Differential muscle hypertrophy is associated with satellite cell numbers and Akt pathway activation following activin type IIB receptor inhibition in Mtm1 p.R69C mice

American Journal of Pathology

Volumn 184, Issue 6, 2014, Pages 1831-1842

  Lawlor, Michael W ^a,b   Viola, Marissa G ^a   Meng, Hui ^b   Edelstein, Rachel V ^a   Liu, Fujun ^c   Yan, Ke ^b   Luna, Elizabeth J ^d   Lerch Gaggl, Alexandra ^b   Hoffmann, Raymond G ^b   Pierson, Christopher R ^e   Buj Bello, Anna ^f   Lachey, Jennifer L ^g   Pearsall, Scott ^g   Yang, Lin ^c   Hillard, Cecilia J ^b   Beggs, Alan H ^a  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b MEDICAL COLLEGE OF WISCONSIN   (United States)

^c UNIVERSITY OF KENTUCKY   (United States)

^d UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^e NATIONWIDE CHILDREN S HOSPITAL   (United States)

^f GÉNÉTHON   (France)

^g Acceleron Pharma Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVIN RECEPTOR 2; ELONGATION FACTOR 2 KINASE; MYOSIN; PROTEIN KINASE B; PROTEIN S6; TRANSCRIPTION FACTOR PAX7; MUSCLE PROTEIN; MYOTUBULARIN; NON RECEPTOR PROTEIN TYROSINE PHOSPHATASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CENTRONUCLEAR MYOPATHY; CONTROLLED STUDY; CROSS REACTION; ENZYME ACTIVATION; FORELIMB; GASTROCNEMIUS MUSCLE; GRIP STRENGTH; HANGING; HISTOPATHOLOGY; HYPERTROPHY; MOUSE; NONHUMAN; PHYSICAL PERFORMANCE; PRIORITY JOURNAL; QUADRICEPS FEMORIS MUSCLE; SATELLITE CELL; UPREGULATION; X LINKED MYOTUBULAR MYOPATHY; ANIMAL; DISEASE MODEL; GENETICS; METABOLISM; MUTANT MOUSE STRAIN; MYOPATHY; PATHOLOGY; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; SKELETAL MUSCLE SATELLITE CELL;

ACTIVIN RECEPTORS, TYPE II; ANIMALS; DISEASE MODELS, ANIMAL; MICE; MICE, MUTANT STRAINS; MUSCLE PROTEINS; MUSCLE, SKELETAL; MYOPATHIES, STRUCTURAL, CONGENITAL; PROTEIN TYROSINE PHOSPHATASES, NON-RECEPTOR; PROTO-ONCOGENE PROTEINS C-AKT; SATELLITE CELLS, SKELETAL MUSCLE; SIGNAL TRANSDUCTION;

EID: 84901020192     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2014.03.003     Document Type: Article

References (37)

1. J.Z. Heckmatt, C.A. Sewry, D. Hodes, and V. Dubowitz Congenital centronuclear (myotubular) myopathy. A clinical, pathological and genetic study in eight children Brain 108 1985 941 964
2. H. Jungbluth, C. Wallgren-Pettersson, and J. Laporte Centronuclear (myotubular) myopathy Orphanet J Rare Dis 3 2008 26
3. A. Buj-Bello, F. Fougerousse, Y. Schwab, N. Messaddeq, D. Spehner, C.R. Pierson, M. Durand, C. Kretz, O. Danos, A.M. Douar, A.H. Beggs, P. Schultz, M. Montus, P. Denefle, and J.L. Mandel AAV-mediated intramuscular delivery of myotubularin corrects the myotubular myopathy phenotype in targeted murine muscle and suggests a function in plasma membrane homeostasis Hum Mol Genet 17 2008 2132 2143
4. C. Cao, J.M. Backer, J. Laporte, E.J. Bedrick, and A. Wandinger-Ness Sequential actions of myotubularin lipid phosphatases regulate endosomal PI(3)P and growth factor receptor trafficking Mol Biol Cell 19 2008 3334 3346
5. J.J. Dowling, A.P. Vreede, S.E. Low, E.M. Gibbs, J.Y. Kuwada, C.G. Bonnemann, and E.L. Feldman Loss of myotubularin function results in T-tubule disorganization in zebrafish and human myotubular myopathy PLoS Genet 5 2009 e1000372
6. J. Laporte, L.J. Hu, C. Kretz, J.L. Mandel, P. Kioschis, J.F. Coy, S.M. Klauck, A. Poustka, and N. Dahl A gene mutated in X-linked myotubular myopathy defines a new putative tyrosine phosphatase family conserved in yeast Nat Genet 13 1996 175 182
7. K. Hnia, H. Tronchere, K.K. Tomczak, L. Amoasii, P. Schultz, A.H. Beggs, B. Payrastre, J.L. Mandel, and J. Laporte Myotubularin controls desmin intermediate filament architecture and mitochondrial dynamics in human and mouse skeletal muscle J Clin Invest 121 2011 70 85
8. M.W. Lawlor, M.S. Alexander, M.G. Viola, H. Meng, R. Joubert, V. Gupta, N. Motohashi, R.A. Manfready, C.P. Hsu, P. Huang, A. Buj-Bello, L.M. Kunkel, A.H. Beggs, and E. Gussoni Myotubularin-deficient myoblasts display increased apoptosis, delayed proliferation, and poor cell engraftment Am J Pathol 181 2012 961 968
9. C.R. Pierson, K. Tomczak, P. Agrawal, B. Moghadaszadeh, and A.H. Beggs X-linked myotubular and centronuclear myopathies J Neuropathol Exp Neurol 64 2005 555 564
10. C.R. Pierson, P.B. Agrawal, J. Blasko, and A.H. Beggs Myofiber size correlates with MTM1 mutation type and outcome in X-linked myotubular myopathy Neuromuscul Disord 17 2007 562 568
11. L. Al-Qusairi, N. Weiss, A. Toussaint, C. Berbey, N. Messaddeq, C. Kretz, D. Sanoudou, A.H. Beggs, B. Allard, J.L. Mandel, J. Laporte, V. Jacquemond, and A. Buj-Bello T-tubule disorganization and defective excitation-contraction coupling in muscle fibers lacking myotubularin lipid phosphatase Proc Natl Acad Sci U S A 106 2009 18763 18768
12. M.W. Lawlor, B.P. Read, R. Edelstein, N. Yang, C.R. Pierson, M.J. Stein, A. Wermer-Colan, A. Buj-Bello, J.L. Lachey, J.S. Seehra, and A.H. Beggs Inhibition of activin receptor type IIb increases strength and lifespan in myotubularin-deficient mice Am J Pathol 178 2011 784 793
13. C.R. Pierson, A.N. Dulin-Smith, A.N. Durban, M.L. Marshall, J.T. Marshall, A.D. Snyder, N. Naiyer, J.T. Gladman, D.S. Chandler, M.W. Lawlor, A. Buj-Bello, J.J. Dowling, and A.H. Beggs Modeling the human MTM1 p.R69C mutation in murine Mtm1 results in exon 4 skipping and a less severe myotubular myopathy phenotype Hum Mol Genet 21 2012 811 825
14. S. McCroskery, M. Thomas, L. Maxwell, M. Sharma, and R. Kambadur Myostatin negatively regulates satellite cell activation and self-renewal J Cell Biol 162 2003 1135 1147
15. D. Joulia-Ekaza, and G. Cabello Myostatin regulation of muscle development: molecular basis, natural mutations, physiopathological aspects Exp Cell Res 312 2006 2401 2414
16. S.M. Cadena, K.N. Tomkinson, T.E. Monnell, M.S. Spaits, R. Kumar, K.W. Underwood, R.S. Pearsall, and J.L. Lachey Administration of a soluble activin type IIB receptor promotes skeletal muscle growth independent of fiber type J Appl Physiol 109 2010 635 642
17. O. Meyuhas Physiological roles of ribosomal protein S6: one of its kind Int Rev Cell Mol Biol 268 2008 1 37
18. A. Buj-Bello, V. Laugel, N. Messaddeq, H. Zahreddine, J. Laporte, J.F. Pellissier, and J.L. Mandel The lipid phosphatase myotubularin is essential for skeletal muscle maintenance but not for myogenesis in mice Proc Natl Acad Sci U S A 99 2002 15060 15065
19. M.H. Brooke, and W.K. Engel The histographic analysis of human muscle biopsies with regard to fiber types. 4. Children's biopsies Neurology 19 1969 591 605
20. D. Wattanasirichaigoon, K.J. Swoboda, F. Takada, H.Q. Tong, V. Lip, S.T. Iannaccone, C. Wallgren-Pettersson, N.G. Laing, and A.H. Beggs Mutations of the slow muscle alpha-tropomyosin gene, TPM3, are a rare cause of nemaline myopathy Neurology 59 2002 613 617
21. H.Q. Han, X. Zhou, W.E. Mitch, and A.L. Goldberg Myostatin/activin pathway antagonism: molecular basis and therapeutic potential Int J Biochem Cell Biol 45 2013 2333 2347
22. G.L. Razidlo, D. Katafiasz, and G.S. Taylor Myotubularin regulates Akt-dependent survival signaling via phosphatidylinositol 3-phosphate J Biol Chem 286 2011 20005 20019
23. L. Al-Qusairi, I. Prokic, L. Amoasii, C. Kretz, N. Messaddeq, J.L. Mandel, and J. Laporte Lack of myotubularin (MTM1) leads to muscle hypotrophy through unbalanced regulation of the autophagy and ubiquitin-proteasome pathways FASEB J 27 2013 3384 3394
24. M.R. Morissette, S.A. Cook, C. Buranasombati, M.A. Rosenberg, and A. Rosenzweig Myostatin inhibits IGF-I-induced myotube hypertrophy through Akt Am J Physiol Cell Physiol 297 2009 C1124 C1132
25. J.J. Hulmi, B.M. Oliveira, M. Silvennoinen, W.M. Hoogaars, H. Ma, P. Pierre, A. Pasternack, H. Kainulainen, and O. Ritvos Muscle protein synthesis, mTORC1/MAPK/Hippo signaling, and capillary density are altered by blocking of myostatin and activins Am J Physiol Endocrinol Metab 304 2013 E41 E50
26. S. Kalista, O. Schakman, H. Gilson, P. Lause, B. Demeulder, L. Bertrand, M. Pende, and J.P. Thissen The type 1 insulin-like growth factor receptor (IGF-IR) pathway is mandatory for the follistatin-induced skeletal muscle hypertrophy Endocrinology 153 2012 241 253
27. S. Welle, K. Burgess, and S. Mehta Stimulation of skeletal muscle myofibrillar protein synthesis, p70 S6 kinase phosphorylation, and ribosomal protein S6 phosphorylation by inhibition of myostatin in mature mice Am J Physiol Endocrinol Metab 296 2009 E567 E572
28. M.D. Goncalves, E.E. Pistilli, A. Balduzzi, M.J. Birnbaum, J. Lachey, T.S. Khurana, and R.S. Ahima Akt deficiency attenuates muscle size and function but not the response to ActRIIB inhibition PLoS One 5 2010 e12707
29. I. Ruvinsky, N. Sharon, T. Lerer, H. Cohen, M. Stolovich-Rain, T. Nir, Y. Dor, P. Zisman, and O. Meyuhas Ribosomal protein S6 phosphorylation is a determinant of cell size and glucose homeostasis Genes Dev 19 2005 2199 2211
30. I. Ruvinsky, M. Katz, A. Dreazen, Y. Gielchinsky, A. Saada, N. Freedman, E. Mishani, G. Zimmerman, J. Kasir, and O. Meyuhas Mice deficient in ribosomal protein S6 phosphorylation suffer from muscle weakness that reflects a growth defect and energy deficit PLoS One 4 2009 e5618
31. S.J. Lee, T.V. Huynh, Y.S. Lee, S.M. Sebald, S.A. Wilcox-Adelman, N. Iwamori, C. Lepper, M.M. Matzuk, and C.M. Fan Role of satellite cells versus myofibers in muscle hypertrophy induced by inhibition of the myostatin/activin signaling pathway Proc Natl Acad Sci U S A 109 2012 E2353 E2360
32. Q. Wang, and A.C. McPherron Myostatin inhibition induces muscle fibre hypertrophy prior to satellite cell activation J Physiol 590 2012 2151 2165
33. H. Gilson, O. Schakman, S. Kalista, P. Lause, K. Tsuchida, and J.P. Thissen Follistatin induces muscle hypertrophy through satellite cell proliferation and inhibition of both myostatin and activin Am J Physiol Endocrinol Metab 297 2009 E157 E164
34. Y. Dong, J.S. Pan, and L. Zhang Myostatin suppression of Akirin1 mediates glucocorticoid-induced satellite cell dysfunction PLoS One 8 2013 e58554
35. J. Jeong, M.J. Conboy, and I.M. Conboy Pharmacological inhibition of myostatin/TGF-beta receptor/pSmad3 signaling rescues muscle regenerative responses in mouse model of type 1 diabetes Acta Pharmacol Sin 34 2013 1052 1060
36. L. Zhang, V. Rajan, E. Lin, Z. Hu, H.Q. Han, X. Zhou, Y. Song, H. Min, X. Wang, J. Du, and W.E. Mitch Pharmacological inhibition of myostatin suppresses systemic inflammation and muscle atrophy in mice with chronic kidney disease FASEB J 25 2011 1653 1663
37. M.W. Lawlor, D. Armstrong, M.G. Viola, J.J. Widrick, H. Meng, R.W. Grange, M.K. Childers, C.P. Hsu, M. O'Callaghan, C.R. Pierson, A. Buj-Bello, and A.H. Beggs Enzyme replacement therapy rescues weakness and improves muscle pathology in mice with X-linked myotubular myopathy Hum Mol Genet 22 2013 1525 1538