Cloning of an octopamine/tyramine receptor and plasticity of its expression as a function of adult sexual maturation in the male moth Agrotis ipsilon

Insect Molecular Biology

Volumn 19, Issue 4, 2010, Pages 489-499

  Duportets, L ^a   Barrozo, R B ^b   Bozzolan, F ^a   Gaertner, C ^b   Anton, S ^b   Gadenne, C ^b   Debernard, S ^a  

^a SORBONNE UNIVERSITÉ   (France)

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

Author keywords

antennal lobe; expression plasticity; maturation; octopamine tyramine receptor; olfactory processing

Indexed keywords

NORSYNEPHRINE RECEPTOR; RECEPTOR; TYRAMINE RECEPTOR;

AGING; AMINO ACID SEQUENCE; ANIMAL; ARTICLE; CHEMISTRY; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; ISOLATION AND PURIFICATION; MALE; MOLECULAR CLONING; MOLECULAR GENETICS; MOTH; NUCLEOTIDE SEQUENCE; PHYLOGENY; SEQUENCE HOMOLOGY; SEXUAL MATURATION;

AGING; AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CLONING, MOLECULAR; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MALE; MOLECULAR SEQUENCE DATA; MOTHS; PHYLOGENY; RECEPTORS, BIOGENIC AMINE; SEQUENCE HOMOLOGY, AMINO ACID; SEXUAL MATURATION;

AGROTIS IPSILON; LEPIDOPTERA;

EID: 77954339408     PISSN: 09621075     EISSN: 13652583     Source Type: Journal    
DOI: 10.1111/j.1365-2583.2010.01009.x     Document Type: Article

References (76)

1. Anton, S. Gadenne, C. (1999) Effect of juvenile hormone on the central nervous processing of sex pheromone in an insect. Proc Natl Acad Sci U S A 96 : 5764 5767.
2. Arakawa, S., Gocayne, J.D., McCombie, W.R., Urquhart, D.A., Hall, L.M., Fraser, C.M. et al 1990) Cloning, localization, and permanent expression of a Drosophila octopamine receptor. Neuron 4 : 343 354.
3. Baldwin, J.M., Schertler, G.F. Unger, V.M. (1997) An alpha-carbon template for the transmembrane helices in the rhodopsin family of G-protein-coupled receptors. J Mol Biol 272 : 144 164.
4. Barron, A.B., Schulz, D.J. Robinson, G.E. (2002) Octopamine modulates responsiveness to foraging-related stimuli in honey bees (Apis mellifera). J Comp Physiol 188 : 603 610.
5. Barrozo, R.B., Jarriault, D., Simeone, X., Gaertner, C., Gadenne, C. Anton, S. (2010) Mating-induced transient inhibition of responses to sex pheromone in a male moth is not mediated by octopamine or serotonin. J Exp Biol 213 : 1100 1106.
6. Blenau, W. Baumann, A. (2001) Molecular and pharmacological properties of insect biogenic amine receptors: lessons from Drosophila melanogaster and Apis mellifera. Arch Insect Biochem Physiol 48 : 13 38.
7. Blenau, W., Balfanz, S. Baumann, A. (2000) Amtyr1: Characterization of a gene from honeybee (Apis mellifera) brain encoding a functional tyramine receptor. J Neurochem 74 : 900 908.
8. Bräunig, P. (1991) Suboesophageal DUM neurons innervate the principal neuropiles of the locust brain. Phil Trans R Soc Lond B 332 : 221 240.
9. Brigaud, I., Grosmaître, X., François, M.C. Jacquin-Joly, E. (2009) Cloning and expression pattern of a putative octopamine/tyramine receptor in antennae of the noctuid moth Mamestra brassicae. Cell Tissue Res 335 : 455 463.
10. Connolly, J.B., Roberts, I.J., Armstrong, J.D., Kaiser, K., Forte, M., Tully, T. et al 1996) Associative learning disrupted by impaired Gs signaling in Drosophila mushroom bodies. Science 274 : 2104 2107.
11. Corpet, F. (1988) Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res 16 : 10881 10890.
12. Dacks, A.M., Christensen, T.A., Agricola, H.J., Wollweber, L. Hildebrand, J.G. (2005) Octopamine-immunoreactive neurons in the brain and subesophageal ganglion of the hawkmoth Manduca sexta. J Comp Neurol 488 : 255 268.
13. David, J.C. Coulon, J.F. (1985) Octopamine in invertebrates and vertebrates. Prog Neurobiol 24 : 141 185.
14. Dixon, R.A., Sigal, I.S., Candelore, M.R., Register, R.B., Scattergood, W., Rands, E. et al 1987) Structural features required for ligand binding to the beta-adrenergic receptor. EMBO J 6 : 3269 3275.
15. Donini, A. Lange, A.B. (2004) Evidence for a possible neurotransmitter/neuromodulator role of tyramine on the locust oviducts. J Insect Physiol 50 : 351 361.
16. Downer, R.G.H., Hiripi, L. Juhos, S. (1993) Characterization of the tyraminergic system in the central nervous system of the locust, Locusta migratoria migratoides. Neurochem Res 18 : 1245 1248.
17. Duportets, L., Dufour, M.C., Couillaud, F. Gadenne, C. (1998) Biosynthetic activity of corpora allata, growth of sex accessory glands and mating in the male moth Agrotis ipsilon (Hufnagel). J Exp Biol 201 : 2425 2432.
18. Evans, P.D. (1980) Biogenic amines in the insect nervous system. Adv Insect Physiol 15 : 317 473.
19. Evans, P.D. Maqueira, B. (2005) Insect octopamine receptors: a new classification scheme based on studies of cloned Drosophila G-protein coupled receptors. Invert Neurosci 5 : 111 118.
20. Evans, P.D., Robb, S., Cheek, T.R., Reale, V., Hannan, F.L., Swales, L.S. et al 1995) Agonist-specific coupling of G-protein-coupled receptors to second messenger systems. Prog Brain Res 106 : 259 268.
21. Farooqui, T. (2007a) Octopamine-mediated neuromodulation of insect senses. Neurochem Res 32 : 1511 1529.
22. Farooqui, T. (2007b) Octopamine-mediated neuronal plasticity in honeybees: implications for olfactory dysfunction in humans. Neuroscientist 13 : 304 322.
23. Farooqui, T., Robinson, K., Vaessin, H. Smith, B.H. (2003) Modulation of early olfactory processing by an octopaminergic reinforcement pathway in the honeybee. J Neurosci 23 : 5370 5380.
24. Fox, L.E., Soll, D.R. Wu, C.F. (2006) Coordination and modulation of locomotion pattern generators in Drosophila larvae: effects of altered biogenic amine levels by the tyramine β-hydroxylase mutation. J Neurosci 26 : 1486 1498.
25. Fraser, C.M., Chung, F.Z., Wang, C.D. Venter, J.C. (1988) Site-directed mutagenesis of human beta-adrenergic receptors: substitution of aspartic acid-130 by asparagine produces a receptor with high-affinity agonist binding that is uncoupled from adenylate cyclase. Proc Natl Acad Sci U S A 85 : 5478 5482.
26. Gadenne, C. Anton, S. (2000) Central processing of sex pheromone stimuli is differentially regulated by juvenile hormone in a male moth. J Insect Physiol 46 : 1195 1206.
27. Gadenne, C., Renou, M. Sreng, L. (1993) Hormonal control of pheromone responsiveness in the male black cutworm Agrotis ipsilon. Experentia 49 : 721 724.
28. Grohmann, L., Blenau, W., Erber, J., Ebert, P.R., Strünker, T. Baumann, A. (2003) Molecular and functional characterization of an octopamine receptor from honeybee (Apis mellifera) brain. J Neurochem 86 : 725 735.
29. Grosmaitre, X., Marion-Poll, F. Renou, M. (2001) Biogenic amines modulate olfactory receptor neurons firing activity in Mamestra brassicae. Chem Senses 26 : 653 661.
30. Homberg, U. (1994) Distribution or neurotransmitters in the insect brain. In Progress in Zoology (Rathmayer, W. Fischer, G., eds), pp. 1 88. Jena
31. Huber, R. (2005) Amines and motivated behaviors: a simpler systems approach to complex behavioral phenomena. J Comp Physiol 191 : 231 239.
32. Humphries, M.A., Mustard, J.A., Hunter, S.J., Mercer, A., Ward, V. Ebert, P.R. (2003) Invertebrate D2 type dopamine receptor exhibits age-based plasticity of expression in the mushroom bodies of the honeybee brain. J Neurobiol 55 : 315 330.
33. Iwano, M. Kanzaki, R. (2005) Immunocytochemical identification of neuroactive substances in the antennal lobe of the male silkworm moth Bombyx mori. Zoolog Sci 22 : 199 211.
34. Jarriault, D., Barrozo, R.B., de Carvalho Pinto, C.J., Greiner, B., Dufour, M.C., Masante-Roca, I. et al 2009) Age-dependent plasticity of sex pheromone response in the moth, Agrotis ipsilon: combined effects of octopamine and juvenile hormone. Horm Behav 56 : 185 191.
35. Kenakin, T. (1995) Agonist-receptor efficacy. II. Agonist trafficking of receptor signals. Trends Pharmacol Sci 16 : 232 238.
36. Kononenko, N.L., Wolfenberg, H. Pflüger, H.J. (2009) Tyramine as an independent transmitter and a precursor of octopamine in the locust central nervous system: an immunocytochemical study. J Comp Neurol 512 : 433 452.
37. Kreissl, S., Eichmüller, S., Bicker, G., Rapus, J. Eckert, M. (1994) Octopamine-like immunoreactivity in the brain and subesophageal ganglion of the honeybee. J Comp Neurol 348 : 583 595.
38. Kutsukake, M., Komatsu, A., Yamamoto, D. Ishiwa-Chigusa, S. (2000) A tyramine receptor gene mutation causes a defective olfactory behavior in Drosophila melanogaster. Gene 245 : 31 42.
39. Lange, A.B. (2009) Tyramine: from octopamine precursor to neuroactive chemical in insects. Gen Comp Endocrinol 162 : 18 26.
40. Libersat, F. Pflueger, H.J. (2004) Monoamines and the orchestration of behavior. BioScience 54 : 17 25.
41. Linn, C.E. Roelofs, W. (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 : 161 172.
42. Linn, C.E. Roelofs, W. (1992) Role of photoperiod cues in regulating the modulatory action of octopamine on pheromone-response thresholds in the cabbage looper moth. Arch Insect Biochem Physiol 20 : 285 302.
43. Linn, C.E., Campbell, M.G. Roelofs, W.L. (1992) Photoperiod cues and the modulatory action of octopamine and 5-hydroxytryptamine on locomotor and pheromone in male gypsy moths, Lymantria dispar. Arch Insect Biochem Physiol 20 : 265 284.
44. Linn, C.E., Campbell, M.G., Poole, K.R., Wu, W.Q. Roelofs, W.L. (1996) Effects of photoperiod on the circadian timing of pheromone response in male Trichoplusia ni: relationship to the modulatory action of octopamine. J Insect Physiol 42 : 881 891.
45. Menzel, R. (2001) Searching for the memory trace in a mini-brain, the honeybee. Learn Mem 8 : 53 62. (Pubitemid 32297801)
46. Menzel, R. Muller, U. (1996) Learning and memory in honeybees: from behavior to neural substrates. Annu Rev Neurosci 19 : 379 404.
47. Molaei, G., Paluzzi, J.P., Bendena, W.G. Lange, A.B. (2005) Isolation, cloning, and tissue expression of a putative octopamine/tyramine receptor from locust visceral muscle tissues. Arch Insect Biochem Physiol 59 : 132 149.
48. Mustard, J.A., Kurshan, P.T., Hamilton, I.S., Blenau, W. Mercer, A.R. (2005) Developmental expression of a tyramine receptor gene in the brain of the honey bee, Apis mellifera. J Comp Neurol 483 : 66 75.
49. Nagaya, Y., Kutsukake, M., Chigusa, S.I. Komatsu, A. (2002) A trace amine, tyramine, functions as a neuromodulator in Drosophila melanogaster. Neurosci Lett 329 : 324 328.
50. O'Dowd, B.F., Hnatowich, M., Caron, M.G., Lefkowitz, R.J. Bouvier, M. (1989) Palmitoylation of the human beta 2-adrenergic receptor. Mutation of Cys341 in the carboxyl tail leads to an uncoupled nonpalmitoylated form of the receptor. J Biol Chem 264 : 7564 7569.
51. Ohta, H., Utsumi, T. Ozoe, Y. (2003) B96Bom encodes a Bombyx mori tyramine receptor negatively coupled to adenylate cyclase. Insect Mol Biol 12 : 217 223.
52. Ohtani, A., Arai, Y., Ozoe, F., Ohta, H., Narusuye, K., Huang, J. et al 2006) Molecular cloning and heterologous expression of an alpha-adrenergic-like octopamine receptor from the silkworm Bombyx mori. Insect Mol Biol 15 : 763 772.
53. Oliveira, L., Paiva, A.C. Vriend, G. (1999) A low resolution model for the interaction of G proteins with G protein-coupled receptors. Protein En 12 : 1087 1095.
54. Poels, J., Suner, M.M., Needham, M., Torfs, H., De Rijck, J., De Loof, A. et al 2001) Functional expression of a locust tyramine receptor in murine erythroleukaemia cells. Insect Mol Biol 10 : 541 548.
55. Poitout, S. Bues, R. (1974) Linolenic acid requirements of lepidoptera Noctuidae Quadrifinae Plusiinae: Chrysodeixis chalcites Esp., Autographa gamma L.' Macdunnoughia confusa Stph., Trichoplusia ni Hbn. reared on artificial diets. Ann Nutr Aliment 28 : 173 187.
56. Robb, S., Cheek, T.R., Hannan, F.L., Hall, L.M., Midgley, J.M. Evans, P.D. (1994) Agonist-specific coupling of a cloned Drosophila octopamine/tyramine receptor to multiple second messenger systems. EMBO J 13 : 1325 1330.
57. Robinson, G.E., Heuser, L.M., Le Conte, Y., Lenquette, F. Hollingworth, R.M. (1999) Neurochemicals aid bee nestmate recognition. Nature 399 : 534 535.
58. Roeder, T. (1999) Octopamine in invertebrates. Prog Neurobiol 59 : 533 536.
59. Roeder, T. (2005) Tyramine and octopamine: ruling behavior and metabolism. Annu Rev Entomol 50 : 447 477.
60. Roeder, T., Seifert, M., Kähler, C. Gewecke, M. (2003) Tyramine and octopamine: antagonistic modulators of behavior and metabolism. Arch Insect Biochem Physiol 54 : 1 13.
61. Rogers, S.M., Matheson, T., Sasaki, K., Kendrick, K., Simpson, S.J. Burrows, M. (2004) Substantial changes in central nervous system neurotransmitters and neuromodulators accompany phase change in locust. J Exp Biol 207 : 3603 3617.
62. Roman, G. Davis, R.L. (2001) Molecular biology and anatomy of Drosophila olfactory associative learning. Bioessays 23 : 571 581.
63. Saraswati, S., Fox, L.E., Soll, D.R. Wu, C.F. (2004) Tyramine and octopamine have opposite effects on the locomotion of Drosophila larvae. J Neurobiol 58 : 425 441.
64. Sasaki, K. Harano, K.I. (2007) Potential effects of tyramine on the transition to reproductive workers in honeybees (Apis mellifera L. Physiol Entomol 32 : 194 198.
65. Saudou, F., Amlaiky, N., Plassat, J.L., Borrelli, E. Hen, R. (1990) Cloning and characterization of a Drosophila tyramine receptor. EMBO J 9 : 3611 3617.
66. Scheiner, R., Plückhahn, S., Oney, B., Blenau, W. Erber, J. (2002) Behavioural pharmacology of octopamine, tyramine and dopamine in honey bees. Behav Brain Res 136 : 545 553.
67. Schulz, D.J., Sullivan, J.P. Robinson, G.E. (2002) Juvenile hormone and octopamine in the regulation of division of labor in honeybee colonies. Horm Behav 42 : 222 231.
68. Stern, M., Thompson, K.S.J., Zhon, P., Watson, D.G., Midgley, J.M., Gewecke, M. et al 1995) Octopaminergic neurons in the locust brain: morphological, biochemical and electrophysiological characterisation of potential modulators of the visual system. J Comp Physiol 177A : 611 625.
69. Strader, C.D., Candelore, M.R., Hill, W.S., Sigal, I.S. Dixon, R.A. (1989) Identification of two serine residues involved in agonist activation of the beta-adrenergic receptor. J Biol Chem 264 : 13572 13578.
70. Strader, C.D., Fong, T.M., Graziano, M.P. Tota, M.R. (1995) The family of G-protein-coupled receptors. FASEB J 9 : 745 754.
71. Sunghoon, L., Byungwook, L., Insoo, J., Sangsoo, K. Jong, B. (2006) Localizome: a server for identifying transmembrane topologies and TM helices of eukaryotic proteins utilizing domain information. Nucleic Acids Res 34 : 99 103.
72. Tamura, K., Dudley, J., Nei, M. Kumar, S. (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24 : 1596 1599.
73. Valdenaire, O. Vernier, P. (1997) G protein coupled receptors as modules of interacting proteins: a family meeting. Prog Drug Res 49 : 173 218.
74. Vanden Broeck, J., Vulsteke, V., Huybrechts, R. De Loof, A. (1995) Characterization of a cloned locust tyramine receptor cDNA by functional expression in permanently transformed Drosophila S2 cells. J Neurochem 64 : 2387 2395.
75. Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B., Van Roy, N., De Paepe, A. et al 2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 18 : 3:RESEARCH0034.
76. Von Nickisch-Rosenegk, E.V., Krigger, J., Kubick, S., Laage, R., Strobel, J., Strotmann, J. et al 1996) Cloning of biogenic amine receptor from moths (Bombyx mori and Heliothis virescens). Insect Biochem Mol Biol 26 : 817 827.