RYR1 and CACNA1S genetic variants identified with statin-associated muscle symptoms

References

• 1 Rosenbaum D, Dallongeville J, Sabouret P, Bruckert E. Discontinuation of statin therapy due to muscular side effects: a survey in real life. Nutr. Metab. Cardiovasc. Dis. 23, 871–875 (2013).Crossref, Medline, CAS, Google Scholar
• 2 Cohen JD, Brinton EA, Ito MK, Jacobson TA. Understanding statin use in America and gaps in patient education (USAGE): an internet-based survey of 10,138 current and former statin users. J. Clin. Lipidol. 6, 208–215 (2012).Crossref, Medline, Google Scholar
• 3 Shek A, Ferrill MJ. Statin–fibrate combination therapy. Ann. Pharmacother. 35, 908–917 (2001).Crossref, Medline, CAS, Google Scholar
• 4 SEARCH Collaborative Group; Link E, Parish S et al. SLCO1B1 variants and statin-induced myopathy – a genomewide study. N. Engl. J. Med. 359, 789–799 (2008).Crossref, Medline, Google Scholar
• 5 Oh J, Ban MR, Miskie BA, Pollex RL, Hegele RA. Genetic determinants of statin intolerance. Lipids Health Dis. 6, 7 (2007).Crossref, Medline, Google Scholar
• 6 Isackson PJ, Ochs-Balcom HM, Ma C et al. Association of common variants in the human eyes shut ortholog (EYS) with statin-induced myopathy: evidence for additional functions of EYS. Muscle Nerve 44, 531–538 (2011).Crossref, Medline, CAS, Google Scholar
• 7 Mangravite LM, Engelhardt BE, Medina MW et al. A statin-dependent QTL for GATM expression is associated with statin-induced myopathy. Nature 502, 377–380 (2013).Crossref, Medline, CAS, Google Scholar
• 8 Luzum JA, Kitzmiller JP, Isackson PJ et al. GATM polymorphism associated with the risk for statin-induced myopathy does not replicate in case–control analysis of 715 dyslipidemic individuals. Cell Metab. 21, 622–627 (2015).Crossref, Medline, CAS, Google Scholar
• 9 Floyd JS, Bis JC, Brody JA, Heckbert SR, Rice K, Psaty BM. GATM locus does not replicate in rhabdomyolysis study. Nature 513, E1–E3 (2014).Crossref, Medline, CAS, Google Scholar
• 10 Santos PC, Gagliardi AC, Miname MH et al. SLCO1B1 haplotypes are not associated with atorvastatin-induced myalgia in Brazilian patients with familial hypercholesterolemia. Eur. J. Clin. Pharmacol. 68, 273–279 (2012).Crossref, Medline, CAS, Google Scholar
• 11 Brunham LR, Lansberg PJ, Zhang L et al. Differential effect of the rs4149056 variant in SLCO1B1 on myopathy associated with simvastatin and atorvastatin. Pharmacogenomics 12, 233–237 (2012).Crossref, Medline, CAS, Google Scholar
• 12 Vladutiu GD, Simmons Z, Isackson PJ et al. Genetic risk factors associated with lipid-lowering drug-induced myopathies. Muscle Nerve 34, 153–162 (2006).Crossref, Medline, CAS, Google Scholar
• 13 Hamel Y, Mamoune A, Mauvais FX et al. Acute rhabdomyolysis and inflammation. J. Inherit. Metab. Dis. 38, 621–628 (2015).Crossref, Medline, CAS, Google Scholar
• 14 Hunter JM, Ahearn ME, Balak CD et al. Novel pathognic variants and genes for myopathies identified by whole exome sequencing. Mol. Genet. Genomic Med. 3, 283–301 (2015).Crossref, Medline, CAS, Google Scholar
• 15 Efthymiou S, Manole A, Houlden H. Next-generation sequencing in neuromuscular diseases. Curr. Opin. Neurol. 29, 527–536 (2016).Crossref, Medline, CAS, Google Scholar
• 16 Abath Neto O, Tassy O, Biancalana V, Zanoteli E, Pourquié O, Laporte J. Integrative data mining highlights candidate genes for monogenic myopathies. PLoS ONE 9, e110888 (2014).Crossref, Medline, Google Scholar
• 17 Knoblauch M, Dagnino-Acosta A, Hamilton SL. Mice with RyR1 mutation (Y524S) undergo hypermetabolic response to simvastatin. Skelet. Muscle 3(1), 22 (2013).Crossref, Medline, Google Scholar
• 18 Carpenter D, Ringrose C, Leo V et al. The role of CACNA1S in predisposition to malignant hyperthermia. BMC Med. Genet. 10, 104 (2009).Crossref, Medline, Google Scholar
• 19 Horstick EJ, Linsley JW, Dowling JJ et al. Stac3 is a component of the excitation–contraction coupling machinery and mutated in Native American myopathy. Nat. Commun. 4, 1952 (2013).Crossref, Medline, Google Scholar
• 20 Voermans NC, Snoeck M, Jungbluth H. RYR-1 related rhabdomyolysis: a common but probably underdiagnosed manifestation of skeletal muscle ryanodine receptor dysfunction. Rev. Neurol. 172, 546–558 (2016).Crossref, Medline, CAS, Google Scholar
• 21 Rosenberg H, Davis M, James D, Pollock N, Stowell K. Malignant hyperthermia. Orphanet. J. Rare Dis. 2, 21 (2007).Crossref, Medline, Google Scholar
• 22 Monnier N, Krivosic-Horber R, Payen JF et al. 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).Crossref, Medline, CAS, Google Scholar
• 23 Robinson R, Carpenter D, Shaw MA, Halsall J, Hopkins P. Mutations in RYR1 in malignant hyperthermia and central core disease. Human Mutat. 27, 977–989 (2006).Crossref, Medline, CAS, Google Scholar
• 24 Amburgey K, Bailey A, Hwang JH et al. Genotype–phenotype correlations in recessive RYR1-related myopathies. Orphanet. J. Rare Dis. 8, 117 (2013).Crossref, Medline, Google Scholar
• 25 Attali R, Aharoni S, Treves S et al. Variable myopathic presentation in a single family with novel skeletal RYR1 mutation. PLoS ONE 8, e69296 (2013).Crossref, Medline, CAS, Google Scholar
• 26 Duarte ST, Oliveira J, Santos R et al. Dominant and recessive RYR1 mutations in adults with core lesions and mild muscle symptoms. Muscle Nerve 44, 102–108 (2011).Crossref, Medline, CAS, Google Scholar
• 27 Dlamini N, Voermans NC, Lillis S et al. Mutations in RYR1 are a common cause of exertional myalgia and rhabdomyolysis. Neuromuscul. Disord. 23, 540–548 (2013).Crossref, Medline, CAS, Google Scholar
• 28 Vladutiu GD, Isackson PJ, Kaufman Ket al.. Genetic risk for malignant hyperthermia in non-anesthesia-induced myopathies. Mol. Genet. Metab. 104, 167–173 (2011).Crossref, Medline, CAS, Google Scholar
• 29 Tammaro A, Di Martino A, Bracco A et al. Novel missense mutations and unexpected multiple changes of RYR1 gene in 75 malignant hyperthermia families. Clin. Genet. 79, 438–447 (2011).Crossref, Medline, CAS, Google Scholar
• 30 Roux-Buisson N, Monnier N, Sagui E et al. Identification of variants of the ryanodine receptor type 1 in patients with exertional heat stroke and positive response to the malignant hyperthermia in vitro contracture test. Br. J. Anaesth. 116, 566–568 (2016).Crossref, Medline, CAS, Google Scholar
• 31 Fiszer D, Shaw MA, Fisher NA et al. Next-generation sequencing of RYR1 and CACNA1S in malignant hyperthermia and exertional heat illness. Anesthesiology 122, 1033–1046 (2015).Crossref, Medline, CAS, Google Scholar
• 32 Stroes ES, Thompson P, Corsini A et al. Statin-associated muscle symptoms: impact on statin therapy. Eur. Heart J. 36(17), 1012–1022 (2015).Crossref, Medline, CAS, Google Scholar
• 33 Kim JH, Jarvik GP, Browning BL et al. Exome sequencing reveals novel rare variants in the ryanodine receptor and calcium channel genes in malignant hyperthermia families. Anesthesiology 119, 1054–1065 (2013).Crossref, Medline, CAS, Google Scholar
• 34 Wang K, Li M, Hakonarson H. ANNOVAR: functional annotation of genetic variants from next-generation sequencing data. Nucleic Acids Res. 38, e164 (2010).Crossref, Medline, CAS, Google Scholar
• 35 Schiemann AH, Stowell KM. Comparison of pathogenicity prediction tools on missense variants in RYR1 and CACNA1S associated with malignant hyperthermia. Br. J. Anaesth. 117, 124–128 (2016).Crossref, Medline, CAS, Google Scholar
• 36 Lopes MC, Joyce C, Ritchie GR et al. A combined functional annotation score for non-synonymous variants. Hum. Hered. 73(1), 47–51 (2012).Crossref, Medline, CAS, Google Scholar
• 37 Gonzalez-Perez A, Lopez-Bigas N. Improving the assessment of the outcome of nonsynonymous SNVs with a consensus deleteriousness score, Condel. Am. J. Hum. Genet. 88(4), 440–449 (2011).Crossref, Medline, CAS, Google Scholar
• 38 Ioannidis NM, Rothstein JH, Pejaver V et al. REVEL: an ensemble method for predicting the pathogenicity of rare missense variants. Am. J. Hum. Genet. 99, 877–885 (2016).Crossref, Medline, CAS, Google Scholar
• 39 Klein A, Lillis S, Munteanu I, Scoto M et al. Clinical and genetic findings in a large cohort of patients with ryanodine receptor 1 gene-associated myopathies. Hum. Mutat. 33, 981–988 (2012).Crossref, Medline, CAS, Google Scholar
• 40 Maggi L, Scoto M, Cirak S et al. Congenital myopathies – clinical features and frequency of individual subtypes diagnosed over a 5-year period in the United Kingdom. Neuromuscul. Disord. 23, 195–205 (2013).Crossref, Medline, CAS, Google Scholar
• 41 Guis S, Figarella-Branger D, Monnier N et al. Multiminicore disease in a family susceptible to malignant hyperthermia: histology, in vitro contracture tests, and genetic characterization. Arch. Neurol. 61, 106–113 (2004).Crossref, Medline, Google Scholar
• 42 Levano S, Vukcevic M, Singer Met al.. Increasing the number of diagnostic mutations in malignant hyperthermia. Hum. Mutat. 30, 590–598 (2009).Crossref, Medline, CAS, Google Scholar
• 43 Roscioli T, Kamsteeg E-J, Buysse K et al. Mutations in ISPD cause Walker–Warburg syndrome and defective glycosylation of alpha-dystroglycan. Nature Genet. 44(581–585), (2012).Google Scholar
• 44 Willer T, Lee H, Lommel M et al. ISPD loss-of-function mutations disrupt dystroglycan O-mannosylation and cause Walker–Warburg syndrome. Nat. Genet. 44, 575–580 (2012).Crossref, Medline, CAS, Google Scholar
• 45 Stephens J, Schiemann AH, Roesl C et al. Functional analysis of RYR1 variants linked to malignant hyperthermia. Temperature (Austin) 3(2), 328–339 (2016).Crossref, Medline, Google Scholar
• 46 Romero NB, Monnier N, Viollet L et al. Dominant and recessive central core disease associated RYR1 mutations and fetal akinesia. Brain 126, 2341–2349 (2003).Crossref, Medline, Google Scholar
• 47 Kimlicka L, Lau K, Tung CC, Van Petegem F. Disease mutations in the ryanodine receptor N-terminal region couple to a mobile intersubumit interface. Nature Commun. 4, 1506 (2013).Crossref, Medline, Google Scholar
• 48 Wang Y, Peng W, Guo HY et al. Next-generation sequencing-based molecular diagnosis of neonatal hypotonia in Chinese population. Sci. Rep. 6, 29088 (2016).Crossref, Medline, CAS, Google Scholar
• 49 Monnier N, Kozak-Ribbens G, Krivosic-Horber R et al. Correlations between genotype and pharmacological, histological, functional, and clinical phenotypes in malignant hyperthermia susceptibility. Hum. Mutat. 26(5), 413–425 (2005).Crossref, Medline, CAS, Google Scholar
• 50 Beckmann JS, Spencer M. Calpain 3, the “gatekeeper” of proper sarcomere assembly, turnover and maintenance. Neuromuscul. Disord. 18(12), 913–921 (2008).Crossref, Medline, Google Scholar
• 51 Gundesli H, Talim B, Korkusuz P et al. Mutation in exon 1f of PLEC, leading to disruption of plectin isoform 1f, causes autosomal-recessive limb-girdle muscular dystrophy. Am. J. Hum. Genet. 87, 834–841 (2010).Crossref, Medline, CAS, Google Scholar
• 52 Hernández-Laín A, Esteban-Pérez J, Montenegro DC, Domínguez-González C. Myosin myopathy with external ophthalmoplegia associated with a novel homozygous mutation in MYH2. Muscle Nerve 55(2), E8–E10 (2017).Crossref, Medline, CAS, Google Scholar
• 53 Tajsharghi HHS, Lindberg C, Lossos A et al. Recessive myosin myopathy with external ophthalmoplegia associated with MYH2 mutations. Eur. J. Hum. Genet. 22(6), 801–808 (2014).Crossref, Medline, CAS, Google Scholar
• 54 Yuchi Z, Yuen SM, Lau K et al. Crystal structures of ryanodine receptor SPRY1 and tandom-repeat domains reveal a critical FKBP12 binding determinant. Nat. Commun. 6, 7947 (2015).Crossref, Medline, CAS, Google Scholar
• 55 Fichna JP, Potulska-Chromik A, Miszta P et al. A novel dominant D109A CRYAB muation in a family with myofibrillar myopathy affects αB-crystallin structure. BBA Cln. 7, 1–7 (2017).Crossref, Medline, Google Scholar
• 56 Vincent AE, Grady JP, Rocha MC et al. Mitochondrial dysfunction in myofibrillar myopathy. Neuromuscul. Disord. 26(10), 691–701 (2016).Crossref, Medline, Google Scholar
• 57 Yan Z, Bai XC, Yan C et al. Structure of the rabbit ryanodine receptor RyR1 at near-atomic resolution. Nature 517, 50–55 (2015).Crossref, Medline, CAS, Google Scholar
• 58 Walsh R, Rutland C, Thomas R, Loughna S. Cardiomyopathy: a systematic review of disease-causing mutations in myosin heavy chain 7 and their phenotypic manifestations. Cardiology 115(1), 49–60 (2010).Crossref, Medline, CAS, Google Scholar
• 59 Oldfors A. Hereditary myosin myopathies. Neuromuscul. Disord. 17(5), 355–367 (2007).Crossref, Medline, Google Scholar
• 60 Patel NJ, Van Dyke KW, Espinoza LR. Limb-girdle muscular dystrophy 2B and Myoshi presentations in dysferlinopathy. Am. J. Med. Sci. 353(5), 484–491 (2017).Crossref, Medline, Google Scholar
• 61 Amato AA, Brown RH Jr. Dysferlinopathies. Handb. Clin. Neurol. 101, 111–118 (2011).Crossref, Medline, Google Scholar
• 62 Lampe LK, Bushby KM. Collagen VI-related muscle disorders. J. Med. Genet. 42(9), 673–685 (2005).Crossref, Medline, CAS, Google Scholar
• 63 Bushby KM, Collins J, Hicks D. Collagen type VI myopathies. Adv. Exp. Med. Biol. 802, 185–199 (2014).Crossref, Medline, CAS, Google Scholar
• 64 Musumeci O, Brady S, Rodolico C et al. Recurrent rhabdomyolysis due to muscle β-enolase deficiency: very rare or underestimated? J. Neurol. 261(12), 2424–2428 (2014).Crossref, Medline, Google Scholar
• 65 Tanabe T, Beam KG, Adams BA, Niidome T, Numa S. Regions of the skeletal muscle dihydropyridine receptor critical for excitation–contraction coupling. Nature 346, 567–569 (1990).Crossref, Medline, CAS, Google Scholar
• 66 Lu X, Xu L, Meissner G. Activation of the skeletal muscle calcium release channel by a cytoplasmic loop of the dihydropyridine receptor. J. Biol. Chem. 269, 6511–6516 (1994).Crossref, Medline, CAS, Google Scholar
• 67 Dorschner MO, Amendola LM, Turner EH et al. Actionable, pathogenic incidental findings in 1,000 participants’ exomes. Am. J. Hum. Genet. 93, 631–640 (2013).Crossref, Medline, CAS, Google Scholar
• 68 Gonsalves SG, Ng D, Johnston JJ et al. Using exome data to identify malignant hyperthermia susceptibility mutations. Anesthesiology 119, 1043–1053 (2013).Crossref, Medline, CAS, Google Scholar
• 69 Nicole S, Chaouch A, Torbergsen T et al. Agrin mutations lead to a congenital myasthenic syndrome with distal muscle weakness and atrophy. Brain 137, 2429–2443 (2014).Crossref, Medline, Google Scholar
• 70 Kraeva N, Sapa A, Dowling JJ, Riazi S. Malignant hyperthermia susceptibility in patients with exertional rhabdomyolysis: a retrospective cohort study and updated systematic review. Can. J. Anaesth. 64(7), 736–743 (2017).Crossref, Medline, Google Scholar
• 71 McCarthy TV, Quane K, Lynch PJ. Ryanodine receptor mutations in malignant hyperthermia and central core disease. Hum. Mutat. 15, 410–417 (2000).Crossref, Medline, CAS, Google Scholar
• 72 Avila G, Dirksen RT. Functional effects of central core disease mutations in the cytoplasmic region of the skeletal muscle ryanodine receptor. J. Gen. Physiol. 118, 277–290 (2001).Crossref, Medline, CAS, Google Scholar
• 73 Dirksen RT, Avila G. Distinct effects on Ca2⁺ handling caused by malignant hyperthermia and central core disease mutations in RYR1. Biophys. J. 87, 3193–3204 (2004).Crossref, Medline, CAS, Google Scholar
• 74 Monnier N, Romero NB, Lerale J et al. Familial and sporadic forms of central core disease are associated with mutations in the C-terminal domain of the skeletal muscle ryanodine receptor. Human Mol. Genet. 10, 2581–2592 (2001).Crossref, Medline, CAS, Google Scholar
• 75 Dirksen RT, Avila G. Altered ryanodine receptor function in central core disease: leaky or uncoupled Ca(2⁺) release channels? Trends Cardiovasc. Med. 12, 189–197 (2002).Crossref, Medline, CAS, Google Scholar
• 76 Efremov RG, Leitner A, Aebersold R, Raunser S. Architecture and conformational switch mechanism of the ryanodine receptor. Nature 517, 39–43 (2015).Crossref, Medline, CAS, Google Scholar
• 77 Zalk R, Clarke OB, des Georges A et al. Structure of a mammalian ryanodine receptor. Nature 517, 44–49 (2015).Crossref, Medline, CAS, Google Scholar
• 78 des Georges A, Clarke OB, Zalk R et al. Structural basis for gating and activation of RYR1. Cell 167, 145–157 (2016).Crossref, Medline, CAS, Google Scholar
• 79 Tung CC, Lobo PA, Kimlicka L, Van Petegem F. The amino-terminal disease hotspot of ryanodine receptors forms a cytoplasmic vestibule. Nature 468, 585–588 (2010).Crossref, Medline, CAS, Google Scholar
• 80 Lobo PA, Van Petegem F. Crystal structures of the N-terminal domains of cardiac and skeletal muscle ryanodine receptors: insights into disease mutations. Structure 17, 1505–1514 (2009).Crossref, Medline, CAS, Google Scholar
• 81 Yuchi Z, Van Petegem F. Ryanodine receptors under the magnifying lens: Insights and limitations of cryo-electron microscopy and x-ray crystallography studies. Cell Calcium 59, 209–227 (2016).Crossref, Medline, CAS, Google Scholar
• 82 Brillantes A-MB, Ondrias K, Scott A et al. Stabilization of calcium release channel (ryanodine receptor) function by FK506-binding protein. Cell 77, 513–523 (1994).Crossref, Medline, CAS, Google Scholar