The GPCR membrane receptor, DopEcR, mediates the actions of both dopamine and ecdysone to control sex pheromone perception in an insect

Frontiers in Behavioral Neuroscience

Volumn 8, Issue SEP, 2014, Pages

  Abrieux, Antoine ^a,b   Duportets, Line ^b,c   Debernard, Stéphane ^b   Gadenne, Christophe ^a   Anton, Sylvia ^a  

^a UNIVERSITÉ D'ANGERS   (France)

^b UPMC University Paris 06   (France)

^c UNIVERSITÉ PARIS SACLAY   (France)

Author keywords

Antennal lobe; Dopamine; Ecdysone; GPCR; Insect; Wind tunnel

Indexed keywords

CELL NUCLEUS RECEPTOR; DOPAMINE; DOUBLE STRANDED RNA; ECDYSONE; ECDYSONE RECEPTOR; ECDYSTERONE; G PROTEIN COUPLED RECEPTOR; PROTEIN DOPECR; SEX PHEROMONE; ULTRASPIRACLE; UNCLASSIFIED DRUG;

ADULT; AGROTIS IPSILON; ANIMAL EXPERIMENT; ANTENNAL LOBE NEURON; ARTICLE; CONTROLLED STUDY; FEMALE; GENE SILENCING; MALE; NERVE CELL; NEUROMODULATION; NONHUMAN; PERCEPTION; SEX PHEROMONE PERCEPTION; SEXUAL BEHAVIOR;

EID: 84908161708     PISSN: 16625153     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnbeh.2014.00312     Document Type: Article

References (50)

1. Abrieux, A., Debernard, S., Maria, A., Gaertner, C., Anton, S., Gadenne, C., et al. (2013). Involvement of the G-protein-coupled dopamine/ecdysteroid receptor dopecr in the behavioral response to sex pheromone in an insect. PLoS One 8:e72785. doi: 10.1371/journal.pone.0072785
2. Anton, S., Dufour, M.-C., and Gadenne, C. (2007). Plasticity of olfactory-guided behaviour and its neurobiological basis: lessons from moths and locusts. Entomol. Exp. Appl. 123, 1-11. doi: 10.1111/j.1570-7458.2007.00516.x
3. Anton, S., and 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. doi: 10.1073/pnas.96.10.5764
4. Barrozo, R. B., Gadenne, C., and Anton, S. (2010). Switching attraction to inhibition: mating-induced reversed role of sex pheromone in an insect. J. Exp. Biol. 213, 2933-2939. doi: 10.1242/jeb.043430
5. Bigot, L., Shaik, H. A., Bozzolan, F., Party, V., Lucas, P., Debernard, S., et al. (2012). Peripheral regulation by ecdysteroids of olfactory responsiveness in male Egyptian cotton leaf worms, Spodoptera littoralis. Insect Biochem. Mol. Biol. 42, 22-31. doi: 10.1016/j.ibmb.2011.10.003
6. Blenau, W., and 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. doi: 10.1002/arch.1055
7. Bloch, G., and Meshi, A. (2007). Influences of octopamine and juvenile hormone on locomotor behavior and period gene expression in the honeybee, Apis mellifera. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 193, 181-199. doi: 10.1007/s00359-006-0179-5
8. Causse, R., Buès, R., Barthes, J., and Toubon, J. (1988). "Mise en évidence expérimentale de nouveaux constituants des phéromones sexuelles de Scotia ipsilon et Mamestra suasa," in Médiateurs Chimiques: Comportement et Systématique des Lépidoptères. Coll. INRA no. 46, ed INRA (Paris: INRA), 75-82.
9. Christensen, T. A., and Hildebrand, J. G. (1987). Male-specific, sex pheromone-selective projection neurons in the antennal lobes of the moth, Manduca sexta. J. Comp. Physiol. A 160, 553-569. doi: 10.1007/bf00611929
10. Cooper, R. L., and Ruffner, M. E. (1998). Depression of synaptic efficacy at intermolt in crayfish neuromuscular junctions by 20-hydroxyecdysone, a molting hormone. J. Neurophysiol. 79, 1931-1941.
11. Duportets, L., Barrozo, R. B., Bozzolan, F., Gaertner, C., Anton, S., Gadenne, C., et al. (2010). 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 Mol. Biol. 19, 489-499. doi: 10.1111/j.1365-2583.2010.01009.x
12. Duportets, L., Maria, A., Vitecek, S., Gadenne, C., and Debernard, S. (2013). Steroid hormone signaling is involved in the age-dependent behavioral response to sex pheromone in the adult male moth Agrotis ipsilon. Gen. Comp. Endocrinol. 186, 58-66. doi: 10.1016/j.ygcen.2013.02.024
13. 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. doi: 10.1016/s00796123(08)61222-4
14. Evans, P., Srivastava, D., and Reale, V. (2009). "Rapid, non-genomic responses to ecdysteroids and catecholamines mediated by a novel Drosophila G-Protein-coupled receptor," in Ecdysone: Structures and Functions, ed G. Smagghe (New York: Springer), 425-443.
15. Fahrbach, S. E., Smagghe, G., and Velarde, R. A. (2012). Insect nuclear receptors. Annu. Rev. Entomol. 57, 83-106. doi: 10.1146/annurev-ento-120710-100607
16. Gadenne, C., and 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. doi: 10.1016/s0022-1910(00)00040-8
17. Gadenne, C., Renou, M., and Sreng, L. (1993). Hormonal control of sex pheromone responsiveness in the male black cutworm, Agrotis ipsilon. Experientia 49, 721-724. doi: 10.1007/bf01923960
18. Geddes, L. H., Mcquillan, H. J., Aiken, A., Vergoz, V., and Mercer, A. R. (2013). Steroid hormone (20-hydroxyecdysone) modulates the acquisition of aversive olfactory memories in pollen forager honeybees. Learn. Mem. 20, 399-409. doi: 10.1101/lm.030825.113
19. Gemeno, C., and Haynes, K. F. (1998). Chemical and behavioral evidence for a third pheromone component in a north american population of the black cutworm moth, Agrotis ipsilon. J. Chem. Ecol. 24, 999-1011. doi: 10.1023/A:1022398318465
20. Gruntenko, N. E., Karpova, E. K., Alekseev, A. A., Chentsova, N. A., Bogomolova, E. V., Bownes, M., et al. (2007). Effects of octopamine on reproduction, juvenile hormone metabolism, dopamine and 20-hydroxyecdysone contents in Drosophila. Arch. Insect Biochem. Physiol. 65, 85-94. doi: 10.1002/arch.20187
21. Hull, E. M. (2011). Sex, drugs and gluttony: how the brain controls motivated behaviors. Physiol. Behav. 104, 173-177. doi: 10.1016/j.physbeh.2011.04.057
22. Hull, E. M., Muschamp, J. W., and Sato, S. (2004). Dopamine and serotonin: influences on male sexual behavior. Physiol. Behav. 83, 291-307. doi: 10.1016/j.physbeh.2004.08.018
23. Inagaki, H. K., Bentabou De-Leon, S., Wong, A. M., Jagadish, S., Ishimoto, H., Barnea, G., et al. (2012). Visualizing neuromodulation in vivo: TANGO-mapping of dopamine signaling reveals appetite control of sugar sensing. Cell 148, 583-595. doi: 10.1016/j.cell.2011.12.022
24. Ishimoto, H., Wang, Z., Rao, Y., Wu, C.-F., and Kitamoto, T. (2013). A novel role for ecdysone in Drosophila conditioned behavior: linking GPCR-mediated non-canonical steroid action to cAMP signaling in the adult brain. PLoS Genet. 9:e1003843. doi: 10.1371/journal.pgen.1003843
25. 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. doi: 10.1016/j.yhbeh.2009.04.005
26. Keleman, K., Vrontou, E., Krüttner, S., Yu, J. Y., Kurtovic-Kozaric, A., and Dickson, B. J. (2012). Dopamine neurons modulate pheromone responses in Drosophila courtship learning. Nature 489, 145-149. doi: 10.1038/nature11345
27. Kenakin, T. (1995). Agonist-receptor efficacy II: agonist trafficking of receptor signals. Trends Pharmacol. Sci. 16, 232-238. doi: 10.1016/s0165-6147(00)89032-x
28. Kravitz, E. A. (2000). Serotonin and aggression: insights gained from a lobster model system and speculations on the role of amine neurons in a complex behavior. J. Comp. Physiol. A 186, 221-238. doi: 10.1007/s003590050423
29. Lange, A. B. (2009). Tyramine: from octopamine precursor to neuroactive chemical in insects. Gen. Comp. Endocrinol. 162, 18-26. doi: 10.1016/j.ygcen.2008.05.021
30. Lehman, K. K., Klukas, K. A., Gilchrist, L. S., and Mesce, K. A. (2000). Steroid regulation of octopamine expression during metamorphic development of the moth Manduca sexta. J. Comp. Neurol. 424, 283-296. doi: 10.1002/1096-9861(20000821)424:2<283::AID-CNE7>3.0.CO;2-Z
31. Li, H., Harrison, D., Jones, G., Jones, D., and Cooper, R. L. (2001). Alterations in development, behavior and physiology in Drosophila larva that have reduced ecdysone production. J. Neurophysiol. 85, 98-104.
32. Linn, C. E., Campbell, M. G., and 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. doi: 10.1002/arch.940200404
33. Linn, C. E., Poole, K. R., and Roelofs, W. L. (1994). Studies on biogenic amines and their metabolites in nervous tissue and hemolymph of adult male cabbage looper moths. III. Fate of injected octopamine 5-hydroxy tryptamine and dopamine. Comp. Biochem. Physiol. 108, 99-106.
34. Liu, T., Dartevelle, L., Yuan, C., Wei, H., Wang, Y., Ferveur, J. F., et al. (2008). Increased dopamine level enhances male-male courtship in Drosophila. J. Neurosci. 28, 5539-5546. doi: 10.1523/jneurosci.5290-07.2008
35. McQuillan, H. J., Barron, A. B., and Mercer, A. R. (2012). Age-and behavior-related changes in the expression of biogenic amine receptor genes in the antennae of honey bees (Apis mellifera). J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 198, 753-761. doi: 10.1007/s00359-012-0745-y
36. Picimbon, J. F., Gadenne, C., Bécard, J. M., Clément, J. L., and Sreng, L. (1997). Sex pheromone of the french black cutworm moth, Agrotis ipsilon (Lepi-doptera:Noctuidae): identification and regulation of a multicomponent blend. J. Chem. Ecol. 23, 211-230. doi: 10.1023/b:joec.0000006355.13207.91
37. Poitout, S., and Buès, R. (1974). Elevage de plusieurs espèces de lépidoptères sur milieu artificiel simplifié. Ann. Zool. Ecol. Anim. 2, 79-91.
38. Rauschenbach, I. Y., Laukhina, O. V., Alekseev, A. A., Adonyeva, N. V., Bogomolova, E. V., and Gruntenko, N. E. (2012). Dopamine effect on 20-hydroxyecdysone level is mediated by juvenile hormone in Drosophila females. Dokl. Biochem. Biophys. 446, 263-265. doi: 10.1134/s1607672912050171
39. Reale, V., Hannan, F., Hall, L. M., and Evans, P. D. (1997). Agonist-specific coupling of a cloned Drosophila melanogaster D1-like dopamine receptor to multiple second messenger pathways by synthetic agonists. J. Neurosci. 17, 6545-6553.
40. Roeder, T. (2005). Tyramine and octopamine: ruling behavior and metabolism. Annu. Rev. Entomol. 50, 447-477. doi: 10.1146/annurev.ento.50.071803.130404
41. Ruegg, R. P., Orchard, I., and Davey, K. G. (1982). 20-Hydroxy-ecdysone as a modulator of electrical-activity in neurosecretory-cells of Rhodnius prolixus. J. Insect Physiol. 28, 243-248. doi: 10.1016/0022-1910(82)90083-x
42. Ruffner, M. E., Cromarty, S. I., and Cooper, R. L. (1999). Depression of synaptic efficacy in high-and low-output Drosophila neuromuscular junctions by the molting hormone (20-HE). J. Neurophysiol. 81, 788-794.
43. Schulz, D. J., Sullivan, J. P., and Robinson, G. E. (2002). Juvenile hormone and octopamine in the regulation of division of labor in honey bee colonies. Horm. Behav. 42, 222-231. doi: 10.1006/hbeh.2002.1806
44. Sigg, D., Thompson, C. M., and Mercer, A. R. (1997). Activity-dependent changes to the brain and behavior of the honey bee, Apis mellifera (L.). J. Neurosci. 17, 7148-7156.
45. Sokal, R. R., and Rohlf, F. J. (1995). Biometry: The Principles and Practice of Statistics in Biological Research. New York: Freeman, W. H.
46. Srivastava, D. P., Woolfrey, K. M., Jones, K. A., Shum, C. Y., Lash, L. L., Swanson, G. T., et al. (2008). Rapid enhancement of two-step wiring plasticity by estrogen and NMDA receptor activity. Proc. Natl. Acad. Sci. U S A 105, 14650-14655. doi: 10.1073/pnas.0801581105
47. Srivastava, D. P., Yu, E. J., Kennedy, K., Chatwin, H., Reale, V., Hamon, M., et al. (2005). Rapid, nongenomic responses to ecdysteroids and catecholamines mediated by a novel Drosophila G-protein-coupled receptor. J. Neurosci. 25, 6145-6155. doi: 10.1523/jneurosci.1005-05.2005
48. Van Swinderen, B., and Andretic, R. (2011). Dopamine in Drosophila: setting arousal thresholds in a miniature brain. Proc. Biol. Sci. 278, 906-913. doi: 10.1098/rspb.2010.2564
49. Vitecek, S., Maria, A., Blais, C., Duportets, L., Gaertner, C., Dufour, M.-C., et al. (2013). Is the rapid post-mating inhibition of pheromone response triggered by ecdysteroids or other factors from the sex accessory glands in the male moth Agrotis ipsilon? Horm. Behav. 63, 700-708. doi: 10.1016/j.yhbeh.2013.03.010
50. Walikonis, R., Schoun, D., Zacharias, D., Henley, J., Coburn, P., and Stout, J. (1991). Attractiveness of the male Acheta domesticus calling song to females. III. The relation of age-correlated changes in syllabe period recognition and phonotactic threshold to juvenile hormone III biosynthesis. J. Comp. Physiol. A 169, 751-764.