Calmodulin in a Heartbeat

FEBS Journal

Volumn 280, Issue 21, 2013, Pages 5511-5532

  Sorensen, Anders B ^a   Søndergaard, Mads T ^a   Overgaard, Michael T ^a  

^a AALBORG UNIVERSITY   (Denmark)

Author keywords

arrhythmia; calcium signalling; calmodulin; cardiomyocyte; disease mutation

Indexed keywords

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CALCIUM ION; CALMODULIN; CYCLIC NUCLEOTIDE GATED CHANNEL; RYANODINE RECEPTOR 2; SODIUM CHANNEL NAV1.5; VOLTAGE GATED CALCIUM CHANNEL; VOLTAGE GATED POTASSIUM CHANNEL;

ADRENERGIC SYSTEM; ALLELE; ARRHYTHMOGENESIS; BIOACCUMULATION; CALCIUM CELL LEVEL; CALCIUM HOMEOSTASIS; CALCIUM SIGNALING; CALCIUM TRANSPORT; CALM GENE; CARBOXY TERMINAL SEQUENCE; CATECHOLAMINERGIC POLYMORPHIC VENTRICULAR TACHYCARDIA; CONFERENCE PAPER; DISEASE SEVERITY; DOMINANT INHERITANCE; EUKARYOTIC CELL; GENE MUTATION; GENETIC DISORDER; HEART ARREST; HEART ARRHYTHMIA; HEART BEAT; HEART CONTRACTION; HEART DEPOLARIZATION; HEART ELECTROPHYSIOLOGY; HEART MUSCLE CELL; HEART MUSCLE POTENTIAL; HUMAN; HUMAN GENOME; LONG QT SYNDROME; NONHUMAN; PHENOTYPE; POTASSIUM CURRENT; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; SECOND MESSENGER; SIGNAL TRANSDUCTION; SUDDEN CARDIAC DEATH; SYMPTOM; VERTEBRATE;

ARRHYTHMIA; CALCIUM SIGNALLING; CALMODULIN; CARDIOMYOCYTE; DISEASE MUTATION;

ANIMALS; ARRHYTHMIAS, CARDIAC; CALCIUM; CALMODULIN; HUMANS; MUSCLE CONTRACTION; MUTATION;

EUKARYOTA; VERTEBRATA;

EID: 84886089376     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.12337     Document Type: Conference Paper

References (169)

1. Berridge MJ, Bootman MD, &, Roderick HL, (2003) Calcium signaling: dynamics, homeostasis and remodelling. Nat Rev Mol Cell Biol 4, 517-529.
2. Clapham DE, (2007) Calcium signaling. Cell 131, 1047-1058.
3. O'Neil KT, &, DeGrado WF, (1990) How calmodulin binds its targets: sequence independent recognition of amphiphilic alpha-helices. Trends Biochem Sci 15, 59-64.
4. Friedberg F, &, Rhoads AR, (2001) Evolutionary aspects of calmodulin. IUBMB Life 51, 215-221.
5. Abzhanov A, Kuo WP, Hartmann C, Grant BR, Grant PR, &, Tabin CJ, (2006) The calmodulin pathway and evolution of elongated beak morphology in Darwin's finches. Nature 442, 563-567.
6. Linse S, Helmersson A, &, Forsén S, (1991) Calcium binding to calmodulin and its globular domains. J Biol Chem 266, 8050-8054.
7. VanScyoc WS, Sorensen BR, Rusinova E, Laws WR, Ross JBA, &, Shea MA, (2002) Calcium binding to calmodulin mutants monitored by domain-specific intrinsic phenylalanine and tyrosine fluorescence. Biophys J 83, 2767-2780.
8. Zhang M, Abrams C, Wang L, Gizzi A, He L, Lin R, Chen Y, Loll PJ, Pascal JM, &, Zhang J-F, (2012) Structural basis for calmodulin as a dynamic calcium sensor. Structure 20, 911-923.
9. Tidow H, Poulsen LR, Andreeva A, Knudsen M, Hein KL, Wiuf C, Palmgren MG, &, Nissen P, (2012) A bimodular mechanism of calcium control in eukaryotes. Nature 491, 468-472.
10. 2+ channel. Cell 133, 1228-1240.
11. Yamniuk AP, &, Vogel HJ, (2004) Calmodulin's flexibility allows for promiscuity in its interactions with target proteins and peptides. Mol Biotechnol 27, 33-57.
12. Hoeflich KP, &, Ikura M, (2002) Calmodulin in action: diversity in target recognition and activation mechanisms. Cell 108, 739-742.
13. Vogel HJ, (1994) The Merck Frosst Award Lecture 1994. Calmodulin: a versatile calcium mediator protein. Biochem Cell Biol 72, 357-376.
14. Chin D, &, Means AR, (2000) Calmodulin: a prototypical calcium sensor. Trends Cell Biol 10, 322-328.
15. Yap KL, Kim J, Truong K, Sherman M, Yuan T, &, Ikura M, (2000) Calmodulin target database. J Struct Funct Genomics 1, 8-14.
16. Persechini A, &, Stemmer PM, (2002) Calmodulin is a limiting factor in the cell. Trends Cardiovasc Med 12, 32-37.
17. 2+ signaling in cardiac myocytes. J Mol Cell Cardiol 52, 312-316.
18. Toutenhoofd SL, &, Strehler EE, (2000) The calmodulin multigene family as a unique case of genetic redundancy: multiple levels of regulation to provide spatial and temporal control of calmodulin pools? Cell Calcium 28, 83-96.
19. Nyegaard M, Overgaard MT, Søndergaard MT, Vranas M, Behr ER, Hildebrandt LL, Lund J, Hedley PL, Camm AJ, Wettrell G, et al,. (2012) Mutations in calmodulin cause ventricular tachycardia and sudden cardiac death. Am J Hum Genet 91, 703-712.
20. Crotti L, Johnson CN, Graf E, De Ferrari GM, Cuneo BF, Ovadia M, Papagiannis J, Feldkamp MD, Rathi SG, Kunic JD, et al,. (2013) Calmodulin mutations associated with recurrent cardiac arrest in infants. Circulation 127, 1009-1017.
21. Tang W, Sencer S, &, Hamilton SL, (2002) Calmodulin modulation of proteins involved in excitation-contraction coupling. Front Biosci 7, d1583-d1589.
22. Pitt GS, (2007) Calmodulin and CaMKII as molecular switches for cardiac ion channels. Cardiovasc Res 73, 641-647.
23. Grant AO, (2009) Cardiac ion channels. Circ Arrhythm Electrophysiol 2, 185-194.
24. Amin AS, Tan HL, &, Wilde AAM, (2010) Cardiac ion channels in health and disease. Heart Rhythm 7, 117-126.
25. Klabunde R, (2011) Cardiovascular Physiology Concepts. Lippincott Williams & Wilkins, Philadelphia.
26. Nerbonne JM, &, Kass RS, (2005) Molecular physiology of cardiac repolarization. Physiol Rev 85, 1205-1253.
27. Noble D, &, Noble PJ, (2006) Late sodium current in the pathophysiology of cardiovascular disease: consequences of sodium-calcium overload. Heart 92 (Suppl 4), iv1-iv5.
28. Fearnley CJ, Roderick HL, &, Bootman MD, (2011) Calcium signaling in cardiac myocytes. Cold Spring Harb Perspect Biol 3, a004242.
29. Giudicessi JR, &, Ackerman MJ, (2012) Potassium-channel mutations and cardiac arrhythmias-diagnosis and therapy. Nat Rev Cardiol 9, 319-332.
30. Abriel H, (2010) Cardiac sodium channel Na(v)1.5 and interacting proteins: physiology and pathophysiology. J Mol Cell Cardiol 48, 2-11.
31. Catterall WA, (2000) From ionic currents to molecular mechanisms: the structure and function of voltage-gated sodium channels. Neuron 26, 13-25.
32. Rook MB, Evers MM, Vos MA, &, Bierhuizen MFA, (2012) Biology of cardiac sodium channel Nav1.5 expression. Cardiovasc Res 93, 12-23.
33. Ruan Y, Liu N, &, Priori SG, (2009) Sodium channel mutations and arrhythmias. Nat Rev Cardiol 6, 337-348.
34. West JW, Patton DE, Scheuer T, Wang Y, Goldin AL, &, Catterall WA, (1992) A cluster of hydrophobic amino acid residues required for fast Na(+)-channel inactivation. PNAS 89, 10910-10914.
35. Ulbricht W, (2005) Sodium channel inactivation: molecular determinants and modulation. Physiol Rev 85, 1271-1301.
36. Sarhan MF, Van Petegem F, &, Ahern CA, (2009) A double tyrosine motif in the cardiac sodium channel domain III-IV linker couples calcium-dependent calmodulin binding to inactivation gating. J Biol Chem 284, 33265-33274.
37. Tan HL, Kupershmidt S, Zhang R, Stepanovic S, Roden DM, Wilde AAM, Anderson ME, &, Balser JR, (2002) A calcium sensor in the sodium channel modulates cardiac excitability. Nature 415, 442-447.
38. Wingo TL, Shah VN, Anderson ME, Lybrand TP, Chazin WJ, &, Balser JR, (2004) An EF-hand in the sodium channel couples intracellular calcium to cardiac excitability. Nat Struct Mol Biol 11, 219-225.
39. Young KA, &, Caldwell JH, (2005) Modulation of skeletal and cardiac voltage-gated sodium channels by calmodulin. J Physiol (London) 565, 349-370.
40. Biswas S, DiSilvestre D, Tian Y, Halperin VL, &, Tomaselli GF, (2009) Calcium-mediated dual-mode regulation of cardiac sodium channel gating. Circ Res 104, 870-878.
41. Maier LS, (2012) Ca(2+)/calmodulin-dependent protein kinase II (CaMKII) in the heart. Adv Exp Med Biol 740, 685-702.
42. Potet F, Chagot B, Anghelescu M, Viswanathan PC, Stepanovic SZ, Kupershmidt S, Chazin WJ, &, Balser JR, (2009) Functional interactions between distinct sodium channel cytoplasmic domains through the action of calmodulin. J Biol Chem 284, 8846-8854.
43. Chagot B, &, Chazin WJ, (2011) Solution NMR structure of Apo-calmodulin in complex with the IQ motif of human cardiac sodium channel NaV1.5. J Mol Biol 406, 106-119.
44. Sarhan MF, Tung C-C, Van Petegem F, &, Ahern CA, (2012) Crystallographic basis for calcium regulation of sodium channels. PNAS 109, 3558-3563.
45. Wang C, Chung BC, Yan H, Lee S-Y, &, Pitt GS, (2012) Crystal structure of the ternary complex of a NaV C-terminal domain, a fibroblast growth factor homologous factor, and calmodulin. Structure 20, 1167-1176.
46. Splawski I, Shen J, Timothy KW, Lehmann MH, Priori S, Robinson JL, Moss AJ, Schwartz PJ, Towbin JA, Vincent GM, et al,. (2000) Spectrum of mutations in long-QT syndrome genes. KVLQT1, HERG, SCN5A, KCNE1, and KCNE2. Circulation 102, 1178-1185.
47. Grant AO, Carboni MP, Neplioueva V, Starmer CF, Memmi M, Napolitano C, &, Priori S, (2002) Long QT syndrome, Brugada syndrome, and conduction system disease are linked to a single sodium channel mutation. J Clin Invest 110, 1201-1209.
48. Smits JPP, Eckardt L, Probst V, Bezzina CR, Schott JJ, Remme CA, Haverkamp W, Breithardt G, Escande D, Schulze-Bahr E, et al,. (2002) Genotype-phenotype relationship in Brugada syndrome: electrocardiographic features differentiate SCN5A-related patients from non-SCN5A-related patients. J Am Coll Cardiol 40, 350-356.
49. Napolitano C, Priori SG, Schwartz PJ, Bloise R, Ronchetti E, Nastoli J, Bottelli G, Cerrone M, &, Leonardi S, (2005) Genetic testing in the long QT syndrome: development and validation of an efficient approach to genotyping in clinical practice. JAMA 294, 2975-2980.
50. + channels. J Clin Invest 116, 3127-3138.
51. + channel in rat ventricular myocytes. J Mol Cell Cardiol 47, 475-484.
52. 2+/calmodulin-dependent protein kinase II in guinea-pig ventricular myocytes. Cardiovasc Res 85, 454-463.
53. Shy D, Gillet L, &, Abriel H, (2012) Cardiac sodium channel Na(V)1.5 distribution in myocytes via interacting proteins: the multiple pool model. Biochim Biophys Acta. 1833, 886-894.
54. Niwa N, &, Nerbonne JM, (2010) Molecular determinants of cardiac transient outward potassium current (I(to)) expression and regulation. J Mol Cell Cardiol 48, 12-25.
55. An WF, Bowlby MR, Betty M, Cao J, Ling HP, Mendoza G, Hinson JW, Mattsson KI, Strassle BW, Trimmer JS, et al,. (2000) Modulation of A-type potassium channels by a family of calcium sensors. Nature 403, 553-556.
56. Ghosh S, Nunziato DA, &, Pitt GS, (2006) KCNQ1 assembly and function is blocked by long-QT syndrome mutations that disrupt interaction with calmodulin. Circ Res 98, 1048-1054.
57. Shamgar L, Ma L, Schmitt N, Haitin Y, Peretz A, Wiener R, Hirsch J, Pongs O, &, Attali B, (2006) Calmodulin is essential for cardiac IKS channel gating and assembly: impaired function in long-QT mutations. Circ Res 98, 1055-1063.
58. Tang Q, Jin M-W, Xiang J-Z, Dong M-Q, Sun H-Y, Lau C-P, &, Li G-R, (2007) The membrane permeable calcium chelator BAPTA-AM directly blocks human ether a-go-go-related gene potassium channels stably expressed in HEK 293 cells. Biochem Pharmacol 74, 1596-1607.
59. Yus-Najera E, Santana-Castro I, &, Villarroel A, (2002) The identification and characterization of a noncontinuous calmodulin-binding site in noninactivating voltage-dependent KCNQ potassium channels. J Biol Chem 277, 28545-28553.
60. Benitah J-P, Alvarez JL, &, Gõmez AM, (2010) L-type Ca(2+) current in ventricular cardiomyocytes. J Mol Cell Cardiol 48, 26-36.
61. Bodi I, Mikala G, Koch SE, Akhter SA, &, Schwartz A, (2005) The L-type calcium channel in the heart: the beat goes on. J Clin Invest 115, 3306-3317.
62. Catterall WA, (2011) Voltage-gated calcium channels. Cold Spring Harb Perspect Biol 3, a003947.
63. Venetucci L, Denegri M, Napolitano C, &, Priori SG, (2012) Inherited calcium channelopathies in the pathophysiology of arrhythmias. Nat Rev Cardiol 9, 561-575.
64. Findlay I, Suzuki S, Murakami S, &, Kurachi Y, (2008) Physiological modulation of voltage-dependent inactivation in the cardiac muscle L-type calcium channel: a modelling study. Prog Biophys Mol Biol 96, 482-498.
65. 2+ channels in the heart: structure and regulation. Medicina (Kaunas) 44, 491-499.
66. 2+ channels by calmodulin. Sci STKE 2005, re15.
67. 2+-dependent inactivation are modified by mutation of the Ca(v)1.2 channel IQ motif. J Biol Chem 286, 26702-26707.
68. 2+ calmodulin-binding sites on the CaV1.2 channel. Biophys J 85, 1538-1547.
69. 2+/calmodulin complex. Nat Struct Mol Biol 12, 1108-1115.
70. Nie H-G, Hao L-Y, Xu J-J, Minobe E, Kameyama A, &, Kameyama M, (2007) Distinct roles of CaM and Ca(2+)/CaM-dependent protein kinase II in Ca(2+)-dependent facilitation and inactivation of cardiac L-type Ca(2+) channels. J Physiol Sci 57, 167-173.
71. 2+ selectivity in the calmodulin regulation of CaV channels. Nature 451, 830-834.
72. Minor DL, &, Findeisen F, (2010) Progress in the structural understanding of voltage-gated calcium channel (CaV) function and modulation. Channels (Austin) 4, 459-474.
73. 2+ channels. Biochim Biophys Acta 1820, 1243-1252.
74. Evans TIA, Hell JW, &, Shea MA, (2011) Thermodynamic linkage between calmodulin domains binding calcium and contiguous sites in the C-terminal tail of Ca(V)1.2. Biophys Chem 159, 172-187.
75. 2+ channel CaM preassociation. Neuron 39, 97-107.
76. Kim EY, Rumpf CH, Van Petegem F, Arant RJ, Findeisen F, Cooley ES, Isacoff EY, &, Minor DL, (2010) Multiple C-terminal tail Ca(2+)/CaMs regulate Ca(V)1.2 function but do not mediate channel dimerization. EMBO J 29, 3924-3938.
77. 2+ channels. J Pharmacol Sci 112, 397-404.
78. 2+ channels. J Biol Chem 276, 30794-30802.
79. 2+ channels. Science 304, 432-435.
80. Wang W-Y, Hao L-Y, Minobe E, Saud ZA, Han D-Y, &, Kameyama M, (2009) CaMKII phosphorylates a threonine residue in the C-terminal tail of Cav1.2 Ca(2+) channel and modulates the interaction of the channel with calmodulin. J Physiol Sci 59, 283-290.
81. Houdusse A, Gaucher J-F, Krementsova E, Mui S, Trybus KM, &, Cohen C, (2006) Crystal structure of apo-calmodulin bound to the first two IQ motifs of myosin V reveals essential recognition features. PNAS 103, 19326-19331.
82. Liu Z, &, Vogel HJ, (2012) Structural basis for the regulation of L-type voltage-gated calcium channels: interactions between the N-terminal cytoplasmic domain and Ca(2+)-calmodulin. Front Mol Neurosci 5, 38.
83. 2+ signals for facilitation. J Cell Biol 171, 537-547.
84. 2+ channel facilitation mediated by phosphorylation of the beta subunit by CaMKII. Mol Cell 23, 641-650.
85. Lee T-S, Karl R, Moosmang S, Lenhardt P, Klugbauer N, Hofmann F, Kleppisch T, &, Welling A, (2006) Calmodulin kinase II is involved in voltage-dependent facilitation of the L-type Cav1.2 calcium channel: identification of the phosphorylation sites. J Biol Chem 281, 25560-25567.
86. Blaich A, Welling A, Fischer S, Wegener JW, Köstner K, Hofmann F, &, Moosmang S, (2010) Facilitation of murine cardiac L-type Ca(v)1.2 channel is modulated by calmodulin kinase II-dependent phosphorylation of S1512 and S1570. PNAS 107, 10285-10289.
87. 2+ channels. Cardiovasc Res 65, 28-39.
88. De Jongh KS, Murphy BJ, Colvin AA, Hell JW, Takahashi M, &, Catterall WA, (1996) Specific phosphorylation of a site in the full-length form of the alpha 1 subunit of the cardiac L-type calcium channel by adenosine 3′,5′-cyclic monophosphate-dependent protein kinase. Biochemistry 35, 10392-10402.
89. Haase H, Bartel S, Karczewski P, Morano I, &, Krause EG, (1996) In-vivo phosphorylation of the cardiac L-type calcium channel beta-subunit in response to catecholamines. Mol Cell Biochem 163-164, 99-106.
90. Puri TS, Gerhardstein BL, Zhao XL, Ladner MB, &, Hosey MM, (1997) Differential effects of subunit interactions on protein kinase A- and C-mediated phosphorylation of L-type calcium channels. Biochemistry 36, 9605-9615.
91. Langer GA, &, Peskoff A, (1996) Calcium concentration and movement in the diadic cleft space of the cardiac ventricular cell. Biophys J 70, 1169-1182.
92. 2+ signaling in the heart. J Cell Sci 122, 1005-1013.
93. Yu Z, Holst MJ, Hayashi T, Bajaj CL, Ellisman MH, McCammon JA, &, Hoshijima M, (2008) Three-dimensional geometric modeling of membrane-bound organelles in ventricular myocytes: bridging the gap between microscopic imaging and mathematical simulation. J Struct Biol 164, 304-313.
94. Bers DM, (2008) Calcium cycling and signaling in cardiac myocytes. Annu Rev Physiol 70, 23-49.
95. Bers DM, (2002) Cardiac excitation-contraction coupling. Nature 415, 198-205.
96. Cheng H, &, Lederer WJ, (2008) Calcium sparks. Physiol Rev 88, 1491-1545.
97. Bers DM, (2000) Calcium fluxes involved in control of cardiac myocyte contraction. Circ Res 87, 275-281.
98. 2+ release channel (ryanodine receptor) of rabbit skeletal muscle sarcoplasmic reticulum. J Biol Chem 269, 22698-22704.
99. Van Petegem F, (2012) Ryanodine receptors: structure and function. J Biol Chem 287, 31624-31632.
100. Liu Z, &, Wagenknecht T, (2005) Three-Dimensional Reconstruction of Ryanodine Receptors. In Ryanodine Receptors (Wehrens XH & Marks AR, eds), pp. 25-34, Springer, New York.
101. Kimlicka L, &, Van Petegem F, (2011) The structural biology of ryanodine receptors. Sci China Life Sci 54, 712-724.
102. Lanner JT, Georgiou DK, Joshi AD, &, Hamilton SL, (2010) Ryanodine receptors: structure, expression, molecular details, and function in calcium release. Cold Spring Harb Perspect Biol 2, a003996.
103. Song DW, Lee J-G, Youn H-S, Eom SH, &, Kim DH, (2011) Ryanodine receptor assembly: a novel systems biology approach to 3D mapping. Prog Biophys Mol Biol 105, 145-161.
104. Terentyev D, Cala SE, Houle TD, Viatchenko-Karpinski S, Gyorke I, Terentyeva R, Williams SC, &, Gyorke S, (2005) Triadin overexpression stimulates excitation-contraction coupling and increases predisposition to cellular arrhythmia in cardiac myocytes. Circ Res 96, 651-658.
105. Bers DM, (2004) Macromolecular complexes regulating cardiac ryanodine receptor function. J Mol Cell Cardiol 37, 417-429.
106. Bezprozvanny I, Watras J, &, Ehrlich BE, (1991) Bell-shaped calcium-response curves of Ins(1,4,5)P3- and calcium-gated channels from endoplasmic reticulum of cerebellum. Nature 351, 751-754.
107. Balshaw DM, Xu L, Yamaguchi N, Pasek DA, &, Meissner G, (2001) Calmodulin binding and inhibition of cardiac muscle calcium release channel (ryanodine receptor). J Biol Chem 276, 20144-20153.
108. 2+-insensitive mutants of calmodulin. Biochemistry 42, 2740-2747.
109. Yamaguchi N, Xu L, Pasek DA, Evans KE, &, Meissner G, (2003) Molecular basis of calmodulin binding to cardiac muscle Ca(2+) release channel (ryanodine receptor). J Biol Chem 278, 23480-23486.
110. 2+-calmodulin bind to neighboring locations on the ryanodine receptor. J Biol Chem 277, 1349-1353.
111. Xiong L-W, Newman RA, Rodney GG, Thomas O, Zhang J-Z, Persechini A, Shea MA, &, Hamilton SL, (2002) Lobe-dependent regulation of ryanodine receptor type 1 by calmodulin. J Biol Chem 277, 40862-40870.
112. 2+ release channel. J Biol Chem 278, 8348-8355.
113. Maximciuc AA, Putkey JA, Shamoo Y, &, Mackenzie KR, (2006) Complex of calmodulin with a ryanodine receptor target reveals a novel, flexible binding mode. Structure 14, 1547-1556.
114. Huang X, Fruen B, Farrington DT, Wagenknecht T, &, Liu Z, (2012) Calmodulin-binding locations on the skeletal and cardiac ryanodine receptors. J Biol Chem 287, 30328-30335.
115. Kimura Y, Asahi M, Kurzydlowski K, Tada M, &, MacLennan DH, (1998) Phospholamban domain Ib mutations influence functional interactions with the Ca2+-ATPase isoform of cardiac sarcoplasmic reticulum. J Biol Chem 273, 14238-14241.
116. MacLennan DH, &, Kranias EG, (2003) Phospholamban: a crucial regulator of cardiac contractility. Nat Rev Mol Cell Biol 4, 566-577.
117. Brittsan AG, &, Kranias EG, (2000) Phospholamban and cardiac contractile function. J Mol Cell Cardiol 32, 2131-2139.
118. 2+ transport by cyclic 3′,5′-AMP-dependent and calcium-calmodulin-dependent phosphorylation of cardiac sarcoplasmic reticulum. Biochim Biophys Acta 844, 193-199.
119. Mohamed TMA, Oceandy D, Zi M, Prehar S, Alatwi N, Wang Y, Shaheen MA, Abou-Leisa R, Schelcher C, Hegab Z, et al,. (2011) Plasma membrane calcium pump (PMCA4)-neuronal nitric-oxide synthase complex regulates cardiac contractility through modulation of a compartmentalized cyclic nucleotide microdomain. J Biol Chem 286, 41520-41529.
120. Schuh K, Uldrijan S, Telkamp M, Rothlein N, &, Neyses L, (2001) The plasma membrane calmodulin-dependent calcium pump: a major regulator of nitric oxide synthase I. J Cell Biol 155, 201-205.
121. 2+ signaling in cardiovascular disease: the role of the plasma membrane calcium pumps. Sci China Life Sci 54, 691-698.
122. Hare JM, &, Stamler JS, (1999) NOS: modulator, not mediator of cardiac performance. Nat Med 5, 273-274.
123. Arking DE, Pfeufer A, Post W, Kao WHL, Newton-Cheh C, Ikeda M, West K, Kashuk C, Akyol M, Perz S, et al,. (2006) A common genetic variant in the NOS1 regulator NOS1AP modulates cardiac repolarization. Nat Genet 38, 644-651.
124. Ueda K, Valdivia C, Medeiros-Domingo A, Tester DJ, Vatta M, Farrugia G, Ackerman MJ, &, Makielski JC, (2008) Syntrophin mutation associated with long QT syndrome through activation of the nNOS-SCN5A macromolecular complex. PNAS 105, 9355-9360.
125. 2+ ATPase of animal cells: structure, function and regulation. Arch Biochem Biophys 476, 65-74.
126. 2+ pump. J Membr Biol 165, 101-109.
127. Fuller MD, Emrick MA, Sadilek M, Scheuer T, &, Catterall WA, (2010) Molecular mechanism of calcium channel regulation in the fight-or-flight response. Sci Signal 3, ra70.
128. Steinberg SF, (1999) The molecular basis for distinct beta-adrenergic receptor subtype actions in cardiomyocytes. Circ Res 85, 1101-1111.
129. Defer N, Best-Belpomme M, &, Hanoune J, (2000) Tissue specificity and physiological relevance of various isoforms of adenylyl cyclase. Am J Physiol Renal Physiol 279, F400-F416.
130. Cooper DMF, (2003) Regulation and organization of adenylyl cyclases and cAMP. Biochem J 375, 517-529.
131. Omori K, &, Kotera J, (2007) Overview of PDEs and their regulation. Circ Res 100, 309-327.
132. Vandeput F, Wolda SL, Krall J, Hambleton R, Uher L, McCaw KN, Radwanski PB, Florio V, &, Movsesian MA, (2007) Cyclic nucleotide phosphodiesterase PDE1C1 in human cardiac myocytes. J Biol Chem 282, 32749-32757.
133. Francis SH, Blount MA, &, Corbin JD, (2011) Mammalian cyclic nucleotide phosphodiesterases: molecular mechanisms and physiological functions. Physiol Rev 91, 651-690.
134. Maier LS, &, Bers DM, (2002) Calcium, calmodulin, and calcium-calmodulin kinase II: heartbeat to heartbeat and beyond. J Mol Cell Cardiol 34, 919-939.
135. Rosenberg OS, Deindl S, Sung R-J, Nairn AC, &, Kuriyan J, (2005) Structure of the autoinhibited kinase domain of CaMKII and SAXS analysis of the holoenzyme. Cell 123, 849-860.
136. Meyer T, Hanson PI, Stryer L, &, Schulman H, (1992) Calmodulin trapping by calcium-calmodulin-dependent protein kinase. Science 256, 1199-1202.
137. Anderson ME, (2005) Calmodulin kinase signaling in heart: an intriguing candidate target for therapy of myocardial dysfunction and arrhythmias. Pharmacol Ther 106, 39-55.
138. Zhang T, Maier LS, Dalton ND, Miyamoto S, Ross J, Bers DM, &, Brown JH, (2003b) The deltaC isoform of CaMKII is activated in cardiac hypertrophy and induces dilated cardiomyopathy and heart failure. Circ Res 92, 912-919.
139. 2+ release. Circ Res 92, 904-911.
140. Koval OM, Guan X, Wu Y, Joiner M-L, Gao Z, Chen B, Grumbach IM, Luczak ED, Colbran RJ, Song L-S, et al,. (2010) CaV1.2 beta-subunit coordinates CaMKII-triggered cardiomyocyte death and after depolarizations. PNAS 107, 4996-5000.
141. Currie S, Loughrey CM, Craig M-A, &, Smith GL, (2004) Calcium/calmodulin-dependent protein kinase IIdelta associates with the ryanodine receptor complex and regulates channel function in rabbit heart. Biochem J 377, 357-366.
142. 2+/calmodulin-dependent protein kinase II phosphorylation regulates the cardiac ryanodine receptor. Circ Res 94, e61-e70.
143. Berridge MJ, Lipp P, &, Bootman MD, (2000) The versatility and universality of calcium signaling. Nat Rev Mol Cell Biol 1, 11-21.
144. 2+ and the heart. Cell Calcium 44, 77-91.
145. Pizzo P, Lissandron V, Capitanio P, &, Pozzan T, (2011) Ca(2+) signaling in the Golgi apparatus. Cell Calcium 50, 184-192.
146. Beutner G, Sharma VK, Lin L, Ryu S-Y, Dirksen RT, &, Sheu S-S, (2005) Type 1 ryanodine receptor in cardiac mitochondria: transducer of excitation-metabolism coupling. Biochim Biophys Acta 1717, 1-10.
147. Ghafourifar P, &, Cadenas E, (2005) Mitochondrial nitric oxide synthase. Trends Pharmacol Sci 26, 190-195.
148. 2+ peaks in cardiomyocytes. PNAS 109, 12986-12991.
149. Wallace DC, (2000) Mitochondrial defects in cardiomyopathy and neuromuscular disease. Am Heart J 139, S70-S85.
150. Nadif Kasri N, Bultynck G, Sienaert I, Callewaert G, Erneux C, Missiaen L, Parys JB, &, De Smedt H, (2002) The role of calmodulin for inositol 1,4,5-trisphosphate receptor function. Biochim Biophys Acta 1600, 19-31.
151. Exome Variant Server, University of Washington, Seattle, WA, USA. [online] http://evs.gs.washington.edu/EVS/ (accessed 27 March 2013).
152. Coumel P, Fidelle J, &, Lucet V, (1978) Catecholaminergic-induced severe ventricular arrhythmias with Adams-Stokes syndrome in children: report of four cases. Br Heart J 40 (Suppl), 28-37.
153. Napolitano C, &, Priori SG, (2007) Diagnosis and treatment of catecholaminergic polymorphic ventricular tachycardia. Heart Rhythm 4, 675-678.
154. Aizawa Y, Komura S, Okada S, Chinushi M, Aizawa Y, Morita H, &, Ohe T, (2006) Distinct U wave changes in patients with catecholaminergic polymorphic ventricular tachycardia (CPVT). Int Heart J 47, 381-389.
155. Viitasalo M, Oikarinen L, Väänänen H, Kontula K, Toivonen L, &, Swan H, (2008) U-waves and T-wave peak to T-wave end intervals in patients with catecholaminergic polymorphic ventricular tachycardia, effects of beta-blockers. Heart Rhythm 5, 1382-1388.
156. Lahat H, Eldar M, Levy-Nissenbaum E, Bahan T, Friedman E, Khoury A, Lorber A, Kastner DL, Goldman B, &, Pras E, (2001) Autosomal recessive catecholamine- or exercise-induced polymorphic ventricular tachycardia: clinical features and assignment of the disease gene to chromosome 1p13-21. Circulation 103, 2822-2827.
157. Priori SG, Napolitano C, Tiso N, Memmi M, Vignati G, Bloise R, Sorrentino V, &, Danieli GA, (2001) Mutations in the cardiac ryanodine receptor gene (hRyR2) underlie catecholaminergic polymorphic ventricular tachycardia. Circulation 103, 196-200.
158. Laitinen PJ, Brown KM, Piippo K, Swan H, Devaney JM, Brahmbhatt B, Donarum EA, Marino M, Tiso N, Viitasalo M, et al,. (2001) Mutations of the cardiac ryanodine receptor (RyR2) gene in familial polymorphic ventricular tachycardia. Circulation 103, 485-490.
159. Lahat H, Pras E, &, Eldar M, (2003) RYR2 and CASQ2 mutations in patients suffering from catecholaminergic polymorphic ventricular tachycardia. Circulation 107, e29; author reply e29.
160. Wehrens XHT, Lehnart SE, Huang F, Vest JA, Reiken SR, Mohler PJ, Sun J, Guatimosim S, Song L-S, Rosemblit N, et al,. (2003) FKBP12.6 deficiency and defective calcium release channel (ryanodine receptor) function linked to exercise-induced sudden cardiac death. Cell 113, 829-840.
161. Lehnart SE, Wehrens XHT, Laitinen PJ, Reiken SR, Deng S-X, Cheng Z, Landry DW, Kontula K, Swan H, &, Marks AR, (2004) Sudden death in familial polymorphic ventricular tachycardia associated with calcium release channel (ryanodine receptor) leak. Circulation 109, 3208-3214.
162. 2+ release (SOICR). PNAS 101, 13062-13067.
163. 2+ activation are common defects of RyR2 mutations linked to ventricular tachycardia and sudden death. Circ Res 97, 1173-1181.
164. Terentyev D, Nori A, Santoro M, Viatchenko-Karpinski S, Kubalova Z, Gyorke I, Terentyeva R, Vedamoorthyrao S, Blom NA, Valle G, et al,. (2006) Abnormal interactions of calsequestrin with the ryanodine receptor calcium release channel complex linked to exercise-induced sudden cardiac death. Circ Res 98, 1151-1158.
165. Roux-Buisson N, Cacheux M, Fourest-Lieuvin A, Fauconnier J, Brocard J, Denjoy I, Durand P, Guicheney P, Kyndt F, Leenhardt A, et al,. (2012) Absence of triadin, a protein of the calcium release complex, is responsible for cardiac arrhythmia with sudden death in human. Hum Mol Genet 21, 2759-2767.
166. Mohler PJ, Splawski I, Napolitano C, Bottelli G, Sharpe L, Timothy K, Priori SG, Keating MT, &, Bennett V, (2004) A cardiac arrhythmia syndrome caused by loss of ankyrin-B function. PNAS 101, 9137-9142.
167. Tester DJ, Arya P, Will M, Haglund CM, Farley AL, Makielski JC, &, Ackerman MJ, (2006) Genotypic heterogeneity and phenotypic mimicry among unrelated patients referred for catecholaminergic polymorphic ventricular tachycardia genetic testing. Heart Rhythm 3, 800-805.
168. Anderson ME, (2007) Multiple downstream proarrhythmic targets for calmodulin kinase II: moving beyond an ion channel-centric focus. Cardiovasc Res 73, 657-666.
169. McCue HV, Haynes LP, &, Burgoyne RD, (2010) The diversity of calcium sensor proteins in the regulation of neuronal function. Cold Spring Harb Perspect Biol 2, a004085.