Dysregulation of calcium homeostasis in muscular dystrophies

Ainara Vallejo-Illarramendi; Ivan Toral-Ojeda; Garazi Aldanondo; Adolfo López de Munain

doi:10.1017/erm.2014.17

Dysregulation of calcium homeostasis in muscular dystrophies

Published online by Cambridge University Press: 08 October 2014

Ainara Vallejo-Illarramendi ,

Ivan Toral-Ojeda ,

Garazi Aldanondo and

Adolfo López de Munain

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Ainara Vallejo-Illarramendi*: Affiliation:
Neuroscience Area, Biodonostia Institute, San Sebastian, Spain Centro de Investigación Biomédica en Red para Enfermedades Neurodegenerativas (CIBERNED), Instituto de Salud Carlos III, San Sebastian, Spain Euskampus, University of the Basque Country (UPV-EHU), San Sebastian, Spain
Ivan Toral-Ojeda: Affiliation:
Neuroscience Area, Biodonostia Institute, San Sebastian, Spain Centro de Investigación Biomédica en Red para Enfermedades Neurodegenerativas (CIBERNED), Instituto de Salud Carlos III, San Sebastian, Spain
Garazi Aldanondo: Affiliation:
Neuroscience Area, Biodonostia Institute, San Sebastian, Spain
Adolfo López de Munain: Affiliation:
Neuroscience Area, Biodonostia Institute, San Sebastian, Spain Centro de Investigación Biomédica en Red para Enfermedades Neurodegenerativas (CIBERNED), Instituto de Salud Carlos III, San Sebastian, Spain Department of Neuroscience, University of the Basque Country (UPV-EHU), San Sebastian, Spain Department of Neurology, Donostia Hospital, San Sebastian, Spain
*: *Corresponding author: Ainara Vallejo-Illarramendi, Instituto Biodonostia, Po Dr Begiristain s/n, 20014 San Sebastian, Spain. E-mail: ainaravallejo@yahoo.es

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Abstract

Muscular dystrophies are a group of diseases characterised by the primary wasting of skeletal muscle, which compromises patient mobility and in the most severe cases originate a complete paralysis and premature death. Existing evidence implicates calcium dysregulation as an underlying crucial event in the pathophysiology of several muscular dystrophies, such as dystrophinopathies, calpainopathies or myotonic dystrophy among others. Duchenne muscular dystrophy is the most frequent myopathy in childhood, and calpainopathy or LGMD2A is the most common form of limb-girdle muscular dystrophy, whereas myotonic dystrophy is the most frequent inherited muscle disease worldwide. In this review, we summarise recent advances in our understanding of calcium ion cycling through the sarcolemma, the sarcoplasmic reticulum and mitochondria, and its involvement in the pathogenesis of these dystrophies. We also discuss some of the clinical implications of recent findings regarding Ca2+ handling as well as novel approaches to treat muscular dystrophies targeting Ca2+ regulatory proteins.

Type: Review Article
Information: Expert Reviews in Molecular Medicine , Volume 16 , 2014 , e16

DOI: https://doi.org/10.1017/erm.2014.17 [Opens in a new window]
Copyright: Copyright © Cambridge University Press 2014

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References

1Berridge, M.J., Bootman, M.D. and Roderick, H.L. (2003) Calcium signalling: dynamics, homeostasis and remodelling. Nature Reviews Molecular Cell Biology 4, 517-529CrossRef Google Scholar PubMed

2Leong, P. and MacLennan, D.H. (1998) Complex interactions between skeletal muscle ryanodine receptor and dihydropyridine receptor proteins. Biochemistry and Cell Biology 76, 681-694CrossRef Google Scholar PubMed

3Melzer, W., Herrmann-Frank, A. and Luttgau, H.C. (1995) The role of Ca²⁺ ions in excitation–contraction coupling of skeletal muscle fibres. Biochimica et Biophysica Acta 1241, 59-116CrossRef Google Scholar PubMed

4Murray, B.E. et al. (1998) Excitation–contraction–relaxation cycle: role of Ca²⁺-regulatory membrane proteins in normal, stimulated and pathological skeletal muscle (review). International Journal of Molecular Medicine 1, 677-687Google Scholar PubMed

5Baylor, S.M. and Hollingworth, S. (2012) Intracellular calcium movements during excitation–contraction coupling in mammalian slow-twitch and fast-twitch muscle fibers. Journal of General Physiology 139, 261-272CrossRef Google Scholar PubMed

6Chin, E.R. and Allen, D.G. (1996) The role of elevations in intracellular [Ca²⁺] in the development of low frequency fatigue in mouse single muscle fibres. Journal of Physiology 491(Pt 3), 813-824CrossRef Google Scholar PubMed

7Allen, D.G., Lamb, G.D. and Westerblad, H. (2008) Impaired calcium release during fatigue. Journal of Applied Physiology 104, 296-305CrossRef Google Scholar PubMed

8Andersson, D.C. et al. (2011) Ryanodine receptor oxidation causes intracellular calcium leak and muscle weakness in aging. Cell Metabolism 14, 196-207CrossRef Google Scholar PubMed

9Alderton, J.M. and Steinhardt, R.A. (2000) How calcium influx through calcium leak channels is responsible for the elevated levels of calcium-dependent proteolysis in dystrophic myotubes. Trends in Cardiovascular Medicine 10, 268-272CrossRef Google Scholar PubMed

10Culligan, K. and Ohlendieck, K. (2002) Diversity of the brain dystrophin–glycoprotein complex. Journal of Biomedicine and Biotechnology 2, 31-36CrossRef Google Scholar PubMed

11Gailly, P. (2002) New aspects of calcium signaling in skeletal muscle cells: implications in Duchenne muscular dystrophy. Biochimica et Biophysica Acta 1600, 38-44CrossRef Google Scholar PubMed

12Gillis, J.M. (1996) Membrane abnormalities and Ca homeostasis in muscles of the mdx mouse, an animal model of the Duchenne muscular dystrophy: a review. Acta Physiologica Scandinavica 156, 397-406CrossRef Google Scholar PubMed

13Ruegg, U.T. et al. (2002) Pharmacological control of cellular calcium handling in dystrophic skeletal muscle. Neuromuscular Disorders 12(Suppl 1), S155-S161CrossRef Google Scholar PubMed

14Schiaffino, S. and Reggiani, C. (2011) Fiber types in mammalian skeletal muscles. Physiological Reviews 91, 1447-1531CrossRef Google Scholar PubMed

15Purves, D. and Williams, S.M. (2001) Neuroscience ( 2nd edn).Sinauer Associates, Sunderland, Mass.Google Scholar

16Scott, W., Stevens, J. and Binder-Macleod, S.A. (2001) Human skeletal muscle fiber type classifications. Physical Therapy 81, 1810-1816CrossRef Google Scholar PubMed

17Lamboley, C.R., et al. (2013) Endogenous and maximal sarcoplasmic reticulum calcium content and calsequestrin expression in type I and type II human skeletal muscle fibres. Journal of Physiology 591(Pt 23), 6053-6068CrossRef Google Scholar PubMed

18Lamboley, C.R., et al. (2014) Sarcoplasmic reticulum Ca²⁺ uptake and leak properties, and SERCA isoform expression, in type I and type II fibres of human skeletal muscle. Journal of Physiology 592(Pt 6), 1381-1395CrossRef Google Scholar PubMed

19Pette, D. and Staron, R.S. (1997) Mammalian skeletal muscle fiber type transitions. International Review of Cytology 170, 143-223CrossRef Google Scholar PubMed

20Webster, C. et al. (1988) Fast muscle fibers are preferentially affected in Duchenne muscular dystrophy. Cell 52, 503-513CrossRef Google Scholar PubMed

21Kramerova, I. et al. (2012) Impaired calcium calmodulin kinase signaling and muscle adaptation response in the absence of calpain 3. Human Molecular Genetics 21, 3193-3204CrossRef Google Scholar PubMed

22Zeiger, U., Mitchell, C.H. and Khurana, T.S. (2010) Superior calcium homeostasis of extraocular muscles. Experimental Eye Research 91, 613-622CrossRef Google Scholar PubMed

23Stutzmann, G.E. and Mattson, M.P. (2011) Endoplasmic reticulum Ca⁽²⁺⁾ handling in excitable cells in health and disease. Pharmacological Reviews 63, 700-727CrossRef Google Scholar PubMed

24Franzini-Armstrong, C. and Jorgensen, A.O. (1994) Structure and development of E–C coupling units in skeletal muscle. Annual Review of Physiology 56, 509-534CrossRef Google Scholar PubMed

25Periasamy, M. and Kalyanasundaram, A. (2007) SERCA pump isoforms: their role in calcium transport and disease. Muscle & Nerve 35, 430-442CrossRef Google Scholar PubMed

26Sacchetto, R. et al. (1996) Colocalization of the dihydropyridine receptor, the plasma-membrane calcium ATPase isoform 1 and the sodium/calcium exchanger to the junctional-membrane domain of transverse tubules of rabbit skeletal muscle. European Journal of Biochemistry 237, 483-488CrossRef Google Scholar

27Gilabert, J.A. (2012) Cytoplasmic calcium buffering. Advances in Experimental Medicines and Biology 740, 483-498CrossRef Google Scholar PubMed

28Schwaller, B. et al. (1999) Prolonged contraction-relaxation cycle of fast-twitch muscles in parvalbumin knockout mice. American Journal of Physiology 276(2 Pt 1), C395-C403CrossRef Google Scholar PubMed

29Heizmann, C.W., Berchtold, M.W. and Rowlerson, A.M. (1982) Correlation of parvalbumin concentration with relaxation speed in mammalian muscles. Proceedings of the National Academy of Sciences of the United States of America 79, 7243-7247CrossRef Google Scholar PubMed

30Kurebayashi, N. and Ogawa, Y. (2001) Depletion of Ca²⁺ in the sarcoplasmic reticulum stimulates Ca²⁺ entry into mouse skeletal muscle fibres. Journal of Physiology 533(Pt 1), 185-199CrossRef Google Scholar PubMed

31Pan, Z. et al. (2002) Dysfunction of store-operated calcium channel in muscle cells lacking mg29. Nature Cell Biology 4, 379-383CrossRef Google Scholar PubMed

32Rosenberg, P. et al. (2004) TRPC3 channels confer cellular memory of recent neuromuscular activity. Proceedings of the National Academy of Sciences of the United States of America 101, 9387-9392CrossRef Google Scholar PubMed

33Stiber, J. et al. (2008) STIM1 signalling controls store-operated calcium entry required for development and contractile function in skeletal muscle. Nature Cell Biology 10, 688-697CrossRef Google Scholar PubMed

34Darbellay, B. et al. (2009) STIM1- and Orai1-dependent store-operated calcium entry regulates human myoblast differentiation. Journal of Biological Chemistry 284, 5370-5380CrossRef Google Scholar PubMed

35Cherednichenko, G. et al. (2004) Conformational activation of Ca²⁺ entry by depolarization of skeletal myotubes. Proceedings of the National Academy of Sciences of the United States of America 101, 15793-15798CrossRef Google Scholar PubMed

36Haws, C.M. and Lansman, J.B. (1991) Developmental regulation of mechanosensitive calcium channels in skeletal muscle from normal and mdx mice. Proceedings of the Royal Society B: Biological Sciences 245, 173-177Google Scholar PubMed

37Suzuki, M. et al. (1999) Cloning of a stretch-inhibitable nonselective cation channel. Journal of Biological Chemistry 274, 6330-6335CrossRef Google Scholar PubMed

38Hopf, F.W. et al. (1996) A capacitative calcium current in cultured skeletal muscle cells is mediated by the calcium-specific leak channel and inhibited by dihydropyridine compounds. Journal of Biological Chemistry 271, 22358-223567CrossRef Google Scholar PubMed

39Vandebrouck, A. et al. (2006) Regulation of store-operated calcium entries and mitochondrial uptake by minidystrophin expression in cultured myotubes. FASEB Journal 20, 136-138CrossRef Google Scholar PubMed

40Vandebrouck, C. et al. (2002) Involvement of TRPC in the abnormal calcium influx observed in dystrophic (mdx) mouse skeletal muscle fibers. Journal of Cell Biology 158, 1089-1096CrossRef Google Scholar PubMed

41Al-Qusairi, L. and Laporte, J. (2011) T-tubule biogenesis and triad formation in skeletal muscle and implication in human diseases. Skeletal Muscle 1, 26CrossRef Google Scholar PubMed

42Rossi, A.E. and Dirksen, R.T. (2006) Sarcoplasmic reticulum: the dynamic calcium governor of muscle. Muscle & Nerve 33, 715-731CrossRef Google Scholar PubMed

43Murphy, R.M. et al. (2009) Calsequestrin content and SERCA determine normal and maximal Ca²⁺ storage levels in sarcoplasmic reticulum of fast- and slow-twitch fibres of rat. Journal of Physiology 587(Pt 2), 443-460CrossRef Google Scholar PubMed

44Arvanitis, D.A. et al. (2007) Histidine-rich Ca-binding protein interacts with sarcoplasmic reticulum Ca-ATPase. American Journal of Physiology: Heart and Circulatory Physiology 293, H1581-H1589Google Scholar PubMed

45Lee, H.G. et al. (2001) Interaction of HRC (histidine-rich Ca⁽²⁺⁾-binding protein) and triadin in the lumen of sarcoplasmic reticulum. Journal of Biological Chemistry 276, 39533-39538CrossRef Google Scholar PubMed

46Paolini, C. et al. (2007) Reorganized stores and impaired calcium handling in skeletal muscle of mice lacking calsequestrin-1. Journal of Physiology 583(Pt 2), 767-784CrossRef Google Scholar PubMed

47Beard, N.A., Wei, L. and Dulhunty, A.F. (2009) Control of muscle ryanodine receptor calcium release channels by proteins in the sarcoplasmic reticulum lumen. Clinical and Experimental Pharmacology and Physiology 36, 340-345CrossRef Google Scholar PubMed

48Sztretye, M. et al. (2011) Measurement of RyR permeability reveals a role of calsequestrin in termination of SR Ca⁽²⁺⁾ release in skeletal muscle. Journal of General Physiology 138, 231-247CrossRef Google Scholar PubMed

49Capes, E.M., Loaiza, R. and Valdivia, H.H. (2011) Ryanodine receptors. Skeletal Muscle 1, 18CrossRef Google Scholar PubMed

50Mackrill, J.J. (2010) Ryanodine receptor calcium channels and their partners as drug targets. Biochemistry and Pharmacology 79, 1535-1543CrossRef Google Scholar PubMed

51Van Petegem, F. (2012) Ryanodine receptors: structure and function. Journal of Biological Chemistry 287, 31624-31632CrossRef Google Scholar PubMed

52Mackrill, J.J. (2012) Ryanodine receptor calcium release channels: an evolutionary perspective. Advances in Experimental Medicines and Biology 740, 159-182CrossRef Google Scholar PubMed

53Andersson, D.C., et al. (2012) Stress-induced increase in skeletal muscle force requires protein kinase A phosphorylation of the ryanodine receptor. Journal of Physiology 590(Pt 24), 6381-6387CrossRef Google Scholar PubMed

54Ward, C.W. et al. (2003) Defects in ryanodine receptor calcium release in skeletal muscle from post-myocardial infarct rats. FASEB Journal 17, 1517-1519CrossRef Google Scholar PubMed

55Reiken, S. et al. (2003) PKA phosphorylation activates the calcium release channel (ryanodine receptor) in skeletal muscle: defective regulation in heart failure. Journal of Cell Biology 160, 919-928CrossRef Google Scholar PubMed

56Jiang, D., et al. (2008) Reduced threshold for luminal Ca²⁺ activation of RyR1 underlies a causal mechanism of porcine malignant hyperthermia. Journal of Biological Chemistry 283, 20813-20820CrossRef Google Scholar PubMed

57Palade, P., Mitchell, R.D. and Fleischer, S. (1983) Spontaneous calcium release from sarcoplasmic reticulum. General description and effects of calcium. Journal of Biological Chemistry 258, 8098-8107CrossRef Google Scholar PubMed

58MacLennan, D.H. and Chen, S.R. (2009) Store overload-induced Ca²⁺ release as a triggering mechanism for CPVT and MH episodes caused by mutations in RYR and CASQ genes. Journal of Physiology 587(Pt 13), 3113-3115CrossRef Google Scholar PubMed

59Marks, A.R. (1997) Intracellular calcium-release channels: regulators of cell life and death. American Journal of Physiology 272(2 Pt 2), H597-H605Google Scholar PubMed

60Blaauw, B. et al. (2012) No evidence for inositol 1,4,5-trisphosphate-dependent Ca²⁺ release in isolated fibers of adult mouse skeletal muscle. Journal of General Physiology 140, 235-241CrossRef Google Scholar PubMed

61Zayas, R., Groshong, J.S. and Gomez, C.M. (2007) Inositol-1,4,5-triphosphate receptors mediate activity-induced synaptic Ca²⁺ signals in muscle fibers and Ca²⁺ overload in slow-channel syndrome. Cell Calcium 41, 343-352CrossRef Google Scholar PubMed

62Tjondrokoesoemo, A. et al. (2013) Type 1 inositol (1,4,5)-trisphosphate receptor activates ryanodine receptor 1 to mediate calcium spark signaling in adult mammalian skeletal muscle. Journal of Biological Chemistry 288, 2103-2109CrossRef Google Scholar PubMed

63Maack, C. and O'Rourke, B. (2007) Excitation–contraction coupling and mitochondrial energetics. Basic Research in Cardiology 102, 369-392CrossRef Google Scholar PubMed

64Macdonald, W.A. and Stephenson, D.G. (2001) Effects of ADP on sarcoplasmic reticulum function in mechanically skinned skeletal muscle fibres of the rat. Journal of Physiology 532(Pt 2), 499-508CrossRef Google Scholar PubMed

65MacLennan, D.H., Asahi, M. and Tupling, A.R. (2003) The regulation of SERCA-type pumps by phospholamban and sarcolipin. Annals of the New York Academy of Sciences 986, 472-480CrossRef Google Scholar PubMed

66Lancel, S. et al. (2010) Oxidative posttranslational modifications mediate decreased SERCA activity and myocyte dysfunction in Galphaq-overexpressing mice. Circulation Research 107, 228-232CrossRef Google Scholar PubMed

67Vangheluwe, P. et al. (2005) Modulating sarco(endo)plasmic reticulum Ca²⁺ ATPase 2 (SERCA2) activity: cell biological implications. Cell Calcium 38, 291-302CrossRef Google Scholar PubMed

68Bigelow, D.J. (2009) Nitrotyrosine-modified SERCA2: a cellular sensor of reactive nitrogen species. Pflugers Archiv 457, 701-710CrossRef Google Scholar PubMed

69Franzini-Armstrong, C. (2007) ER-mitochondria communication. How privileged? Physiology (Bethesda) 22, 261-268Google Scholar PubMed

70Eisenberg, B.R. (2011) Quantitative ultrastructure of mammalian skeletal muscle. Comprehensive Physiology, Supplement 27: Handbook of Physiology, Skeletal Muscle: 73-112.Google Scholar

71Hajnoczky, G. et al. (2000) The machinery of local Ca²⁺ signalling between sarco-endoplasmic reticulum and mitochondria. Journal of Physiology 529 (Pt 1), 69-81CrossRef Google Scholar PubMed

72Rizzuto, R. et al. (2009) Ca⁽²⁺⁾ transfer from the ER to mitochondria: when, how and why. Biochimica et Biophysica Acta 1787, 1342-1351CrossRef Google Scholar PubMed

73Challet, C. et al. (2001) Mitochondrial calcium oscillations in C2C12 myotubes. Journal of Biological Chemistry 276, 3791-3797CrossRef Google Scholar PubMed

74Kavanagh, N.I., Ainscow, E.K. and Brand, M.D. (2000) Calcium regulation of oxidative phosphorylation in rat skeletal muscle mitochondria. Biochimica et Biophysica Acta 1457, 57-70CrossRef Google Scholar PubMed

75Yi, J. et al. (2011) Mitochondrial calcium uptake regulates rapid calcium transients in skeletal muscle during excitation–contraction (E–C) coupling. Journal of Biological Chemistry 286, 32436-32443CrossRef Google Scholar PubMed

76Pizzo, P. et al. (2012) Mitochondrial Ca⁽²⁺⁾ homeostasis: mechanism, role, and tissue specificities. Pflugers Archiv 464, 3-17CrossRef Google Scholar

77Ascah, A. et al. (2011) Stress-induced opening of the permeability transition pore in the dystrophin-deficient heart is attenuated by acute treatment with sildenafil. American Journal of Physiology: Heart and Circulatory Physiology 300, H144-H153Google Scholar PubMed

78Fraysse, B. et al. (2010) Ca²⁺ overload and mitochondrial permeability transition pore activation in living delta-sarcoglycan-deficient cardiomyocytes. American Journal of Physiology: Cell Physiology 299, C706-C713CrossRef Google Scholar PubMed

79Logan, C.V. et al. (2014) Loss-of-function mutations in MICU1 cause a brain and muscle disorder linked to primary alterations in mitochondrial calcium signaling. Nature Genetics 46, 188-193CrossRef Google Scholar

80Emery, A.E. (2002) The muscular dystrophies. Lancet 359, 687-695CrossRef Google Scholar PubMed

81Hoffman, E.P., Brown, R.H. Jr. and Kunkel, L.M. (1987) Dystrophin: the protein product of the Duchenne muscular dystrophy locus. Cell 51, 919-928CrossRef Google Scholar PubMed

82Blake, D.J., et al. (2002) Function and genetics of dystrophin and dystrophin-related proteins in muscle. Physiological Reviews 82, 291-329CrossRef Google Scholar PubMed

83Petrof, B.J. et al. (1993) Dystrophin protects the sarcolemma from stresses developed during muscle contraction. Proceedings of the National Academy of Sciences of the United States of America 90, 3710-3714CrossRef Google Scholar PubMed

84Allen, D.G. et al. (2010) Calcium and the damage pathways in muscular dystrophy. Canadian Journal of Physiology and Pharmacology 88, 83-91CrossRef Google Scholar PubMed

85Bodensteiner, J.B. and Engel, A.G. (1978) Intracellular calcium accumulation in Duchenne dystrophy and other myopathies: a study of 567,000 muscle fibers in 114 biopsies. Neurology 28, 439-446CrossRef Google Scholar PubMed

86Millay, D.P., et al. (2009) Calcium influx is sufficient to induce muscular dystrophy through a TRPC-dependent mechanism. Proceedings of the National Academy of Sciences of the United States of America 106, 19023-19028CrossRef Google Scholar PubMed

87Bertorini, T.E., et al. (1984) Calcium and magnesium content in fetuses at risk and prenecrotic Duchenne muscular dystrophy. Neurology 34, 1436-1440CrossRef Google Scholar PubMed

88Turner, P.R. et al. (1988) Increased protein degradation results from elevated free calcium levels found in muscle from mdx mice. Nature 335, 735-738CrossRef Google Scholar PubMed

89Yeung, E.W. et al. (2005) Effects of stretch-activated channel blockers on [Ca²⁺]i and muscle damage in the mdx mouse. Journal of Physiology 562(Pt 2), 367-380CrossRef Google Scholar

90Fong, P.Y., et al. (1990) Increased activity of calcium leak channels in myotubes of Duchenne human and mdx mouse origin. Science 250, 673-676CrossRef Google Scholar PubMed

91Franco, A. Jr. and Lansman, J.B. (1990) Calcium entry through stretch-inactivated ion channels in mdx myotubes. Nature 344, 670-673CrossRef Google Scholar PubMed

92Vandebrouck, A. et al. (2007) Regulation of capacitative calcium entries by alpha1-syntrophin: association of TRPC1 with dystrophin complex and the PDZ domain of alpha1-syntrophin. FASEB Journal 21, 608-617CrossRef Google Scholar PubMed

93Deval, E., et al. (2002) Na⁽⁺⁾/Ca⁽²⁺⁾ exchange in human myotubes: intracellular calcium rises in response to external sodium depletion are enhanced in DMD. Neuromuscular Disorders 12, 665-673CrossRef Google Scholar

94Lyfenko, A.D. and Dirksen, R.T. (2008) Differential dependence of store-operated and excitation–coupled Ca²⁺ entry in skeletal muscle on STIM1 and Orai1. Journal of Physiology 586(Pt 20), 4815-4824CrossRef Google Scholar PubMed

95Edwards, J.N. et al. (2010) Upregulation of store-operated Ca²⁺ entry in dystrophic mdx mouse muscle. American Journal of Physiology: Cell Physiology 299, C42-C50CrossRef Google Scholar PubMed

96Zhao, X. et al. (2012) Orai1 mediates exacerbated Ca⁽²⁺⁾ entry in dystrophic skeletal muscle. PLoS ONE 7, e49862CrossRef Google Scholar PubMed

97Sabourin, J. et al. (2012) Dystrophin/alpha1-syntrophin scaffold regulated PLC/PKC-dependent store-operated calcium entry in myotubes. Cell Calcium 52, 445-456CrossRef Google Scholar PubMed

98Boittin, F.X. et al. (2010) Phospholipase A2-derived lysophosphatidylcholine triggers Ca²⁺ entry in dystrophic skeletal muscle fibers. Biochemical and Biophysical Research Communications 391, 401-406CrossRef Google Scholar PubMed

99Lindahl, M. et al. (1995) Phospholipase A2 activity in dystrophinopathies. Neuromuscular Disorders 5, 193-199CrossRef Google Scholar PubMed

100Ismail, H.M. et al. (2013) Inhibition of iPLA2 beta and of stretch-activated channels by doxorubicin alters dystrophic muscle function. British Journal of Pharmacology 169, 1537-1550CrossRef Google Scholar PubMed

101Bellinger, A.M. et al. (2009) Hypernitrosylated ryanodine receptor calcium release channels are leaky in dystrophic muscle. Nature Medicine 15, 325-330CrossRef Google Scholar PubMed

102Brillantes, A.B. et al. (1994) Stabilization of calcium release channel (ryanodine receptor) function by FK506-binding protein. Cell 77, 513-523CrossRef Google Scholar PubMed

103Bellinger, A.M. et al. (2008) Remodeling of ryanodine receptor complex causes “leaky” channels: a molecular mechanism for decreased exercise capacity. Proceedings of the National Academy of Sciences of the United States of America 105, 2198-202CrossRef Google Scholar PubMed

104Altamirano, F. et al. (2012) Increased resting intracellular calcium modulates NF-kappaB-dependent inducible nitric-oxide synthase gene expression in dystrophic mdx skeletal myotubes. Journal of Biological Chemistry 287, 20876-20887CrossRef Google Scholar PubMed

105Liberona, J.L. et al. (1998) Differences in both inositol 1,4,5-trisphosphate mass and inositol 1,4,5-trisphosphate receptors between normal and dystrophic skeletal muscle cell lines. Muscle & Nerve 21, 902-9093.0.CO;2-A>CrossRef Google Scholar PubMed

106Basset, O. et al. (2004) Involvement of inositol 1,4,5-trisphosphate in nicotinic calcium responses in dystrophic myotubes assessed by near-plasma membrane calcium measurement. Journal of Biological Chemistry 279, 47092-47100CrossRef Google Scholar PubMed

107Cardenas, C. et al. (2010) Abnormal distribution of inositol 1,4,5-trisphosphate receptors in human muscle can be related to altered calcium signals and gene expression in Duchenne dystrophy-derived cells. FASEB Journal 24, 3210-3221CrossRef Google Scholar PubMed

108Balghi, H. et al. (2006) Mini-dystrophin expression down-regulates overactivation of G protein-mediated IP3 signaling pathway in dystrophin-deficient muscle cells. Journal of General Physiology 127, 171-182CrossRef Google Scholar PubMed

109Robert, V. et al. (2001) Alteration in calcium handling at the subcellular level in mdx myotubes. Journal of Biological Chemistry 276, 4647-4651CrossRef Google Scholar PubMed

110Basset, O. et al. (2006) Bcl-2 overexpression prevents calcium overload and subsequent apoptosis in dystrophic myotubes. Biochemical Journal 395, 267-276CrossRef Google Scholar PubMed

111Giacomotto, J. et al. (2013) Chemical genetics unveils a key role of mitochondrial dynamics, cytochrome c release and IP3R activity in muscular dystrophy. Human Molecular Genetics 22, 4562-4578CrossRef Google Scholar PubMed

112Williams, I.A. and Allen, D.G. (2007) Intracellular calcium handling in ventricular myocytes from mdx mice. American Journal of Physiology: Heart and Circulatory Physiology 292, H846-H855Google Scholar PubMed

113Jung, C. et al. (2008) Dystrophic cardiomyopathy: amplification of cellular damage by Ca²⁺ signalling and reactive oxygen species-generating pathways. Cardiovascular Research 77, 766-773CrossRef Google Scholar PubMed

114Viola, H.M. et al. (2013) L-type Ca⁽²⁺⁾ channel contributes to alterations in mitochondrial calcium handling in the mdx ventricular myocyte. American Journal of Physiology: Heart and Circulatory Physiology 304, H767-H775Google Scholar PubMed

115Khairallah, M. et al. (2007) Metabolic and signaling alterations in dystrophin-deficient hearts precede overt cardiomyopathy. Journal of Molecular Cell Cardiology 43, 119-129CrossRef Google Scholar PubMed

116Robin, G., Berthier, C. and Allard, B. (2012) Sarcoplasmic reticulum Ca²⁺ permeation explored from the lumen side in mdx muscle fibers under voltage control. Journal of General Physiology 139, 209-218CrossRef Google Scholar PubMed

117Goonasekera, S.A. et al. (2011) Mitigation of muscular dystrophy in mice by SERCA overexpression in skeletal muscle. Journal of Clinical Investigation 121, 1044-1052CrossRef Google Scholar PubMed

118Gehrig, S.M. et al. (2012) Hsp72 preserves muscle function and slows progression of severe muscular dystrophy. Nature 484, 394-398CrossRef Google Scholar PubMed

119Culligan, K. et al. (2002) Drastic reduction of calsequestrin-like proteins and impaired calcium binding in dystrophic mdx muscle. Journal of Applied Physiology 92, 435-445CrossRef Google Scholar PubMed

120Doran, P. et al. (2004) Subproteomics analysis of Ca⁺-binding proteins demonstrates decreased calsequestrin expression in dystrophic mouse skeletal muscle. European Journal of Biochemistry 271, 3943-3952CrossRef Google Scholar PubMed

121Dowling, 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. Biochemical Journal 379(Pt 2), 479-488CrossRef Google Scholar

122Ferretti, R. et al. (2009) Sarcoplasmic-endoplasmic-reticulum Ca²⁺-ATPase and calsequestrin are overexpressed in spared intrinsic laryngeal muscles of dystrophin-deficient mdx mice. Muscle & Nerve 39, 609-615CrossRef Google Scholar PubMed

123Pertille, A. et al. (2010) Calcium-binding proteins in skeletal muscles of the mdx mice: potential role in the pathogenesis of Duchenne muscular dystrophy. International Journal of Experimental Pathology 91, 63-71CrossRef Google Scholar PubMed

124Laval, S.H. and Bushby, K.M. (2004) Limb-girdle muscular dystrophies – from genetics to molecular pathology. Neuropathology and Applied Neurobiology 30, 91-105CrossRef Google Scholar PubMed

125Saenz, A., et al. (2005) LGMD2A: genotype–phenotype correlations based on a large mutational survey on the calpain 3 gene. Brain 128(Pt 4), 732-742CrossRef Google Scholar PubMed

126Urtasun, M., et al. (1998) Limb-girdle muscular dystrophy in Guipuzcoa (Basque Country, Spain). Brain 121 (Pt 9), 1735-1747CrossRef Google Scholar PubMed

127Hauerslev, S. et al. (2012) Calpain 3 is important for muscle regeneration: evidence from patients with limb girdle muscular dystrophies. BMC Musculoskeletal Disorders 13, 43CrossRef Google Scholar PubMed

128Richard, I. et al. (1995) Mutations in the proteolytic enzyme calpain 3 cause limb-girdle muscular dystrophy type 2A. Cell 81, 27-40CrossRef Google Scholar PubMed

129Beckmann, J.S. and Spencer, M. (2008) Calpain 3, the “gatekeeper” of proper sarcomere assembly, turnover and maintenance. Neuromuscular Disorders 18, 913-921CrossRef Google Scholar PubMed

130Murphy, R.M. and Lamb, G.D. (2009) Endogenous calpain-3 activation is primarily governed by small increases in resting cytoplasmic [Ca²⁺] and is not dependent on stretch. Journal of Biological Chemistry 284, 7811-7819CrossRef Google Scholar

131Kramerova, I. et al. (2004) Null mutation of calpain 3 (p94) in mice causes abnormal sarcomere formation in vivo and in vitro. Human Molecular Genetics 13, 1373-1388CrossRef Google Scholar PubMed

132Ojima, K. et al. (2011) Non-proteolytic functions of calpain-3 in sarcoplasmic reticulum in skeletal muscles. Journal of Molecular Biology 407, 439-449CrossRef Google Scholar PubMed

133Kramerova, I. et al. (2008) Novel role of calpain-3 in the triad-associated protein complex regulating calcium release in skeletal muscle. Human Molecular Genetics 17, 3271-3280CrossRef Google Scholar PubMed

134Dayanithi, G. et al. (2009) Alteration of sarcoplasmic reticulum Ca²⁺ release in skeletal muscle from calpain 3-deficient mice. International Journal of Cell Biology 2009, 340-346CrossRef Google Scholar PubMed

135Kockskamper, J., Zima, A.V. and Blatter, L.A. (2005) Modulation of sarcoplasmic reticulum Ca²⁺ release by glycolysis in cat atrial myocytes. Journal of Physiology 564(Pt 3), 697-714CrossRef Google Scholar PubMed

136Seo, I.R. et al. (2006) Aldolase potentiates DIDS activation of the ryanodine receptor in rabbit skeletal sarcoplasmic reticulum. Biochemistry Journal 399, 325-333CrossRef Google Scholar PubMed

137Kreuder, J. et al. (1996) Brief report: inherited metabolic myopathy and hemolysis due to a mutation in aldolase A. New England Journal of Medicine 334, 1100-1104CrossRef Google Scholar PubMed

138Yao, D.C. et al. (2004) Hemolytic anemia and severe rhabdomyolysis caused by compound heterozygous mutations of the gene for erythrocyte/muscle isozyme of aldolase, ALDOA(Arg303X/Cys338Tyr). Blood 103, 2401-2403CrossRef Google Scholar PubMed

139Sacchetto, R., et al. (2000) Coordinate expression of Ca²⁺-ATPase slow-twitch isoform and of beta calmodulin-dependent protein kinase in phospholamban-deficient sarcoplasmic reticulum of rabbit masseter muscle. FEBS Letters 481, 255-260CrossRef Google Scholar PubMed

140Rose, A.J. et al. (2007) Regulation and function of Ca²⁺-calmodulin-dependent protein kinase II of fast-twitch rat skeletal muscle. Journal of Physiology 580(Pt.3), 993-1005CrossRef Google Scholar PubMed

141Kramerova, I., Beckmann, J.S. and Spencer, M.J. (2007) Molecular and cellular basis of calpainopathy (limb girdle muscular dystrophy type 2A). Biochimica et Biophysica Acta 1772, 128-44CrossRef Google Scholar PubMed

142Kramerova, I. et al. (2009) Mitochondrial abnormalities, energy deficit and oxidative stress are features of calpain 3 deficiency in skeletal muscle. Human Molecular Genetics 18(17), 3194-3205CrossRef Google Scholar PubMed

143Harper, P.S. (2009) Myotonic dystrophy (2nd edn).Oxford University Press, Oxford, New YorkCrossRef Google Scholar

144Brook, J.D. et al. (1992) Molecular basis of myotonic dystrophy: expansion of a trinucleotide (CTG) repeat at the 3′ end of a transcript encoding a protein kinase family member. Cell 68, 799-808CrossRef Google Scholar PubMed

145Dansithong, W. et al. (2005) MBNL1 is the primary determinant of focus formation and aberrant insulin receptor splicing in DM1. Journal of Biological Chemistry 280, 5773-5780CrossRef Google Scholar PubMed

146Philips, A.V., Timchenko, L.T. and Cooper, T.A. (1998) Disruption of splicing regulated by a CUG-binding protein in myotonic dystrophy. Science 280, 737-741CrossRef Google Scholar PubMed

147Timchenko, N.A. et al. (2001) RNA CUG repeats sequester CUGBP1 and alter protein levels and activity of CUGBP1. Journal of Biological Chemistry 276, 7820-7826CrossRef Google Scholar PubMed

148Tang, Z.Z. et al. (2012) Muscle weakness in myotonic dystrophy associated with misregulated splicing and altered gating of Ca(V)1.1 calcium channel. Human Molecular Genetics 21, 1312-1324CrossRef Google Scholar PubMed

149Kimura, T. et al. (2005) Altered mRNA splicing of the skeletal muscle ryanodine receptor and sarcoplasmic/endoplasmic reticulum Ca²⁺-ATPase in myotonic dystrophy type 1. Human Molecular Genetics 14, 2189-2200CrossRef Google Scholar PubMed

150Santoro, M. et al. (2014) Alternative splicing alterations of Ca⁽²⁺⁾ handling genes are associated with Ca⁽²⁺⁾ signal dysregulation in myotonic dystrophy type 1 (DM1) and type 2 (DM2) myotubes. Neuropathology and Applied Neurobiology 40, 464-476CrossRef Google Scholar PubMed

151Benders, A.A. et al. (1997) Myotonic dystrophy protein kinase is involved in the modulation of the Ca²⁺ homeostasis in skeletal muscle cells. Journal of Clinical Investigation 100, 1440-1447CrossRef Google Scholar PubMed

152Jacobs, A.E. et al. (1990) The calcium homeostasis and the membrane potential of cultured muscle cells from patients with myotonic dystrophy. Biochimica et Biophysica Acta 1096, 14-19CrossRef Google Scholar PubMed

153Vihola, A. et al. (2013) Altered expression and splicing of Ca⁽²⁺⁾ metabolism genes in myotonic dystrophies DM1 and DM2. Neuropathology and Applied Neurobiology 39, 390-405CrossRef Google Scholar PubMed

154Murphy, R.M. et al. (2013) Ca²⁺-dependent proteolysis of junctophilin-1 and junctophilin-2 in skeletal and cardiac muscle. Journal of Physiology 591(Pt 3), 719-729CrossRef Google Scholar PubMed

155Toral-Ojeda, I., Aldanondo, G. and Vallejo-Illarramendi, A. (2013) Junctophilins and mu-calpain: partners in excitation–contraction uncoupling. Journal of Physiology 591(Pt 15), 3679-3680CrossRef Google Scholar PubMed

156Andersson, D.C. et al. (2012) Leaky ryanodine receptors in beta-sarcoglycan deficient mice: a potential common defect in muscular dystrophy. Skeletal Muscle 2, 9CrossRef Google Scholar PubMed

157Kendall, G.C. et al. (2012) Dantrolene enhances antisense-mediated exon skipping in human and mouse models of Duchenne muscular dystrophy. Science Translational Medicine 4, 164ra160.CrossRef Google Scholar PubMed

158Altamirano, F. et al. (2013) Nifedipine treatment reduces resting calcium concentration, oxidative and apoptotic gene expression, and improves muscle function in dystrophic mdx mice. PLoS ONE 8, e81222CrossRef Google Scholar PubMed

159Matsumura, C.Y. et al. (2009) Diltiazem and verapamil protect dystrophin-deficient muscle fibers of MDX mice from degeneration: a potential role in calcium buffering and sarcolemmal stability. Muscle & Nerve 39, 167-176CrossRef Google Scholar PubMed

160Phillips, M.F. and Quinlivan, R. (2008) Calcium antagonists for Duchenne muscular dystrophy. Cochrane Database of Systematic Reviews 4, CD004571Google Scholar

161Iwata, Y. et al. (2009) Dominant-negative inhibition of Ca²⁺ influx via TRPV2 ameliorates muscular dystrophy in animal models. Human Molecular Genetics 18, 824-834CrossRef Google Scholar PubMed

162Finsterer, J. and Cripe, L. (2014) Treatment of dystrophin cardiomyopathies. Nature Reviews Cardiology 11, 168-179CrossRef Google Scholar PubMed

163Kwon, H.W. et al. (2012) The effect of enalapril and carvedilol on left ventricular dysfunction in middle childhood and adolescent patients with muscular dystrophy. Korean Circulation Journal 42, 184-191CrossRef Google Scholar PubMed

164Shareef, M.A., Anwer, L.A. and Poizat, C. (2014) Cardiac SERCA2A/B: therapeutic targets for heart failure. European Journal of Pharmacology 724, 1-8CrossRef Google Scholar PubMed

165Morine, K.J. et al. (2010) Overexpression of SERCA1a in the mdx diaphragm reduces susceptibility to contraction-induced damage. Human Gene Therapy 21, 1735-1739CrossRef Google Scholar PubMed

166Katsetos, C.D., Koutzaki, S. and Melvin, J.J. (2013) Mitochondrial dysfunction in neuromuscular disorders. Seminars in Pediatric Neurology 20, 202-215CrossRef Google Scholar PubMed

167Buyse, G.M. et al. (2011) Idebenone as a novel, therapeutic approach for Duchenne muscular dystrophy: results from a 12 month, double-blind, randomized placebo-controlled trial. Neuromuscular Disorders 21, 396-405CrossRef Google Scholar PubMed

168Kotlikoff, M.I. (2007) Genetically encoded Ca²⁺ indicators: using genetics and molecular design to understand complex physiology. Journal of Physiology 578(Pt 1), 55-67CrossRef Google Scholar PubMed

169Mank, M. et al. (2008) A genetically encoded calcium indicator for chronic in vivo two-photon imaging. Nature Methods 5, 805-811CrossRef Google Scholar PubMed

170Rochefort, N.L. and Konnerth, A. (2008) Genetically encoded Ca²⁺ sensors come of age. Nature Methods 5, 761-762CrossRef Google Scholar PubMed

171Schoenenberger, P., Scharer, Y.P. and Oertner, T.G. (2011) Channelrhodopsin as a tool to investigate synaptic transmission and plasticity. Experimental Physiology 96, 34-39CrossRef Google Scholar PubMed

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Dysregulation of calcium homeostasis in muscular dystrophies

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Dysregulation of calcium homeostasis in muscular dystrophies

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