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Electrophysiological Studies and Pharmacological Properties of Insect Native Nicotinic Acetylcholine Receptors

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

Abstract

The existence of several nicotinic acetylcholine receptor genes in insects suggests that many nicotinic receptor subtypes are present, but the identification and characterization of these subtypes in native neurons has been limited. Their pharmacological properties came from electrophysiological studies in which variations in the sensitivity of insect neurons were correlated with time course, current amplitudes, desensitization rates occurring in varying proportions in different cells. Thus pressure application of agonists on cultured cells induced inward currents showing that acetylcholine and nicotine were partial agonists of some cells with a lower efficacy while they were full agonists in other neurons. The variation in kinetics appeared to be due to differential expression of distinct nicotinic receptor subtypes as corroborated by the blocking activity induced by antagonists. In fact, the alpha-bungarotoxin-sensitive nicotinic receptor subtypes described as homomeric could be also heteromeric receptors. Interestingly, some receptors mediating nicotinic responses have been termed ‘mixed’ receptors because they were blocked by a range of nicotinic and muscarinic antagonists.

Following electrophysiological studies, it has been also demonstrated that insect nicotinic receptors were modulated by Ca2+ pathways. Ca2+ permeability through insect nicotinic receptors, voltage-gated Ca2+ channels or released from intracellular stores represents an important indication of insect native nicotinic acetylcholine receptor modulation. The Ca2+ flow may trigger a variety of cytosolic Ca2+ pathways underlying many cellular processes such Calmodulin kinase, PKA and PKC. Most of the studies suggested that the effect of phosphorylation mechanism was dependent on the receptor subtype.

Keywords

Nicotinic Receptor Nicotinic Acetylcholine Receptor Mushroom Body Antennal Lobe Kenyon Cell 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. 1.
    Thany SH, Lenaers G, Raymond-Delpech V et al. Exploring the pharmacological properties of insect nicotinic acetylcholine receptors. Trends Pharmacol Sci 2007; 28(1):14–22.PubMedCrossRefGoogle Scholar
  2. 2.
    Goldberg F, Grunewald B, Rosenboom H et al. Nicotinic acetylcholine currents of cultured Kenyon cells from the mushroom bodies of the honey bee Apis mellifera. J Physiol 1999; 514(Pt 3):759–68.PubMedCrossRefGoogle Scholar
  3. 3.
    Deglise P, Grunewald B, Gauthier M. The insecticide imidacloprid is a partial agonist of the nicotinic receptor of honeybee Kenyon cells. Neurosci Lett 2002; 321(1–2):13–6.PubMedCrossRefGoogle Scholar
  4. 4.
    Wustenberg DG, Grunewald B. Pharmacology of the neuronal nicotinic acetylcholine receptor of cultured kenyon cells of the honeybee, Apis mellifera. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 2004; 190(10):807–21.PubMedCrossRefGoogle Scholar
  5. 5.
    Barbara GS, Grunewald B, Paute S et al. Study of nicotinic acetylcholine receptors on cultured antennal lobe neurones from adult honeybee brains. Invert Neurosci 2008; 8(1):19–29.PubMedCrossRefGoogle Scholar
  6. 6.
    Lapied B, Le Corronc H, Hue B. Sensitive nicotinic and mixed nicotinic-muscarinic receptors in insect neurosecretory cells. Brain Res 1990; 533(1):132–6.PubMedCrossRefGoogle Scholar
  7. 7.
    Courjaret R, Lapied B. Complex intracellular messenger pathways regulate one type of neuronal alpha-bungarotoxin-resistant nicotinic acetylcholine receptors expressed in insect neurosecretory cells (dorsal unpaired median neurons). Mol Pharmacol 2001; 60(1):80–91.PubMedGoogle Scholar
  8. 8.
    Courjaret R, Grolleau F, Lapied B. Two distinct calcium-sensitive and-insensitive pkc up-and down-regulate an alpha-bungarotoxin-resistant nAChR1 in insect neurosecretory cells (DUM neurons). Eur J Neurosci 2003; 17(10):2023–34.PubMedCrossRefGoogle Scholar
  9. 9.
    Thany SH, Courjaret R, Lapied B. Effect of calcium on nicotine-induced current expressed by an atypical alpha-bungarotoxin-insensitive nAChR2. Neurosci Lett 2008; 438(3):317–21.PubMedCrossRefGoogle Scholar
  10. 10.
    Thany SH. Agonist actions of clothianidin on synaptic and extrasynaptic nicotinic acetylcholine receptors expressed on cockroach sixth abdominal ganglion. Neurotoxicology 2009 (In press).Google Scholar
  11. 11.
    Cayre M, Buckingham SD, Yagodin S et al. Cultured insect mushroom body neurons express functional receptors for acetylcholine, gaba, glutamate, octopamine and dopamine. J Neurophysiol 1999; 81(1):1–14.PubMedGoogle Scholar
  12. 12.
    Su H, O’Dowd DK. Fast synaptic currents in drosophila mushroom body Kenyon cells are mediated by alpha-bungarotoxin-sensitive nicotinic acetylcholine receptors and picrotoxin-sensitive gaba receptors. J Neurosci 2003; 23(27):9246–53.PubMedGoogle Scholar
  13. 13.
    Rohrbough J, Broadie K. Electrophysiological analysis of synaptic transmission in central neurons of drosophila larvae. J Neurophysiol 2002; 88(2):847–60.PubMedGoogle Scholar
  14. 14.
    Wegener C, Hamasaka Y, Nassel DR. Acetylcholine increases intracellular Ca2+ via nicotinic receptors in cultured pdf-containing clock neurons of drosophila. J Neurophysiol 2004; 91(2):912–23.PubMedCrossRefGoogle Scholar
  15. 15.
    Hermsen B, Stetzer E, Thees R et al. Neuronal nicotinic receptors in the locust Locusta migratoria. Cloning and expression. J Biol Chem 1998; 273(29):18394–404.PubMedCrossRefGoogle Scholar
  16. 16.
    Guez D, Belzunces LP, Maleszka R. Effects of imidacloprid metabolites on habituation in honeybees suggest the existence of two subtypes of nicotinic receptors differentially expressed during adult development. Pharmacol Biochem Behav 2003; 75(1):217–22.PubMedCrossRefGoogle Scholar
  17. 17.
    Dacher M, Lagarrigue A, Gauthier M. Antennal tactile learning in the honeybee: Effect of nicotinic antagonists on memory dynamics. Neuroscience 2005; 130(1):37–50.PubMedCrossRefGoogle Scholar
  18. 18.
    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(3):e63.PubMedCrossRefGoogle Scholar
  19. 19.
    Gauthier M, Dacher M, Thany SH et al. Involvement of alpha-bungarotoxin-sensitive nicotinic receptors in long-term memory formation in the honeybee (Apis mellifera). Neurobiol Learn Mem 2006; 86(2):164–74.PubMedCrossRefGoogle Scholar
  20. 20.
    Thany SH, Crozatier M, Raymond-Delpech V et al. Apisalpha2, apisalpha7-1 and apisalpha7-2: Three new neuronal nicotinic acetylcholine receptor alpha-subunits in the honeybee brain. Gene 2005; 344:125–32.PubMedCrossRefGoogle Scholar
  21. 21.
    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
  22. 22.
    Chamaon K, Schulz R, Smalla KH et al. Neuronal nicotinic acetylcholine receptors of Drosophila melanogaster: The alpha-subunit dalpha3 and the beta-type subunit ard co-assemble within the same receptor complex. FEBS Lett 2000; 482(3):189–92.PubMedCrossRefGoogle Scholar
  23. 23.
    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(1):149–57.PubMedCrossRefGoogle Scholar
  24. 24.
    Vermehren A, Qazi S, Trimmer BA. The nicotinic alpha subunit mara1 is necessary for cholinergic evoked calcium transients in manduca neurons. Neurosci Lett 2001; 313(3):113–6.PubMedCrossRefGoogle Scholar
  25. 25.
    Salgado VL, Saar R. Desensitizing and nondesensitizing subtypes of alpha-bungarotoxin-sensitive nicotinic acetylcholine receptors in cockroach neurons. J Insect Physiol 2004; 50(10):867–79.PubMedCrossRefGoogle Scholar
  26. 26.
    Nauen R, Ebbinghaus-Kintscher U, Schmuck R. Toxicity and nicotinic acetylcholine receptor interaction of imidacloprid and its metabolites in Apis mellifera (hymenoptera: Apidae). Pest Manag Sci 2001; 57(7):577–86.PubMedCrossRefGoogle Scholar
  27. 27.
    Barbara GS, Zube C, Rybak J et al. Acetylcholine, gaba and glutamate induce ionic currents in cultured antennal lobe neurons of the honeybee, Apis mellifera. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 2005; 191(9):823–36.PubMedCrossRefGoogle Scholar
  28. 28.
    David JA, Pitman RM. The pharmacology of alpha-bungarotoxin-resistant acetylcholine rececptors on an identified cockroach motoneurone. J Comp Physiol [A] 1993; 172:359–368.CrossRefGoogle Scholar
  29. 29.
    Hancox JC, Pitman RM. Plateau potentials drive axonal impulse burst in insect motoneurons. Proc R Soc Lond B 1991; 244:33–38.CrossRefGoogle Scholar
  30. 30.
    Hancox JC, Pitman RM. A time-dependent excitability change in the soma of an identified insect motoneuron. J Exp Biol 1992; 162:251–263.Google Scholar
  31. 31.
    Hancox JC, Pitman RM. Plateau potentials in an insect motoneuron can be driven by synaptic stimulation. J Exp Biol 1993; 176:307–310.Google Scholar
  32. 32.
    Mills JD, Pitman RM. Electrical properties of a cockroach motor neuron soma depend on different characteristics of individual ca components. J Neurophysiol 1997; 78(5):2455–66.PubMedGoogle Scholar
  33. 33.
    Mills JD, Pitman RM. Contribution of potassium conductances to a time-dependent transition in electrical properties of a cockroach motoneuron soma. J Neurophysiol 1999; 81(5):2253–66.PubMedGoogle Scholar
  34. 34.
    Benson JA. Electrophysiological pharmacology of the nicotinic and muscarinic cholinergic responses of isolated neuronal somata from locust thoracic ganglia. J Exp Biol 1992; 170:203–233.Google Scholar
  35. 35.
    Elgoyhen AB, Johnson DS, Boulter J et al. Alpha 9: An acetylcholine receptor with novel pharmacological properties expressed in rat cochlear hair cells. Cell 1994; 79(4):705–15.PubMedCrossRefGoogle Scholar
  36. 36.
    Verbitsky M, Rothlin CV, Katz E et al. Mixed nicotinic-muscarinic properties of the alpha9 nicotinic cholinergic receptor. Neuropharmacology 2000; 39(13):2515–24.PubMedCrossRefGoogle Scholar
  37. 37.
    Elgoyhen AB, Vetter DE, Katz E et al. Alpha10: A determinant of nicotinic cholinergic receptor function in mammalian vestibular and cochlear mechanosensory hair cells. Proc Natl Acad Sci USA 2001; 98(6):3501–6.PubMedCrossRefGoogle Scholar
  38. 38.
    Hiel H, Elgoyhen AB, Drescher DG et al. Expression of nicotinic acetylcholine receptor mrna in the adult rat peripheral vestibular system. Brain Res 1996; 738(2):347–52.PubMedCrossRefGoogle Scholar
  39. 39.
    Morley BJ, Li HS, Hiel H et al. Identification of the subunits of the nicotinic cholinergic receptors in the rat cochlea using RT-PCR and in situ hybridization. Brain Res Mol Brain Res 1998; 53(1–2):78–87.PubMedCrossRefGoogle Scholar
  40. 40.
    Changeux JP, Bertrand D, Corringer PJ et al. Brain nicotinic receptors: Structure and regulation, role in learning and reinforcement. Brain Res Brain Res Rev 1998; 26(2–3):198–216.PubMedCrossRefGoogle Scholar
  41. 41.
    Paterson D, Nordberg A. Neuronal nicotinic receptors in the human brain. Prog Neurobiol 2000; 61(1):75–111.PubMedCrossRefGoogle Scholar
  42. 42.
    Oertner TG, Single S, Borst A. Separation of voltage-and ligand-gated calcium influx in locust neurons by optical imaging. Neurosci Lett 1999; 274(2):95–8.PubMedCrossRefGoogle Scholar
  43. 43.
    Fucile S, Sucapane A, Eusebi F. Ca2+ permeability through rat cloned alpha9-containing nicotinic acetylcholine receptors. Cell Calcium 2006; 39(4):349–55.PubMedCrossRefGoogle Scholar
  44. 44.
    Dajas-Bailador F, Wonnacott S. Nicotinic acetylcholine receptors and the regulation of neuronal signalling. Trends Pharmacol Sci 2004; 25(6):317–24.PubMedCrossRefGoogle Scholar
  45. 45.
    Vermehren A, Trimmer BA. Expression and function of two nicotinic subunits in insect neurons. J Neurobiol 2005; 62(3):289–98.PubMedCrossRefGoogle Scholar
  46. 46.
    Grolleau F, Lapied B, Buckingham SD et al. Nicotine increases [Ca2+]i and regulates electrical activity in insect neurosecretory cells (DUM neurons) via an acetylcholine receptor with ‘mixed’ nicotinic-muscarinic pharmacology. Neurosci Lett 1996; 220(2):142–6.PubMedCrossRefGoogle Scholar
  47. 47.
    Heine M, Wicher D. Ca2+ resting current and Ca2+-induced Ca2+ release in insect neurosecretory neurons. Neuroreport 1998; 9(14):3309–14.PubMedCrossRefGoogle Scholar
  48. 48.
    Wicher D, Messutat S, Lavialle C et al. A new regulation of noncapacitative calcium entry in insect pacemaker neurosecretory neurons. Involvement of arachidonic acid, no-guanylyl cyclase/cGMP and cAMP. J Biol Chem 2004; 279(48):50410–9.PubMedCrossRefGoogle Scholar
  49. 49.
    Berridge MJ, Lipp P, Bootman MD. The versatility and universality of calcium signalling. Nat Rev Mol Cell Biol 2000; 1(1):11–21.PubMedCrossRefGoogle Scholar
  50. 50.
    Newton AC. Protein kinase C. Seeing two domains. Curr Biol 1995; 5(9):973–6.PubMedCrossRefGoogle Scholar
  51. 51.
    Newton AC. Protein kinase C: Structure, function and regulation. J Biol Chem 1995; 270(48):28495–8.PubMedGoogle Scholar
  52. 52.
    Newton AC. Protein kinase C: Structural and spatial regulation by phosphorylation, cofactors and macromolecular interactions. Chem Rev 2001; 101(8):2353–64.PubMedCrossRefGoogle Scholar
  53. 53.
    Hou J, Kuromi H, Fukasawa Y et al. Repetitive exposures to nicotine induce a hyper-responsiveness via the cAMP/PKA/CREB signal pathway in drosophila. J Neurobiol 2004; 60(2):249–61.PubMedCrossRefGoogle Scholar
  54. 54.
    Dymond GR, Evans PD. Biogenic amines in the nervous system of the cockroach, Periplaneta americana: Association of octopamine with mushroom bodies and dorsal unpaired median (DUM) neurones. Insect Biochem 1979; 9:535–545.CrossRefGoogle Scholar
  55. 55.
    Sloley BD, Owen MD. The effects of reserpine on amine concentrations in the nervous system of the cockroach (Periplaneta americana). Insect Biochem 1982; 12:469–476.CrossRefGoogle Scholar
  56. 56.
    Shafi N, Midgley JM, Matson DG et al. Analysis of biogenic-amines in the brain of the american cockroach (Periplaneta americana) by gas-chromatography negative-ion chemical ionization mass-spectrometry. J Chromatog Biomed Applications 1989; 490:9–19.CrossRefGoogle Scholar
  57. 57.
    Butt SJ, Pitman RM. Modulation by 5-hydroxytryptamine of nicotinic acetylcholine responses recorded from an identified cockroach (Periplaneta americana) motoneuron. Eur J Neurosci 2002; 15(3):429–38.PubMedCrossRefGoogle Scholar
  58. 58.
    Butt SJ, Pitman RM. Indirect phosphorylation-dependent modulation of postsynaptic nicotinic acetylcholine responses by 5-hydroxytryptamine. Eur J Neurosci 2005; 21(5):1181–8.PubMedCrossRefGoogle Scholar
  59. 59.
    Butt SJB, Pitman RM. Modulation by monoamines of ACh responses recorded from an identified cockroach (Periplaneta americana) motoneurone. J Physiol (London) 1998; 513:102P.Google Scholar
  60. 60.
    Jackson C, Bermudez I, Beadle DJ. Pharmacological properties of nicotinic acetylcholine receptors in isolated locusta migratoria neurones. Microsc Res Tech 2002; 56(4):249–55.PubMedCrossRefGoogle Scholar
  61. 61.
    Benson JA. Bicuculline blocks the response to acetylcholine and nicotine but not to muscarinie or gaba in isolated insect neuronal somata. Brain Res 1988; 458:45–71.CrossRefGoogle Scholar
  62. 62.
    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(13):4391–8.PubMedGoogle Scholar
  63. 63.
    Buckingham SD, Hue B, Sattelle DB. Actions of bicuculline on cell body and neuropilar membranes of identified insect neurones. J Exp Biol 1994; 186:235–44.PubMedGoogle Scholar
  64. 64.
    Akasu T, Koketsu K. 5-hydroxytryptamine decrease the sensitivity of nicotinic acetylcholine receptors in bull-frog sympathetic ganglion. J Physiol 1986; 380:93–109.PubMedGoogle Scholar
  65. 65.
    Grassi F, Polenzani L, Mileo AM et al. Blockage of nicotinic acetylcholine receptors by 5-hydroxytryptamine. J Neurosci Res 1993; 34(5):562–70.PubMedCrossRefGoogle Scholar
  66. 66.
    Schrattenholz A, Pereira EF, Roth U et al. Agonist responses of neuronal nicotinic acetylcholine receptors are potentiated by a novel class of allosterically acting ligands. Mol Pharmacol 1996; 49(1):1–6.PubMedGoogle Scholar
  67. 67.
    Garcia-Colunga J, Miledi R. Blockage of mouse muscle nicotinic receptors by serotonergic compounds. Exp Physiol 1999; 84(5):847–64.PubMedCrossRefGoogle Scholar
  68. 68.
    Nakazawa K, Ohno Y. Block by 5-hydroxytryptamine and apomorphine of recombinant human neuronal nicotinic receptors. Eur J Pharmacol 1999; 374(2):293–9.PubMedCrossRefGoogle Scholar
  69. 69.
    Blanton MP, McCardy EA, Fryer JD et al. 5-hydroxytryptamine interaction with the nicotinic acetylcholine receptor. Eur J Pharmacol 2000; 389(2–3):155–63.PubMedCrossRefGoogle Scholar
  70. 70.
    Inagaki S, Kaku K, Dunlap DY et al. Sequences of cDNAs encoding calmodulin and partial structures of calmodulin kinase and a calcium channel of kdr-resistant and-susceptible german cockroaches, Blattella germanica. Comp Biochem Physiol C Pharmacol Toxicol Endocrinol 1998; 120(2):225–33.PubMedCrossRefGoogle Scholar
  71. 71.
    Kamikouchi A, Takeuchi H, Sawata M et al. Concentrated expression of Ca2+/calmodulin-dependent protein kinase II and protein kinase C in the mushroom bodies of the brain of the honeybee Apis mellifera. J Comp Neurol 2000; 417(4):501–10.PubMedCrossRefGoogle Scholar
  72. 72.
    Charpantier E, Wiesner A, Huh KH et al. Alpha7 neuronal nicotinic acetylcholine receptors are negatively regulated by tyrosine phosphorylation and SRC-family kinases. J Neurosci 2005; 25(43):9836–49.PubMedCrossRefGoogle Scholar
  73. 73.
    Marszalec W, Yeh JZ, Narahashi T. Desensitization of nicotine acetylcholine receptors: Modulation by kinase activation and phosphatase inhibition. Eur J Pharmacol 2005; 514(2–3):83–90.PubMedGoogle Scholar
  74. 74.
    Kuo YP, Xu L, Eaton JB et al. Roles for nicotinic acetylcholine receptor subunit large cytoplasmic loop sequences in receptor expression and function. J Pharmacol Exp Ther 2005; 314(1):455–66.PubMedCrossRefGoogle Scholar
  75. 75.
    Bertrand D, Galzi JL, Devillers-Thiéry A et al. Mutations at two distinct sites within the channel domain M2 alter calcium permeability of neuronal alpha7 nicotinic receptor. Proc Natl Acad Sci USA 1993; 90(1):6971–6975PubMedCrossRefGoogle Scholar

Copyright information

© Landes Bioscience and Springer Science+Business Media 2010

Authors and Affiliations

  • Steeve Hervé Thany
    • 1
  1. 1.Laboratoire Récepteurs et Canaux Ioniques Membranaires (RCIM), UPRES EA 2647/USC INRA 2023, IFR 149 QUASAVUniversité d’Angers, UFR de SciencesAngersFrance

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