Expression profile of G-protein βγ subunit gene transcripts in the mouse olfactory sensory epithelia

Frontiers in Cellular Neuroscience

Volumn , Issue MAY, 2013, Pages

  Sathyanesan, Aaron ^a   Feijoo, Adrian A ^a   Mehta, Saloni T ^a   Nimarko, Akua F ^a   Lin, Weihong ^a  

^a UNIVERSITY OF MARYLAND BALTIMORE COUNTY   (United States)

Author keywords

Olfactory sensory neurons; Phospholipase C; Postnatal development; Sensory transduction; TRPM5; Vomeronasal

Indexed keywords

GUANINE NUCLEOTIDE BINDING PROTEIN BETA SUBUNIT; GUANINE NUCLEOTIDE BINDING PROTEIN GAMMA SUBUNIT; RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BASAL CELL; BASEMENT MEMBRANE; BRAIN NERVE CELL; CELL POPULATION; CONTROLLED STUDY; DEVELOPMENTAL STAGE; FEMALE; GENE EXPRESSION PROFILING; GENE IDENTIFICATION; GENETIC TRANSCRIPTION; IN VITRO STUDY; MALE; MOUSE; NEUROEPITHELIUM; NONHUMAN; OLFACTORY EPITHELIUM; OLFACTORY SYSTEM; PERINATAL PERIOD; POSTNATAL DEVELOPMENT; PROTEIN ANALYSIS; SENSORY NERVE CELL; TRANSIENT EXPRESSION; VOMERONASAL ORGAN;

EID: 84878266604     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2013.00084     Document Type: Article

References (65)

1. Bakalyar, H.A., and Reed, R.R. (1990). Identification of a specialized adenylyl cyclase that may mediate odorant detection. Science 250, 1403-1406.
2. Belluscio, L., Gold, G.H., Nemes, A., and Axel, R. (1998). Mice deficient in G(olf) are anosmic. Neuron 20, 69-81.
3. Berghard, A., and Buck, L.B. (1996). Sensory transduction in vomeronasal neurons: evidence for G alpha o, G alpha i2, and adenylyl cyclase II as major components of a pheromone signaling cascade. J Neurosci 16, 909-918.
4. Bezencon, C., Le Coutre, J., and Damak, S. (2007). Taste-signaling proteins are coexpressed in solitary intestinal epithelial cells. Chem Senses 32, 41-49.
5. Bruch, R.C., Medler, K.F., Tran, H.N., and Hamlin, J.A. (1997). G-protein beta gamma subunit genes expressed in olfactory receptor neurons. Chem Senses 22, 587-592.
6. Chamero, P., Katsoulidou, V., Hendrix, P., Bufe, B., Roberts, R., Matsunami, H., Abramowitz, J., Birnbaumer, L., Zufall, F., and Leinders-Zufall, T. (2011). G protein G(alpha)o is essential for vomeronasal function and aggressive behavior in mice. Proc Natl Acad Sci U S A 108, 12898-12903.
7. Chesler, A.T., Zou, D.J., Le Pichon, C.E., Peterlin, Z.A., Matthews, G.A., Pei, X., Miller, M.C., and Firestein, S. (2007). A G protein/cAMP signal cascade is required for axonal convergence into olfactory glomeruli. Proc Natl Acad Sci U S A 104, 1039-1044.
8. Dingus, J., Wells, C.A., Campbell, L., Cleator, J.H., Robinson, K., and Hildebrandt, J.D. (2005). G Protein betagamma dimer formation: Gbeta and Ggamma differentially determine efficiency of in vitro dimer formation. Biochemistry 44, 11882-11890.
9. Dupre, D.J., Robitaille, M., Rebois, R.V., and Hebert, T.E. (2009). The role of Gbetagamma subunits in the organization, assembly, and function of GPCR signaling complexes. Annu Rev Pharmacol Toxicol 49, 31-56.
10. Gotta, M., and Ahringer, J. (2001). Distinct roles for Galpha and Gbetagamma in regulating spindle position and orientation in Caenorhabditis elegans embryos. Nat Cell Biol 3, 297-300.
11. Halpern, M., Shapiro, L.S., and Jia, C. (1995). Differential localization of G proteins in the opossum vomeronasal system. Brain Res 677, 157-161.
12. Hoon, M.A., Adler, E., Lindemeier, J., Battey, J.F., Ryba, N.J., and Zuker, C.S. (1999). Putative mammalian taste receptors: a class of taste-specific GPCRs with distinct topographic selectivity. Cell 96, 541-551.
13. Huang, L., Max, M., Margolskee, R.F., Su, H., Masland, R.H., and Euler, T. (2003). G protein subunit G gamma 13 is coexpressed with G alpha o, G beta 3, and G beta 4 in retinal ON bipolar cells. J Comp Neurol 455, 1-10.
14. Huang, L., Shanker, Y.G., Dubauskaite, J., Zheng, J.Z., Yan, W., Rosenzweig, S., Spielman, A.I., Max, M., and Margolskee, R.F. (1999). Ggamma13 colocalizes with gustducin in taste receptor cells and mediates IP3 responses to bitter denatonium. Nat Neurosci 2, 1055-1062.
15. Imai, T., Suzuki, M., and Sakano, H. (2006). Odorant receptor-derived cAMP signals direct axonal targeting. Science 314, 657-661.
16. Ishii, T., Omura, M., and Mombaerts, P. (2004). Protocols for two-and three-color fluorescent RNA in situ hybridization of the main and accessory olfactory epithelia in mouse. J Neurocytol 33, 657-669.
17. Izumi, Y., Ohta, N., Itoh-Furuya, A., Fuse, N., and Matsuzaki, F. (2004). Differential functions of G protein and Baz-aPKC signaling pathways in Drosophila neuroblast asymmetric division. J Cell Biol 164, 729-738.
18. Jansen, G., Weinkove, D., and Plasterk, R.H. (2002). The G-protein gamma subunit gpc-1 of the nematode C.elegans is involved in taste adaptation. EMBO J 21, 986-994.
19. Jia, C., and Halpern, M. (1996). Subclasses of vomeronasal receptor neurons: differential expression of G proteins (Gi alpha 2 and G(o alpha)) and segregated projections to the accessory olfactory bulb. Brain Res 719, 117-128.
20. Jones, D.T., and Reed, R.R. (1989). Golf: an olfactory neuron specific-G protein involved in odorant signal transduction. Science 244, 790-795.
21. Keresztes, G., Martemyanov, K.A., Krispel, C.M., Mutai, H., Yoo, P.J., Maison, S.F., Burns, M.E., Arshavsky, V.Y., and Heller, S. (2004). Absence of the RGS9.Gbeta5 GTPase-activating complex in photoreceptors of the R9AP knockout mouse. J Biol Chem 279, 1581-1584.
22. Kerr, D.S., Von Dannecker, L.E., Davalos, M., Michaloski, J.S., and Malnic, B. (2008). Ric-8B interacts with G alpha olf and G gamma 13 and co-localizes with G alpha olf, G beta 1 and G gamma 13 in the cilia of olfactory sensory neurons. Mol Cell Neurosci 38, 341-348.
23. Kisselev, O., and Gautam, N. (1993). Specific interaction with rhodopsin is dependent on the gamma subunit type in a G protein. J Biol Chem 268, 24519-24522.
24. Kleuss, C., Scherubl, H., Hescheler, J., Schultz, G., and Wittig, B. (1993). Selectivity in signal transduction determined by gamma subunits of heterotrimeric G proteins. Science 259, 832-834.
25. Krasteva, G., Canning, B.J., Hartmann, P., Veres, T.Z., Papadakis, T., Muhlfeld, C., Schliecker, K., Tallini, Y.N., Braun, A., Hackstein, H., Baal, N., Weihe, E., Schutz, B., Kotlikoff, M., Ibanez-Tallon, I., and Kummer, W. (2011). Cholinergic chemosensory cells in the trachea regulate breathing. Proc Natl Acad Sci U S A 108, 9478-9483.
26. Kulaga, H.M., Leitch, C.C., Eichers, E.R., Badano, J.L., Lesemann, A., Hoskins, B.E., Lupski, J.R., Beales, P.L., Reed, R.R., and Katsanis, N. (2004). Loss of BBS proteins causes anosmia in humans and defects in olfactory cilia structure and function in the mouse. Nat Genet 36, 994-998.
27. Lehmann, D.M., Seneviratne, A.M., and Smrcka, A.V. (2008). Small molecule disruption of G protein beta gamma subunit signaling inhibits neutrophil chemotaxis and inflammation. Mol Pharmacol 73, 410-418.
28. Li, F., Ponissery-Saidu, S., Yee, K.K., Wang, H., Chen, M.L., Iguchi, N., Zhang, G., Jiang, P., Reisert, J., and Huang, L. (2013). Heterotrimeric g protein subunit ggamma13 is critical to olfaction. J Neurosci 33, 7975-7984.
29. Lin, W., Margolskee, R., Donnert, G., Hell, S.W., and 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, 2471-2476.
30. Lin, W., Ogura, T., Margolskee, R.F., Finger, T.E., and Restrepo, D. (2008). TRPM5-expressing solitary chemosensory cells respond to odorous irritants. J Neurophysiol 99, 1451-1460.
31. Liu, P., Shah, B.P., Croasdell, S., and Gilbertson, T.A. (2011). Transient receptor potential channel type M5 is essential for fat taste. J Neurosci 31, 8634-8642.
32. Liu, Z., Fenech, C., Cadiou, H., Grall, S., Tili, E., Laugerette, F., Wiencis, A., Grosmaitre, X., and Montmayeur, J.P. (2012). Identification of new binding partners of the chemosensory signaling protein Ggamma13 expressed in taste and olfactory sensory cells. Front Cell Neurosci 6, 26.
33. Livak, K.J., and Schmittgen, T.D. (2001). Analysis of relative gene expression data using realtime quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25, 402-408.
34. Luo, A.H., Cannon, E.H., Wekesa, K.S., Lyman, R.F., Vandenbergh, J.G., and Anholt, R.R. (2002). Impaired olfactory behavior in mice deficient in the alpha subunit of G(o). Brain Res 941, 62-71.
35. Malbon, C.C. (2005). G proteins in development. Nat Rev Mol Cell Biol 6, 689-701.
36. Menco, B.P., Tekula, F.D., Farbman, A.I., and Danho, W. (1994). Developmental expression of G-proteins and adenylyl cyclase in peripheral olfactory systems. Light microscopic and freeze-substitution electron microscopic immunocytochemistry. J Neurocytol 23, 708-727.
37. Munger, S.D., Leinders-Zufall, T., and Zufall, F. (2009). Subsystem organization of the mammalian sense of smell. Annu Rev Physiol 71, 115-140.
38. Neptune, E.R., and Bourne, H.R. (1997). Receptors induce chemotaxis by releasing the betagamma subunit of Gi, not by activating Gq or Gs. Proc Natl Acad Sci U S A 94, 14489-14494.
39. Nishiguchi, K.M., Sandberg, M.A., Kooijman, A.C., Martemyanov, K.A., Pott, J.W., Hagstrom, S.A., Arshavsky, V.Y., Berson, E.L., and Dryja, T.P. (2004). Defects in RGS9 or its anchor protein R9AP in patients with slow photoreceptor deactivation. Nature 427, 75-78.
40. Norgren, R.B., Jr., Gao, C., Ji, Y., and Fritzsch, B. (1995). Tangential migration of luteinizing hormone-releasing hormone (LHRH) neurons in the medial telencephalon in association with transient axons extending from the olfactory nerve. Neurosci Lett 202, 9-12.
41. Ogura, T., Krosnowski, K., Zhang, L., Bekkerman, M., and Lin, W. (2010). Chemoreception regulates chemical access to mouse vomeronasal organ: role of solitary chemosensory cells. PLoS One 5, e11924.
42. Ogura, T., Szebenyi, S.A., Krosnowski, K., Sathyanesan, A., Jackson, J., and Lin, W. (2011). Cholinergic microvillous cells in the mouse main olfactory epithelium and effect of acetylcholine on olfactory sensory neurons and supporting cells. J Neurophysiol 106, 1274-1287.
43. Oike, H., Wakamori, M., Mori, Y., Nakanishi, H., Taguchi, R., Misaka, T., Matsumoto, I., and Abe, K. (2006). Arachidonic acid can function as a signaling modulator by activating the TRPM5 cation channel in taste receptor cells. Biochim Biophys Acta 1761, 1078-1084.
44. Okae, H., and Iwakura, Y. (2010). Neural tube defects and impaired neural progenitor cell proliferation in Gbeta1-deficient mice. Dev Dyn 239, 1089-1101.
45. 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.
46. Peracino, B., Borleis, J., Jin, T., Westphal, M., Schwartz, J.M., Wu, L., Bracco, E., Gerisch, G., Devreotes, P., and Bozzaro, S. (1998). G protein beta subunit-null mutants are impaired in phagocytosis and chemotaxis due to inappropriate regulation of the actin cytoskeleton. J Cell Biol 141, 1529-1537.
47. Perez, C.A., Huang, L., Rong, M., Kozak, J.A., Preuss, A.K., Zhang, H., Max, M., and Margolskee, R.F. (2002). A transient receptor potential channel expressed in taste receptor cells. Nat Neurosci 5, 1169-1176.
48. Ren, X., Zhou, L., Terwilliger, R., Newton, S.S., and de Araujo, I.E. (2009). Sweet taste signaling functions as a hypothalamic glucose sensor. Front Integr Neurosci 3, 12.
49. Ruiz-Velasco, V., Ikeda, S.R., and Puhl, H.L. (2002). Cloning, tissue distribution, and functional expression of the human G protein beta 4-subunit. Physiol Genomics 8, 41-50.
50. Runnenburger, K., Breer, H., and Boekhoff, I. (2002). Selective G protein beta gamma-subunit compositions mediate phospholipase C activation in the vomeronasal organ. Eur J Cell Biol 81, 539-547.
51. Sathyanesan, A., Ogura, T., and Lin, W. (2012). Automated measurement of nerve fiber density using line intensity scan analysis. J Neurosci Methods 206, 165-175.
52. Schaefer, M., Petronczki, M., Dorner, D., Forte, M., and Knoblich, J.A. (2001). Heterotrimeric G proteins direct two modes of asymmetric cell division in the Drosophila nervous system. Cell 107, 183-194.
53. Smrcka, A.V. (2008). G protein betagamma subunits: central mediators of G protein-coupled receptor signaling. Cell Mol Life Sci 65, 2191-2214.
54. Stephens, L., Smrcka, A., Cooke, F.T., Jackson, T.R., Sternweis, P.C., and Hawkins, P.T. (1994). A novel phosphoinositide 3 kinase activity in myeloid-derived cells is activated by G protein beta gamma subunits. Cell 77, 83-93.
55. Sullivan, S.L., Bohm, S., Ressler, K.J., Horowitz, L.F., and Buck, L.B. (1995). Targetindependent pattern specification in the olfactory epithelium. Neuron 15, 779-789.
56. Wang, Q., Mullah, B., Hansen, C., Asundi, J., and Robishaw, J.D. (1997). Ribozyme-mediated suppression of the G protein gamma7 subunit suggests a role in hormone regulation of adenylylcyclase activity. J Biol Chem 272, 26040-26048.
57. Wang, Q., Mullah, B.K., and Robishaw, J.D. (1999). Ribozyme approach identifies a functional association between the G protein beta1gamma7 subunits in the beta-adrenergic receptor signaling pathway. J Biol Chem 274, 17365-17371.
58. Weiler, E., Mcculloch, M.A., and Farbman, A.I. (1999). Proliferation in the vomeronasal organ of the rat during postnatal development. Eur J Neurosci 11, 700-711.
59. Wekesa, K.S., and Anholt, R.R. (1999). Differential expression of G proteins in the mouse olfactory system. Brain Res 837, 117-126.
60. Welch, H.C., Coadwell, W.J., Ellson, C.D., Ferguson, G.J., Andrews, S.R., Erdjument-Bromage, H., Tempst, P., Hawkins, P.T., and Stephens, L.R. (2002). P-Rex1, a PtdIns(3,4,5)P3-and Gbetagamma-regulated guanine-nucleotide exchange factor for Rac. Cell 108, 809-821.
61. Yamada, K., Hirotsu, T., Matsuki, M., Kunitomo, H., and Iino, Y. (2009). GPC-1, a G protein gamma-subunit, regulates olfactory adaptation in Caenorhabditis elegans. Genetics 181, 1347-1357.
62. Yu, F., Cai, Y., Kaushik, R., Yang, X., and Chia, W. (2003). Distinct roles of Galphai and Gbeta13F subunits of the heterotrimeric G protein complex in the mediation of Drosophila neuroblast asymmetric divisions. J Cell Biol 162, 623-633.
63. Zhang, J.H., Pandey, M., Seigneur, E.M., Panicker, L.M., Koo, L., Schwartz, O.M., Chen, W., Chen, C.K., and Simonds, W.F. (2011). Knockout of G protein beta5 impairs brain development and causes multiple neurologic abnormalities in mice. J Neurochem 119, 544-554.
64. Zhang, Z., Zhao, Z., Margolskee, R., and Liman, E. (2007). The transduction channel TRPM5 is gated by intracellular calcium in taste cells. J Neurosci 27, 5777-5786.
65. Zwaal, R.R., Ahringer, J., Van Luenen, H.G., Rushforth, A., Anderson, P., and Plasterk, R.H. (1996). G proteins are required for spatial orientation of early cell cleavages in C. elegans embryos. Cell 86, 619-629.