Role of Go/i subgroup of G proteins in olfactory signaling of Drosophila melanogaster

European Journal of Neuroscience

Volumn 39, Issue 8, 2014, Pages 1245-1255

  Ignatious Raja, Jennifer S ^a   Katanayeva, Natalya ^b   Katanaev, Vladimir L ^b   Galizia, C Giovanni ^a  

^a UNIVERSITY OF KONSTANZ   (Germany)

^b UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

G proteins; Insect odorant receptors; Olfaction; Signaling

Indexed keywords

CALCIUM; GUANINE NUCLEOTIDE BINDING PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN BETA SUBUNIT; GUANINE NUCLEOTIDE BINDING PROTEIN GAMMA SUBUNIT; INHIBITORY GUANINE NUCLEOTIDE BINDING PROTEIN; PROTEIN OR22A; RECEPTOR PROTEIN; UNCLASSIFIED DRUG; DROSOPHILA PROTEIN; G-PROTEIN BETA GAMMA; OLFACTORY RECEPTOR; OR22A PROTEIN, DROSOPHILA; PERTUSSIS TOXIN; PROTEIN BINDING;

ANIMAL EXPERIMENT; ARTICLE; CALCIUM TRANSPORT; CELL STRAIN HEK293; CONTROLLED STUDY; EMBRYO; FEMALE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MALE; NONHUMAN; ODOR; OLFACTORY RECEPTOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SENSORY NERVE CELL; SIGNAL TRANSDUCTION; SMELLING; ANIMAL; ANTAGONISTS AND INHIBITORS; CALCIUM SIGNALING; DROSOPHILA MELANOGASTER; GENETICS; HEK293 CELL LINE; METABOLISM; PHYSIOLOGY;

ANIMALS; CALCIUM SIGNALING; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GTP-BINDING PROTEIN ALPHA SUBUNITS, GI-GO; GTP-BINDING PROTEIN BETA SUBUNITS; GTP-BINDING PROTEIN GAMMA SUBUNITS; HEK293 CELLS; HUMANS; PERTUSSIS TOXIN; PROTEIN BINDING; RECEPTORS, ODORANT; SENSORY RECEPTOR CELLS; SMELL;

EID: 84899088695     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/ejn.12481     Document Type: Article

References (62)

1. Atwood, B.K., Lopez, J., Wager-Miller, J., Mackie, K. & Straiker, A. (2011) Expression of G protein-coupled receptors and related proteins in HEK293, AtT20, BV2, and N18 cell lines as revealed by microarray analysis. BMC Genomics, 12, 14.
2. Bargmann, C.I. (2006) Comparative chemosensation from receptors to ecology. Nature, 444, 295-301.
3. Benton, R., Sachse, S., Michnick, S.W. & Vosshall, L.B. (2006) Atypical membrane topology and heteromeric function of Drosophila odorant receptors in vivo. PLoS Biol., 4, e20.
4. Benton, R., Vannice, K.S., Gomez-Diaz, C. & Vosshall, L.B. (2009) Variant ionotropic glutamate receptors as chemosensory receptors in Drosophila. Cell, 136, 149-162.
5. Berghard, A. & 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.
6. Berghard, A., Buck, L.B. & Liman, E.R. (1996) Evidence for distinct signaling mechanisms in two mammalian olfactory sense organs. Proc. Natl. Acad. Sci. USA, 93, 2365-2369.
7. Boto, T., Gomez-Diaz, C. & Alcorta, E. (2010) Expression analysis of the 3 G-protein subunits, Gα, Gβ, and Gγ, in the olfactory receptor organs of adult Drosophila melanogaster. Chem. Senses, 35, 183-193.
8. Bredendiek, N., Hutte, J., Steingraber, A., Hatt, H., Gisselmann, G. & Neuhaus, E.M. (2011) Go alpha is involved in sugar perception in Drosophila. Chem. Senses, 36, 69-81.
9. de Bruyne, M., Foster, K. & Carlson, J.R. (2001) Odor coding in the Drosophila antenna. Neuron, 30, 537-552.
10. Buck, L. & Axel, R. (1991) A novel multigene family may encode odorant receptors - a molecular-basis for odor recognition. Cell, 65, 175-187.
11. Cavarra, M.S., Assef, Y.A. & Kotsias, B.A. (2003) Effects of ionomycin and thapsigargin on ion currents in oocytes of Bufo arenarum. J. Exp. Zool., 297A, 130-137.
12. Chatterjee, A., Roman, G. & Hardin, P.E. (2009) Go contributes to olfactory reception in Drosophila melanogaster. BMC Physiol., 9, 22.
13. Clyne, P.J., Warr, C.G., Freeman, M.R., Lessing, D., Kim, J. & Carlson, J.R. (1999) A novel family of divergent seven-transmembrane proteins: candidate odorant receptors in Drosophila. Neuron, 22, 327-338.
14. Deng, Y., Zhang, W., Farhat, K., Oberland, S., Gisselmann, G. & Neuhaus, E.M. (2011) The stimulatory Galpha(s) protein is involved in olfactory signal transduction in Drosophila. PLoS ONE, 6, e18605.
15. Dietzl, G., Chen, D., Schnorrer, F., Su, K.-C., Barinova, Y., Fellner, M., Gasser, B., Kinsey, K., Oppel, S., Scheiblauer, S., Couto, A., Marra, V., Keleman, K. & Dickson, B.J. (2007) A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature, 448, 151-156.
16. Dobritsa, A.A. & van der Goes van Naters, W., Warr, C.G., Steinbrecht, R.A. & Carlson, J.R. (2003) Integrating the molecular and cellular basis of odor coding in the Drosophila antenna. Neuron, 37, 827-841.
17. Duffy, J.B. (2002) GAL4 system in Drosophila: a fly geneticist's Swiss army knife. Genesis, 34, 1-15.
18. Gao, Q. & Chess, A. (1999) Identification of candidate Drosophila olfactory receptors from genomic DNA sequence. Genomics, 60, 31-39.
19. Getahun, M.N., Olsson, S.B., Lavista-Llanos, S., Hansson, B.S. & Wicher, D. (2013) Insect odorant response sensitivity is tuned by metabotropically autoregulated olfactory receptors. PLoS ONE, 8, e58889.
20. Gilman, A.G. (1987) G proteins: transducers of receptor-generated signals. Annu. Rev. Biochem., 56, 615-649.
21. Hallem, E.A., Ho, M.G. & Carlson, J.R. (2004) The molecular basis of odor coding in the Drosophila antenna. Cell, 117, 965-979.
22. Hermans, E. (2003) Biochemical and pharmacological control of the multiplicity of coupling at G-protein-coupled receptors. Pharmacol. Therapeut., 99, 25-44.
23. Jones, D.T. & Reed, R.R. (1989) Golf: an olfactory neuron specific-G protein involved in odorant signal transduction. Science, 244, 790-795.
24. Kain, P., Chakraborty, T.S., Sundaram, S., Siddiqi, O., Rodrigues, V. & Hasan, G. (2008) Reduced odor responses from antennal neurons of Gq, phospholipase C, and rdgA mutants in Drosophila support a role for a phospholipid intermediate in insect olfactory transduction. J. Neurosci., 28, 4745-4755.
25. Kang, G.-J., Gong, Z.-J., Cheng, J.-A., Mao, C.-G. & Zhu, Z.-R. (2011) Cloning and expression analysis of a G-protein subunit- in the rice water weevil Lissorhoptrus oryzophilus Kuschel. Arch. Insect Biochem., 76, 43-54.
26. Katanaev, V.L. & Tomlinson, A. (2006) Multiple roles of a trimeric G protein in Drosophila cell polarization. Cell Cycle, 5, 2464-2472.
27. Katanaev, V.L., Ponzielli, R., Sémériva, M. & Tomlinson, A. (2005) Trimeric G protein-dependent frizzled signaling in Drosophila. Cell, 120, 111-122.
28. Katanayeva, N., Kopein, D., Portmann, R., Hess, D. & Katanaev, V.L. (2010) Competing activities of heterotrimeric G proteins in Drosophila wing maturation. PLoS ONE, 5, e12331.
29. Kaupp, U.B. (2010) Olfactory signalling in vertebrates and insects: differences and commonalities. Nat. Rev. Neurosci., 11, 188-200.
30. Kopein, D. & Katanaev, V.L. (2009) Drosophila GoLoco-protein pins is a target of Galpha(o)-mediated G protein-coupled receptor signaling. Mol. Biol. Cell, 20, 3865-3877.
31. Larsson, M.C., Domingos, A.I., Jones, W.D., Chiappe, M.E., Amrein, H. & Vosshall, L.B. (2004) Or83b encodes a broadly expressed odorant receptor essential for Drosophila olfaction. Neuron, 43, 703-714.
32. Leinders-Zufall, T., Greer, C.A., Shepherd, G.M. & Zufall, F. (1998) Imaging odor-induced calcium transients in single olfactory cilia: specificity of activation and role in transduction. J. Neurosci., 18, 5630-5639.
33. Lucas, P., Ukhanov, K., Leinders-Zufall, T. & Zufall, F. (2003) A diacylglycerol-gated cation channel in vomeronasal neuron dendrites is impaired in TRPC2 mutant mice: mechanism of pheromone transduction. Neuron, 40, 551-561.
34. Lundin, C., Kall, L., Kreher, S.A., Kapp, K., Sonnhammer, E.L., Carlson, J.R., Heijne, G. & Nilsson, I. (2007) Membrane topology of the Drosophila OR83b odorant receptor. FEBS Lett., 581, 5601-5604.
35. 2+ influx in rat thymic lymphocytes. Biochem. J., 296, 33-39.
36. 2+ release channels and their regulation by endogenous effectors. Annu. Rev. Physiol., 56, 485-508.
37. Miura, N., Atsumi, S., Tabunoki, H. & Sato, R. (2005) Expression and localization of three G protein alpha subunits, Go, Gq, and Gs, in adult antennae of the silkmoth (Bombyx mori). J. Comp. Neurol., 485, 143-152.
38. Mombaerts, P. (1999) Seven-transmembrane proteins as odorant and chemosensory receptors. Science, 286, 707-711.
39. 2+ influx by stimulating store-regulated cation entry and not by a direct action at the plasma membrane. Biochem. J., 300, 665-672.
40. Nakagawa, T., Pellegrino, M., Sato, K., Vosshall, L.B. & Touhara, K. (2012) Amino acid residues contributing to function of the heteromeric insect olfactory receptor complex. PLoS ONE, 7, e32372.
41. 2+ probe composed of a single green fluorescent protein. Nat. Biotechnol., 19, 137-141.
42. Neuhaus, E.M., Gisselmann, G., Zhang, W., Dooley, R., Störtkuhl, K. & Hatt, H. (2005) Odorant receptor heterodimerization in the olfactory system of Drosophila melanogaster. Nat. Neurosci., 8, 15-17.
43. Nichols, A.S., Chen, S. & Luetje, C.W. (2011) Subunit contributions to insect olfactory receptor function: channel block and odorant recognition. Chem. Senses, 36, 781-790.
44. Olsen, S.R. & Wilson, R.I. (2008) Lateral presynaptic inhibition mediates gain control in an olfactory circuit. Nature, 452, 956-960.
45. Pask, G.M., Jones, P.L., Rutzler, M., Rinker, D.C. & Zwiebel, L.J. (2011) Heteromeric Anopheline odorant receptors exhibit distinct channel properties. PLoS ONE, 6, e28774.
46. Pelz, D., Roeske, T., Syed, Z., de Bruyne, M. & Galizia, C.G. (2006) The molecular receptive range of an olfactory receptor in vivo (Drosophila melanogaster Or22a). J. Neurobiol., 66, 1544-1563.
47. Querfurth, H.W., Haughey, N.J., Greenway, S.C., Yacono, P.W., Golan, D.E. & Geiger, J.D. (1998) Expression of ryanodine receptors in human embryonic kidney (HEK293) cells. Biochem. J., 334, 79-86.
48. Reeves, P.J., Thurmond, R.L. & Khorana, H.G. (1996) Structure and function in rhodopsin: high level expression of a synthetic bovine opsin gene and its mutants in stable mammalian cell lines. Proc. Natl. Acad. Sci. USA, 93, 11487-11492.
49. Root, C.M., Masuyama, K., Green, D.S., Enell, L.E., Nässel, D.R., Lee, C.-H. & Wang, J.W. (2008) A presynaptic gain control mechanism fine-tunes olfactory behavior. Neuron, 59, 311-321.
50. Rutzler, M., Lu, T. & Zwiebel, L.J. (2006) Galpha encoding gene family of the malaria vector mosquito Anopheles gambiae: expression analysis and immunolocalization of AGalphaq and AGalphao in female antennae. J. Comp. Neurol., 499, 533-545.
51. Sargsyan, V., Getahun, M.N., Llanos, S.L., Olsson, S.B., Hansson, B.S. & Wicher, D. (2011) Phosphorylation via PKC regulates the function of the Drosophila odorant co-receptor. Front. Cell. Neurosci., 5, 5.
52. Sato, K., Pellegrino, M., Nakagawa, T., Nakagawa, T., Vosshall, L.B. & Touhara, K. (2008) Insect olfactory receptors are heteromeric ligand-gated ion channels. Nature, 452, 1002-1006.
53. Silbering, A.F. & Galizia, C.G. (2007) Processing of odor mixtures in the Drosophila antennal lobe reveals both global inhibition and glomerulus-specific interactions. J. Neurosci., 27, 11966-11977.
54. Smart, R., Kiely, A., Beale, M., Vargas, E., Carraher, C., Kralicek, A.V., Christie, D.L., Chen, C., Newcomb, R.D. & Warr, C.G. (2008) Drosophila odorant receptors are novel seven transmembrane domain proteins that can signal independently of heterotrimeric G proteins. Insect Biochem. Molec., 38, 770-780.
55. Sutko, J.L., Airey, J.A., Welch, W. & Ruest, L. (1997) The pharmacology of ryanodine and related compounds. Pharmacol. Rev., 49, 53-98.
56. Touhara, K. & Vosshall, L.B. (2009) Sensing odorants and pheromones with chemosensory receptors. Annu. Rev. Physiol., 71, 307-332.
57. Tsitoura, P., Andronopoulou, E., Tsikou, D., Agalou, A., Papakonstantinou, M.P., Kotzia, G.A., Labropoulou, V., Swevers, L., Georgoussi, Z. & Iatrou, K. (2010) Expression and membrane topology of Anopheles gambiae odorant receptors in Lepidopteran insect cells. PLoS ONE, 5, e15428.
58. Vosshall, L.B., Amrein, H., Morozov, P.S., Rzhetsky, A. & Axel, R. (1999) A spatial map of olfactory receptor expression in the Drosophila antenna. Cell, 96, 725-736.
59. Wang, J.W., Wong, A.M., Flores, J., Vosshall, L.B. & Axel, R. (2003) Two-photon calcium imaging reveals an odor-evoked map of activity in the fly brain. Cell, 112, 271-282.
60. Wicher, D., Schäfer, R., Bauernfeind, R., Stensmyr, M.C., Heller, R., Heinemann, S.H. & Hansson, B.S. (2008) Drosophila odorant receptors are both ligand-gated and cyclic-nucleotide-activated cation channels. Nature, 452, 1007-1011.
61. 2-sensing neurons in Drosophila. J. Neurosci., 30, 4562-4572.
62. 2+ from intracellular stores in response to ionomycin in oocytes of the frog Xenopus laevis. J. Physiol., 458, 307-318.