy and ventricular remodeling. Circ Res 101:313-321 (Pubitemid 47351119)
102. Oku E, Kanaji T, Takata y et al (2008) Periostin and bone marrow fibrosis. Int J Hematol 88:57-63
103. Pannu J, Trojanowska M (2004) Recent advances in fibroblast signaling and biology in scleroderma. Curr Opin Rheumatol 16:739-745 (Pubitemid 39425548)
104. Pannu J, Gore-Hyer E, Yamanaka M et al (2004) An increased transforming growth factor beta receptor type I:type II ratio contributes to elevated collagen protein synthesis that is resistant to inhibition via a kinase-deficient transforming growth factor beta receptor type II in scleroderma. Arthritis Rheum 50:1566-1577 (Pubitemid 38608079)
105. Papazafiropoulou A, Tentolouris N, Soldatos RP et al (2009) Mortality in diabetic and nondiabetic patients after amputations performed from 1996 to 2005 in a tertiary hospital population: a 3-year follow-up study. J Diab Complications 23:7-11
106. Pastar I, Stojadinovic O, Krzyzanowska A et al (2010) Attenuation of the transforming growth factor beta-signaling pathway in chronic venous ulcers. Mol Med 16:92-101
107. Pierce GF, Mustoe TA, Senior RM et al (1988) In vivo incisional wound healing augmented by platelet-derived growth factor and recombinant c-sis gene homodimeric proteins. J Exp Med 167:974-987
108. Pierce GF, Mustoe TA, Lingelbach J et al (1989) Platelet-derived growth factor and transforming growth factor-beta enhance tissue repair activities by unique mechanisms. J Cell Biol 109:429-440 (Pubitemid 19180149)
109. Pierce GF, Tarpley JE, Tseng J et al (1995) Detection of plateletderived 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
110. Ploeg AJ, Lardenoye J-W, Vrancken Peeters M-P F M et al (2005) Contemporary series of morbidity and mortality after lower limb amputation. In: Eur J Vasc Endovasc Surg 633-637 (Pubitemid 40614349)
111. Qin Y, Gilding DK (1996) Alginate fibres and wound dressings. Med Device Technol 7:32-41
112. Queen D, Orsted H, Sanada H et al (2004) A dressing history. Int Wound J 1:59-77
113. Reiber GE (1996) The epidemiology of diabetic foot problems. Diabet Med 13(Suppl 1):S6-S11
114. Roberts AB, Sporn MB (1993) Physiological actions and clinical applications of transforming growth factor-beta (TGF-beta). Growth Factors 8:1-9 (Pubitemid 23093206)
115. Robson MC (1997) The role of growth factors in the healing of chronic wounds. Wound Repair Regen 5:12-17 (Pubitemid 127686715)
116. Robson MC, Phillips LG, Thomason A et al (1992) Platelet-derived growth factor BB for the treatment of chronic pressure ulcers. Lancet 339:23-25
117. Robson MC, Phillip LG, Cooper DM et al (1995) Safety and effect of transforming growth factor-beta (2) for treatment of venous stasis ulcers. Wound Repair Regen 3:157-167
118. Santiago B, Gutierrez-Canas I, Dotor J et al (2005) Topical application of a peptide inhibitor of transforming growth factor-beta1 ameliorates bleomycin-induced skin fibrosis. J Invest Dermatol 125:450-455
119. Schultz GS, Grant MB (1991) Neovascular growth factors. Eye (Lond) 5 (Pt 2):170-180
120. Schultz GS, Mast BA (1998) Molecular analysis of the environments of healing and chronic wounds: cytokines, proteases and growth factors. Wounds 10(suppl F):F1-F9
121. Schultz GS, Wysocki A (2009) Interactions between extracellular matrix and growth factors in wound healing. Wound Repair Regen 17:153-162
122. Schultz-Cherry S, Murphy-Ullrich JE (1993) Thrombospondin causes activation of latent transforming growth factor-beta secreted by endothelial cells by a novel mechanism. J Cell Biol 122:923-932 (Pubitemid 23241101)
123. Sen CK, Gordillo GM, Roy S et al (2009) Human skin wounds: a major and snowballing threat to public health and the economy. Wound Repair Regen 17:763-771
124. Seppa H, Grotendorst G, Seppa S et al (1982) Platelet-derived growth factor in chemotactic for fibroblasts. J Cell Biol 92:584-588 (Pubitemid 12157432)
125. Serini G, Bochaton-Piallat ML, Ropraz P et al (1998) The fibronectin domain ED-A is crucial for myofibroblastic phenotype induction by transforming growth factor-beta1. J Cell Biol 142:873-881 (Pubitemid 28381502)
126. Sethi KK, Yannas IV, Mudera V et al (2002) Evidence for sequential utilization of fibronectin, vitronectin, and collagen during fibroblast-mediated collagen contraction. Wound Repair Regen 10:397-408 (Pubitemid 36025339)
127. Shah M, Foreman DM, Ferguson MW (1992) Control of scarring in adult wounds by neutralising antibody to transforming growth factor beta. Lancet 339:213-214
128. 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 (Pt 3):985-1002
129. Shao R, Bao S, Bai X et al (2004) Acquired expression of periostin by human breast cancers promotes tumor angiogenesis through upregulation of vascular endothelial growth factor receptor 2 expression. Mol Cell Biol 24:3992-4003 (Pubitemid 38496176)
130. Shimazaki M, Nakamura K, Kii I et al (2008) Periostin is essential for cardiac healing after acute myocardial infarction. J Exp Med 205:295-303 (Pubitemid 351281595)
131. Shi-wen X, Stanton LA, Kennedy L et al (2006) CCN2 is necessary for adhesive responses to transforming growth factor-beta1 in embryonic fibroblasts. J Biol Chem 281:10715-10726 (Pubitemid 43855493)
132. Sidhu SS, Yuan S, Innes AL et al (2010) Roles of epithelial cellderived periostin in TGF-beta activation, collagen production, and collagen gel elasticity in asthma. Proc Natl Acad Sci USA 107:14170-14175
133. Siitonen OI, Niskanen LK, Laakso M et al (1993) Lower-extremity amputations in diabetic and nondiabetic patients. A populationbased study in eastern Finland. Diabetes Care 16:16-20 (Pubitemid 23013819)
134. Simpson DM, Ross R (1972) The neutrophilic leukocyte in wound repair a study with antineutrophil serum. J Clin Invest 51:2009-2023
135. Singer AJ, Clark RA (1999) Cutaneous wound healing. N Engl J Med 341:738-746 (Pubitemid 29407375)
136. Singh N, Armstrong DG, Lipsky BA (2005) Preventing foot ulcers in patients with diabetes. JAMA 293:217-228 (Pubitemid 40095873)
137. Sodek J, Ganss B, McKee MD (2000) Osteopontin. Crit Rev Oral Biol Med 11:279-303
138. Stanley AC, Park HY, Phillips TJ et al (1997) Reduced growth of dermal fibroblasts from chronic venous ulcers can be stimulated with growth factors. J Vasc Surg 26:994-999, discussion 9-1001
139. Stansfield WE, Andersen NM, Tang RH et al (2009) Periostin is a novel factor in cardiac remodeling after experimental and clinical unloading of the failing heart. Ann Thorac Surg 88:1916-1921
140. Steed DL (1995) Clinical evaluation of recombinant human plateletderived growth factor for the treatment of lower extremity diabetic ulcers. Diabetic Ulcer Study Group. J Vasc Surg 21:71-78, discussion 9-81
141. Takayama G, Arima K, Kanaji T et al (2006) Periostin: a novel component of subepithelial fibrosis of bronchial asthma downstream of IL-4 and IL-13 signals. J Allergy Clin Immunol 118:98-104 (Pubitemid 43946467)
142. Takehara K (2003) Hypothesis: pathogenesis of systemic sclerosis. J Rheumatol 30:755-759
143. Takeshita S, Kikuno R, Tezuka K et al (1993) Osteoblast-specific factor 2: cloning of a putative bone adhesion protein with homology with the insect protein fasciclin I. Biochem J 294 (Pt 1):271-278 (Pubitemid 23251940)
144. Tan EM, Qin H, Kennedy SH et al (1995) Platelet-derived growth factors-AA and-BB regulate collagen and collagenase gene expression differentially in human fibroblasts. Biochem J 310 (Pt 2):585-588
145. Thannickal VJ, Lee DY, White ES et al (2003) Myofibroblast differentiation by transforming growth factor-beta1 is dependent on cell adhesion and integrin signaling via focal adhesion kinase. J Biol Chem 278:12384-12389 (Pubitemid 36800223)
146. Tomasek JJ, Gabbiani G, Hinz B et al (2002) Myofibroblasts and mechano-regulation of connective tissue remodelling. Nat Rev Mol Cell Biol 3:349-363 (Pubitemid 34619269)
147. Trengove NJ, Bielefeldt-Ohmann H, Stacey MC (2000) Mitogenic activity and cytokine levels in non-healing and healing chronic leg ulcers. Wound Repair Regen 8:13-25 (Pubitemid 30140796)
148. Trojanowska M (2008) Role of PDGF in fibrotic diseases and systemic sclerosis. Rheumatology (Oxford) 47(Suppl 5):V2-V4
149. Vaalamo M, Leivo T, Saarialho-Kere U (1999) Differential expression of tissue inhibitors of metalloproteinases (TIMP-1,-2,-3, and-4) in normal and aberrant wound healing. Hum Pathol 30:795-802 (Pubitemid 29325786)
150. Varga J, Abraham D (2007) Systemic sclerosis: a prototypic multisystem fibrotic disorder. J Clin Invest 117:557-567 (Pubitemid 46348510)
151. Varga J, Pasche B (2009) Transforming growth factor beta as a therapeutic target in systemic sclerosis. Nat Rev Rheumatol 5:200-206
152. Verrecchia F, Chu ML, Mauviel A (2001) Identification of novel TGF-beta/Smad gene targets in dermal fibroblasts using a combined cDNA microarray/promoter transactivation approach. J Biol Chem 276:17058-17062
153. Vi L, Feng L, Zhu RD et al (2009) Periostin differentially induces proliferation, contraction and apoptosis of primary Dupuytren's disease and adjacent palmar fascia cells. Exp Cell Res 315:3574-3586
154. Voytik-Harbin SL, Brightman AO, Kraine MR et al (1997) Identification of extractable growth factors from small intestinal submucosa. J Cell Biochem 67:478-491 (Pubitemid 27508401)
155. Wang Q, Nie FF, Zhao X et al (2007) The expression of periostin in hyperplasic scars and the relations to TGF-beta1 and its receptors. Zhonghua Zheng Xing Wai Ke Za Zhi 23:229-232
156. Wei J, Bhattacharyya S, Tourtellotte WG et al (2010) Fibrosis in systemic sclerosis: Emerging concepts and implications for targeted therapy. Autoimmun Rev
157. Wieman TJ, Smiell JM, Su y (1998) Efficacy and safety of a topical gel formulation of recombinant human platelet-derived growth factor-BB (becaplermin) in patients with chronic neuropathic diabetic ulcers. A phase III randomized placebo-controlled double-blind study. Diabetes Care 21:822-827 (Pubitemid 28487079)
158. Wild S, Roglic G, Green A et al (2004) Global prevalence of diabetes: estimates for the year 2000 and projections for 2030. Diabetes Care 27:1047-1053 (Pubitemid 38579764)
159. Woodbury MG, Houghton PE (2004) Prevalence of pressure ulcers in Canadian healthcare settings. Ostomy/Wound Management 50:22-38
160. Woodbury MG, Houghton PE (2005) The extent of chronic wounds in Canada. Wound Care Canada 3:18-22
161. Woods A (2001) Syndecans: transmembrane modulators of adhesion and matrix assembly. J Clin Invest 107:935-941 (Pubitemid 32323401)
162. Wu L, Xia YP, Roth SI et al (1999) Transforming growth factor-beta1 fails to stimulate wound healing and impairs its signal transduction in an aged ischemic ulcer model: importance of oxygen and age. Am J Pathol 154:301-309 (Pubitemid 29031637)
163. Wu SC, Driver VR, Wrobel JS et al (2007) Foot ulcers in the diabetic patient, prevention and treatment. Vasc Health Risk Manag 3:65-76 (Pubitemid 46860717)
164. Wynn TA (2007) Common and unique mechanisms regulate fibrosis in various fibroproliferative diseases. J Clin Invest 117:524-529 (Pubitemid 46348506)
165. Wysocki AB, Staiano-Coico L, Grinnell F (1993) Wound fluid from chronic leg ulcers contains elevated levels of metalloproteinases MMP-2 and MMP-9. J Invest Dermatol 101:64-68 (Pubitemid 23213014)
166. Yamamoto T, Nishioka K (2005) Cellular and molecular mechanisms of bleomycin-induced murine scleroderma: current update and future perspective. Exp Dermatol 14:81-95 (Pubitemid 40277574)
167. Yan W, Shao R (2006) Transduction of a mesenchyme-specific gene periostin into 293T cells induces cell invasive activity through epithelial-mesenchymal transformation. J Biol Chem 281:19700-19708
168. Yang C, Zhu P, Yan L et al (2009) Dynamic changes in matrix metalloproteinase 9 and tissue inhibitor of metalloproteinase 1 levels during wound healing in diabetic rats. J Am Podiatr Med Assoc 99:489-496
169. Zhao LL, Davidson JD, Wee SC et al (1994) Effect of hyperbaric oxygen and growth factors on rabbit ear ischemic ulcers. Arch Surg 129:1043-1049 (Pubitemid 24320797)
170. Zheng XY, Zhang JZ, Tu P et al (1998) Expression of platelet-derived growth factor B-chain and platelet-derived growth factor betareceptor in fibroblasts of scleroderma. J Dermatol Sci 18:90-97
171. Zhou HM, Wang J, Elliott C et al (2010) Spatiotemporal expression of periostin during skin development and incisional wound healing: lessons for human fibrotic scar formation. J Cell Commun Signal 4:99-107