An RYR1 mutation associated with malignant hyperthermia is also associated with bleeding abnormalities

Science Signaling

Volumn 9, Issue 435, 2016, Pages

  Lopez, Rubèn J ^a   Byrne, Susan ^b   Vukcevic, Mirko ^a   Sekulic Jablanovic, Marijana ^a   Xu, Lifen ^a   Brink, Marijke ^a   Alamelu, Jay ^b   Voermans, Nicol ^c   Snoeck, Marc ^d   Clement, Emma ^e   Muntoni, Francesco ^f   Zhou, Haiyan ^f   Radunovic, Aleksandar ^g   Mohammed, Shehla ^e   Wraige, Elizabeth ^b   Zorzato, Francesco ^a,h   Treves, Susan ^a,h   Jungbluth, Heinz ^b,i,j  

^a UNIVERSITY HOSPITAL BASEL   (Switzerland)

^b ST THOMAS HOSPITAL   (United Kingdom)

^c RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^d CANISIUS WILHELMINA HOSPITAL   (Netherlands)

^e GUY S HOSPITAL   (United Kingdom)

^f UNIVERSITY COLLEGE LONDON   (United Kingdom)

^g ROYAL LONDON HOSPITAL   (United Kingdom)

^h UNIVERSITY OF FERRARA   (Italy)

ⁱ KING'S COLLEGE LONDON   (United Kingdom)

^j KING'S COLLEGE LONDON   (United Kingdom)

more..

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; DANTROLENE; RYANODINE; RYANODINE RECEPTOR 1; VON WILLEBRAND FACTOR; RYANODINE RECEPTOR; RYANODINE RECEPTOR 1, MOUSE;

ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLEEDING DISORDER; BLEEDING TIME; CALCIUM HOMEOSTASIS; CELL FUNCTION; CONTROLLED STUDY; FEMALE; GAIN OF FUNCTION MUTATION; GENETIC ASSOCIATION; GENETIC SUSCEPTIBILITY; HUMAN; HUMAN CELL; MALE; MALIGNANT HYPERTHERMIA; MEMBRANE POTENTIAL; MENORRHAGIA; MOUSE; MUSCLE CONTRACTION; NONHUMAN; POSTPARTUM HEMORRHAGE; PRIORITY JOURNAL; RHABDOMYOLYSIS; SPONTANEOUS ABORTION; THROMBOCYTE FUNCTION; VASCULAR SMOOTH MUSCLE CELL; AMINO ACID SUBSTITUTION; ANIMAL; BLOOD CLOTTING DISORDER; CALCIUM SIGNALING; GENETICS; METABOLISM; MISSENSE MUTATION; MUTANT MOUSE STRAIN; PATHOLOGY; SMOOTH MUSCLE CELL; VASCULAR SMOOTH MUSCLE;

AMINO ACID SUBSTITUTION; ANIMALS; BLOOD COAGULATION DISORDERS; CALCIUM SIGNALING; DANTROLENE; FEMALE; HUMANS; MALE; MALIGNANT HYPERTHERMIA; MICE; MICE, MUTANT STRAINS; MUSCLE, SMOOTH, VASCULAR; MUTATION, MISSENSE; MYOCYTES, SMOOTH MUSCLE; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL;

EID: 84978394446     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.aad9813     Document Type: Article

References (56)

1. D. L. Kasper, Harrison's Principles of Internal Medicine, D. L. Kasper, A. Fauci, S. L. Hauser, D. L. Longo, J. L. Jameson, J. Loscalzo, Eds. (McGraw Hill Education Medical, New York, ed. 19, 2015).
2. A. Tosetto, G. Castaman, F. Rodeghiero, Bleeders, bleeding rates, and bleedingscore. J. Thromb. Haemost. 11 (Suppl. 1), 142-150 (2013).
3. P. H. Shaw, S. Reynolds, S. Gunawardena, L. Krishnamurti, A. K. Ritchey, The prevalence of bleeding disorders among healthy pediatric patients with abnormal preprocedural coagulation studies. J. Pediatr. Hematol. Oncol. 30, 135-141 (2008).
4. N. Monnier, R. Krivosic-Horber, J.-F. Payen, G. Kozak-Ribbens, Y. Nivoche, P. Adnet, H. Reyford, J. Lunardi, Presence of two different genetic traits in malignant hyperthermia families: Implication for genetic analysis, diagnosis, and incidence of malignant hyperthermia susceptibility. Anesthesiology 97, 1067-1074 (2002).
5. N. Dlamini, N. C. Voermans, S. Lillis, K. Stewart, E.-J. Kamstee, G. Drost, R. Quinlivan, M. Snoeck, F. Norwood, A. Radonovic, V. Straub, M. Roberts, A. E. Vrancken, W. L. van der Pol, R. I. F. M. de Coo, A. Y. Manzur, S. Abbs, A. King, M. Lammens, P. M. Hopkins, S. Mohammed, S. Treves, F. Muntoni, E.Wraige, M. R. Davis, B. van Engelen, H. Jungbluth, Mutations in RYR1 are a common cause of exertional myalgia and rhabdomyolysis. Neuromuscul. Disord. 23, 540-548 (2013).
6. S. Treves, H. Jungbluth, F. Muntoni, F. Zorzato, Congenital muscle disorders with cores: The ryanodine receptor calcium channel paradigm. Curr. Opin. Pharmacol.319-326 (2008).
7. I. Colombo, M. Scoto, S. A. Robb, L. Maggi, V. Gowda, T. Cullup, M. Yau, R. Phadke,C. Sewry, H. Jungbluth, F. Muntoni, Congenital myopathies: Natural history of a large pediatric cohort. Neurology 84, 28-35 (2015).
8. M. Denborough, Malignant Hyperthermia. Lancet 352, 1131-1135 (1998).
9. C. R. Stephen, Fulminant hyperthermia during anesthesia and surgery. JAMA 202, 178-182 (1967).
10. W. G. Cullen, Malignant hyperpyrexia during general anaesthesia: A report of two cases. Can. Anaesth. Soc. J. 13, 437-443 (1966).
11. J. C. Daniels, I. M. Polayes, R. Villar, F. W. Hehre, Malignant hyperthermia with disseminated intravascular coagulation during general anesthesia: A case report. Anesth. Analg. 48, 877-883 (1969).
12. M. Chelu, S. A. Goonasekera, W. J. Durham, W. Tang, J. D. Lueck, J. Riehl, I. N. Pessah, P. Zhang, M. B. Bhattacharjee, R. T. Dirksen, S. L. Hamilton, Heat- and anesthesia-induced malignant hyperthermia in an RyR1 knock-in mouse. FASEB J. 20, 329-330 (2006).
13. M. J. Berridge, Smooth muscle cell calcium activation mechanisms. J. Physiol. 586, 5047-5061 (2008).
14. Y.-M. Zheng, Q.-S. Wang, Q.-H. Liu, R. Rathore, V. Yadav, Y.-X. Wang, Heterogeneous gene expression and functional activity of ryanodine receptors in resistance and conduit pulmonary as well as mesenteric artery smooth muscle cells. J. Vasc. Res. 45, 469-479 (2008).
15. T. Vaithianathan, D. Narayanan, M. T. Asuncion-Chin, L. H. Jeyakumar, J. Liu, S. Fleischer, J. H. Jaggar, A. M. Dopico, Subtype identification and functional characterization of ryanodine receptors in rat cerebral artery myocytes. Am. J. Physiol. Cell Physiol. 299, C264-C278 (2010).
16. X.-Q. Li, Y.-M. Zheng, R. Rathore, J. Ma, H. Takeshima, Y.-X. Wang, Genetic evidence for functional role of ryanodine receptor 1 in pulmonary artery smooth muscle cells. Pflugers Arch. 457, 771-783 (2009).
17. E. B. Westcott, E. L. Goodwin, S. S Segal, W. F. Jackson, Function and expression of ryanodine receptors and inositol 1,4,5-trisphopshate receptors in smooth muscle cells of murine feed arteries and arterioles. J. Physiol. 590, 1849-1869 (2012).
18. M. T. Nelson, H. Cheng, M. Rubart, L. F. Santana, A. D. Bonev, H. J. Knot,W. J. Lederer, Relaxation of arterial smooth muscle by calcium sparks. Science 270, 633-637 (1995).
19. J. H. Jaggar, V. A. Porter, W. J. Lederer, M. T. Nelson, Calcium sparks in smooth muscle. Am. J. Physiol. Cell Phyiol. 278, C235-C256 (2000).
20. T. Krause, M. U. Gerbershagen, M. Fiege, R. Weibhorn, F. Wappler, Dantrolene- A review of its pharmacology, therapeutic use and new developments. Anaesthesia 59, 364-373 (2004).
21. B. R. Fruen, J. R. Mickelson, C. F. Louis, Dantrolene inhibition of sarcoplasmic reticulum Ca2+ release by direct and specific action at skeletal muscle ryanodine receptors. J. Biol. Chem. 272, 26965-26971 (1997).
22. M. Snoeck, B. G. van Engelen, B. Kusters, M. Lammens, R. Meijer, J. P. F. Molenaar, J. Raaphorst, C. C. Verschuuren-Bemelmans, C. S. M. Straathof, L. T. L. Sie, I. F. de Coo, W. L. van der Pol, M. de Visser, H. Scheffer, S. Treves, H. Jungbluth, N. C. Voermans, E.-J. Kamsteeg, RYR1-related myopathies: A wide spectrum of phenotypes throughout life. Eur. J. Neurol. 22, 1094-1112 (2015).
23. H. Zhou, S. Lillis, R. E. Loy, F. Ghassemi, M. R. Rose, F. Norwood, K. Mills, S. Al-Sarraj, R. J. M. Lane, L. Feng, E. Matthews, C. A. Sewry, S. Abbs, S. Buk, M. Hanna, S. Treves, R. T. Dirksen, G. Meissner, F. Muntoni, H. Jungbluth, Multi-minicore disease and atypical periodic paralysis associated with novel mutations in the skeletal muscle ryanodine receptor (RYR1) gene. Neuromuscul. Disord. 20, 166-173 (2010).
24. Y. Liu, N. L. Jennings, A. M. Dart, X.-J. Du, Standardizing a simpler, more sensitive and accurate tail bleeding assay in mice. World J. Exp. Med. 2, 30-36 (2012).
25. M. Vukcevic, F. Zorzato, S. Keck, D. A. Tsakiris, J. Keiser, R. M. Maizels, S. Treves, Gain of function in the immune system caused by a ryanodine receptor 1 mutation. J. Cell Sci. 126, 3485-3492 (2013).
26. C. J. Hartley, A. K. Reddy, S. Mandala, M. L. Entman, L. H. Michael, G. E. Taffet, Doppler velocity measurements from large and small arteries of mice. Am. J. Physiol. Heart Circ. Physiol. 301, H269-H278 (2011).
27. J. C. Sullivan, B. Wang, E. I. Boesen, G. D'Angelo, J. S. Pollock, D. M. Pollock, Novel use of ultrasound to examine regional blood flow in the mouse kidney. Am. J. Physiol. Renal Physiol. 297, F228-F235 (2009).
28. P. J. Pritchard, J. C. Leylegian, R. Bhaskaran, Fox and McDonald's Introduction to Fluid Mechanics (John Wiley & Sons, New York, ed. 8, 2015).
29. D. Paulin, Z. Li, Desmin: A major intermediate filament protein essential for the structural integrity and function of muscle. Exp. Cell Res. 301, 1-7 (2004).
30. M. F. Navedo, G. C. Amberg, R. E.Westenbroeck, M. J. Sinnegger-Brauns,W. A. Catterall, J. Striessnig, L. F. Santana, Cav1.3 channels produce persistent calcium sparklets, but Cav1.2 channels are responsible for sparklets in mouse arterial smooth muscle. Am. J. Physiol. Heart Circ. Physiol. 293, H1359-H1370 (2007).
31. M. Gollasch, H. Haase, C. Ried, C. Lindschau, I. Morano, F. C. Luft, H. L. Haller, L-typecalcium channel expression depends on the differentiated state of vascular smooth muscle cells. FASEB J. 12, 593-601 (1998).
32. X.-R. Yang, M.-J. Lin, K.-P. Yip, L. H. Jeyakumar, S. Fleischer, G. P. H. Leing, J. S. K. Sham, Multiple ryanodine receptor subtypes and heterogeneous ryanodine receptor-gated Ca2+ stores in pulmonary arterial smooth muscle cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 289, L338-L348 (2005).
33. R. E. Lesh, G. F. Nixon, S. Fleischer, J. A. Airey, A. P. Somplyo, A. V. Somlyo, Localization of ryanodine receptors in smooth muscle. Circ. Res. 82, 175-185 (1998).
34. L. M. Lifshitz, J. D. Carmichael, F. A. Lai, V. Sorrentino, K. Bellvè, K. E. Fogarty, R. ZhuGe, Spatial organization of RYRs and BK channels underlying the activation of STOCs by Ca2+ sparks in airway myocytes. J. Gen. Physiol. 138, 195-209 (2011).
35. J. H. Clark, N. P. Kinnear, S. Kalujnaia, G. Cramb, S. Fleischer, L. H. Jeyakumar, F. Wuytack, A. M. Evans, Identification of functionally segregated sarcoplasmic reticulum calcium stores in pulmonary arterial smooth muscle cells. J. Biol. Chem. 285, 13542-13549 (2010).
36. P. T. Nowiki, S. Flavahan, H. Hassanain, S. Mitra, S. Holland, P. J. Goldschmidt-Clemont, N. A. Flavahan, Redox signalling of the arteriolar myogenic response. Circ. Res. 89, 114-116 (2001).
37. S. Treves, A. A. Anderson, S. Ducreux, A. Divet, C. Bleunven, C. Grasso, S. Paesante, F. Zorzato, Ryanodine receptor 1 mutation, dysregulation of calcium homeostasis and neuromuscular disorders. Neuromuscul. Disord. 15, 577-587 (2005).
38. R. Robinson, D. Carpenter, M.-A. Shaw, J. Halsall, P. Hopkins, Mutations in RYR1 in malignant hyperthermia and central core disease. Hum. Mutat. 27, 977-989 (2006).
39. A. D. Lyfenko, S. A. Goonasekera, R. T. Dirksen, Dynamic alterations in myoplasmic Ca2+ in malignant hyperthermia and central core disease. Biochem. Biophys. Res. Commun. 322, 1256-1266 (2004).
40. T. Girard, D. Cavagna, E. Padovan, G. Spagnoli, A. Urwyler, F. Zorzato, S. Treves, B-lymphocytes from malignant hyperthermia-susceptible patients have an increased sensitivity to skeletal muscle ryanodine receptor activators. J. Biol. Chem. 276, 48077-48082 (2001).
41. S. Fleischer, M. Inui, Biochemistry and biophysics of excitation-contraction coupling. Annu. Rev. Biophys. Biophys. Chem. 18, 333-364 (1989).
42. L. Xu, Y. Wang, N. Yamaguchi, D. A. Pasek, G. Meissner, Single channel properties of heterotetrameric mutant RyR1 ion channels linked to core myopathies. J. Biol. Chem. 283, 6321-6329 (2008).
43. S. C. Jackson, L. Odiaman, R. T. Card, J. G. van der Bom, M.-C. Poon, Suspected collagen disorders in the bleeding disorder clinic: A case-control study. Haemophilia 19, 246-250 (2013).
44. G. Wiegand, M. Hofbeck, M. Zenker, U. Budde, R. Rauch, Bleeding diathesis in Noonan syndrome: Is acquired von Willebrand syndrome the clue? Thromb. Res. 130, e251-e254 (2012).
45. G. Krishnamoorthy, S. K. Sonkusare, T. J. Heppner, M. T. Nelson, Opposing roles of smooth muscle BK channels and ryanodine receptors in the regulation of nerveevoked constriction of mesenteric resistance arteries. Am. J. Physiol. Heart Circ. Physiol. 306, H981-H988 (2014).
46. H. Cheng, W. J. Lederer, Calcium sparks. Physiol. Rev. 88, 1491-1545 (2008).
47. Y. Li, R. A. Lorca, X. Ma, A. Rhodes, S. K. England, BK channels regulate myometrial contraction by modulating nuclear translocation of NF-kB. Endocrinology 155, 3112-3122 (2014).
48. 2+-activated and voltage-activated K+ channels contribute to the rise and maintenance of estrogen-induced uterine vasodilation and maintenance of blood pressure. Endocrinology 153, 6012-6020 (2012).
49. 2+ sparks in urinary bladder smooth muscle. J. Cell Sci. 120, 3784-3791(2007).
50. M. Bowman, G. Mundell, J. Grabell, W. M. Hopman, D. Rapson, D. Lillicrap, P. James, Generation and validation of the condensed MCMDM-1VWD bleeding questionnaire for von Willebrand disease. J. Thromb. Haemost. 6, 2062-2066 (2008).
51. S. Tao, D. Yamazaki, S. Komazaki, C. Zhao, T. Iida, S. Kakizawa, Y. Imaizumi, H. Takeshima, Facilitated hyperpolarization signaling in vascular smooth muscle-overexpressing TRIC-A channels. J. Biol. Chem. 288, 15581-15589 (2013).
52. M. Sekulic-Jablanovic, A. Palmowski-Wolfe, F. Zorzato, S. Treves, Characterization of excitation-contraction coupling components in human extraocular muscles. Biochem. J. 466, 29-36 (2015).
53. J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preiblisch, C. Rueden, S. Saalfeld, B. Schmid, J. Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, A. Cardona, Fiji: An open-source platform for biological-image analysis. Nat. Methods 9, 676-682 (2012).
54. E. Picht, A. V. Zima, L. A. Blatter, D. M. Bers, SparkMaster: Automated calcium spark analysis with ImageJ. Am. J. Physiol. Cell Physiol. 293, C1073-C1081 (2007).
55. H. Zhou, O. Rokach, L. Feng, I. Munteanu, K. Mamchaoui, J. M. Wilmshurst, C. Sewry, A. Y. Manzur, K. Pillay, V. Mouly, M. Duchen, H. Jungbluth, S. Treves, F. Muntoni, RyR1 deficiency in congenital myopathies disrupts excitation-contraction coupling. Hum. Mutat. 34, 986-996 (2013).
56. V.Dell'Asta,R. Gatti,G.Orlandini,P.A.Rossi,B.M.Rotoli,R. Sala,O.Bussolati,G.C.Gazzola, Membrane potential changes visualized in complete growth media through confocal laser scanning microscopy of bis-oxonol-loaded cells. Exp. Cell Res. 231, 260-267 (1997).