Accelerated Activation of SOCE Current in Myotubes from Two Mouse Models of Anesthetic- and Heat-Induced Sudden Death

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Yarotskyy, Viktor ^a   Protasi, Feliciano ^b   Dirksen, Robert T ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^b UNIVERSITY OF CHIETI   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ANESTHETIC AGENT; AZUMOLENE; CALCIUM CHANNEL; CALCIUM ION; CALSEQUESTRIN; CALSEQUESTRIN 1; CALSEQUESTRIN 2; RYANODINE RECEPTOR 1; STORE OPERATED CALCIUM ENTRY CHANNEL; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CALCIUM CURRENT; CALCIUM SIGNALING; CELL MEMBRANE DEPOLARIZATION; CONTROLLED STUDY; DRUG MECHANISM; GENE TARGETING; HEAT STRESS; KNOCKOUT MOUSE; MALIGNANT HYPERTHERMIA; MOUSE; MYOTUBE; NEWBORN; NONHUMAN; PATCH CLAMP; PROTECTION; PROTEIN INDUCTION; ROOM TEMPERATURE; SUDDEN DEATH; WHOLE CELL; WILD TYPE;

ACCELERATION; ANESTHETICS; ANIMALS; CALCIUM; CALCIUM CHANNELS; CALCIUM-BINDING PROTEINS; CALSEQUESTRIN; DEATH, SUDDEN; DISEASE MODELS, ANIMAL; ELECTROPHYSIOLOGICAL PROCESSES; GENE KNOCK-IN TECHNIQUES; GENE KNOCKOUT TECHNIQUES; HOT TEMPERATURE; IMIDAZOLES; MICE; MUSCLE FIBERS, SKELETAL; OXAZOLES; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL;

EID: 84885446786     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0077633     Document Type: Article

References (49)

1. Rosenberg H, Sambuughin N, Dirksen R, (2010) Malignant hyperthermia susceptibility: In: GeneReviews at GeneTests: Medical Genetics Information Resource [database online]. Copyright, Seattle: University of Washington, 1997-2010.
2. Larach MG, Brandom BW, Allen GC, Gronert GA, Lehman EB, (2008) Cardiac arrests and deaths associated with malignant hyperthermia in north america from 1987 to 2006: a report from the north american malignant hyperthermia registry of the malignant hyperthermia association of the United States. Anesthesiology 108: 603-611. doi:10.1097/ALN.0b013e318167aee2. PubMed: 18362591.
3. Hopkins PM, Ellis FR, Halsall PJ, (1991) Evidence for related myopathies in exertional heat stroke and malignant hyperthermia. Lancet 338: 1491-1492. doi:10.1016/0140-6736(91)92304-K. PubMed: 1683922.
4. Tobin JR, Jason DR, Challa VR, Nelson TE, Sambuughin N, (2001) Malignant hyperthermia and apparent heat stroke. JAMA 286: 168-169. doi:10.1001/jama.286.2.168. PubMed: 11448278.
5. Wappler F, Fiege M, Steinfath M, Agarwal K, Scholz J, et al. (2001) Evidence for susceptibility to malignant hyperthermia in patients with exercise-induced rhabdomyolysis. Anesthesiology 94: 95-100. doi:10.1097/00000542-200101000-00019. PubMed: 11135728.
6. Davis M, Brown R, Dickson A, Horton H, James D, et al. (2002) Malignant hyperthermia associated with exercise-induced rhabdomyolysis or congenital abnormalities and a novel RYR1 mutation in New Zealand and Australian pedigrees. Br J Anaesth 88: 508-515. doi:10.1093/bja/88.4.508. PubMed: 12066726.
7. Capacchione JF, Muldoon SM, (2009) The relationship between exertional heat illness, exertional rhabdomyolysis, and malignant hyperthermia. Anesth Analg 109: 1065-1069. doi:10.1213/ane.0b013e3181a9d8d9. PubMed: 19617585.
8. Nishio H, Sato T, Fukunishi S, Tamura A, Iwata M, et al. (2009) Identification of malignant hyperthermia-susceptible ryanodine receptor type 1 gene (RYR1) mutations in a child who died in a car after exposure to a high environmental temperature. Leg Med (Tokyo) 11: 142-143. doi:10.1016/j.legalmed.2008.12.004.
9. Groom L, Muldoon SM, Tang ZZ, Brandom BW, Bayarsaikhan M, et al. (2011) Identical de novo mutation in the type 1 ryanodine receptor gene associated with fatal, stress-induced malignant hyperthermia in two unrelated families. Anesthesiology 115: 938-945. doi:10.1097/ALN.0b013e3182320068. PubMed: 21918424.
10. Chelu MG, Goonasekera SA, Durham WJ, Tang W, Lueck JD, et al. (2006) Heat- and anesthesia-induced malignant hyperthermia in an RyR1 knock-in mouse. FASEB J 20: 329-330. PubMed: 16284304.
11. Yang T, Riehl J, Esteve E, Matthaei KI, Goth S, et al. (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. PubMed: 17122579.
12. Dainese M, Quarta M, Lyfenko AD, Paolini C, Canato M, et al. (2009) Anesthetic- and heat-induced sudden death in calsequestrin-1-knockout mice. FASEB J 23: 1710-1720. doi:10.1096/fj.08-121335. PubMed: 19237502.
13. Protasi F, Paolini C, Dainese M, (2009) Calsequestrin-1: a new candidate gene for malignant hyperthermia and exertional/environmental heat stroke. J Physiol 587: 3095-3100. doi:10.1113/jphysiol.2009.171967. PubMed: 19417098.
14. Andronache Z, Hamilton SL, Dirksen RT, Melzer W, (2009) A retrograde signal from RyR1 alters DHP receptor inactivation and limits window Ca2+ release in muscle fibers of Y522S RyR1 knock-in mice. Proc Natl Acad Sci U S A 106: 4531-4536. doi:10.1073/pnas.0812661106. PubMed: 19246389.
15. Canato M, Scorzeto M, Giacomello M, Protasi F, Reggiani C, et al. (2010) Massive alterations of sarcoplasmic reticulum free calcium in skeletal muscle fibers lacking calsequestrin revealed by a genetically encoded probe. Proc Natl Acad Sci U S A 107: 22326-22331. doi:10.1073/pnas.1009168108. PubMed: 21135222.
16. Nelson TE, Bedell DM, Jones EW, (1975) Porcine malignant hyperthermia: effects of temperature and extracellular calcium concentration on halothane-induced contracture of susceptible skeletal muscle. Anesthesiology 42: 301-306. doi:10.1097/00000542-197503000-00011. PubMed: 1115384.
17. Nelson TE, Chausmer AB, (1981) Calcium content and contracture in isolated muscle of malignant hyperthermia in pigs. J Pharmacol Exp Ther 219: 107-111. PubMed: 7288598.
18. Fletcher JE, Huggins FJ, Rosenberg H, (1990) The importance of calcium ions for in vitro malignant hyperthermia testing. Can J Anaesth 37: 695-698. doi:10.1007/BF03006495. PubMed: 2208545.
19. Adnet PJ, Krivosic-Horber RM, Adamantidis MM, Reyford H, Cordonnier C, et al. (1991) Effects of calcium-free solution, calcium antagonists, and the calcium agonist BAY K 8644 on mechanical responses of skeletal muscle from patients susceptible to malignant hyperthermia. Anesthesiology 75: 413-419. doi:10.1097/00000542-199109001-00413. PubMed: 1716078.
20. Duke AM, Hopkins PM, Calaghan SC, Halsall JP, Steele DS, (2010) Store-operated Ca2+ entry in malignant hyperthermia-susceptible human skeletal muscle. J Biol Chem 285: 25645-25653. doi:10.1074/jbc.M110.104976. PubMed: 20566647.
21. Shin DW, Pan Z, Kim EK, Lee JM, Bhat MB, et al. (2003) A retrograde signal from calsequestrin for the regulation of store-operated Ca2+ entry in skeletal muscle. J Biol Chem 278: 3286-3292. doi:10.1074/jbc.M209045200. PubMed: 12419813.
22. Zhao X, Min CK, Ko JK, Parness J, Kim do H, et al. (2010) Increased store-operated Ca2+ entry in skeletal muscle with reduced calsequestrin-1 expression. Biophys J 99: 1556-1564. doi:10.1016/j.bpj.2010.06.050. PubMed: 20816068.
23. Zhao X, Weisleder N, Han X, Pan Z, Parness J, et al. (2006) Azumolene inhibits a component of store-operated calcium entry coupled to the skeletal muscle ryanodine receptor. J Biol Chem 281: 33477-33486. doi:10.1074/jbc.M602306200. PubMed: 16945924.
24. Yarotskyy V, Dirksen RT, (2012) Temperature and RyR1 Regulate the Activation Rate of Store-Operated Ca(2+) Entry Current in Myotubes. Biophys J 103: 202-211. doi:10.1016/j.bpj.2012.06.001. PubMed: 22853897.
25. Avila G, Dirksen RT, (2000) Functional impact of the ryanodine receptor on the skeletal muscle L-type Ca(2+) channel. J Gen Physiol 115: 467-480. doi:10.1085/jgp.115.4.467. PubMed: 10736313.
26. Wang Y, Xu L, Duan H, Pasek DA, Eu JP, et al. (2006) Knocking down type 2 but not type 1 calsequestrin reduces calcium sequestration and release in C2C12 skeletal muscle myotubes. J Biol Chem 281: 15572-15581. doi:10.1074/jbc.M600090200. PubMed: 16595676.
27. Paolini C, Quarta M, d'Onofrio L, Reggiani C, Protasi F, (2011) Differential effect of calsequestrin ablation on structure and function of fast and slow twitch skeletal fibers J Biomed Biotechnol (In press).
28. Royer L, Sztretye M, Manno C, Pouvreau S, Zhou J, et al. (2010) Paradoxical buffering of calcium by calsequestrin demonstrated for the calcium store of skeletal muscle. J Gen Physiol 136: 325-338. doi:10.1085/jgp.201010454. PubMed: 20713548.
29. Durham WJ, Aracena-Parks P, Long C, Rossi AE, Goonasekera SA, et al. (2008) RyR1 S-nitrosylation underlies environmental heat stroke and sudden death in Y522S RyR1 knockin mice. Cell 133: 53-65. doi:10.1016/j.cell.2008.02.042. PubMed: 18394989.
30. Sztretye M, Yi J, Figueroa L, Zhou J, Royer L, et al. (2011) Measurement of RyR permeability reveals a role of calsequestrin in termination of SR Ca(2+) release in skeletal muscle. J Gen Physiol 138: 231-247. doi:10.1085/jgp.201010592. PubMed: 21788611.
31. Xiao B, Coste B, Mathur J, Patapoutian A, (2011) Temperature-dependent STIM1 activation induces Ca(2)+ influx and modulates gene expression. Nat Chem Biol 7: 351-358. doi:10.1038/nchembio.558. PubMed: 21499266.
32. Launikonis BS, Ríos E, (2007) Store-operated Ca2+ entry during intracellular Ca2+ release in mammalian skeletal muscle. J Physiol 583: 81-97. doi:10.1113/jphysiol.2007.135046. PubMed: 17569733.
33. Edwards JN, Murphy RM, Cully TR, von Wegner F, Friedrich O, et al. (2010) Ultra-rapid activation and deactivation of store-operated Ca(2+) entry in skeletal muscle. Cell Calcium 47: 458-467. doi:10.1016/j.ceca.2010.04.001. PubMed: 20434768.
34. Dirksen RT, (2009) Checking your SOCCs and feet: the molecular mechanisms of Ca2+ entry in skeletal muscle. J Physiol 587: 3139-3147. doi:10.1113/jphysiol.2009.172148. PubMed: 19406875.
35. Pan Z, Yang D, Nagaraj RY, Nosek TA, Nishi M, et al. (2002) Dysfunction of store-operated calcium channel in muscle cells lacking mg29. Nat Cell Biol 4: 379-383. doi:10.1038/ncb788. PubMed: 11988740.
36. Lyfenko AD, Dirksen RT, (2008) Differential dependence of store-operated and excitation-coupled Ca2+ entry in skeletal muscle on STIM1 and Orai1. J Physiol 586: 4815-4824. doi:10.1113/jphysiol.2008.160481. PubMed: 18772199.
37. Launikonis BS, Barnes M, Stephenson DG, (2003) Identification of the coupling between skeletal muscle store-operated Ca2+ entry and the inositol trisphosphate receptor. Proc Natl Acad Sci U S A 100: 2941-2944. doi:10.1073/pnas.0536227100. PubMed: 12601149.
38. Launikonis BS, Zhou J, Royer L, Shannon TR, Brum G, et al. (2006) Depletion "skraps" and dynamic buffering inside the cellular calcium store. Proc Natl Acad Sci U S A 103: 2982-2987. doi:10.1073/pnas.0511252103. PubMed: 16473932.
39. Paolini C, Quarta M, Nori A, Boncompagni S, Canato M, et al. (2007) Reorganized stores and impaired calcium handling in skeletal muscle of mice lacking calsequestrin-1. J Physiol 583: 767-784. doi:10.1113/jphysiol.2007.138024. PubMed: 17627988.
40. Harrison GG, (1975) Control of the malignant hyperpyrexic syndrome in MHS swine by dantrolene sodium. Br J Anaesth 47: 62-65. doi:10.1093/bja/47.1.62. PubMed: 1148076.
41. Wappler F, (2010) Anesthesia for patients with a history of malignant hyperthermia. Curr Opin Anaesthesiol, 23: 417-22. PubMed: 20173632.
42. Palnitkar SS, Mickelson JR, Louis CF, Parness J, (1997) Pharmacological distinction between dantrolene and ryanodine binding sites: evidence from normal and malignant hyperthermia-susceptible porcine skeletal muscle. Biochem J 326(3):: 847-852. PubMed: 9307036.
43. Parness J, Palnitkar SS, (1995) Identification of dantrolene binding sites in porcine skeletal muscle sarcoplasmic reticulum. J Biol Chem 270: 18465-18472. doi:10.1074/jbc.270.31.18465. PubMed: 7629173.
44. Zhang Y, Rodney GG, Schneider MF, (2005) Effects of azumolene on Ca2+ sparks in skeletal muscle fibers. J Pharmacol Exp Ther 314: 94-102. doi:10.1124/jpet.105.084046. PubMed: 15831441.
45. Kobayashi S, Bannister ML, Gangopadhyay JP, Hamada T, Parness J, et al. (2005) Dantrolene stabilizes domain interactions within the ryanodine receptor. J Biol Chem 280: 6580-6587. doi:10.1074/jbc.M408375200. PubMed: 15611117.
46. Cherednichenko G, Ward CW, Feng W, Cabrales E, Michaelson L, et al. (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. PubMed: 18171728.
47. Fruen BR, Mickelson JR, Louis CF, (1997) Dantrolene inhibition of sarcoplasmic reticulum Ca2+ release by direct and specific action at skeletal muscle ryanodine receptors. J Biol Chem 272: 26965-26971. doi:10.1074/jbc.272.43.26965. PubMed: 9341133.
48. Szentesi P, Collet C, Sárközi S, Szegedi C, Jona I, et al. (2001) Effects of dantrolene on steps of excitation-contraction coupling in mammalian skeletal muscle fibers. J Gen Physiol 118: 355-375. doi:10.1085/jgp.118.4.355. PubMed: 11585849.
49. Bannister RA, Pessah IN, Beam KG, (2009) The skeletal L-type Ca(2+) current is a major contributor to excitation-coupled Ca(2+) entry. J Gen Physiol 133: 79-91. doi:10.1085/jgp.200810105. PubMed: 19114636.