The deletion of exon 3 in the cardiac ryanodine receptor is rescued by β strand switching

Structure

Volumn 19, Issue 6, 2011, Pages 790-798

  Lobo, Paolo A ^a   Kimlicka, Lynn ^a   Tung, Ching Chieh ^a   Van Petegem, Filip ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; RYANODINE RECEPTOR 1; RYANODINE RECEPTOR 2; TREFOIL PEPTIDE;

ALLOSTERISM; AMINO TERMINAL SEQUENCE; ARTICLE; BETA SHEET; CALCIUM TRANSPORT; CONTROLLED STUDY; CRYSTAL STRUCTURE; EXON; GENE DELETION; MOLECULAR MECHANICS; PLASTICITY; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN STRUCTURE; SEQUENCE ALIGNMENT; THERMOSTABILITY;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; EXONS; GENETIC DISEASES, INBORN; HUMANS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MICE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MYOCARDIUM; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PROTEIN UNFOLDING; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL; SEQUENCE DELETION; STRUCTURAL HOMOLOGY, PROTEIN; SURFACE PROPERTIES; TACHYCARDIA, VENTRICULAR; TRANSITION TEMPERATURE;

LOTUS;

EID: 79958173577     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2011.03.016     Document Type: Article

References (53)

1. P.D. Adams, P.V. Afonine, G. Bunkoczi, V.B. Chen, I.W. Davis, N. Echols, J.J. Headd, L.W. Hung, G.J. Kapral, and R.W. Grosse-Kunstleve PHENIX: a comprehensive Python-based system for macromolecular structure solution Acta Crystallogr. D Biol. Crystallogr. 66 2010 213 221
2. F.J. Amador, S. Liu, N. Ishiyama, M.J. Plevin, A. Wilson, D.H. MacLennan, and M. Ikura Crystal structure of type I ryanodine receptor amino-terminal beta-trefoil domain reveals a disease-associated mutation "hot spot" loop Proc. Natl. Acad. Sci. USA 106 2009 11040 11044
3. D.M. Bers Macromolecular complexes regulating cardiac ryanodine receptor function J. Mol. Cell. Cardiol. 37 2004 417 429 (Pubitemid 38953370)
4. M.J. Betzenhauser, and A.R. Marks Ryanodine receptor channelopathies Pflugers Arch. 460 2010 467 480
5. Z.A. Bhuiyan, M.P. van den Berg, J.P. van Tintelen, M.T. Bink-Boelkens, A.C. Wiesfeld, M. Alders, A.V. Postma, I. van Langen, M.M. Mannens, and A.A. Wilde Expanding spectrum of human RYR2-related disease: new electrocardiographic, structural, and genetic features Circulation 116 2007 1569 1576 (Pubitemid 47511420)
6. A. Cabello, and J.R. Ricoy-Campo [Congenital myopathies] Rev. Neurol. 37 2003 779 786
7. G. d'Amati, A. Bagattin, B. Bauce, A. Rampazzo, C. Autore, C. Basso, K. King, M.D. Romeo, P. Gallo, and G. Thiene Juvenile sudden death in a family with polymorphic ventricular arrhythmias caused by a novel RyR2 gene mutation: evidence of specific morphological substrates Hum. Pathol. 36 2005 761 767 (Pubitemid 41112031)
8. H. Edelhoch Spectroscopic determination of tryptophan and tyrosine in proteins Biochemistry 6 1967 1948 1954
9. P. Emsley, and K. Cowtan Coot: model-building tools for molecular graphics Acta Crystallogr. D Biol. Crystallogr. 60 2004 2126 2132 (Pubitemid 41742764)
10. H.A. Fozzard Afterdepolarizations and triggered activity Basic Res. Cardiol. 87 Suppl 2 1992 105 113 (Pubitemid 23081262)
11. C.H. George, G.V. Higgs, and F.A. Lai Ryanodine receptor mutations associated with stress-induced ventricular tachycardia mediate increased calcium release in stimulated cardiomyocytes Circ. Res. 93 2003 531 540 (Pubitemid 37163233)
12. C.H. George, H. Jundi, N.L. Thomas, D.L. Fry, and F.A. Lai Ryanodine receptors and ventricular arrhythmias: emerging trends in mutations, mechanisms and therapies J. Mol. Cell. Cardiol. 42 2007 34 50 (Pubitemid 44958614)
13. G. Giannini, A. Conti, S. Mammarella, M. Scrobogna, and V. Sorrentino The ryanodine receptor/calcium channel genes are widely and differentially expressed in murine brain and peripheral tissues J. Cell Biol. 128 1995 893 904
14. Y. Hakamata, J. Nakai, H. Takeshima, and K. Imoto Primary structure and distribution of a novel ryanodine receptor/calcium release channel from rabbit brain FEBS Lett. 312 1992 229 235
15. N. Ikemoto, and T. Yamamoto Regulation of calcium release by interdomain interaction within ryanodine receptors Front. Biosci. 7 2002 d671 d683
16. D. Jiang, B. Xiao, L. Zhang, and S.R. Chen Enhanced basal activity of a cardiac Ca2+ release channel (ryanodine receptor) mutant associated with ventricular tachycardia and sudden death Circ. Res. 91 2002 218 225 (Pubitemid 34875676)
17. D. Jiang, B. Xiao, D. Yang, R. Wang, P. Choi, L. Zhang, H. Cheng, and S.R. Chen RyR2 mutations linked to ventricular tachycardia and sudden death reduce the threshold for store-overload-induced Ca2+ release (SOICR) Proc. Natl. Acad. Sci. USA 101 2004 13062 13067 (Pubitemid 39167583)
18. D. Jiang, R. Wang, B. Xiao, H. Kong, D.J. Hunt, P. Choi, L. Zhang, and S.R. Chen Enhanced store overload-induced Ca2+ release and channel sensitivity to luminal Ca2+ activation are common defects of RyR2 mutations linked to ventricular tachycardia and sudden death Circ. Res. 97 2005 1173 1181
19. D. Jiang, W. Chen, R. Wang, L. Zhang, and S.R. Chen Loss of luminal Ca2+ activation in the cardiac ryanodine receptor is associated with ventricular fibrillation and sudden death Proc. Natl. Acad. Sci. USA 104 2007 18309 18314 (Pubitemid 350210863)
20. D. Jiang, W. Chen, J. Xiao, R. Wang, H. Kong, P.P. Jones, L. Zhang, B. Fruen, and S.R. Chen Reduced threshold for luminal Ca2+ activation of RyR1 underlies a causal mechanism of porcine malignant hyperthermia J. Biol. Chem. 283 2008 20813 20820
21. P.P. Jones, X. Meng, B. Xiao, S. Cai, J. Bolstad, T. Wagenknecht, Z. Liu, and S.R. Chen Localization of PKA phosphorylation site, Ser(2030), in the three-dimensional structure of cardiac ryanodine receptor Biochem. J. 410 2008 261 270 (Pubitemid 351346184)
22. A. Koop, P. Goldmann, S.R. Chen, R. Thieleczek, and M. Varsanyi ARVC-related mutations in divergent region 3 alter functional properties of the cardiac ryanodine receptor Biophys. J. 94 2008 4668 4677
23. P.J. Laitinen, K.M. Brown, K. Piippo, H. Swan, J.M. Devaney, B. Brahmbhatt, E.A. Donarum, M. Marino, N. Tiso, and M. Viitasalo Mutations of the cardiac ryanodine receptor (RyR2) gene in familial polymorphic ventricular tachycardia Circulation 103 2001 485 490 (Pubitemid 32116230)
24. M.W. Ledbetter, J.K. Preiner, C.F. Louis, and J.R. Mickelson Tissue distribution of ryanodine receptor isoforms and alleles determined by reverse transcription polymerase chain reaction J. Biol. Chem. 269 1994 31544 31551 (Pubitemid 24379513)
25. S.E. Lehnart, X.H. Wehrens, S. Reiken, S. Warrier, A.E. Belevych, R.D. Harvey, W. Richter, S.L. Jin, M. Conti, and A.R. Marks Phosphodiesterase 4D deficiency in the ryanodine-receptor complex promotes heart failure and arrhythmias Cell 123 2005 25 35 (Pubitemid 41414526)
26. S.E. Lehnart, M. Mongillo, A. Bellinger, N. Lindegger, B.X. Chen, W. Hsueh, S. Reiken, A. Wronska, L.J. Drew, and C.W. Ward Leaky Ca2+ release channel/ryanodine receptor 2 causes seizures and sudden cardiac death in mice J. Clin. Invest. 118 2008 2230 2245 (Pubitemid 351872341)
27. Z. Liu, J. Zhang, M.R. Sharma, P. Li, S.R. Chen, and T. Wagenknecht Three-dimensional reconstruction of the recombinant type 3 ryanodine receptor and localization of its amino terminus Proc. Natl. Acad. Sci. USA 98 2001 6104 6109 (Pubitemid 32488200)
28. Z. Liu, R. Wang, X. Tian, X. Zhong, J. Gangopadhyay, R. Cole, N. Ikemoto, S.R. Chen, and T. Wagenknecht Dynamic, inter-subunit interactions between the N-terminal and central mutation regions of cardiac ryanodine receptor J. Cell Sci. 123 2010 1775 1784
29. P.A. Lobo, and F. Van Petegem Crystal structures of the N-terminal domains of cardiac and skeletal muscle ryanodine receptors: insights into disease mutations Structure 17 2009 1505 1514
30. S.J. Ludtke, I.I. Serysheva, S.L. Hamilton, and W. Chiu The pore structure of the closed RyR1 channel Structure 13 2005 1203 1211 (Pubitemid 41111487)
31. D.H. MacLennan, and M.S. Phillips Malignant hyperthermia Science 256 1992 789 794
32. D.H. MacLennan, and S.R. Chen Store overload-induced Ca2+ release as a triggering mechanism for CPVT and MH episodes caused by mutations in RYR and CASQ genes J. Physiol. 587 2009 3113 3115
33. E. Marban, S.W. Robinson, and W.G. Wier Mechanisms of arrhythmogenic delayed and early afterdepolarizations in ferret ventricular muscle J. Clin. Invest. 78 1986 1185 1192 (Pubitemid 17181555)
34. A. Marjamaa, P. Laitinen-Forsblom, A.M. Lahtinen, M. Viitasalo, L. Toivonen, K. Kontula, and H. Swan Search for cardiac calcium cycling gene mutations in familial ventricular arrhythmias resembling catecholaminergic polymorphic ventricular tachycardia BMC Med. Genet. 10 2009 12
35. S.O. Marx, S. Reiken, Y. Hisamatsu, T. Jayaraman, D. Burkhoff, N. Rosemblit, and A.R. Marks PKA phosphorylation dissociates FKBP12.6 from the calcium release channel (ryanodine receptor): defective regulation in failing hearts Cell 101 2000 365 376
36. A.A. Maximciuc, J.A. Putkey, Y. Shamoo, and K.R. Mackenzie Complex of calmodulin with a ryanodine receptor target reveals a novel, flexible binding mode Structure 14 2006 1547 1556 (Pubitemid 44486817)
37. A.J. McCoy, R.W. Grosse-Kunstleve, P.D. Adams, M.D. Winn, L.C. Storoni, and R.J. Read Phaser crystallographic software J. Appl. Crystallgr. 40 2007 658 674 (Pubitemid 47080256)
38. A. Medeiros-Domingo, Z.A. Bhuiyan, D.J. Tester, N. Hofman, H. Bikker, J.P. van Tintelen, M.M. Mannens, A.A. Wilde, and M.J. Ackerman 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. 54 2009 2065 2074
39. G.N. Murshudov, A.A. Vagin, and E.J. Dodson Refinement of macromolecular structures by the maximum-likelihood method Acta Crystallogr. D Biol. Crystallogr. 53 1997 240 255 (Pubitemid 27235885)
40. S.G. Priori, C. Napolitano, N. Tiso, M. Memmi, G. Vignati, R. Bloise, V. Sorrentino, and G.A. Danieli Mutations in the cardiac ryanodine receptor gene (hRyR2) underlie catecholaminergic polymorphic ventricular tachycardia Circulation 103 2001 196 200 (Pubitemid 32095402)
41. R. Robinson, D. Carpenter, M.A. Shaw, J. Halsall, and P. Hopkins Mutations in RYR1 in malignant hyperthermia and central core disease Hum. Mutat. 27 2006 977 989 (Pubitemid 44454050)
42. M. Samso, T. Wagenknecht, and P.D. Allen Internal structure and visualization of transmembrane domains of the RyR1 calcium release channel by cryo-EM Nat. Struct. Mol. Biol. 12 2005 539 544 (Pubitemid 43085885)
43. M. Samso, W. Feng, I.N. Pessah, and P.D. Allen Coordinated movement of cytoplasmic and transmembrane domains of RyR1 upon gating PLoS Biol. 7 2009 e85
44. M.R. Sharma, P. Penczek, R. Grassucci, H.B. Xin, S. Fleischer, and T. Wagenknecht Cryoelectron microscopy and image analysis of the cardiac ryanodine receptor J. Biol. Chem. 273 1998 18429 18434 (Pubitemid 28334770)
45. S. Shepherd, F. Ellis, J. Halsall, P. Hopkins, and R. Robinson RYR1 mutations in UK central core disease patients: more than just the C-terminal transmembrane region of the RYR1 gene J. Med. Genet. 41 2004 e33
46. F.W. Studier Protein production by auto-induction in high density shaking cultures Protein Expr. Purif. 41 2005 207 234
47. S. Takasawa, M. Kuroki, K. Nata, N. Noguchi, T. Ikeda, A. Yamauchi, H. Ota, A. Itaya-Hironaka, S. Sakuramoto-Tsuchida, and I. Takahashi A novel ryanodine receptor expressed in pancreatic islets by alternative splicing from type 2 ryanodine receptor gene Biochem. Biophys. Res. Commun. 397 2010 140 145
48. H. Tateishi, M. Yano, M. Mochizuki, T. Suetomi, M. Ono, X. Xu, H. Uchinoumi, S. Okuda, T. Oda, and S. Kobayashi Defective domain-domain interactions within the ryanodine receptor as a critical cause of diastolic Ca2+ leak in failing hearts Cardiovasc. Res. 81 2009 536 545
49. N.L. Thomas, C.H. George, A.J. Williams, and F.A. Lai Ryanodine receptor mutations in arrhythmias: advances in understanding the mechanisms of channel dysfunction Biochem. Soc. Trans. 35 2007 946 951 (Pubitemid 350206402)
50. C.C. Tung, P.A. Lobo, L. Kimlicka, and F. Van Petegem The amino-terminal disease hotspot of ryanodine receptors forms a cytoplasmic vestibule Nature 468 2010 585 588
51. R. Wang, W. Chen, S. Cai, J. Zhang, J. Bolstad, T. Wagenknecht, Z. Liu, and S.R. Chen Localization of an NH(2)-terminal disease-causing mutation hot spot to the "clamp" region in the three-dimensional structure of the cardiac ryanodine receptor J. Biol. Chem. 282 2007 17785 17793 (Pubitemid 47100309)
52. N.T. Wright, B.L. Prosser, K.M. Varney, D.B. Zimmer, M.F. Schneider, and D.J. Weber S100A1 and calmodulin compete for the same binding site on ryanodine receptor J. Biol. Chem. 283 2008 26676 26683
53. R. Zalk, S.E. Lehnart, and A.R. Marks Modulation of the ryanodine receptor and intracellular calcium Annu. Rev. Biochem. 76 2007 367 385