Biophysical Reviews

, Volume 6, Issue 1, pp 133–160 | Cite as

The excitation–contraction coupling mechanism in skeletal muscle

Review

Abstract

First coined by Alexander Sandow in 1952, the term excitation–contraction coupling (ECC) describes the rapid communication between electrical events occurring in the plasma membrane of skeletal muscle fibres and Ca2+ release from the SR, which leads to contraction. The sequence of events in twitch skeletal muscle involves: (1) initiation and propagation of an action potential along the plasma membrane, (2) spread of the potential throughout the transverse tubule system (T-tubule system), (3) dihydropyridine receptors (DHPR)-mediated detection of changes in membrane potential, (4) allosteric interaction between DHPR and sarcoplasmic reticulum (SR) ryanodine receptors (RyR), (5) release of Ca2+ from the SR and transient increase of Ca2+ concentration in the myoplasm, (6) activation of the myoplasmic Ca2+ buffering system and the contractile apparatus, followed by (7) Ca2+ disappearance from the myoplasm mediated mainly by its reuptake by the SR through the SR Ca2+ adenosine triphosphatase (SERCA), and under several conditions movement to the mitochondria and extrusion by the Na+/Ca2+ exchanger (NCX). In this text, we review the basics of ECC in skeletal muscle and the techniques used to study it. Moreover, we highlight some recent advances and point out gaps in knowledge on particular issues related to ECC such as (1) DHPR-RyR molecular interaction, (2) differences regarding fibre types, (3) its alteration during muscle fatigue, (4) the role of mitochondria and store-operated Ca2+ entry in the general ECC sequence, (5) contractile potentiators, and (6) Ca2+ sparks.

Keywords

Excitation–contraction coupling Ca2+ transients Skeletal muscle Fibre types Mitochondria 

Notes

Acknowledgments

The financial support comes from University of Antioquia, Medellín, Colombia (J.C.C.) and Venezuelan Institute for Scientific Research, Venezuela (P.B. and C.C.). We want to acknowledge Alis Guillén for help in obtaining some experimental results presented in this review and Carolina Figueroa por sharing some information with us.

Conflict of interest

Juan C. Calderón, Pura Bolaños and Carlo Caputo declare that they have no conflict of interest.

Human and animal studies

This article does not contain any studies with human or animal subjects performed by any of the authors.

References

  1. Abbiss C, Laursen P (2005) Models to explain fatigue during prolonged endurance cycling. Sports Med 35:865–898PubMedGoogle Scholar
  2. Adams B, Tanabe T, Mikami A, Numa S, Beam K (1990) Intramembrane charge movement restored in dysgenic skeletal muscle by injection of dihydropyridine receptor cDNAs. Nature 346:569–572PubMedGoogle Scholar
  3. Adrian R, Costantin L, Peachey L (1969) Radial spread and contraction in frog muscle fibres. J Physiol 204:231–257PubMedCentralPubMedGoogle Scholar
  4. Allen D, Lee J, Westerblad H (1989) Intracellular calcium and tension during fatigue in isolated single muscle fibres from Xenopus laevis. J Physiol 415:433–458PubMedCentralPubMedGoogle Scholar
  5. Allen D, Lännergren J, Westerblad H (1997) The role of ATP in the regulation of intracellular Ca2+ release in single fibres of mouse skeletal muscle. J Physiol 498:587–600PubMedCentralPubMedGoogle Scholar
  6. Allen D, Lännergren J, Westerblad H (2002) Intracellular ATP measured with luciferin/luciferase in isolated single mouse skeletal muscle fibres. Pflugers Arch 443(5–6):836–842PubMedGoogle Scholar
  7. Allen D, Lamb G, Westerblad H (2008) Skeletal muscle fatigue: cellular mechanisms. Physiol Rev 88:287–332PubMedGoogle Scholar
  8. Alonso M, Villalobos C, Chamero P, Alvarez J, Garcia-Sancho J (2006) Calcium microdomains in mitochondria and nucleus. Cell Calcium 40:513–525PubMedGoogle Scholar
  9. Anderson A, Altafaj X, Zheng Z, Wang Z, Delbono O, Ronjat M et al (2006) The junctional SR protein JP-45 affects the functional expression of the voltage-dependent Ca2+ channel Cav1.1. J Cell Sci 119:2145–2155PubMedCentralPubMedGoogle Scholar
  10. Apostol S, Ursu D, Lehmann-Horn F, Melzer W (2009) Local calcium signals induced by hyper-osmotic stress in mammalian skeletal muscle cells. J Muscle Res Cell Motil 30:97–109PubMedGoogle Scholar
  11. Appelt D, Buenviaje B, Champ C, Franzini-Armstrong C (1989) Quantitation of “junctional feet” content in two types of muscle fiber from hind limb muscles of the rat. Tissue Cell 21:783–794PubMedGoogle Scholar
  12. Armstrong C, Bezanilla F, Horowitz P (1972) Twitches in the presence of ethylene glycol bis(-aminoethyl ether)-N, N′-tetracetic acid. Biochim Biophys Acta 267:605–608PubMedGoogle Scholar
  13. Ávila G, Dirksen R (2000) Functional impact of the ryanodine receptor on the skeletal muscle L-type Ca2+ channel. J Gen Physiol 114:467–480Google Scholar
  14. Axelsson J, Thesleff S (1958) Activation of the contractile mechanism in striated muscle. Acta Physiol Scand 44:55–66PubMedGoogle Scholar
  15. Balnave C, Allen D (1998) Evidence for Na+/Ca2+ Exchange in intact single skeletal muscle fibers from the mouse. Am J Physiol Cell Physiol 274:940–946Google Scholar
  16. Bangsbo J, Juel C (2006) Lactic acid accumulation is a disadvantage during muscle activity. J Appl Physiol 100:1412–1413PubMedGoogle Scholar
  17. Bär A, Pette D (1988) Three fast myosin heavy chains in adult rat skeletal muscle. FEBS Lett 235:153–155PubMedGoogle Scholar
  18. Barclay J, Hansel M (1991) Free radicals may contribute to oxidative skeletal muscle fatigue. Can J Physiol Pharmacol 69:279–284PubMedGoogle Scholar
  19. Baughman JM, Perocchi F, Girgis HS, Plovanich M, Belcher-Timme CA, Sancak Y, Bao XR, Strittmatter L, Goldberger O, Bogorad RL, Koteliansky V, Mootha VK (2011) Integrative genomics identifies MCU as an essential component of the mitochondrial calcium uniporter. Nature 476:341–345PubMedCentralPubMedGoogle Scholar
  20. Baylor S, Hollingworth S (1988) Fura-2 calcium transients in frog skeletal muscle fibres. J Physiol 403:151–192PubMedCentralPubMedGoogle Scholar
  21. Baylor S, Hollingworth S (2003) Sarcoplasmic reticulum calcium release compared in slow-twitch and fast-twitch fibres of mouse muscle. J Physiol 551:125–138PubMedCentralPubMedGoogle Scholar
  22. Baylor S, Hollingworth S (2011) Calcium indicators and calcium signalling in skeletal muscle fibres during excitation-contraction coupling. Prog Biophys Mol Biol 105:162–179PubMedCentralPubMedGoogle Scholar
  23. Beam K, Franzini-Armstong C (1997) Functional and structural approaches to the study of excitation-contraction coupling. Methods Cell Biol 52:283–306PubMedGoogle Scholar
  24. Beam K, Knudson C, Powell J (1986) A lethal mutation in mice eliminates the slow calcium current in skeletal muscle cells. Nature 320:168–170PubMedGoogle Scholar
  25. Bekoff A, Betz W (1977) Physiological properties of dissociated muscle fibres obtained from innervated and denervated adult rat muscle. J Physiol 271:25–40PubMedCentralPubMedGoogle Scholar
  26. Bergström M, Hultman E (1988) Energy cost and fatigue during intermittent electrical stimulation of human skeletal muscle. J Appl Physiol 65:1500–1505PubMedGoogle Scholar
  27. Bernardi P (1992) Modulation of the mitochondrial cyclosporin A-sensitive permeability transition pore by the proton electrochemical gradient. Evidence that the pore can be opened by membrane depolarization. J Biol Chem 267:8834–8839PubMedGoogle Scholar
  28. Bernardi P (1999) Mitochondrial transport of cations: channels, exchangers, and permeability transition. Physiol Rev 79:1127–1155PubMedGoogle Scholar
  29. Bernardi P, von Stockum S (2012) The permeability transition pore as a Ca(2+) release channel: new answers to an old question. Cell Calcium 52:22–27PubMedCentralPubMedGoogle Scholar
  30. Berridge M (2006) Calcium microdomains: organization and function. Cell Calcium 40:405–412PubMedGoogle Scholar
  31. Beutner G, Sharma V, Giovannucci D, Yule D, Sheu S (2001) Identification of a ryanodine receptor in rat heart mitochondria. J Biol Chem 276:21482–21488PubMedGoogle Scholar
  32. Beutner G, Sharma V, Lin L, Ryu S, Dirksen R, Sheu S (2005) Type 1 ryanodine receptor in cardiac mitochondria: transducer of excitation-metabolism coupling. Biochim Biophys Acta 1717:1–10PubMedGoogle Scholar
  33. Bezanilla F (2000) The voltage sensor in voltage-dependent ion channels. Physiol Rev 80:555–592PubMedGoogle Scholar
  34. Bezanilla F, Caputo C, González-Serratos H, Venosa R (1972) Sodium dependence of the inward spread of activation in isolated twitch muscle fibres of the frog. J Physiol 223:507–523PubMedCentralPubMedGoogle Scholar
  35. Bigland-Ritchie B, Woods J (1984) Changes in muscle contractile properties and neural control during human muscular fatigue. Muscle Nerve 7:691–699PubMedGoogle Scholar
  36. Bleunven C, Treves S, Jinyu X, Leo E, Ronjat M, De Waard M et al (2008) SRP-27 is a novel component of the supramolecular signaling complex involved in skeletal muscle excitation-contraction coupling. Biochem J 411:343–349PubMedGoogle Scholar
  37. Block B, Imagawa T, Campbell K, Franzini-Armstrong C (1988) Structural evidence for direct interaction between the molecular components of the transverse tubule/sarcoplasmic reticulum junction in skeletal muscle. J Cell Biol 107:2587–2600PubMedGoogle Scholar
  38. Bolaños P, Guillén A, Rojas H, Boncompagni S, Caputo C (2008) The use of CalciumOrange-5N as a specific marker of mitochondrial Ca2+ in mouse skeletal muscle fibers. Pflugers Arch 455:721–731PubMedGoogle Scholar
  39. Bolaños P, Guillén A, DiPolo R, Caputo C (2009) Factors affecting SOCE activation in mammalian skeletal muscle fibers. J Physiol Sci 59:317–328PubMedGoogle Scholar
  40. Boncompagni S, Rossi A, Micaroni M, Beznoussenko G, Polishchuk R, Dirksen R, Protasi F (2009) Mitochondria are linked to calcium stores in striated muscle by developmentally regulated tethering structures. Mol Biol Cell 20:1058–1067PubMedCentralPubMedGoogle Scholar
  41. Boncompagni S, Thomas M, Lopez J, Allen P, Yuan Q, Kranias E, Franzini-Armstrong C, Perez C (2013) Triadin/Junctin double null mouse reveals a differential role for Triadin and Junctin in anchoring CASQ to the jSR and regulating Ca(2+) homeostasis. PLoS ONE 7:e39962Google Scholar
  42. Bottinelli R, Reggiani C (2000) Human skeletal muscle fibres: molecular and functional diversity. Prog Biophys Mol Biol 73:195–262PubMedGoogle Scholar
  43. Brochet D, Yang D, Di Maio A, Lederer W, Franzini-Armstrong C, Cheng H (2005) Ca2+ blinks: rapid nanoscopic store calcium signaling. Proc Natl Acad Sci U S A 102:3099–3104PubMedCentralPubMedGoogle Scholar
  44. Brooke M, Kaiser K (1970) Three “myosin adenosine triphosphatase” systems: the nature of their pH lability and sulfhydryl dependence. J Histochem Cytochem 18:670–672PubMedGoogle Scholar
  45. Brotto M, Nosek T (1996) Hydrogen peroxide disrupts Ca2+ release from the sarcoplasmic reticulum of rat skeletal muscle fibers. J Appl Physiol 81:731–737PubMedGoogle Scholar
  46. Bruton J, Tavi P, Aydin J, Wasterblad H, Lanergren J (2003) Mitochondrial and myoplasmic [Ca2+] in single fibers from Mouse limb muscles during repeated tetanic contraction. J Physiol 551:179–190PubMedCentralPubMedGoogle Scholar
  47. Bruton J, Place N, Yamada T, Silva J, Andrade F, Dahlstedt A, Zhang S, Katz A, Larsson N, Westerblad H (2008) Reactive oxygen species and fatigue-induced prolonged low-frequency force depression in skeletal muscle fibres of rats, mice and SOD2 overexpressing mice. J Physiol 586:175–184PubMedCentralPubMedGoogle Scholar
  48. Bruton J, Cheng A, Westerblad H (2012) Methods to detect Ca2+ in living cells. Adv Exp Med Biol 740:27–43PubMedGoogle Scholar
  49. Buck E, Nguyen H, Pessah I, Allen P (1997) Dyspedic mouse skeletal muscle expresses major elements of the triadic junction but lacks detectable ryanodine receptor protein and function. J Biol Chem 272:7360–7367PubMedGoogle Scholar
  50. Buntinas L, Gunter K, Sparagna G, Gunter T (2001) The rapid mode of calcium uptake into heart mitochondria (RaM): comparison to RaM in liver mitochondria. Biochim Biophys Acta 1504:248–261PubMedGoogle Scholar
  51. Burke R, Levine D, Tsairis P, Zajac F (1973) Physiological types and histochemical profiles in motor units of the cat gastrocnemius. J Physiol 234:723–748PubMedCentralPubMedGoogle Scholar
  52. Calderón J (2013) Enzymatic dissociation of long muscles from mouse: a model for the study of fiber types in skeletal muscle. Iatreia 26:117–126Google Scholar
  53. Calderón JC, Bolaños P, Torres SH, Rodriguez-Arroyo G, Caputo C (2009) Different fibre populations distinguished by their calcium transient characteristics in enzymatically dissociated murine flexor digitorum brevis and soleus muscles. J Muscle Res Cell Motil 30:125–137PubMedGoogle Scholar
  54. Calderón JC, Bolaños P, Caputo C (2010) Myosin heavy chain isoform composition and Ca2+ transients in fibres from enzymatically dissociated murine soleus and extensor digitorum longus muscles. J Physiol 588(1):267–279PubMedCentralPubMedGoogle Scholar
  55. Calderón JC, Bolaños P, Caputo C (2011) Kinetic changes in tetanic calcium transients in enzymatically dissociated muscle fibres under repetitive stimulation. J Physiol 589(21):5269–5283PubMedCentralPubMedGoogle Scholar
  56. Calderón J, Raigosa D, Giraldo M, Bolaños P, Caputo C (2013) Calibration of Ca2+ transients obtained with the fast Ca2+ and Mg2+ dye Magfluo-4. Biophys J 104(2–S1):293a. abstract,1502-PosGoogle Scholar
  57. Calderón-Vélez J, Figueroa-Gordon C (2009) El acoplamiento exitación-contracción en el músculo esquelético: preguntas por responder a pesar de 50 años de studio. Biomedica 29:140–160PubMedGoogle Scholar
  58. Caputo C (1983) Pharmacological investigations of excitation-contraction coupling. Chapter 14. In: Peachey L, Adrian R (eds) Handbook of physiology. American Physiological Society, BethesdaGoogle Scholar
  59. Caputo C, Bolaños P (2008) Effect of mitochondria poisoning by FCCP on Ca2+ signaling in mouse skeletal muscle fibers. Pflugers Arch 455:733–743PubMedGoogle Scholar
  60. Caputo C, Giménez M (1967) Effects of external Ca2+ deprivation on single muscle fibres. J Gen Physiol 50:2177–2195PubMedCentralPubMedGoogle Scholar
  61. Caputo C, Edman K, Lou F, Sun Y (1994) Variation in myoplasmic Ca concentration during contraction and relaxation studied by the indicator fluo-3 in frog muscle fibres. J Physiol 478:137–148PubMedCentralPubMedGoogle Scholar
  62. Caputo C, Bolaños P, Escobar A (1999) Fast calcium removal during single twitches in amphibian skeletal muscle fibres. J Muscle Res Cell Motil 20:555–567PubMedGoogle Scholar
  63. Caputo C, Bolaños P, González A (2004) Inactivation of Ca2+ transients in amphibian and mammalian muscle fibres. J Muscle Res Cell Motil 25:315–328PubMedGoogle Scholar
  64. Carafoli E, Tiozzo R, Lugli G, Crovetti F, Kratzing C (1974) The release of calcium from heart mitochondria by sodium. J Mol Cell Cardiol 6:361–371PubMedGoogle Scholar
  65. Carroll S, Klein M, Schneider M (1997) Decay of calcium transients after electrical stimulation in rat fast- and slow-twitch skeletal muscle fibres. J Physiol 501:573–588PubMedCentralPubMedGoogle Scholar
  66. Casarotto M, Cui Y, Karunasekara Y, Harvey P, Norris N, Borrad P et al (2006) Structural and functional characterization of interactions between the dihydropyridine receptor II-III loop and the ryanodine receptor. Clin Exp Pharmacol Physiol 33:1114–1117PubMedGoogle Scholar
  67. Casas M, Figueroa R, Jorquera G, Escobar M, Molgó J, Jaimovich E (2010) IP(3)-dependent, post-tetanic calcium transients induced by electrostimulation of adult skeletal muscle fibers. J Gen Physiol 136:455–467PubMedCentralPubMedGoogle Scholar
  68. Cheng H, Lederer W (2008) Calcium sparks. Physiol Rev 88:1491–1545Google Scholar
  69. Cheng H, Lederer W, Cannell M (1993) Calcium sparks: elementary events underlying excitation-contraction coupling in heart muscle. Science 262:740–744Google Scholar
  70. Cheung A, Dantzig J, Hollingworth S, Baylor S, Goldman Y, Mitchison T, Straight A (2002) A small-molecule inhibitor of skeletal muscle myosin II. Nat Cell Biol 4:83–89PubMedGoogle Scholar
  71. Chin E, Allen D (1998) The contribution of pH-dependent mechanisms to fatigue at different intensities in mammalian single muscle fibres. J Physiol 512:831–840PubMedCentralPubMedGoogle Scholar
  72. Coronado R, Morrissette J, Sukhareva, Vaughan D (1994) Structure and function of ryanodine receptors. Am J Physiol 266:C1485–C1504PubMedGoogle Scholar
  73. Craig R, Padrón R (2004) Molecular structure of the sarcomere. Chapter 7. In: Engel A, Franzini-Armstrong C (eds) Myology, 3rd edn. McGrawHill, New York, pp 129–166Google Scholar
  74. Csordás G, Renken C, Várnai P, Walter L, Weaver D, Buttle K, Balla T, Mannella C, Hajnóczky G (2006) Structural and functional features and significance of the physical linkage between ER and mitochondria. J Cell Biol 174:915–921PubMedCentralPubMedGoogle Scholar
  75. Cully T, Launikonis B (2013) Store-operated Ca2+ entry is not required for store refilling in skeletal muscle. Clin Exp Pharmacol Physiol 40:338–344PubMedGoogle Scholar
  76. Dahlstedt AJ, Katz A, Westerblad H (2001) Role of myoplasmic phosphate in contractile function of skeletal muscle: studies on creatine kinase-deficient mice. J Physiol 533:379–388PubMedCentralPubMedGoogle Scholar
  77. Damiani E, Margreth A (1994) Characterization study of the ryanodine receptor and of calsequestrin isoforms of mammalian skeletal muscles in relation to fibre types. J Muscle Res Cell Motil 15:86–101PubMedGoogle Scholar
  78. Darnley G, Duke A, Steele D, MacFarlane N (2001) Effects of reactive oxygen species on aspects of excitation-contraction coupling in chemically skinned rabbit diaphragm muscle fibres. Exp Physiol 86:161–168PubMedGoogle Scholar
  79. Davies K, Quintanilha A, Brooks G, Packer L (1982) Free radicals and tissue damage produced by exercise. Biochem Biophys Res Commun 107:1198–1205PubMedGoogle Scholar
  80. de Brito O, Scorrano L (2008) Mitofusin 2 tethers endoplasmic reticulum to mitochondria. Nature 456:605–610PubMedGoogle Scholar
  81. De Stefani D, Raffaello A, Teardo E, Szabo I, Rizzuto R (2011) A forty-kilodalton protein of the inner membrane is the mitochondrial calcium uniporter. Nature 476:336–340PubMedGoogle Scholar
  82. Delay M, Garcia D, Sanchez J (1990) The effects of lyotropic anion on charge movement, calcium currents and calcium signals in frog skeletal muscle fibres. J Physiol 425:449–469PubMedCentralPubMedGoogle Scholar
  83. Delbono O, Stefani E (1993) Calcium transients in single mammalian skeletal muscle fibres. J Physiol 463:689–707PubMedCentralPubMedGoogle Scholar
  84. DiFranco M, Neco P, Capote J, Meera P, Vergara J (2006) Quantitative evaluation of mammalian skeletal muscle as a heterologous protein expression system. Protein Expr Purif 47:281–288PubMedGoogle Scholar
  85. DiFranco M, Tran P, Quiñonez M, Vergara J (2011) Functional expression of transgenic 1sDHPR channels in adult mammalian skeletal muscle fibres. J Physiol 589:1421–1442Google Scholar
  86. Dirksen R (2009a) Checking your SOCCs and feet: the molecular mechanisms of Ca2+ entry in skeletal muscle. J Physiol 587:3139–3147PubMedCentralPubMedGoogle Scholar
  87. Dirksen R (2009b) Sarcoplasmic reticulum-mitochondrial through-space coupling in skeletal muscle. Appl Physiol Nutr Metab 34:389–395PubMedCentralPubMedGoogle Scholar
  88. Doyle D, Morais Cabral J, Pfuetzner R, Kuo A, Gulbis J, Cohen S et al (1998) The structure of potassium channel: molecular basis of K+ conduction and selectivity. Science 280:69–77PubMedGoogle Scholar
  89. Drago I, De Stefani D, Rizzuto R, Pozzan T (2012) Mitochondrial Ca2+ uptake contributes to buffering cytoplasmic Ca2+ peaks in cardiomyocytes. Proc Natl Acad Sci U S A 109:12986–12991PubMedCentralPubMedGoogle Scholar
  90. Dubowitz V, Pearse A (1960) A comparative histochemical study of oxidative enzyme and phophorylase activity in skeletal muscle. Histochemie 2:105–117PubMedGoogle Scholar
  91. Ducret T, Vandebrouck C, Cao M, Lebacq J, Gailly P (2006) Functional role of store-operated and stretch-activated channels in murine adult skeletal muscle fibres. J Physiol 575:913–924PubMedCentralPubMedGoogle Scholar
  92. Duke A, Steele D (2000) Characteristics of phosphate-induced Ca(2+) efflux from the SR in mechanically skinned rat skeletal muscle fibers. Am J Physiol Cell Physiol 278:C126–C135PubMedGoogle Scholar
  93. Dulhunty A, Banyard M, Medveczky C (1987) Distribution of calcium ATPase in the sarcoplasmic reticulum of fast- and slow-twitch muscles determined with monoclonal antibodies. J Membr Biol 99:79–92PubMedGoogle Scholar
  94. Dutka T, Cole L, Lamb G (2005) Calcium phosphate precipitation in the sarcoplasmic reticulum reduces action potential-mediated Ca2+ release in mammalian skeletal muscle. Am J Physiol 289:C1502–C1512Google Scholar
  95. Ebashi S (1974) Regulatory mechanism of muscle contraction with special reference to the Ca-troponin-tropomyosin system. Essays Biochem 10:1–36PubMedGoogle Scholar
  96. Ebashi S, Endo M, Ohtsuki I (1969) Control of muscle contraction. Q Rev Biophys 2:351–384PubMedGoogle Scholar
  97. Edman K (2005) Contratile properties of mouse single muscle fibers, a comparison with amphibian muscle fibers. J Exp Biol 208:1905–1913PubMedGoogle Scholar
  98. Edwards J, Murphy R, Cully T, von Wegner F, Friedrich O, Launikonis B (2010) Ultra-rapid activation and deactivation of store-operated Ca(2+) entry in skeletal muscle. Cell Calcium 47:458–467PubMedGoogle Scholar
  99. Edwards J, Cully T, Shannon T, Stephenson D, Launikonis B (2012) Longitudinal and transversal propagation of excitation along the tubular system of rat fast-twitch muscle fibres studied by high speed confocal microscopy. J Physiol 590:475–492PubMedCentralPubMedGoogle Scholar
  100. Eisenberg B (1983) Quantitative ultrastructure of mammalian skeletal muscle. In: Peachey LD (ed) Handbook of Physiology Skeletal Muscle. American Physiological Society, Bethesda, p 95Google Scholar
  101. Eisner V, Csordás G, Hajnóczky G (2013) Interactions between sarco-endoplasmic reticulum and mitochondria in cardiac and skeletal muscle - pivotal roles in Ca2+ and reactive oxygen species signaling. J Cell Sci 126:2965–2978PubMedGoogle Scholar
  102. el-Hayek R, Antoniu B, Wang J, Hamilton SL, Ikemoto N (1995) Identification of calcium release-triggering and blocking regions of the II-III loop of the skeletal muscle dihydropyridine receptor. J Biol Chem 270:22116–22118PubMedGoogle Scholar
  103. Endo M (1975) Mechanism of action of caffeine on the sarcoplasmic reticulum of skeletal muscle. Proc Jpn Acad 51:479–484Google Scholar
  104. Endo M (2009) Calcium-induced calcium release in skeletal muscle. Physiol Rev 89:1153–1176PubMedGoogle Scholar
  105. Endo M, Tanaka M, Ogawa Y (1970) Calcium induced release of calcium from the sarcoplasmic reticulum of skinned skeletal muscle fibres. Nature 228:34–36PubMedGoogle Scholar
  106. Escobar A, Monck J, Fernandez J, Vergara J (1994) Localization of the site of Ca2+ release at the level of a single sarcomere in skeletal muscle fibres. Nature 367:739–741PubMedGoogle Scholar
  107. Eusebi F, Miledi R, Takahashi T (1980) Calcium transients in mammalian muscles. Nature 284:560–561PubMedGoogle Scholar
  108. Fabiato A (1984) Dependence of the Ca2+-induced release from the sarcoplasmic reticulum of skinned skeletal muscle fibres from the frog semitendinosus on the rate of change of free Ca2+ concentration at the outer surface of the sarcoplasmic reticulum. J Physiol 353:56PGoogle Scholar
  109. Farkas D, Wei M, Febbroriello P, Carson J, Loew L (1989) Simultaneous imaging of cell and mitochondrial membrane potentials. Biophys J 56:1053–1069PubMedCentralPubMedGoogle Scholar
  110. Felder E, Franzini-Armstrong C (2002) Type 3 ryanodine receptors of skeletal muscle are segregated in a parajunctional position. Proc Natl Acad Sci U S A 99:1695–1700PubMedCentralPubMedGoogle Scholar
  111. Ferguson D, Franzini-Armstrong C (1988) The Ca2+ ATPase content of slow and fast twitch fibers of guinea pig. Muscle Nerve 11:561–570PubMedGoogle Scholar
  112. Feske S, Gwack Y, Prakriya M, Srikanth S, Puppel S, Tanasa B, Hogan P, Lewis R, Daly M, Rao A (2006) A mutation in Orai1 causes immune deficiency by abrogating CRAC channel function. Nature 441:179–185PubMedGoogle Scholar
  113. Fieni F, Lee SB, Jan YN, Kirichok Y (2012) Activity of the mitochondrial calcium uniporter varies greatly between tissues. Nat Commun 3:1317PubMedGoogle Scholar
  114. Figueroa L, Shkryl VM, Zhou J, Manno C, Momotake A, Brum G, Blatter LA, Ellis-Davies GC, Ríos E (2012) Synthetic localized calcium transients directly probe signalling mechanisms in skeletal muscle. J Physiol 590:1389–1411PubMedCentralPubMedGoogle Scholar
  115. Fill M, Copello J (2002) Ryanodine receptor calcium release channels. Physiol Rev 82:893–922PubMedGoogle Scholar
  116. Fitts R (1994) Cellular mechanisms of muscle fatigue. Physiol Rev 74:49–94PubMedGoogle Scholar
  117. Foulks J, Miller J, Perry F (1973) Repolarization-induced reactivation ofcontracture tension in frog skeletal muscle. Can J Physiol Pharmacol 51:324–334PubMedGoogle Scholar
  118. Fourest-Lieuvin A, Rendu J, Osseni A, Pernet-Gallay K, Rossi D, Oddoux S, Brocard J, Sorrentino V, Marty I, Fauré J (2012) Role of triadin in the organization of reticulum membrane at the muscle triad. J Cell Sci 125:3443–3453PubMedGoogle Scholar
  119. Franke W, Kartenbeck J (1971) Outer mitochondrial membrane continuous with endoplasmic reticulum. Protoplasma 73:35–41PubMedGoogle Scholar
  120. Franzini-Armstrong C (1999) The sarcoplasmic reticulum and the control of muscle contraction. FASEB J 13:S266–S270PubMedGoogle Scholar
  121. Franzini-Armstrong C (2007) ER-mitochondria communication. How privileged? Physiology (Bethesda) 22:261–268Google Scholar
  122. Franzini-Armstrong C, Boncompagni S (2011) The evolution of the mitochondria-to-calcium release units relationship in vertebrate skeletal muscles. J Biomed Biotechnol 2011:830573PubMedCentralPubMedGoogle Scholar
  123. Franzini-Armstrong C, Jorgensen A (1994) Structure and development of e-c coupling units in skeletal muscle. Annu Rev Physiol 56:509–534PubMedGoogle Scholar
  124. Franzini-Armstrong C, Porter K (1964) Sarcolemmal invaginations constituting the T system in fish muscle fibres. J Cell Biol 22:675–696PubMedCentralPubMedGoogle Scholar
  125. Franzini-Armstrong C, Ferguson D, Champ C (1988) Discrimination between fast- and slow-twitch fibres of guinea pig skeletal muscle using the relative surface density of junctional transverse tubule membrane. J Muscle Res Cell Motil 9:403–414PubMedGoogle Scholar
  126. Fraysse B, Rouaud T, Millour M, Fontaine-Pérus J, Gardahaut M, Levitsky D (2001) Expression of the Na+/Ca2+ exchanger in skeletal muscle. Am J Physiol 280:C146–C154Google Scholar
  127. Fryer M, Stephenson G (1996) Total and sarcoplasmic reticulum calcium contents of skinned fibres from rat skeletal muscle. J Physiol 493:357–370PubMedCentralPubMedGoogle Scholar
  128. Fryer M, Owen V, Lamb G, Stephenson G (1995) Effects of creatine phosphate and Pi on Ca movements and tension development in rat skinned skeletal muscle fibres. J Physiol 482:123–140PubMedCentralPubMedGoogle Scholar
  129. Füchtbauer E, Rowlerson A, Gotz K, Friedrich G, Mabuchi K, Gergely J, Jockusch H (1991) Direct correlation of parvalbumin levels with myosin isoforms and succinate dehydrogenase activity on frozen sections of rodent muscle. J Histochem Cytochem 39:355–361PubMedGoogle Scholar
  130. Gauthier G, Padykula H (1966) Cytological studies of fiber types in skeletal muscle. J Cell Biol 28:333–354Google Scholar
  131. Gillis J (1997) Inhibition of mitochondrial calcium uptake slows down relaxation in mitochondria-rich skeletal muscles. J Muscle Res Cell Motil 18:473–483PubMedGoogle Scholar
  132. Gillis J, Thomason D, Lefévre J, Kretsinger R (1982) Parvalbumins and muscle relaxation: a computer simulation study. J Muscle Res Cell Motil 3:377–398PubMedGoogle Scholar
  133. Giorgio V, von Stockum S, Antoniel M, Fabbro A, Fogolari F, Forte M, Glick G, Petronilli V, Zoratti M, Szabo I, Lippe G, Bernardi P (2013) Dimers of mitochondrial ATP synthase form the permeability transition pore. Proc Natl Acad Sci U S A 110:5887–5892PubMedCentralPubMedGoogle Scholar
  134. Glitsch M, Bakowski D, Parekh A (2002) Store-operated Ca2+ entry depends on mitochondrial Ca2+ uptake. EMBO J 21:6744–6754PubMedCentralPubMedGoogle Scholar
  135. Gollnick P, Korge P, Karpakka J, Saltin B (1991) Elongation of skeletal muscle relaxation during exercise is linked to reduced calcium uptake by the sarcoplasmic reticulum in man. Acta Physiol Scand 142:135–136PubMedGoogle Scholar
  136. Gomolla M, Gottschalk G, Lüttgau H (1983) Perchlorate-induced alterations in electrical and mechanical parameters of frog skeletal muscle fibres. J Physiol 343:197–214PubMedCentralPubMedGoogle Scholar
  137. Gonzalez Narvaez A, Castillo A (2007) Ca2+ store determines gating of store operated calcium entry in mammalian skeletal muscle. J Muscle Res Cell Motil 28:105–113PubMedGoogle Scholar
  138. González-Serratos H (1971) Inward spread of activation in vertebrate muscle fibres. J Physiol 212:777–799PubMedCentralPubMedGoogle Scholar
  139. Goonasekera S, Beard N, Groom L, Kimura T, Lyfenko A, Rosenfeld A, Marty I, Dulhunty A, Dirksen R (2007) Triadin binding to the C-terminal luminal loop of the ryanodine receptor is important for skeletal muscle excitation-contraction coupling. J Gen Physiol 130:365–378PubMedCentralPubMedGoogle Scholar
  140. Grabowski W, Lobsiger E, Luttgau H (1972) The effect of repetitive stimulation at low frequencies upon the electrical and mechanical activity of single muscle fibres. Pflugers Arch 334:222–239PubMedGoogle Scholar
  141. Green H (1998) Cation pumps in skeletal muscle: potential role in muscle fatigue. Acta Physiol Scand 162:201–213PubMedGoogle Scholar
  142. Grynkiewicz G, Poenie M, Tsien R (1985) A New Generation of Ca2+ Indicators with Greatly Improved Fluorescence Properties. J Biol Chem 260:3440–3450PubMedGoogle Scholar
  143. Gunter T, Pfeiffer D (1990) Mechanisms by which mitochondria transport calcium. Am J Physiol 258:C755–C786PubMedGoogle Scholar
  144. Gunter T, Gunter K, Sheu S, Gavin C (1994) Mitochondrial calcium transport: physiological and pathological relevance. Am J Physiol 267:C313–C339PubMedGoogle Scholar
  145. Gustafsson M (2000) Surpassing the lateral resolution limit by a factor of two using structured illumination microscopy. J Microsc 198:82–87PubMedGoogle Scholar
  146. Hasselbach W (1964) Relaxing factor and the relaxation of muscle. Prog Biophys Mol Biol 14:167–222Google Scholar
  147. Hasselbach W (1998) The Ca2+-ATPase of the sarcoplasmic reticulum in skeletal and cardiac muscle. Ann NY Acad Sci 853:1–8PubMedGoogle Scholar
  148. Hasselbach W, Makinose M (1961) The calcium pump of the “relaxing granules” of muscle and its dependence on ATP splitting. Biochem Z 333:518–528PubMedGoogle Scholar
  149. Hasselbach W, Suko J, Stromer M, The R (1975) Mechanism of calcium transport in sarcoplasmic reticulum. Ann NY Acad Sci 264:335–349PubMedGoogle Scholar
  150. He ZH, Bottinelli R, Pellegrino MA, Ferenczi MA, Reggiani C (2000) ATP consumption and efficiency of human single muscle fibers with different myosin isoform composition. Biophys J 79:945–961PubMedCentralPubMedGoogle Scholar
  151. Heilbrunn L, Wiercinsky F (1947) The action of various cations on muscle protoplasm. J Cell Comp Physiol 29:15–32Google Scholar
  152. Heizmann C, Berchtold M, Rowlerson A (1982) Correlation of parvalbumin concentration with relaxation speed in mammalian muscle. Proc Natl Acad Sci U S A 79:7243–7247PubMedCentralPubMedGoogle Scholar
  153. Hell SW, Wichmann J (1994) Breaking the diffraction resolution limit by stimulated emission: stimulated-emission-depletion fluorescence microscopy. Opt Lett 19:780–782PubMedGoogle Scholar
  154. Hernández-Ochoa E, Schneider M (2012) Voltage clamp methods for the study of membrane currents and SR Ca2+ release in adult skeletal muscle fibres. Prog Biophys Mol Biol 108:98–118PubMedCentralPubMedGoogle Scholar
  155. Hidalgo C (2005) Cross talk between Ca2+ and redox signaling cascades in muscle and neurons through the combined activation of ryanodine receptors/Ca2+ release channels. Phil Trans R Soc B 360:2237–2246PubMedCentralPubMedGoogle Scholar
  156. Hill A (1949) The abrupt transition from rest to activity in muscle. Proc R Soc B 136:399–420Google Scholar
  157. Hill A, Kupalov P (1929) Anaerobic and aerobic activity in isolated muscle. Proc R Soc London B 105:313–322Google Scholar
  158. Hille B, Campbell T (1976) An improved Vaseline gap voltage clamp for skeletal muscle fibers. J Gen Physiol 67:265–293PubMedGoogle Scholar
  159. Hodgkin A, Horowicz P (1959) The influence of potassium and chloride ions on the membrane potential of single muscle fibres. J Physiol 148:127–160PubMedCentralPubMedGoogle Scholar
  160. Hodgkin A, Horowicz P (1960) The effect of nitrate and other anions on the mechanical response of single muscle fibers. J Physiol 153:404–412PubMedCentralPubMedGoogle Scholar
  161. Hodgkin A, Huxley A (1952) A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol 117:500–544PubMedCentralPubMedGoogle Scholar
  162. Hollingworth S, Marshall M (1981) A comparative study of charge movement in rat and frog skeletal muscle fibres. J Physiol 321:583–602PubMedCentralPubMedGoogle Scholar
  163. Hollingworth S, Gee K, Baylor S (2009) Low-affinity Ca2+ indicators compared in measurements of skeletal muscle Ca2+ transients. Biophys J 97:1864–1872PubMedCentralPubMedGoogle Scholar
  164. Hollingworth S, Kim M, Baylor S (2012) Measurement and simulation of myoplasmic calcium transients in mouse slow-twitch muscle fibres. J Physiol 590:575–594PubMedCentralPubMedGoogle Scholar
  165. Horowicz P (1961) Influence of ions on the membrane potential of muscle fibres. In: Shanes A (ed) Biophysics of physiological and pharmacological actions. Washington, American Association for the Advancement of Science, pp 217–234Google Scholar
  166. Hoth M, Penner R (1992) Depletion of intracellular calcium stores activates a calcium current in mast cells. Nature 355:353–356PubMedGoogle Scholar
  167. Hoth M, Button D, Lewis R (2000) Mitochondrial control of calcium-channel gating: a mechanism for sustained signaling and transcriptional activation in T lymphocytes. Proc Natl Acad Sci U S A 97:10607–10612PubMedCentralPubMedGoogle Scholar
  168. Hudecova S, Vadaszova A, Soukup T, Krizanova O (2004) Effect of thyroid hormones on the gene expression of calcium transport systems in rat muscles. Life Sci 75:923–931PubMedGoogle Scholar
  169. Hunter D, Haworth R (1979) The Ca2+-induced membrane transition in mitochondria. III. Transitional Ca2+ release. Arch Biochem Biophys 195:468–477PubMedGoogle Scholar
  170. Huxley H (1964) Evidence for continuity between the central elements of the triads and extracellular space in frog sartorius muscle. Nature 202:1067PubMedGoogle Scholar
  171. Huxley H (1969) The mechanism of muscular contraction. Science 164:1356–1366PubMedGoogle Scholar
  172. Isaeva E, Shirokova N (2003) Metabolic regulation of Ca2+ release in permeabilized mammalian skeletal muscle fibres. J Physiol 547:453–462PubMedGoogle Scholar
  173. Isaeva E, Shkryl V, Shirokova N (2005) Mitochondrial redox state and Ca2+ sparks in permeabilized mammalian skeletal muscle. J Physiol 565:855–872PubMedCentralPubMedGoogle Scholar
  174. James P, Inui M, Tada M, Chiesi M, Carafoli E (1989) Nature and site of phospholamban regulation of the Ca2+ pump of sarcoplasmic reticulum. Nature 342:90–92PubMedGoogle Scholar
  175. Jayasinghe I, Baddeley D, Kong C, Wehrens X, Cannell M, Soeller C (2012) Nanoscale organization of junctophilin-2 and ryanodine receptors within peripheral couplings of rat ventricular cardiomyocytes. Biophys J 102(5):L19–L21PubMedCentralPubMedGoogle Scholar
  176. Jiang Y, Lee A, Chen J, Cadene M, Chalt B, MacKinnon R (2002) The open pore conformation of potassium channels. Nature 417:523–526PubMedGoogle Scholar
  177. Jiang D, Zhao L, Clapham D (2009) Genome-wide RNAi screen identifies Letm1 as a mitochondrial Ca2+/H+ antiporter. Science 326:144–147PubMedGoogle Scholar
  178. Jorgensen A, Jones L (1986) Localization of phospholamban in slow but not fast canine skeletal muscle fibers. J Biol Chem 261:3775–3781PubMedGoogle Scholar
  179. Jung D, Baysal K, Brierley G (1995) The sodium-calcium antiport of heart mitochondria is not electroneutral. J Biol Chem 270:672–678PubMedGoogle Scholar
  180. Jung D, Mo S, Kim D (2006) Calumenin, a multiple EF-hands Ca2+-binding protein, interacts with ryanodine receptor-1 in rabbit skeletal sarcoplasmic reticulum. Biochem Biophys Res Commun 34:34–42Google Scholar
  181. Kahn A, Sandow A (1950) The potentiation of muscular contraction by the nitrate-ion. Science 112:647–649PubMedGoogle Scholar
  182. Kanter M, Nolte L, Holloszy J (1993) Effects of an antioxidant vitamin mixture on lipid peroxidation at rest and postexercise. J Appl Physiol 74:965–969PubMedGoogle Scholar
  183. Kao C, Stanfield P (1968) Action of some ions on the electrical properties and mechanical threshold of frog twitch muscle. J Physiol 198:291–309PubMedCentralPubMedGoogle Scholar
  184. Kao J, Li G, Auston D (2010) Practical aspects of measuring intracellular calcium signals with fluorescent indicators. Methods Cell Biol 99:113–152PubMedGoogle Scholar
  185. Katerinopoulos H, Foukaraki E (2002) Polycarboxylate fluorescent indicators as ion concentration probes in biological systems. Curr Med Chem 9:275–306PubMedGoogle Scholar
  186. Kent-Braun J (1999) Central and peripheral contributions to muscle fatigue in humans during sustained maximal effort. Eur J Appl Physiol 80:57–63Google Scholar
  187. Kent-Braun J, Miller R, Weiner M (1993) Phases of metabolism during progressive exercise to fatigue in human skeletal muscle. J Appl Physiol 75:573–580PubMedGoogle Scholar
  188. Kinnally K, Campo M, Tedeschi H (1989) Mitochondrial channel activity studied by patch-clamping mitoplasts. J Bioenerg Biomembr 21:497–506PubMedGoogle Scholar
  189. Kirichok Y, Krapivinsky G, Clapham D (2004) The mitochondrial calcium uniporter is a highly selective ion channel. Nature 427:360–364PubMedGoogle Scholar
  190. Klar T, Jakobs S, Dyba M, Egner A, Hell S (2000) Fluorescence microscopy with diffraction resolution barrier broken by stimulated emission. Proc Natl Acad Sci U S A 97:8206–8210PubMedCentralPubMedGoogle Scholar
  191. Klein M, Simon B, Szucs G, Schneider M (1988) Simultaneous recording of calcium transients in skeletal muscle using high and low-affinity calcium indicators. Biophys J 53:971–988PubMedCentralPubMedGoogle Scholar
  192. Knuth S, Dave H, Peters J, Fitts R (2006) Low cell pH depresses peak power in rat skeletal muscle fibres at both 30 °C and 15 °C: implications for muscle fatigue. J Physiol 575:887–899PubMedCentralPubMedGoogle Scholar
  193. Konishi M, Hollingworth S, Harkins A, Baylor S (1991) Myoplasmic calcium transients in intact frog skeletal muscle fibers monitored with the fluorescent indicator furaptra. J Gen Physiol 97:271–301PubMedGoogle Scholar
  194. Kornmann B, Currie E, Collins SR, Schuldiner M, Nunnari J, Weissman J, Walter P (2009) An ER-mitochondria tethering complex revealed by a synthetic biology screen. Science 325:477–481PubMedCentralPubMedGoogle Scholar
  195. Kovács L, Schneider M (1978) Contractile activation by voltage clamp depolarization of cut skeletal muscle fibres. J Physiol 277:483–506PubMedCentralPubMedGoogle Scholar
  196. Kovács L, Ríos E, Schneider M (1983) Measurement and modification of free calcium transients in frog skeletal muscle fibres by a metallochromic indicator dye. J Physiol 343:161–196PubMedCentralPubMedGoogle Scholar
  197. Kurebayashi N, Ogawa Y (2001) Depletion of Ca2+ in the sarcoplasmic reticulum stimulates Ca2+ entry into mouse skeletal muscle fibres. J Physiol 533:185–199PubMedCentralPubMedGoogle Scholar
  198. Kuznetsov A, Troppmair J, Sucher R, Hermann M, Saks V, Margreiter R (2006) Mitochondrial subpopulations and heterogeneity revealed by confocal imaging: possible physiological role? Biochim Biophys Acta 1757:686–691PubMedGoogle Scholar
  199. Lacampagne A, Lederer W, Schneider M, Klein M (1996) Repriming and activation alter the frequency of stereotyped discrete Ca2+ release events in frog skeletal muscle. J Physiol 497:581–588Google Scholar
  200. Lai F, Erickson H, Rousseau E, Liu Q, Meissner G (1988) Purification and reconstitution of the calcium release channel from skeletal muscle. Nature 331:315–319PubMedGoogle Scholar
  201. Lamb G (2002) Excitation-contraction coupling and fatigue mechanisms in skeletal muscle: studies with mecanically skinned fibres. J Muscle Res Cell Motil 23:81–91PubMedGoogle Scholar
  202. Lamb G, Stephenson D (1994) Effects of intracellular pH and [Mg2+] on excitation-contraction coupling in skeletal muscle fibres of the rat. J Physiol 478:331–339PubMedCentralPubMedGoogle Scholar
  203. Lamb G, Walsh T (1987) Calcium currents, charge movement and dihydropyridine binding in fast- and slow-twitch muscles of rat and rabbit. J Physiol 393:595–617PubMedCentralPubMedGoogle Scholar
  204. Lamb G, Junankar P, Stephenson D (1995) Raised intracellular Ca2+ abolishes excitation-contraction coupling in skeletal muscle fibres of rat and toad. J Physiol 489:349–362PubMedCentralPubMedGoogle Scholar
  205. Lännergren J, Westerblad H (1987) The temperature dependence of isometric contractions of single, intact fibres dissected from a mouse foot muscle. J Physiol 390:285–293PubMedCentralPubMedGoogle Scholar
  206. Lännergren J, Westerblad H, Bruton J (2001) Changes in mitochondrial Ca2+ detected with Rhod-2 in single frog and mouse skeletal muscle fibres during and after repeated tetanic contractions. J Muscle Res Cell Motil 22:265–275PubMedGoogle Scholar
  207. Launikonis B, Ríos E (2007) Store-operated Ca2+ entry during intracellular Ca2+ release in mammalian skeletal muscle. J Physiol 583:81–97PubMedCentralPubMedGoogle Scholar
  208. Launikonis BS, Zhou J, Royer L, Shannon T, Brum G, Ríos E (2005) Confocal imaging of [Ca2+] in cellular organelles by SEER, shifted excitation and emission ratioing of fluorescence. J Physiol 567:523–543PubMedCentralPubMedGoogle Scholar
  209. Leberer E, Pette D (1986) Immunochemical quantification of sarcoplasmic reticulum Ca-ATPase, of calsequestrin and of parvalbumin in rabbit skeletal muscles. Eur J Biochem 156:489–496PubMedGoogle Scholar
  210. Leong P, MacLennan D (1998) A 37-amino acid sequence in the skeletal muscle ryanodine receptor interacts with the cytoplasmic loop between domains II and III in the skeletal muscle dihydropyridine receptor. J Biol Chem 273:7791–7794PubMedGoogle Scholar
  211. Leppik J, Aughey R, Medved I, Fairweather I, Carey M, McKenna M (2004) Prolongued exercise to fatigue in humans impairs skeletal muscle Na-K ATPase activity, sarcoplasmic reticulum Ca release and Ca uptake. J Appl Physiol 97:1414–1423PubMedGoogle Scholar
  212. Lewis J, Tata J (1973) A rapidly sedimenting fraction of rat liver endoplasmic reticulum. J Cell Sci 13:447–459PubMedGoogle Scholar
  213. Lindinger M, Heigenhauser G (1991) The roles of ion fluxes in skeletal muscle fatigue. Can J Physiol Pharmacol 69:246–253PubMedGoogle Scholar
  214. Liou J, Kim M, Heo W, Jones J, Myers J, Ferrell J Jr, Meyer T (2005) STIM is a Ca2+ sensor essential for Ca2+-store-depletion-triggered Ca2+ influx. Curr Biol 15:1235–1241PubMedCentralPubMedGoogle Scholar
  215. Lipp P, Niggli E (1996) Submicroscopic calcium signals as fundamental events of excitation--contraction coupling in guinea-pig cardiac myocytes. J Physiol 492:31–38Google Scholar
  216. Ludtke S, Serysheva I, Hamilton S, Chiu W (2005) The pore structure of the closed RyR1 channel. Structure 13:1203–1211PubMedCentralPubMedGoogle Scholar
  217. Luff A, Atwood H (1972) Membrane properties and contraction of single muscle fibers in the mouse. Am J Physiol 222:1435–1440PubMedGoogle Scholar
  218. Luik R, Wu M, Buchanan J, Lewis R (2006) The elementary unit of store-operated Ca2+ entry: local activation of CRAC channels by STIM1 at ER-plasma membrane junctions. J Cell Biol 174:815–825PubMedCentralPubMedGoogle Scholar
  219. Luttgau H (1965) The effect of metabolic inhibitors on the fatigue of the action potential in single muscle fibres. J Physiol 178:45–67PubMedCentralGoogle Scholar
  220. Lüttgau H, Oetliker H (1968) The action of caffeine on the activation of the contractile mechanism in striated muscle fibres. J Physiol 194:51–74PubMedCentralPubMedGoogle Scholar
  221. Ma J, Pan Z (2003) Junctional membrane structure and store operated calcium entry in muscle cells. Front Biosci 8:d242–d255PubMedGoogle Scholar
  222. MacLennan D, Brandl C, Korczak B, Green N (1985) Amino-acid sequence of a Ca2++Mg2+-dependent ATPase from rabbit muscle sarcoplasmic reticulum, deduced from its complementary DNA sequence. Nature 316:696–700PubMedGoogle Scholar
  223. Mannella C, Colombini M, Frank J (1983) Structural and functional evidence for multiple channel complexes in the outer membrane of Neurospora crassa mitochondria. Proc Natl Acad Sci U S A 80:2243–2247PubMedCentralPubMedGoogle Scholar
  224. Mannella C, Buttle K, Rath B, Marko M (1998) Electron microscopic tomography of rat-liver mitochondria and their interaction with the endoplasmic reticulum. Biofactors 8:225–228PubMedGoogle Scholar
  225. Manno C, Figueroa L, Fitts R, Ríos E (2013) Confocal imaging of transmembrane voltage by SEER of di-8-ANEPPS. J Gen Physiol 141(3):371–387PubMedCentralPubMedGoogle Scholar
  226. Martonosi A, Pikula S (2003) The structure of the Ca2+-ATPase of sarcoplasmic reticulum. Acta Biochim Pol 50:337–365PubMedGoogle Scholar
  227. McCully K, Clark B, Kent J, Wilson J, Chance B (1991) Biochemical adaptations to training: implications for resisting muscle fatigue. Can J Physiol Pharmacol 69:274–278PubMedGoogle Scholar
  228. McLaughlin S, Bruder A, Chen S, Moser C (1975) Chaotropic anions and the surface potential of bilayer membranes. Biochim Biophys Acta 394:304–313PubMedGoogle Scholar
  229. Meier P, Spycher M, Meyer U (1981) Isolation and characterization of rough endoplasmic reticulum associated with mitochondria from normal rat liver. Biochim Biophys Acta 646:283–297PubMedGoogle Scholar
  230. Meissner G (1984) Adenine nucleotide stimulation of Ca2+-induced Ca2+ release in sarcoplasmic reticulum. J Biol Chem 259:2365–2374PubMedGoogle Scholar
  231. Michaelson L, Shi G, Ward C, Rodney G (2010) Mitochondrial redox potential during contraction in single intact muscle fibers. Muscle Nerve 42:522–529PubMedCentralPubMedGoogle Scholar
  232. Miledi R, Parker I, Schalow G (1977) Calcium transients in frog slow muscle fibres. Nature 268:750–752PubMedGoogle Scholar
  233. Minta A, Kao J, Tsien R (1989) Fluorescent indicators for cytosolic calcium based on rhodamine and fluorescein chromophores. J Biol Chem 264:8171–8178PubMedGoogle Scholar
  234. Mitchell P, Moyle J (1967) Chemiosmotic hypothesis of oxidative phosphorylation. Nature 213:137–139PubMedGoogle Scholar
  235. Moopanar T, Allen D (2005) Reactive oxygen species reduce myofibrillar Ca2+ sensitivity in fatiguing mouse skeletal muscle at 37 °C. J Physiol 564:189–199PubMedCentralPubMedGoogle Scholar
  236. Moopanar T, Allen D (2006) The activity-induced reduction of myofibrillar Ca2+ sensitivity in mouse skeletal muscle is reversed by dithiothreitol. J Physiol 571:191–200PubMedCentralPubMedGoogle Scholar
  237. Moore R, Nguyen H, Galceran J, Pessah I, Allen P (1998) A transgenic myogenic cell line lacking ryanodine receptor protein for homologous expression studies: reconstitution of Ry1R protein and function. J Cell Biol 140:843–851PubMedCentralPubMedGoogle Scholar
  238. Morre D, Merritt W, Lembi C (1971) Connections between mitochondria and endoplasmic reticulum in rat liver and onion stem. Protoplasma 73:43–49PubMedGoogle Scholar
  239. Mosca B, Delbono O, Messi M, Bergamelli L, Wang Z, Vukcevic M, Lopez R, Treves S, Nishi M, Takeshima H, Paolini C, Martini M, Rispoli G, Protasi F, Zorzato F (2013) Enhanced dihydropyridine receptor calcium channel activity restores muscle strength in JP45/CASQ1 double knockout mice. Nat Commun 4:1541PubMedGoogle Scholar
  240. Moussavi R, Carson P, Boska M, Weiner M, Miller R (1989) Nonmetabolic fatigue in exercising human muscle. Neurology 39:1222–1226PubMedGoogle Scholar
  241. Muik M, Fahrner M, Derler I, Schindl R, Bergsmann J, Frischauf I, Groschner K, Romanin C (2009) A Cytosolic Homomerization and a Modulatory Domain within STIM1 C Terminus Determine Coupling to ORAI1 Channels. J Biol Chem 284:8421–8426PubMedCentralPubMedGoogle Scholar
  242. Naghdi S, Waldeck-Weiermair M, Fertschai I, Poteser M, Graier W, Malli R (2010) Mitochondrial Ca2+ uptake and not mitochondrial motility is required for STIM1-Orai1-dependent store-operated Ca2+ entry. J Cell Sci 123:2553–2564PubMedGoogle Scholar
  243. Nakai J, Dirksen R, Nguyen H, Pessah I, Beam K, Allen P (1996) Enhanced dihydropyridine receptor channel activity in the presence of ryanodine receptor. Nature 380:72–75PubMedGoogle Scholar
  244. Nassar-Gentina V, Passonneau J, Vergara J, Rapoport S (1978) Metabolic correlates of fatigue and recovery from fatigue in single frog muscle fibers. J Gen Physiol 72:593–606PubMedGoogle Scholar
  245. Natori R (1954) The property and contraction process of isolated myofibrils. Jikeikai Med J 1:119–126Google Scholar
  246. Niedergerke R (1955) Local muscular shortening by intracellularly applied calcium. J Physiol 128:12P–13PGoogle Scholar
  247. Oba T, Kurono C, Nakajima R, Takaishi T, Ishida K, Fuller G, Klomkleaw W, Yamaguchi M (2002) H2O2 activates ryanodine receptor but has little effect on recovery of release Ca2+ content after fatigue. J Appl Physiol 93:1999–2008PubMedGoogle Scholar
  248. O'Brien J, Valdivia H, Block B (1995) Physiological differences between the alpha and beta ryanodine receptors of fish skeletal muscle. Biophys J 68:471–482PubMedCentralPubMedGoogle Scholar
  249. Odermatt A, Becker S, Khanna V, Kurzydlowski K, Leisner E, Pette D, MacLennan D (1998) Sarcolipin regulates the activity of SERCA1, the fast-twitch skeletal muscle sarcoplasmic reticulum Ca2+-ATPase. J Biol Chem 273:12360–12369PubMedGoogle Scholar
  250. Ogata T, Yamasaki Y (1985) Scanning electron-microscopic studies on the three-dimensional structure of sarcoplasmic reticulum in the mammalian red, white and intermediate muscle fibers. Cell Tissue Res 242:461–467PubMedGoogle Scholar
  251. Pacher P, Thomas A, Hajnoczky G (2002) Ca2+ marks: miniature calcium signals in single mitochondria driven by ryanodine receptors. Proc Natl Acad Sci U S A 99:2380–2385PubMedCentralPubMedGoogle Scholar
  252. Pal R, Li S, Thakur P, Rodney G (2013) Real-time imaging of NADPH oxidase activity in living cell by using novel bio-sensor. Biophys J 104(2–S1):530a. abstract,2722-PosGoogle Scholar
  253. Palmer A, Tsien R (2006) Measuring calcium signaling using genetically targetable fluorescent indicators. Nat Protoc 1:1057–1065PubMedGoogle Scholar
  254. Pan Z, Yang D, Nagaraj RY, Nosek TA, Nishi M, Takeshima H, Cheng H, Ma J (2002) Dysfunction of store-operated calcium channel in muscle cells lacking mg29. Nat Cell Biol 4:379–383PubMedGoogle Scholar
  255. Paolini C, Fessenden J, Pessah I, Franzini-Armstrong C (2004) Evidence for conformational coupling between two calcium channels. Proc Natl Acad Sci U S A 101:12748–12752PubMedCentralPubMedGoogle Scholar
  256. Paolini C, Quarta M, Nori A, Boncompagni S, Canato M, Volpe P, Allen PD, Reggiani C, Protasi F (2007) Reorganized stores and impaired calcium handling in skeletal muscle of mice lacking calsequestrin-1. J Physiol 583:767–784PubMedCentralPubMedGoogle Scholar
  257. Papadopoulus S, Leuranguer V, Bannister R, Beam K (2004) Mapping sites of potential proximity between the DHPR and RyR1 in muscle using a cyan fluorescent protein-yellow fluorescent protein tandem as a fluorescent resonance energy transfer probe. J Biol Chem 279:44046–44056Google Scholar
  258. Parekh A (2003) Store-operated Ca2+ entry: dynamic interplay between endoplasmic reticulum, mitochondria and plasma membrane. J Physiol 547:333–348PubMedCentralPubMedGoogle Scholar
  259. Parekh A, Penner R (1997) Store depletion and calcium influx. Physiol Rev 77:901–930PubMedGoogle Scholar
  260. Parekh A, Putney J Jr (2005) Store-operated calcium channels. Physiol Rev 85:757–810PubMedGoogle Scholar
  261. Peachey L (1965) The sarcoplasmic reticulum and transverse tubules of the frog’s Sartorius. J Cell Biol 25:209–231PubMedCentralPubMedGoogle Scholar
  262. Pedersen T, Nielsen O, Lamb G, Stephenson D (2004) Intracellular acidosis enhances the excitability of working muscle. Science 305:1144–1147PubMedGoogle Scholar
  263. Perez C, Thomas M, Franzini-Armstrong C (2013) Carboxyl-terminal domain of DHPR β1A is essential for DHPR tetrad formation. Biophys J 104(2–S1):104a. abstract,542-PosGoogle Scholar
  264. Periasamy M, Kalyanasundaram A (2007) Serca pump isoforms: their role in calcium transport and disease. Muscle Nerve 35:430–442PubMedGoogle Scholar
  265. Petrofsky J, Lind A (1979) Isometric endurance in fast and slow muscles in the cat. Am J Physiol 236:C185–C191PubMedGoogle Scholar
  266. Petronilli V, Szabo I, Zoratti M (1989) The inner mitochondrial membrane contains ion-conducting channels similar to those found in bacteria. FEBS Lett 259:137–143PubMedGoogle Scholar
  267. Picard M, Hepple R, Burelle Y (2012) Mitochondrial functional specialization in glycolytic and oxidative muscle fibers: tailoring the organelle for optimal function. Am J Physiol Cell Physiol 302:C629–C641PubMedGoogle Scholar
  268. Place N, Yamada T, Bruton JD, Westerblad H (2008) Interpolated twitches in fatiguing single mouse muscle fibres: implications for the assessment of central fatigue. J Physiol 586:2799–2805PubMedCentralPubMedGoogle Scholar
  269. Place N, Yamada T, Zhang S, Westerblad H, Bruton J (2009) High temperature does not alter fatigability in intact mouse skeletal muscle fibres. J Physiol 587:4717–4724PubMedCentralPubMedGoogle Scholar
  270. Place N, Yamada T, Bruton J, Westerblad H (2010) Muscle fatigue: from observations in humans to underlying mechanisms studied in intact single muscle fibres. Eur J Appl Physiol 110:1–15PubMedGoogle Scholar
  271. Porter K, Palade G (1957) Studies on the endoplasmic reticulum. III. Its form and distribution in striated muscle cells. J Biophys Biochem Cytol 3(2):269–300PubMedCentralPubMedGoogle Scholar
  272. Posterino G, Lamb G (2003) Effect of sarcoplasmic reticulum Ca2+ content on action-potential induced Ca2+ release in rat skeletal muscle fibres. J Physiol 551:219–237PubMedCentralPubMedGoogle Scholar
  273. Pouvreau S, Collet C, Allard B, Jacquemond V (2007a) Whole-cell voltage clamp on skeletal muscle fibers with silicone-clamp technique. Methods Mol Biol 403:185–194PubMedGoogle Scholar
  274. Pouvreau S, Royer L, Yi J, Brum G, Meissner G, Ríos E, Zhou J (2007b) Ca(2+) sparks operated by membrane depolarization require isoform 3 ryanodine receptor channels in skeletal muscle. Proc Natl Acad Sci U S A 104:5235–5240PubMedCentralPubMedGoogle Scholar
  275. Prakriya M, Feske S, Gwack Y, Srikanth S, Rao A, Hogan P (2006) Orai1 is an essential pore subunit of the CRAC channel. Nature 443:230–233PubMedGoogle Scholar
  276. Prosser B, Wright N, Hernandez-Ochoa E, Varney K, Liu Y, Olojo R, Zimmer D, Weber D, Schneider M (2008) S100A1 binds to the calmodulin binding site of ryanodine receptor and modulates skeletal muscle coupling. J Biol Chem 283:5046–5057PubMedGoogle Scholar
  277. Prosser B, Hernández-Ochoa E, Lovering R, Andronache Z, Zimmer D, Melzer W, Schneider M (2010) S100A1 promotes action potential-initiated calcium release flux and force production in skeletal muscle. Am J Physiol Cell Physiol 299:C891–C902PubMedCentralPubMedGoogle Scholar
  278. Protasi F, Paolini C, Nakai J, Beam K, Franzini-Armstrong C, Allen P (2002) Multiple regions of RyR1 mediate functional and structural interactions with α1s-dihidropyridine receptors in skeletal muscle. Biophys J 83:3220–3244Google Scholar
  279. Putney J Jr (1986) A model for receptor-regulated calcium entry. Cell Calcium 7:1–12PubMedGoogle Scholar
  280. Racay P, Gregory P, Schwaller B (2006) Parvalbumin deficiency in fast-twitch muscles leads to increased 'slow-twitch type' mitochondria, but does not affect the expression of fiber specific proteins. FEBS J 273:96–108PubMedGoogle Scholar
  281. Raju B, Murphy E, Levy L, Hall R, London R (1989) A fluorescent indicator for measuring cytosolic free magnesium. Am J Physiol 256:C540–C548PubMedGoogle Scholar
  282. Ramesh V, Sharma V, Sheu S, Franzini-Armstrong C (1998) Structural proximity of mitochondria to calcium release units in rat ventricular myocardium may suggest a role in Ca2+ sequestration. Ann N Y Acad Sci 853:341–344PubMedGoogle Scholar
  283. Rando T, Blau H (1994) Primary mouse myoblast purification, characterization and transplantation for cell-mediated gene therapy. J Cell Biol 125:1275–1287PubMedGoogle Scholar
  284. Ranvier L (1873) Propriétés et structures différentes des muscles rouges et des muscles blancs, chez les Lapins et chez les Raies. Compt Rendus 77:1030–1034Google Scholar
  285. Rapizzi E, Pinton P, Szabadkai G, Wieckowski M, Vandecasteele G, Baird G, Tuft R, Fogarty K, Rizzuto R (2002) Recombinant expression of the voltage-dependent anion channel enhances the transfer of Ca2+ microdomains to mitochondria. J Cell Biol 159:613–624PubMedCentralPubMedGoogle Scholar
  286. Rausch M, Treves S, Zorzato F (2013) 3D Structural illumination microscopy of the skeletal muscle excitation-contraction coupling macromolecular complex. Biophys J 104(2–S1):105a. abstract,544-PosGoogle Scholar
  287. Reardon T, Allen D (2009) Time to fatigue is increased in mouse muscle at 37 °C; the role of iron and reactive oxygen species. J Physiol 587:4705–4716PubMedCentralPubMedGoogle Scholar
  288. Rebbeck R, Willemse H, Groom L, Dirksen R, Dulhunty A (2013) Interactions between dihydropyridine β1A subunit and ryanodine receptor isoforms. Biophys J 104(2–S1):105a. abstract,543-PosGoogle Scholar
  289. Reggiani C, te Kronnie T (2006) RyR isoforms and fibre-type specific expression of proteins controlling intracellular calcium concentration in skeletal muscles. J Muscle Res Cell Motil 27:327–335PubMedGoogle Scholar
  290. Reid M (2001) Plasticity in Skeletal, Cardiac, and Smooth Muscle. Invited Review: Redox modulation of skeletal muscle contraction: what we know and what we don’t. J Appl Physiol 90:724–731PubMedGoogle Scholar
  291. Reid M, Haack K, Kathleen F, Valberg P, Kobzik L, West S (1992) Reactive oxygen in skeletal muscle. I. Intracellular oxidant kinetics and fatigue in vitro. J Appl Physiol 73:1797–1804PubMedGoogle Scholar
  292. Ridgway E, Ashley C (1967) Calcium transients in single muscle fibres. Biochem Biophys Res Commun 29:229–234PubMedGoogle Scholar
  293. Ríos E, Brum G (1987) Involvement of dihydropyridine receptors in excitation-contraction coupling in skeletal muscle. Nature 325:717–720Google Scholar
  294. Ríos E, Pizarro G (1988) Voltage sensors and calcium channels of excitation-contraction coupling. News Physiol Sci 3:223–227Google Scholar
  295. Ríos E, Pizarro G (1991) Voltage sensor of excitation-contraction coupling in skeletal muscle. Physiol Rev 71:849–908PubMedGoogle Scholar
  296. Ríos E, Karhanek M, Ma J, González A (1993) An Allosteric model of the molecular interactions of excitation-contraction coupling in skeletal muscle. J Gen Physiol 102:449–481PubMedGoogle Scholar
  297. Rizzuto R, Pozzan T (2006) Microdomains of intracellular Ca2+: molecular determinants and functional consequences. Physiol Rev 86:369–408PubMedGoogle Scholar
  298. Rizzuto R, Simpson AW, Brini M, Pozzan T (1992) Rapid changes of mitochondrial Ca2+ revealed by specifically targeted recombinant aequorin. Nature 358:325–327PubMedGoogle Scholar
  299. Rizzuto R, Brini M, Murgia M, Pozzan T (1993) Microdomains with high Ca2+ close to IP3-sensitive channels that are sensed by neighboring mitochondria. Science 262:744–747PubMedGoogle Scholar
  300. Rizzuto R, Pinton P, Carrington W, Fay FS, Fogarty KE, Lifshitz LM, Tuft R, Pozzan T (1998) Close contacts with the endoplasmic reticulum as determinants of mitochondrial Ca2+ responses. Science 280:1763–1766PubMedGoogle Scholar
  301. Rizzuto R, Bernardi P, Pozzan T (2000) Mitochondria as all-round players of the calcium game. J Physiol 529:37–47PubMedCentralPubMedGoogle Scholar
  302. Rizzuto R, Marchi S, Bonora M, Aguiari P, Bononi A, De Stefani D, Giorgi C, Leo S, Rimessi A, Siviero R, Zecchini E, Pinton P (2009) Ca(2+) transfer from the ER to mitochondria: when, how and why. Biochim Biophys Acta 1787:1342–1351PubMedCentralPubMedGoogle Scholar
  303. Rogers K, Picaud S, Roncali E, Boisgard R, Colasante C, Stinnakre J, Tavitian B, Brulet P (2007) Non-invasive in vivo imaging of calcium signaling in mice. PLoS One 2:e974PubMedCentralPubMedGoogle Scholar
  304. Roos J, DiGregorio PJ, Yeromin AV, Ohlsen K, Lioudyno M, Zhang S, Safrina O, Kozak JA, Wagner SL, Cahalan MD, Velicelebi G, Stauderman K (2005) STIM1, an essential and conserved component of store-operated Ca2+ channel function. J Cell Biol 169:435–445PubMedCentralPubMedGoogle Scholar
  305. Rossi R, Bottinelli R, Sorrentino V, Reggiani C (2001) Response to caffeine and ryanodine receptor isoforms in mouse skeletal muscle. Am J Physiol Cell Physiol 281:C585–C594PubMedGoogle Scholar
  306. Rossi A, Boncompagni S, Wei L, Protasi F, Dirksen R (2011) Differential impact of mitochondrial positioning on mitochondrial Ca(2+) uptake and Ca(2+) spark suppression in skeletal muscle. Am J Physiol Cell Physiol 301:C1128–C1139PubMedCentralPubMedGoogle Scholar
  307. Rousseau E, Pinkos J (1990) pH modulates conducting and gating behaviour of single calcium release channels. Pflugers Arch 415:645–657PubMedGoogle Scholar
  308. Royer L, Sztretye M, Manno C, Pouvreau S, Zhou J, Knollmann B, Protasi F, Allen P, Rios E (2010) Paradoxical buffering of calcium by calsequestrin demonstrated for the calcium store of skeletal muscle. J Gen Physiol 136:325–338PubMedCentralPubMedGoogle Scholar
  309. Rudolf R, Mongillo M, Magalhaes P, Pozzan T (2004) In vivo monitoring of Ca2+ uptake into mitochondria of mouse skeletal muscle during contraction. J Cell Biol 166:527–536PubMedCentralPubMedGoogle Scholar
  310. Ryu S, Beutner G, Dirksen R, Kinnally K, Sheu S (2010) Mitochondrial ryanodine receptors and other mitochondrial Ca2+ permeable channels. FEBS Lett 584:1948–1955PubMedCentralPubMedGoogle Scholar
  311. Ryu S, Beutner G, Kinnally K, Dirksen R, Sheu S (2011) Single channel characterization of the mitochondrial ryanodine receptor in heart mitoplasts. J Biol Chem 286:21324–21329PubMedCentralPubMedGoogle Scholar
  312. Samsó M, Wagenknecht T, Allen D (2005) Internal structure and visualization of transmembrane domains of the RyR1 calcium release channel by cryo-EM. Nat Struct Mol Biol 12:539–544PubMedCentralPubMedGoogle Scholar
  313. Samsó M, Feng W, Pessah I, Allen P (2009) Coordinated movement of cytoplasmic and transmembrane domains of RyR1 upon gating. PLoS Biol 7:e85Google Scholar
  314. Sandow A (1952) Excitation-contraction coupling in muscular response. Yale J Biol Med XXV:176–201. In his classical review article Professor Sandow coined the term “Excitation–Contraction Coupling” to define the chain of events that starting with the action potential, ended with force development, at a time when the nature of all the intermediate events was unknown, indicating the way for future research. The term has become so popular that it is used even in the absence of excitation as when caffeine is used to induce contraction, or to describe another phenomenon, as when the term “Excitation–Secretion Coupling”is usedGoogle Scholar
  315. Sandow A (1964) Potentiation of muscular contraction. Arch Phys Med Rehabil 45:62–81PubMedGoogle Scholar
  316. Sandow A (1965) Excitation-Contraction Coupling in skeletal muscle. Pharmacol Rev 17:265–320PubMedGoogle Scholar
  317. Sandow A, Isaacson A (1966) Topochemical factors in potentiation of contraction by heavy metal cations. J Gen Physiol 49:937–961PubMedCentralPubMedGoogle Scholar
  318. Sandow A, Taylor S, Preiser H (1965) Role of the action potential in excitation-contraction coupling. Fed Proc 24:1116–1123PubMedGoogle Scholar
  319. Santo-Domingo J, Demaurex N (2010) Calcium uptake mechanisms of mitochondria. Biochim Biophys Acta 1797:907–912PubMedGoogle Scholar
  320. Saris N, Carafoli E (2005) A historical review of cellular calcium handling, with emphasis on mitochondria. Biochemistry (Mosc) 70:187–194Google Scholar
  321. Schein S, Colombini M, Finkelstein A (1976) Reconstitution in planar lipid bilayers of a voltage-dependent anion-selective channel obtained from paramecium mitochondria. J Membr Biol 30:99–120PubMedGoogle Scholar
  322. Schermelleh L, Heintzmann R, Leonhardt H (2010) A guide to super-resolution fluorescence microscopy. J Cell Biol 190:165–175PubMedCentralPubMedGoogle Scholar
  323. Schiaffino S, Gorza L, Sartore S, Saggin L, Ausoni S, Vianello M, Gundersen K, Lømo T (1989) Three myosin heavy chain isoforms in type 2 skeletal muscle fibres. J Muscle Res Cell Motil 10:197–205PubMedGoogle Scholar
  324. Schmitt T, Pette D (1991) Fiber type-specific distribution of parvalbumin in rabbit skeletal muscle. Histochemistry 96:459–465PubMedGoogle Scholar
  325. Schneider M, Chandler W (1973) Voltage dependent charge movement in skeletal muscle: a possible step in excitation-contraction coupling. Nature 242:244–246PubMedGoogle Scholar
  326. Scriven D, Tafteh R, Chou K, Moore E (2013) Super-resolution localization and distribution of proteins within the mammalian couplon. Biophys J 104(2–S1):105a. abstract,545-PosGoogle Scholar
  327. Sembrowich W, Quintinskie J, Li G (1985) Calcium uptake in mitochondria from different skeletal muscle types. J Appl Physiol 59:137–141PubMedGoogle Scholar
  328. Sen C (1995) Oxidants and antioxidants in exercise. J Appl Physiol 79:675–686PubMedGoogle Scholar
  329. Serysheva I, Chiu W, Ludtke S (2007) Single-particle electron cryomicroscopy of the ion channels in the excitation-contraction coupling junction. Methods Cell Biol 79:407–435PubMedGoogle Scholar
  330. Shaw M, Ostap E, Goldman Y (2003) Mechanism of inhibition of skeletal muscle actomyosin by N-benzyl-p-toluene sulphonamide. Biochemistry 42:6128–6135PubMedGoogle Scholar
  331. Shirokova N, Ríos E (1997) Small event Ca2+ release: a probable precursor of Ca2+ sparks in frog skeletal muscle. J Physiol 502:3–11Google Scholar
  332. Shirokova N, García J, Pizarro G, Ríos E (1996) Ca2+ release from the sarcoplasmic reticulum compared in amphibian and mammalian skeletal muscle. J Gen Physiol 107:1–18Google Scholar
  333. Shkryl V, Shirokova N (2006) Transfer and tunneling of Ca2+ from sarcoplasmic reticulum to mitochondria in skeletal muscle. J Biol Chem 281:1547–1554PubMedGoogle Scholar
  334. Shore G, Tata J (1977) Two fractions of rough endoplasmic reticulum from rat liver. I. Recovery of rapidly sedimenting endoplasmic reticulum in association with mitochondria. J Cell Biol 72:714–725PubMedGoogle Scholar
  335. Shtifman A, Ward C, Wang J, Valdivia H, Schneider M (2000) Effects of imperatoxin A on local sarcoplasmic reticulum Ca(2+) release in frog skeletal muscle. Biophys J 79:814–827PubMedCentralPubMedGoogle Scholar
  336. Smets I, Caplanusi A, Despa S, Molnar Z, Radu M, VandeVen M, Ameloot M, Steels P (2004) Ca2+ uptake in mitochondria occurs via the reverse action of the Na+/Ca2+ exchanger in metabolically inhibited MDCK cells. Am J Physiol Ren Physiol 286:F784–F794Google Scholar
  337. Smith J, Imagawa T, Ma J, Fill M, Campbell K, Coronado R (1988) Purified ryanodine receptor from rabbit skeletal muscle is the Ca2+release channel of the SR. J Gen Physiol 92:1–26PubMedGoogle Scholar
  338. Smyth J, Dehaven W, Jones B, Mercer J, Trebak M, Vazquez G, Putney J Jr (2006) Emerging perspectives in store-operated Ca2+ entry: roles of Orai, Stim and TRP. Biochim Biophys Acta 1763:1147–1160PubMedGoogle Scholar
  339. Soboloff J, Spassova M, Dziadek M, Gill D (2006) Calcium signals mediated by STIM and Orai proteins–a new paradigm in inter-organelle communication. Biochim Biophys Acta 1763:1161–1168PubMedGoogle Scholar
  340. Sparagna G, Gunter K, Sheu S, Gunter T (1995) Mitochondrial calcium uptake from physiological-type pulses of calcium. A description of the rapid uptake mode. J Biol Chem 270:27510–27515PubMedGoogle Scholar
  341. Stern M (1992) Buffering of calcium in the vicinity of a channel pore. Cell Calcium 13:183–192PubMedGoogle Scholar
  342. Stiber J, Hawkins A, Zhang Z, Wang S, Burch J, Graham V, Ward C, Seth M, Finch E, Malouf N, Williams R, Eu J, Rosenberg P (2008) STIM1 signalling controls store-operated calcium entry required for development and contractile function in skeletal muscle. Nat Cell Biol 10:688–697PubMedCentralPubMedGoogle Scholar
  343. Sun Y, Lou F, Edman K (2001) 2,3-Butanedione monoxime increases speed of relaxation in single muscle fibres of frog. Acta Physiol Scand 172:53–61PubMedGoogle Scholar
  344. Szentesi P, Jacquemond V, Kovács L, Csernoch L (1997) Intramembrane charge movement and sarcoplasmic calcium release in enzymatically isolated mammalian skeletal muscle fibres. J Physiol 502:371–384Google Scholar
  345. Takahashi A, Camacho P, Lechleiter J, Herman B (1999) Measurement of intracellular calcium. Physiol Rev 79:1089–1125PubMedGoogle Scholar
  346. Takehura H, Fujinami N, Nishizawa T, Ogasawara H, Kasuga N (2001) Eccentric exercise-induced morphological changes in the membrane systems involved in excitation-contraction coupling in rat skeletal muscle. J Physiol 533:571–583Google Scholar
  347. Takeshima H, Nishimura S, Matsumoto T, Ishida H, Kangawa K, Minamino N, Matsuo H, Ueda M, Hanaoka M, Hirose T et al (1989) Primary structure and expression from complementary DNA of skeletal muscle ryanodine receptor. Nature 339:439–445PubMedGoogle Scholar
  348. Tanabe T, Takeshima H, Mikami A, Flockerzi V, Takahashi H, Kangawa K, Kojima M, Matsuo H, Hirose T, Numa S (1987) Primary structure of the receptor for calcium channel blockers from skeletal muscle. Nature 328:313–318PubMedGoogle Scholar
  349. Tanabe T, Beam K, Powell J, Numa S (1988) Restoration of excitation-contraction coupling and slow calcium current in dysgenic muscle by dihydropyridine receptor complementary DNA. Nature 336:134–139PubMedGoogle Scholar
  350. Tanabe T, Beam K, Adams B, Niidome T, Numa S (1990) Regions of the skeletal dihydropyridine receptor critical for excitation-contraction coupling. Nature 346:567–569PubMedGoogle Scholar
  351. Tang S, Wong H, Wang Z, Huang Y, Zhuo Y, Pennati A, Gadda G, Delbono O, Yang J (2011) Design and application of a class of sensors to monitor Ca2+ dynamics in high Ca2+ concentration cellular compartments. Proc Natl Acad Sci U S A 108:16265–16270PubMedCentralPubMedGoogle Scholar
  352. Toyoshima H, Mizutani T (2004) Crystal structure of the calcium pump with a bound ATP analogue. Nature 430:529–535PubMedGoogle Scholar
  353. Treves S, Vukcevic M, Maj M, Thurnheer R, Mosca B, Zorzato F (2009) Minor sarcoplasmic reticulum membrane components that modulate excitation-contraction coupling in striated muscles. J Physiol 587:3071–3079PubMedCentralPubMedGoogle Scholar
  354. Treves S, Thurnheer R, Mosca B, Vukcevic M, Bergamelli L, Voltan R, Oberhauser V, Ronjat M, Csernoch L, Szentesi P, Zorzato F (2012) SRP-35, a newly identified protein of the skeletal muscle sarcoplasmic reticulum, is a retinol dehydrogenase. Biochem J 441:731–741PubMedGoogle Scholar
  355. Tsien R (1981) A non-disruptive technique for loading calcium buffers and indicators into cells. Nature 290:527–528PubMedGoogle Scholar
  356. Tsugorka A, Ríos E, Blatter L (1995) Imaging elementary events of calcium release in skeletal muscle cells. Science 269:1723–1726Google Scholar
  357. Tung C, Lobo P, Kimlicka L, Van Petegem F (2010) The amino-terminal disease hotspot of ryanodine receptors forms a cytoplasmic vestibule. Nature 468:585–58PubMedGoogle Scholar
  358. Tupling R (2004) The sarcoplasmic reticulum in muscle fatigue and disease: role of the sarco(endo)plasmic reticulum Ca2+-ATPase. Can J Appl Physiol 29:308–329PubMedGoogle Scholar
  359. van der Poel C, Edwards J, Macdonald W, Stephenson D (2008) Effect of temperature-induced reactive oxygen species production on excitation-contraction coupling in mammalian skeletal muscle. Clin Exp Pharmacol Physiol 35:1482–1487PubMedGoogle Scholar
  360. Vendelin M, Beraud N, Guerrero K, Andrienko T, Kuznetsov A, Olivares J, Kay L, Saks V (2005) Mitochondrial regular arrangement in muscle cells: a "crystal-like" pattern. Am J Physiol Cell Physiol 288:C757–C767PubMedGoogle Scholar
  361. Verburg E, Murphy R, Stephenson G, Lamb G (2005) Disruption of excitation-contraction coupling and titin by endogenous Ca2+-activated proteases in toad muscle fibres. J Physiol 564:775–789PubMedCentralPubMedGoogle Scholar
  362. Verburg E, Dutka T, Lamb G (2006) Long-lasting muscle fatigue: partial disruption of excitation-contraction coupling by elevated cytosolic Ca2+ concentration during contractions. Am J Physiol 290:C1199–C1208Google Scholar
  363. Vig M, Peinelt C, Beck A, Koomoa DL, Rabah D, Koblan-Huberson M, Kraft S, Turner H, Fleig A, Penner R, Kinet J (2006) CRACM1 is a plasma membrane protein essential for store-operated Ca2+ entry. Science 312:1220–1223PubMedGoogle Scholar
  364. Vig M, DeHaven W, Bird G, Billingsley J, Wang H, Rao P, Hutchings A, Jouvin M, Putney J, Kinet J (2008) Defective mast cell effector functions in mice lacking the CRACM1 pore subunit of store-operated calcium release-activated calcium channels. Nat Immunol 9:89–96PubMedCentralPubMedGoogle Scholar
  365. Wagenknecht T, Grassucci R, Frank J, Saito A, Inui M, Fleischer S (1989) Three-dimensional architecture of the calcium channel/foot structure of sarcoplasmic reticulum. Nature 338:167–170PubMedGoogle Scholar
  366. Wagenknecht T, Hsieh C-E, Rath B, Fleischer S, Marko M (2002) Electron tomography of frozen-hydrated isolated triad junctions. Biophys J 83:2491–2501PubMedCentralPubMedGoogle Scholar
  367. Wang Z, Zheng Z, Messi M, Delbono O (2007) Muscle fibers from senescent mice retain excitation-contraction coupling properties in culture. In vitro Cell Dev Biol 43:222–234Google Scholar
  368. Wang Z, Tang S, Messi M, Yang J, Delbono (2012) Residual sarcoplasmic reticulum Ca2+ concentration after Ca2+ release in skeletal myofibers from young adult and old mice. Pflugers Arch 463:615–624PubMedCentralPubMedGoogle Scholar
  369. Ward C, Prosser B, Greiser M, Westerblad H, Khairallah R, Lederer W (2011) A novel assay of mechano-transduction in single muscle cells. Biophys J 100:589a. abstract,3185-PosGoogle Scholar
  370. Weber A (1959) On the role of calcium in the activity of adenosine 5′-triphosphate hydrolysis by actomyosin. J Biol Chem 234:2764–2769PubMedGoogle Scholar
  371. Weber A, Herz R (1968) The relationship between caffeine contracture in intact muscle and the effect of caffeine on Reticulum. J Gen Physiol 52:750–759PubMedCentralPubMedGoogle Scholar
  372. Wei L, Varsányi M, Dulhunty A, Beard N (2006) The conformation of calsequestrin determines its ability to regulate skeletal ryanodine receptors. Biophys J 91:1288–1301PubMedCentralPubMedGoogle Scholar
  373. Weisleder N, Zhou J, Ma J (2012) Detection of calcium sparks in intact and permeabilized skeletal muscle fibers. Methods Mol Biol 798:395–410Google Scholar
  374. Westerblad H (1999) The role of pH and inorganic phosphate ions in skeletal muscle fatigue. Chapter 12. In: Hargreaves M, Thompson M (eds) Biochemistry of exercise X. Champaign, USA, Human Kinetics, pp p147–p154Google Scholar
  375. Westerblad H, Allen D (1991) Changes of myoplasmic calcium concentration during fatigue in single mouse muscle fibers. J Gen Physiol 98:615–635PubMedGoogle Scholar
  376. Westerblad H, Allen D (1992) Myoplasmic free Mg2+ concentration during repetitive stimulation of single fibres from mouse skeletal muscle. J Physiol 453:413–434PubMedCentralPubMedGoogle Scholar
  377. Westerblad H, Allen D (1993) The contribution of [Ca2+]i to the slowing of relaxation in fatigued single fibres from mouse skeletal muscle. J Physiol 468:729–740PubMedCentralPubMedGoogle Scholar
  378. Westerblad H, Lännergren J (1991) Slowing of relaxation during fatigue in single mouse muscle fibres. J Physiol 434:323–336Google Scholar
  379. Westerblad H, Allen D, Lännergren J (2002) Muscle fatigue: lactic acid or inorganic phosphate the major cause? News Physiol Sci 17:17–21PubMedGoogle Scholar
  380. Williams D, Head S, Bakker A, Stephenson G (1990) Resting calcium concentrations in isolated skeletal muscle fibres of dystrophic mice. J Physiol 428:243–256Google Scholar
  381. Winegrad S (1968) Intracellular calcium movements of frog skeletal muscle during recovery from tetanus. J Gen Physiol 51:65–83PubMedCentralPubMedGoogle Scholar
  382. Wium E, Dulhunty A, Beard N (2012) A skeletal muscle ryanodine receptor interaction domain in triadin. PLoS One 7:e43817PubMedCentralPubMedGoogle Scholar
  383. Wong J, Baddeley D, Bushong E, Yu Z, Ellisman M, Hoshijima M, Soeller C (2013) Nanoscale distribution of ryanodine receptors and caveolin-3 in mouse ventricular myocytes: dilation of T-tubules near the junctions. Biophys J 104:L22–L24PubMedGoogle Scholar
  384. Wood D, Zollman J, Reuben J (1975) Human skeletal muscle properties of the “chemically skinned” fiber. Science 187:1075–1076PubMedGoogle Scholar
  385. Woods C, Novo D, DiFranco M, Vergara J (2004) The action potential-evoked sarcoplasmic reticulum calcium release is impaired in mdx mouse muscle fibres. J Physiol 557:59–75PubMedCentralPubMedGoogle Scholar
  386. Yaffe D, Saxel O (1977) Serial passaging and differentiation of myogenic cells isolated from dystrophic mouse muscle. Nature 270:725–727PubMedGoogle Scholar
  387. Yi J, Ma C, Li Y, Weisleder N, Rios E, Ma J, Zhou J (2011) Mitochondrial calcium uptake regulates rapid calcium transients in skeletal muscle during excitation-contraction (E-C) coupling. J Biol Chem 286:32436–32443PubMedCentralPubMedGoogle Scholar
  388. Zalman L, Nikaido H, Kagawa Y (1980) Mitochondrial outer membrane contains a protein producing nonspecific diffusion channels. J Biol Chem 255:1771–1774PubMedGoogle Scholar
  389. Zhang S, Yu Y, Roos J, Kozak J, Deerinck T, Ellisman M, Stauderman K, Cahalan M (2005) STIM1 is a Ca2+ sensor that activates CRAC channels and migrates from the Ca2+ store to the plasma membrane. Nature 437:902–905PubMedCentralPubMedGoogle Scholar
  390. Zhou J, Launikonis B, Ríos E, Brum G (2004) Regulation of Ca2+ sparks by Ca2+ and Mg2+ in mammalian and amphibian muscle. An RyR isoform-specific role in excitation-contraction coupling? J Gen Physiol 124:409–428Google Scholar
  391. Zhou J, Yi J, Royer L, Launikonis B, González A, García J, Ríos 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–C553Google Scholar
  392. Zoratti M, Szabo I, De Marchi U (2005) Mitochondrial permeability transitions: how many doors to the house? Biochim Biophys Acta 1706:40–52PubMedGoogle Scholar
  393. Zorzato F, Fujii J, Otsu M, Phillips M, Green N, Lai F, Meissner G, MacLennan D (1990) Molecular cloning of cDNA encoding human and rabbit forms of the Ca2+ release channel (ryanodine receptor) of skeletal muscle sarcoplasmic reticulum. J Biol Chem 265:2244–2256PubMedGoogle Scholar

Copyright information

© International Union for Pure and Applied Biophysics (IUPAB) and Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Juan C. Calderón
    • 1
    • 2
    • 3
  • Pura Bolaños
    • 2
  • Carlo Caputo
    • 2
  1. 1.Physiology and Biochemistry Research Group-Physis, Department of Physiology and Biochemistry, Faculty of MedicineUniversity of Antioquia UdeAMedellínColombia
  2. 2.Laboratory of Cellular Physiology, Centre of Biophysics and BiochemistryVenezuelan Institute for Scientific Research (IVIC)CaracasVenezuela
  3. 3.Departamento de Fisiología y Bioquímica, Grupo de Investigación en Fisiología y Bioquímica-Physis, Facultad de MedicinaUniversidad de AntioquiaMedellínColombia

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