Novel mutations in human and mouse SCN4A implicate AMPK in myotonia and periodic paralysis

Brain

Volumn 137, Issue 12, 2014, Pages 3171-3185

  Corrochano, Silvia ^a   Männikkö, Roope ^b   Joyce, Peter I ^a   McGoldrick, Philip ^b   Wettstein, Jessica ^c   Lassi, Glenda ^d   Rayan, Dipa L Raja ^b   Blanco, Gonzalo ^e   Quinn, Colin ^f   Liavas, Andrianos ^b   Lionikas, Arimantas ^c   Amior, Neta ^b   Dick, James ^b   Healy, Estelle G ^b   Stewart, Michelle ^a   Carter, Sarah ^a   Hutchinson, Marie ^a   Bentley, Liz ^a   Fratta, Pietro ^b   Cortese, Andrea ^g   Cox, Roger ^a   Steve, D ^a   Tucci, Valter ^d   Wackerhage, Henning ^c   Amato, Anthony A ^f   Greensmith, Linda ^b   Koltzenburg, Martin ^b   Hanna, Michael G ^b   Acevedo Arozena, Abraham ^a   more..

^a MRC MAMMALIAN GENETICS UNIT   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF ABERDEEN   (United Kingdom)

^d ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

^e UNIVERSITY OF YORK   (United Kingdom)

^f HARVARD MEDICAL SCHOOL   (United States)

^g C MONDINO NATIONAL NEUROLOGICAL INSTITUTE   (Italy)

Author keywords

AMPK; Mice; Myotonia; Periodic paralysis; SCN4A

Indexed keywords

ETHYLNITROSOUREA; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; LEPTIN; POTASSIUM; SODIUM CHANNEL NAV1.4; SCN4A PROTEIN, HUMAN; SCN4A PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHROMOSOME 11; CONTROLLED STUDY; ELECTROMYOGRAM; ENZYME ACTIVATION; EXOME; EXTENSOR DIGITORUM LONGUS MUSCLE; FEMALE; GRIP STRENGTH; HOMOZYGOSITY; HUMAN; IMMOBILITY; IN VITRO STUDY; MALE; MISSENSE MUTATION; MOTOR COORDINATION; MOUSE; MUSCLE ACTION POTENTIAL; MUSCLE STRENGTH; MUTAGENESIS; MYOTONIA; NONHUMAN; PERIODIC PARALYSIS; PHENOTYPE; POINT MUTATION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; TIBIALIS ANTERIOR MUSCLE; ANIMAL; CHANNELOPATHY; GENETICS; MUTATION; PEDIGREE;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; CHANNELOPATHIES; HUMANS; MICE; MUTATION; MYOTONIA; MYOTONIC DISORDERS; NAV1.4 VOLTAGE-GATED SODIUM CHANNEL; PARALYSES, FAMILIAL PERIODIC; PEDIGREE;

EID: 84922359133     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awu292     Document Type: Article

References (65)

1. Acevedo-Arozena A, Wells S, Potter P, Kelly M, Cox RD, Brown SD. ENU mutagenesis, a way forward to understand gene function. Ann Rev Genomics Hum Genet 2008; 9: 49-69.
2. Agbulut O, Destombes J, Thiesson D, Butler-Browne G. Age-related appearance of tubular aggregates in the skeletal muscle of almost all male inbred mice. Histochem Cell Biol 2000; 114: 477-81.
3. Alesutan I, Munoz C, Sopjani M, Dermaku-Sopjani M, Michael D, Fraser S, et al. Inhibition of Kir2.1 (KCNJ2) by the AMP-activated protein kinase. Biochem Biophys Res Commun 2011; 408: 505-10.
4. Andersen MN, Rasmussen HB. AMPK: a regulator of ion channels. Commun Integr Biol 2012; 5: 480-4.
5. Bendahhou S, Cummins TR, Hahn AF, Langlois S, Waxman SG, Ptacek LJ. A double mutation in families with periodic paralysis defines new aspects of sodium channel slow inactivation. J Clin Invest 2000; 106: 431-8.
6. Bloemberg D, Quadrilatero J. Rapid determination of myosin heavy chain expression in rat, mouse, and human skeletal muscle using multicolor immunofluorescence analysis. PLoS One 2012; 7: e35273.
7. Bradley WG, Taylor R, Rice DR, Hausmanowa-Petruzewicz I, Adelman LS, Jenkison M, et al. Progressive myopathy in hyperkalemic periodic paralysis. Arch Neurol 1990; 47: 1013-7.
8. Cannon SC. Ion-channel defects and aberrant excitability in myotonia and periodic paralysis. Trends Neurosci 1996a; 19: 3-10.
9. Cannon SC. Sodium channel defects in myotonia and periodic paralysis. Ann Rev Neurosci 1996b; 19: 141-64.
10. Cannon SC. Pathomechanisms in channelopathies of skeletal muscle and brain. Ann Rev Neurosci 2006; 29: 387-415.
11. Charles G, Zheng C, Lehmann-Horn F, Jurkat-Rott K, Levitt J. Characterization of hyperkalemic periodic paralysis: a survey of genetically diagnosed individuals. J Neurol 2013; 260: 2606-13.
12. Cheng X, Dib-Hajj SD, Tyrrell L, Waxman SG. Mutation I136V alters electrophysiological properties of the Na(v)1.7 channel in a family with onset of erythromelalgia in the second decade. Mol Pain 2008; 4: 1.
13. Engel WK, Bishop DW, Cunningham GG. Tubular aggregates in type II muscle fibers: ultrastructural and histochemical correlation. J Ultrastruct Res 1970; 31: 507-25.
14. Evans AM, Peers C, Wyatt CN, Kumar P, Hardie DG. Ion channel regulation by the LKB1-AMPK signalling pathway: the key to carotid body activation by hypoxia and metabolic homeostasis at the whole body level. Adv Exp Med Biol 2012; 758: 81-90.
15. Feng Y, Ji X, Sun X, Wang H, Zhang C. Severe phenotypes of paralysis periodica paramyotonia are associated with the Met1592Val mutation in the voltage-gated sodium channel gene (SCN4A) in a Chinese family. J Clin Neurosci 2011; 18: 1138-40.
16. Feng Y, Wang H, Luo XG, Ren Y. Permanent myopathy caused by mutation of SCN4A Metl592Val: observation on myogenesis in vitro and on effect of basic fibroblast growth factor on the muscle. Neurosci Bull 2009; 25: 61-6.
17. Fontaine B, Khurana TS, Hoffman EP, Bruns GA, Haines JL, Trofatter JA, et al. Hyperkalemic periodic paralysis and the adult muscle sodium channel alpha-subunit gene. Science 1990; 250: 1000-2.
18. Fournier E, Arzel M, Sternberg D, Vicart S, Laforet P, Eymard B, et al. Electromyography guides toward subgroups of mutations in muscle channelopathies. Ann Neurol 2004; 56: 650-61.
19. Fournier E, Viala K, Gervais H, Sternberg D, Arzel-Hezode M, Laforet P, et al. Cold extends electromyography distinction between ion channel mutations causing myotonia. Ann Neurol 2006; 60: 356-65.
20. Friedrichsen M, Mortensen B, Pehmoller C, Birk JB, Wojtaszewski JF. Exercise-induced AMPK activity in skeletal muscle: role in glucose uptake and insulin sensitivity. Mol Cell Endocrinol 2013; 366: 204-14.
21. Hardie DG, Sakamoto K. AMPK: a key sensor of fuel and energy status in skeletal muscle. Physiology 2006; 21: 48-60.
22. Hawley SA, Davison M, Woods A, Davies SP, Beri RK, Carling D, et al. Characterization of the AMP-activated protein kinase kinase from rat liver and identification of threonine 172 as the major site at which it phosphorylates AMP-activated protein kinase. J Biol Chem 1996; 271: 27879-87.
23. Hayward LJ, Kim JS, Lee MY, Zhou H, Kim JW, Misra K, et al. Targeted mutation of mouse skeletal muscle sodium channel produces myotonia and potassium-sensitive weakness. J Clin Invest 2008; 118: 1437-49.
24. Hayward LJ, Sandoval GM, Cannon SC. Defective slow inactivation of sodium channels contributes to familial periodic paralysis. Neurology 1999; 52: 1447-53.
25. Ingwersen MS, Kristensen M, Pilegaard H, Wojtaszewski JF, Richter EA, Juel C. Na, K-ATPase activity in mouse muscle is regulated by AMPK and PGC-1alpha. J Membr Biol 2011; 242: 1-10.
26. Jurkat-Rott K, Holzherr B, Fauler M, Lehmann-Horn F. Sodium channe-lopathies of skeletal muscle result from gain or loss of function. Pflugers Arch 2010; 460: 239-48.
27. Jurkat-Rott K, Lehmann-Horn F. Genotype-phenotype correlation and therapeutic rationale in hyperkalemic periodic paralysis. Neurotherapeutics 2007; 4: 216-24.
28. Ke Q, Luo B, Qi M, Du Y, Wu W. Gender differences in penetrance and phenotype in hypokalemic periodic paralysis. Muscle Nerve 2013; 47: 41-5.
29. Kim MK, Lee SH, Park MS, Kim BC, Cho KH, Lee MC, et al. Mutation screening in Korean hypokalemic periodic paralysis patients: a novel SCN4A Arg672Cys mutation. Neuromuscul Disord 2004; 14: 727-31.
30. Kokunai Y, Goto K, Kubota T, Fukuoka T, Sakoda S, Ibi T, et al. A sodium channel myotonia due to a novel SCN4A mutation accompanied by acquired autoimmune myasthenia gravis. Neurosci Lett 2012; 519: 67-72.
31. Li FF, Li QQ, Tan ZX, Zhang SY, Liu J, Zhao EY, et al. A novel mutation in CACNA1S gene associated with hypokalemic periodic paralysis which has a gender difference in the penetrance. J Mol Neurosci 2012; 46: 378-83.
32. Light PE, Wallace CH, Dyck JR. Constitutively active adenosine mono-phosphate-activated protein kinase regulates voltage-gated sodium channels in ventricular myocytes. Circulation 2003; 107: 1962-5.
33. Lossin C, Nam TS, Shahangian S, Rogawski MA, Choi SY, Kim MK, et al. Altered fast and slow inactivation of the N440K Nav1.4 mutant in a periodic paralysis syndrome. Neurology 2012; 79: 1033-40.
34. Luan X, Chen B, Liu Y, Zheng R, Zhang W, Yuan Y. Tubular aggregates in paralysis periodica paramyotonica with T704M mutation of SCN4A. Neuropathology 2009; 29: 579-84.
35. Matthews E, Fialho D, Tan SV, Venance SL, Cannon SC, Sternberg D, et al. The non-dystrophic myotonias: molecular pathogenesis, diagnosis and treatment. Brain 2010; 133 (Pt 1): 9-22.
36. McClatchey AI, McKenna-Yasek D, Cros D, Worthen HG, Kuncl RW, DeSilva SM, et al. Novel mutations in families with unusual and variable disorders of the skeletal muscle sodium channel. Nat Genet 1992; 2: 148-52.
37. Mortensen B, Hingst JR, Frederiksen N, Hansen RW, Christiansen CS, Iversen N, et al. Effect of birth weight and 12 weeks of exercise training on exercise-induced AMPK signaling in human skeletal muscle. Am J Physiol Endocrinol Metabol 2013; 304: E1379-90.
38. Moxley RT 3rd, Ricker K, Kingston WJ, Bohlen R. Potassium uptake in muscle during paramyotonic weakness. Neurology 1989; 39: 952-5.
39. Mu J, Brozinick JT Jr, Valladares O, Bucan M, Birnbaum MJ. A role for AMP-activated protein kinase in contraction-and hypoxia-regulated glucose transport in skeletal muscle. Mol Cell 2001; 7: 1085-94.
40. Nagamitsu S, Matsuura T, Khajavi M, Armstrong R, Gooch C, Harati Y, et al. A "dystrophic" variant of autosomal recessive myotonia conge-nita caused by novel mutations in the CLCN1 gene. Neurology 2000; 55: 1697-703.
41. Nolan PM, Hugill A, Cox RD. ENU mutagenesis in the mouse: application to human genetic disease. Brief Funct Genomics Proteomics 2002; 1: 278-89.
42. Nolan PM, Peters J, Strivens M, Rogers D, Hagan J, Spurr N, et al. A systematic, genome-wide, phenotype-driven mutagenesis programme for gene function studies in the mouse. Nat Genet 2000; 25: 440-3.
43. O'Neill HM, Holloway GP, Steinberg GR. AMPK regulation of fatty acid metabolism and mitochondrial biogenesis: implications for obesity. Mol Cell Endocrinol 2013; 366: 135-51.
44. Okuda S, Kanda F, Nishimoto K, Sasaki R, Chihara K. Hyperkalemic periodic paralysis and paramyotonia congenita-a novel sodium channel mutation. J Neurol 2001; 248: 1003-4.
45. Oswal A, Yeo G. Leptin and the control of body weight: a review of its diverse central targets, signaling mechanisms, and role in the patho-genesis of obesity. Obesity 2010; 18: 221-9.
46. Pedersen BK, Febbraio MA. Muscles, exercise and obesity: skeletal muscle as a secretory organ. Nat Rev Endocrinol 2012; 8: 457-65.
47. Petitprez S, Tiab L, Chen L, Kappeler L, Rosler KM, Schorderet D, et al. A novel dominant mutation of the Nav1.4 alpha-subunit domain I leading to sodium channel myotonia. Neurology 2008; 71: 1669-75.
48. Plassart E, Reboul J, Rime CS, Recan D, Millasseau P, Eymard B, et al. Mutations in the muscle sodium channel gene (SCN4A) in 13 French families with hyperkalemic periodic paralysis and paramyotonia con-genita: phenotype to genotype correlations and demonstration of the predominance of two mutations. Eur J Hum Genet 1994; 2: 110-24.
49. Rojas CV, Wang JZ, Schwartz LS, Hoffman EP, Powell BR, Brown RH Jr. A Met-to-Val mutation in the skeletal muscle Na+ channel alpha-sub-unit in hyperkalaemic periodic paralysis. Nature 1991; 354: 387-9.
50. Sasaki R, Takano H, Kamakura K, Kaida K, Hirata A, Saito M, et al. A novel mutation in the gene for the adult skeletal muscle sodium channel alpha-subunit (SCN4A) that causes paramyotonia congenita of von Eulenburg. Arch Neurol 1999; 56: 692-6.
51. Schiaffino S. Tubular aggregates in skeletal muscle: just a special type of protein aggregates? Neuromuscul Dis 2012; 22: 199-207.
52. Schoser BG, Schroder JM, Grimm T, Sternberg D, Kress W. A large German kindred with cold-aggravated myotonia and a heterozygous A1481D mutation in the SCN4A gene. Muscle Nerve 2007; 35: 599-606.
53. Tan SV, Matthews E, Barber M, Burge JA, Rajakulendran S, Fialho D, et al. Refined exercise testing can aid DNA-based diagnosis in muscle channelopathies. Ann Neurol 2011; 69: 328-40.
54. Tengan CH, Oliveira AS, Morita Mda P, Kiyomoto BH, Schmidt B, Gabbai AA. [Periodic paralysis: anatomo-pathological study of skeletal muscles in 14 patients]. Arq Neuropsiquiatr 1994; 52: 32-40.
55. Trip J, Pillen S, Faber CG, van Engelen BG, Zwarts MJ, Drost G. Muscle ultrasound measurements and functional muscle parameters in non-dystrophic myotonias suggest structural muscle changes. Neuromuscul Dis 2009; 19: 462-7.
56. Tsujino A, Maertens C, Ohno K, Shen XM, Fukuda T, Harper CM, et al. Myasthenic syndrome caused by mutation of the SCN4A sodium channel. Proc Natl Acad Sci USA 2003; 100: 7377-82.
57. Vicart S, Sternberg D, Fontaine B, Meola G. Human skeletal muscle sodium channelopathies. Neurol Sci 2005; 26: 194-202.
58. Vicart S, Sternberg D, Fournier E, Ochsner F, Laforet P, Kuntzer T, et al. New mutations of SCN4A cause a potassium-sensitive normokalemic periodic paralysis. Neurology 2004; 63: 2120-7.
59. Wagner S, Lerche H, Mitrovic N, Heine R, George AL, Lehmann-Horn F. A novel sodium channel mutation causing a hyperkalemic paralytic and paramyotonic syndrome with variable clinical expressivity. Neurology 1997; 49: 1018-25.
60. Webb J, Cannon SC. Cold-induced defects of sodium channel gating in atypical periodic paralysis plus myotonia. Neurology 2008; 70: 755-61.
61. Winder WW, Hardie DG. Inactivation of acetyl-CoA carboxylase and activation of AMP-activated protein kinase in muscle during exercise. Am J Physiol 1996; 270 (2 Pt 1): E299-304.
62. Wu F, Mi W, Burns DK, Fu Y, Gray HF, Struyk AF, et al. A sodium channel knockin mutant (NaV1.4-R669H) mouse model of hypokal-emic periodic paralysis. J Clin Invest 2011; 121: 4082-94.
63. Wu F, Mi W, Hernandez-Ochoa EO, Burns DK, Fu Y, Gray HF, et al. A calcium channel mutant mouse model of hypokalemic periodic paralysis. J Clin Invest 2012; 122: 4580-91.
64. Yoshida H, Bao L, Kefaloyianni E, Taskin E, Okorie U, Hong M, et al. AMP-activated protein kinase connects cellular energy metabolism to KATP channel function. J Mol Cell Cardiol 2012; 52: 410-8.
65. Yoshinaga H, Sakoda S, Good JM, Takahashi MP, Kubota T, Arikawa-Hirasawa E, et al. A novel mutation in SCN4A causes severe myotonia and school-age-onset paralytic episodes. J Neurol Sci 2012; 315: 15-9.