• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of geneticsGeneticsCurrent IssueInformation for AuthorsEditorial BoardSubscribeSubmit a Manuscript
Genetics. Dec 2000; 156(4): 1649–1660.
PMCID: PMC1461398

A role for RIC-8 (Synembryn) and GOA-1 (G(o)alpha) in regulating a subset of centrosome movements during early embryogenesis in Caenorhabditis elegans.

Abstract

RIC-8 (synembryn) and GOA-1 (G(o)alpha) are key components of a signaling network that regulates neurotransmitter secretion in Caenorhabditis elegans. Here we show that ric-8 and goa-1 reduction of function mutants exhibit partial embryonic lethality. Through Nomarski analysis we show that goa-1 and ric-8 mutant embryos exhibit defects in multiple events that involve centrosomes, including one-cell posterior centrosome rocking, P(1) centrosome flattening, mitotic spindle alignment, and nuclear migration. In ric-8 reduction of function backgrounds, the embryonic lethality, spindle misalignments and delayed nuclear migration are strongly enhanced by a 50% reduction in maternal goa-1 gene dosage. Several other microfilament- and microtubule-mediated events, as well as overall embryonic polarity, appear unperturbed in the mutants. In addition, our results suggest that RIC-8 and GOA-1 do not have roles in centrosome replication, in the diametric movements of daughter centrosomes along the nuclear membrane, or in the extension of microtubules from centrosomes. Through immunostaining we show that GOA-1 (G(o)alpha) localizes to cell cortices as well as near centrosomes. Our results demonstrate that two components of a neuronal signal transduction pathway also play a role in centrosome movements during early embryogenesis.

Full Text

The Full Text of this article is available as a PDF (450K).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Lu B, Jan LY, Jan YN. Asymmetric cell division: lessons from flies and worms. Curr Opin Genet Dev. 1998 Aug;8(4):392–399. [PubMed]
  • Malone CJ, Fixsen WD, Horvitz HR, Han M. UNC-84 localizes to the nuclear envelope and is required for nuclear migration and anchoring during C. elegans development. Development. 1999 Jun;126(14):3171–3181. [PubMed]
  • Mendel JE, Korswagen HC, Liu KS, Hajdu-Cronin YM, Simon MI, Plasterk RH, Sternberg PW. Participation of the protein Go in multiple aspects of behavior in C. elegans. Science. 1995 Mar 17;267(5204):1652–1655. [PubMed]
  • Miller KG, Alfonso A, Nguyen M, Crowell JA, Johnson CD, Rand JB. A genetic selection for Caenorhabditis elegans synaptic transmission mutants. Proc Natl Acad Sci U S A. 1996 Oct 29;93(22):12593–12598. [PMC free article] [PubMed]
  • Miller KG, Emerson MD, Rand JB. Goalpha and diacylglycerol kinase negatively regulate the Gqalpha pathway in C. elegans. Neuron. 1999 Oct;24(2):323–333. [PubMed]
  • Miller KG, Emerson MD, McManus JR, Rand JB. RIC-8 (Synembryn): a novel conserved protein that is required for G(q)alpha signaling in the C. elegans nervous system. Neuron. 2000 Aug;27(2):289–299. [PubMed]
  • Morris NR, Xiang X, Beckwith SM. Nuclear migration advances in fungi. Trends Cell Biol. 1995 Jul;5(7):278–282. [PubMed]
  • Nurrish S, Ségalat L, Kaplan JM. Serotonin inhibition of synaptic transmission: Galpha(0) decreases the abundance of UNC-13 at release sites. Neuron. 1999 Sep;24(1):231–242. [PubMed]
  • Brundage L, Avery L, Katz A, Kim UJ, Mendel JE, Sternberg PW, Simon MI. Mutations in a C. elegans Gqalpha gene disrupt movement, egg laying, and viability. Neuron. 1996 May;16(5):999–1009. [PubMed]
  • Raff JW, Glover DM. Centrosomes, and not nuclei, initiate pole cell formation in Drosophila embryos. Cell. 1989 May 19;57(4):611–619. [PubMed]
  • Duerr JS, Frisby DL, Gaskin J, Duke A, Asermely K, Huddleston D, Eiden LE, Rand JB. The cat-1 gene of Caenorhabditis elegans encodes a vesicular monoamine transporter required for specific monoamine-dependent behaviors. J Neurosci. 1999 Jan 1;19(1):72–84. [PubMed]
  • Roychowdhury S, Rasenick MM. G protein beta1gamma2 subunits promote microtubule assembly. J Biol Chem. 1997 Dec 12;272(50):31576–31581. [PubMed]
  • Foe VE, Alberts BM. Studies of nuclear and cytoplasmic behaviour during the five mitotic cycles that precede gastrulation in Drosophila embryogenesis. J Cell Sci. 1983 May;61:31–70. [PubMed]
  • Roychowdhury S, Panda D, Wilson L, Rasenick MM. G protein alpha subunits activate tubulin GTPase and modulate microtubule polymerization dynamics. J Biol Chem. 1999 May 7;274(19):13485–13490. [PubMed]
  • Goldstein B. Cell contacts orient some cell division axes in the Caenorhabditis elegans embryo. J Cell Biol. 1995 May;129(4):1071–1080. [PMC free article] [PubMed]
  • Schaefer M, Shevchenko A, Shevchenko A, Knoblich JA. A protein complex containing Inscuteable and the Galpha-binding protein Pins orients asymmetric cell divisions in Drosophila. Curr Biol. 2000 Apr 6;10(7):353–362. [PubMed]
  • Hajdu-Cronin YM, Chen WJ, Patikoglou G, Koelle MR, Sternberg PW. Antagonism between G(o)alpha and G(q)alpha in Caenorhabditis elegans: the RGS protein EAT-16 is necessary for G(o)alpha signaling and regulates G(q)alpha activity. Genes Dev. 1999 Jul 15;13(14):1780–1793. [PMC free article] [PubMed]
  • Schlesinger A, Shelton CA, Maloof JN, Meneghini M, Bowerman B. Wnt pathway components orient a mitotic spindle in the early Caenorhabditis elegans embryo without requiring gene transcription in the responding cell. Genes Dev. 1999 Aug 1;13(15):2028–2038. [PMC free article] [PubMed]
  • Hawkins N, Garriga G. Asymmetric cell division: from A to Z. Genes Dev. 1998 Dec 1;12(23):3625–3638. [PubMed]
  • Ségalat L, Elkes DA, Kaplan JM. Modulation of serotonin-controlled behaviors by Go in Caenorhabditis elegans. Science. 1995 Mar 17;267(5204):1648–1651. [PubMed]
  • Heil-Chapdelaine RA, Adames NR, Cooper JA. Formin' the connection between microtubules and the cell cortex. J Cell Biol. 1999 Mar 8;144(5):809–811. [PMC free article] [PubMed]
  • Seydoux G, Mello CC, Pettitt J, Wood WB, Priess JR, Fire A. Repression of gene expression in the embryonic germ lineage of C. elegans. Nature. 1996 Aug 22;382(6593):713–716. [PubMed]
  • Hyman AA. Centrosome movement in the early divisions of Caenorhabditis elegans: a cortical site determining centrosome position. J Cell Biol. 1989 Sep;109(3):1185–1193. [PMC free article] [PubMed]
  • Skop AR, White JG. The dynactin complex is required for cleavage plane specification in early Caenorhabditis elegans embryos. Curr Biol. 1998 Oct 8;8(20):1110–1116. [PMC free article] [PubMed]
  • Hyman AA, White JG. Determination of cell division axes in the early embryogenesis of Caenorhabditis elegans. J Cell Biol. 1987 Nov;105(5):2123–2135. [PMC free article] [PubMed]
  • Strome S, Wood WB. Generation of asymmetry and segregation of germ-line granules in early C. elegans embryos. Cell. 1983 Nov;35(1):15–25. [PubMed]
  • Jan YN, Jan LY. Polarity in cell division: what frames thy fearful asymmetry? Cell. 2000 Mar 17;100(6):599–602. [PubMed]
  • Strome S, Martin P, Schierenberg E, Paulsen J. Transformation of the germ line into muscle in mes-1 mutant embryos of C. elegans. Development. 1995 Sep;121(9):2961–2972. [PubMed]
  • Karki S, Holzbaur EL. Cytoplasmic dynein and dynactin in cell division and intracellular transport. Curr Opin Cell Biol. 1999 Feb;11(1):45–53. [PubMed]
  • Kawasaki I, Shim YH, Kirchner J, Kaminker J, Wood WB, Strome S. PGL-1, a predicted RNA-binding component of germ granules, is essential for fertility in C. elegans. Cell. 1998 Sep 4;94(5):635–645. [PubMed]
  • Wang N, Rasenick MM. Tubulin-G protein interactions involve microtubule polymerization domains. Biochemistry. 1991 Nov 12;30(45):10957–10965. [PubMed]
  • Kemphues KJ, Priess JR, Morton DG, Cheng NS. Identification of genes required for cytoplasmic localization in early C. elegans embryos. Cell. 1988 Feb 12;52(3):311–320. [PubMed]
  • White J, Strome S. Cleavage plane specification in C. elegans: how to divide the spoils. Cell. 1996 Jan 26;84(2):195–198. [PubMed]
  • Yu F, Morin X, Cai Y, Yang X, Chia W. Analysis of partner of inscuteable, a novel player of Drosophila asymmetric divisions, reveals two distinct steps in inscuteable apical localization. Cell. 2000 Feb 18;100(4):399–409. [PubMed]
  • Lackner MR, Nurrish SJ, Kaplan JM. Facilitation of synaptic transmission by EGL-30 Gqalpha and EGL-8 PLCbeta: DAG binding to UNC-13 is required to stimulate acetylcholine release. Neuron. 1999 Oct;24(2):335–346. [PubMed]
  • Zwaal RR, Ahringer J, van Luenen HG, Rushforth A, Anderson P, Plasterk RH. G proteins are required for spatial orientation of early cell cleavages in C. elegans embryos. Cell. 1996 Aug 23;86(4):619–629. [PubMed]
  • Lee L, Tirnauer JS, Li J, Schuyler SC, Liu JY, Pellman D. Positioning of the mitotic spindle by a cortical-microtubule capture mechanism. Science. 2000 Mar 24;287(5461):2260–2262. [PubMed]

Articles from Genetics are provided here courtesy of Genetics Society of America

Formats:

Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...

Links

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...