Reducing CTGF/CCN2 slows down mdx muscle dystrophy and improves cell therapy

Human Molecular Genetics

Volumn 22, Issue 24, 2013, Pages 4938-4951

  Morales, Maria Gabriela ^a   Gutierrez, Jaime ^a   Cabello Verrugio, Claudio ^b   Cabrera, Daniel ^a   Lipson, Kenneth E ^c   Goldschmeding, Roel ^d   Brandan, Enrique ^a  

^a PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^b UNIVERSIDAD ANDRÉS BELLO   (Chile)

^c FIBROGEN INC   (United States)

^d UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CONNECTIVE TISSUE GROWTH FACTOR; DYSTROPHIN; FG 3019; IMMUNOGLOBULIN G; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL THERAPY; CELL TRANSPLANTATION; CONTROLLED STUDY; DISEASE COURSE; DISEASE SEVERITY; DUCHENNE MUSCULAR DYSTROPHY; ENDURANCE TRAINING; FEMALE; GASTROCNEMIUS MUSCLE; GENE DELETION; HEMIZYGOTE; MOUSE; MUSCLE INJURY; MUSCLE STRENGTH; MUSCULAR DYSTROPHY; MYOFIBROSIS; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; SKELETAL MUSCLE SATELLITE CELL; X CHROMOSOME LINKED MUSCULAR DYSTROPHIC MOUSE;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIBODIES, NEUTRALIZING; APOPTOSIS; CELL- AND TISSUE-BASED THERAPY; CONNECTIVE TISSUE GROWTH FACTOR; DISEASE MODELS, ANIMAL; EXTRACELLULAR MATRIX; FIBROSIS; GENOTYPE; GRAFT SURVIVAL; MICE; MICE, INBRED MDX; MICE, KNOCKOUT; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; MUSCLE STRENGTH; MUSCLE, SKELETAL; MUSCULAR DYSTROPHY, DUCHENNE; P38 MITOGEN-ACTIVATED PROTEIN KINASES; SIGNAL TRANSDUCTION; SMAD PROTEINS; STEM CELL TRANSPLANTATION; TRANSFORMING GROWTH FACTOR BETA1;

EID: 84888186233     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddt352     Document Type: Article

References (94)

1. Liu, S., Shi-wen, X., Abraham, D.J. and Leask, A. (2011) CCN2 is required for bleomycin-induced skin fibrosis in mice. Arthritis Rheum., 63, 239-246.
2. Brigstock, D.R. (1999) The connective tissue growth factor/cysteine-rich 61/nephroblastoma overexpressed (CCN) family. Endocr. Rev., 20, 189-206.
3. Leask, A. and Abraham, D.J. (2006) All in the CCN family: essential matricellular signaling modulators emerge from the bunker. J. Cell. Sci., 119, 4803-4810.
4. Igarashi, A., Nashiro, K., Kikuchi, K., Sato, S., Ihn, H., Fujimoto, M., Grotendorst, G.R. and Takehara, K. (1996) Connective tissue growth factor gene expression in tissue sections from localized scleroderma, keloid, and other fibrotic skin disorders. J. Invest. Dermatol., 106, 729-733.
5. Oemar, B.S., Werner, A., Garnier, J.M., Do, D.D., Godoy, N., Nauck, M., Marz, W., Rupp, J., Pech, M. and Luscher, T.F. (1997) Human connective tissue growth factor is expressed in advanced atherosclerotic lesions. Circulation, 95, 831-839.
6. Lasky, J.A., Ortiz, L.A., Tonthat, B., Hoyle, G.W., Corti, M., Athas, G., Lungarella, G., Brody, A. and Friedman, M. (1998) Connective tissue growth factor mRNA expression is upregulated in bleomycin-induced lung fibrosis. Am. J. Physiol., 275, L365-L371.
7. Ito, Y., Aten, J., Bende, R.J., Oemar, B.S., Rabelink, T.J., Weening, J.J. and Goldschmeding, R. (1998) Expression of connective tissue growth factor in human renal fibrosis. Kidney Int., 53, 853-861.
8. di Mola, F.F., Friess, H., Martignoni, M.E., Di Sebastiano, P., Zimmermann, A., Innocenti, P., Graber, H., Gold, L.I., Korc, M. and Buchler, M.W. (1999) Connective tissue growth factor is a regulator for fibrosis in human chronic pancreatitis. Ann. Surg., 230, 63-71.
9. Paradis, V., Dargere, D., Vidaud, M., De Gouville, A.C., Huet, S., Martinez, V., Gauthier, J.M., Ba, N., Sobesky, R., Ratziu, V. et al. (1999) Expression of connective tissue growth factor in experimental rat and human liver fibrosis. Hepatology, 30, 968-976.
10. Fadic, R., Mezzano, V., Alvarez, K., Cabrera, D., Holmgren, J. and Brandan, E. (2006) Increase in decorin and biglycan in Duchenne muscular dystrophy: role of fibroblasts as cell source of these proteoglycans in the disease. J. Cell Mol. Med., 10, 758-769.
11. Porter, J.D., Merriam, A.P., Leahy, P., Gong, B., Feuerman, J., Cheng, G. and Khanna, S. (2004) Temporal gene expression profiling of dystrophin-deficient (mdx) mouse diaphragm identifies conserved and muscle group-specific mechanisms in the pathogenesis of muscular dystrophy. Hum. Mol. Genet., 13, 257-269.
12. Reed, P. and Bloch, R.J. (2005) Postnatal changes in sarcolemmal organization in the mdx mouse. Neuromuscul. Disord., 15, 552-561.
13. Bernasconi, P., Di Blasi, C., Mora, M., Morandi, L., Galbiati, S., Confalonieri, P., Cornelio, F. and Mantegazza, R. (1999) Transforming growth factor-beta1 and fibrosis in congenital muscular dystrophies. Neuromuscul. Disord, 9, 28-33.
14. Hartel, J.V., Granchelli, J.A., Hudecki, M.S., Pollina, C.M. and Gosselin, L.E. (2001) Impact of prednisone on TGF-beta1 and collagen in diaphragm muscle from mdx mice. Muscle Nerve, 24, 428-432.
15. Sun, G., Haginoya, K., Wu, Y., Chiba, Y., Nakanishi, T., Onuma, A., Sato, Y., Takigawa, M., Iinuma, K. and Tsuchiya, S. (2008) Connective tissue growth factor is overexpressed in muscles of human muscular dystrophy. J. Neurol. Sci., 267, 48-56.
16. Passerini, L., Bernasconi, P., Baggi, F., Confalonieri, P., Cozzi, F., Cornelio, F. and Mantegazza, R. (2002) Fibrogenic cytokines and extent of fibrosis in muscle of dogs with X-linked golden retriever muscular dystrophy. Neuromuscul. Disord, 12, 828-835.
17. Porter, J.D., Merriam, A.P., Leahy, P., Gong, B. and Khanna, S. (2003) Dissection of temporal gene expression signatures of affected and spared muscle groups in dystrophin-deficient (mdx) mice. Hum. Mol. Genet., 12, 1813-1821.
18. Acuña, M.J., Vio, C.P., Santos, R.A., Cabello-Verrugio, C. and Brandan, E. (2012) Angiotensin 1-7, a novel agent that reduces fibrosis and improves strength in dystrophic skeletal muscle. New Directions in Biology and Disease of Skeletal Muscle Conference, New Orleans, Louisiana, USA.
19. Vial, C., Zuniga, L.M., Cabello-Verrugio, C., Canon, P., Fadic, R. and Brandan, E. (2008) Skeletal muscle cells express the profibrotic cytokine connective tissue growth factor (CTGF/CCN2), which induces their dedifferentiation. J. Cell Physiol., 215, 410-421.
20. Morales, G., Cabello-Verrugio, C., Cabrera, D., Goldschmeding, R. and Brandan, E. (2011) CTGF/CCN-2 overexpression can directly induce features of skeletal muscle dystrophy. J. Pathol., 225, 490-501.
21. Partridge, T.A., Morgan, J.E., Coulton, G.R., Hoffman, E.P. and Kunkel, L.M. (1989) Conversion of mdx myofibres from dystrophin-negative to-positive by injection of normal myoblasts. Nature, 337, 176-179.
22. Miller, R.G., Sharma, K.R., Pavlath, G.K., Gussoni, E., Mynhier, M., Lanctot, A.M., Greco, C.M., Steinman, L. and Blau, H.M. (1997) Myoblast implantation in Duchenne muscular dystrophy: the San Francisco study. Muscle Nerve, 20, 469-478.
23. Skuk, D., Goulet, M., Roy, B., Chapdelaine, P., Bouchard, J.P., Roy, R., Dugre, F.J., Sylvain, M., Lachance, J.G., Deschenes, L. et al. (2006) Dystrophin expression in muscles of duchenne muscular dystrophy patients after high-density injections of normal myogenic cells. J. Neuropathol. Exp. Neurol., 65, 371-386.
24. Gargioli, C., Coletta, M.,DeGrandis, F., Cannata, S.M. and Cossu, G. (2008) PlGF-MMP-9-expressing cells restore microcirculation and efficacy of cell therapy in aged dystrophic muscle. Nat. Med., 14, 973-978.
25. Li, G., Xie, Q., Shi, Y., Li, D., Zhang, M., Jiang, S., Zhou, H., Lu, H. and Jin, Y. (2006) Inhibition of connective tissue growth factor by siRNA prevents liver fibrosis in rats. J. Gene Med., 8, 889-900.
26. Guha, M., Xu, Z.G., Tung, D., Lanting, L. and Natarajan, R. (2007) Specific down-regulation of connective tissue growth factor attenuates progression of nephropathy in mouse models of type 1 and type 2 diabetes. FASEB J, 21, 3355-3368.
27. Vial, C., Gutiérrez, J., Santander, C., Cabrera, D. and Brandan, E. (2011) Decorin interacts withCTGF/CCN2 throughLRR12inhibiting its biological activity. J. Biol. Chem., 286, 24242-24252.
28. Ivkovic, S., Yoon, B.S., Popoff, S.N., Safadi, F.F., Libuda, D.E., Stephenson, R.C., Daluiski, A. and Lyons, K.M. (2003) Connective tissue growth factor coordinates chondrogenesis and angiogenesis during skeletal development. Development, 130, 2779-2791.
29. Kuiper, E.J., Roestenberg, P., Ehlken, C., Lambert, V., van Treslong-de Groot, H.B., Lyons, K.M., Agostini, H.J., Rakic, J.M., Klaassen, I., Van Noorden, C.J. et al. (2007) Angiogenesis is not impaired in connective tissue growth factor (CTGF) knock-out mice. J. Histochem. Cytochem., 55, 1139-1147.
30. Kuiper, E.J., van Zijderveld, R., Roestenberg, P., Lyons, K.M., Goldschmeding, R., Klaassen, I., Van Noorden, C.J. and Schlingemann, R.O. (2008) Connective tissue growth factor is necessary for retinal capillary basal lamina thickening in diabetic mice. J. Histochem.Cytochem., 56, 785-792.
31. Ikawa, Y., Ng, P.S., Endo, K., Kondo,M., Chujo, S., Ishida, W., Shirasaki, F., Fujimoto, M. and Takehara, K. (2008) Neutralizing monoclonal antibody to human connective tissue growth factor ameliorates transforming growth factor-beta-induced mouse fibrosis. J. Cell Physiol., 216, 680-687.
32. Wang, Q., Usinger, W., Nichols, B., Gray, J., Xu, L., Seeley, T.W., Brenner, M., Guo, G., Zhang, W., Oliver, N. et al. (2011) Cooperative interaction of CTGF and TGF-beta in animal models of fibrotic disease. Fibrogenesis. Tissue Repair, 4, 4.
33. Adler, S.G., Schwartz, S., Williams, M.E., Arauz-Pacheco, C., Bolton, W.K., Lee, T., Li, D., Neff, T.B., Urquilla, P.R. and Sewell, K.L. (2010) Phase 1 study of anti-CTGF monoclonal antibody in patients with diabetes and microalbuminuria. Clin. J. Am. Soc. Nephrol, 5, 1420-1428.
34. Hamer, P.W., McGeachie, J.M., Davies, M.J. and Grounds, M.D. (2002) Evans blue dye as an in vivo marker of myofibre damage: optimising parameters for detecting initial myofibre membrane permeability. J. Anat, 200, 69-79.
35. Whalen, R.G., Butler-Browne, G.S., Bugaisky, L.B., Harris, J.B. and Herliocoviez, D. (1985) Myosin isozyme transitions in developing and regenerating rat muscle. Adv. Exp. Med. Biol., 182, 249-257.
36. Mann, C.J., Perdiguero, E., Kharraz, Y., Aguilar, S., Pessina, P., Serrano, A.L. and Munoz-Canoves, P. (2011) Aberrant repair and fibrosis development in skeletal muscle. Skeletal Muscle, 1, 21.
37. Aikawa, T., Gunn, J., Spong, S.M., Klaus, S.J. and Korc, M. (2006) Connective tissue growth factor-specific antibody attenuates tumor growth, metastasis, and angiogenesis in an orthotopic mouse model of pancreatic cancer. Mol. Cancer Ther., 5, 1108-1116.
38. Brigstock, D.R. (2009) Strategies for blocking the fibrogenic actions of connective tissue growth factor (CCN2): from pharmacological inhibition in vitro to targeted siRNA therapy in vivo. J. Cell Commun. Signal, 3, 5-18.
39. Lynch, G.S., Hinkle, R.T., Chamberlain, J.S., Brooks, S.V. and Faulkner, J.A. (2001) Force and power output of fast and slow skeletal muscles from mdx mice 6-28 months old. J. Physiol., 535, 591-600.
40. Connolly, A.M., Keeling, R.M., Mehta, S., Pestronk, A. and Sanes, J.R. (2001) Three mouse models of muscular dystrophy: the natural history of strength and fatigue in dystrophin, dystrophin/utrophin, and laminin alpha2-deficient mice. Neuromuscul. Disord., 11, 703-712.
41. De Luca, A., Pierno, S., Liantonio, A., Cetrone, M., Camerino, C., Fraysse, B., Mirabella, M., Servidei, S., Ruegg, U.T. and Conte Camerino, D. (2003) Enhanced dystrophic progression in mdx mice by exercise and beneficial effects of taurine and insulin-like growth factor-1. J Pharmacol. Exp. Ther., 304, 453-463.
42. De Luca, A., Pierno, S., Liantonio, A. and Conte Camerino, D. (2002) Pre-clinical trials in Duchenne dystrophy: what animal models can tell us about potential drug effectiveness. Neuromuscular Disord, 12 (Suppl. 1), S142.
43. Okabe, M., Ikawa, M., Kominami, K., Nakanishi, T. and Nishimune, Y. (1997) 'Green mice' as a source of ubiquitous green cells. FEBS Lett. 407, 313-S319.
44. Joshi, M., Keith Pittman, H., Haisch, C. and Verbanac, K. (2008) Real-time PCR to determine transgene copy number and to quantitate the biolocalization of adoptively transferred cells from EGFP-transgenic mice. BioTechniques, 45, 247-258.
45. Pellegrini, K.L. and Beilharz, M.W. (2011) The survival of myoblasts after intramuscular transplantation is improved when fewer cells are injected. Transplantation, 91, 522-526.
46. Crean, J.K., Lappin, D., Godson, C. and Brady, H.R. (2001) Connective tissue growth factor: an attractive therapeutic target in fibrotic renal disease. Expert Opin. Ther. Targets, 5, 519-530.
47. Shi-Wen, X., Leask, A. and Abraham, D. (2008) Regulation and function of connective tissue growth factor/CCN2 in tissue repair, scarring and fibrosis. Cytokine Growth Factor Rev., 19, 133-144.
48. Abdel-Salam, E., Abdel-Meguid, I. and Korraa, S.S. (2009) Markers of degeneration and regeneration in Duchenne muscular dystrophy. Acta Myol., 28, 94-100.
49. Honda, A., Abe, S., Hiroki, E., Honda, H., Iwanuma, O., Yanagisawa, N. and Ide, Y. (2007) Activation of caspase 3, 9, 12, and Bax in masseter muscle of mdx mice during necrosis. J. Muscle Res. Cell Motil., 28, 243-247.
50. Bernardi, P. (1999) Mitochondria in muscle cell death. Ital. J. Neurol. Sci., 20, 395-400.
51. Enwere, E.K., Boudreault, L., Holbrook, J., Timusk, K., Earl, N., LaCasse, E., Renaud, J.M. and Korneluk, R.G. (2013) Loss of cIAP1 attenuates soleus muscle pathology and improves diaphragm function in mdx mice. Hum. Mol. Genet., 22, 867-878.
52. Acharyya, S., Villalta, S.A., Bakkar, N., Bupha-Intr, T., Janssen, P.M., Carathers, M., Li, Z.W., Beg, A.A., Ghosh, S., Sahenk, Z. et al. (2007) Interplay of IKK/NF-kappaB signaling in macrophages and myofibers promotes muscle degeneration in Duchenne muscular dystrophy. J. Clin. Invest., 117, 889-901.
53. Tang, Y., Reay, D.P., Salay, M.N., Mi, M.Y., Clemens, P.R., Guttridge, D.C., Robbins, P.D., Huard, J. and Wang, B. (2010) Inhibition of the IKK/ NF-kappaB pathway byAAVgene transfer improves muscle regeneration in older mdx mice. Gene Ther., 17, 1476-1483.
54. Kular, L., Rivat, C., Lelongt, B., Calmel, C., Laurent, M., Pohl, M., Kitabgi, P., Melik-Parsadaniantz, S. and Martinerie, C. (2012) NOV/CCN3 attenuates inflammatory pain through regulation of matrix metalloproteinases-2 and-9. J. Neuroinflammation, 9, 36.
55. Wang, X., McLennan, S.V., Allen, T.J. and Twigg, S.M. (2010) Regulation of pro-inflammatory and pro-fibrotic factors by CCN2/CTGF in H9c2 cardiomyocytes. J. Cell Commun. Signal, 4, 15-23.
56. Wu, S.H., Wu, X.H., Lu, C., Dong, L., Zhou, G.P. and Chen, Z.Q. (2006) Lipoxin A4 inhibits connective tissue growth factor-induced production of chemokines in rat mesangial cells. Kidney Int., 69, 248-256.
57. Sanchez-Lopez, E., Rodrigues Diez, R., Rodriguez Vita, J., Rayego Mateos, S., Rodrigues Diez, R.R., Rodriguez Garcia, E., Lavoz Barria, C., Mezzano, S., Egido, J., Ortiz, A. et al. (2009) Connective tissue growth factor (CTGF): a key factor in the onset and progression of kidney damage. Nefrologia, 29, 382-391.
58. Nethery, D., Callahan, L.A., Stofan, D., Mattera, R., DiMarco, A. and Supinski, G. (2000) PLA(2) dependence of diaphragm mitochondrial formation of reactive oxygen species. J. Appl. Physiol, 89, 72-80.
59. Rando, T.A. (2002) Oxidative stress and the pathogenesis of muscular dystrophies. Am. J. Phys. Med. Rehabil., 81, S175-S186.
60. Whitehead, N.P., Yeung, E.W. and Allen, D.G. (2006) Muscle damage in mdx (dystrophic) mice: role of calcium and reactive oxygen species. Clin. Exp. Pharmacol. Physiol., 33, 657-662.
61. Tidball, J.G. and Wehling-Henricks, M. (2007) The role of free radicals in the pathophysiology of muscular dystrophy. J. Appl. Physiol., 102, 1677-1686.
62. Whitehead, N.P., Pham, C., Gervasio, O.L. and Allen, D.G. (2008) N-Acetylcysteine ameliorates skeletal muscle pathophysiology in mdx mice. J. Physiol., 586, 2003-2014.
63. Chen, C.C., Young, J.L., Monzon, R.I., Chen, N., Todorovic, V. and Lau, L.F. (2007) Cytotoxicity of TNFalpha is regulated by integrin-mediated matrix signaling. EMBO J., 26, 1257-1267.
64. Chen, C.C. and Lau, L.F. (2010) Deadly liaisons: fatal attraction between CCN matricellular proteins and the tumor necrosis factor family of cytokines. J. Cell Commun. Signal, 4, 63-69.
65. Capparelli, C., Whitaker-Menezes, D., Guido, C., Balliet, R., Pestell, T.G., Howell, A., Sneddon, S., Pestell, R.G., Martinez-Outschoorn, U., Lisanti, M.P. et al. (2012) CTGF Drives autophagy, glycolysis and senescence in cancer-associated fibroblasts via HIF1 activation, metabolically promoting tumor growth. Cell Cycle, 11, 2272-2284.
66. Cabello-Verrugio, C., Acuna, M.J., Morales, M.G., Becerra, A., Simon, F. and Brandan, E. (2011) Fibrotic response induced by angiotensin-II requires NAD(P)H oxidase-induced reactive oxygen species (ROS) in skeletal muscle cells. Biochem. Biophys. Res. Commun., 410, 665-670.
67. Cáceres, S., Cuellar, C., Casar, J.C., Garrido, J., Schaefer, L., Kresse, H. and Brandan, E. (2000) Synthesis of proteoglycans is augmented in dystrophic mdx mouse skeletal muscle. Eur. J. Cell Biol., 79, 173-181.
68. Alvarez, K., Fadic, R. and Brandan, E. (2002) Augmented synthesis and differential localization of heparan sulfate proteoglycans in Duchenne muscular dystrophy. J. Cell. Biochem, 85, 703-713.
69. Mezzano, V., Cabrera, D., Vial, C. and Brandan, E. (2007) Constitutively activated dystrophic muscle fibroblasts show a paradoxical response to TGF-beta and CTGF/CCN2. J. Cell Commun. Signal, 1, 205-217.
70. Willmann, R., Possekel, S., Dubach-Powell, J., Meier, T. and Ruegg, M.A. (2009) Mammalian animal models for Duchenne muscular dystrophy. Neuromuscul. Disord., 19, 241-249.
71. Leask, A. (2009) Signaling in fibrosis: targeting the TGF beta, endothelin-1 and CCN2 axis in scleroderma. Front. Biosci., 1, 115-122.
72. de Winter, P., Leoni, P. and Abraham, D. (2008) Connective tissue growth factor: structure-function relationships of a mosaic, multifunctional protein. Growth Factors, 26, 80-91.
73. Leask, A. and Abraham, D.J. (2004) TGF-beta signaling and the fibrotic response. FASEB J., 18, 816-827.
74. Mori, T., Kawara, S., Shinozaki, M., Hayashi, N., Kakinuma, T., Igarashi, A., Takigawa, M., Nakanishi, T. and Takehara, K. (1999) Role and interaction of connective tissue growth factor with transforming growth factor-beta in persistent fibrosis: a mouse fibrosis model. J. Cell. Physiol., 181, 153-159.
75. Holmes, A., Abraham, D.J., Sa, S., Shiwen, X., Black, C.M. and Leask, A. (2001) CTGF And SMADs, maintenance of scleroderma phenotype is independent of SMAD signaling. J. Biol. Chem., 276, 10594-10601.
76. Ng, C.M., Cheng, A., Myers, L.A., Martinez-Murillo, F., Jie, C., Bedja, D., Gabrielson, K.L., Hausladen, J.M., Mecham, R.P., Judge, D.P. et al. (2004) TGF-beta-dependent pathogenesis of mitral valve prolapse in a mouse model of Marfan syndrome. J. Clin. Invest., 114, 1586-1592.
77. Cohn, R.D., van Erp, C., Habashi, J.P., Soleimani, A.A., Klein, E.C., Lisi, M.T., Gamradt, M., ap Rhys, C.M., Holm, T.M., Loeys, B.L. et al. (2007) Angiotensin II type 1 receptor blockade attenuates TGF-beta-induced failure of muscle regeneration in multiple myopathic states. Nat. Med., 13, 204-210.
78. Fukushima, K., Badlani, N., Usas, A., Riano, F., Fu, F. and Huard, J. (2001) The use of an antifibrosis agent to improve muscle recovery after laceration. Am. J. Sports Med., 29, 394-402.
79. Li, Y., Li, J., Zhu, J., Sun, B., Branca, M., Tang, Y., Foster, W., Xiao, X. and Huard, J. (2007) Decorin gene transfer promotes muscle cell differentiation and muscle regeneration. Mol. Ther., 15, 1616-1622.
80. Melo, F., Carey, D.J. and Brandan, E. (1996) Extracellular matrix is required for skeletal muscle differentiation but not myogenin expression. J. Cell. Biochem., 62, 227-239.
81. Osses, N. and Brandan, E. (2002) ECM is required for skeletal muscle differentiation independently of muscle regulatory factor expression. Am. J. Physiol. Cell Physiol., 282, C383-C394.
82. Fadic, R. (2005) Cell surface and gene expression regulation molecules in dystrophinopathy: mdx versus Duchenne. Biol. Res, 38, 375-380.
83. Cohn, R.D., Mayer, U., Saher, G., Herrmann, R., van der Flier, A., Sonnenberg, A., Sorokin, L. and Voit, T. (1999) Secondary reduction of alpha7B integrin in laminin alpha2 deficient congenital muscular dystrophy supports an additional transmembrane link in skeletal muscle. J. Neurol. Sci., 163, 140-152.
84. Cornelison, D., Filla, M., Stanley, H., Rapraeger, A. and Olwin, B. (2001) Syndecan-3 and syndecan-4 specifically mark skeletal muscle satellite cells and are implicated in satellite cell maintenance and muscle regeneration. Dev. Biol., 239, 79-94.
85. Cornelison, D.D., Wilcox-Adelman, S.A., Goetinck, P.F., Rauvala, H., Rapraeger, A.C. and Olwin, B.B. (2004) Essential and separable roles for syndecan-3 and syndecan-4 in skeletal muscle development and regeneration. Genes Dev., 18, 2231-2236.
86. Casar, J.C., Cabello-Verrugio, C., Olguin, H., Aldunate, R., Inestrosa, N.C. and Brandan, E. (2004) Heparan sulfate proteoglycans are increased during skeletal muscle regeneration: requirement of syndecan-3 for successful fiber formation. J. Cell Sci., 117, 73-84.
87. Gutierrez, J. and Brandan, E. (2010) A novel mechanism of sequestering fibroblast growth factor 2 by glypican in lipid rafts, allowing skeletal muscle differentiation. Mol. Cell Biol., 30, 1634-1649.
88. Chen, C.C. and Lau, L.F. (2009) Functions and mechanisms of action of CCN matricellular proteins. Int. J. Biochem. Cell Biol., 41, 771-783.
89. Nishida, T., Kawaki, H., Baxter, R.M., Deyoung, R.A., Takigawa, M. and Lyons, K.M. (2007) CCN2 (connective tissue growth factor) is essential for extracellular matrix production and integrin signaling in chondrocytes. J. Cell Commun. Signal, 1, 45-58.
90. Chen, Y., Abraham, D.J., Shi-Wen, X., Pearson, J.D., Black, C.M., Lyons, K.M. and Leask, A. (2004) CCN2 (connective tissue growth factor) promotes fibroblast adhesion to fibronectin. Mol. Biol. Cell, 15, 5635-5646.
91. Gao, R. and Brigstock, D.R. (2004) Connective tissue growth factor (CCN2) induces adhesion of rat activated hepatic stellate cells by binding of its C-terminal domain to integrin alpha(v)beta(3) and heparan sulfate proteoglycan. J. Biol. Chem., 279, 8848-8855.
92. Collins, C.A. andZammit, P.S. (2009) Isolationand grafting of single muscle fibres. Methods Mol. Biol., 482, 319-330.
93. Kuang, S., Charge, S.B., Seale, P., Huh, M. and Rudnicki, M.A. (2006) Distinct roles for Pax7 and Pax3 in adult regenerative myogenesis. J. Cell Biol., 172, 103-113.
94. Cabello-Verrugio, C., Morales, M.G., Cabrera, D., Vio, C.P. and Brandan, E. (2012) Angiotensin II receptor type 1 blockade decreases CTGF/ CCN2-mediated damage and fibrosis in normal and dystrophic skeletal muscles. J. Cell Mol. Med., 16, 752-764.