Subsystem organization of the mammalian sense of smell

Annual Review of Physiology

Volumn 71, Issue , 2009, Pages 115-140

  Munger, Steven D ^a   Leinders Zufall, Trese ^b   Zufall, Frank ^b  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b SAARLAND UNIVERSITY   (Germany)

Author keywords

G protein coupled receptor; Odor; Pheromone; Vomeronasal

Indexed keywords

G PROTEIN COUPLED RECEPTOR; PHEROMONE; TRACE AMINE ASSOCIATED RECEPTOR; TRANSIENT RECEPTOR POTENTIAL CHANNEL; TRANSIENT RECEPTOR POTENTIAL CHANNEL 2; TRANSIENT RECEPTOR POTENTIAL CHANNEL 5; TRANSIENT RECEPTOR POTENTIAL CHANNEL 6; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; BEHAVIORAL SCIENCE; CHEMORECEPTOR; CHEMOSENSITIZATION; ELECTROPHYSIOLOGY; GENE TARGETING; MAMMAL; NERVE FIBER; NONHUMAN; NOSE CAVITY; OLFACTORY DISCRIMINATION; PRIORITY JOURNAL; REVIEW; SENSORY NERVE; SIGNAL TRANSDUCTION; SMELLING; STIMULUS RESPONSE; TRIGEMINAL NERVE;

ANIMALS; CHEMORECEPTOR CELLS; HUMANS; OLFACTORY PATHWAYS; OLFACTORY PERCEPTION; OLFACTORY RECEPTOR NEURONS; SENSORY RECEPTOR CELLS; SIGNAL TRANSDUCTION; SMELL;

EID: 65949121688     PISSN: 00664278     EISSN: 15451585     Source Type: Book Series    
DOI: 10.1146/annurev.physiol.70.113006.100608     Document Type: Review

References (168)

1. Breer H, Fleischer J, Strotmann J. 2006. The sense of smell: multiple olfactory subsystems. Cell. Mol. Life Sci. 63:1465-1475 (Pubitemid 44156743)
2. Ma M. 2007. Encoding olfactory signals via multiple chemosensory systems. Crit. Rev. Biochem. Mol. Biol. 42:463-480 (Pubitemid 350232896)
3. Tirindelli R, Mucignat-Caretta C, Ryba NJ. 1998. Molecular aspects of pheromonal communication via the vomeronasal organ of mammals. Trends Neurosci. 21:482-486 (Pubitemid 28506139)
4. Gold GH. 1999. Controversial issues in vertebrate olfactory transduction. Annu. Rev. Physiol. 61:857-871
5. Buck LB. 2000. The molecular architecture of odor and pheromone sensing in mammals. Cell 100:611-618
6. Firestein S. 2001. How the olfactory system makes sense of scents. Nature 413:211-218 (Pubitemid 32867886)
7. Zufall F, Munger SD. 2001. From odor and pheromone transduction to the organization of the sense of smell. Trends Neurosci. 24:191-193 (Pubitemid 32204365)
8. Mombaerts P. 2004. Genes and ligands for odorant, vomeronasal and taste receptors. Nat. Rev. Neurosci. 5:263-278 (Pubitemid 38478654)
9. Ache BW, Young JM. 2005. Olfaction: diverse species, conserved principles. Neuron 48:417-430
10. Brennan PA, Zufall F. 2006. Pheromonal communication in vertebrates. Nature 444:308-315
11. Dulac C, Wagner S. 2006. Genetic analysis of brain circuits underlying pheromone signaling. Annu. Rev. Genet. 40:449-467 (Pubitemid 44970425)
12. Zufall F, Leinders-Zufall T. 2007. Mammalian pheromone sensing. Curr. Opin. Neurobiol. 17:483-489
13. Fulle HJ, Vassar R, Foster DC, Yang RB, Axel R, Garbers DL. 1995.Areceptor guanylyl cyclase expressed specifically in olfactory sensory neurons. Proc. Natl. Acad. Sci. USA 92:3571-3575
14. Juilfs DM, Fulle HJ, Zhao AZ, Houslay MD, Garbers DL, Beavo JA. 1997. A subset of olfactory neurons that selectively express cGMP-stimulated phosphodiesterase (PDE2) and guanylyl cyclase-D define a unique olfactory signal transduction pathway. Proc. Natl. Acad. Sci. USA 94:3388-3395
15. Meyer MR, Angele A, Kremmer E, Kaupp UB, Muller F. 2000. A cGMP-signaling pathway in a subset of olfactory sensory neurons. Proc. Natl. Acad. Sci. USA 97:10595-10600 (Pubitemid 30707312)
16. Leinders-Zufall T, Cockerham RE, Michalakis S, Biel M, Garbers DL, et al. 2007. Contribution of the receptor guanylyl cyclase GC-D to chemosensory function in the olfactory epithelium. Proc. Natl. Acad. Sci. USA 104:14507-14512 (Pubitemid 350003291)
17. Buck L, Axel R. 1991. A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 65:175-187 (Pubitemid 121001224)
18. Glusman G, Yanai I, Rubin I, Lancet D. 2001. The complete human olfactory subgenome. Genome Res. 11:685-702
19. Zozulya S, Echeverri F, Nguyen T. 2001. The human olfactory receptor repertoire. Genome Biol. 2:RESEARCH0018
20. Young JM, Friedman C, Williams EM, Ross JA, Tonnes-Priddy L, Trask BJ. 2002. Different evolutionary processes shaped the mouse and human olfactory receptor gene families. Hum. Mol. Genet. 11:535-546 (Pubitemid 34257490)
21. Zhang X, Firestein S. 2002. The olfactory receptor gene superfamily of the mouse. Nat. Neurosci. 5:124-133 (Pubitemid 34121579)
22. Pace U, Hanski E, Salomon Y, Lancet D. 1985. Odorant-sensitive adenylate cyclase may mediate olfactory reception. Nature 316:255-258 (Pubitemid 15073690)
23. Pace U, Lancet D. 1986. Olfactory GTP-binding protein: signal-transducing polypeptide of vertebrate chemosensory neurons. Proc. Natl. Acad. Sci. USA 83:4947-4951 (Pubitemid 16075516)
24. Sklar PB, Anholt RR, Snyder SH. 1986. The odorant-sensitive adenylate cyclase of olfactory receptor cells. Differential stimulation by distinct classes of odorants. J. Biol. Chem. 261:15538-15543
25. Anholt RR, Mumby SM, Stoffers DA, Girard PR, Kuo JF, Snyder SH. 1987. Transduction proteins of olfactory receptor cells: identification of guanine nucleotide binding proteins and protein kinase C. Biochemistry 26:788-795 (Pubitemid 17021057)
26. Nakamura T, Gold GH. 1987. A cyclic nucleotide-gated conductance in olfactory receptor cilia. Nature 325:442-444 (Pubitemid 17056411)
27. Jones DT, Reed RR. 1989. Golf: an olfactory neuron specific-G protein involved in odorant signal transduction. Science 244:790-795
28. Bakalyar HA, Reed RR. 1990. Identification of a specialized adenylyl cyclase that may mediate odorant detection. Science 250:1403-1406
29. Dhallan RS, Yau KW, Schrader KA, Reed RR. 1990. Primary structure and functional expression of a cyclic nucleotide-activated channel from olfactory neurons. Nature 347:184-187 (Pubitemid 20315877)
30. Bradley J, Li J, Davidson N, Lester HA, Zinn K. 1994. Heteromeric olfactory cyclic nucleotide-gated channels: a subunit that confers increased sensitivity to cAMP. Proc. Natl. Acad. Sci. USA 91:8890-8894
31. Liman ER, Buck LB. 1994. A second subunit of the olfactory cyclic nucleotide-gated channel confers high sensitivity to cAMP. Neuron 13:611-621
32. Bonigk W, Bradley J, Muller F, Sesti F, Boekhoff I, et al. 1999. The native rat olfactory cyclic nucleotidegated channel is composed of three distinct subunits. J. Neurosci. 19:5332-5347 (Pubitemid 29300200)
33. Kleene SJ, Gesteland RC. 1991. Calcium-activated chloride conductance in frog olfactory cilia. J. Neurosci. 11:3624-3629
34. Kurahashi T, Yau KW. 1993. Co-existence of cationic and chloride components in odorant-induced current of vertebrate olfactory receptor cells. Nature 363:71-74 (Pubitemid 23144963)
35. Lowe G, Gold GH. 1993. Nonlinear amplification by calcium-dependent chloride channels in olfactory receptor cells. Nature 366:283-286 (Pubitemid 23359714)
36. Pifferi S, Pascarella G, Boccaccio A, Mazzatenta A, Gustincich S, et al. 2006. Bestrophin-2 is a candidate calcium-activated chloride channel involved in olfactory transduction. Proc. Natl. Acad. Sci. USA 103:12929-12934 (Pubitemid 44298663)
37. Von Dannecker LE, Mercadante AF, Malnic B. 2005. Ric-8B, an olfactory putativeGTPexchange factor, amplifies signal transduction through the olfactory-specific G-protein Gαolf. J. Neurosci. 25:3793-3800 (Pubitemid 40570412)
38. Kerr DS, Von Dannecker LE, Davalos M, Michaloski JS, Malnic B. 2008. Ric-8B interacts with Gaolf and Gg13 and colocalizes with Gaolf, Gb1 and G13 in the cilia of olfactory sensory neurons. Mol. Cell. Neurosci. 38:341-348
39. Yan C, Zhao AZ, Bentley JK, Loughney K, Ferguson K, Beavo JA. 1995. Molecular cloning and characterization of a calmodulin-dependent phosphodiesterase enriched in olfactory sensory neurons. Proc. Natl. Acad. Sci. USA 92:9677-9681
40. Cherry JA, Davis RL. 1995. A mouse homolog of dunce, a gene important for learning and memory in Drosophila, is preferentially expressed in olfactory receptor neurons. J. Neurobiol. 28:102-113
41. Keller A, Margolis FL. 1976. Isolation and characterization of rat olfactory marker protein. J. Biol. Chem. 251:6232-6237
42. Buiakova OI, Baker H, Scott JW, Farbman A, Kream R, et al. 1996. Olfactory marker protein (OMP) gene deletion causes altered physiological activity of olfactory sensory neurons. Proc. Natl. Acad. Sci. USA 93:9858-9863 (Pubitemid 26296699)
43. Krautwurst D, Yau KW, Reed RR. 1998. Identification of ligands for olfactory receptors by functional expression of a receptor library. Cell 95:917-926 (Pubitemid 29019044)
44. Zhao H, Ivic L, Otaki JM, Hashimoto M, Mikoshiba K, Firestein S. 1998. Functional expression of a mammalian odorant receptor. Science 279:237-242 (Pubitemid 28103883)
45. Malnic B, Hirono J, Sato T, Buck LB. 1999. Combinatorial receptor codes for odors. Cell 96:713-723
46. Wachowiak M, Shipley MT. 2006. Coding and synaptic processing of sensory information in the glomerular layer of the olfactory bulb. Semin. Cell Dev. Biol. 17:411-423 (Pubitemid 44301929)
47. Kajiya K, Inaki K, Tanaka M, Haga T, Kataoka H, Touhara K. 2001. Molecular bases of odor discrimination: reconstitution of olfactory receptors that recognize overlapping sets of odorants. J. Neurosci. 21:6018-6025 (Pubitemid 32737735)
48. Abaffy T, Matsunami H, Luetje CW. 2006. Functional analysis of a mammalian odorant receptor subfamily. J. Neurochem. 97:1506-1518 (Pubitemid 43725588)
49. Spehr M, Gisselmann G, Poplawski A, Riffell JA, Wetzel CH, et al. 2003. Identification of a testicular odorant receptor mediating human sperm chemotaxis. Science 299:2054-2058 (Pubitemid 36383730)
50. Shirokova E, Schmiedeberg K, Bedner P, Niessen H, Willecke K, et al. 2005. Identification of specific ligands for orphan olfactory receptors. G protein-dependent agonism and antagonism of odorants. J. Biol. Chem. 280:11807-11815 (Pubitemid 40418495)
51. Spehr M, Schwane K, Heilmann S, Gisselmann G, Hummel T, Hatt H. 2004. Dual capacity of a human olfactory receptor. Curr. Biol. 14: R832-83 (Pubitemid 39301149)
52. Oka Y, Nakamura A, Watanabe H, Touhara K. 2004. An odorant derivative as an antagonist for an olfactory receptor. Chem. Senses 29:815-822 (Pubitemid 41289281)
53. Wysocki CJ, Beauchamp GK. 1984. Ability to smell androstenone is genetically determined. Proc. Natl. Acad. Sci. USA 81:4899-4902
54. Keller A, Zhuang H, Chi Q, Vosshall LB, Matsunami H. 2007. Genetic variation in a human odorant receptor alters odour perception. Nature 449:468-472 (Pubitemid 47509549)
55. Menashe I, ManO, Lancet D, Gilad Y. 2003. Different noses for different people. Nat. Genet. 34:143-144
56. Menashe I, Abaffy T, Hasin Y, Goshen S, Yahalom V, et al. 2007. Genetic elucidation of human hyperosmia to isovaleric acid. PLoS Biol. 5:e284 (Pubitemid 350276922)
57. Bozza T, Feinstein P, Zheng C, Mombaerts P. 2002. Odorant receptor expression defines functional units in the mouse olfactory system. J. Neurosci. 22:3033-3043 (Pubitemid 35379192)
58. Katada S, Hirokawa T, Oka Y, Suwa M, Touhara K. 2005. Structural basis for a broad but selective ligand spectrum of a mouse olfactory receptor: mapping the odorant-binding site. J. Neurosci. 25:1806-1815 (Pubitemid 40279286)
59. Lagerstrom MC, Schioth HB. 2008. Structural diversity ofGprotein-coupled receptors and significance for drug discovery. Nat. Rev. Drug Discov. 7:339-357
60. Saito H, Kubota M, Roberts RW, Chi Q, Matsunami H. 2004. RTP family members induce functional expression of mammalian odorant receptors. Cell 119:679-691 (Pubitemid 39535755)
61. Belluscio L, Gold GH, Nemes A, Axel R. 1998. Mice deficient in Golf are anosmic. Neuron 20:69-81 (Pubitemid 28078350)
62. Jones DT, Reed RR. 1987. Molecular cloning of five GTP-binding protein cDNA species from rat olfactory neuroepithelium. J. Biol. Chem. 262:14241-14249
63. Wong ST, Trinh K, Hacker B, Chan GC, Lowe G, et al. 2000. Disruption of the type III adenylyl cyclase gene leads to peripheral and behavioral anosmia in transgenic mice. Neuron 27:487-497 (Pubitemid 30951851)
64. Kaupp UB, Seifert R. 2002. Cyclic nucleotide-gated ion channels. Physiol. Rev. 82:769-824
65. Brunet LJ, Gold GH, Ngai J. 1996. General anosmia caused by a targeted disruption of the mouse olfactory cyclic nucleotide-gated cation channel. Neuron 17:681-693 (Pubitemid 26365347)
66. Lin W, Arellano J, Slotnick B, Restrepo D. 2004. Odors detected by mice deficient in cyclic nucleotide-gated channel subunit A2 stimulate the main olfactory system. J. Neurosci. 24:3703-3710 (Pubitemid 38481128)
67. 2+-calmodulin- dependent odor adaptation. Science 294:2172-2175
68. Michalakis S, Reisert J, Geiger H, Wetzel C, Zong X, et al. 2006. Loss of CNGB1 protein leads to olfactory dysfunction and subciliary cyclic nucleotide-gated channel trapping. J. Biol. Chem. 281:35156-35166 (Pubitemid 46036555)
69. Kelliher KR, Ziesmann J, Munger SD, Reed RR, Zufall F. 2003. Importance of the CNGA4 channel gene for odor discrimination and adaptation in behaving mice. Proc. Natl. Acad. Sci. USA 100:4299-4304 (Pubitemid 36418197)
70. Kurahashi T, Menini A. 1997. Mechanism of odorant adaptation in the olfactory receptor cell. Nature 385:725-729 (Pubitemid 27098093)
71. 2+/CaM via the B1b subunit affects response termination but not sensitivity to recurring stimulation. Neuron 58:374-386
72. Spehr M, Kelliher KR, Li XH, Boehm T, Leinders-Zufall T, Zufall F. 2006. Essential role of the main olfactory system in social recognition of major histocompatibility complex peptide ligands. J. Neurosci. 26:1961-1970 (Pubitemid 43295848)
73. Borowsky B, Adham N, Jones KA, Raddatz R, Artymyshyn R, et al. 2001. Trace amines: identification of a family of mammalian G protein-coupled receptors. Proc. Natl. Acad. Sci. USA 98:8966-8971 (Pubitemid 32743853)
74. Liberles SD, Buck LB. 2006. A second class of chemosensory receptors in the olfactory epithelium. Nature 442:645-650
75. Gloriam DE, Bjarnadottir TK, Yan YL, Postlethwait JH, Schioth HB, Fredriksson R. 2005. The repertoire of trace amine G-protein-coupled receptors: large expansion in zebrafish. Mol. Phylogenet. Evol. 35:470-482 (Pubitemid 40413411)
76. Mueller JC, Steiger S, Fidler AE, Kempenaers B. 2008. Biogenic trace amine-associated receptors (TAARS) are encoded in avian genomes: evidence and possible implications. J. Hered. 99:174-176
77. Gibson AD, Garbers DL. 2000. Guanylyl cyclases as a family of putative odorant receptors. Annu. Rev. Neurosci. 23:417-439
78. Walz A, Feinstein P, Khan M, Mombaerts P. 2007. Axonal wiring of guanylate cyclase-D-expressing olfactory neurons is dependent on neuropilin 2 and semaphorin 3F. Development 134:4063-4072 (Pubitemid 350269423)
79. MaM, Grosmaitre X, Iwema CL, Baker H, Greer CA, ShepherdGM.2003. Olfactory signal transduction in the mouse septal organ. J. Neurosci. 23:317-324
80. Shinoda K, Shiotani Y, Osawa Y. 1989. "Necklace olfactory glomeruli" form unique components of the rat primary olfactory system. J. Comp. Neurol. 284:362-373 (Pubitemid 19173265)
81. Hu J, Zhong C, Ding C, Chi Q, Walz A, et al. 2007. Detection of near-atmospheric concentrations of CO2 by an olfactory subsystem in the mouse. Science 317:953-957 (Pubitemid 47301324)
82. Forte LR Jr. 2004. Uroguanylin and guanylin peptides: pharmacology and experimental therapeutics. Pharmacol. Ther. 104:137-162 (Pubitemid 39424257)
83. Baker H, Cummings DM, Munger SD, Margolis JW, Franzen L, et al. 1999. Targeted deletion of a cyclic nucleotide-gated channel subunit (OCNC1): biochemical and morphological consequences in adult mice. J. Neurosci. 19:9313-9321 (Pubitemid 30228085)
84. Young JM, Waters H, Dong C, Fulle HJ, Liman ER. 2007. Degeneration of the olfactory guanylyl cyclase D gene during primate evolution. PLoS ONE 2:e884
85. Fain GL. 2003. Sensory Transduction. Sunderland, MA: Sinauer Assoc.
86. Duda T, Sharma RK. 2008.ONE-GCmembrane guanylate cyclase, a trimodal odorant signal transducer. Biochem. Biophys. Res. Commun. 367:440-445
87. Venkatachalam K, Montell C. 2007. TRP channels. Annu. Rev. Biochem. 76:387-417
88. Liman ER, Corey DP, Dulac C. 1999. TRP2: a candidate transduction channel for mammalian pheromone sensory signaling. Proc. Natl. Acad. Sci. USA 96:5791-5796 (Pubitemid 29234697)
89. Elsaesser R, Montani G, Tirindelli R, Paysan J. 2005. Phosphatidyl-inositide signaling proteins in a novel class of sensory cells in the mammalian olfactory epithelium. Eur. J. Neurosci. 21:2692-2700 (Pubitemid 40835112)
90. Hansel DE, Eipper BA, Ronnett GV. 2001. Neuropeptide Y functions as a neuroproliferative factor. Nature 410:940-944
91. Montani G, Tonelli S, Elsaesser R, Paysan J, Tirindelli R. 2006. Neuropeptide Y in the olfactory microvillar cells. Eur. J. Neurosci. 24:20-24
92. Lin W, Ogura T, Margolskee RF, Finger TE, Restrepo D. 2008. TRPM5-expressing solitary chemosensory cells respond to odorous irritants. J. Neurophysiol. 99:1451-1460
93. Lin W, Margolskee R, Donnert G, Hell SW, Restrepo D. 2007. Olfactory neurons expressing transient receptor potential channel M5 (TRPM5) are involved in sensing semiochemicals. Proc. Natl. Acad. Sci. USA 104:2471-2476 (Pubitemid 46391420)
94. Boekhoff I, Tareilus E, Strotmann J, Breer H. 1990. Rapid activation of alternative second messenger pathways in olfactory cilia from rats by different odorants. EMBO J. 9:2453-2458 (Pubitemid 20218341)
95. Dulac C, Torello AT. 2003. Molecular detection of pheromone signals in mammals: from genes to behavior. Nat. Rev. Neurosci. 4:551-562 (Pubitemid 37271366)
96. Halpern M, Martinez-Marcos A. 2003. Structure and function of the vomeronasal system: an update. Prog. Neurobiol. 70:245-318 (Pubitemid 37287601)
97. Bigiani A, Mucignat-Caretta C, Montani G, Tirindelli R. 2005. Pheromone reception in mammals. Rev. Physiol. Biochem. Pharmacol. 154:1-35
98. Zufall F, Leinders-Zufall T, Puche A. 2008. Accessory olfactory system. In The Senses: A Comprehensive Reference, ed. AI Basbaum, A Kaneko,GMShepherd, GWestheimer, pp. 783-814. San Diego: Academic
99. Luo M, Katz LC. 2004. Encoding pheromonal signals in the mammalian vomeronasal system. Curr. Opin. Neurobiol. 14:428-434 (Pubitemid 39078489)
100. Broad KD, Keverne EB. 2008. More to pheromones than meets the nose. Nat. Neurosci. 11:128-129 (Pubitemid 351170489)
101. Berghard A, Buck LB, Liman ER. 1996. Evidence for distinct signaling mechanisms in two mammalian olfactory sense organs. Proc. Natl. Acad. Sci. USA 93:2365-2369 (Pubitemid 26104356)
102. Jia C, Halpern M. 1996. Subclasses of vomeronasal receptor neurons: differential expression ofGproteins (Giα2 and Goα) and segregated projections to the accessory olfactory bulb. Brain Res. 719:117-128 (Pubitemid 126334262)
103. Mohedano-Moriano A, Pro-Sistiaga P, Ubeda-Banon I, Crespo C, Insausti R, Martinez-Marcos A. 2007. Segregated pathways to the vomeronasal amygdala: differential projections from the anterior and posterior divisions of the accessory olfactory bulb. Eur. J. Neurosci. 25:2065-2080 (Pubitemid 46581744)
104. Dulac C, Axel R. 1995. A novel family of genes encoding putative pheromone receptors in mammals. Cell 83:195-206
105. Zhang X, Firestein S. 2007. Comparative genomics of odorant and pheromone receptor genes in rodents. Genomics 89:441-450 (Pubitemid 46413675)
106. Rodriguez I, Mombaerts P. 2002. Novel human vomeronasal receptor-like genes reveal species-specific families. Curr. Biol. 12:R409-11 (Pubitemid 34703315)
107. Rodriguez I, Feinstein P, Mombaerts P. 1999. Variable patterns of axonal projections of sensory neurons in the mouse vomeronasal system. Cell 97:199-208 (Pubitemid 29194271)
108. Grus WE, Shi P, Zhang J. 2007. Largest vertebrate vomeronasal type 1 receptor gene repertoire in the semiaquatic platypus. Mol. Biol. Evol. 24:2153-2157 (Pubitemid 47574727)
109. Belluscio L, Koentges G, Axel R, Dulac C. 1999. A map of pheromone receptor activation in the mammalian brain. Cell 97:209-220 (Pubitemid 29194272)
110. Wagner S, Gresser AL, Torello AT, Dulac C. 2006. A multireceptor genetic approach uncovers an ordered integration of VNO sensory inputs in the accessory olfactory bulb. Neuron 50:697-709 (Pubitemid 43775740)
111. Leinders-Zufall T, Lane AP, Puche AC, Ma W, Novotny MV, et al. 2000. Ultrasensitive pheromone detection by mammalian vomeronasal neurons. Nature 405:792-796 (Pubitemid 30407851)
112. Leinders-Zufall T, Brennan P, Widmayer P, Chandramani SP, Maul-Pavicic A, et al. 2004. MHC class I peptides as chemosensory signals in the vomeronasal organ. Science 306:1033-1037 (Pubitemid 39482906)
113. Del Punta K, Leinders-Zufall T, Rodriguez I, Jukam D, Wysocki CJ, et al. 2002. Deficient pheromone responses in mice lacking a cluster of vomeronasal receptor genes. Nature 419:70-74 (Pubitemid 34987871)
114. Boschat C, Pelofi C, Randin O, Roppolo D, Luscher C, et al. 2002. Pheromone detection mediated by a V1r vomeronasal receptor. Nat. Neurosci. 5:1261-1262 (Pubitemid 35422711)
115. He J, Ma L, Kim S, Nakai J, Yu CR. 2008. Encoding gender and individual information in the mouse vomeronasal organ. Science 320:535-538 (Pubitemid 351590667)
116. Holekamp TF, Turaga D, Holy TE. 2008. Fast three-dimensional fluorescence imaging of activity in neural populations by objective-coupled planar illumination microscopy. Neuron 57:661-672 (Pubitemid 351337670)
117. Chamero P, Marton TF, Logan DW, Flanagan K, Cruz JR, et al. 2007. Identification of protein pheromones that promote aggressive behavior. Nature 450:899-902 (Pubitemid 350231315)
118. Ukhanov K, Leinders-Zufall T, Zufall F. 2007. Patch-clamp analysis of gene-targeted vomeronasal neurons expressing a defined V1r or V2r receptor: ionic mechanisms underlying persistent firing. J. Neurophysiol. 98:2357-2369 (Pubitemid 47584418)
119. Zufall F, Ukhanov K, Lucas P, Liman ER, Leinders-Zufall T. 2005. Neurobiology of TRPC2: from gene to behavior. Pfl̈ug. Arch. 451:61-71
120. Lucas P, Ukhanov K, Leinders-Zufall T, Zufall F. 2003. A diacylglycerol-gated cation channel in vomeronasal neuron dendrites is impaired in TRPC2 mutant mice: mechanism of pheromone transduction. Neuron 40:551-561 (Pubitemid 37494704)
121. Leypold BG, Yu CR, Leinders-Zufall T, Kim MM, Zufall F, Axel R. 2002. Altered sexual and social behaviors in trp2 mutant mice. Proc. Natl. Acad. Sci. USA 99:6376-6381 (Pubitemid 34493319)
122. 2+ signaling. Cell Calcium 40:261-275
123. Holy TE, Dulac C, Meister M. 2000. Responses of vomeronasal neurons to natural stimuli. Science 289:1569-1572 (Pubitemid 30677479)
124. Yang H, Shi P, Zhang YP, Zhang J. 2005. Composition and evolution of the V2r vomeronasal receptor gene repertoire in mice and rats. Genomics 86:306-315 (Pubitemid 41096700)
125. Young JM, Trask BJ. 2007. V2R gene families degenerated in primates, dog and cow, but expanded in opossum. Trends Genet. 23:212-215
126. Silvotti L, Moiani A, Gatti R, Tirindelli R. 2007. Combinatorial coexpression of pheromone receptors, V2Rs. J. Neurochem. 103:1753-1763 (Pubitemid 350126612)
127. Ishii T, Hirota J, Mombaerts P. 2003. Combinatorial coexpression of neural and immune multigene families in mouse vomeronasal sensory neurons. Curr. Biol. 13:394-400 (Pubitemid 36280456)
128. Loconto J, Papes F, Chang E, Stowers L, Jones EP, et al. 2003. Functional expression of murine V2R pheromone receptors involves selective association with the M10 and M1 families of MHC class Ib molecules. Cell 112:607-618 (Pubitemid 36331774)
129. Olson R, Huey-Tubman KE, Dulac C, Bjorkman PJ. 2005. Structure of a pheromone receptor-associated MHC molecule with an open and empty groove. PLoS Biol. 3:e257 (Pubitemid 41213263)
130. Olson R, Dulac C, Bjorkman PJ. 2006. MHC homologs in the nervous system-They haven't lost their groove. Curr. Opin. Neurobiol. 16:351-357 (Pubitemid 43913456)
131. Ishii T, Mombaerts P. 2008. Expression of nonclassical class I major histocompatibility genes defines a tripartite organization of the mouse vomeronasal system. J. Neurosci. 28:2332-2341 (Pubitemid 351348179)
132. Kimoto H, Haga S, Sato K, Touhara K. 2005. Sex-specific peptides from exocrine glands stimulate mouse vomeronasal sensory neurons. Nature 437:898-901 (Pubitemid 41486766)
133. Boehm T, Zufall F. 2006. MHC peptides and the sensory evaluation of genotype. Trends Neurosci. 29:100-107 (Pubitemid 43202599)
134. Villinger J, Waldman B. 2008. Self-referent MHC type matching in frog tadpoles. Proc. Biol. Sci. 275:1225-1230
135. Kimoto H, Sato K, Nodari F, Haga S, Holy TE, Touhara K. 2007. Sex- and strain-specific expression and vomeronasal activity of mouse ESP family peptides. Curr. Biol. 17:1879-1884 (Pubitemid 350016920)
136. Touhara K. 2007. Molecular biology of peptide pheromone production and reception in mice. Adv. Genet. 59:147-171
137. Cheetham SA, Thom MD, Jury F, Ollier WE, Beynon RJ, Hurst JL. 2007. The genetic basis of individualrecognition signals in the mouse. Curr. Biol. 17:1771-1777 (Pubitemid 47576673)
138. More L. 2006. Mouse major urinary proteins trigger ovulation via the vomeronasal organ. Chem. Senses 31:393-401 (Pubitemid 43978550)
139. Stowers L, Holy TE, Meister M, Dulac C, Koentges G. 2002. Loss of sex discrimination and male-male aggression in mice deficient for TRP2. Science 295:1493-1500 (Pubitemid 34173998)
140. Kimchi T, Xu J, Dulac C. 2007. A functional circuit underlying male sexual behavior in the female mouse brain. Nature 448:1009-1014 (Pubitemid 47345587)
141. Kelliher KR, Spehr M, Li XH, Zufall F, Leinders-Zufall T. 2006. Pheromonal recognition memory induced by TRPC2-independent vomeronasal sensing. Eur. J. Neurosci. 23:3385-3390 (Pubitemid 43911717)
142. Levai O, Feistel T, Breer H, Strotmann J. 2006. Cells in the vomeronasal organ express odorant receptors but project to the accessory olfactory bulb. J. Comp. Neurol. 498:476-490 (Pubitemid 44232689)
143. M̈uller W. 1971. Vergleichende elektrophysiologische Untersuchungen an den Sinnesepithelien des Jacobsonschen Organs und der Nase von Amphibien (Rana), Reptilien (Lacerta) und S̈augetieren (Mus). Z. Vergl. Physiol. 72:370-385
144. Tucker D. 1971. Nonolfactory responses from the nasal cavity: Jacobson's organ and the trigeminal system. In Handbook of Sensory Physiology, ed. H Autrum, R Jung, WR Loewenstein, DM MacKay, HL Teuber, pp. 152-181 Berlin/Heidelberg/New York: Springer-Verlag
145. Sam M, Vora S, Malnic B, Ma W, Novotny MV, Buck LB. 2001. Odorants may arouse instinctive behaviors. Nature 412:142 (Pubitemid 32674701)
146. Trinh K, Storm DR. 2003. Vomeronasal organ detects odorants in absence of signaling through main olfactory epithelium. Nat. Neurosci. 6:519-525 (Pubitemid 36514700)
147. Xu F, Schaefer M, Kida I, Schafer J, Liu N, et al. 2005. Simultaneous activation of mouse main and accessory olfactory bulbs by odors or pheromones. J. Comp. Neurol. 489:491-500 (Pubitemid 41076962)
148. Weiler E, Farbman AI. 2003. The septal organ of the rat during postnatal development. Chem. Senses 28:581-593 (Pubitemid 39144850)
149. Kaluza JF, Gussing F, Bohm S, Breer H, Strotmann J. 2004. Olfactory receptors in the mouse septal organ. J. Neurosci. Res. 76:442-452 (Pubitemid 38580460)
150. Tian H, Ma M. 2004. Molecular organization of the olfactory septal organ. J. Neurosci. 24:8383-8390 (Pubitemid 39280817)
151. Levai O, Strotmann J. 2003. Projection pattern of nerve fibers from the septal organ: DiI-tracing studies with transgenic OMP mice. Histochem. Cell Biol. 120:483-492 (Pubitemid 38058203)
152. Marshall DA, Maruniak JA. 1986. Masera's organ responds to odorants. Brain Res. 366:329-332
153. Grosmaitre X, Santarelli LC, Tan J, Luo M, Ma M. 2007. Dual functions of mammalian olfactory sensory neurons as odor detectors and mechanical sensors. Nat. Neurosci. 10:348-354 (Pubitemid 46310475)
154. Gr̈uneberg H. 1973. A ganglion probably belonging to the N. terminalis system in the nasal mucosa of the mouse. Z Anat. Entwickl. 140:39-52
155. Fuss SH, Omura M, Mombaerts P. 2005. The Grueneberg ganglion of the mouse projects axons to glomeruli in the olfactory bulb. Eur. J. Neurosci. 22:2649-2654 (Pubitemid 41759007)
156. Koos DS, Fraser SE. 2005. The Grueneberg ganglion projects to the olfactory bulb. Neuroreport 16:1929-1932
157. Fleischer J, Hass N, Schwarzenbacher K, Besser S, Breer H. 2006. A novel population of neuronal cells expressing the olfactory marker protein (OMP) in the anterior/dorsal region of the nasal cavity. Histochem. Cell Biol. 125:337-349 (Pubitemid 43376199)
158. Roppolo D, Ribaud V, Jungo VP, Luscher C, Rodriguez I. 2006. Projection of the Gruneberg ganglion to the mouse olfactory bulb. Eur. J. Neurosci. 23:2887-2894 (Pubitemid 43882867)
159. Storan MJ, Key B. 2006. Septal organ of Gr̈uneberg is part of the olfactory system. J. Comp. Neurol. 494:834-844 (Pubitemid 43054229)
160. Fleischer J, Schwarzenbacher K, Besser S, Hass N, Breer H. 2006. Olfactory receptors and signaling elements in the Grueneberg ganglion. J. Neurochem. 98:543-554 (Pubitemid 44133157)
161. Fleischer J, Schwarzenbacher K, Breer H. 2007. Expression of trace amine-associated receptors in the Grueneberg ganglion. Chem. Senses 32:623-631 (Pubitemid 47261079)
162. Bryant BP. 2000. Chemesthesis: the common chemical sense. In The Neurobiology of Taste and Smell, ed. TE Finger,WL Silver, D Restrepo, pp. 73-100. New York: Wiley
163. Finger TE, Bottger B, Hansen A, Anderson KT, Alimohammadi H, Silver WL. 2003. Solitary chemoreceptor cells in the nasal cavity serve as sentinels of respiration. Proc. Natl. Acad. Sci. USA 100:8981-8986 (Pubitemid 36899209)
164. Kaske S, Krasteva G, Konig P, Kummer W, Hofmann T, et al. 2007. TRPM5, a taste-signaling transient receptor potential ion-channel, is a ubiquitous signaling component in chemosensory cells. BMC Neurosci. 8:49 (Pubitemid 47163145)
165. Kobayakawa K, Kobayakawa R, Matsumoto H, Oka Y, Imai T, et al. 2007. Innate versus learned odour processing in the mouse olfactory bulb. Nature 450:503-508 (Pubitemid 350190245)
166. Mousley A, Polese G, Marks NJ, Eisthen HL. 2006. Terminal nerve-derived neuropeptide Y modulates physiological responses in the olfactory epithelium of hungry axolotls (Ambystoma mexicanum). J. Neurosci. 26:7707-7717 (Pubitemid 44315190)
167. Von Bartheld CS. 2004. The terminal nerve and its relation with extrabulbar "olfactory" projections: lessons from lampreys and lungfishes. Microsc. Res. Tech. 65:13-24
168. Mombaerts P, Wang F, Dulac C, Chao SK, Nemes A, et al. 1996. Visualizing an olfactory sensory map. Cell 87:675-686