The Gα12-RGS RhoGEF-RhoA signalling pathway regulates neurotransmitter release in C. elegans

EMBO Journal

Volumn 25, Issue 24, 2006, Pages 5884-5895

  Hiley, Emma ^a   McMullan, Rachel ^a   Nurrish, Stephen J ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

C. elegans; G protein; mUNC13; Neurotransmitter; Rho GTPase

Indexed keywords

ACETYLCHOLINE; BINDING PROTEIN; DIACYLGLYCEROL; GUANINE NUCLEOTIDE BINDING PROTEIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS; CAENORHABDITIS ELEGANS PROTEIN; CHOLINERGIC RECEPTOR STIMULATING AGENT; GPA 12 PROTEIN, C ELEGANS; GPA-12 PROTEIN, C ELEGANS; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; GUANINE NUCLEOTIDE EXCHANGE FACTOR; MUTANT PROTEIN; RGS PROTEIN; RHGF 1 PROTEIN, C ELEGANS; RHGF-1 PROTEIN, C ELEGANS; RHO GUANINE NUCLEOTIDE EXCHANGE FACTOR P115; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; UNC 13 PROTEIN, C ELEGANS; UNC-13 PROTEIN, C ELEGANS;

ACETYLCHOLINE RELEASE; ARTICLE; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; DOWNSTREAM PROCESSING; NERVE CELL; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; ANIMAL; BIOLOGICAL MODEL; CHEMISTRY; CONGENITAL MALFORMATION; CYTOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOTONEURON; PATHOLOGY; PHARYNX; PROMOTER REGION; SECRETION; SYNAPTOSOME;

CAENORHABDITIS ELEGANS;

ACETYLCHOLINE; ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CHOLINERGIC AGENTS; GTP-BINDING PROTEIN ALPHA SUBUNITS, G12-G13; GUANINE NUCLEOTIDE EXCHANGE FACTORS; MODELS, BIOLOGICAL; MOTOR NEURONS; MUTANT PROTEINS; NEUROTRANSMITTER AGENTS; PHARYNX; PRESYNAPTIC TERMINALS; PROMOTER REGIONS (GENETICS); RGS PROTEINS; RHOA GTP-BINDING PROTEIN; SIGNAL TRANSDUCTION;

EID: 33845709798     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/sj.emboj.7601458     Document Type: Article

References (31)

1. Barrett K, Leptin M, Settleman J (1997) The Rho GTPase and a putative RhoGEF mediate a signaling pathway for the cell shape changes in Drosophila gastrulation. Cell 91: 905-915
2. Betz A, Ashery U, Rickmann M, Augustin I, Neher E, Sudhof TC, Rettig J, Brose N (1998) Munc13-1 is a presynaptic phorbol ester receptor that enhances neurotransmitter release. Neuron 21: 123-136
3. Brenner S (1974) The genetics of Caenorhabditis elegans. Genetics 77: 71-94
4. Brundage L, Avery L, Katz A, Kim UJ, Mendel JE, Sternberg PW, Simon MI (1996) Mutations in a C. elegans Gqalpha gene disrupt movement, egg laying, and viability. Neuron 16: 999-1009
5. Chase DL, Pepper JS, Koelle MR (2004) Mechanism of extrasynaptic dopamine signaling in Caenorhabditis elegans. Nat Neurosci 7: 1096-1103
6. Hacker U, Perrimon N (1998) DRhoGEF2 encodes a member of the Dbl family of oncogenes and controls cell shape changes during gastrulation in Drosophila. Genes Dev 12: 274-284
7. Hart MJ, Jiang X, Kozasa T, Roscoe W, Singer WD, Gilman AG, Sternweis PC, Bollag G (1998) Direct stimulation of the guanine nucleotide exchange activity of p115 RhoGEF by Galpha13. Science 280: 2112-2114
8. Jaffe AB, Hall A (2005) Rho GTPases: biochemistry and biology. Annu Rev Cell Dev Biol 21: 247-269
9. Jaffe AB, Hall A, Schmidt A (2005) Association of CNK1 with Rho guanine nucleotide exchange factors controls signaling specificity downstream of Rho. Curr Biol 15: 405-412
10. Kozasa T, Jiang X, Hart MJ, Sternweis PM, Singer WD, Gilman AG, Bollag G, Sternweis PC (1998) p115 RhoGEF, a GTPase activating protein for Galpha12 and Galpha13. Science 280: 2109-2111
11. Kristelly R, Gao G, Tesmer JJ (2004) Structural determinants of RhoA binding and nucleotide exchange in leukemia-associated Rho guanine-nucleotide exchange factor. J Biol Chem 279: 47352-47362
12. Lackner MR, Nurrish SJ, Kaplan JM (1999) Facilitation of synaptic transmission by EGL-30 Gqalpha and EGL-8 PLCbeta: DAG binding to UNC-13 is required to stimulate acetylcholine release. Neuron 24: 335-346
13. Marinissen MJ, Gutkind JS (2005) Scaffold proteins dictate Rho GTPase-signaling specificity. Trends Biochem Sci 30: 423-426
14. McMullan R, Hiley E, Morrison P, Nurrish SJ (2006) Rho is a presynaptic activator of neurotransmitter release at pre-existing synapses in C. elegans. Genes Dev 20: 65-76
15. Mello C, Fire A (1995) DNA transformation. Methods Cell Biol 48: 451-482
16. Mendel JE, Korswagen HC, Liu KS, Hajdu-Cronin YM, Simon MI, Plasterk RH, Sternberg PW (1995) Participation of the protein Go in multiple aspects of behavior in C. elegans. Science 267: 1652-1655
17. Miller KG, Alfonso A, Nguyen M, Crowell JA, Johnson CD, Rand JB (1996) A genetic selection for Caenorhabditis elegans synaptic transmission mutants. Proc Natl Acad Sci USA 93: 12593-12598
18. Miller KG, Emerson MD, Rand JB (1999) Goalpha and diacylglycerol kinase negatively regulate the Gqalpha pathway in C. elegans. Neuron 24: 323-333
19. Nguyen M, Alfonso A, Johnson CD, Rand JB (1995) Caenorhabditis elegans mutants resistant to inhibitors of acetylcholinesterase. Genetics 140: 527-535
20. Nonet ML, Grundahl K, Meyer BJ, Rand JB (1993) Synaptic function is impaired but not eliminated in C. elegans mutants lacking synaptotagmin. Cell 73: 1291-1305
21. Nurrish S, Segalat L, Kaplan JM (1999) Serotonin inhibition of synaptic transmission: Galpha(0) decreases the abundance of UNC-13 at release sites. Neuron 24: 231-242
22. Parks S, Wieschaus E (1991) The Drosophila gastrulation gene concertina encodes a G alpha-like protein. Cell 64: 447-458
23. Richmond JE, Weimer RM, Jorgensen EM (2001) An open form of syntaxin bypasses the requirement for UNC-13 in vesicle priming. Nature 412: 338-341
24. Schade MA, Reynolds NK, Dollins CM, Miller KG (2005) Mutations that rescue the paralysis of Caenorhabditis elegans ric-8 (synembryn) mutants activate the G alpha(s) pathway and define a third major branch of the synaptic signaling network. Genetics 169: 631-649
25. Schmidt A, Hall A (2002) Guanine nucleotide exchange factors for Rho GTPases: turning on the switch. Genes Dev 16: 1587-1609
26. Segalat L, Elkes DA, Kaplan JM (1995) Modulation of serotonin-controlled behaviors by Go in Caenorhabditis elegans. Science 267: 1648-1651
27. Sieburth D, Ch'ng Q, Dybbs M, Tavazoie M, Kennedy S, Wang D, Dupuy D, Rual JF, Hill DE, Vidal M, Ruvkun G, Kaplan JM (2005) Systematic analysis of genes required for synapse structure and function. Nature 436: 510-517
28. Smith FD, Scott JD (2002) Signaling complexes: junctions on the intracellular information super highway. Curr Biol 12: R32-R40
29. Steven R, Zhang L, Culotti J, Pawson T (2005) The UNC-73/Trio RhoGEF-2 domain is required in separate isoforms for the regulation of pharynx pumping and normal neurotransmission in C. elegans. Genes Dev 19: 2016-2029
30. van der Linden AM, Moorman C, Cuppen E, Korswagen HC, Plasterk RH (2003) Hyperactivation of the G12-mediated signaling pathway in Caenorhabditis elegans induces a developmental growth arrest via protein kinase C. Curr Biol 13: 516-521
31. Yau DM, Yokoyama N, Goshima Y, Siddiqui ZK, Siddiqui SS, Kozasa T (2003) Identification and molecular characterization of the G alpha12-Rho guanine nucleotide exchange factor pathway in Caenorhabditis elegans. Proc Natl Acad Sci USA 100: 14748-14753