Identification of ATP-Binding Regions in the RyR1 Ca2+ Release Channel

PLoS ONE

Volumn 7, Issue 11, 2012, Pages

  Popova, Olga B ^a   Baker, Mariah R ^a   Tran, Tina P ^a   Le, Tri ^a   Serysheva, Irina I ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 AZIDOADENOSINE 5' TRIPHOSPHATE 2',3' BIOTIN LONG CHAIN HYDRAZONE; ADENOSINE TRIPHOSPHATE; AMINO ACID; AZIDE; GLYCINE; RYANODINE RECEPTOR 1; TETRAMER; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ANIMAL TISSUE; ARTICLE; BINDING SITE; BIOTINYLATION; CELL LABELING; CONCENTRATION RESPONSE; CONFORMATIONAL TRANSITION; CYTOPLASM; ENZYME ACTIVATION; IC 50; MOLECULAR WEIGHT; NONHUMAN; NUCLEOTIDE BINDING SITE; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN CROSS LINKING; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; REGULATORY MECHANISM; SEQUENCE ANALYSIS;

ADENOSINE TRIPHOSPHATE; AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; AZIDES; BINDING SITES; CONSENSUS SEQUENCE; CONSERVED SEQUENCE; HYDRAZONES; MOLECULAR SEQUENCE DATA; PROTEIN ISOFORMS; PROTEIN STRUCTURE, TERTIARY; PROTEOLYSIS; RABBITS; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL; SEQUENCE ALIGNMENT;

EID: 84868674865     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0048725     Document Type: Article

References (74)

1. Timerman AP, Ogunbumni E, Freund E, Wiederrecht G, Marks AR, et al. (1993) The calcium release channel of sarcoplasmic reticulum is modulated by FK-506-binding protein. Dissociation and reconstitution of FKBP-12 to the calcium release channel of skeletal muscle sarcoplasmic reticulum. J Biol Chem 268: 22992-22999.
2. Brillantes AB, Ondrias K, Scott A, Kobrinsky E, Ondriasova E, et al. (1994) Stabilization of calcium release channel (ryanodine receptor) function by FK506-binding protein. Cell 77: 513-523.
3. Yamaguchi N, Xu L, Pasek DA, Evans KE, Meissner G, (2003) Molecular basis of calmodulin binding to cardiac muscle Ca2+ release channel (ryanodine receptor). J Biol Chem 278: 23480-23486.
4. 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: 439-445.
5. 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: 2244-2256.
6. Du GG, Sandhu B, Khanna VK, Guo XH, MacLennan DH, (2002) Topology of the Ca2+ release channel of skeletal muscle sarcoplasmic reticulum (RyR1). Proc Natl Acad Sci U S A 99: 16725-16730.
7. Coronado R, Morrissette J, Sukhareva M, Vaughan DM, (1994) Structure and function of ryanodine receptors. Am J Physiol 266: C1485-1504.
8. Meissner G, (1994) Ryanodine receptor/Ca2+ release channels and their regulation by endogenous effectors. Annu Rev Physiol 56: 485-508.
9. Ogawa Y, (1994) Role of ryanodine receptors. Crit Rev Biochem Mol Biol 29: 229-274.
10. Hamilton SL, Serysheva II, (2008) Ryanodine receptor structure: Progress and challenges. J Biol Chem 284: 4047-4051.
11. Miki T, Nagashima K, Seino S, (1999) The structure and function of the ATP-sensitive K+ channel in insulin-secreting pancreatic beta-cells. J Mol Endocrinol 22: 113-123.
12. Ashcroft FM, (2006) K(ATP) channels and insulin secretion: a key role in health and disease. Biochem Soc Trans 34: 243-246.
13. Aguilar-Bryan L, Nichols CG, Wechsler SW, Clement JP 4th, Boyd AE 3rd, et al (1995) Cloning of the beta cell high-affinity sulfonylurea receptor: a regulator of insulin secretion. Science 268: 423-426.
14. Inagaki N, Gonoi T, Clement JP 4th, Namba N, Inazawa J, et al (1995) Reconstitution of IKATP: an inward rectifier subunit plus the sulfonylurea receptor. Science 270: 1166-1170.
15. Meissner G, (1984) Adenine nucleotide stimulation of Ca2+-induced Ca2+ release in sarcoplasmic reticulum. J Biol Chem 259: 2365-2374.
16. Lai FA, Erickson HP, Rousseau E, Liu QY, Meissner G, (1988) Purification and reconstitution of the calcium release channel from skeletal muscle. Nature 331: 315-319.
17. Liu QY, Lai FA, Rousseau E, Jones RV, Meissner G, (1989) Multiple conductance states of the purified calcium release channel complex from skeletal sarcoplasmic reticulum. Biophys J 55: 415-424.
18. Laver DR, (2007) Ca2+ stores regulate ryanodine receptor Ca2+ release channels via luminal and cytosolic Ca2+ sites. Biophys J 92: 3541-3555.
19. Smith JS, Coronado R, Meissner G, (1986) Single-channel measurements of calcium release channel from skeletal muscle sarcoplasmic reticulum. J Gen Physiol 88: 573-588.
20. Laver DR, Lenz GK, Lamb GD, (2001) Regulation of the calcium release channel from rabbit skeletal muscle by the nucleotides ATP, AMP, IMP and adenosine. J Physiol 537: 763-778.
21. Rousseau E, Ladine J, Liu QY, Meissner G, (1988) Activation of the Ca2+ release channel of skeletal muscle sarcoplasmic reticulum by caffeine and related compounds. Arch Biochem Biophys 267: 75-86.
22. Zucchi R, Ronca-Testoni S, (1997) The sarcoplasmic reticulum Ca2+ channel/ryanodine receptor: modulation by endogenous effectors, drugs and disease states. Pharmacol Rev 49: 1-51.
23. Laver DR, (2010) Regulation of RyR1 channel gating by Ca2+, Mg2+ and ATP. In: Current Topics in Membranes Serysheva II, ed. 66: 69-89.
24. Hohnegger M, Herrmann-Frank A, Richter M, Lehmann-Horn F, (1995) Activation and labelling of the purified skeletal muscle ryanodine receptor by an oxydized ATP analog. Biochem J 308: 119-125.
25. Dias JM, Szegedi C, Jona I, Vogel PD, (2006) Insights into the regulation of the ryanodine receptor: differential effects of Mg2+ and Ca2+ on ATP binding. Biochemistry 45: 9408-9415.
26. Dias JM, Vogel PD, (2009) Effects of small molecule modulators on ATP binding to skeletal ryanodine receptor. Protein J 28: 240-246.
27. Smith JS, Coronado R, Meissner G, (1985) Sarcoplasmic reticulum contains adenine nucleotide-activated calcium channels. Nature 316: 446-449.
28. Serysheva II, Ludtke S, Chiu W, Hamilton SL, (2000) Structure of skeletal muscle calcium release channel by electron cryomicroscopy: approaching high resolution. Biophys Journal 78: 485A.
29. Chan WM, Welch W, Sitsapesan R, (2003) Structural characteristics that govern binding to, and modulation through the cardiac ryanodine receptor nucleotide binding site. The Journal of Biological Chemistry 63: 174-182.
30. Walker JE, Saraste M, Runswick MJ, Gay NJ, (1982) Distantly related sequences in the alpha- and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. Embo J 1: 945-951.
31. Wierenga RK, Hol WG, (1983) Predicted nucleotide-binding properties of p21 protein and its cancer-associated variant. Nature 302: 842-844.
32. Martin J, Geromanos S, Tempst P, Hartl FU, (1993) Identification of nucleotide-binding regions in the chaperonin proteins GroEL and GroES. Nature 366: 279-282.
33. Otsu K, Willard HF, Khanna VK, Zorzato F, Green NM, et al. (1990) Molecular cloning of cDNA encoding the Ca2+ release channel (ryanodine receptor) of rabbit cardiac muscle sarcoplasmic reticulum. J Biol Chem 265: 13472-13483.
34. Du GG, Oyamada H, Khanna VK, MacLennan DH, (2001) Mutations to Gly2370, Gly2373 or Gly2375 in malignant hyperthermia domain 2 decrease caffeine and cresol sensitivity of the rabbit skeletal-muscle Ca2+-release channel (ryanodine receptor isoform 1). Biochem J 360: 97-105.
35. Hawkes MJ, Diaz-Munoz M, Hamilton SL, (1989) A procedure for purification of the ryanodine receptor from skeletal muscle. Membr Biochem 8: 133-145.
36. Serysheva II, Schatz M, van Heel M, Chiu W, Hamilton SL, (1999) Structure of the Skeletal Muscle Calcium Release Channel activated with Ca2+ and AMP-PCP. Biophysical journal 77: 1936-1944.
37. Zhang H, Zhang JZ, Danila CI, Hamilton SL, (2003) A Noncontiguous, Intersubunit Binding Site for Calmodulin on the Skeletal Muscle Ca2+ Release Channel. J Biol Chem 278: 8348-8355.
38. Laemmli UK, (1970) Cleavage of strcutural proteins during assembly of the head of bacteriophage T4. Nature 227: 680-683.
39. Le Gendre N, Matsudaira P (1989) In:Matsudaira P T, ed. A practical guide to protein and peptide purification for microsequencing. 49-69.
40. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948.
41. Zarka A, Shoshan-Barmatz V, (1993) Characterization and photoaffinity labeling of the ATP binding site of the ryanodine receptor from skeletal muscle. Eur J Biochem 213: 147-154.
42. Guo W, Campbell KP, (1995) Association of triadin with the ryanodine receptor and calsequestrin in the lumen of the sarcoplasmic reticulum. J Biol Chem 270: 9027-9030.
43. Zhang X, Wen J, Bidasee KR, Besch HR Jr, Rubin RP, (1997) Ryanodine receptor expression is associated with intracellular Ca2+ release in rat parotid acinar cells. Am J Physiol 273: C1306-1314.
44. Yamaguchi N, Kasai M, (1998) Identification of 30 kDa calsequestrin-binding protein, which regulates calcium release from sarcoplasmic reticulum of rabbit skeletal muscle. Biochem J 335: 541-547.
45. MacLennan DH, (1974) Isolation of a second form of calsequestrin. J Biol Chem 249: 980-984.
46. Tung CC, Lobo PA, Kimlicka L, Van Petegem F, (2010) The amino-terminal disease hotspot of ryanodine receptors forms a cytoplasmic vestibule. Nature 468: 585-588.
47. Galperin MY, Koonin EV, (1997) A diverse superfamily of enzymes with ATP-dependent carboxylate-amine/thyol ligase activity. Protein Sci 6: 2639-2643.
48. Betzenhauser MJ, Yule DI, (2010) Regulation of inositol 1,4,5-triphosphate receptors by phosphorylation and adenine nucleotides. In: Current Topics in Membranes Serysheva II, ed. 66: 273-298.
49. Maes K, Missiaen L, Parys JB, De Smet P, Sienaert I, et al. (2001) Mapping of the atp-binding sites on inositol 1,4,5-trisphosphate receptor type 1 and type 3 homotetramers by controlled proteolysis and photoaffinity labeling. J Biol Chem 276: 3492-3497.
50. Kawakami H, Ozaki S, Suzuki S, Nakamura K, Senriuchi T, et al. (2006) The exceptionally tight affinity of DnaA for ATP/ADP requires a unique aspartic acid residue in the AAA+ sensor 1 motif. Molecular Microbiology 62: 1310-1324.
51. Jha S, Karnani N, Dhar SK, Mukhopadhayay K, Shukla S, et al. (2003) Purification and characterization of the N-terminal nucleotide binding domain of an ABC drug transporter of Candida albicans: uncommon cysteine 193 of Walker A is critical for ATP hydrolysis. Biochemistry 42: 10822-10832.
52. Jeoung J-H, Giese T, Grunwald M, Dobbek H, (2009) CooCl from Carboxydothermus hydrogenformans is a nickel-binding ATPase. Biochemistry 48: 11505-11513.
53. Nagy M, Wu H-C, Liu Z, Kedzierska-Mieszkowska S, Zolkiewski M, (2009) Walker-A threonine couples nucleotide occupancy with the chaperone activity of the AAA+ ATPase ClpB. protein Sci 18: 287-293.
54. Blayney L, Nomikos M, Beck K, D'Cruz L, McDonald E, et al. (2010) Distincrt properties of CPVT mutations in the central domain of human RyR2. Biophys J 98: Suppl 1. Abstarct 2649-Pos.
55. Yamamoto Y, Ikemoto N, (2002) Spectroscopic monitoring of local comformational changes during the intramolecular domain-domain interaction of the ryanodine receptor. Biochemistry 41: 1492-1501.
56. Baker ML, Serysheva, II, Sencer S, Wu Y, Ludtke SJ, et al. (2002) The skeletal muscle Ca2+ release channel has an oxidoreductase-like domain. Proc Natl Acad Sci U S A 99: 12155-12160.
57. Liu Z, Wang R, Zhang J, Chen SR, Wagenknecht T, (2005) Localization of a disease-associated mutation site in the three-dimensional structure of the cardiac muscle ryanodine receptor. J Biol Chem 280: 37941-37947.
58. Liu Z, Zhang J, Sharma MR, Li P, Chen SR, et al. (2001) Three-dimensional reconstruction of the recombinant type 3 ryanodine receptor and localization of its amino terminus. Proc Natl Acad Sci U S A 98: 6104-6109.
59. Jones PP, Meng X, Xiao B, Cai S, Bolstad J, et al. (2008) Localization of PKA phosphorylation site, Ser(2030), in the three-dimensional structure of cardiac ryanodine receptor. Biochem J 410: 261-270.
60. Meng X, Xiao B, Cai S, Huang X, Li F, et al. (2007) Three-dimensional localization of serine 2808, a phosphorylation site in cardiac ryanodine receptor. J Biol Chem 282: 25929-25939.
61. Peralvez-Marin A, Tae HS, Board PG, Casarotto MG, Dulhunty AF, et al. (2011) 3D mapping of the SPRY2 domain of ryanodine receptor 1 by single-particle cryo-EM. PloS One 282: 17785-17793.
62. Liu Z, Wang R, Tian X, Zhong X, Gangopadhyay J, et al. (2010) Dynamic, inter-subunit interactions between the N-terminal and central mutation regions of cardiac ryanodine receptor. J Cell Sci 123: 1775-1784.
63. Ludtke SJ, Serysheva, II, Hamilton SL, Chiu W, (2005) The pore structure of the closed RyR1 channel. Structure (Camb) 13: 1203-1211.
64. Serysheva, II, Ludtke SJ, Baker ML, Cong Y, Topf M, et al. (2008) Subnanometer-resolution electron cryomicroscopy-based domain models for the cytoplasmic region of skeletal muscle RyR channel. Proc Natl Acad Sci U S A 105: 9610-9615.
65. Wang R, Chen W, Cai S, Zhang J, Bolstad J, et al. (2007) 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: 17785-17793.
66. Tae HS, Casarotto MG, Dulhunty AF, (2009) Ubiqitous SPRY domains and their role in the skeletal type ryanodine receptor. Eur Biophys J 39: 51-59.
67. Paolini C, Protasi F, Franzini-Armstrong C, (2004) The relative position of RyR feet and DHPR tetrads in skeletal muscle. J Mol Biol 342: 145-153.
68. Pegan S, Arrabit C, Zhou W, Kwiatkowski W, Collins A, et al. (2005) Cytoplasmic domain structures of Kir2.1 and Kir3.1 show sites for modulating gating and rectification. Nat Neurosci 8: 279-287.
69. Kuo A, Gulbis JM, Antcliff JF, Rahman T, Lowe ED, et al. (2003) Crystal structure of the potassium channel KirBac1.1 in the closed state. Science 300: 1922-1926.
70. Nishida M, Cadene M, Chait BT, MacKinnon R, (2007) Crystal structure of a Kir3.1-prokaryotic Kir channel chimera. EMBO J 26: 4005-4015.
71. Haider S, Grottesi A, Hall BA, Ashcroft FM, Sansom MSP, (2005) Conformational dynamics of the ligand-binding domain of inward rectifier K channels as revealed by molecular dynamics simulations: toward an understanding of Kir channel gating. Biophys J 88: 3310-3320.
72. Liu Z, Zhang J, Li P, Chen SR, Wagenknecht T, (2002) Three-dimensional reconstruction of the recombinant type 2 ryanodine receptor and localization of its divergent region 1. J Biol Chem 277: 46712-46719.
73. Sharma MR, Penczek P, Grassucci R, Xin HB, Fleischer S, et al. (1998) Cryoelectron microscopy and image analysis of the cardiac ryanodine receptor. J Biol Chem 273: 18429-18434.
74. Sharma MR, Jeyakumar LH, Fleischer S, Wagenknecht T, (2006) Three-dimensional visualization of FKBP12.6 binding to an open conformation of cardiac ryanodine receptor. Biophys J 90: 164-172.