The conformation of calsequestrin determines its ability to regulate skeletal ryanodine receptors

Biophysical Journal

Volumn 91, Issue 4, 2006, Pages 1288-1301

  Wei, Lan ^a   Varsányi, Magdolna ^b   Dulhunty, Angela F ^a   Beard, Nicole A ^a  

^a Biology and Environment   (Australia)

^b RUHR UNIVERSITY BOCHUM   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CALSEQUESTRIN; RYANODINE RECEPTOR;

ARTICLE; CALCIUM TRANSPORT; CONFORMATIONAL TRANSITION; DEPOLYMERIZATION; MUSCLE FATIGUE; PROTEIN CONFORMATION; SARCOPLASMIC RETICULUM;

EID: 33746839364     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.106.082610     Document Type: Article

References (49)

1. 2+ sensing sites. Biophys. J. 75:2801-2810.
2. Lukyanenko, V., I. Gyorke, and S. Gyorke. 1996. Regulation of calcium release by calcium inside the sarcoplasmic reticulum in ventricular myocytes. Pflugers Arch. 432:1047-1054.
3. 2+ sensitive leak in rat ventricular myocytes. Biophys. J. 81:785-798.
4. 2+ releasing action of caffeine and depolarisation in skeletal muscle fibres of the rat. J. Physiol. 531:715-728.
5. 2+ influx: how many mechanisms for how many channels? Trends Pharmacol. Sci. 15:77-83.
6. Hoth, M., and R. Penner. 1992. Depletion of intracellular calcium stores activates a calcium current in mast cells. Nature. 355:353-356.
7. 2+ stores. Proc. Natl. Acad. Sci. USA. 90:6295-6299.
8. Donoso, P., H. Prieto, and C. Hidalgo. 1995. Luminal calcium regulates calcium release in triads isolated from frog and rabbit skeletal muscle. Biophys. J. 68:507-515.
9. 2+. Biophys. J. 75:2302-2312.
10. 2+ buffer inside the sarcoplasmic reticulum. Biochem. J. 337:19-22.
11. Ma, J., M. Fill, C. M. Knudson, K. P. Campbell, and R. Coronado. 1988. Ryanodine receptor of skeletal muscle is a gap junction-type channel. Science. 242:99-102.
12. 2+ release channel. Biophys. J. 70:2600-2615.
13. 2+. J. Membr. Biol. 146:133-144.
14. 2+ activation and inactivation sites on the luminal side of the cardiac ryanodine receptor complex. Circ. Res. 87:201-206.
15. Gyorke, I., N. A. Hester, L. R. Jones, and S. Gyorke. 2004. The role of calsequestrin, triadin, and junctin in conferring cardiac ryanodine receptor responsiveness to luminal calcium. Biophys. J. 86:2121-2128.
16. Franzini-Armstrong, C., L. J. Kenney, and E. Varriano-Marston. 1987. The structure of calsequestrin in triads of vertebrate skeletal muscle: a deep-etch study. J. Cell Biol. 105:49-56.
17. Wang, J., N. A. Maertz, A. J. Lokua, E. G. Kranias, and H. H. Valdivia. 2001. Regulation of cardiac ryanodine receptors activity by calsequestrin. Biophys. J. 80:590a (Abstr.)
18. Beard, N. A., D. R. Laver, and A. F. Dulhunty. 1999. Regulation of skeletal muscle ryanodine receptors by calsequestrin. Proc Aust Physiol Pharm Soc. 30:43 (abstr.).
19. Zhang, L., J. Kelley, G. Schmeisser, Y. M. Kobayashi, and L. R. Jones. 1997. Complex formation between junctin, triadin, calsequestrin, and the ryanodine receptor. Proteins of the cardiac junctional sarcoplasmic reticulum membrane. J. Biol. Chem. 272:23389-23397.
20. Wang, S., W. R. Trumble, H. Liao, C. R. Wesson, A. K. Dunker, and C. H. Kang. 1998. Crystal structure of calsequestrin from rabbit skeletal muscle sarcoplasmic reticulum. Nat. Struct. Biol. 5:476-483.
21. Beard, N. A., D. R. Laver, and A. F. Dulhunty. 2004. Calsequestrin and the calcium release channel of skeletal and cardiac muscle. Prog. Biophys. Mol. Biol. 155:33-69.
22. 2+ regulation. J. Biol. Chem. 278:16176-16182.
23. Fliegel, L., E. Newton, K. Burns, and M. Michalak. 1990. Molecular cloning of cDNA encoding a 55-kDa multifunctional thyroid hormone binding protein of skeletal muscle sarcoplasmic reticulum. J. Biol. Chem. 265:15496-15502.
24. Scott, B. T., H. K. Simmerman, J. H. Collins, B. Nadal-Ginard, and L. R. Jones. 1988. Complete amino acid sequence of canine cardiac calsequestrin deduced by cDNA cloning. J. Biol. Chem. 263:8958-8964.
25. Beard, N. A., M. M. Sakowska, A. F. Dulhunty, and D. R. Laver. 2002. Calsequestrin is an inhibitor of skeletal muscle ryanodine receptor calcium release channels. Biophys. J. 82:310-320.
26. 2+ and phosphorylation. Biophys. J. 88:3444-3454.
27. Saito, A., S. Seiler, A. Chu, and S. Fleischer. 1984. Preparation and morphology of sarcoplasmic reticulum terminal cisternae from rabbit skeletal muscle. J. Cell Biol. 99:875-885.
28. Ahern, G. P., P. R. Junankar, and A. F. Dulhunty. 1994. Single channel activity of the ryanodine receptor calcium release channel is modulated by FK-506. FEBS Lett. 352:369-374.
29. Costello, B., C. Chadwick, A. Saito, A. Chu, A. Maurer, and S. Fleischer. 1986. Characterization of the junctional face membrane from terminal cisternae of sarcoplasmic reticulum. J. Cell Biol. 103:741-753.
30. Beard, N. A. 2003. Regulation of the skeletal muscle ryanodine receptor by calsequestrin. PhD thesis. Australian National University, Canberra.
31. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227:680-685.
32. Towbin, H., T. Staehelin, and J. Gordon. 1992. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. 1979. Biotechnology. 24:145-149.
33. 2+ release channels from rabbit skeletal muscle. Biophys. J. 78:1835-1851.
34. Minium, E. W., B. M. King, and G. Bear. 1993. Statistical Reasoning in Psychology and Education. John Wiley & Sons, New York.
35. 2+ and interacts with triadin. FEBS Lett. 486:178-182.
36. Guo, W., and K. P. Campbell. 1995. Association of triadin with the ryanodine receptor and calsequestrin in the lumen of the sarcoplasmic reticulum. J. Biol. Chem. 270:9027-9030.
37. Dulhunty, A. F., D. R. Laver, E. M. Gallant, M. G. Casarotto, S. M. Pace, and S. Curtis. 1999. Activation and inhibition of skeletal RyR channels by a part of the skeletal DHPR II-III loop: effects of DHPR Ser687 and FKBP12. Biophys. J. 77:189-203.
38. Ohkura, M., K. Furukawa, H. Fujimori, A. Kuruma, S. Kawano, M. Hiraoka, A. Kuniyasu, H. Nakayama, and Y. Ohizumi. 1998. Dual regulation of the skeletal muscle ryanodine receptor by triadin and calsequestrin. Biochemistry. 37:12987-12993.
39. 2+ inhibition of skeletal RyRs reconstituted as isolated channels or coupled clusters. J. Gen. Physiol. 124:741-758.
40. Ostwald, T. J., D. H. MacLennan, and K. J. Dorrington. 1974. Effects of cation binding on the conformation of calsequestrin and the high affinity calcium-binding protein of sarcoplasmic reticulum. J. Biol. Chem. 249:5867-5871.
41. Ikemoto, N., G. M. Bhatnagar, B. Nagy, and J. Gergely. 1972. Interaction of divalent cations with the 55,000-dalton protein component of the sarcoplasmic reticulum. Studies of fluorescence and circular dichroism. J. Biol. Chem. 247:7835-7837.
42. Fill, M., R. Coronado, J. R. Mickelson, J. Vilven, J. J. Ma, B. A. Jacobson, and C. F. Louis. 1990. Abnormal ryanodine receptor channels in malignant hyperthermia. Biophys. J. 57:471-475.
43. 2+ release channel/ryanodine receptor complex of skeletal muscle sarcoplasmic reticulum by luminal calcium. Pflugers Arch. 432:155-157.
44. 2+ release channels (ryanodine receptors) by multiple mechanisms. J. Biol. Chem. 274:32680-32691.
45. Marengo, J. J., C. Hidalgo, and R. Bull. 1998. Sulfhydryl oxidation modifies the calcium dependence of ryanodine-sensitive calcium channels of excitable cells. Biophys. J. 74:1263-1277.
46. Pessah, I. N., K. H. Kim, and W. Feng. 2002. Redox sensing properties of the ryanodine receptor complex. Front. Biosci. 7:a72-a79.
47. Launikonis, B. S., J. Zhou, L. Royer, T. R. Shannon, G. Brum, and E. Rios. 2006. Depletion "skraps" and dynamic buffering inside the cellular calcium store. Proc. Natl. Acad. Sci. USA. 103:2982-2987.
48. Lamb, G. D. 2000. Excitation-contraction coupling in skeletal muscle: comparisons with cardiac muscle. Clin. Exp. Pharmacol. Physiol. 27:216-224.
49. Laver, D. R., T. M. Baynes, and A. F. Dulhunty. 1997. Magnesium inhibition of ryanodine-receptor calcium channels: evidence for two independent mechanisms. J. Membr. Biol. 156:213-229.