Ryanodine receptors under the magnifying lens: Insights and limitations of cryo-electron microscopy and X-ray crystallography studies

Cell Calcium

Volumn 59, Issue 5, 2016, Pages 209-227

  Yuchi, Zhiguang ^a   Van Petegem, Filip ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; FKBP PROTEIN; ISOPROTEIN; RYANODINE RECEPTOR; SPROUTY PROTEIN; UNCLASSIFIED DRUG; CALCIUM;

AMINO ACID SEQUENCE; BINDING SITE; CONFORMATIONAL TRANSITION; CRYOELECTRON MICROSCOPY; CRYSTAL STRUCTURE; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN TARGETING; REVIEW; STRUCTURE ANALYSIS; X RAY CRYSTALLOGRAPHY; ANIMAL; CYTOPLASM; CYTOSOL; METABOLISM; MUSCLE CONTRACTION; PHYSIOLOGY; PROCEDURES; SARCOPLASMIC RETICULUM;

ANIMALS; CALCIUM; CRYOELECTRON MICROSCOPY; CRYSTALLOGRAPHY, X-RAY; CYTOPLASM; CYTOSOL; HUMANS; MUSCLE CONTRACTION; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL; SARCOPLASMIC RETICULUM;

EID: 84966283893     PISSN: 01434160     EISSN: 15321991     Source Type: Journal    
DOI: 10.1016/j.ceca.2016.04.003     Document Type: Review

References (145)

1. Rogers E.F., Koniuszy F.R., et al. Plant insecticides; ryanodine, a new alkaloid from Ryania speciosa Vahl. J. Am. Chem. Soc. 1948, 70:3086-3088.
2. Lai F.A., Erickson H.P., Rousseau E., Liu Q.Y., Meissner G. Purification and reconstitution of the calcium release channel from skeletal muscle. Nature 1988, 331:315-319.
3. Inui M., Saito A., Fleischer S. Purification of the ryanodine receptor and identity with feet structures of junctional terminal cisternae of sarcoplasmic reticulum from fast skeletal muscle. J. Biol. Chem. 1987, 262:1740-1747.
4. Takeshima H., Nishimura S., Matsumoto T., Ishida H., Kangawa K., Minamino N., Matsuo H., Ueda M., Hanaoka M., Hirose T., et al. Primary structure and expression from complementary DNA of skeletal muscle ryanodine receptor. Nature 1989, 339:439-445.
5. 2+ release channel (ryanodine receptor) of skeletal muscle sarcoplasmic reticulum. J. Biol. Chem. 1990, 265:2244-2256.
6. 2+ release channel (ryanodine receptor) of rabbit cardiac muscle sarcoplasmic reticulum. J. Biol. Chem. 1990, 265:13472-13483.
7. Nakai J., Imagawa T., Hakamat Y., Shigekawa M., Takeshima H., Numa S. Primary structure and functional expression from cDNA of the cardiac ryanodine receptor/calcium release channel. FEBS Lett. 1990, 271:169-177.
8. Hakamata Y., Nakai J., Takeshima H., Imoto K. Primary structure and distribution of a novel ryanodine receptor/calcium release channel from rabbit brain. FEBS Lett. 1992, 312:229-235.
9. Lanner J.T., Georgiou D.K., Joshi A.D., Hamilton S.L. Ryanodine receptors: structure, expression, molecular details, and function in calcium release. Cold Spring Harb. Perspect. Biol. 2010, 2:a003996.
10. 2+ release channel. J. Biol. Chem. 1993, 268:19785-19790.
11. Endo M., Tanaka M., Ogawa Y. Calcium induced release of calcium from the sarcoplasmic reticulum of skinned skeletal muscle fibres. Nature 1970, 228:34-36.
12. Fabiato A. Calcium-induced release of calcium from the cardiac sarcoplasmic reticulum. Am. J. Physiol. 1983, 245:C1-14.
13. Rios E., Brum G. Involvement of dihydropyridine receptors in excitation-contraction coupling in skeletal muscle. Nature 1987, 325:717-720.
14. Tanabe T., Beam K.G., Powell J.A., Numa S. Restoration of excitation-contraction coupling and slow calcium current in dysgenic muscle by dihydropyridine receptor complementary DNA. Nature 1988, 336:134-139.
15. Block B.A., Imagawa T., Campbell K.P., Franzini-Armstrong C. Structural evidence for direct interaction between the molecular components of the transverse tubule/sarcoplasmic reticulum junction in skeletal muscle. J. Cell Biol. 1988, 107:2587-2600.
16. Adams B.A., Tanabe T., Mikami A., Numa S., Beam K.G. Intramembrane charge movement restored in dysgenic skeletal muscle by injection of dihydropyridine receptor cDNAs. Nature 1990, 346:569-572.
17. Takekura H., Bennett L., Tanabe T., Beam K.G., Franzini-Armstrong C. Restoration of junctional tetrads in dysgenic myotubes by dihydropyridine receptor cDNA. Biophys. J . 1994, 67:793-803.
18. Maclennan D.H., Zvaritch E. Mechanistic models for muscle diseases and disorders originating in the sarcoplasmic reticulum. Biochim. Biophys. Acta 2011, 1813:948-964.
19. Priori S.G., Napolitano C., Tiso N., Memmi M., Vignati G., Bloise R., Sorrentino V., Danieli G.A. Mutations in the cardiac ryanodine receptor gene (hRyR2) underlie catecholaminergic polymorphic ventricular tachycardia. Circulation 2001, 103:196-200.
20. Lahat H., Pras E., Olender T., Avidan N., Ben-Asher E., Man O., Levy-Nissenbaum E., Khoury A., Lorber A., Goldman B., Lancet D., Eldar M. 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. 2001, 69:1378-1384.
21. Roux-Buisson N., Cacheux M., Fourest-Lieuvin A., Fauconnier J., Brocard J., Denjoy I., Durand P., Guicheney P., Kyndt F., Leenhardt A., Le Marec H., Lucet V., Mabo P., Probst V., Monnier N., Ray P.F., Santoni E., Tremeaux P., Lacampagne A., Faure J., Lunardi J., Marty I. Absence of triadin a protein of the calcium release complex, is responsible for cardiac arrhythmia with sudden death in human. Hum. Mol. Genet. 2012, 21:2759-2767.
22. Nyegaard M., Overgaard M.T., Sondergaard M.T., Vranas M., Behr E.R., Hildebrandt L.L., Lund J., Hedley P.L., Camm A.J., Wettrell G., Fosdal I., Christiansen M., Borglum A.D. Mutations in calmodulin cause ventricular tachycardia and sudden cardiac death. Am. J. Hum. Genet. 2012, 91:703-712.
23. Gillard E.F., Otsu K., Fujii J., Khanna V.K., de Leon S., Derdemezi J., Britt B.A., Duff C.L., Worton R.G., MacLennan D.H. A substitution of cysteine for arginine 614 in the ryanodine receptor is potentially causative of human malignant hyperthermia. Genomics 1991, 11:751-755.
24. Mulley J.C., Kozman H.M., Phillips H.A., Gedeon A.K., McCure J.A., Iles D.E., Gregg R.G., Hogan K., Couch F.J., MacLennan D.H., et al. Refined genetic localization for central core disease. Am. J. Hum. Genet. 1993, 52:398-405.
25. Quane K.A., Healy J.M., Keating K.E., Manning B.M., Couch F.J., Palmucci L.M., Doriguzzi C., Fagerlund T.H., Berg K., Ording H., et al. Mutations in the ryanodine receptor gene in central core disease and malignant hyperthermia. Nat. Genet. 1993, 5:51-55.
26. Jungbluth H., Zhou H., Hartley L., Halliger-Keller B., Messina S., Longman C., Brockington M., Robb S.A., Straub V., Voit T., Swash M., Ferreiro A., Bydder G., Sewry C.A., Muller C., Muntoni F. Minicore myopathy with ophthalmoplegia caused by mutations in the ryanodine receptor type 1 gene. Neurology 2005, 65:1930-1935.
27. Kimlicka L., Van Petegem F. The structural biology of ryanodine receptors, science China. Life Sci. 2011, 54:712-724.
28. Franzini-Armstrong C. STUDIES OF THE TRIAD: I. Structure of the junction in frog twitch fibers. J. Cell Biol. 1970, 47:488-499.
29. Kuhlbrandt W. Biochemistry. the resolution revolution. Science 2014, 343:1443-1444.
30. Efremov R.G., Leitner A., Aebersold R., Raunser S. Architecture and conformational switch mechanism of the ryanodine receptor. Nature 2015, 517:39-43.
31. Zalk R., Clarke O.B., des Georges A., Grassucci R.A., Reiken S., Mancia F., Hendrickson W.A., Frank J., Marks A.R. Structure of a mammalian ryanodine receptor. Nature 2015, 517:44-49.
32. Yan Z., Bai X.C., Yan C., Wu J., Li Z., Xie T., Peng W., Yin C.C., Li X., Scheres S.H., Shi Y., Yan N. Structure of the rabbit ryanodine receptor RyR1 at near-atomic resolution. Nature 2015, 517:50-55.
33. Wu J., Yan Z., Li Z., Yan C., Lu S., Dong M., Yan N. Structure of the voltage-gated calcium channel Cav1.1 complex. Science 2015, 350:aad2395.
34. Saito A., Inui M., Radermacher M., Frank J., Fleischer S. Ultrastructure of the calcium release channel of sarcoplasmic reticulum. J. Cell Biol. 1988, 107:211-219.
35. Wagenknecht T., Grassucci R., Frank J., Saito A., Inui M., Fleischer S. Three-dimensional architecture of the calcium channel/foot structure of sarcoplasmic reticulum. Nature 1989, 338:167-170.
36. Samso M., Wagenknecht T., Allen P.D. Internal structure and visualization of transmembrane domains of the RyR1 calcium release channel by cryo-EM. Nat. Struct. Mol. Biol. 2005, 12:539-544.
37. Samso M., Feng W., Pessah I.N., Allen P.D. Coordinated movement of cytoplasmic and transmembrane domains of RyR1 upon gating. PLoS Biol. 2009, 7:e85.
38. Ludtke S.J., Serysheva I.I., Hamilton S.L., Chiu W. The pore structure of the closed RyR1 channel. Structure 2005, 13:1203-1211.
39. Sharma M.R., Penczek P., Grassucci R., Xin H.B., Fleischer S., Wagenknecht T. Cryoelectron microscopy and image analysis of the cardiac ryanodine receptor. J. Biol. Chem. 1998, 273:18429-18434.
40. Sharma M.R., Jeyakumar L.H., Fleischer S., Wagenknecht T. Three-dimensional structure of ryanodine receptor isoform three in two conformational states as visualized by cryo-electron microscopy. J. Biol. Chem. 2000, 275:9485-9491.
41. Tung C.C., Lobo P.A., Kimlicka L., Van Petegem F. The amino-terminal disease hotspot of ryanodine receptors forms a cytoplasmic vestibule. Nature 2010, 468:585-588.
42. Yuchi Z., Yuen S.M., Lau K., Underhill A.Q., Cornea R.L., Fessenden J.D., Van Petegem F. Crystal structures of ryanodine receptor SPRY1 and tandem-repeat domains reveal a critical FKBP12 binding determinant. Nat. Commun. 2015, 6:7947.
43. Amador F.J., Liu S., Ishiyama N., Plevin M.J., Wilson A., MacLennan D.H., Ikura M. Crystal structure of type I ryanodine receptor amino-terminal beta-trefoil domain reveals a disease-associated mutation hot spot loop. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:11040-11044.
44. Lobo P.A., Van Petegem F. Crystal structures of the N-terminal domains of cardiac and skeletal muscle ryanodine receptors: insights into disease mutations. Structure 2009, 17:1505-1514.
45. Kimlicka L., Tung C.C., Carlsson A.C., Lobo P.A., Yuchi Z., Van Petegem F. The cardiac ryanodine receptor N-terminal region contains an anion binding site that is targeted by disease mutations. Structure 2013, 21:1440-1449.
46. Kimlicka L., Lau K., Tung C.C., Van Petegem F. Disease mutations in the ryanodine receptor N-terminal region couple to a mobile intersubunit interface. Nat. Commun. 2013, 4:1506.
47. Borko L., Bauerova-Hlinkova V., Hostinova E., Gasperik J., Beck K., Lai F.A., Zahradnikova A., Sevcik J. Structural insights into the human RyR2 N-terminal region involved in cardiac arrhythmias. Acta Crystallogr. Sect. D Biol. Crystallogr. 2014, 70:2897-2912.
48. Lau K., Van Petegem F. Crystal structures of wild type and disease mutant forms of the ryanodine receptor SPRY2 domain. Nat. Commun. 2014, 5:5397.
49. Yuchi Z., Lau K., Van Petegem F. Disease mutations in the ryanodine receptor central region: crystal structures of a phosphorylation hot spot domain. Structure 2012, 20:1201-1211.
50. Sharma P., Ishiyama N., Nair U., Li W., Dong A., Miyake T., Wilson A., Ryan T., Maclennan D.H., Kislinger T., Ikura M., Dhe-Paganon S., Gramolini A.O. Structural determination of the phosphorylation domain of the ryanodine receptor. FEBS J. 2012, 279:3952-3964.
51. Euden J., Mason S.A., Williams A.J. Functional characterization of the cardiac ryanodine receptor pore-forming region. PLoS One 2013, 8:e66542.
52. Palade P., Mitchell R.D., Fleischer S. Spontaneous calcium release from sarcoplasmic reticulum. General description and effects of calcium. J. Biol. Chem. 1983, 258:8098-8107.
53. 2+ release (SOICR). Proc. Natl. Acad. Sci. U. S. A. 2004, 101:13062-13067.
54. Chen W., Wang R., Chen B., Zhong X., Kong H., Bai Y., Zhou Q., Xie C., Zhang J., Guo A., Tian X., Jones P.P., O'Mara M.L., Liu Y., Mi T., Zhang L., Bolstad J., Semeniuk L., Cheng H., Chen J., Tieleman D.P., Gillis A.M., Duff H.J., Fill M., Song L.S., Chen S.R. The ryanodine receptor store-sensing gate controls Ca(2+) waves and Ca(2+)-triggered arrhythmias. Nat. Med. 2014, 20:184-192.
55. Lobo P.A., Kimlicka L., Tung C.C., Van Petegem F. The deletion of exon 3 in the cardiac ryanodine receptor is rescued by beta strand switching. Structure 2011, 19:790-798.
56. Zhong X., Liu Y., Zhu L., Meng X., Wang R., Van Petegem F., Wagenknecht T., Chen S.R., Liu Z. Conformational dynamics inside amino-terminal disease hotspot of ryanodine receptor. Structure 2013, 21:2051-2060.
57. Girgenrath T., Mahalingam M., Svensson B., Nitu F.R., Cornea R.L., Fessenden J.D. N-terminal and central segments of the type 1 ryanodine receptor mediate its interaction with FK506-binding proteins. J. Biol. Chem. 2013, 288:16073-16084.
58. X.L. Zhong, Y. Meng, X. Wang, R. Van Petegem, F. Wagenknecht, T. Chen, S.R. Liu, Z. Conformational Dynamics Inside Amino-Terminal Disease Hotspot of Ryanodine Receptor, Biophysical journal, 102 (2012) 304 a.
59. Bosanac I., Alattia J.R., Mal T.K., Chan J., Talarico S., Tong F.K., Tong K.I., Yoshikawa F., Furuichi T., Iwai M., Michikawa T., Mikoshiba K., Ikura M. Structure of the inositol 1,4,5-trisphosphate receptor binding core in complex with its ligand. Nature 2002, 420:696-700.
60. Bosanac I., Yamazaki H., Matsu-Ura T., Michikawa T., Mikoshiba K., Ikura M. Crystal structure of the ligand binding suppressor domain of type 1 inositol 1,4,5-trisphosphate receptor. Mol. Cell 2005, 17:193-203.
61. Chan J., Yamazaki H., Ishiyama N., Seo M.D., Mal T.K., Michikawa T., Mikoshiba K., Ikura M. Structural studies of inositol 1,4,5-trisphosphate receptor: coupling ligand binding to channel gating. J. Biol. Chem. 2010, 285:36092-36099.
62. Seo M.D., Velamakanni S., Ishiyama N., Stathopulos P.B., Rossi A.M., Khan S.A., Dale P., Li C., Ames J.B., Ikura M., Taylor C.W. Structural and functional conservation of key domains in InsP(3) and ryanodine receptors. Nature 2012, 483:108-112.
63. Lin C.C., Baek K., Lu Z. Apo and InsP-bound crystal structures of the ligand-binding domain of an InsP receptor. Nat. Struct. Mol. Biol. 2011, 18:1172-1174.
64. Fan G., Baker M.L., Wang Z., Baker M.R., Sinyagovskiy P.A., Chiu W., Ludtke S.J. Serysheva, II, Gating machinery of InsPR channels revealed by electron cryomicroscopy. Nature 2015.
65. 2+ sensor protein, inhibits inositol trisphosphate receptors by clamping intersubunit interactions. Proc. Natl. Acad. Sci. U. S. Am. 2013, 110:8507-8512.
66. Jones J.L., Reynolds D.F., Lai F.A., Blayney L.M. Ryanodine receptor binding to FKBP12 is modulated by channel activation state. J. Cell Sci. 2005, 118:4613-4619.
67. Timerman A.P., Wiederrecht G., Marcy A., Fleischer S. Characterization of an exchange reaction between soluble FKBP-12 and the FKBP.ryanodine receptor complex. Modulation by FKBP mutants deficient in peptidyl-prolyl isomerase activity. J. Biol. Chem. 1995, 270:2451-2459.
68. Wehrens X.H., Lehnart S.E., Huang F., Vest J.A., Reiken S.R., Mohler P.J., Sun J., Guatimosim S., Song L.S., Rosemblit N., D'Armiento J.M., Napolitano C., Memmi M., Priori S.G., Lederer W.J., Marks A.R. FKBP12.6 deficiency and defective calcium release channel (ryanodine receptor) function linked to exercise-induced sudden cardiac death. Cell 2003, 113:829-840.
69. Brillantes A.B., Ondrias K., Scott A., Kobrinsky E., Ondriasova E., Moschella M.C., Jayaraman T., Landers M., Ehrlich B.E., Marks A.R. Stabilization of calcium release channel (ryanodine receptor) function by FK506-binding protein. Cell 1994, 77:513-523.
70. 2+ release channels (ryanodine receptors). Science 1998, 281:818-821.
71. Marx S.O., Gaburjakova J., Gaburjakova M., Henrikson C., Ondrias K., Marks A.R. Coupled gating between cardiac calcium release channels (ryanodine receptors). Circ. Res. 2001, 88:1151-1158.
72. Samso M., Shen X., Allen P.D. Structural characterization of the RyR1-FKBP12 interaction. J. Mol. Biol. 2006, 356:917-927.
73. Sharma M.R., Jeyakumar L.H., Fleischer S., Wagenknecht T. Three-dimensional visualization of FKBP12.6 binding to an open conformation of cardiac ryanodine receptor. Biophys. J . 2006, 90:164-172.
74. Cui Y., Tae H.S., Norris N.C., Karunasekara Y., Pouliquin P., Board P.G., Dulhunty A.F., Casarotto M.G. A dihydropyridine receptor alpha1s loop region critical for skeletal muscle contraction is intrinsically unstructured and binds to a SPRY domain of the type 1 ryanodine receptor. Int. J. Biochem. Cell Biol. 2009, 41:677-686.
75. Tae H.S., Cui Y., Karunasekara Y., Board P.G., Dulhunty A.F., Casarotto M.G. Cyclisation of the intrinsically disordered 1s dihydropyridine receptor II-III loop enhances secondary structure and in vitro function. J. Biol. Chem. 2011, 286:22589-22599.
76. Tae H.S., Norris N.C., Cui Y., Karunasekara Y., Board P.G., Dulhunty A.F., Casarotto M.G. Molecular recognition of the disordered dihydropyridine receptor II-iII loop by a conserved spry domain of the type 1 ryanodine receptor. Clin. Exp. Pharmacol. Physiol. 2009, 36:346-349.
77. Mackrill J.J. Ryanodine receptor calcium release channels: an evolutionary perspective. Adv. Exp. Med. Biol. 2012, 740:159-182.
78. Marks A.R., Fleischer S., Tempst P. Surface topography analysis of the ryanodine receptor/junctional channel complex based on proteolysis sensitivity mapping. The J. Biol. Chem. 1990, 265:13143-13149.
79. Ferguson D.G., Schwartz H.W., Franzini-Armstrong C. Subunit structure of junctional feet in triads of skeletal muscle: a freeze-drying rotary-shadowing study. J. Cell Biol. 1984, 99:1735-1742.
80. 2+ release units and couplons in skeletal and cardiac muscles. Biophys. J. 1999, 77:1528-1539.
81. Yin C.C., Lai F.A. Intrinsic lattice formation by the ryanodine receptor calcium-release channel. Nat. Cell Biol. 2000, 2:669-671.
82. Dobrev D., Wehrens X.H. Role of RyR2 phosphorylation in heart failure and arrhythmias: controversies around ryanodine receptor phosphorylation in cardiac disease. Circ. Res. 2014, 114:1311-1319.
83. Houser S.R. 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. 2014, 114:1320-1327.
84. Zalk R., Lehnart S.E., Marks A.R. Modulation of the ryanodine receptor and intracellular calcium. Annu. Rev. Biochem. 2007, 76:367-385.
85. Witcher D.R., Kovacs R.J., Schulman H., Cefali D.C., Jones L.R. Unique phosphorylation site on the cardiac ryanodine receptor regulates calcium channel activity. J. Biol. Chem. 1991, 266:11144-11152.
86. Marx S.O., Reiken S., Hisamatsu Y., Jayaraman T., Burkhoff D., Rosemblit N., Marks A.R. PKA phosphorylation dissociates FKBP12.6 from the calcium release channel (ryanodine receptor): defective regulation in failing hearts. Cell 2000, 101:365-376.
87. 2+/calmodulin-dependent protein kinase II phosphorylation regulates the cardiac ryanodine receptor. Circ. Res. 2004, 94:e61-70.
88. 2+, and adenine nucleotides. Biochemistry 1986, 25:236-244.
89. 2+ release channel. Biochemistry 1998, 37:4804-4814.
90. Fessenden J.D., Feng W., Pessah I.N., Allen P.D. Mutational analysis of putative calcium binding motifs within the skeletal ryanodine receptor isoform, RyR1. The J. Biol. Chem. 2004, 279:53028-53035.
91. 2+ activation of the cardiac ryanodine receptor. J. Biol. Chem. 2016, 291:2150-2160.
92. 2+ activation of the mouse cardiac Ca(2)+ release channel (ryanodine receptor). J. Gen. Physiol. 2001, 118:33-44.
93. 2+ sensor. J. Biol. Chem. 1998, 273:14675-14678.
94. Fessenden J.D., Chen L., Wang Y., Paolini C., Franzini-Armstrong C., Allen P.D., Pessah I.N. Ryanodine receptor point mutant E4032A reveals an allosteric interaction with ryanodine. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:2865-2870.
95. Fan G., Baker M.L., Wang Z., Baker M.R., Sinyagovskiy P.A., Chiu W., Ludtke S.J. Serysheva, II gating machinery of InsP3R channels revealed by electron cryomicroscopy. Nature 2015, 527:336-341.
96. 2+ signaling. EMBO J. 2001, 20:1674-1680.
97. Tu H., Nosyreva E., Miyakawa T., Wang Z., Mizushima A., Iino M., Bezprozvanny I. Functional and biochemical analysis of the type 1 inositol (1,4,5)-trisphosphate receptor calcium sensor. Biophys. J . 2003, 85:290-299.
98. 2+-binding domain in RyR1 that interacts with the calmodulin binding site and modulates channel activity. Biophys. J. 2006, 90:173-182.
99. Lau K., Chan M.M., Van Petegem F. Lobe-specific calmodulin binding to different ryanodine receptor isoforms. Biochemistry 2014, 53:932-946.
100. Maximciuc A.A., Putkey J.A., Shamoo Y., Mackenzie K.R. Complex of calmodulin with a ryanodine receptor target reveals a novel, flexible binding mode. Structure 2006, 14:1547-1556.
101. 2+ release channel. Biochemistry 1999, 38:8532-8537.
102. Xiao B., Zhong G., Obayashi M., Yang D., Chen K., Walsh M.P., Shimoni Y., Cheng H., Ter Keurs H., Chen S.R. Ser-2030 but not Ser-2808, is the major phosphorylation site in cardiac ryanodine receptors responding to protein kinase A activation upon beta-adrenergic stimulation in normal and failing hearts. Biochem. J. 2006, 396:7-16.
103. 2+ release channel (ryanodine receptor). J. Biol. Chem. 2000, 275:11778-11783.
104. Yamazawa T., Takeshima H., Shimuta M., Iino M. A region of the ryanodine receptor critical for excitation-contraction coupling in skeletal muscle. J. Biol. Chem. 1997, 272:8161-8164.
105. Perez C.F., Mukherjee S., Allen P.D. Amino acids 1-1,680 of ryanodine receptor type 1 hold critical determinants of skeletal type for excitation-contraction coupling. Role of divergence domain D2. J. Biol. Chem. 2003, 278:39644-39652.
106. Hayek S.M., Zhu X., Bhat M.B., Zhao J., Takeshima H., Valdivia H.H., Ma J. Characterization of a calcium-regulation domain of the skeletal-muscle ryanodine receptor. Biochem. J. 2000, 351:57-65.
107. Medeiros-Domingo A., Bhuiyan Z.A., Tester D.J., Hofman N., Bikker H., van Tintelen J.P., Mannens M.M., Wilde A.A., Ackerman M.J. The RYR2-encoded ryanodine receptor/calcium release channel in patients diagnosed previously with either catecholaminergic polymorphic ventricular tachycardia or genotype negative, exercise-induced long QT syndrome: a comprehensive open reading frame mutational analysis. J. Am. Coll. Cardiol. 2009, 54:2065-2074.
108. Bhuiyan Z.A., van den Berg M.P., van Tintelen J.P., Bink-Boelkens M.T., Wiesfeld A.C., Alders M., Postma A.V., van Langen I., Mannens M.M., Wilde A.A. Expanding spectrum of human RYR2-related disease: new electrocardiographic, structural, and genetic features. Circulation 2007, 116:1569-1576.
109. Marjamaa A., Laitinen-Forsblom P., Lahtinen A.M., Viitasalo M., Toivonen L., Kontula K., Swan H. Search for cardiac calcium cycling gene mutations in familial ventricular arrhythmias resembling catecholaminergic polymorphic ventricular tachycardia. BMC Med. Genet. 2009, 10:12.
110. Amador F.J., Kimlicka L., Stathopulos P.B., Gasmi-Seabrook G.M., Maclennan D.H., Van Petegem F., Ikura M. Type 2 ryanodine receptor domain a contains a unique and dynamic alpha-helix that transitions to a beta-strand in a mutant linked with a heritable cardiomyopathy. J. Mol. Biol. 2013, 425:4034-4046.
111. Zheng W. Toward decrypting the allosteric mechanism of the ryanodine receptor based on coarse-grained structural and dynamic modeling. Proteins 2015, 83:2307-2318.
112. Galli L., Orrico A., Cozzolino S., Pietrini V., Tegazzin V., Sorrentino V. Mutations in the RYR1 gene in Italian patients at risk for malignant hyperthermia: evidence for a cluster of novel mutations in the C-terminal region. Cell Calcium 2002, 32:143-151.
113. Monnier N., Krivosic-Horber R., Payen J.F., Kozak-Ribbens G., Nivoche Y., Adnet P., Reyford H., Lunardi J. Presence of two different genetic traits in malignant hyperthermia families: implication for genetic analysis, diagnosis, and incidence of malignant hyperthermia susceptibility. Anesthesiology 2002, 97:1067-1074.
114. 2+ release channel (ryanodine receptor). Biophys. J. 1997, 73:1904-1912.
115. Tian X., Liu Y., Wang R., Wagenknecht T., Liu Z., Chen S.R. Ligand-dependent conformational changes in the clamp region of the cardiac ryanodine receptor. The J. Biol. Chem. 2013, 288:4066-4075.
116. 2+-induced Ca2+ release in the sarcoplasmic reticulum of rabbit skeletal muscle fibres. J. Physiol. 1995, 487(Pt. 3):573-582.
117. 2+ release channel (ryanodine receptor). Biophys. J. 1995, 69:106-119.
118. 2+ release channel (ryanodine receptor) by calmodulin. Biochem. Biophys. Res. Commun. 1995, 213:1082-1090.
119. Fuentes O., Valdivia C., Vaughan D., Coronado R., Valdivia H.H. Calcium-dependent block of ryanodine receptor channel of swine skeletal muscle by direct binding of calmodulin. Cell Calcium 1994, 15:305-316.
120. 2+-calmodulin bind to neighboring locations on the ryanodine receptor. J. Biol. Chem. 2002, 277:1349-1353.
121. Huang X., Fruen B., Farrington D.T., Wagenknecht T., Liu Z. Calmodulin-binding locations on the skeletal and cardiac ryanodine receptors. J. Biol. Chem. 2012, 287:30328-30335.
122. Van Petegem F. Ryanodine receptors: allosteric ion channel giants. J. Mol. Biol. 2015, 427:31-53.
123. 2+ release channel (ryanodine receptor) of rabbit skeletal muscle sarcoplasmic reticulum. J. Biol. Chem. 1994, 269:22698-22704.
124. Menegazzi P., Larini F., Treves S., Guerrini R., Quadroni M., Zorzato F. Identification and characterization of three calmodulin binding sites of the skeletal muscle ryanodine receptor. Biochemistry 1994, 33:9078-9084.
125. 2+ channels: modulation by the catalytic subunit of cAMP-dependent protein kinase?. Biochemistry 1995, 34:5120-5129.
126. Rodney G.G., Moore C.P., Williams B.Y., Zhang J.Z., Krol J., Pedersen S.E., Hamilton S.L. Calcium binding to calmodulin leads to an N-terminal shift in its binding site on the ryanodine receptor. J. Biol. Chem. 2001, 276:2069-2074.
127. 2+ release channel (ryanodine receptor). J. Biol. Chem. 2003, 278:23480-23486.
128. Balshaw D.M., Xu L., Yamaguchi N., Pasek D.A., Meissner G. Calmodulin binding and inhibition of cardiac muscle calcium release channel (ryanodine receptor). J. Biol. Chem. 2001, 276:20144-20153.
129. Xiong L.W., Newman R.A., Rodney G.G., Thomas O., Zhang J.Z., Persechini A., Shea M.A., Hamilton S.L. Lobe-dependent regulation of ryanodine receptor type 1 by calmodulin. J. Biol. Chem. 2002, 277:40862-40870.
130. 2+ release channel. J. Biol. Chem. 2003, 278:8348-8355.
131. Zhu X., Ghanta J., Walker J.W., Allen P.D., Valdivia H.H. The calmodulin binding region of the skeletal ryanodine receptor acts as a self-modulatory domain. Cell Calcium 2004, 35:165-177.
132. 2+-binding protein S100A1 in the heart leads to increased in vivo myocardial contractile performance. J. Biol. Chem. 2003, 278:33809-33817.
133. 2+ release channel (ryanodine receptor) of skeletal muscle. Biochemistry 1997, 36:11496-11503.
134. Prosser B.L., Wright N.T., Hernandez-Ochoa E.O., Varney K.M., Liu Y., Olojo R.O., Zimmer D.B., Weber D.J., Schneider M.F. S100A1 binds to the calmodulin-binding site of ryanodine receptor and modulates skeletal muscle excitation-contraction coupling. J. Biol. Chem. 2008, 283:5046-5057.
135. Du X.J., Cole T.J., Tenis N., Gao X.M., Kontgen F., Kemp B.E., Heierhorst J. Impaired cardiac contractility response to hemodynamic stress in S100A1-deficient mice. Mol. Cell. Biol. 2002, 22:2821-2829.
136. Wright N.T., Prosser B.L., Varney K.M., Zimmer D.B., Schneider M.F., Weber D.J. S100A1 and calmodulin compete for the same binding site on ryanodine receptor. J. Biol. Chem. 2008, 283:26676-26683.
137. Rosenberg H., Pollock N., Schiemann A., Bulger T., Stowell K. Malignant hyperthermia: a review. Orphanet J. Rare Dis. 2015, 10:93.
138. 2+, and ATP. Am. J. Physiol. Cell Physiol. 2008, 94:C1103-1112.
139. Brath U., Lau K., Van Petegem F., Erdelyi M. Mapping the sevoflurane-binding sites of calmodulin. Pharmacol. Res. Perspect. 2014, 2:5.
140. Brath U., Swamy S.I., Veiga A.X., Tung C.C., Van Petegem F., Erdelyi M. Paramagnetic ligand tagging to identify protein binding sites. J. Am. Chem. Soc. 2015, 137:11391-11398.
141. Krause T., Gerbershagen M.U., Fiege M., Weisshorn R., Wappler F. Dantrolene-a review of its pharmacology, therapeutic use and new developments. Anaesthesia 2004, 59:364-373.
142. Paul-Pletzer K., Yamamoto T., Bhat M.B., Ma J., Ikemoto N., Jimenez L.S., Morimoto H., Williams P.G., Parness J. Identification of a dantrolene-binding sequence on the skeletal muscle ryanodine receptor. J. Biol. Chem. 2002, 277:34918-34923.
143. 2+ release channels. Molecular mechanism and isoform selectivity. J. Biol. Chem. 2001, 276:13810-13816.
144. Oo Y.W., Gomez-Hurtado N., Walweel K., van Helden D.F., Imtiaz M.S., Knollmann B.C., Laver D.R. Essential role of calmodulin in RyR inhibition by dantrolene. Mol. Pharmacol. 2015, 88:57-63.
145. Seo M.D., Enomoto M., Ishiyama N., Stathopulos P.B., Ikura M. Structural insights into endoplasmic reticulum stored calcium regulation by inositol 14,5-trisphosphate and ryanodine receptors. Biochim. Biophys. Acta 2014, 1853:1980-1991.