Evolution of nicotinic acetylcholine receptor subunits

Molecular Biology and Evolution

Volumn 15, Issue 5, 1998, Pages 518-527

  Tsunoyama, Kazuhisa ^a,b   Gojobori, Takashi ^a,b  

^a GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

^b NATIONAL INSTITUTE OF GENETICS   (Japan)

Author keywords

Acetylcholine receptor; Evolution; Functional constraints

Indexed keywords

NICOTINIC RECEPTOR; RECEPTOR SUBUNIT;

AMINO ACID SEQUENCE; ARTICLE; HUMAN; MOLECULAR EVOLUTION; MULTIGENE FAMILY; MUSCLE; NERVOUS SYSTEM; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; UNINDEXED SEQUENCE;

EID: 0031954683     PISSN: 07374038     EISSN: None     Source Type: Journal    
DOI: 10.1093/oxfordjournals.molbev.a025951     Document Type: Article

References (79)

1. AJUH, P. M., and T. G. EGWANG. 1994. Cloning of a cDNA encoding a putative nicotinic acetylcholine receptor subunit of the human filarial parasite Onchocerca volvulus. Gene 144:127-129.
2. ANAND, R., and J. LINDSTROM. 1990. Nucleotide sequence of the human nicotinic acetylcholine receptor beta 2 subunit gene. Nucleic Acids Res. 18:4272.
3. BALDWIN, T. J., C. M. YOSHIHARA, K. BLACKMER, C. R. KINTNER, and S. J. BURDEN. 1988. Regulation of acetylcholine receptor transcript expression during development in Xenopus laevis. J. Cell Biol. 106:469-478.
4. BALLIVET, M., J. PATRICK, J. S. LEE, and S. HEINEMANN. 1982. Molecular cloning of cDNA coding for the gamma subunit of Torpedo acetylcholine receptor. Proc. Natl. Acad. Sci. USA 79:4466-4470.
5. BEESON, D., M. BRYDSON, M. BETTY, S. JEREMIAH, S. POVEY, A. VINCENT, and J. NEWSOM-DAVIS. 1993. Primary structure of the human muscle acetylcholine receptor. cDNA cloning of the gamma and epsilon subunits. Eur. J. Biochem. 215:229-238.
6. BEESON, D., M. BRYDSON, and J. NEWSOM-DAVIS. 1989. Nucleotide sequence of human muscle acetylcholine receptor beta-subunit. Nucleic Acids Res. 17:4391.
7. BOSSY, B., M. BALLIVET, and P. SPIERER. 1988. Conservation of neural nicotinic acetylcholine receptors from Drosophila to vertebrate central nervous systems. EMBO J. 7:611-618.
8. BOULTER, J., J. CONNOLLY, E. S. DENERIS, D. J. GOLDMAN, S. F. HEINEMANN, and J. PATRICK. 1987. Functional expression of two neuronal nicotinic acetylcholine receptors from cDNA clones identifies a gene family. Proc. Natl. Acad. Sci. USA 84:7763-7767.
9. BOULTER, J., K. EVANS, D. GOLDMAN, G. MARTIN, D. TRECO, S. HEINEMANN, and J. PATRICK. 1986. Isolation of a cDNA clone coding for a possible neural nicotinic acetylcholine receptor alpha-subunit. Nature 319:368-374.
10. BOULTER, J., A. O'SHEA-GREENFIELD, R. M. DUVOISIN et al. (12 co-authors). 1990. Alpha-3, alpha-5, and beta-4: three members of the rat neuronal nicotinic acetylocholine receptor-related gene family form a gene cluster. J. Biol. Chem. 265:4472-4482.
11. BUONANNO, A., J. MUDD, V. SHAH, and J. P. MERLIE. 1986. A universal oligonucleotide probe for acetylcholine receptor genes: selection and sequencing of cDNA clones for the mouse muscle beta subunit. J. Biol. Chem. 261:16451-16458.
12. CAULEY, K., B. W. AGRANOFF, and D. GOLDMAN. 1989. Identification of a novel nicotinic acetylcholine receptor structural subunit expressed in goldfish retina. J. Cell Biol. 108: 637-645.
13. _. 1990. Multiple nicotinic acetylcholine receptor genes are expressed in goldfish retina and tectum. J. Neurosci. 10: 670-683.
14. CHANGEUX, J. P. 1990. Functional architecture and dynamics of the nicotinic acetylcholine receptor: an allosteric ligandgated ion channel. Raven Press, New York.
15. CHANGEUX, J. P., A. BESSIS, J. P. BOURGEOIS et al. (11 co-authors). 1996. Nicotinic receptors and brian plasticity. Cold Spring Harb. Symp. Quant. Biol. 61:343-362.
16. CHINI, B., F. CLEMENTI, N. HUKOVIC, and E. SHER. 1992. Neuronal-type alpha-bungarotoxin receptors and the alpha 5-nicotinic receptor subunit gene are expressed in neuronal and nonneuronal human cell lines. Proc. Natl. Acad. Sci. USA 89:1572-1576.
17. CLAUDIO, T., M. BALLIVET, J. PATRICK, and S. HEINEMANN. 1983. Nucleotide and deduced amino acid sequences of Torpedo californica acetylcholine receptor gamma subunit. Proc. Natl. Acad. Sci. USA 80:1111-1115.
18. 7) is developmentally regulated and forms a homo-oligomeric channel blocked by α-BTX. Neuron 5: 847-856.
19. COUTURIER, S., L. ERKMAN, S. VALERA, D. RUNGGER, S. BERTRAND, J. BOULTER, M. BALLIVET, and D. BERTRAND. 1990. Alpha 5, alpha 3, and non-alpha 3. Three clustered avian genes encoding neuronal nicotinic acetylcholine receptor-related subunits. J. Biol. Chem. 265:17560-17567.
20. CRIADO, M., V. WITZEMANN, M. KOENEN, and B. SAKMANN. 1988. Nucleotide sequence of the rat muscle acetylcholine receptor epsilon-subunit. Nucleic Acids Res. 16:10920.
21. 3: a new member of nicotinic acetylcholine receptor gene family is expressed in brain. J. Biol. Chem. 264:6268-6272.
22. DEVILLERS-THIERY, A., J. GIRAUDAT, M. BENTABOULET, and J. P. CHANGEUX. 1983. Complete mRNA coding sequence of the acetylcholine binding alpha-subunit of Torpedo marmorata acetylcholine receptor: a model for the transmembrane organization of the polypeptide chain. Proc. Natl. Acad. Sci. USA 80:2067-2071.
23. DEVILLERS-THIERY, A., J. GIRAUDAT, M. BENTABOULET, A. KLARSFELD, and J. P. CHANGEUX. 1984. Molecular genetics of Torpedo marmorata acetylcholine receptor. Adv. Exp. Med. Biol. 181:17-29.
24. 9: an acetylcholine receptor with novel pharmacological properties expressed in rat cochlear hair cells. Cell 79:705-715.
25. ELLIOTT, K. J., S. B. ELLIS, K. J. BERCKHAN, A. URRUTIA, L. E. CHAVEZ-NORIEGA, E. C. JOHNSON, G. VELICELEBI, and M. M. HARPOLD. 1996. Comparative structure of human neuronal alpha 2-alpha 7 and beta 2-beta 4 nicotinic acetylcholine receptor subunits and functional expression of the alpha 2, alpha 3, alpha 4, alpha 7, beta 2, and beta 4 subunits. J. Mol. Neurosci. 7:217-228.
26. ENDO, T, K. IKEO, and T. GOJOBORI. 1996. Large-scale search for genes on which positive selection may operate. Mol. Biol. Evol. 13:685-690.
27. GALZI, J. L., and J. P. CHANGEUX. 1994. Ligand-gated channel as unconventional allosteric proteins. Curr. Opin. Struct. Biol. 4:554-565.
28. GARCIA-GUZMAN, M., F. SALA, S. SALA, A. CAMPOS-CARO, W. STUHMER, L. M. GUTIERREZ, and M. CRIADO. 1995. Alpha-bungarotoxin-sensitive nicotinic receptors on bovine chromaffin cells: molecular cloning, functional expression and alternative splicing of the alpha 7. Eur. J. Neurosci. 7:647-655.
29. GARDNER, P. D. 1990. Nucleotide sequence of the epsilon-subunit of the mouse muscle nicotinic acetylcholine receptor. Nucleic Acids Res. 18:6714.
30. GOLDMAN, D. J., E. S. DENERIS, W. LUYTEN, A. KOCHHAR, J. PATRICK, and S. F. HEINEMANN. 1987. Members of a nicotinic acetylcholine receptor gene family are expressed in different regions of the mammalian central nervous systems. Cell 48:965-973.
31. GUNDELFINGER, E. D. 1995. Evolution and desensitization of LGIC receptors. Trends Neurosci. 18:297.
32. HERNANDEZ, M. C., L. ERKMAN, L. MATTER-SADZINSKI, T. ROZTOCIL, M. BALLIVET, and J. M. MATTER. 1995. Characterization of the nicotinic acetylcholine receptor beta 3 gene. Its regulation within the avian nervous system is effected by a promoter 143 base pairs in length. J. Biol. Chem. 270:3224-3233.
33. HIEBER, V., J. BOUCHEY, B. W. AGRANOFF, and D. GOLDMAN. 1990. Nucleotide and deduced amino acid sequence of the goldfish neural nicotinic acetylcholine receptor beta-2 subunit. Nucleic Acids Res. 18:5307.
34. HOEKSTRA, R., A. VISSER, L. J. WILEY, A. S. WEISS, N. C. SANGSTER, and M. H. ROOS. 1997. Characterization of an acetylcholine receptor gene of haemonchus contortus in relation to levamisole resistance. Mol. Biochem. Parasitol. 84: 179-187.
35. ISENBERG, K. E., J. MUDD, V. SHAH, and J. P. MERLIE. 1986. Nucleotide sequence of the mouse muscle nicotinic acetylcholine receptor alpha subunit. Nucleic Acids Res. 14:5111.
36. JUKES, T. H., and C. R. CANTOR. 1969. Evolution of protein molecules. Pp. 21-132 in H. N. MUNRO, ed. Mammalian protein metabolism. Academic Press, New York.
37. KARLIN, A. 1993. Structure of nicotinic acetylcholine receptors. Curr. Opin. Neurobiol. 3:299-309.
38. KIMURA, M. 1983. The neutral theory of molecular evolution. Cambridge University Press, Cambridge, England.
39. KUBO, S., M. NODA, T. TAKAI et al. (13 co-authors). 1985. Primary structure of delta subunit precursor of calf muscle acetylcholine receptor deduced from cDNA sequence. Eur. J. Biochem. 149:5-13.
40. KULLBERG, R. W., Y. C. ZHENG, W. TODT, J. L. OWENS, S. E. FRASER, and G. MANDEL. 1994. Structure and expression of the nicotinic acetylcholine receptor beta subunit of Xenopus laevis. Receptors Channels 2:23-31.
41. LE NOVÈRE, N., and J. P. CHANGEUX. 1995. Molecular evolution of the nicotinic acetylchopline receptor: an example of multigene family in excitable cells. J. Mol. Evol. 40:155-172.
42. LUTHER, M. A., R. SCHOEPFER, P. WHITING, B. CASEY, Y. BLATT, M. S. MONTAL, M. MONTAL, and J. LINSTROM. 1989. A muscle acetylcholine receptor is expressed in the human cerebellar medulloblastoma cell line TE671. J. Neurosci. 9:1082-1096.
43. MCGEHEE, D. S., M. J. S. HEATH, S. GEIBER, P. DEVAY, and L. W. ROLE. 1995. Nicotine enhancement of fast excitatory synaptic transmission in CNS by presynaptic receptors. Science 269:1692-1696.
44. MARICQ, A. V., A. S. PETERSON, A. J. BRAKE, R. M. MEYERS, and D. JULIUS. 1991. Primary structure and functional expression of the 5HT3 receptor, a serotonin-gated ion channel. Science 254:432-437.
45. MARSHALL, J., S. D. BUCKINGHAM, R. SHINGAI, G. G. LUNT, M. W. GOOSEY, M. G. DARLISON, D. B. SATTELLE, and E. A. BARNARD. 1990. Sequence and functional expression of a single alpha subunit of an insect nicotinic acetylcholine receptor. EMBO J. 9:4391-4398.
46. MIHOVILOVIC, M., and A. D. ROSES. 1991. Expression of mRNAs in human thymus coding for the alpha 3 subunit of a neuronal acetylcholine receptor. Exp. Neurol. 111:175-180.
47. MONTEGGIA, L. M., M. GOPALAKRISHNAN, E. TOUMA, K. IDLER, N. NASH, S. P. ARNERIC, J. P. SULLIVAN, and T. GIORDANO. 1995. The cloning and transient expression of the human alpha 4 and beta 2 neuronal nicotinic acetylcholine receptor (nAChR) subunits. Gene 155:189-193.
48. MURRAY, N., Y. ZHENG, G. MANDEL, P. BREHM, R. BOLINGER, Q. REUER, and R. KULLBERG. 1995. A single site on the epsilon subunit is responsible for the change in ACh receptor channel conductance during skeletal muscle development. Neuron 14:865-870.
49. NEF, P., A. MAURON, R. STALDER, C. ALLIOD, and M. BALLIVET. 1984. Structure, linkage, and sequence of the two genes encoding the delta and gamma subunits of the nicotinic acetylcholine receptor. Proc. Natl. Acad. Sci. USA 81:7975-7979.
50. NEF, P., C. ONEYSER, C. ALLIOD, S. COUTURIER, and M. BALLIVET. 1988. Genes expressed in the brain define three distinct neuronal nicotinic acetylcholine receptors. EMBO J. 7:595-601.
51. NEI, M., and T. GOJOBORI. 1986. Simple methods for estimating the number of synonymous and nonsynonymous substitutions. Mol. Biol. Evol. 3:418-426.
52. NODA, M., Y. FURUTANI, H. TAKAHASHI et al. (11 co-authors). 1983. Cloning and sequence analysis of calf cDNA and human genomic DNA encoding alpha-subunit precursor of muscle acetylcholine receptor. Nature 305:818-823.
53. NODA, M., H. TAKAHASHI, T. TANABE, M. TOYOSATO, Y. FURUTANI, T. HIROSE, M. ASAI, S. INAYAMA, T. MIYATA, and S. NUMA. 1982. Primary structure of alpha-subunit precursor of Torpedo californica acteylcholine receptor deduced from cDNA sequence. Nature 299:793-797.
54. NUMA, S., M. NODA, H. TAKAHASHI, T. TANABE, M. TOYOSATO, Y. FURUTANI, and S. KIKYOTANI. 1983. Molecular structure of the nicotinic acetylcholine receptor. Cold Spring Harb. Symp. Quant. Biol. 48:57-69.
55. OHNO, K., D. O. HUTCHINSON, M. MILONE, J. M. BRENGMAN, C. BOUZAT, S. M. SINE, and A. G. ENGEL. 1995. Congenital myasthenic syndrome caused by prolonged acetylcholine receptor channel openings due to a mutation in the M2 domain of the ε subunit Proc. Natl. Acad. Sci. USA 92:758-762.
56. ORR-URTREGER, A., M. F. SELDIN, A. BALDINI, and A. L. BEAUDET. 1995. Cloning and mapping of the mouse alpha 7-neuronal nicotinicacetylcholine receptor. Genomics 26: 399-402.
57. ORTELLS, M. O., and G. G. LUNT. 1995. Evolutionary history of the ligand-gated ion-channel superfamily of receptors. Trends Neurosci. 18:121-127.
58. PENG, X., M. KATZ, V. GERZANICH, R. ANAND, and J. LINDSTROM. 1994. Human alpha 7 acetylcholine receptor: cloning of the alpha 7 subunit from the SH-SY5Y cell line and determination of pharmacological properties of native receptors and functional alpha 7 homomers expressed in Xenopus oocytes. Mol. Pharmacol. 45:546-554.
59. 5 subunit to neuronal acetylcholine receptor channels. Nature 380: 347-351.
60. ROLE, L. W., and D. K. BERG. 1996. Nicotinic receptors in the development and modulation of CNS synapses. Neuron 16: 1077-1085.
61. SAITOU, N., and M. NEI. 1987. Neighbor-joining: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4:406-425.
62. SAWRUK, E., P. SCHLOSS, H. BETZ, and B. SCHMITT. 1990a. Heterogeneity of Drosophila nicotinic acetylcholine receptors: SAD, a novel developmentally regulated alpha-subunit. EMBO J. 9:2671-2677.
63. SAWRUK, E., C. UDRI, H. BETZ, and B. SCHMITT. 1990e. SBD, a novel structural subunit of the Drosophila nicotinic acetylcholine receptor, shares its genomic localization with two alpha-subunits. FEBS Lett. 273:177-181.
64. SCHOEPFER, R., W. G. CONROY, P. WHITING, M. GORE, and J. LINDSTROM. 1990. Brain alpha-bungarotoxin binding protein cDNAs and MAbs reveal subtypes of this branch of the ligand-gated ion channel gene superfamily. Neuron 5: 35-48.
65. SCHOEPFER, R., P. WHITING, F. ESCH, R. BLACHER, S. SHIMASAKI, and J. LINDSTROM. 1988. cDNA clones coding for the structural subunit of a chicken brain nicotinic acetylcholine receptor. Neuron 1:241-248.
66. SHIBAHARA, S., T. KUBO, H. J. PERSKI, H. TAKAHASHI, M. NODA, and S. NUMA. 1985. Cloning and sequence analysis of human genomic DNA encoding gamma subunit precursor of muscle acetylcholine receptor. Eur. J. Biochem. 146: 15-22.
67. SIVILOTTI, L., and D. COLQUHOUN. 1995. Acetylcholine receptors: too many channels, too few functions. Science 269: 1681-1682.
68. SQUIRE, M. D., C. TORNOE, H. A. BAYLIS, J. T. FLEMING, E. A. BARNARD, and D. B. SATTELLE. 1995. Molecular cloning and functional co-expression of a Caenorhabditis elegans nicotinic acetylcholine receptor subunit (acr-2). Receptors Channels 3:107-115.
69. SUMIKAWA, K., M. HOUGHTO, J. C. SMITH, L. BELL, B. M. RICHARDS, and E. A. BARNARD. 1982. The molecular cloning and characterization of cDNA coding for the alpha subunit of the acetylcholine receptor. Nucleic Acids Res. 10: 5809-5822.
70. TAKAI, T., M. NODA, Y. FURUTANI et al. (12 co-authors). 1984. Primary structure of gamma subunit precursor of calf-muscle acetylcholine receptor deduced from the cDNA sequence. Eur. J. Biochem. 143:109-115.
71. TAKAI, T., M. NODA, M. MISHINA et al. (12 co-authors). 1985. Cloning, sequencing and expression of cDNA for a novel subunit of acetylcholine receptor from calf muscle. Nature 315:761-764.
72. TANABE, T., M. NODA, Y. FURUTANI, T. TAKAI, H. TAKAHASHI, K. TANAKA, T. HIROSE, S. INAYAMA, and S. NUMA. 1984. Primary structure of beta subunit precursor of calf muscle acetylcholine receptor deduced from cDNA sequence. Eur. J. Biochem. 144:11-17.
73. TARRONI, P., F. RUBBOLI, B. CHINI, R. ZWART, M. OORTGIESEN, E. SHER, and F. CLEMENTI. 1992. Neuronal-type nicotinic receptors in human neuroblastoma and small-cell lung carcinoma cell lines. FEBS Lett. 312:66-70.
74. THOMPSON, J. D., D. G. HIGGINS, and T. J. GIBSON. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.
75. WADA, K., M. BALLIVET, J. BOULTER, J. CONNOLLY, E. WADA, E. S. DENERIS, L. W. SWANSON, S. HEINEMANN, and J. PATRICK. 1988. Functional expression of a new pharmacological subtype of brain nicotinic acetylcholine receptor. Science 240:330-334.
76. WADSWORTH, S. C., L. S. ROSENTHAL, K. L. KAMMERMEYER, M. B. POTTER, and D. J. NELSON. 1988. Expression of a Drosophila melanogaster acetylcholine receptor-related gene in the central nervous system. Mol. Cell. Biol. 8:778-785.
77. WILLOUGHBY, J. J., N. N. NINKINA, M. M. BEECH, D. S. LATCHMAN, and J. N. WOOD. 1993. Molecular cloning of a human neuronal nicotinic acetylcholine receptor beta 3-like subunit. Neurosci. Lett. 155:136-139.
78. WITZEMANN, V., E. STEIN, B. BARG, T. KONNO, M. KOENEN, W. KUES, M. CRIADO, M. HOFMANN, and B. SAKMANN. 1990. Primary structure and functional expression of the alpha-, beta-, gamma-, delta-and epsilon-subunits of the acetylcholine receptor from rat muscle. Eur. J. Biochem. 194:437-448.
79. YU, L., R. J. LAPOLLA, and N. DAVIDSON. 1986. Mouse muscle nicotinic acetylcholine receptor gamma subunit: cDNA sequence and gene expression. Nucleic Acids Res. 14:3539-3555.