Identification of a novel Gnao-mediated alternate olfactory signaling pathway in murine OSNs

Frontiers in Cellular Neuroscience

Volumn 10, Issue MAR2016, 2016, Pages

  Scholz, Paul ^a   Mohrhardt, Julia ^a   Jansen, Fabian ^a   Kalbe, Benjamin ^a   Haering, Claudia ^a   Klasen, Katharina ^a   Hatt, Hanns ^a   Osterloh, Sabrina ^a  

^a RUHR UNIVERSITY BOCHUM   (Germany)

Author keywords

Electrophysiology; GPCR signal transduction; Olfactory pathways; Olfactory receptor neurons; Patch clamp techniques

Indexed keywords

ADENYLATE CYCLASE; CALCIUM ACTIVATED CHLORIDE CHANNEL; CALCIUM ION; CYCLIC AMP; CYCLIC NUCLEOTIDE GATED CHANNEL; PHOSPHATIDYLINOSITOL 3 KINASE;

ADOLESCENT; ADULT; ANIMAL TISSUE; ARTICLE; CALCIUM TRANSPORT; CONTROLLED STUDY; ELECTROPHYSIOLOGICAL PROCEDURES; FEMALE; INTRACELLULAR SIGNALING; MALE; NONHUMAN; OLFACTORY RECEPTOR; PROTEIN MICROARRAY; REAL TIME POLYMERASE CHAIN REACTION; SENSORY NERVE CELL; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

EID: 84963756132     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2016.00063     Document Type: Article

References (46)

1. Ache, B. W. (2010). Odorant-specific modes of signaling in mammalian olfaction.Chem. Senses 35, 533-539. doi: 10.1093/chemse/bjq045
2. Bakalyar, H., and Reed, R. (1990). Identification of a specialized adenylyl cyclase that may mediate odorant detection. Science 250, 1403-1406. doi: 10.1126/science.2255909
3. Baud, O., Etter, S., Spreafico, M., Bordoli, L., Schwede, T., Vogel, H., et al. (2011). The mouse eugenol odorant receptor: structural and functional plasticity of a broadly tuned odorant binding pocket. Biochemistry 50, 843-853. doi: 10.1021/bi1017396
4. Belluscio, L., Gold, G. H., Nemes, A., and Axel, R. (1998). Mice deficient in G(olf) are anosmic. Neuron 20, 69-81. doi: 10.1016/S0896-6273(00)80435-3
5. Breer, H., Boekhoff, I., and Tareilus, E. (1990). Rapid kinetics of second messenger formation in olfactory transduction. Nature 345, 65-68. doi: 10.1038/345065a0
6. Brunert, D., Klasen, K., Corey, E. A., and Ache, B. W. (2010). PI3Kgamma-dependent signaling in mouse olfactory receptor neurons. Chem. Senses 35, 301-308. doi: 10.1093/chemse/bjq020
7. Buck, L., and Axel, R. (1991). A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 65, 175-187. doi: 10.1016/0092-8674(91)90418-X
8. Burns, D. L. (1988). Subunit structure and enzymic activity of pertussis toxin.Microbiol. Sci. 5, 285-287.
9. Calvert, P. D., Krasnoperova, N. V., Lyubarsky, A. L., Isayama, T., Nicoló, M., Kosaras, B., et al. (2000). Phototransduction in transgenic mice after targeted deletion of the rod transducin α-subunit. Proc. Natl. Acad. Sci. U.S.A. 97, 13913-13918. doi: 10.1073/pnas.250478897
10. Chamero, P., Katsoulidou, V., Hendrix, P., Bufe, B., Roberts, R., Matsunami, H., et al. (2011). G protein Gαo is essential for vomeronasal function and aggressive behavior in mice. Proc. Natl. Acad. Sci. U.S.A. 108, 12898-12903. doi: 10.1073/pnas.1107770108
11. Chidekel, A. S., Friedman, J. E., and Haddad, G. G. (1997). Anoxia-induced neuronal injury: role of Na+ entry and Na+-dependent transport. Exp. Neurol. 146, 403-413. doi: 10.1006/exnr.1997.6544
12. Dhallan, R. S., Yau, K. W., Schrader, K. A., and Reed, R. R. (1990). Primary structure and functional expression of a cyclic nucleotide-activated channel from olfactory neurons. Nature 347, 184-187. doi: 10.1038/347184a0
13. Frings, S., Lynch, J. W., and Lindemann, B. (1992). Properties of cyclic nucleotide-gated channels mediating olfactory transduction. Activation, selectivity, and blockage. J. Gen. Physiol. 100, 45-67. doi: 10.1085/jgp.100.1.45
14. González-Maeso, J. C., and Sealfon, S. (2012). Functional selectivity in GPCR heterocomplexes. Mini Rev. Med. Chem. 12, 851-855. doi: 10.2174/138955712800959152
15. Gurwitz, D., Haring, R., Heldman, E., Fraser, C. M., Manor, D., and Fisher, A. (1994). Discrete activation of transduction pathways associated with acetylcholine m1 receptor by several muscarinic ligands. Eur. J. Pharmacol. 267, 21-31. doi: 10.1016/0922-4106(94)90220-8
16. Jones, D. T., and Reed, R. R. (1989). Golf: an olfactory neuron specific-G protein involved in odorant signal transduction. Science 244, 790-795. doi: 10.1126/science.2499043
17. Juilfs, D. M., Fülle, H. J., Zhao, A. Z., Houslay, M. D., Garbers, D. L., and Beavo, J. A. (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. U.S.A. 94, 3388-3395. doi: 10.1073/pnas.94.7.3388
18. Katada, S., Hirokawa, T., Oka, Y., Suwa, M., and 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. doi: 10.1523/JNEUROSCI.4723-04.2005
19. Kato, A., Katada, S., and Touhara, K. (2008). Amino acids involved in conformational dynamics and G protein coupling of an odorant receptor: targeting gain-of-function mutation. J. Neurochem. 107, 1261-1270. doi: 10.1111/j.1471-4159.2008.05693.x
20. Kenakin, T. (1995). Agonist-receptor efficacy. II. Agonist trafficking of receptor signals. Trends Pharmacol. Sci. 16, 232-238. doi: 10.1016/S0165-6147(00)89032-X
21. Klasen, K., Corey, E. A., Kuck, F., Wetzel, C. H., Hatt, H., and Ache, B. W. (2010). Odorant-stimulated phosphoinositide signaling in mammalian olfactory receptor neurons. Cell. Signal. 22, 150-157. doi: 10.1016/j.cellsig.2009.09.026
22. Kleene, S. J., and Gesteland, R. C. (1991). Calcium-activated chloride conductance in frog olfactory cilia. J. Neurosci. 11, 3624-3629.
23. Knauf, P. A., and Mann, N. A. (1984). Use of niflumic acid to determine the nature of the asymmetry of the human erythrocyte anion exchange system. J. Gen. Physiol. 83, 703-725. doi: 10.1085/jgp.83.5.703
24. Liberles, S. D., and Buck, L. B. (2006). A second class of chemosensory receptors in the olfactory epithelium. Nature 442, 645-650. doi: 10.1038/nature05066
25. Mombaerts, P. (2004). Genes and ligands for odorant, vomeronasal and taste receptors. Nat. Rev. Neurosci. 5, 263-278. doi: 10.1038/nrn1365
26. Offermanns, S. (2003). G-proteins as transducers in transmembrane signalling. Prog. Biophys. Mol. Biol. 83, 101-130. doi: 10.1016/S0079-6107(03)00052-X
27. Oka, Y., Katada, S., Omura, M., Suwa, M., Yoshihara, Y., and Touhara, K. (2006). Odorant receptor map in the mouse olfactory bulb: in vivo sensitivity and specificity of receptor-defined glomeruli. Neuron 52, 857-869. doi: 10.1016/j.neuron.2006.10.019
28. Oka, Y., Omura, M., Kataoka, H., and Touhara, K. (2004). Olfactory receptor antagonism between odorants. EMBO J. 23, 120-126. doi: 10.1038/sj.emboj.7600032
29. Pace, U., and Lancet, D. (1986). Olfactory GTP-binding protein: signal-transducing polypeptide of vertebrate chemosensory neurons. Proc. Natl. Acad. Sci. U.S.A. 83, 4947-4951. doi: 10.1073/pnas.83.13.4947
30. Powis, G., Seewald, M. J., Gratas, C., Melder, D., Riebow, J., and Modest, E. J. (1992). Selective inhibition of phosphatidylinositol phospholipase C by cytotoxic ether lipid analogues. Cancer Res. 52, 2835-2840.
31. Rasche, S., Toetter, B., Adler, J., Tschapek, A., Doerner, J. F., Kurtenbach, S., et al. (2010). Tmem16b is specifically expressed in the cilia of olfactory sensory neurons.Chem. Senses 35, 239-245. doi: 10.1093/chemse/bjq007
32. Reisert, J., Bauer, P. J., Yau, K.-W., and Frings, S. (2003). The Ca-activated Cl channel and its control in rat olfactory receptor neurons. J. Gen. Physiol. 122, 349-363. doi: 10.1085/jgp.200308888
33. Ritter, S. L., and Hall, R. A. (2009). Fine-tuning of GPCR activity by receptor-interacting proteins. Nat. Rev. Mol. Cell Biol. 10, 819-830. doi: 10.1038/nrm2803
34. Rose, C. R., and Ransom, B. R. (1997). Regulation of intracellular sodium in cultured rat hippocampal neurones. J. Physiol. 499 (Pt 3), 573-587. doi: 10.1113/jphysiol.1997.sp021951
35. Scholz, P., Kalbe, B., Jansen, F., Altmueller, J., Becker, C., Mohrhardt, J., et al. (2016). Transcriptome analysis of murine olfactory sensory neurons during development using single cell RNA-Seq. Chem. Senses. doi: 10.1093/chemse/bjw003. [Epub ahead of print].
36. Simasko, S. M. (1994). A background sodium conductance is necessary for spontaneous depolarizations in rat pituitary cell line GH3. Am. J. Physiol. 266, C709-C719.
37. Spehr, M., Wetzel, C. H., Hatt, H., and Ache, B. W. (2002). 3-Phosphoinositides Modulate Cyclic Nucleotide Signaling in Olfactory Receptor Neurons. Neuron 33, 731-739. doi: 10.1016/S0896-6273(02)00610-4
38. Stephan, A. B., Shum, E. Y., Hirsh, S., Cygnar, K. D., Reisert, J., and Zhao, H. (2009). ANO2 is the cilial calcium-activated chloride channel that may mediate olfactory amplification. Proc. Natl. Acad. Sci. U.S.A. 106, 11776-11781. doi: 10.1073/pnas.0903304106
39. Tanaka, M., Treloar, H., Kalb, R. G., Greer, C. A., and Strittmatter, S. M. (1999). G(o) protein-dependent survival of primary accessory olfactory neurons. Proc. Natl. Acad. Sci. U.S.A. 96, 14106-14111. doi: 10.1073/pnas.96.24.14106
40. Ukhanov, K., Bobkov, Y., Corey, E. A., and Ache, B. W. (2014). Ligand-selective activation of heterologously-expressed mammalian olfactory receptor. Cell Calcium56, 245-256. doi: 10.1016/j.ceca.2014.07.012
41. Ukhanov, K., Brunert, D., Corey, E. A., and Ache, B. W. (2011). Phosphoinositide 3-kinase-dependent antagonism in Mammalian olfactory receptor neurons. J. Neurosci.31, 273-280. doi: 10.1523/JNEUROSCI.3698-10.2011
42. Ukhanov, K., Corey, E. A., Brunert, D., Klasen, K., and Ache, B. W. (2010). Inhibitory odorant signaling in Mammalian olfactory receptor neurons. J. Neurophysiol. 103, 1114-1122. doi: 10.1152/jn.00980.2009
43. Vlahos, C. J., Matter, W. F., Hui, K. Y., and Brown, R. F. (1994). A specific inhibitor of phosphatidylinositol 3-kinase, 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran-4-one (LY294002). J. Biol. Chem. 269, 5241-5248.
44. Wong, G. T., Gannon, K. S., and Margolskee, R. F. (1996). Transduction of bitter and sweet taste by gustducin. Nature 381, 796-800. doi: 10.1038/381796a0
45. Yu, Y., Boyer, N. P., and Zhang, C. (2014). Three structurally similar odorants trigger distinct signaling pathways in a mouse olfactory neuron. Neuroscience 275, 194-210. doi: 10.1016/j.neuroscience.2014.05.063
46. Zocher, M., Fung, J. J., Kobilka, B. K., and Müller, D. J. (2012). Ligand-specific interactions modulate kinetic, energetic, and mechanical properties of the human β2 adrenergic receptor. Structure 20, 1391-1402. doi: 10.1016/j.str.2012.05.010