Conditional expression of TGF-β1 in skeletal muscles causes endomysial fibrosis and myofibers atrophy

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Narola, Jigna ^a   Pandey, Sachchida Nand ^a   Glick, Adam ^b   Chen, Yi Wen ^a,c  

^a CHILDREN'S NATIONAL MEDICAL CENTER   (United States)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

^c GEORGE WASHINGTON UNIVERSITY SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSFORMING GROWTH FACTOR BETA1;

ANIMAL; ANTIBODY SPECIFICITY; FEMALE; FIBROSIS; GENE EXPRESSION; GENETICS; MALE; METABOLISM; MOUSE; MUSCLE ATROPHY; MUSCLE WEAKNESS; PATHOLOGY; PHENOTYPE; SKELETAL MUSCLE; TRANSGENE;

ANIMALS; FEMALE; FIBROSIS; GENE EXPRESSION; MALE; MICE; MUSCLE WEAKNESS; MUSCLE, SKELETAL; MUSCULAR ATROPHY; ORGAN SPECIFICITY; PHENOTYPE; TRANSFORMING GROWTH FACTOR BETA1; TRANSGENES;

EID: 84893650310     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0079356     Document Type: Article

References (52)

1. Massague J (1990) The transforming growth factor-beta family. Annu Rev Cell Biol 6: 597-641.
2. Kim BC, Kim HT, Park SH, Cha JS, Yufit T, et al. (2003) Fibroblasts from chronic wounds show altered TGF-beta-signaling and decreased TGF-beta Type II receptor expression. J Cell Physiol 195: 331-336. (Pubitemid 36529861)
3. Shull MM, Ormsby I, Kier AB, Pawlowski S, Diebold RJ, et al. (1992) Targeted disruption of the mouse transforming growth factor-beta 1 gene results in multifocal inflammatory disease. Nature 359: 693-699.
4. Bartram U, Speer CP (2004) The role of transforming growth factor beta in lung development and disease. Chest 125: 754-765. (Pubitemid 38223659)
5. Bernasconi P, Di Blasi C, Mora M, Morandi L, Galbiati S, et al. (1999) Transforming growth factor-beta1 and fibrosis in congenital muscular dystrophies. Neuromuscul Disord 9: 28-33. (Pubitemid 29079470)
6. Dale PD, Sherratt JA, Maini PK (1997) Role of fibroblast migration in collagen fiber formation during fetal and adult dermal wound healing. Bull Math Biol 59: 1077-1100. (Pubitemid 28381415)
7. Miyazawa K, Kikuchi S, Fukuyama J, Hamano S, Ujiie A (1995) Inhibition of PDGF- and TGF-beta 1-induced collagen synthesis, migration and proliferation by tranilast in vascular smooth muscle cells from spontaneously hypertensive rats. Atherosclerosis 118: 213-221. (Pubitemid 26011483)
8. Mizuno S, Nakamura T (2004) Suppressions of chronic glomerular injuries and TGF-beta 1 production by HGF in attenuation of murine diabetic nephropathy. Am J Physiol Renal Physiol 286: F134-143. (Pubitemid 38045051)
9. Rout UK, Saed GM, Diamond MP (2002) Transforming growth factor-beta1 modulates expression of adhesion and cytoskeletal proteins in human peritoneal fibroblasts. Fertil Steril 78: 154-161. (Pubitemid 34722686)
10. Wells RG (2000) Fibrogenesis. V. TGF-beta signaling pathways. Am J Physiol Gastrointest Liver Physiol 279: G845-850.
11. Grainger DJ, Kemp PR, Witchell CM, Weissberg PL, Metcalfe JC (1994) Transforming growth factor beta decreases the rate of proliferation of rat vascular smooth muscle cells by extending the G2 phase of the cell cycle and delays the rise in cyclic AMP before entry into M phase. Biochem J 299 (Pt 1): 227-235. (Pubitemid 24106314)
12. Allen RE, Boxhorn LK (1987) Inhibition of skeletal muscle satellite cell differentiation by transforming growth factor-beta. J Cell Physiol 133: 567-572.
13. Cusella-De Angelis MG, Molinari S, Le Donne A, Coletta M, Vivarelli E, et al. (1994) Differential response of embryonic and fetal myoblasts to TGF beta: a possible regulatory mechanism of skeletal muscle histogenesis. Development 120: 925-933. (Pubitemid 24111556)
14. Hathaway MR, Pampusch MS, Hembree JR, Dayton WR (1994) Transforming growth factor beta-1 facilitates establishing clonal populations of ovine muscle satellite cells. J Anim Sci 72: 2001-2007.
15. Lefaucheur JP, Sebille A (1995) Muscle regeneration following injury can be modified in vivo by immune neutralization of basic fibroblast growth factor, transforming growth factor beta 1 or insulin-like growth factor I. J Neuroimmunol 57: 85-91.
16. Li Y, Foster W, Deasy BM, Chan Y, Prisk V, et al. (2004) 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 164: 1007-1019. (Pubitemid 38235482)
17. Schabort EJ, van der Merwe M, Loos B, Moore FP, Niesler CU (2009) TGFbeta's delay skeletal muscle progenitor cell differentiation in an isoform-independent manner. Exp Cell Res 315: 373-384.
18. Zhu S, Goldschmidt-Clermont PJ, Dong C (2004) Transforming growth factor-beta-induced inhibition of myogenesis is mediated through Smad pathway and is modulated by microtubule dynamic stability. Circ Res 94: 617-625. (Pubitemid 38387744)
19. Annes JP, Munger JS, Rifkin DB (2003) Making sense of latent TGFbeta activation. J Cell Sci 116: 217-224. (Pubitemid 36163863)
20. Heydemann A, Ceco E, Lim JE, Hadhazy M, Ryder P, et al. (2009) Latent TGF-beta-binding protein 4 modifies muscular dystrophy in mice. J Clin Invest 119: 3703-3712.
21. Taipale J, Saharinen J, Hedman K, Keski-Oja J (1996) Latent transforming growth factor-beta 1 and its binding protein are components of extracellular matrix microfibrils. J Histochem Cytochem 44: 875-889. (Pubitemid 26266744)
22. Ishitobi M, Haginoya K, Zhao Y, Ohnuma A, Minato J, et al. (2000) Elevated plasma levels of transforming growth factor beta1 in patients with muscular dystrophy. Neuroreport 11: 4033-4035. (Pubitemid 32038799)
23. Chen YW, Nagaraju K, Bakay M, McIntyre O, Rawat R, et al. (2005) Early onset of inflammation and later involvement of TGFbeta in Duchenne muscular dystrophy. Neurology 65: 826-834. (Pubitemid 41362124)
24. Andreetta F, Bernasconi P, Baggi F, Ferro P, Oliva L, et al. (2006) Immunomodulation of TGF-beta 1 in mdx mouse inhibits connective tissue proliferation in diaphragm but increases inflammatory response: implications for antifibrotic therapy. J Neuroimmunol 175: 77-86.
25. Nelson CA, Hunter RB, Quigley LA, Girgenrath S, Weber WD, et al. (2011) Inhibiting TGF-beta activity improves respiratory function in mdx mice. Am J Pathol 178: 2611-2621.
26. Briguet A, Courdier-Fruh I, Foster M, Meier T, Magyar JP (2004) Histological parameters for the quantitative assessment of muscular dystrophy in the mdx-mouse. Neuromuscul Disord 14: 675-682. (Pubitemid 39194668)
27. Bernasconi P, Torchiana E, Confalonieri P, Brugnoni R, Barresi R, et al. (1995) Expression of transforming growth factor-beta 1 in dystrophic patient muscles correlates with fibrosis. Pathogenetic role of a fibrogenic cytokine. J Clin Invest 96: 1137-1144.
28. Katsuno M, Adachi H, Minamiyama M, Waza M, Doi H, et al. (2010) Disrupted transforming growth factor-beta signaling in spinal and bulbar muscular atrophy. J Neurosci 30: 5702-5712.
29. Millino C, Fanin M, Vettori A, Laveder P, Mostacciuolo ML, et al. (2009) Different atrophy-hypertrophy transcription pathways in muscles affected by severe and mild spinal muscular atrophy. BMC Med 7: 14.
30. Serrano AL, Munoz-Canoves P (2010) Regulation and dysregulation of fibrosis in skeletal muscle. Exp Cell Res 316: 3050-3058.
31. Rodriguez-Barbero A, Obreo J, Yuste L, Montero JC, Rodriguez-Pena A, et al. (2002) Transforming growth factor-beta1 induces collagen synthesis and accumulation via p38 mitogen-activated protein kinase (MAPK) pathway in cultured L(6)E(9) myoblasts. FEBS Lett 513: 282-288. (Pubitemid 34251279)
32. Liu D, Black BL, Derynck R (2001) TGF-beta inhibits muscle differentiation through functional repression of myogenic transcription factors by Smad3. Genes Dev 15: 2950-2966. (Pubitemid 33078946)
33. Mendias CL, Gumucio JP, Davis ME, Bromley CW, Davis CS, et al. (2012) Transforming growth factor-beta induces skeletal muscle atrophy and fibrosis through the induction of atrogin-1 and scleraxis. Muscle Nerve 45: 55-59.
34. Lynch GS, Rafael JA, Hinkle RT, Cole NM, Chamberlain JS, et al. (1997) Contractile properties of diaphragm muscle segments from old mdx and old transgenic mdx mice. Am J Physiol 272: C2063-2068.
35. Smith PE, Calverley PM, Edwards RH, Evans GA, Campbell EJ (1987) Practical problems in the respiratory care of patients with muscular dystrophy. N Engl J Med 316: 1197-1205. (Pubitemid 17069954)
36. Stedman HH, Sweeney HL, Shrager JB, Maguire HC, Panettieri RA, et al. (1991) The mdx mouse diaphragm reproduces the degenerative changes of Duchenne muscular dystrophy. Nature 352: 536-539.
37. Nakamura A, Kobayashi M, Kuraoka M, Yuasa K, Yugeta N, et al. (2013) Initial Pulmonary Respiration Causes Massive Diaphragm Damage and Hyper-CKemia in Duchenne Muscular Dystrophy Dog. Sci Rep 3: 2183.
38. Yokota T, Lu QL, Partridge T, Kobayashi M, Nakamura A, et al. (2009) Efficacy of systemic morpholino exon-skipping in Duchenne dystrophy dogs. Ann Neurol 65: 667-676.
39. Sanjabi S, Zenewicz LA, Kamanaka M, Flavell RA (2009) Anti-inflammatory and pro-inflammatory roles of TGF-beta, IL-10, and IL-22 in immunity and autoimmunity. Curr Opin Pharmacol 9: 447-453.
40. Kulkarni AB, Huh CG, Becker D, Geiser A, Lyght M, et al. (1993) Transforming growth factor beta 1 null mutation in mice causes excessive inflammatory response and early death. Proc Natl Acad Sci U S A 90: 770-774. (Pubitemid 23028947)
41. Nelson CA, Hunter RB, Quigley LA, Girgenrath S, Weber WD, et al. (2011) Inhibiting TGF-beta activity improves respiratory function in mdx mice. Am J Pathol 178: 2611-2621.
42. Aoki H, Ohnishi H, Hama K, Shinozaki S, Kita H, et al. (2006) Existence of autocrine loop between interleukin-6 and transforming growth factor-beta1 in activated rat pancreatic stellate cells. J Cell Biochem 99: 221-228. (Pubitemid 44297966)
43. Pegoraro E, Hoffman EP, Piva L, Gavassini BF, Cagnin S, et al. (2011) SPP1 genotype is a determinant of disease severity in Duchenne muscular dystrophy. Neurology 76: 219-226.
44. Pardo A, Gibson K, Cisneros J, Richards TJ, Yang Y, et al. (2005) Up-regulation and profibrotic role of osteopontin in human idiopathic pulmonary fibrosis. PLoS Med 2: e251.
45. Vetrone SA, Montecino-Rodriguez E, Kudryashova E, Kramerova I, Hoffman EP, et al. (2009) Osteopontin promotes fibrosis in dystrophic mouse muscle by modulating immune cell subsets and intramuscular TGF-beta. J Clin Invest 119: 1583-1594.
46. Collins AR, Schnee J, Wang W, Kim S, Fishbein MC, et al. (2004) Osteopontin modulates angiotensin II-induced fibrosis in the intact murine heart. J Am Coll Cardiol 43: 1698-1705. (Pubitemid 38561355)
47. Husmann I, Soulet L, Gautron J, Martelly I, Barritault D (1996) Growth factors in skeletal muscle regeneration. Cytokine Growth Factor Rev 7: 249-258. (Pubitemid 27200309)
48. Noirez P, Torres S, Cebrian J, Agbulut O, Peltzer J, et al. (2006) TGF-beta1 favors the development of fast type identity during soleus muscle regeneration. J Muscle Res Cell Motil 27: 1-8. (Pubitemid 44072117)
49. Carlson ME, Conboy MJ, Hsu M, Barchas L, Jeong J, et al. (2009) Relative roles of TGF-beta1 and Wnt in the systemic regulation and aging of satellite cell responses. Aging Cell 8: 676-689.
50. Liu X, Alexander V, Vijayachandra K, Bhogte E, Diamond I, et al. (2001) Conditional epidermal expression of TGFbeta 1 blocks neonatal lethality but causes a reversible hyperplasia and alopecia. Proc Natl Acad Sci U S A 98: 9139-9144. (Pubitemid 32743882)
51. Pandey SN, Cabotage J, Shi R, Dixit M, Sutherland M, et al. (2012) Conditional over-expression of PITX1 causes skeletal muscle dystrophy in mice. Biol Open 1: 629-639.
52. Spurney CF, Sali A, Guerron AD, Iantorno M, Yu Q, et al. (2011) Losartan decreases cardiac muscle fibrosis and improves cardiac function in dystrophin-deficient mdx mice. J Cardiovasc Pharmacol Ther 16: 87-95. Development