Skip to main content Accessibility help
×
Home

Dysregulation of calcium homeostasis in muscular dystrophies

  • Ainara Vallejo-Illarramendi (a1) (a2) (a3), Ivan Toral-Ojeda (a1) (a2), Garazi Aldanondo (a1) and Adolfo López de Munain (a1) (a2) (a4) (a5)

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.

Copyright

Corresponding author

*Corresponding author: Ainara Vallejo-Illarramendi, Instituto Biodonostia, Po Dr Begiristain s/n, 20014 San Sebastian, Spain. E-mail: ainaravallejo@yahoo.es

References

Hide All
1Berridge, M.J., Bootman, M.D. and Roderick, H.L. (2003) Calcium signalling: dynamics, homeostasis and remodelling. Nature Reviews Molecular Cell Biology 4, 517-529
2Leong, P. and MacLennan, D.H. (1998) Complex interactions between skeletal muscle ryanodine receptor and dihydropyridine receptor proteins. Biochemistry and Cell Biology 76, 681-694
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, 59-116
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, 677-687
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, 261-272
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), 813-824
7Allen, D.G., Lamb, G.D. and Westerblad, H. (2008) Impaired calcium release during fatigue. Journal of Applied Physiology 104, 296-305
8Andersson, D.C. et al. (2011) Ryanodine receptor oxidation causes intracellular calcium leak and muscle weakness in aging. Cell Metabolism 14, 196-207
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, 268-272
10Culligan, K. and Ohlendieck, K. (2002) Diversity of the brain dystrophin–glycoprotein complex. Journal of Biomedicine and Biotechnology 2, 31-36
11Gailly, P. (2002) New aspects of calcium signaling in skeletal muscle cells: implications in Duchenne muscular dystrophy. Biochimica et Biophysica Acta 1600, 38-44
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, 397-406
13Ruegg, U.T. et al. (2002) Pharmacological control of cellular calcium handling in dystrophic skeletal muscle. Neuromuscular Disorders 12(Suppl 1), S155-S161
14Schiaffino, S. and Reggiani, C. (2011) Fiber types in mammalian skeletal muscles. Physiological Reviews 91, 1447-1531
15Purves, D. and Williams, S.M. (2001) Neuroscience ( 2nd edn).Sinauer Associates, Sunderland, Mass.
16Scott, W., Stevens, J. and Binder-Macleod, S.A. (2001) Human skeletal muscle fiber type classifications. Physical Therapy 81, 1810-1816
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), 6053-6068
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), 1381-1395
19Pette, D. and Staron, R.S. (1997) Mammalian skeletal muscle fiber type transitions. International Review of Cytology 170, 143-223
20Webster, C. et al. (1988) Fast muscle fibers are preferentially affected in Duchenne muscular dystrophy. Cell 52, 503-513
21Kramerova, I. et al. (2012) Impaired calcium calmodulin kinase signaling and muscle adaptation response in the absence of calpain 3. Human Molecular Genetics 21, 3193-3204
22Zeiger, U., Mitchell, C.H. and Khurana, T.S. (2010) Superior calcium homeostasis of extraocular muscles. Experimental Eye Research 91, 613-622
23Stutzmann, G.E. and Mattson, M.P. (2011) Endoplasmic reticulum Ca(2+) handling in excitable cells in health and disease. Pharmacological Reviews 63, 700-727
24Franzini-Armstrong, C. and Jorgensen, A.O. (1994) Structure and development of E–C coupling units in skeletal muscle. Annual Review of Physiology 56, 509-534
25Periasamy, M. and Kalyanasundaram, A. (2007) SERCA pump isoforms: their role in calcium transport and disease. Muscle & Nerve 35, 430-442
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, 483-488
27Gilabert, J.A. (2012) Cytoplasmic calcium buffering. Advances in Experimental Medicines and Biology 740, 483-498
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-C403
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, 7243-7247
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), 185-199
31Pan, Z. et al. (2002) Dysfunction of store-operated calcium channel in muscle cells lacking mg29. Nature Cell Biology 4, 379-383
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, 9387-9392
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, 688-697
34Darbellay, B. et al. (2009) STIM1- and Orai1-dependent store-operated calcium entry regulates human myoblast differentiation. Journal of Biological Chemistry 284, 5370-5380
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, 15793-15798
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, 173-177
37Suzuki, M. et al. (1999) Cloning of a stretch-inhibitable nonselective cation channel. Journal of Biological Chemistry 274, 6330-6335
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, 22358-223567
39Vandebrouck, A. et al. (2006) Regulation of store-operated calcium entries and mitochondrial uptake by minidystrophin expression in cultured myotubes. FASEB Journal 20, 136-138
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, 1089-1096
41Al-Qusairi, L. and Laporte, J. (2011) T-tubule biogenesis and triad formation in skeletal muscle and implication in human diseases. Skeletal Muscle 1, 26
42Rossi, A.E. and Dirksen, R.T. (2006) Sarcoplasmic reticulum: the dynamic calcium governor of muscle. Muscle & Nerve 33, 715-731
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), 443-460
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-H1589
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, 39533-39538
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), 767-784
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, 340-345
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, 231-247
49Capes, E.M., Loaiza, R. and Valdivia, H.H. (2011) Ryanodine receptors. Skeletal Muscle 1, 18
50Mackrill, J.J. (2010) Ryanodine receptor calcium channels and their partners as drug targets. Biochemistry and Pharmacology 79, 1535-1543
51Van Petegem, F. (2012) Ryanodine receptors: structure and function. Journal of Biological Chemistry 287, 31624-31632
52Mackrill, J.J. (2012) Ryanodine receptor calcium release channels: an evolutionary perspective. Advances in Experimental Medicines and Biology 740, 159-182
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), 6381-6387
54Ward, C.W. et al. (2003) Defects in ryanodine receptor calcium release in skeletal muscle from post-myocardial infarct rats. FASEB Journal 17, 1517-1519
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, 919-928
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, 20813-20820
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, 8098-8107
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), 3113-3115
59Marks, A.R. (1997) Intracellular calcium-release channels: regulators of cell life and death. American Journal of Physiology 272(2 Pt 2), H597-H605
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, 235-241
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, 343-352
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, 2103-2109
63Maack, C. and O'Rourke, B. (2007) Excitation–contraction coupling and mitochondrial energetics. Basic Research in Cardiology 102, 369-392
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), 499-508
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, 472-480
66Lancel, S. et al. (2010) Oxidative posttranslational modifications mediate decreased SERCA activity and myocyte dysfunction in Galphaq-overexpressing mice. Circulation Research 107, 228-232
67Vangheluwe, P. et al. (2005) Modulating sarco(endo)plasmic reticulum Ca2+ ATPase 2 (SERCA2) activity: cell biological implications. Cell Calcium 38, 291-302
68Bigelow, D.J. (2009) Nitrotyrosine-modified SERCA2: a cellular sensor of reactive nitrogen species. Pflugers Archiv 457, 701-710
69Franzini-Armstrong, C. (2007) ER-mitochondria communication. How privileged? Physiology (Bethesda) 22, 261-268
70Eisenberg, B.R. (2011) Quantitative ultrastructure of mammalian skeletal muscle. Comprehensive Physiology, Supplement 27: Handbook of Physiology, Skeletal Muscle: 73-112.
71Hajnoczky, G. et al. (2000) The machinery of local Ca2+ signalling between sarco-endoplasmic reticulum and mitochondria. Journal of Physiology 529 (Pt 1), 69-81
72Rizzuto, R. et al. (2009) Ca(2+) transfer from the ER to mitochondria: when, how and why. Biochimica et Biophysica Acta 1787, 1342-1351
73Challet, C. et al. (2001) Mitochondrial calcium oscillations in C2C12 myotubes. Journal of Biological Chemistry 276, 3791-3797
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, 57-70
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, 32436-32443
76Pizzo, P. et al. (2012) Mitochondrial Ca(2+) homeostasis: mechanism, role, and tissue specificities. Pflugers Archiv 464, 3-17
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-H153
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-C713
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, 188-193
80Emery, A.E. (2002) The muscular dystrophies. Lancet 359, 687-695
81Hoffman, E.P., Brown, R.H. Jr. and Kunkel, L.M. (1987) Dystrophin: the protein product of the Duchenne muscular dystrophy locus. Cell 51, 919-928
82Blake, D.J., et al. (2002) Function and genetics of dystrophin and dystrophin-related proteins in muscle. Physiological Reviews 82, 291-329
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, 3710-3714
84Allen, D.G. et al. (2010) Calcium and the damage pathways in muscular dystrophy. Canadian Journal of Physiology and Pharmacology 88, 83-91
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, 439-446
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, 19023-19028
87Bertorini, T.E., et al. (1984) Calcium and magnesium content in fetuses at risk and prenecrotic Duchenne muscular dystrophy. Neurology 34, 1436-1440
88Turner, P.R. et al. (1988) Increased protein degradation results from elevated free calcium levels found in muscle from mdx mice. Nature 335, 735-738
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), 367-380
90Fong, P.Y., et al. (1990) Increased activity of calcium leak channels in myotubes of Duchenne human and mdx mouse origin. Science 250, 673-676
91Franco, A. Jr. and Lansman, J.B. (1990) Calcium entry through stretch-inactivated ion channels in mdx myotubes. Nature 344, 670-673
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, 608-617
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, 665-673
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), 4815-4824
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-C50
96Zhao, X. et al. (2012) Orai1 mediates exacerbated Ca(2+) entry in dystrophic skeletal muscle. PLoS ONE 7, e49862
97Sabourin, J. et al. (2012) Dystrophin/alpha1-syntrophin scaffold regulated PLC/PKC-dependent store-operated calcium entry in myotubes. Cell Calcium 52, 445-456
98Boittin, F.X. et al. (2010) Phospholipase A2-derived lysophosphatidylcholine triggers Ca2+ entry in dystrophic skeletal muscle fibers. Biochemical and Biophysical Research Communications 391, 401-406
99Lindahl, M. et al. (1995) Phospholipase A2 activity in dystrophinopathies. Neuromuscular Disorders 5, 193-199
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, 1537-1550
101Bellinger, A.M. et al. (2009) Hypernitrosylated ryanodine receptor calcium release channels are leaky in dystrophic muscle. Nature Medicine 15, 325-330
102Brillantes, A.B. et al. (1994) Stabilization of calcium release channel (ryanodine receptor) function by FK506-binding protein. Cell 77, 513-523
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, 2198-202
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, 20876-20887
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, 902-909
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, 47092-47100
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, 3210-3221
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, 171-182
109Robert, V. et al. (2001) Alteration in calcium handling at the subcellular level in mdx myotubes. Journal of Biological Chemistry 276, 4647-4651
110Basset, O. et al. (2006) Bcl-2 overexpression prevents calcium overload and subsequent apoptosis in dystrophic myotubes. Biochemical Journal 395, 267-276
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, 4562-4578
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-H855
113Jung, C. et al. (2008) Dystrophic cardiomyopathy: amplification of cellular damage by Ca2+ signalling and reactive oxygen species-generating pathways. Cardiovascular Research 77, 766-773
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-H775
115Khairallah, M. et al. (2007) Metabolic and signaling alterations in dystrophin-deficient hearts precede overt cardiomyopathy. Journal of Molecular Cell Cardiology 43, 119-129
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, 209-218
117Goonasekera, S.A. et al. (2011) Mitigation of muscular dystrophy in mice by SERCA overexpression in skeletal muscle. Journal of Clinical Investigation 121, 1044-1052
118Gehrig, S.M. et al. (2012) Hsp72 preserves muscle function and slows progression of severe muscular dystrophy. Nature 484, 394-398
119Culligan, K. et al. (2002) Drastic reduction of calsequestrin-like proteins and impaired calcium binding in dystrophic mdx muscle. Journal of Applied Physiology 92, 435-445
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, 3943-3952
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), 479-488
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, 609-615
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, 63-71
124Laval, S.H. and Bushby, K.M. (2004) Limb-girdle muscular dystrophies – from genetics to molecular pathology. Neuropathology and Applied Neurobiology 30, 91-105
125Saenz, A., et al. (2005) LGMD2A: genotype–phenotype correlations based on a large mutational survey on the calpain 3 gene. Brain 128(Pt 4), 732-742
126Urtasun, M., et al. (1998) Limb-girdle muscular dystrophy in Guipuzcoa (Basque Country, Spain). Brain 121 (Pt 9), 1735-1747
127Hauerslev, S. et al. (2012) Calpain 3 is important for muscle regeneration: evidence from patients with limb girdle muscular dystrophies. BMC Musculoskeletal Disorders 13, 43
128Richard, I. et al. (1995) Mutations in the proteolytic enzyme calpain 3 cause limb-girdle muscular dystrophy type 2A. Cell 81, 27-40
129Beckmann, J.S. and Spencer, M. (2008) Calpain 3, the “gatekeeper” of proper sarcomere assembly, turnover and maintenance. Neuromuscular Disorders 18, 913-921
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, 7811-7819
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, 1373-1388
132Ojima, K. et al. (2011) Non-proteolytic functions of calpain-3 in sarcoplasmic reticulum in skeletal muscles. Journal of Molecular Biology 407, 439-449
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, 3271-3280
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, 340-346
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), 697-714
136Seo, I.R. et al. (2006) Aldolase potentiates DIDS activation of the ryanodine receptor in rabbit skeletal sarcoplasmic reticulum. Biochemistry Journal 399, 325-333
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, 1100-1104
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, 2401-2403
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, 255-260
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), 993-1005
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, 128-44
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), 3194-3205
143Harper, P.S. (2009) Myotonic dystrophy (2nd edn).Oxford University Press, Oxford, New York
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, 799-808
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, 5773-5780
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, 737-741
147Timchenko, N.A. et al. (2001) RNA CUG repeats sequester CUGBP1 and alter protein levels and activity of CUGBP1. Journal of Biological Chemistry 276, 7820-7826
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, 1312-1324
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, 2189-2200
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, 464-476
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, 1440-1447
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, 14-19
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, 390-405
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), 719-729
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), 3679-3680
156Andersson, D.C. et al. (2012) Leaky ryanodine receptors in beta-sarcoglycan deficient mice: a potential common defect in muscular dystrophy. Skeletal Muscle 2, 9
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.
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, e81222
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, 167-176
160Phillips, M.F. and Quinlivan, R. (2008) Calcium antagonists for Duchenne muscular dystrophy. Cochrane Database of Systematic Reviews 4, CD004571
161Iwata, Y. et al. (2009) Dominant-negative inhibition of Ca2+ influx via TRPV2 ameliorates muscular dystrophy in animal models. Human Molecular Genetics 18, 824-834
162Finsterer, J. and Cripe, L. (2014) Treatment of dystrophin cardiomyopathies. Nature Reviews Cardiology 11, 168-179
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, 184-191
164Shareef, M.A., Anwer, L.A. and Poizat, C. (2014) Cardiac SERCA2A/B: therapeutic targets for heart failure. European Journal of Pharmacology 724, 1-8
165Morine, K.J. et al. (2010) Overexpression of SERCA1a in the mdx diaphragm reduces susceptibility to contraction-induced damage. Human Gene Therapy 21, 1735-1739
166Katsetos, C.D., Koutzaki, S. and Melvin, J.J. (2013) Mitochondrial dysfunction in neuromuscular disorders. Seminars in Pediatric Neurology 20, 202-215
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, 396-405
168Kotlikoff, M.I. (2007) Genetically encoded Ca2+ indicators: using genetics and molecular design to understand complex physiology. Journal of Physiology 578(Pt 1), 55-67
169Mank, M. et al. (2008) A genetically encoded calcium indicator for chronic in vivo two-photon imaging. Nature Methods 5, 805-811
170Rochefort, N.L. and Konnerth, A. (2008) Genetically encoded Ca2+ sensors come of age. Nature Methods 5, 761-762
171Schoenenberger, P., Scharer, Y.P. and Oertner, T.G. (2011) Channelrhodopsin as a tool to investigate synaptic transmission and plasticity. Experimental Physiology 96, 34-39

Disease pages in OMIM:

Dysregulation of calcium homeostasis in muscular dystrophies

  • Ainara Vallejo-Illarramendi (a1) (a2) (a3), Ivan Toral-Ojeda (a1) (a2), Garazi Aldanondo (a1) and Adolfo López de Munain (a1) (a2) (a4) (a5)

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed