Caenorhabditis elegans levamisole resistance genes lev-1, unc-29, and unc-38 encode functional nicotinic acetylcholine receptor subunits

Journal of Neuroscience

Volumn 17, Issue 15, 1997, Pages 5843-5857

  Fleming, John T ^a,e   Squire, Michael D ^a,b   Barnes, Thomas M ^a,f   Tornoe, Camilla ^b   Matsuda, Kazuhiko ^b,g   Ahnn, Joohong ^c,h   Fire, Andrew ^c   Sulston, John E ^a,i   Barnard, Eric A ^a,j   Sattelle, David B ^b   Lewis, James A ^d  

^a MEDICAL RESEARCH COUNCIL   (United Kingdom)

^b BABRAHAM INSTITUTE   (United Kingdom)

^c GEOPHYSICAL LABORATORY   (United States)

^d UNIVERSITY OF TEXAS AT SAN ANTONIO   (United States)

^e MASSACHUSETTS GENERAL HOSPITAL   (United States)

^f MCGILL UNIVERSITY   (Canada)

^g KINKI UNIVERSITY   (Japan)

^h Gwangju Institute of Science and Technology (GIST)   (South Korea)

ⁱ WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^j ROYAL FREE HOSPITAL   (United Kingdom)

more..

Author keywords

Acetylcholine receptor; Caenorhabditis elegans; Confocal microscopy; Evolution; GFP; lev 1; Levamisole resistance genes; Nematode; Receptor localization; Receptor mutations; Transmembrane domain mutation; unc 29; Unc 38; Xenopus oocyte expression

Indexed keywords

ALPHA BUNGAROTOXIN; CHOLINERGIC RECEPTOR; ION CHANNEL; LEVAMISOLE; MECAMYLAMINE; NEOSURUGATOXIN; NICOTINIC RECEPTOR; RECEPTOR SUBUNIT; TUBOCURARINE CHLORIDE;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; CAENORHABDITIS ELEGANS; CONFOCAL MICROSCOPY; DESENSITIZATION; EVOLUTION; GENE EXPRESSION; GENETIC ANALYSIS; ION CONDUCTANCE; NONHUMAN; OOCYTE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SEQUENCE ANALYSIS; XENOPUS LAEVIS;

EID: 17444443158     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.17-15-05843.1997     Document Type: Article

References (95)

1. Abramson SN, Culver P, Kline T, Li Y, Guest P, Gutman L, Taylor P (1988) Lophotoxin and related coral toxins covalently label the α-subunit of the nicotinic acetylcholine receptor. J Biol Chem 263:18568-18573.
2. 190 in the α-subunit of the nicotinic acetylcholine receptor. J Biol Chem 264:12666-12672.
3. Ajuh PM, Egwang TG (1994) Cloning of a cDNA encoding a putative nicotinic acetylcholine receptor subunit of the human filarial parasite Onchocerca volvulus. Gene 144:127-129.
4. Alfonso A, Grundahl K, McManus JR, Rand JB (1994) Cloning and characterization of the choline acetyltransferase structural gene (cha-1) from C. elegans. J Neurosci 14:2290-2300.
5. Arpagaus M, Fedon Y, Cousin X, Chatonne A, Berge J-B, Fournier D, Toutant J-P (1994) cDNA sequence, gene structure, and in vitro expression of ace-1, the gene encoding acetylcholinesterase of class A in the nematode Caenorhabditis elegans. J Biol Chem 269:9957-9965.
6. Bai D, Abramson SN, Sattelle DB (1993) Actions of a coral toxin analogue (Bipinnatin-B) on an insect nicotinic acetylcholine receptor. Arch Insect Biochem Physiol 23:155-159.
7. Ballivet M, Alliod C, Bertrand S, Bertrand D (1996) Nicotinic acetylcholine receptors in the nematode Caenorhabditis elegans. J Mol Biol 258:261-269.
8. Barchan D, Kachalsky S, Neumann D, Vogel Z, Ovadia M, Kochva E, Fuchs S (1992) How the mongoose can fight the snake: the binding site of the mongoose acetylcholine receptor. Proc Natl Acad Sci USA 89:7717-7721.
9. Bargmann CI, Avery L (1995) Laser killing of cell in Caenorhabditis elegans. In: Methods in cell biology, Vol 48, Caenorhabditis elegans: modern biological analysis of an organism (Epstein HF, Shakes DC, eds), pp 225-250. New York: Academic.
10. Barnard EA (1992) Receptor classes and neurotransmitter-gated ion channels. Trends Biochem Sci 17:368-374.
11. Barnes TM (1990) Echolocation: a PCR-based strategy for reliably and rapidly mapping transposon insertion sites. Nucleic Acids Res 18:6741-6742.
12. Baylis HA, Matsuda K, Squire MD, Fleming JT, Harvey RJ, Darlison MG, Barnard EA, Sattelle DB (1997) ACR-3, a Caenorhabditis elegans nicotinic acetylcholine receptor subunit: molecular cloning and functional expression. Receptors Channels, in press.
13. Bossy B, Ballivet M, Spierer P (1988) Conservation of neuronal nicotinic acetylcholine receptors from Drosophila to vertebrate central nervous systems. EMBO J 7:611-618.
14. Brenner S (1974) The genetics of Caenorhabditis elegans. Genetics 77:71-94.
15. Buonanno A, Mudd J, Merlie JP (1989) Isolation and characterization of the β and ∈ subunit genes of mouse muscle acetylcholine receptor. J Biol Chem 264:7611-7616.
16. Chalfie M, Tu Y, Euskirchen G, Ward WW, Prasher DC (1994) Green fluorescent protein as a marker for gene expression. Science 263:802-805.
17. Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162:156-159.
18. Claudio T, Paulson HL, Green WN, Ross AF, Hartman DS, Hayden D (1989) Fibroblasts transfected with Torpedo acetylcholine receptor β-, γ-, and δ-subunit cDNAs express functional receptors when infected with a retroviral α recombinant. J Cell Biol 108:2277-2290.
19. Collins J, Saari B, Anderson P (1987) Activation of a transposable element in the germ line but not the soma of Caenorhabditis elegans. Nature 328:726-728.
20. Colquhoun LM, Holden-Dye L, Walker RJ (1993) The action of nicotinic receptor specific toxins on the somatic muscle cells of the parasitic nematode Ascaris suum. Mol Neuropharmacol 3:11-16.
21. Coulson A, Sulston J, Brenner S, Karn J (1986) Towards a physical map of the genome of the nematode Caenorhabditis elegans. Proc Natl Acad Sci USA 83:7821-7825.
22. Couturier S, Bertrand D, Matter JM, Hernandez MC, Bertrand S, Millar N, Valera S, Barkas T, Ballivet M (1990) A neuronal nicotinic acetylcholine receptor subunit (α 7) is developmentally regulated and forms a homo-oligomeric channel blocked by α-BTX. Neuron 5:847-856.
23. Craxton M (1991) Linear amplification sequencing, a powerful method for sequencing DNA. Methods Companion Methods Enzymol 3:20-26.
24. Czajkowski C, Kaufmann C, Karlin A (1993) Negatively charged amino acid residues in the nicotinic receptor δ subunit that contribute to the binding of acetylcholine. Proc Natl Acad Sci USA 90:6285-6289.
25. Dascal N, Landau EM, Lass Y (1984) Xenopus oocyte resting potential, muscarinic responses and the role of calcium and guanosine 3′,5′-cyclic monophosphate. J Physiol (Lond) 352:551-574.
26. Devillers-Thiery A, Galzi JL, Eisele JL, Bertrand S, Bertrand D, Changeux JP (1993) Functional architecture of the nicotinic acetylcholine receptor: a prototype of ligand-gated ion channels. J Membr Biol 136:97-112.
27. Felsenstein J (1992) Estimating effective population size from samples of sequences: a bootstrap Monte Carlo integration method. Genet Res 60:209-220.
28. Fire A (1986) Integrative transformation of Caenorhabditis elegans. EMBO J 5:2673-2680.
29. Fleming JT, Riina HA, Sattelle DB (1991) Acetylcholine and GABA receptors of Caenorhabditis elegans expressed in Xenopus oocytes. J Physiol (Lond) 438:371p.
30. Fleming JT, Tornoe C, Riina HA, Coadwell J, Lewis JA, Sattelle DB (1993) Acetylcholine receptor molecules of the nematode Caenorhabditis elegans. In: Comparative molecular neurobiology (Pichon Y, ed), pp 65-80. Basel: Birkhauser Verlag.
31. Frohman MA, Dush MK, Martin GR (1988) Rapid production of full-length cDNAs from rare transcripts: amplification using a single gene-specific oligonucleotide primer. Proc Natl Acad Sci USA 85:8998-9002.
32. Galzi J-L, Devillers-Thiery A, Hussy N, Bertrand S, Changeux J-P, Bertrand D (1992) Mutations in the channel domain of a neuronal nicotinic receptor convert ion selectivity from cationic to anionic. Nature 359:500-505.
33. Gautam M, Noakes PG, Mudd J, Nichol M, Chu GC, Sanes JR, Merlie JP (1995) Failure of postsynaptic specialization to develop at neuromuscular junctions of rapsyn-deficient mice. Nature 377:232-236.
34. Gautam M, Noakes PG, Moscoso L, Rupp F, Scheller RH, Merlie JP, Sanes JR (1996) Defective neuromuscular synaptogenesis in agrin-deficient mutant mice. Cell 85:525-535.
35. Godzik A, Sander C (1989) Conservation of residue interactions in a family of Ca-binding proteins. Protein Eng 2:589-596.
36. Greenwald I (1985) lin-12, a nematode homeotic gene, is homologous to a set of mammalian proteins that includes epidermal growth factor. Cell 43:583-590.
37. Harrow ID, Gration KAF (1985) Mode of action of the anthelmintics morantel, pyrantel and levamisole on muscle cell membrane of the nematode Ascaris suum. Pestic Sci 16:662-672.
38. Heim R, Prasher DC, Tsien RY (1994) Wavelength mutations and posttranslational autoxidation of green fluorescent protein. Proc Natl Acad Sci USA 91:12501-12504.
39. Hermans-Borgmeyer I, Zopf D, Ryseck R-P, Hovemann B, Betz H, Gundelfinger ED (1986) Primary structure of a developmentally regulated nicotinic acetylcholine receptor protein from Drosophila. EMBO J 5:1503-1508.
40. Higgins DG, Bleasby AJ, Fuchs R (1992) CLUSTALV: improved software for multiple sequence alignment. Comput Appl Biosci 8:189-191.
41. Huelsenbeck JP, Hillis DM (1993) Success of phylogenetic methods in the four-taxon case. J Systematic Biol 42:247-264.
42. Huganir RL (1988) Regulation of the nicotinic acetylcholine receptor channel by protein phosphorylation. Curr Top Membr Transp 33:147-163.
43. Huganir RL, Greengard P (1983) cAMP-dependent protein kinase phosphorylates the nicotinic acetylcholine receptor. Proc Natl Acad Sci USA 80:1130-1134.
44. Huganir RL, Miles K, Greengard P (1984) Phosphorylation of the nicotinic acetylcholine receptor by an endogenous tyrosine-specific protein kinase. Proc Natl Acad Sci USA 81:6968-6972.
45. Imoto K, Busch C, Sakmann B, Mishina M, Konno T, Nakai J, Bujo H, Mori Y, Fukuda K, Numa S (1988) Rings of negatively charged amino acids determine the acetylcholine receptor channel conductance. Nature 335:645-648.
46. + RNA. Methods Enzymol 152:254-261.
47. Jin Y, Hoskins R, Horvitz HR (1994) Control of type-D GABAergic neuron differentiation by C. elegans UNC-30 homeodomain protein. Nature 372:780-783.
48. Johnson CD, Stretton AOW (1980) Neural control of locomotion in Ascaris: anatomy, electrophysiology, and biochemistry. In: Nematodes as biological models, Vol 1, Behavioral and developmental models (Zuckerman BM, ed), pp 159-196. New York: Academic.
49. Kao PN, Karlin A (1986) Acetylcholine receptor binding site contains a disulfide crosslink between adjacent half-cystinyl residues. J Biol Chem 261:8085-8088.
50. Karlin A (1993) Structure of nicotinic acetylcholine receptors. Curr Opin Neurobiol 3:299-309.
51. Karlin A, Akabas MH (1995) Toward a structural basis for the function of nicotinic acetylcholine receptors and their cousins. Neuron 15:1231-1244.
52. Konno T, Busch C, Von Kitzing E, Imoto K, Wang F, Nakai J, Mishina M, Numa S, Sakmann B (1991) Rings of anionic amino acids as structural determinants of ion selectivity in the acetylcholine receptor channel. Proc R Soc Lond [Biol] 244:69-79.
53. Krause M, Hirsh D (1987) A trans-spliced leader sequence on actin mRNA in C. elegans. Cell 49:753-761.
54. Lewis JA, Wu C-H, Berg H, Levine JH (1980a) The genetics of levamisole resistance in the nematode Caenorhabditis elegans. Genetics 95:905-928.
55. Lewis JA, Wu C-H, Levine JH, Berg H (1980b) Levamisole-resistant mutants of the nematode Caenorhabditis elegans appear to lack pharmacological acetylcholine receptors. Neuroscience 5:967-989.
56. Lewis JA, Fleming JT, McLafferty S, Murphy H, Wu C (1987a) The levamisole receptor, a cholinergic receptor of the nematode Caenorhabditis elegans. Mol Pharmacol 31:185-193.
57. Lewis JA, Elmer JS, Skimming J, McLafferty S, Fleming J, McGee T (1987b) Cholinergic receptor mutants of the nematode Caenorhabditis elegans. J Neurosci 7:3059-3071.
58. Marshall J, Buckingham SD, Shingai R, Lunt GG, Goosey MW, Darlison MG, Sattelle DB, Barnard EA (1990) Sequence and functional expression of a single a subunit of an insect nicotinic acetylcholine receptor. EMBO J 9:4391-4398.
59. Martin RJ, Pennington AJ, Duittoz AH, Robertson S, Kusel JR (1991) The physiology and pharmacology of neuromuscular transmission in the nematode parasite Ascaris suum. Parasitology 102:S41-S58.
60. McCombie WR, Kirkness E, Fleming JT, Kerlavage AR, Iovannisci DM, Martin-Gallardo A (1991) The use of exonuclease III deletions in automated DNA sequencing. Methods Companion Methods Enzymol 3:33-40.
61. Mello C, Fire A (1995) DNA transformation. In: Methods in cell biology, Vol 48, Caenorhabditis elegans: modern biological analysis of an organism (Epstein HF, Shakes DC, eds), pp 451-482. New York: Academic.
62. Mello CC, Kramer JM, Stinchcomb D, Ambros V (1991) Efficient gene transfer in C. elegans: extrachromosomal maintenance and integration of transforming sequences. EMBO J 10:3959-3970.
63. Miller KG, Alfonso A, Nguyen M, Crowell JA, Johnson CD, Rand JB (1996a) A genetic selection for Caenorhabditis elegans synaptic transmission mutants. Proc Natl Acad Sci USA 93:12593-12598.
64. Miller LM, Waring DA, Kim S (1996b) Mosaic analysis using a ncl-1 (+) extrachromosomal array reveals that lin-31 acts in the Pn.p cells during Caenorhabditis elegans vulval development. Genetics 143:1181-1191.
65. Moerman DG, Waterston RH (1984) Spontaneous unstable unc-22 IV mutations in C. elegans var. Bergerac. Genetics 108:859-877.
66. Moerman DG, Benian GM, Waterston RH (1986) Molecular cloning of the muscle gene unc-22 in Caenorhabditis elegans by Tc1 transposon tagging. Proc Natl Acad Sci USA 83:2579-2583.
67. Moerman DG, Benian GM, Barstead RJ, Schriefer LA, Waterston RH (1988) Identification and intracellular localization of the unc-22 gene product of Caenorhabditis elegans. Genes Dev 2:93-105.
68. Nef P, Mauron A, Stalder R, Alliod C, Ballivet M (1984) Structure, linkage, and sequence of the two genes encoding the δ and γ subunits of the nicotinic acetylcholine receptor. Proc Natl Acad Sci USA 81:7975-7979.
69. Nef P, Oneyser C, Alliod C, Couturier S, Ballivet M (1988) Genes expressed in the brain define three distinct neuronal nicotinic acetylcholine receptors. EMBO J 7:595-601.
70. Neumann D, Barchan D, Horowitz M, Kochva E, Fuchs S (1989) Snake acetylcholine receptor: cloning of the domain containing the four extracellular cysteines of the α subunit. Proc Natl Acad Sci USA 86:7255-7259.
71. Nonet ML, Grundahl K, Meyer BJ, Rand JB (1993) Synaptic function is impaired but not eliminated in C. elegans mutants lacking synaptotagmin. Cell 73:1291-1305.
72. Okkema PG, Harrison SW, Plunger V, Aryana A, Fire A (1993) Sequence requirements for myosin gene expression and regulation in Caenorhabditis elegans. Genetics 135:385-404.
73. Ortells MO, Lunt GG (1995) Evolutionary history of the ligand-gated ion-channel superfamily of receptors. Trends Neurosci 18:121-127.
74. Pedersen SE, Cohen JB (1990) d-Tubocurarine binding sites are located at α-γ and α-δ subunit interfaces of the nicotinic acetylcholine receptor. Proc Natl Acad Sci USA 87:2785-2789.
75. Revah F, Bertrand D, Galzi J-L, Devillers-Thiery A, Hussy N, Mulle C, Bertrand S, Ballivet M, Changeux J-P (1991) Mutations in the channel domain alter desensitization of a neuronal nicotinic receptor. Nature 353:846-849.
76. Robertson S, Martin RJ (1993) Levamisole-activated single-channel currents from muscle of the nematode parasite Ascaris suum. Br J Pharmacol 108:170-178.
77. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406-425.
78. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: A laboratory manual, Ed 2. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
79. Sargent PB (1993) The diversity of neural nicotinic acetylcholine receptors. Annu Rev Neurosci 16:403-443.
80. Schuler GD, Altschul SF, Lipman DJ (1991) A workbench for multiple alignment construction and analysis. Proteins 9:180-190.
81. Squire MD, Tornoe C, Baylis HA, Fleming JT, Barnard EA, Sattelle DB (1995) Molecular cloning and functional co-expression of a Caenorhabditis elegans nicotinic acetylcholine receptor subunit (acr-2). Receptors Channels 3:107-115.
82. Swofford DL (1991) PAUP: phylogenetic analysis using parsimony, version 3.0 sec +3. Champaign, IL: Illinois Natural History Survey.
83. Swofford DL, Olsen GJ (1990) Phylogeny reconstruction. In: Molecular systematics (Hillis DM, Moritz C, eds), pp 411-501. Sunderland, MA: Sinauer.
84. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673-4680.
85. Tornoe C, Bai D, Holden-Dye L, Abramson SN, Sattelle DB (1995) Actions of neurotoxins (bungarotoxins, neosurugatoxin, and lophotoxins) on insect and nematode nicotinic acetylcholine receptors. Toxicon 33:411-424.
86. Treinin M, Chalfie M (1995) A mutated acetylcholine receptor subunit causes neuronal degeneration in C. elegans. Neuron 14:871-877.
87. Unwin N (1989) The structure of ion channels in membranes of excitable cells. Neuron 3:665-676.
88. Unwin N (1993a) Neurotransmitter Action: opening of ligand-gated ion channels. Cell 72:31-41.
89. Unwin N (1993b) Nicotinic acetylcholine receptor at 9Å resolution. J Mol Biol 229:1101-1124.
90. Unwin N (1995) Acetylcholine receptor channel imaged in the open state. Nature 373:37-43.
91. Wiley LJ, Weiss AS, Sangster NC, Qun Li (1996) Cloning and sequence analysis of the candidate nicotinic acetylcholine receptor alpha subunit gene tar1 from Trichostrongylus colubriformis. Gene 182:97-100.
92. Williams BD, Waterston RH (1994) Genes critical for muscle development and function in Caenorhabditis elegans identified through lethal mutations. J Cell Biol 124:475-490.
93. Williams BD, Schrank B, Huynh C, Shownkeen R, Waterston RH (1992) A genetic mapping system in Caenorhabditis elegans based on polymorphic sequence-tagged sites. Genetics 131:609-624.
94. Yuan J, Shaham S, Ledoux S, Ellis HM, Horvitz HR (1993) The C. elegans cell death gene ced-3 encodes a protein similar to mammalian interleukin-1B-converting enzyme. Cell 75:641-652.
95. Zorio DAR, Cheng NSN, Blumenthal TE, Spieth J (1994) Operons as a common form of chromosomal organization in C. elegans. Nature 372:270-272.