Differential collagen-glycosaminoglycan matrix remodeling by superficial and deep dermal fibroblasts: Potential therapeutic targets for hypertrophic scar

Biomaterials

Volumn 32, Issue 30, 2011, Pages 7581-7591

  Varkey, Mathew ^a   Ding, Jie ^a   Tredget, Edward E ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Biomechanical; Collagen glycosaminoglycan; Deep dermal fibroblast; Hypertrophic scar; Remodeling

Indexed keywords

BIOMECHANICAL; COLLAGEN-GLYCOSAMINOGLYCAN; DERMAL FIBROBLASTS; HYPERTROPHIC SCAR; REMODELING;

BIOMECHANICS; COLLAGEN; FIBROBLASTS; TENSILE STRENGTH; TISSUE;

CELL CULTURE;

ANGIOTENSIN II; COLLAGEN; CONNECTIVE TISSUE GROWTH FACTOR; DECORIN; FIBROMODULIN; GLYCOSAMINOGLYCAN; HEAT SHOCK PROTEIN 47; HYDROXYPROLINE; HYPOXANTHINE PHOSPHORIBOSYLTRANSFERASE; INTERSTITIAL COLLAGENASE; LYMPHOTOXIN; OSTEOPONTIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PROTEOGLYCAN; TRANSFORMING GROWTH FACTOR BETA1; TUMOR NECROSIS FACTOR ALPHA; VERSICAN;

ABDOMINOPLASTY; ACELLULAR DERMAL MATRIX; ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CELL VIABILITY; CONTROLLED STUDY; DEEP DERMAL FIBROBLAST; DERMIS; EXTRACELLULAR MATRIX; FIBROBLAST; GENE EXPRESSION; HUMAN; HUMAN CELL; HYPERTROPHIC SCAR; MYOFIBROBLAST; PRIORITY JOURNAL; PROTEIN EXPRESSION; SUPERFICIAL DERMAL FIBROBLAST; TENSILE STRENGTH; TISSUE REPAIR;

BIOMECHANICS; CELL DIFFERENTIATION; CELL SURVIVAL; CELLS, CULTURED; CICATRIX, HYPERTROPHIC; COLLAGEN; DERMIS; EXTRACELLULAR MATRIX; FIBROBLASTS; GLYCOSAMINOGLYCANS; HUMANS; MYOFIBROBLASTS; POROSITY; SKIN, ARTIFICIAL; TISSUE SCAFFOLDS; TRANSFORMING GROWTH FACTOR BETA1;

EID: 80051547353     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2011.06.070     Document Type: Article

References (64)

1. Boyce S.T., Kagan R.J., Yakuboff K.P., Meyer N.A., Rieman M.T., Greenhalgh D.G., et al. Cultured skin substitutes reduce donor skin harvesting for closure of excised, full-thickness burns. Ann Surg 2002, 235:269-279.
2. Scott P.G., Ghahary A., Tredget E.E. Molecular and cellular aspects of fibrosis following thermal injury. Hand Clin 2000, 16:271-287.
3. Bombaro K.M., Engrav L.H., Carrougher G.J., Wiechman S.A., Faucher L., Costa B.A., et al. What is the prevalence of hypertrophic scarring following burns?. Burns 2003, 29:299-302.
4. Monstrey S., Hoeksema H., Verbelen J., Pirayesh A., Blondeel P. Assessment of burn depth and burn wound healing potential. Burns 2008, 34:761-769.
5. Cubison T.C., Pape S.A., Parkhouse N. Evidence for the link between healing time and the development of hypertrophic scars (HTS) in paediatric burns due to scald injury. Burns 2006, 32:992-999.
6. Dunkin C.S., Pleat J.M., Gillespie P.H., Tyler M.P., Roberts A.H., McGrouther D.A. Scarring occurs at a critical depth of skin injury: precise measurement in a graduated dermal scratch in human volunteers. Plast Reconstr Surg 2007, 119:1722-1732. discussion 33-4.
7. Sorrell J.M., Caplan A.I. Fibroblast heterogeneity: more than skin deep. J Cell Sci 2004, 117:667-675.
8. Schafer I.A., Pandy M., Ferguson R., Davis B.R. Comparative observation of fibroblasts derived from the papillary and reticular dermis of infants and adults: growth kinetics, packing density at confluence and surface morphology. Mech Ageing Dev 1985, 31:275-293.
9. Azzarone B., Macieira-Coelho A. Heterogeneity of the kinetics of proliferation within human skin fibroblastic cell populations. J Cell Sci 1982, 57:177-187.
10. Sorrell J.M., Baber M.A., Caplan A.I. 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.
11. Ali-Bahar M., Bauer B., Tredget E.E., 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.
12. Armour A., Scott P.G., Tredget E.E. Cellular and molecular pathology of HTS: basis for treatment. Wound Repair Regen 2007, 15(Suppl. 1):S6-S17.
13. Wang J., Dodd C., Shankowsky H.A., Scott P.G., Tredget E.E. Deep dermal fibroblasts contribute to hypertrophic scarring. Lab Invest 2008, 88:1278-1290.
14. Wang R., Ghahary A., Shen Q., Scott P.G., Roy K., Tredget E.E. Hypertrophic scar tissues and fibroblasts produce more transforming growth factor-beta1 mRNA and protein than normal skin and cells. Wound Repair Regen 2000, 8:128-137.
15. Berman J.S., Serlin D., Li X., Whitley G., Hayes J., Rishikof D.C., et al. Altered bleomycin-induced lung fibrosis in osteopontin-deficient mice. Am J Physiol Lung Cell Mol Physiol 2004, 286:L1311-L1318.
16. Persy V.P., Verhulst A., Ysebaert D.K., De Greef K.E., De Broe M.E. Reduced postischemic macrophage infiltration and interstitial fibrosis in osteopontin knockout mice. Kidney Int 2003, 63:543-553.
17. Lenga Y., Koh A., Perera A.S., McCulloch C.A., Sodek J., Zohar R. Osteopontin expression is required for myofibroblast differentiation. Circ Res 2008, 102:319-327.
18. Boyce S.T., Kagan R.J., Greenhalgh D.G., Warner P., Yakuboff K.P., Palmieri T., et al. Cultured skin substitutes reduce requirements for harvesting of skin autograft for closure of excised, full-thickness burns. J Trauma 2006, 60:821-829.
19. Swope V.B., Boyce S.T. Differential expression of matrix metalloproteinase-1 in vitro corresponds to tissue morphogenesis and quality assurance of cultured skin substitutes. J Surg Res 2005, 128:79-86.
20. Powell H.M., Boyce S.T. EDC cross-linking improves skin substitute strength and stability. Biomaterials 2006, 27:5821-5827.
21. Tomasek J.J., Gabbiani G., Hinz B., Chaponnier C., Brown R.A. Myofibroblasts and mechano-regulation of connective tissue remodelling. Nat Rev Mol Cell Biol 2002, 3:349-363.
22. Desmouliere A., Redard M., Darby I., Gabbiani G. Apoptosis mediates the decrease in cellularity during the transition between granulation tissue and scar. Am J Pathol 1995, 146:56-66.
23. Fluck J., Querfeld C., Cremer A., Niland S., Krieg T., Sollberg S. Normal human primary fibroblasts undergo apoptosis in three-dimensional contractile collagen gels. J Invest Dermatol 1998, 110:153-157.
24. Miller C.C., Godeau G., Lebreton-DeCoster C., Desmouliere A., Pellat B., Dubertret L., et al. Validation of a morphometric method for evaluating fibroblast numbers in normal and pathologic tissues. Exp Dermatol 2003, 12:403-411.
25. Grinnell F., Zhu M., Carlson M.A., Abrams J.M. Release of mechanical tension triggers apoptosis of human fibroblasts in a model of regressing granulation tissue. Exp Cell Res 1999, 248:608-619.
26. Jiang H., Rhee S., Ho C.H., Grinnell F. Distinguishing fibroblast promigratory and procontractile growth factor environments in 3-D collagen matrices. FASEB J 2008, 22:2151-2160.
27. Dunn M.G., Silver F.H., Swann D.A. Mechanical analysis of hypertrophic scar tissue: structural basis for apparent increased rigidity. J Invest Dermatol 1985, 84:9-13.
28. Clark J.A., Cheng J.C., Leung K.S. Mechanical properties of normal skin and hypertrophic scars. Burns 1996, 22:443-446.
29. Rudolph R. Wide spread scars, hypertrophic scars, and keloids. Clin Plast Surg 1987, 14:253-260.
30. Cohen I.K. Can collagen metabolism be controlled: theoretical considerations. J Trauma 1985, 25:410-412.
31. Wynn T.A. Cellular and molecular mechanisms of fibrosis. J Pathol 2008, 214:199-210.
32. Engler A.J., Griffin M.A., Sen S., Bonnemann C.G., Sweeney H.L., Discher D.E. Myotubes differentiate optimally on substrates with tissue-like stiffness: pathological implications for soft or stiff microenvironments. J Cell Biol 2004, 166:877-887.
33. Georges P.C., Miller W.J., Meaney D.F., Sawyer E.S., Janmey P.A. Matrices with compliance comparable to that of brain tissue select neuronal over glial growth in mixed cortical cultures. Biophys J 2006, 90:3012-3018.
34. McDaniel D.P., Shaw G.A., Elliott J.T., Bhadriraju K., Meuse C., Chung K.H., et al. The stiffness of collagen fibrils influences vascular smooth muscle cell phenotype. Biophys J 2007, 92:1759-1769.
35. Li Z., Dranoff J.A., Chan E.P., Uemura M., Sevigny J., Wells R.G. Transforming growth factor-beta and substrate stiffness regulate portal fibroblast activation in culture. Hepatology 2007, 46:1246-1256.
36. Wipff P.J., Rifkin D.B., Meister J.J., Hinz B. Myofibroblast contraction activates latent TGF-beta1 from the extracellular matrix. J Cell Biol 2007, 179:1311-1323.
37. Georges P.C., Hui J.J., Gombos Z., McCormick M.E., Wang A.Y., Uemura M., et al. Increased stiffness of the rat liver precedes matrix deposition: implications for fibrosis. Am J Physiol Gastrointest Liver Physiol 2007, 293:G1147-G1154.
38. Hinz B., Phan S.H., Thannickal V.J., Galli A., Bochaton-Piallat M.L., Gabbiani G. The myofibroblast: one function, multiple origins. Am J Pathol 2007, 170:1807-1816.
39. Aarabi S., Bhatt K.A., Shi Y., Paterno J., Chang E.I., Loh S.A., et al. Mechanical load initiates hypertrophic scar formation through decreased cellular apoptosis. FASEB J 2007, 21:3250-3261.
40. Tredget E.E. Pathophysiology and treatment of fibroproliferative disorders following thermal injury. Ann N Y Acad Sci 1999, 888:165-182.
41. Brigstock D.R. The CCN family: a new stimulus package. J Endocrinol 2003, 178:169-175.
42. Nagata K. Hsp47: a collagen-specific molecular chaperone. Trends Biochem Sci 1996, 21:22-26.
43. Ghahary A., Shen Y.J., Nedelec B., Wang R., Scott P.G., Tredget E.E. Collagenase production is lower in post-burn hypertrophic scar fibroblasts than in normal fibroblasts and is reduced by insulin-like growth factor-1. J Invest Dermatol 1996, 106:476-481.
44. Mori R., Shaw T.J., 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.
45. Marshall R.P., Gohlke P., Chambers R.C., Howell D.C., Bottoms S.E., Unger T., et al. Angiotensin II and the fibroproliferative response to acute lung injury. Am J Physiol Lung Cell Mol Physiol 2004, 286:L156-L164.
46. Berk B.C., Fujiwara K., Lehoux S. ECM remodeling in hypertensive heart disease. J Clin Invest 2007, 117:568-575.
47. Mezzano S.A., Ruiz-Ortega M., Egido J. Angiotensin II and renal fibrosis. Hypertension 2001, 38:635-638.
48. Peruccio D., Castagnoli C., Stella M., D'Alfonso S., Momigliano P.R., Magliacani G., et al. Altered biosynthesis of tumour necrosis factor (TNF) alpha is involved in postburn hypertrophic scars. Burns 1994, 20:118-121.
49. Singer A.J., Clark R.A. Cutaneous wound healing. N Engl J Med 1999, 341:738-746.
50. Abraham D.J., Shiwen X., Black C.M., Sa S., Xu Y., Leask A. Tumor necrosis factor alpha suppresses the induction of connective tissue growth factor by transforming growth factor-beta in normal and scleroderma fibroblasts. J Biol Chem 2000, 275:15220-15225.
51. Goldberg M.T., Han Y.P., Yan C., Shaw M.C., Garner W.L. TNF-alpha suppresses alpha-smooth muscle actin expression in human dermal fibroblasts: an implication for abnormal wound healing. J Invest Dermatol 2007, 127:2645-2655.
52. Ghosh A.K., Bhattacharyya S., Wei J., Kim S., Barak Y., Mori Y., et al. Peroxisome proliferator-activated receptor-gamma abrogates Smad-dependent collagen stimulation by targeting the p300 transcriptional coactivator. FASEB J 2009, 23:2968-2977.
53. Burgess H.A., Daugherty L.E., Thatcher T.H., Lakatos H.F., Ray D.M., Redonnet M., et al. PPARgamma agonists inhibit TGF-beta induced pulmonary myofibroblast differentiation and collagen production: implications for therapy of lung fibrosis. Am J Physiol Lung Cell Mol Physiol 2005, 288:L1146-L1153.
54. Zafiriou S., Stanners S.R., Saad S., Polhill T.S., Poronnik P., Pollock C.A. Pioglitazone inhibits cell growth and reduces matrix production in human kidney fibroblasts. J Am Soc Nephrol 2005, 16:638-645.
55. Galli A., Crabb D.W., Ceni E., Salzano R., Mello T., Svegliati-Baroni G., et al. Antidiabetic thiazolidinediones inhibit collagen synthesis and hepatic stellate cell activation in vivo and in vitro. Gastroenterology 2002, 122:1924-1940.
56. Masamune A., Kikuta K., Satoh M., Sakai Y., Satoh A., Shimosegawa T. Ligands of peroxisome proliferator-activated receptor-gamma block activation of pancreatic stellate cells. J Biol Chem 2002, 277:141-147.
57. Diep Q.N., Benkirane K., Amiri F., Cohn J.S., Endemann D., Schiffrin E.L. PPAR alpha activator fenofibrate inhibits myocardial inflammation and fibrosis in angiotensin II-infused rats. J Mol Cell Cardiol 2004, 36:295-304.
58. Zhang H., Pi R., Li R., Wang P., Tang F., Zhou S., et al. PPARbeta/delta activation inhibits angiotensin II-induced collagen type I expression in rat cardiac fibroblasts. Arch Biochem Biophys 2007, 460:25-32.
59. Scott P.G., Dodd C.M., Ghahary A., Shen Y.J., Tredget E.E. Fibroblasts from post-burn hypertrophic scar tissue synthesize less decorin than normal dermal fibroblasts. Clin Sci (Lond) 1998, 94:541-547.
60. Sayani K., Dodd C.M., Nedelec B., Shen Y.J., Ghahary A., Tredget E.E., et al. Delayed appearance of decorin in healing burn scars. Histopathology 2000, 36:262-272.
61. Hildebrand A., Romaris M., Rasmussen L.M., Heinegard D., Twardzik D.R., Border W.A., et al. Interaction of the small interstitial proteoglycans biglycan, decorin and fibromodulin with transforming growth factor beta. Biochem J 1994, 302(Pt 2):527-534.
62. Wight T.N. Versican: a versatile extracellular matrix proteoglycan in cell biology. Curr Opin Cell Biol 2002, 14:617-623.
63. Stoff A., Rivera A.A., Mathis J.M., Moore S.T., Banerjee N.S., Everts M., et al. Effect of adenoviral mediated overexpression of fibromodulin on human dermal fibroblasts and scar formation in full-thickness incisional wounds. J Mol Med 2007, 85:481-496.
64. Soo C., Hu F.Y., Zhang X., Wang Y., Beanes S.R., Lorenz H.P., et al. Differential expression of fibromodulin, a transforming growth factor-beta modulator, in fetal skin development and scarless repair. Am J Pathol 2000, 157:423-433.