A Novel Family of Divergent Seven-Transmembrane Proteins
Open accessAbstract
Although insects have proven to be valuable models for exploring the function, organization, and development of the olfactory system, the receptor molecules that bind odors have not been identified in any insect. We have developed a novel search algorithm, used it to search the Drosophila genomic sequence database, and identified a large multigene family encoding seven transmembrane domain proteins that are expressed in olfactory organs. We show that expression is restricted to subsets of olfactory receptor neurons (ORNs) for a number of these genes. Different members of the family initiate expression at different times during antennal development. Some of the genes are not expressed in a mutant of the Acj6 POU-domain transcription factor, a mutant in which a subset of ORNs show abnormal odorant specificities.
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In Drosophila olfactory GPCRs, the most divergent regions are the first extracellular loop, the third transmembrane helix, as well as the first and second transmembrane domains.
“whereas in Drosophila the most divergent regions are the first extracellular loop, the third transmembrane helix, as well as the first and second transmembrane domains (Clyne et al., 1999).”
From Opsins and clusters of sensory G-protein-coupled receptors in the sea urchin genome (2006) · cites this paper as Clyne et al., 1999
Cites
Basic local alignment search tool
Altschul, S. F., Gish, W., Miller, W., Myers, E. W., & Lipman, D. J. (1990) · Journal of Molecular Biology · doi:10.1006/jmbi.1990.9999 · Cited by 98,669 · see citing works
A simple method for displaying the hydropathic character of a protein
Kyte, J., & Doolittle, R. F. (1982) · Journal of Molecular Biology · doi:10.1016/0022-2836(82)90515-0 · Cited by 22,694 · see citing works
A novel multigene family may encode odorant receptors: A molecular basis for odor recognition
Buck, L., & Axel, R. (1991) · Cell · doi:10.1016/0092-8674(91)90418-x · Cited by 4,987 · see citing works
Visualizing an Olfactory Sensory Map
Mombaerts, P., Wang, F., Dulac, C. G., Chao, S. K., Nemes, A., Mendelsohn, M. M., Edmondson, J., & Axel, R. (1996) · Cell · doi:10.1016/s0092-8674(00)81387-2 · Cited by 1,992 · see citing works
IDENTIFYING NONPOLAR TRANSBILAYER HELICES IN AMINO ACID SEQUENCES OF MEMBRANE PROTEINS
Engelman, D. M., Steitz, T. A., & Goldman, A. (1986) · Annual Review of Biophysics and Biophysical Chemistry · doi:10.1146/annurev.bb.15.060186.001541 · Cited by 1,508 · see citing works
MECHANISMS OF OLFACTORY DISCRIMINATION: Converging Evidence for Common Principles Across Phyla
Hildebrand, J. G., & Shepherd, G. M. (1997) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.20.1.595 · Cited by 1,066 · see citing works
A zonal organization of odorant receptor gene expression in the olfactory epithelium
Ressler, K. J., Sullivan, S. L., & Buck, L. B. (1993) · Cell · doi:10.1016/0092-8674(93)90145-g · Cited by 1,054 · see citing works
The organization of the chemosensory system in Drosophila melanogaster: a rewiew
Stocker, R. F. (1994) · Cell and Tissue Research · doi:10.1007/bf00305372 · Cited by 950 · see citing works
Spatial segregation of odorant receptor expression in the mammalian olfactory epithelium
Vassar, R. J., Ngai, J., & Axel, R. (1993) · Cell · doi:10.1016/0092-8674(93)90422-m · Cited by 874 · see citing works
Sequence Alignment of the G-Protein Coupled Receptor Superfamily
PROBST, W. C., Snyder, L., Schuster, D. I., Brosius, J., & Sealfon, S. C. (1992) · DNA and Cell Biology · doi:10.1089/dna.1992.11.1 · Cited by 841 · see citing works
Divergent seven transmembrane receptors are candidate chemosensory receptors in C. elegans
Troemel, E. R., Chou, J. H., Dwyer, N. D., Colbert, H. A., & Bargmann, C. I. (1995) · Cell · doi:10.1016/0092-8674(95)90162-0 · Cited by 684 · see citing works
Functional Expression of a Mammalian Odorant Receptor
Zhao, H., Ivic, L., Otaki, J. M., Hashimoto, M., Mikoshiba, K., & Firestein, S. (1998) · Science · doi:10.1126/science.279.5348.237 · Cited by 622 · see citing works
Odorant Receptors Govern the Formation of a Precise Topographic Map
Wang, F., Nemes, A., Mendelsohn, M. M., & Axel, R. (1998) · Cell · doi:10.1016/s0092-8674(00)81145-9 · Cited by 611 · see citing works
Sengupta, P., Chou, J. H., & Bargmann, C. I. (1996) · Cell · doi:10.1016/s0092-8674(00)81068-5 · Cited by 556 · see citing works
Information Coding in the Vertebrate Olfactory System
Buck, L. B. (1996) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.19.030196.002505 · Cited by 539 · see citing works
Rapid kinetics of second messenger formation in olfactory transduction
Breer, H., Boekhoff, I., & Tareilus, E. (1990) · Nature · doi:10.1038/345065a0 · Cited by 440 · see citing works
Three‐dimensional reconstruction of the antennal lobe in Drosophila melanogaster
Laissue, P. P., Reiter, C., Hiesinger, P. R., Halter, S., Fischbach, K. F., & Stocker, R. F. (1999) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19990322)405:4 · Cited by 421 · see citing works
Ashburner, M. (1989) · Cold Spring Harbor Laboratory eBooks · Cited by 417 · see citing works
The family of genes encoding odorant receptors in the channel catfish
Ngal, J. (1993) · Cell · doi:10.1016/0092-8674(93)90395-7 · Cited by 404 · see citing works
Splicing signals inDrosophila: intron size, information content, and consensus sequences
Mount, S. M., Burks, C., Herts, G., et al. (1992) · Nucleic Acids Research · doi:10.1093/nar/20.16.4255 · Cited by 379 · see citing works
Putative Drosophila pheromone-binding proteins expressed in a subregion of the olfactory system.
McKenna, M. P., Hekmat‐Scafe, D. S., Gaines, P. C. W., & Carlson, J. R. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)34013-9 · Cited by 362 · see citing works
Self-citationNgai, J. (1993) · Cell · doi:10.1016/0092-8674(93)90396-8 · Cited by 348 · see citing works
The C. elegans gene odr-7 encodes an olfactory-specific member of the nuclear receptor superfamily
Sengupta, P., Colbert, H. A., & Bargmann, C. I. (1994) · Cell · doi:10.1016/0092-8674(94)90028-0 · Cited by 216 · see citing works
The chromosomal distribution of mouse odorant receptor genes.
Sullivan, S. L., Adamson, M. C., Ressler, K. J., Kozak, C. A., & Buck, L. B. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.2.884 · Cited by 210 · see citing works
Odorant response of individual sensilla on theDrosophila antenna
Clyne, P. J., Grant, A. P., O’Connell, R. J., & Carlson, J. R. (1997) · Invertebrate Neuroscience · doi:10.1007/bf02480367 · Cited by 201 · see citing works
Self-citationAnalysis of chemical signals by nervous systems.
Hildebrand, J. G. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.1.67 · Cited by 198 · see citing works
Baumann, A., Frings, S., Godde, M., et al. (1994) · The EMBO Journal · doi:10.1002/j.1460-2075.1994.tb06833.x · Cited by 180 · see citing works
Vosshall, L. B. (2000) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(00)00111-2 · Cited by 172 · see citing works
Robertson, H. M. (1998) · Genome Research · doi:10.1101/gr.8.5.449 · Cited by 170 · see citing works
Clyne, P. J., Certel, S. J., de Bruyne, M., Zaslavsky, L., Johnson, W. A., & Carlson, J. R. (1999) · Neuron · doi:10.1016/s0896-6273(00)81094-6 · Cited by 153 · see citing works
Self-citationWhite, S. H. (1994) · Springer eBooks · doi:10.1007/978-1-4614-7515-6 · Cited by 146 · see citing works
SIGNAL TRANSDUCTION IN THE CAENORHABDITIS ELEGANS NERVOUS SYSTEM
Bargmann, C. I., & Kaplan, J. M. (1998) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.21.1.279 · Cited by 143 · see citing works
Asynchronous Onset of Odorant Receptor Expression in the Developing Zebrafish Olfactory System
Barth, A. L., Justice, N. J., & Ngai, J. (1996) · Neuron · doi:10.1016/s0896-6273(00)80020-3 · Cited by 142 · see citing works
Olfaction in Drosophila: from odor to behavior
Carlson, J. R. (1996) · Trends in Genetics · doi:10.1016/0168-9525(96)10015-9 · Cited by 131 · see citing works
Self-citationSingh, R., & Nayak, S. V. (1985) · International Journal of Insect Morphology and Embryology · doi:10.1016/0020-7322(85)90044-3 · Cited by 124 · see citing works
A novel multigene family may encode odorant receptors.
Buck, L. B. (1992) · PubMed · Cited by 113 · see citing works
Ayer, R. K., & Carlson, J. R. (1992) · Journal of Neurobiology · doi:10.1002/neu.480230804 · Cited by 109 · see citing works
Self-citationRiesgo‐Escovar, J. R., Raha, D., & Carlson, J. R. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.7.2864 · Cited by 107 · see citing works
Self-citationSensilla on the third antennal segment of Drosophila melanogaster meigen (Diptera : Drosophilidae)
Venkatesh, S., & Singh, R. (1984) · International Journal of Insect Morphology and Embryology · doi:10.1016/0020-7322(84)90032-1 · Cited by 105 · see citing works
Temporal and spatial distribution of transcripts from the Deformed gene of Drosophila
Chadwick, R. A., & McGinnis, W. J. (1987) · The EMBO Journal · doi:10.1002/j.1460-2075.1987.tb04820.x · Cited by 92 · see citing works
Neurogenetics of olfaction in Drosophila melanogaster
Siddiqi, O. H. (1987) · Trends in Genetics · doi:10.1016/0168-9525(87)90204-6 · Cited by 84 · see citing works
Pheromone-induced second-messenger signaling in insect antennae
Boekhoff, I., Seifert, E., Göggerle, S., Lindemann, M., Krüger, B.-W., & Breer, H. (1993) · Insect Biochemistry and Molecular Biology · doi:10.1016/0965-1748(93)90063-x · Cited by 77 · see citing works
(1991) · Analytical Biochemistry · doi:10.1016/0003-2697(91)90450-8 · Cited by 69 · see citing works
Noncoordinate Expression of Odorant Receptor Genes Tightly Linked in the Zebrafish Genome
Barth, A. L., Dugas, J. C., & Ngai, J. (1997) · Neuron · doi:10.1016/s0896-6273(00)80945-9 · Cited by 69 · see citing works
Odorant-sensitive phospholipase C in insect antennae
Boekhoff, I., Strotmann, J. M., Raming, K., et al. (1990) · Cellular Signalling · doi:10.1016/0898-6568(90)90032-6 · Cited by 67 · see citing works
Cellular Events during Development of the Olfactory Sense Organs in Drosophila melanogaster
Ray, K., & Rodrigues, V. (1995) · Developmental Biology · doi:10.1006/dbio.1995.1039 · Cited by 66 · see citing works
acj6: a gene affecting olfactory physiology and behavior in Drosophila.
Ayer, R. K., & Carlson, J. R. (1991) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.88.12.5467 · Cited by 61 · see citing works
Self-citationReddy, G. V., Gupta, B. P., Ray, K., et al. (1997) · Development · doi:10.1242/dev.124.3.703 · Cited by 57 · see citing works
The Drosophila antenna: ultrastructural and physiological studies in wild-type and lozenge mutants
Riesgo‐Escovar, J. R., Piekos, W. B., & Carlson, J. R. (1997) · Journal of Comparative Physiology A · doi:10.1007/s003590050036 · Cited by 45 · see citing works
Self-citationLienhard, M. C., & Stocker, R. F. (1991) · Development · doi:10.1242/dev.112.4.1063 · Cited by 44 · see citing works
Haenlin, M., Roos, C., Cassab, A., et al. (1987) · The EMBO Journal · doi:10.1002/j.1460-2075.1987.tb04822.x · Cited by 40 · see citing works
Wood, E. (1992) · Biochemical Education · doi:10.1016/0307-4412(92)90013-c · Cited by 34 · see citing works
Hydropathy Plots and the Prediction of Membrane Protein Topology
White, S. H. (1994) · Springer eBooks · doi:10.1007/978-1-4614-7515-6_4 · Cited by 33 · see citing works
Stocker, R. F., Tissot, M., & Gendre, N. (1995) · Development Genes and Evolution · doi:10.1007/bf00188844 · Cited by 31 · see citing works
Olfactory signalling in antennal receptor neurones of the locust (Locusta migratoria)
Wegener, J. W., Boekhoff, I., Tareilus, E., et al. (1993) · Journal of Insect Physiology · doi:10.1016/0022-1910(93)90107-3 · Cited by 18 · see citing works
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Root, C. M., Ko, K. I., Jafari, A., & Wang, J. W. (2011) · Cell · doi:10.1016/j.cell.2011.02.008 · Cited by 526 · see citing works
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Burke, R. D., Angerer, L. M., Elphick, M. R., Humphrey, G. W., Yaguchi, S., Kiyama, T., Liang, S., Mu, X., Agca, C., Klein, W. H., et al. (2006) · Developmental Biology · doi:10.1016/j.ydbio.2006.08.007 · Cited by 293 · see citing works
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- Authors
- Clyne, P. J., Warr, C. G., Freeman, M. R., Lessing, D., Kim, J., & Carlson, J. R.
- Affiliations
- Yale University (US)
- Corresponding author
- Carlson, John R.
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 1999-02
- Volume
- 22
- Issue
- 2
- Pages
- 327-338
- ISSN
- 0896-6273 (ISSN-L)
- OpenAlex
- W2004026630
- Cited by
- 1,155
- References
- 55
- Citations by year
- 2026: 25 · 2025: 34 · 2024: 53 · 2023: 28 · 2022: 45 · 2021: 49 · 2020: 65 · 2019: 43 · 2018: 42 · 2017: 30 · 2016: 52 · 2015: 42 · 2014: 52 · 2013: 33 · 2012: 26
- FWCI
- 20.24
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Neuron (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- Figshare (submittedVersion)
- Funders
- National Institute on Deafness and Other Communication Disorders (DC02174, R01DC002174)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
- Life Sciences › Neuroscience › Sensory Systems › Olfactory and Sensory Function Studies
- Life Sciences › Agricultural and Biological Sciences › Insect Science › Insect Pheromone Research and Control
- Keywords
- seven-transmembrane proteins, G protein-coupled receptors, insect olfaction, olfactory sensory neurons, Drosophila, gene family, antennal development, odorant specificity, olfactory system evolution
- MeSH terms
- Amino Acid Sequence, Animals, DNA-Binding Proteins, Drosophila, Multigene Family, Molecular Sequence Data, Nerve Tissue Proteins, Odorants, Olfactory Pathways, Sensory Receptor Cells, Transcription Factors, Gene Expression Regulation, Developmental, GTP-Binding Proteins, Drosophila Proteins, POU Domain Factors
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