A mouse model of the slow channel myasthenic syndrome: Neuromuscular physiology and effects of ephedrine treatment

Experimental Neurology

Volumn 248, Issue , 2013, Pages 286-298

  Webster, R G ^a   Cossins, J ^a   Lashley, D ^a   Maxwell, S ^a   Liu, W W ^a   Wickens, J R ^b   Martinez Martinez, P ^c   de Baets, M ^c   Beeson, D ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c MAASTRICHT UNIVERSITY   (Netherlands)

Author keywords

Acetylcholine receptor; Congenital myasthenia; Electromyography; Ephedrine; Fluorescent endplates; Mouse model; Neuromuscular junction; Slow channel syndrome

Indexed keywords

CHOLINERGIC RECEPTOR; ENHANCED GREEN FLUORESCENT PROTEIN; EPHEDRINE; SALBUTAMOL;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONGENITAL MYASTHENIC SYNDROME; CONTROLLED STUDY; ELECTROMYOGRAPHY; MOUSE; MUSCLE ACTION POTENTIAL; MUSCLE WEAKNESS; NERVOUSNESS; NEUROMUSCULAR TRANSMISSION; NONHUMAN; PHRENIC NERVE; POSTSYNAPTIC MEMBRANE; PRIORITY JOURNAL; PROMOTER REGION; TRANSGENIC MOUSE;

ACETYLCHOLINE RECEPTOR; CONGENITAL MYASTHENIA; ELECTROMYOGRAPHY; EPHEDRINE; FLUORESCENT ENDPLATES; MOUSE MODEL; NEUROMUSCULAR JUNCTION; SLOW CHANNEL SYNDROME;

ADRENERGIC AGENTS; ANIMALS; DISEASE MODELS, ANIMAL; EPHEDRINE; MEMBRANE POTENTIALS; MICE; MICE, TRANSGENIC; MINIATURE POSTSYNAPTIC POTENTIALS; MUTATION; MYASTHENIC SYNDROMES, CONGENITAL; NEUROMUSCULAR JUNCTION; RECEPTORS, CHOLINERGIC; SYNAPTIC TRANSMISSION; TREATMENT OUTCOME;

EID: 84880398716     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2013.06.012     Document Type: Article

References (41)

1. Beeson D., Brydson M., Betty M., Jeremiah S., Povey S., Vincent A., Newsom-Davis J. Primary structure of the human muscle acetylcholine receptor. cDNA cloning of the gamma and epsilon subunits. Eur. J. Biochem. 1993, 215:229-238.
2. Beeson D., Vincent A., Morris A., Brydson M., Jacobson L., Baggi F., Jeremiah S., Povey S., Newsom-Davis J. cDNA and genomic clones encoding the human muscle acetylcholine receptor. Ann. N. Y. Acad. Sci. 1993, 681:165-167.
3. Beeson D., Higuchi O., Palace J., Cossins J., Spearman H., Maxwell S., Newsom-Davis J., Burke G., Fawcett P., Motomura M., Muller J.S., Lochmuller H., Slater C., Vincent A., Yamanashi Y. Dok-7 mutations underlie a neuromuscular junction synaptopathy. Science (New York, N.Y.) 2006, 313:1975-1978.
4. Bestue-Cardiel M., Saenz de Cabezon-Alvarez A., Capablo-Liesa J.L., Lopez-Pison J., Pena-Segura J.L., Martin-Martinez J., Engel A.G. Congenital endplate acetylcholinesterase deficiency responsive to ephedrine. Neurology 2005, 65:144-146.
5. Brinster R.L., Allen J.M., Behringer R.R., Gelinas R.E., Palmiter R.D. Introns increase transcriptional efficiency in transgenic mice. Proc. Natl. Acad. Sci. U. S. A. 1988, 85:836-840.
6. Chan S.H., Wong V.C., Engel A.G. Neuromuscular junction acetylcholinesterase deficiency responsive to albuterol. Pediatr. Neurol. 2012, 47:137-140.
7. Chaouch A., Beeson D., Hantai D., Lochmuller H. 186th ENMC international workshop: congenital myasthenic syndromes 24-26 June 2011, Naarden, The Netherlands. Neuromuscul. Disord. 2012, 22:566-576.
8. Chevessier F., Peter C., Mersdorf U., Girard E., Krejci E., McArdle J.J., Witzemann V. A new mouse model for the slow-channel congenital myasthenic syndrome induced by the AChR epsilonL221F mutation. Neurobiol. Dis. 2012, 45:851-861.
9. Cossins J., Webster R., Maxwell S., Burke G., Vincent A., Beeson D. A mouse model of AChR deficiency syndrome with a phenotype reflecting the human condition. Hum. Mol. Genet. 2004, 13:2947-2957.
10. Cossins J., Webster R., Maxwell S., Vincent A., Beeson D. Fluorescent receptors to light up the neuromuscular junction. Neuromuscul. Disord. 2011, 21:S12-S13.
11. Croxen R., Hatton C., Shelley C., Brydson M., Chauplannaz G., Oosterhuis H., Vincent A., Newsom-Davis J., Colquhoun D., Beeson D. Recessive inheritance and variable penetrance of slow-channel congenital myasthenic syndromes. Neurology 2002, 59:162-168.
12. Ealing J., Webster R., Brownlow S., Abdelgany A., Oosterhuis H., Muntoni F., Vaux D.J., Vincent A., Beeson D. Mutations in congenital myasthenic syndromes reveal an epsilon subunit C-terminal cysteine, C470, crucial for maturation and surface expression of adult AChR. Hum. Mol. Genet. 2002, 11:3087-3096.
13. Edgeworth H. A report of progress on the use of ephedrine in a case of myasthenia gravis. JAMA 1930, 94:1136-1136.
14. Edgeworth H. The effect of ephedrine in the treatment of myasthenia gravis: second report. JAMA 1933, 100:1401-1401.
15. Engel A.G. The therapy of congenital myasthenic syndromes. Neurotherapeutics 2007, 4:252-257.
16. Engel A.G. Congenital myasthenic syndromes in 2012. Curr. Neurol. Neurosci. Rep. 2012, 12:92-101.
17. Engel A.G., Lambert E.H., Mulder D.M., Torres C.F., Sahashi K., Bertorini T.E., Whitaker J.N. A newly recognized congenital myasthenic syndrome attributed to a prolonged open time of the acetylcholine-induced ion channel. Ann. Neurol. 1982, 11:553-569.
18. Engel A.G., Shen X.M., Selcen D., Sine S.M. What have we learned from the congenital myasthenic syndromes. J. Mol. Neurosci. 2010, 40:143-153.
19. Finlayson S., Spillane J., Kullmann D.M., Howard R., Webster R., Palace J., Beeson D. Slow channel congenital myasthenic syndrome responsive to a combination of fluoxetine and salbutamol. Muscle Nerve 2012, 47:279-282.
20. Hatton C.J., Shelley C., Brydson M., Beeson D., Colquhoun D. Properties of the human muscle nicotinic receptor, and of the slow-channel myasthenic syndrome mutant epsilonL221F, inferred from maximum likelihood fits. J. Physiol. 2003, 547:729-760.
21. Katz B., Thesleff S. On the factors which determine the amplitude of the miniature end-plate potential. J. Physiol. 1957, 137:267-278.
22. Kinali M., Beeson D., Pitt M.C., Jungbluth H., Simonds A.K., Aloysius A., Cockerill H., Davis T., Palace J., Manzur A.Y., Jimenez-Mallebrera C., Sewry C., Muntoni F., Robb S.A. Congenital myasthenic syndromes in childhood: diagnostic and management challenges. J. Neuroimmunol. 2008, 201-202:6-12.
23. Kummer T.T., Misgeld T., Sanes J.R. Assembly of the postsynaptic membrane at the neuromuscular junction: paradigm lost. Curr. Opin. Neurobiol. 2006, 16:74-82.
24. Lashley D., Palace J., Jayawant S., Robb S., Beeson D. Ephedrine treatment in congenital myasthenic syndrome due to mutations in DOK7. Neurology 2010, 74:1517-1523.
25. Lynch G.S., Ryall J.G. Role of beta-adrenoceptor signaling in skeletal muscle: implications for muscle wasting and disease. Physiol. Rev. 2008, 88:729-767.
26. McLachlan E.M., Martin A.R. Non-linear summation of end-plate potentials in the frog and mouse. J. Physiol. 1981, 311:307-324.
27. Mihaylova V., Muller J.S., Vilchez J.J., Salih M.A., Kabiraj M.M., D'Amico A., Bertini E., Wolfle J., Schreiner F., Kurlemann G., Rasic V.M., Siskova D., Colomer J., Herczegfalvi A., Fabriciova K., Weschke B., Scola R., Hoellen F., Schara U., Abicht A., Lochmuller H. Clinical and molecular genetic findings in COLQ-mutant congenital myasthenic syndromes. Brain 2008, 131:747-759.
28. Milone M., Engel A.G. Block of the endplate acetylcholine receptor channel by the sympathomimetic agents ephedrine, pseudoephedrine, and albuterol. Brain Res. 1996, 740:346-352.
29. Misgeld T., Kummer T.T., Lichtman J.W., Sanes J.R. Agrin promotes synaptic differentiation by counteracting an inhibitory effect of neurotransmitter. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:11088-11093.
30. Missias A.C., Mudd J., Cunningham J.M., Steinbach J.H., Merlie J.P., Sanes J.R. Deficient development and maintenance of postsynaptic specializations in mutant mice lacking an 'adult' acetylcholine receptor subunit. Development 1997, 124:5075-5086.
31. Ohno K., Hutchinson D.O., Milone M., Brengman J.M., Bouzat C., Sine S.M., Engel A.G. Congenital myasthenic syndrome caused by prolonged acetylcholine receptor channel openings due to a mutation in the M2 domain of the epsilon subunit. Proc. Natl. Acad. Sci. U. S. A. 1995, 92:758-762.
32. Oosterhuis H.J., Newsom-Davis J., Wokke J.H., Molenaar P.C., Weerden T.V., Oen B.S., Jennekens F.G., Veldman H., Vincent A., Wray D.W., et al. The slow channel syndrome. Two new cases. Brain 1987, 110(Pt 4):1061-1079.
33. Palace J., Beeson D. The congenital myasthenic syndromes. J. Neuroimmunol. 2008, 201-202:2-5.
34. Pickup M.E., May C.S., Ssendagire R., Paterson J.W. The pharmacokinetics of ephedrine after oral dosage in asthmatics receiving acute and chronic treatment. Br. J. Clin. Pharmacol. 1976, 3:123-134.
35. Sadeh M., Shen X.M., Engel A.G. Beneficial effect of albuterol in congenital myasthenic syndrome with epsilon-subunit mutations. Muscle Nerve 2011, 44:289-291.
36. Schara U., Barisic N., Deschauer M., Lindberg C., Straub V., Strigl-Pill N., Wendt M., Abicht A., Muller J.S., Lochmuller H. Ephedrine therapy in eight patients with congenital myasthenic syndrome due to DOK7 mutations. Neuromuscul. Disord. 2009, 19:828-832.
37. Selcen D., Milone M., Shen X.M., Harper C.M., Stans A.A., Wieben E.D., Engel A.G. Dok-7 myasthenia: phenotypic and molecular genetic studies in 16 patients. Ann. Neurol. 2008, 64:71-87.
38. Sieb J.P., Engel A.G. Ephedrine: effects on neuromuscular transmission. Brain Res. 1993, 623:167-171.
39. Sine S.M., Ohno K., Bouzat C., Auerbach A., Milone M., Pruitt J.N., Engel A.G. Mutation of the acetylcholine receptor alpha subunit causes a slow-channel myasthenic syndrome by enhancing agonist binding affinity. Neuron 1995, 15:229-239.
40. Verschuuren J.J., Spaans F., De Baets M.H. Single-fiber electromyography in experimental autoimmune myasthenia gravis. Muscle Nerve 1990, 13:485-492.
41. Wood S.J., Slater C.R. Safety factor at the neuromuscular junction. Prog. Neurobiol. 2001, 64:393-429.