Novel excitation-contraction coupling related genes reveal aspects of muscle weakness beyond atrophy-new hopes for treatment of musculoskeletal diseases

Frontiers in Physiology

Volumn 5 FEB, Issue , 2014, Pages

  Manring, Heather ^a   Abreu, Eduardo ^b   Brotto, Leticia ^b   Weisleder, Noah ^a   Brotto, Marco ^b,c  

^a OHIO STATE UNIVERSITY   (United States)

^b UNIVERSITY OF MISSOURI KANSAS CITY   (United States)

^c UNIVERSITY OF MISSOURI KANSAS CITY SCHOOL OF MEDICINE   (United States)

Author keywords

Aging; Calcium homeostasis; KLF15; MG29; MTMR14; Musculoskeletal diseases; Sarcalumenin; Sarcopenia

Indexed keywords

CALCIUM; KRUPPEL LIKE FACTOR 15; MEMBRANE PROTEIN; MITSUGUMIN 29; MYOTUBULARIN; SARCALUMENIN; UNCLASSIFIED DRUG;

AGING; ALCOHOL CONSUMPTION; CALCIUM TRANSPORT; CENTRONUCLEAR MYOPATHY; DISEASE ASSOCIATION; EXCITATION CONTRACTION COUPLING; GENE; GENE EXPRESSION; GENE MUTATION; GENETIC ASSOCIATION; HUMAN; KLF15 GENE; MG29 GENE; MOLECULAR PATHOLOGY; MTMR14 GENE; MUSCLE ATROPHY; MUSCLE FATIGUE; MUSCLE FUNCTION; MUSCLE METABOLISM; MUSCLE WEAKNESS; MUSCULAR DYSTROPHY; NONHUMAN; PROTEIN FUNCTION; REGULATORY MECHANISM; REVIEW; SAR GENE; SIGNAL TRANSDUCTION;

EID: 84895437062     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2014.00037     Document Type: Review

References (110)

1. Albert, A. P., and Large, W. A. (2003). Store-operated Ca2+-permeable non-selective cation channels in smooth muscle cells. Cell Calcium 33, 345-356. doi: 10.1016/S0143-4160(03)00048-4.
2. Allen, D. G., Lamb, G. D., and Westerblad, H. (2008). Skeletal muscle fatigue: cellular mechanisms. Physiol. Rev. 88, 287-332. doi: 10.1152/physrev.00015.2007.
3. Alonso, A., Sasin, J., Bottini, N., Friedberg, I., Osterman, A., Godzik, A., et al. (2004). Protein tyrosine phosphatases in the human genome. Cell 117, 699-711. doi: 10.1016/j.cell.2004.05.018.
4. Andersson, D. C., Betzenhauser, M. J., Reiken, S., Meli, A. C., Umanskaya, A., Xie, W., et al. (2011). Ryanodine receptor oxidation causes intracellular calcium leak and muscle weakness in aging. Cell Metab. 14, 196-207. doi: 10.1016/j.cmet.2011.05.014.
5. Atherton, P. J., and Smith, K. (2012). Muscle protein synthesis in response to nutrition and exercise. J. Physiol. 590(Pt 5), 1049-1057. doi: 10.1113/jphysiol.2011.225003.
6. Bellinger, A. M., Reiken, S., Dura, M., Murphy, P. W., Deng, S. X., Landry, D. W., et al. (2008). Remodeling of ryanodine receptor complex causes "leaky" channels: a molecular mechanism for decreased exercise capacity. Proc. Natl. Acad. Sci. U.S.A. 105, 2198-2202. doi: 10.1073/pnas.0711074105.
7. Bieker, J. J. (1996). Isolation, genomic structure, and expression of human erythroid Kruppel-like factor (EKLF). DNA Cell Biol. 15, 347-352. doi: 10.1089/dna.1996.15.347.
8. Bitoun, M., Maugenre, S., Jeannet, P. Y., Lacene, E., Ferrer, X., Laforet, P., et al. (2005). Mutations in dynamin 2 cause dominant centronuclear myopathy. Nat. Genet. 37, 1207-1209. doi: 10.1038/ng1657.
9. Bodine, S. C., Stitt, T. N., Gonzalez, M., Kline, W. O., Stover, G. L., Bauerlein, R., et al. (2001). Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo. Nat. Cell Biol. 3, 1014-1019. doi: 10.1038/ncb1101-1014.
10. Bonaldo, P., and Sandri, M. (2013). Cellular and molecular mechanisms of muscle atrophy. Dis. Model. Mech. 6, 25-39. doi: 10.1242/dmm.010389.
11. Booth, F. W., Gordon, S. E., Carlson, C. J., and Hamilton, M. T. (2000). Waging war on modern chronic diseases: primary prevention through exercise biology. J. Appl. Physiol. 88, 774-787.
12. Booth, F. W., and Vyas, D. R. (2001). Genes, environment, and exercise. Adv. Exp. Med. Biol. 502, 13-20. doi: 10.1007/978-1-4757-3401-0_3.
13. Bortz, W. M. T., and Bortz, W. M. 2nd. (1996). How fast do we age? Exercise performance over time as a biomarker. J. Gerontol. A Biol. Sci. Med. Sci. 51, M223-M225. doi: 10.1093/gerona/51A.5.M223.
14. Brooks, S. V., and Faulkner, J. A. (1994). Skeletal muscle weakness in old age: underlying mechanisms. Med. Sci. Sports Exerc. 26, 432-439. doi: 10.1249/00005768-199404000-00006.
15. Brotto, M., and Abreu, E. L. (2012). Sarcopenia: pharmacology of today and tomorrow. J. Pharmacol. Exp. Ther. 343, 540-546. doi: 10.1124/jpet.112.191759.
16. Brotto, M. A., Nosek, T. M., and Kolbeck, R. C. (2002). Influence of ageing on the fatigability of isolated mouse skeletal muscles from mature and aged mice. Exp. Physiol. 87, 77-82. doi: 10.1113/eph8702224.
17. Bruton, J. D., Lannergren, J., and Westerblad, H. (1998). Mechanisms underlying the slow recovery of force after fatigue: importance of intracellular calcium. Acta Physiol. Scand. 162, 285-293. doi: 10.1046/j.1365-201X.1998.0292f.x.
18. Chaillou, T., Lee, J. D., England, J. H., Esser, K. A., and McCarthy, J. J. (1985). Time course of gene expression during mouse skeletal muscle hypertrophy. J. Appl. Physiol. 115, 1065-1074. doi: 10.1152/japplphysiol.00611.2013.
19. Chawla, J. (2011). Stepwise approach to myopathy in systemic disease. Front. Neurol. 2:49. doi: 10.3389/fneur.2011.00049.
20. de Paula Brotto, M., van Leyen, S. A., Brotto, L. S., Jin, J. P., Nosek, C. M., and Nosek, T. M. (2001). Hypoxia/fatigue-induced degradation of troponin I and troponin C: new insights into physiologic muscle fatigue. Pflugers Arch. 442, 738-744. doi: 10.1007/s004240100587.
21. Dmitriev, P., Petrov, A., Ansseau, E., Stankevicins, L., Charron, S., Kim, E., et al. (2011). The Kruppel-like factor 15 as a molecular link between myogenic factors and a chromosome 4q transcriptional enhancer implicated in facioscapulohumeral dystrophy. J. Biol. Chem. 286, 44620-44631. doi: 10.1074/jbc.M111.254052.
22. Dowling, J. J., Low, S. E., Busta, A. S., and Feldman, E. L. (2010). Zebrafish MTMR14 is required for excitation-contraction coupling, developmental motor function and the regulation of autophagy. Hum. Mol. Genet. 19, 2668-2681. doi: 10.1093/hmg/ddq153.
23. Dowling, J. J., Vreede, A. P., Low, S. E., Gibbs, E. M., Kuwada, J. Y., Bonnemann, C. G., et al. (2009). Loss of myotubularin function results in T-tubule disorganization in zebrafish and human myotubular myopathy. PLoS Genet. 5:e1000372. doi: 10.1371/journal.pgen.1000372.
24. Dowling, P., Doran, P., and Ohlendieck, K. (2004). Drastic reduction of sarcalumenin in Dp427 (dystrophin of 427 kDa)-deficient fibres indicates that abnormal calcium handling plays a key role in muscular dystrophy. Biochem. J. 379, 479-488. doi: 10.1042/BJ20031311.
25. Drummond, M. J., and Rasmussen, B. B. (2008). Leucine-enriched nutrients and the regulation of mammalian target of rapamycin signalling and human skeletal muscle protein synthesis. Curr. Opin. Clin. Nutr. Metab. Care 11, 222-226. doi: 10.1097/MCO.0b013e3282fa17fb.
26. Elliott, A. C. (2001). Recent developments in non-excitable cell calcium entry. Cell Calcium 30, 73-93. doi: 10.1054/ceca.2001.0215.
27. Estruch, R., Nicolas, J. M., Villegas, E., Junque, A., and Urbano-Marquez, A. (1993). Relationship between ethanol-related diseases and nutritional status in chronically alcoholic men. Alcohol Alcohol. 28, 543-550.
28. Faulkner, J. A., Brooks, S. V., and Zerba, E. (1995). Muscle atrophy and weakness with aging: contraction-induced injury as an underlying mechanism. J. Gerontol. A Biol. Sci. Med. Sci. 50(Spec No), 124-129.
29. Fernandez-Sola, J., Preedy, V. R., Lang, C. H., Gonzalez-Reimers, E., Arno, M., Lin, J. C., et al. (2007). Molecular and cellular events in alcohol-induced muscle disease. Alcohol. Clin. Exp. Res. 31, 1953-1962. doi: 10.1111/j.1530-0277.2007.00530.x.
30. Fisch, S., Gray, S., Heymans, S., Haldar, S. M., Wang, B., Pfister, O., et al. (2007). Kruppel-like factor 15 is a regulator of cardiomyocyte hypertrophy. Proc. Natl. Acad. Sci. U.S.A. 104, 7074-7079. doi: 10.1073/pnas.0701981104.
31. Fujino, T., Kondo, J., Ishikawa, M., Morikawa, K., and Yamamoto, T. T. (2001). Acetyl-CoA synthetase 2, a mitochondrial matrix enzyme involved in the oxidation of acetate. J. Biol. Chem. 276, 11420-11426. doi: 10.1074/jbc.M008782200.
32. Gibbs, E. M., Feldman, E. L., and Dowling, J. J. (2010). The role of MTMR14 in autophagy and in muscle disease. Autophagy 6, 819-820. doi: 10.4161/auto.6.6.12624.
33. Goldberg, A. L., Tischler, M., DeMartino, G., and Griffin, G. (1980). Hormonal regulation of protein degradation and synthesis in skeletal muscle. Fed. Proc. 39, 31-36.
34. Gonzalez, E., and Delbono, O. (2001a). Age-dependent fatigue in single intact fast-and slow fibers from mouse EDL and soleus skeletal muscles. Mech. Ageing Dev. 122, 1019-1032. doi: 10.1016/S0047-6374(01)00229-9.
35. Gonzalez, E., and Delbono, O. (2001b). Recovery from fatigue in fast and slow single intact skeletal muscle fibers from aging mouse. Muscle Nerve 24, 1219-1224. doi: 10.1002/mus.1135.
36. Gonzalez, E., Messi, M. L., and Delbono, O. (2000). The specific force of single intact extensor digitorum longus and soleus mouse muscle fibers declines with aging. J. Membr. Biol. 178, 175-183. doi: 10.1007/s002320010025.
37. Gonzalez-Reimers, E., Duran-Castellon, M. C., Lopez-Lirola, A., Santolaria-Fernandez, F., Abreu-Gonzalez, P., Alvisa-Negrin, J., et al. (2010). Alcoholic myopathy: vitamin D deficiency is related to muscle fibre atrophy in a murine model. Alcohol Alcohol. 45, 223-230. doi: 10.1093/alcalc/agq010.
38. Gray, S., Wang, B., Orihuela, Y., Hong, E. G., Fisch, S., Haldar, S., et al. (2007). Regulation of gluconeogenesis by Kruppel-like factor 15. Cell Metab. 5, 305-312. doi: 10.1016/j.cmet.2007.03.002.
39. Haldar, S. M., Ibrahim, O. A., and Jain, M. K. (2007). Kruppel-like Factors (KLFs) in muscle biology. J. Mol. Cell. Cardiol. 43, 1-10. doi: 10.1016/j.yjmcc.2007.04.005.
40. Haldar, S. M., Jeyaraj, D., Anand, P., Zhu, H., Lu, Y., Prosdocimo, D. A., et al. (2012). Kruppel-like factor 15 regulates skeletal muscle lipid flux and exercise adaptation. Proc. Natl. Acad. Sci. U.S.A. 109, 6739-6744. doi: 10.1073/pnas.1121060109.
41. Hofer, T., Badouard, C., Bajak, E., Ravanat, J. L., Mattsson, A., and Cotgreave, I. A. (2005). Hydrogen peroxide causes greater oxidation in cellular RNA than in DNA. Biol. Chem. 386, 333-337. doi: 10.1515/BC.2005.040.
42. Hong-Brown, L. Q., Brown, C. R., Huber, D. S., and Lang, C. H. (2006). Alcohol and indinavir adversely affect protein synthesis and phosphorylation of MAPK and mTOR signaling pathways in C2C12 myocytes. Alcohol. Clin. Exp. Res. 30, 1297-1307. doi: 10.1111/j.1530-0277.2006.00157.x.
43. Jungbluth, H., Wallgren-Pettersson, C., and Laporte, J. (2008). Centronuclear (myotubular) myopathy. Orphanet J. Rare Dis. 3, 26. doi: 10.1186/1750-1172-3-26.
44. Lang, C. H., Frost, R. A., Deshpande, N., Kumar, V., Vary, T. C., Jefferson, L. S., et al. (2003). Alcohol impairs leucine-mediated phosphorylation of 4E-BP1, S6K1, eIF4G, and mTOR in skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 285, E1205-E1215. doi: 10.1152/ajpendo.00177.2003.
45. Lang, C. H., Wu, D., Frost, R. A., Jefferson, L. S., Kimball, S. R., and Vary, T. C. (1999). Inhibition of muscle protein synthesis by alcohol is associated with modulation of eIF2B and eIF4E. Am. J. Physiol. 277(2 Pt 1), E268-E276.
46. Laporte, J., Bedez, F., Bolino, A., and Mandel, J. L. (2003). Myotubularins, a large disease-associated family of cooperating catalytically active and inactive phosphoinositides phosphatases. Hum. Mol. Genet. 12(Spec No 2), R285-R292. doi: 10.1093/hmg/ddg273.
47. Laporte, J., Hu, L. J., Kretz, C., Mandel, J. L., Kioschis, P., Coy, J. F., et al. (1996). A gene mutated in X-linked myotubular myopathy defines a new putative tyrosine phosphatase family conserved in yeast. Nat. Genet. 13, 175-182. doi: 10.1038/ng0696-175.
48. Leberer, E., Charuk, J. H., Green, N. M., and MacLennan, D. H. (1989). Molecular cloning and expression of cDNA encoding a lumenal calcium binding glycoprotein from sarcoplasmic reticulum. Proc. Natl. Acad. Sci. U.S.A. 86, 6047-6051. doi: 10.1073/pnas.86.16.6047.
49. Leberer, E., Timms, B. G., Campbell, K. P., and MacLennan, D. H. (1990). Purification, calcium binding properties, and ultrastructural localization of the 53, 000-and 160, 000 (sarcalumenin)-dalton glycoproteins of the sarcoplasmic reticulum. J. Biol. Chem. 265, 10118-10124.
50. Lewis, R. S. (2007). The molecular choreography of a store-operated calcium channel. Nature 446, 284-287. doi: 10.1038/nature05637.
51. Lexell, J. (1993). Ageing and human muscle: observations from Sweden. Can. J. Appl. Physiol. 18, 2-18. doi: 10.1139/h93-002.
52. Lofberg, E., Gutierrez, A., Wernerman, J., Anderstam, B., Mitch, W. E., Price, S. R., et al. (2002). Effects of high doses of glucocorticoids on free amino acids, ribosomes and protein turnover in human muscle. Eur. J. Clin. Invest. 32, 345-353. doi: 10.1046/j.1365-2362.2002.00993.x.
53. Lowe, D. A., Husom, A. D., Ferrington, D. A., and Thompson, L. V. (2004). Myofibrillar myosin ATPase activity in hindlimb muscles from young and aged rats. Mech. Ageing Dev. 125, 619-627. doi: 10.1016/j.mad.2004.07.002.
54. Lowe, D. A., Thomas, D. D., and Thompson, L. V. (2002). Force generation, but not myosin ATPase activity, declines with age in rat muscle fibers. Am. J. Physiol. Cell Physiol. 283, C187-C192. doi: 10.1152/ajpcell.00008.2002.
55. Ma, J., and Pan, Z. (2003). Retrograde activation of store-operated calcium channel. Cell Calcium 33, 375-384. doi: 10.1016/S0143-4160(03)00050-2.
56. Ma, R., Du, J., Sours, S., and Ding, M. (2006). Store-operated Ca2+ channel in renal microcirculation and glomeruli. Exp. Biol. Med. (Maywood) 231, 145-153.
57. Manini, T. M., and Clark, B. C. (2012). Dynapenia and aging: an update. J. Gerontol. A Biol. Sci. Med. Sci. 67, 28-40. doi: 10.1093/gerona/glr010.
58. Mitchell, W. K., Williams, J., Atherton, P., Larvin, M., Lund, J., and Narici, M. (2012). Sarcopenia, dynapenia, and the impact of advancing age on human skeletal muscle size and strength; a quantitative review. Front. Physiol. 3:260. doi: 10.3389/fphys.2012.00260.
59. Murray, C. J., Vos, T., Lozano, R., Naghavi, M., Flaxman, A. D., Michaud, C., et al. (2010). Disability-adjusted life years (DALYs) for 291 diseases and injuries in 21 regions, 1990-2010, a systematic analysis for the Global Burden of Disease Study. Lancet 380, 2197-2223. doi: 10.1016/S0140-6736(12)61689-4.
60. Nagaraj, R. Y., Nosek, C. M., Brotto, M. A., Nishi, M., Takeshima, H., Nosek, T. M., et al. (2000). Increased susceptibility to fatigue of slow-and fast-twitch muscles from mice lacking the MG29 gene. Physiol. Genomics 4, 43-49.
61. Nakahara, T., Hashimoto, K., Hirano, M., Koll, M., Martin, C. R., and Preedy, V. R. (2003). Acute and chronic effects of alcohol exposure on skeletal muscle c-myc, p53, and Bcl-2 mRNA expression. Am. J. Physiol. Endocrinol. Metab. 285, E1273-E1281. doi: 10.1152/ajpendo.00019.2003.
62. Nakahara, T., Hunter, R., Hirano, M., Uchimura, H., McArdle, A., Broome, C. S., et al. (2006). Alcohol alters skeletal muscle heat shock protein gene expression in rats: these effects are moderated by sex, raised endogenous acetaldehyde, and starvation. Metabolism 55, 843-851. doi: 10.1016/j.metabol.2006.02.009.
63. Nilius, B. (2004). Store-operated Ca2+ entry channels: still elusive! Sci. STKE 2004, pe36. doi: 10.1126/stke.2342004pe36.
64. Nishi, M., Komazaki, S., Kurebayashi, N., Ogawa, Y., Noda, T., Iino, M., et al. (1999). Abnormal features in skeletal muscle from mice lacking mitsugumin29. J. Cell Biol. 147, 1473-1480. doi: 10.1083/jcb.147.7.1473.
65. Noordzij, M., Boeschoten, E. W., Bos, W. J., Dekker, F. W., Bossuyt, P. M., Krediet, R. T., et al. (2007). Disturbed mineral metabolism is associated with muscle and skin complaints in a prospective cohort of dialysis patients. Nephrol. Dial. Transplant 22, 2944-2949. doi: 10.1093/ndt/gfm319.
66. O'Connell, K., Gannon, J., Doran, P., and Ohlendieck, K. (2008). Reduced expression of sarcalumenin and related Ca2+-regulatory proteins in aged rat skeletal muscle. Exp. Gerontol. 43, 958-961. doi: 10.1016/j.exger.2008.07.006.
67. Pan, Z., Yang, D., Nagaraj, R. Y., Nosek, T. A., Nishi, M., Takeshima, H., et al. (2002). Dysfunction of store-operated calcium channel in muscle cells lacking mg29. Nat. Cell Biol. 4, 379-383. doi: 10.1038/ncb788.
68. Parekh, A. B., and Putney, J. W. Jr. (2005). Store-operated calcium channels. Physiol. Rev. 85, 757-810. doi: 10.1152/physrev.00057.2003.
69. Pearson, R., Fleetwood, J., Eaton, S., Crossley, M., and Bao, S. (2008). Kruppel-like transcription factors: a functional family. Int. J. Biochem. Cell Biol. 40, 1996-2001. doi: 10.1016/j.biocel.2007.07.018.
70. Pierson, C. R., Tomczak, K., Agrawal, P., Moghadaszadeh, B., and Beggs, A. H. (2005). X-linked myotubular and centronuclear myopathies. J. Neuropathol. Exp. Neurol. 64, 555-564. doi: 10.1097/01.jnen.0000171653.17213.2e.
71. Place, N., Bruton, J. D., and Westerblad, H. (2009). Mechanisms of fatigue induced by isometric contractions in exercising humans and in mouse isolated single muscle fibres. Clin. Exp. Pharmacol. Physiol. 36, 334-339. doi: 10.1111/j.1440-1681.2008.05021.x.
72. Preedy, V. R., Adachi, J., Ueno, Y., Ahmed, S., Mantle, D., Mullatti, N., et al. (2001a). Alcoholic skeletal muscle myopathy: definitions, features, contribution of neuropathy, impact and diagnosis. Eur. J. Neurol. 8, 677-687. doi: 10.1046/j.1468-1331.2001.00303.x.
73. Preedy, V. R., Paice, A., Mantle, D., Dhillon, A. S., Palmer, T. N., and Peters, T. J. (2001b). Alcoholic myopathy: biochemical mechanisms. Drug Alcohol Depend. 63, 199-205. doi: 10.1016/S0376-8716(00)00219-2.
74. Preedy, V. R., and Peters, T. J. (1988). The effect of chronic ethanol ingestion on protein metabolism in type-I-and type-II-fibre-rich skeletal muscles of the rat. Biochem. J. 254, 631-639.
75. Putney, J. W. Jr., Broad, L. M., Braun, F. J., Lievremont, J. P., and Bird, G. S. (2001). Mechanisms of capacitative calcium entry. J. Cell Sci. 114(Pt 12), 2223-2229.
76. Rahimov, F., and Kunkel, L. M. (2013). The cell biology of disease: cellular and molecular mechanisms underlying muscular dystrophy. J. Cell Biol. 201, 499-510. doi: 10.1083/jcb.201212142.
77. Romanick, M., Thompson, L. V., and Brown-Borg, H. M. (2013). Murine models of atrophy, cachexia, and sarcopenia in skeletal muscle. Biochim. Biophys. Acta 1832, 1410-1420. doi: 10.1016/j.bbadis.2013.03.011.
78. Romero, N. B. (2010). Centronuclear myopathies: a widening concept. Neuromuscul. Disord. 20, 223-228. doi: 10.1016/j.nmd.2010.01.014.
79. Romero, N. B., and Bitoun, M. (2011). Centronuclear myopathies. Semin. Pediatr. Neurol. 18, 250-256. doi: 10.1016/j.spen.2011.10.006.
80. Romero-Suarez, S., Shen, J., Brotto, L., Hall, T., Mo, C., Valdivia, H. H., et al. (2010). Muscle-specific inositide phosphatase (MIP/MTMR14) is reduced with age and its loss accelerates skeletal muscle aging process by altering calcium homeostasis. Aging (Albany NY). 2, 504-513.
81. Rossi, A. E., and Dirksen, R. T. (2006). Sarcoplasmic reticulum: the dynamic calcium governor of muscle. Muscle Nerve 33, 715-731. doi: 10.1002/mus.20512.
82. Russ, D. W., Gregg-Cornell, K., Conaway, M. J., and Clark, B. C. (2012) Evolving concepts on the age-related changes in "muscle quality." J. Cachexia Sarcopenia Muscle 3, 95-109. doi: 10.1007/s13539-011-0054-2.
83. Schakman, O., Kalista, S., Barbe, C., Loumaye, A., and Thissen, J. P. (2013). Glucocorticoid-induced skeletal muscle atrophy. Int. J. Biochem. Cell Biol. 45, 2163-2172. doi: 10.1016/j.biocel.2013.05.036.
84. Sewry, C. A. (2008). Pathological defects in congenital myopathies. J. Muscle Res. Cell Motil. 29, 231-238. doi: 10.1007/s10974-008-9155-8.
85. Shen, J., Yu, W. M., Brotto, M., Scherman, J. A., Guo, C., Stoddard, C., et al. (2009). Deficiency of MIP/MTMR14 phosphatase induces a muscle disorder by disrupting Ca(2+) homeostasis. Nat. Cell Biol. 11, 769-776. doi: 10.1038/ncb1884.
86. Shimizu, N., Yoshikawa, N., Ito, N., Maruyama, T., Suzuki, Y., Takeda, S., et al. (2011). Crosstalk between glucocorticoid receptor and nutritional sensor mTOR in skeletal muscle. Cell Metab. 13, 170-182. doi: 10.1016/j.cmet.2011.01.001.
87. Smaili, S. S., Pereira, G. J., Costa, M. M., Rocha, K. K., Rodrigues, L., do Carmo, L. G., et al. (2013). The role of calcium stores in apoptosis and autophagy. Curr. Mol. Med. 13, 252-265. doi: 10.2174/156652413804810772.
88. Takeshima, H., Shimuta, M., Komazaki, S., Ohmi, K., Nishi, M., Iino, M., et al. (1998). Mitsugumin29, a novel synaptophysin family member from the triad junction in skeletal muscle. Biochem. J. 331(Pt 1), 317-322.
89. Targos, B., Baranska, J., and Pomorski, P. (2005). Store-operated calcium entry in physiology and pathology of mammalian cells. Acta Biochim. Pol. 52, 397-409.
90. Teixeira Vde, O., Filippin, L. I., and Xavier, R. M. (2012). Mechanisms of muscle wasting in sarcopenia. Rev. Bras. Reumatol. 52, 252-259. doi: 10.1590/S0482-50042012000200009.
91. Thiele, C., Hannah, M. J., Fahrenholz, F., and Huttner, W. B. (2000). Cholesterol binds to synaptophysin and is required for biogenesis of synaptic vesicles. Nat. Cell Biol. 2, 42-49. doi: 10.1038/71366.
92. Thomas, L., and Betz, H. (1990). Synaptophysin binds to physophilin, a putative synaptic plasma membrane protein. J. Cell Biol. 111(5 Pt 1), 2041-2052. doi: 10.1083/jcb.111.5.2041.
93. Thomas, L., Hartung, K., Langosch, D., Rehm, H., Bamberg, E., Franke, W. W., et al. (1988). Identification of synaptophysin as a hexameric channel protein of the synaptic vesicle membrane. Science 242, 1050-1053. doi: 10.1126/science.2461586.
94. Thomas, S. G., Takahashi, M., Neill, J. D., and Clarke, I. J. (1998). Components of the neuronal exocytotic machinery in the anterior pituitary of the ovariectomised ewe and the effects of oestrogen in gonadotropes as studied with confocal microscopy. Neuroendocrinology 67, 244-259. doi: 10.1159/000054320.
95. Tomas, F. M., Munro, H. N., and Young, V. R. (1979). Effect of glucocorticoid administration on the rate of muscle protein breakdown in vivo in rats, as measured by urinary excretion of N tau-methylhistidine. Biochem. J. 178, 139-146.
96. Tosch, V., Rohde, H. M., Tronchere, H., Zanoteli, E., Monroy, N., Kretz, C., et al. (2006). A novel PtdIns3P and PtdIns(3, 5)P2 phosphatase with an inactivating variant in centronuclear myopathy. Hum. Mol. Genet. 15, 3098-3106. doi: 10.1093/hmg/ddl250.
97. Turner, J., and Crossley, M. (1999). Basic Kruppel-like factor functions within a network of interacting haematopoietic transcription factors. Int. J. Biochem. Cell Biol. 31, 1169-1174. doi: 10.1016/S1357-2725(99)00067-9.
98. Urbano-Marquez, A., Estruch, R., Fernandez-Sola, J., Nicolas, J. M., Pare, J. C., and Rubin, E. (1995). The greater risk of alcoholic cardiomyopathy and myopathy in women compared with men. JAMA 274, 149-154. doi: 10.1001/jama.1995.03530020067034.
99. Urbano-Marquez, A., and Fernandez-Sola, J. (2004). Effects of alcohol on skeletal and cardiac muscle. Muscle Nerve 30, 689-707. doi: 10.1002/mus.20168.
100. Vergne, I., Roberts, E., Elmaoued, R. A., Tosch, V., Delgado, M. A., Proikas-Cezanne, T., et al. (2009). Control of autophagy initiation by phosphoinositide 3-phosphatase Jumpy. EMBO J. 28, 2244-2258. doi: 10.1038/emboj.2009.159.
101. Vos, T., Flaxman, A. D., Naghavi, M., Lozano, R., Michaud, C., Ezzati, M., et al. (2010). Years lived with disability (YLDs) for 1160 sequelae of 289 diseases and injuries 1990-2010, a systematic analysis for the Global Burden of Disease Study. Lancet 380, 2163-2196. doi: 10.1016/S0140-6736(12)61729-2.
102. Wallgren-Pettersson, C., Clarke, A., Samson, F., Fardeau, M., Dubowitz, V., Moser, H., et al. (1995). The myotubular myopathies: differential diagnosis of the X linked recessive, autosomal dominant, and autosomal recessive forms and present state of DNA studies. J. Med. Genet. 32, 673-679. doi: 10.1136/jmg.32.9.673.
103. Weisleder, N., Brotto, M., Komazaki, S., Pan, Z., Zhao, X., Nosek, T., et al. (2006). Muscle aging is associated with compromised Ca2+ spark signaling and segregated intracellular Ca2+ release. J. Cell Biol. 174, 639-645. doi: 10.1083/jcb.200604166.
104. Wishart, M. J., and Dixon, J. E. (2002). PTEN and myotubularin phosphatases: from 3-phosphoinositide dephosphorylation to disease. Trends Cell Biol. 12, 579-585. doi: 10.1016/S0962-8924(02)02412-1.
105. Yamamoto, J., Ikeda, Y., Iguchi, H., Fujino, T., Tanaka, T., Asaba, H., et al. (2004). A Kruppel-like factor KLF15 contributes fasting-induced transcriptional activation of mitochondrial acetyl-CoA synthetase gene AceCS2. J. Biol. Chem. 279, 16954-16962. doi: 10.1074/jbc.M312079200.
106. Yoshida, M., Minamisawa, S., Shimura, M., Komazaki, S., Kume, H., Zhang, M., et al. (2005). Impaired Ca2+ store functions in skeletal and cardiac muscle cells from sarcalumenin-deficient mice. J. Biol. Chem. 280, 3500-3506. doi: 10.1074/jbc.M406618200.
107. Zahn, J. M., Sonu, R., Vogel, H., Crane, E., Mazan-Mamczarz, K., Rabkin, R., et al. (2006). Transcriptional profiling of aging in human muscle reveals a common aging signature. PLoS Genet. 2:e115. doi: 10.1371/journal.pgen.0020115.
108. Zhao, X., Weisleder, N., Thornton, A., Oppong, Y., Campbell, R., Ma, J., et al. (2008). Compromised store-operated Ca2+ entry in aged skeletal muscle. Aging Cell 7, 561-568. doi: 10.1111/j.1474-9726.2008.00408.x.
109. Zhao, X., Yoshida, M., Brotto, L., Takeshima, H., Weisleder, N., Hirata, Y., et al. (2005). Enhanced resistance to fatigue and altered calcium handling properties of sarcalumenin knockout mice. Physiol. Genomics 23, 72-78. doi: 10.1152/physiolgenomics.00020.2005.
110. Zhu, X., and Birnbaumer, L. (1998). Calcium channels formed by mammalian Trp homologues. News Physiol. Sci. 13, 211-217.