Antagonism between G(o)α and G(q)α in Caenorhabditis elegans: The RGS protein EAT-16 is necessary for G(o)α signaling and regulates G(q)α activity

Genes and Development

Volumn 13, Issue 14, 1999, Pages 1780-1793

  Hajdu Cronin, Yvonne M ^a   Chen, Wen J ^a   Patikoglou, Georgia ^b   Koelle, Michael R ^b   Sternberg, Paul W ^a  

^a CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^b YALE UNIVERSITY   (United States)

Author keywords

C. elegans; G(o) protein; G(q) protein; Regulation; RGS protein; Signaling

Indexed keywords

GUANINE NUCLEOTIDE BINDING PROTEIN; PROTEIN EAT 16; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

ALPHA CHAIN; ARTICLE; CAENORHABDITIS ELEGANS; CELL STRAIN COS1; CELL VIABILITY; ENZYME ACTIVITY; GENE EXPRESSION; GENE MUTATION; LETHAL MUTANT; NEGATIVE FEEDBACK; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ANIMALIA; CAENORHABDITIS ELEGANS; INVERTEBRATA; MAMMALIA;

EID: 0033565671     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.13.14.1780     Document Type: Article

References (65)

1. Akerib, C.C. and B.J. Meyer. 1994. Identification of X chromosome regions in Caenorhabditis elegans that contain sex-determination signal elements. Genetics 138: 1105-1125.
2. Aroian, R.V., A.D. Levy, M. Koga, Y. Ohshima, J.M. Kramer, and P.W. Sternberg. 1993. Splicing in Caeonorhabditis elegans does not require an AG at the 3′ splice acceptor site. Mol. Cell. Biol. 13: 626-637.
3. Arshavsky, V.Y. and E.N. Pugh Jr. 1998. Lifetime regulation of G protein-effector complex: Emerging importance of RGS proteins. Neuron 20: 11-14.
4. Avery, L. 1993. The genetics of feeding in Caenorhabditis elegans. Genetics 133: 897-917.
5. Berman, D.M. and A.G. Gilman. 1998. Mammalian RGS proteins: Barbarians at the gate. J. Biol. Chem. 273: 1269-1272.
6. Berman, D.M., T. Kozasa, and A.G. Gilman. 1996a. The GTPase-activating protein RGS4 stabilizes the transition state for nucleotide hydrolysis. J. Biol. Chem. 271: 27209-27212.
7. Berman, D.M., T.M. Wilkie, and A.G. Gilman. 1996b. GAIP and RGS4 are GTPase-Activating Proteins for the Gi subfamily of G protein α subunits. Cell 88: 445-452.
8. Berridge, M.J. 1993. Inositol trisphosphate and calcium signalling. Nature 361: 315-325.
9. Berstein, G., J.L. Blank, D.Y. Jhon, J.H. Exton, S.G. Rhee, and E.M. Ross. 1992. Phospholipase C-beta 1 is a GTPase-activating protein for Gq/11, its physiologic regulator. Cell 70: 411-418.
10. Birnbaumer, L. 1992. Receptor-to-effector signaling through G proteins: Roles for beta gamma dimers as well as alpha subunits. Cell 71: 1069-1072.
11. Bourne, H.R., D.A. Sanders, and F. McCormick. 1990. The GTPase superfamily: A conserved switch for diverse cell functions. Nature 348: 125-132.
12. Bourne, H.R., D.A. Sanders, and F. McCormick. 1991. The GTPase superfamily: Conserved structure and molecular mechanism. Nature 349: 117-127.
13. Brenner, S. 1974. The genetics of Caenorhabditis elegans. Genetics 77: 71-94.
14. Brundage, L., L. Avery, A. Katz, U.J. Kim, J.E. Mendel, P.W. Sternberg, and M.I. Simon. 1996. Mutations in a C. elegans Gqalpha gene disrupt movement, egg laying, and viability. Neuron 16: 999-1009.
15. elegans Sequencing Consortium. 1998. Genome sequence of the nematode C. elegans: A platform for investigating biology [published erratum appears in Science 1999 Jan 1; 283: (5398)35]. Science 282: 2012-2018.
16. Clark, S.G., X. Lu, and H.R. Horvitz. 1994. The Caenorhabditis elegans locus lin-15, a negative regulator of a tyrosine kinase signaling pathway, encodes two different proteins. Genetics 137: 987-997.
17. Coulson, A., J. Sulston, S. Brenner, and J. Karn. 1986. Toward a physical map of the genome of the nematode Caenorhabditis elegans. Proc. Natl. Acad. Sci. 83: 7821-7825.
18. Coulson, A., R. Waterston, J. Kiff, J. Sulston, and Y. Kohara. 1988. Genome linking with yeast artificial chromosomes. Nature 335: 184-186.
19. De Vries, L., M. Mousli, A. Wurmser, and M.G. Farquhar. 1995. GAIP, a protein that specifically interacts with the trimeric G protein G alpha i3, is a member of a protein family with a highly conserved core domain. Proc. Natl. Acad. Sci. 92: 11916-11920.
20. Dohlman, H.G., J. Song, D. Ma, W.E. Courchesne, and J. Thorner. 1996. Sst2, a negative regulator of pheromone signaling in the yeast Saccharomyces cerevisiae: Expression, localization, and genetic interaction and physical association with Gpa1 (the G-protein alpha subunit). Mol. Cell. Biol. 16: 5194-5209.
21. Dohlman, H.G. and J. Thorner. 1997. RGS proteins and signaling by heterotrimeric G proteins. J. Biol. Chem. 272: 3871-3874.
22. Ellis, R.E. and J. Kimble. 1995. The fog-3 gene and regulation of cell fate in the germ line of Caenorhabditis elegans. Genetics 139: 561-577.
23. Faurobert, E. and J.B. Hurley. 1997. The core domain of a new retina specific RGS protein stimulates the GTPase activity of transducin in vitro. Proc. Natl. Acad. Sci. 94: 2945-2950.
24. Freyd, G., S.K. Kim, and H.R. Horvitz. 1990. Novel cysteine-rich motif and homeodomain in the product of the Caenorhabditis elegans cell lineage gene lin-11. Nature 344: 876-879.
25. Graziano, M.P. and A.G. Gilman. 1989. Synthesis in Escherichia coli of GTPase-deficient mutants of Gs alpha. J. Biol. Chem. 264: 15475-15482.
26. Hepler, J.R. and A.G. Gilman. 1992. G proteins. Trends Biochem. Sci. 17: 383-387.
27. Heximer, S.P., N. Watson, M.E. Linder, K.J. Blumer, and J.R. Hepler. 1997. RGS2/G0S8 is a selective inhibitor of Gq alpha function. Proc. Natl. Acad. Sci. 94: 14389-14393.
28. Hodgkin, M.N., T.R. Pettitt, A. Martin, R.H. Michell, A.J. Pemberton, and M.J. Wakelam. 1998. Diacylglycerols and phosphatidates: Which molecular species are intracellular messengers? Trends Biochem. Sci. 23: 200-204.
29. Hsu, W.H., U. Rudolph, J. Sanford, P. Bertrand, J. Olate, C. Nelson, L.G. Moss, A.E. Boyd, J. Codina, and L. Birnbaumer. 1990. Molecular cloning of a novel splice variant of the alpha subunit of the mammalian Go protein. J. Biol. Chem. 265: 11220-11226.
30. Huang, L.S., P. Tzou, and P.W. Sternberg. 1994. The lin-15 locus encodes two negative regulators of Caenorhabditis elegans vulval development. Mol. Biol. Cell 5: 395-411.
31. Hunt, T.W., T.A. Fields, P.J. Casey, and E.G. Peralta. 1996. RGS10 is a selective activator of Gai GTPase activity. Nature 383: 175-177.
32. Koelle, M.R. 1997. A new family of G-protein regulators - the RGS proteins. Curr. Opin. Cell Biol. 9: 143-147.
33. Koelle, M.R. and H.R. Horvitz. 1996. EGL-10 regulates G protein signaling in the C. elegans nervous system and shares a conserved domain with many mammalian proteins. Cell 84: 115-125.
34. Korswagen, H.C., J.H. Park, Y. Ohshima, and R.H. Plasterk. 1997. An activating mutation in a Caenorhabditis elegans Gs protein induces neural degeneration. Genes & Dev. 11: 1493-1503.
35. Kretz, K.A., G.S. Carson, and J.S. O'Brien. 1989. Direct sequencing from low-melt agarose with Sequenase [published erratum appears in Nucleic Acids Res. 1990. 18: (2)400]. Nucleic Acids Res. 17: 5864.
36. Lavu, S., J. Clark, R. Swarup, K. Matsushima, K. Paturu, J. Moss, and H.F. Kung. 1988. Molecular cloning and DNA sequence analysis of the human guanine nucleotide-binding protein Go alpha [published erratum appears in Biochem. Biophys. Res. Commun. 1988. 153: (1)487]. Biochem. Biophys. Res. Commun. 150: 811-815.
37. Liu, M. and M.I. Simon. 1996. Regulation by cAMP-dependent protein kinease of a G-protein-mediated phospholipase C. Nature 382: 83-87.
38. Lochrie, M.A., J.E. Mendel, P.W. Sternberg, and M.I. Simon. 1991. Homologous and unique G protein alpha subunits in the nematode Caenorhabditis elegans. Cell Regul. 2: 135-154.
39. Lundquist, E.A. and R.K. Herman. 1994. The mec-8 gene of Caenorhabditis elegans affects muscle and sensory neuron function and interacts with three other genes: unc-52, smu-1 and smu-2. Genetics 138: 83-101.
40. Maniatis, T., E.F. Fritsch, and J. Sambrook. 1982. Molecular cloning: A laboratory manual, Vol. 1, pp. 2.60-2.63. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
41. Mello, C. and A. Fire. 1995. DNA Transformation. In Caenorhabditis elegans: Modern biological analysis of an organism (ed. D.C. Shakes and H.F. Epstein), pp. 451-482. Academic Press, San Diego, CA.
42. Mello, C.C., J.M. Kramer, D. Stinchcomb, and V. Ambros. 1991. Efficient gene transfer in C. elegans: Extrachromosomal maintenance and integration of transforming sequences. EMBO J. 10: 3959-3970.
43. Mendel, J.E., H.C. Korswagen, K.S. Liu, Y.M. Hajdu-Cronin, M.I. Simon, R.H. Plasterk, and P.W. Sternberg. 1995. Participation of the protein Go in multiple aspects of behavior in C. elegans. Science 267: 1652-1655.
44. Miller, K.G., A. Alfonso, M. Nguyen, J.A. Crowell, C.D. Johnson, and J.B. Rand. 1996. A genetic selection for Caenorhabditis elegans synaptic transmission mutants. Proc. Natl. Acad. Sci. 93: 12593-12598.
45. Natochin, M. and N.O. Artemyev. 1998. A single mutation Asp229 → Ser confers upon Gs alpha the ability to interact with regulators of G protein signaling. Biochemistry 37: 13776-13780.
46. Offermanns, S., T. Wieland, D. Homann, J. Sandmann, E. Bombien, K. Spicher, G. Schultz, and K.H. Jakobs. 1994. Transfected muscarinic acetylcholine receptors selectively couple to Gi-type G proteins and Gq/11. Mol. Pharmacol. 45: 890-898.
47. Olate, J., H. Jorquera, P. Purcell, J. Codina, L. Birnbaumer, and J.E. Allende. 1989. Molecular cloning and sequence determination of a cDNA coding for the alpha-subunit of a Go-type protein of Xenopus laevis oocytes [published erratum appears in FEBS Lett. 1990 Jul 16; 267: (2)316]. FEBS Lett. 244: 188-192.
48. Ségalat, L., D.A. Elkes, and J.M. Kaplan. 1995. Modulation of serotonin-controlled behaviors by Go in Caenorhabditis elegans. Science 267: 1648-1651.
49. Selbie, L.A. and S.J. Hill. 1998. G protein-coupled-receptor cross-talk: The fine-tuning of multiple receptor-signalling pathways. Trends Pharmacol. Sci. 19: 87-93.
50. Simon, M.I., M.P. Strathmann, and N. Gautam. 1991. Diversity of G proteins in signal transduction. Science 252: 802-808.
51. Snow, B.E., A.M. Krumins, G.M. Brothers, S.F. Lee, M.A. Wall, S. Chung, J. Mangion, S. Arya, A.G. Gilman, and D.P. Siderovski. 1998. A G protein gamma subunit-like domain shared between RGS11 and other RGS proteins specifies binding to Gbeta5 subunits. Proc. Natl. Acad. Sci. 95: 13307-13312.
52. Sondek, J., D.G. Lambright, J.P. Noel, H.E. Hamm, and P.B. Sigler. 1994. GTPase mechanism of G proteins from the 1.7-A crystal structure of transducin alpha-GDP-AIF-4. Nature 372: 276-279.
53. Starr, T., A.M. Howell, J. McDowall, K. Peters, and A.M. Rose. 1989. Isolation and mapping of DNA probes within the linkage group I gene cluster of Caenorhabditis elegans. Genome 32: 365-372.
54. Sternweis, P.C. and J.D. Robishaw. 1984. Isolation of two proteins with high affinity for guanine nucleotides from membranes of bovine brain. J. Biol. Chem. 259: 13806-13813.
55. Sulston, J., Z. Du, K. Thomas, R. Wilson, L. Hillier, R. Staden, N. Halloran, P. Green, J. Thierry-Mieg, L. Qiu et al. 1992. The C. elegans genome sequencing project: A beginning. Nature 356: 37-41.
56. Tesmer, J.J., D.M. Berman, A.G. Gilman, and S.R. Sprang. 1997. Structure of RGS4 bound to AIF4-activated Gial: Stabilization of the transition state for GTP hydrolysis. Cell 89: 251-261.
57. Trent, C., N. Tsung, and H.R. Horvitz. 1983. Egg-laying defective mutants of the nematode Caenorhabditis elegans. Genetics 104: 619-647.
58. van der Voorn, L., M. Gebbink, R.H.A. Plasterk, and H.L. Ploegh. 1990. Characterization of a G-protein b-subunit gene from the Caenorhabditis elegans. J. Mol. Biol. 213: 17-26.
59. Van Meurs, K.P., C.W. Angus, S. Lavu, H.F. Kung, S.K. Czarnecki, J. Moss, and M. Vaughan. 1987. Deduced amino acid sequence of bovine retinal Go alpha: Similarities to other guanine nucleotide-binding proteins. Proc. Natl. Acad. Sci. 84: 3107-3111.
60. Watson, N., M.E. Linder, K.M. Druey, J.H. Kehrl, and K.J. Blumer. 1996. RGS family members: GTPase-activating proteins for heterotrimeric G-proteins a-subunits. Nature 383: 172-175.
61. Williams, B.D., B. Schrank, C. Huynh, R. Shownkeen, and R.H. Waterston. 1992. A genetic mapping system in Caenorhabditis elegans based on polymorphic sequence-tagged sites. Genetics 131: 609-624.
62. Wu, D.Q., C.H. Lee, S.G. Rhee, and M.I. Simon. 1992. Activation of phospholipase C by the alpha subunits of the Gq and G11 proteins in transfected Cos-7 cells. J. Biol. Chem. 267: 1811-1817.
63. Yandell, M.D., L.G. Edgar, and W.B. Wood. 1994. Trimethylpsoralen induces small deletion mutations in Caenorhabditis elegans. Proc. Natl. Acad. Sci. 91: 1381-1385.
64. Yoon, J., R.D. Shortridge, B.T. Bloomquist, S. Schneuwly, M.H. Perdew, and W.L. Pak. 1989. Molecular characterization of Drosophila gene encoding Go alpha subunit homolog. J. Biol. Chem. 264: 18536-18543.
65. Zhang, S., N. Watson, J. Zahner, J.N. Rottman, K.J. Blumer, and A.J. Muslin. 1998. RGS3 and RGS4 are GTPase activating proteins in the heart. J. Mol. Cell. Cardiol. 30: 269-276.