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Atypical Membrane Topology and Heteromeric Function of Drosophila Odorant Receptors In Vivo
Open accessAbstract
Drosophila olfactory sensory neurons (OSNs) each express two odorant receptors (ORs): a divergent member of the OR family and the highly conserved, broadly expressed receptor OR83b. OR83b is essential for olfaction in vivo and enhances OR function in vitro, but the molecular mechanism by which it acts is unknown. Here we demonstrate that OR83b heterodimerizes with conventional ORs early in the endomembrane system in OSNs, couples these complexes to the conserved ciliary trafficking pathway, and is essential to maintain the OR/OR83b complex within the sensory cilia, where odor signal transduction occurs. The OR/OR83b complex is necessary and sufficient to promote functional reconstitution of odor-evoked signaling in sensory neurons that normally respond only to carbon dioxide. Unexpectedly, unlike all known vertebrate and nematode chemosensory receptors, we find that Drosophila ORs and OR83b adopt a novel membrane topology with their N-termini and the most conserved loops in the cytoplasm. These loops mediate direct association of ORs with OR83b. Our results reveal that OR83b is a universal and integral part of the functional OR in Drosophila. This atypical heteromeric and topological design appears to be an insect-specific solution for odor recognition, making the OR/OR83b complex an attractive target for the development of highly selective insect repellents to disrupt olfactory-mediated host-seeking behaviors of insect disease vectors.
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Citations
Cites
Thompson, J. (1997) · Nucleic Acids Research · doi:10.1093/nar/25.24.4876 · Cited by 38,993
Krogh, A., Larsson, B., von Heijne, G., & Sonnhammer, E. L. L. (2001) · Journal of Molecular Biology · doi:10.1006/jmbi.2000.4315 · Cited by 12,654
Targeted gene expression as a means of altering cell fates and generating dominant phenotypes
Brand, A. H., & Perrimon, N. (1993) · Development · doi:10.1242/dev.118.2.401 · Cited by 9,612
Crystal Structure of Rhodopsin: A G Protein-Coupled Receptor
Palczewski, K., Kumasaka, T., Hori, T., Behnke, C. A., Motoshima, H., Fox, B. A., Trong, I. L., Teller, D. C., Okada, T., Stenkamp, R. E., et al. (2000) · Science · doi:10.1126/science.289.5480.739 · Cited by 5,637
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
Lee, T., & Luo, L. (1999) · Neuron · doi:10.1016/s0896-6273(00)80701-1 · Cited by 2,571
Combinatorial Receptor Codes for Odors
Malnic, B., Hirono, J., Sato, T., & Buck, L. B. (1999) · Cell · doi:10.1016/s0092-8674(00)80581-4 · Cited by 2,316
Tmbase-A database of membrane spanning protein segments
Hofmann, K., & Stoffel, W. (1993) · Medical Entomology and Zoology · Cited by 2,240
The HMMTOP transmembrane topology prediction server
Tusnády, G. E., & Simon, I. (2001) · Bioinformatics · doi:10.1093/bioinformatics/17.9.849 · Cited by 1,907
Mammalian sweet taste receptors
Nelson, G., Hoon, M. A., Chandrashekar, J., Zhang, Y., Ryba, N. J. P., & Zuker, C. S. (2001) · Cell · doi:10.1016/s0092-8674(01)00451-2 · Cited by 1,702
A high signal-to-noise Ca2+ probe composed of a single green fluorescent protein
Nakai, J., Ohkura, M., & Imoto, K. (2001) · Nature Biotechnology · doi:10.1038/84397 · Cited by 1,616
Nelson, G., Chandrashekar, J., Hoon, M. A., Feng, L., Zhao, G., Ryba, N. J. P., & Zuker, C. S. (2002) · Nature · doi:10.1038/nature726 · Cited by 1,518
Or83b Encodes a Broadly Expressed Odorant Receptor Essential for Drosophila Olfaction
Larsson, M. C., Domingos, A. I., Jones, W. D., Chiappe, M. E., Amrein, H., & Vosshall, L. B. (2004) · Neuron · doi:10.1016/j.neuron.2004.08.019 · Cited by 1,407
Self-citationThe Receptors for Mammalian Sweet and Umami Taste
Zhao, G. Q., Zhang, Y., Hoon, M. A., Chandrashekar, J., Erlenbach, I., Ryba, N. J. P., & Zuker, C. S. (2003) · Cell · doi:10.1016/s0092-8674(03)00844-4 · Cited by 1,340
Spatiotemporal Rescue of Memory Dysfunction in Drosophila
McGuire, S. E., Le, P. T., Osborn, A. J., Matsumoto, K., & Davis, R. L. (2003) · Science · doi:10.1126/science.1089035 · Cited by 1,316
A Spatial Map of Olfactory Receptor Expression in the Drosophila Antenna
Vosshall, L. B., Amrein, H., Morozov, P. S., Rzhetsky, A., & Axel, R. (1999) · Cell · doi:10.1016/s0092-8674(00)80582-6 · Cited by 1,177
Self-citationA Novel Family of Divergent Seven-Transmembrane Proteins
Clyne, P. J., Warr, C. G., Freeman, M. R., Lessing, D., Kim, J., & Carlson, J. R. (1999) · Neuron · doi:10.1016/s0896-6273(00)81093-4 · Cited by 1,155
An Olfactory Sensory Map in the Fly Brain
Vosshall, L. B., Wong, A. M., & Axel, R. (2000) · Cell · doi:10.1016/s0092-8674(00)00021-0 · Cited by 1,101
Self-citationMECHANISMS 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 1,074
The Molecular Basis of Odor Coding in the Drosophila Antenna
Hallem, E. A., Ho, M. G., & Carlson, J. R. (2004) · Cell · doi:10.1016/j.cell.2004.05.012 · Cited by 991
Molecular, Anatomical, and Functional Organization of the Drosophila Olfactory System
Couto, A., Alenius, M., & Dickson, B. J. (2005) · Current Biology · doi:10.1016/j.cub.2005.07.034 · Cited by 984
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
The Olfactory Bulb: Coding and Processing of Odor Molecule Information
Mori, K., Nagao, H., & Yoshihara, Y. (1999) · Science · doi:10.1126/science.286.5440.711 · Cited by 933
Extended Life-Span and Stress Resistance in the Drosophila Mutant methuselah
Lin, Y.-J., Seroude, L., & Benzer, S. (1998) · Science · doi:10.1126/science.282.5390.943 · Cited by 815
Molecular evolution of the insect chemoreceptor gene superfamily in Drosophila melanogaster
Robertson, H. M., Warr, C. G., & Carlson, J. R. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2335847100 · Cited by 804
Two-Photon Calcium Imaging Reveals an Odor-Evoked Map of Activity in the Fly Brain
Wang, J. W., Wong, A. M., Flores, J., Vosshall, L. B., & Axel, R. (2003) · Cell · doi:10.1016/s0092-8674(03)00004-7 · Cited by 801
Self-citationOdor Coding in the Drosophila Antenna
de Bruyne, M., Foster, K., & Carlson, J. R. (2001) · Neuron · doi:10.1016/s0896-6273(01)00289-6 · Cited by 730
A chemosensory gene family encoding candidate gustatory and olfactory receptors in Drosophila.
Scott, K., Brady, R., Cravchik, A., Morozov, P., Rzhetsky, A., Zuker, C., & Axel, R. (2001) · Cell · doi:10.1016/s0092-8674(01)00263-x · Cited by 720
Erythropoietin Receptor Activation by a Ligand-Induced Conformation Change
Remy, I., Wilson, I. A., & Michnick, S. W. (1999) · Science · doi:10.1126/science.283.5404.990 · Cited by 634
Self-citationGenetic and Functional Subdivision of the Drosophila Antennal Lobe
Fishilevich, E., & Vosshall, L. B. (2005) · Current Biology · doi:10.1016/j.cub.2005.07.066 · Cited by 619
Self-citationRTP Family Members Induce Functional Expression of Mammalian Odorant Receptors
Saito, H., Kubota, M., Roberts, R. W., Chi, Q., & Matsunami, H. (2004) · Cell · doi:10.1016/j.cell.2004.11.021 · Cited by 613
A modular set of lacZ fusion vectors for studying gene expression in Caenorhabditis elegans
Fire, A., Harrison, S. W., & Dixon, D. (1990) · Gene · doi:10.1016/0378-1119(90)90224-f · Cited by 606
Gradient Formation of the TGF-β Homolog Dpp
Entchev, E. V., Schwabedissen, A., & González-Gaitán, M. (2000) · Cell · doi:10.1016/s0092-8674(00)00200-2 · Cited by 605
Mice Deficient in Golf Are Anosmic
Belluscio, L., Gold, G. H., Nemes, A., & Axel, R. (1998) · Neuron · doi:10.1016/s0896-6273(00)80435-3 · Cited by 565
Suh, G. S. B., Wong, A. M., Hergarden, A. C., Wang, J. W., Simon, A. F., Benzer, S., Axel, R., & Anderson, D. J. (2004) · Nature · doi:10.1038/nature02980 · Cited by 562
Integrating the Molecular and Cellular Basis of Odor Coding in the Drosophila Antenna
Dobritsa, A. A., van der Goes van Naters, W., Warr, C. G., Steinbrecht, R. A., & Carlson, J. R. (2003) · Neuron · doi:10.1016/s0896-6273(03)00094-1 · Cited by 553
Insect Sex-Pheromone Signals Mediated by Specific Combinations of Olfactory Receptors
Nakagawa, T., Sakurai, T., Nishioka, T., & Touhara, K. (2005) · Science · doi:10.1126/science.1106267 · Cited by 524
Avidor-Reiss, T., Maer, A. M., Koundakjian, E., Polyanovsky, A., Keil, T., Subramaniam, S., & Zuker, C. S. (2004) · Cell · doi:10.1016/s0092-8674(04)00412-x · Cited by 505
Identification of Candidate Drosophila Olfactory Receptors from Genomic DNA Sequence
Gao, Q., & Chess, A. (1999) · Genomics · doi:10.1006/geno.1999.5894 · Cited by 498
Ng, M., Roorda, R. D., Lima, S. Q., Zemelman, B. V., Morcillo, P., & Miesenböck, G. (2002) · Neuron · doi:10.1016/s0896-6273(02)00975-3 · Cited by 475
Seven-Transmembrane Proteins as Odorant and Chemosensory Receptors
Mombaerts, P. (1999) · Science · doi:10.1126/science.286.5440.707 · Cited by 450
Convergent projections of Drosophila olfactory neurons to specific glomeruli in the antennal lobe
Gao, Q., Yuan, B., & Chess, A. (2000) · Nature Neuroscience · doi:10.1038/77680 · Cited by 436
Odorant Receptor Expression Defines Functional Units in the Mouse Olfactory System
Bozza, T., Feinstein, P., Zheng, C., & Mombaerts, P. (2002) · The Journal of Neuroscience · doi:10.1523/jneurosci.22-08-03033.2002 · Cited by 412
Sakurai, T., Nakagawa, T., Mitsuno, H., Mori, H., Endo, Y., Tanoue, S., Yasukochi, Y., Touhara, K., & Nishioka, T. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0407596101 · Cited by 397
PKB/Akt modulates TGF-β signalling through a direct interaction with Smad3
Remy, I., Montmarquette, A., & Michnick, S. W. (2004) · Nature Cell Biology · doi:10.1038/ncb1113 · Cited by 372
Self-citationThe mouse olfactory receptor gene family
Godfrey, P. A., Malnic, B., & Buck, L. B. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0308051100 · Cited by 362
Atlas of olfactory organs of Drosophila melanogaster
Shanbhag, S. R., Müller, B., & Steinbrecht, R. A. (1999) · International Journal of Insect Morphology and Embryology · doi:10.1016/s0020-7322(99)00039-2 · Cited by 357
Odorant receptor heterodimerization in the olfactory system of Drosophila melanogaster
Neuhaus, E. M., Gisselmann, G., Zhang, W., Dooley, R., Störtkuhl, K., & Hatt, H. (2005) · Nature Neuroscience · doi:10.1038/nn1371 · Cited by 339
Roayaie, K., Crump, J. G., Sagasti, A., & Bargmann, C. I. (1998) · Neuron · doi:10.1016/s0896-6273(00)80434-1 · Cited by 315
Uses of lac fusions for the study of biological problems
Silhavy, T. J., & Beckwith, J. (1985) · Microbiological Reviews · doi:10.1128/mmbr.49.4.398-418.1985 · Cited by 301
Mombaerts, P. (2004) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2004.01.014 · Cited by 295
The Frizzled family: receptors for multiple signal transduction pathways.
Huang, H., & Klein, P. S. (2004) · Genome biology · doi:10.1186/gb-2004-5-7-234 · Cited by 294
Loconto, J., Papes, F., Chang, E., Stowers, L., Jones, E. P., Takada, T., Kumánovics, A., Lindahl, K. F., & Dulac, C. (2003) · Cell · doi:10.1016/s0092-8674(03)00153-3 · Cited by 292
Functional conservation of an insect odorant receptor gene across 250 million years of evolution
Jones, W. D., Nguyen, T., Kloss, B., Lee, K. J., & Vosshall, L. B. (2005) · Current Biology · doi:10.1016/j.cub.2005.02.007 · Cited by 287
Self-citationDrosophila melanogaster G Protein–Coupled Receptors
Brody, T., & Cravchik, A. (2000) · The Journal of Cell Biology · doi:10.1083/jcb.150.2.f83 · Cited by 268
Coexpression of Two Functional Odor Receptors in One Neuron
Goldman, A. L., Van der Goes van Naters, W., Lessing, D., Warr, C. G., & Carlson, J. R. (2005) · Neuron · doi:10.1016/j.neuron.2005.01.025 · Cited by 268
A candidate olfactory receptor subtype highly conserved across different insect orders
Krieger, J., Klink, O., Mohl, C., Raming, K., & Breer, H. (2003) · Journal of Comparative Physiology A · doi:10.1007/s00359-003-0427-x · Cited by 264
Olfactory receptor antagonism between odorants
Oka, Y., Omura, M., Kataoka, H., & Touhara, K. (2004) · The EMBO Journal · doi:10.1038/sj.emboj.7600032 · Cited by 259
Dwyer, N. D., Troemel, E. R., Sengupta, P., & Bargmann, C. I. (1998) · Cell · doi:10.1016/s0092-8674(00)81173-3 · Cited by 248
Fiala, A., Spall, T., Diegelmann, S., Eisermann, B., Sachse, S., Devaud, J.-M., Buchner, E., & Galizia, C. G. (2002) · Current Biology · doi:10.1016/s0960-9822(02)01239-3 · Cited by 220
Self-citationNovel Genomic cDNA Hybrids Produce Effective RNA Interference in Adult Drosophila
Kalidas, S., & Smith, D. P. (2002) · Neuron · doi:10.1016/s0896-6273(02)00560-3 · Cited by 211
Pitts, R. J., Fox, A. N., & Zwiebel, L. J. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0308146101 · Cited by 209
Wetzel, C. H., Behrendt, H.-J., Gisselmann, G., Störtkuhl, K. F., Hovemann, B., & Hatt, H. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.151103998 · Cited by 196
Odorant Receptors on Axon Termini in the Brain
Barnea, G., O'Donnell, S., Mancia, F., Sun, X., Nemes, A., Mendelsohn, M., & Axel, R. (2004) · Science · doi:10.1126/science.1096146 · Cited by 186
Yanagawa, S.-I., Lee, J.-S., & Ishimoto, A. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.48.32353 · Cited by 173
The odor coding system of Drosophila
Hallem, E. A., & Carlson, J. R. (2004) · Trends in Genetics · doi:10.1016/j.tig.2004.06.015 · Cited by 173
Lu, M., Echeverri, F., & Moyer, B. D. (2003) · Traffic · doi:10.1034/j.1600-0854.2003.00097.x · Cited by 169
Ueno, K., Ohta, M., Morita, H., Mikuni, Y., Nakajima, S., Yamamoto, K., & Isono, K. (2001) · Current Biology · doi:10.1016/s0960-9822(01)00450-x · Cited by 161
Elmore, T., Ignell, R., Carlson, J. R., & Smith, D. P. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-30-09906.2003 · Cited by 146
Functional analysis of an olfactory receptor in Drosophila melanogaster
Störtkuhl, K. F., & Kettler, R. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.151105698 · Cited by 111
Olfactory Receptor Trafficking Involves Conserved Regulatory Steps
Gimelbrant, A. A., Haley, S., & McClintock, T. S. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m005433200 · Cited by 95
Towards a molecular understanding of drosophila hearing
Caldwell, J. C., & Eberl, D. F. (2002) · Journal of Neurobiology · doi:10.1002/neu.10126 · Cited by 89
Kim, J., Moriyama, E. N., Warr, C. G., Clyne, P. J., & Carlson, J. R. (2000) · Bioinformatics · doi:10.1093/bioinformatics/16.9.767 · Cited by 87
Trafficking prerogatives of olfactory receptors
McClintock, T. S., & Sammeta, N. (2003) · Neuroreport · doi:10.1097/00001756-200308260-00001 · Cited by 82
Talluri, S., Bhatt, A., & Smith, D. P. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.25.11475 · Cited by 82
Truncation Releases Olfactory Receptors from the Endoplasmic Reticulum of Heterologous Cells
Gimelbrant, A. A., Stoss, T. D., Landers, T. M., & McClintock, T. S. (1999) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.1999.0722301.x · Cited by 77
Protein phosphatase 2C binds selectively to and dephosphorylates metabotropic glutamate receptor 3
Flajolet, M., Rakhilin, S., Wang, H., Starkova, N. N., Nuangchamnong, N., Nairn, A. C., & Greengard, P. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2136600100 · Cited by 71
Three new Drosophila markers of intracellular membranes
LaJeunesse, D., Buckner, S. M., Lake, J., Na, C., Pirt, A., & Fromson, K. (2004) · BioTechniques · doi:10.2144/04365st01 · Cited by 63
Mapping Biochemical Networks with Protein Fragment Complementation Assays
Remy, I., & Michnick, S. W. (2015) · Methods in molecular biology · doi:10.1007/978-1-4939-2425-7_31 · Cited by 54
Self-citationPutative Drosophila odor receptor OR43b localizes to dendrites of olfactory neurons
Elmore, T., & Smith, D. P. (2001) · Insect Biochemistry and Molecular Biology · doi:10.1016/s0965-1748(00)00184-3 · Cited by 43
Miura, N., Atsumi, S., Tabunoki, H., & Sato, R. (2005) · The Journal of Comparative Neurology · doi:10.1002/cne.20488 · Cited by 42
Conti‐Fine, B. M., Lei, S., & McLane, K. E. (1996) · Annual Review of Biophysics and Biomolecular Structure · doi:10.1146/annurev.bb.25.060196.001213 · Cited by 23
Michnick, S. W. (2004) · Drug Discovery Today · doi:10.1016/s1359-6446(03)03022-8 · Cited by 20
Self-citationInomata, N., Goto, H., Itoh, M., & Isono, K. (2004) · Genetics · doi:10.1534/genetics.104.027045 · Cited by 20
Isono, K. (2005) · Chemical Senses · doi:10.1093/chemse/bjh221 · Cited by 12
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Metadata
- Authors
- Benton, R., Sachse, S., Michnick, S. W., & Vosshall, L. B.
- Venue
- PLoS Biology
- Publisher
- Public Library of Science (PLoS)
- Published
- 2006-01-17
- Volume
- 4
- Issue
- 2
- Pages
- e20
- ISSN
- 1544-9173 (ISSN-L)
- 1545-7885
- OpenAlex
- W2082788644
- Cited by
- 1,015
- References
- 85
- FWCI
- 18.16
- Type
- journal article
- Language
- en
- Open access
- gold
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