Structural determination of the phosphorylation domain of the ryanodine receptor

FEBS Journal

Volumn 279, Issue 20, 2012, Pages 3952-3964

  Sharma, Parveen ^a   Ishiyama, Noboru ^b   Nair, Usha ^a,c   Li, Wenping ^a   Dong, Aiping ^a,c   Miyake, Tetsuaki ^a   Wilson, Aaron ^a   Ryan, Tim ^a   MacLennan, David H ^c   Kislinger, Thomas ^a,b   Ikura, Mitsuhiko ^a,b   Dhe Paganon, Sirano ^a,c,d   Gramolini, Anthony O ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b PRINCESS MARGARET HOSPITAL   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

^d BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

excitation contraction; malignant hyperthermia; phosphorylation site; RyR; X ray crystallography

Indexed keywords

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE; CALCIUM ION; INOSITOL 1,4,5 TRISPHOSPHATE RECEPTOR; ISOPROTEIN; MEMBRANE PROTEIN; RYANODINE RECEPTOR; SERINE;

ARTICLE; BETA SHEET; BINDING SITE; CONTROLLED STUDY; CRYSTAL STRUCTURE; ELECTRON MICROSCOPY; GENE MUTATION; MATHEMATICAL MODEL; NUCLEOTIDE SEQUENCE; PHOSPHORYLATION DOMAIN; PRIORITY JOURNAL; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; PURIFICATION;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; BLOTTING, WESTERN; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CRYOELECTRON MICROSCOPY; CRYSTALLOGRAPHY, X-RAY; HEK293 CELLS; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN ISOFORMS; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RABBITS; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 84867100863     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2012.08755.x     Document Type: Article

References (56)

1. 2+ channels. J Biol Chem 273, 13403-13406.
2. 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.
3. MacLennan DH, &, Phillips MS, (1992) Malignant hyperthermia. Science 256, 789-794.
4. 2+ release channels. Am J Med 104, 470-486.
5. 2+ signalling and muscle disease. Eur J Biochem 267, 5291-5297.
6. Inui M, Saito A, &, Fleischer S, (1987) Isolation of the ryanodine receptor from cardiac sarcoplasmic reticulum and identity with the feet structures. J Biol Chem 262, 15637-15642.
7. 2+-permeable pore of the calcium release channel. J Biol Chem 262, 16636-16643.
8. Lai FA, Erickson H, Block BA, &, Meissner G, (1987) Evidence for a junctional feet-ryanodine receptor complex from sarcoplasmic reticulum. Biochem Biophys Res Commun 143, 704-709.
9. 2+ release channel (ryanodine receptor) of skeletal muscle sarcoplasmic reticulum. J Biol Chem 265, 2244-2256.
10. Suko J, Maurer-Fogy I, Plank B, Bertel O, Wyskovsky W, Hohenegger M, &, Hellmann G, (1993) Phosphorylation of serine 2843 in ryanodine receptor-calcium release channel of skeletal muscle by cAMP-, cGMP- and CaM-dependent protein kinase. Biochim Biophys Acta 1175, 193-206.
11. Ibarra M CA, Wu S, Murayama K, Minami N, Ichihara Y, Kikuchi H, Noguchi S, Hayashi YK, Ochiai R, &, Nishino I, (2006) Malignant hyperthermia in Japan: mutation screening of the entire ryanodine receptor type 1 gene coding region by direct sequencing. Anesthesiology 104, 1146-1154.
12. Robinson R, Carpenter D, Shaw M-A, Halsall J, &, Hopkins P, (2006) Mutations in RYR1 in malignant hyperthermia and central core disease. Hum Mutat 27, 977-989.
13. Serysheva II, Orlova EV, Chiu W, Sherman MB, Hamilton SL, &, Heel MV, (1995) Electron cryomicroscopy and angular reconstitution used to visualize the skeletal muscle calcium release channel. Nat Struct Mol Biol 2, 18-24.
14. Radermacher M, Rao V, Grassucci R, Frank J, Timerman AP, Fleischer S, &, Wagenknecht T, (1994) Cryo-electron microscopy and three-dimensional reconstruction of the calcium release channel/ryanodine receptor from skeletal muscle. J Cell Biol 127, 411-423.
15. Samso M, Wagenknecht T, &, Allen PD, (2005) Internal structure and visualization of transmembrane domains of the RyR1 calcium release channel by cryo-EM. Nat Struct Mol Biol 12, 539-544.
16. Samso M, Feng W, Pessah I, &, Allen PD, (2009) Coordinated movement of cytoplasmic and transmembrane domains of RyR1 upon gating. PLoS Biol 7, e1000085.
17. Amador FJ, Liu S, Ishiyama N, Plevin MJ, Wilson A, MacLennan DH, &, Ikura M, (2009) Crystal structure of type I ryanodine receptor amino-terminal β-trefoil domain reveals a disease-associated mutation 'hot spot' loop. Proc Natl Acad Sci USA 106, 11040-11044.
18. 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, 585-588.
19. Ryan T, Sharma P, Ignatchenko A, MacLennan DH, Kislinger T, &, Gramolini AO, (2011) Identification of novel ryanodine receptor 1 (RyR1) protein interaction with calcium homeostasis endoplasmic reticulum protein (CHERP). J Biol Chem 286, 17060-17068.
20. Zhang L, Kelley J, Schmeisser G, Kobayashi YM, &, Jones LR, (1997) Complex formation between junctin, triadin, calsequestrin, and the ryanodine receptor. J Biol Chem 272, 23389-23397.
21. Brillantes A-MB, Ondrias K, Scott A, Kobrinsky E, Ondriasová E, Moschella MC, Jayaraman T, Landers M, Ehrlich BE, &, Marks AR, (1994) Stabilization of calcium release channel (ryanodine receptor) function by FK506-binding protein. Cell 77, 513-523.
22. Dolinski K, &, Botstein D, (2007) Orthology and functional conservation in eukaryotes. Annu Rev Genet 41, 465-507.
23. Sharma P, Nair U, Li W, Ryan T, Miyake T, Dong A, Kislinger T, Dhe-Paganon S, &, Gramolini A, (2011) Comprehensive analysis of ryanodine receptor through proteomic interaction analysis and high resolution crystal structure determination. Circulation 124, A15352.
24. Obenauer JC, Cantley LC, &, Yaffe MB, (2003) Scansite 2.0: proteome-wide prediction of cell signaling interactions using short sequence motifs. Nucleic Acids Res 31, 3635-3641.
25. Holm L, Kääriäinen S, Wilton C, &, Plewczynski D, (2006) Using Dali for structural comparison of proteins. Curr Protoc Bioinformatics 14, 5.5.1-5.5.24.
26. Wriggers W, Milligan RA, &, McCammon JA, (1999) Situs: a package for docking crystal structures into low-resolution maps from electron microscopy. J Struct Biol 125, 185-195.
27. Meng X, Xiao B, Cai S, Huang X, Li F, Bolstad J, Trujillo R, Airey J, Chen SR, Wagenknecht T, et al,. (2007) Three-dimensional localization of serine 2808, a phosphorylation site in cardiac ryanodine receptor. J Biol Chem 282, 25929-25939.
28. 2030, in the three-dimensional structure of cardiac ryanodine receptor. Biochem J 410, 261-270.
29. 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, 1201-1211.
30. Hamilton SL, &, Serysheva II, (2009) Ryanodine receptor structure: progress and challenges. J Biol Chem 284, 4047-4051.
31. Galli L, Orrico A, Lorenzini S, Censini S, Falciani M, Covacci A, Tegazzin V, &, Sorrentino V, (2006) Frequency and localization of mutations in the 106 exons of the RYR1 gene in 50 individuals with malignant hyperthermia. Hum Mutat 27, 830.
32. Monnier N, Kozak-Ribbens G, Krivosic-Horber R, Nivoche Y, Qi D, Kraev N, Loke J, Sharma P, Tegazzin V, Figarella-Branger D, et al,. (2005) Correlations between genotype and pharmacological, histological, functional, and clinical phenotypes in malignant hyperthermia susceptibility. Hum Mutat 26, 413-425.
33. Zhou H, Jungbluth H, Sewry CA, Feng L, Bertini E, Bushby K, Straub V, Roper H, Rose MR, Brockington M, et al,. (2007) Molecular mechanisms and phenotypic variation in RYR1-related congenital myopathies. Brain 130, 2024-2036.
34. Bosanac I, Michikawa T, Mikoshiba K, &, Ikura M, (2004) Structural insights into the regulatory mechanism of IP3 receptor. Biochim Biophys Acta 1742, 89-102.
35. Berridge MJ, (1993) Inositol trisphosphate and calcium signalling. Nature 361, 315-325.
36. Seo M-D, Velamakanni S, Ishiyama N, Stathopulos PB, Rossi AM, Khan SA, Dale P, Li C, Ames JB, Ikura M, et al,. (2012) Structural and functional conservation of key domains in InsP3 and ryanodine receptors. Nature 483, 108-112.
37. 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, 2587-2600.
38. Pearson RB, Woodgett JR, Cohen P, &, Kemp BE, (1985) Substrate specificity of a multifunctional calmodulin-dependent protein kinase. J Biol Chem 260, 14471-14476.
39. 2+- calmodulin-dependent protein kinases IV and II reveals shared and distinctive features. J Biol Chem 273, 3166-3172.
40. Westcott EB, &, Jackson WF, (2011) Heterogeneous function of ryanodine receptors, but not IP3 receptors, in hamster cremaster muscle feed arteries and arterioles. Am J Physiol 300, H1616-H1630.
41. Chu A, Sumbilla C, Inesi G, Jay SD, &, Campbell KP, (1990) Specific association of calmodulin-dependent protein kinase and related substrates with the junctional sarcoplasmic reticulum of skeletal muscle. Biochemistry 29, 5899-5905.
42. 2+/calmodulin-dependent protein kinase II phosphorylation regulates the cardiac ryanodine receptor. Circ Res 94, e61-e70.
43. Said M, Becerra R, Valverde CA, Kaetzel MA, Dedman JR, Mundiña-Weilenmann C, Wehrens XH, Vittone L, &, Mattiazzi A, (2011) Calcium-calmodulin dependent protein kinase II (CaMKII): a main signal responsible for early reperfusion arrhythmias. J Mol Cell Cardiol 51, 936-944.
44. Pogwizd SM, &, Bers DM, (2004) Cellular basis of triggered arrhythmias in heart failure. Trends Cardiovasc Med 14, 61-66.
45. van Oort RJ, McCauley MD, Dixit SS, Pereira L, Yang Y, Respress JL, Wang Q, De Almeida AC, Skapura DG, Anderson ME, et al,. (2010) Ryanodine receptor phosphorylation by calcium/calmodulin-dependent protein kinase II promotes life-threatening ventricular arrhythmias in mice with heart failure. Circulation 122, 2669-2679.
46. Farr MA, &, Basson CT, (2004) Sparking the failing heart. New Engl J Med 351, 185-187.
47. 2+ leak, and atrial fibrillation. Trends Cardiovasc Med 20, 30-34.
48. Alenkin D, Yermekbayeva L, Mujib S, Vesterberg A, Newman E, Yamazaki K, Cossar D, &, Dhe-Paganon S, (2011) A centrifugation-free high-throughput protein purification system using in-line microfluidization. Protein Expr Purif 79, 204-209.
49. Minor W, Cymborowski M, Otwinowski Z, &, Chruszcz M, (2006) HKL-3000: the integration of data reduction and structure solution-from diffraction images to an initial model in minutes. Acta Crystallogr D Biol Crystallogr 62, 859-866.
50. Sheldrick GM, (2008) A short history of SHELX. Acta Crystallogr A 64, 112-122.
51. Terwilliger TC, &, Berendzen J, (1999) Automated MAD and MIR structure solution. Acta Crystallogr D Biol Crystallogr 55, 849-861.
52. Terwilliger T, (2003) Automated main-chain model building by template matching and iterative fragment extension. Acta Crystallogr D Biol Crystallogr 59, 38-44.
53. Emsley P, &, Cowtan K, (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60, 2126-2132.
54. Bricogne G, Blanc E, Brandl M, Flensburg C, Keller P, Paciorek W, Roversi P, Smart OS, Vonrhein C, &, Womack TO, (2009) BUSTER, Version 2.8.0. Global Phasing Ltd, Cambridge, UK.
55. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, &, Ferrin TE, (2004) UCSF Chimera-a visualization system for exploratory research and analysis. J Comput Chem 25, 1605-1612.
56. 2+ signaling in HEK-293 and skeletal muscle cells expressing recombinant ryanodine receptors harboring malignant hyperthermia and central core disease mutations. J Biol Chem 280, 15380-15389.