Diversity of Biotransformation Enzymes in Insect Antennae: Possible Roles in Odorant Inactivation and Xenobiotic Processing

  • Claudia Steiner
  • Thomas Chertemps
  • Martine MaïbècheEmail author


The mechanisms that could interfere with ligand/receptor interaction or with ligand properties within the insect olfactory organ are intensely studied. These perireceptor events involve various proteins present in the environment of receptors that could contribute to the signal detection, before or after ligand binding. The step of signal termination that sustains the kinetics of the olfactory system is still poorly documented. One hypothesis proposes that biotransformation enzymes called Odorant-Degrading Enzymes (ODEs) could be involved in the rapid degradation of odorant chemicals into inactive compounds (i.e. which cannot elicit receptor response anymore) and could thus play an important role in signal inactivation. ODEs could also play a complex role in odorant clearance. Extracellular ODEs may indeed participate in the catabolism of odorant molecules in excess within the sensillar lymph to avoid an overstimulation of the olfactory receptors and therefore play a role in olfactory sensitivity and dynamics, whereas intracellular ODEs could produce various odorant-derived metabolites that will be excreted outside the sensilla. However, despite their high diversity, as revealed by recent transcriptomic analyses in various species, only very few antennal biotransformation enzymes have been yet functionally characterized as ODEs.

We will present the diversity of these enzymes in insect olfactory organs and discuss their potential role in odorant processing. Their possible involvement in detoxification processes within the olfactory organ will be also discussed, as well as their potential as targets to develop specific inhibitors that could interfere with pest insect ability to respond to olfactory cues.


  1. Ahmad S, Kirkland KE, Blomquist GJ (1987) Evidence for a sex pheromone metabolizing cytochrome P450 monooxygenase in house fly. Arch Insect Biochem Physiol 6:121–140CrossRefGoogle Scholar
  2. Ahn S, Vogel H, Heckel D (2012) Comparative analysis of the UDP-glycosyltransferase multigene family in insects. Insect Biochem Mol Biol 42:133–147CrossRefPubMedGoogle Scholar
  3. Ahnolt R, Williams T (2010) The soluble proteome of the drosophila antennae. Chem Senses 35:21–30CrossRefGoogle Scholar
  4. Ai J, Zhu Y, Duan J, Yu Q, Zhang G, Wan F, Xiang ZH (2011) Genome-wide analysis of cytochrome P450 monooxygenase genes in the silkworm, Bombyx mori. Genetics 480:42–50Google Scholar
  5. Andersson MN, Larsson MC, Blaženec M, Jakuš R, Zhang QH, Schlyter F (2010) Peripheral modulation of pheromone response by inhibitory host compound in a beetle. J Exp Biol 213:3332–3339CrossRefPubMedGoogle Scholar
  6. Arrese EL, Soulages JL (2010) Insect fat body: energy, metabolism, and regulation. Annu Rev Entomol 55:207–225CrossRefPubMedPubMedCentralGoogle Scholar
  7. Baker T, Vogt R (1988) Measured behavioural latency in response to sex-pheromone loss in the large silk moth Antheraea polyphemus. J Exp Biol 137:29–38PubMedGoogle Scholar
  8. Bau J, Martínez D, Renou M, Guerrero A (1999) Pheromone-triggered orientation flight of male moths can be disrupted by trifluoromethyl ketones. Chem Senses 24:473–480CrossRefPubMedGoogle Scholar
  9. Bousquet F, Nojima T, Houot B, Chauvel I, Chaudy S, Dupas S, Yamamoto D, Ferveur JF (2012) Expression of a desaturase gene, desat1, in neural and nonneural tissues separately affects perception and emission of sex pheromones in Drosophila. Proc Natl Acad Sci U S A 109:249–254CrossRefPubMedGoogle Scholar
  10. Bozzolan F, Siaussat D, Maria A, Durand N, Pottier MA, Chertemps T, Maïbèche-Coisne M (2014) Antennal uridine diphosphate (UDP)-glycosyltransferases in a pest insect: diversity and putative function in odorant and xenobiotics clearance. Insect Mol Biol 23:539–549CrossRefPubMedGoogle Scholar
  11. Cano-Ramírez C, López MF, Cesar-Ayala AK, Pineda-Martínez V, Sullivan BT, Zúñiga G (2012) Isolation and expression of cytochrome P450 genes in the antennae and gut of pine beetle Dendroctonus rhizophagus (Curculionidae: Scolytinae) following exposure to host monoterpenes. Gene 520:47–63CrossRefPubMedGoogle Scholar
  12. Carraher C, Dalziel J, Jordan MD, Christie DL, Newcomb RD, Kralicek AV (2015) Towards an understanding of the structural basis for insect olfaction by odorant receptors. Insect Biochem Mol Biol 66:31–41CrossRefPubMedGoogle Scholar
  13. Chen H, Lin L, Xie M, Zhang G, Su W (2014) De novo sequencing, assembly and characterization of antennal transcriptome of Anomala corpulenta Motschulsky (Coleoptera: Rutelidae). PLoS One 10:e0127303CrossRefGoogle Scholar
  14. Chertemps T, François A, Durand N, Rosell G, Dekker T, Lucas P, Maїbèche-Coisne M (2012) A carboxylesterase, Esterase-6, modulates sensory physiological and behavioral response dynamics to pheromone in Drosophila. BMC Biol 10:56CrossRefPubMedPubMedCentralGoogle Scholar
  15. Chertemps T, Younus F, Steiner C, Durand N, Coppin CW, Pandey G, Oakshott JG, Maїbèche M (2015) An antennal carboxylesterase from Drosophila melanogaster, esterase 6, is a candidate odorant-degrading enzyme toward food odorants. Front Physiol 6:315CrossRefPubMedPubMedCentralGoogle Scholar
  16. Choo Y, Pelletier J, Atungulu E, Leal WS (2013) Identification and characterization of an antennae-specific aldehyde oxidase from the navel orangeworm. PLoS One 8:e67794CrossRefPubMedPubMedCentralGoogle Scholar
  17. Claudianos C, Ranson H, Johnson RM, Biswas S, Schuler MA, Berenbaum MR, Feyereisen R, Oakeshott JG (2006) A deficit of detoxification enzymes: pesticide sensitivity and environmental response in the honeybee. Insect Mol Biol 15:615–636CrossRefPubMedPubMedCentralGoogle Scholar
  18. Corcoran JA, Jordan MD, Thrimawithana AH, Crowhurst RN, Newcomb RD (2015) The peripheral olfactory repertoire of the lightbrown apple moth, Epiphyas postvittana. PLoS One 10:e0128596CrossRefPubMedPubMedCentralGoogle Scholar
  19. Després L, David JP, Gallet C (2007) The evolutionary ecology of insect resistance to plant chemicals. Trends Ecol Evol 22:298–307CrossRefPubMedGoogle Scholar
  20. Dierick H, Greenspan R (2006) Molecular analysis of flies selected for aggressive behavior. Nat Genet 38:1023–1031CrossRefPubMedGoogle Scholar
  21. Ding X, Kaminsky L (2003) Human extrahepatic cytochromes P450: function in xenobiotic metabolism and tissue-selective chemical toxicity in the respiratory and gastrointestinal tracts. Annu Rev Pharmacol Toxicol 43:149–173CrossRefPubMedGoogle Scholar
  22. Dow JAT, Davies SA (2006) The malpighian tubule: rapid insights from post-genomic biology. J Insect Physiol 52:365–378CrossRefPubMedGoogle Scholar
  23. Dunkelblum E, Kehat M, Harel M, Gordon D (1987) Sexual behaviour and pheromone titre of the Spodoptera littoralis female moth. Entomol Exp Appl 44:241–247CrossRefGoogle Scholar
  24. Durand N, Carot-Sans G, Chertemps T, Bozzolan F, Party V, Renou M, Derbernard S, Rosell G, Maїbèche-Coisne M (2010a) Characterization of an antennal carboxylesterase from the pest moth Spodoptera littoralis degrading a host plant odorant. PLoS One 5:e15026CrossRefPubMedPubMedCentralGoogle Scholar
  25. Durand N, Carot-Sans G, Chertemps T, Montagné N, Jacquin-Joly E, Debernard S, Maïbèche-Coisne M (2010b) A diversity of putative carboxylesterases is expressed in the antennae of the noctuid moth Spodoptera littoralis. Insect Mol Biol 19:87–97CrossRefPubMedGoogle Scholar
  26. Durand N, Carot-Sans G, Bozzolan F, Rosell G, Siaussat D, Debernard S, Chertemps T, Maїbèche-Coisne M (2011) Degradation of pheromone and plant volatile components by a same odorant-degrading enzyme in the cotton leafworm, Spodoptera littoralis. PLoS One 6:e29147CrossRefPubMedPubMedCentralGoogle Scholar
  27. Durand N, Chertemps T, Maïbèche-Coisne M (2012) Antennal carboxylesterases in a moth, structural and functional diversity. Commun Integr Biol 5:284–286CrossRefPubMedPubMedCentralGoogle Scholar
  28. Durand N, Chertemps T, Bozzolan F, Maїbèche M (2016) Expression and modulation of neuroligin and neurexin in the olfactory organ of the cotton leaf worm Spodoptera littoralis. Insect Sci 24:210–221CrossRefPubMedGoogle Scholar
  29. Fang Y, Song F, Zhang L, Aleku DW, Han B, Feng M, Li J (2012) Differential antennal proteome comparison of adult honeybee drone, worker and queen (Apis mellifera L.). J Proteomics 75:756–773CrossRefPubMedGoogle Scholar
  30. Feng M, Song F, Aleku DW, Han B, Fang Y, Li J (2011) Antennal proteome comparison of sexually mature drone and forager honeybees. J Proteome Res 10:3246–3260CrossRefPubMedGoogle Scholar
  31. Ferkovich SM, Mayer MS, Rutter RR (1973a) Conversion of the sex pheromone of the cabbage looper. Nature 242:53–55CrossRefGoogle Scholar
  32. Ferkovich SM, Mayer MS, Rutter RR (1973b) Sex pheromone of the cabbage looper: reactions with antennal proteins in vitro. J Insect Physiol 19:2231–2243CrossRefGoogle Scholar
  33. Ferkovich SM, van Essen F, Taylor T (1980) Hydrolysis of sex pheromone by antennal esterases of the cabbage looper, Trichoplusia ni. Chem Senses 5:33–45CrossRefGoogle Scholar
  34. Ferkovich SM, Oliver JE, Dillard C (1982) Pheromone hydrolysis by cuticular and interior esterases of the antennae, legs and wings of the cabbage looper moth, Trichoplusia ni. J Chem Ecol 8:859–866CrossRefPubMedGoogle Scholar
  35. Feyereisen R (2006) Evolution of insect P450. Biochem Soc Trans 34:1252–1255CrossRefPubMedGoogle Scholar
  36. Feyereisen R (2012) Insect CYP genes and P450 enzymes. In: Gilbert LI (ed) Insect molecular biology and biochemistry. Elsevier, London, pp 236–316CrossRefGoogle Scholar
  37. Getchell TV, Margolis FL, Getchell ML (1984) Perireceptor and receptor events in vertebrate olfaction. Prog Neurobiol 23:317–345CrossRefPubMedGoogle Scholar
  38. Gu XC, Zhang YN, Kang K, Dong SL, Zhang LW (2015) Antennal transcriptome analysis of odorant reception genes in the red turpentine beetle (rtb), Dendroctonus valens. PLoS One 10:e0125159CrossRefPubMedPubMedCentralGoogle Scholar
  39. Hakim RS, Baldwin K, Smagghe G (2010) Regulation of midgut growth, development, and metamorphosis. Annu Rev Entomol 55:593–608CrossRefPubMedGoogle Scholar
  40. Hallem EA, Ho MG, Carlson JR (2004) The molecular basis of odor coding in the Drosophila antenna. Cell 117:965–979CrossRefGoogle Scholar
  41. He P, Zhang J, Li ZQ, Yang K, Zhu JY, Liu SJ, Dong SL (2014a) An antennae-enriched carboxylesterase from Spodoptera exigua displays degradation activity in both plant volatiles and female sex pheromones. Insect Mol Biol 23:475–486CrossRefPubMedGoogle Scholar
  42. He P, Zhang J, Li ZQ, Zhang YN, Yang K, Dong SL (2014b) Functional characterization of an antennal esterase from the noctuid moth, Spodoptera exigua. Arch Insect Biochem Physiol 86:85–99CrossRefPubMedGoogle Scholar
  43. He P, Zhang YN, Yang K, Li ZQ, Dong SL (2015) An antenna-biased carboxylesterase is specifically active to plant volatiles in Spodoptera exigua. Pestic Biochem Physiol 123:93–100CrossRefPubMedGoogle Scholar
  44. Heydel J, Holsztynska EJ, Legendre A, Thiebaud N, Artur Y, Le Bon AM (2010) UDP-glucuronosyltransferases (UGTs) in neuro-olfactory tissues: expression, regulation, and function. Drug Metab Rev 42:74–97CrossRefPubMedGoogle Scholar
  45. Hu P, Wang J, Cui M, Tao J, Luo Y (2016) Antennal transcriptome analysis of the asian longhorned beetle Anoplophora glabripennis. Sci Rep 6:26652CrossRefPubMedPubMedCentralGoogle Scholar
  46. Huang F, Chai CL, Zhang Z, Liu ZH, Dai FY, Lu C, Xiang ZH (2008) The UDP-glucosyltransferase multigene family in Bombyx mori. BMC Genomics 9:563CrossRefPubMedPubMedCentralGoogle Scholar
  47. Huang X, Liu L, Su X, Feng J (2016) Identification of biotransformation enzymes in the antennae of codling moth Cydia pomonella. Gene 580:73–79CrossRefPubMedGoogle Scholar
  48. Ishida Y, Leal WS (2002) Cloning of putative odorant-degrading enzyme and integumental esterase cDNAs from the wild silkmoth, Antheraea polyphemus. Insect Biochem Mol Biol 32:1775–1780CrossRefPubMedGoogle Scholar
  49. Ishida Y, Leal WS (2005) Rapid inactivation of a moth pheromone. Proc Natl Acad Sci U S A 102:14075–14079CrossRefPubMedPubMedCentralGoogle Scholar
  50. Ishida Y, Leal WS (2008) Chiral discrimination of the Japanese beetle sex pheromone and a behavioral antagonist by a pheromone-degrading enzyme. Proc Natl Acad Sci U S A 105:9076–9080CrossRefPubMedPubMedCentralGoogle Scholar
  51. Jacquin-Joly E, Maïbèche-Coisne M (2009) Molecular mechanisms of sex pheromone reception in Lepidoptera. In: Chandrasekar R (ed) Short views on insect molecular biology. Bharathidasan University, Trichy, pp 147–158Google Scholar
  52. Jordan MD, Stanley D, Marshall SDG, De Silva D, Crowhurst RN, Gleave AP, Greenwood DR, Newcomb RD (2008) Expressed sequence tags and proteomics of antennae from the tortricid moth, Epiphyas postvittana. Insect Mol Biol 17:361–373CrossRefPubMedGoogle Scholar
  53. Kaissling KE (2001) Olfactory perireceptor and receptor events in moths: a kinetic model. Chem Senses 26:125–150CrossRefPubMedGoogle Scholar
  54. Kaissling KE (2009) Olfactory perireceptor and receptor events in moths: a kinetic model revised. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 195:895–922CrossRefPubMedPubMedCentralGoogle Scholar
  55. Kaissling KE (2014) Chapter 4: Pheromone reception in insects: the example of silkmoths. In: Mucignat-Caretta C (ed) Neurobiology of chemical communication. CRC Press/Taylor & Francis, Boca-Raton, pp 99–138CrossRefGoogle Scholar
  56. Kaissling KE, Priesner E (1970) Smell threshold of the silkworm. Naturwissenschaften 57:23–28CrossRefPubMedGoogle Scholar
  57. Kamikouchi A, Morioka M, Kubo T (2004) Identification of honeybee antennal proteins/genes expressed in a sex- and/or caste selective manner. Zool Sci 21:53–62CrossRefPubMedGoogle Scholar
  58. Kasang G (1971) Bombykol reception and metabolism on the antennae of the silkmoth Bombyx mori. In: Ohloff G, Thomas AF (eds) Gustation and olfaction. Academic, London, pp 245–250Google Scholar
  59. Kasang G, Nicholls M, von Proff L (1989a) Sex-pheromone conversion and degradation in antennae of the silk moth Bombyx mori. Experientia 45:81–87CrossRefGoogle Scholar
  60. Kasang G, Nicholls M, Keil T (1989b) Enzymatic conversion of sex pheromones in olfactory hairs of the male silkworm moth Antheraea polyphemus. Z Naturforsch 44c:920–926CrossRefGoogle Scholar
  61. Keeling C, Henderson H, Li M, Dullat HK, Ohnishi T, Bohlmann J (2013) CYP345E2, an antenna-specific cytochrome P450 from the mountain pine beetle, Dendroctonus ponderosae Hopkins, catalyses the oxidation of pine host monoterpene volatiles. Insect Biochem Mol Biol 43:1142–1151CrossRefPubMedGoogle Scholar
  62. Kleene S (2008) The electrochemical basis of odor transduction in vertebrate olfactory cilia. Chem Senses 33:839–859CrossRefPubMedGoogle Scholar
  63. Klun J, Schwartz M, Uebel E (1991) European corn borer: pheromonal catabolism and behavioral response to sex pheromone. J Chem Ecol 17:317–332CrossRefPubMedGoogle Scholar
  64. Lalouette L, Pottier MA, Wycke MA, Boitard C, Bozzolan F, Maria A, Demondion E, Chertemps T, Lucas P, Renault D, Maїbèche M, Siaussat D (2016) Unexpected effects of sublethal doses of insecticide on the peripheral olfactory response and sexual behavior in a pest insect. Environ Sci Pollut Res Int 23:3073–3085CrossRefPubMedGoogle Scholar
  65. Lazard D, Zupko K, Poria Y, Nef P, Lazarovits J, Horn S, Khen M, Lancet D (1991) Odorant signal termination by olfactory UDP glucuronosyl transferase. Nature 349:790–793CrossRefPubMedGoogle Scholar
  66. Le Goff G, Hilliou F, Siegfried BD, Boundy S, Wajnbarg E, Sofer L, Audant P, French-Constant RH, Feyereisen R (2006) Xenobiotic response in Drosophila melanogaster: sex dependence of P450 and GST gene induction. Insect Biochem Mol Biol 36:674–682CrossRefPubMedGoogle Scholar
  67. Leal W (2013) Odorant reception in insects: roles of receptors, binding proteins, and degrading enzymes. Annu Rev Entomol 58:373–391CrossRefPubMedGoogle Scholar
  68. Legeai F, Malpel S, Montagné N, Monsempes C, Cousserans F, Merlin C, François MC, Maïbeche-Coisné M, Gavory F, Poulin J, Jacquin-Joly E (2011) An expressed sequence tag collection from the male antennae of the Noctuid moth Spodoptera littoralis: a resource for olfactory and pheromone detection research. BMC Genomics 12:86PubMedPubMedCentralGoogle Scholar
  69. Leitch O, Papanicolaou A, Lennard C, Kirkbride KP, Anderson A (2015) Chemosensory genes identified in the antennal transcriptome of the blowfly Calliphora stygia. BMC Genomics 16:255CrossRefPubMedPubMedCentralGoogle Scholar
  70. Li X, Schuler MA, Berenbaum MR (2007) Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. Annu Rev Entomol 52:231–253CrossRefPubMedGoogle Scholar
  71. Li X, Yang H, Liu YF, Liao QR, Du J, Jin DC (2012) Transcriptome and gene expression analysis of the rice leaf folder, Cnaphalocrosis medinalis. PLoS One 7:e47401CrossRefPubMedPubMedCentralGoogle Scholar
  72. Li Z, Ni JD, Huang J, Montell C (2014) Requirement for Drosophila SNMP1 for rapid activation and termination of pheromone-induced activity. PLoS Genet 10:e1004600CrossRefPubMedPubMedCentralGoogle Scholar
  73. Liu S, Gong ZJ, Rao XJ, Li MY, Li SG (2015a) Identification of putative carboxylesterase and glutathione S-transferase genes from the antennae of the Chilo suppressalis (Lepidoptera: Pyralidae). J Insect Sci 15:103CrossRefPubMedPubMedCentralGoogle Scholar
  74. Liu S, Rao XJ, Li MY, Feng MF, He MZ, Li SG (2015b) Glutathione S-transferase genes in the rice leaffolder, Cnaphalocrocis medinalis (Lepidoptera: Pyralidae): identification and expression profiles. Arch Insect Biochem Physiol 90:1–13CrossRefPubMedGoogle Scholar
  75. López M, Cano-Ramírez C, Cesar-Ayala AK, Ruiz EA, Zúñiga G (2013) Diversity and expression of P450 genes from Dendroctonus valens LeConte (Curculionidae: Scolytinae) in response to different kairomones. Insect Biochem Mol Biol 43:417–432CrossRefPubMedGoogle Scholar
  76. Loughrin J, Manukian A, Heath RR, Turlings TC, Tumlinson JH (1994) Diurnal cycle of emission of induced volatile terpenoids by herbivore-injured cotton plants. Proc Natl Acad Sci U S A 91:11836–11840CrossRefPubMedPubMedCentralGoogle Scholar
  77. Low WY, Feil SC, Gorman MA, Morton CJ, Pyke J, McConville MJ, Bieri M, Mok YF, Robin C, Gooley PR, Parker MW, Batterham P (2010) Recognition and detoxification of the insecticide DDT by Drosophila melanogaster glutathione S-transferase D1. J Mol Biol 399:358–366CrossRefPubMedGoogle Scholar
  78. Luque T, O’Reilly D (2002) Functional and phylogenetic analyses of a putative Drosophila melanogaster UDP-glycosyltransferase gene. Insect Biochem Mol Biol 32:1597–1604CrossRefPubMedGoogle Scholar
  79. Maïbèche-Coisne M, Jacquin-Joly E, François MC, Nagnan-Le Meillour P (2002) cDNA cloning of biotransformation enzymes belonging to the cytochrome P450 family in the antennae of the noctuid moth Mamestra brassicae. Insect Mol Biol 11:273–281CrossRefPubMedGoogle Scholar
  80. Maïbèche-Coisne M, Merlin C, François MC, Queguiner I, Porcheron P, Jacquin-Joly E (2004a) Putative odorant-degrading esterase cDNA from the moth Mamestra brassicae: cloning and expression patterns in male and female antennae. Chem Senses 29:381–390CrossRefPubMedGoogle Scholar
  81. Maïbèche-Coisne M, Nikonov AA, Ishida Y, Jacquin-Joly E, Leal WS (2004b) Pheromone anosmia in a scarab beetle induced by in vivo inhibition of a pheromone-degrading enzyme. Proc Natl Acad Sci U S A 101:11459–11464CrossRefPubMedPubMedCentralGoogle Scholar
  82. Maïbèche-Coisne M, Merlin C, François MC, Porcheron P, Jacquin-Joly E (2005) P450 and P450 reductase cDNAs from the moth Mamestra brassicae: cloning and expression patterns in male antennae. Gene 346:195–203CrossRefPubMedGoogle Scholar
  83. Mamidala P, Wijeratne AJ, Wijeratne S, Poland T, Qazi SS, Doucet D, Cusson M, Beliveau C, Mittapalli O (2013) Identification of odor-processing genes in the emerald ash borer, Agrilus planipennis. PLoS One 8:e56555CrossRefPubMedPubMedCentralGoogle Scholar
  84. Mane S, Tompkins M, Richmond R (1983) Male esterase 6 catalyzes the synthesis of a sex pheromone in Drosophila melanogaster females. Science 28:419–421CrossRefGoogle Scholar
  85. Matzkin L (2008) The molecular basis of host adaptation in cactophilic Drosophila: molecular evolution of a glutathione S-transferase gene (GstD1) in Drosophila mojavensis. Genetics 178:1073–1083CrossRefPubMedPubMedCentralGoogle Scholar
  86. Mayer MS (1975) Hydrolysis of sex pheromone by the antennae of Trichoplusia ni. Experientia 31:452–454CrossRefPubMedGoogle Scholar
  87. Merlin C, François MC, Bozzolan F, Pelletier J, Jacquin-Joly E, Maïbèche-Coisne M (2005) A new aldehyde oxidase selectively expressed in chemosensory organs of insects. Bioch Biophys Res Comm 332:4–10CrossRefGoogle Scholar
  88. Merlin C, Rosell G, Carot-Sans G, François MC, Bozzolan F, Pelletier J, Jacquin-Joly E, Guerrero A, Maïbèche-Coisne M (2006) Antennal Esterase cDNAs from two pest moths, Sesamia nonagrioides and Spodoptera littoralis, potentially involved in odorant degradation. Insect Mol Biol 16:73–81CrossRefGoogle Scholar
  89. Merrill CE, Riesgo-Escovar J, Pitts RJ, Kafatos FC, Carlson JR, Zwiebel LJ (2002) Visual arrestins in olfactory pathways of Drosophila and the malaria vector mosquito Anopheles gambiae. Proc Natl Acad Sci U S A 99:1633–1638CrossRefPubMedPubMedCentralGoogle Scholar
  90. Merrill CE, Sherertz TM, Walker WB, Zwiebel LJ (2005) Odorant-specific requirements for arrestin function in Drosophila olfaction. J Neurobiol 63:15–28CrossRefPubMedGoogle Scholar
  91. Montagné N, de Fouchier A, Newcomb RD, Jacquin-Joly E (2015) Advances in the identification and characterization of olfactory receptors in insects. Prog Mol Biol Transl Sci 130:55–80CrossRefPubMedGoogle Scholar
  92. Morozova T, Anholt R, Mackay T (2007) Phenotypic and transcriptional response to selection for alcohol sensitivity in Drosophila melanogaster. Genome Biol 8:R231CrossRefPubMedPubMedCentralGoogle Scholar
  93. Nagashima A, Touhara K (2010) Enzymatic conversion of odorants in nasal mucis affects olfactory glomerular activation patterns and odor perception. J Neurosci 30:16391–16398CrossRefPubMedGoogle Scholar
  94. Oakeshott J, Claudianos C, Campbell RM, Newcomb RD, Russel RJ (2005) Biochemical genetics and genomics of insect esterases. In: Gilbert LI, Iatrou K, Gill S (eds) Comprehensive molecular insect science, vol 5. Elsevier, Oxford, pp 309–381CrossRefGoogle Scholar
  95. Oakeshott JG, Johnson RM, Berenbaum MR, Ranson H, Cristino AS, Claudianos C (2010) Metabolic enzymes associated with xenobiotic and chemosensory responses in Nasonia vitripennis. Insect Mol Biol 119:147–163CrossRefGoogle Scholar
  96. Ono H, Ozaki K, Yoshikawa H (2005) Identification of cytochrome P450 and glutathione-S-transferase genes preferentially expressed in chemosensory organs of the swallowtail butterfly, Papilio xuthus L. Insect Biochem Mol Biol 35:837–846CrossRefPubMedGoogle Scholar
  97. Party V, Hanot C, Said I, Rochat D, Renou M (2009) Plant terpenes affect intensity and temporal parameters of pheromone detection in a moth. Chem Senses 34:763–774CrossRefPubMedGoogle Scholar
  98. Pelletier J, Bozzolan F, Solvar M, François MC, Jacquin-Joly E, Maïbèche-Coisne M (2007) Identification of candidate aldehyde oxidases from the silkworm Bombyx mori potentially involved in antennal pheromone degradation. Gene 404:31–40CrossRefPubMedGoogle Scholar
  99. Pophof B (1998) Inhibitors of sensillar esterase reversibly block the responses of moth pheromone receptor cells. J Comp Physiol A 183:153–164CrossRefGoogle Scholar
  100. Pophof B, Gebauer T, Ziegelberger G (2000) Decyl-thio-trifluoropropanone, a competitive inhibitor of moth pheromone receptors. J Comp Physiol A 186:315–323CrossRefPubMedGoogle Scholar
  101. Pottier MA, Bozzolan F, Chertemps T, Jacquin-Joly E, Lalouette L, Siaussat D, Maïbèche-Coisne M (2012) Cytochrome P450s and cytochrome P450 reductase in the olfactory organ of the cotton leafworm Spodoptera littoralis. Insect Mol Biol 21:568–580CrossRefPubMedGoogle Scholar
  102. Prestwich GD, Vogt RG, Riddiford LM (1986) Binding and hydrolysis of radiolabeled pheromone and several analogs by male-specific antennal proteins of the moth Antheraea polyphemus. J Chem Ecol 12:323–333CrossRefPubMedGoogle Scholar
  103. Prestwich GD, McG Graham S, Handley M, Latli B, Streinz L, Tasayco MLJ (1989) Enzymatic processing of pheromones and pheromone analogs. Experientia 45:263–270CrossRefGoogle Scholar
  104. Quero C, Camps F, Guerrero A (1995) Behavior of processionary males (Thaumetopoea pityocampa) induced by sex pheromone and analogs in a wind tunnel. J Chem Ecol 21:1957–1969CrossRefPubMedGoogle Scholar
  105. Renou M, Guerrero A (2000) Insect parapheromones in olfaction research and semiochemical-bases pest control strategies. Annu Rev Entomol 48:605–630CrossRefGoogle Scholar
  106. Renou M, Lucas P, Malo E, Guerrero A (1997) Effects of trifluoromethyl ketones and related compounds on the EAG and behavioural responses to pheromones in male moths. Chem Senses 22:407–416CrossRefPubMedGoogle Scholar
  107. Richmond R, Gilbert DG, Sheehan KB, Gromko MH, Butterworth FM (1980) Esterase 6 and reproduction in Drosophila melanogaster. Science 207:1483–1485CrossRefPubMedGoogle Scholar
  108. 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 272:14792–14799CrossRefPubMedGoogle Scholar
  109. Rogers M, Jani M, Vogt R (1999) An olfactory-specific gluthanione S-transferase in the sphinx moth Manduca sexta. J Exp Biol 202:1625–1637PubMedGoogle Scholar
  110. Ronderos D, Smith D (2010) Activation of the T1 neuronal circuit is necessary and sufficient to induce sexually dimorphic mating behavior in Drosophila melanogaster. J Neurosci 17:2595–2599CrossRefGoogle Scholar
  111. Rützler M, Zwiebel L (2005) Molecular biology of insect olfaction: recent progress and conceptual models. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 191:777–790CrossRefPubMedGoogle Scholar
  112. Rybczynski R, Reagan J, Lerner M (1989) A pheromone-degrading aldehyde-oxidase in the antennae of the moth Manduca sexta. J Neurosci 9:1341–1353CrossRefPubMedGoogle Scholar
  113. Rybczynski R, Vogt RG, Lerner M (1990) Antennal-specific pheromone-degrading aldehyde oxidases from the moths Antheraea polyphemus and Bombyx mori. J Biol Chem 265:19712–19715PubMedGoogle Scholar
  114. Saisawang C, Wongsantichon J, Ketterman A (2012) A preliminary characterization of the cytosolic glutathione transferase proteome from Drosophila melanogaster. Biochem J 442:181–190CrossRefPubMedGoogle Scholar
  115. Sheehan K, Richmond R, Cochrane B (1979) Studies of esterase 6 in Drosophila melanogaster. III. The developmental pattern and tissue distribution. Insect Biochem 9:443–450CrossRefGoogle Scholar
  116. Siaussat D, Chertemps T, Maïbèche M (2014) Detoxification, stress and immune responses in insect antenna: new insights from transcriptomics. In: Chandrasekar R (ed) Short views on insect molecular biology. Bharathidasan University, Trichy, pp 75–98Google Scholar
  117. Steinbrecht RA, Osaki M, Ziegelberger G (1992) Immunological localization of pheromone-binding proteins in moth antennae. Cell Tissue Res 270:287–302CrossRefGoogle Scholar
  118. Syed Z, Ishida Y, Taylor K, Kimbrell DA, Leal WS (2006) Pheromone reception in fruit flies expressing a moth’s odorant receptor. Proc Natl Acad Sci U S A 103:16538–16543Google Scholar
  119. Tan X, Hu XM, Zhong XW, Chen QM, Xia QY, Zhao P (2014) Antenna-specific glutathione S-transferase in male silkmoth Bombyx mori. Int J Mol Sci 15:7429–7443CrossRefPubMedPubMedCentralGoogle Scholar
  120. Tasayco M, Prestwich GD (1990a) A specific affinity reagent to distinguish aldehyde dehydrogenases and oxidases. Enzymes catalyzing aldehyde oxidation in an adult moth. J Biol Chem 265:3094–3101PubMedGoogle Scholar
  121. Tasayco M, Prestwich GD (1990b) Aldehyde oxidases and dehydrogeneses in antennae of five moth species. Insect Biochem 20:691–700CrossRefGoogle Scholar
  122. Tasayco M, Prestwich GD (1990c) Aldehyde-oxidizing enzymes in an adult moth: in vitro study of aldehyde metabolism in Heliothis virescens. Arch Biochem Biophys 278:444–451CrossRefPubMedGoogle Scholar
  123. Taylor TR, Ferkovich SM, van Essen F (1981) Increased pheromone catabolism by antennal esterases after adult eclosion of the cabbage looper moth. Experientia 37:729–731CrossRefGoogle Scholar
  124. Thiebaud N, Veloso Da Silvia S, Jakob I, Sicard G, Chevalier J, Ménétrier F, Berdeaux O, Artur Y, Heydel JM, Le Bon AM (2013) Odorant metabolism catalyzed by olfactory mucosal enzymes influences peripheral olfactory responses in rats. PLoS One 8:e59547CrossRefPubMedPubMedCentralGoogle Scholar
  125. Tijet N, Helvig C, Feyereisen R (2001) The cytochrome P450 gene superfamily in Drosophila melanogaster: annotation, intron-exon organization and phylogeny. Gene 262:189–198CrossRefPubMedGoogle Scholar
  126. Tillman JA, Seybold SJ, Jurenka RA, Blomquist GJ (1999) Insect pheromones – an overview of biosynthesis and endocrine regulation. Insect Biochem Mol Biol 29:481–514CrossRefPubMedGoogle Scholar
  127. Tu C, Akgü B (2005) Drosophila glutathione S-transferases. Methods Enzymol 401:204–226CrossRefPubMedGoogle Scholar
  128. Vogt RG (2003) Biochemical diversity of odor detection: OBPs, ODEs and SNMPs. In: Blomquist GJ, Vogt RG (eds) Insect pheromone biochemistry and molecular miology – the biosynthesis and detection of pheromones and plant volatiles. Elsevier Academic Press, London/San Diego, pp 391–445CrossRefGoogle Scholar
  129. Vogt RG (2005) Molecular basis of pheromone detection in insects. In: Gilbert LI, Iatrou K, Gill S (eds) Comprehensive insect physiology, biochemistry, pharmacology and molecular biology, Endocrinology, vol 3. Elsevier, London, pp 753–804Google Scholar
  130. Vogt RG, Riddiford LM (1981) Pheromone binding and inactivation by moth antennae. Nature 293:161–163CrossRefGoogle Scholar
  131. Vogt RG, Riddiford LM, Prestwich GD (1985) Kinetic properties of a sex pheromone-degrading enzyme: the sensillar esterase of Antheraea polyphemus. Proc Natl Acad Sci U S A 82:8827–8831CrossRefPubMedPubMedCentralGoogle Scholar
  132. Wang B, Shahzad MF, Zhang Z, Sun H, Han P, Li F, Han Z (2014) Genome-wide analysis reveals the expansion of cytochrome P450 genes associated with xenobiotic metabolism in rice striped stem borer, Chilo suppressalis. Biochem Biophys Res Commun 443:756–760CrossRefPubMedGoogle Scholar
  133. Wang L, Anderson D (2010) Identification of an aggression-promoting pheromone and its receptor neurons in Drosophila. Nature 463:227–231CrossRefPubMedGoogle Scholar
  134. Wang L, Dankert H, Perona P, Anderson DJ (2008) A common genetic target for environmental and heritable influences on aggressiveness in Drosophila. Proc Natl Acad Sci U S A 105:5657–5663CrossRefPubMedPubMedCentralGoogle Scholar
  135. Wang SP, He GL, Chen RR, Li F, Li GQ (2012) The involvement of cytochrome P450 monooxygenases in methanol elimination in Drosophila melanogaster larvae. Arch Insect Biochem Physiol 79:264–275CrossRefPubMedGoogle Scholar
  136. Wang SP, Hu XX, Meng QW, Muhammad SA, Chen RR, Li F, Li GQ (2013) The involvement of several enzymes in methanol detoxification in Drosophila melanogaster adults. Comp Biochem Physiol B Biochem Mol Biol 166:7–14CrossRefPubMedGoogle Scholar
  137. Wojtasek H, Leal WS (1999) Degradation of an alkaloid pheromone from the pale-brown chafer, Phyllopertha diversa (Coleoptera: Scarabaeidae), by an insect olfactory cytochrome P450. FEBS Lett 458:333–336CrossRefPubMedGoogle Scholar
  138. Wu Z, Bin S, He H, Wang Z, Li M, Lin J (2016) Differential expression analysis of chemoreception genes in the striped flea beetle Phyllotreta striolata using a transcriptomic approach. PLoS One 11:e0153067CrossRefPubMedPubMedCentralGoogle Scholar
  139. Xuan N, Guo X, Xie HY, Lou XB, Liu GX, Picimbon JF (2015) Increased expression of CSP and CYP genes in adult silkworm females exposed to avermectins. Insect Sci 22:203–219CrossRefPubMedGoogle Scholar
  140. Younus F, Chertemps T, Pearce SL, Pandey G, Bozzolan F, Coppin CW, Russel RJ, Maïbèche-Coisne M, Oakeshott JG (2014) Identification of candidate odorant degrading gene/enzyme systems in the antennal transcriptome of Drosophila melanogaster. Insect Biochem Mol Biol 53:30–43CrossRefGoogle Scholar
  141. Yu Q, Lu C, Li B, Fang S, Zuo W, Dai F, Zhang Z, Xiang Z (2008) Identification, genomic organization and expression pattern of glutathione S-transferase in the silkworm, Bombyx mori. Insect Biochem Mol Biol 38:1158–1164CrossRefPubMedGoogle Scholar
  142. Yu Q, Lu C, Li WL, Xiang ZH, Zhang Z (2009) Annotation and expression of carboxylesterases in the silkworm, Bombyx mori. BMC Genomics 40:100–112Google Scholar
  143. Zhang YN, Xia YH, Zhu JY, Li SY, Dong SL (2014) Putative pathway of sex pheromone biosynthesis and degradation by expression patterns of genes identified from female pheromone gland and adult antenna of Sesamia inferens (Walker). J Chem Ecol 40:439–451CrossRefPubMedGoogle Scholar
  144. Zhao Y, Li H, Miao X (2015) Proteomic analysis of silkworm antennae. J Chem Ecol 41:1037–1042CrossRefPubMedGoogle Scholar
  145. Ziegelberger G (1995) Redox-shift of the pheromone-binding protein in the silkmoth Antheraea polyphemus. Eur J Biochem 232:706–711CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Claudia Steiner
    • 1
  • Thomas Chertemps
    • 2
  • Martine Maïbèche
    • 2
    Email author
  1. 1.Institut d’Ecologie et des Sciences de l’Environnement de ParisSorbonne Université, UPEC, Univ. P7, INRA, CNRS, IRDParisFrance
  2. 2.UMR 7618 iEES-Paris, Sorbonne Université, CNRS, INRA, IRDParisFrance

Personalised recommendations