Abstract
We investigated here the role of transmissions mediated by GABA and glutamate-gated chloride channels (GluCls) in olfactory learning and memory in honeybees, both of these channels being a target for fipronil. To do so, we combined olfactory conditioning with injections of either the GABA- and glutamate-interfering fipronil alone, or in combination with the blocker of glutamate transporter l-trans-Pyrrolidine-2,4-Dicarboxylicacid (l -trans-PDC), or the GABA analog Trans-4-Aminocrotonic Acid (TACA). Our results show that a low dose of fipronil (0.1 ng/bee) impaired olfactory memory, while a higher dose (0.5 ng/bee) had no effect. The detrimental effect induced by the low dose of fipronil was rescued by the coinjection of l-trans-PDC but was rather increased by the coinjection of TACA. Moreover, using whole-cell patch-clamp recordings, we observed that l-trans-PDC reduced glutamate-induced chloride currents in antennal lobe cells. We interpret these results as reflecting the involvement of both GluCl and GABA receptors in the impairment of olfactory memory induced by fipronil.
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References
Aliouane Y, El Hassani AK, Gary V, Armengaud C, Lambin M, Gauthier M (2009) Subchronic exposure of honeybees to sublethal doses of pesticides: effects on behavior. Environ Toxicol Chem 28:113–122
Aydar E, Beadle DJ (1999) The pharmacological profile of GABA receptors on cultured insect neurones. J Insect Physiol 45:213–219
Balanca G, de Visscher M (1997) Impacts on non-target insects of a new insecticide compound used against the desert locust [Schistocerca gregaria (Forskal 1775)]. Arch Environ Contam Toxicol 32:58–62
Barbara GS, Zube C, Rybak J, Gauthier M, Grünewald B (2005) Acetylcholine, GABA and glutamate induce ionic currents in cultured antennal lobe neurons of the honeybee, Apis mellifera. J Comp Physiol A 191:823–836
Bitterman ME, Menzel R, Fietz A, Schäfer S (1983) Classical conditioning of proboscis extension in honeybees (Apis mellifera). J Comp Psychol 97:107–119
Bloomquist JR (2003) Chloride channels as tools for developing selective insecticides. Arch Insect Biochem Physiol 54:145–156
Buckingham SD, Sattelle DB (2005) GABA receptors of Insects. In: Gilbert LI, Iatrou K, Gill SS (eds) Comprehensive molecular insect science pharmacology. Elsevier Press, Oxford United Kingdom, pp 107–142
Cole LM, Nicholson RA, Casida JE (1993) Action of phenylpyrazole insecticides at the GABA gated chloride channel. Pestic Biochem Physiol 46:47–54
Decourtye A (2002) Etude de l’impact des produits phytopharmaceutiques sur la survie et l’apprentissage associatif chez l’abeille domestiques (Apis mellifera). PhD Thesis, University of Paris XI Orsay
Decourtye A, Devillers J, Genecque E, Le Menach K, Budzinski H, Cluzeau S, Pham-Délègue MH (2005) Comparative sublethal toxicity of nine pesticides on olfactory learning performances of the honeybee Apis mellifera. Arch Environ Contam Toxicol 48:242–250
El Hassani AK, Dacher M, Gauthier M, Armengaud C (2005) Effects of sublethal doses of fipronil on the behavior of the honeybee (Apis mellifera). Pharmacol Biochem Behav 82:30–39
El Hassani AK, Giurfa M, Gauthier M, Armengaud C (2008) Inhibitory neurotransmission and olfactory memory in honeybee. Neurobiol Learn Mem 90:589–595
Fairman WA, Vandenberg RJ, Arriza JL, Kavanaugh MP, Amara SG (1995) An excitatory amino-acid transporter with properties of a ligand-gated chloride channel. Nature 375:599–603
Guerrieri F, Schubert M, Sandoz J-C, Giurfa M (2005) Perceptual and neural olfactory similarity in honeybees. PLoS Biol 3:e60
Hamill OP, Marty A, Neher E, Sakmann B, Sigworth FJ (1981) Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch 391:85–100
Horoszok L, Raymond V, Sattelle DB, Wolstenholme AJ (2001) GLC-3: a novel fipronil and BIDN-sensitive, but picrotoxin-insensitive, l-glutamate-gated chloride channel subunit from Caenorhabditis elegans. Br J Pharmacol 132:1247–1254
Hosie AM, Sattelle DB (1996) Agonist pharmacology of two Drosophila GABA receptor splice variants. Br J Pharmacol 119:1577–1585
Hosler J, Buxton K, Smith B (2000) Impairment of olfactory discrimination by blockade of GABA and nitric oxide activity in the honeybee antennal lobes. Behav Neurosci 114:514–525
Ikeda T, Zhao X, Kono Y, Yeh J, Narahashi T (2003) Fipronil modulation of glutamate-induced chloride currents in cockroach thoracic ganglion neurons. Neurotoxicology 24:807–815
Janssen D, Derst C, Buckinx R, Van den Eynden J, Rigo JM, Van Kerkhove E (2007) Dorsal unpaired median neurons of Locusta migratoria express ivermectin- and fipronil-sensitive glutamate-gated chloride channels. J Neurophysiol 97:2642–2650
Kehoe JS, Vulfius C (2000) Independence of and interactions between GABA, glutamate, and acetylcholine-activated Cl conductances in Aplysia neurons. J Neurosci 20:8585–8596
Kreissl S, Bicker G (1992) Dissociated neurons of the pupal honeybee brain in cell culture. J Neurocytol 21:545–556
Kullmann DM, Lamsa KP (2007) Long-term synaptic plasticity in hippocampal interneurons. Nat Rev Neurosci 8:687–699
Liu X, William C, Krause L, Davis RL (2007) GABAA receptor RDL inhibits Drosophila olfactory associative learning. Neuron 56:1090–1102
Locatelli F, Bundrock G, Müller U (2005) Focal and temporal release of glutamate in the mushroom bodies improves olfactory memory in Apis mellifera. J Neurosci 25:11614–11618
Lozano VC, Bonnard E, Gauthier M, Richard D (1996) Mecamylamine-induced impairment of acquisition and retrieval of olfactory conditioning in the honeybee. Behav Brain Res 81:215–222
Maleszka R, Helliwell P, Kucharski R (2000) Pharmacological interference with glutamate re-uptake impairs long-term memory in the honeybee, Apis mellifera. Behav Brain Res 115:49–53
Mwilaria EK, Ghatak C, Daly KC (2008) Disruption of GABAA in the insect antennal lobe generally increases odor detection and discrimination thresholds. Chem Senses 33:267–281
Narahashi T, Zhao X, Ikeda T, Nagata K, Yeh JZ (2007) Differential actions of insecticides on target sites: basis for selective toxicity. Hum Exp Toxicol 26:361–366
Nässel DR (1999) Histamine in the brain of insects: a review. Microsc Res Tech 44:121–136
Okada R, Rybak J, Manz G, Menzel R (2007) Learning-related plasticity in PE1 and other mushroom body-extrinsic neurons in the honeybee brain. J Neurosci 27:11736–11747
Priestley CM, Williamson EM, Wafford KA, Sattelle DB (2003) Thymol, a constituent of thyme essential oil, is a positive allosteric modulator of human GABA(A) receptors and homo-oligomeric GABA receptor from Drosophila melanogaster. Br J Pharmacol 140:1363–1372
Raymond V, Sattelle DB (2002) Novel animal-health drug targets from ligand-gated chloride channels. Nat Rev Drug Discov 1:427–436
Raymond V, Sattelle DB, Lapied B (2000) Co-existence in DUM neurones of two GluCl channels that differ in their picrotoxin sensitivity. Neuroreport 11:2695–2701
Raymond-Delpech V, Matsuda K, Sattelle BM, Rauh JJ, Sattelle DB (2005) Ion channels: molecular targets of neuroactive insecticides. Invert Neurosci 5:119–133
Sachse S, Galizia CG (2002) Role of inhibition for temporal and spatial odor representation in olfactory output neurons: a calcium imaging study. J Neurophysiol 87:1106–1117
Sachse S, Rappert A, Galizia CG (1999) The spatial representation of chemical structures in the antennal lobe of honeybees: steps towards the olfactory code. Eur J Neurosci 11:3970–3982
Si A, Helliwell P, Maleszka R (2004) Effects of NMDA receptor antagonists on olfactory learning and memory in the honeybee (Apis mellifera). Pharmacol Biochem Behav 77:191–197
Stopfer M, Bhagavan S, Smith B, Laurent G (1997) Impaired odour discrimination on desynchronisation of odour-encoding neural assemblies. Nature 390:70–74
Tingle CC, Rother JA, Dewhust CF, Lauer S, King WJ (2003) Fipronil: environmental fate, ecotoxicology, and human health concerns. Rev Environ Contam Toxicol 176:1–66
Vidau C, Brunet JL, Badiou A, Belzunces LP (2009) Phenylpyrazole insecticides induce cytotoxicity by altering mechanisms involved in cellular energy supply in the human epithelial cell model Caco-2. Toxicol In Vitro 23:589–597
Zhang W, Liu GJ, Takeuchi H, Kurono M (1996) Effects of l-glutamic acid and its agonists on snail neurones. Gen Pharmacol 27:487–497
Zhao X, Salgado VL, Yeh JZ, Narahashi T (2004) Kinetic and pharmacological characterization of desensitizing and non-desensitizing glutamate-gated chloride channels in cockroach neurons. Neurotoxicology 25:967–980
Acknowledgments
We thank Dr. Valerie Raymond and Guillaume Barbara for valuable discussions. This work was supported by a BDI grant from the French Research Council (CNRS) to A. Kacimi El Hassani and a CNRS post-doctoral grant to J. P. Dupuis.
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Abdessalam Kacimi El Hassani and Julien Pierre Dupuis contributed equally to this work.
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El Hassani, A.K., Dupuis, J.P., Gauthier, M. et al. Glutamatergic and GABAergic effects of fipronil on olfactory learning and memory in the honeybee. Invert Neurosci 9, 91 (2009). https://doi.org/10.1007/s10158-009-0092-z
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DOI: https://doi.org/10.1007/s10158-009-0092-z