Cellular and molecular constituents of olfactory sensation in vertebrates

Comparative Biochemistry and Physiology - A Molecular and Integrative Physiology

Volumn 126, Issue 1, 2000, Pages 17-32

  Nakamura, Tadashi ^a,b  

^a Dept of Appl Physics and Chemistry   (Japan)

^b Univ E   (Japan)

Author keywords

Adaptation; Enzyme cascade; Excitation pattern; Ion channel; Odor discrimination; Odorant receptor protein; Second messenger; Transduction

Indexed keywords

CYCLIC AMP; ION CHANNEL; PROTEIN G; RECEPTOR; RECEPTOR PROTEIN;

ADAPTATION; NONHUMAN; ODOR; OLFACTORY BULB; OLFACTORY DISCRIMINATION; OLFACTORY EPITHELIUM; OLFACTORY RECEPTOR; OLFACTORY SYSTEM; PROTEIN PHOSPHORYLATION; REVIEW; SECOND MESSENGER; SIGNAL TRANSDUCTION; VERTEBRATE;

EID: 0033924501     PISSN: 10956433     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1095-6433(00)00191-4     Document Type: Review

References (136)

1. Bakalyar H.A., Reed R.R. Identification of a specialized adenylyl cyclase that may mediate odorant detection. Science. 250:1990;1403-1406.
2. Balasubramanian S., Lynch J.W., Barry P.H. Concentration dependence of sodium permeation and sodium ion interactions in the cyclic AMP-gated channels of mammalian olfactory receptor neurons. J. Membr. Biol. 159:1997;41-52.
3. olf are anosmic. Neuron. 20:1998;69-81.
4. Biel M., Zong X., Hofmann F. Cyclic nucleotide-gated cation channels: molecular diversity, structure, and cellular functions. Trends Cardiovasc. Med. 6:1996;274-280.
5. Bitensky M.W., Miller W.H., Gorman R.E., Neufeld A.H., Robinson R. The role of cyclic AMP in visual excitation. Adv. Cyclic Nucleotide Res. 1:1972;317-335.
6. Boekhoff I., Inglese J., Schleicher S., Koch W.J., Lefkowitz R.J., Breer H. Olfactory desensitization requires membrane targeting of receptor kinase mediated by beta gamma-subunits of heterotrimeric G proteins. J. Biol. Chem. 269:1994;37-40.
7. Boekhoff I., Schleicher S., Strotmann J., Breer H. Odor-induced phosphorylation of olfactory cilia proteins. Proc. Natl. Acad. Sci. USA. 89:1992;11983-11987.
8. Boekhoff I., Tareilus E., Strotmann J., Breer H. Rapid activation of alternative second messenger pathways in olfactory cilia from rats by different odorants. EMBO J. 9:1990;2453-2458.
9. Boekhoff I., Touhara K., Danner S. et al. Phosducin, potential role in modulation of olfactory signaling. J. Biol. Chem. 272:1997;4606-4612.
10. Bonigk W., Bradley J., Muller F. et al. The native rat olfactory cyclic nucleotide-gated channel is composed of three distinct subunits. J. Neurosci. 19:1999;5332-5347.
11. Borisy F.F., Hwang P.N., Ronnett G.V., Snyder S.H. High-affinity cAMP phosphodiesterase and adenosine localized in sensory organs. Brain Res. 610:1993;199-207.
12. Borisy F.F., Ronnett G.V., Cunningham A.M., Juilfs D., Beavo J., Snyder S.H. Calcium/calmodulin-activated phosphodiesterase expressed in olfactory receptor neurons. J. Neurosci. 12:1992;915-923.
13. Bradley J., Zhang Y., Bakin R., Lester H.A., Ronnett G.V., Zinn K. Functional expression of the heteromeric 'olfactory' cyclic nucleotide-gated channel in the hippocampus: a potential effector of synaptic plasticity in brain neurons. J. Neurosci. 17:1997;1993-2005.
14. Breer H., Boekhoff I. Second messenger signalling in olfaction. Curr. Opin. Neurobiol. 2:1992;439-443.
15. Breer H., Boekhoff I., Tareilus E. Rapid kinetics of second messenger formation in olfactory transduction. Nature. 345:1990;65-68.
16. Breer H., Klemm T., Boekhoff I. Nitric oxide mediated formation of cyclic GMP in the olfactory system. Neuroreport. 3:1992;1030-1032.
17. Breer H., Raming K., Krieger J. Signal recognition and transduction in olfactory neurons. Biochim. Biophys. Acta. 1224:1994;277-287.
18. Brunet L.J., Gold G.H., Ngai J. General anosmia caused by a targeted disruption of the mouse olfactory cyclic nucleotide-gated cation channel. Neuron. 17:1996;681-693.
19. Buck L., Axel R. A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell. 65:1991;175-187.
20. Chen C., Nakamura T., Koutalos Y. Cyclic AMP diffusion coefficient in frog olfactory cilia. Biophys. J. 76:1999;2861-2867.
21. 2+-calmodulin of cyclic nucleotide-activated channel of rat olfactory receptor neurons. Nature. 368:1994;545-548.
22. Chess A., Buck L., Dowling M.M., Axel R., Ngai J. Molecular biology of smell: expression of the multigene family encoding putative odorant receptors. Cold Spring Harb. Symp. Quant. Biol. 57:1992;505-516.
23. Chess A., Simon I., Cedar H., Axel R. Allelic inactivation regulates olfactory receptor gene expression. Cell. 78:1994;823-834.
24. Chiu D., Nakamura T., Gold G.H. Ionic composition of toad olfactory mucus measured wsith ion selective microelectrodes. Chemical Senses. 13:1989;677-678.
25. Cinelli A.R., Hamilton K.A., Kauer J.S. Salamander olfactory bulb neuronal activity observed by video rate, voltage-sensitive dye imaging. III: spatial and temporal properties of responses evoked by odorant stimulation. J. Neurophysiol. 73:1995;2053-2071.
26. Dawson T.M., Arriza J.L., Jaworsky D.E. et al. Beta-adrenergic receptor kinase-2 and beta-arrestin-2 as mediators of odorant-induced desensitization. Science. 259:1993;825-829.
27. Delay R.J., Dubin A.E., Dionne V.E. A cyclic nucleotide-dependent chloride conductance in olfactory receptor neurons. J. Membr. Biol. 159:1997;53-60.
28. Dhallan R.S., Yau K.W., Schrader K.A., Reed R.R. Primary structure and functional expression of a cyclic nucleotide-activated channel from olfactory neurons. Nature. 347:1990;184-187.
29. Dubin A.E., Dionne V.E. Action potentials and chemosensitive conductances in the dendrites of olfactory neurons suggest new features for odor transduction. J. Gen. Physiol. 103:1994;181-201.
30. Duchamp-Viret P., Chaput M.A., Duchamp A. Odor response properties of rat olfactory receptor neurons. Science. 284:1999;2171-2174.
31. Fesenko E.E., Kolesnikov S.S., Lyubarsky A.L. Induction by cyclic GMP of cationic conductance in plasma membrane of retinal rod outer segment. Nature. 313:1985;310-313.
32. Finn J.T., Grunwald M.E., Yau K.-W. Cyclic nucleotide-gated ion channels: An extended family with diverse functions. Annu. Rev. Physiol. 58:1996;395-426.
33. Firestein S., Darrow B., Shepherd G.M. Activation of the sensory current in salamander olfactory receptor neurons depends on a G protein-mediated cAMP second messenger system. Neuron. 6:1991;825-835.
34. Firestein S., Picco C., Menini A. The relation between stimulus and response in olfactory receptor cells of the tiger salamander. J. Physiol. (Lond). 468:1993;1-10.
35. Firestein S., Shepherd G.M. Interaction of anionic and cationic currents leads to a voltage dependence in the odor response of olfactory receptor neurons. J. Neurophysiol. 73:1995;562-567.
36. Firestein S., Zufall F., Shepherd G.M. Single odor-sensitive channels in olfactory receptor neurons are also gated by cyclic nucleotides. J. Neurosci. 11:1991;3565-3572.
37. Frings S. Protein kinase C sensitizes olfactory adenylate cyclase. J. Gen. Physiol. 101:1993;183-205.
38. Fulle H.J., Vassar R., Foster D.C., Yang R.B., Axel R., Garbers D.L. A receptor guanylyl cyclase expressed specifically in olfactory sensory neurons. Proc. Natl. Acad. Sci. USA. 92:1995;3571-3575.
39. Gautier-Courteille C., Salanova M., Conti M. The olfactory adenylyl cyclase III is expressed in rat germ cells during spermiogenesis. Endocrinology. 139:1998;2588-2599.
40. Getchell T.V. Induction of odorant-evoked current transients in Xenopus oocytes injected with mRNA isolated from the olfactory mucosa of Rana pipiens. Neurosci. Lett. 91:1988;217-221.
41. Gierer A. Possible involvement of gradients in guidance of receptor cell axons towards their target position on the olfactory bulb. Eur. J. Neurosci. 10:1998;388-391.
42. Gold G.H. Controversial issues in vertebrate olfactory transduction. Annu. Rev. Physiol. 61:1999;857-871.
43. Gold G.H., Nakamura T. Cyclic nucleotide-gated conductances: a new class of ionic channels mediates visual and olfactory transduction. Trends Pharmacol. 8:1987;312-316.
44. Goulding E.H., Tibbs G.R., Siegelbaum S.A. Molecular mechanism of cyclic-nucleotide-gated channel activation. Nature. 372:1994;369-374.
45. Griff I.C., Reed R.R. The genetic basis for specific anosmia to isovaleric acid in the mouse. Cell. 83:1995;407-414.
46. Hallani M., Lynch J.W., Barry P.H. Characterization of calcium-activated chloride channels in patches excised from the dendritic knob of mammmalian olfactory receptor neurons. J. Membrane Biol. 161:1998;163-171.
47. i increases in isolated olfactory receptor neurons retaining their original spatial relationship in intact tissue. J. Neurosci. Methods. 42:1992;185-194.
48. Huque T., Bruch R.C. Odorant- and guanine nucleotide-stimulated phosphoinositide turnover in olfactory cilia. Biochem. Biophys. Res. Commun. 137:1986;36-42.
49. Ingi T., Ronnett G.V. Direct demonstration of a physiological role for carbon monoxide in olfactory receptor neurons. J. Neurosci. 15:1995;8214-8222.
50. Jaworsky D.E., Matsuzaki O., Borisy F.F., Ronnett G.V. Calcium modulates the rapid kinetics of the odorant-induced cyclic AMP signal in rat olfactory cilia. J. Neurosci. 15:1995;310-318.
51. Johnson B.A., Woo C.C., Leon M. Spatial coding of odorant features in the glomerular layer of the rat olfactory bulb. J. Comp. Neurol. 393:1998;457-471.
52. olf: an olfactory neuron specific-G protein involved in odorant signal transduction. Science. 244:1989;790-795.
53. Juilfs D.M., Fulle H.J., Zhao A.Z., Houslay M.D., Garbers D.L., Beavo J.A. 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. 94:1997;3388-3395.
54. Jung A., Lischka F.W., Engel J., Schild D. Sodium/calcium exchanger in olfactory receptor neurones of Xenopus laevis. Neuroreport. 5:1994;1741-1744.
55. 2+ uptake in frog olfactory receptor cells. Biochem. Biophys. Res. Commun. 225:1996;666-671.
56. --dependence of the turtle olfactory response to odorants and forskolin. Comp. Biochem. Physiol. 115A:1996;43-52.
57. Kashiwayanagi M., Kurihara K. Odor discrimination in single turtle olfactory receptor neuron. Neurosci. Lett. 170:1994;233-236.
58. Kauer J.S., Cinelli A.R. Are there structural and functional modules in the vertebrate olfactory bulb? Microsc. Res. Tech. 24:1993;157-167.
59. Kiefer H., Krieger J., Olszewski J.D., Von Heijne G., Prestwich G.D., Breer H. Expression of an olfactory receptor in Escherichia coli: purification, reconstitution, and ligand binding. Biochemistry. 35:1996;16077-16084.
60. Kingston P.A., Zufall F., Barnstable C.J. Rat hippocampal neurons express genes for both rod retinal and olfactory cyclic nucleotide-gated channels: novel targets for cAMP/cGMP function. Proc. Natl. Acad. Sci. USA. 93:1996;10440-10445.
61. Kleene S.J. Both external and internal calcium reduce the sensitivity of the olfactory cyclic-nucleotide-gated channel to CAMP. J. Neurophysiol. 81:1999;2675-2682.
62. Kleene S.J., Gesteland R.C. Calcium-activated chloride conductance in frog olfactory cilia. J. Neurosci. 11:1991;3624-3629.
63. Kleene S.J., Gesteland R.C., Bryant S.H. An electrophysiological survey of frog olfactory cilia. J. Exp. Biol. 195:1994;307-328.
64. Krautwurst D., Yau K.W., Reed R.R. Identification of ligands for olfactory receptors by functional expression of a receptor library. Cell. 95:1998;917-926.
65. Krieger J., Schleicher S., Strotmann J. et al. Probing olfactory receptors with sequence-specific antibodies. Eur. J. Biochem. 219:1994;829-835.
66. Kroner C., Boekhoff I., Lohmann S.M., Genieser H.G., Breer H. Regulation of olfactory signalling via cGMP-dependent protein kinase. Eur. J. Biochem. 236:1996;632-637.
67. Kurahashi T., Kaneko A. High density cAMP-gated channels at the ciliary membrane in the olfactory receptor cell. Neuroreport. 2:1991;5-8.
68. Kurahashi T., Menini A. Mechanism of odorant adaptation in the olfactory receptor cell. Nature. 385:1997;725-729.
69. Kurahashi T., Yau K.W. Co-existence of cationic and chloride components in odorant-induced current of vertebrate olfactory receptor cells. Nature. 363:1993;71-74.
70. Kurihara K., Koyama N. High activity of adenyl cyclase in olfactory and gustatory organs. Biochem. Biophys. Res. Commun. 48:1972;30-34.
71. Leinders-Zufall T., Greer C.A., Shepherd G.M., Zufall F. Imaging odor-induced calcium transients in single olfactory cilia: specificity of activation and role in transduction. J. Neurosci. 18:1998;5630-5639.
72. Leinders-Zufall T., Rand M.N., Shepherd G.M., Greer C.A., Zufall F. Calcium entry through cyclic nucleotide-gated channels in individual cilia of olfactory receptor cells: spatiotemporal dynamics. J. Neurosci. 17:1997;4136-4148.
73. Liman E.R., Buck L.B. A second subunit of the olfactory cyclic nucleotide-gated channel confers high sensitivity to cAMP. Neuron. 13:1994;611-621.
74. Lischka F.W., Zviman M.M., Teeter J.H., Restrepo D. Characterization of inositol-1,4,5-trisphosphate-gated channels in the plasma membrane of rat olfactory neurons. Biophys. J. 76:1999;1410-1422.
75. Liu M., Chen T.Y., Ahamed B., Li J., Yau K.W. Calcium-calmodulin modulation of the olfactory cyclic nucleotide-gated cation channel. Science. 266:1994;1348-1354.
76. Lowe G., Gold G.H. Contribution of the ciliary cyclic nucleotide-gated conductance to olfactory transduction in the salamander. J. Physiol. (Lond). 462:1993;175-196.
77. Lowe G., Gold G.H. Nonlinear amplification by calcium-dependent chloride channels in olfactory receptor cells. Nature. 366:1993;283-286.
78. Ludwig J., Margalit T., Eismann E., Lancet D., Kaupp U.B. Primary structure of cAMP-gated channel from bovine olfactory epithelium. FEBS Lett. 270:1990;24-29.
79. Malnic B., Hirono J., Sato T., Buck L.B. Combinatorial receptor codes for odors. Cell. 96:1999;713-723.
80. Miyamoto T., Restrepo D., Cragoe E.J. Jr., Teeter J.H. IP3- and cAMP-induced responses in isolated olfactory receptor neurons from the channel catfish. J. Membr. Biol. 127:1992;173-183.
81. Mombaerts, P., Wang, F., Dulac, C., Chao, S.K., Nemes, A., Mendelsohn, M., Edmondson, J., Axel, R., 1996. Visualizing an olfactory sensory map. Cell 87, 675-686.
82. Moon C., Jaberi P., Otto-Bruc A., Baehr W., Palczewski K., Ronnett G.V. Calcium-sensitive particulate guanylyl cyclase as a modulator of cAMP in olfactory receptor neurons. J. Neurosci. 18:1998;3195-3205.
83. Morales B., Madrid R., Bacigalupo J. Calcium mediates the activation of the inhibitory current induced by odorants in toad olfactory receptor neurons. FEBS Lett. 402:1997;259-264.
84. Muller F., Bonigk W., Sesti F., Frings S. Phosphorylation of mammalian olfactory cyclic nucleotide-gated channels increases ligand sensitivity. J. Neurosci. 18:1998;164-173.
85. Nakamura T., Gold G.H. A cyclic nucleotide-gated conductance in olfactory receptor cilia. Nature. 325:1987;442-444.
86. Nakamura T., Kaneko H., Nishida N. Direct measurement of the chloride concentration in newt olfactory receptors with the fluorescent probe. Neurosci. Lett. 237:1997;5-8.
87. Nakamura T., Lee H.H., Kobayashi H., Satoh T.O. Gated conductances in native and reconstituted membranes from frog olfactory cilia. Biophys. J. 70:1996;813-817.
88. Nakamura T., Satoh T.O., Miyamoto S. Ligand-gated ionic conductances in the olfactory cilia. Biophysics. 40:1995;193-199.
89. Nakamura T., Satoh T.-O., Lee H.-H., Kobayashi H., Noguchi S. Ionic mechanisms in olfactory reception: perspective through ion channels in the vertebrate olfactory cilia. Baum G.L., Priel Z., Roth Y., Liron N., Ostfeld E. Cilia, Mucus, and Mucociliary Interactions. 1998;79-85 Marcel Dekker. Inc, New York, Basel, Hong Kong.
90. 2+ concentration by second messengers in newt olfactory receptor cell. Neurosci Lett. 171:1994;197-200.
91. Ngai J., Dowling M.M., Buck L., Axel R., Chess A. The family of genes encoding odorant receptors in the channel catfish. Cell. 72:1993;657-666.
92. Noe J., Tareilus E., Boekhoff I., Breer H. Sodium/calcium exchanger in rat olfactory neurons. Neurochem. Int. 30:1997;523-531.
93. Pace U., Hanski E., Salomon Y., Lancet D. Odorant-sensitive adenylate cyclase may mediate olfactory reception. Nature. 316:1985;255-258.
94. Paulssen R.H., Johansen P.W., Gordeladze J.O., Nymoen O., Paulssen E.J., Gautvik K.M. Cell-specific expression and function of adenylyl cyclases in rat pituitary tumour cell lines. Eur. J. Biochem. 222:1994;97-103.
95. Peppel K., Boekhoff I., McDonald P., Breer H., Caron M.G., Lefkowitz R.J. G protein-coupled receptor kinase 3 (GRK3) gene disruption leads to loss of odorant receptor desensitization. J. Biol. Chem. 272:1997;25425-25428.
96. Raming K., Krieger J., Strotmann J. et al. Cloning and expression of odorant receptors. Nature. 361:1993;353-356.
97. 2+ extrusion governs response recovery in frog olfactory receptor cells. J. Gen. Physiol. 112:1998;529-535.
98. Ressler K.J., Sullivan S.L., Buck L.B. A zonal organization of odorant receptor gene expression in the olfactory epithelium. Cell. 73:1993;597-609.
99. 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. 79:1994;1245-1255.
100. Restrepo D., Boekhoff I., Breer H. Rapid kinetic measurements of second messenger formation in olfactory cilia from channel catfish. Am. J. Physiol. 264C:1993;906-911.
101. i] in olfactory neurons of the catfish (Ictalurus punctatus). J. Membr. Biol. 120:1991;223-232.
102. Restrepo D., Miyamoto T., Bryant B.P., Teeter J.H. Odor stimuli trigger influx of calcium into olfactory neurons of the channel catfish. Science. 249:1990;1166-1168.
103. 2+ gradients in rat olfactory neurons. J. Gen. Physiol. 102:1993;907-924.
104. Restrepo D., Teeter J.H., Honda E., Boyle A.G., Marecek J.F., Prestwich G.D., Kalinoski D.L. Evidence for an InsP3-gated channel protein in isolated rat olfactory cilia. Am. J. Physiol. 263C:1992;667-673.
105. Restrepo D., Teeter J.H., Schild D. Second messenger signaling in olfactory transduction. J. Neurobiol. 30:1996;37-48.
106. Reuter D., Zierold K., Schroder W.H., Frings S. A depolarizing chloride current contributes to chemoelectrical transduction in olfactory sensory neurons in situ. J. Neurosci. 18:1998;6623-6630.
107. Ronnett G.V., Cho H., Hester L.D., Wood S.F., Snyder S.H. Odorants differentially enhance phosphoinositide turnover and adenylyl cyclase in olfactory receptor neuronal cultures. J. Neurosci. 13:1993;1751-1758.
108. Ronnett G.V., Hester L.D., Snyder S.H. Primary culture of neonatal rat olfactory neurons. J. Neurosci. 11:1991;1243-1255.
109. Ronnett G.V., Parfitt D.J., Hester L.D., Snyder S.H. Odorant-sensitive adenylate cyclase: rapid, potent activation and desensitization in primary olfactory neuronal cultures. Proc. Natl. Acad. Sci. USA. 88:1991;2366-2369.
110. Roskams A.J., Bredt D.S., Dawson T.M., Ronnett G.V. Nitric oxide mediates the formation of synaptic connections in developing and regenerating olfactory receptor neurons. Neuron. 13:1994;289-299.
111. 2+ evoked by odor in isolated frog olfactory receptor neurons. Neuroreport. 2:1991;229-232.
112. Sato T., Hirono J., Tonoike M., Takebayashi M. Tuning specificities to aliphatic odorants in mouse olfactory receptor neurons and their local distribution. J. Neurophysiol. 72:1994;2980-2989.
113. Schild D., Restrepo D. Transduction mechanisms in vertebrate olfactory receptor cells. Physiol. Rev. 78:1998;429-466.
114. Schleicher S., Boekhoff I., Arriza J., Lefkowitz R.J., Breer H. A beta-adrenergic receptor kinase-like enzyme is involved in olfactory signal termination. Proc. Natl. Acad. Sci. USA. 90:1993;1420-1424.
115. Sklar P.B., Anholt R.R., Snyder S.H. The odorant-sensitive adenylate cyclase of olfactory receptor cells: differential stimulation by distinct classes of odorants. J. Biol. Chem. 261:1986;15538-15543.
116. Strotmann J., Wanner I., Helfrich T., Beck A., Breer H. Rostro-caudal patterning of receptor-expressing olfactory neurones in the rat nasal cavity. Cell Tissue Res. 278:1994;11-20.
117. Strotmann J., Wanner I., Krieger J., Raming K., Breer H. Expression of odorant receptors in spatially restricted subsets of chemosensory neurones. Neuroreport. 3:1992;1053-1056.
118. Sullivan S.L., Bohm S., Ressler K.J., Horowitz L.F., Buck L.B. Target-independent pattern specification in the olfactory epithelium. Neuron. 15:1995;779-789.
119. Sullivan S.L., Dryer L. Information processing in mammalian olfactory system. J. Neurobiol. 30:1996;20-36.
120. Takagi S.F. Human Olfaction. 1989;University Tokyo Press, Tokyo.
121. Tareilus E., Noe J., Breer H. Calcium signals in olfactory neurons. Biochim. Biophys. Acta. 1269:1995;129-138.
122. Touhara K., Sengoku S., Inaki K. et al. Functional identification and reconstitution of an odorant receptor in single olfactory neurons. Proc. Natl. Acad. Sci. USA. 96:1999;4040-4045.
123. Vassar R., Chao S.K., Sitcheran R., Nunez J.M., Vosshall L.B., Axel R. Topographic organization of sensory projections to the olfactory bulb. Cell. 79:1994;981-991.
124. Vassar R., Ngai J., Axel R. Spatial segregation of odorant receptor expression in the mammalian olfactory epithelium. Cell. 74:1993;309-318.
125. Verma A., Hirsch D.J., Glatt C.E., Ronnett G.V., Snyder S.H. Carbon monoxide: a putative neural messenger. Science. 259:1993;381-384.
126. Wang F., Nemes A., Mendelsohn M., Axel R. Odorant receptors govern the formation of a precise topographic map. Cell. 93:1998;47-60.
127. Wang H.W., Wysocki C.J., Gold G.H. Induction of olfactory receptor sensitivity in mice. Science. 260:1993;998-1000.
128. Wei J., Wayman G., Storm D.R. Phosphorylation and inhibition of type III adenylyl cyclase by calmodulin-dependent protein kinase II in vivo. J. Biol. Chem. 271:1996;24231-24235.
129. Yan C., Zhao A.Z., Bentley J.K., Beavo J.A. The calmodulin-dependent phosphodiesterase gene PDE1C encodes several functionally different splice variants in a tissue-specific manner. J. Biol. Chem. 271:1996;25699-25706.
130. Yan C., Zhao A.Z., Bentley J.K., Loughney K., Ferguson K., Beavo J.A. Molecular cloning and characterization of a calmodulin-dependent phosphodiesterase enriched in olfactory sensory neurons. Proc. Natl. Acad. Sci. USA. 92:1995;9677-9681.
131. Yee K.K., Costanzo R.M. Changes in odor quality discrimination following recovery from olfactory nerve transection. Chem. Senses. 23:1998;513-519.
132. Youngentob S.L., Margolis F.L. OMP gene deletion causes an elevation in behavioral threshold sensitivity. Neuroreport. 10:1999;15-19.
133. Zhainazarov A.B., Ache B.W. Odor-induced currents in Xenopus olfactory receptor cells measured with perforated-patch recording. J. Neurophysiol. 74:1995;479-483.
134. Zhao H., Ivic L., Otaki J.M., Hashimoto M., Mikoshiba K., Firestein S. Functional expression of a mammalian odorant receptor. Science. 279:1998;237-242.
135. Zufall F., Leinders-Zufall T. Identification of a long-lasting form of odor adaptation that depends on the carbon monoxide/cGMP second-messenger system. J. Neurosci. 17:1997;2703-2712.
136. Zufall F., Shepherd G.M., Barnstable C.J. Cyclic nucleotide gated channels as regulators of CNS development and plasticity. Curr. Opin. Neurobiol. 7:1997;404-412.