Ca2+ stabilizes the membrane potential of moth olfactory receptor neurons at rest and is essential for their fast repolarization

Chemical Senses

Volumn 32, Issue 4, 2007, Pages 305-317

  Pézier, Adeline ^a   Acquistapace, Adrien ^a   Renou, Michel ^a   Rospars, Jean Pierre ^a   Lucas, Philippe ^a  

^a INRA Institut National de la Recherche Agronomique   (France)

Author keywords

Calcium signaling; Depolarization; Insect olfactory transduction; Patch clamp; Repolarization; Single sensillum recording

Indexed keywords

CALCIUM ACTIVATED POTASSIUM CHANNEL; CALCIUM ION; N (6 AMINOHEXYL) 5 CHLORO 1 NAPHTHALENESULFONAMIDE; SEX PHEROMONE; CALCIUM; PHEROMONE;

ARTICLE; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CELL MEMBRANE DEPOLARIZATION; CONTROLLED STUDY; EXTRACELLULAR CALCIUM; IN VIVO STUDY; MALE; MOTH; NERVE CELL INHIBITION; NERVE CELL MEMBRANE STEADY POTENTIAL; NERVE CELL STIMULATION; NERVE POTENTIAL; NONHUMAN; OLFACTORY RECEPTOR; PRIORITY JOURNAL; REPOLARIZATION; SIGNAL TRANSDUCTION; ANIMAL; ARMYWORM; CELL CULTURE; DRUG EFFECT; EVOKED RESPONSE; PATCH CLAMP; PHYSIOLOGY;

HEXAPODA; LEPIDOPTERA; SPODOPTERA LITTORALIS;

ANIMALS; CALCIUM; CELLS, CULTURED; EVOKED POTENTIALS; MALE; OLFACTORY RECEPTOR NEURONS; PATCH-CLAMP TECHNIQUES; PHEROMONES; SPODOPTERA;

EID: 34447120189     PISSN: 0379864X     EISSN: 14643553     Source Type: Journal    
DOI: 10.1093/chemse/bjl059     Document Type: Article

References (64)

1. Berridge MJ. 1993. Inositol trisphosphate and calcium signalling. Nature. 361:315-325.
2. Bigiani A, Mucignat-Caretta C, Montani G, Tirindelli R. 2005. Pheromone reception in mammals. Rev Physiol Biochem Pharmacol. 154:1-35.
3. Boekhoff I, Raming K, Breer H. 1990. Pheromone-induced stimulation of inositol-triphosphate formation in insect antennae is mediated by G-proteins. J Comp Physiol A. 160:99-103.
4. Boekhoff I, Seifert E, Goggerle S, Lindemann M, Kruger B-W, Breer H. 1993. Pheromone-induced second-messenger signaling in insect antennae. Insect Biochem Mol Biol. 23:757-762.
5. Boekhoff I, Strotmann J, Raming K, Tareilus E, Breer H. 1990. Odorant-sensitive phospholipase C in insect antennae. Cell Signal. 2:49-56.
6. Courjaret R, Lapied B. 2001. 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. 60:80-91.
7. Deshpande M, Venkatesh K, Rodrigues V, Hasan G. 2000. The inositol 1,4,5-trisphosphate receptor is required for maintenance of olfactory adaptation in Drosophila antennae. J Neurobiol. 43:282-288.
8. Dolzer J. 2002. Mechanisms of modulation and adaptation in pheromone-sensitive trichoid sensilla of the hawkmoth Manduca sexta Marburg (Germany): Philipps-Universität. p. 119.
9. Dolzer J, Fischer K, Stengl M. 2003. Adaptation in pheromone-sensitive trichoid sensilla of the hawkmoth Manduca sexta. J Exp Biol. 206: 1575-1588.
10. Dougherty DP, Wright GA, Yew AC. 2005. Computational model of the cAMP-mediated sensory response and calcium-dependent adaptation in vertebrate olfactory receptor neurons. Proc Natl Acad Sci USA. 102:10415-10420.
11. Eide PE, Caldwell JM, Marks EP. 1975. Establishment of two cell lines from embryonic tissue of the tobacco hornworm, Manduca sexta (L). In Vitro. 11:395-399.
12. Gold GH, Lowe G. 1995. Single odorant molecules? Nature. 376:27.
13. Haab JE, Vergara C, Bacigalupo J, O'Day PM. 2000. Coordinated gating of TRP-dependent channels in rhabdomeral membranes from Drosophila retinas. J Neurosci. 20:7193-7198.
14. 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. Pflügers Arch. 391:85-100.
15. Hansson BS, Anton S. 2000. Function and morphology of the antennal lobe: new developments. Annu Rev Entomol. 45:203-231.
16. Jacquin-Joly E, Lucas P. 2005. Pheromone reception and transduction: mammals and insects illustrate converging mechanisms across phyla. Curr Top Neurochem. 4:75-105.
17. Kaissling K-E. 1974. Sensory transduction in insect olfactory receptors. In: Jaenick L, editor. 25 Mosbacher Colloquium der Gesellschaft für biologische Chemie, 25-27 April 1974: Biochemistry of sensory functions. New York: Springer-Verlag. p. 243-271.
18. Kaissling K-E. 1986. Chemo-electrical transduction in insect olfactory receptors. Annu Rev Neurosci. 9:121-145.
19. Kaissling K-E. 1987. R.H. Wright lectures on insect olfaction. British Columbia (Canada): Simon Fraser University.
20. Kaissling K-E. 2004. Physiology of pheromone reception in insects (an example of moths). ANIR. 6:73-91.
21. Kaissling K-E, Priesner E. 1970. Die Riechschwelle des Seidenspinners. Naturwissenschaften. 57:23-28.
22. Kaissling K-E, Thorson J. 1980. Insect olfactory sensilla: Structural, chemical and electrical aspects of the functional organization. In: Sattelle DB, Hall LM, Hildebrand JG, editors. Receptors for neurotransmitters, hormones and pheromones in insects. Amsterdam (The Netherlands): Elsevier. p. 261-282.
23. Kaissling K-E, Zack Strausfeld C, Rumbo ER. 1987. Adaptation processes in insect receptors. Mechanisms and behavioral significance. Ann N Y Acad Sci. 510:104-112.
24. Kalidas S, Smith DP. 2002. Novel genomic cDNA hybrids produce effective RNA interference in adult Drosophila. Neuron. 33:177-184.
25. Kleene SJ. 2000. Spontaneous gating of olfactory cyclic-nucleotide-gated channels. J Membr Biol. 178:49-54.
26. Kleene SJ. 2002. The calcium-activated chloride conductance in olfactory receptor neurons. Curr Top Membr. 53:119-134.
27. Küppers J, Thurm U. 1979. Active ion transport by a sensory epithelium. I. Transepithelial short circuit current, potential difference, and their dependence on metabolism. J Comp Physiol. 134:131-136.
28. Leinders-Zufall T, Greer CA, Shepherd GM, Zufall F. 1998. Imaging odor-induced calcium transients in single olfactory cilia: Specificity of activation and role in transduction. J Neurosci. 18:5630-5639.
29. 2+-activated cation channel from hamster vomeronasal sensory neurons. J Physiol. 548:777-787.
30. Ljungberg H, Anderson P, Hansson BS. 1993. Physiology and morphology of pheromone-specific sensilla on the antennae of male and female Spodoptera littoralis (Lepidoptera: Noctuidae). J Insect Physiol. 39: 253-260.
31. Lowe G, Gold GH. 1995. Olfactory transduction is intrinsically noisy. Proc Natl Acad Sci USA. 92:7864-7868.
32. Lucas P, Nagnan-Le Meillour P. 1997. Primary culture of antennal cells of Mamestra brassicae: Morphology of cell types and evidence for biosynthesis of pheromone-binding proteins in vitro. Cell Tissue Res. 289: 375-382.
33. Lucas P, Pézier A. 2006. DAG, calcium, and chloride: Partners involved in insect olfactory transduction. ECRO XVII. Chem Senses. 31:E81.
34. Lucas P, Shimahara T. 2002. Voltage- and calcium-activated currents in cultured olfactory receptor neurons of male Mamestra brassicae (Lepidoptera). Chem Senses. 27:599-610.
35. Lucas P, Ukhanov K, Leinders-Zufall T, Zufall F. 2003. A diacylglycerolgated cation channel in vomeronasal neuron dendrites is impaired in TRPC2 mutant mice: Mechanism of pheromone transduction. Neuron. 40:551-561.
36. Marion-Poll F. 1995. Object-oriented approach to fast display of electrophysiological data under MS-Windows. J Neurosci Methods. 63:197-204.
37. Matthews HR, Reisert J. 2003. Calcium, the two-faced messenger of olfactory transduction and adaptation. Curr Opin Neurobiol. 13:469-475.
38. Menini A. 1999. Calcium signalling and regulation in olfactory neurons. Curr Opin Neurobiol. 9:419-426.
39. Menini A, Picco C, Firestein S. 1995. Quantal-like current fluctuations induced by odorants in olfactory receptor cells. Nature. 373:435-437.
40. Minor AV, Kaissling K-E. 2003. Cell responses to single pheromone molecules may reflect the activation kinetics of olfactory receptor molecules. J Comp Physiol A. 189:221-230.
41. Nakamura T, Gold GH. 1987. A cyclic nucleotide-gated conductance in olfactory receptor cilia. Nature. 325:442-444.
42. - current in moth olfactory receptor neurons. ECRO XVII. Chem Senses. 31:E94.
43. Poitout S, Bues R, Le Rumeur C. 1972. Elevage sur milieu artificiel simple de deux noctuelles parasites du coton Earias insulana et Spodoptera littoralis. Entomol Exp Appl. 15:341-350.
44. Pophof B. 2002. Moth pheromone binding proteins contribute to the excitation of olfactory receptor cells. Naturwissenschaften. 89:515-518.
45. Pophof B, Van Der Goes Van Naters W. 2002. Activation and inhibition of the transduction process in silkmoth olfactory receptor neurons. Chem Senses. 27:435-443.
46. Quero C, Lucas P, Renou M, Guerrero A. 1996. Behavioral responses of Spodoptera littoralis males to sex pheromone components and virgin females in wind tunnel. J Chem Ecol. 22:1087-1102.
47. Redkozubov A. 1995. High electrical resistance of the bombykol cell in an olfactory sensillum of Bombyx mori: Voltage- and current-clamp analysis. J Insect Physiol. 41:451-455.
48. Redkozubov A. 1996. Protein kinase C is involved in the activation of receptor neurons in the olfactory sensilla of the gypsy moth. Sens Syst. 10: 307-312.
49. Redkozubov A. 2000a. Guanosine 3′,5′-cyclic monophosphate reduces the response of the moth's olfactory receptor neuron to pheromone. Chem Senses. 25:381-385.
50. Redkozubov A. 2000b. Elementary receptor currents elicited by a single pheromone molecule exhibit quantal composition. Pflügers Arch. 440:896-901.
51. 2+ extrusion governs response recovery in frog olfactory receptor cells. J Gen Physiol. 112: 529-535.
52. Schild D, Restrepo D. 1998. Transduction mechanisms in vertebrate olfactory receptor cells. Physiol Rev. 78:429-466.
53. Schulze DH, Pyrski M, Ruknudin A, Margolis JW, Polumuri SK, Margolis FL. 2002. Sodium-calcium exchangers in olfactory tissue. Ann N Y Acad Sci. 976:67-72.
54. Seno K, Nakamura T, Ozaki M. 2005. Biochemical and physiological evidence that calmodulin is involved in the taste response of the sugar receptor cells of the blowfly, Phormia regina. Chem Senses. 30:497-504.
55. Stengl M. 1993. Intracellular-messenger-mediated cation channels in cultured olfactory receptor neurons. J Exp Biol. 178:125-147.
56. Stengl M. 1994. Inositol-triphosphate-dependent calcium currents precede cation currents in insect olfactory receptor neurons in vitro. J Comp Physiol. 174:187-194.
57. Stengl M, Ziegelberger G, Boekhoff I, Krieger J. 1999. Perireceptor events and transduction mechanisms in insect olfaction. In: Hansson BS, editor. Insect olfaction. Berlin (Germany): Springer Verlag. p. 49-66.
58. Thurm U, Wessel G. 1979. Metabolism-dependent transepithelial potential differences at epidermal receptors of Arthropods. I. Comparative data. J Comp Physiol. 134:119-130.
59. Vermeulen A, Rospars J-P. 2001. Membrane potential and its electrode-recorded counterpart in an electrical model of an olfactory sensillum. Eur Biophys J. 29:587-596.
60. Wegener JW, Tareilus E, Breer H. 1992. Characterization of calcium-dependent potassium channels in antennal receptor neurones of Locusta migratoria. J Insect Physiol. 38:237-248.
61. Willis MA, Baker TC. 1984. Effect of intermittent and continuous pheromone stimulation on the flight behaviour of the oriental fruit moth, Grapholita molesta. Physiol Entomol. 9:341-358.
62. Zack SC, Kaissling KE. 1986. Localized adaptation processes in olfactory sensilla of Saturniid moths. Chem Senses. 11:499-512.
63. Zufall F, Hatt H. 1991. Dual activation of a sex pheromone-dependent ion channel from insect olfactory dendrites by protein kinase C activators and cyclic GMP. Proc Natl Acad Sci USA. 88:8520-8524.
64. 2+ release and its role in olfactory signal transduction. J Neurophysiol. 83:501-512.