Calcium Channelopathies: Structural Insights into Disorders of the Muscle Excitation–Contraction Complex

Literature Cited

1. 1.  Adams BA, Tanabe T, Mikami A, Numa S, Beam KG 1990. Intramembrane charge movement restored in dysgenic skeletal muscle by injection of dihydropyridine receptor cDNAs. Nature 346:569–72
   [Google Scholar]
2. 2.  Adams PJ, Ben-Johny M, Dick IE, Inoue T, Yue DT 2014. Apocalmodulin itself promotes ion channel opening and Ca²⁺ regulation. Cell 159:608–22
   [Google Scholar]
3. 3.  Amador FJ, Kimlicka L, Stathopulos PB, Gasmi-Seabrook GMC, MacLennan DH et al. 2013. Type 2 ryanodine receptor domain A contains a unique and dynamic α-helix that transitions to a β-strand in a mutant linked with a heritable cardiomyopathy. J. Mol. Biol. 425:4034–46
   [Google Scholar]
4. 4.  Antzelevitch C, Pollevick GD, Cordeiro JM, Casis O, Sanguinetti MC et al. 2007. Loss-of-function mutations in the cardiac calcium channel underlie a new clinical entity characterized by ST-segment elevation, short QT intervals, and sudden cardiac death. Circulation 115:442–49
   [Google Scholar]
5. 5.  Avila G, Dirksen RT 2000. Functional impact of the ryanodine receptor on the skeletal muscle L-type Ca²⁺ channel. J. Gen. Physiol. 115:467–80
   [Google Scholar]
6. 6.  Avila G, Dirksen RT 2001. Functional effects of central core disease mutations in the cytoplasmic region of the skeletal muscle ryanodine receptor. J. Gen. Physiol. 118:277–90
   [Google Scholar]
7. 7.  Avila G, O'Brien JJ, Dirksen RT 2001. Excitation–contraction uncoupling by a human central core disease mutation in the ryanodine receptor. PNAS 98:4215–20
   [Google Scholar]
8. 8.  Avila G, O'Connell KM, Dirksen RT 2003. The pore region of the skeletal muscle ryanodine receptor is a primary locus for excitation–contraction uncoupling in central core disease. J. Gen. Physiol. 121:277–86
   [Google Scholar]
9. 9.  Bai XC, Yan Z, Wu J, Li Z, Yan N 2016. The Central domain of RyR1 is the transducer for long-range allosteric gating of channel opening. Cell Res 26:995–1006
   [Google Scholar]
10. 10.  Bailey AG, Bloch EC 1987. Malignant hyperthermia in a three-month-old American Indian infant. Anesthesia Analgesia 66:1043–45
    [Google Scholar]
11. 11.  Ben-Johny M, Yue DT 2014. Calmodulin regulation (calmodulation) of voltage-gated calcium channels. J. Gen. Physiol. 143:679–92
    [Google Scholar]
12. 12.  Betzenhauser MJ, Pitt GS, Antzelevitch C 2015. Calcium channel mutations in cardiac arrhythmia syndromes. Curr. Mol. Pharmacol. 8:133–42
    [Google Scholar]
13. 13.  Block BA, Imagawa T, Campbell KP, 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. 107:2587–600
    [Google Scholar]
14. 14.  Boczek NJ, Best JM, Tester DJ, Giudicessi JR, Middha S et al. 2013. Exome sequencing and systems biology converge to identify novel mutations in the L-type calcium channel, CACNA1C, linked to autosomal dominant long QT syndrome. Circ. Cardiovasc. Genet. 6:279–89
    [Google Scholar]
15. 15.  Boczek NJ, Gomez-Hurtado N, Ye D, Calvert ML, Tester DJ et al. 2016. Spectrum and prevalence of CALM1-, CALM2-, and CALM3-encoded calmodulin (CaM) variants in long QT syndrome (LQTS) and functional characterization of a novel LQTS-associated CaM missense variant, E141G. Circ. Cardiovasc. Genet. 9:136–46
    [Google Scholar]
16. 16.  Bourdin B, Shakeri B, Tétreault MP, Sauvé R, Lesage S, Parent L 2015. Functional characterization of Ca_Vα2δ mutations associated with sudden cardiac death. J. Biol. Chem. 290:2854–69
    [Google Scholar]
17. 17.  Brath U, Lau K, Van Petegem F, Erdélyi M 2014. Mapping the sevoflurane-binding sites of calmodulin. Pharmacol. Res. Perspect. 2:5
    [Google Scholar]
18. 18.  Brath U, Swamy SI, Veiga AX, Tung C-C, Van Petegem F, Erdélyi M 2015. Paramagnetic ligand tagging to identify protein binding sites. J. Am. Chem. Soc. 137:11391–98
    [Google Scholar]
19. 19.  Brillantes A-MB, Ondrias K, Scott A, Kobrinsky E, Ondriašová E et al. 1994. Stabilization of calcium release channel (ryanodine receptor) function by FK506-binding protein. Cell 77:513–23
    [Google Scholar]
20. 20.  Brugada P, Brugada J 1992. Right bundle branch block, persistent ST segment elevation and sudden cardiac death: a distinct clinical and electrocardiographic syndrome. A multicenter report. J. Am. Coll. Cardiol. 20:1391–96
    [Google Scholar]
21. 21.  Bulman DE, Scoggan KA, van Oene MD, Nicolle MW, Hahn AF et al. 1999. A novel sodium channel mutation in a family with hypokalemic periodic paralysis. Neurology 53:1932–36
    [Google Scholar]
22. 22.  Buratti R, Prestipino G, Menegazzi P, Treves S, Zorzato F 1995. Calcium dependent activation of skeletal muscle Ca²⁺ release channel (ryanodine receptor) by calmodulin. Biochem. Biophys. Res. Commun. 213:1082–90
    [Google Scholar]
23. 23.  Campiglio M, Costé de Bagneaux P, Ortner NJ, Tuluc P, Van Petegem F, Flucher BE 2018. STAC proteins associate to the IQ domain of Ca_V1.2 and inhibit calcium-dependent inactivation. PNAS 115:1376–81
    [Google Scholar]
24. 24.  Campiglio M, Flucher BE 2017. STAC3 stably interacts through its C1 domain with Ca_V1.1 in skeletal muscle triads. Sci. Rep. 7:41003
    [Google Scholar]
25. 25.  Cannon SC 2015. Channelopathies of skeletal muscle excitability. Compr. Physiol. 5:761–90
    [Google Scholar]
26. 26.  Cao E, Liao M, Cheng Y, Julius D 2013. TRPV1 structures in distinct conformations reveal activation mechanisms. Nature 504:113–18
    [Google Scholar]
27. 27.  Chen W, Wang R, Chen B, Zhong X, Kong H et al. 2014. The ryanodine receptor store-sensing gate controls Ca²⁺ waves and Ca²⁺-triggered arrhythmias. Nat. Med. 20:184–92
    [Google Scholar]
28. 28.  Chen Y-H, Li M-H, Zhang Y, He L-L, Yamada Y et al. 2004. Structural basis of the α₁–β subunit interaction of voltage-gated Ca²⁺ channels. Nature 429:675–80
    [Google Scholar]
29. 29.  Collins JH 1991. Sequence analysis of the ryanodine receptor: possible association with a 12K, FK506-binding immunophilin/protein kinase C inhibitor. Biochem. Biophys. Res. Commun. 178:1288–90
    [Google Scholar]
30. 30.  Cordeiro JM, Marieb M, Pfeiffer R, Calloe K, Burashnikov E, Antzelevitch C 2009. Accelerated inactivation of the L-type calcium current due to a mutation in CACNB2b underlies Brugada syndrome. J. Mol. Cell. Cardiol. 46:695–703
    [Google Scholar]
31. 31.  Crotti L, Johnson CN, Graf E, De Ferrari GM, Cuneo BF et al. 2013. Calmodulin mutations associated with recurrent cardiac arrest in infants. Circulation 127:1009–17
    [Google Scholar]
32. 32.  Davies A, Kadurin I, Alvarez-Laviada A, Douglas L, Nieto-Rostro M et al. 2010. The α₂δ subunits of voltage-gated calcium channels form GPI-anchored proteins, a posttranslational modification essential for function. PNAS 107:1654–59
    [Google Scholar]
33. 33.  des Georges A, Clarke OB, Zalk R, Yuan Q, Condon KJ et al. 2016. Structural basis for gating and activation of RyR1. Cell 167:145–57.e17
    [Google Scholar]
34. 34.  Dolphin AC 2012. Calcium channel auxiliary α₂δ and β subunits: trafficking and one step beyond. Nat. Rev. Neurosci. 13:542–55
    [Google Scholar]
35. 35.  Efremov RG, Leitner A, Aebersold R, Raunser S 2015. Architecture and conformational switch mechanism of the ryanodine receptor. Nature 517:39–43
    [Google Scholar]
36. 36.  Eltit JM, Bannister RA, Moua O, Altamirano F, Hopkins PM et al. 2012. Malignant hyperthermia susceptibility arising from altered resting coupling between the skeletal muscle L-type Ca²⁺ channel and the type 1 ryanodine receptor. PNAS 109:7923–28
    [Google Scholar]
37. 37.  Endo M, Tanaka M, Ogawa Y 1970. Calcium induced release of calcium from the sarcoplasmic reticulum of skinned skeletal muscle fibres. Nature 228:34–36
    [Google Scholar]
38. 38.  Fabiato A 1983. Calcium-induced release of calcium from the cardiac sarcoplasmic reticulum. Am. J. Physiol. 245:C1–14
    [Google Scholar]
39. 39.  Fabiato A 1992. Two kinds of calcium-induced release of calcium from the sarcoplasmic reticulum of skinned cardiac cells. Adv. Exp. Med. Biol. 311:245–62
    [Google Scholar]
40. 40.  Fallon JL, Halling DB, Hamilton SL, Quiocho FA 2005. Structure of calmodulin bound to the hydrophobic IQ domain of the cardiac Ca_V1.2 calcium channel. Structure 13:1881–86
    [Google Scholar]
41. 41.  Franzini-Armstrong C 1970. Studies of the triad: I. Structure of the junction in frog twitch fibers. J. Cell Biol. 47:488–99
    [Google Scholar]
42. 42.  Fuentes O, Valdivia C, Vaughan D, Coronado R, Valdivia HH 1994. Calcium-dependent block of ryanodine receptor channel of swine skeletal muscle by direct binding of calmodulin. Cell Calcium 15:305–16
    [Google Scholar]
43. 43.  Fujii J, Otsu K, Zorzato F, de Leon S, Khanna VK et al. 1991. Identification of a mutation in porcine ryanodine receptor associated with malignant hyperthermia. Science 253:448–51
    [Google Scholar]
44. 44.  Fukuyama M, Wang Q, Kato K, Ohno S, Ding W-G et al. 2014. Long QT syndrome type 8: novel CACNA1C mutations causing QT prolongation and variant phenotypes. Europace 16:1828–37
    [Google Scholar]
45. 45.  Fuster C, Perrot J, Berthier C, Jacquemond V, Charnet P, Allard B 2017. Na leak with gating pore properties in hypokalemic periodic paralysis V876E mutant muscle Ca channel. J. Gen. Physiol. 149:1139–48
    [Google Scholar]
46. 46.  Galfré E, Pitt SJ, Venturi E, Sitsapesan M, Zaccai NR et al. 2012. FKBP12 activates the cardiac ryanodine receptor Ca²⁺-release channel and is antagonised by FKBP12.6. PLOS ONE 7:e31956
    [Google Scholar]
47. 47.  Gee NS, Brown JP, Dissanayake VUK, Offord J, Thurlow R, Woodruff GN 1996. The novel anticonvulsant drug, gabapentin (Neurontin), binds to the α₂δ subunit of a calcium channel. J. Biol. Chem. 271:5768–76
    [Google Scholar]
48. 48.  Gillard EF, Otsu K, Fujii J, Khanna VK, de Leon S et al. 1991. A substitution of cysteine for arginine 614 in the ryanodine receptor is potentially causative of human malignant hyperthermia. Genomics 11:751–55
    [Google Scholar]
49. 49.  Gomez-Hurtado N, Boczek NJ, Kryshtal DO, Johnson CN, Sun J et al. 2016. Novel CPVT-associated calmodulin mutation in CALM3 (CALM3-A103V) activates arrhythmogenic Ca waves and sparks. Circ. Arrhythmia Electrophysiol. 9:e004161
    [Google Scholar]
50. 50.  Hakamata Y, Nakai J, Takeshima H, Imoto K 1992. Primary structure and distribution of a novel ryanodine receptor/calcium release channel from rabbit brain. FEBS Lett 312:229–35
    [Google Scholar]
51. 51.  Horstick EJ, Linsley JW, Dowling JJ, Hauser MA, McDonald KK et al. 2013. Stac3 is a component of the excitation–contraction coupling machinery and mutated in Native American myopathy. Nat. Commun. 4:1952
    [Google Scholar]
52. 52.  Huang H, Tan BZ, Shen Y, Tao J, Jiang F et al. 2012. RNA editing of the IQ domain in Ca_V1.3 channels modulates their Ca²⁺-dependent inactivation. Neuron 73:304–16
    [Google Scholar]
53. 53.  Hwang HS, Nitu FR, Yang Y, Walweel K, Pereira L et al. 2014. Divergent regulation of ryanodine receptor 2 calcium release channels by arrhythmogenic human calmodulin missense mutants. Circ. Res. 114:1114–24
    [Google Scholar]
54. 54.  Ikemoto T, Iino M, Endo M 1995. Enhancing effect of calmodulin on Ca²⁺-induced Ca²⁺ release in the sarcoplasmic reticulum of rabbit skeletal muscle fibres. J. Physiol. 487 3:573–82
    [Google Scholar]
55. 55.  Inui M, Saito A, Fleischer S 1987. Purification of the ryanodine receptor and identity with feet structures of junctional terminal cisternae of sarcoplasmic reticulum from fast skeletal muscle. J. Biol. Chem. 262:1740–47
    [Google Scholar]
56. 56.  Jayaraman T, Brillantes AM, Timerman AP, Fleischer S, Erdjument-Bromage H et al. 1992. FK506 binding protein associated with the calcium release channel (ryanodine receptor). J. Biol. Chem. 267:9474–77
    [Google Scholar]
57. 57.  Jiang D, Chen W, Wang R, Zhang L, Chen SR 2007. Loss of luminal Ca²⁺ activation in the cardiac ryanodine receptor is associated with ventricular fibrillation and sudden death. PNAS 104:18309–14
    [Google Scholar]
58. 58.  Jiang D, Chen W, Xiao J, Wang R, Kong H et al. 2008. Reduced threshold for luminal Ca²⁺ activation of RyR1 underlies a causal mechanism of porcine malignant hyperthermia. J. Biol. Chem. 283:20813–20
    [Google Scholar]
59. 59.  Jiang D, Xiao B, Yang D, Wang R, Choi P et al. 2004. RyR2 mutations linked to ventricular tachycardia and sudden death reduce the threshold for store-overload-induced Ca²⁺ release (SOICR). PNAS 101:13062–67
    [Google Scholar]
60. 60.  Jurkat-Rott K, Lehmann-Horn F, Elbaz A, Heine R, Gregg RG et al. 1994. A calcium channel mutation causing hypokalemic periodic paralysis. Hum. Mol. Genet. 3:1415–19
    [Google Scholar]
61. 61.  Kim EY, Rumpf CH, Fujiwara Y, Cooley ES, Van Petegem F, Minor DL Jr 2008. Structures of Ca_V2 Ca²⁺/CaM-IQ domain complexes reveal binding modes that underlie calcium-dependent inactivation and facilitation. Structure 16:1455–67
    [Google Scholar]
62. 62.  Kimlicka L, Lau K, Tung C-C, Van Petegem F 2013. Disease mutations in the ryanodine receptor N-terminal region couple to a mobile intersubunit interface. Nat. Commun. 4:1506
    [Google Scholar]
63. 63.  Kimlicka L, Tung C-C, Carlsson AC, Lobo PA, Yuchi Z, Van Petegem F 2013. The cardiac ryanodine receptor N-terminal region contains an anion binding site that is targeted by disease mutations. Structure 21:1440–49
    [Google Scholar]
64. 64.  Krause T, Gerbershagen MU, Fiege M, Weißhorn R, Wappler F 2004. Dantrolene—a review of its pharmacology, therapeutic use and new developments. Anaesthesia 59:364–73
    [Google Scholar]
65. 65.  Kühlbrandt W 2014. The resolution revolution. Science 343:1443–44
    [Google Scholar]
66. 66.  Kursula P 2014. The many structural faces of calmodulin: a multitasking molecular jackknife. Amino Acids 46:2295–304
    [Google Scholar]
67. 67.  Lahat H, Pras E, Olender T, Avidan N, Ben-Asher E et al. 2001. A missense mutation in a highly conserved region of CASQ2 is associated with autosomal recessive catecholamine-induced polymorphic ventricular tachycardia in Bedouin families from Israel. Am. J. Hum. Genet. 69:1378–84
    [Google Scholar]
68. 68.  Lai FA, Erickson HP, Rousseau E, Liu QY, Meissner G 1988. Purification and reconstitution of the calcium release channel from skeletal muscle. Nature 331:315–19
    [Google Scholar]
69. 69.  Laitinen PJ, Brown KM, Piippo K, Swan H, Devaney JM et al. 2001. Mutations of the cardiac ryanodine receptor (RyR2) gene in familial polymorphic ventricular tachycardia. Circulation 103:485–90
    [Google Scholar]
70. 70.  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
    [Google Scholar]
71. 71.  Lau K, Van Petegem F 2014. Crystal structures of wild type and disease mutant forms of the ryanodine receptor SPRY2 domain. Nat. Commun. 5:5397
    [Google Scholar]
72. 72.  Lee CS, Hanna AD, Wang H, Dagnino-Acosta A, Joshi AD et al. 2017. A chemical chaperone improves muscle function in mice with a RyR1 mutation. Nat. Commun. 8:14659
    [Google Scholar]
73. 73.  Liao M, Cao E, Julius D, Cheng Y 2013. Structure of the TRPV1 ion channel determined by electron cryo-microscopy. Nature 504:107–12
    [Google Scholar]
74. 74.  Lieve KV, van der Werf C, Wilde AA 2016. Catecholaminergic polymorphic ventricular tachycardia. Circ. J. 80:1285–91
    [Google Scholar]
75. 75.  Limpitikul WB, Dick IE, Joshi-Mukherjee R, Overgaard MT, George AL Jr, Yue DT 2014. Calmodulin mutations associated with long QT syndrome prevent inactivation of cardiac L-type Ca²⁺ currents and promote proarrhythmic behavior in ventricular myocytes. J. Mol. Cell. Cardiol. 74:115–24
    [Google Scholar]
76. 76.  Liu Y, Kimlicka L, Hiess F, Tian X, Wang R et al. 2013. The CPVT-associated RyR2 mutation G230C enhances store overload-induced Ca²⁺ release and destabilizes the N-terminal domains. Biochem. J. 454:123–31
    [Google Scholar]
77. 77.  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 Ca²⁺-calmodulin. Front. Mol. Neurosci. 5:38
    [Google Scholar]
78. 78.  Lobo PA, Kimlicka L, Tung C-C, Van Petegem F 2011. The deletion of exon 3 in the cardiac ryanodine receptor is rescued by β strand switching. Structure 19:790–98
    [Google Scholar]
79. 79.  Loy RE, Orynbayev M, Xu L, Andronache Z, Apostol S et al. 2011. Muscle weakness in Ryr1^I4895T/WT knock-in mice as a result of reduced ryanodine receptor Ca²⁺ ion permeation and release from the sarcoplasmic reticulum. J. Gen. Physiol. 137:43–57
    [Google Scholar]
80. 80.  MacLennan DH, Phillips MS 1992. Malignant hyperthermia. Science 256:789–94
    [Google Scholar]
81. 81.  MacLennan DH, Zvaritch E 2011. Mechanistic models for muscle diseases and disorders originating in the sarcoplasmic reticulum. Biochim. Biophys. Acta 1813:948–64
    [Google Scholar]
82. 82.  Makita N, Yagihara N, Crotti L, Johnson CN, Beckmann BM et al. 2014. Novel calmodulin mutations associated with congenital arrhythmia susceptibility. Circ. Cardiovasc. Genet. 7:466–74
    [Google Scholar]
83. 83.  Marsman RF, Barc J, Beekman L, Alders M, Dooijes D et al. 2014. A mutation in CALM1 encoding calmodulin in familial idiopathic ventricular fibrillation in childhood and adolescence. J. Am. Coll. Cardiol. 63:259–66
    [Google Scholar]
84. 84.  Marx SO, Gaburjakova J, Gaburjakova M, Henrikson C, Ondrias K, Marks AR 2001. Coupled gating between cardiac calcium release channels (ryanodine receptors). Circ. Res. 88:1151–58
    [Google Scholar]
85. 85.  Marx SO, Ondrias K, Marks AR 1998. Coupled gating between individual skeletal muscle Ca²⁺ release channels (ryanodine receptors). Science 281:818–21
    [Google Scholar]
86. 86.  Maximciuc AA, Putkey JA, Shamoo Y, Mackenzie KR 2006. Complex of calmodulin with a ryanodine receptor target reveals a novel, flexible binding mode. Structure 14:1547–56
    [Google Scholar]
87. 87.  Meli AC, Refaat MM, Dura M, Reiken S, Wronska A et al. 2011. A novel ryanodine receptor mutation linked to sudden death increases sensitivity to cytosolic calcium. Circ. Res. 109:281–90
    [Google Scholar]
88. 88.  Mori MX, Vander Kooi CW, Leahy DJ, Yue DT 2008. Crystal structure of the Ca_V2 IQ domain in complex with Ca²⁺/calmodulin: high-resolution mechanistic implications for channel regulation by Ca²⁺. Structure 16:607–20
    [Google Scholar]
89. 89.  Mulley JC, Kozman HM, Phillips HA, Gedeon AK, McCure JA et al. 1993. Refined genetic localization for central core disease. Am. J. Hum. Genet. 52:398–405
    [Google Scholar]
90. 90.  Nakai J, Dirksen RT, Nguyen HT, Pessah IN, Beam KG, Allen PD 1996. Enhanced dihydropyridine receptor channel activity in the presence of ryanodine receptor. Nature 380:72–75
    [Google Scholar]
91. 91.  Nakai J, Imagawa T, Hakamat Y, Shigekawa M, Takeshima H, Numa S 1990. Primary structure and functional expression from cDNA of the cardiac ryanodine receptor/calcium release channel. FEBS Lett 271:169–77
    [Google Scholar]
92. 92.  Napolitano C, Antzelevitch C 2011. Phenotypical manifestations of mutations in the genes encoding subunits of the cardiac voltage-dependent L-type calcium channel. Circ. Res. 108:607–18
    [Google Scholar]
93. 93.  Nelson BR, Wu F, Liu Y, Anderson DM, McAnally J et al. 2013. Skeletal muscle-specific T-tubule protein STAC3 mediates voltage-induced Ca²⁺ release and contractility. PNAS 110:11881–86
    [Google Scholar]
94. 94.  Nyegaard M, Overgaard MT, Søndergaard MT, Vranas M, Behr ER et al. 2012. Mutations in calmodulin cause ventricular tachycardia and sudden cardiac death. Am. J. Hum. Genet. 91:703–12
    [Google Scholar]
95. 95.  Oo YW, Gomez-Hurtado N, Walweel K, van Helden DF, Imtiaz MS et al. 2015. Essential role of calmodulin in RyR inhibition by dantrolene. Mol. Pharmacol. 88:57–63
    [Google Scholar]
96. 96.  Opatowsky Y, Chen C-C, Campbell KP, Hirsch JA 2004. Structural analysis of the voltage-dependent calcium channel β subunit functional core and its complex with the α1 interaction domain. Neuron 42:387–99
    [Google Scholar]
97. 97.  Otsu K, Willard HF, Khanna VK, Zorzato F, Green NM, MacLennan DH 1990. Molecular cloning of cDNA encoding the Ca²⁺ release channel (ryanodine receptor) of rabbit cardiac muscle sarcoplasmic reticulum. J. Biol. Chem. 265:13472–83
    [Google Scholar]
98. 98.  Peng W, Shen H, Wu J, Guo W, Pan X et al. 2016. Structural basis for the gating mechanism of the type 2 ryanodine receptor RyR2. Science 354:aah5324
    [Google Scholar]
99. 99.  Perni S, Lavorato M, Beam KG 2017. De novo reconstitution reveals the proteins required for skeletal muscle voltage-induced Ca²⁺ release. PNAS 114:13822–27
    [Google Scholar]
100. 100.  Peterson BZ, DeMaria CD, Adelman JP, Yue DT 1999. Calmodulin is the Ca²⁺ sensor for Ca²⁺-dependent inactivation of L-type calcium channels. Neuron 22:549–58
     [Google Scholar]
101. 101.  Pirone A, Schredelseker J, Tuluc P, Gravino E, Fortunato G et al. 2010. Identification and functional characterization of malignant hyperthermia mutation T1354S in the outer pore of the Ca_Vα_1S-subunit. Am. J. Physiol. Cell Physiol. 299:C1345–54
     [Google Scholar]
102. 102.  Polster A, Nelson BR, Olson EN, Beam KG 2016. Stac3 has a direct role in skeletal muscle-type excitation–contraction coupling that is disrupted by a myopathy-causing mutation. PNAS 113:10986–91
     [Google Scholar]
103. 103.  Polster A, Nelson BR, Papadopoulos S, Olson EN, Beam KG 2018. Stac proteins associate with the critical domain for excitation–contraction coupling in the II–III loop of Ca_V1.1. J. Gen. Physiol. 150:613–24
     [Google Scholar]
104. 104.  Polster A, Perni S, Bichraoui H, Beam KG 2015. Stac adaptor proteins regulate trafficking and function of muscle and neuronal L-type Ca²⁺ channels. PNAS 112:602–6
     [Google Scholar]
105. 105.  Pragnell M, De Waard M, Mori Y, Tanabe T, Snutch TP, Campbell KP 1994. Calcium channel β-subunit binds to a conserved motif in the I–II cytoplasmic linker of the α 1-subunit. Nature 368:67–70
     [Google Scholar]
106. 106.  Priori SG, Napolitano C, Tiso N, Memmi M, Vignati G et al. 2001. Mutations in the cardiac ryanodine receptor gene (hRyR2) underlie catecholaminergic polymorphic ventricular tachycardia. Circulation 103:196–200
     [Google Scholar]
107. 107.  Prosser BL, Ward CW, Lederer WJ 2010. Subcellular Ca²⁺ signaling in the heart: the role of ryanodine receptor sensitivity. J. Gen. Physiol. 136:135–42
     [Google Scholar]
108. 108.  Ptacek LJ, Tawil R, Griggs RC, Engel AG, Layzer RB et al. 1994. Dihydropyridine receptor mutations cause hypokalemic periodic paralysis. Cell 77:863–68
     [Google Scholar]
109. 109.  Quane KA, Healy JM, Keating KE, Manning BM, Couch FJ et al. 1993. Mutations in the ryanodine receptor gene in central core disease and malignant hyperthermia. Nat. Genet. 5:51–55
     [Google Scholar]
110. 110.  Rios E, Brum G 1987. Involvement of dihydropyridine receptors in excitation–contraction coupling in skeletal muscle. Nature 325:717–20
     [Google Scholar]
111. 111.  Rogers EF, Koniuszy FR, Shavel J Jr, Folkers K 1948. Plant insecticides. I. Ryanodine, a new alkaloid from Ryania speciosa Vahl. J. Am. Chem. Soc. 70:3086–88
     [Google Scholar]
112. 112.  Roux-Buisson N, Cacheux M, Fourest-Lieuvin A, Fauconnier J, Brocard J 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. 21:2759–67
     [Google Scholar]
113. 113.  Samso M, Feng W, Pessah IN, Allen PD 2009. Coordinated movement of cytoplasmic and transmembrane domains of RyR1 upon gating. PLOS Biol 7:e85
     [Google Scholar]
114. 114.  Søndergaard MT, Liu Y, Larsen KT, Nani A, Tian X et al. 2017. The arrhythmogenic calmodulin p.Phe142Leu mutation impairs C-domain Ca²⁺ binding but not calmodulin-dependent inhibition of the cardiac ryanodine receptor. J. Biol. Chem. 292:1385–95
     [Google Scholar]
115. 115.  Søndergaard MT, Sorensen AB, Skov LL, Kjaer-Sorensen K, Bauer MC et al. 2015. Calmodulin mutations causing catecholaminergic polymorphic ventricular tachycardia confer opposing functional and biophysical molecular changes. FEBS J 282:803–16
     [Google Scholar]
116. 116.  Søndergaard MT, Tian X, Liu Y, Wang R, Chazin WJ et al. 2015. Arrhythmogenic calmodulin mutations affect the activation and termination of cardiac ryanodine receptor-mediated Ca²⁺ release. J. Biol. Chem. 290:26151–62
     [Google Scholar]
117. 117.  Splawski I, Timothy KW, Sharpe LM, Decher N, Kumar P et al. 2004. Ca_V1.2 calcium channel dysfunction causes a multisystem disorder including arrhythmia and autism. Cell 119:19–31
     [Google Scholar]
118. 118.  Stewart SL, Hogan K, Rosenberg H, Fletcher JE 2001. Identification of the Arg1086His mutation in the alpha subunit of the voltage-dependent calcium channel (CACNA1S) in a North American family with malignant hyperthermia. Clin. Genet. 59:178–84
     [Google Scholar]
119. 119.  Takekura H, Bennett L, Tanabe T, Beam KG, Franzini-Armstrong C 1994. Restoration of junctional tetrads in dysgenic myotubes by dihydropyridine receptor cDNA. Biophys. J. 67:793–803
     [Google Scholar]
120. 120.  Takeshima H, Nishimura S, Matsumoto T, Ishida H, Kangawa K et al. 1989. Primary structure and expression from complementary DNA of skeletal muscle ryanodine receptor. Nature 339:439–45
     [Google Scholar]
121. 121.  Tanabe T, Beam KG, Powell JA, Numa S 1988. Restoration of excitation–contraction coupling and slow calcium current in dysgenic muscle by dihydropyridine receptor complementary DNA. Nature 336:134–39
     [Google Scholar]
122. 122.  Tanabe T, Takeshima H, Mikami A, Flockerzi V, Takahashi H et al. 1987. Primary structure of the receptor for calcium channel blockers from skeletal muscle. Nature 328:313–18
     [Google Scholar]
123. 123.  Tang Y, Tian X, Wang R, Fill M, Chen SR 2012. Abnormal termination of Ca²⁺ release is a common defect of RyR2 mutations associated with cardiomyopathies. Circ. Res. 110:968–77
     [Google Scholar]
124. 124.  Templin C, Ghadri JR, Rougier JS, Baumer A, Kaplan V et al. 2011. Identification of a novel loss-of-function calcium channel gene mutation in short QT syndrome (SQTS6). Eur. Heart J. 32:1077–88
     [Google Scholar]
125. 125.  Tidow H, Nissen P 2013. Structural diversity of calmodulin binding to its target sites. FEBS J 280:5551–65
     [Google Scholar]
126. 126.  Tripathy A, Xu L, Mann G, Meissner G 1995. Calmodulin activation and inhibition of skeletal muscle Ca²⁺ release channel (ryanodine receptor). Biophys. J. 69:106–19
     [Google Scholar]
127. 127.  Tung C-C, Lobo PA, Kimlicka L, Van Petegem F 2010. The amino-terminal disease hotspot of ryanodine receptors forms a cytoplasmic vestibule. Nature 468:585–88
     [Google Scholar]
128. 128.  Van Petegem F 2012. Ryanodine receptors: structure and function. J. Biol. Chem. 287:31624–32
     [Google Scholar]
129. 129.  Van Petegem F, Chatelain FC, Minor DL Jr 2005. Insights into voltage-gated calcium channel regulation from the structure of the Ca_V1.2 IQ domain-Ca²⁺/calmodulin complex. Nat. Struct. Mol. Biol. 12:1108–15
     [Google Scholar]
130. 130.  Van Petegem F, Clark KA, Chatelain FC, Minor DL Jr 2004. Structure of a complex between a voltage-gated calcium channel β-subunit and an α-subunit domain. Nature 429:671–75
     [Google Scholar]
131. 132.  Watanabe H, Chopra N, Laver D, Hwang HS, Davies SS et al. 2009. Flecainide prevents catecholaminergic polymorphic ventricular tachycardia in mice and humans. Nat. Med. 15:380–83
     [Google Scholar]
132. 131.  Weber F, Lehmann-Horn F 2002. Hypokalemic periodic paralysis. GeneReviews MP Adam, HH Ardinger, RA Pagon, SE Wallace, LJH Bean et al. Seattle: Univ. Wash https://www.ncbi.nlm.nih.gov/books/NBK1338/
     [Google Scholar]
133. 133.  Wei R, Wang X, Zhang Y, Mukherjee S, Zhang L et al. 2016. Structural insights into Ca²⁺-activated long-range allosteric channel gating of RyR1. Cell Res 26:977–94
     [Google Scholar]
134. 134.  Weiss RG, O'Connell KM, Flucher BE, Allen PD, Grabner M, Dirksen RT 2004. Functional analysis of the R1086H malignant hyperthermia mutation in the DHPR reveals an unexpected influence of the III-IV loop on skeletal muscle EC coupling. Am. J. Physiol. Cell Physiol. 287:C1094–102
     [Google Scholar]
135. 135.  Wong King Yuen SM, Campiglio M, Tung C-C, Flucher BE, Van Petegem F 2017. Structural insights into binding of STAC proteins to voltage-gated calcium channels. PNAS 114:E9520–28
     [Google Scholar]
136. 136.  Wright NT, Prosser BL, Varney KM, Zimmer DB, Schneider MF, Weber DJ 2008. S100A1 and calmodulin compete for the same binding site on ryanodine receptor. J. Biol. Chem. 283:26676–83
     [Google Scholar]
137. 137.  Wu F, Mi W, Burns DK, Fu Y, Gray HF et al. 2011. A sodium channel knockin mutant (Na_V1.4-R669H) mouse model of hypokalemic periodic paralysis. J. Clin. Investig. 121:4082–94
     [Google Scholar]
138. 138.  Wu F, Mi W, Hernandez-Ochoa EO, Burns DK, Fu Y et al. 2012. A calcium channel mutant mouse model of hypokalemic periodic paralysis. J. Clin. Investig. 122:4580–91
     [Google Scholar]
139. 139.  Wu F, Quinonez M, DiFranco M, Cannon SC 2018. Stac3 enhances expression of human Ca_V1.1 in Xenopus oocytes and reveals gating pore currents in HypoPP mutant channels. J. Gen. Physiol. 150:475–89
     [Google Scholar]
140. 140.  Wu J, Yan Z, Li Z, Qian X, Lu S et al. 2016. Structure of the voltage-gated calcium channel Ca_V1.1 at 3.6 Å resolution. Nature 537:191–96
     [Google Scholar]
141. 141.  Wu J, Yan Z, Li Z, Yan C, Lu S et al. 2015. Structure of the voltage-gated calcium channel Ca_V1.1 complex. Science 350:aad2395
     [Google Scholar]
142. 142.  Yan Z, Bai XC, Yan C, Wu J, Li Z et al. 2015. Structure of the rabbit ryanodine receptor RyR1 at near-atomic resolution. Nature 517:50–55
     [Google Scholar]
143. 143.  Yuchi Z, Lau K, Van Petegem F 2012. Disease mutations in the ryanodine receptor central region: crystal structures of a phosphorylation hot spot domain. Structure 20:1201–11
     [Google Scholar]
144. 144.  Yuchi Z, Van Petegem F 2016. Ryanodine receptors under the magnifying lens: insights and limitations of cryo-electron microscopy and X-ray crystallography studies. Cell Calcium 59:209–27
     [Google Scholar]
145. 145.  Yuchi Z, Wong King Yuen SM, Lau K, Underhill AQ, Cornea RL et al. 2015. Crystal structures of ryanodine receptor SPRY1 and tandem-repeat domains reveal a critical FKBP12 binding determinant. Nat. Commun. 6:7947
     [Google Scholar]
146. 146.  Zamponi GW, Striessnig J, Koschak A, Dolphin AC 2015. The physiology, pathology, and pharmacology of voltage-gated calcium channels and their future therapeutic potential. Pharmacol. Rev. 67:821–70
     [Google Scholar]
147. 147.  Zorzato F, Fujii J, Otsu K, Phillips M, Green NM et al. 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. 265:2244–56
     [Google Scholar]
148. 148.  Zorzato F, Yamaguchi N, Xu L, Meissner G, Müller CR et al. 2003. Clinical and functional effects of a deletion in a COOH-terminal lumenal loop of the skeletal muscle ryanodine receptor. Hum. Mol. Genet. 12:379–88
     [Google Scholar]
149. 149.  Zuhlke RD, Pitt GS, Deisseroth K, Tsien RW, Reuter H 1999. Calmodulin supports both inactivation and facilitation of L-type calcium channels. Nature 399:159–62
     [Google Scholar]