Diversity of Insect Nicotinic Acetylcholine Receptor Subunits

Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 683)

Abstract

Nicotinic acetylcholine receptors (nAChRs) are ligand-gated ion channels that mediate fast synaptic transmission in the insect nervous system and are targets of a major group of insecticides, the neonicotinoids. They consist of five subunits arranged around a central ion channel. Since the subunit composition determines the functional and pharmacological properties of the receptor the presence of nAChR families comprising several subunit-encoding genes provides a molecular basis for broad functional diversity. Analyses of genome sequences have shown that nAChR gene families remain compact in diverse insect species, when compared to their nematode and vertebrate counterparts. Thus, the fruit fly (Drosophila melanogaster), malaria mosquito (Anopheles gambiae), honey bee (Apis mellifera), silk worm (Bombyx mori) and the red flour beetle (Tribolium castaneum) possess 10–12 nAChR genes while human and the nematode Caenorhabditis elegans have 16 and 29 respectively. Although insect nAChR gene families are amongst the smallest known, receptor diversity can be considerably increased by the posttranscriptional processes alternative splicing and mRNA A-to-I editing which can potentially generate protein products which far outnumber the nAChR genes. These two processes can also generate species-specific subunit isoforms. In addition, each insect possesses at least one highly divergent nAChR subunit which may perform species-specific functions. Species-specific subunit diversification may offer promising targets for future rational design of insecticides that target specific pest insects while sparing beneficial species.

Keywords

Fermentation Schizophrenia Neurol Sponge Malaria 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Sine SM, Engel AG. Recent advances in Cys-loop receptor structure and function. Nature 2006; 440:448–455.PubMedCrossRefGoogle Scholar
  2. 2.
    Connolly CN, Wafford KA. The Cys-loop superfamily of ligand-gated ion channels: the impact of receptor structure on function. Biochem Soc Trans. 2004; 32:529–534.PubMedCrossRefGoogle Scholar
  3. 3.
    Changeux JP, Taly A. Nicotinic receptors, allosteric proteins and medicine. Trends Mol Med. 2008; 14:93–102.PubMedGoogle Scholar
  4. 4.
    Green WN, Wanamaker CP. The role of the cystine loop in acetylcholine receptor assembly. J Biol Chem. 1997; 272:20945–20953.PubMedCrossRefGoogle Scholar
  5. 5.
    Grutter T, de Carvalho LP, Dufresne V et al. Molecular tuning of fast gating in pentameric ligand-gated ion channels. Proc Natl Acad Sci. USA 2005; 102:18207–18212.PubMedCrossRefGoogle Scholar
  6. 6.
    Corringer PJ, Le Novere N, Changeux JP. Nicotinic receptors at the amino acid level. Annu Rev Pharmacol Toxicol. 2000; 40:431–458.PubMedCrossRefGoogle Scholar
  7. 7.
    Kao PN, Karlin A. Acetylcholine receptor binding site contains a disulfide cross-link between adjacent half-cystinyl residues. J Biol Chem. 1986; 261:8085–8088.PubMedGoogle Scholar
  8. 8.
    Millar NS, Gotti C. Diversity of vertebrate nicotinic acetylcholine receptors. Neuropharmacology. 2009;56(1):237–46PubMedCrossRefGoogle Scholar
  9. 9.
    Unwin N. Refined structure of the nicotinic acetylcholine receptor at 4A resolution. J Mol Biol. 2005; 346:967–989.PubMedCrossRefGoogle Scholar
  10. 10.
    Dellisanti CD, Yao Y, Stroud JC et al. Crystal structure of the extracellular domain of nAChR alpha1 bound to alpha-bungarotoxin at 1.94 A resolution. Nat Neurosci. 2007; 10:953–962.PubMedCrossRefGoogle Scholar
  11. 11.
    Changeux JP, Kasai M, Lee CY. Use of a snake venom toxin to characterize the cholinergic receptor protein. Proc Natl Acad Sci USA. 1970; 67:1241–1247.PubMedCrossRefGoogle Scholar
  12. 12.
    Brejc K, van Dijk WJ, Klaassen RV et al. Crystal structure of an ACh-binding protein reveals the ligand-binding domain of nicotinic receptors. Nature 2001; 411:269–276.PubMedCrossRefGoogle Scholar
  13. 13.
    Hilf RJ, Dutzler R. X-ray structure of a prokaryotic pentameric ligand-gated ion channel. Nature 2008; 452:375–379.PubMedCrossRefGoogle Scholar
  14. 14.
    Hogg RC, Bertrand D. Nicotinic acetylcholine receptors as drug targets. Curr Drug Targets CNS Neurol Disord. 2004; 3:123–130.PubMedCrossRefGoogle Scholar
  15. 15.
    Combi R, Dalpra L, Tenchini ML et al. Autosomal dominant nocturnal frontal lobe epilepsy—a critical overview. J Neurol. 2004; 251:923–934.PubMedCrossRefGoogle Scholar
  16. 16.
    Engel AG, Sine SM. Current understanding of congenital myasthenic syndromes. Curr Opin Pharmacol. 2005; 5:308–321.PubMedCrossRefGoogle Scholar
  17. 17.
    Hughes BW, Moro De Casillas ML, Kaminski HJ. Pathophysiology of myasthenia gravis. Semin Neurol. 2004; 24:21–30.PubMedCrossRefGoogle Scholar
  18. 18.
    Watson R, Jepson JE, Bermudez I et al. Alpha7-acetylcholine receptor antibodies in two patients with Rasmussen encephalitis. Neurology 2005; 65:1802–1804.PubMedCrossRefGoogle Scholar
  19. 19.
    Gotti C, Zoli M, Clementi F. Brain nicotinic acetylcholine receptors: native subtypes and their relevance. Trends Pharmacol Sci. 2006; 27:482–491.PubMedCrossRefGoogle Scholar
  20. 20.
    Brown LA, Jones AK, Buckingham SD et al. Contributions from Caenorhabditis elegans functional genetics to antiparasitic drug target identification and validation: nicotinic acetylcholine receptors, a case study. Int J Parasitol. 2006; 36:617–624.PubMedCrossRefGoogle Scholar
  21. 21.
    Kaminsky R, Ducray P, Jung M et al. A new class of anthelmintics effective against drug-resistant nematodes. Nature 2008; 452:176–180.PubMedCrossRefGoogle Scholar
  22. 22.
    Baylis HA, Sattelle DB, Lane NJ. Genetic analysis of cholinergic nerve terminal function in invertebrates. J Neurocytol. 1996; 25:747–762.PubMedCrossRefGoogle Scholar
  23. 23.
    Matsuda K, Buckingham SD, Kleier D et al. Neonicotinoids: insecticides acting on insect nicotinic acetylcholine receptors. Trends Pharmacol Sci. 2001; 22:573–580.PubMedCrossRefGoogle Scholar
  24. 24.
    Jeschke P, Nauen R. Neonicotinoids-from zero to hero in insecticide chemistry. Pest Manag Sci. 2008; 64(11):1084–98.PubMedCrossRefGoogle Scholar
  25. 25.
    Lind RJ, Clough MS, Reynolds SE et al. H-3 imidacloprid labels high-and low-affinity nicotinic acetylcholine receptor-like binding sites in the aphid Myzus persicae (Hemiptera: Aphididae). Pesticide Bioch Physiol. 1998; 62:3–14.CrossRefGoogle Scholar
  26. 26.
    Liu M-Y, Casida JE. High-affinity binding of H-3 imidacloprid in the insect acetylcholine receptor. Pesticide Biochem Physiol. 1993; 46:40–46.CrossRefGoogle Scholar
  27. 27.
    Zhang A, Kayser H, Maienfisch P et al. Insect nicotinic acetylcholine receptor: conserved neonicotinoid specificity of [(3)H]imidacloprid binding site. J Neurochem. 2000; 75:1294–1303.PubMedCrossRefGoogle Scholar
  28. 28.
    Bai B, Lummis SCR, Leicht W et al. Actions of imidacloprid and a related nitromethylene on cholinergic receptors of an identified insect motor-neuron. Pescticide Sci. 1991; 33:197–204.CrossRefGoogle Scholar
  29. 29.
    Jepson JE, Brown LA, Sattelle DB. The actions of the neonicotinoid imidacloprid on cholinergic neurons of Drosophila melanogaster. Invert Neurosci. 2006; 6:33–40.PubMedCrossRefGoogle Scholar
  30. 30.
    Brown LA, Ihara M, Buckingham SD et al. Neonicotinoid insecticides display partial and super agonist actions on native insect nicotinic acetylcholine receptors. J Neurochem. 2006; 99:608–615.PubMedCrossRefGoogle Scholar
  31. 31.
    Tomizawa M, Casida JE. Selective toxicity of neonicotinoids attributable to specificity of insect and mammalian nicotinic receptors. Annu Rev Entomol. 2003; 48:339–364.PubMedCrossRefGoogle Scholar
  32. 32.
    Nishiwaki H, Nakagawa Y, Kuwamura M et al. Correlations of the electrophysiological activity of neonicotinoids with their binding and insecticidal activities. Pest Manag Sci 2003; 59:1023–1030.PubMedCrossRefGoogle Scholar
  33. 33.
    Ballivet M, Patrick J, Lee J et al. Molecular cloning of cDNA coding for the gamma subunit of Torpedo acetylcholine receptor. Proc Natl Acad Sci USA. 1982; 79:4466–4470.PubMedCrossRefGoogle Scholar
  34. 34.
    Devillers-Thiery A, Giraudat J, Bentaboulet M et al. 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. 1983; 80:2067–2071.PubMedCrossRefGoogle Scholar
  35. 35.
    Noda M, Takahashi H, Tanabe T et al. Primary structure of alpha-subunit precursor of Torpedo californica acetylcholine receptor deduced from cDNA sequence. Nature 1982; 299:793–797.PubMedCrossRefGoogle Scholar
  36. 36.
    Noda M, Takahashi H, Tanabe T et al. Primary structures of beta-and delta-subunit precursors of Torpedo californica acetylcholine receptor deduced from cDNA sequences. Nature 1983; 301:251–255.PubMedCrossRefGoogle Scholar
  37. 37.
    Sumikawa K, Houghton M, Smith JC et al. The molecular cloning and characterisation of cDNA coding for the alpha subunit of the acetylcholine receptor. Nucleic Acids Res. 1982; 10:5809–5822.PubMedCrossRefGoogle Scholar
  38. 38.
    Hermans-Borgmeyer I, Zopf D, Ryseck RP et al. Primary structure of a developmentally regulated nicotinic acetylcholine receptor protein from Drosophila. EMBO J. 1986; 5:1503–1508.PubMedGoogle Scholar
  39. 39.
    Bossy B, Ballivet M, Spierer P. Conservation of neural nicotinic acetylcholine receptors from Drosophila to vertebrate central nervous systems. EMBO J. 1988; 7:611–618.PubMedGoogle Scholar
  40. 40.
    Grauso M, Reenan RA, Culetto E et al. Novel putative nicotinic acetylcholine receptor subunit genes, Dalpha5, Dalpha6 and Dalpha7, in Drosophila melanogaster identify a new and highly conserved target of adenosine deaminase acting on RNA-mediated A-to-I pre-mRNA editing. Genetics 2002; 160:1519–1533.PubMedGoogle Scholar
  41. 41.
    Jonas P, Baumann A, Merz B et al. Structure and developmental expression of the D alpha 2 gene encoding a novel nicotinic acetylcholine receptor protein of Drosophila melanogaster. FEBS Lett. 1990; 269:264–268.PubMedCrossRefGoogle Scholar
  42. 42.
    Lansdell SJ, Millar NS. Cloning and heterologous expression of Dalpha4, a Drosophila neuronal nicotinic acetylcholine receptor subunit: identification of an alternative exon influencing the efficiency of subunit assembly. Neuropharmacology 2000; 39:2604–2614.PubMedCrossRefGoogle Scholar
  43. 43.
    Lansdell SJ, Millar NS. Dbeta3, an atypical nicotinic acetylcholine receptor subunit from Drosophila: molecular cloning, heterologous expression and coassembly. J Neurochem. 2002; 80:1009–1018.PubMedCrossRefGoogle Scholar
  44. 44.
    Sawruk E, Schloss P, Betz H et al. Heterogeneity of Drosophila nicotinic acetylcholine receptors: SAD, a novel developmentally regulated alpha-subunit. EMBO J. 1990; 9:2671–2677.PubMedGoogle Scholar
  45. 45.
    Sawruk E, Udri C, Betz H et al. SBD, a novel structural subunit of the Drosophila nicotinic acetylcholine receptor, shares its genomic localization with two alpha-subunits. FEBS Lett. 1990; 273:177–181.PubMedCrossRefGoogle Scholar
  46. 46.
    Schulz R, Sawruk E, Mulhardt C et al. D alpha3, a new functional alpha subunit of nicotinic acetylcholine receptors from Drosophila. J Neurochem. 1998; 71:853–862.PubMedCrossRefGoogle Scholar
  47. 47.
    Adams MD, Celniker SE, Holt RA et al. The genome sequence of Drosophila melanogaster. Science 2000; 287:2185–2195.PubMedCrossRefGoogle Scholar
  48. 48.
    Littleton JT, Ganetzky B. Ion channels and synaptic organization: analysis of the Drosophila genome. Neuron 2000; 26:35–43.PubMedCrossRefGoogle Scholar
  49. 49.
    Jones AK, Davis P, Hodgkin J et al. The nicotinic acetylcholine receptor gene family of the nematode Caenorhabditis elegans: an update on nomenclature. Invert Neurosci. 2007; 7:129–131.PubMedCrossRefGoogle Scholar
  50. 50.
    Fayyazuddin A, Zaheer MA, Hiesinger PR et al. The nicotinic acetylcholine receptor Dalpha7 is required for an escape behavior in Drosophila. PLoS Biol. 2006; 4:e63.PubMedCrossRefGoogle Scholar
  51. 51.
    Chamaon K, Smalla KH, Thomas U et al. Nicotinic acetylcholine receptors of Drosophila: three subunits encoded by genomically linked genes can co-assemble into the same receptor complex. J Neurochem. 2002; 80:149–157.PubMedCrossRefGoogle Scholar
  52. 52.
    Buckingham SD, Pym L, Sattelle DB. Oocytes as an expression system for studying receptor/channel targets of drugs and pesticides. Methods Mol Biol. 2006; 322:331–345.PubMedCrossRefGoogle Scholar
  53. 53.
    Towers PR, Sattelle DB. A Drosophila melanogaster cell line (S2) facilitates postgenome functional analysis of receptors and ion channels. Bioessays 2002; 24:1066–1073.PubMedCrossRefGoogle Scholar
  54. 54.
    Ihara M, Matsuda K, Otake M et al. Diverse actions of neonicotinoids on chicken alpha7, alpha4beta2 and Drosophila-chicken SADbeta2 and ALSbeta2 hybrid nicotinic acetylcholine receptors expressed in Xenopus laevis oocytes. Neuropharmacology 2003; 45:133–144.PubMedCrossRefGoogle Scholar
  55. 55.
    Matsuda K, Buckingham SD, Freeman JC et al. Effects of the alpha subunit on imidacloprid sensitivity of recombinant nicotinic acetylcholine receptors. Br J Pharmacol. 1998; 123:518–524.PubMedCrossRefGoogle Scholar
  56. 56.
    Shimomura M, Yokota M, Matsuda K et al. Roles of loop C and the loop B-C interval of the nicotinic receptor alpha subunit in its selective interactions with imidacloprid in insects. Neurosci Lett. 2004; 363:195–198.PubMedCrossRefGoogle Scholar
  57. 57.
    Shimomura M, Yokota M, Ihara M et al. Role in the selectivity of neonicotinoids of insect-specific basic residues in loop D of the nicotinic acetylcholine receptor agonist binding site. Mol Pharmacol. 2006; 70:1255–1263.PubMedCrossRefGoogle Scholar
  58. 58.
    Shimomura M, Yokota M, Okumura M et al. Combinatorial mutations in loops D and F strongly influence responses of the alpha7 nicotinic acetylcholine receptor to imidacloprid. Brain Res. 2003; 991:71–77.PubMedCrossRefGoogle Scholar
  59. 59.
    Shimomura M, Okuda H, Matsuda K et al. Effects of mutations of a glutamine residue in loop D of the alpha7 nicotinic acetylcholine receptor on agonist profiles for neonicotinoid insecticides and related ligands. Br J Pharmacol. 2002; 137:162–169.PubMedCrossRefGoogle Scholar
  60. 60.
    Amiri S, Shimomura M, Vijayan R et al. A role for Leu118 of loop E in agonist binding to the alpha 7 nicotinic acetylcholine receptor. Mol Pharmacol. 2008; 73:1659–1667.PubMedCrossRefGoogle Scholar
  61. 61.
    Ihara M, Shimomura M, Ishida C et al. A hypothesis to account for the selective and diverse actions of neonicotinoid insecticides at their molecular targets, nicotinic acetylcholine receptors: catch and release in hydrogen bond networks. Invert Neurosci. 2007; 7:47–51.PubMedCrossRefGoogle Scholar
  62. 62.
    Ihara M, Okajima T, Yamashita A et al. Crystal structures of Lymnaea stagnalis AChBP in complex with neonicotinoid insecticides imidacloprid and clothianidin. Invert Neurosci. 2008; 8:71–81.PubMedCrossRefGoogle Scholar
  63. 63.
    Tomizawa M, Maltby D, Talley TT et al. Atypical nicotinic agonist bound conformations conferring subtype selectivity. Proc Natl Acad Sci USA. 2008; 105:1728–1732.PubMedCrossRefGoogle Scholar
  64. 64.
    Bret BL. Biological properties of spinosad. Down Earth 1997; 52:6–13.Google Scholar
  65. 65.
    Salgado VL. The modes of action of spinosad and other insect control products. Down Earth 1997; 52:35–43.Google Scholar
  66. 66.
    Salgado VL. Studies on the mode of action of spinosad: insect symptoms and physiological correlates. Pestic Biochem Physiol. 1998; 60:91–102.CrossRefGoogle Scholar
  67. 67.
    Perry T, McKenzie JA, Batterham P. A Dalpha6 knockout strain of Drosophila melanogaster confers a high level of resistance to spinosad. Insect Biochem Mol Biol. 2007; 37:184–188.PubMedCrossRefGoogle Scholar
  68. 68.
    Holt RA, Subramanian GM, Halpern A et al. The genome sequence of the malaria mosquito Anopheles gambiae. Science. 2002; 298:129–149.PubMedCrossRefGoogle Scholar
  69. 69.
    Jones AK, Grauso M, Sattelle DB. The nicotinic acetylcholine receptor gene family of the malaria mosquito, Anopheles gambiae. Genomics. 2005; 85:176–187.PubMedCrossRefGoogle Scholar
  70. 70.
    Jones AK, Raymond-Delpech V, Thany SH et al. The nicotinic acetylcholine receptor gene family of the honey bee, Apis mellifera. Genome Res. 2006; 16:1422–1430.PubMedCrossRefGoogle Scholar
  71. 71.
    The Honeybee Genome Sequencing Consortium. Insights into social insects from the genome of the honeybee Apis mellifera. Nature. 2006; 443:931–949.CrossRefGoogle Scholar
  72. 72.
    Jones AK, Sattelle DB. The cys-loop ligand-gated ion channel gene superfamily of the red flour beetle, Tribolium castaneum. BMC Genomics. 2007; 8:327.PubMedCrossRefGoogle Scholar
  73. 73.
    Richards S, Gibbs RA, Weinstock GM et al. The genome of the model beetle and pest Tribolium castaneum. Nature. 2008; 452:949–955.PubMedCrossRefGoogle Scholar
  74. 74.
    Shao YM, Dong K, Zhang CX. The nicotinic acetylcholine receptor gene family of the silkworm, Bombyx mori. BMC Genomics. 2007; 8:324.PubMedCrossRefGoogle Scholar
  75. 75.
    Xia Q, Zhou Z, Lu C et al. A draft sequence for the genome of the domesticated silkworm (Bombyx mori). Science. 2004; 306:1937–1940.PubMedCrossRefGoogle Scholar
  76. 76.
    Jones AK, Brown LA, Sattelle DB. Insect nicotinic acetylcholine receptor gene families: from genetic model organism to vector, pest and beneficial species. Invert Neurosci. 2007; 7(1):67–73.PubMedCrossRefGoogle Scholar
  77. 77.
    Thany SH, Lenaers G, Raymond-Delpech V et al. Exploring the pharmacological properties of insect nicotinic acetylcholine receptors. Trends Pharmacol Sci. 2007; 28:14–22.PubMedCrossRefGoogle Scholar
  78. 78.
    Mongan NP, Jones AK, Smith GR et al. Novel alpha7-like nicotinic acetylcholine receptor subunits in the nematode Caenorhabditis elegans. Protein Sci. 2002; 11:1162–1171.PubMedCrossRefGoogle Scholar
  79. 79.
    Williamson SM, Walsh TK, Wolstenholme AJ. The cys-loop ligand-gated ion channel gene family of Brugia malayi and Trichinella spiralis: a comparison with Caenorhabditis elegans. Invert Neurosci. 2007; 7:219–226.PubMedCrossRefGoogle Scholar
  80. 80.
    Bentley GN, Jones AK, Oliveros Parra WG et al. ShAR1alpha and ShAR1beta: novel putative nicotinic acetylcholine receptor subunits from the platyhelminth blood fluke Schistosoma. Gene. 2004; 329:27–38.PubMedCrossRefGoogle Scholar
  81. 81.
    Bass C, Lansdell SJ, Millar NS et al. Molecular characterisation of nicotinic acetylcholine receptor subunits from the cat flea, Ctenocephalides felis (Siphonaptera: Pulicidae). Insect Biochem Mol Biol. 2006; 36:86–96.PubMedCrossRefGoogle Scholar
  82. 82.
    Hermsen B, Stetzer E, Thees R et al. Neuronal nicotinic receptors in the locust Locusta migratoria. Cloning and expression. J Biol Chem. 1998; 273:18394–18404.PubMedCrossRefGoogle Scholar
  83. 83.
    Gao JR, Deacutis JM, Scott JG. Characterization of the nicotinic acetylcholine receptor subunit gene Mdalpha2 from the house fly, Musca domestica. Arch Insect Biochem Physiol. 2007; 64:30–42.PubMedCrossRefGoogle Scholar
  84. 84.
    Gao JR, Deacutis JM, Scott JG. The nicotinic acetylcholine receptor subunits Mdalpha5 and Mdbeta3 on autosome 1 of Musca domestica are not involved in spinosad resistance. Insect Mol Biol. 2007; 16:691–701.PubMedCrossRefGoogle Scholar
  85. 85.
    Gao JR, Deacutis JM, Scott JG. The nicotinic acetylcholine receptor subunit Mdalpha6 from Musca domestica is diversified via posttranscriptional modification. Insect Mol Biol. 2007; 16:325–334.PubMedCrossRefGoogle Scholar
  86. 86.
    Huang Y, Williamson MS, Devonshire AL et al. Cloning, heterologous expression and co-assembly of Mpbeta1, a nicotinic acetylcholine receptor subunit from the aphid Myzus persicae. Neurosci Lett. 2000; 284:116–120.PubMedCrossRefGoogle Scholar
  87. 87.
    Sgard F, Fraser SP, Katkowska MJ et al. Cloning and functional characterisation of two novel nicotinic acetylcholine receptor alpha subunits from the insect pest Myzus persicae. J Neurochem. 1998; 71:903–912.PubMedCrossRefGoogle Scholar
  88. 88.
    Liu Z, Williamson MS, Lansdell SJ et al. A nicotinic acetylcholine receptor mutation conferring target-site resistance to imidacloprid in Nilaparvata lugens (brown planthopper). Proc Natl Acad Sci USA. 2005; 102:8420–8425.PubMedCrossRefGoogle Scholar
  89. 89.
    Jones AK, Marshall J, Blake AD et al. Sgbeta1, a novel locust (Schistocerca gregaria) non-alpha nicotinic acetylcholine receptor-like subunit with homology to the Drosophila melanogaster Dbeta1 subunit. Invert Neurosci. 2005; 5:147–155.PubMedCrossRefGoogle Scholar
  90. 90.
    Marshall J, Buckingham SD, Shingai R et al. Sequence and functional expression of a single alpha subunit of an insect nicotinic acetylcholine receptor. EMBO J. 1990; 9:4391–4398.PubMedGoogle Scholar
  91. 91.
    Jensen ML, Schousboe A, Ahring PK. Charge selectivity of the Cys-loop family of ligand-gated ion channels. J Neurochem. 2005; 92:217–225.PubMedCrossRefGoogle Scholar
  92. 92.
    Jin Y, Tian N, Cao J et al. RNA editing and alternative splicing of the insect nAChR subunit alpha6 transcript: evolutionary conservation, divergence and regulation. BMC Evol Biol. 2007; 7:98.PubMedCrossRefGoogle Scholar
  93. 93.
    Revah F, Bertrand D, Galzi JL et al. Mutations in the channel domain alter desensitization of a neuronal nicotinic receptor. Nature 1991; 353:846–849.PubMedCrossRefGoogle Scholar
  94. 94.
    Borges LS, Ferns M. Agrin-induced phosphorylation of the acetylcholine receptor regulates cytoskeletal anchoring and clustering. J Cell Biol. 2001; 153:1–12.PubMedCrossRefGoogle Scholar
  95. 95.
    Hopfield JF, Tank DW, Greengard P et al. Functional modulation of the nicotinic acetylcholine receptor by tyrosine phosphorylation. Nature. 1988; 336:677–680.PubMedCrossRefGoogle Scholar
  96. 96.
    Sattelle DB, Jones AK, Sattelle BM et al. Edit, cut and paste in the nicotinic acetylcholine receptor gene family of Drosophila melanogaster. Bioessays. 2005; 27:366–376.PubMedCrossRefGoogle Scholar
  97. 97.
    Smit AB, Brejc K, Syed N et al. Structure and function of AChBP, homologue of the ligand-binding domain of the nicotinic acetylcholine receptor. Ann N Y Acad Sci. 2003; 998:81–92.PubMedCrossRefGoogle Scholar
  98. 98.
    Saragoza PA, Modir JG, Goel N et al. Identification of an alternatively processed nicotinic receptor alpha7 subunit RNA in mouse brain. Brain Res Mol Brain Res 2003; 117:15–26.PubMedCrossRefGoogle Scholar
  99. 99.
    Seeburg PH. A-to-I editing: new and old sites, functions and speculations. Neuron 2002; 35:17–20.PubMedCrossRefGoogle Scholar
  100. 100.
    Hoopengardner B, Bhalla T, Staber C et al. Nervous system targets of RNA editing identified by comparative genomics. Science 2003; 301:832–836.PubMedCrossRefGoogle Scholar
  101. 101.
    Tonkin LA, Saccomanno L, Morse DP et al. RNA editing by ADARs is important for normal behavior in Caenorhabditis elegans. EMBO J 2002; 21:6025–6035.PubMedCrossRefGoogle Scholar
  102. 102.
    Palladino MJ, Keegan LP, O’Connell MA et al. A-to-I pre-mRNA editing in Drosophila is primarily involved in adult nervous system function and integrity. Cell 2000; 102:437–449.PubMedCrossRefGoogle Scholar
  103. 103.
    Higuchi M, Maas S, Single FN et al. Point mutation in an AMPA receptor gene rescues lethality in mice deficient in the RNA-editing enzyme ADAR2. Nature 2000; 406:78–81.PubMedCrossRefGoogle Scholar
  104. 104.
    Guzman GR, Santiago J, Ricardo A et al. Tryptophan scanning mutagenesis in the alphaM3 transmembrane domain of the Torpedo californica acetylcholine receptor: functional and structural implications. Biochemistry 2003; 42:12243–12250.PubMedCrossRefGoogle Scholar
  105. 105.
    Tamamizu S, Lee Y, Hung B et al. Alteration in ion channel function of mouse nicotinic acetylcholine receptor by mutations in the M4 transmembrane domain. J Membr Biol 1999; 170:157–164.PubMedCrossRefGoogle Scholar
  106. 106.
    Gehle VM, Walcott EC, Nishizaki T et al. N-glycosylation at the conserved sites ensures the expression of properly folded functional ACh receptors. Brain Res Mol Brain Res 1997; 45:219–229.PubMedCrossRefGoogle Scholar
  107. 107.
    Nishizaki T. N-glycosylation sites on the nicotinic ACh receptor subunits regulate receptor channel desensitization and conductance. Brain Res Mol Brain Res 2003; 114:172–176.PubMedCrossRefGoogle Scholar
  108. 108.
    Yang Y, Lv J, Gui B et al. A-to-I RNA editing alters less-conserved residues of highly conserved coding regions: implications for dual functions in evolution. RNA 2008; 14:1516–1525.PubMedCrossRefGoogle Scholar
  109. 109.
    Clark AG, Eisen MB, Smith DR et al. Evolution of genes and genomes on the Drosophila phylogeny. Nature 2007; 450:203–218.PubMedCrossRefGoogle Scholar
  110. 110.
    Nene V, Wortman JR, Lawson D et al. Genome sequence of Aedes aegypti, a major arbovirus vector. Science 2007; 316:1718–1723.PubMedCrossRefGoogle Scholar
  111. 111.
    Pittendrigh BR, Clark JM, Johnston JS et al. Sequencing of a new target genome: the Pediculus humanus humanus (Phthiraptera: Pediculidae) genome project. J Med Entomol 2006; 43:1103–1111.PubMedCrossRefGoogle Scholar
  112. 112.
    Harrow ID, Hue B, Pelhate M et al. Cockroach giant interneurones stained by cobalt-backfilling of dissected axons. J Exp Biol 1980; 84:341–343.PubMedGoogle Scholar
  113. 113.
    Lane NJ, Sattelle DB, Hufnagel LA. Pre-and postsynaptic structures in insect CNS: intramembranous features and sites of alpha-bungarotoxin binding. Tissue Cell 1983; 15:921–937.PubMedCrossRefGoogle Scholar
  114. 114.
    Lummis SC, Sattelle DB. Binding of N-[propionyl-3H]propionylated alpha-bungarotoxin and L-[benzilic-4,4′-3H] quinuclidinyl benzilate to CNS extracts of the cockroach Periplaneta americana. Comp Biochem Physiol C 1985; 80:75–83.PubMedCrossRefGoogle Scholar
  115. 115.
    Fire A, Xu S, Montgomery MK et al. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 1998; 391:806–811.PubMedCrossRefGoogle Scholar
  116. 116.
    Kamath RS, Fraser AG, Dong Y et al. Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 2003; 421:231–237.PubMedCrossRefGoogle Scholar
  117. 117.
    Sepp KJ, Hong P, Lizarraga SB et al. Identification of neural outgrowth genes using genome-wide RNAi. PLoS Genet 2008; 4:e1000111.PubMedCrossRefGoogle Scholar
  118. 118.
    Thany SH, Gauthier M. Nicotine injected into the antennal lobes induces a rapid modulation of sucrose threshold and improves short-term memory in the honeybee Apis mellifera. Brain Res 2005; 1039:216–219.PubMedCrossRefGoogle Scholar
  119. 119.
    Lozano VC, Armengaud C, Gauthier M. Memory impairment induced by cholinergic antagonists injected into the mushroom bodies of the honeybee. J Comp Physiol [A] 2001; 187:249–254.CrossRefGoogle Scholar
  120. 120.
    Lozano VC, Bonnard E, Gauthier M et al. Mecamylamine-induced impairment of acquisition and retrieval of olfactory conditioning in the honeybee. Behav Brain Res 1996; 81:215–222.PubMedCrossRefGoogle Scholar
  121. 121.
    Dacher M, Lagarrigue A, Gauthier M. Antennal tactile learning in the honeybee: effect of nicotinic antagonists on memory dynamics. Neuroscience 2005; 130:37–50.PubMedCrossRefGoogle Scholar
  122. 122.
    Hogg RC, Raggenbass M, Bertrand D. Nicotinic acetylcholine receptors: from structure to brain function. Rev Physiol Biochem Pharmacol 2003; 147:1–46.PubMedCrossRefGoogle Scholar
  123. 123.
    Rocher A, Marchand-Geneste N. Homology modelling of the Apis mellifera nicotinic acetylcholine receptor (nAChR) and docking of imidacloprid and fipronil insecticides and their metabolites. SAR QSAR Environ Res 2008; 19:245–261.PubMedCrossRefGoogle Scholar
  124. 124.
    Altschul SF, Gish W, Miller W et al. Basic local alignment search tool. J Mol Biol 1990; 215:403–410.PubMedGoogle Scholar
  125. 125.
    Kondrashov FA, Koonin EV. Origin of alternative splicing by tandem exon duplication. Hum Mol Genet 2001; 10:2661–2669.PubMedCrossRefGoogle Scholar

Copyright information

© Landes Bioscience and Springer Science+Business Media 2010

Authors and Affiliations

  1. 1.MRC Functional Genomics Unit, Department of Physiology, Anatomy and GeneticsUniversity of OxfordOxfordUK

Personalised recommendations