Pheromone transduction in moths

Frontiers in Cellular Neuroscience

Volumn 4, Issue DEC, 2010, Pages

  Stengl, Monika ^a  

^a UNIVERSITY OF KASSEL   (Germany)

Author keywords

Circadian rhythms; Field potentials; Insect olfaction; Octopamine; Second messengers; Signal transduction cascades; Subthreshold membrane potential oscillations; Temporal encoding

Indexed keywords

EID: 79952308126     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2010.00133     Document Type: Article

References (164)

1. Ackermann, F. (2004). Ionenkanäle in der Antenne des Tabakschwärmers Manduca sexta. Identifizierung eines Homologs der TRP-Kanalfamilie. Dissertation, University of Marburg.
2. Almaas, T. J., Christensen, T. A., and Mustaparta, H. (1991). Chemical communication in heliothine moths. I. Antennal receptor neurons encode several features of intra- and interspecific odorants in the male corn earworm moth Helicoverpa zea. J. Comp. Physiol. A 169, 249-258.
3. Altner, H., and Prillinger, L. (1980). Ultrastructure of invertebrate chemo-, thermo-, and hygroreceptors and its functional significance. Int. Rev. Cytol. 67, 69-139.
4. Baker, T. C., Hansson, B. S., Lofstedt, C., and Lofquvist, J. (1988). Adaptation of antennal neurons in moths is associated with cessation of pheromonemediated upwind flight. Proc. Natl. Acad. Sci. U.S.A. 85, 9826-9830.
5. Baker, T. C., and Haynes, K. F. (1989). Field and laboratory electroantennographic measurements of pheromone plume structure correlated with oriental fruit moth behavior. Physiol. Entomol. 14, 1-12.
6. Baker, T. C., and Vogt, R. G. (1988). Measured behavioral latency in response to sex-pheromone loss in the large silk moth Antheraea polyphemus. J. Exp. Biol. 137, 29-38.
7. Baker, T. C., Willis, M., Haynes, K. F., and Phelan, P. L. (1985). A pulsed cloud of sex pheromone elicits upwind flight in male moths. Physiol. Entomol. 10, 257-265.
8. Benton, R. (2009). Evolution and revolution in odor detection. Science 326, 282-283.
9. Benton, R., Sachse, S., Michnick, S. W., and Vosshall, L. B. (2006). Atypical membrane topology and heteromeric function of Drosophila odorant receptors in vivo. PLoS Biol. 4, e20.doi: 10.1371/ journal.pbio.0040020
10. Benton, R., Vannice, K. S., and Vosshall, L. B. (2007). An essential role for a CD36-related receptor in pheromone detection in Drosophila. Nature 450, 289-293.
11. Boekhoff, I., Seifert, E., Goggerle, S., Lindemann, M., Kruger, B.-W., and Breer, H. (1993). Pheromone-induced second messenger signalling in insect antennae. Insect Biochem. Mol. Biol. 23, 757-762.
12. Boekhoff, I., Strotmann, J., Raming, K., Tareilus, E., and Breer, H. (1990). Odorant-sensitive phospholipase C in insect antennae. Cell. Signal. 2, 49-56.
13. Boto, T., Gomez-Diaz, C., and Alcorta, E. (2010). Expression analysis of the 3 G-protein subunits, Gα, Gβ, Gγ, in the olfactory receptor organs of adult Drosophila melanogaster. Chem. Senses 35, 183-193.
14. Breer, H., Boekhoff, I., and Tareilus, E. (1990). Rapid kinetics of second messenger formation in olfactory transduction. Nature 345, 65-68.
15. Brigaud, I., Montagne, N., Monsempes, C., Francois M.-C., and Macquin-Joly, E. (2009). Identification of an atypical insect olfactory receptor subtype highly conserved within noctuids. FEBS J. 276, 6537-6547.
16. Broillet, M.-C., and Firestein, S. (1997). β Subunits of the olfactory cyclic nucleotide-gated channel form a nitric oxide activated Ca2+ channel. Neuron 18, 951-958.
17. Chatterjee, A., Roman, G., and Hardin, P. E. (2009). Go contributes to olfactory reception in Drosophila melanogaster. BMC Physiol. 9, 1-7. doi: 10.1186/1472-6793-9-22
18. Chouquet, B., Bozzolan, R., Solvar, M., Duportets, L., Jacquin-Joly, E., Lucas, P., and Debernard, S. (2008). Molecular cloning and expression patterns of a putative olfactory diacylglycerol kinase from the noctuid moth Spodoptera littoralis. Insect Mol. Biol. 17, 485-493.
19. Chouquet, B., Debernard, S., Bozzolan, R., Solvar, M., Maibeche-Coisne, M., and Lucas, P. (2009). A TRP channel is expressed in Spodoptera littoralis antennae and is potentially involved in insect olfactory transduction. Insect Mol. Biol. 18, 213-222.
20. Chouquet, B., Lucas, P., Bozzolan, R., Solvar, M., Maibeche-Coisne, M., Durand, N., and Debernard, S. (2010). Molecular characterization of a phospholipase C {beta} potentially involved in moth olfactory transduction. Chem. Senses. 35, 363-373.
21. Dacks, A. M., Dacks, J. B., Christensen, T. A., and Nighorn, A. J. (2006). The cloning of one putative octopamine receptor and two putative serotonin receptors from the tobacco hawkmoth Manduca sexta. Insect Biochem. Mol. Biol. 36, 741-747.
22. De Bruyne, M., and Baker, T. C. (2008). Odor detection in insects: volatile codes. J. Chem. Ecol. 34, 882-897.
23. De Bruyne, M., Foster, K., and Carlson, J. R. (2001). Odor coding in the Drosophila antenna. Neuron 30, 537-552.
24. Dolzer, J. (2002). Mechanisms of Modulation and Adaptation in Pheromone-Sensitive Trichoid Sensilla of the Hawkmoth Manduca sexta. Dissertation, University of Marburg, 1-120.
25. Dolzer, J., Fischer, K., and Stengl, M. (2003). Adaptation in pheromonesensitive trichoid sensilla of the hawkmoth Manduca sexta. J. Exp. Biol. 206, 1575-1588.
26. Dolzer, J., Krannich, S., Fischer, K., and Stengl, M. (2001). Oscillations of the transepithelial potential of moth olfactory sensilla are influenced by octopamine and serotonin. J. Exp. Biol. 204, 2781-2794.
27. Dolzer, J., Krannich, S., and Stengl, M. (2008). Pharmacological investigation of protein kinase C and cGMPdependent ion channels in cultured olfactory receptor neurons of the hawkmoth Manduca sexta. Chem. Senses 33, 803-813.
28. Dong, X.-P., Wang, X., and Xu, H. (2010). TRP channels of intracellular membranes. J. Neurochem. 1013, 313-328.
29. Duchamp-Viret, P., Kostal, L., Chaput, M., Lansky, P., and Rospars, J. P. (2005). Patterns of spontaneous activity in single rat olfactory receptor neurons are different in normally breathing and tracheotomized animals. J. Neurobiol. 65, 97-114.
30. Eschrich, R., Kumar, G. L., Keil, T. A., and Guckenberger, R. (1998). Atomicforce microscopy on the olfactory dendrites oft he silkmoths Antheraea polyphemus and A. pernyi. Cell Tissue Res. 294, 179-185.
31. Flecke, C., Dolzer, J., and Stengl, M. (2006). Perfusion with cGMP adapts the action potential response in pheromone-dependent trichoid sensilla in the moth Manduca sexta. J. Exp. Biol. 209, 3898-3912.
32. Flecke, C., Nolte, A., and Stengl, M. (2010). Perfusion with cAMP analog affects pheromone-sensitive trichoid sensilla of the hawkmoth Manduca sexta in a time-dependent manner. J. Exp. Biol. 213, 842-852.
33. Flecke, C., and Stengl, M. (2009). Octopamine and tyramine sensitize pheromone-sensitive olfactory sensilla of the hawkmoth Manduca sexta in a daytime-dependent manner. J. Comp. Physiol. A 195, 529-545.
34. Fleischer, J., Breer, H., and Strotmann, J. (2009). Mammalian olfactory receptors. Front. Cell. Neurosci. 3:9. doi: 10.3389/neuro.03.009.2009
35. Forstner, M., Breer, H., and Krieger, J. (2009). A receptor and binding protein interplay in the detection of a distinct pheromone component in the silkmoth Antheraea polyphemus. Int. J. Biol. Sci. 5, 745-757.
36. Forstner, M., Gohl, T., Breer, H., and Krieger, J. (2006). Candidate pheromone binding proteins of the silkmoth Bombyx mori. Invert. Neurosci. 6, 177-187.
37. Forstner, M., Gohl, T., Gondesen, I., Raming, K., Breer, H., and Krieger, J. (2008). Differential expression of SNMP-1 and SNMP-2 proteins in pheromone-sensitive hairs of moths. Chem. Senses 33, 291-299.
38. Gesteland, R. C. (1971). "Neural coding in olfactory receptor cells," in Handbook of Sensory Physiol, Vol. IV, Chem. Senses, ed. L. M. Beidler (Berlin: Springer), 132-150.
39. Grosse-Wilde, E., Gohl, T., Bouche, E., Breer, H., and Krieger, J. (2007). Candidate pheromone receptors provide the basis for the response of distinct antennal neurons to pheromonal compounds. Eur. J. Neurosci. 25, 2364-2373.
40. Grosse-Wilde, E., Svatos, A., and Krieger, J. (2006). A pheromone-binding protein mediates the bombykol-induced activation of a pheromone receptor in vitro. Chem. Senses 31, 547-555.
41. Gu, Y., Lucas, P., and Rospars, J.-P. (2009). Computational model of the insect pheromone transduction cascade. PLoS Comput. Biol. 5, e1000321. doi: 10.1371/journal.pcbi.1000321
42. Hardie, R. C., and Raghu, P. (2001). Visual transduction in Drosophila. Nature 413, 186-193.
43. Huang, J., Hamasaki, T., Ozoe, F., and Ozoe, Y. (2008). Single amino acid switch for distinct G protein couplings. Biochem. Biophys. Res. Commun. 371, 610-604.
44. Itagaki, H., and Conner, W. E. (1988). Calling behavior of Manduca sexta (Lepidoptera: Sphingidae) with notes on the morphology of the female sex pheromone gland. Ann. Entomol. Soc. Am. 81, 798-807.
45. Ito, I., Bazhenov, M., Ong, R. C., Raman, B., and Stopfer, M. (2009). Frequency transitions in odor-evoked neural oscillations. Neuron 64, 692-706.
46. Ito, I., Ong, R. C., Raman, B., and Stopfer, M. (2008). Olfactory learning and spike timing dependent plasticity. Commun. Integr. Biol. 1, 170-171.
47. Jacquin-Joly, E., Francois, M. C., Burnet, M. Lucas, P., Bourrat, F., and Maida, R. (2002). Expression pattern in the antennae of a newly isolated lepidopteran Gq protein alpha subunit cDNA. Eur. J. Biochem. 269, 2133-2142.
48. Jin, X., Ha, T. S., and Smith, D. P. (2008). SNMP is a signaling component required for pheromone sensitivity in Drosophila. Proc. Natl. Acad. Sci. U.S.A. 105, 10996.
49. Johnson, B. R., Vligt, R., Merrill, C. L., and Atema, J. (1991). Across-fiber patterns may contain a sensory code for stimulus intensity. Brain Res. Bull. 26, 327-331.
50. Junek, S., Kludt, E., Wolf, R., and Schild, D. (2010). Olfactory coding with patterns of response latencies. Neuron 67, 872-884.
51. Justus, K. A., Carde, R. T., and French, A. S. (2005). Dynamic properties of antennal responses to pheromone in two moth species. J. Neurophysiol. 93, 2233-2239.
52. Kain, P., Chandrashekaran, S., Rodrigues, V., and Hasan, G. (2008). Drosophila mutants in phospholipid signaling have reduced olfactory responses as adults and larvae. J. Neurogenet. 23, 303-312.
53. Kaissling, K.-E. (1987). "Stimulus transduction," in R. H. Wright Lectures on Insect Olfaction, ed. K. Colbow (Burnaby, BC: Simon Fraser University Press), 1-190.
54. Kaissling, K.-E. (2009). Olfactory perireceptor and receptor events in moths: a kinetic model revised. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 195, 895-922.
55. Kaissling, K.-E., and Boekhoff, I. (1993). "Transduction and intracellular messengers in pheromone receptor cells of the moth Antheraea polyphemus," in Sensory Systems of Arthropods, eds K. Wiese, F. G. Gribakin, A. V. Popov, and G. Renninger (Berlin: Birkhauser), 489-502.
56. Kaissling, K.-E., Hildebrand, J. G., and Tumlinson, J. H. (1989). Pheromone receptor cells in the male moth Manduca sexta. Arch. Insect Biochem. Physiol. 10, 273-279.
57. Kaissling, K.-E., and Priesner, E. (1970). Smell threshold of the silkmoth. Naturwissenschaften 57, 23-28.
58. Kaissling, K.-E., and Thorson, J. (1980). "Insect olfactory sensilla: structural chemical and electrical aspects of the functional organization," in Receptors for Neurotransmitters, Hormones, and Pheromones in Insects, eds D. B. Satelle, L. M. Hall, and J. G. Hildebrand (Amsterdam: Elsevier/ North-Holland Biomedical Press), 261-282.
59. Kalidas, S., and Smith, D. P. (2002). Novel genomic cDNA hybrids produce effective RNA interference in adult Drosophila. Neuron 33, 177-184.
60. Kaupp, U. B. (2010). Olfactory signaling in vertebrates and insects: differences and commonalities. Nat. Rev. Neurosci. 11, 188-200.
61. Keil, T. (1989). Fine structure of the pheromone-sensitive sensilla on the antenna of the hawkmoth, Manduca sexta. Tissue Cell 21, 139-151.
62. Keil, T. A. (1993). Dynamics of "immotile" olfactory cilia in the silkmoth Antheraea. Tissue Cell 25, 573-587.
63. Keil, T. A. (1999). "Morphology and development of the peripheral olfactory organs," in Insect olfaction, ed. B. S. Hansson (Berlin: Springer), 6-47.
64. Keil, T. A., and Steinbrecht, R. A. (1984). "Mechanosensitive and olfactory sensilla of insects," in Insect Ultrastructure, Vol. 2, eds R. C. King and H. Akai (New York: Plenum Press), 435-475.
65. Kennedy, J. S., Ludlov, A. R., and Sanders, D. J. (1981). Guidance of flying male moths by wind-born sex pheromone. Physiol. Entomol. 6, 395-412.
66. Klein, U., and Keil, T. A. (1984). Dendritic membrane from insect olfactory hairs: isolation method and electron microscopic observations. Cell. Mol. Neurobiol. 4, 385-396.
67. Knusel, P., Carlsson, M. A., Hansson, B. S., Pearce, T. C., and Verschure, P. R. M. J. (2007). Time and space are complementary encoding dimensions in the moth antennal lobe. Network 18, 35-62.
68. Koehl, M. A. R. (2006). The fluid mechanics of arthropod sniffing in turbulent odor plumes. Chem. Senses 31, 93-105.
69. Krannich, S. (2008). Electrophysiological and Pharmacological Characterization of Ion Channels Involved in Moth Olfactory Transduction Cascades. Dissertation, University of Marburg, 1-114.
70. Krannich, S., and Stengl, M. (2008). Cyclic nucleotide-activated currents in cultured olfactory receptor neurons of the hawkmoth Manduca sexta. J. Neurophysiol. 100, 2866-2877.
71. Krieger, J., Gondesen, I., Forstner, M., Gohl, T., Dewer, Y. M., and Breer, H. (2009). HR11 and HR13 receptor-expressing neurons are housed together in pheromone- responsive sensilla trichodea of male Heliothis virescens. Chem. Senses 34, 469-477.
72. Krieger, J., Grosse-Wilde, E., Gohl, T., and Breer, H. (2005). Candidate pheromone receptors of the silkmoth Bombyx mori. Eur. J. Neurosci. 21, 2167-2176.
73. Krieger, J., Grosse-Wilde, E., Gohl, T., Dewer Y. M. E., Raming, K., and Breer, H. (2004). Genes encoding candidate pheromone receptors in a moth (Heliothis virescens). Proc. Natl. Acad. Sci. U.S.A. 101, 11645-11850.
74. Krieger, J., Klink, O., Mohl, C., Raming, K., and Breer, H. (2003). A candidate olfactory receptor subtype highly conserved across different insect orders. J. Comp. Physiol. A 189, 519-526.
75. Krieger, J., Raming, K., Dewer, Y. M. E., Bette S., Conzelmann, S., and Breer, H. (2002). A divergent gene family encoding candidate olfactory receptors of the moth Heliothis virescens. Eur. J. Neurosci. 16, 619-628.
76. Krishnan, B., Dryer, S. E., and Hardin, P. E. (1999). Circadian rhythms in olfactory responses of Drosophila melanogaster. Nature 400, 375-378.
77. Krishnan, P., Chatterjee, A., Tanoue, S., and Hardin, P. E. (2008). Spike amplitude of single-unit responses in antennal sensillae is controlled by the Drosophila circadian clock. Curr. Biol. 18, 803-807.
78. Larsson, M. C., Domingos, A. L., Jones, W. D., Chiappe, M. E., Amrein, H., and Vosshall, L. B. (2004). Or83b encodes a broadly expressed odorant receptor essential for Drosophila olfaction. Neuron 43, 703-714.
79. Laue, M., Maida, R., and Redkozubov, A. (1997). G-protein activation, identification and immunolocalization in pheromone-sensitive sensilla trichodea of moths. Cell Tissue Res. 288, 149-158.
80. Laue, M., and Steinbrecht, R. A. (1997). Topochemistry of moth olfactory sensilla. Int. J. Insect Morphol. Embryol. 26, 217-228.
81. Laughlin, J. D., Ha, T. S., Jones, D. N. M., and Smith, D. P. (2008). Activation of pheromone-sensitive neurons is mediated by conformational activation of pheromone-binding protein. Cell 133, 1255-1265.
82. Laurent, G. (2002). Olfactory network dynamics and the coding of multidimensional signals. Nat. Rev. Neurosci. 3, 884-895.
83. Leal, W. S., Chen, A. M., Ishida, Y., Chiang, V. P., Erickson, M. L., Morgan, T. I., and Tsuruda, J. M. (2005). Kinetics and molecular properties of pheromone binding and release. Proc. Natl. Acad. Sci. U.S.A. 102, 5386-5391.
84. Lee, J. K., and Strausfeld, N. J. (1990). Structure, distribution, and number of surface sensilla and their receptor cells on the antennal flagellum of the male sphinx moth Manduca sexta. J. Neurocytol. 19, 519-538.
85. Lehman, H. K. (1990). Circadian control of Manduca sexta flight. Abstr. Soc. Neurosci. 16, 1334.
86. Lei, H., Riffell, J. A., Gage, S. L., and Hildebrand, J. G. (2009). Contrast enhancement of stimulus intermittency in a primary olfactory network and its behavioral significance. J. Biol. 8, 1-15.
87. Linn, C. E. Jr., and Roelofs, W. L. (1986). Modulatory effects of octopamine and serotonin on male sensitivity and periodicity of response to sex pheromone in the cabbage looper moth, Trichoplusia ni. Arch. Insect. Biochem. Physiol. 3, 161-171.
88. Lucas, P., and Pezier, A. (2006). DAG, calcium and chloride: partners involved in insect olfactory transduction. Chem. Senses 31, E81.
89. Lundin, C., Kall, L., Kreher, S. A., Kapp, K., Sonnhammer, S. L., Carson, J. R., Heijne, G., and Nilsson, I. (2007). Membrane topology of the Drosophila OR83b odorant receptor. FEBS Lett. 581, 5601-5604.
90. Maida, R., Redkozubov, A., and Ziegelberger, G. (2000). Identification of PLC beta and PKC in pheromone receptor neurons of Antheraea polyphemus. Neuroreport 11, 1773-1776.
91. Malpel, S., Merlin, C., Francois, M. C., and Jacquin-Joly, E. (2008). Molecular identification and characterization of two new Lepidoptera chemoreceptors belonging to the Drosophila melanogaster OR83b family. Insect. Mol. Biol. 17, 587-596.
92. Merlin, C., Francois, M. C., Queguiner, I., Maibeche-Coisne, M., and Jacquin- Joly, E. (2006). Evidence for a putative antennal clock in Mamestra brassicae: molecular cloning and characterization of two clock genes - period and cryptochrome - in antennae. Insect. Mol. Biol. 15, 137-145.
93. Merlin, C., Lucas, P., Rochat, D., Francois, M. C., Maibeche-Coisne, M., and Jacquin-Joly, E. (2007). An antennal circadian clock and circadian rhythms in peripheral pheromone reception in the moth Spodoptera littoralis. J. Biol. Rhythms 22, 502-514.
94. Milner, P. (1974). A model for visual shape recognition. Psychol. Rev. 81, 521-535.
95. Minor, A. V., and 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.
96. Miura, N., Atsumi, S., Tabunoki, H., and Sato, R. (2005). Expression and localization of three G protein subunits, Go, Gq, and Gs, in adult antennae of the silkmoth (Bombyx mori). J. Comp. Neurol. 485, 143-152.
97. Mohl, C., Breer, H., and Krieger, J. (2002). Species-specific pheromonal compounds induce distinct conformational changes of pheromone binding protein subtypes from Antheraea polyphemus. Invert. Neurosci. 4, 165-174.
98. Morton, D. (2004). Invertebrates yield a plethora of atypical guanylyl cyclases. Mol. Neurobiol. 29, 97-116.
99. Morton, D., and Nighorn, A. (2003). MsGC-II, a receptor guanylyl cyclase isolated from the CNS of Manduca sexta that is inhibited by calcium. J. Neurochem. 84, 363-372.
100. Murlis, J., and Jones, C. (1981). Fine-scale structure of odour plumes in relation to insect orientation to distant pheromone and other attractant sources. Physiol. Entomol. 6, 71-86.
101. Nadasdy, Z. (2010). Binding by asynchrony: the neuronal phase code. Front. Neurosci. 4:51. doi: 10.3389/ fnins.2010.00051
102. Nakagawa, T., Sakurai, T., Nishioka, T., and Touhara, K. (2005). Insect sex pheromone signals mediated by specific combinations of olfactory receptors. Science 307, 1638-1642.
103. Nakagawa, T., and Vosshall, L. (2009). Controversy and consensus: noncanonical signaling mechanisms in the insect olfactory system. Curr. Opin. Neurobiol. 19, 284-292.
104. Nighorn, A., Simpson, P. J., and Morton, D. B. (2001). The novel guanylyl cyclase Ms GC-I is strongly expressed in higher order neuropils in the brain of Manduca sexta. J. Exp. Biol. 204, 305-314.
105. Patch, H., Velarde, R. A., Walden, K. K. O., and Robertson, H. M. (2009). A candidate pheromone receptor and two odorant receptors of the hawkmoth Manduca sexta. Chem. Senses 34, 305-316.
106. Pelosi, P., Zhou, J. J., Ban, L. P., and Calvello, M. (2006). Soluble proteins in insect chemical communication. Cell. Mol. Life Sci. 63, 1658-1676.
107. Pezier, A., Acquistapace, A., Renou, M., Rospars, J.-P., and Lucas, P. (2007). Ca2+ stabilizes the membrane potential of moth olfactory receptor neurons at rest and is essential for their fast repolarization. Chem. Senses 32, 305-317.
108. Pezier, A., Grauso, M., Acquistapace, A., Monsempes, C., Rospars, J.-P., and Lucas, P. (2010). Calcium activates a chloride conductance likely involved in olfactory receptor neuron repolarization in the moth Spodoptera littoralis. J. Neurosci. 30, 6323-6333.
109. Pophof, B. (2000). Octopamine modulates the sensitivity of silkmoth pheromone receptor neurons. J. Comp. Physiol. A 186, 307-313.
110. Pophof, B. (2002). Octopamine enhances moth olfactory responses to pheromones, but not those to general odorants. J. Comp. Physiol. A 188, 659-662.
111. Pophof, B. (2004). Pheromone-binding proteins contribute to the activation of olfactory receptor neurons in the silkmoths Antheraea polyphemus and Bombyx mori. Chem. Senses 29, 117-125.
112. Pophof, B., and van der Goes van Naters, W. (2002). Activation and inhibition of the transduction process in silkmoth olfactory receptor neurons. Chem. Senses 27, 435-443.
113. Raman, B., Tang, J. J., and Stopfer, M. (2010). Temporally diverse firing patterns in olfactory receptor neurons underlie spatiotemporal neural codes for odors. J. Neurosci. 30, 1994-2006.
114. Raming, K., Krieger, J., and Breer, H. (1989). Molecular cloning of an insect pheromone-binding protein. FEBS Lett. 256, 215-218.
115. Rogers, M. E., Steinbrecht, R. A., and Vogt, R. G. (2001a). Expression of SNMP-1 in olfactory neurons and sensilla of male and female antennae of the silkmoth Antheraea polyphemus. Cell Tissue Res. 303, 433-446.
116. Rogers, M. E., Krieger, J., and Vogt, R. G. (2001b). Antennal SNMPs (sensory neuron membrane proteins) of Lepidoptera define a unique family of invertebrate CD36-like proteins. J. Neurobiol. 49, 47-61.
117. Rogers, M. E., Sun, M., Lerner, M. R., and Vogt, R. G. (1997). SNMP-1, a novel membrane protein of olfactory neurons of the silk moth Antheraea polyphemus with homology to the CD36 family of membrane proteins. J. Biol. Chem. 272, 14792-14799.
118. Rutzeler, M., and Zwiebel, I. J. (2005). Molecular biology of insect olfaction: recent progress and conceptual models. J. Comp. Physiol. A 191, 777-790.
119. Saifullah, A. S., and Page, T. L. (2009). Circadian regulation of olfactory receptor neurons in the cockroach antenna. J. Biol. Rhythms 24, 144-152.
120. Sakurai, T., Nakagawa, T., Mitsuno, H., Mori, H., Endo, Y., Tanoue, S., Yasukochi, Y., Touhara, K., and Nishioka, T. (2004). Identification and functional characterization of a sex pheromone receptor in the silkmoth Bombyx mori. Eur. J. Neurosci. 21, 2167-2176.
121. Sanes, J. R., and Hildebrand, J. G. (1976). Origin and morphogenesis of sensory neurons in an insect antenna. Dev. Biol. 51, 300-319.
122. Sato, K., Pellegrino, M., Nakagawa, T., Nakagawa, T., Vosshall, L. B., and Touhara, K. (2008). Insect olfactory receptors are heteromeric ligandgated ion channels. Nature 452, 1002-1006.
123. Schleicher, S., Boekhoff, I., Konietzko, U., and Breer, H. (1994). Pheromoneinduced phosphorylation of antennal proteins from insects. J. Comp. Physiol. B 164, 76-80.
124. Schmidt, C. J., Garen-Fazio, S., Chow, Y. K., and Neer, E. J. (1998). Neuronal expression of a newly identified Drosophila melanogaster G protein alpha o subunit. Cell Regul. 1, 125-134.
125. Schneider, N.-L., and Stengl, M. (2005). Pigment-dispersing factor and GABA synchronize insect circadian clock cells. J. Neurosci. 25, 5138-5147.
126. Schneider, N.-L., and Stengl, M. (2006). Gap junctions between accessory medulla neurons appear to synchronize circadian clock cells. J. Neurophysiol. 95, 1996-2002.
127. Schneider, N.-L., and Stengl, M. (2007). Long term recordings of the isolated circadian pacemaker center of the cockroach Leucophaea maderae reveals circadian and ultradian rhythms. J. Comp. Physiol. A 193, 35-42.
128. Schuckel, J., Siwicki, K. K., and Stengl, M. (2007). Putative circadian pacemaker cells in the antenna of the hawkmoth Manduca sexta. Cell Tissue Res. 330, 271-278.
129. Silbering, A. F., and Benton, R. (2010). Ionotropic and metabotropic mechanisms in chemoreception: "chance or design"? EMBO Rep. 11, 173-179.
130. Silverstein, R. L., and Febbraio, M. (2009). CD36, a scavenger receptor involved in immunity, metabolism, angiogenesis, and behavior. Sci. Signal. 2, re3.
131. Simpson, P. J., Nighorn, A., and Morton, D. B. (1999). Identification of a novel guanylyl cyclase that is related to receptor guanylyl cyclases, but lacks extracellular and transmembrane domains. J. Biol. Chem. 274, 4440-4446.
132. Singer, W. and Gray, C.(1995). Visual feature integration and the temporal correlation hypothesis. Annu. Rev. Neurosci. 18, 555-586.
133. Smart, R., Kiely, A., Beale, M., Vargas, E., Carraher, C., Kraliecek, A. V., Christie, D. L., Chen, C., Newcomb, R. D., and Warr, C. G. (2008). Drosophila odorant receptors are novel seven transmembrane domain proteins that can signal independently of heterotrimeric G proteins. Insect Biochem. Mol. Biol. 38, 770-780.
134. Steinbrecht, R. A., Laue, M., and Ziegelberger, G. (1995). Immunocytochemistry of odorantbinding protein and general binding protein in olfactory sensilla of the silk moths Antheraea and Bombyx. Cell Tissue Res. 282, 203-217.
135. Stengl, M. (1990). Development of an In Vitro Model System to Study Primary Sensory Transduction Mechanisms. Dissertation, ARL, University of Arizona, 1-177.
136. Stengl, M. (1993). Intracellular-messengermediated cation channels in cultured olfactory receptor neurons. J. Exp. Biol. 178, 125-147.
137. Stengl, M. (1994). Inositol-trisphosphatedependent calcium currents precede cation currents in insect olfactory receptor neurons. J. Comp. Physiol. A 174, 187-194.
138. Stengl, M., and Hildebrand, J. G. (1990). Insect olfactory neurons in vitro: morphological and immunocytochemical characterization of male-specific antennal receptor cells from developing antennae of male Manduca sexta. J. Neurosci. 10, 837-847.
139. Stengl, M., and Zintl, R. (1996). NADPHdiaphorase staining in the antenna of the moth Manduca sexta. J. Exp. Biol. 199, 1063-1072.
140. Stengl, M., Homberg, U., and Hildebrand, J. G. (1990). Acetylcholinesterase activity in antennal receptor neurons of the sphinx moth Manduca sexta. Cell Tissue Res. 262, 245-252.
141. Stengl, M., Ziegelberger, G., Boekhoff, I., and Krieger, J. (1999). "Perireceptor events and transduction mechanisms in insect olfaction," in Insect Olfaction, ed. B. S. Hansson (Berlin: Springer), 49-66.
142. Stengl, M., Zintl, R., de Vente, J., and Nighorn, A. (2001). Localization of cGMP-immunoreactivity and of soluble guanylyl cyclase in antennal sensilla of the hawkmoth Manduca sexta. Cell Tissue Res. 304, 409-421.
143. Stengl, M., Zufall, F., Hatt, H., and Hildebrand, J. G. (1992). Olfactory receptor neurons from antennae of developing male Manduca sexta respond to components of the species-specific sex pheromone in vitro. J. Neurosci. 12, 2523-2531.
144. Talluri, S., Bhatt, A., and Smith, D. P. (1995). Identification of a Drosophila G protein alpha subunit (dGq alpha-3) expressed in chemosensory cells and central neurons. Proc. Natl. Acad. Sci. U.S.A. 92, 11475-11479.
145. Tanoue, S., Krishnan, P., Chatterjee, A., and Hardin, P. E. (2008). G proteincoupled receptor kinase 2 is required for rhythmic olfactory responses in Drosophila. Curr. Biol. 18, 787-794.
146. Tanoue, S., Krishnan, T., Krishnan, B., Dryer, S. E., and Hardin, P. E. (2004). Circadian clocks in antennal neurons are necessary and sufficient for olfaction rhythms in Drosophila. Curr. Biol. 14, 638-649.
147. Thurm, U., and Kuppers, J. (1980). "Epithelial physiology of insect sensilla," in Insect Biology in the Future, eds M. Locke and D. S. Smith (New York: Academic Press), 735-763.
148. Tripathy, S., Peters, O. J., Staudacher, E. M., Kalwar, F. R., Hatfield, M. N., and Daly, K. C. (2010). Odors pulsed at wing beat frequencies are tracked by primary olfactory networks and enhance odor detection. Front. Cell. Neurosci. 16:1.
149. Tumlinson, J. H., Brennan, M. M., Doolittle, R. E., Mitchell, E. R., Brabham, A., Mazomemos, B. E., Baumhover, A. H., and Jackson, D. M. (1989). Identification of a pheromone blend attractive to Manduca sexta (L.) males in a wind tunnel. Arch. Insect Biochem. Physiol. 10, 255-271.
150. Vickers, N. J. (2000). Mechanisms of animal navigation in odor plumes. Biol. Bull. 198, 203-212.
151. Vickers, N. J., and Baker, T. C. (1992). Male Heliothis virescens maintain upwind flight in response to experimentally pulsed filaments of their sex pheromone (Lepidoptera: Noctuidae). J. Insect Behav. 5, 669-687.
152. Vogt, R. G., Miller, N. E., Litvack, R., Fandino, R. A., Sparks, J., Staples, J., Friedman, R., and Dickens, J. C. (2009). The insect SNMP gene family. Insect Biochem. Mol. Biol. 39, 448-456.
153. Vogt, R. G., and Riddiford, L. M. (1981). Pheromone binding and inactivation by moth antennae. Nature 293, 161-163.
154. Vogt, R. G., and Riddiford, L. M. (1986). "Pheromone reception: a kinetic equilibrium," Mechanisms in Insect Olfaction, eds T. L. Payne, M. C. Birch and E. J. Kennedy (Oxford: Clarendon), 201-208.
155. von Frisch, K. (1921). Über den Sitz des Geruchssinnes bei Insekten. Zool. Jahrb. Abt. Allgem. Zool. Physiol. Tiere 38, 449-516.
156. Von Nickisch-Rosenegk, E., Krieger, J., Kubick, S., Laage, R., Strobel, J., Stotmann, H., and Breer, H. (1996). Cloning of biogenic amine receptors from moths (Bombyx mori and Heliothis virescens). Insect Biochem. Mol. Biol. 26, 817-827.
157. Wegener, J. W., Hanke, W., and Breer, H. (1997). Second messenger-controlled membrane conductance in locust (Locusta migratoria) olfactor y receptor neurons. J. Insect. Physiol. 43, 595-605.
158. Wicher, D, Schäfer, R., Bauernfeind, R., Stensmyr, M. C., Heller, R., Heinemann, S. H., and Hansson, B. S. (2008). Drosophila odorant receptors are both ligand-gated and cyclicnucleotide- activated cation channels. Nature 452, 1007-1011.
159. Xu, P. X., Atkinson, R., Jones, D. N. M., and Smith, D. P. (2005). Drosophila OBP LUSH is required for activity of pheromone-sensitive neurons. Neuron 45, 193-200.
160. Ziegelberger, G. (1995). Redox-shift of the pheromone-binding protein in the silkmoth Antheraea polyphemus. Eur. J. Biochem. 232, 706-711.
161. Ziegelberger, G., Van den Berg, M. J., Kaissling, K.-E., Klumpp, S., and Schultz, J. E. (1990). Cyclic nucleotide levels and guanylate cyclase activity in pheromonesensitive antennae of the silkmoths Antheraea polyphemus and Bombyx mori. J. Neurosci. 10, 1217-1225.
162. Zufall, F., and 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. U.S.A. 88, 8520-8524.
163. Zufall, F., Stengl, M., Franke, C., Hildebrand, J. G., and Hatt, H. (1991a). Ionic currents of cultured olfactory receptor neurons from antennae of male Manduca sexta. J. Neurosci. 11, 956-965.
164. Zufall, F., Franke, C., and Hatt, H. (1991b). A calcium-activated nonspecific cation channel from olfactory receptor neurons of the silkmoth Antheraea polyphemus. J. Exp. Biol. 161, 455-468.