Central core disease mutations R4892W, I4897T and G4898E in the ryanodine receptor isoform 1 reduce the Ca2+ sensitivity and amplitude of Ca2+-dependent Ca2+ release

Biochemical Journal

Volumn 382, Issue 2, 2004, Pages 557-564

  Du, Guo Guang ^a   Khanna, Vijay K ^a   Guo, Xinghua ^a   MacLennan, David H ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

45Ca 2+ uptake and release; Ca2+ dependent Ca2+ release; Central core disease; Excitation contraction coupling; Ryanodine receptor; Skeletal muscle sarcoplasmic reticulum

Indexed keywords

BIOASSAY; BIOLOGICAL MEMBRANES; CELL CULTURE; MUSCULOSKELETAL SYSTEM;

DEPOLARIZATION; MUTANTS; PEAK AMPLITUDES;

BIOCHEMISTRY;

ADENOSINE TRIPHOSPHATASE (CALCIUM); CAFFEINE; CALCIUM; RYANODINE RECEPTOR; RYANODINE RECEPTOR 1; UNCLASSIFIED DRUG;

AMPLITUDE MODULATION; ARTICLE; AUTOSOMAL DOMINANT DISORDER; CALCIUM TRANSPORT; CELL LINE; CENTRAL CORE DISEASE; CENTRONUCLEAR MYOPATHY; CONTROLLED STUDY; EMBRYO; ENDOPLASMIC RETICULUM; EXCITATION CONTRACTION COUPLING; GENE MUTATION; HUMAN; HUMAN CELL; MUTANT; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR BINDING; SARCOPLASMIC RETICULUM; SKELETAL MUSCLE; WILD TYPE;

ADENOSINE TRIPHOSPHATE; ARGININE; CALCIUM; CALCIUM ISOTOPES; CALCIUM-TRANSPORTING ATPASES; CELL LINE; GLUTAMIC ACID; GLYCINE; HUMANS; ISOLEUCINE; KIDNEY; MICROSOMES; MUTAGENESIS, SITE-DIRECTED; MUTATION, MISSENSE; MYOPATHY, CENTRAL CORE; OXALATES; PHOTOMETRY; PROTEIN ISOFORMS; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL; SARCOPLASMIC RETICULUM CALCIUM-TRANSPORTING ATPASES; THREONINE; TRYPTOPHAN;

EID: 4544355520     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20040580     Document Type: Article

References (53)

1. Franzini-Armstrong, C. and Protasi, F. (1997) Ryanodine receptors of striated muscles: a complex channel capable of multiple interactions. Physiol. Rev. 77, 699-729
2. Ptacek, L. J., Tawil, R., Griggs, R. C., Engel, A. G., Layzer, R. B., Kwiecinski, H., McManis, P. G., Santiago, L., Moore, M., Fouad, G. et al. (1994) Dihydropyridine receptor mutations cause hypokalemic periodic paralysis. Cell (Cambridge, Mass.) 77, 863-868
3. Jurkat-Rott, K., Lehmann-Horn, F., Elbaz, A., Heine, R., Gregg, R. G., Hogan, K., Powers, P. A., Lapie, P., Vale-Santos, J. E., Weissenbach, J. et al. (1994) A calcium channel mutation causing hypokalemic periodic paralysis. Hum. Mol. Genet. 3, 1415-1419
4. Monnier, N., Procaccio, V., Stieglitz, P and Lunardi, J. (1997) Malignant-hyperthermia susceptibility is associated with a mutation of the alpha 1-subunit of the human dihydropyridine-sensitive L-type voltage-dependent calcium-channel receptor in skeletal muscle. Am. J. Hum. Genet. 60, 1316-1325
5. Gillard, E. F., Otsu, K., Fujii, J., Khanna, V. K., de Leon, S., Derdemezi, J., Britt, B. A., Duff, C. L., Worton, R. G. and MacLennan, D. H. (1991) A substitution of cysteine for arginine 614 in the ryanodine receptor is potentially causative of human malignant hyperthermia. Genomics 11, 751-755
6. Fujii, J., Otsu, K., Zorzato, F., de Leon, S., Khanna, V. K., Weiler, J. E., O'Brien, P. J. and MacLennan, D. H. (1991) Identification of a mutation in porcine ryanodine receptor associated with malignant hyperthermia. Science 253, 448-451
7. Roberts, M. C., Mickelson, J. R., Patterson, E. E., Nelson, T. E., Armstrong, P. J., Brunson, D. B. and Hogan, K. (2001) Autosomal dominant canine malignant hyperthermia is caused by a mutation in the gene encoding the skeletal muscle calcium release channel (RYR1). Anesthesiology 95, 716-725
8. 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. (1993) Mutations in the ryanodine receptor gene in central core disease and malignant hyperthermia. Nat. Genet. 5, 51-55
9. Zhang, Y., Chen, H. S., Khanna, V. K., De Leon, S., Phillips, M. S., Schappert, K., Britt, B. A., Browell, A. K. and MacLennan, D. H. (1993) A mutation in the human ryanodine receptor gene associated with central core disease. Nat. Genet. 5, 46-50
10. 2+ regulation defects. Physiol. Rev. 76, 537-592
11. 2+ release channels. Am. J. Med. 104, 470-486
12. McCarthy, T. V., Quane, K. A. and Lynch, P. J. (2000) Ryanodine receptor mutations in malignant hyperthermia and central core disease. Hum. Mutat. 15, 410-417
13. Jurkat-Rott, K., McCarthy, T. and Lehmann-Horn, F. (2000) Genetics and pathogenesis of malignant hyperthermia. Muscle Nerve 23, 4-17
14. Dirksen, R. T. and Avila, G. (2002) Altered ryanodine receptor function in central core disease: leaky or uncoupled Ca(2+) release channels? Trends Cardiovasc. Med. 12, 189-197
15. Galli, L., Orrico, A., Cozzolino, S., Pietrini, V., Tegazzin, V. and Sorrentino, V. (2002) 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 32, 143-151
16. Davis, M. R., Haan, E., Jungbluth, H., Sewry, C., North, K., Muntoni, F., Kuntzer, T., Lamont, P., Bankier, A., Tomlinson, P. et al. (2003) Principal mutation hotspot for central core disease and related myopathies in the C-terminal transmembrane region of the RYR1 gene. Neuromuscul. Disord. 13, 151-157
17. Monnier, N., Ferreiro, A., Marty, I., Labarre-Vila, A., Mezin, P. and Lunardi, J. (2003) A homozygous splicing mutation causing a depletion of skeletal muscle RYR1 is associated with multi-minicore disease congenital myopathy with ophthalmoplegia. Hum. Mol. Genet. 12, 1171-1178
18. Zorzato, F., Yamaguchi, N., Xu, L., Meissner, G., Muller, C. R., Pouliquin, P., Muntoni, F., Sewry, C., Girard, T. and Treves, S. (2003) Clinical and functional effects of a deletion in a COOH-terminal lumenal loop of the skeletal muscle ryanodine receptor. Hum. Mol. Genet. 12, 379-388
19. Tammaro, A., Bracco, A., Cozzolino, S., Esposito, M., Di Martino, A., Savoia, G., Zeuli, L., Piluso, G., Aurino, S. and Nigro, V. (2003) Scanning for mutations of the ryanodine receptor (RYR1) gene by denaturing HPLC: detection of three novel malignant hyperthermia alleles. Clin. Chem. 49, 761-768
20. 2+ release channel of skeletal muscle sarcoplasmic reticulum (RyR1). Proc. Natl. Acad. Sci. U.S.A. 99, 16725-16730
21. Censier, K., Urwyler, A., Zorzato, F. and Treves, S. (1998) Intracellular calcium homeostasis in human primary muscle cells from malignant hyperthermia-susceptible and normal individuals. Effect of overexpression of recombinant wild-type and Arg163Cys mutated ryanodine receptors. J. Clin. Invest. 101, 1233-1242
22. Wehner, M., Rueffert, H., Koenig, F., Meinecke, C. D. and Olthoff, D. (2003) The IIe2453Thr mutation in the ryanodine receptor gene 1 is associated with facilitated calcium release from sarcoplasmic reticulum by 4-chloro-m-cresol in human myotubes. Cell Calcium 34, 163-168
23. 2+ release channel of skeletal sarcoplasmic reticulum is responsible for hypersensitivity to caffeine and halothane in malignant hyperthermia. J. Biol. Chem. 269, 9413-9415
24. 2+ transients in COS-7 cells transfected with the cDNA encoding skeletal-muscle ryanodine receptor carrying a mutation associated with malignant hyperthermia. Biochem. J. 301, 661-665
25. 2+ release is altered by 15 calcium release channel (ryanodine receptor) mutations associated with malignant hyperthermia and/or central core disease. J. Biol. Chem. 272, 26332-26339
26. Yang, T., Ta, T. A., Pessah, I. N. and Allen, P. D. (2003) Functional defects in six ryanodine receptor isoform-1 (RyR1) mutations associated with malignant hyperthermia and their impact on skeletal excitation-contraction coupling. J. Biol. Chem. 278, 25722-25730
27. 2+ release channels. J. Biol. Chem. 274, 693-702
28. MacLennan, D. H., Phillips, M. S. and Zhang, Y. (1996) The genetic and physiological basis of malignant hyperthermia. In Molecular Biology of Membrane Transport Disorders (Schultz, S. G., Andreoli, T. E., Brown, A. M., Fambrough, D. J. H. and Welsh, M. J., eds.), chapter 10, pp. 181-200, Plenum Press, New York
29. Avila, G. and Dirksen, R. T. (2001) Functional effects of central core disease mutations in the cytoplasmic region of the skeletal muscle ryanodine receptor. J. Gen. Physiol. 118, 277-290
30. Avila, G., O'Brien, J. J. and Dirksen, R. T. (2001) Excitation- contraction uncoupling by a human central core disease mutation in the ryanodine receptor. Proc. Natl. Acad. Sci. U.S.A. 98, 4215-4220
31. Avila, G., O'Connell, K. M. and Dirksen, R. T. (2003) The pore region of the skeletal muscle ryanodine receptor is a primary locus for excitation-contraction uncoupling in central core disease. J. Gen. Physiol. 121, 277-286
32. 2+ release channel function and severe central core disease. Proc. Natl. Acad. Sci. U.S.A. 96, 4164-4169
33. Monnier, N., Romero, N. B., Lerale, J., Nivoche, Y., Qi, D., MacLennan, D. H., Fardeau, M. and Lunardi, J. (2000) An autosomal dominant congenital myopathy with cores and rods is associated with a neomutalion in the RYR1 gene encoding the skeletal muscle ryanodine receptor. Hum. Mol. Genet. 9, 2599-2608
34. Tilgen, N., Zorzato, F., Halliger-Keller, B., Muntoni, F., Sewry, C., Palmucci, L. M., Schneider, C., Hauser, E., Lehmann-Horn, F., Muller, C. R. et al. (2001) Identification of four novel mutations in the C-terminal membrane spanning domain of the ryanodine receptor 1: association with central core disease and alteration of calcium homeostasis. Hum. Mol. Genet. 10, 2879-2887
35. Gao, L., Balshaw, D., Xu, L., Tripathy, A., Xin, C. and Meissner, G. (2000) Evidence for a role of the lumenal M3-M4 loop in skeletal muscle Ca(2+) release channel (ryanodine receptor) activity and conductance. Biophys. J. 79, 828-840
36. Du, G. G., Guo, X., Khanna, V. K. and MacLennan, D. H. (2001) Functional characterization of mutants in the predicted pore region of the rabbit cardiac muscle Ca(2+) release channel (ryanodine receptor isoform 2). J. Biol. Chem. 276, 31760-31771
37. 2+ sensor. J. Biol. Chem. 273, 14675-14678
38. 3H]ryanodine binding assay. J. Biol. Chem. 273, 33259-33266
39. 2+-release channel (ryanodine receptor isoform 1). Biochem. J. 360, 97-105
40. 2+-ATPase expressed in COS-1 cells. Proc. Natl. Acad. Sci. U.S.A. 85, 3314-3318
41. Lowry, O. H., Rosebrough, N. J., Farr, A. L. and Randall, R. J. (1951) Protein measurement with the Polin phenol reagent. J. Biol. Chem. 193, 265-275
42. Fabiato, A. (1988) Computer programs for calculating total from specified free or free from specified total ionic concentrations in aqueous solutions containing multiple metals and ligands. Methods Enzymol. 157, 378-417
43. Boehning, D. and Joseph, S. K. (2000) Functional properties of recombinant type I and type III inositol 1,4,5-trisphosphate receptor isoforms expressed in COS-7 cells. J. Biol. Chem. 275, 21492-21499
44. 2+ release channels with ryanodine in junctional terminal cisternae of sarcoplasmic reticulum of fast skeletal muscle. Proc. Natl. Acad. Sci. U.S.A. 82, 7256-7259
45. 2+ release channel of sarcoplasmic reticulum. J. Biol. Chem. 261, 6300-6306
46. Xu, L., Tripathy, A., Pasek, D. A. and Meissner, G. (1999) Ruthenium red modifies the cardiac and skeletal muscle Ca(2+) release channels (ryanodine receptors) by multiple mechanisms. J. Biol. Chem. 274, 32680-32691
47. 2+ store that is responsive to stop-flow medium changes and insensitive to caffeine and ryanodine. Biochem. J. 343, 39-44
48. 2+, and adenine nucleotides. Biochemistry 25, 236-244
49. Herrmann-Frank, A., Luttgau, H. C. and Stephenson, D. G. (1999) Caffeine and excitation-contraction coupling in skeletal muscle: a stimulating story. J. Muscle Res. Cell Motil. 20, 223-237
50. Zhao, M., Li, P., Li, X., Zhang, L., Winkfein, R. J. and Chen, S. R. (1999) Molecular identification of the ryanodine receptor pore-forming segment. J. Biol. Chem. 274, 25971-25974
51. Block, B. A., Imagawa, T., Campbell, K. P. and 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
52. Klein, M. G., Cheng, H., Santana, L. F., Jiang, Y. H., Lederer, W. J. and Schneider, M. F. (1996) Two mechanisms of quantized calcium release in skeletal muscle. Nature (London) 379, 455-458
53. Shuaib, A., Paasuke, R. T. and Brownell, K. W. (1987) Central core disease. Clinical features in 13 patients. Medicine (Baltimore) 66, 389-396