Skip to main content
SpringerLink
Log in

Role of defective Ca2+ signaling in skeletal muscle weakness: Pharmacological implications

  • Review
  • Published:
Journal of Cell Communication and Signaling Aims and scope

Abstract

The misbehaving attitude of Ca2+ signaling pathways could be the probable reason in many muscular disorders such as myopathies, systemic disorders like hypoxia, sepsis, cachexia, sarcopenia, heart failure, and dystrophy. The present review throws light upon the calcium flux regulating signaling channels like ryanodine receptor complex (RyR1), SERCA (Sarco-endoplasmic Reticulum Calcium ATPase), DHPR (Dihydropyridine Receptor) or Cav1.1 and Na+/Ca2+ exchange pump in detail and how remodelling of these channels contribute towards disturbed calcium homeostasis. Understanding these pathways will further provide an insight for establishing new therapeutic approaches for the prevention and treatment of muscle atrophy under stress conditions, targeting calcium ion channels and associated regulatory proteins.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Adhihetty PJ, Hood DA (2003) Mechanisms of apoptosis in skeletal muscle. Basic Appl Myol 13:171–179

    Google Scholar 

  • Aghdasi B, Reid MB, Hamilton SL (1997) Nitric oxide protects the skeletal muscle Ca2+ Release Channel from oxidation induced activation. J Biol Chem 272:25462–25467

    CAS  PubMed  Google Scholar 

  • Agrawal A, Rathor R, Suryakumar G (2017) Oxidative protein modification alters proteostasis under acute hypobaric hypoxia in skeletal muscles: a comprehensive in vivo study. Cell Stress Chaper 22:429–443

    CAS  Google Scholar 

  • Aley PK, Porter KE, Boyle JP, Kemp PJ, Peers C (2005) Hypoxic modulation of Ca2+signaling in human venous endothelial cells. Multiple roles for reactive oxygen species J Biol Chem 280:13349–13354

    CAS  PubMed  Google Scholar 

  • Aley PK, Murray HJ, Boyle JP, Pearson HA, Peers C (2006) Hypoxia stimulates Ca2+ release from intracellular stores in astrocytes via cyclic ADP ribose-mediated activation of ryanodine receptors. Cell Calcium 39:95–100

    CAS  PubMed  Google Scholar 

  • Altamirano F, Valladares D, Henríquez-Olguín C, Casas M, López JR, Allen PD, Jaimovich E (2013) Nifedipine treatment reduces resting calcium concentration, oxidative and apoptotic gene expression, and improves muscle function in dystrophic mdx mice. PLoS One 8:e81222

    PubMed  PubMed Central  Google Scholar 

  • Anderson DM, Anderson KM, Chang CL, Makarewich CA, Nelson BR, McAnally JR, Kasaragod P, Shelton JM, Liou J, Bassel-Duby R, Olson EN (2015) A micropeptide encoded by a putative long noncoding RNA regulates muscle performance. Cell 160(4):595–606

    CAS  PubMed  PubMed Central  Google Scholar 

  • Andersson DC, Betzenhauser MJ, Reiken S, Meli AC, Umanskaya A, Xie W, Shiomi T, Zalk R, Lacampagne A, Marks AR (2011) Ryanodine receptor oxidation causes intracellular calcium leak and muscle weakness in aging. Cell Metab 14:196–207

    CAS  PubMed  PubMed Central  Google Scholar 

  • Andersson DC, Meli AC, Reiken S, Betzenhauser MJ, Umanskaya A, Shiomi T, D'Armiento J, Marks AR (2012) Leaky ryanodine receptors in β-sarcoglycan deficient mice: a potential common defect in muscular dystrophy. Skelet Muscle 2(1):9

    CAS  PubMed  PubMed Central  Google Scholar 

  • Aracena P, Sanchez G, Donoso P, Hamilton SL, Hidalgo C (2003) S-glutathionylation decreases Mg2+ inhibition and S-nitrosylation enhances Ca2+ activation of RyR1 channels. J Biol Chem 278:42927–42935

    CAS  PubMed  Google Scholar 

  • Aracena P, Tang W, Hamilton S, Hidalgo C (2005) Effects of S-glutathionylation and S-nitrosylation on calmodulin binding to triads and FKBP12 binding to type 1 calcium release channels. Antioxid Redox Signal 7:870–881

    CAS  PubMed  Google Scholar 

  • Aracena-Parks P, Goonasekera SA, Gilman CP, Dirksen RT, Hidalgo C, Hamilton SL (2006) Identification of cysteines involved in S-nitrosylation, S-glutathionylation, and oxidation to disulfides in ryanodine receptor type 1. J Biol Chem 281:40354–40368

    CAS  PubMed  Google Scholar 

  • Armstrong CM, Bezanilla FM, Horowicz P (1972) Twitches in the presence of ethylene glycol bis (β-aminoethyl ether)-N,N -tetracetic acid. Biochim Biophys Acta 267:605–608

    CAS  PubMed  Google Scholar 

  • Avdonin PV (2012) Orai and TRP channels in skeletal muscle cells. Biochemistry (Moscow) Supplement Series A: Membrane and Cell Biol 6(2):159–168

    Google Scholar 

  • Barreiro E, Hussain SN (2010) Protein carbonylation in skeletal muscles: impact on function. Antioxid Redox Signal 12:417–429

    CAS  PubMed  Google Scholar 

  • Batchelor CL, Winder SJ (2006) Sparks, signals and shock absorbers: how dystrophin loss causes muscular dystrophy. Trends Cell Biol 16:198–205

    CAS  PubMed  Google Scholar 

  • Beard NA, Laver DR, Dulhunty AF (2004) Calsequestrin and the calcium release channel of skeletal and cardiac muscle. Prog Biophys Mol Biol 85:33–69

    CAS  PubMed  Google Scholar 

  • Bellinger AM, Reiken S, Dura M, Murphy PW, Deng SX, Landry DW, Nieman D, Lehnart SE, Samaru M, LaCampagne A, Marks AR (2008) Remodelling of ryanodine receptor complex causes “leaky” channels: a molecular mechanism for decreased exercise capacity. PNAS 105:2198–2202

    CAS  PubMed  Google Scholar 

  • Bellinger AM, Reiken S, Carlson C, Mongillo M, Liu X, Rothman L, Matecki S, Lacampagne A, Marks AR (2009) Hypernitrosylated ryanodine receptor calcium release channels are leaky in dystrophic muscle. Nat Med 15:325–330

    CAS  PubMed  PubMed Central  Google Scholar 

  • Berridge MJ (2002) The endoplasmic reticulum: a multifunctional signaling organelle. Cell Calcium 32:235–249

    CAS  PubMed  Google Scholar 

  • Berridge MJ, Lipp P, Bootman MD (2000) The versatility and universality of calcium signaling. Nat Rev Mol Cell Biol 1:11–21

    CAS  PubMed  Google Scholar 

  • Bers DM (2001) Excitation-contraction coupling and cardiac contractile force. Develop Cardiovas Med 237:978–994

    Google Scholar 

  • Bers DM (2002) Cardiac excitation–contraction coupling. Nature 415:198–205

    CAS  PubMed  Google Scholar 

  • Bers DM (2004) Macromolecular complexes regulating cardiac ryanodine receptor function. J Mol Cell Cardiol 37:417–429

    CAS  PubMed  Google Scholar 

  • Bianchi CP, Shanes AM (1959) Calcium influx in skeletal muscle at rest, during activity and during potassium contracture. J Gen Physiol 42:803–815

    CAS  PubMed  PubMed Central  Google Scholar 

  • Booth FW, Giannetta CL (1973) Effect of hindlimb immobilization upon skeleton muscle calcium in rat. Calcif Tissue Res 13:327–330

    CAS  PubMed  Google Scholar 

  • Bootman MD, Lipp P, Berridge MJ (2001) The organization and functions of local Ca2+ signals. J Cell Sci 114:2213–2222

    CAS  PubMed  Google Scholar 

  • Bosanac I, Alattia JR, Mal TK, Chan J, Talarico S, Tong FK, Tong KI, Yoshikawa F, Furuichi T, Iwai M, Michikawa T, Mikoshiba K, Ikura M (2002) Structure of the inositol 1,4,5-trisphosphate receptor binding core in the complex with its ligand. Nature 420:696–700

    CAS  PubMed  Google Scholar 

  • Brillantes AB, Ondrias K, Scott A, Kobrinsky E, Ondriasová E, Moschella MC, Jayaraman T, Landers M, Ehrlich BE, Marks AR (1994) Stabilization of calcium release channel (ryanodine receptor) function by FK506-binding protein. Cell 77:513–523

    CAS  PubMed  Google Scholar 

  • Burk SE, Lytton J, MacLennan DH, Shull GE (1989) cDNA cloning, functional expression and mRNA tissue distribution of a third organellar Ca2+ pump. J Biol Chem 264:18561–18568

    CAS  PubMed  Google Scholar 

  • Burr AR, Molkentin JD (2015) Genetic evidence in the mouse solidifies the calcium hypothesis of myofiber death in muscular dystrophy. Cell Death Differ 22:1402–1412

    CAS  PubMed  PubMed Central  Google Scholar 

  • Burr AR, Millay DP, Goonasekera SA, Park KH, Sargent MA, Collins J, Altamirano F, Philipson KD, Allen PD, Ma J, López JR, Molkentin JD (2014) Na+ dysregulation coupled with Ca2+ entry through NCX1 promotes muscular dystrophy in mice. Mol Cell Biol 34:1991–2002

    PubMed  PubMed Central  Google Scholar 

  • Cannell MB, Soeller C (1997) Numerical analysis of ryanodine receptor activation by L-type channel activity in the cardiac muscle diad. Biophys J 73:112–122

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cannell MB, Cheng H, Lederer WJ (1995) The control of calcium release in heart muscle. Science 268:1045–1049

    CAS  PubMed  Google Scholar 

  • Catterall WA (1991) Excitation-contraction coupling in vertebrate skeletal muscle: a tale of two calcium channels. Cell 64:871–874

    CAS  PubMed  Google Scholar 

  • Chaudhury P, Suryakumar G, Prasad R, Singh SM, Ali S, Ilavazhagan G (2012) Chronic hypobaric hypoxia mediated skeletal muscle atrophy: role of ubiquitin–proteasome pathway and calpains. Mol Cell Biochem 364:101–113

    Google Scholar 

  • Chen L, Lu XY, Li J, Fu JD, Zhou ZN, Yang HT (2006) Intermittent hypoxia protects cardiomyocytes against ischemia-reperfusion injury-induced alterations in Ca2+ homeostasis and contraction via the sarcoplasmic reticulum and Na+/Ca2+ exchange mechanisms. Am J Physiol Cell Physiol 290:C1221–C1229

    CAS  PubMed  Google Scholar 

  • Cheng H, Lederer WJ, Cannell MB (1993) Calcium sparks: elementary events underlying excitation-contraction coupling in heart muscle. Science 262:740–744

    CAS  PubMed  Google Scholar 

  • Cheong E, Tumbev V, Abramson J, Salama G, Stoyanovsky DA (2005) Nitroxyl triggers Ca2+ release from skeletal and cardiac sarcoplasmic reticulum by oxidizing ryanodine receptors. Cell Calcium 37:87–96

    CAS  PubMed  Google Scholar 

  • Clapham DE (2007) Calcium signaling. Cell 131:1047–1058

    CAS  PubMed  Google Scholar 

  • Divet A, Huchet-Cadiou C (2002) Sarcoplasmic reticulum functions in slow- and fast-twitch skeletal muscles from mdx mice. Pflugers Arch 444:634–643

    CAS  PubMed  Google Scholar 

  • Dulhunty AF, Haarmann CS, Green D, Laver DR, Board PG, Casarotto MG (2002) Interactions between dihydropyridine receptors and ryanodine receptors in striated muscle. Prog Biophys Mol Biol 79:45–75

    CAS  PubMed  Google Scholar 

  • Dulhunty AF, Wei-La PL, Casarotto MG, Beard NA (2017) Core skeletal muscle ryanodine receptor calcium release complex. Clin Exper Pharmacol Physiol 44:3–12

    CAS  Google Scholar 

  • Durham WJ, Aracena-Parks P, Long C, Rossi AE, Goonasekera SA, Boncompagni S, Galvan DL, Gilman CP, Baker MR, Shirokova N, Protasi F, Dirksen R, Hamilton SL (2008) RyR1 S-nitrosylation underlies environmental heat stroke and sudden death in Y522S RyR1knockin mice. Cell 133:53–65

    CAS  PubMed  PubMed Central  Google Scholar 

  • Eltit JM, Hidalgo J, Liberona JL, Jaimovich E (2004) Slow calcium signals after tetanic electrical stimulation in skeletal myotubes. Biophys J 86:3042–3051

    CAS  PubMed  PubMed Central  Google Scholar 

  • Endo M (1975) Conditions required for calcium-induced release of calcium from the sarcoplasmic reticulum. Proc Jap Acad 51:467–472

    CAS  Google Scholar 

  • Endo M (1981) Mechanism of calcium-induced calcium release in the SR membrane. Academic, pp 257–264

  • Endo M (2009) Calcium-induced calcium release in skeletal muscle. Physiol Rev 89:1153–1176

    CAS  PubMed  Google Scholar 

  • Endo M, Tanaka M, Ogawa Y (1970) Calcium induced release of calcium from the sarcoplasmic reticulum of skinned skeletal muscle fibres. Nature 228:34–36

    CAS  PubMed  Google Scholar 

  • Eu JP, Sun J, Xu L, Stamler JS, Meissner G (2000) The skeletal muscle calcium release channel: coupled O2 sensor and NO signaling functions. Cell 102:499–509

    CAS  PubMed  Google Scholar 

  • Fabiato A (1989) Appraisal of the physiological relevance of two hypotheses for the mechanism of calcium release from the mammalian cardiac sarcoplasmic reticulum: calcium-induced release versus charge coupled release. Mol Cell Biochem 89:135–140

    CAS  PubMed  Google Scholar 

  • Fabiato A, Fabiato F (1975) Contractions induced by a calcium-triggered release of calcium from the sarcoplasmic reticulum of single skinned cardiac cells. J Physiol Lond 249:469–495

    CAS  PubMed  PubMed Central  Google Scholar 

  • Farrell EF, Antaramian A, Rueda A, Gomez AM, Valdivia HH (2003) Sorcin inhibits calcium release and modulates excitation-contraction coupling in the heart. J Biol Chem 278:34660–34666

    CAS  PubMed  Google Scholar 

  • Fauconnier J, Thireau J, Reiken S, Cassan C, Richard S, Matecki S, Marks AR, Lacampagne A (2010) Leaky RyR2 trigger ventricular arrhythmias in Duchenne muscular dystrophy. Proc Natl Acad Sci 107:1559–1564

    CAS  PubMed  Google Scholar 

  • Favero TG, Zable AC, Bowman MB, Thompson A, Abramson JJ (1995) Metabolic end products inhibit sarcoplasmic reticulum Ca2+ release and [3H] ryanodine binding. J Appl Physiol 78:1665–1672

    CAS  PubMed  Google Scholar 

  • Felix R, Gurnett CA, Waard DM, Campbell KP (1997) Dissection of functional domains of the voltage-dependent Ca2+ channel α2δ subunit. J Neurosci 17:6884–6891

    CAS  PubMed  Google Scholar 

  • Feng W, Liu G, Allen PD, Pessah IN (2000) Transmembrane redox sensor of ryanodine receptor complex. J Biol Chem 275:35902–35907

    CAS  PubMed  Google Scholar 

  • Ferreira R, Neuparth MJ, Vitorino R, Appell HJ, Amado F, Duarte JA (2008) Evidences of apoptosis during the early phases of soleus muscle atrophy in hindlimb suspended mice. Physiol Res 57:601–611

    CAS  PubMed  Google Scholar 

  • Fill M, Copello JA (2002) Ryanodine receptor calcium release channels. Physiol Rev 82:893–922

    CAS  PubMed  Google Scholar 

  • Flucher BE, Tuluc P (2017) How and why are calcium currents curtailed in the skeletal muscle voltage-gated calcium channels? J Physiol 595:1451–1463

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fontana J, Fritz N, Brismar H, Aperia A (2015) Apoptosis caused by excessive mitochondrial albumin uptake in renal cells is initiated by increased mitochondrial calcium concentration. FASEB J 29:845–830

    Google Scholar 

  • Foskett JK, White C, Cheung KH, Mak DO (2007) Inositol trisphosphate receptor Ca2+ release channels. Physiol Rev 87:593–658

    CAS  PubMed  PubMed Central  Google Scholar 

  • Franzini-Armstrong C, Protasi F, Ramesh V (1998) Comparative ultrastructure of Ca2+ release units in skeletal and cardiac muscle. Ann N Y Acad Sci 16:20–30

    Google Scholar 

  • Furuichi T, Furutama D, Hakamata Y, Nakai J, Takeshima H, Mikoshiba K (1994) Multiple types of ryanodine receptor/Ca2+ release channels are differentially expressed in rabbit brain. J Neurosci14:4794–4805

    CAS  PubMed  Google Scholar 

  • Gehlert S, Bloch W, Suhr F (2015) Ca2+ dependent regulations and signaling in skeletal muscle: from electro-mechanical coupling. Int J Mol Sci 16:1066–1095

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gehrig SM, van der Poel C, Sayer TA, Schertzer JD, Henstridge DC, Church JE, Lamon S, Russell AP, Davies KE, Febbraio MA, Lynch GS (2012) Hsp72 preserves muscle function and slows progression of severe muscular dystrophy. Nature 484:394–398

    CAS  PubMed  Google Scholar 

  • Giannini G, Conti A, Mammarella S, Scrobogna M, Sorrentino V (1995) The ryanodine receptor/calcium channel genes are widely and differentially expressed in murine brain and peripheral tissues. J Cell Biol 128:893–904

    CAS  PubMed  Google Scholar 

  • Goonasekera SA, Lam CK, Millay DP, Sargent MA, Hajjar RJ, Kranias EG, Molkentin JD (2011) Mitigation of muscular dystrophy in mice by SERCA overexpression in skeletal muscle. J Clin Invest 121:1044–1052

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hakamata Y, Nakai J, Takeshima H, Imoto K (1992) Primary structure and distribution of a novel ryanodine receptor/calcium release channel from rabbit brain. FEBS Lett 312:229–235

    CAS  PubMed  Google Scholar 

  • Hidalgo C, Sanchez G, Barrientos G, Aracena-Parks P (2006) A transverse tubule NADPH oxidase activity stimulates calcium release from isolated triads via ryanodine receptor type 1 S-glutathionylation. J Biol Chem 281:26473–26482

    CAS  PubMed  Google Scholar 

  • Hoang-Trong TM, Ullah A, Jafri SM (2015) Calcium sparks in the heart: dynamics and regulation. Res Rep Biol 6:203–214

    CAS  PubMed  PubMed Central  Google Scholar 

  • Horstick EJ, Linsley JW, Dowling JJ, Hauser MA, McDonald KK, Ashley-Koch A, Saint-Amant L, Satish A, Cui WW, Zhou W, Sprague SM, Stamm DS, Powell CM, Speer MC, Franzini-Armstrong C, Hirata H, Kuwada JY (2013) Stac3 is a component of the excitation–contraction coupling machinery and mutated in native American myopathy. Nature Comm 4:1952

    Google Scholar 

  • Jackson MJ (2009) Strategies for reducing oxidative damage in ageing skeletal muscle. Adv Drug Deliv Rev 61:1363–1368

    CAS  PubMed  Google Scholar 

  • Jaggar JH, Stevenson AS, Nelson MT (1998) Voltage dependence of Ca2+ sparks in intact cerebral arteries. Am J Physiol Cell Physiol 274:C1755–C1761

    CAS  Google Scholar 

  • Jaggar JH, Valerie A, Porter W, Lederer J, Nelson MT (2000) Calcium sparks in smooth muscle. Am J Physiol Cell Physiol 278:C235–C256

    CAS  PubMed  Google Scholar 

  • Jain K, Suryakumar G, Prasad R, Singh SM, Ganju L (2013a) Differential activation of myocardial ER stress response: a possible role in hypoxic tolerance. Int J Cardiol 168:4667–4677

    PubMed  Google Scholar 

  • Jain K, Suryakumar G, Prasad R, Singh SM, Ganju L (2013b) Myocardial ER chaperone activation and protein degradation occurs due to synergistic, not individual, cold and hypoxic stress. Biochimie 95:1897–1908

    CAS  PubMed  Google Scholar 

  • Jayaraman T, Brillantes AM, Timerman AP, Fleischer S, Erdjument-Bromage H, Tempst P, Marks AR (1992) FK506 binding protein associated with the calcium release channel (ryanodine receptor). J Biol Chem 267:9474–9477

    CAS  PubMed  Google Scholar 

  • Jeong HN, Park HJ, Lee JH, Shin HY, Kim SH, Kim SM, Choi YC (2018) Clinical and pathologic findings of Korean patients with RYR1-related congenital myopathy. J Clin Neurol 14(1):58–65

    PubMed  Google Scholar 

  • Kanatous SB, Mammen PPA, Rosenberg PB, Martin CM, White MD, DiMaio JM, Huang G, Muallem S, Garry DJ (2009) Hypoxia reprograms calcium signaling and regulates myoglobin expression. Am J Physiol-Cell Physiol 296(3):C393–C402

    CAS  PubMed  Google Scholar 

  • Kimura T, Nakamori M, Lueck JD, Pouliquin P, Aoike F, Fujimura H, Dirksen RT, Takahashi MP, Dulhunty AF, Sakoda S (2005) Altered mRNA splicing of the skeletal muscle ryanodine receptor and sarcoplasmic/endoplasmic reticulum Ca2+-ATPase in myotonic dystrophy type 1. Hum Mol Genet 14:2189–2200

    CAS  PubMed  Google Scholar 

  • Kiviluoto S, Decuypere JP, De Smedt H, Missiaen L, Parys JB, Bultynck G (2011) STIM1 as a key regulator for Ca2+ homeostasis in skeletal-muscle development and function. Skelet Muscle 1(1):16

    CAS  PubMed  PubMed Central  Google Scholar 

  • Klein MG, Cheng H, Santana LF, Jiang YH, Lederer WJ, Schneider MF (1996) Two mechanisms of quantized calcium release in skeletal muscle. Nature 379:455–458

    CAS  PubMed  Google Scholar 

  • Kranias EG, Hajjar RJ (2012) Modulation of cardiac contractility by the phospholamban/SERCA2a regulatome. Circ Res 110:1646–1660

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kuwajima G, Futatsugi A, Niinobe M, Nakanishi S, Mikoshiba K (1992) Two types of ryanodine receptors in mouse brain: skeletal muscle type exclusively in Purkinje cells and cardiac muscle type in various neurons. Neuron 9:1133–1142

    CAS  PubMed  Google Scholar 

  • Lai FA, Dent M, Wickenden C, Xu L, Kumari G, Misra M, Lee HB, Sar M, Meissner G (1992) Expression of a cardiac Ca2+-release channel isoform in mammalian brain. Biochem J 288:553–564

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lehnart SE, Wehrens XH, Reiken S, Warrier S, Belevych AE, Harvey RD, Richter W, Jin SL, Conti M, Marks AR (2005) Phosphodiesterase 4D deficiency in the ryanodine-receptor complex promotes heart failure and arrhythmias. Cell 123:25–35

    CAS  PubMed  PubMed Central  Google Scholar 

  • Leung FP, Yung LM, Yao X, Laher I, Huang Y (2008) Store-operated calcium entry in vascular smooth muscle. Br J Pharmacol 153:846–857

    CAS  PubMed  Google Scholar 

  • Liu X, Harlow L, Graham ZA, Bauman WA, Cardoz C (2016) Spinal cord injury leads to Hyperoxidation and Nitrosylation of skeletal muscle ryanodine Receptor-1 associated with upregulation of NADH oxidase 4. J Neurotrauma 34(12):2069–2074

    Google Scholar 

  • Lunde PK, Dahlstedt AJ, Bruton JD, Lannergren J, Thoren P, Sejersted OM, Westerblad (2001) Contraction and intracellular Ca2+ handling in isolated skeletal muscle of rats with congestive heart failure. Circ Res 88:1299–1305

  • MacLennan DH, Rice WJ, Green NM (1997) The mechanism of Ca2þ transport by sarco (endo) plasmic reticulum Ca2+ ATPases. J Biol Chem 272:28815–28818

    CAS  PubMed  Google Scholar 

  • MacLennan DH, Asahi M, Tupling AR (2003) The regulation of SERCA-type pumps by phospholamban and sarcolipin. Ann N Y Acad Sci 986:472–480

    CAS  PubMed  Google Scholar 

  • Marks AR, Tempst P, Hwang KS, Taubman MB, Inui M, Chadwick C, Fleischer S, Nadal-Ginard B (1989) Molecular cloning and characterization of the rynodine receptor/junctional channel complex cDNA from skeletal muscle sarcoplasmic reticulum. Proc Natl Acad Sci 86:8683–8687

    CAS  PubMed  Google Scholar 

  • Martonosi AN, Pikula S (2003) The network of calcium regulation in muscle. Acta Biochim Pol 50:1–30

    CAS  PubMed  Google Scholar 

  • Marx SO, Reiken S, Hisamatsu Y, Jayaraman T, Burkhoff D, Rosemblit N, Marks AR (2000) PKA phosphorylation dissociates FKBP12.6 from the calcium release channel (ryanodine receptor): defective regulation in failing hearts. Cell 101:365–376

    CAS  PubMed  Google Scholar 

  • Melzer W, Herrmann-Frank A, Luttgau HC (1995) The role of Ca2+ ions in excitation-contraction coupling of skeletal muscle fibres. Biochim Biophys Acta 1241:59–116

    PubMed  Google Scholar 

  • Michalak M, Robert Parker JM, Opas M (2002) Ca2+ signaling and calcium binding chaperones of the endoplasmic reticulum. Cell Calcium 32:269–278

    CAS  PubMed  Google Scholar 

  • Milner RE, Famulski KS, Michalak M (1992) Calcium binding proteins in the sarcoplasmic/endoplasmic reticulum of muscles and non muscles cells. Mol Cell Biochem 112:1–13

    CAS  PubMed  Google Scholar 

  • Missiaen L, De Smedt H, Droogmans G, Casteels R (1992) Ca2+ release induced by inositol 1, 4, 5-trisphosphate is a steady-state phenomenon controlled by luminal Ca2+ in permeabilized cells. Nature 357:599–602

    CAS  PubMed  Google Scholar 

  • Moore CP, Rodney G, Zhang JZ, Santacruz-Toloza L, Strasburg G, Hamilton SL (1999) Apocalmodulin and Ca2+ calmodulin bind to the same region on the skeletal muscle Ca2+ release channel. Biochemistry 38:8532–8537

    CAS  PubMed  Google Scholar 

  • Mosca B, Eckhardt J, Bergamelli L, Treves S, Bongianino R, Negri MD, Priori SG, Protasi F, Zorzato F (2016) Role of the JP45-Calsequestrin complex on calcium entry in slow twitch skeletal muscles. J Biol Chem 291(39):20824

    CAS  PubMed  PubMed Central  Google Scholar 

  • Muller FL, Lustgarten MS, Jang Y, Richardson A, Van Remmen H (2007) Trends in oxidative aging theories. Free Radic Biol Med 43:477–503

    CAS  PubMed  Google Scholar 

  • Nakanishi S, Kuwajima G, Mikoshiba K (1992) Immunohistochemical localization of ryanodine receptors in mouse central nervous system. Neurosci Res 15:130–142

    CAS  PubMed  Google Scholar 

  • Nelson MT, Cheng H, Rubart M, Santana LF, Bonev AD, Knot HJ, Lederer WJ (1995) Relaxation of arterial smooth muscle by calcium sparks. Science 270:633–637

    CAS  PubMed  Google Scholar 

  • Neylon CB, Richards SM, Larsen MA, Agrotis A, Bobik A (1995) Multiple types of ryanodine receptor/Ca2+ release channels are expressed in vascular smooth muscle. Biochem Biophys Res Commun 215:814–821

    CAS  PubMed  Google Scholar 

  • Nixon GF, Mignery GA, Somlyo AV (1994) Immunogold localization of inositol 1,4,5-triphosphate receptors and characterization of ultrastructural features of the sarcoplasmic reticulum in phasic and tonic smooth muscle. J Muscle Res Cell Motil 15:682–700

    CAS  PubMed  Google Scholar 

  • Oba T, Murayama T, Ogawa Y (2002) Redox states of type 1 ryanodine receptor alters Ca2+ release channel response to modulators. Am J Phys 282:C684–C692

    CAS  Google Scholar 

  • Ohrtman J, Ritter B, Polster A, Beam KG, Papadopoulos S (2008) Sequence differences in the IQ motifs of CaV1.1 and CaV1.2 strongly impact calmodulin binding and calcium-dependent inactivation. The J Biochem 283(43):29301–29311

    CAS  Google Scholar 

  • Otsu K, Willard HF, Khanna VK, Zorzato F, Green NM, MacLennan DH (1990) Molecular cloning of cDNA encoding the Ca2+ release channel (ryanodine receptor) of rabbit cardiac muscle sarcoplasmic reticulum. J Biol Chem 265:13472–13483

    CAS  PubMed  Google Scholar 

  • Ottini L, Marziali G, Conti A, Charlesworth A, Sorrentino V (1996) Alpha and beta isoforms of ryanodine receptor from chicken skeletal muscle are the homologues of mammalian RyR1 and RyR3. Biochem J 315:207–216

    CAS  PubMed  PubMed Central  Google Scholar 

  • Papp S, Dziak E, Michalak M, Opas M (2003) Is all of the endoplasmic reticulum created equal? The effects of the heterogeneous distribution of endoplasmic reticulum Ca2+ handling proteins. J Cell Biol 160:475–479

    CAS  PubMed  PubMed Central  Google Scholar 

  • Parekh AB (2003) Store-operated Ca2+ entry: dynamic interplay between endoplasmic reticulum, mitochondria and plasma membrane. J Physiol 547:333–348

    CAS  PubMed  PubMed Central  Google Scholar 

  • Parekh AB, Putney JW Jr (2005) Store-operated calcium channels. Physiol Rev 85(2):757–810

    CAS  PubMed  Google Scholar 

  • Periasamy M, Kalyanasundaram A (2007) SERCA pump isoforms: their role in calcium transport and disease. Muscle Nerve 35(4):430–442

    CAS  PubMed  Google Scholar 

  • Putney JW Jr (1986) A model for receptor-regulated calcium entry. Cell Calcium 7:1–12

    CAS  PubMed  Google Scholar 

  • Ravel-Chapuis A, Bélanger G, Côté J, Michel RN, Jasmin BJ (2017) Misregulation of calcium-handling proteins promotes hyperactivation of calcineurin-NFAT signaling in skeletal muscle of DM1 mice. Hum Mol Genet 26(12):2192–2206

    CAS  PubMed  Google Scholar 

  • Reiken S, Lacampagne A, Zhou H, Kherani A, Lehnart SE, Ward C, Huang F, Gaburjakova M, Gaburjakova J, Rosemblit N, Warren MS, He KL, Yi GH, Wang J, Burkhoff D, Vassort G, Marks AR (2003) PKA phosphorylation activates the calcium release channel (ryanodine receptor) in skeletal muscle: defective regulation in heart failure. J Cell Biol 160:919–928

    CAS  PubMed  PubMed Central  Google Scholar 

  • Reuben JP, Brandt PW, Grundfest H (1974) Regulation of myoplasmic calcium concentration in intact crayfish muscle fibers. J Mechano Chem Cell Motil 12:269–285

    Google Scholar 

  • Rios E, Pizarro G (1991) Voltage sensor of excitation-contraction coupling in skeletal muscle. Physiol Rev 71:849–908

    CAS  PubMed  Google Scholar 

  • Roos J, PJ DG, Yeromin AV, Ohlsen K, Lioudyno M, Zhang S, Safrina O, Kozak JA, Wagner SL, Cahalan MD, Veliçelebi G, Stauderman KA (2005) STIM1, an essential and conserved component of store-operated Ca2+ channel function. J Cell Biol 169(3):435–445

    CAS  PubMed  PubMed Central  Google Scholar 

  • Salama G, Menshikova EV, Abramson JJ (2000) Molecular interaction between nitric oxide and ryanodine receptors of skeletal and cardiac sarcoplasmic reticulum. Antioxid Redox Signal 2:5–16

    CAS  PubMed  Google Scholar 

  • Sammels E, Parys JB, Missiaen L, De Smedt H, Bultynck G (2010) Intracellular Ca2+ storage in health and disease: a dynamic equilibrium. Cell Calcium 47:297–314

    CAS  PubMed  Google Scholar 

  • Samso M (2015) 3D structure of the Dihydropyridine receptor of skeletal muscle. Eur J Transl Myol 25(1):4840

    PubMed  PubMed Central  Google Scholar 

  • Schartner V, Romero NB, Donkervoort S, Treves S, Munot P, Pierson TM, Dabaj I, Malfatti E, Zaharieva IT, Zorzato F, Abath Neto O, Brochier G, Lornage X, Eymard B, Taratuto AL, Böhm J, Gonorazky H, Ramos-Platt L, Feng L, Phadke R, Bharucha-Goebel DX, Sumner CJ, Bui MT, Lacene E, Beuvin M, Labasse C, Dondaine N, Schneider R, Thompson J, Boland A, Deleuze JF, Matthews E, Pakleza AN, Sewry CA, Biancalana V, Quijano-Roy S, Muntoni F, Fardeau M, Bönnemann CG, Laporte J (2017) Dihydropyridine receptor (DHPR, CACNA1S) congenital myopathy. Acta Neuropathol 133(4):517–533

    CAS  PubMed  Google Scholar 

  • Scherer NM, Deamer DW (1986) Oxidative stress impairs the function of sarcoplasmic reticulum by oxidation of sulfhydryl groupsin the Ca2+- ATPase. Arch Biochem Biophys 246:589–601

    CAS  PubMed  Google Scholar 

  • Schneider MF (1994) Control of calcium release in functioning skeletal muscle fibers. Annu Rev Physiol 56:463–484

    CAS  PubMed  Google Scholar 

  • Schreiber D, Donoghue P, Reilly C, Ohlendieck K (2004) Role of Calsequestrin and related luminal Ca2+-binding proteins as mediators of excitation-contraction coupling. Basic Appl Myol 14:313–322

    Google Scholar 

  • Sencer S, Papineni RV, Halling DB, Pate P, Krol J, Zhang JZ, Hamilton SLJ (2001) Coupling of RYR1 and L-type calcium channels via calmodulin binding domains. J Biol Chem 276:38237–38241

    CAS  PubMed  Google Scholar 

  • Seta KA, Yuan Y, Spicer Z, Lu G, Bedard J, Ferguson TK, Pathrose P, Cole-Strauss A, Kaufhold A, Millhorn DE (2004) The role of calcium in hypoxia-induced signal transduction and gene expression. Cell Calcium 36:331–340

    CAS  PubMed  Google Scholar 

  • Shan J, Betzenhauser MJ, Kushnir A, Reiken S, Meli AC, Wronska A, Dura M, Chen BX, Marks AR (2010a) Role of chronic ryanodine receptor phosphorylation in heart failure and beta-adrenergic receptor blockade in mice. J Clin Invest 120:4375–4387

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shan J, Kushnir A, Betzenhauser MJ, Reiken S, Li J, Lehnart SE, Lindegger N, Mongillo M, Mohler PJ, Marks AR (2010b) Phosphorylation of the ryanodine receptor mediates the cardiac fight or flight response in mice. J Clin Invest 120:4388–4398

    CAS  PubMed  PubMed Central  Google Scholar 

  • Smith JS, Coronado R, Meissner G (1986) Single-channel measurement of the calcium release channel from skeletal muscle sarcoplasmic reticulum. J Gen Physiol 88:573–588

    CAS  PubMed  Google Scholar 

  • Stamler JS, Meissner G (2001) Physiology of nitric oxide in skeletal muscle. Physiol Rev 81:209–237

    CAS  PubMed  Google Scholar 

  • Sun JH, Xu L, Eu JP, Stamler JS, Meissner G (2001a) Classes of thiols that influence the activity of the skeletal muscle calcium release channel. J Biol Chem 276:15625–15630

    CAS  PubMed  Google Scholar 

  • Sun J, Xin C, Eu JP, Stamler JS, Meissner G (2001b) Cysteine-3635 is responsible for skeletal muscle ryanodine receptor modulation by NO. PNAS 98:11158–11162

    CAS  PubMed  Google Scholar 

  • Takeshima H (1993) Primary structure and expression from cDNAs of the ryanodine receptor. Ann N Y Acad Sci 707:165–177

    CAS  PubMed  Google Scholar 

  • Treves S, Jungbluth H, Voermans N, Muntoni F, Zorzato F (2016) Ca2+ handling abnormalities in early-onset muscle diseases: novel concepts and perspectives. Semin Cell Dev Biol 64:201–212

    PubMed  Google Scholar 

  • Tsugorka A, Rios E, Blatter LA (1995) Imaging elementary events of calcium release in skeletal muscle cells. Science 269:1723–1726

    CAS  PubMed  Google Scholar 

  • Tupling AR, Bombardier E, Gupta SC, Hussain D, Vigna C, Bloemberg D, Quadrilatero J, Trivieri MG, Babu GJ, Backx PH, Periasamy M, MacLennan DH, Gramolini AO (2011) Enhanced Ca2+ transport and muscle relaxation in skeletal muscle from sarcolipin-null mice. Am J Physiol Cell Physiol 301:C841–C849

    CAS  PubMed  PubMed Central  Google Scholar 

  • Vukcevic M, Broman M, Islander G, Bodelsson M, Ranklev-Twetman E, CR M¨l, Treves S (2010) Functional properties of RYR1 mutations identified in Swedish patients with malignant hyperthermia and central Core disease. Anesthesia Analgesia 111:185–190

    CAS  PubMed  Google Scholar 

  • Wei L, Dirksen RT (2010) Ryanodinopathies: RyR-linked muscle diseases. Curr Top Membr 66:139–167

    CAS  PubMed  Google Scholar 

  • Wu X, Gao Y, Zhao X, Cui J (2012) Effects of tetramethylpyrazine on nitric oxide synthase activity and calcium ion concentration of skeletal muscle in hindlimb unloading rats. Zhong hua yi xue za zhi 92:2075–2077

    CAS  Google Scholar 

  • Wuytack F, Raeymaekers L, De Smedt H, Eggermont JA, Missiaen L, Van Den Bosch L, De Jaegere S, Verboomen H, Plessers L, Casteels R (1992) Ca2+ transport ATPases and their regulation in muscle and brain. Ann N Y Acad Sci 671:82–91

    CAS  PubMed  Google Scholar 

  • Xia R, Stangler T, Abramson JJ (2000) Skeletal muscle ryanodine receptor is a redox sensor with a well defined redox potential that is sensitive to channel modulators. J Biol Chem 275:36556–36561

    CAS  PubMed  Google Scholar 

  • Xia R, Webb JA, Gnall LL, Cutler K, Abramson JJ (2003) Skeletal muscle sarcoplasmic reticulum contains a NADH-dependent oxidase that generates superoxide. Am J Phys 285:C215–C221

    CAS  Google Scholar 

  • Xu C, Bailly-Maitre B, Reed JC (2005) Endoplasmic reticulum stress: cell life and death decisions. J Clin Invest 115:2656–2664

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yamada T, Fedotovskaya O, Cheng AJ, Cornachione AS, Minozzo FC, Aulin C, Fridén C, Turesson C, Andersson DC, Glenmark B, Lundberg IE, Rassier DE, Westerblad H, Lanner JT (2015) Nitrosative modifications of the Ca2+ release complex and actin underlie arthritis-induced muscle weakness. Ann Rheum Dis 74(10):1907–1914

    CAS  PubMed  Google Scholar 

  • Yamaguchi N, Xin C, Meissner G (2001) Identification of apocalmodulin and Ca2+-calmodulin regulatory domain in skeletal muscle Ca2+ release channel, ryanodine receptor. J Biol Chem 276(25):22579–22585

    CAS  PubMed  Google Scholar 

  • Yuan JP, Zeng W, Huang GN, Worley PF, Muallem S (2007) STIM1 heteromultimerizes TRPC channels to determine their function as store-operated channels. Nat Cell Biol 9(6):636–645

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zalk R, Lehnart SE, Marks AR (2007) Modulation of the rynodine receptor and intracellular calcium. Annu Rev Biochem 76:367–385

    CAS  PubMed  Google Scholar 

  • Zeng W, Yuan JP, Kim MS, Choi YJ, Huang GN, Worley PF, Muallem S (2008) STIM1 gates TRPC channels, but not Orai1, by electrostatic interaction. Mol Cell 32(3):439–448

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors are thankful to Dr. Bhuvnesh Kumar, Director, DIPAS for his constant support and encouragement. One of the authors, Ms. Akanksha Agrawal is thankful for obtaining Senior Research Fellowship from DRDO.

Author information

Authors and Affiliations

  1. DRDO, Defence Institute of Physiology and Allied Sciences, Lucknow Road, Timarpur, Delhi, 110054, India

    Akanksha Agrawal, Geetha Suryakumar & Richa Rathor

Authors
  1. Akanksha Agrawal
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Geetha Suryakumar
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Richa Rathor
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Richa Rathor.

Ethics declarations

Disclosures

No conflicts of interest, financial or otherwise, are declared by the author(s).

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Agrawal, A., Suryakumar, G. & Rathor, R. Role of defective Ca2+ signaling in skeletal muscle weakness: Pharmacological implications. J. Cell Commun. Signal. 12, 645–659 (2018). https://doi.org/10.1007/s12079-018-0477-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12079-018-0477-z

Keywords

Search

Navigation