A physiological role for connective tissue growth factor in early wound healing

Laboratory Investigation

Volumn 93, Issue 1, 2013, Pages 81-95

  Alfaro, Maria P ^a   Deskins, Desirae L ^a   Wallus, Meredith ^a   DasGupta, Jayasri ^a   Davidson, Jeffrey M ^a,b   Nanney, Lillian B ^a   A Guney, Michelle ^a   Gannon, Maureen ^a,b,c   Young, Pampee P ^a,b,c  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

fibrosis; mouse models; repair and regeneration; stem cells; wound healing

Indexed keywords

CALRETICULIN; COL1A2 PROTEIN; COLLAGEN; CONNECTIVE TISSUE GROWTH FACTOR; CYSTATIN C; DYSTROGLYCAN; FOLLISTATIN RELATED PROTEIN; FRUCTOSE BISPHOSPHATE ALDOLASE; GAMMA GLUTAMYL HYDROLASE; GLYPICAN 1; LACTADHERIN; LIPOCORTIN 2; MESOTHELIN; MESSENGER RNA; METALLOPROTEINASE INHIBITOR; PLASMINOGEN ACTIVATOR INHIBITOR 1; POLYVINYL ALCOHOL; PROCOLLAGEN C PROTEINASE; PROSAPOSIN; PROTEASE NEXIN I; PROTEIN LYSINE 6 OXIDASE; SECRETED FRIZZLED RELATED PROTEIN 2; TENASCIN; THIOL OXIDASE; THROMBOSPONDIN 1; TRANSCOBALAMIN II; TRANSCRIPTION FACTOR RUNX2; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BURN; CONTROLLED STUDY; DERMATOME; FIBROBLAST; GRANULATION TISSUE; HAPLOINSUFFICIENCY; HISTOLOGY; HUMAN; HUMAN TISSUE; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; KERATINOCYTE; LIQUID CHROMATOGRAPHY; MESENCHYMAL STEM CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SKIN INJURY; TANDEM MASS SPECTROMETRY; TISSUE REPAIR; VASCULARIZATION; WOUND HEALING;

ANALYSIS OF VARIANCE; ANIMALS; BURNS; CELL PHYSIOLOGICAL PROCESSES; COLLAGEN; CONNECTIVE TISSUE GROWTH FACTOR; CULTURE MEDIA, CONDITIONED; HUMANS; IMMUNOHISTOCHEMISTRY; MEMBRANE PROTEINS; MESENCHYMAL STROMAL CELLS; MICE; MICE, KNOCKOUT; PROTEOMICS; SKIN; UP-REGULATION; WOUND HEALING;

EID: 84871765176     PISSN: 00236837     EISSN: 15300307     Source Type: Journal    
DOI: 10.1038/labinvest.2012.162     Document Type: Article

References (48)

1. Gnecchi M, Zhang Z, Ni A, et al. Paracrine mechanisms in adult stem cell signaling and therapy. Circ Res 2008;103:1204-1219.
2. Caplan AI, Dennis JE. Mesenchymal stem cells as trophic mediators. J Cell Biochem 2006;98:1076-1084. (Pubitemid 44128350)
3. Alfaro MP, Pagni M, Vincent A, et al. The Wnt modulator sFRP2 enhances mesenchymal stem cell engraftment, granulation tissue formation and myocardial repair. Proc Natl Acad Sci USA 2008;105:18366-18371.
4. Mirotsou M, Zhang Z, Deb A, et al. Secreted frizzled related protein 2 (Sfrp2) is the key Akt-mesenchymal stem cell-released paracrine factor mediating myocardial survival and repair. Proc Natl Acad Sci USA 2007;104:1643-1648. (Pubitemid 46214644)
5. Estrada R, Li N, Sarojini H, et al. Secretome from mesenchymal stem cells induces angiogenesis via Cyr61. J Cell Physiol 2009;219:563-571.
6. Salasznyk RM, Westcott AM, Klees RF, et al. Comparing the protein expression profiles of human mesenchymal stem cells and human osteoblasts using gene ontologies. Stem Cells Dev 2005;14:354-366. (Pubitemid 41243698)
7. Polacek M, Bruun JA, Elvenes J, et al. The secretory profiles of cultured human articular chondrocytes and mesenchymal stem cells: implications for autologous cell transplantation strategies. Cell Transplant 2010;20:1381-1393.
8. Shi-Wen X, Leask A, Abraham D. Regulation and function of connective tissue growth factor/CCN2 in tissue repair, scarring and fibrosis. Cytokine Growth Factor Rev 2008;19:133-144. (Pubitemid 351382279)
9. Rachfal AW, Brigstock DR. Structural and functional properties of CCN proteins. Vitam Horm 2005;70:69-103. (Pubitemid 43589023)
10. Chen CC, Lau LF. Functions and mechanisms of action of CCN matricellular proteins. Int J Biochem Cell Biol 2010;41:771-783.
11. Ito Y, Aten J, Bende RJ, et al. Expression of connective tissue growth factor in human renal fibrosis. Kidney Int 1998;53:853-861. (Pubitemid 28155657)
12. di Mola FF, Friess H, Martignoni ME, et al. Connective tissue growth factor is a regulator for fibrosis in human chronic pancreatitis. Ann Surg 1999;230:63-71. (Pubitemid 30190366)
13. Igarashi A, Nashiro K, Kikuchi K, et al. Connective tissue growth factor gene expression in tissue sections from localized scleroderma, keloid, and other fibrotic skin disorders. J Invest Dermatol 1996;106:729-733. (Pubitemid 26119731)
14. Crawford LA, Guney MA, Oh YA, et al. Connective tissue growth factor (CTGF) inactivation leads to defects in islet cell lineage allocation and beta-cell proliferation during embryogenesis. Mol Endocrinol 2009;23:324-336.
15. Subramaniam M, Saffaripour S, Van De Water L, et al. Role of endothelial selectins in wound repair. Am J Pathol 1997;150:1701-1709. (Pubitemid 27193817)
16. Shi Y, Reitmaier B, Regenbogen J, et al. CARP, a cardiac ankyrin repeat protein, is up-regulated during wound healing and induces angiogenesis in experimental granulation tissue. Am J Pathol 2005;166:303-312. (Pubitemid 40051682)
17. Tropel P, Noël D, Platet N, et al. Isolation and characterisation of mesenchymal stem cells from adult mouse bone marrow. Exp Cell Res 2004;295:395-406. (Pubitemid 38490494)
18. Higdon R, Hogan JM, Van Belle G, et al. Randomized sequence databases for tandem mass spectrometry peptide and protein identification. OMICS 2005;9:364-379. (Pubitemid 43235291)
19. Elias JE, Haas W, Faherty BK, et al. Comparative evaluation of mass spectrometry platforms used in large-scale proteomics investigations. Nat Methods 2005;2:667-675. (Pubitemid 41223093)
20. Tabb DL, Friedman DB, Ham AJ. Verification of automated peptide identifications from proteomic tandem mass spectra. Nat Protoc 2006; 1:2213-2222.
21. Ma ZQ, Dasari S, Chambers MC, et al. IDPicker 2.0: improved protein assembly with high discrimination peptide identification filtering. J Proteome Res 2009;8:3872-3881.
22. Alfaro MP, Vincent A, Saraswati S, et al. sFRP2 suppression of bone morphogenic protein (BMP) and Wnt signaling mediates mesenchymal stem cell (MSC) self-renewal promoting engraftment and myocardial repair. J Biol Chem 2010;285:35645-35653.
23. Igarashi A, Okochi H, Bradham DM, et al. Regulation of connective tissue growth factor gene expression in human skin fibroblasts and during wound repair. Mol Biol Cell 1993;4:637-645. (Pubitemid 23183611)
24. Leask A, Abraham DJ. The role of connective tissue growth factor, a multifunctional matricellular protein, in fibroblast biology. Biochem Cell Biol 2003;81:355-363. (Pubitemid 38186975)
25. Krummel TM, Michna BA, Thomas BL, et al. Transforming growth factor beta (TGF-beta) induces fibrosis in a fetal wound model. J Pediatr Surg 1988;23:647-652.
26. Cooney R, Iocono J, Maish G, et al. Tumor necrosis factor mediates impaired wound healing in chronic abdominal sepsis. J Trauma 1997;42:415-420. (Pubitemid 27155076)
27. Lee CH, Shah B, Moioli EK, et al. 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.
28. Frazier K, Williams S, Kothapalli D, et al. Stimulation of fibroblast cell growth, matrix production, and granulation tissue formation by connective tissue growth factor. J Invest Dermatol 1996;107:404-411. (Pubitemid 26284351)
29. Ivkovic S, Yoon BS, Popoff SN, et al. Connective tissue growth factor coordinates chondrogenesis and angiogenesis during skeletal development. Development 2003;130:2779-2791. (Pubitemid 37069592)
30. Liu S, Shi-wen X, Abraham DJ, et al. CCN2 is required for bleomycin-induced skin fibrosis in mice. Arthritis Rheum 2011;63:239-246.
31. Ujike K, Shinji T, Hirasaki S, et al. Kinetics of expression of connective tissue growth factor gene during liver regeneration after partial hepatectomy and D-galactosamine-induced liver injury in rats. Biochem Biophys Res Commun 2000;277:448-454.
32. Mori T, Kawara S, Shinozaki M, et al. Role and interaction of connective tissue growth factor with transforming growth factor-beta in persistent fibrosis: a mouse fibrosis model. J Cell Physiol 1999;181:153-159. (Pubitemid 29400382)
33. Bonniaud P, Margetts PJ, Kolb M, et al. Adenoviral gene transfer of connective tissue growth factor in the lung induces transient fibrosis. Am J Respir Crit Care Med 2003;168:770-778. (Pubitemid 37188299)
34. Ikawa Y, Ng PS, Endo K, et al. Neutralizing monoclonal antibody to human connective tissue growth factor ameliorates transforming growth factor-beta-induced mouse fibrosis. J Cell Physiol 2008;216:680-687.
35. Chen Y, Shi-Wen X, van Beek J, et al. 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 2005;167:1699-1711. (Pubitemid 41713321)
36. Arnold F, West DC. Angiogenesis in wound healing. Pharmacol Ther 1991;52:407-422.
37. Liu LD, Shi HJ, Jiang L, et al. The repairing effect of a recombinant human connective-tissue growth factor in a burn-wounded rhesus-monkey (Macaca mulatta) model. Biotechnol Appl Biochem 2007;47 (Pt 2):105-112. (Pubitemid 46867110)
38. Darby I, Skalli O, Gabbiani G. Alpha-smooth muscle actin is transiently expressed by myofibroblasts during experimental wound healing. Lab Invest 1990;63:21-29. (Pubitemid 20234670)
39. Guney MA, Petersen CP, Boustani A, et al. Connective tissue growth factor acts within both endothelial cells and b cells to promote proliferation of developing b cells. Proc Natl Acad Sci 2011;108:15242-15247.
40. Hilfiker-Kleiner D, Kaminski K, Kaminska A, et al. Regulation of proangiogenic factor CCN1 in cardiac muscle. Circulation 2004;109:2227-2233.
41. Chen CC, Chen N, Lau LF. The angiogenic factors Cyr61 and connective tissue growth factor induce adhesive signaling in primary human skin fibroblasts. J Biol Chem 2001;276:10443-10452.
42. Lin YT, Tang CH, Chuang WJ, et al. Inhibition of adipogenesis by RGD-dependent disintegrin. Biochem Pharmacol 2005;70:1469-1478.
43. Kubota S, Takigawa M. CCN family proteins and angiogenesis: from embryo to adulthood. Angiogenesis 2007;10:1-11. (Pubitemid 46356220)
44. Cicha I, Garlichs CD, Daniel WG, et al. Activated human platelets release connective tissue growth factor. Thromb Haemost 2004;91:636-847.
45. Sisco M, Kryger ZB, O'Shaughnessy KD, et al. Antisense inhibition of connective tissue growth factor (CTGF/CCN2) mRNA limits hypertrophic scarring without affecting wound healing in vivo. Wound Rep Reg 2008;16:661-673.
46. Hall-Glenn F, De Young RA, Huang B. CCN2/Connective tissue growth factor is essential for pericyte adhesion and endothelial basement membrane formation during angiogenesis. PLoS One 2011;7:e30562.
47. Jedsaydayanmata A, Lau LF, Chen CC, et al. Activation-dependent adhesion of human platelets to Cyr61 and Fisp12/mouse connective tissue growth factor is mediated through integrin alpha(IIb)beta(3). J Biol Chem 1999;274:24321-24327.
48. Schober JM, Chen N, Grzeszkiewicz TM, et al. Identification of integrin aMb2 as an adhesion receptor on peripheral blood monocytes for Cyr61 (CCN1) and connective tissue growth factor (CCN2): immediate-early gene products expressed in atherosclerotic lesions. Blood 2002;99:4457-4465. (Pubitemid 34627215)