Acetylcholine receptor gating in a zebrafish model for slow-channel syndrome

Journal of Neuroscience

Volumn 32, Issue 23, 2012, Pages 7941-7948

  Walogorsky, Michael ^a   Mongeon, Rebecca ^a,b   Wen, Hua ^a   Mandel, Gail ^a,b   Brehm, Paul ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCHOLINE; CHOLINE; CHOLINERGIC RECEPTOR; LYSINE; PROLINE; QUINIDINE; TUBOCURARINE CHLORIDE;

ANIMAL EXPERIMENT; ARTICLE; BEHAVIOR; CALCIUM CURRENT; CHANNEL GATING; CONGENITAL MYASTHENIC SYNDROME; CONTROLLED STUDY; EVOKED MUSCLE RESPONSE; EXCITATORY POSTSYNAPTIC POTENTIAL; FEMALE; GENE MUTATION; MALE; MEMBRANE POTENTIAL; NONHUMAN; OOCYTE; PATCH CLAMP; PRIORITY JOURNAL; SPIKE; SWIMMING; SYNAPSE; XENOPUS; ZEBRA FISH;

ACTION POTENTIALS; ANIMALS; CALCIUM; CHANNELOPATHIES; CHOLINERGIC AGONISTS; CHOLINERGIC ANTAGONISTS; DOSE-RESPONSE RELATIONSHIP, DRUG; ION CHANNEL GATING; ISOMERISM; MOVEMENT; MUSCLE, SKELETAL; MYASTHENIC SYNDROMES, CONGENITAL; OOCYTES; PATCH-CLAMP TECHNIQUES; QUINIDINE; RECEPTORS, CHOLINERGIC; SYNAPTIC TRANSMISSION; XENOPUS; ZEBRAFISH;

EID: 84861893419     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0158-12.2012     Document Type: Article

References (32)

1. Auerbach A (2010) The gating isomerization of neuromuscular acetylcholine receptors. J Physiol 588:573-586.
2. Burgess HA, Granato M (2007) Modulation of locomotor activity in larval zebrafish during light adaptation. J Exp Biol 210:2526-2539.
3. Colquhoun D, Hawkes AG (1982) On the stochastic properties of bursts of single ion channel openings and of clusters of bursts. Philos Trans R Soc Lond B Biol Sci 300:1-59.
4. Drapeau P, Buss RR, Ali DW, Legendre P, Rotundo RL (2001) Limits to the development of fast neuromuscular transmission in zebrafish. J Neurophysiol 86:2951-2956.
5. Engel AG, Lambert EH, Mulder DM, Torres CF, Sahashi K, Bertorini TE, Whitaker JN (1982) A newly recognized congenital myasthenic syndrome attributed to a prolonged open time of the acetylcholine-induced ion channel. Ann Neurol 11:553-569.
6. Engel AG, Hutchinson DO, Nakano S, Murphy L, Griggs RC, Gu Y, Hall ZW, Lindstrom J (1993) Myasthenic syndromes attributed to mutations affecting the epsilon subunit of the acetylcholine receptor. Ann N Y Acad Sci 681:496-508.
7. Engel AG, Ohno K, Milone M, Wang HL, Nakano S, Bouzat C, Pruitt JN 2nd, Hutchinson DO, Brengman JM, Bren N, Sieb JP, Sine SM (1996a) New mutations in acetylcholine receptor subunit genes reveal heterogeneity in the slow-channel congenital myasthenic syndrome. Hum Mol Genet 5:1217-1227.
8. Engel AG, Ohno K, Bouzat C, Sine SM, Griggs RC (1996b) End-plate acetylcholine receptor deficiency due to nonsense mutations in the epsilon subunit. Ann Neurol 40:810-817.
9. Fukudome T, Ohno K, Brengman JM, Engel AG (1998) AChR channel blockade by quinidine sulfate reduces channel open duration in the slow-channel congenital myasthenic syndrome. Ann N Y Acad Sci 841:199-202.
10. Gomez CM, Maselli R, Gammack J, Lasalde J, Tamamizu S, Cornblath DR, Lehar M, McNamee M, Kuncl RW (1996) A beta-subunit mutation in the acetylcholine receptor channel gate causes severe slow-channel syndrome. Ann Neurol 39:712-723.
11. Gomez CM, Maselli R, Gundeck JE, Chao M, Day JW, Tamamizu S, Lasalde JA, McNamee M, Wollmann RL (1997) Slow-channel transgenic mice: a model of postsynaptic organellar degeneration at the neuromuscular junction. J Neurosci 17:4170-4179.
12. Gomez CM, Maselli RA, Groshong J, Zayas R, Wollmann RL, Cens T, Charnet P (2002) Active calcium accumulation underlies severe weakness in a panel of mice with slow-channel syndrome. J Neurosci 22:6447-6457.
13. Grosman C, Auerbach A (2000) Kinetic, mechanistic, and structural aspects of unliganded gating of acetylcholine receptor channels: a single-channel study of second transmembrane segment 12' mutants. J Gen Physiol 115:621-635.
14. Harper CM, Engel AG (1998) Quinidine sulfate therapy for the slowchannel congenital myasthenic syndrome. Ann Neurol 43:480-484.
15. Hoffmann K, Muller JS, Stricker S, Megarbane A, Rajab A, Lindner TH, Cohen M, Chouery E, Adaimy L, Ghanem I, Delague V, Boltshauser E, Talim B, Horvath R, Robinson PN, Lochmüller H, Hübner C, Mundlos S (2006) Escobar syndrome is a prenatal myasthenia caused by disruption of the acetylcholine receptor fetal gamma subunit. Am J Hum Genet 79:303-312.
16. Jackson MB (1984) Spontaneous openings of the acetylcholine receptor channel. Proc Natl Acad Sci U S A 81:3901-3904.
17. Jackson MB (1986) Kinetics of unliganded acetylcholine receptor channel gating. Biophys J 49:663-672.
18. Jadey SV, Purohit P, Bruhova I, Gregg TM, Auerbach A (2011) Design and control of acetylcholine receptor conformational change. Proc Natl Acad Sci U S A 108:4328-4333.
19. Kullberg RW, Mikelberg FS, CohenMW (1980) Contribution of cholinesterase to developmental decreases in the time course of synaptic potentials at an amphibian neuromuscular junction. Dev Biol 75:255-267.
20. Lefebvre JL, Ono F, Puglielli C, Seidner G, Franzini-Armstrong C, Brehm P, Granato M (2004) Increased neuromuscular activity causes axonal defects and muscular degeneration. Development 131:2605-2618.
21. Leonard JP, Salpeter MM (1979) Agonist-induced myopathy at the neuromuscular junction is mediated by calcium. J Cell Biol 82:811-819.
22. Leonard JP, Salpeter MM (1982) Calcium-mediated myopathy at neuromuscular junctions of normal and dystrophic muscle. Exp Neurol 76:121-138.
23. Milone M, Wang HL, Ohno K, Fukudome T, Pruitt JN, Bren N, Sine SM, Engel AG (1997) Slow-channel myasthenic syndrome caused by enhanced activation, desensitization, and agonist binding affinity attributable to mutation in the M2 domain of the acetylcholine receptor α subunit. J Neurosci 17:5651-5665.
24. Mongeon R, Walogorsky M, Urban J, Mandel G, Ono F, Brehm P (2011) An acetylcholine receptor lacking both gamma and epsilon subunits mediates transmission in zebrafish slow muscle synapses. J Gen Physiol 138: 353-366.
25. Nguyen PV, Aniksztejn L, Catarsi S, Drapeau P (1999) Maturation of neuromuscular transmission during early development in zebrafish. J Neurophysiol 81:2852-2861.
26. Ohno K, Hutchinson DO, Milone M, Brengman JM, Bouzat C, Sine SM, Engel AG (1995) 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 92:758-762.
27. Paradiso K, Brehm P (1998) Long-term desensitization of nicotinic acetylcholine receptors is regulated via protein kinase A-mediated phosphorylation. J Neurosci 18:9227-9237.
28. Purohit P, Auerbach A (2009) Unliganded gating of acetylcholine receptor channels. Proc Natl Acad Sci U S A 106:115-120.
29. Sine SM, Steinbach JH (1986) Activation of acetylcholine receptors on clonal mammalian BC3H-1 cells by low concentration of agonist. J Physiol 373;129-162.
30. Sine SM, Ohno K, Bouzat C, Auerbach A, Milone M, Pruitt JN, Engel AG (1995) Mutation of the acetylcholine receptor alpha subunit causes a slow-channel myasthenic syndrome by enhancing agonist binding affinity. Neuron 15:229-239.
31. Wen H, Brehm P (2005) Paired motor neuron-muscle recordings in zebrafish test the receptor blockade model for shaping synaptic current. J Neurosci 25:8104-8111.
32. Zhou M, Engel AG, Auerbach A (1999) Serum choline activates mutant acetylcholine receptors that cause slow channel congenital myasthenic syndromes. Proc Natl Acad Sci U S A 96:10466-10471.