Excess SMAD signaling contributes to heart and muscle dysfunction in muscular dystrophy

Human Molecular Genetics

Volumn 23, Issue 25, 2014, Pages 6722-6731

  Goldstein, Jeffery A ^a   Bogdanovich, Sasha ^a   Beiriger, Anastasia ^b   Wren, Lisa M ^a   Rossi, Ann E ^a   Gao, Quan Q ^b   Gardner, Brandon B ^a   Earley, Judy U ^a   Molkentin, Jeffery D ^d   McNally, Elizabeth M ^a,c  

^a UNIVERSITY OF CHICAGO   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

^c THE UNIVERSITY OF CHICAGO   (United States)

^d UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM BINDING PROTEIN; LATENT TRANSFORMING GROWTH FACTOR BETA BINDING PROTEIN; SARCOGLYCAN; SMAD2 PROTEIN; SMAD2 PROTEIN, MOUSE; SMAD3 PROTEIN; SMAD3 PROTEIN, MOUSE; SMAD4 PROTEIN; SMAD4 PROTEIN, MOUSE; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL; BODY WEIGHT; CARDIAC MUSCLE; DEFICIENCY; DISEASE MODEL; GENE EXPRESSION REGULATION; GENETICS; HEART FUNCTION TEST; HUMAN; INJURIES; KNOCKOUT MOUSE; METABOLISM; MOUSE; MUSCULAR DYSTROPHY; MUTATION; PATHOLOGY; PHOSPHORYLATION; SIGNAL TRANSDUCTION; SKELETAL MUSCLE;

ANIMALS; BODY WEIGHT; CALCIUM-BINDING PROTEINS; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION; HEART FUNCTION TESTS; HUMANS; LATENT TGF-BETA BINDING PROTEINS; MICE; MICE, KNOCKOUT; MUSCLE, SKELETAL; MUSCULAR DYSTROPHIES; MUTATION; MYOCARDIUM; PHOSPHORYLATION; SARCOGLYCANS; SIGNAL TRANSDUCTION; SMAD2 PROTEIN; SMAD3 PROTEIN; SMAD4 PROTEIN; TRANSFORMING GROWTH FACTOR BETA;

EID: 84922134591     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddu390     Document Type: Article

References (35)

1. Neptune, E.R., Frischmeyer, P.A., Arking, D.E., Myers, L., Bunton, T.E., Gayraud, B., Ramirez, F., Sakai, L.Y. and Dietz, H.C. (2003) Dysregulation of TGF-beta activation contributes to pathogenesis in Marfan syndrome. Nat. Genet., 33, 407 – 411.
2. Lan, H.Y. (2011) Diverse roles of TGF-beta/Smads in renal fibrosis and inflammation. Int. J. Biol. Sci., 7, 1056–1067.
3. Hersh, C.P., Demeo, D.L., Lazarus, R., Celedon, J.C., Raby, B.A., Benditt, J.O., Criner, G., Make, B., Martinez, F.J., Scanlon, P.D. et al. (2006) Genetic association analysis of functional impairment in chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med., 173, 977 – 984.
4. Hoffman, E.P., Brown, R.H. Jr and Kunkel, L.M. (1987) Dystrophin: the protein product of the Duchenne muscular dystrophy locus. Cell, 51, 919–928.
5. Bernasconi, P., Torchiana, E., Confalonieri, P., Brugnoni, R., Barresi, R., Mora, M., Cornelio, F., Morandi, L. and Mantegazza, R. (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.
6. Burks, T.N. and Cohn, R.D. (2011) Role of TGF-beta signaling in inherited and acquired myopathies. Skelet. Muscle, 1, 19.
7. Rybakova, I.N., Patel, J.R. and Ervasti, J.M. (2000) The dystrophin complex forms a mechanically strong link between the sarcolemma and costameric actin. J. Cell. Biol., 150, 1209 – 1214.
8. Noguchi, S., McNally, E.M., Ben Othmane, K., Hagiwara, Y., Mizuno, Y., Yoshida, M., Yamamoto, H., Bonnemann, C.G., Gussoni, E., Denton, P.H. et al. (1995) Mutations in the dystrophin-associated protein gamma-sarcoglycan in chromosome 13 muscular dystrophy. Science, 270, 819–822.
9. Hack, A.A., Ly, C.T., Jiang, F., Clendenin, C.J., Sigrist, K.S., Wollmann, R.L. and McNally, E.M. (1998) Gamma-sarcoglycan deficiency leads to muscle membrane defects and apoptosis independent of dystrophin. J. Cell Biol., 142, 1279–1287.
10. 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.
11. Nelson, C.A., Hunter, R.B., Quigley, L.A., Girgenrath, S., Weber, W.D., McCullough, J.A., Dinardo, C.J., Keefe, K.A., Ceci, L., Clayton, N.P. et al. (2011) Inhibiting TGF-beta activity improves respiratory function in mdx mice. Am. J. Pathol., 178, 2611–2621.
12. Dasch, J.R., Pace, D.R., Waegell, W., Inenaga, D. and Ellingsworth, L. (1989) Monoclonal antibodies recognizing transforming growth factor-beta. Bioactivity neutralization and transforming growth factor beta 2 affinity purification. J. Immunol., 142, 1536 – 1541.
13. Feng, X.H. and Derynck, R. (2005) Specificity and versatility in tgf-beta signaling through Smads. Annu. Rev. Cell Dev. Biol., 21, 659–693.
14. Delaney, J.R. and Mlodzik, M. (2006) TGF-beta activated kinase-1: new insights into the diverse roles of TAK1 in development and immunity. Cell Cycle, 5, 2852–2855.
15. Heydemann, A., Ceco, E., Lim, J.E., Hadhazy, M., Ryder, P., Moran, J.L., Beier, D.R., Palmer, A.A. and McNally, E.M. (2009) Latent TGF-beta-binding protein 4 modifies muscular dystrophy in mice. J. Clin. Invest., 119, 3703–3712.
16. Petrof, B.J., Shrager, J.B., Stedman, H.H., Kelly, A.M. and Sweeney, H.L. (1993) Dystrophin protects the sarcolemma from stresses developed during muscle contraction. Proc. Natl. Acad. Sci. USA, 90, 3710–3714.
17. Lin, A.H., Luo, J., Mondshein, L.H., ten Dijke, P., Vivien, D., Contag, C.H. and Wyss-Coray, T. (2005) Global analysis of Smad2/3-dependent TGF-beta signaling in living mice reveals prominent tissue-specific responses to injury. J. Immunol., 175, 547–554.
18. Chu, G.C., Dunn, N.R., Anderson, D.C., Oxburgh, L. and Robertson, E.J. (2004) Differential requirements for Smad4 in TGFbeta-dependent patterning of the early mouse embryo. Development, 131, 3501–3512.
19. Wu, R.Y., Zhang, Y., Feng, X.H. and Derynck, R. (1997) Heteromeric and homomeric interactions correlate with signaling activity and functional cooperativity of Smad3 and Smad4/DPC4. Mol. Cell. Biol., 17, 2521 – 2528.
20. Heydemann, A., Huber, J.M., Demonbreun, A., Hadhazy, M. and McNally, E.M. (2005) Genetic background influences muscular dystrophy. Neuromuscu. Disord., 15, 601 – 609.
21. Matsuda, R., Nishikawa, A. and Tanaka, H. (1995) Visualization of dystrophic muscle fibers in mdx mouse by vital staining with Evans blue: evidence of apoptosis in dystrophin-deficient muscle. J. Biochem., 118, 959–964.
22. Millay, D.P., Goonasekera, S.A., Sargent, M.A., Maillet, M., Aronow, B.J. and Molkentin, J.D. (2009) Calcium influx is sufficient to induce muscular dystrophy through a TRPC-dependent mechanism. Proc. Natl. Acad. Sci. USA, 106, 19023–19028.
23. Goonasekera, S.A., Lam, C.K., Millay, D.P., Sargent, M.A., Hajjar, R.J., Kranias, E.G. and Molkentin, J.D. (2011) Mitigation of muscular dystrophy in mice by SERCA overexpression in skeletal muscle. J. Clin. Invest., 121, 1044 – 1052.
24. Meyers, M.B., Pickel, V.M., Sheu, S.S., Sharma, V.K., Scotto, K.W. and Fishman, G.I. (1995) Association of sorcin with the cardiac ryanodine receptor. J. Biol. Chem., 270, 26411–26418.
25. Lokuta, A.J., Meyers, M.B., Sander, P.R., Fishman, G.I. and Valdivia, H.H. (1997) Modulation of cardiac ryanodine receptors by sorcin. J. Biol. Chem., 272, 25333 – 25338.
26. Zamparelli, C., Macquaide, N., Colotti, G., Verzili, D., Seidler, T., Smith, G.L. and Chiancone, E. (2010) Activation of the cardiac Na(+)-Ca(2+) exchanger by sorcin via the interaction of the respective Ca(2+)-binding domains. J. Mol. Cell. Cardiol., 49, 132–141.
27. Goldstein, J.A., Kelly, S.M., LoPresti, P.P., Heydemann, A., Earley, J.U., Ferguson, E.L., Wolf, M.J. and McNally, E.M. (2011) SMAD signaling drives heart and muscle dysfunction in a Drosophila model of muscular dystrophy. Hum. Mol. Genet., 20, 894–904.
28. Bellinger, A.M., Reiken, S., Carlson, C., Mongillo, M., Liu, X., Rothman, L., Matecki, S., Lacampagne, A. and Marks, A.R. (2009) Hypernitrosylated ryanodine receptor calcium release channels are leaky in dystrophic muscle. Nat. Med., 15, 325 – 330.
29. Ali, R., Huang, Y., Maher, S.E., Kim, R.W., Giordano, F.J., Tellides, G. and Geirsson, A. (2012) miR-1 mediated suppression of Sorcin regulates myocardial contractility through modulation of Ca(2+) signaling. J. Mol. Cell. Cardiol., 52, 1027–1037.
30. Meyers, M.B., Fischer, A., Sun, Y.J., Lopes, C.M., Rohacs, T., Nakamura, T.Y., Zhou, Y.Y., Lee, P.C., Altschuld, R.A., McCune, S.A. et al. (2003) Sorcin regulates excitation-contraction coupling in the heart. J. Biol. Chem., 278, 28865 – 28871.
31. Koitabashi, N., Danner, T., Zaiman, A.L., Pinto, Y.M., Rowell, J., Mankowski, J., Zhang, D., Nakamura, T., Takimoto, E. and Kass, D.A. (2011) Pivotal role of cardiomyocyte TGF-beta signaling in the murine pathological response to sustained pressure overload. J. Clin. Invest., 121, 2301–2312.
32. Tallquist, M.D. and Soriano, P. (2000) Epiblast-restricted Cre expression in MORE mice: a tool to distinguish embryonic versus extra-embryonic gene function. Genesis, 26, 113 – 115.
33. Rueda, A., Song, M., Toro, L., Stefani, E. and Valdivia, H.H. (2006) Sorcin modulation of Ca2+ sparks in rat vascular smooth muscle cells. J. Physiol., 576, 887–901.
34. Barton, E.R., Lynch, G. and Khurana, T.S. (2008) Measuring isometric force of isolated mouse muscles in vitro. In Willmann, R. (ed), Experimental Protocols for DMD Animal Models. Treat-NMD Neuromuscular Network, Vol. DMD_M.1.2.002, p. 14.
35. Arimura, T., Helbling-Leclerc, A., Massart, C., Varnous, S., Niel, F., Lacene, E., Fromes, Y., Toussaint, M., Mura, A.M., Keller, D.I. et al. (2005) Mouse model carrying H222P-Lmna mutation develops muscular dystrophy and dilated cardiomyopathy similar to human striated muscle laminopathies. Hum. Mol. Genet., 14, 155 – 169.