Cellular and molecular mechanisms regulating fibrosis in skeletal muscle repair and disease

Current Topics in Developmental Biology

Volumn 96, Issue , 2011, Pages 167-201

  Serrano, Antonio L ^a   Mann, Christopher J ^a   Vidal, Berta ^a   Ardite, Esther ^a   Perdiguero, Eusebio ^a   Muñoz Cánoves, Pura ^a,b  

^a UNIVERSITAT POMPEU FABRA   (Spain)

^b INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

Author keywords

Extracellular Matrix; Fibrosis; Growth Factors; Inflammation; Regeneration; Skeletal Muscle

Indexed keywords

AGING; ANIMAL; BOOK; EXTRACELLULAR MATRIX; FIBROSIS; HUMAN; INJURY; METABOLISM; MUSCULAR DYSTROPHY; PATHOLOGY; PHYSIOLOGY; REGENERATION; SKELETAL MUSCLE;

AGING; ANIMALS; EXTRACELLULAR MATRIX; FIBROSIS; HUMANS; MUSCLE, SKELETAL; MUSCULAR DYSTROPHIES; REGENERATION;

EID: 79957439689     PISSN: 00702153     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-385940-2.00007-3     Document Type: Book

References (104)

1. Alexakis C., Partridge T., Bou-Gharios G. Implication of the satellite cell in dystrophic muscle fibrosis: A self-perpetuating mechanism of collagen overproduction. Am. J. Physiol. Cell Physiol. 2007, 293:C661-C669.
2. Andreetta F., Bernasconi P., Baggi F., Ferro P., Oliva L., Arnoldi E., Cornelio F., Mantegazza R., Confalonieri P. Immunomodulation of TGF-beta 1 in mdx mouse inhibits connective tissue proliferation in diaphragm but increases inflammatory response: Implications for antifibrotic therapy. J. Neuroimmunol. 2006, 175:77-86.
3. Angelini C. The role of corticosteroids in muscular dystrophy: A critical appraisal. Muscle Nerve 2007, 36:424-435.
4. Arnold L., Henry A., Poron F., Baba-Amer Y., van Rooijen N., Plonquet A., Gherardi R.K., Chazaud B. Inflammatory monocytes recruited after skeletal muscle injury switch into antiinflammatory macrophages to support myogenesis. J. Exp. Med. 2007, 204:1057-1069.
5. Bedair H.S., Karthikeyan T., Quintero A., Li Y., Huard J. Angiotensin II receptor blockade administered after injury improves muscle regeneration and decreases fibrosis in normal skeletal muscle. Am. J. Sports Med. 2008, 36:1548-1554.
6. Beggs M.L., Nagarajan R., Taylor-Jones J.M., Nolen G., Macnicol M., Peterson C.A. Alterations in the TGFbeta signaling pathway in myogenic progenitors with age. Aging Cell 2004, 3:353-361.
7. Bizario J.C., Cerri D.G., Rodrigues L.C., Oliveira G.L., Nomizo A., de Araujo D.D., Fukuhara P.S., Ribeiro J.C., de Castro F.A., Costa M.C. Imatinib mesylate ameliorates the dystrophic phenotype in exercised mdx mice. J. Neuroimmunol. 2009, 212:93-101.
8. Blake D.J., Weir A., Newey S.E., Davies K.E. Function and genetics of dystrophin and dystrophin-related proteins in muscle. Physiol. Rev. 2002, 82:291-329.
9. Bonner J.C. Regulation of PDGF and its receptors in fibrotic diseases. Cytokine Growth Factor Rev. 2004, 15:255-273.
10. Bonniaud P., Margetts P.J., Ask K., Flanders K., Gauldie J., Kolb M. TGF-beta and Smad3 signaling link inflammation to chronic fibrogenesis. J. Immunol. 2005, 175:5390-5395.
11. Brack A.S., Conboy M.J., Roy S., Lee M., Kuo C.J., Keller C., Rando T.A. Increased Wnt signaling during aging alters muscle stem cell fate and increases fibrosis. Science 2007, 317:807-810.
12. Brack A.S., Conboy I.M., Conboy M.J., Shen J., Rando T.A. A temporal switch from notch to Wnt signaling in muscle stem cells is necessary for normal adult myogenesis. Cell Stem Cell 2008, 2:50-59.
13. Brack A.S., Murphy-Seiler F., Hanifi J., Deka J., Eyckerman S., Keller C., Aguet M., Rando T.A. BCL9 is an essential component of canonical Wnt signaling that mediates the differentiation of myogenic progenitors during muscle regeneration. Dev. Biol. 2009, 335:93-105.
14. Brandan E., Cabello-Verrugio C., Vial C. Novel regulatory mechanisms for the proteoglycans decorin and biglycan during muscle formation and muscular dystrophy. Matrix Biol. 2008, 27:700-708.
15. Cai B., Spencer M.J., Nakamura G., Tseng-Ong L., Tidball J.G. Eosinophilia of dystrophin-deficient muscle is promoted by perforin-mediated cytotoxicity by T cell effectors. Am. J. Pathol. 2000, 156:1789-1796.
16. Carlson M.E., Hsu M., Conboy I.M. Imbalance between pSmad3 and Notch induces CDK inhibitors in old muscle stem cells. Nature 2008, 454:528-532.
17. Carlson M.E., Conboy M.J., Hsu M., Barchas L., Jeong J., Agrawal A., Mikels A.J., Agrawal S., Schaffer D.V., Conboy I.M. Relative roles of TGF-beta1 and Wnt in the systemic regulation and aging of satellite cell responses. Aging Cell 2009, 8:676-689.
18. Casar J.C., McKechnie B.A., Fallon J.R., Young M.F., Brandan E. Transient up-regulation of biglycan during skeletal muscle regeneration: Delayed fiber growth along with decorin increase in biglycan-deficient mice. Dev. Biol. 2004, 268:358-371.
19. Cencetti F., Bernacchioni C., Nincheri P., Donati C., Bruni P. Transforming growth factor-beta1 induces transdifferentiation of myoblasts into myofibroblasts via up-regulation of sphingosine kinase-1/S1P3 axis. Mol. Biol. Cell 2010, 21:1111-1124.
20. Chan Y.S., Li Y., Foster W., Horaguchi T., Somogyi G., Fu F.H., Huard J. Antifibrotic effects of suramin in injured skeletal muscle after laceration. J. Appl. Physiol. 2003, 95:771-780.
21. Chazaud B., Brigitte M., Yacoub-Youssef H., Arnold L., Gherardi R., Sonnet C., Lafuste P., Chretien F. Dual and beneficial roles of macrophages during skeletal muscle regeneration. Exerc. Sport Sci. Rev. 2009, 37:18-22.
22. Chen X., Li Y. Role of matrix metalloproteinases in skeletal muscle: Migration, differentiation, regeneration and fibrosis. Cell. Adh. Migr. 2009, 3:337-341.
23. Cohn R.D., Liang H.Y., Shetty R., Abraham T., Wagner K.R. Myostatin does not regulate cardiac hypertrophy or fibrosis. Neuromuscul. Disord. 2007, 17:290-296.
24. Cornelison D.D. Context matters: In vivo and in vitro influences on muscle satellite cell activity. J. Cell. Biochem. 2008, 105:663-669.
25. Desguerre I., Mayer M., Leturcq F., Barbet J.P., Gherardi R.K., Christov C. Endomysial fibrosis in Duchenne muscular dystrophy: A marker of poor outcome associated with macrophage alternative activation. J. Neuropathol. Exp. Neurol. 2009, 68:762-773.
26. Di Marco S., Mazroui R., Dallaire P., Chittur S., Tenenbaum S.A., Radzioch D., Marette A., Gallouzi I.E. NF-kappa B-mediated MyoD decay during muscle wasting requires nitric oxide synthase mRNA stabilization, HuR protein, and nitric oxide release. Mol. Cell. Biol. 2005, 25:6533-6545.
27. Durbeej M., Campbell K.P. Muscular dystrophies involving the dystrophin-glycoprotein complex: An overview of current mouse models. Curr. Opin. Genet. Dev. 2002, 12:349-361.
28. Emery A.E. The muscular dystrophies. Lancet 2002, 359:687-695.
29. Evangeliou A., Vasilaki K., Karagianni P., Nikolaidis N. Clinical applications of creatine supplementation on paediatrics. Curr. Pharm. Biotechnol. 2009, 10:683-690.
30. Farini A., Meregalli M., Belicchi M., Battistelli M., Parolini D., D'Antona G., Gavina M., Ottoboni L., Constantin G., Bottinelli R., Torrente Y. T and B lymphocyte depletion has a marked effect on the fibrosis of dystrophic skeletal muscles in the scid/mdx mouse. J. Pathol. 2007, 213:229-238.
31. Fibbi G., Barletta E., Dini G., Del Rosso A., Pucci M., Cerletti M., Del Rosso M. Cell invasion is affected by differential expression of the urokinase plasminogen activator/urokinase plasminogen activator receptor system in muscle satellite cells from normal and dystrophic patients. Lab. Invest. 2001, 81:27-39.
32. Fukushima K., Nakamura A., Ueda H., Yuasa K., Yoshida K., Takeda S., Ikeda S. Activation and localization of matrix metalloproteinase-2 and -9 in the skeletal muscle of the muscular dystrophy dog (CXMDJ). BMC Musculoskelet. Disord. 2007, 8:54.
33. Gargioli C., Coletta M., De Grandis F., Cannata S.M., Cossu G. PlGF-MMP-9-expressing cells restore microcirculation and efficacy of cell therapy in aged dystrophic muscle. Nat. Med. 2008, 14:973-978.
34. Glass D.J. Signaling pathways perturbing muscle mass. Curr. Opin. Clin. Nutr. Metab. Care 2010, 13:225-229.
35. Green D.R., Ferguson T., Zitvogel L., Kroemer G. Immunogenic and tolerogenic cell death. Nat. Rev. Immunol. 2009, 9:353-363.
36. Grounds M.D., Sorokin L., White J. Strength at the extracellular matrix-muscle interface. Scand. J. Med. Sci. Sports 2005, 15:381-391.
37. Haus J.M., Carrithers J.A., Trappe S.W., Trappe T.A. Collagen, cross-linking, and advanced glycation end products in aging human skeletal muscle. J. Appl. Physiol. 2007, 103:2068-2076.
38. Heydemann A., Ceco E., Lim J.E., Hadhazy M., Ryder P., Moran J.L., Beier D.R., Palmer A.A., McNally E.M. Latent TGF-beta-binding protein 4 modifies muscular dystrophy in mice. J. Clin. Invest. 2009, 119:3703-3712.
39. Hidestrand M., Richards-Malcolm S., Gurley C.M., Nolen G., Grimes B., Waterstrat A., Zant G.V., Peterson C.A. Sca-1-expressing nonmyogenic cells contribute to fibrosis in aged skeletal muscle. J. Gerontol. A Biol. Sci. Med. Sci. 2008, 63:566-579.
40. 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.
41. Huang P., Zhao X.S., Fields M., Ransohoff R.M., Zhou L. Imatinib attenuates skeletal muscle dystrophy in mdx mice. FASEB J. 2009, 23:2539-2548.
42. Huebner K.D., Jassal D.S., Halevy O., Pines M., Anderson J.E. Functional resolution of fibrosis in mdx mouse dystrophic heart and skeletal muscle by halofuginone. Am. J. Physiol. Heart Circ. Physiol. 2008, 294:H1550-H1561.
43. Joe A.W., Yi L., Natarajan A., Le Grand F., So L., Wang J., Rudnicki M.A., Rossi F.M. Muscle injury activates resident fibro/adipogenic progenitors that facilitate myogenesis. Nat. Cell Biol. 2010, 12:153-163.
44. Jorgensen L.H., Jensen C.H., Wewer U.M., Schroder H.D. Transgenic overexpression of ADAM12 suppresses muscle regeneration and aggravates dystrophy in aged mdx mice. Am. J. Pathol. 2007, 171:1599-1607.
45. Kaar J.L., Li Y., Blair H.C., Asche G., Koepsel R.R., Huard J., Russell A.J. Matrix metalloproteinase-1 treatment of muscle fibrosis. Acta Biomater. 2008, 4:1411-1420.
46. Kaariainen M., Jarvinen T., Jarvinen M., Rantanen J., Kalimo H. Relation between myofibers and connective tissue during muscle injury repair. Scand. J. Med. Sci. Sports 2000, 10:332-337.
47. Kafadar K.A., Yi L., Ahmad Y., So L., Rossi F., Pavlath G.K. Sca-1 expression is required for efficient remodeling of the extracellular matrix during skeletal muscle regeneration. Dev. Biol. 2009, 326:47-59.
48. Kherif S., Lafuma C., Dehaupas M., Lachkar S., Fournier J.-G., Verdiere-Sahuque M., Fardeau M., Alameddine H.S. Expression of matrix metalloproteinases 2 and 9 in regenerating skeletal muscle: A study in experimentally injured and mdx muscles. Dev. Biol. 1999, 205:158-170.
49. Kollias H.D., McDermott J.C. Transforming growth factor-beta and myostatin signaling in skeletal muscle. J. Appl. Physiol. 2008, 104:579-587.
50. Lahoute C., Sotiropoulos A., Favier M., Guillet-Deniau I., Charvet C., Ferry A., Butler-Browne G., Metzger D., Tuil D., Daegelen D. Premature aging in skeletal muscle lacking serum response factor. PLoS ONE 2008, 3:e3910.
51. Li Y., Foster W., Deasy B.M., Chan Y., Prisk V., Tang Y., Cummins J., Huard J. Transforming growth factor-beta1 induces the differentiation of myogenic cells into fibrotic cells in injured skeletal muscle: A key event in muscle fibrogenesis. Am. J. Pathol. 2004, 164:1007-1019.
52. Li Y., Fu F.H., Huard J. Cutting-edge muscle recovery: Using antifibrosis agents to improve healing. Phys. Sportsmed. 2005, 33:44-50.
53. Li Y., Li J., Zhu J., Sun B., Branca M., Tang Y., Foster W., Xiao X., Huard J. Decorin gene transfer promotes muscle cell differentiation and muscle regeneration. Mol. Ther. 2007, 15:1616-1622.
54. Li Z.B., Kollias H.D., Wagner K.R. Myostatin directly regulates skeletal muscle fibrosis. J. Biol. Chem. 2008, 283:19371-19378.
55. Li H., Mittal A., Makonchuk D.Y., Bhatnagar S., Kumar A. Matrix metalloproteinase-9 inhibition ameliorates pathogenesis and improves skeletal muscle regeneration in muscular dystrophy. Hum. Mol. Genet. 2009, 18:2584-2598.
56. Lluis F., Roma J., Suelves M., Parra M., Aniorte G., Gallardo E., Illa I., Rodriguez L., Hughes S.M., Carmeliet P., Roig M., Munoz-Canoves P. Urokinase-dependent plasminogen activation is required for efficient skeletal muscle regeneration in vivo. Blood 2001, 97:1703-1711.
57. Lluri G., Langlois G.D., McClellan B., Soloway P.D., Jaworski D.M. Tissue inhibitor of metalloproteinase-2 (TIMP-2) regulates neuromuscular junction development via a beta1 integrin-mediated mechanism. J. Neurobiol. 2006, 66:1365-1377.
58. Mantovani A., Sica A., Sozzani S., Allavena P., Vecchi A., Locati M. The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol. 2004, 25:677-686.
59. Mauro A. Satellite cells of skeletal fibers. J. Biophys. Biochem. Cytol. 1961, 9:493-495.
60. McCroskery S., Thomas M., Platt L., Hennebry A., Nishimura T., McLeay L., Sharma M., Kambadur R. Improved muscle healing through enhanced regeneration and reduced fibrosis in myostatin-null mice. J. Cell Sci. 2005, 118:3531-3541.
61. Morrison J., Lu Q.L., Pastoret C., Partridge T., Bou-Gharios G. T-cell-dependent fibrosis in the mdx dystrophic mouse. Lab. Invest. 2000, 80:881-891.
62. Morrison J., Palmer D.B., Cobbold S., Partridge T., Bou-Gharios G. Effects of T-lymphocyte depletion on muscle fibrosis in the mdx mouse. Am. J. Pathol. 2005, 166:1701-1710.
63. Muir L.A., Chamberlain J.S. Emerging strategies for cell and gene therapy of the muscular dystrophies. Expert Rev. Mol. Med. 2009, 11:e18.
64. Nagamine Y., Medcalf R.L., Munoz-Canoves P. Transcriptional and posttranscriptional regulation of the plasminogen activator system. Thromb. Haemost. 2005, 93:661-675.
65. Nahirney P.C., Dow P.R., Ovalle W.K. Quantitative morphology of mast cells in skeletal muscle of normal and genetically dystrophic mice. Anat. Rec. 1997, 247:341-349.
66. Ohtake Y., Tojo H., Seiki M. Multifunctional roles of MT1-MMP in myofiber formation and morphostatic maintenance of skeletal muscle. J. Cell Sci. 2006, 119:3822-3832.
67. Ono Y., Sensui H., Okutsu S., Nagatomi R. Notch2 negatively regulates myofibroblastic differentiation of myoblasts. J. Cell. Physiol. 2007, 210:358-369.
68. Pelosi L., Giacinti C., Nardis C., Borsellino G., Rizzuto E., Nicoletti C., Wannenes F., Battistini L., Rosenthal N., Molinaro M., Musaro A. Local expression of IGF-1 accelerates muscle regeneration by rapidly modulating inflammatory cytokines and chemokines. FASEB J. 2007, 21:1393-1402.
69. Pesce J.T., Ramalingam T.R., Mentink-Kane M.M., Wilson M.S., El Kasmi K.C., Smith A.M., Thompson R.W., Cheever A.W., Murray P.J., Wynn T.A. Arginase-1-expressing macrophages suppress Th2 cytokine-driven inflammation and fibrosis. PLoS Pathog. 2009, 5:e1000371.
70. Peterson J.M., Guttridge D.C. Skeletal muscle diseases, inflammation, and NF-kappaB signaling: Insights and opportunities for therapeutic intervention. Int. Rev. Immunol. 2008, 27:375-387.
71. Porter J.D., Khanna S., Kaminski H.J., Rao J.S., Merriam A.P., Richmonds C.R., Leahy P., Li J., Guo W., Andrade F.H. A chronic inflammatory response dominates the skeletal muscle molecular signature in dystrophin-deficient mdx mice. Hum. Mol. Genet. 2002, 11:263-272.
72. Radley H.G., Davies M.J., Grounds M.D. Reduced muscle necrosis and long-term benefits in dystrophic mdx mice after cV1q (blockade of TNF) treatment. Neuromuscul. Disord. 2008, 18:227-238.
73. Roffe S., Hagai Y., Pines M., Halevy O. Halofuginone inhibits Smad3 phosphorylation via the PI3K/Akt and MAPK/ERK pathways in muscle cells: Effect on myotube fusion. Exp. Cell Res. 2010, 316:1061-1069.
74. Ruffell D., Mourkioti F., Gambardella A., Kirstetter P., Lopez R.G., Rosenthal N., Nerlov C. A CREB-C/EBPbeta cascade induces M2 macrophage-specific gene expression and promotes muscle injury repair. Proc. Natl. Acad. Sci. USA 2009, 106:17475-17480.
75. Ryall J.G., Schertzer J.D., Lynch G.S. Cellular and molecular mechanisms underlying age-related skeletal muscle wasting and weakness. Biogerontology 2008, 9:213-228.
76. Segawa M., Fukada S., Yamamoto Y., Yahagi H., Kanematsu M., Sato M., Ito T., Uezumi A., Hayashi S., Miyagoe-Suzuki Y., Takeda S., Tsujikawa K., et al. Suppression of macrophage functions impairs skeletal muscle regeneration with severe fibrosis. Exp. Cell Res. 2008, 314:3232-3244.
77. Shi Y., Massague J. Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell 2003, 113:685-700.
78. Snijders T., Verdijk L.B., van Loon L.J. The impact of sarcopenia and exercise training on skeletal muscle satellite cells. Ageing Res. Rev. 2009, 8:328-338.
79. Spencer M.J., Montecino-Rodriguez E., Dorshkind K., Tidball J.G. Helper (CD4(+)) and cytotoxic (CD8(+)) T cells promote the pathology of dystrophin-deficient muscle. Clin. Immunol. 2001, 98:235-243.
80. Suelves M., Lopez-Alemany R., Lluis F., Aniorte G., Serrano E., Parra M., Carmeliet P., Munoz-Canoves P. Plasmin activity is required for myogenesis in vitro and skeletal muscle regeneration in vivo. Blood 2002, 99:2835-2844.
81. Suelves M., Vidal B., Ruiz V., Baeza-Raja B., Diaz-Ramos A., Cuartas I., Lluis F., Parra M., Jardi M., Lopez-Alemany R., Serrano A.L., Munoz-Canoves P. The plasminogen activation system in skeletal muscle regeneration: Antagonistic roles of urokinase-type plasminogen activator (uPA) and its inhibitor (PAI-1). Front. Biosci. 2005, 10:2978-2985.
82. Suelves M., Vidal B., Serrano A.L., Tjwa M., Roma J., Lopez-Alemany R., Luttun A., de Lagran M.M., Diaz-Ramos A., Jardi M., Roig M., Dierssen M., et al. uPA deficiency exacerbates muscular dystrophy in MDX mice. J. Cell Biol. 2007, 178:1039-1051.
83. Sun G., Haginoya K., Wu Y., Chiba Y., Nakanishi T., Onuma A., Sato Y., Takigawa M., Iinuma K., Tsuchiya S. Connective tissue growth factor is overexpressed in muscles of human muscular dystrophy. J. Neurol. Sci. 2008, 267:48-56.
84. Tidball J.G. Inflammatory processes in muscle injury and repair. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2005, 288:R345-R353.
85. Tidball J.G., Villalta S.A. Regulatory interactions between muscle and the immune system during muscle regeneration. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2010, 298:R1173-R1187.
86. Trensz F., Haroun S., Cloutier A., Richter M.V., Grenier G. A muscle resident cell population promotes fibrosis in hindlimb skeletal muscles of mdx mice through the wnt canonical pathway. Am. J. Physiol. Cell Physiol. 2010, 299(5):C939-C947.
87. Uezumi A., Fukada S., Yamamoto N., Takeda S., Tsuchida K. Mesenchymal progenitors distinct from satellite cells contribute to ectopic fat cell formation in skeletal muscle. Nat. Cell Biol. 2010, 12:143-152.
88. Vetrone S.A., Montecino-Rodriguez E., Kudryashova E., Kramerova I., Hoffman E.P., Liu S.D., Miceli M.C., Spencer M.J. Osteopontin promotes fibrosis in dystrophic mouse muscle by modulating immune cell subsets and intramuscular TGF-beta. J. Clin. Invest. 2009, 119:1583-1594.
89. Vial C., Zuniga L.M., Cabello-Verrugio C., Canon P., Fadic R., Brandan E. Skeletal muscle cells express the profibrotic cytokine connective tissue growth factor (CTGF/CCN2), which induces their dedifferentiation. J. Cell. Physiol. 2008, 215:410-421.
90. Vidal B., Serrano A.L., Tjwa M., Suelves M., Ardite E., De Mori R., Baeza-Raja B., Martinez de Lagran M., Lafuste P., Ruiz-Bonilla V., Jardi M., Gherardi R., et al. Fibrinogen drives dystrophic muscle fibrosis via a TGFbeta/alternative macrophage activation pathway. Genes Dev. 2008, 22:1747-1752.
91. Villalta S.A., Nguyen H.X., Deng B., Gotoh T., Tidball J.G. Shifts in macrophage phenotypes and macrophage competition for arginine metabolism affect the severity of muscle pathology in muscular dystrophy. Hum. Mol. Genet. 2009, 18:482-496.
92. Visse R., Nagase H. Matrix metalloproteinases and tissue inhibitors of metalloproteinases: Structure, function, and biochemistry. Circ. Res. 2003, 92:827-839.
93. Wagner K.R., McPherron A.C., Winik N., Lee S.J. Loss of myostatin attenuates severity of muscular dystrophy in mdx mice. Ann. Neurol. 2002, 52:832-836.
94. Wehling M., Spencer M.J., Tidball J.G. A nitric oxide synthase transgene ameliorates muscular dystrophy in mdx mice. J. Cell Biol. 2001, 155:123-131.
95. Wehling-Henricks M., Sokolow S., Lee J.J., Myung K.H., Villalta S.A., Tidball J.G. Major basic protein-1 promotes fibrosis of dystrophic muscle and attenuates the cellular immune response in muscular dystrophy. Hum. Mol. Genet. 2008, 17:2280-2292.
96. Wu N., Jansen E.D., Davidson J.M. Comparison of mouse matrix metalloproteinase 13 expression in free-electron laser and scalpel incisions during wound healing. J. Invest. Dermatol. 2003, 121:926-932.
97. Wynn T.A. Fibrotic disease and the T(H)1/T(H)2 paradigm. Nat. Rev. Immunol. 2004, 4:583-594.
98. Wynn T.A. Cellular and molecular mechanisms of fibrosis. J. Pathol. 2008, 214:199-210.
99. Wynn T.A., Barron L. Macrophages: Master regulators of inflammation and fibrosis. Semin. Liver Dis. 2010, 30:245-257.
100. Yogo Y., Fujishima S., Inoue T., Saito F., Shiomi T., Yamaguchi K., Ishizaka A. Macrophage derived chemokine (CCL22), thymus and activation-regulated chemokine (CCL17), and CCR4 in idiopathic pulmonary fibrosis. Respir. Res. 2009, 10:80.
101. Zanotti S., Negri T., Cappelletti C., Bernasconi P., Canioni E., Di Blasi C., Pegoraro E., Angelini C., Ciscato P., Prelle A., Mantegazza R., Morandi L., et al. Decorin and biglycan expression is differentially altered in several muscular dystrophies. Brain 2005, 128:2546-2555.
102. Zanotti S., Saredi S., Ruggieri A., Fabbri M., Blasevich F., Romaggi S., Morandi L., Mora M. Altered extracellular matrix transcript expression and protein modulation in primary Duchenne muscular dystrophy myotubes. Matrix Biol. 2007, 26:615-624.
103. Zhou L., Porter J.D., Cheng G., Gong B., Hatala D.A., Merriam A.P., Zhou X., Rafael J.A., Kaminski H.J. Temporal and spatial mRNA expression patterns of TGF-beta1, 2, 3 and TbetaRI, II, III in skeletal muscles of mdx mice. Neuromuscul. Disord. 2006, 16:32-38.
104. Zhu J., Li Y., Shen W., Qiao C., Ambrosio F., Lavasani M., Nozaki M., Branca M.F., Huard J. Relationships between transforming growth factor-beta1, myostatin, and decorin: Implications for skeletal muscle fibrosis. J. Biol. Chem. 2007, 282:25852-25863.