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Toward the roles of store-operated Ca2+ entry in skeletal muscle

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Abstract

Store-operated Ca2+ entry (SOCE) has been found to be a rapidly activated robust mechanism in skeletal muscle fibres. It is conducted across the junctional membranes by stromal interacting molecule 1 (STIM1) and Orai1, which are housed in the sarcoplasmic reticulum (SR) and tubular (t-) system, respectively. These molecules that conduct SOCE appear evenly distributed throughout the SR and t-system of skeletal muscle, allowing for rapid and local control in response to depletions of Ca2+ from SR. The significant depletion of SR Ca2+ required to reach the activation threshold for SOCE could only be achieved during prolonged bouts of excitation–contraction coupling (EC coupling) in a healthy skeletal muscle fibre, meaning that this mechanism is not responsible for refilling the SR with Ca2+ during periods of fibre quiescence. While Ca2+ in SR remains below the activation threshold for SOCE, a low-amplitude persistent Ca2+ influx is provided to the junctional cleft. This article reviews the properties of SOCE in skeletal muscle and the proposed molecular mechanism, assesses its potential physiological roles during EC coupling, namely refilling the SR with Ca2+ and simple balancing of Ca2+ within the cell, and also proposes the possibility of SOCE as a potential regulator of t-system and SR membrane protein function.

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Abbreviations

SR:

Sarcoplasmic reticulum

SOCE:

Store-operated Ca2+ entry

t-system:

Tubular system

EC coupling:

Excitation–contraction coupling

ER:

Endoplasmic reticulum

CSQ:

Calsequestrin

DHPR:

Dihydropyridine receptor

RyR:

Ryanodine receptor

STIM:

Stromal interacting molecule

TnC:

Troponin C

References

  1. Allard B, Couchoux H, Pouvreau S, Jacquemond V (2006) Sarcoplasmic reticulum Ca2+ release and depletion fail to affect sarcolemmal ion channel activity in mouse skeletal muscle. J Physiol 575:69–81

    Article  CAS  PubMed  Google Scholar 

  2. Allen DG, Lamb GD, Westerblad H (2008) Impaired calcium release during fatigue. J Appl Physiol 104:296–305

    Article  CAS  PubMed  Google Scholar 

  3. Allen DG, Lamb GD, Westerblad H (2008) Skeletal muscle fatigue: cellular mechanisms. Physiol Rev 88:287–332

    Article  CAS  PubMed  Google Scholar 

  4. Almers W, Fink R, Palade PT (1981) Calcium depletion in frog muscle tubules: the decline of calcium current under maintained depolarization. J Physiol 312:177–207

    CAS  PubMed  Google Scholar 

  5. Arruda AP, Oliveira GM, Carvalho DP, De Meis L (2005) Thyroid hormones differentially regulate the distribution of rabbit skeletal muscle Ca2+-ATPase (SERCA) isoforms in light and heavy sarcoplasmic reticulum. Mol Membr Biol 22:529–537

    Article  CAS  PubMed  Google Scholar 

  6. Baylor SM, Hollingworth S (2003) Sarcoplasmic reticulum calcium release compared in slow-twitch and fast-twitch fibres of mouse muscle. J Physiol 551:125–138

    Article  CAS  PubMed  Google Scholar 

  7. Beard NA, Wei L, Dulhunty AF (2009) Ca2+ signaling in striated muscle: the elusive roles of triadin, junctin, and calsequestrin. Eur Biophys J 39:27–36

    Article  CAS  PubMed  Google Scholar 

  8. Berbey C, Allard B (2009) Electrically silent divalent cation entries in resting and active voltage-controlled muscle fibers. Biophys J 96:2648–2657

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  10. Bolanos P, Guillen A, DiPolo R, Caputo C (2009) Factors affecting SOCE activation in mammalian skeletal muscle fibers. J Physiol Sci 59:317–328

    Article  CAS  PubMed  Google Scholar 

  11. Brum G, Fitts R, Pizarro G, Rios E (1988) Voltage sensors of the frog skeletal muscle membrane require calcium to function in excitation–contraction coupling. J Physiol 398:475–505

    CAS  PubMed  Google Scholar 

  12. Brum G, Rios E, Stefani E (1988) Effects of extracellular calcium on calcium movements of excitation–contraction coupling in frog skeletal muscle fibres. J Physiol 398:441–473

    CAS  PubMed  Google Scholar 

  13. Cahalan MD (2009) STIMulating store-operated Ca2+ entry. Nat Cell Biol 11:669–677

    Article  CAS  PubMed  Google Scholar 

  14. Collet C, Ma J (2004) Calcium-dependent facilitation and graded deactivation of store-operated calcium entry in fetal skeletal muscle. Biophys J 87:268–275

    Article  CAS  PubMed  Google Scholar 

  15. Curtis BA (1966) Ca fluxes in single twitch muscle fibers. J Gen Physiol 50:255–267

    Article  CAS  PubMed  Google Scholar 

  16. Curtis BA, Eisenberg RS (1985) Calcium influx in contracting and paralyzed frog twitch muscle fibers. J Gen Physiol 85:383–408

    Article  CAS  PubMed  Google Scholar 

  17. Dirksen RT (2009) Checking your SOCCs and feet: the molecular mechanisms of Ca2+ entry in skeletal muscle. J Physiol 587:3139–3147

    Article  CAS  PubMed  Google Scholar 

  18. Ducret T, Vandebrouck C, Cao ML, Lebacq J, Gailly P (2006) Functional role of store-operated and stretch-activated channels in murine adult skeletal muscle fibres. J Physiol 575:913–924

    Article  CAS  PubMed  Google Scholar 

  19. Duke AM, Steele DS (2008) The presence of a functional t-tubule network increases the sensitivity of RyR1 to agonists in skinned rat skeletal muscle fibres. Cell Calcium 44:411–421

    Article  CAS  PubMed  Google Scholar 

  20. Edwards JN, Friedrich O, Cully TR, von Wegner F, Murphy RM, Launikonis BS (2010) Upregulation of store-operated Ca2+ entry in dystrophic mdx mouse muscle. Am J Physiol Cell Physiol 299:C42–C50

    Article  CAS  PubMed  Google Scholar 

  21. Edwards JN, Launikonis BS (2008) The accessibility and interconnectivity of the tubular system network in toad skeletal muscle. J Physiol 586:5077–5089

    Article  CAS  PubMed  Google Scholar 

  22. Edwards JN, Murphy RM, Cully TR, von Wegner F, Friedrich O, Launikonis BS (2010) Ultra-rapid activation and deactivation of store-operated Ca2+ entry in skeletal muscle. Cell Calcium 47:458–467

    Article  CAS  PubMed  Google Scholar 

  23. Franzini-Armstrong C (2009) Architecture and regulation of the Ca2+ delivery system in muscle cells. Appl Physiol Nutr Metab 34:323–327

    Article  CAS  PubMed  Google Scholar 

  24. Fryer MW, Owen VJ, Lamb GD, Stephenson DG (1995) Effects of creatine phosphate and Pi on Ca2+ movements and tension development in rat skinned skeletal muscle fibres. J Physiol 482:123–140

    CAS  PubMed  Google Scholar 

  25. Fryer MW, Stephenson DG (1996) Total and sarcoplasmic reticulum calcium contents of skinned fibres from rat skeletal muscle. J Physiol 493:357–370

    CAS  PubMed  Google Scholar 

  26. Gissel H, Clausen T (1999) Excitation-induced Ca2+ uptake in rat skeletal muscle. Am J Physiol 276:R331–R339

    CAS  PubMed  Google Scholar 

  27. Gonzalez Narvaez AA, Castillo A (2007) Ca2+ store determines gating of store operated calcium entry in mammalian skeletal muscle. J Muscle Res Cell Motil 28:105–113

    Article  CAS  PubMed  Google Scholar 

  28. Gwack Y, Srikanth S, Feske S, Cruz-Guilloty F, Oh-hora M, Neems DS, Hogan PG, Rao A (2007) Biochemical and functional characterization of Orai proteins. J Biol Chem 282:16232–16243

    Article  CAS  PubMed  Google Scholar 

  29. Ikemoto N, Antoniu B, Kang JJ, Meszaros LG, Ronjat M (1991) Intravesicular calcium transient during calcium release from sarcoplasmic reticulum. Biochemistry 30:5230–5237

    Article  CAS  PubMed  Google Scholar 

  30. Kurebayashi N, Ogawa Y (2001) Depletion of Ca2+ in the sarcoplasmic reticulum stimulates Ca2+ entry into mouse skeletal muscle fibres. J Physiol 533:185–199

    Article  CAS  PubMed  Google Scholar 

  31. Lamb GD, Junankar PR, Stephenson DG (1995) Raised intracellular [Ca2+] abolishes excitation–contraction coupling in skeletal muscle fibres of rat and toad. J Physiol 489:349–362

    CAS  PubMed  Google Scholar 

  32. Lamb GD, Stephenson DG (1991) Effect of Mg2+ on the control of Ca2+ release in skeletal muscle fibres of the toad. J Physiol 434:507–528

    CAS  PubMed  Google Scholar 

  33. Launikonis BS, Barnes M, Stephenson DG (2003) Identification of the coupling between skeletal muscle store-operated Ca2+ entry and the inositol trisphosphate receptor. Proc Natl Acad Sci USA 100:2941–2944

    Article  CAS  PubMed  Google Scholar 

  34. Launikonis BS, Brum G, Rios E, Zhou J (2005) How the calcium-precipitating anions inorganic phosphate and SO 2−4 alter intra-SR calcium in skeletal muscle cells. Biophys J 88:89a

    Google Scholar 

  35. Launikonis BS, Rios E (2007) Store-operated Ca2+ entry during intracellular Ca2+ release in mammalian skeletal muscle. J Physiol 583:81–97

    Article  CAS  PubMed  Google Scholar 

  36. Launikonis BS, Stephenson DG, Friedrich O (2009) Rapid Ca2+ flux through the transverse tubular membrane, activated by individual action potentials in mammalian skeletal muscle. J Physiol 587:2299–2312

    Article  CAS  PubMed  Google Scholar 

  37. Launikonis BS, Zhou J, Royer L, Shannon TR, Brum G, Rios E (2006) Depletion "skraps" and dynamic buffering inside the cellular calcium store. Proc Natl Acad Sci USA 103:2982–2987

    Article  CAS  PubMed  Google Scholar 

  38. Laver DR, O'Neill ER, Lamb GD (2004) Luminal Ca2+-regulated Mg2+ inhibition of skeletal RyRs reconstituted as isolated channels or coupled clusters. J Gen Physiol 124:741–758

    Article  CAS  PubMed  Google Scholar 

  39. Lee KP, Yuan JP, Zeng W, So I, Worley PF, Muallem S (2009) Molecular determinants of fast Ca2+-dependent inactivation and gating of the Orai channels. Proc Natl Acad Sci USA 106:14687–14692

    Article  CAS  PubMed  Google Scholar 

  40. Lewis RS (2007) The molecular choreography of a store-operated calcium channel. Nature 446:284–287

    Article  CAS  PubMed  Google Scholar 

  41. Luik RM, Wang B, Prakriya M, Wu MM, Lewis RS (2008) Oligomerization of STIM1 couples ER calcium depletion to CRAC channel activation. Nature 454:538–542

    Article  CAS  PubMed  Google Scholar 

  42. Luik RM, Wu MM, Buchanan J, Lewis RS (2006) The elementary unit of store-operated Ca2+ entry: local activation of CRAC channels by STIM1 at ER-plasma membrane junctions. J Cell Biol 174:815–825

    Article  CAS  PubMed  Google Scholar 

  43. Lyfenko AD, Dirksen RT (2008) Differential dependence of store-operated and excitation-coupled Ca2+ entry in skeletal muscle on STIM1 and Orai1. J Physiol 586:4815–4824

    Article  CAS  PubMed  Google Scholar 

  44. Lyfenko AD, Dirksen RT (2010) Molecular mechanism of store-operated Ca2+ entry in adult mammalian skeletal muscle. Biophys J 98:202a

    Article  Google Scholar 

  45. McCarl CA, Picard C, Khalil S, Kawasaki T, Rother J, Papolos A, Kutok J, Hivroz C, Ledeist F, Plogmann K, Ehl S, Notheis G, Albert MH, Belohradsky BH, Kirschner J, Rao A, Fischer A, Feske S (2009) ORAI1 deficiency and lack of store-operated Ca2+ entry cause immunodeficiency, myopathy, and ectodermal dysplasia. J Allergy Clin Immunol 124(1311–1318):e1317

    Google Scholar 

  46. 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 

  47. Mullins FM, Park CY, Dolmetsch RE, Lewis RS (2009) STIM1 and calmodulin interact with Orai1 to induce Ca2+-dependent inactivation of CRAC channels. Proc Natl Acad Sci USA 106:15495–15500

    Article  CAS  PubMed  Google Scholar 

  48. Murphy RM, Larkins NT, Mollica JP, Beard NA, Lamb GD (2009) Calsequestrin content and SERCA determine normal and maximal Ca2+ storage levels in sarcoplasmic reticulum of fast- and slow-twitch fibres of rat. J Physiol 587:443–460

    Article  CAS  PubMed  Google Scholar 

  49. Ng SW, di Capite J, Singaravelu K, Parekh AB (2008) Sustained activation of the tyrosine kinase Syk by antigen in mast cells requires local Ca2+ influx through Ca2+ release-activated Ca2+ channels. J Biol Chem 283:31348–31355

    Article  CAS  PubMed  Google Scholar 

  50. Parekh AB (2008) Ca2+ microdomains near plasma membrane Ca2+ channels: impact on cell function. J Physiol 586:3043–3054

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  52. Park CY, Hoover PJ, Mullins FM, Bachhawat P, Covington ED, Raunser S, Walz T, Garcia KC, Dolmetsch RE, Lewis RS (2009) STIM1 clusters and activates CRAC channels via direct binding of a cytosolic domain to Orai1. Cell 136:876–890

    Article  CAS  PubMed  Google Scholar 

  53. Park H, Park IY, Kim E, Youn B, Fields K, Dunker AK, Kang C (2004) Comparing skeletal and cardiac calsequestrin structures and their calcium binding: a proposed mechanism for coupled calcium binding and protein polymerization. J Biol Chem 279:18026–18033

    Article  CAS  PubMed  Google Scholar 

  54. Penna A, Demuro A, Yeromin AV, Zhang SL, Safrina O, Parker I, Cahalan MD (2008) The CRAC channel consists of a tetramer formed by Stim-induced dimerization of Orai dimers. Nature 456:116–120

    Article  CAS  PubMed  Google Scholar 

  55. Posterino GS, Lamb GD (2003) Effect of sarcoplasmic reticulum Ca2+ content on action potential-induced Ca2+ release in rat skeletal muscle fibres. J Physiol 551:219–237

    Article  CAS  PubMed  Google Scholar 

  56. Posterino GS, Lamb GD, Stephenson DG (2000) Twitch and tetanic force responses and longitudinal propagation of action potentials in skinned skeletal muscle fibres of the rat. J Physiol 527:131–137

    Article  CAS  PubMed  Google Scholar 

  57. Rome LC (2006) Design and function of superfast muscles: new insights into the physiology of skeletal muscle. Annu Rev Physiol 68:193–221

    Article  CAS  PubMed  Google Scholar 

  58. Royer L, Rios E (2009) Deconstructing calsequestrin. Complex buffering in the calcium store of skeletal muscle. J Physiol 587:3101–3111

    Article  CAS  PubMed  Google Scholar 

  59. Stiber J, Hawkins A, Zhang ZS, Wang S, Burch J, Graham V, Ward CC, Seth M, Finch E, Malouf N, Williams RS, Eu JP, Rosenberg P (2008) STIM1 signalling controls store-operated calcium entry required for development and contractile function in skeletal muscle. Nat Cell Biol 10:688–697

    Article  CAS  PubMed  Google Scholar 

  60. Vandebrouck C, Martin D, Colson-Van Schoor M, Debaix H, Gailly P (2002) Involvement of TRPC in the abnormal calcium influx observed in dystrophic (mdx) mouse skeletal muscle fibers. J Cell Biol 158:1089–1096

    Article  CAS  PubMed  Google Scholar 

  61. Veratti E (1961) Investigations on the fine structure of striated muscle fiber (read before the Reale Istituto Lombardo, 13 March 1902). J Biophys Biochem Cytol 10(4 Suppl):1–59

    Article  PubMed  Google Scholar 

  62. Zhao X, Yoshida M, Brotto L, Takeshima H, Weisleder N, Hirata Y, Nosek TM, Ma J, Brotto M (2005) Enhanced resistance to fatigue and altered calcium handling properties of sarcalumenin knockout mice. Physiol Genomics 23:72–78

    Article  CAS  PubMed  Google Scholar 

  63. Zhou J, Yi J, Royer L, Launikonis BS, Gonzalez A, Garcia J, Rios E (2006) A probable role of dihydropyridine receptors in repression of Ca2+ sparks demonstrated in cultured mammalian muscle. Am J Physiol Cell Physiol 290:C539–C553

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank D. George Stephenson (La Trobe University, Melbourne) for the helpful comments on the manuscript. This work was supported by the Australian Research Council Discovery Project and the National Health and Medical Research Council (NHMRC; Australia) Project Grant to BS Launikonis. RM Murphy was a Peter Doherty Fellow of the NHMRC.

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Correspondence to Bradley S. Launikonis.

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Launikonis, B.S., Murphy, R.M. & Edwards, J.N. Toward the roles of store-operated Ca2+ entry in skeletal muscle. Pflugers Arch - Eur J Physiol 460, 813–823 (2010). https://doi.org/10.1007/s00424-010-0856-7

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