Comparative chemosensation from receptors to ecology

Nature

Volumn 444, Issue 7117, 2006, Pages 295-301

  Bargmann, Cornelia I ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ECOLOGY; NEUROLOGY; ODOR CONTROL; PROTEINS; SENSORY PERCEPTION;

CHEMOSENSATION; DROSOPHILA MELANOGASTER; ODORANTS; OLFACTORY NEURONS;

CHEMICAL SENSORS;

G PROTEIN COUPLED RECEPTOR;

CHEMORECEPTION; FLY; ODOR; OLFACTORY CUE; PROTEIN;

CHEMOREACTIVITY; CHEMORECEPTOR; COMPARATIVE STUDY; DROSOPHILA MELANOGASTER; ENVIRONMENTAL FACTOR; HUMAN; NONHUMAN; ODOR; OLFACTORY NERVE; OLFACTORY SYSTEM; PRIORITY JOURNAL; RECEPTOR INTRINSIC ACTIVITY; REVIEW; SMELLING; SPECIES DIFFERENCE;

DROSOPHILA MELANOGASTER; INSECTA; RODENTIA;

EID: 33751118221     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature05402     Document Type: Review

References (100)

1. Buck, L. & Axel, R. A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 65, 175-187 (1991).
2. Niimura, Y. & Nei, M. Comparative evolutionary analysis of olfactory receptor gene clusters between humans and mice. Gene 14, 13-21 (2005).
3. Niimura, Y. & Nei, M. Evolutionary changes of the number of olfactory receptor genes in the human and mouse lineages. Gene 346, 23-28 (2005).
4. Robertson, H. A. & Thomas, J. H. The putative chemoreceptor families of C. elegans. Wormbook 〈http://www.wormbook.org〉 doi/10.1895/ wormbook.1.66.1 (2006).
5. Troemel, E. R., Chou, J. H., Dwyer, N. D., Colbert, H. A. & Bargmann, C. I. Divergent seven transmembrane receptors are candidate chemosensory receptors in C. elegans. Cell 83, 207-218 (1995).
6. Colosimo, M. E. et al. Identification of thermosensory and olfactory neuron-specific genes via expression profiling of single neuron types. Curr. Biol. 14, 2245-2251 (2004).
7. McCarroll, S. A., Li, H. & Bargmann, C. I. Identification of transcriptional regulatory elements in chemosensory receptor genes by probabilistic segmentation. Curr. Biol. 15, 347-352 (2005).
8. Chen, N. et al. Identification of a nematode chemosensory gene family. Proc. Natl Acad. Sci. USA 102, 146-151 (2005).
9. Gray, J. M. et al. Oxygen sensation and social feeding mediated by a C. elegans guanylate cyclase homologue. Nature 430, 317-322 (2004).
10. Cheung, B. H., Cohen, M., Rogers, C., Albayram, O. & de Bono, M. Experience-dependent modulation of C. elegans behavior by ambient oxygen. Curr. Biol. 15, 905-917 (2005).
11. Yu, S., Avery, L., Baude, E. & Garbers, D. L. Guanylyl cyclase expression in specific sensory neurons: a new family of chemosensory receptors. Proc. Natl Acad. Sci. USA 94, 3384-3387 (1997).
12. Clyne, P. J. et al. A novel family of divergent seven-transmembrane proteins: candidate odorant receptors in Drosophila. Neuron 22, 327-338 (1999).
13. Vosshall, L. B., Amrein, H., Morozov, P. S., Rzhetsky, A. & Axel, R. A spatial map of olfactory receptor expression in the Drosophila antenna. Cell 96, 725-736 (1999).
14. Benton, R., Sachse, S., Michnick, S. W. & Vosshall, L. B. Atypical membrane topology and heteromeric function of Drosophila odorant receptors in vivo. PLoS Biol. 4, e20 (2006).
15. Wistrand, M., Kall, L. & Sonnhammer, E. L. A general model of G protein-coupled receptor sequences and its application to detect remote homologs. Protein Sci. 15, 509-521 (2006).
16. Neuhaus, E. M. et al. Odorant receptor heterodimerization in the olfactory system of Drosophila melanogaster. Nature Neurosci. 8, 15-17 (2005).
17. Zhao, H. et al. Functional expression of a mammalian odorant receptor. Science 279, 237-242 (1998).
18. Krautwurst, D., Yau, K. W. & Reed, R. R. Identification of ligands for olfactory receptors by functional expression of a receptor library. Cell 95, 917-926 (1998).
19. Malnic, B., Hirono, J., Sato, T. & Buck, L. B. Combinatorial receptor codes for odors. Cell 96, 713-723 (1999).
20. Wetzel, C. H. et al. Specificity and sensitivity of a human olfactory receptor functionally expressed in human embryonic kidney 293 cells and Xenopus laevis oocytes. J. Neurosci. 19, 7426-7433 (1999).
21. Kajiya, K. et al. Molecular bases of odor discrimination: reconstitution of olfactory receptors that recognize overlapping sets of odorants. J. Neurosci. 21, 6018-6025 (2001).
22. Touhara, K. et al. Functional identification and reconstitution of an odorant receptor in single olfactory neurons. Proc. Natl Acad. Sci. USA 96, 4040-4045 (1999).
23. Araneda, R. C., Kini, A. D. & Firestein, S. The molecular receptive range of an odorant receptor. Nature Neurosci. 3, 1248-1255 (2000).
24. Spehr, M. et al. Identification of a testicular odorant receptor mediating human sperm chemotaxis. Science 299, 2054-2058 (2003).
25. Gether, U. & Kobilka, B. K. G protein-coupled receptors. II. Mechanism of agonist activation. J. Biol. Chem. 273, 17979-17982 (1998).
26. Palczewski, K. et al. Crystal structure of rhodopsin: a G protein-coupled receptor. Science 289, 739-745 (2000).
27. Lu, Z. L., Saldanha, J. W. & Hulme, E. C. Seven-transmembrane receptors: crystals clarify. Trends Pharmacol. Sci. 23, 140-146 (2002).
28. Katada, S., Hirokawa, T., Oka, Y., Suwa, M. & Touhara, K. Structural basis for a broad but selective ligand spectrum of a mouse olfactory receptor: mapping the odorant-binding site. J. Neurosci. 25, 1806-1815 (2005).
29. Oka, Y., Omura, M., Kataoka, H. & Touhara, K. Olfactory receptor antagonism between odorants. EMBO J. 14, 120-126 (2004).
30. de Bruyne, M., Clyne, P. J. & Carlson, J. R. Odor coding in a model olfactory organ: the Drosophila maxillary palp. J. Neurosci. 19, 4520-4532 (1999).
31. de Bruyne, M., Foster, K. & Carlson, J. R. Odor coding in the Drosophila antenna. Neuron 30, 537-552 (2001).
32. Wang, J. W., Wong, A. M., Flores, J., Vosshall, L. B. & Axel, R. Two-photon calcium imaging reveals an odor-evoked map of activity in the fly brain. Cell 112, 271-282 (2003).
33. Elmore, T., Ignell, R., Carlson, J. R. & Smith, D. P. Targeted mutation of a Drosophila odor receptor defines receptor requirement in a novel class of sensillum. J. Neurosci. 23, 9906-9912 (2003).
34. Yao, C. A., Ignell, R. & Carlson, J. R. Chemosensory coding by neurons in the coeloconic sensilla of the Drosophila antenna. J. Neurosci. 25, 8539-8567 (2005).
35. Hallem, E. A., Ho, M. G. & Carlson, J. R. The molecular basis of odor coding in the Drosophila antenna. Cell 117, 965-979 (2004).
36. Kreher, S. A., Kwon, J. Y. & Carlson, J. R. The molecular basis of odor coding in the Drosophila larva. Neuron 46, 445-456 (2005).
37. Hallem, E. A. & Carlson, J. R. Coding of odors by a receptor repertoire. Cell 125, 143-160 (2006).
38. Sengupta, P., Chou, J. C. & Bargmann, C. I. odr-10 encodes a seven transmembrane domain olfactory receptor required for responses to the odorant diacetyl. Cell 84, 899-909 (1996).
39. Chess, A., Simon, I., Cedar, H. & Axel, R. Allelic inactivation regulates olfactory receptor gene expression. Cell 78, 823-834 (1994).
40. Serizawa, S. et al. Negative feedback regulation ensures the one receptor-one olfactory neuron rule in mouse. Science 302, 2088-2094 (2003).
41. Ressler, K. J., Sullivan, S. L. & Buck, L. B. A zonal organization of odorant receptor gene expression in the olfactory epithelium. Cell 73, 597-609 (1993).
42. Vassar, R., Ngai, J. & Axel, R. Spatial segregation of odorant receptor expression in the mammalian olfactory epithelium. Cell 74, 309-318 (1993).
43. Qasba, P. & Reed, R. R. Tissue and zonal-specific expression of an olfactory receptor transgene. J. Neurosci. 18, 227-236 (1998).
44. Lewcock, J. W. & Reed, R. R. A feedback mechanism regulates monoallelic odorant receptor expression. Proc. Natl Acad. Sci. USA 101, 1069-1074 (2004).
45. Shykind, B. M. et al. Gene switching and the stability of odorant receptor gene choice. Cell 117, 801-815 (2004).
46. Larsson, M. C. et al. Or83b encodes a broadly expressed odorant receptor essential for Drosophila olfaction. Neuron 43, 703-714 (2004).
47. Fishilevich, E. & Vosshall, L. B. Genetic and functional subdivision of the Drosophila antennal lobe. Curr. Biol. 15, 1548-1553 (2005).
48. Couto, A., Alenius, M. & Dickson, B. J. Molecular, anatomical, and functional organization of the Drosophila olfactory system. Curr. Biol. 15, 1535-1547 (2005).
49. Dobritsa, A. A. et al. Integrating the molecular and cellular basis of odor coding in the Drosophila antenna. Neuron 37, 827-841 (2003).
50. Goldman, A. L., Van der Goes van Naters, W., Lessing, D., Warr, C. G. & Carlson, J. R. Coexpression of two functional odor receptors in one neuron. Neuron 45, 661-666 (2005).
51. Sengupta, P., Colbert, H. A. & Bargmann, C. I. The C. elegans gene odr-7 encodes an olfactory-specific member of the nuclear receptor superfamily. Cell 79, 971-980 (1994).
52. Lanjuin, A. & Sengupta, P. Specification of chemosensory neuron subtype identities in Caenorhabditis elegans. Curr. Opin. Neurobiol. 14, 22-30 (2004).
53. Johnston, R. J. J., Chang, S., Etchberger, J. F., Ortiz, C. O. & Hobert, O. MicroRNAs acting in a double-negative feedback loop to control a neuronal cell fate decision. Proc. Natl Acad. Sci. USA 102, 12449-12454 (2005).
54. Troemel, E. R., Sagasti, A. & Bargmann, C. I. Lateral signaling mediated by axon contact and calcium entry regulates asymmetric odorant receptor expression in C. elegans. Cell 99, 387-398 (1999).
55. Peckol, E. L., Troemel, E. R. & Bargmann, C. I. Sensory experience and sensory activity regulate chemosensory receptor gene expression in Caenorhabditis elegans. Proc. Natl Acad. Sci. USA 98, 11032-11038 (2001).
56. Nolan, K. M., Sarafi-Reinach, T. R., Horne, J. G., Saffer, A. M. & Sengupta, P. The DAF-7 TGF-β signaling pathway regulates chemosensory receptor gene expression in C. elegans. Genes Dev. 16, 3061-3073 (2002).
57. Fox, A. N., Pitts, R. J., Robertson, H. M., Carlson, J. R. & Zwiebel, L. J. Candidate odorant receptors from the malaria vector mosquito Anopheles gambiae and evidence of downregulation in response to blood feeding. Proc. Natl Acad. Sci. USA 98, 14693-14697 (2001).
58. Fishilevich, E. et al. Chemotaxis behavior mediated by single larval olfactory neurons in Drosophila. Curr. Biol. 15, 2086-2096 (2005).
59. Barth, A. L., Justice, N. J. & Ngai, J. Asynchronous onset of odorant receptor expression in the developing zebrafish olfactory system. Neuron 16, 23-34 (1996).
60. Ressler, K. J., Sullivan, S. L. & Buck, L. B. Information coding in the olfactory system: evidence for a stereotyped and highly organized epitope map in the olfactory bulb. Cell 79, 1245-1256 (1994).
61. Vassar, R. et al. Topographic organization of sensory projections to the olfactory bulb. Cell 79, 981-992 (1994).
62. Strotmann, J. et al. Local permutations in the glomerular array of the mouse olfactory bulb. J. Neurosci. 20, 6927-6938 (2000).
63. Komiyama, T. & Luo, L. Development of wiring specificity in the olfactory system. Curr. Opin. Neurobiol. 16, 67-73 (2006).
64. White, J. G., Southgate, E., Thomson, J. N. & Brenner, S. The structure of the nervous system of the nematode Caenorhabditis elegans. Phil. Trans. R. Soc. Lond. B 314, 1-340 (1986).
65. Mori, K., Takahashi, Y. K., Igarashi, K. M. & Yamaguchi, M. Maps of odorant molecular features in the mammalian olfactory bulb. Physiol. Rev. 86, 409-433 (2006).
66. Rubin, B. & Katz, L. Optical imaging of odorant representations in the mammalian olfactory bulb. Neuron 23, 499-511 (1999).
67. Meister, M. & Bonhoeffer, T. Tuning and topography in an animal olfactory bulb. J. Neurosci. 15, 1351-1360 (2001).
68. Baier, H. & Korsching, S. Olfactory glomeruli in the zebrafish form an invariant pattern and are identifiable across animals. J. Neurosci. 14, 219-230 (1994).
69. Friedrich, R. W. & Korsching, S. I. Combinatorial and chemotopic odorant coding in the zebrafish olfactory bulb visualized by optical imaging. Neuron 18, 737-752 (1997).
70. Wilson, R. I., Turner, G. C. & Laurent, G. Transformation of olfactory representations in the Drosophila antennal lobe. Science 303, 366-370 (2004).
71. Wilson, R. I. & Laurent, G. Role of GABAergic inhibition in shaping odor-evoked spatiotemporal patterns in the Drosophila antennal lobe. J. Neurosci. 25, 9069-9079 (2005).
72. Ng, M. et al. Transmission of olfactory information between three populations of neurons in the antennal lobe of the fly. Neuron 36, 463-474 (2002).
73. Shields, V. D. & Hildebrand, J. G. Responses of a population of antennal olfactory receptor cells in the female moth Manduca sexta to plant-associated volatile organic compounds. J. Comp. Physiol. A 186, 1135-1151 (2001).
74. Galizia, C. G. & Menzel, R. The role of glomeruli in the neural representation of odours: results from optical recording studies. J. Insect Physiol. 47, 115-130 (2001).
75. Christensen, T. A. & Hildebrand, J. G. Male-specific, sex pheromone-selective projection neurons in the antennal lobes of the moth Manduca sexta. J. Comp. Physiol. A 160, 553-569 (1987).
76. Hansson, B. S., Christensen, T. A. & Hildebrand, J. G. Functionally distinct subdivisions of the macroglomerular complex in the antennal lobe of the male sphinx moth Manduca sexta. J. Comp. Neurol. 312, 264-278 (1991).
77. Christensen, T. A., Waldrop, B. R., Harrow, I. D. & Hildebrand, J. G. Local interneurons and information processing in the olfactory glomeruli of the moth Manduca sexta. J. Comp. Physiol. A 173, 385-399 (1993).
78. Lin, D. Y., Shea, S. D. & Katz, L. C. Representation of natural stimuli in the rodent main olfactory bulb. Neuron 50, 937-949 (2006).
79. Bargmann, C. I. & Mori, I. in C. elegans II (eds Riddle, D. L., Blumenthal, T., Meyer, B. J. & Priess, J. R.) 717-737 (Cold Spring Harbor Laboratory Press, New York, 1997).
80. Troemel, E. R., Kimmel, B. E. & Bargmann, C. I. Reprogramming chemotaxis responses: sensory neurons define olfactory preferences in C. elegans. Cell 91, 161-169 (1997).
81. Tobin, D. et al. Combinatorial expression of TRPV channel proteins defines their sensory functions and subcellular localization in C. elegans neurons. Neuron 35, 307-318 (2002).
82. Mueller, K. L. et al. The receptors and coding logic for bitter taste. Nature 434, 225-229 (2005).
83. Zhao, G. Q. et al. The receptors for mammalian sweet and umami taste. Cell 115, 255-266 (2003).
84. Marella, S. et al. Imaging taste responses in the fly brain reveals a functional map of taste category and behavior. Neuron 49, 285-295 (2006).
85. Suh, G. S. et al. A single population of olfactory sensory neurons mediates an innate avoidance behaviour in Drosophila. Nature 431, 854-859 (2004).
86. 2 reveals flower profitability to moths. J. Chem. Ecol. 30, 1285-1288 (2004).
87. Stockinger, P., Kvitsiani, D., Rotkopf, S., Tirian, L. & Dickson, B. J. Neural circuitry that governs Drosophila male courtship behavior. Cell 121, 795-807 (2005).
88. Mongeau, R., Miller, G. A., Chiang, E. & Anderson, D. J. Neural correlates of competing fear behaviors evoked by an innately aversive stimulus. J. Neurosci. 23, 3855-3868 (2003).
89. Mandiyan, V. S., Coats, J. K. & Shah, N. M. Deficits in sexual and aggressive behaviors in Cnga2 mutant mice. Nature Neurosci. 8, 1660-1662 (2005).
90. Quinn, W. G., Harris, W. A. & Benzer, S. Conditioned behavior in Drosophila melanogaster. Proc. Natl Acad. Sci. USA 71, 708-712 (1974).
91. Zhang, Y., Lu, H. & Bargmann, C. Pathogenic bacteria induce aversive olfactory learning in Caenorhabditis elegans. Nature 438, 179-184 (2005).
92. Glusman, G. et al. The olfactory receptor gene superfamily: data mining, classification, and nomenclature. Mamm. Genome 11, 1016-1023 (2000).
93. Niimura, Y. & Nei, M. Evolutionary dynamics of olfactory receptor genes in fishes and tetrapods. Proc. Natl Acad. Sci. USA 102, 6039-6044 (2005).
94. Freitag, J., Krieger, J., Strotmann, J. & Breer, H. Two classes of olfactory receptors in Xenopus laevis. Neuron 15, 1383-1392 (1995).
95. Crane, P. R., Friis, E. M. & Pedersen, K. R. The origin and early diversification of angiosperms. Nature 374, 27-33 (1995).
96. Bernays, E. A. Evolution of feeding behavior in insect herbivores. Bioscience 48, 35-44 (1998).
97. Lomvardas, S. et al. Interchromosomal interactions and olfactory receptor choice. Cell 126, 403-413 (2006).
98. Marin, E. C., Jefferis, G. S., Komiyama, T., Zhu, H. & Luo, L. Representation of the glomerular olfactory map in the Drosophila brain. Cell 109, 243-255 (2002).
99. Wong, A. M., Wang, J. W. & Axel, R. Spatial representation of the glomerular map in the Drosophila protocerebrum. Cell 109, 229-241 (2002).
100. Zou, Z., Horowitz, L. F., Montmayeur, J. P., Snapper, S. & Buck, L. B. Genetic tracing reveals a stereotyped sensory map in the olfactory cortex. Nature 414, 173-179 (2001).