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. 1992 Jan;11(1):7–17. doi: 10.1002/j.1460-2075.1992.tb05021.x

A family of Drosophila serotonin receptors with distinct intracellular signalling properties and expression patterns.

F Saudou 1, U Boschert 1, N Amlaiky 1, J L Plassat 1, R Hen 1
PMCID: PMC556419  PMID: 1310937

Abstract

Biogenic amines such as serotonin elicit or modulate a wide range of behaviours by interacting with multiple receptor subtypes. We have isolated cDNA clones encoding three distinct Drosophila serotonin receptors which belong to the G protein-coupled receptor family. When expressed in mammalian cells, these receptors activate different intracellular effector systems. The 5HT-dro1 receptor stimulates adenylate cyclase while the 5HT-dro2A and the 5HT-dro2B receptors inhibit adenylate cyclase and activate phospholipase C. Expression of all three receptors starts in late embryos and is restricted to distinct populations of cells in the central nervous system. The 5HT-dro2A receptor is predominantly expressed in midline motor neurons (VUM neurons) that innervate larval muscles thus suggesting a role for this receptor in motor control.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Amlaiky N., Caron M. G. Photoaffinity labeling of the D2-dopamine receptor using a novel high affinity radioiodinated probe. J Biol Chem. 1985 Feb 25;260(4):1983–1986. [PubMed] [Google Scholar]
  2. Arakawa S., Gocayne J. D., McCombie W. R., Urquhart D. A., Hall L. M., Fraser C. M., Venter J. C. Cloning, localization, and permanent expression of a Drosophila octopamine receptor. Neuron. 1990 Mar;4(3):343–354. doi: 10.1016/0896-6273(90)90047-j. [DOI] [PubMed] [Google Scholar]
  3. Atwater J. A., Wisdom R., Verma I. M. Regulated mRNA stability. Annu Rev Genet. 1990;24:519–541. doi: 10.1146/annurev.ge.24.120190.002511. [DOI] [PubMed] [Google Scholar]
  4. Bicker G., Menzel R. Chemical codes for the control of behaviour in arthropods. Nature. 1989 Jan 5;337(6202):33–39. doi: 10.1038/337033a0. [DOI] [PubMed] [Google Scholar]
  5. Bunzow J. R., Van Tol H. H., Grandy D. K., Albert P., Salon J., Christie M., Machida C. A., Neve K. A., Civelli O. Cloning and expression of a rat D2 dopamine receptor cDNA. Nature. 1988 Dec 22;336(6201):783–787. doi: 10.1038/336783a0. [DOI] [PubMed] [Google Scholar]
  6. Cavener D. R. Comparison of the consensus sequence flanking translational start sites in Drosophila and vertebrates. Nucleic Acids Res. 1987 Feb 25;15(4):1353–1361. doi: 10.1093/nar/15.4.1353. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cotecchia S., Kobilka B. K., Daniel K. W., Nolan R. D., Lapetina E. Y., Caron M. G., Lefkowitz R. J., Regan J. W. Multiple second messenger pathways of alpha-adrenergic receptor subtypes expressed in eukaryotic cells. J Biol Chem. 1990 Jan 5;265(1):63–69. [PubMed] [Google Scholar]
  8. Cotecchia S., Schwinn D. A., Randall R. R., Lefkowitz R. J., Caron M. G., Kobilka B. K. Molecular cloning and expression of the cDNA for the hamster alpha 1-adrenergic receptor. Proc Natl Acad Sci U S A. 1988 Oct;85(19):7159–7163. doi: 10.1073/pnas.85.19.7159. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Cymborowski B. The assumed participation of 5-hydroxytryptamine in regulation of the circadian rhythm of locomotor activity in Acheta domesticus L. Comp Gen Pharmacol. 1970 Sep;1(3):316–322. doi: 10.1016/0010-4035(70)90025-x. [DOI] [PubMed] [Google Scholar]
  10. Dearry A., Gingrich J. A., Falardeau P., Fremeau R. T., Jr, Bates M. D., Caron M. G. Molecular cloning and expression of the gene for a human D1 dopamine receptor. Nature. 1990 Sep 6;347(6288):72–76. doi: 10.1038/347072a0. [DOI] [PubMed] [Google Scholar]
  11. Drummond A. H., Bucher F., Levitan I. B. d-[3H]Lysergic acid diethylamide binding to serotonin receptors in the molluscan nervous system. J Biol Chem. 1980 Jul 25;255(14):6679–6686. [PubMed] [Google Scholar]
  12. Dudai Y. Neurogenetic dissection of learning and short-term memory in Drosophila. Annu Rev Neurosci. 1988;11:537–563. doi: 10.1146/annurev.ne.11.030188.002541. [DOI] [PubMed] [Google Scholar]
  13. Dudai Y., Zvi S. Aminergic receptors in Drosophila melanogaster: properties of [3H]dihydroergocryptine binding sites. J Neurochem. 1982 Jun;38(6):1551–1558. doi: 10.1111/j.1471-4159.1982.tb06632.x. [DOI] [PubMed] [Google Scholar]
  14. Eisenberg D., Schwarz E., Komaromy M., Wall R. Analysis of membrane and surface protein sequences with the hydrophobic moment plot. J Mol Biol. 1984 Oct 15;179(1):125–142. doi: 10.1016/0022-2836(84)90309-7. [DOI] [PubMed] [Google Scholar]
  15. Eskin A., Takahashi J. S. Adenylate cyclase activation shifts the phase of a circadian pacemaker. Science. 1983 Apr 1;220(4592):82–84. doi: 10.1126/science.6298939. [DOI] [PubMed] [Google Scholar]
  16. Fargin A., Raymond J. R., Lohse M. J., Kobilka B. K., Caron M. G., Lefkowitz R. J. The genomic clone G-21 which resembles a beta-adrenergic receptor sequence encodes the 5-HT1A receptor. Nature. 1988 Sep 22;335(6188):358–360. doi: 10.1038/335358a0. [DOI] [PubMed] [Google Scholar]
  17. Frielle T., Collins S., Daniel K. W., Caron M. G., Lefkowitz R. J., Kobilka B. K. Cloning of the cDNA for the human beta 1-adrenergic receptor. Proc Natl Acad Sci U S A. 1987 Nov;84(22):7920–7924. doi: 10.1073/pnas.84.22.7920. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Green S., Issemann I., Sheer E. A versatile in vivo and in vitro eukaryotic expression vector for protein engineering. Nucleic Acids Res. 1988 Jan 11;16(1):369–369. doi: 10.1093/nar/16.1.369. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Higgins D. G., Sharp P. M. CLUSTAL: a package for performing multiple sequence alignment on a microcomputer. Gene. 1988 Dec 15;73(1):237–244. doi: 10.1016/0378-1119(88)90330-7. [DOI] [PubMed] [Google Scholar]
  20. Julius D., MacDermott A. B., Axel R., Jessell T. M. Molecular characterization of a functional cDNA encoding the serotonin 1c receptor. Science. 1988 Jul 29;241(4865):558–564. doi: 10.1126/science.3399891. [DOI] [PubMed] [Google Scholar]
  21. Julius D. Molecular biology of serotonin receptors. Annu Rev Neurosci. 1991;14:335–360. doi: 10.1146/annurev.ne.14.030191.002003. [DOI] [PubMed] [Google Scholar]
  22. Kadan M. J., Hartig P. R. Autoradiographic localization and characterization of [125I]lysergic acid diethylamide binding to serotonin receptors in Aplysia. Neuroscience. 1988 Mar;24(3):1089–1102. doi: 10.1016/0306-4522(88)90090-5. [DOI] [PubMed] [Google Scholar]
  23. Kandel E. R., Abrams T., Bernier L., Carew T. J., Hawkins R. D., Schwartz J. H. Classical conditioning and sensitization share aspects of the same molecular cascade in Aplysia. Cold Spring Harb Symp Quant Biol. 1983;48(Pt 2):821–830. doi: 10.1101/sqb.1983.048.01.085. [DOI] [PubMed] [Google Scholar]
  24. Klein P., Kanehisa M., DeLisi C. The detection and classification of membrane-spanning proteins. Biochim Biophys Acta. 1985 May 28;815(3):468–476. doi: 10.1016/0005-2736(85)90375-x. [DOI] [PubMed] [Google Scholar]
  25. Klämbt C., Jacobs J. R., Goodman C. S. The midline of the Drosophila central nervous system: a model for the genetic analysis of cell fate, cell migration, and growth cone guidance. Cell. 1991 Feb 22;64(4):801–815. doi: 10.1016/0092-8674(91)90509-w. [DOI] [PubMed] [Google Scholar]
  26. Kobilka B. K., Matsui H., Kobilka T. S., Yang-Feng T. L., Francke U., Caron M. G., Lefkowitz R. J., Regan J. W. Cloning, sequencing, and expression of the gene coding for the human platelet alpha 2-adrenergic receptor. Science. 1987 Oct 30;238(4827):650–656. doi: 10.1126/science.2823383. [DOI] [PubMed] [Google Scholar]
  27. Kravitz E. A. Hormonal control of behavior: amines and the biasing of behavioral output in lobsters. Science. 1988 Sep 30;241(4874):1775–1781. doi: 10.1126/science.2902685. [DOI] [PubMed] [Google Scholar]
  28. Libert F., Parmentier M., Lefort A., Dinsart C., Van Sande J., Maenhaut C., Simons M. J., Dumont J. E., Vassart G. Selective amplification and cloning of four new members of the G protein-coupled receptor family. Science. 1989 May 5;244(4904):569–572. doi: 10.1126/science.2541503. [DOI] [PubMed] [Google Scholar]
  29. Mohana Rao J. K., Argos P. A conformational preference parameter to predict helices in integral membrane proteins. Biochim Biophys Acta. 1986 Jan 30;869(2):197–214. doi: 10.1016/0167-4838(86)90295-5. [DOI] [PubMed] [Google Scholar]
  30. O'Dowd B. F., Lefkowitz R. J., Caron M. G. Structure of the adrenergic and related receptors. Annu Rev Neurosci. 1989;12:67–83. doi: 10.1146/annurev.ne.12.030189.000435. [DOI] [PubMed] [Google Scholar]
  31. Pritchett D. B., Bach A. W., Wozny M., Taleb O., Dal Toso R., Shih J. C., Seeburg P. H. Structure and functional expression of cloned rat serotonin 5HT-2 receptor. EMBO J. 1988 Dec 20;7(13):4135–4140. doi: 10.1002/j.1460-2075.1988.tb03308.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Provost N. M., Somers D. E., Hurley J. B. A Drosophila melanogaster G protein alpha subunit gene is expressed primarily in embryos and pupae. J Biol Chem. 1988 Aug 25;263(24):12070–12076. [PubMed] [Google Scholar]
  33. Quan F., Wolfgang W. J., Forte M. A. The Drosophila gene coding for the alpha subunit of a stimulatory G protein is preferentially expressed in the nervous system. Proc Natl Acad Sci U S A. 1989 Jun;86(11):4321–4325. doi: 10.1073/pnas.86.11.4321. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Saudou F., Amlaiky N., Plassat J. L., Borrelli E., Hen R. Cloning and characterization of a Drosophila tyramine receptor. EMBO J. 1990 Nov;9(11):3611–3617. doi: 10.1002/j.1460-2075.1990.tb07572.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Sink H., Whitington P. M. Location and connectivity of abdominal motoneurons in the embryo and larva of Drosophila melanogaster. J Neurobiol. 1991 Apr;22(3):298–311. doi: 10.1002/neu.480220309. [DOI] [PubMed] [Google Scholar]
  36. Takahashi J. S., Zatz M. Regulation of circadian rhythmicity. Science. 1982 Sep 17;217(4565):1104–1111. doi: 10.1126/science.6287576. [DOI] [PubMed] [Google Scholar]
  37. Tautz D., Pfeifle C. A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchback. Chromosoma. 1989 Aug;98(2):81–85. doi: 10.1007/BF00291041. [DOI] [PubMed] [Google Scholar]
  38. Uzzan A., Dudai Y. Aminergic receptors in Drosophila melanogaster: responsiveness of adenylate cyclase to putative neurotransmitters. J Neurochem. 1982 Jun;38(6):1542–1550. doi: 10.1111/j.1471-4159.1982.tb06631.x. [DOI] [PubMed] [Google Scholar]
  39. Vallés A. M., White K. Serotonin-containing neurons in Drosophila melanogaster: development and distribution. J Comp Neurol. 1988 Feb 15;268(3):414–428. doi: 10.1002/cne.902680310. [DOI] [PubMed] [Google Scholar]
  40. Wharton K. A., Yedvobnick B., Finnerty V. G., Artavanis-Tsakonas S. opa: a novel family of transcribed repeats shared by the Notch locus and other developmentally regulated loci in D. melanogaster. Cell. 1985 Jan;40(1):55–62. doi: 10.1016/0092-8674(85)90308-3. [DOI] [PubMed] [Google Scholar]
  41. Witz P., Amlaiky N., Plassat J. L., Maroteaux L., Borrelli E., Hen R. Cloning and characterization of a Drosophila serotonin receptor that activates adenylate cyclase. Proc Natl Acad Sci U S A. 1990 Nov;87(22):8940–8944. doi: 10.1073/pnas.87.22.8940. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Zetina C. R., Goldberg M. E. Kinetics of renaturation and self-assembly of intermediates on the pathway of folding of the beta 2-subunit of Escherichia coli tryptophan-synthetase. J Mol Biol. 1982 May 5;157(1):133–148. doi: 10.1016/0022-2836(82)90516-2. [DOI] [PubMed] [Google Scholar]

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