Journal of Comparative Physiology A

, Volume 199, Issue 11, pp 897–909 | Cite as

The role of the coreceptor Orco in insect olfactory transduction

Review

Abstract

Insects sense odorants with specialized odorant receptors (ORs). Each antennal olfactory receptor neuron expresses one OR with an odorant binding site together with a conserved coreceptor called Orco which does not bind odorants. Orco is necessary for localization of ORs to dendritic membranes and, thus, is essential for odorant detection. It forms a spontaneously opening cation channel, activated via phosphorylation by protein kinase C. Thereafter, Orco is also activated via cyclic adenosine monophosphate (cAMP). Orco forms homo—as well as heteromers with ORs with unknown stoichiometry. Contradictory publications suggest different mechanisms of olfactory transduction. On the one hand, evidence accumulates for the employment of more than one G protein-coupled olfactory transduction cascade in different insects. On the other hand, results from other studies suggest that the OR–Orco complex functions as an odorant-gated cation channel mediating ionotropic signal transduction. This review analyzes conflicting hypotheses concerning the role of Orco in insect olfactory transduction. In conclusion, in situ studies in hawkmoths falsify the hypothesis that Orco underlies odorant-induced ionotropic signal transduction in all insect species. Instead, Orco forms a metabotropically gated, slow cation channel which controls odorant response threshold and kinetics of the sensory neuron.

Keywords

Insect olfaction Odorant receptor Pheromones Ionotropic receptor Metabotropic signal transduction cascade 

Abbreviations

cAMP

Cyclic adenosine monophosphate

cGMP

Cyclic guanosine monophosphate

GR

Gustatory receptor

Ii

Ionotropic current

Im

Metabotropic current

It

Transduction current

IP3

Inositol 1,4,5-trisphosphate

IR

Ionotropic receptor

OR

Odorant receptor

Orco

Olfactory receptor coreceptor

ORN

Olfactory receptor neuron

PKC

Protein kinase C

PLCβ

Phospholipase Cβ

SNMP

Sensory neuron membrane protein

TM

transmembrane domain

References

  1. Abdel-Latief M (2007) A family of chemoreceptors in Tribolium castaneum (Tenebrionidae: Coleoptera). PLoS One 2(12):e1319PubMedGoogle Scholar
  2. Abuin L, Bargeton B, Ulbrich MH, Isacoff EY, Kellenberger S, Benton R (2011) Functional architecture of olfactory ionotropic glutamate receptors. Neuron 69(1):44–60PubMedGoogle Scholar
  3. Altner H, Prillinger L (1980) Ultrastructure of invertebrate chemo-, thermo- and hygroreceptors and its functional significance. Int Rev Cytol 67:69–139Google Scholar
  4. Atema J (1995) Chemical signals in the marine environment: dispersal, detection, and temporal signal analysis. Proc Natl Acad Sci USA 92(1):62–66PubMedGoogle Scholar
  5. Baker TC, Hansson BS, Lofstedt C, Lofqvist J (1988) Adaptation of antennal neurons in moths is associated with cessation of pheromone-mediated upwind flight. Proc Natl Acad Sci USA 85(24):9826–9830PubMedGoogle Scholar
  6. Benton R, Sachse S, Michnick SW, Vosshall LB (2006) Atypical membrane topology and heteromeric function of Drosophila odorant receptors in vivo. PLoS Biol 4(2):e20PubMedGoogle Scholar
  7. Benton R, Vannice KS, Vosshall LB (2007) An essential role for a CD36-related receptor in pheromone detection in Drosophila. Nature 450(7167):289–293PubMedGoogle Scholar
  8. Benton R, Vannice KS, Gomez-Diaz C, Vosshall LB (2009) Variant ionotropic glutamate receptors as chemosensory receptors in Drosophila. Cell 136(1):149–162PubMedGoogle Scholar
  9. Boekhoff I, Strotmann J, Raming K, Tareilus E, Breer H (1990) Odorant-sensitive phospholipase C in insect antennae. Cell Signal 2(1):49–56PubMedGoogle Scholar
  10. Boekhoff I, Seifert E, Göggerle S, Lindemann M, Krüger BW, Breer H (1993) Pheromone-induced second-messenger signaling in insect antennae. Insect Biochem Mol Biol 23(7):757–762Google Scholar
  11. Bohbot JD, Dickens JC (2012) Odorant receptor modulation: ternary paradigm for mode of action of insect repellents. Neuropharmacology 62(5–6):2086–2095PubMedGoogle Scholar
  12. Breer H, Boekhoff I, Tareilus E (1990) Rapid kinetics of second messenger formation in olfactory transduction. Nature 345(6270):65–68PubMedGoogle Scholar
  13. Chatterjee A, Roman G, Hardin PE (2009) Go contributes to olfactory reception in Drosophila melanogaster. BMC Physiol 9:22PubMedGoogle Scholar
  14. Chen S, Luetje CW (2012) Identification of new agonists and antagonists of the insect odorant receptor co-receptor subunit. PLoS One 7(5):e36784PubMedGoogle Scholar
  15. Clyne PJ, Warr CG, Freeman MR, Lessing D, Kim J, Carlson JR (1999) A novel family of divergent seven-transmembrane proteins: candidate odorant receptors in Drosophila. Neuron 22(2):327–338PubMedGoogle Scholar
  16. Corey EA, Bobkov Y, Ukhanov K, Ache BW (2013) Ionotropic crustacean olfactory receptors. PLoS One 8(4):e60551PubMedGoogle Scholar
  17. Couto A, Alenius M, Dickson BJ (2005) Molecular, anatomical, and functional organization of the Drosophila olfactory system. Curr Biol 15(17):1535–1547PubMedGoogle Scholar
  18. Croset V, Rytz R, Cummins SF, Budd A, Brawand D, Kaessmann H, Gibson TJ, Benton R (2010) Ancient protostome origin of chemosensory ionotropic glutamate receptors and the evolution of insect taste and olfaction. PLoS Genet 6(8):e1001064PubMedGoogle Scholar
  19. de Bruyne M, Baker TC (2008) Odor detection in insects: volatile codes. J Chem Ecol 34(7):882–897PubMedGoogle Scholar
  20. de Bruyne M, Clyne PJ, Carlson JR (1999) Odor coding in a model olfactory organ: the Drosophila maxillary palp. J Neurosci 19(11):4520–4532PubMedGoogle Scholar
  21. de Bruyne M, Foster K, Carlson JR (2001) Odor coding in the Drosophila antenna. Neuron 30(2):537–552PubMedGoogle Scholar
  22. Deng Y, Zhang W, Farhat K, Oberland S, Gisselmann G, Neuhaus EM (2011) The stimulatory Gαs protein is involved in olfactory signal transduction in Drosophila. PLoS One 6(4):e18605PubMedGoogle Scholar
  23. Dobritsa AA, van der Goes van Naters W, Warr CG, Steinbrecht RA, Carlson JR (2003) Integrating the molecular and cellular basis of odor coding in the Drosophila antenna. Neuron 37(5):827–841PubMedGoogle Scholar
  24. Dolzer J, Fischer K, Stengl M (2003) Adaptation in pheromone-sensitive trichoid sensilla of the hawkmoth Manduca sexta. J Exp Biol 206(Pt 9):1575–1588PubMedGoogle Scholar
  25. Elmore T, Ignell R, Carlson JR, Smith DP (2003) Targeted mutation of a Drosophila odor receptor defines receptor requirement in a novel class of sensillum. J Neurosci 23(30):9906–9912PubMedGoogle Scholar
  26. Flecke C, Stengl M (2009) Octopamine and tyramine modulate pheromone-sensitive olfactory sensilla of the hawkmoth Manduca sexta in a time-dependent manner. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 195(6):529–545PubMedGoogle Scholar
  27. Flecke C, Dolzer J, Krannich S, Stengl M (2006) Perfusion with cGMP analogue adapts the action potential response of pheromone-sensitive sensilla trichoidea of the hawkmoth Manduca sexta in a daytime-dependent manner. J Exp Biol 209(Pt 19):3898–3912PubMedGoogle Scholar
  28. Flecke C, Nolte A, Stengl M (2010) Perfusion with cAMP analogue affects pheromone-sensitive trichoid sensilla of the hawkmoth Manduca sexta in a time-dependent manner. J Exp Biol 213(Pt 5):842–852PubMedGoogle Scholar
  29. Forstner M, Gohl T, Gondesen I, Raming K, Breer H, Krieger J (2008) Differential expression of SNMP-1 and SNMP-2 proteins in pheromone-sensitive hairs of moths. Chem Senses 33(3):291–299PubMedGoogle Scholar
  30. German PF, van der Poel S, Carraher C, Kralicek AV, Newcomb RD (2013) Insights into subunit interactions within the insect olfactory receptor complex using FRET. Insect Biochem Mol Biol 43(2):138–145PubMedGoogle Scholar
  31. Getahun MN, Wicher D, Hansson BS, Olsson SB (2012) Temporal response dynamics of Drosophila olfactory sensory neurons depends on receptor type and response polarity. Front Cell Neurosci 6:54PubMedGoogle Scholar
  32. Getahun MN, Olsson SB, Lavista-Llanos S, Hansson BS, Wicher D (2013) Insect odorant response sensitivity is tuned by metabotropically autoregulated olfactory receptors. PLoS One 8(3):e58889PubMedGoogle Scholar
  33. Goldman AL, van der Goes van Naters W, Lessing D, Warr CG, Carlson JR (2005) Coexpression of two functional odor receptors in one neuron. Neuron 45(5):661–666PubMedGoogle Scholar
  34. Grosse-Wilde E, Svatoš A, Krieger J (2006) A pheromone-binding protein mediates the bombykol-induced activation of a pheromone receptor in vitro. Chem Senses 31(6):547–555PubMedGoogle Scholar
  35. Grosse-Wilde E, Stieber R, Forstner M, Krieger J, Wicher D, Hansson BS (2010) Sex-specific odorant receptors of the tobacco hornworm Manduca sexta. Front Cell Neurosci 4:22PubMedGoogle Scholar
  36. Grosse-Wilde E, Kuebler LS, Bucks S, Vogel H, Wicher D, Hansson BS (2011) Antennal transcriptome of Manduca sexta. Proc Natl Acad Sci USA 108(18):7449–7454PubMedGoogle Scholar
  37. Guo S, Kim J (2010) Dissecting the molecular mechanism of Drosophila odorant receptors through activity modeling and comparative analysis. Proteins 78(2):381–399PubMedGoogle Scholar
  38. Hallem EA, Ho MG, Carlson JR (2004a) The molecular basis of odor coding in the Drosophila antenna. Cell 117(7):965–979PubMedGoogle Scholar
  39. Hallem EA, Nicole Fox A, Zwiebel LJ, Carlson JR (2004b) Olfaction: mosquito receptor for human-sweat odorant. Nature 427(6971):212–213PubMedGoogle Scholar
  40. Hallem EA, Dahanukar A, Carlson JR (2006) Insect odor and taste receptors. Annu Rev Entomol 51:113–135PubMedGoogle Scholar
  41. Hardie RC, Raghu P (2001) Visual transduction in Drosophila. Nature 413(6852):186–193PubMedGoogle Scholar
  42. Harini K, Sowdhamini R (2012) Molecular modelling of oligomeric states of DmOR83b, an olfactory receptor in D. melanogaster. Bioinform Biol Insights 6:33–47PubMedGoogle Scholar
  43. Hill CA, Fox AN, Pitts RJ, Kent LB, Tan PL, Chrystal MA, Cravchik A, Collins FH, Robertson HM, Zwiebel LJ (2002) G protein-coupled receptors in Anopheles gambiae. Science 298(5591):176–178PubMedGoogle Scholar
  44. Isono K, Morita H (2010) Molecular and cellular designs of insect taste receptor system. Front Cell Neurosci 4:20PubMedGoogle Scholar
  45. Ito I, Ong RC, Raman B, Stopfer M (2008) Sparse odor representation and olfactory learning. Nat Neurosci 11(10):1177–1184PubMedGoogle Scholar
  46. Jin X, Ha TS, Smith DP (2008) SNMP is a signaling component required for pheromone sensitivity in Drosophila. Proc Natl Acad Sci USA 105(31):10996–11001PubMedGoogle Scholar
  47. Jones WD, Nguyen TA, Kloss B, Lee KJ, Vosshall LB (2005) Functional conservation of an insect odorant receptor gene across 250 million years of evolution. Curr Biol 15(4):R119–R121PubMedGoogle Scholar
  48. Jones PL, Pask GM, Rinker DC, Zwiebel LJ (2011) Functional agonism of insect odorant receptor ion channels. Proc Natl Acad Sci USA 108(21):8821–8825PubMedGoogle Scholar
  49. Jones PL, Pask GM, Romaine IM, Taylor RW, Reid PR, Waterson AG, Sulikowski GA, Zwiebel LJ (2012) Allosteric antagonism of insect odorant receptor ion channels. PLoS One 7(1):e30304PubMedGoogle Scholar
  50. Jordan MD, Anderson A, Begum D, Carraher C, Authier A, Marshall SD, Kiely A, Gatehouse LN, Greenwood DR, Christie DL, Kralicek AV, Trowell SC, Newcomb RD (2009) Odorant receptors from the light brown apple moth (Epiphyas postvittana) recognize important volatile compounds produced by plants. Chem Senses 34(5):383–394PubMedGoogle Scholar
  51. Junek S, Kludt E, Wolf F, Schild D (2010) Olfactory coding with patterns of response latencies. Neuron 67(5):872–884PubMedGoogle Scholar
  52. Justus KA, Carde RT, French AS (2005) Dynamic properties of antennal responses to pheromone in two moth species. J Neurophysiol 93(4):2233–2239PubMedGoogle Scholar
  53. Kain P, Chakraborty TS, Sundaram S, Siddiqi O, Rodrigues V, Hasan G (2008) Reduced odor responses from antennal neurons of Gqα, phospholipase Cβ, and rdgA mutants in Drosophila support a role for a phospholipid intermediate in insect olfactory transduction. J Neurosci 28(18):4745–4755PubMedGoogle Scholar
  54. Kaissling KE (1987) Stimulus transduction. In: Colbow K (ed) R. H. Wright lectures on insect olfaction. Simon Fraser University Press, Burnaby, BC, pp 1–190Google Scholar
  55. Kaissling KE, Priesner E (1970) Die Riechschwelle des Seidenspinners. Naturwissenschaften 57(1):23–28PubMedGoogle Scholar
  56. Keil TA, Steinbrecht RA (1984) Mechanosensitive and olfactory sensilla of insects. In: KR C, Hiromu A (eds) Insect ultrastructure vol 2. Plenum Press, New York, pp 477–516Google Scholar
  57. Kennedy JS, Ludlow AR, Sanders CJ (1981) Guidance of flying male moths by wind-borne sex-pheromone. Physiol Entomol 6(4):395–412Google Scholar
  58. Kiely A (2008) Functional and structural analyses of an olfactory receptor from Drosophila melanogaster. Dissertation, University of AucklandGoogle Scholar
  59. Kiely A, Authier A, Kralicek AV, Warr CG, Newcomb RD (2007) Functional analysis of a Drosophila melanogaster olfactory receptor expressed in Sf9 cells. J Neurosci Methods 159(2):189–194PubMedGoogle Scholar
  60. Koehl MA (2006) The fluid mechanics of arthropod sniffing in turbulent odor plumes. Chem Senses 31(2):93–105PubMedGoogle Scholar
  61. Krieger J, Raming K, Dewer YM, Bette S, Conzelmann S, Breer H (2002) A divergent gene family encoding candidate olfactory receptors of the moth Heliothis virescens. Eur J Neurosci 16(4):619–628PubMedGoogle Scholar
  62. Krieger J, Klink O, Mohl C, Raming K, Breer H (2003) A candidate olfactory receptor subtype highly conserved across different insect orders. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 189(7):519–526PubMedGoogle Scholar
  63. Larsson MC, Domingos AI, Jones WD, Chiappe ME, Amrein H, Vosshall LB (2004) Or83b encodes a broadly expressed odorant receptor essential for Drosophila olfaction. Neuron 43(5):703–714PubMedGoogle Scholar
  64. Laue M, Maida R, Redkozubov A (1997) G-protein activation, identification and immunolocalization in pheromone-sensitive sensilla trichodea of moths. Cell Tissue Res 288(1):149–158PubMedGoogle Scholar
  65. Laurent G (2002) Olfactory network dynamics and the coding of multidimensional signals. Nat Rev Neurosci 3(11):884–895PubMedGoogle Scholar
  66. Lei H, Riffell JA, Gage SL, Hildebrand JG (2009) Contrast enhancement of stimulus intermittency in a primary olfactory network and its behavioral significance. J Biol 8(2):21PubMedGoogle Scholar
  67. Lundin C, Kall L, Kreher SA, Kapp K, Sonnhammer EL, Carlson JR, Heijne G, Nilsson I (2007) Membrane topology of the Drosophila OR83b odorant receptor. FEBS Lett 581(29):5601–5604PubMedGoogle Scholar
  68. Martin JP, Beyerlein A, Dacks AM, Reisenman CE, Riffell JA, Lei H, Hildebrand JG (2011) The neurobiology of insect olfaction: sensory processing in a comparative context. Prog Neurobiol 95(3):427–447PubMedGoogle Scholar
  69. Melo AC, Rutzler M, Pitts RJ, Zwiebel LJ (2004) Identification of a chemosensory receptor from the yellow fever mosquito, Aedes aegypti, that is highly conserved and expressed in olfactory and gustatory organs. Chem Senses 29(5):403–410PubMedGoogle Scholar
  70. Miller R, Tu Z (2008) Odorant receptor c-terminal motifs in divergent insect species. J Insect Sci 8:53Google Scholar
  71. Mitsuno H, Sakurai T, Murai M, Yasuda T, Kugimiya S, Ozawa R, Toyohara H, Takabayashi J, Miyoshi H, Nishioka T (2008) Identification of receptors of main sex-pheromone components of three Lepidopteran species. Eur J Neurosci 28(5):893–902PubMedGoogle Scholar
  72. Montagne N, Chertemps T, Brigaud I, Francois A, Francois MC, de Fouchier A, Lucas P, Larsson MC, Jacquin-Joly E (2012) Functional characterization of a sex pheromone receptor in the pest moth Spodoptera littoralis by heterologous expression in Drosophila. Eur J Neurosci 36(5):2588–2596PubMedGoogle Scholar
  73. Murlis J, Jones CD (1981) Fine-scale structure of odor-plumes in relation to insect orientation to distant pheromone and other attractant sources. Physiol Entomol 6(1):71–86Google Scholar
  74. Nadasdy Z (2010) Binding by asynchrony: the neuronal phase code. Front Neurosci 4:51PubMedGoogle Scholar
  75. Nakagawa T, Vosshall LB (2009) Controversy and consensus: noncanonical signaling mechanisms in the insect olfactory system. Curr Opin Neurobiol 19(3):284–292PubMedGoogle Scholar
  76. Nakagawa T, Sakurai T, Nishioka T, Touhara K (2005) Insect sex-pheromone signals mediated by specific combinations of olfactory receptors. Science 307(5715):1638–1642PubMedGoogle Scholar
  77. Nakagawa T, Pellegrino M, Sato K, Vosshall LB, Touhara K (2012) Amino acid residues contributing to function of the heteromeric insect olfactory receptor complex. PLoS One 7(3):e32372PubMedGoogle Scholar
  78. Neuhaus EM, Gisselmann G, Zhang W, Dooley R, Stortkuhl K, Hatt H (2005) Odorant receptor heterodimerization in the olfactory system of Drosophila melanogaster. Nat Neurosci 8(1):15–17PubMedGoogle Scholar
  79. Nichols AS, Chen S, Luetje CW (2011) Subunit contributions to insect olfactory receptor function: channel block and odorant recognition. Chem Senses 36(9):781–790PubMedGoogle Scholar
  80. Nolte A, Funk NW, Mukunda L, Gawalek P, Werckenthin A, Hansson BS, Wicher D, Stengl M (2013) In situ tip-recordings found no evidence for an Orco-based ionotropic mechanism of pheromone-transduction in Manduca sexta. PLoS One 8(5):e62648PubMedGoogle Scholar
  81. Olafson PU (2013) Molecular characterization and immunolocalization of the olfactory co-receptor Orco from two blood-feeding muscid flies, the stable fly (Stomoxys calcitrans, L.) and the horn fly (Haematobia irritans irritans, L.). Insect Mol Biol 22(2):131–142PubMedGoogle Scholar
  82. Pask GM, Jones PL, Rutzler M, Rinker DC, Zwiebel LJ (2011) Heteromeric anopheline odorant receptors exhibit distinct channel properties. PLoS One 6(12):e28774PubMedGoogle Scholar
  83. Pask GM, Bobkov YV, Corey EA, Ache BW, Zwiebel LJ (2013) Blockade of insect odorant receptor currents by amiloride derivatives. Chem Senses 38(3):221–229PubMedGoogle Scholar
  84. Patch HM, Velarde RA, Walden KK, Robertson HM (2009) A candidate pheromone receptor and two odorant receptors of the hawkmoth Manduca sexta. Chem Senses 34(4):305–316PubMedGoogle Scholar
  85. Peñalva-Arana DC, Lynch M, Robertson HM (2009) The chemoreceptor genes of the waterflea Daphnia pulex: many Grs but no Ors. BMC Evol Biol 9:79PubMedGoogle Scholar
  86. Pitts RJ, Fox AN, Zwiebel LJ (2004) A highly conserved candidate chemoreceptor expressed in both olfactory and gustatory tissues in the malaria vector Anopheles gambiae. Proc Natl Acad Sci USA 101(14):5058–5063PubMedGoogle Scholar
  87. Robertson HM, Gadau J, Wanner KW (2010) The insect chemoreceptor superfamily of the parasitoid jewel wasp Nasonia vitripennis. Insect Mol Biol 19(Suppl 1):121–136PubMedGoogle Scholar
  88. Rogers ME, Sun M, Lerner MR, Vogt RG (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(23):14792–14799PubMedGoogle Scholar
  89. Rogers ME, Steinbrecht RA, Vogt RG (2001a) Expression of SNMP-1 in olfactory neurons and sensilla of male and female antennae of the silkmoth Antheraea polyphemus. Cell Tissue Res 303(3):433–446PubMedGoogle Scholar
  90. Rogers ME, Krieger J, Vogt RG (2001b) Antennal SNMPs (sensory neuron membrane proteins) of Lepidoptera define a unique family of invertebrate CD36-like proteins. J Neurobiol 49(1):47–61PubMedGoogle Scholar
  91. Röllecke K, Werner M, Ziemba PM, Neuhaus EM, Hatt H, Gisselmann G (2013) Amiloride derivatives are effective blockers of insect odorant receptors. Chem Senses 38(3):231–236PubMedGoogle Scholar
  92. Sakurai T, Nakagawa T, Mitsuno H, Mori H, Endo Y, Tanoue S, Yasukochi Y, Touhara K, Nishioka T (2004) Identification and functional characterization of a sex pheromone receptor in the silkmoth Bombyx mori. Proc Natl Acad Sci USA 101(47):16653–16658PubMedGoogle Scholar
  93. Sargsyan V, Getahun MN, Llanos SL, Olsson SB, Hansson BS, Wicher D (2011) Phosphorylation via PKC regulates the function of the Drosophila odorant co-receptor. Front Cell Neurosci 5:5PubMedGoogle Scholar
  94. Sato K, Pellegrino M, Nakagawa T, Vosshall LB, Touhara K (2008) Insect olfactory receptors are heteromeric ligand-gated ion channels. Nature 452(7190):1002–1006PubMedGoogle Scholar
  95. Sato K, Tanaka K, Touhara K (2011) Sugar-regulated cation channel formed by an insect gustatory receptor. Proc Natl Acad Sci USA 108(28):11680–11685PubMedGoogle Scholar
  96. Schuckel J, Siwicki KK, Stengl M (2007) Putative circadian pacemaker cells in the antenna of the hawkmoth Manduca sexta. Cell Tissue Res 330(2):271–278PubMedGoogle Scholar
  97. Singer W, Gray CM (1995) Visual feature integration and the temporal correlation hypothesis. Annu Rev Neurosci 18:555–586PubMedGoogle Scholar
  98. Smadja C, Shi P, Butlin RK, Robertson HM (2009) Large gene family expansions and adaptive evolution for odorant and gustatory receptors in the pea aphid, Acyrthosiphon pisum. Mol Biol Evol 26(9):2073–2086PubMedGoogle Scholar
  99. Smart R, Kiely A, Beale M, Vargas E, Carraher C, Kralicek AV, Christie DL, Chen C, Newcomb RD, Warr CG (2008) Drosophila odorant receptors are novel seven transmembrane domain proteins that can signal independently of heterotrimeric G proteins. Insect Biochem Mol Biol 38(8):770–780PubMedGoogle Scholar
  100. Stengl M (1993) Intracellular-messenger-mediated cation channels in cultured olfactory receptor neurons. J Exp Biol 178:125–147PubMedGoogle Scholar
  101. Stengl M (1994) Inositol-trisphosphate-dependent calcium currents precede cation currents in insect olfactory receptor neurons in vitro. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 174(2):187–194Google Scholar
  102. Stengl M (2010) Pheromone transduction in moths. Front Cell Neurosci 4:133PubMedGoogle Scholar
  103. Stengl M, Zufall F, Hatt H, Hildebrand JG (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(7):2523–2531PubMedGoogle Scholar
  104. Su CY, Menuz K, Reisert J, Carlson JR (2012) Non-synaptic inhibition between grouped neurons in an olfactory circuit. Nature 492(7427):66–71PubMedGoogle Scholar
  105. Taylor RW, Romaine IM, Liu C, Murthi P, Jones PL, Waterson AG, Sulikowski GA, Zwiebel LJ (2012) Structure-activity relationship of a broad-spectrum insect odorant receptor agonist. ACS Chem Biol 7(10):1647–1652PubMedGoogle Scholar
  106. Tripathy SJ, Peters OJ, Staudacher EM, Kalwar FR, Hatfield MN, Daly KC (2010) Odors pulsed at wing beat frequencies are tracked by primary olfactory networks and enhance odor detection. Front Cell Neurosci 4:1PubMedGoogle Scholar
  107. Tsitoura P, Andronopoulou E, Tsikou D, Agalou A, Papakonstantinou MP, Kotzia GA, Labropoulou V, Swevers L, Georgoussi Z, Iatrou K (2010) Expression and membrane topology of Anopheles gambiae odorant receptors in lepidopteran insect cells. PLoS One 5(11):e15428PubMedGoogle Scholar
  108. Vickers NJ (2000) Mechanisms of animal navigation in odor plumes. Biol Bull 198(2):203–212PubMedGoogle Scholar
  109. Vickers NJ, Baker TC (1992) Male Heliothis virescens maintain upwind flight in response to experimentally pulsed filaments of their sex-pheromone (Lepidoptera, Noctuidae). J Insect Behav 5(6):669–687Google Scholar
  110. Vogt RG, Miller NE, Litvack R, Fandino RA, Sparks J, Staples J, Friedman R, Dickens JC (2009) The insect SNMP gene family. Insect Biochem Mol Biol 39(7):448–456PubMedGoogle Scholar
  111. Vosshall LB, Hansson BS (2011) A unified nomenclature system for the insect olfactory coreceptor. Chem Senses 36(6):497–498PubMedGoogle Scholar
  112. Vosshall LB, Amrein H, Morozov PS, Rzhetsky A, Axel R (1999) A spatial map of olfactory receptor expression in the Drosophila antenna. Cell 96(5):725–736PubMedGoogle Scholar
  113. Vosshall LB, Wong AM, Axel R (2000) An olfactory sensory map in the fly brain. Cell 102(2):147–159PubMedGoogle Scholar
  114. Wang X, Zhong M, Wen J, Cai J, Jiang H, Liu Y, Aly SM, Xiong F (2012) Molecular characterization and expression pattern of an odorant receptor from the myiasis-causing blowfly, Lucilia sericata (Diptera: Calliphoridae). Parasitol Res 110(2):843–851PubMedGoogle Scholar
  115. Wanner KW, Nichols AS, Allen JE, Bunger PL, Garczynski SF, Linn CE, Robertson HM, Luetje CW (2010) Sex pheromone receptor specificity in the European corn borer moth, Ostrinia nubilalis. PLoS One 5(1):e8685PubMedGoogle Scholar
  116. Wegener JW, Hanke W, Breer H (1997) Second messenger-controlled membrane conductance in locust (Locusta migratoria) olfactory neurons. J Insect Physiol 43(6):595–603PubMedGoogle Scholar
  117. Wetzel CH, Behrendt HJ, Gisselmann G, Stortkuhl KF, Hovemann B, Hatt H (2001) Functional expression and characterization of a Drosophila odorant receptor in a heterologous cell system. Proc Natl Acad Sci USA 98(16):9377–9380PubMedGoogle Scholar
  118. Wicher D, Schäfer R, Bauernfeind R, Stensmyr MC, Heller R, Heinemann SH, Hansson BS (2008) Drosophila odorant receptors are both ligand-gated and cyclic-nucleotide-activated cation channels. Nature 452(7190):1007–1011PubMedGoogle Scholar
  119. Wistrand M, Kall L, Sonnhammer EL (2006) A general model of G protein-coupled receptor sequences and its application to detect remote homologs. Protein Sci 15(3):509–521PubMedGoogle Scholar
  120. Xia Y, Zwiebel LJ (2006) Identification and characterization of an odorant receptor from the West Nile virus mosquito, Culex quinquefasciatus. Insect Biochem Mol Biol 36(3):169–176PubMedGoogle Scholar
  121. Yang Y, Krieger J, Zhang L, Breer H (2012) The olfactory co-receptor Orco from the migratory locust (Locusta migratoria) and the desert locust (Schistocerca gregaria): identification and expression pattern. Int J Biol Sci 8(2):159–170PubMedGoogle Scholar
  122. Yao CA, Carlson JR (2010) Role of G-proteins in odor-sensing and CO2-sensing neurons in Drosophila. J Neurosci 30(13):4562–4572PubMedGoogle Scholar
  123. Zhang HJ, Anderson AR, Trowell SC, Luo AR, Xiang ZH, Xia QY (2011) Topological and functional characterization of an insect gustatory receptor. PLoS One 6(8):e24111PubMedGoogle Scholar
  124. Zheng W, Zhu C, Peng T, Zhang H (2012) Odorant receptor co-receptor Orco is upregulated by methyl eugenol in male Bactrocera dorsalis (Diptera: Tephritidae). J Insect Physiol 58(8):1122–1127PubMedGoogle Scholar
  125. Ziegelberger G, van den Berg MJ, Kaissling KE, Klumpp S, Schultz JE (1990) Cyclic GMP levels and guanylate cyclase activity in pheromone-sensitive antennae of the silkmoths Antheraea polyphemus and Bombyx mori. J Neurosci 10(4):1217–1225PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  1. 1.FB 10, Biology, Animal PhysiologyUniversity of KasselKasselGermany

Personalised recommendations