Mode switching kinetics produced by a naturally occurring mutation in the cytoplasmic loop of the human acetylcholine receptor ε subunit

Neuron

Volumn 20, Issue 3, 1998, Pages 575-588

  Milone, Margherita ^a   Wang, Hai Long ^a   Ohno, Kinji ^a   Prince, Richard ^a   Fukudome, Takayasu ^a   Shen, Xin Ming ^a   Brengman, Joan M ^a   Griggs, Robert C ^b   Sine, Steven M ^a   Engel, Andrew G ^a  

^a MAYO CLINIC   (United States)

^b UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCHOLINE; CHOLINERGIC RECEPTOR;

ADULT; ARTICLE; CASE REPORT; CONTROLLED STUDY; FEMALE; GENE DUPLICATION; GENE MUTATION; HUMAN; HUMAN TISSUE; MYASTHENIA; NERVE ENDING; PRIORITY JOURNAL; SYNAPTIC POTENTIAL;

EID: 0032031997     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0896-6273(00)80996-4     Document Type: Article

References (40)

1. Betz, H. (1990). Ligand-gated ion channels in the brain: the amino acid receptor superfamily. Neuron 5, 383-392.
2. Blount, P., and Merlie, J.P. (1990). Mutational analysis of muscle nicotinic acetylcholine receptor subunit assembly. J. Cell Biol. 111, 2613-2622.
3. Bouzat, C., Bren, N., and Sine, S.M. (1994). Structural basis of different gating kinetics of fetal and adult acetylcholine receptors. Neuron 13, 1395-1402.
4. Clay, J.R., and DeFelice, L.J. (1983). Relationship between membrane excitability and single channel open-close kinetics. Biophys. J. 42, 151-157.
5. Colquhoun, D., and Sakmann, B. (1985). Fast events in single channel currents activated by acetylcholine and its analogues at the frog muscle end-plate. J. Physiol. (Lond.) 369, 501-557.
6. Engel, A.G. (1994). Quantitative morphological studies of muscle. In Myology: Basic and Clinical, Second Edition, A.G. Engel and C. Franzini-Armstrong, eds. (New York: McGraw-Hill), pp. 1018-1045.
7. Engel, A.G., Lindstrom, J.M., Lambert, E.H., and Lennon, V.A. (1977). Ultrastructural localization of the acetylcholine receptor in myasthenia gravis and in its experimental autoimmune model. Neurology 27, 307-315.
8. Engel, A.G., Nagel, A., Walls, T.J., Harper, C.M., and Waisburg, H.A. (1993). Congenital myasthenic syndromes. I. Deficiency and short open-time of the acetylcholine receptor. Muscle Nerve 16, 1284-1292.
9. Engel, A.G., Ohno, K., Bouzat, C., Sine, S.M., and Griggs, R.G. (1996a). End-plate acetylcholine receptor deficiency due to nonsense mutations in the ∈ subunit. Ann. Neurol. 40, 810-817.
10. Engel, A.G., Ohno, K., Milone, M., Wang, H.-L., Nakano, S., Bouzat, C., Pruitt, J.N., Hutchinson, D.O., Brengman, J.M., Bren, N., et al. (1996b). New mutations in acetylcholine receptor subunit genes reveal heterogeneity in the slow-channel congenital myasthenic syndrome. Hum. Mol. Genet. 5, 1217-1227.
11. Fu, D.-X., and Sine, S.M. (1996). Asymmetric contribution of the conserved disulfide loop to subunit oligomerization and assembly of the nicotinic acetylcholine receptor. J. Biol. Chem. 271, 31479-31484.
12. Gibb, A.J., Kojima, H., Carr, J.A., and Colquhoun, D. (1990). Expression of cloned receptor subunits produces multiple receptors. Proc. R. Soc. Lond. [Biol.] 242, 108-112.
13. Green, W.N., and Claudio, T. (1993). Acetylcholine receptor assembly: subunit folding and oligomerization occur sequentially. Cell 74, 57-69.
14. Green, W.N., and Wanamaker, C.P. (1997). The role of the cystine loop in acetylcholine receptor assembly. J. Biol. Chem. 272, 20945-20953.
15. Hamill, O.P., Marty, A., Neher, E., Sakmann, B., and Sigworth, F.J. (1981). Improved patch clamp techniques for high resolution current recording from cells and cell-free membrane patches. Pflügers. Arch. 391, 85-100.
16. Karlin, A., and Akabas, M.H. (1994). Toward a structural basis for the function of nicotinic acetylcholine receptors and their cousins. Neuron 15, 1231-1244.
17. Lee, B.S., Gunn, R.B., and Kopito, R.R. (1991 ). Functional differences among nonerythroid anion exchangers expressed in a transfected human cell line. J. Biol. Chem. 266, 11448-11454.
18. Lingle, C.J., Maconochie, D., and Steinbach, J.H. (1992). Activation of skeletal muscle nicotinic acetylcholine receptors. J. Membr. Biol. 126, 195-217.
19. Luther, M.A., Schoepfer, R., Whiting, P., Casey, B., Blatt, Y., Montal, M.S., Montal, M., and Lindstrom, J. (1989). A muscle acetylcholine receptor is expressed in the human cerebellar medulloblastoma cell line TE671. J. Neurosci. 9, 1082-1096.
20. Magleby, K.L., and Stevens, C.F. (1972). A quantitative description of end-plate currents. J. Physiol. (Lond.) 223, 173-197.
21. Milone, M., Hutchinson, D.O., and Engel, A.G. (1994). Patch-clamp analysis of the properties of acetylcholine receptor channels at the normal human endplate. Muscle Nerve 17, 1364-1369.
22. Milone, M., Wang, H.-L., Ohno, K., Fukudome, K., Pruitt, J.N., Bren, N., Sine, S.M., and Engel, A.G. (1997). Slow-channel syndrome caused by enhanced activation, desensitization, and agonist binding affinity due to mutation in the M2 domain of the acetylcholine receptor alpha subunit. J. Neurosci. 17, 5651-5665.
23. Mishina, M., Tobimatsu, T., Imoto, K., Tanaka, K., Fujita, Y., Fukuda, K., Kurasaki, M., Takahashi, H., Morimoto, Y., and Hirose, T. (1985). Location of functional regions of acetylcholine receptor alpha-subunit by site directed mutagenesis. Nature 313, 364-369.
24. Naranjo, D., and Brehm, P. (1993). Modal shifts in acetylcholine receptor channel gating confer subunit-dependent desensitization. Science 260, 1811-1814.
25. Ohno, K., Hutchinson, D.O., Milone, M., Brengman, J.M., Bouzat, C., Sine, S.M., and Engel, A.G. (1995). Congenital myasthenic syndrome caused by prolonged acetylcholine receptor channel openings due to a mutation in the M2 domain of the ∈ subunit. Proc. Natl. Acad. Sci. USA 92, 758-762.
26. Ohno, K., Wang, H.-L., Milone, M., Bren, N., Brengman, J.M., Nakano, S., Quiram, P., Pruitt, J.N., Sine, S.M., and Engel, A.G. (1996). Congenital myasthenic syndrome caused by decreased agonist binding affinity due to a mutation in the acetylcholine receptor ∈ subunit. Neuron 17, 157-170.
27. Ohno, K., Quiram, P., Milone, M., Wang, H.-L., Harper, C.M., Pruitt, J.N., Brengman, J.M., Pao, L., Fischbeck, K.H., Crawford, T.O., et al. (1997). Congenital myasthenic syndromes due to heteroallelic nonsense/missense mutations in the acetylcholine receptor ∈ subunit gene: identification and functional characterization of six new mutations. Hum. Mol. Genet. 6, 753-766.
28. Pearson, R.B., and Kemp, B.E. (1991). Protein kinase phosphorylation site sequences and consensus motifs: tabulations. Methods Enzymol. 200, 62-81.
29. Pennefather, P., and Quastel, D.M.J. (1981). Relation between subsynaptic receptor blockade and response to quantal transmitter at the mouse neuromuscular junction. J. Gen. Physiol. 78, 313-344.
30. Plomp, J.J., van Kempen, G.Th.H., and Molenaar, P.C. (1992). Adaptation of quantal content to decreased postsynaptic sensitivity at single endplates in α-bungarotoxin treated rats. J. Physiol. (Lond.) 458, 487-499.
31. Plomp, J.J., van Kempen, G.Th.H., De Baets, M.B., Graus, Y.M.F., Kuks, J.B.M., and Molenaar, P.C. (1995). Acetylcholine release in myasthenia gravis: regulation at single end-plate level. Ann. Neurol. 37, 627-636.
32. Qin, F., Auerbach, A., and Sachs, F. (1996). Estimating single-channel kinetic parameters from idealized patch-clamp data containing missed events. Biophys. J. 70, 264-280.
33. Sakmann, B., Patlak, J., and Neher, E. (1980). Single acetylcholine-activated channels show burst kinetics in the presence of desensitizing concentrations of agonist. Nature 286, 71-73.
34. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual, Second Edition (Plainview, NY: Cold Spring Harbor).
35. Schoepfer, R., Luther, M., and Lindstrom, J. (1988). The human medulloblastoma cell line TE671 expresses a muscle-like acetylcholine receptor. Cloning of the alpha-subunit cDNA. FEBS Lett. 226, 235-240.
36. Sigworth, F.J., and Sine, S.M. (1987). Data transformation for improved display and fitting of single-channel dwell time histograms. Biophys. J. 52, 1047-1054.
37. + channel, expressed in oocytes. Biophys. J. 70, 2640-2651.
38. Sine, S.M., Ohno, K., Bouzat, C., Auerbach, A., Milone, M., Pruitt, J.N., and Engel, A.G. (1995). Mutation of the acetylcholine receptor α subunit causes a slow-channel myasthenic syndrome by enhancing agonist binding affinity. Neuron 15, 229-239.
39. Uchitel, O., Engel, A.G., Walls, T.J., Nagel, A., Atassi, Z.M., and Bril, V. (1993). Congenital myasthenic syndromes. II. A syndrome attributed to abnormal interaction of acetylcholine with its receptor. Muscle Nerve 16, 1293-1301.
40. Wang, H.-L., Auerbach, A., Bren, N., Ohno, K., Engel, A.G., and Sine, S.M. (1997). Mutation in the M1 domain of the acetylcholine receptor alpha subunit decreases the rate of agonist dissociation. J. Gen. Physiol. 109, 757-766.