Unravelling the olfactory sense: From the Gene to Odor Perception

Chemical Senses

Volumn 41, Issue 2, 2016, Pages 105-121

  Silva Teixeira, Carla S ^a   Cerqueira, Nuno M F S A ^b   Silva Ferreira, António C ^a,c  

^a UNIVERSIDADE CATÓLICA PORTUGUESA   (Portugal)

^b UNIVERSITY OF PORTO   (Portugal)

^c STELLENBOSCH UNIVERSITY   (South Africa)

Author keywords

Aroma perception; Olfactory epithelium; Olfactory GPCRs; Olfactory sense

Indexed keywords

BINDING PROTEIN; CYCLIC AMP; G PROTEIN COUPLED RECEPTOR; ODORANT BINDING PROTEIN; UNCLASSIFIED DRUG; FRAGRANCE; OLFACTORY RECEPTOR;

AMINO ACID SEQUENCE; BRAIN FUNCTION; GENE EXPRESSION; GENE SEQUENCE; GENETIC ASSOCIATION; GENETIC VARIABILITY; HUMAN; MORPHOLOGY; NERVE FIBER; NONHUMAN; ODOR; OLFACTORY BULB; OLFACTORY EPITHELIUM; OLFACTORY RECEPTOR; OLFACTORY SYSTEM; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN STRUCTURE; REVIEW; SENSORY NERVE CELL; SIGNAL TRANSDUCTION; SMELLING; GENETICS; METABOLISM; PHYSIOLOGY;

HUMANS; ODORANTS; OLFACTORY BULB; OLFACTORY PERCEPTION; RECEPTORS, ODORANT; SIGNAL TRANSDUCTION;

EID: 84960101628     PISSN: 0379864X     EISSN: 14643553     Source Type: Journal    
DOI: 10.1093/chemse/bjv075     Document Type: Review

References (179)

1. Abaffy T, Defazio AR. 2011. The location of olfactory receptors within olfactory epithelium is independent of odorant volatility and solubility. BMC Res Notes. 4:137.
2. Adipietro KA, Mainland JD, Matsunami H. 2012. Functional evolution of mammalian odorant receptors. PLoS Genet. 8(7):e1002821.
3. Amoore JE. 1963. Stereochemical theory of olfaction. Nature. 199:912-913.
4. Amoore JE, Venstrom D, Davis AR. 1968. Measurement of specific anosmia. Percept Mot Skills. 26(1):143-164.
5. Apter AJ, Gent JF, Frank ME. 1999. Fluctuating olfactory sensitivity and distorted odor perception in allergic rhinitis. Arch Otolaryngol Head Neck Surg. 125(9):1005-1010.
6. Audouze K, Tromelin A, Le Bon AM, Belloir C, Petersen RK, Kristiansen K, Brunak S, Taboureau O. 2014. Identification of odorant-receptor interactions by global mapping of the human odorome. PLoS One. 9(4):e93037.
7. Aznar M, López R, Cacho JF, Ferreira V. 2001. Identification and quantification of impact odorants of aged red wines from Rioja. GC-olfactometry, quantitative GC-MS, and odor evaluation of HPLC fractions. J Agric Food Chem. 49(6):2924-2929.
8. Bakalyar HA, Reed RR. 1990. Identification of a specialized adenylyl cyclase that may mediate odorant detection. Science. 250(4986):1403-1406.
9. Barratt E, Bingham RJ, Warner DJ, Laughton CA, Phillips SE, Homans SW. 2005. Van der Waals interactions dominate ligand-protein association in a protein binding site occluded from solvent water. J Am Chem Soc. 127(33):11827-11834.
10. Beets MGJ. 1957. Strusscture and odour. In: Industry SoC, editor. Molecular structure and organoleptic quality. London. p. 54-90.
11. Block E, Jang S, Matsunami H, Sekharan S, Dethier B, Ertem MZ, Gundala S, Pan Y, Li S, Li Z, et al. 2015. Implausibility of the vibrational theory of olfaction. Proc Natl Acad Sci U S A. 112(21):E2766-E2774.
12. Boyle JA, Djordjevic J, Olsson MJ, Lundström JN, Jones-Gotman M. 2009. The human brain distinguishes between single odorants and binary mixtures. Cereb Cortex. 19(1):66-71.
13. Braun T, Voland P, Kunz L, Prinz C, Gratzl M. 2007. Enterochromaffin cells of the human gut: sensors for spices and odorants. Gastroenterology. 132(5):1890-1901.
14. Bremner EA, Mainland JD, Khan RM, Sobel N. 2003. The prevalence of androstenone anosmia. Chem Senses. 28(5):423-432.
15. Brenker C, Goodwin N, Weyand I, Kashikar ND, Naruse M, Krähling M, Müller A, Kaupp UB, Strünker T. 2012. The CatSper channel: a polymodal chemosensor in human sperm. EMBO J. 31(7):1654-1665.
16. Briand L, Eloit C, Nespoulous C, Bézirard V, Huet JC, Henry C, Blon F, Trotier D, Pernollet JC. 2002. Evidence of an odorant-binding protein in the human olfactory mucus: location, structural characterization, and odorant-binding properties. Biochemistry. 41(23):7241-7252.
17. Brown KS, Maclean CM, Robinette RR. 1968. The distribution of the sensitivity to chemical odors in man. Hum Biol. 40(4):456-472.
18. Brunert D, Kurtenbach S, Isik S, Benecke H, Gisselmann G, Schuhmann W, Hatt H, Wetzel CH. 2009. Odorant-dependent generation of nitric oxide in Mammalian olfactory sensory neurons. PLoS One. 4(5):e5499.
19. Buck L, Axel R. 1991. A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell. 65(1):175-187.
20. Buettner JA, Glusman G, Ben-Arie N, Ramos P, Lancet D, Evans GA. 1998. Organization and evolution of olfactory receptor genes on human chromosome 11. Genomics. 53(1):56-68.
21. Burd GD. 1993. Morphological study of the effects of intranasal zinc sulfate irrigation on the mouse olfactory epithelium and olfactory bulb. Microsc Res Tech. 24(3):195-213.
22. Bush CF, Hall RA. 2008. Olfactory receptor trafficking to the plasma membrane. Cell Mol Life Sci. 65(15):2289-2295.
23. Bushdid C, Magnasco MO, Vosshall LB, Keller A. 2014. Humans can discriminate more than 1 trillion olfactory stimuli. Science. 343(6177):1370-1372.
24. Cain WS, Gent JF. 1991. Olfactory sensitivity: reliability, generality, and association with aging. J Exp Psychol Hum Percept Perform. 17(2):382-391.
25. Carey RM, Verhagen JV, Wesson DW, Pírez N, Wachowiak M. 2009. Temporal structure of receptor neuron input to the olfactory bulb imaged in behaving rats. J Neurophysiol. 101(2):1073-1088.
26. Chen Y, Getchell ML, Ding X, Getchell TV. 1992. Immunolocalization of two cytochrome P450 isozymes in rat nasal chemosensory tissue. Neuroreport. 3(9):749-752.
27. Chess A, Simon I, Cedar H, Axel R. 1994. Allelic inactivation regulates olfactory receptor gene expression. Cell. 78(5):823-834.
28. Crasto C, Marenco L, Miller P, Shepherd G. 2002. Olfactory Receptor Database: a metadata-driven automated population from sources of gene and protein sequences. Nucleic Acids Res. 30(1):354-360.
29. Dahoun T, Grasso L, Vogel H, Pick H. 2011. Recombinant expression and functional characterization of mouse olfactory receptor mOR256-17 in mammalian cells. Biochemistry. 50(33):7228-7235.
30. Dalton RP, Lomvardas S. 2015. Chemosensory receptor specificity and regulation. Annu Rev Neurosci. 38:331-349.
31. 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(6289):184-187.
32. Escada PA, Lima C, da Silva JM. 2009. The human olfactory mucosa. Eur Arch Otorhinolaryngol. 266(11):1675-1680.
33. Feinstein P, Bozza T, Rodriguez I, Vassalli A, Mombaerts P. 2004. Axon guidance of mouse olfactory sensory neurons by odorant receptors and the beta2 adrenergic receptor. Cell. 117(6):833-846.
34. Feldmesser E, Olender T, Khen M, Yanai I, Ophir R, Lancet D. 2006. Widespread ectopic expression of olfactory receptor genes. BMC Genomics. 7:121.
35. Ferreira V. 2012a. Revisiting psychophysical work on the quantitative and qualitative odour properties of simple odour mixtures: a flavour chemistry view. Part 1: intensity and detectability. A review. Flavour Frag J. 27:124-140.
36. Ferreira V. 2012b. Revisiting psychophysical work on the quantitative and qualitative odour properties of simple odour mixtures: a flavour chemistry view. Part 2: qualitative aspects. A review. Flavour Frag J. 27:201-215.
37. Firestein S, Darrow B, Shepherd GM. 1991. Activation of the sensory current in salamander olfactory receptor neurons depends on a G protein-mediated cAMP second messenger system. Neuron. 6(5):825-835.
38. Flegel C, Manteniotis S, Osthold S, Hatt H, Gisselmann G. 2013. Expression profile of ectopic olfactory receptors determined by deep sequencing. PLoS One. 8(2):e55368.
39. Fleischer J, Breer H, Strotmann J. 2009. Mammalian olfactory receptors. Front Cell Neurosci. 3:9.
40. Fujita Y, Takahashi T, Suzuki A, Kawashima K, Nara F, Koishi R. 2007. Deorphanization of Dresden G protein-coupled receptor for an odorant receptor. J Recept Signal Transduct Res. 27(4):323-334.
41. Fülle HJ, Vassar R, Foster DC, Yang RB, Axel R, Garbers DL. 1995. A receptor guanylyl cyclase expressed specifically in olfactory sensory neurons. Proc Natl Acad Sci U S A. 92(8):3571-3575.
42. Gane S. 2010. What we do not know about olfaction. Part 1: from nostril to receptor. Rhinology. 48(2):131-138.
43. Gane S, Georganakis D, Maniati K, Vamvakias M, Ragoussis N, Skoulakis EM, Turin L. 2013. Molecular vibration-sensing component in human olfaction. PLoS One. 8(1):e55780.
44. Gerkin RC, Castro JB. 2015. The number of olfactory stimuli that humans can discriminate is still unknown. Elife. 4:e08127.
45. Getchell TV, Margolis FL, Getchell ML. 1984. Perireceptor and receptor events in vertebrate olfaction. Prog Neurobiol. 23(4):317-345.
46. Gilbert AN, Kemp SE. 1996. Odor perception phenotypes: multiple, specific hyperosmias to musks. Chem Senses. 21(4):411-416.
47. Glusman G, Bahar A, Sharon D, Pilpel Y, White J, Lancet D. 2000. The olfactory receptor gene superfamily: data mining, classification, and nomenclature. Mamm Genome. 11(11):1016-1023.
48. Glusman G, Yanai I, Rubin I, Lancet D. 2001. The complete human olfactory subgenome. Genome Res. 11(5):685-702.
49. Graziadei GA, Graziadei PP. 1979. Neurogenesis and neuron regeneration in the olfactory system of mammals. II. Degeneration and reconstitution of the olfactory sensory neurons after axotomy. J Neurocytol. 8(2):197-213.
50. Grosch W. 1998. Flavour of coffee. A review. Nahrung. 42(6):344-350.
51. Grosmaitre X, Fuss SH, Lee AC, Adipietro KA, Matsunami H, Mombaerts P, Ma M. 2009. SR1, a mouse odorant receptor with an unusually broad response profile. J Neurosci. 29(46):14545-14552.
52. 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(3):348-354.
53. Gross-Isseroff R, Lancet D. 1988. Concentration-dependent changes of perceived odor quality. Chem Senses. 13:191-204.
54. Hahn CG, Han LY, Rawson NE, Mirza N, Borgmann-Winter K, Lenox RH, Arnold SE. 2005. In vivo and in vitro neurogenesis in human olfactory epithelium. J Comp Neurol. 483(2):154-163.
55. Harris JA, West AK, Chuah MI. 2009. Olfactory ensheathing cells: nitric oxide production and innate immunity. Glia. 57(16):1848-1857.
56. Hegg CC, Irwin M, Lucero MT. 2009. Calcium store-mediated signaling in sustentacular cells of the mouse olfactory epithelium. Glia. 57(6):634-644.
57. Holcomb JD, Graham S, Calof AL. 1996. Neuronal homeostasis in mammalian olfactory epithelium: a review. Am J Rhinol. 10:125-134.
58. Horowitz LF, Saraiva LR, Kuang D, Yoon KH, Buck LB. 2014. Olfactory receptor patterning in a higher primate. J Neurosci. 34(37):12241-12252.
59. Hurtt ME, Thomas DA, Working PK, Monticello TM, Morgan KT. 1988. Degeneration and regeneration of the olfactory epithelium following inhalation exposure to methyl-bromide-pathology, cell-kinetics, and olfactory function. Toxicol Appl Pharm. 94:311-328.
60. Iannario M, Manisera M, Piccolo D, Zuccolotto P. 2012. Sensory analysis in the food industry as a tool for marketing decisions. Adv Data Anal Classi 6:303-321.
61. Imai T, Sakano H, Vosshall LB. 2010. Topographic mapping-the olfactory system. Cold Spring Harb Perspect Biol. 2(8):a001776.
62. Institute of Food Technologists. 1975. Minutes of Sensory Evaluation Division. Business Meeting at the 35th Annual Meeting of the IFT, Chicago, June 10.
63. Ishii T, Serizawa S, Kohda A, Nakatani H, Shiroishi T, Okumura K, Iwakura Y, Nagawa F, Tsuboi A, Sakano H. 2001. Monoallelic expression of the odourant receptor gene and axonal projection of olfactory sensory neurones. Genes Cells. 6(1):71-78.
64. Iwai N, Zhou Z, Roop DR, Behringer RR. 2008. Horizontal basal cells are multipotent progenitors in normal and injured adult olfactory epithelium. Stem Cells. 26(5):1298-1306.
65. Jacoby E, Bouhelal R, Gerspacher M, Seuwen K. 2006. The 7 TM G-proteincoupled receptor target family. ChemMedChem. 1(8):761-782.
66. Jacquier V, Pick H, Vogel H. 2006. Characterization of an extended receptive ligand repertoire of the human olfactory receptor OR17-40 comprising structurally related compounds. J Neurochem. 97(2):537-544.
67. Jadauji JB, Djordjevic J, Lundström JN, Pack CC. 2012. Modulation of olfactory perception by visual cortex stimulation. J Neurosci. 32(9):3095-3100.
68. Jaeger SR, McRae JF, Bava CM, Beresford MK, Hunter D, Jia Y, Chheang SL, Jin D, Peng M, Gamble JC, et al. 2013. A Mendelian trait for olfactory sensitivity affects odor experience and food selection. Curr Biol. 23(16):1601-1605.
69. Jafek BW, Gordon AS, Moran DT, Eller PM. 1990. Congenital anosmia. Ear Nose Throat J. 69(5):331-337.
70. Jafek BW, Murrow B, Michaels R, Restrepo D, Linschoten M. 2002. Biopsies of human olfactory epithelium. Chem Senses. 27(7):623-628.
71. Jones DT, Reed RR. 1989. Golf: an olfactory neuron specific-G protein involved in odorant signal transduction. Science. 244(4906):790-795.
72. Kadohisa M, Wilson DA. 2006. Separate encoding of identity and similarity of complex familiar odors in piriform cortex. Proc Natl Acad Sci U S A. 103(41):15206-15211.
73. 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(7):1806-1815.
74. Katada S, Tanaka M, Touhara K. 2004. Structural determinants for membrane trafficking and G protein selectivity of a mouse olfactory receptor. J Neurochem. 90(6):1453-1463.
75. Kato A, Touhara K. 2009. Mammalian olfactory receptors: pharmacology, G protein coupling and desensitization. Cell Mol Life Sci. 66(23):3743-3753.
76. Keller A, Vosshall LB. 2008. Better smelling through genetics: mammalian odor perception. Curr Opin Neurobiol. 18(4):364-369.
77. Keller A, Zhuang H, Chi Q, Vosshall LB, Matsunami H. 2007. Genetic variation in a human odorant receptor alters odour perception. Nature. 449(7161):468-472.
78. Knaapila A, Keskitalo K, Kallela M, Wessman M, Sammalisto S, Hiekkalinna T, Palotie A, Peltonen L, Tuorila H, Perola M. 2007. Genetic component of identification, intensity and pleasantness of odours: a Finnish family study. Eur J Hum Genet. 15(5):596-602.
79. Krautwurst D, Yau KW, Reed RR. 1998. Identification of ligands for olfactory receptors by functional expression of a receptor library. Cell. 95(7):917-926.
80. Laing DG, Francis GW. 1989. The capacity of humans to identify odors in mixtures. Physiol Behav. 46(5):809-814.
81. Laing DG, Glemarec A. 1992. Selective attention and the perceptual analysis of odor mixtures. Physiol Behav. 52(6):1047-1053.
82. Leopold DA, Hornung DE, Schwob JE. 1992. Congenital lack of olfactory ability. Ann Otol Rhinol Laryngol. 101(3):229-236.
83. Leung CT, Coulombe PA, Reed RR. 2007. Contribution of olfactory neural stem cells to tissue maintenance and regeneration. Nat Neurosci. 10(6):720-726.
84. 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 U S A. 104(7):2471-2476.
85. Livermore A, Laing DG. 1996. Influence of training and experience on the perception of multicomponent odor mixtures. J Exp Psychol Hum Percept Perform. 22(2):267-277.
86. Livermore A, Laing DG. 1998. The influence of odor type on the discrimination and identification of odorants in multicomponent odor mixtures. Physiol Behav. 65(2):311-320.
87. Lu M, Echeverri F, Moyer BD. 2003. Endoplasmic reticulum retention, degradation, and aggregation of olfactory G-protein coupled receptors. Traffic. 4(6):416-433.
88. Lucero MT. 2013. Peripheral modulation of smell: fact or fiction? Semin Cell Dev Biol. 24(1):58-70.
89. Lunde K, Egelandsdal B, Skuterud E, Mainland JD, Lea T, Hersleth M, Matsunami H. 2012. Genetic variation of an odorant receptor OR7D4 and sensory perception of cooked meat containing androstenone. PLoS One. 7(5):e35259.
90. Magnasco MO, Keller A, Vosshall LB. 2015. On the dimensionality of olfactory space. bioRxiv:022103.
91. Mainland JD, Keller A, Li YR, Zhou T, Trimmer C, Snyder LL, Moberly AH, Adipietro KA, Liu WL, Zhuang H, et al. 2014. The missense of smell: functional variability in the human odorant receptor repertoire. Nat Neurosci. 17(1):114-120.
92. Majid A, Burenhult N. 2014. Odors are expressible in language, as long as you speak the right language. Cognition. 130(2):266-270.
93. Malnic B, Hirono J, Sato T, Buck LB. 1999. Combinatorial receptor codes for odors. Cell. 96(5):713-723.
94. Markenscoff-Papadimitriou E, Allen WE, Colquitt BM, Goh T, Murphy KK, Monahan K, Mosley CP, Ahituv N, Lomvardas S. 2014. Enhancer interaction networks as a means for singular olfactory receptor expression. Cell. 159(3):543-557.
95. Matarazzo V, Clot-Faybesse O, Marcet B, Guiraudie-Capraz G, Atanasova B, Devauchelle G, Cerutti M, Etiévant P, Ronin C. 2005. Functional characterization of two human olfactory receptors expressed in the baculovirus Sf9 insect cell system. Chem Senses. 30(3):195-207.
96. Matarazzo V, Zsürger N, Guillemot JC, Clot-Faybesse O, Botto JM, Dal Farra C, Crowe M, Demaille J, Vincent JP, Mazella J, et al. 2002. Porcine odorant-binding protein selectively binds to a human olfactory receptor. Chem Senses. 27(8):691-701.
97. Matulionis DH. 1975. Ultrastructural study of mouse olfactory epithelium following destruction by ZnSO4 and its subsequent regeneration. Am J Anat. 142(1):67-89.
98. Matulionis DH. 1976. Light and electron microscopic study of the degeneration and early regeneration of olfactory epithelium in the mouse. Am J Anat. 145(1):79-99.
99. McRae JF, Mainland JD, Jaeger SR, Adipietro KA, Matsunami H, Newcomb RD. 2012. Genetic variation in the odorant receptor OR2J3 is associated with the ability to detect the "grassy" smelling odor, cis-3-hexen-1-ol. Chem Senses. 37(7):585-593.
100. Meister M. 2015. On the dimensionality of odor space. Elife. 4:e07865.
101. Menashe I, Abaffy T, Hasin Y, Goshen S, Yahalom V, Luetje CW, Lancet D. 2007. Genetic elucidation of human hyperosmia to isovaleric acid. PLoS Biol. 5(11):e284.
102. Menashe I, Man O, Lancet D, Gilad Y. 2003. Different noses for different people. Nat Genet. 34(2):143-144.
103. Menco BP, Morrison EE. 2003. Morphology of the mammalian olfactory epithelium: form, fine structure, function and pathology. In: Doty RL, editor. Handbook of olfaction and gustation. New York: Marcel Dekker, Inc. p. 17-49.
104. Miyamichi K, Serizawa S, Kimura HM, Sakano H. 2005. Continuous and overlapping expression domains of odorant receptor genes in the olfactory epithelium determine the dorsal/ventral positioning of glomeruli in the olfactory bulb. J Neurosci. 25(14):3586-3592.
105. Mombaerts P. 2004a. Genes and ligands for odorant, vomeronasal and taste receptors. Nat Rev Neurosci. 5(4):263-278.
106. Mombaerts P. 2004b. Odorant receptor gene choice in olfactory sensory neurons: the one receptor-one neuron hypothesis revisited. Curr Opin Neurobiol. 14(1):31-36.
107. Mombaerts P, Wang F, Dulac C, Chao SK, Nemes A, Mendelsohn M, Edmondson J, Axel R. 1996. Visualizing an olfactory sensory map. Cell. 87(4):675-686.
108. Moncrieff RW. 1949. What is odor? A new theory. Am Perfumer. 54:453.
109. Mori K, Sakano H. 2011. How is the olfactory map formed and interpreted in the mammalian brain? Annu Rev Neurosci. 34:467-499.
110. Morrot G, Brochet F, Dubourdieu D. 2001. The color of odors. Brain Lang. 79(2):309-320.
111. Mozell MM. 1964. Evidence for sorption as a mechanism of the olfactory analysis of vapours. Nature. 203:1181-1182.
112. Mozell MM, Jagodowicz M. 1973. Chromatographic separation of odorants by the nose: retention times measured across in vivo olfactory mucosa. Science. 181(4106):1247-1249.
113. Mozell MM, Kent PF, Murphy SJ. 1991. The effect of flow-rate upon the magnitude of the olfactory response differs for different odorants. Chem Senses. 16:631-649.
114. Nagashima A, Touhara K. 2010. Enzymatic conversion of odorants in nasal mucus affects olfactory glomerular activation patterns and odor perception. J Neurosci. 30(48):16391-16398.
115. Nakashima T, Kimmelman CP, Snow JB Jr. 1984. Structure of human fetal and adult olfactory neuroepithelium. Arch Otolaryngol. 110(10):641-646.
116. Neuhaus EM, Mashukova A, Zhang W, Barbour J, Hatt H. 2006. A specific heat shock protein enhances the expression of mammalian olfactory receptor proteins. Chem Senses. 31(5):445-452.
117. Niimura Y, Matsui A, Touhara K. 2014. Extreme expansion of the olfactory receptor gene repertoire in African elephants and evolutionary dynamics of orthologous gene groups in 13 placental mammals. Genome Res. 24(9):1485-1496.
118. Oka Y, Omura M, Kataoka H, Touhara K. 2004. Olfactory receptor antagonism between odorants. EMBO J. 23(1):120-126.
119. Olender T, Feldmesser E, Atarot T, Eisenstein M, Lancet D. 2004. The olfactory receptor universe-from whole genome analysis to structure and evolution. Genet Mol Res. 3(4):545-553.
120. Olender T, Waszak SM, Viavant M, Khen M, Ben-Asher E, Reyes A, Nativ N, Wysocki CJ, Ge D, Lancet D. 2012. Personal receptor repertoires: olfaction as a model. BMC Genomics. 13:414.
121. Owen SJ, Batzloff M, Chehrehasa F, Meedeniya A, Casart Y, Logue CA, Hirst RG, Peak IR, Mackay-Sim A, Beacham IR. 2009. Nasal-associated lymphoid tissue and olfactory epithelium as portals of entry for Burkholderia pseudomallei in murine melioidosis. J Infect Dis. 199(12):1761-1770.
122. Pace U, Hanski E, Salomon Y, Lancet D. 1985a. Odorant-sensitive adenylate cyclase may mediate olfactory reception. Nature. 316(6025):255-258.
123. Pace U, Hanski E, Salomon Y, Lancet D. 1985b. Odorant-sensitive adenylatecyclase may mediate olfactory reception. Nature. 316:255-258.
124. Parmentier M, Libert F, Schurmans S, Schiffmann S, Lefort A, Eggerickx D, Ledent C, Mollereau C, Gerard C, Perret J, et al. 1992. Expression of members of the putative olfactory receptor gene family in mammalian germcells. Nature. 355:453-455.
125. Pavlath GK. 2010. A new function for odorant receptors: MOR23 is necessary for normal tissue repair in skeletal muscle. Cell Adh Migr. 4(4):502-506.
126. Peterlin Z, Firestein S, Rogers ME. 2014. The state of the art of odorant receptor deorphanization: a report from the orphanage. J Gen Physiol. 143(5):527-542.
127. Pevsner J, Reed RR, Feinstein PG, Snyder SH. 1988. Molecular cloning of odorant-binding protein: member of a ligand carrier family. Science. 241(4863):336-339.
128. Pietrobon M, Zamparo I, Maritan M, Franchi SA, Pozzan T, Lodovichi C. 2011. Interplay among cGMP, cAMP, and Ca2+ in living olfactory sensory neurons in vitro and in vivo. J Neurosci. 31: 8395-8405.
129. Pluznick JL, Protzko RJ, Gevorgyan H, Peterlin Z, Sipos A, Han J, Brunet I, Wan LX, Rey F, Wang T, et al. 2013. Olfactory receptor responding to gut microbiota-derived signals plays a role in renin secretion and blood pressure regulation. Proc Natl Acad Sci U S A. 110(11):4410-4415.
130. Pointer MR, Attridge GG. 1998. The number of discernible colours. Color Res Appl 23:52-54.
131. Qureshy A, Kawashima R, Imran MB, Sugiura M, Goto R, Okada K, Inoue K, Itoh M, Schormann T, Zilles K, et al. 2000. Functional mapping of human brain in olfactory processing: a PET study. J Neurophysiol. 84(3):1656-1666.
132. Ramón-Cueto A, Avila J. 1998. Olfactory ensheathing glia: properties and function. Brain Res Bull. 46(3):175-187.
133. Reisert J, Matthews HR. 1998. Na+-dependent Ca2+ extrusion governs response recovery in frog olfactory receptor cells. J Gen Physiol. 112(5):529-535.
134. Ressler KJ, Sullivan SL, Buck LB. 1993. A zonal organization of odorant receptor gene expression in the olfactory epithelium. Cell. 73(3):597-609.
135. Royet JP, Koenig O, Gregoire MC, Cinotti L, Lavenne F, Le Bars D, Costes N, Vigouroux M, Farget V, Sicard G, et al. 1999. Functional anatomy of perceptual and semantic processing for odors. J Cogn Neurosci. 11(1):94-109.
136. Safran M, Chalifa-Caspi V, Shmueli O, Olender T, Lapidot M, Rosen N, Shmoish M, Peter Y, Glusman G, Feldmesser E, et al. 2003. Human Gene-Centric Databases at the Weizmann Institute of Science: GeneCards, UDB, CroW 21 and HORDE. Nucleic Acids Res. 31(1):142-146.
137. Sahin-Yilmaz A, Naclerio RM. 2011. Anatomy and physiology of the upper airway. Proc Am Thorac Soc. 8(1):31-39.
138. Saito H, Chi Q, Zhuang H, Matsunami H, Mainland JD. 2009. Odor coding by a Mammalian receptor repertoire. Sci Signal. 2(60):ra9.
139. Saito H, Kubota M, Roberts RW, Chi Q, Matsunami H. 2004. RTP family members induce functional expression of mammalian odorant receptors. Cell. 119(5):679-691.
140. Sanz G, Schlegel C, Pernollet JC, Briand L. 2005. Comparison of odorant specificity of two human olfactory receptors from different phylogenetic classes and evidence for antagonism. Chem Senses. 30(1):69-80.
141. Schmidt C, Schmidt U, Breipohl W, Effenberger F. 1984. The effect of N-methylformimino-methylester on the neural olfactory threshold in albino mice. Arch Otorhinolaryngol. 239(1):25-29.
142. Schmiedeberg K, Shirokova E, Weber HP, Schilling B, Meyerhof W, Krautwurst D. 2007. Structural determinants of odorant recognition by the human olfactory receptors OR1A1 and OR1A2. J Struct Biol. 159(3):400-412.
143. Schroeder BC, Cheng T, Jan YN, Jan LY. 2008. Expression cloning of TMEM16A as a calcium-activated chloride channel subunit. Cell. 134(6):1019-1029.
144. Schwob JE. 2002. Neural regeneration and the peripheral olfactory system. Anat Rec. 269(1):33-49.
145. Schwob JE, Youngentob SL, Mezza RC. 1995. Reconstitution of the rat olfactory epithelium after methyl bromide-induced lesion. J Comp Neurol. 359(1):15-37.
146. Serizawa S, Ishii T, Nakatani H, Tsuboi A, Nagawa F, Asano M, Sudo K, Sakagami J, Sakano H, Ijiri T, et al. 2000. Mutually exclusive expression of odorant receptor transgenes. Nat Neurosci. 3(7):687-693.
147. Serizawa S, Miyamichi K, Nakatani H, Suzuki M, Saito M, Yoshihara Y, Sakano H. 2003. Negative feedback regulation ensures the one receptor-one olfactory neuron rule in mouse. Science. 302(5653): 2088-2094.
148. Serizawa S, Miyamichi K, Sakano H. 2004. One neuron-one receptor rule in the mouse olfactory system. Trends Genet. 20(12):648-653.
149. Shirasu M, Yoshikawa K, Takai Y, Nakashima A, Takeuchi H, Sakano H, Touhara K. 2014. Olfactory receptor and neural pathway responsible for highly selective sensing of musk odors. Neuron. 81(1):165-178.
150. Sobel N, Khan RM, Saltman A, Sullivan EV, Gabrieli JD. 1999. The world smells different to each nostril. Nature. 402(6757):35.
151. Sobel N, Prabhakaran V, Desmond JE, Glover GH, Goode RL, Sullivan EV, Gabrieli JD. 1998. Sniffing and smelling: separate subsystems in the human olfactory cortex. Nature. 392(6673):282-286.
152. Song Y, Cygnar KD, Sagdullaev B, Valley M, Hirsh S, Stephan A, Reisert J, Zhao H. 2008. Olfactory CNG channel desensitization by Ca2+/CaM via the B1b subunit affects response termination but not sensitivity to recurring stimulation. Neuron. 58(3):374-386.
153. Sookoian S, Burgueño A, Gianotti TF, Marillet G, Pirola CJ. 2011. Odor perception between heterosexual partners: its association with depression, anxiety, and genetic variation in odorant receptor OR7D4. Biol Psychol. 86(3):153-157.
154. Spehr M, Gisselmann G, Poplawski A, Riffell JA, Wetzel CH, Zimmer RK, Hatt H. 2003. Identification of a testicular odorant receptor mediating human sperm chemotaxis. Science. 299(5615):2054-2058.
155. Steiger SS, Fidler AE, Valcu M, Kempenaers B. 2008. Avian olfactory receptor gene repertoires: evidence for a well-developed sense of smell in birds? Proc Biol Sci. 275(1649):2309-2317.
156. Stephan AB, Shum EY, Hirsh S, Cygnar KD, Reisert J, Zhao H. 2009. ANO2 is the cilial calcium-activated chloride channel that may mediate olfactory amplification. Proc Natl Acad Sci U S A. 106(28):11776-11781.
157. Stettler DD, Axel R. 2009. Representations of odor in the piriform cortex. Neuron. 63(6):854-864.
158. Suzuki J, Yoshizaki K, Kobayashi T, Osumi N. 2013. Neural crest-derived horizontal basal cells as tissue stem cells in the adult olfactory epithelium. Neurosci Res. 75(2):112-120.
159. Tcatchoff L, Nespoulous C, Pernollet JC, Briand L. 2006. A single lysyl residue defines the binding specificity of a human odorant-binding protein for aldehydes. FEBS Lett. 580(8):2102-2108.
160. Tong J, Mannea E, Aimé P, Pfluger PT, Yi CX, Castaneda TR, Davis HW, Ren X, Pixley S, Benoit S, et al. 2011. Ghrelin enhances olfactory sensitivity and exploratory sniffing in rodents and humans. J Neurosci. 31(15):5841-5846.
161. Tsuboi A, Miyazaki T, Imai T, Sakano H. 2006. Olfactory sensory neurons expressing class I odorant receptors converge their axons on an anterodorsal domain of the olfactory bulb in the mouse. Eur J Neurosci. 23(6):1436-1444.
162. Vassar R, Ngai J, Axel R. 1993. Spatial segregation of odorant receptor expression in the mammalian olfactory epithelium. Cell. 74(2):309-318.
163. Verbeurgt C, Wilkin F, Tarabichi M, Gregoire F, Dumont JE, Chatelain P. 2014. Profiling of olfactory receptor gene expression in whole human olfactory mucosa. PLoS One. 9(5):e96333.
164. Verhagen JV, Wesson DW, Netoff TI, White JA, Wachowiak M. 2007. Sniffing controls an adaptive filter of sensory input to the olfactory bulb. Nat Neurosci. 10(5):631-639.
165. Vidic J, Grosclaude J, Monnerie R, Persuy MA, Badonnel K, Baly C, Caillol M, Briand L, Salesse R, Pajot-Augy E. 2008. On a chip demonstration of a functional role for odorant binding protein in the preservation of olfactory receptor activity at high odorant concentration. Lab Chip. 8(5):678-688.
166. Von Dannecker LE, Mercadante AF, Malnic B. 2006. Ric-8B promotes functional expression of odorant receptors. Proc Natl Acad Sci U S A. 103(24):9310-9314.
167. Wang F, Nemes A, Mendelsohn M, Axel R. 1998. Odorant receptors govern the formation of a precise topographic map. Cell. 93(1):47-60.
168. Weiss T, Snitz K, Yablonka A, Khan RM, Gafsou D, Schneidman E, Sobel N. 2012. Perceptual convergence of multi-component mixtures in olfaction implies an olfactory white. Proc Natl Acad Sci U S A. 109(49):19959-19964.
169. Wetzel CH, Oles M, Wellerdieck C, Kuczkowiak M, Gisselmann G, Hatt H. 1999. Specificity and sensitivity of a human olfactory receptor functionally expressed in human embryonic kidney 293 cells and Xenopus laevis oocytes. J Neurosci. 19(17):7426-7433.
170. Wilson DA. 2000. Odor specificity of habituation in the rat anterior piriform cortex. J Neurophysiol. 83(1):139-145.
171. Wong ST, Trinh K, Hacker B, Chan GC, Lowe G, Gaggar A, Xia Z, Gold GH, Storm DR. 2000. Disruption of the type III adenylyl cyclase gene leads to peripheral and behavioral anosmia in transgenic mice. Neuron. 27(3):487-497.
172. Yang YD, Cho H, Koo JY, Tak MH, Cho Y, Shim WS, Park SP, Lee J, Lee B, Kim BM, et al. 2008. TMEM16A confers receptor-activated calcium-dependent chloride conductance. Nature. 455(7217):1210-1215.
173. Yeshurun Y, Sobel N. 2010. An odor is not worth a thousand words: from multidimensional odors to unidimensional odor objects. Annu Rev Psychol. 61:219-241, C1.
174. Yoshida I, Mori K. 2007. Odorant category profile selectivity of olfactory cortex neurons. J Neurosci. 27(34):9105-9114.
175. Zarzo M. 2007. The sense of smell: molecular basis of odorant recognition. Biol Rev Camb Philos Soc. 82(3):455-479.
176. Zelano C, Bensafi M, Porter J, Mainland J, Johnson B, Bremner E, Telles C, Khan R, Sobel N. 2005. Attentional modulation in human primary olfactory cortex. Nat Neurosci. 8(1):114-120.
177. Zhang X, De la Cruz O, Pinto JM, Nicolae D, Firestein S, Gilad Y. 2007. Characterizing the expression of the human olfactory receptor gene family using a novel DNA microarray. Genome Biol. 8(5):R86.
178. Zhuang H, Matsunami H. 2007. Synergism of accessory factors in functional expression of mammalian odorant receptors. J Biol Chem. 282(20):15284-15293.
179. Zozulya S, Echeverri F, Nguyen T. 2001. The human olfactory receptor repertoire. Genome Biol. 2: RESEARCH0018.