Skip to main content
Log in

The cAMP Transduction Cascade Mediates Olfactory Reception in Drosophila melanogaster

  • Published:
Behavior Genetics Aims and scope Submit manuscript

Abstract

Two main second messenger systems depending on IP3 and cAMP have been related to olfaction in vertebrates as well as invertebrates. In Drosophila melanogaster, the availability of mutations affecting one or the other pathway (rdgB and norpA or rut and dnc, respectively) allowed showing of abnormal olfactory behavior phenotypes associated with olfactory transduction in complete living animals. However, because rut and dnc genes showed ubiquitous expression at olfactory receptor organs and some brain locations, the mutant behavior cannot be assigned exclusively to olfactory reception. In this report, overexpression of the dnc gene directed specifically to different olfactory receptor neuron subsets was used to produce dominant mutants. Abnormal olfactory behavior was found in 62.5% of the 8 lines studied in response to some odorants, depending on the affected neuronal subset. These results suggest that even for a small number of tested odorants (5), cAMP cascade is involved in olfactory reception to an important extent.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Ache, B. W. (1994). Towards a common strategy for transducing olfactory information. Semin. Cell Biol. 5:55-63.

    Google Scholar 

  • Alcorta, E., and Rubio, J. (1989). Intrapopulational variation of olfactory responses in Drosophila melanogaster. Behav. Genet. 19:285-299.

    Google Scholar 

  • Baumann, A., Frings, S., Godde, M., Seifert, R., and Kaupp, U. B. (1994). Primary structure and fuctional expression of a Drosophila cyclic nucleotide-gated channel present in eyes and antennae. EMBO J. 13:5040-5050.

    Google Scholar 

  • Belluscio, L., Gold, G. H., Nemes, A., and Axel, R. (1998). Mice deficient in Golf are anosmic. Neuron 20:69-81.

    Google Scholar 

  • Boekhoff, I., Tarelius, E., Strotmann, J., and Breer, H. (1990). Rapid activation of alternative second messenger pathways in olfactory cilia from rats by different odorants. EMBO J. 9:2453-2458.

    Google Scholar 

  • Brand, A. H., and Perrimon, N. (1993). Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118:401-415.

    Google Scholar 

  • Breer, H. (1994). Odor recognition and second messenger signaling in olfactory receptor neurons. Semin. Cell Biol. 5:25-32.

    Google Scholar 

  • Breer, H., Boekhoff, I., and Tareilus, E. (1990). Rapid kinetics of second messenger formation in olfactory transduction. Nature 345:65-68.

    Google Scholar 

  • Brunet, L. J., Gold, G. H., and Ngai, J. (1996). General anosmia caused by a targeted disruption of the mouse olfactory cyclic nucleotide-gated cation channel. Neuron 17:681-693.

    Google Scholar 

  • Bustin, S. A. (2000). Absolute quantification of mRNA using realtime reverse transcription polymerase chain reaction assays. J. Mol. Endocrinol. 25:169-193.

    Google Scholar 

  • Byers, D., Davis, R. L., and Kieger, J. A. (1981). Defect in cAMP phosphodiesterase due to dunce mutation of learning in Drosophila melanogaster. Nature 289:79-81.

    Google Scholar 

  • Callahan, C. A., and Thomas, J. B. (1994). Tau-β-galactosidase, an axon-targeted fusion protein. Proc. Natl. Acad. Sci. USA. 91:5972-5976.

    Google Scholar 

  • Chen, C-N., Denome, S., and Davis, R. L. (1986). Molecular analysis of cDNA clones and the corresponding genomic coding secuences of the Drosophila dunce + gene, the structural gene for cAMP phosphodiesterase. Proc. Natl. Acad. Sci. USA. 83:9313-9317.

    Google Scholar 

  • Cheung, U. S., Shayan, A. J., Boulianne, G. L., and Atwood, H. L. (1999). Drosophila larval neuromuscular junction's responses to reduction of cAMP in the nervous system. J. Neurobiol. 40:1-13.

    Google Scholar 

  • de Bruyne, M., Foster, K., and Carlson, J. R. (2001). Odor coding in the Drosophila antenna. Neuron 30:537-552.

    Google Scholar 

  • Del Toro, R., Levitsky, K. L., López-Barneo, J., and Chiara, M. D. (2003). Induction of T-type calcium channel gene expression by chronic hypoxia. J. Biol. Chem. 278:22316-22324.

    Google Scholar 

  • Devaud, J. M., Keane, J., and Ferrus, A. (2003). Blocking sensory inputs to identified antennal glomeruli selectively modifies odorant perception in Drosophila. J. Neurobiol. 56:1-12.

    Google Scholar 

  • Dorak, M. T. (2003). Real-Time PCR. Available at http://dorakmt.tripod.com/genetics/realtime.html.

  • Dubin, A. E., Liles, M. M., and Harris, G. L. (1998). The K+ channel gene Ether a go-go is required for the transduction of a subset of odorants in adult Drosophila melanogaster. J. Neurosci. 18:5603-5613.

    Google Scholar 

  • Fadool, D. A., and Ache, B. W. (1992). Plasma membrane inositol 1,4,5-trisphosphate-activated channels mediate signal transduction in lobster olfactory receptor neurons. Neuron 9:907-918.

    Google Scholar 

  • Han, P. L., Levin, L. R., Reed, R. R., and Davis, R. L. (1992). Preferential expression of the Drosophila rutabaga gene in mushroom bodies, neural centers for learning in insects. Neuron 9:619-627.

    Google Scholar 

  • Hasan, G., and Rosbash, M. (1992). Drosophila homologs of two mammalian intracellular Ca2+-release channels: identification and expression patterns of the inositol 1,4,5-triphosphate and the ryanodine receptor genes. Development 116:967-975.

    Google Scholar 

  • Hildebrand, J. G., and Shepherd, G. M. (1997). Mechanisms of olfactory discrimination: converging evidence for common principles across Phyla. Annu. Rev. Neurosci. 20:595-631.

    Google Scholar 

  • Keller, A., Sweeney, S. T., Zars, T., O'Kane, C. J., and Heisenberg, M. (2002). Targeted expression of tetanus neurotoxin interferes with behavioral responses to sensory input in Drosophila. J. Neurobiol. 50:221-233.

    Google Scholar 

  • Levin, L. R., Han, P. L., Hwang, P. M., Feinstein, P. G., Davis, R. L., and Reed, R. R. (1992). The Drosophila learning and memory gene rutabaga encodes a Ca2+/calmodulin-responsive adenylyl cyclase. Cell 68:479-489.

    Google Scholar 

  • Livingstone, M. S., Sziber, P. P., and Quinn, W. G. (1984). Loss of calcium/calmodulin responsiveness in adenylate cyclase of rutabaga, a Drosophila learning mutant. Cell 37:205-215.

    Google Scholar 

  • Malnic, B., Hirono, J., Sato, T., and Buck, L. B. (1999). Combinatorial receptor codes for odors. Cell 96:713-723.

    Google Scholar 

  • Martin, F., Charro, M. J., and Alcorta, E. (2001). Mutations affecting the cAMP transduction pathway modify olfaction in Drosophila. J. Comp. Physiol. A 187:359-370.

    Google Scholar 

  • Martin, F., Kim, M. S., Hovemann, B., and Alcorta, E. (2002). Factor analysis of olfactory responses in Drosophila melanogaster enhancer-trap lines as a method for ascertaining common reception components for different odorants. Behav. Genet. 32:79-88.

    Google Scholar 

  • Marx, T., Gisselmann, G., Stoertkuhl, K., Hovemann, B., and Hatt, H. (1999). Molecular cloning of a putative voltage and cyclic nucleotide-gated ion channel present in the antennae and eyes of Drosophila melanogaster. Invert. Neurosci. 4:53-63.

    Google Scholar 

  • McClintock, T. S., Landers, T. M., Gimelbrant, A. A., Fuller, L. Z., Jackson, B. A., Jayawickreme, C. K., and Lerner, M. R. (1997). Functional expression of olfactory-adrenergic receptor chimeras and intracellular retention of heterologously expressed olfactory receptors. Mol. Brain Res. 48:270-278.

    Google Scholar 

  • Nighorn, A., Healy, M. J., and Davis, R. L. (1991). The cyclic AMP phosphodiesterase encoded by the Drosophila dunce gene is concentrated in the mushroom body neuropil. Neuron 6:455-467.

    Google Scholar 

  • Noé, J., and Breer, H. (1998). Functional and molecular characterization of individual olfactory neurons. J. Neurochem. 71:2286-2293.

    Google Scholar 

  • Prasad, B. C., and Reed, R. R. (1999). Chemosensation: molecular mechanisms in worms and mammals. TIG 15:150-153.

    Google Scholar 

  • Qiu, Y. H., Chen, C. N., Malone, T., Richter, L., Beckendorf, S. K., and Davis, R. L. (1991). Characterization of the memory gene dunce of Drosophila melanogaster. J. Mol. Biol. 222:553-565.

    Google Scholar 

  • Riesgo-Escovar, J., Woodard, C., Gaines, P., and Carlson, J. (1992). Development and organization of the Drosophila olfactory system: an analysis using enhancer traps. J. Neurobiol. 23:947-964.

    Google Scholar 

  • Riesgo-Escovar, J. R., Woodard, C., and Carlson, J. R. (1994). Olfactory physiology in the Drosophila maxillary palp requires the visual system gene rdgB. J. Comp. Physiol. A 175:687-693.

    Google Scholar 

  • Riesgo-Escovar, J., Raha, D., and Carlson, J. R. (1995). Requirement for a phospholipase C in odor response: overlap between olfaction and vision in Drosophila. Proc. Natl. Acad. Sci. USA. 92:2864-2868.

    Google Scholar 

  • Ronnett, G. V., and Moon, C. (2002). G proteins and olfactory signal transduction. Annu. Rev. Physiol. 64:189-222.

    Google Scholar 

  • Schild, D., and Restrepo, D. (1998). Transduction mechanisms in vertebrate olfactory receptor cells. Physiol. Rev. 78:429-466.

    Google Scholar 

  • Shepherd, G. M. (1991). Sensory transduction: entering the mainstream of membrane signaling. Cell 67:845-851.

    Google Scholar 

  • Stengl, M., Hatt, H., and Breer, H. (1992). Peripheral processes in insect olfaction. Annu. Rev. Physiol. 54:665-681.

    Google Scholar 

  • Sweeney, S. T., Broadie, K., Keane, J., Niemann, H., and O'Kane, C. J. (1995). Targeted expression of tetanus toxin light chain in Drosophila specifically eliminates synaptic transmission and causes behavioral defects. Neuron 14:341-351.

    Google Scholar 

  • Tettamanti, M., Armstrong, J. D., Endo, K., Yang, M. Y., Furukubo-Tokunaga, K., Kaiser, K., and Reichert, H. (1997). Early development of the Drosophila mushroom bodies, brain centres for associative learning and memory. Dev. Genes Evol. 207:242-252.

    Google Scholar 

  • Vogl, A., Noé, J., Breer, H., and Boeckhoff, I. (2000). Cross-talk between olfactory second messenger pathways. Eur. J. Biochem. 267:4529-4535.

    Google Scholar 

  • Woodard, C., Alcorta, E., and Carlson, J. R. (1992). The rdgB gene of Drosophila: A link between vision and olfaction. J Neurogenet. 8:17-31.

    Google Scholar 

  • Yoshikawa, S., Tanimura, T., Miyawaki, A., Nakamura, M., Yuzaki, M., Furuichi, T., and Mikoshiba, K. (1992). Molecular cloning and characterization of the inositol 1,4,5-triphosphate receptor in Drosophila melanogaster. J. Biol. Chem. 267:16613-16619.

    Google Scholar 

  • Zhong, Y., and Wu, C. F. (1991). Altered synaptic plasticity in Drosophila memory mutants with a defective cyclic AMP cascade. Science 251:198-201.

    Google Scholar 

  • Zhong, Y., Budnik, V., and Wu, C. F. (1992). Synaptic plasticity in Drosophila memory and hyperexcitable mutants: role of cAMP cascade. J. Neurosci. 12:644-651.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gomez-Diaz, C., Martin, F. & Alcorta, E. The cAMP Transduction Cascade Mediates Olfactory Reception in Drosophila melanogaster . Behav Genet 34, 395–406 (2004). https://doi.org/10.1023/B:BEGE.0000023645.02710.fe

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/B:BEGE.0000023645.02710.fe

Navigation