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Neurotherapeutics

, Volume 15, Issue 4, pp 954–965 | Cite as

Skeletal Muscle Channelopathies

  • Lauren Phillips
  • Jaya R. Trivedi
Review

Abstract

Skeletal muscle channelopathies are rare heterogeneous diseases with marked genotypic and phenotypic variability. These disorders cause lifetime disability and impact quality of life. Despite advances in understanding of the molecular pathology of these disorders, the diverse phenotypic manifestations remain a challenge in diagnosis, therapeutic, genetic counseling, and research planning. Electrodiagnostic testing is useful in directing the diagnosis, but has several limitations: patient discomfort, time consuming, and significant overlap of findings in muscle channelopathies. Although genetic testing is the gold standard in making a definitive diagnosis, a mutation might not be identified in many patients with a well-supported clinical diagnosis of periodic paralysis. In the recent past, there have been landmark clinical trials in non-dystrophic myotonia and periodic paralysis which are encouraging as they demonstrate the ability of robust clinical research consortia to conduct well-controlled trials of rare diseases.

Key Words

Channelopathies ion channel non-dystrophic myotonia periodic paralysis electrophysiology 

References

  1. 1.
    Raja Rayan DL, Hanna MG. Skeletal muscle channelopathies: nondystrophic myotonias and periodic paralysis. Curr Opin Neurol. 2010;23(5):466–76.CrossRefPubMedGoogle Scholar
  2. 2.
    Statland JM, Barohn RJ. Muscle channelopathies: the nondystrophic myotonias and periodic paralyses. Continuum (Minneap Minn). 2013;19(6 Muscle Disease):1598–614.PubMedPubMedCentralGoogle Scholar
  3. 3.
    Paninka RM, Carlos-Lima E, Lindsey SC, Kunii IS, Dias-da-Silva MR, Arcisio-Miranda M. Down-regulation of Kir2.6 channel by c-termini mutation D252N and its association with the susceptibility to Thyrotoxic Periodic Paralysis. Neuroscience. 2017;346:197–202.CrossRefPubMedGoogle Scholar
  4. 4.
    Cannon SC. Pathomechanisms in channelopathies of skeletal muscle and brain. Annu Rev Neurosci. 2006;29:387–415.CrossRefPubMedGoogle Scholar
  5. 5.
    Emery AE. Population frequencies of inherited neuromuscular diseases--a world survey. Neuromuscul Disord. 1991;1(1):19–29.CrossRefPubMedGoogle Scholar
  6. 6.
    Fialho D, Schorge S, Pucovska U, Davies NP, Labrum R, Haworth A, et al. Chloride channel myotonia: exon 8 hot-spot for dominant-negative interactions. Brain. 2007;130(Pt 12):3265–74.CrossRefPubMedGoogle Scholar
  7. 7.
    Hoffman EP, Wang J. Duchenne-Becker muscular dystrophy and the nondystrophic myotonias. Paradigms for loss of function and change of function of gene products. Arch Neurol. 1993;50(11):1227–37.CrossRefPubMedGoogle Scholar
  8. 8.
    Lehmann-Horn F, Rudel R. Channelopathies: the nondystrophic myotonias and periodic paralyses. Semin Pediatr Neurol. 1996;3(2):122–39.CrossRefPubMedGoogle Scholar
  9. 9.
    Pinessi L, Bergamini L, Cantello R, Di Tizio C. Myotonia congenita and myotonic dystrophy: descriptive epidemiological investigation in Turin, Italy (1955-1979). Ital J Neurol Sci. 1982;3(3):207–10.CrossRefPubMedGoogle Scholar
  10. 10.
    Ptacek LJ, George AL, Jr., Griggs RC, Tawil R, Kallen RG, Barchi RL, et al. Identification of a mutation in the gene causing hyperkalemic periodic paralysis. Cell. 1991;67(5):1021–7.CrossRefPubMedGoogle Scholar
  11. 11.
    Sun C, Tranebjaerg L, Torbergsen T, Holmgren G, Van Ghelue M. Spectrum of CLCN1 mutations in patients with myotonia congenita in Northern Scandinavia. Eur J Hum Genet. 2001;9(12):903–9.CrossRefPubMedGoogle Scholar
  12. 12.
    Lion-Francois L, Mignot C, Vicart S, Manel V, Sternberg D, Landrieu P, et al. Severe neonatal episodic laryngospasm due to de novo SCN4A mutations: a new treatable disorder. Neurology. 2010;75(7):641–5.CrossRefPubMedGoogle Scholar
  13. 13.
    Orrell RW, Jurkat-Rott K, Lehmann-Horn F, Lane RJ. Familial cramp due to potassium-aggravated myotonia. J Neurol Neurosurg Psychiatry. 1998;65(4):569–72.CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Lacomis D, Gonzales JT, Giuliani MJ. Fluctuating clinical myotonia and weakness from Thomsen’s disease occurring only during pregnancies. Clin Neurol Neurosurg. 1999;101(2):133–6.CrossRefPubMedGoogle Scholar
  15. 15.
    Fialho D, Kullmann DM, Hanna MG, Schorge S. Non-genomic effects of sex hormones on CLC-1 may contribute to gender differences in myotonia congenita. Neuromuscul Disord. 2008;18(11):869–72.CrossRefPubMedGoogle Scholar
  16. 16.
    Basu A, Nishanth P, Ifaturoti O. Pregnancy in women with myotonia congenita. Int J Gynaecol Obstet. 2009;106(1):62–3.CrossRefPubMedGoogle Scholar
  17. 17.
    Sun C, Van Ghelue M, Tranebjaerg L, Thyssen F, Nilssen O, Torbergsen T. Myotonia congenita and myotonic dystrophy in the same family: coexistence of a CLCN1 mutation and expansion in the CNBP (ZNF9) gene. Clin Genet. 2011;80(6):574–80.CrossRefPubMedGoogle Scholar
  18. 18.
    Suominen T, Schoser B, Raheem O, Auvinen S, Walter M, Krahe R, et al. High frequency of co-segregating CLCN1 mutations among myotonic dystrophy type 2 patients from Finland and Germany. J Neurol. 2008;255(11):1731–6.CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Bugiardini E, Rivolta I, Binda A, Soriano Caminero A, Cirillo F, Cinti A, et al. SCN4A mutation as modifying factor of myotonic dystrophy type 2 phenotype. Neuromuscul Disord. 2015;25(4):301–7.CrossRefPubMedGoogle Scholar
  20. 20.
    Baumann P, Myllyla VV, Leisti J. Myotonia congenita in northern Finland: an epidemiological and genetic study. J Med Genet. 1998;35(4):293–6.CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Colding-Jorgensen E. Phenotypic variability in myotonia congenita. Muscle Nerve. 2005;32(1):19–34.CrossRefPubMedGoogle Scholar
  22. 22.
    Streib EW. Paramyotonia congenita: successful treatment with tocainide. Clinical and electrophysiologic findings in seven patients. Muscle Nerve. 1987;10(2):155–62.CrossRefPubMedGoogle Scholar
  23. 23.
    Becker PE, Knussmann R, Kuhn E. Myotonia congenita and syndromes associated with myotonia : clinical-genetic studies of the nondystrophic myotonias. Stuttgart: Thieme; 1977. x, 181 p. p.Google Scholar
  24. 24.
    Trivedi JR, Bundy B, Statland J, Salajegheh M, Rayan DR, Venance SL, et al. Non-dystrophic myotonia: prospective study of objective and patient reported outcomes. Brain. 2013;136(Pt 7):2189–200.CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Trip J, Drost G, Ginjaar HB, Nieman FH, van der Kooi AJ, de Visser M, et al. Redefining the clinical phenotypes of non-dystrophic myotonic syndromes. J Neurol Neurosurg Psychiatry. 2009;80(6):647–52.CrossRefPubMedGoogle Scholar
  26. 26.
    Ptacek LJ, Trimmer JS, Agnew WS, Roberts JW, Petajan JH, Leppert M. Paramyotonia congenita and hyperkalemic periodic paralysis map to the same sodium-channel gene locus. Am J Hum Genet. 1991;49(4):851–4.PubMedPubMedCentralGoogle Scholar
  27. 27.
    Ptacek LJ, Tyler F, Trimmer JS, Agnew WS, Leppert M. Analysis in a large hyperkalemic periodic paralysis pedigree supports tight linkage to a sodium channel locus. Am J Hum Genet. 1991;49(2):378–82.PubMedPubMedCentralGoogle Scholar
  28. 28.
    Fontaine B. Periodic paralysis, myotonia congenita and sarcolemmal ion channels: a success of the candidate gene approach. Neuromuscul Disord. 1993;3(2):101–7.CrossRefPubMedGoogle Scholar
  29. 29.
    Ptacek LJ, Johnson KJ, Griggs RC. Genetics and physiology of the myotonic muscle disorders. N Engl J Med. 1993;328(7):482–9.CrossRefPubMedGoogle Scholar
  30. 30.
    Matthews E, Tan SV, Fialho D, Sweeney MG, Sud R, Haworth A, et al. What causes paramyotonia in the United Kingdom? Common and new SCN4A mutations revealed. Neurology. 2008;70(1):50–3.CrossRefPubMedGoogle Scholar
  31. 31.
    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.CrossRefPubMedGoogle Scholar
  32. 32.
    Ptacek LJ, George AL, Jr., Barchi RL, Griggs RC, Riggs JE, Robertson M, et al. Mutations in an S4 segment of the adult skeletal muscle sodium channel cause paramyotonia congenita. Neuron. 1992;8(5):891–7.CrossRefPubMedGoogle Scholar
  33. 33.
    Ricker K, Moxley RT, III, Heine R, Lehmann-Horn F. Myotonia fluctuans. A third type of muscle sodium channel disease. Arch Neurol. 1994;51(11):1095–102.CrossRefPubMedGoogle Scholar
  34. 34.
    Trudell RG, Kaiser KK, Griggs RC. Acetazolamide-responsive myotonia congenita. Neurology. 1987;37(3):488–91.CrossRefPubMedGoogle Scholar
  35. 35.
    Singh RR, Tan SV, Hanna MG, Robb SA, Clarke A, Jungbluth H. Mutations in SCN4A: a rare but treatable cause of recurrent life-threatening laryngospasm. Pediatrics. 2014;134(5):e1447–50.CrossRefPubMedGoogle Scholar
  36. 36.
    Matthews E, Silwal A, Sud R, Hanna MG, Manzur AY, Muntoni F, et al. Skeletal Muscle Channelopathies: Rare Disorders with Common Pediatric Symptoms. J Pediatr. 2017;188:181–5 e6.CrossRefPubMedGoogle Scholar
  37. 37.
    Venables GS, Bates D, Shaw DA. Hypothyroidism with true myotonia. J Neurol Neurosurg Psychiatry. 1978;41(11):1013–5.CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Miller TM. Differential diagnosis of myotonic disorders. Muscle Nerve. 2008;37(3):293–9.CrossRefPubMedGoogle Scholar
  39. 39.
    Hanisch F, Kraya T, Kornhuber M, Zierz S. Diagnostic impact of myotonic discharges in myofibrillar myopathies. Muscle Nerve. 2013;47(6):845–8.CrossRefPubMedGoogle Scholar
  40. 40.
    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(5):650–61.CrossRefPubMedGoogle Scholar
  41. 41.
    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(3):356–65.CrossRefPubMedGoogle Scholar
  42. 42.
    McManis PG, Lambert EH, Daube JR. The exercise test in periodic paralysis. Muscle Nerve. 1986;9(8):704–10.CrossRefPubMedGoogle Scholar
  43. 43.
    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(2):328–40.CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Morrow JM, Matthews E, Raja Rayan DL, Fischmann A, Sinclair CD, Reilly MM, et al. Muscle MRI reveals distinct abnormalities in genetically proven non-dystrophic myotonias. Neuromuscul Disord. 2013;23(8):637–46.CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Wu FF, Ryan A, Devaney J, Warnstedt M, Korade-Mirnics Z, Poser B, et al. Novel CLCN1 mutations with unique clinical and electrophysiological consequences. Brain. 2002;125(Pt 11):2392–407.CrossRefPubMedGoogle Scholar
  46. 46.
    Saviane C, Conti F, Pusch M. The muscle chloride channel ClC-1 has a double-barreled appearance that is differentially affected in dominant and recessive myotonia. J Gen Physiol. 1999;113(3):457–68.CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Bryant SH, Morales-Aguilera A. Chloride conductance in normal and myotonic muscle fibres and the action of monocarboxylic aromatic acids. J Physiol. 1971;219(2):367–83.CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Adrian RH, Bryant SH. On the repetitive discharge in myotonic muscle fibres. J Physiol. 1974;240(2):505–15.CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Pusch M, Steinmeyer K, Koch MC, Jentsch TJ. Mutations in dominant human myotonia congenita drastically alter the voltage dependence of the CIC-1 chloride channel. Neuron. 1995;15(6):1455–63.CrossRefPubMedGoogle Scholar
  50. 50.
    Koch MC, Steinmeyer K, Lorenz C, Ricker K, Wolf F, Otto M, et al. The skeletal muscle chloride channel in dominant and recessive human myotonia. Science. 1992;257(5071):797–800.CrossRefPubMedGoogle Scholar
  51. 51.
    George AL, Jr., Crackower MA, Abdalla JA, Hudson AJ, Ebers GC. Molecular basis of Thomsen’s disease (autosomal dominant myotonia congenita). Nat Genet. 1993;3(4):305–10.CrossRefPubMedGoogle Scholar
  52. 52.
    George AL, Jr., Sloan-Brown K, Fenichel GM, Mitchell GA, Spiegel R, Pascuzzi RM. Nonsense and missense mutations of the muscle chloride channel gene in patients with myotonia congenita. Hum Mol Genet. 1994;3(11):2071–2.PubMedGoogle Scholar
  53. 53.
    Meyer-Kleine C, Steinmeyer K, Ricker K, Jentsch TJ, Koch MC. Spectrum of mutations in the major human skeletal muscle chloride channel gene (CLCN1) leading to myotonia. Am J Hum Genet. 1995;57(6):1325–34.PubMedPubMedCentralGoogle Scholar
  54. 54.
    Zhang J, George AL, Jr., Griggs RC, Fouad GT, Roberts J, Kwiecinski H, et al. Mutations in the human skeletal muscle chloride channel gene (CLCN1) associated with dominant and recessive myotonia congenita. Neurology. 1996;47(4):993–8.CrossRefPubMedGoogle Scholar
  55. 55.
    Papponen H, Toppinen T, Baumann P, Myllyla V, Leisti J, Kuivaniemi H, et al. Founder mutations and the high prevalence of myotonia congenita in northern Finland. Neurology. 1999;53(2):297–302.CrossRefPubMedGoogle Scholar
  56. 56.
    Lehmann-Horn F, Rudel R, Dengler R, Lorkovic H, Haass A, Ricker K. Membrane defects in paramyotonia congenita with and without myotonia in a warm environment. Muscle Nerve. 1981;4(5):396–406.CrossRefPubMedGoogle Scholar
  57. 57.
    Lehmann-Horn F, Rudel R, Ricker K, Lorkovic H, Dengler R, Hopf HC. Two cases of adynamia episodica hereditaria: in vitro investigation of muscle cell membrane and contraction parameters. Muscle Nerve. 1983;6(2):113–21.CrossRefPubMedGoogle Scholar
  58. 58.
    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(4983):1000–2.CrossRefPubMedGoogle Scholar
  59. 59.
    Ebers GC, George AL, Barchi RL, Ting-Passador SS, Kallen RG, Lathrop GM, et al. Paramyotonia congenita and hyperkalemic periodic paralysis are linked to the adult muscle sodium channel gene. Ann Neurol. 1991;30(6):810–6.CrossRefPubMedGoogle Scholar
  60. 60.
    Cannon SC. Sodium Channelopathies of Skeletal Muscle. Handb Exp Pharmacol. 2018;246:309–30.CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Rose MR, Sadjadi R, Weinman J, Akhtar T, Pandya S, Kissel JT, et al. Role of disease severity, illness perceptions, and mood on quality of life in muscle disease. Muscle Nerve. 2012;46(3):351–9.CrossRefPubMedGoogle Scholar
  62. 62.
    Sansone VA, Ricci C, Montanari M, Apolone G, Rose M, Meola G. Measuring quality of life impairment in skeletal muscle channelopathies. Eur J Neurol. 2012;19(11):1470–6.CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    Cannon SC. Channelopathies of skeletal muscle excitability. Compr Physiol. 2015;5(2):761–90.CrossRefPubMedPubMedCentralGoogle Scholar
  64. 64.
    Statland J, Phillips L, Trivedi JR. Muscle channelopathies. Neurol Clin. 2014;32(3):801–15, x.CrossRefPubMedGoogle Scholar
  65. 65.
    Statland JM, Bundy BN, Wang Y, Rayan DR, Trivedi JR, Sansone VA, et al. Mexiletine for symptoms and signs of myotonia in nondystrophic myotonia: a randomized controlled trial. JAMA. 2012;308(13):1357–65.CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Arnold WD, Kline D, Sanderson A, Hawash AA, Bartlett A, Novak KR, et al. Open-label trial of ranolazine for the treatment of myotonia congenita. Neurology. 2017;89(7):710–3.CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Dunø M, Colding-Jørgensen E. Myotonia Congenita. In: Pagon RA AM, Bird TD, Dolan CR, Fong CT, Stephens K, editors, editor. GeneReviews [Internet]. University of Washington, Seattle2005 [updated 2011 Apr 12]. .Google Scholar
  68. 68.
    Aichele R, Paik H, Heller AH. Efficacy of phenytoin, procainamide, and tocainide in murine genetic myotonia. Exp Neurol. 1985;87(2):377–81.CrossRefPubMedGoogle Scholar
  69. 69.
    Desaphy JF, Modoni A, Lomonaco M, Camerino DC. Dramatic improvement of myotonia permanens with flecainide: a two-case report of a possible bench-to-bedside pharmacogenetics strategy. Eur J Clin Pharmacol. 2013;69(4):1037–9.CrossRefPubMedGoogle Scholar
  70. 70.
    Berardinelli A, Gorni K, Orcesi S. Response to carbamazepine of recessive-type myotonia congenita. Muscle Nerve. 2000;23(1):138–9.CrossRefPubMedGoogle Scholar
  71. 71.
    B Shapiro RR. Disorders of skeletal muscle membrane excitability: myotonia congenita, paramyotonia congenita, periodic paralysis, and related disorders. In: Katirji B KH, Preston D, Ruff R, Shapiro B, editor. Neuromuscular Disorders in Clinical Practice: Butterworth-Heinemann; 2002. p. 987–1020.Google Scholar
  72. 72.
    Skov M, de Paoli FV, Nielsen OB, Pedersen TH. The anti-convulsants lacosamide, lamotrigine, and rufinamide reduce myotonia in isolated human and rat skeletal muscle. Muscle Nerve. 2017;56(1):136–42.CrossRefPubMedGoogle Scholar
  73. 73.
    Andersen G, Hedermann G, Witting N, Duno M, Andersen H, Vissing J. The antimyotonic effect of lamotrigine in non-dystrophic myotonias: a double-blind randomized study. Brain. 2017;140(9):2295–305.CrossRefPubMedGoogle Scholar
  74. 74.
    Leyburn P, Walton JN. The treatment of myotonia: a controlled clinical trial. Brain. 1959;82(1):81–91.CrossRefPubMedGoogle Scholar
  75. 75.
    Griggs RC, Davis RJ, Anderson DC, Dove JT. Cardiac conduction in myotonic dystrophy. Am J Med. 1975;59(1):37–42.CrossRefPubMedGoogle Scholar
  76. 76.
    Streib EW. AAEE minimonograph #27: differential diagnosis of myotonic syndromes. Muscle Nerve. 1987;10(7):603–15.CrossRefPubMedGoogle Scholar
  77. 77.
    Kwiecinski H, Ryniewicz B, Ostrzycki A. Treatment of myotonia with antiarrhythmic drugs. Acta Neurol Scand. 1992;86(4):371–5.CrossRefPubMedGoogle Scholar
  78. 78.
    Fontaine B. Periodic paralysis. Adv Genet. 2008;63:3–23.CrossRefPubMedGoogle Scholar
  79. 79.
    Miller TM, Dias da Silva MR, Miller HA, Kwiecinski H, Mendell JR, Tawil R, et al. Correlating phenotype and genotype in the periodic paralyses. Neurology. 2004;63(9):1647–55.CrossRefPubMedGoogle Scholar
  80. 80.
    Venance SL, Cannon SC, Fialho D, Fontaine B, Hanna MG, Ptacek LJ, et al. The primary periodic paralyses: diagnosis, pathogenesis and treatment. Brain. 2006;129(Pt 1):8–17.CrossRefPubMedGoogle Scholar
  81. 81.
    Dalakas MC, Engel WK. Treatment of “permanent” muscle weakness in familial Hypokalemic Periodic Paralysis. Muscle Nerve. 1983;6(3):182–6.CrossRefPubMedGoogle Scholar
  82. 82.
    Griggs RC, Engel WK, Resnick JS. Acetazolamide treatment of hypokalemic periodic paralysis. Prevention of attacks and improvement of persistent weakness. Ann Intern Med. 1970;73(1):39–48.CrossRefPubMedGoogle Scholar
  83. 83.
    Links TP, Zwarts MJ, Wilmink JT, Molenaar WM, Oosterhuis HJ. Permanent muscle weakness in familial hypokalaemic periodic paralysis. Clinical, radiological and pathological aspects. Brain. 1990;113 ( Pt 6):1873–89.CrossRefPubMedGoogle Scholar
  84. 84.
    Fialho D, Griggs RC, Matthews E. Periodic paralysis. Handb Clin Neurol. 2018;148:505–20.CrossRefPubMedGoogle Scholar
  85. 85.
    Jeong HN, Yi JS, Lee YH, Lee JH, Shin HY, Choi YC, et al. Lower-extremity magnetic resonance imaging in patients with hyperkalemic periodic paralysis carrying the SCN4A mutation T704M: 30-month follow-up of seven patients. Neuromuscul Disord. 2018.Google Scholar
  86. 86.
    Plassart E, Elbaz A, Santos JV, Reboul J, Lapie P, Chauveau D, et al. Genetic heterogeneity in hypokalemic periodic paralysis (hypoPP). Hum Genet. 1994;94(5):551–6.CrossRefPubMedGoogle Scholar
  87. 87.
    Horga A, Raja Rayan DL, Matthews E, Sud R, Fialho D, Durran SC, et al. Prevalence study of genetically defined skeletal muscle channelopathies in England. Neurology. 2013;80(16):1472–5.CrossRefPubMedPubMedCentralGoogle Scholar
  88. 88.
    Plaster NM, Tawil R, Tristani-Firouzi M, Canun S, Bendahhou S, Tsunoda A, et al. Mutations in Kir2.1 cause the developmental and episodic electrical phenotypes of Andersen’s syndrome. Cell. 2001;105(4):511–9.CrossRefPubMedGoogle Scholar
  89. 89.
    Tristani-Firouzi M, Jensen JL, Donaldson MR, Sansone V, Meola G, Hahn A, et al. Functional and clinical characterization of KCNJ2 mutations associated with LQT7 (Andersen syndrome). J Clin Invest. 2002;110(3):381–8.CrossRefPubMedPubMedCentralGoogle Scholar
  90. 90.
    Ryan DP, da Silva MR, Soong TW, Fontaine B, Donaldson MR, Kung AW, et al. Mutations in potassium channel Kir2.6 cause susceptibility to thyrotoxic hypokalemic periodic paralysis. Cell. 2010;140(1):88–98.CrossRefPubMedPubMedCentralGoogle Scholar
  91. 91.
    Chinnery PF, Walls TJ, Hanna MG, Bates D, Fawcett PR. Normokalemic periodic paralysis revisited: does it exist? Ann Neurol. 2002;52(2):251–2.CrossRefPubMedGoogle Scholar
  92. 92.
    Tawil R, Ptacek LJ, Pavlakis SG, DeVivo DC, Penn AS, Ozdemir C, et al. Andersen’s syndrome: potassium-sensitive periodic paralysis, ventricular ectopy, and dysmorphic features. Ann Neurol. 1994;35(3):326–30.CrossRefPubMedGoogle Scholar
  93. 93.
    Sansone V, Griggs RC, Meola G, Ptacek LJ, Barohn R, Iannaccone S, et al. Andersen’s syndrome: a distinct periodic paralysis. Ann Neurol. 1997;42(3):305–12.CrossRefPubMedGoogle Scholar
  94. 94.
    Lehmann-Horn F, Jurkat-Rott K, Rudel R. Periodic paralysis: understanding channelopathies. Curr Neurol Neurosci Rep. 2002;2(1):61–9.CrossRefPubMedGoogle Scholar
  95. 95.
    Cannon SC. Voltage-sensor mutations in channelopathies of skeletal muscle. J Physiol. 2010;588(Pt 11):1887–95.CrossRefPubMedPubMedCentralGoogle Scholar
  96. 96.
    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 hypokalemic periodic paralysis. J Clin Invest. 2011;121(10):4082–94.CrossRefPubMedPubMedCentralGoogle Scholar
  97. 97.
    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(12):4580–91.CrossRefPubMedPubMedCentralGoogle Scholar
  98. 98.
    Matthews E, Hanna MG. Muscle channelopathies: does the predicted channel gating pore offer new treatment insights for hypokalaemic periodic paralysis? J Physiol. 2010;588(Pt 11):1879–86.CrossRefPubMedPubMedCentralGoogle Scholar
  99. 99.
    Tricarico D, Mele A, Conte Camerino D. Carbonic anhydrase inhibitors ameliorate the symptoms of hypokalaemic periodic paralysis in rats by opening the muscular Ca2+-activated-K+ channels. Neuromuscul Disord. 2006;16(1):39–45.CrossRefPubMedGoogle Scholar
  100. 100.
    Sansone VA. The Dystrophic and Nondystrophic Myotonias. Continuum (Minneap Minn). 2016;22(6, Muscle and Neuromuscular Junction Disorders):1889–915.PubMedGoogle Scholar
  101. 101.
    Lichter PR, Newman LP, Wheeler NC, Beall OV. Patient tolerance to carbonic anhydrase inhibitors. Am J Ophthalmol. 1978;85(4):495–502.CrossRefPubMedGoogle Scholar
  102. 102.
    Tawil R, Moxley RT, III, Griggs RC. Acetazolamide-induced nephrolithiasis: implications for treatment of neuromuscular disorders. Neurology. 1993;43(6):1105–6.CrossRefPubMedGoogle Scholar
  103. 103.
    Griggs RC, Resnick J, Engel WK. Intravenous treatment of hypokalemic periodic paralysis. Arch Neurol. 1983;40(9):539–40.CrossRefPubMedGoogle Scholar
  104. 104.
    Stunnenberg BC, Deinum J, Links TP, Wilde AA, Franssen H, Drost G. Cardiac arrhythmias in hypokalemic periodic paralysis: Hypokalemia as only cause? Muscle Nerve. 2014;50(3):327–32.CrossRefPubMedGoogle Scholar
  105. 105.
    Matthews E, Portaro S, Ke Q, Sud R, Haworth A, Davis MB, et al. Acetazolamide efficacy in hypokalemic periodic paralysis and the predictive role of genotype. Neurology. 2011;77(22):1960–4.CrossRefPubMedPubMedCentralGoogle Scholar
  106. 106.
    Torres CF, Griggs RC, Moxley RT, Bender AN. Hypokalemic periodic paralysis exacerbated by acetazolamide. Neurology. 1981;31(11):1423–8.CrossRefPubMedGoogle Scholar
  107. 107.
    Sternberg D, Maisonobe T, Jurkat-Rott K, Nicole S, Launay E, Chauveau D, et al. Hypokalaemic periodic paralysis type 2 caused by mutations at codon 672 in the muscle sodium channel gene SCN4A. Brain. 2001;124(Pt 6):1091–9.CrossRefPubMedGoogle Scholar
  108. 108.
    Bendahhou S, Cummins TR, Griggs RC, Fu YH, Ptacek LJ. Sodium channel inactivation defects are associated with acetazolamide-exacerbated hypokalemic periodic paralysis. Ann Neurol. 2001;50(3):417–20.CrossRefPubMedGoogle Scholar
  109. 109.
    Matthews E, Labrum R, Sweeney MG, Sud R, Haworth A, Chinnery PF, et al. Voltage sensor charge loss accounts for most cases of hypokalemic periodic paralysis. Neurology. 2009;72(18):1544–7.CrossRefPubMedPubMedCentralGoogle Scholar
  110. 110.
    Sansone V, Meola G, Links TP, Panzeri M, Rose MR. Treatment for periodic paralysis. Cochrane Database Syst Rev. 2008(1):CD005045.Google Scholar
  111. 111.
    Sharp L, Trivedi JR. Treatment and management of neuromuscular channelopathies. Curr Treat Options Neurol. 2014;16(10):313.CrossRefPubMedGoogle Scholar
  112. 112.
    Hanna MG, Stewart J, Schapira AH, Wood NW, Morgan-Hughes JA, Murray NM. Salbutamol treatment in a patient with hyperkalaemic periodic paralysis due to a mutation in the skeletal muscle sodium channel gene (SCN4A). J Neurol Neurosurg Psychiatry. 1998;65(2):248–50.CrossRefPubMedPubMedCentralGoogle Scholar
  113. 113.
    Imbrici P, Liantonio A, Camerino GM, De Bellis M, Camerino C, Mele A, et al. Therapeutic Approaches to Genetic Ion Channelopathies and Perspectives in Drug Discovery. Front Pharmacol. 2016;7:121.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© The American Society for Experimental NeuroTherapeutics, Inc. 2018

Authors and Affiliations

  1. 1.Department of Neurology and NeurotherapeuticsUT Southwestern Medical CenterDallasUSA

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