Chemosensory signals and their receptors in the olfactory neural system

Neuroscience

Volumn 254, Issue , 2013, Pages 45-60

  Ihara, S ^a,b   Yoshikawa, K ^a   Touhara, K ^a,b  

^a UNIVERSITY OF TOKYO   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

Author keywords

Odorant; Olfactory; Pheromone; Receptor

Indexed keywords

ASCAROSIDE; MEMBRANE PROTEIN; SEX PHEROMONE; UNCLASSIFIED DRUG;

AVOIDANCE BEHAVIOR; CAENORHABDITIS ELEGANS; CHEMICAL ANALYSIS; COURTSHIP; DROSOPHILA; FOOD PREFERENCE; INSECT; METABOLIC REGULATION; MOTHER CHILD RELATION; NEUROMODULATION; NONHUMAN; OLFACTORY DISCRIMINATION; OLFACTORY NERVOUS SYSTEM; OLFACTORY RECEPTOR; PLANT INSECT INTERACTION; PREDATOR AVOIDANCE; PRIORITY JOURNAL; REVIEW; SEX DETERMINATION; SEXUAL BEHAVIOR; SIGNAL TRANSDUCTION; SOCIAL BEHAVIOR; WORM; ANIMAL; CHEMORECEPTOR CELL; HUMAN; ODOR; OLFACTORY NERVE; OLFACTORY SYSTEM; PHYSIOLOGY; VOMERONASAL ORGAN;

ANIMALS; CHEMORECEPTOR CELLS; HUMANS; OLFACTORY NERVE; OLFACTORY PATHWAYS; SIGNAL TRANSDUCTION; SMELL; VOMERONASAL ORGAN;

EID: 84885460763     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2013.08.063     Document Type: Review

References (144)

1. Ai M., Min S., Grosjean Y., Leblanc C., Bell R., Benton R., Suh G.S. Acid sensing by the Drosophila olfactory system. Nature 2010, 468:691-695.
2. Arakawa H., Kelliher K.R., Zufall F., Munger S.D. The receptor guanylyl cyclase type D (GC-D) ligand uroguanylin promotes the acquisition of food preferences in mice. Chem Senses 2013, 38:391-397.
3. Bacchini A., Gaetani E., Cavaggioni A. Pheromone binding proteins of the mouse, Mus musculus. Experientia 1992, 48:419-421.
4. Bargmann C.I. Chemosensation in C. elegans. WormBook 2006, 1-29.
5. Bargmann C.I., Horvitz H.R. Control of larval development by chemosensory neurons in Caenorhabditis elegans. Science 1991, 251:1243-1246.
6. Bartelt R.J., Schaner A.M., Jackson L.L. Cis-vaccenyl acetate as an aggregation pheromone in Drosophila melanogaster. J Chem Ecol 1985, 11:1747-1756.
7. Beauchamp G.K., Yamazaki K. Chemical signalling in mice. Biochem Soc Trans 2003, 31:147-151.
8. Becher P.G., Bengtsson M., Hansson B.S., Witzgall P. Flying the fly: long-range flight behavior of Drosophila melanogaster to attractive odors. J Chem Ecol 2010, 36:599-607.
9. Benton R., Sachse S., Michnick S.W., Vosshall L.B. Atypical membrane topology and heteromeric function of Drosophila odorant receptors in vivo. PLoS Biol 2006, 4:e20.
10. Benton R., Vannice K.S., Gomez-Diaz C., Vosshall L.B. Variant ionotropic glutamate receptors as chemosensory receptors in Drosophila. Cell 2009, 136:149-162.
11. Benton R., Vannice K.S., Vosshall L.B. An essential role for a CD36-related receptor in pheromone detection in Drosophila. Nature 2007, 450:289-293.
12. Bjostad L.B., Wolf W.A., Roelofs W.L. Pheromone biosynthesis in lepidopterans: desaturation and chain shortening. Pheromone biochemistry 1987, 77-120. Academic Press, Orlando, FL. G.D. Prestwich, G.J. Blomquist (Eds.).
13. Boschat C., Pelofi C., Randin O., Roppolo D., Luscher C., Broillet M.C., Rodriguez I. Pheromone detection mediated by a V1r vomeronasal receptor. Nat Neurosci 2002, 5:1261-1262.
14. Bronson F.H., Caroom D. Preputial gland of the male mouse; attractant function. J Reprod Fertil 1971, 25:279-282.
15. Buck L., Axel R. A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 1991, 65:175-187.
16. Bufe B., Schumann T., Zufall F. Formyl peptide receptors from immune and vomeronasal system exhibit distinct agonist properties. J Biol Chem 2012, 287:33644-33655.
17. Butcher R.A., Fujita M., Schroeder F.C., Clardy J. Small-molecule pheromones that control dauer development in Caenorhabditis elegans. Nat Chem Biol 2007, 3:420-422.
18. Butcher R.A., Ragains J.R., Kim E., Clardy J. A potent dauer pheromone component in Caenorhabditis elegans that acts synergistically with other components. Proc Natl Acad Sci U S A 2008, 105:14288-14292.
19. Butcher R.A., Ragains J.R., Li W., Ruvkun G., Clardy J., Mak H.Y. Biosynthesis of the Caenorhabditis elegans dauer pheromone. Proc Natl Acad Sci U S A 2009, 106:1875-1879.
20. Butenandt A., Groschel U., Karlson P., Zillig W. N-acetyl tyramine, its isolation from Bombyx cocoons & its chemical & biological properties. Arch Biochem Biophys 1959, 83:76-83.
21. Butterworth F.M. Lipids of Drosophila: a newly detected lipid in the male. Science 1969, 163:1356-1357.
22. Chamero P., Marton T.F., Logan D.W., Flanagan K., Cruz J.R., Saghatelian A., Cravatt B.F., Stowers L. Identification of protein pheromones that promote aggressive behaviour. Nature 2007, 450:899-902.
23. Cheetham S.A., Thom M.D., Jury F., Ollier W.E., Beynon R.J., Hurst J.L. The genetic basis of individual-recognition signals in the mouse. Curr Biol 2007, 17:1771-1777.
24. Coureaud G., Moncomble A.S., Montigny D., Dewas M., Perrier G., Schaal B. A pheromone that rapidly promotes learning in the newborn. Curr Biol 2006, 16:1956-1961.
25. Del Punta K., Leinders-Zufall T., Rodriguez I., Jukam D., Wysocki C.J., Ogawa S., Zufall F., Mombaerts P. Deficient pheromone responses in mice lacking a cluster of vomeronasal receptor genes. Nature 2002, 419:70-74.
26. Dewan A., Pacifico R., Zhan R., Rinberg D., Bozza T. Non-redundant coding of aversive odours in the main olfactory pathway. Nature 2013, 497:486-489.
27. Dielenberg R.A., McGregor I.S. Defensive behavior in rats towards predatory odors: a review. Neurosci Biobehav Rev 2001, 25:597-609.
28. Duan X., Block E., Li Z., Connelly T., Zhang J., Huang Z., Su X., Pan Y., Wu L., Chi Q., Thomas S., Zhang S., Ma M., Matsunami H., Chen G.Q., Zhuang H. Crucial role of copper in detection of metal-coordinating odorants. Proc Natl Acad Sci U S A 2012, 109:3492-3497.
29. Ejima A., Smith B.P., Lucas C., van der Goes van Naters W., Miller C.J., Carlson J.R., Levine J.D., Griffith L.C. Generalization of courtship learning in Drosophila is mediated by cis-vaccenyl acetate. Curr Biol 2007, 17:599-605.
30. Fendt M., Endres T., Lowry C.A., Apfelbach R., McGregor I.S. TMT-induced autonomic and behavioral changes and the neural basis of its processing. Neurosci Biobehav Rev 2005, 29:1145-1156.
31. Ferrero D.M., Lemon J.K., Fluegge D., Pashkovski S.L., Korzan W.J., Datta S.R., Spehr M., Fendt M., Liberles S.D. Detection and avoidance of a carnivore odor by prey. Proc Natl Acad Sci U S A 2011, 108:11235-11240.
32. Ferrero DM, Moeller LM, Osakada T, Horio N, Li Q, D.S. Roy, Cichy A, Spehr M, Touhara K, Liberles SD (2013) A juvenile mouse pheromone inhibits sexual behavior through the vomeronasal system. Nature DOI 10.1038/nature 12579.
33. Ferrero D.M., Wacker D., Roque M.A., Baldwin M.W., Stevens R.C., Liberles S.D. Agonists for 13 trace amine-associated receptors provide insight into the molecular basis of odor selectivity. ACS Chem Biol 2012, 7:1184-1189.
34. Finlayson J.S., Asofsky R., Potter M., Runner C.C. Major urinary protein complex of normal mice: origin. Science 1965, 149:981-982.
35. Forte L.R. Uroguanylin and guanylin peptides: pharmacology and experimental therapeutics. Pharmacol Ther 2004, 104:137-162.
36. Golden J.W., Riddle D.L. A pheromone influences larval development in the nematode Caenorhabditis elegans. Science 1982, 218:578-580.
37. Gomez-Diaz C., Reina J.H., Cambillau C., Benton R. Ligands for pheromone-sensing neurons are not conformationally activated odorant binding proteins. PLoS Biol 2013, 11:e1001546.
38. Grosjean Y., Rytz R., Farine J.P., Abuin L., Cortot J., Jefferis G.S., Benton R. An olfactory receptor for food-derived odours promotes male courtship in Drosophila. Nature 2011, 478:236-240.
39. Ha T.S., Smith D.P. A pheromone receptor mediates 11-cis-vaccenyl acetate-induced responses in Drosophila. J Neurosci 2006, 26:8727-8733.
40. Haga S., Hattori T., Sato T., Sato K., Matsuda S., Kobayakawa R., Sakano H., Yoshihara Y., Kikusui T., Touhara K. The male mouse pheromone ESP1 enhances female sexual receptive behaviour through a specific vomeronasal receptor. Nature 2010, 466:118-122.
41. Harvey S., Jemiolo B., Novotny M. Pattern of volatile compounds in dominant and subordinate male mouse urine. J Chem Ecol 1989, 15:2061-2072.
42. Honda K. Identification of host-plant chemicals stimulating oviposition by swallowtail butterfly, Papilio protenor. J Chem Ecol 1990, 16:325-337.
43. 2 by an olfactory subsystem in the mouse. Science 2007, 317:953-957.
44. Hu P.J. Dauer. WormBook 2007, 1-19.
45. Ichinose T., Honda H. Ovipositional behavior of Papilio protenor demetrius Cramer and the factors involved in its host plants. Appl Entomol Zool 1978, 13:103-114.
46. Isogai Y., Si S., Pont-Lezica L., Tan T., Kapoor V., Murthy V.N., Dulac C. Molecular organization of vomeronasal chemoreception. Nature 2011, 478:241-245.
47. Izrayelit Y., Srinivasan J., Campbell S.L., Jo Y., von Reuss S.H., Genoff M.C., Sternberg P.W., Schroeder F.C. Targeted metabolomics reveals a male pheromone and sex-specific ascaroside biosynthesis in Caenorhabditis elegans. ACS Chem Biol 2012, 7:1321-1325.
48. Jang H., Kim K., Neal S.J., Macosko E., Kim D., Butcher R.A., Zeiger D.M., Bargmann C.I., Sengupta P. Neuromodulatory state and sex specify alternative behaviors through antagonistic synaptic pathways in C. elegans. Neuron 2012, 75:585-592.
49. Jemiolo B., Xie T.M., Novotny M. Socio-sexual olfactory preference in female mice: attractiveness of synthetic chemosignals. Physiol Behav 1991, 50:1119-1122.
50. Jeong P.Y., Jung M., Yim Y.H., Kim H., Park M., Hong E., Lee W., Kim Y.H., Kim K., Paik Y.K. Chemical structure and biological activity of the Caenorhabditis elegans dauer-inducing pheromone. Nature 2005, 433:541-545.
51. Jin X., Ha T.S., Smith D.P. SNMP is a signaling component required for pheromone sensitivity in Drosophila. Proc Natl Acad Sci U S A 2008, 105:10996-11001.
52. Jones W.D., Cayirlioglu P., Kadow I.G., Vosshall L.B. Two chemosensory receptors together mediate carbon dioxide detection in Drosophila. Nature 2007, 445:86-90.
53. Joo H.J., Kim K.Y., Yim Y.H., Jin Y.X., Kim H., Kim M.Y., Paik Y.K. Contribution of the peroxisomal acox gene to the dynamic balance of daumone production in Caenorhabditis elegans. J Biol Chem 2010, 285:29319-29325.
54. Joseph R.M., Devineni A.V., King I.F., Heberlein U. Oviposition preference for and positional avoidance of acetic acid provide a model for competing behavioral drives in Drosophila. Proc Natl Acad Sci U S A 2009, 106:11352-11357.
55. Jurenka R.A. Biochemistry of female moth sex pheromones. Insect pheromone biochemistry and molecular biology 2003, 53-80. Elsevier, Amsterdam. G. Blomquist, R. Vogt (Eds.).
56. Kaissling K.-E., Kasang G., Bestmann H.J., Stransky W., Vostrowsky O. A new pheromone of the silkworm moth Bombyx mori: sensory pathway and behavioral effect. Naturwissenschaften 1978, 65:382-384.
57. Kanzaki R., Soo K., Seki Y., Wada S. Projections to higher olfactory centers from subdivisions of the antennal lobe macroglomerular complex of the male silkmoth. Chem Senses 2003, 28:113-130.
58. Kaplan F., Srinivasan J., Mahanti P., Ajredini R., Durak O., Nimalendran R., Sternberg P.W., Teal P.E.A., Schroeder F.C., Edison A.S., Alborn H.T. Ascaroside expression in Caenorhabditis elegans is strongly dependent on diet and developmental stage. Plos One 2011, 6.
59. Kaupp U.B. Olfactory signalling in vertebrates and insects: differences and commonalities. Nat Rev Neurosci 2010, 11:188-200.
60. Kim K., Sato K., Shibuya M., Zeiger D.M., Butcher R.A., Ragains J.R., Clardy J., Touhara K., Sengupta P. Two chemoreceptors mediate developmental effects of dauer pheromone in C. elegans. Science 2009, 326.
61. Kimoto H., Haga S., Sato K., Touhara K. Sex-specific peptides from exocrine glands stimulate mouse vomeronasal sensory neurons. Nature 2005, 437:898-901.
62. Kimoto H., Sato K., Nodari F., Haga S., Holy T.E., Touhara K. Sex- and strain-specific expression and vomeronasal activity of mouse ESP family peptides. Curr Biol 2007, 17:1879-1884.
63. Kobayakawa K., Kobayakawa R., Matsumoto H., Oka Y., Imai T., Ikawa M., Okabe M., Ikeda T., Itohara S., Kikusui T., Mori K., Sakano H. Innate versus learned odour processing in the mouse olfactory bulb. Nature 2007, 450:503-508.
64. Kurtovic A., Widmer A., Dickson B.J. A single class of olfactory neurons mediates behavioural responses to a Drosophila sex pheromone. Nature 2007, 446:542-546.
65. 2 reception in Drosophila. Proc Natl Acad Sci U S A 2007, 104:3574-3578.
66. Larsson M.C., Domingos A.I., Jones W.D., Chiappe M.E., Amrein H., Vosshall L.B. Or83b encodes a broadly expressed odorant receptor essential for Drosophila olfaction. Neuron 2004, 43:703-714.
67. Laughlin J.D., Ha T.S., Jones D.N., Smith D.P. Activation of pheromone-sensitive neurons is mediated by conformational activation of pheromone-binding protein. Cell 2008, 133:1255-1265.
68. Leinders-Zufall T., Brennan P., Widmayer P., Prashanth Chandramani S., Maul-Pavicic A., Jäger M., Li X.H., Breer H., Zufall F., Boehm T. MHC class I peptides as chemosensory signals in the vomeronasal organ. Science 2004, 306:1033-1037.
69. Leinders-Zufall T., Ishii T., Mombaerts P., Zufall F., Boehm T. Structural requirements for the activation of vomeronasal sensory neurons by MHC peptides. Nat Neurosci 2009, 12:1551-1558.
70. Leinders-Zufall T., Lane A.P., Puche A.C., Ma W., Novotny M.V., Shipley M.T., Zufall F. Ultrasensitive pheromone detection by mammalian vomeronasal neurons. Nature 2000, 405:792-796.
71. Li Q., Korzan W.J., Ferrero D.M., Chang R.B., Roy D.S., Buchi M., Lemon J.K., Kaur A.W., Stowers L., Fendt M., Liberles S.D. Synchronous evolution of an odor biosynthesis pathway and behavioral response. Curr Biol 2012, 23:11-20.
72. Liberles S.D., Buck L.B. A second class of chemosensory receptors in the olfactory epithelium. Nature 2006, 442:645-650.
73. Liberles S.D., Horowitz L.F., Kuang D., Contos J.J., Wilson K.L., Siltberg-Liberles J., Liberles D.A., Buck L.B. Formyl peptide receptors are candidate chemosensory receptors in the vomeronasal organ. Proc Natl Acad Sci U S A 2009, 106:9842-9847.
74. Lin D.Y., Zhang S.Z., Block E., Katz L.C. Encoding social signals in the mouse main olfactory bulb. Nature 2005, 434:470-477.
75. Liu W., Liang X., Gong J., Yang Z., Zhang Y.H., Zhang J.X., Rao Y. Social regulation of aggression by pheromonal activation of Or65a olfactory neurons in Drosophila. Nat Neurosci 2011, 14:896-902.
76. Logan D.W., Brunet L.J., Webb W.R., Cutforth T., Ngai J., Stowers L. Learned recognition of maternal signature odors mediates the first suckling episode in mice. Curr Biol 2012, 22:1998-2007.
77. Logan D.W., Marton T.F., Stowers L. Species specificity in major urinary proteins by parallel evolution. PLoS One 2008, 3:e3280.
78. Ludewig A.H., Schroeder F.C. Ascaroside signaling in C. elegans. WormBook 2013, 12:1-22.
79. Lundin C., Käll L., Kreher S.A., Kapp K., Sonnhammer E.L., Carlson J.R., Heijne G., Nilsson I. Membrane topology of the Drosophila OR83b odorant receptor. FEBS Lett 2007, 581:5601-5604.
80. Macosko E.Z., Pokala N., Feinberg E.H., Chalasani S.H., Butcher R.A., Clardy J., Bargmann C.I. A hub-and-spoke circuit drives pheromone attraction and social behaviour in C. elegans. Nature 2009, 458:1171-1175.
81. Matsumoto H., Kobayakawa K., Kobayakawa R., Tashiro T., Mori K., Sakano H., Mori K. Spatial arrangement of glomerular molecular-feature clusters in the odorant-receptor class domains of the mouse olfactory bulb. J Neurophysiol 2010, 103:3490-3500.
82. Matsumoto S., Hull J.J., Ohnishi A., Moto K., Fónagy A. Molecular mechanisms underlying sex pheromone production in the silkmoth, Bombyx mori: characterization of the molecular components involved in bombykol biosynthesis. J Insect Physiol 2007, 53:752-759.
83. McGrath P.T., Xu Y., Ailion M., Garrison J.L., Butcher R.A., Bargmann C.I. Parallel evolution of domesticated Caenorhabditis species targets pheromone receptor genes. Nature 2011, 477:321-325.
84. Mori K., Sakano H. How is the olfactory map formed and interpreted in the mammalian brain?. Annu Rev Neurosci 2011, 34:467-499.
85. Mucignat-Caretta C., Caretta A., Cavaggioni A. Acceleration of puberty onset in female mice by male urinary proteins. J Physiol 1995, 486(Pt 2):517-522.
86. Mudge J.M., Armstrong S.D., McLaren K., Beynon R.J., Hurst J.L., Nicholson C., Robertson D.H., Wilming L.G., Harrow J.L. Dynamic instability of the major urinary protein gene family revealed by genomic and phenotypic comparisons between C57 and 129 strain mice. Genome Biol 2008, 9:R91.
87. Munger S.D., Leinders-Zufall T., McDougall L.M., Cockerham R.E., Schmid A., Wandernoth P., Wennemuth G., Biel M., Zufall F., Kelliher K.R. An olfactory subsystem that detects carbon disulfide and mediates food-related social learning. Curr Biol 2010, 20:1438-1444.
88. Murakami T. Studies on the relationships between host-plant acceptability and plant constituents in host selection by a swallowtail butterfly, Papilio polytes. J Grad Sch Biosp Sci 2003, 42:58-59.
89. Nakagawa T., Pellegrino M., Sato K., Vosshall L.B., Touhara K. Amino acid residues contributing to function of the heteromeric insect olfactory receptor complex. PLoS One 2012, 7:e32372.
90. Nakagawa T., Sakurai T., Nishioka T., Touhara K. Insect sex-pheromone signals mediated by specific combinations of olfactory receptors. Science 2005, 307:1638-1642.
91. Nei M., Niimura Y., Nozawa M. The evolution of animal chemosensory receptor gene repertoires: roles of chance and necessity. Nat Rev Genet 2008, 9:951-963.
92. Neuhaus E.M., Gisselmann G., Zhang W., Dooley R., Störtkuhl K., Hatt H. Odorant receptor heterodimerization in the olfactory system of Drosophila melanogaster. Nat Neurosci 2005, 8:15-17.
93. Nodari F., Hsu F.F., Fu X., Holekamp T.F., Kao L.F., Turk J., Holy T.E. Sulfated steroids as natural ligands of mouse pheromone-sensing neurons. J Neurosci 2008, 28:6407-6418.
94. Novotny M., Harvey S., Jemiolo B. Chemistry of male dominance in the house mouse, Mus domesticus. Experientia 1990, 46:109-113.
95. Novotny M., Jemiolo B., Harvey S., Wiesler D., Marchlewska-Koj A. Adrenal-mediated endogenous metabolites inhibit puberty in female mice. Science 1986, 231:722-725.
96. Novotny M., Schwende F.J., Wiesler D., Jorgenson J.W., Carmack M. Identification of a testosterone-dependent unique volatile constituent of male mouse urine: 7-exo-ethyl-5-methyl-6,8-dioxabicyclo[3.2.1]-3-octene. Experientia 1984, 40:217-219.
97. Novotny M.V., Ma W., Wiesler D., Zidek L. Positive identification of the puberty-accelerating pheromone of the house mouse: the volatile ligands associating with the major urinary protein. Proc Biol Sci 1999, 266:2017-2022.
98. Ohsugi T., Nishida R., Fukami H. Multi-component system of oviposition stimulants for a Rutaceae-feeding swallowtail butterfly, Papilio xuthus (Lepidoptera: Papilionidae). Appl Entomol Zool 1991, 26:29-40.
99. Ozaki K., Ryuda M., Yamada A., Utoguchi A., Ishimoto H., Calas D., Marion-Poll F., Tanimura T., Yoshikawa H. A gustatory receptor involved in host plant recognition for oviposition of a swallowtail butterfly. Nat Commun 2011, 2:542.
100. Papes F., Logan D.W., Stowers L. The vomeronasal organ mediates interspecies defensive behaviors through detection of protein pheromone homologs. Cell 2010, 141:692-703.
101. Park D., O'Doherty I., Somvanshi R.K., Bethke A., Schroeder F.C., Kumar U., Riddle D.L. Interaction of structure-specific and promiscuous G-protein-coupled receptors mediates small-molecule signaling in Caenorhabditis elegans. Proc Natl Acad Sci U S A 2012, 109:9917-9922.
102. Pungaliya C., Srinivasan J., Fox B.W., Malik R.U., Ludewig A.H., Sternberg P.W., Schroeder F.C. A shortcut to identifying small molecule signals that regulate behavior and development in Caenorhabditis elegans. Proc Natl Acad Sci U S A 2009, 106:7708-7713.
103. Riviere S., Challet L., Fluegge D., Spehr M., Rodriguez I. Formyl peptide receptor-like proteins are a novel family of vomeronasal chemosensors. Nature 2009, 459:574-577.
104. Roberts S.A., Davidson A.J., McLean L., Beynon R.J., Hurst J.L. Pheromonal induction of spatial learning in mice. Science 2012, 338:1462-1465.
105. Roberts S.A., Simpson D.M., Armstrong S.D., Davidson A.J., Robertson D.H., McLean L., Beynon R.J., Hurst J.L. Darcin: a male pheromone that stimulates female memory and sexual attraction to an individual male's odour. BMC Biol 2010, 8:75.
106. Robertson H.M., Thomas J.H. The putative chemoreceptor families of C. elegans. WormBook 2006, 1-12.
107. Saito H, Chi Q, Zhuang H, Matsunami H, Mainland JD Odor coding by a mammalian receptor repertoire. Sci Signal 2009, 2:ra9.
108. Saito H., Kubota M., Roberts R.W., Chi Q., Matsunami H. RTP family members induce functional expression of mammalian odorant receptors. Cell 2004, 119:679-691.
109. Sakurai T., Nakagawa T., Mitsuno H., Mori H., Endo Y., Tanoue S., Yasukochi Y., Touhara K., Nishioka T. Identification and functional characterization of a sex pheromone receptor in the silkmoth Bombyx mori. Proc Natl Acad Sci U S A 2004, 101:16653-16658.
110. Sato K., Pellegrino M., Nakagawa T., Vosshall L.B., Touhara K. Insect olfactory receptors are heteromeric ligand-gated ion channels. Nature 2008, 452:1002-1006.
111. Schaal B., Coureaud G., Langlois D., Ginies C., Semon E., Perrier G. Chemical and behavioural characterization of the rabbit mammary pheromone. Nature 2003, 424:68-72.
112. Schlief M.L., Wilson R.I. Olfactory processing and behavior downstream from highly selective receptor neurons. Nat Neurosci 2007, 10:623-630.
113. Sherborne A.L., Thom M.D., Paterson S., Jury F., Ollier W.E., Stockley P., Beynon R.J., Hurst J.L. The genetic basis of inbreeding avoidance in house mice. Curr Biol 2007, 17:2061-2066.
114. Shirokova E., Raguse J.D., Meyerhof W., Krautwurst D. The human vomeronasal type-1 receptor family-detection of volatiles and cAMP signaling in HeLa/Olf cells. FASEB J 2008, 22:1416-1425.
115. Simon J.M., Sternberg P.W. Evidence of a mate-finding cue in the hermaphrodite nematode Caenorhabditis elegans. Proc Natl Acad Sci U S A 2002, 99:1598-1603.
116. Smart R., Kiely A., Beale M., Vargas E., Carraher C., Kralicek A.V., Christie D.L., Chen C., Newcomb R.D., Warr C.G. Drosophila odorant receptors are novel seven transmembrane domain proteins that can signal independently of heterotrimeric G proteins. Insect Biochem Mol Biol 2008, 38:770-780.
117. Spehr M., Kelliher K.R., Li X.H., Boehm T., Leinders-Zufall T., Zufall F. Essential role of the main olfactory system in social recognition of major histocompatibility complex peptide ligands. J Neurosci 2006, 26:1961-1970.
118. Srinivasan J., Kaplan F., Ajredini R., Zachariah C., Alborn H.T., Teal P.E., Malik R.U., Edison A.S., Sternberg P.W., Schroeder F.C. A blend of small molecules regulates both mating and development in Caenorhabditis elegans. Nature 2008, 454:1115-1118.
119. Srinivasan J., von Reuss S., Bose N., Zaslaver A., Mahanti P., Ho M.C., O'Doherty O.G., Edison A.S., Sternberg P.W., Schroeder F.C. A modular library of small molecule signals regulates social behaviors in Caenorhabditis elegans. Plos Biol 2012, 10.
120. St Angelo A.J. Lipid oxidation on foods. Crit Rev Food Sci Nutr 1996, 36:175-224.
121. Stensmyr M.C., Dweck H.K., Farhan A., Ibba I., Strutz A., Mukunda L., Linz J., Grabe V., Steck K., Lavista-Llanos S., Wicher D., Sachse S., Knaden M., Becher P.G., Seki Y., Hansson B.S. A conserved dedicated olfactory circuit for detecting harmful microbes in Drosophila. Cell 2012, 151:1345-1357.
122. Sturm T., Leinders-Zufall T., Macek B., Walzer M., Jung S., Pommerl B., Stevanovic S., Zufall F., Overath P., Rammensee H.G. Mouse urinary peptides provide a molecular basis for genotype discrimination by nasal sensory neurons. Nat Commun 2013, 4:1616.
123. Suh G.S., Ben-Tabou de Leon S., Tanimoto H., Fiala A., Benzer S., Anderson D.J. Light activation of an innate olfactory avoidance response in Drosophila. Curr Biol 2007, 17:905-908.
124. Suh G.S., Wong A.M., Hergarden A.C., Wang J.W., Simon A.F., Benzer S., Axel R., Anderson D.J. A single population of olfactory sensory neurons mediates an innate avoidance behaviour in Drosophila. Nature 2004, 431:854-859.
125. 2 neurons is activated by bicarbonate. Proc Natl Acad Sci U S A 2009, 106:2041-2046.
126. Szoka P.R., Paigen K. Regulation of mouse major urinary protein production by the Mup-A gene. Genetics 1978, 90:597-612.
127. Takahashi Y.K., Nagayama S., Mori K. Detection and masking of spoiled food smells by odor maps in the olfactory bulb. J Neurosci 2004, 24:8690-8694.
128. Tanaka K., Uda Y., Ono Y., Nakagawa T., Suwa M., Yamaoka R., Touhara K. Highly selective tuning of a silkworm olfactory receptor to a key mulberry leaf volatile. Curr Biol 2009, 19:881-890.
129. Tirindelli R., Dibattista M., Pifferi S., Menini A. From pheromones to behavior. Physiol Rev 2009, 89:921-956.
130. Touhara K., Vosshall L.B. Sensing odorants and pheromones with chemosensory receptors. Annu Rev Physiol 2009, 71:307-332.
131. 2 avoidance behaviour in Drosophila by inhibitory odorants. Nature 2009, 461:277-281.
132. van der Goes van Naters W., Carlson J.R. Receptors and neurons for fly odors in Drosophila. Curr Biol 2007, 17:606-612.
133. Vernet-Maury E (1980) Trimethyl-thiazoline in fox feces: A natural alarming substance for the rat. Olfaction Taste VII 407.
134. von Reuss S., Bose N., Srinivasan J., Yim J.J., Judkins J.C., Sternberg P.W., Schroeder F.C. Comparative metabolomics reveals biogenesis of ascarosides, a modular library of small-molecule signals in C. elegans. J Am Chem Soc 2012, 134:1817-1824.
135. Wang L., Anderson D.J. Identification of an aggression-promoting pheromone and its receptor neurons in Drosophila. Nature 2010, 463:227-231.
136. Wang Z., Balet Sindreu C., Li V., Nudelman A., Chan G.C., Storm D.R. Pheromone detection in male mice depends on signaling through the type 3 adenylyl cyclase in the main olfactory epithelium. J Neurosci 2006, 26:7375-7379.
137. White J.Q., Nicholas T.J., Gritton J., Truong L., Davidson E.R., Jorgensen E.M. The sensory circuitry for sexual attraction in C. elegans males. Curr Biol 2007, 17:1847-1857.
138. Wicher D., Schäfer R., Bauernfeind R., Stensmyr M.C., Heller R., Heinemann S.H., Hansson B.S. Drosophila odorant receptors are both ligand-gated and cyclic-nucleotide-activated cation channels. Nature 2008, 452:1007-1011.
139. Xu P., Atkinson R., Jones D.N., Smith D.P. Drosophila OBP LUSH is required for activity of pheromone-sensitive neurons. Neuron 2005, 45:193-200.
140. Yoshikawa K., Nakagawa H., Mori N., Watanabe H., Touhara K. An unsaturated aliphatic alcohol as a natural ligand for a mouse odorant receptor. Nat Chem Biol 2013, 9:160-162.
141. Yoshikawa K., Touhara K. Myr-Ric-8A enhances G(alpha15)-mediated Ca2+ response of vertebrate olfactory receptors. Chem Senses 2009, 34:15-23.
142. Young J.M., Waters H., Dong C., Fulle H.J., Liman E.R. Degeneration of the olfactory guanylyl cyclase D gene during primate evolution. PLoS One 2007, 2:e884.
143. Zhang J., Pacifico R., Cawley D., Feinstein P., Bozza T. Ultrasensitive detection of amines by a trace amine-associated receptor. J Neurosci 2013, 33:3228-3239.
144. Zwaal R.R., Mendel J.E., Sternberg P.W., Plasterk R.H. Two neuronal G proteins are involved in chemosensation of the Caenorhabditis elegans Dauer-inducing pheromone. Genetics 1997, 145:715-727.