Three structurally similar odorants trigger distinct signaling pathways in a mouse olfactory neuron

Neuroscience

Volumn 275, Issue , 2014, Pages 194-210

  Yu, Y ^a,c   Boyer, N P ^b,d   Zhang, C ^a  

^a Illinois Institute of Technology   (United States)

^b MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Adenylate cyclase; Calcium imaging; Olfactory neuron; Olfactory receptor; Phospholipase C; Sensory transduction

Indexed keywords

1 STEAROYL 2 ARACHIDONOYL SN GLYCEROL; 1 [[6 (3 METHOXYESTRA 1,3,5(10) TRIEN 17BETA YL)AMINO]HEXYL] 1H PYRROLE 2,5 DIONE; 1 [[6 (3 METHOXYESTRA 1,3,5(10) TRIEN 17BETA YL)AMINO]HEXYL] 2,5 PYRROLIDINEDIONE; 2 AMINOETHOXYDIPHENYLBORANE; 2 HEPTANONE; 2 MORPHOLINO 8 PHENYLCHROMONE; 4 HEPTENAL; 8 BROMINE CYCLIC AMP; 9 (TETRAHYDRO 2 FURYL)ADENINE; CHELERYTHRINE CHLORIDE; FLUFENAMIC ACID; G PROTEIN COUPLED RECEPTOR; H 8 DIHYDROCHLORIDE; HEPTYL ALDEHYDE; LIGAND; N (2 PHENYLCYCLOPENTYL)AZACYCLOTRIDECAN 2 IMINE; NEOMYCIN; PHOSPHOLIPASE C; REAGENT; RUTHENIUM RED; UNCLASSIFIED DRUG; 2-HEPTANONE; CALCIUM; KETONE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; EXTRACELLULAR CALCIUM; MOLECULAR IMAGING; MOUSE; NONHUMAN; OLFACTORY EPITHELIUM; OLFACTORY RECEPTOR; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; SIGNAL TRANSDUCTION; STRUCTURE ACTIVITY RELATION; ANIMAL; DRUG EFFECTS; METABOLISM; ODOR; OLFACTORY SYSTEM; PHYSIOLOGY;

ANIMALS; CALCIUM; KETONES; MICE; ODORS; OLFACTORY PATHWAYS; OLFACTORY RECEPTOR NEURONS; SIGNAL TRANSDUCTION; SMELL;

EID: 84903551274     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2014.05.063     Document Type: Article

References (96)

1. Ambrosio M., Zurn A., Lohse M.J. Sensing G protein-coupled receptor activation. Neuropharmacology 2011, 60:45-51.
2. Araneda R.C., Kini A.D., Firestein S. The molecular receptive range of an odorant receptor. Nat Neurosci 2000, 3:1248-1255.
3. Arias-Montano J.A., Floran B., Floran L., Aceves J., Young J.M. Dopamine D(1) receptor facilitation of depolarization-induced release of gamma-amino-butyric acid in rat striatum is mediated by the cAMP/PKA pathway and involves P/Q-type calcium channels. Synapse 2007, 61:310-319.
4. olf are anosmic. Neuron 1998, 20:69-81.
5. Berridge M.J. Neuronal calcium signaling. Neuron 1998, 21:13-26.
6. Bird G.S., Aziz O., Lievremont J.P., Wedel B.J., Trebak M., Vazquez G., Putney J.W. Mechanisms of phospholipase C-regulated calcium entry. Curr Mol Med 2004, 4:291-301.
7. Bobkov Y.V., Ache B.W. Pharmacological properties and functional role of a TRP-related ion channel in lobster olfactory receptor neurons. J Neurophysiol 2005, 93:1372-1380.
8. - currents in isolated mouse olfactory sensory neurons. J Neurophysiol 2007, 98:153-160.
9. 2+ release. FASEB J 2002, 16:1145-1150.
10. Bozza T., Feinstein P., Zheng C., Mombaerts P. Odorant receptor expression defines functional units in the mouse olfactory system. J Neurosci 2002, 22:3033-3043.
11. Brady J.D., Rich E.D., Martens J.R., Karpen J.W., Varnum M.D., Brown R.L. Interplay between PIP3 and calmodulin regulation of olfactory cyclic nucleotide-gated channels. Proc Natl Acad Sci USA 2006, 103:15635-15640.
12. 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 1996, 17:681-693.
13. Buck L.B. The molecular architecture of odor and pheromone sensing in mammals. Cell 2000, 100:611-618.
14. Buck L.B. Unraveling the sense of smell (Nobel lecture). Angew Chem Int Ed Engl 2005, 44:6128-6140.
15. Buck L.B. Olfactory receptors and odor coding in mammals. Nutr Rev 2004, 62:S184-S188.
16. Chess A., Simon I., Cedar H., Axel R. Allelic inactivation regulates olfactory receptor gene expression. Cell 1994, 78:823-834.
17. de Groot T., Lee K., Langeslag M., Xi Q., Jalink K., Bindels R.J., Hoenderop J.G. Parathyroid hormone activates TRPV5 via PKA-dependent phosphorylation. J Am Soc Nephrol 2009, 20:1693-1704.
18. Delmas P., Crest M., Brown D.A. Functional organization of PLC signaling microdomains in neurons. Trends Neurosci 2004, 27:41-47.
19. Elsaesser R., Montani G., Tirindelli R., Paysan J. Phosphatidyl-inositide signalling proteins in a novel class of sensory cells in the mammalian olfactory epithelium. Eur J Neurosci 2005, 21:2692-2700.
20. Erb L., Liao Z., Seye C.I., Weisman G.A. P2 receptors: intracellular signaling. Pflugers Arch 2006, 452:552-562.
21. Fadool D.A., Ache B.W. Plasma membrane inositol 1,4,5-trisphosphate-activated channels mediate signal transduction in lobster olfactory receptor neurons. Neuron 1992, 9:907-918.
22. Ferre S., Casado V., Devi L.A., Filizola M., Jockers R., Lohse M.J., Milligan G., Pin J.P., Guitart X. G protein-coupled receptor oligomerization revisited: functional and pharmacological perspectives. Pharmacol Rev 2014, 66:413-434.
23. Firestein S., Picco C., Menini A. The relation between stimulus and response in olfactory receptor cells of the tiger salamander. J Physiol 1993, 468:1-10.
24. Fischer H., Illek B., Sachs L., Finkbeiner W.E., Widdicombe J.H. CFTR and calcium-activated chloride channels in primary cultures of human airway gland cells of serous or mucous phenotype. Am J Physiol Lung Cell Mol Physiol 2010, 299:L585-L594.
25. Gabev E., Kasianowicz J., Abbott T., McLaughlin S. Binding of neomycin to phosphatidylinositol 4,5-bisphosphate (PIP2). Biochim Biophys Acta 1989, 979:105-112.
26. George S.R., O'Dowd B.F., Lee S.P. G-protein-coupled receptor oligomerization and its potential for drug discovery. Nat Rev Drug Discov 2002, 1:808-820.
27. Hagiwara M., Inagaki M., Hidaka H. Specific binding of a novel compound, N-[2-(methylamino)ethyl]-5-isoquinolinesulfonamide (H-8) to the active site of cAMP-dependent protein kinase. Mol Pharmacol 1987, 31:523-528.
28. Hara T.J. Mechanisms of olfaction. Fish chemoreception 1992, 150-170. Chapman and Hall, New York. T.J. Hara (Ed.).
29. Hatt H., Ache B.W. Cyclic nucleotide- and inositol phosphate-gated ion channels in lobster olfactory receptor neurons. Proc Natl Acad Sci USA 1994, 91:6264-6268.
30. Hegg C.C., Greenwood D., Huang W., Han P., Lucero M.T. Activation of purinergic receptor subtypes modulates odor sensitivity. J Neurosci 2003, 23:8291-8301.
31. Hegg C.C., Jia C., Chick W.S., Restrepo D., Hansen A. Microvillous cells expressing IP3 receptor type 3 in the olfactory epithelium of mice. Eur J Neurosci 2010, 32:1632-1645.
32. 2+ channel Ca(V)1.2 by PKA rekindles excitement. Sci Signal 2010, 3:e33.
33. Herbert J.M., Augereau J.M., Gleye J., Maffrand J.P. Chelerythrine is a potent and specific inhibitor of protein kinase C. Biochem Biophys Res Commun 1990, 172:993-999.
34. Hermans E. Biochemical and pharmacological control of the multiplicity of coupling at G-protein-coupled receptors. Pharmacol Ther 2003, 99:25-44.
35. Hidaka H., Inagaki M., Kawamoto S., Sasaki Y. Isoquinolinesulfonamides, novel and potent inhibitors of cyclic nucleotide dependent protein kinase and protein kinase C. Biochemistry 1984, 23:5036-5041.
36. Jeske N.A., Diogenes A., Ruparel N.B., Fehrenbacher J.C., Henry M., Akopian A.N., Hargreaves K.M. A-kinase anchoring protein mediates TRPV1 thermal hyperalgesia through PKA phosphorylation of TRPV1. Pain 2008, 138:604-616.
37. Kajiya K., Inaki K., Tanaka M., Haga T., Kataoka H., Touhara K. Molecular bases of odor discrimination: reconstitution of olfactory receptors that recognize overlapping sets of odorants. J Neurosci 2001, 21:6018-6025.
38. Kang J.S., Caprio J. Electro-olfactogram and multiunit olfactory receptor responses to complex mixtures of amino acids in the channel catfish, Ictalurus punctatus. J Gen Physiol 1991, 98:699-721.
39. Kato A., Touhara K. Mammalian olfactory receptors: pharmacology, G protein coupling and desensitization. Cell Mol Life Sci 2009, 66:3743-3753.
40. Khan M., Vaes E., Mombaerts P. Regulation of the probability of mouse odorant receptor gene choice. Cell 2011, 147:907-921.
41. Lin W., Arellano J., Slotnick B., Restrepo D. Odors detected by mice deficient in cyclic nucleotide-gated channel subunit A2 stimulate the main olfactory system. J Neurosci 2004, 24:3703-3710.
42. Lin W., Margolskee R., Donnert G., Hell S.W., Restrepo D. Olfactory neurons expressing transient receptor potential channel M5 (TRPM5) are involved in sensing semiochemicals. Proc Natl Acad Sci USA 2007, 104:2471-2476.
43. Lin W., Ogura T., Margolskee R.F., Finger T.E., Restrepo D. TRPM5-expressing solitary chemosensory cells respond to odorous irritants. J Neurophysiol 2008, 99:1451-1460.
44. Liu X., Ambudkar I.S. Characteristics of a store-operated calcium-permeable channel: sarcoendoplasmic reticulum calcium pump function controls channel gating. J Biol Chem 2001, 276:29891-29898.
45. Lowe G., Gold G.H. Nonlinear amplification by calcium-dependent chloride channels in olfactory receptor cells. Nature 1993, 366:283-286.
46. Lucas P., Ukhanov K., Leinders-Zufall T., Zufall F. A diacylglycerol-gated cation channel in vomeronasal neuron dendrites is impaired in TRPC2 mutant mice: mechanism of pheromone transduction. Neuron 2003, 40:551-561.
47. Ma M., Shepherd G.M. Functional mosaic organization of mouse olfactory receptor neurons. Proc Natl Acad Sci USA 2000, 97:12869-12874.
48. Maggio R., Novi F., Scarselli M., Corsini G.U. The impact of G-protein-coupled receptor hetero-oligomerization on function and pharmacology. FEBS J 2005, 272:2939-2946.
49. Malnic B., Hirono J., Sato T., Buck L.B. Combinatorial receptor codes for odors. Cell 1999, 96:713-723.
50. Maue R.A., Dionne V.E. Patch-clamp studies of isolated mouse olfactory receptor neurons. J Gen Physiol 1987, 90:95-125.
51. 2+ entry in pulmonary artery smooth muscle cells. Cell Calcium 2009, 46:99-106.
52. Miyamoto T., Restrepo D., Teeter J.H. Voltage-dependent and odorant-regulated currents in isolated olfactory receptor neurons of the channel catfish. J Gen Physiol 1992, 99:505-529.
53. 2+ influx through TRPC3. Neurochem Int 2010, 57:923-934.
54. Mombaerts P. Odorant receptor gene choice in olfactory sensory neurons: the one receptor-one neuron hypothesis revisited. Curr Opin Neurobiol 2004, 14:31-36.
55. Mombaerts P. Axonal wiring in the mouse olfactory system. Annu Rev Cell Dev Biol 2006, 22:713-737.
56. 2+ influx through TRPM2 channels in rat dorsal root ganglion neurons activated by ADP-ribose and rotenone. J Membr Biol 2011, 241:69-75.
57. Nelson G., Hoon M.A., Chandrashekar J., Zhang Y., Ryba N.J., Zuker C.S. Mammalian sweet taste receptors. Cell 2001, 106:381-390.
58. Neuhaus E.M., Gisselmann G., Zhang W., Dooley R., Stortkuhl K., Hatt H. Odorant receptor heterodimerization in the olfactory system of Drosophila melanogaster. Nat Neurosci 2005, 8:15-17.
59. 2+ increase in isolated frog taste cells. Eur J Neurosci 1998, 10:1376-1382.
60. Okada Y., Teeter J.H., Restrepo D. Inositol 1,4,5-trisphosphate-gated conductance in isolated rat olfactory neurons. J Neurophysiol 1994, 71:595-602.
61. Peppiatt C.M., Collins T.J., Mackenzie L., Conway S.J., Holmes A.B., Bootman M.D., Berridge M.J., Seo J.T., Roderick H.L. 2-Aminoethoxydiphenyl borate (2-APB) antagonises inositol 1,4,5-trisphosphate-induced calcium release, inhibits calcium pumps and has a use-dependent and slowly reversible action on store-operated calcium entry channels. Cell Calcium 2003, 34:97-108.
62. Pian P., Bucchi A., Robinson R.B., Siegelbaum S.A. Regulation of gating and rundown of HCN hyperpolarization-activated channels by exogenous and endogenous PIP2. J Gen Physiol 2006, 128:593-604.
63. i. Proc Natl Acad Sci USA 2003, 100:15166-15171.
64. Rawson N.E., Eberwine J., Dotson R., Jackson J., Ulrich P., Restrepo D. Expression of mRNAs encoding for two different olfactory receptors in a subset of olfactory receptor neurons. J Neurochem 2000, 75:185-195.
65. Reisert J., Matthews H.R. Response properties of isolated mouse olfactory receptor cells. J Physiol 2001, 530:113-122.
66. Restrepo D., Miyamoto T., Bryant B.P., Teeter J.H. Odor stimuli trigger influx of calcium into olfactory neurons of the channel catfish. Science 1990, 249:1166-1168.
67. 2+ channels by lipids. Cell Calcium 2009, 45:589-601.
68. Rochais F., Vandecasteele G., Lefebvre F., Lugnier C., Lum H., Mazet J.L., Cooper D.M., Fischmeister R. Negative feedback exerted by cAMP-dependent protein kinase and cAMP phosphodiesterase on subsarcolemmal cAMP signals in intact cardiac myocytes: an in vivo study using adenovirus-mediated expression of CNG channels. J Biol Chem 2004, 279:52095-52105.
69. Rohacs T. Phosphoinositide regulation of non-canonical transient receptor potential channels. Cell Calcium 2009, 45:554-565.
70. Rohacs T., Thyagarajan B., Lukacs V. Phospholipase C mediated modulation of TRPV1 channels. Mol Neurobiol 2008, 37:153-163.
71. 2+ influx and glutamate release in rat cerebrocortical synaptosomes. Neurosci Lett 1994, 178:155-158.
72. Rosenbaum T, Simon SA (2007) TRPV1 receptors and signal transduction.
73. Sato Y., Miyasaka N., Yoshihara Y. Hierarchical regulation of odorant receptor gene choice and subsequent axonal projection of olfactory sensory neurons in zebrafish. J Neurosci 2007, 27:1606-1615.
74. Schild D., Restrepo D. Transduction mechanisms in vertebrate olfactory receptor cells. Physiol Rev 1998, 78:429-466.
75. Schleicher S., Boekhoff I., Arriza J., Lefkowitz R.J., Breer H. A β-adrenergic receptor kinase-like enzyme is involved in olfactory signal termination. Proc Natl Acad Sci USA 1993, 90:1420-1424.
76. Stokes A.J., Shimoda L.M., Koblan-Huberson M., Adra C.N., Turner H. A TRPV2-PKA signaling module for transduction of physical stimuli in mast cells. J Exp Med 2004, 200:137-147.
77. Sullivan S.L., Ressler K.J., Buck L.B. Odorant receptor diversity and patterned gene expression in the mammalian olfactory epithelium. Prog Clin Biol Res 1994, 390:75-84.
78. 2+ channel. Circ Res 2008, 102:1378-1388.
79. Ukhanov K., Corey E.A., Brunert D., Klasen K., Ache B.W. Inhibitory odorant signaling in mammalian olfactory receptor neurons. J Neurophysiol 2010, 103:1114-1122.
80. Urban JD, Clarke WP, von ZM, Nichols DE, Kobilka B, Weinstein H, Javitch JA, Roth BL, Christopoulos A, Sexton PM, Miller KJ, Spedding M, Mailman RB (2007) Functional selectivity and classical concepts of quantitative pharmacology. J Pharmacol Exp Ther 320:1-13.
81. Vassar R., Ngai J., Axel R. Spatial segregation of odorant receptor expression in the mammalian olfactory epithelium. Cell 1993, 74:309-318.
82. Vickers J.D. U73122 affects the equilibria between the phosphoinositides as well as phospholipase C activity in unstimulated and thrombin-stimulated human and rabbit platelets. J Pharmacol Exp Ther 1993, 266:1156-1163.
83. Vlahos C.J., Matter W.F., Hui K.Y., Brown R.F. A specific inhibitor of phosphatidylinositol 3-kinase, 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran-4-one (LY294002). J Biol Chem 1994, 269:5241-5248.
84. Wachowiak M., Cohen L.B. Representation of odorants by receptor neuron input to the mouse olfactory bulb. Neuron 2001, 32:723-735.
85. Wade F., Espagne A., Persuy M.A., Vidic J., Monnerie R., Merola F., Pajot-Augy E., Sanz G. Relationship between homo-oligomerization of a mammalian olfactory receptor and its activation state demonstrated by bioluminescence resonance energy transfer. J Biol Chem 2011, 286:15252-15259.
86. Wetzel C.H., Spehr M., Hatt H. Phosphorylation of voltage-gated ion channels in rat olfactory receptor neurons. Eur J Neurosci 2001, 14:1056-1064.
87. Wong S.K. G protein selectivity is regulated by multiple intracellular regions of GPCRs. Neurosignals 2003, 12:1-12.
88. Wong S.T., Trinh K., Hacker B., Chan G.C., Lowe G., Gaggar A., Xia Z., Gold G.H., Storm D.R. Disruption of the type III adenylyl cyclase gene leads to peripheral and behavioral anosmia in transgenic mice. Neuron 2000, 27:487-497.
89. Woo A.Y., Wang T.B., Zeng X., Zhu W., Abernethy D.R., Wainer I.W., Xiao R.P. Stereochemistry of an agonist determines coupling preference of beta2-adrenoceptor to different G proteins in cardiomyocytes. Mol Pharmacol 2009, 75:158-165.
90. Ying S.W., Tibbs G.R., Picollo A., Abbas S.Y., Sanford R.L., Accardi A., Hofmann F., Ludwig A., Goldstein P.A. PIP2-mediated HCN3 channel gating is crucial for rhythmic burst firing in thalamic intergeniculate leaflet neurons. J Neurosci 2011, 31:10412-10423.
91. Yu Y., Zhang C. Purinergic signaling negatively regulates activity of an olfactory receptor in an odorant-dependent manner. Neuroscience 2014, XXX. XXX-XXX.
92. Zhainazarov A.B., Spehr M., Wetzel C.H., Hatt H., Ache B.W. Modulation of the olfactory CNG channel by Ptdlns(3,4,5)P3. J Membr Biol 2004, 201:51-57.
93. Zhang C. Gap junctions in olfactory neurons modulate olfactory sensitivity. BMC Neurosci 2010, 11:108.
94. Zhang C., Hara T.J. Lake char (Salvelinus namaycush) olfactory neurons are highly sensitive and specific to bile acids. J Comp Physiol A: Neuroethol Sens Neural Behav Physiol 2009, 195:203-215.
95. Zhao H., Reed R.R. X inactivation of the OCNC1 channel gene reveals a role for activity-dependent competition in the olfactory system. Cell 2001, 104:651-660.
96. Zufall F., Munger S.D. Receptor guanylyl cyclases in mammalian olfactory function. Mol Cell Biochem 2010, 334:191-197.