A malignant hyperthermia-inducing mutation in RYR1 (R163C): Alterations in Ca2+ entry, release, and retrograde signaling to the DHPR

Journal of General Physiology

Volumn 135, Issue 6, 2010, Pages 619-628

  Estève, Eric ^a,e   Eltit, José M ^a,b   Bannister, Roger A ^c   Pessah, Isaac N ^d   Beam, Kurt G ^c   Allen, Paul D ^a   López, José R ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b UNIVERSITY OF CHILE   (Chile)

^c UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e UNIVERSITÉ DE BORDEAUX   (France)

Author keywords

[No Author keywords available]

Indexed keywords

1,4 DIHYDRO 2,6 DIMETHYL 5 NITRO 4 [2 (TRIFLUOROMETHYL)PHENYL] 3 PYRIDINECARBOXYLIC ACID METHYL ESTER; CALCIUM; CALCIUM CHANNEL L TYPE; CALCIUM CHANNEL STIMULATING AGENT; RYANODINE RECEPTOR;

ANIMAL; ARTICLE; C57BL MOUSE; CALCIUM SIGNALING; CELL CULTURE; CELL MEMBRANE; CELL MEMBRANE POTENTIAL; DRUG EFFECT; EXCITATION CONTRACTION COUPLING; GENETICS; MALIGNANT HYPERTHERMIA; METABOLISM; MOUSE; MOUSE MUTANT; MYOBLAST; PATHOPHYSIOLOGY; PROTEIN CONFORMATION; SARCOPLASMIC RETICULUM; STRUCTURE ACTIVITY RELATION; TIME;

3-PYRIDINECARBOXYLIC ACID, 1,4-DIHYDRO-2,6-DIMETHYL-5-NITRO-4-(2-(TRIFLUOROMETHYL)PHENYL)-, METHYL ESTER; ANIMALS; CALCIUM; CALCIUM CHANNEL AGONISTS; CALCIUM CHANNELS, L-TYPE; CALCIUM SIGNALING; CELL MEMBRANE; CELLS, CULTURED; EXCITATION CONTRACTION COUPLING; MALIGNANT HYPERTHERMIA; MEMBRANE POTENTIALS; MICE; MICE, INBRED C57BL; MICE, MUTANT STRAINS; MYOBLASTS, SKELETAL; PROTEIN CONFORMATION; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL; SARCOPLASMIC RETICULUM; STRUCTURE-ACTIVITY RELATIONSHIP; TIME FACTORS;

EID: 77953066485     PISSN: 00221295     EISSN: 15407748     Source Type: Journal    
DOI: 10.1085/jgp.200910328     Document Type: Article

References (61)

1. Almers, W., and P.T. Palade. 1981. Slow calcium and potassium currents across frog muscle membrane: measurements with a vaseline-gap technique. J. Physiol. 312:159-176.
2. Araya, R., J.L. Liberona, J.C. Cárdenas. N. Riveros, M. Estrada, J.A. Powell, M.A. Carrasco, and E. Jaimovich. 2003. Dihydropyridine receptors as voltage sensors for a depolarization-evoked, IP3Rmediated, slow calcium signal in skeletal muscle cells. J. Gen. Physiol. 121:3-16. doi:10.1085/jgp.20028671
3. Armstrong, C.M., F.M. Bezanilla, and P. Horowicz. 1972. Twitches in the presence of ethylene glycol bis(-ammoethyl etlier)-N,N'tetracetic acid. Biochim. Biophys. Acta. 267:605-608. doi:10.1016/ 0005-2728(72)90194-6
4. 2+ entry in dysgenic and dyspedic myotubes. Channels (Austin). 3:268-273.
5. 2+ entry. J. Gen. Physiol. 133:79-91. doi:10.1085/jgp.200810105
6. Bannister, RA., E. Estève, J.M. Eltit, I.N. Pessah, P.D. Allen, J.R. López, and K.G. Beam. 2010. A malignant hyperthermia-inducing mutation in RYR1 (R163C) : consequent alterations in the functional properties of DHPR channels. J. Gen. Physiol. 135:629-640.
7. Bianchi, C.P., and A.M. Shanes. 1959. Calcium influx in skeletal muscle at rest, during activity, and during potassium contracture. J. Gen. Physiol. 42:803-815. doi:10.1085/jgp.42.4.803
8. Blinks, J.R., R. Rüdel, and S.R. Taylor. 1978. Calcium transients in isolated amphibian skeletal muscle fibres: detection with aequorin. J. Physiol. 277:291-323.
9. Bolaños, P., C. Caputo, and L. Velaz. 1986. Effects of calcium, barium and lanthanum on depolarization-contraction coupling in skeletal muscle fibres of Rana pipiens. J. Physiol. 370:39-60.
10. Brum, G., E. Ríos, and E. Stefani. 1988. Effects of extracellular calcium on calcium movements of excitation-contraction coupling in frog skeletal muscle fibres. J. Physiol. 398:441-473.
11. Caputo, C. 1972a. The effect of low temperature on the excitation-contraction coupling phenomena of frog single muscle fibres. J. Physiol. 223:461-482.
12. Caputo, C. 1972b. The time course of potassium contractures of single muscle fibres. J. Physiol. 223:483-505.
13. Caputo, C. 1976. The effect of caffeine and tetracaine on the time course of potassium contractures of single muscle fibres. J. Physiol. 255:191-207.
14. Caputo, C. 1981. Nickel substitution for calcium and the time course of potassium contractures of single muscle fibres. J. Muscle Res. Cell Motil 2:167-182. doi:10.1007/BF00711867
15. Caputo, C., and P. Bolaños. 1994. Fluo-3 signals associated with potassium contractures in single amphibian muscle fibres. J. Physiol. 481:119-128.
16. Caputo, C., and M. Gimenez. 1967. Effecte of external calcium deprivation on single muscle fibers. J. Get Physiol. 50:2177-2195. doi:10.1085/jgp.50.9. 2177
17. Chelu, M.G., S.A. Goonasekera, W.J. Durham, W. Tang, J.D. Lueck, J. Richl, I.N. Pessah, P. Zhang, M.B. Bhattacharjee, R.T. Dirksen, and S.L. Hamilton. 2006. Heat- and anesthesia-induced malignant hyperthermia in an RyR1 knock-in mouse. FASEB J. 20:329-330.
18. Cherednichenko, G., A.M. Hurne, J.D. Fessenden, E.H. Lee, P.D. Allen, K.G. Beam, and I.N. Pessah 2004. Conformational activation of Ca2+ entry by depolarization of skeletal myotubes. Proc. Nati, Acad, Sci. USA. 101:15793-15798. dor.10.1073/pnas.0403485101
19. Cherednichenko, G., C.W. Ward, W. Feng, E. Cabrales, L. Michaelson, M. Samso, J.R. López, P.D. Allen, and I.N. Pessah. 2008. Enhanced excitation-coupled calcium entry in myotubes expressing malignant hyperthermia mutation R163C is attenuated by dantrolene. Mol. Pharmacol 73:1203-1212. doi:10.1124/mol.107.043299
20. Cota, G., and E. Stefani. 1981. Effects of external calcium reduction on the kinetics of potassium contractures in frog twitch muscle fibres. J. Physiol. 317:303-316.
21. Dirksen, R.T., and K.G. Beam. 1999. Role of calcium permeation in dihydropyridine receptor function. Insights into channel gating and excitation-contraction coupling. J. Gen. Physiol. 114:393-403. doi:10.1085/jgp.114.3.393
22. Dulhunty, A.F. 1992. The voltage-activation of contraction in skeletal muscle. Prog. Biophys. Mol. Biol. 57:181-223. doi:10.1016/ 0079-6107(92)90024-Z
23. Dulhunty, A.F., and P.W. Gage. 1988. Effects of extracellular calcium concentration and dihydropyridines on contraction in mammalian skeletal muscle. J. Physiol. 399:63-80.
24. Ebata, H., J.S. Mills, K. Nemcek, and J.D.Johnson. 1990. Calcium binding to extracellular sites of skeletal muscle calcium channels regulates dihydropyridine binding. J. Biol Chem. 265: 177-182.
25. Frank, G.B. 1960. Effects of changes in extracellular calcium concentration on the potassium-induced contracture of frog's skeletal muscle. J. Physiol. 151:518-538.
26. Gallant, E.M., and L.R. Lentz. 1992. Excitation-contraction coupling in pigs heterozygous for malignant hyperthermia. Am. J. Physiol. 262:C422-C426.
27. Gallant, E.M., G.A. Gronert, and S.R. Taylor. 1982. Cellular membrane potentials and contractile threshold in mammalian skeletal muscle susceptible to malignant hyperthermia. Neurosa. Lett. 28:181-186. doi:10.1016/0304-3940(82) 90149-5
28. Hodgkin, A.L., and P. Horowicz. 1959. The influence of potassium and chloride ions on the membrane potential of single muscle fibres. J. Physiol. 148:127-160.
29. Hodgkin, A.L., and P. Horowicz. 1960a. The effect of sudden changes in ionic concentrations on the membrane potential of single muscle fibres. J. Physiol. 153:370-385.
30. Hodgkin, A.L., and P. Horowicz. 1960b. Potassium contractures in single muscle fibres. J. Physiol. 153:386-403.
31. Jong, D.S., P.C. Pape, S.M. Baylor, and W.K. Chandler. 1995. Calcium inactivation of calcium release in frog cut muscle fibers that contain millimolar EGTA or Fura-2. J. Gen. Physiol. 106:337-388. doi:10 .1085/jgp.106.2.337
32. Jurkat-Rott, K., T. McCarthy, and F. Lehmann-Hom. 2000. Genetics and pathogenesis of malignant hyperthermia. Muscle Nerve, 23:4-17. doi:10.1002/(SICI)1097-4598(200001)23:1<4:AID-MUS3>3.0.CO2-D
33. 2+ entry blockers. Jpn.. J. Pharmacol. 81:253-258. doi:10.1254/jjp.81.253
34. López, J.R., L. Alamo, C. Caputo, R. DiPolo, and S. Vergara. 1983. Determination of ionic calcium in frog skeletal muscle fibers. Biophys. J. 43:1-4. doi:10.1016/S0006-3495(83)84316-l
35. López, J.R., L. Alamo, C. Caputo, J. Wikinski, and D. Ledezma. 1985. Intracellular ionized calcium concentration in muscles from humans with malignant hyperthermia. Muscle Nerve. 8:355-358. doi:10.1002/mus.880080502
36. 2+] during a malignant hyperthermia episode in swine. Muscle Nerve. 11:82-88. doi:10.1002/mus.880110113
37. i. Am. J. PhysioL Cell Physiol. 288:C606-C612. doi:10 .1152/ajpcell.00297.2004
38. Lorkovic, H., and R. Rudel. 1983. Influence of divalent cations on potassium contracture duration in frog muscle fibres. Pflugers Arch. 398:114-119. doi:10.1007/BF00581057
39. Lüttgau, H.C., and W. Spiecker. 1979. The effects of calcium deprivation upon mechanical and electrophysiological parameters in skeletal muscle fibres of the frog. J. Physiol, 296:411-429.
40. Monnier, N., V. Procaccio, P. Stieglitz, andJ. Lunardi. 1997. Malignanthyperthermia 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. doi:10.1086/515454
41. NakaiJ., R.T. Dirksen, H.T. Nguyen, I.N. Pessah, K.G. Beam, and P.D. Allen. 1996. Enhanced dihydropyridine receptor channel activity in the presence of ryanodine receptor. Nature. 380:72-75. doi:10 .1038/380072a0
42. 2+ channels. J. Biol. Chem. 273:13403-13406. doi:10 .1074/JDC.273.22.13403
43. Nelson, T.E. 2001. Heat production during anesthetic-induced malignant hyperthermia. Biosci. Rep. 21:169-179. dor.10.1023/ A1013696124358
44. ++ regulating proteins. Curr. Mol. Med 2:347-369. doi:10.2174/1566524023362429
45. v3.1 (α1G) T-type calcium channels. J. Gen. Physiol. 132:239-250. doi:10 .1085/jgp.200809988
46. Palade, P.T., and W. Aimers. 1985. Slow calcium and potassium currents in frog skeletal muscle: uieir relationship and pharmacologic properties. Pflugers Arch. 405:91-101. doi:10.1007/BF00584528
47. Rando, T.A., and H.M. Blau. 1994. Primary mouse myoblast purification, characterization, and transplantation for cell-mediated gene therapy. J. Cell Biol. 125:1275-1287. doi:10.1083/jcb.125.6.1275
48. Rios, E., and G. Brum. 1987. Involvement of dihydropyridine receptors in excitation-contraction coupling in skeletal muscle. Nature. 325:717-720. doi:10.1038/3257l7a0
49. Rivet, M., C. Cognard, and G. Raymond. 1989. The slow inward calcium current is responsible for a part of the contraction of patchclamped rat myoballs. Pflugers Arch. 413:316-318. doi:10.1007/ BF00583547
50. Robinson, R., D. Carpenter, M.A. Shaw, J. Halsall, and P. Hopkins. 2006. Mutations in RYR1 in malignant hyperthermia and central core disease. Hum. Mutal. 27:977-989. doi:10.1002/humu.20356
51. Simon, B.J., M.G. Klein, and M.F. Schneider. 1991. Calcium dependence of inactivation of calcium release from the sarcoplasmic reticulum in skeletal muscle fibers. J. Gen. Physiol. 97:437-471. doi:10.1085/jgp.97.3.437
52. Smith, J.S., R. Coronado, and G. Meissner. 1985. Sarcoplasmic reticulum contains adenine nucleotide-activated calcium channels. Nature. 316:446-449. doi:10.1038/316446a0
53. Snowdowne, K.W. 1985. Subcontracture depolarizations increase sarcoplasmic ionized calcium in frog skeletal muscle. Am. J. Physiol. 248:C520-C526.
54. Stefani, E., and D.J. Chiarandini. 1973. Skeletal muscle: dependence of potassium contractures on extracellular calcium. Pflugers Arch. 343:143-150. doi:10.1007/BF00585709
55. Suarez-Isla, B.A, C. Orozco, P.F. Heller, and J.P. Froehlich. 1986. Single calcium channels in native sarcoplasmic reticulum membranes fromskeletalmuscle. Proc. Natl. Acad. Sci. USA. 83:7741-7745. doi:10 .1073/pnas.83.20.7741
56. Tanabe. T., K.G. Beam, BA Adams, T. Niidome, and S. Numa. 1990. Regions of the skeletal muscle dihydropyridine receptor critical for excitation-contraction coupling. Nature. 346:567-569. doi:10.1038/346567a0
57. Treves, S., A.A. Anderson, S. Ducreux, A. Divet, C. Bleunven, C. Grasso, S. Paesante, and F. Zorzato. 2005. Ryanodine receptor 1 mutations, dysregulation of calcium homeostasis and neuromuscular disorders. Neuromuscul, Disord. 15:577-587. doi:10.1016/ j.nmd.2005.06.008
58. Yang, T., T.A. Ta, I.N. Pessah, and P.D. Allen. 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. doi:10.1074/jbc.M302165200
59. Yang, T., J. Riehl, E. Esteve, K.I. Matthaei, S. Goth, P.D. Allen, I.N. Pessah, and J.R. Lopez. 2006. Pharmacologic and functional characterization of malignant hyperthermia in the R163C RyR1 knock-in mouse. Anesthesiology. 105:1164-1175. doi:10.1097/ 00000542-200612000-00016
60. Yang, T., P.D. Allen, I.N. Pessah, and J.R. Lopez. 2007a. Enhanced excitation-coupled calcium entry in myotubes is associated with expression of RyR1 malignant hyperthermia mutations. J. Biol. Chem. 282:37471-37478. doi:10.1074/jbc.M701379200
61. i in myotubes expressing malignant hyperthermia RyR1 cDNAs is partially restored by modulation of passive calcium leak from the SR. Am. J. Physiol. Cell Physiol. 292:0591-0598. doi:10.1152/ajpcell .00133.2006