Calcium Microdomains in Cardiac Cells

  • A. M. Gómez
  • T. R. R. Mesquita
  • J. J. Mercadier
  • J. L. Álvarez
  • J. P. Benitah
Chapter
Part of the Cardiac and Vascular Biology book series (Abbreviated title: Card. vasc. biol.)

Abstract

Calcium (Ca2+) is a universal intracellular second messenger. In the heart, it plays a key role by activating contraction through the excitation-contraction coupling (EC coupling) mechanism. Although this is its key role in the heart, Ca2+ has other important functions, not only being involved in cell growth (in the heart named excitation-transcription coupling, ET coupling) but also in mitochondrial function (excitation-metabolism coupling, EM coupling) and cell death. Moreover, as Ca2+ is electrically charged, its movement across membranes generates an electrical current, which is important in cardiomyocyte electrophysiology and, if disturbed, may be involved in arrhythmias. The cardiac myocyte may discriminate between Ca2+ signals by creating “spaces” where Ca2+ diffusion is limited, creating gradients of [Ca2+]i at the micrometer scale, which are named microdomains. They are maintained by the cellular architecture and location of Ca2+-handling proteins and buffers.

Keywords

Calcium Ventricular cardiomyocyte Sarcoplasmic reticulum Ryanodine receptor Calcium sparks 

Notes

Acknowledgments

Funding was provided by the National Agency of Research (ANR-13-BSV1-0023, ANR-15-CE14-0005) Inserm, and University Paris-Sud. We thank the program Jean d’Alembert (Université Paris-Sud, Université Paris-Saclay) for providing an invited scientist fellowship to JLA. We are in debt to Françoise Boussac for administrative assistance.

Compliance with Ethical Standards

Conflict of Interest Statement

The authors declare that they have no conflict of interest.

References

  1. Abriel H, Rougier JS, Jalife J (2015) Ion channel macromolecular complexes in cardiomyocytes: roles in sudden cardiac death. Circ Res 116:1971–1988PubMedPubMedCentralCrossRefGoogle Scholar
  2. Acsai K, Antoons G, Livshitz L et al (2011) Microdomain [Ca(2)(+)] near ryanodine receptors as reported by L-type Ca(2)(+) and Na+/Ca(2)(+) exchange currents. J Physiol 589:2569–2583PubMedPubMedCentralCrossRefGoogle Scholar
  3. Adachi-Akahane S, Cleemann L, Morad M (1996) Cross-signaling between L-type Ca2+ channels and ryanodine receptors in rat ventricular myocytes. J Gen Physiol 108:435–454PubMedCrossRefGoogle Scholar
  4. Ai X, Curran JW, Shannon TR et al (2005) Ca2+/calmodulin-dependent protein kinase modulates cardiac ryanodine receptor phosphorylation and sarcoplasmic reticulum Ca2+ leak in heart failure. Circ Res 97:1314–1322PubMedCrossRefGoogle Scholar
  5. Alvarez BV, Perez NG, Ennis IL et al (1999) Mechanisms underlying the increase in force and Ca(2+) transient that follow stretch of cardiac muscle: a possible explanation of the Anrep effect. Circ Res 85:716–722PubMedCrossRefGoogle Scholar
  6. Andrienko TN, Picht E, Bers DM (2009) Mitochondrial free calcium regulation during sarcoplasmic reticulum calcium release in rat cardiac myocytes. J Mol Cell Cardiol 46:1027–1036PubMedPubMedCentralCrossRefGoogle Scholar
  7. Awasthi S, Izu LT, Mao Z et al (2016) Multimodal SHG-2PF imaging of microdomain Ca2 + −contraction coupling in live cardiac myocytes. Circ Res 118:e19–e28PubMedCrossRefGoogle Scholar
  8. Baartscheer A, Schumacher CA, van Borren MM et al (2003) Increased Na+/H + −exchange activity is the cause of increased [Na+]i and underlies disturbed calcium handling in the rabbit pressure and volume overload heart failure model. Cardiovasc Res 57:1015–1024PubMedCrossRefGoogle Scholar
  9. Baines CP (2009) The molecular composition of the mitochondrial permeability transition pore. J Mol Cell Cardiol 46:850–857PubMedPubMedCentralCrossRefGoogle Scholar
  10. Balaban RS, Bose S, French SA, Territo PR (2003) Role of calcium in metabolic signaling between cardiac sarcoplasmic reticulum and mitochondria in vitro. Am J Physiol Cell Physiol 284:C285–C293PubMedCrossRefGoogle Scholar
  11. Balshaw DM, Xu L, Yamaguchi N et al (2001) Calmodulin binding and inhibition of cardiac muscle calcium release channel (ryanodine receptor). J Biol Chem 276:20144–20153PubMedCrossRefGoogle Scholar
  12. Barta J, Toth A, Edes I et al (2005) Calpain-1-sensitive myofibrillar proteins of the human myocardium. Mol Cell Biochem 278:1–8PubMedCrossRefGoogle Scholar
  13. Bassani JW, Bassani RA, Bers DM (1994) Relaxation in rabbit and rat cardiac cells: species-dependent differences in cellular mechanisms. J Physiol 476:279–293PubMedPubMedCentralCrossRefGoogle Scholar
  14. Baughman JM, Perocchi F, Girgis HS et al (2011) Integrative genomics identifies MCU as an essential component of the mitochondrial calcium uniporter. Nature 476:341–345PubMedPubMedCentralCrossRefGoogle Scholar
  15. Bazil JN, Dash RK (2011) A minimal model for the mitochondrial rapid mode of Ca(2) + uptake mechanism. PLoS One 6:e21324PubMedPubMedCentralCrossRefGoogle Scholar
  16. Becerra R, Roman B, Di Carlo MN et al (2016) Reversible redox modifications of ryanodine receptor ameliorate ventricular arrhythmias in the ischemic-reperfused heart. Am J Physiol Heart Circ Physiol 311:H713–H724PubMedPubMedCentralCrossRefGoogle Scholar
  17. Benitah JP, Perrier E, Gómez AM, Vassort G (2001) Effects of aldosterone on transient outward K+ current density in rat ventricular myocytes. J Physiol Lond 537:151–160Google Scholar
  18. Benitah JP, Kerfant BG, Vassort G et al (2002) Altered communication between L-type calcium channels and ryanodine receptors in heart failure. Front Biosci 7:E263–E275PubMedCrossRefGoogle Scholar
  19. Benitah JP, Alvarez JL, Gómez AM (2010) L-type Ca(2+) current in ventricular cardiomyocytes. J Mol Cell Cardiol 48:26–36Google Scholar
  20. Ben-Johny M, Yue DT (2014) Calmodulin regulation (calmodulation) of voltage-gated calcium channels. J Gen Physiol 143:679–692PubMedPubMedCentralCrossRefGoogle Scholar
  21. Benkusky NA, Weber CS, Scherman JA et al (2007) Intact beta-adrenergic response and unmodified progression toward heart failure in mice with genetic ablation of a major protein kinase a phosphorylation site in the cardiac ryanodine receptor. Circ Res 101:819–829PubMedCrossRefGoogle Scholar
  22. Bernardi P, Di Lisa F (2015) The mitochondrial permeability transition pore: molecular nature and role as a target in cardioprotection. J Mol Cell Cardiol 78:100–106PubMedPubMedCentralCrossRefGoogle Scholar
  23. Bernardi P, Forte M (2007) The mitochondrial permeability transition pore. Novartis Found Symp 287:157–164; discussion 164–159Google Scholar
  24. Bers DM (2008) Calcium cycling and signaling in cardiac myocytes. Annu Rev Physiol 70:23–49PubMedCrossRefGoogle Scholar
  25. Bers DM (2013) Membrane receptor neighborhoods: snuggling up to the nucleus. Circ Res 112:224–226PubMedPubMedCentralCrossRefGoogle Scholar
  26. Bers DM (2014) Cardiac sarcoplasmic reticulum calcium leak: basis and roles in cardiac dysfunction. Annu Rev Physiol 76:107–127PubMedCrossRefGoogle Scholar
  27. Best JM, Kamp TJ (2012) Different subcellular populations of L-type Ca2+ channels exhibit unique regulation and functional roles in cardiomyocytes. J Mol Cell Cardiol 52:376–387PubMedCrossRefGoogle Scholar
  28. Bito V, Biesmans L, Gellen B et al (2013) FKBP12.6 overexpression does not protect against remodelling after myocardial infarction. Exp Physiol 98:134–148PubMedCrossRefGoogle Scholar
  29. Bolli R, Marban E (1999) Molecular and cellular mechanisms of myocardial stunning. Physiol Rev 79:609–634PubMedCrossRefGoogle Scholar
  30. Bossuyt J, Bers DM (2013) Visualizing CaMKII and CaM activity: a paradigm of compartmentalized signaling. J Mol Med (Berl) 91:907–916CrossRefGoogle Scholar
  31. Brandes R, Bers DM (1997) Intracellular Ca2+ increases the mitochondrial NADH concentration during elevated work in intact cardiac muscle. Circ Res 80:82–87PubMedCrossRefGoogle Scholar
  32. Brandes R, Bers DM (2002) Simultaneous measurements of mitochondrial NADH and Ca(2+) during increased work in intact rat heart trabeculae. Biophys J 83:587–604PubMedPubMedCentralCrossRefGoogle Scholar
  33. Brillantes AB, Ondrias K, Scott A et al (1994) Stabilization of calcium release channel (ryanodine receptor) function by FK506-binding protein. Cell 77:513–523PubMedCrossRefGoogle Scholar
  34. Brini M, Carafoli E (2000) Calcium signalling: a historical account, recent developments and future perspectives. Cell Mol Life Sci 57:354–370PubMedCrossRefGoogle Scholar
  35. Brochet DX, Yang D, Di Maio A et al (2005) Ca2+ blinks: rapid nanoscopic store calcium signaling. Proc Natl Acad Sci U S A 102:3099–3104PubMedPubMedCentralCrossRefGoogle Scholar
  36. Bush EW, Hood DB, Papst PJ et al (2006) Canonical transient receptor potential channels promote cardiomyocyte hypertrophy through activation of calcineurin signaling. J Biol Chem 281:33487–33496PubMedCrossRefGoogle Scholar
  37. Calderon-Sanchez EM, Ruiz-Hurtado G, Smani T et al (2011) Cardioprotective action of urocortin in postconditioning involves recovery of intracellular calcium handling. Cell Calcium 50:84–90PubMedCrossRefGoogle Scholar
  38. Cali T, Ottolini D, Brini M (2012) Mitochondrial Ca(2+) as a key regulator of mitochondrial activities. Adv Exp Med Biol 942:53–73PubMedCrossRefGoogle Scholar
  39. Carafoli E, Tiozzo R, Lugli G et al (1974) The release of calcium from heart mitochondria by sodium. J Mol Cell Cardiol 6:361–371PubMedCrossRefGoogle Scholar
  40. Carter S, Colyer J, Sitsapesan R (2006) Maximum phosphorylation of the cardiac ryanodine receptor at serine-2809 by protein kinase a produces unique modifications to channel gating and conductance not observed at lower levels of phosphorylation. Circ Res 98:1506–1513PubMedCrossRefGoogle Scholar
  41. Chen X, Nakayama H, Zhang X et al (2011) Calcium influx through Cav1.2 is a proximal signal for pathological cardiomyocyte hypertrophy. J Mol Cell Cardiol 50:460–470PubMedCrossRefGoogle Scholar
  42. Cheng H, Lederer WJ (2008) Calcium sparks. Physiol Rev 88:1491–1545PubMedCrossRefGoogle Scholar
  43. Cheng H, Lederer WJ, Cannell MB (1993) Calcium sparks: elementary events underlying excitation-contraction coupling in heart muscle. Science 262:740–744PubMedCrossRefGoogle Scholar
  44. Cheng H, Lederer MR, Lederer WJ, Cannell MB (1996) Calcium sparks and [Ca2+]i waves in cardiac myocytes. Am J Phys 270:C148–C159CrossRefGoogle Scholar
  45. Chiang CS, Huang CH, Chieng H et al (2009) The Ca(v)3.2 T-type Ca(2+) channel is required for pressure overload-induced cardiac hypertrophy in mice. Circ Res 104:522–530PubMedCrossRefGoogle Scholar
  46. Chopra N, Knollmann BC (2013) Triadin regulates cardiac muscle couplon structure and microdomain Ca(2+) signalling: a path towards ventricular arrhythmias. Cardiovasc Res 98:187–191PubMedPubMedCentralCrossRefGoogle Scholar
  47. Correll RN, Goonasekera SA, van Berlo JH et al (2015) STIM1 elevation in the heart results in aberrant Ca(2)(+) handling and cardiomyopathy. J Mol Cell Cardiol 87:38–47PubMedPubMedCentralCrossRefGoogle Scholar
  48. Crocini C, Coppini R, Ferrantini C et al (2014) Defects in T-tubular electrical activity underlie local alterations of calcium release in heart failure. Proc Natl Acad Sci U S A 111:15196–15201PubMedPubMedCentralCrossRefGoogle Scholar
  49. De Stefani D, Raffaello A, Teardo E et al (2011) A forty-kilodalton protein of the inner membrane is the mitochondrial calcium uniporter. Nature 476:336–340PubMedPubMedCentralCrossRefGoogle Scholar
  50. De Stefani D, Rizzuto R, Pozzan T (2016) Enjoy the trip: calcium in mitochondria back and forth. Annu Rev Biochem 85:161–192PubMedCrossRefGoogle Scholar
  51. Delgado C, Artiles A, Gómez AM, Vassort G (1999) Frequency-dependent increase in cardiac Ca2+ current is due to reduced Ca2+ release by the sarcoplasmic reticulum. J Mol Cell Cardiol 31:1783–1793PubMedCrossRefGoogle Scholar
  52. Denton RM, McCormack JG (1990) Ca2+ as a second messenger within mitochondria of the heart and other tissues. Annu Rev Physiol 52:451–466PubMedCrossRefGoogle Scholar
  53. Dominguez-Rodriguez A, Ruiz-Hurtado G, Benitah JP, Gómez AM (2012) The other side of cardiac Ca(2+) signaling: transcriptional control. Front Physiol 3:452Google Scholar
  54. 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 109:12986–12991PubMedPubMedCentralCrossRefGoogle Scholar
  55. Eder P, Molkentin JD (2011) TRPC channels as effectors of cardiac hypertrophy. Circ Res 108:265–272PubMedCrossRefGoogle Scholar
  56. Egger M, Gómez AM, Schwaller B et al (2001) Na+/Ca2+ exchange activity in the post-myocardial infarction rat model. Biophys J 80:2710Google Scholar
  57. Eisner DA, Diaz ME, O’Neill SC, Trafford AW (2004) Physiological and pathological modulation of ryanodine receptor function in cardiac muscle. Cell Calcium 35:583–589PubMedCrossRefGoogle Scholar
  58. Erickson JR, Pereira L, Wang L et al (2013) Diabetic hyperglycaemia activates CaMKII and arrhythmias by O-linked glycosylation. Nature 502:372–376PubMedPubMedCentralCrossRefGoogle Scholar
  59. Fabiato A, Fabiato F (1975) Contractions induced by a calcium-triggered release of calcium from the sarcoplasmic reticulum of single skinned cardiac cells. J Physiol 249:469–495PubMedPubMedCentralCrossRefGoogle Scholar
  60. Farrell EF, Antaramián A, Rueda A et al (2003) Sorcin inhibits calcium release and modulates excitation-contraction coupling in the heart. J Biol Chem 278:34660–34666PubMedCrossRefGoogle Scholar
  61. Fernandez-Velasco M, Rueda A, Rizzi N et al (2009) Increased Ca2+ sensitivity of the ryanodine receptor mutant RyR2R4496C underlies catecholaminergic polymorphic ventricular tachycardia. Circ Res 104:201–209PubMedCrossRefGoogle Scholar
  62. Fernández-Velasco M, Ruiz-Hurtado G, Rueda A et al (2011) RyRCa2+ leak limits cardiac Ca2+ window current overcoming the tonic effect of calmodulinin mice. PLoS One 6:e20863PubMedPubMedCentralCrossRefGoogle Scholar
  63. Fill M, Copello JA (2002) Ryanodine receptor calcium release channels. Physiol Rev 82:893–922PubMedCrossRefGoogle Scholar
  64. Finkel T, Menazza S, Holmstrom KM et al (2015) The ins and outs of mitochondrial calcium. Circ Res 116:1810–1819PubMedCrossRefGoogle Scholar
  65. Galfre E, Pitt SJ, Venturi E et al (2012) FKBP12 activates the cardiac ryanodine receptor Ca2 + −release channel and is antagonised by FKBP12.6. PLoS One 7:e31956PubMedPubMedCentralCrossRefGoogle Scholar
  66. Gangopadhyay JP, Ikemoto N (2011) Aberrant interaction of calmodulin with the ryanodine receptor develops hypertrophy in the neonatal cardiomyocyte. Biochem J 438:379–387PubMedPubMedCentralCrossRefGoogle Scholar
  67. Gao H, Wang F, Wang W et al (2012) Ca(2+) influx through L-type Ca(2+) channels and transient receptor potential channels activates pathological hypertrophy signaling. J Mol Cell Cardiol 53:657–667PubMedPubMedCentralCrossRefGoogle Scholar
  68. Gellen B, Fernandez-Velasco M, Briec F et al (2008) Conditional FKBP12.6 overexpression in mouse cardiac myocytes prevents triggered ventricular tachycardia through specific alterations in excitation-contraction coupling. Circulation 117:1778–1786PubMedCrossRefGoogle Scholar
  69. Gómez AM, Cheng HP, Lederer WJ, Bers DM (1996) Ca2+ diffusion and sarcoplasmic reticulum transport both contribute to Ca2+ (i) decline during Ca2+ sparks in rat ventricular myocytes. J Physiol Lond 496:575–581PubMedPubMedCentralCrossRefGoogle Scholar
  70. Gómez AM, Valdivia HH, Cheng H et al (1997) Defective excitation-contraction coupling in experimental cardiac hypertrophy and heart failure. Science 276:800–806PubMedCrossRefGoogle Scholar
  71. Gómez AM, Guatimosim S, Dilly KW, Vassort G, Lederer WJ (2001) Heart failure after myocardial infarction: altered excitation-contraction coupling. Circulation 104:688–693PubMedCrossRefGoogle Scholar
  72. Gómez AM, Schuster I, Fauconnier J et al (2004) FKBP12.6 overexpression decreases Ca2+ spark amplitude but enhances [Ca2+](i) transient in rat cardiac myocytes. Am J Phys Heart Circ Phys 287:H1987–H1993Google Scholar
  73. Gómez AM, Rueda A, Sainte-Marie Y et al (2009) Mineralocorticoid modulation of cardiac ryanodine receptor activity is associated with downregulation of FK506-binding proteins. Circulation 119:2179–U2189PubMedCrossRefGoogle Scholar
  74. Gonzalez DR, Treuer AV, Castellanos J et al (2010) Impaired S-nitrosylation of the ryanodine receptor caused by xanthine oxidase activity contributes to calcium leak in heart failure. J Biol Chem 285:28938–28945PubMedPubMedCentralCrossRefGoogle Scholar
  75. Gunter TE, Pfeiffer DR (1990) Mechanisms by which mitochondria transport calcium. Am J Phys 258:C755–C786CrossRefGoogle Scholar
  76. Guo T, Zhang T, Mestril R, Bers DM (2006) Ca2+/calmodulin-dependent protein kinase II phosphorylation of ryanodine receptor does affect calcium sparks in mouse ventricular myocytes. Circ Res 99:398–406PubMedCrossRefGoogle Scholar
  77. Guo T, Cornea RL, Huke S et al (2010) Kinetics of FKBP12.6 binding to ryanodine receptors in permeabilized cardiac myocytes and effects on Ca sparks. Circ Res 106:1743–1752PubMedPubMedCentralCrossRefGoogle Scholar
  78. Gyorke I, Gyorke S (1998) Regulation of the cardiac ryanodine receptor channel by luminal Ca2+ involves luminal Ca2+ sensing sites. Biophys J 75:2801–2810PubMedPubMedCentralCrossRefGoogle Scholar
  79. Gyorke S, Terentyev D (2008) Modulation of ryanodine receptor by luminal calcium and accessory proteins in health and cardiac disease. Cardiovasc Res 77:245–255PubMedCrossRefGoogle Scholar
  80. Hanna AD, Lam A, Thekkedam C et al (2014) Cardiac ryanodine receptor activation by a high Ca(2)(+) store load is reversed in a reducing cytoplasmic redox environment. J Cell Sci 127:4531–4541PubMedPubMedCentralCrossRefGoogle Scholar
  81. Harzheim D, Movassagh M, Foo RS et al (2009) Increased InsP3Rs in the junctional sarcoplasmic reticulum augment Ca2+ transients and arrhythmias associated with cardiac hypertrophy. Proc Natl Acad Sci U S A 106:11406–11411PubMedPubMedCentralCrossRefGoogle Scholar
  82. Heineke J, Molkentin JD (2006) Regulation of cardiac hypertrophy by intracellular signalling pathways. Nat Rev Mol Cell Biol 7:589–600PubMedCrossRefGoogle Scholar
  83. Ho HT, Belevych AE, Liu B et al (2016) Muscarinic stimulation facilitates sarcoplasmic reticulum Ca release by modulating ryanodine receptor 2 phosphorylation through protein kinase G and Ca/calmodulin-dependent protein kinase II. Hypertension 68(5):1171–1178PubMedPubMedCentralCrossRefGoogle Scholar
  84. Holton ML, Wang W, Emerson M et al (2010) Plasma membrane calcium ATPase proteins as novel regulators of signal transduction pathways. World J Biol Chem 1:201–208PubMedPubMedCentralCrossRefGoogle Scholar
  85. Horiba M, Muto T, Ueda N et al (2008) T-type Ca2+ channel blockers prevent cardiac cell hypertrophy through an inhibition of calcineurin-NFAT3 activation as well as L-type Ca2+ channel blockers. Life Sci 82:554–560PubMedCrossRefGoogle Scholar
  86. Hoth M, Button DC, Lewis RS (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 97:10607–10612PubMedPubMedCentralCrossRefGoogle Scholar
  87. Houser SR (2014) Role of RyR2 phosphorylation in heart failure and arrhythmias: protein kinase A-mediated hyperphosphorylation of the ryanodine receptor at serine 2808 does not alter cardiac contractility or cause heart failure and arrhythmias. Circ Res 114:1320–1327; discussion 1327Google Scholar
  88. Huang F, Shan J, Reiken S et al (2006) Analysis of calstabin2 (FKBP12.6)-ryanodine receptor interactions: rescue of heart failure by calstabin2 in mice. Proc Natl Acad Sci U S A 103:3456–3461PubMedPubMedCentralCrossRefGoogle Scholar
  89. Huang H, Wang W, Liu P et al (2009) TRPC1 expression and distribution in rat hearts. Eur J Histochem: EJH 53:e26PubMedPubMedCentralCrossRefGoogle Scholar
  90. Hudmon A, Schulman H, Kim J et al (2005) CaMKII tethers to L-type Ca2+ channels, establishing a local and dedicated integrator of Ca2+ signals for facilitation. J Cell Biol 171:537–547PubMedPubMedCentralCrossRefGoogle Scholar
  91. Huke S, Bers DM (2008) Ryanodine receptor phosphorylation at serine 2030, 2808 and 2814 in rat cardiomyocytes. Biochem Biophys Res Commun 376:80–85PubMedPubMedCentralCrossRefGoogle Scholar
  92. Hunton DL, Zou L, Pang Y, Marchase RB (2004) Adult rat cardiomyocytes exhibit capacitative calcium entry. Am J Physiol Heart Circ Physiol 286:H1124–H1132PubMedCrossRefGoogle Scholar
  93. Huser J, Blatter LA, Sheu SS (2000) Mitochondrial calcium in heart cells: beat-to-beat oscillations or slow integration of cytosolic transients? J Bioenerg Biomembr 32:27–33PubMedCrossRefGoogle Scholar
  94. Ibarra C, Vicencio JM, Varas-Godoy M et al (2014) An integrated mechanism of cardiomyocyte nuclear Ca(2+) signaling. J Mol Cell Cardiol 75:40–48PubMedPubMedCentralCrossRefGoogle Scholar
  95. Iribe G, Ward CW, Camelliti P et al (2009) Axial stretch of rat single ventricular cardiomyocytes causes an acute and transient increase in Ca2+ spark rate. Circ Res 104:787–795PubMedPubMedCentralCrossRefGoogle Scholar
  96. Isenberg G, Kazanski V, Kondratev D et al (2003) Differential effects of stretch and compression on membrane currents and [Na+]c in ventricular myocytes. Prog Biophys Mol Biol 82:43–56PubMedCrossRefGoogle Scholar
  97. Iwata Y, Katanosaka Y, Arai Y et al (2003) A novel mechanism of myocyte degeneration involving the Ca2 + −permeable growth factor-regulated channel. J Cell Biol 161:957–967PubMedPubMedCentralCrossRefGoogle Scholar
  98. Jeyakumar LH, Ballester L, Cheng DS et al (2001) FKBP binding characteristics of cardiac microsomes from diverse vertebrates. Biochem Biophys Res Commun 281:979–986PubMedCrossRefGoogle Scholar
  99. Jiang MT, Lokuta AJ, Farrell EF et al (2002) Abnormal Ca2+ release, but normal ryanodine receptors, in canine and human heart failure. Circ Res 91:1015–1022PubMedCrossRefGoogle Scholar
  100. Kamkin A, Kiseleva I, Isenberg G (2003) Ion selectivity of stretch-activated cation currents in mouse ventricular myocytes. Pflugers Arch 446:220–231PubMedCrossRefGoogle Scholar
  101. Kirichok Y, Krapivinsky G, Clapham DE (2004) The mitochondrial calcium uniporter is a highly selective ion channel. Nature 427:360–364PubMedCrossRefGoogle Scholar
  102. Kobrinsky E, Duong SQ, Sheydina A, Soldatov NM (2011) Microdomain organization and frequency-dependence of CREB-dependent transcriptional signaling in heart cells. FASEB J 25:1544–1555PubMedPubMedCentralCrossRefGoogle Scholar
  103. Kohl P, Cooper PJ, Holloway H (2003) Effects of acute ventricular volume manipulation on in situ cardiomyocyte cell membrane configuration. Prog Biophys Mol Biol 82:221–227PubMedCrossRefGoogle Scholar
  104. Kushnir A, Marks AR (2012) Ryanodine receptor patents. Recent Pat Biotechnol 6:157–166PubMedPubMedCentralCrossRefGoogle Scholar
  105. Kuwahara K, Wang Y, McAnally J et al (2006) TRPC6 fulfills a calcineurin signaling circuit during pathologic cardiac remodeling. J Clin Invest 116:3114–3126PubMedPubMedCentralCrossRefGoogle Scholar
  106. Lab MJ (1996) Mechanoelectric feedback (transduction) in heart: concepts and implications. Cardiovasc Res 32:3–14PubMedCrossRefGoogle Scholar
  107. Lam E, Martin MM, Timerman AP et al (1995) A novel FK506 binding protein can mediate the immunosuppressive effects of FK506 and is associated with the cardiac ryanodine receptor. J Biol Chem 270:26511–26522PubMedCrossRefGoogle Scholar
  108. Li Y, Kranias EG, Mignery GA, Bers DM (2002) Protein kinase a phosphorylation of the ryanodine receptor does not affect calcium sparks in mouse ventricular myocytes. Circ Res 90:309–316PubMedCrossRefGoogle Scholar
  109. Lindner M, Brandt MC, Sauer H et al (2002) Calcium sparks in human ventricular cardiomyocytes from patients with terminal heart failure. Cell Calcium 31:175–182PubMedCrossRefGoogle Scholar
  110. Ljubojevic S, Bers DM (2015) Nuclear calcium in cardiac myocytes. J Cardiovasc Pharmacol 65:211–217PubMedPubMedCentralCrossRefGoogle Scholar
  111. Lokuta AJ, Meyers MB, Sander PR et al (1997) Modulation of cardiac ryanodine receptors by sorcin. J Biol Chem 272:25333–25338PubMedCrossRefGoogle Scholar
  112. Loughrey CM, Seidler T, Miller SL et al (2004) Over-expression of FK506-binding protein FKBP12.6 alters excitation-contraction coupling in adult rabbit cardiomyocytes. J Physiol 556(Pt 3):919–934PubMedPubMedCentralCrossRefGoogle Scholar
  113. Loyer X, Gómez AM, Milliez P et al (2008) Cardiomyocyte overexpression of neuronal nitric oxide synthase delays transition toward heart failure in response to pressure overload by preserving calcium cycling. Circulation 117:3187–3198PubMedCrossRefGoogle Scholar
  114. Luo X, Hojayev B, Jiang N et al (2012) STIM1-dependent store-operated Ca(2) entry is required for pathological cardiac hypertrophy. J Mol Cell Cardiol 52:136–147PubMedCrossRefGoogle Scholar
  115. Maack C, Cortassa S, Aon MA et al (2006) Elevated cytosolic Na + decreases mitochondrial Ca2+ uptake during excitation-contraction coupling and impairs energetic adaptation in cardiac myocytes. Circ Res 99:172–182PubMedPubMedCentralCrossRefGoogle Scholar
  116. Makarewich CA, Correll RN, Gao H et al (2012) A caveolae-targeted L-type Ca(2) + channel antagonist inhibits hypertrophic signaling without reducing cardiac contractility. Circ Res 110:669–674PubMedPubMedCentralCrossRefGoogle Scholar
  117. Makarewich CA, Zhang H, Davis J et al (2014) Transient receptor potential channels contribute to pathological structural and functional remodeling after myocardial infarction. Circ Res 115:567–580PubMedPubMedCentralCrossRefGoogle Scholar
  118. Malli R, Frieden M, Osibow K, Graier WF (2003) Mitochondria efficiently buffer subplasmalemmal Ca2+ elevation during agonist stimulation. J Biol Chem 278:10807–10815PubMedCrossRefGoogle Scholar
  119. Marx SO, Reiken S, Hisamatsu Y et al (2000) PKA phosphorylation dissociates FKBP12.6 from the calcium release channel (ryanodine receptor): defective regulation in failing hearts. Cell 101:365–376PubMedCrossRefGoogle Scholar
  120. Meyers MB, Pickel VM, Sheu SS et al (1995a) Association of sorcin with the cardiac ryanodine receptor. J Biol Chem 270:26411–26418PubMedCrossRefGoogle Scholar
  121. Meyers MB, Zamparelli C, Verzili D et al (1995b) Calcium-dependent translocation of sorcin to membranes: functional relevance in contractile tissue. FEBS Lett 357:230–234PubMedCrossRefGoogle Scholar
  122. Meyers MB, Puri TS, Chien AJ et al (1998) Sorcin associates with the pore-forming subunit of voltage-dependent L-type Ca2+ channels. J Biol Chem 273:18930–18935PubMedCrossRefGoogle Scholar
  123. Mitchell P (1961) Coupling of phosphorylation to electron and hydrogen transfer by a chemi-osmotic type of mechanism. Nature 191:144–148PubMedCrossRefGoogle Scholar
  124. Morad M, Soldatov N (2005) Calcium channel inactivation: possible role in signal transduction and Ca2+ signaling. Cell Calcium 38:223–231PubMedCrossRefGoogle Scholar
  125. Nakayama H, Wilkin BJ, Bodi I, Molkentin JD (2006) Calcineurin-dependent cardiomyopathy is activated by TRPC in the adult mouse heart. FASEB J 20:1660–1670PubMedPubMedCentralCrossRefGoogle Scholar
  126. Nakayama H, Bodi I, Maillet M et al (2010) The IP3 receptor regulates cardiac hypertrophy in response to select stimuli. Circ Res 107:659–666PubMedPubMedCentralCrossRefGoogle Scholar
  127. Naranjo JR, Mellstrom B (2012) Ca2 + −dependent transcriptional control of Ca2+ homeostasis. J Biol Chem 287:31674–31680PubMedPubMedCentralCrossRefGoogle Scholar
  128. Nicholls DG, Crompton M (1980) Mitochondrial calcium transport. FEBS Lett 111:261–268PubMedCrossRefGoogle Scholar
  129. Nichols CB, Rossow CF, Navedo MF et al (2010) Sympathetic stimulation of adult cardiomyocytes requires association of AKAP5 with a subpopulation of L-type calcium channels. Circ Res 107:747–756PubMedCrossRefGoogle Scholar
  130. Nicolli A, Basso E, Petronilli V et al (1996) Interactions of cyclophilin with the mitochondrial inner membrane and regulation of the permeability transition pore, and cyclosporin A-sensitive channel. J Biol Chem 271:2185–2192PubMedCrossRefGoogle Scholar
  131. O'Brien F, Venturi E, Sitsapesan R (2015) The ryanodine receptor provides high throughput Ca2 + −release but is precisely regulated by networks of associated proteins: a focus on proteins relevant to phosphorylation. Biochem Soc Trans 43:426–433PubMedCrossRefGoogle Scholar
  132. Ong HL, Ambudkar IS (2011) The dynamic complexity of the TRPC1 channelosome. Channels (Austin) 5:424–431CrossRefGoogle Scholar
  133. Ono K, Yano M, Ohkusa T et al (2000) Altered interaction of FKBP12.6 with ryanodine receptor as a cause of abnormal Ca(2+) release in heart failure. Cardiovasc Res 48:323–331PubMedCrossRefGoogle Scholar
  134. Onohara N, Nishida M, Inoue R et al (2006) TRPC3 and TRPC6 are essential for angiotensin II-induced cardiac hypertrophy. EMBO J 25:5305–5316PubMedPubMedCentralCrossRefGoogle Scholar
  135. O'Rourke B, Blatter LA (2009) Mitochondrial Ca2+ uptake: tortoise or hare? J Mol Cell Cardiol 46:767–774PubMedCrossRefGoogle Scholar
  136. Overend CL, Eisner DA, O'Neill SC (2001) Altered cardiac sarcoplasmic reticulum function of intact myocytes of rat ventricle during metabolic inhibition. Circ Res 88:181–187PubMedCrossRefGoogle Scholar
  137. Pacher P, Thomas AP, Hajnoczky G (2002) Ca2+ marks: miniature calcium signals in single mitochondria driven by ryanodine receptors. Proc Natl Acad Sci U S A 99:2380–2385PubMedPubMedCentralCrossRefGoogle Scholar
  138. Palty R, Silverman WF, Hershfinkel M et al (2010) NCLX is an essential component of mitochondrial Na+/Ca2+ exchange. Proc Natl Acad Sci U S A 107:436–441PubMedCrossRefGoogle Scholar
  139. Parks C, Alam MA, Sullivan R, Mancarella S (2016) STIM1-dependent Ca(2+) microdomains are required for myofilament remodeling and signaling in the heart. Sci Rep 6:25372PubMedPubMedCentralCrossRefGoogle Scholar
  140. Pessah IN, Waterhouse AL, Casida JE (1985) The calcium-ryanodine receptor complex of skeletal and cardiac muscle. Biochem Biophys Res Commun 128:449–456PubMedCrossRefGoogle Scholar
  141. Petroff MG, Kim SH, Pepe S et al (2001) Endogenous nitric oxide mechanisms mediate the stretch dependence of Ca2+ release in cardiomyocytes. Nat Cell Biol 3:867–873PubMedCrossRefGoogle Scholar
  142. Pinali C, Bennett H, Davenport JB et al (2013) Three-dimensional reconstruction of cardiac sarcoplasmic reticulum reveals a continuous network linking transverse-tubules: this organization is perturbed in heart failure. Circ Res 113:1219–1230PubMedCrossRefGoogle Scholar
  143. Poteser M, Schleifer H, Lichtenegger M et al (2011) PKC-dependent coupling of calcium permeation through transient receptor potential canonical 3 (TRPC3) to calcineurin signaling in HL-1 myocytes. Proc Natl Acad Sci U S A 108:10556–10561PubMedPubMedCentralCrossRefGoogle Scholar
  144. Prosser BL, Ward CW, Lederer WJ (2011) X-ROS signaling: rapid mechano-chemo transduction in heart. Science 333:1440–1445PubMedCrossRefGoogle Scholar
  145. Reiken S, Gaburjakova M, Guatimosim S et al (2003) Protein kinase a phosphorylation of the cardiac calcium release channel (ryanodine receptor) in normal and failing hearts - role of phosphatases and response to isoproterenol. J Biol Chem 278:444–453PubMedCrossRefGoogle Scholar
  146. Ringer S (1883) A further contribution regarding the influence of the different constituents of the blood on the contraction of the heart. J Physiol 4(29–42):23Google Scholar
  147. Rizzuto R, Pozzan T (2006) Microdomains of intracellular Ca2+: molecular determinants and functional consequences. Physiol Rev 86:369–408PubMedCrossRefGoogle Scholar
  148. 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 262:744–747PubMedCrossRefGoogle Scholar
  149. Robert V, Gurlini P, Tosello V et al (2001) Beat-to-beat oscillations of mitochondrial [Ca2+] in cardiac cells. EMBO J 20:4998–5007PubMedPubMedCentralCrossRefGoogle Scholar
  150. Rodriguez P, Bhogal MS, Colyer J (2003) Stoichiometric phosphorylation of cardiac ryanodine receptor on serine 2809 by calmodulin-dependent kinase II and protein kinase a. J Biol Chem 278:38593–38600PubMedCrossRefGoogle Scholar
  151. Ronkainen JJ, Hanninen SL, Korhonen T et al (2011) Ca2 + −calmodulin-dependent protein kinase II represses cardiac transcription of the L-type calcium channel alpha(1C)-subunit gene (Cacna1c) by DREAM translocation. J Physiol 589:2669–2686PubMedPubMedCentralCrossRefGoogle Scholar
  152. Ruiz-Hurtado G, Li L, Fernández-Velasco M et al (2015) Reconciling depressed Ca2+ sparks occurrence with enhanced RyR2 activity in failing mice cardiomyocytes. J Gen Physiol 146(4):295–306PubMedPubMedCentralCrossRefGoogle Scholar
  153. Sag CM, Kohler AC, Anderson ME et al (2011) CaMKII-dependent SR Ca leak contributes to doxorubicin-induced impaired Ca handling in isolated cardiac myocytes. J Mol Cell Cardiol 51:749–759PubMedPubMedCentralCrossRefGoogle Scholar
  154. Sancak Y, Markhard AL, Kitami T et al (2013) EMRE is an essential component of the mitochondrial calcium uniporter complex. Science 342:1379–1382PubMedPubMedCentralCrossRefGoogle Scholar
  155. Santana LF, Cheng H, Gómez AM et al (1996) Relation between the sarcolemmal Ca2+ current and Ca2+ sparks and local control theories for cardiac excitation-contraction coupling. Circ Res 78:166–171PubMedCrossRefGoogle Scholar
  156. Saris NE, Allshire A (1989) Calcium ion transport in mitochondria. Methods Enzymol 174:68–85PubMedCrossRefGoogle Scholar
  157. Sasaki N, Mitsuiye T, Noma A (1992) Effects of mechanical stretch on membrane currents of single ventricular myocytes of Guinea-pig heart. Jpn J Physiol 42:957–970PubMedCrossRefGoogle Scholar
  158. Saucerman JJ, Bers DM (2012) Calmodulin binding proteins provide domains of local Ca2+ signaling in cardiac myocytes. J Mol Cell Cardiol 52:312–316PubMedCrossRefGoogle Scholar
  159. Shah SJ, Aistrup GL, Gupta DK et al (2014) Ultrastructural and cellular basis for the development of abnormal myocardial mechanics during the transition from hypertension to heart failure. Am J Physiol Heart Circ Physiol 306:H88–100PubMedCrossRefGoogle Scholar
  160. Sham JS (1997) Ca2+ release-induced inactivation of Ca2+ current in rat ventricular myocytes: evidence for local Ca2+ signalling. J Physiol 500(Pt 2):285–295PubMedPubMedCentralCrossRefGoogle Scholar
  161. Shang W, Lu F, Sun T et al (2014) Imaging Ca2+ nanosparks in heart with a new targeted biosensor. Circ Res 114:412–420PubMedCrossRefGoogle Scholar
  162. Sharma VK, Ramesh V, Franzini-Armstrong C, Sheu SS (2000) Transport of Ca2+ from sarcoplasmic reticulum to mitochondria in rat ventricular myocytes. J Bioenerg Biomembr 32:97–104PubMedCrossRefGoogle Scholar
  163. Sparagna GC, Gunter KK, Sheu SS, Gunter TE (1995) Mitochondrial calcium uptake from physiological-type pulses of calcium. A description of the rapid uptake mode. J Biol Chem 270:27510–27515PubMedCrossRefGoogle Scholar
  164. Stange M, Xu L, Balshaw D et al (2003) Characterization of recombinant skeletal muscle (Ser-2843) and cardiac muscle (Ser-2809) ryanodine receptor phosphorylation mutants. J Biol Chem 278:51693–51702PubMedCrossRefGoogle Scholar
  165. Stern MD (1992) Theory of excitation-contraction coupling in cardiac muscle. Biophys J 63:497–517PubMedPubMedCentralCrossRefGoogle Scholar
  166. Suarez J, Belke DD, Gloss B et al (2004) In vivo adenoviral transfer of sorcin reverses the cardiac contractile abnormalities of diabetic cardiomyopathy. Am J Physiol Heart Circ Physiol 286:H68–H75PubMedCrossRefGoogle Scholar
  167. Szabadkai G, Bianchi K, Varnai P et al (2006) Chaperone-mediated coupling of endoplasmic reticulum and mitochondrial Ca2+ channels. J Cell Biol 175:901–911PubMedPubMedCentralCrossRefGoogle Scholar
  168. Tandan S, Wang Y, Wang TT et al (2009) Physical and functional interaction between calcineurin and the cardiac L-type Ca2+ channel. Circ Res 105:51–60PubMedPubMedCentralCrossRefGoogle Scholar
  169. Tanskanen AJ, Greenstein JL, Chen A et al (2007) Protein geometry and placement in the cardiac dyad influence macroscopic properties of calcium-induced calcium release. Biophys J 92:3379–3396PubMedPubMedCentralCrossRefGoogle Scholar
  170. Terentyev D, Gyorke I, Belevych AE et al (2008) Redox modification of ryanodine receptors contributes to sarcoplasmic reticulum Ca2+ leak in chronic heart failure. Circ Res 103:1466–1472PubMedPubMedCentralCrossRefGoogle Scholar
  171. Territo PR, Mootha VK, French SA, Balaban RS (2000) Ca(2+) activation of heart mitochondrial oxidative phosphorylation: role of the F(0)/F(1)-ATPase. Am J Physiol Cell Physiol 278:C423–C435PubMedCrossRefGoogle Scholar
  172. Timerman AP, Onoue H, Xin HB et al (1996) Selective binding of FKBP12.6 by the cardiac ryanodine receptor. J Biol Chem 271:20385–20391PubMedCrossRefGoogle Scholar
  173. Trafford AW, Diaz ME, Sibbring GC, Eisner DA (2000) Modulation of CICR has no maintained effect on systolic Ca2+: simultaneous measurements of sarcoplasmic reticulum and sarcolemmal Ca2+ fluxes in rat ventricular myocytes. J Physiol 522(Pt 2):259–270PubMedPubMedCentralCrossRefGoogle Scholar
  174. Trollinger DR, Cascio WE, Lemasters JJ (1997) Selective loading of Rhod 2 into mitochondria shows mitochondrial Ca2+ transients during the contractile cycle in adult rabbit cardiac myocytes. Biochem Biophys Res Commun 236:738–742PubMedCrossRefGoogle Scholar
  175. Ullrich ND, Valdivia HH, Niggli E (2012) PKA phosphorylation of cardiac ryanodine receptor modulates SR luminal Ca2+ sensitivity. J Mol Cell Cardiol 53:33–42PubMedPubMedCentralCrossRefGoogle Scholar
  176. Vais H, Mallilankaraman K, Mak DO et al (2016) EMRE is a matrix Ca(2+) sensor that governs gatekeeping of the mitochondrial Ca(2+) uniporter. Cell Rep 14:403–410PubMedPubMedCentralCrossRefGoogle Scholar
  177. Valdivia HH (1998) Modulation of intracellular Ca2+ levels in the heart by sorcin and FKBP12, two accessory proteins of ryanodine receptors. Trends Pharmacol Sci 19:479–482PubMedCrossRefGoogle Scholar
  178. Valdivia HH (2012) Ryanodine receptor phosphorylation and heart failure: phasing out S2808 and “criminalizing” S2814. Circ Res 110:1398–1402PubMedPubMedCentralCrossRefGoogle Scholar
  179. Valdivia HH, Kaplan JH, Ellis-Davies GC, Lederer WJ (1995) Rapid adaptation of cardiac ryanodine receptors: modulation by Mg2+ and phosphorylation. Science 267:1997–2000PubMedPubMedCentralCrossRefGoogle Scholar
  180. Vinet L, Pezet M, Bito V et al (2012) Cardiac FKBP12.6 overexpression protects against triggered ventricular tachycardia in pressure overloaded mouse hearts. Basic Res Cardiol 107:246PubMedCrossRefGoogle Scholar
  181. Viola HM, Hool LC (2011) Targeting calcium and the mitochondria in prevention of pathology in the heart. Curr Drug Targets 12:748–760PubMedCrossRefGoogle Scholar
  182. Viola HM, Hool LC (2013) Role of the cytoskeleton in communication between L-type Ca(2+) channels and mitochondria. Clin Exp Pharmacol Physiol 40:295–304PubMedCrossRefGoogle Scholar
  183. Viola HM, Hool LC (2014) How does calcium regulate mitochondrial energetics in the heart?—new insights. Heart Lung Circ 23:602–609PubMedCrossRefGoogle Scholar
  184. Viola HM, Arthur PG, Hool LC (2007) Transient exposure to hydrogen peroxide causes an increase in mitochondria-derived superoxide as a result of sustained alteration in L-type Ca2+ channel function in the absence of apoptosis in ventricular myocytes. Circ Res 100:1036–1044PubMedCrossRefGoogle Scholar
  185. Viola HM, Arthur PG, Hool LC (2009) Evidence for regulation of mitochondrial function by the L-type Ca2+ channel in ventricular myocytes. J Mol Cell Cardiol 46:1016–1026PubMedCrossRefGoogle Scholar
  186. Viola HM, Davies SM, Filipovska A, Hool LC (2013) L-type Ca(2+) channel contributes to alterations in mitochondrial calcium handling in the mdx ventricular myocyte. Am J Physiol Heart Circ Physiol 304:H767–H775PubMedCrossRefGoogle Scholar
  187. Vlahos CJ, McDowell SA, Clerk A (2003) Kinases as therapeutic targets for heart failure. Nat Rev Drug Discov 2:99–113PubMedCrossRefGoogle Scholar
  188. Wang SQ, Song LS, Lakatta EG, Cheng H (2001) Ca2+ signalling between single L-type Ca2+ channels and ryanodine receptors in heart cells. Nature 410:592–596PubMedCrossRefGoogle Scholar
  189. Watanabe H, Chopra N, Laver D et al (2009) Flecainide prevents catecholaminergic polymorphic ventricular tachycardia in mice and humans. Nat Med 15:380–383PubMedPubMedCentralCrossRefGoogle Scholar
  190. Wehrens XH, Lehnart SE, Reiken SR et al (2004) Protection from cardiac arrhythmia through ryanodine receptor-stabilizing protein calstabin2. Science 304:292–296PubMedCrossRefGoogle Scholar
  191. Wehrens XH, Lehnart SE, Marks AR (2005) Intracellular calcium release and cardiac disease. Annu Rev Physiol 67:69–98PubMedCrossRefGoogle Scholar
  192. Wheeler DG, Barrett CF, Groth RD et al (2008) CaMKII locally encodes L-type channel activity to signal to nuclear CREB in excitation-transcription coupling. J Cell Biol 183:849–863PubMedPubMedCentralCrossRefGoogle Scholar
  193. Williams GS, Boyman L, Chikando AC et al (2013) Mitochondrial calcium uptake. Proc Natl Acad Sci U S A 110:10479–10486PubMedPubMedCentralCrossRefGoogle Scholar
  194. Wu X, Bers DM (2007) Free and bound intracellular calmodulin measurements in cardiac myocytes. Cell Calcium 41:353–364PubMedCrossRefGoogle Scholar
  195. Wu X, Eder P, Chang B, Molkentin JD (2010) TRPC channels are necessary mediators of pathologic cardiac hypertrophy. Proc Natl Acad Sci U S A 107:7000–7005PubMedPubMedCentralCrossRefGoogle Scholar
  196. Xiao RP, Valdivia HH, Bogdanov K et al (1997) The immunophilin FK506-binding protein modulates Ca2+ release channel closure in rat heart. J Physiol Lond 500:343–354PubMedPubMedCentralCrossRefGoogle Scholar
  197. Xiao B, Sutherland C, Walsh MP, Chen SR (2004) Protein kinase a phosphorylation at serine-2808 of the cardiac Ca2 + −release channel (ryanodine receptor) does not dissociate 12.6-kDa FK506-binding protein (FKBP12.6). Circ Res 94:487–495PubMedCrossRefGoogle Scholar
  198. Xiao J, Tian X, Jones PP et al (2007) Removal of FKBP12.6 does not alter the conductance and activation of the cardiac ryanodine receptor or the susceptibility to stress-induced ventricular arrhythmias. J Biol Chem 282:34828–34838PubMedPubMedCentralCrossRefGoogle Scholar
  199. Xu L, Mann G, Meissner G (1996) Regulation of cardiac Ca2+ release channel (ryanodine receptor) by Ca2+, H+, Mg2+, and adenine nucleotides under normal and simulated ischemic conditions. Circ Res 79:1100–1109PubMedCrossRefGoogle Scholar
  200. Xu L, Eu JP, Meissner G, Stamler JS (1998) Activation of the cardiac calcium release channel (ryanodine receptor) by poly-S-nitrosylation. Science 279:234–237PubMedCrossRefGoogle Scholar
  201. Yano M, Ono K, Ohkusa T et al (2000) Altered stoichiometry of FKBP12.6 versus ryanodine receptor as a cause of abnormal Ca(2+) leak through ryanodine receptor in heart failure. Circulation 102:2131–2136PubMedCrossRefGoogle Scholar
  202. Yano M, Yamamoto T, Ikeda Y, Matsuzaki M (2006) Mechanisms of disease: ryanodine receptor defects in heart failure and fatal arrhythmia. Nat Clin Pract Cardiovasc Med 3:43–52PubMedCrossRefGoogle Scholar
  203. Zamparelli C, Ilari A, Verzili D et al (2000) Structure-function relationships in sorcin, a member of the penta EF-hand family. Interaction of sorcin fragments with the ryanodine receptor and an Escherichia coli model system. Biochemistry 39:658–666PubMedCrossRefGoogle Scholar
  204. Zhang YH, Youm JB, Sung HK et al (2000) Stretch-activated and background non-selective cation channels in rat atrial myocytes. J Physiol 523(Pt 3):607–619PubMedPubMedCentralCrossRefGoogle Scholar
  205. Zhang H, Makarewich CA, Kubo H et al (2012) Hyperphosphorylation of the cardiac ryanodine receptor at serine 2808 is not involved in cardiac dysfunction after myocardial infarction. Circ Res 110:831–840PubMedPubMedCentralCrossRefGoogle Scholar
  206. Zhang HL, Gómez AM, Wang XH et al (2013) ROS regulation of microdomain Ca2+ signalling at the dyads. Cardiovasc Res 98:248–258PubMedCrossRefGoogle Scholar
  207. Zhao YT, Valdivia CR, Gurrola GB et al (2015) Arrhythmogenesis in a catecholaminergic polymorphic ventricular tachycardia mutation that depresses ryanodine receptor function. Proc Natl Acad Sci U S A 112:E1669–E1677PubMedPubMedCentralCrossRefGoogle Scholar
  208. Zima AV, Bovo E, Mazurek SR et al (2014) Ca handling during excitation-contraction coupling in heart failure. Pflugers Arch 466:1129–1137PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  • A. M. Gómez
    • 1
  • T. R. R. Mesquita
    • 1
  • J. J. Mercadier
    • 1
    • 2
  • J. L. Álvarez
    • 1
    • 3
  • J. P. Benitah
    • 1
  1. 1.Inserm, UMR-S 1180, Univ. Paris-Sud, Université Paris-SaclayChâtenay-MalabryFrance
  2. 2.Univ. Paris Diderot, Sorbonne Paris Cité and Assistance Publique—Hôpitaux de ParisParisFrance
  3. 3.Laboratorio de Electrofisiología, Instituto de Cardiología y Cirugía CardiovascularLa HabanaCuba

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