Diminished type III collagen promotes myofibroblast differentiation and increases scar deposition in cutaneous wound healing

Cells Tissues Organs

Volumn 194, Issue 1, 2011, Pages 25-37

  Volk, Susan W ^a   Wang, Yanjian ^a   Mauldin, Elizabeth A ^a   Liechty, Kenneth W ^b   Adams, Sherrill L ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF MISSISSIPPI SCHOOL OF MEDICINE   (United States)

Author keywords

Extracellular matrix; Mouse; Myofibroblast; Scar; Type III collagen; Wound healing

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; COLLAGEN TYPE 3;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; EMBRYO; GRANULATION TISSUE; IN VITRO STUDY; MOUSE; MYOFIBROBLAST; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SCAR FORMATION; SKIN FIBROBLAST; WOUND CLOSURE; WOUND CONTRACTION; WOUND HEALING;

ANIMALS; CELL DIFFERENTIATION; COLLAGEN TYPE III; MICE; MICE, INBRED STRAINS; MYOFIBROBLASTS; SKIN; WOUND HEALING;

ANIMALIA; MURINAE; MUS;

EID: 79959377314     PISSN: 14226405     EISSN: 14226421     Source Type: Journal    
DOI: 10.1159/000322399     Document Type: Article

References (51)

1. Arora, P.D., C.A. McCulloch (1994) Dependence of collagen remodelling on alpha-smooth muscle actin expression by fibroblasts. J Cell Physiol 159: 161-17 5. (Pubitemid 24234588)
2. Badillo, A.T., R.A. Redden, L. Zhang, E.J. Doo-lin, K.W. Liechty (2007) Treatment of diabetic wounds with fetal murine mesenchymal stromal cells enhances wound closure. Cell Tissue Res 329: 301-311. (Pubitemid 47020518)
3. Burk, C.J., C. Aber, E.A. Connelly (2006) Ehlers-Danlos syndrome type IV: keloidal plaques of the lower extemities, amniotic band limb deformity and a new mutation. J Am Acad Dermatol 56: S53-S54. (Pubitemid 46074285)
4. Byers, P.H., K.A. Holbrook, B. McGillivray, P.M. MacLeod, R.B. Lowry (1979) Clinical and ultrastructural heterogeneity of type IV Ehlers-Danlos syndrome. Hum Genet 47: 141-150. (Pubitemid 9244927)
5. Cass, D.L., K.G. Sylvester, E.Y. Yang, T.M. Crom-bleholme, N.S. Adzick (1997) Myofibroblast persistence in fetal sheep wounds is associated with scar formation. J Pediatr Surg 32: 1017-1021.
6. Cook, H., K.J. Davies, K.G. Harding, D.W. Thomas (2000) Defective extracellular matrix reorganization by chronic wound fibro-blasts is associated with alterations in TIMP-1, TIMP-2, and MMP-2 activity. J Invest Der-matol 115: 225-233. (Pubitemid 30637192)
7. Cooper, T.K., Q. Zhong, M. Krawczyk, H.J. Tae, G.A. Müller, R. Schubert, L.A. Myers, H.C. Dietz, M.I. Talan, W. Briest (2010) The hap-loinsufficient Col3a1 mouse as a model for vascular Ehlers-Danlos syndrome. Vet Pathol 47: 1028-1039.
8. Cutt le, L., M. Nataatmadja, J.F. Fraser, M. Kempf, R.M. Kimble, M.T. Hayes (2005) Collagen in the scarless fetal skin wound: detection with Picrosirius-polarization. Wound Repair Re-gen 13: 198-204. (Pubitemid 40489870)
9. Desmouliere, A., A. Geinoz, F. Gabbiani, G. Gabbiani (1993) Transforming growth factor-beta 1 induces alpha-smooth muscle ac-tin expression in GT myofibroblasts and in quiescent and growing cultured fibroblasts. J Cell Biol 122: 103-111. (Pubitemid 23188802)
10. Desmouliere, A., M. Redard, I. Darby, G. Gab-biani (1995) Apoptosis mediates the decrease in cellularity during the transition between granulation tissue and scar. Am J Pathol 146: 56-66.
11. Ehrlich, H.P. (1988) The modulation of contraction of fibroblast populated collagen lattices by types I, II, and III collagen. Tissue Cell 20: 47-50. (Pubitemid 18084549)
12. Gabbiani, G. (2003) The myofibroblast in wound healing and fibrocontractive diseases. J Pathol 200: 500-503. (Pubitemid 36818250)
13. Germain, D.P. (2007) Ehlers-Danlos syndrome type IV. Orphanet J Rare Dis 2: 32-41.
14. Goldberg, S.R., G.L. Quirk, V.W. Sykes, T. Kor-dula, D.A. Lanning (2007) Altered procol-lagen gene expression in mid-gestational mouse embryonic wounds. J Surg Res 143: 27-34. (Pubitemid 47562460)
15. Grinnell, F., C.H. Ho, Y.C. Lin, G. Skuta (1999a) Differences in the regulation of fibroblast contraction of floating versus stressed collagen matrices. J Biol Chem 2: 918-923.
16. Grinnell, F., M. Zhu, M.A. Carlson, J.M. Abrams (1999b) Release of mechanical tension triggers apoptosis of human fibroblasts in a model of regressing granulation tissue. Exp Cell Res 248: 608-619. (Pubitemid 29394821)
17. Hinz, B., G. Celetta, J.J. Tomasek, G. Gabbiani, C. Chaponnier (2001) Alpha-smooth muscle actin expression upregulates fibroblast contractile activity. Mol Biol Cell 12: 2730-2741. (Pubitemid 33051938)
18. Hinz, B., G. Gabbiani (2003) Mechanisms of force generation and transmission by myofi-broblasts. Curr Opin Biotechnol 14: 546.
19. Hurme, T., H. Kalimo, M. Sandberg, J.M. Lehto, E. Vuorio (1991) Localization of type I and III collagen and fibronectin production in injured gastrocnemius muscle. Lab Invest 64: 76-84.
20. Järveläinen, H., P. Puolakkainen, S. Pakkanen, E.L. Brown, M. Höök, R.V. Iozzo, E.H. Sage, T.N. Wight (2006) A role for decorin in cutaneous wound healing and angiogenesis. Wound Repair Regen 14: 443-452. (Pubitemid 44266601)
21. Kyriakides, T.R., P. Bornstein (2003) Matricel-lular proteins as modulators of wound healing and the foreign body response. Thromb Haemost 90: 986-992. (Pubitemid 38008022)
22. Lee, T.Y., G.S. Chin, W.J. Kim, D. Chau, G.K. Gittes, M.T. Longaker (1999) Expression of transforming growth factor beta 1, 2, and 3 proteins in keloids. Ann Plast Surg 43: 179-184. (Pubitemid 29380019)
23. Liao, H., J. Zakhaleva, W. Chen (2009) Cells and tissue interactions with glycated collagen and their relevance to delayed diabetic wound healing. Biomaterials 30: 1689-1696.
24. Lin, R.Y., K.M. Sullivan, P.A. Argenta, M. Meuli, H.P. Lorenz, N.S. Adzick (1995) Exogenous transforming growth factor-beta amplifies its own expression and induces scar formation in a model of human fetal skin repair. Ann Surg 222: 146-154.
25. Liu, S.H., R.S. Yang, R. Al-Haikh, J.M. Lane (1995) Collagen in tendon, ligament and bone healing: a current review. Clin Orthop Relat Res 318: 265-278.
26. Liu, X., H. Wu, M. Burne, S. Krane, R. Jaenisch (1997) Type III collagen is crucial for collagen I fibrillogenesis and for normal cardiovascular development. Proc Natl Acad Sci USA 94: 1852-1856. (Pubitemid 27113925)
27. Lygoe, K.A., I. Wall, P. Stephens, C. Li (2007) Role of vitronectin and fibronectin receptors in oral mucosal and dermal myofibroblast differentiation. Biol Cell 99: 601-614. (Pubitemid 350120980)
28. McGrath, M.H., S.A. Hundahl (1982) The spatial and temporal quantification of myofibro-blasts. Plast Reconstr Surg 69: 975-985.
29. Merkel, J.R., B.R. DiPaolo, G.G. Hallock, D.C. Rice (1988) Type I and type III collagen content of healing wounds in fetal and adult rats. Proc Soc Exp Biol Med 187: 493-497.
30. Mochitate, K., P. Pawelek, F. Grinnell (1991) Stress relaxation of contracted collagen gels: disruption of actin filament bundles, release of cell surface fibronectin, and down-regulation of DNA and protein synthesis. Exp Cell Res 193: 198-207. (Pubitemid 121004353)
31. Neptune, E.R., P.A. Frischmeyer, D.E. Arking, L. Myers, T.E. Bunton, B. Gayraud, F. Ramirez, L.Y. Sakai, H.C. Dietz (2003) Dysregulation of TGF-beta activation contributes to patho-genesis in Marfan syndrome. Nat Genet 33: 407-411. (Pubitemid 36278859)
32. Occleston, N.L., A.D. Metcalfe, A. Boanas, N.J. Burgoyne, K. Nield, S. O'Kane, M.W. Ferguson (2010) Therapeutic improvement in scarring: mechanisms of scarless and scar-forming healing and approaches to the discovery of new treatments. Derm Res Pract 2010, E-pub ahead of print.
33. Oderich, G.S., J.M. Panneton, T.C. Bower, N.M. Lindor, K.J. Cherry, A.A. Noel, M. Kalra, T. Sullivan, J. Glowacki (2005) The spectrum, management and clinical outcome of Ehlers Danlos syndrome IV: a 30-year experience. J Vasc Surg 42: 98-106. (Pubitemid 40966082)
34. Oganesian, A., S. Au, J.A. Horst, L.C. Holzhau-sen, A.J. Macy, J.M. Pace, P. Bornstein (2006) The NH2-terminal propeptide of type I pro-collagen acts intracellularly to modulate cell function. J Biol Chem 281: 38507-38518. (Pubitemid 46041975)
35. Parizi, M., E.W. Howard, J.J. Tomasek (2000) Regulation of LPA-promoted myofibroblast contraction: role of Rho, myosin light chain kinase, and myosin light chain phosphatase. Exp Cell Res 254: 210-220. (Pubitemid 30080577)
36. Pepin, M., U. Schwarze, A. Superti-Furga, P.H. Byers (2000) Clinical and genetic features of Ehlers-Danlos syndrome type IV, the vascular form. New Engl J Med 342: 673-680. (Pubitemid 30131419)
37. Phillips, L.G., L. Seppinen, R. Sormunen, Y. Soi-ni, H. Elamaa, R. Heljasvaara, T. Phihlajani-emi (2008) Lack of collagen XVIII accelerates cutaneous wound healing, while overex-pression of its endostatin domain leads to delayed hea ling. Matrix Biol 27: 535-546.
38. Powell, D.W., R.C. Mifflin, J.D. Valentich, S.E. Crowe, J.I. Saada, A.B. West (1999) Myofi-broblasts: paracrine cells important in health and disease. Am J Physiol 277: C1-9.
39. Reid, R.R., H.K. Said, J.E. Mogford, T.A. Mustoe (2004) The future of wound healing: pursuing surgical models in transgenic and knockout mice. J Am Coll Surg 199: 578-585. (Pubitemid 39420210)
40. Romanic, A.M., E. Adachi, K.E. Kadler, Y. Ho-jima, D.J. Prockop (1991) Copolymerization of pN collagen III a nd col lagen I: pN col lagen III decreases the rate of incorporation of collagen I into fibrils, the amount of collagen I incorporated and the diameter of the fibrils formed. J Biol Chem 266: 12703-12709. (Pubitemid 21907152)
41. Rungger-Brandle, E., G. Gabbiani (1983) The role of the cytoskeletal and cytocontractile elements in pathologic processes. Am J Pathol 110: 361-385.
42. Schwarze, U., W.I. Schievink, E. Petty, M.R. Jaff, D. Babovic-Vuksanovic, K.J. Cherry, M. Pe-pin, P.H. Byers (2001) Haploinsufficiency for one Col3A1 allele of type III procollagen results in a phenotype similar to the vascular form of Ehlers-Danlos syndrome, Ehlers-Danlos syndrome type IV. Am J Hum Genet 69: 989-1001. (Pubitemid 33015814)
43. Serini, G., G. Gabbiani (1999) Mechanisms of myofibroblast activity and phenotypic modulation. Exp Cell Res 250: 273-283. (Pubitemid 29367440)
44. Shah, M., D.M. Foreman, M.W. Ferguson (1995) Neutalisation of TGF-ß1 and TGF-ß2 or exogenous addition of TGF-ß3 to cutaneous rat wounds reduces scarring. J Cell Sci 108: 985-1002.
45. Sharma, N.L., V.K. Mahajan, N. Gupta, N. Ran-jan, A. Lath (2009) Ehlers-Danlos syndrome-vascular type (ecchymotic variant): cutaneous and dermatopathologic features. J Cutan Pathol 36: 486-492.
46. Stevenson, K., U. Kucich, C. Whitbeck, R.M. Levin, P.S. Howard (2006) Functional changes in bladder tissue from type III collagen-deficient mice. Mol Cell Biochem 283: 107-114.
47. Tomasek, J.J., C.J. Haaksma, R.J. Eddy, M.B. Vaughan (1992) Fibroblast contraction occurs on release of tension in attached collagen lattices: dependency on an organized ac-tin cytoskeleton and serum. Anat Rec 232: 359-368.
48. Vaughan, M.B., E.W. Howard, J.J. Tomasek (2000) Transforming growth factor-ß1 promotes the morphological and functional differentiation of the myofibroblast. Exp Cell Res 257: 180-189. (Pubitemid 30324656)
49. Volk, S.W., A. Radu, L. Zhang, K.W. Liechty (2007) Stromal progenitor cell therapy corrects the wound healing defect in the isch-emic rabbit ear model of chronic wound repair. Wound Repair Regen 15: 736-747. (Pubitemid 47493889)
50. Zhu, Y., A. Oganesian, D.R. Keene, L.J. Sandell (1999) Type IIA procollagen containing the cysteine-rich amino propeptide is deposited in the extracellular matrix of prechondro-genic tissue and binds to TGFß1 and BMP2. J Cell Biol 144: 1069-1080. (Pubitemid 29238979)
51. Zoppi, N., R. Gardella, A. DePaepe, S. Barlati, M. Colombi (2004) Human fibroblasts with mutations in COL5A1 and COL3A1 genes do not organize collagens and fibronectin in the extracellular matrix, down-regulate α2 1 1 integrin, and recruit αvß3 instead of α5ß integrin. J Biol Chem 279: 18157-18168. (Pubitemid 38623228)