Skip to main content
PMC home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1993 May 2;121(4):775–783. doi: 10.1083/jcb.121.4.775

Oocyte maturation in starfish is mediated by the beta gamma-subunit complex of a G-protein

PMCID: PMC2119795  PMID: 8491771

Abstract

The stimulation of meiotic maturation of starfish oocytes by the hormone 1-methyladenine is mimicked by injection of beta gamma subunits of G-proteins from either retina or brain. Conversely, the hormone response is inhibited by injection of the GDP-bound forms of alpha i1 or alpha t subunits, or by injection of phosducin; all of these proteins should bind free beta gamma. alpha-subunit forms with reduced affinity for beta gamma (alpha i1 or alpha t bound to hydrolysis- resistant GTP analogs, or alpha i1-GMPPCP treated with trypsin to remove the amino terminus of the protein) are less effective inhibitors of 1-methyladenine action. These results indicate that the beta gamma subunit of a G-protein mediates 1-methyladenine stimulation of oocyte maturation.

Full Text

The Full Text of this article is available as a PDF (1.7 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Blank J. L., Brattain K. A., Exton J. H. Activation of cytosolic phosphoinositide phospholipase C by G-protein beta gamma subunits. J Biol Chem. 1992 Nov 15;267(32):23069–23075. [PubMed] [Google Scholar]
  2. Blumer K. J., Thorner J. Receptor-G protein signaling in yeast. Annu Rev Physiol. 1991;53:37–57. doi: 10.1146/annurev.ph.53.030191.000345. [DOI] [PubMed] [Google Scholar]
  3. Boyer J. L., Waldo G. L., Harden T. K. Beta gamma-subunit activation of G-protein-regulated phospholipase C. J Biol Chem. 1992 Dec 15;267(35):25451–25456. [PubMed] [Google Scholar]
  4. Camps M., Carozzi A., Schnabel P., Scheer A., Parker P. J., Gierschik P. Isozyme-selective stimulation of phospholipase C-beta 2 by G protein beta gamma-subunits. Nature. 1992 Dec 17;360(6405):684–686. doi: 10.1038/360684a0. [DOI] [PubMed] [Google Scholar]
  5. Camps M., Hou C., Sidiropoulos D., Stock J. B., Jakobs K. H., Gierschik P. Stimulation of phospholipase C by guanine-nucleotide-binding protein beta gamma subunits. Eur J Biochem. 1992 Jun 15;206(3):821–831. doi: 10.1111/j.1432-1033.1992.tb16990.x. [DOI] [PubMed] [Google Scholar]
  6. Carozzi A., Camps M., Gierschik P., Parker P. J. Activation of phosphatidylinositol lipid-specific phospholipase C-beta 3 by G-protein beta gamma subunits. FEBS Lett. 1993 Jan 11;315(3):340–342. doi: 10.1016/0014-5793(93)81190-b. [DOI] [PubMed] [Google Scholar]
  7. Carty D. J., Padrell E., Codina J., Birnbaumer L., Hildebrandt J. D., Iyengar R. Distinct guanine nucleotide binding and release properties of the three Gi proteins. J Biol Chem. 1990 Apr 15;265(11):6268–6273. [PubMed] [Google Scholar]
  8. Chiba K., Kado R. T., Jaffe L. A. Development of calcium release mechanisms during starfish oocyte maturation. Dev Biol. 1990 Aug;140(2):300–306. doi: 10.1016/0012-1606(90)90080-3. [DOI] [PubMed] [Google Scholar]
  9. Chiba K., Tadenuma H., Matsumoto M., Takahashi K., Katada T., Hoshi M. The primary structure of the alpha subunit of a starfish guanosine-nucleotide-binding regulatory protein involved in 1-methyladenine-induced oocyte maturation. Eur J Biochem. 1992 Aug 1;207(3):833–838. doi: 10.1111/j.1432-1033.1992.tb17114.x. [DOI] [PubMed] [Google Scholar]
  10. Dascal N., Ifune C., Hopkins R., Snutch T. P., Lübbert H., Davidson N., Simon M. I., Lester H. A. Involvement of a GTP-binding protein in mediation of serotonin and acetylcholine responses in Xenopus oocytes injected with rat brain messenger RNA. Brain Res. 1986 Dec;387(3):201–209. doi: 10.1016/0169-328x(86)90026-4. [DOI] [PubMed] [Google Scholar]
  11. Daya-Makin M., Pelech S. L., Levitzki A., Hudson A. T. Erbstatin and tyrphostins block protein-serine kinase activation and meiotic maturation of sea star oocytes. Biochim Biophys Acta. 1991 Jun 7;1093(1):87–94. doi: 10.1016/0167-4889(91)90142-k. [DOI] [PubMed] [Google Scholar]
  12. Dorée M., Kishimoto T., Le Peuch C. J., Demaille J. G., Kanatani H. Calcium-mediated transduction of the hormonal message in meiosis reinitiation of starfish oocytes: modulation following injection of cholera toxin and cAMP-dependent protein kinase. Exp Cell Res. 1981 Oct;135(2):237–249. doi: 10.1016/0014-4827(81)90159-2. [DOI] [PubMed] [Google Scholar]
  13. Duronio R. J., Jackson-Machelski E., Heuckeroth R. O., Olins P. O., Devine C. S., Yonemoto W., Slice L. W., Taylor S. S., Gordon J. I. Protein N-myristoylation in Escherichia coli: reconstitution of a eukaryotic protein modification in bacteria. Proc Natl Acad Sci U S A. 1990 Feb;87(4):1506–1510. doi: 10.1073/pnas.87.4.1506. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Eide B., Gierschik P., Milligan G., Mullaney I., Unson C., Goldsmith P., Spiegel A. GTP-binding proteins in brain and neutrophil are tethered to the plasma membrane via their amino termini. Biochem Biophys Res Commun. 1987 Nov 13;148(3):1398–1405. doi: 10.1016/s0006-291x(87)80287-5. [DOI] [PubMed] [Google Scholar]
  15. Federman A. D., Conklin B. R., Schrader K. A., Reed R. R., Bourne H. R. Hormonal stimulation of adenylyl cyclase through Gi-protein beta gamma subunits. Nature. 1992 Mar 12;356(6365):159–161. doi: 10.1038/356159a0. [DOI] [PubMed] [Google Scholar]
  16. Fukada Y., Takao T., Ohguro H., Yoshizawa T., Akino T., Shimonishi Y. Farnesylated gamma-subunit of photoreceptor G protein indispensable for GTP-binding. Nature. 1990 Aug 16;346(6285):658–660. doi: 10.1038/346658a0. [DOI] [PubMed] [Google Scholar]
  17. Fung B. K., Nash C. R. Characterization of transducin from bovine retinal rod outer segments. II. Evidence for distinct binding sites and conformational changes revealed by limited proteolysis with trypsin. J Biol Chem. 1983 Sep 10;258(17):10503–10510. [PubMed] [Google Scholar]
  18. Gao B. N., Gilman A. G. Cloning and expression of a widely distributed (type IV) adenylyl cyclase. Proc Natl Acad Sci U S A. 1991 Nov 15;88(22):10178–10182. doi: 10.1073/pnas.88.22.10178. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Gilman A. G. G proteins: transducers of receptor-generated signals. Annu Rev Biochem. 1987;56:615–649. doi: 10.1146/annurev.bi.56.070187.003151. [DOI] [PubMed] [Google Scholar]
  20. Guerrier P., Doree M. Hormonal control of reinitiation of meiosis in starfish. The requirement of 1-methyladenine during nuclear maturation. Dev Biol. 1975 Dec;47(2):341–348. doi: 10.1016/0012-1606(75)90288-2. [DOI] [PubMed] [Google Scholar]
  21. Haga K., Haga T. Activation by G protein beta gamma subunits of agonist- or light-dependent phosphorylation of muscarinic acetylcholine receptors and rhodopsin. J Biol Chem. 1992 Feb 5;267(4):2222–2227. [PubMed] [Google Scholar]
  22. Hekman M., Holzhöfer A., Gierschik P., Im M. J., Jakobs K. H., Pfeuffer T., Helmreich E. J. Regulation of signal transfer from beta 1-adrenoceptor to adenylate cyclase by beta gamma subunits in a reconstituted system. Eur J Biochem. 1987 Dec 1;169(2):431–439. doi: 10.1111/j.1432-1033.1987.tb13630.x. [DOI] [PubMed] [Google Scholar]
  23. Hiramoto Y. A method of microinjection. Exp Cell Res. 1974 Aug;87(2):403–406. doi: 10.1016/0014-4827(74)90503-5. [DOI] [PubMed] [Google Scholar]
  24. Ito H., Tung R. T., Sugimoto T., Kobayashi I., Takahashi K., Katada T., Ui M., Kurachi Y. On the mechanism of G protein beta gamma subunit activation of the muscarinic K+ channel in guinea pig atrial cell membrane. Comparison with the ATP-sensitive K+ channel. J Gen Physiol. 1992 Jun;99(6):961–983. doi: 10.1085/jgp.99.6.961. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Iñiguez-Lluhi J. A., Simon M. I., Robishaw J. D., Gilman A. G. G protein beta gamma subunits synthesized in Sf9 cells. Functional characterization and the significance of prenylation of gamma. J Biol Chem. 1992 Nov 15;267(32):23409–23417. [PubMed] [Google Scholar]
  26. Jelsema C. L., Axelrod J. Stimulation of phospholipase A2 activity in bovine rod outer segments by the beta gamma subunits of transducin and its inhibition by the alpha subunit. Proc Natl Acad Sci U S A. 1987 Jun;84(11):3623–3627. doi: 10.1073/pnas.84.11.3623. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Jones T. L., Simonds W. F., Merendino J. J., Jr, Brann M. R., Spiegel A. M. Myristoylation of an inhibitory GTP-binding protein alpha subunit is essential for its membrane attachment. Proc Natl Acad Sci U S A. 1990 Jan;87(2):568–572. doi: 10.1073/pnas.87.2.568. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Jones T. L., Woodard C., Spiegel A. M. Baculovirus expression and purification of a soluble, mutant G-protein alpha subunit. Protein Expr Purif. 1993 Feb;4(1):64–71. doi: 10.1006/prep.1993.1010. [DOI] [PubMed] [Google Scholar]
  29. Kanatani H., Hiramoto Y. Site of action of 1-methyladenine in inducing oocyte maturation in starfish. Exp Cell Res. 1970 Aug;61(2):280–284. doi: 10.1016/0014-4827(70)90448-9. [DOI] [PubMed] [Google Scholar]
  30. Kanatani H., Shirai H., Nakanishi K., Kurokawa T. Isolation and indentification on meiosis inducing substance in starfish Asterias amurensis. Nature. 1969 Jan 18;221(5177):273–274. doi: 10.1038/221273a0. [DOI] [PubMed] [Google Scholar]
  31. Katada T., Kusakabe K., Oinuma M., Ui M. A novel mechanism for the inhibition of adenylate cyclase via inhibitory GTP-binding proteins. Calmodulin-dependent inhibition of the cyclase catalyst by the beta gamma-subunits of GTP-binding proteins. J Biol Chem. 1987 Sep 5;262(25):11897–11900. [PubMed] [Google Scholar]
  32. Katz A., Wu D., Simon M. I. Subunits beta gamma of heterotrimeric G protein activate beta 2 isoform of phospholipase C. Nature. 1992 Dec 17;360(6405):686–689. doi: 10.1038/360686a0. [DOI] [PubMed] [Google Scholar]
  33. Kiehart D. P. Microinjection of echinoderm eggs: apparatus and procedures. Methods Cell Biol. 1982;25(Pt B):13–31. doi: 10.1016/s0091-679x(08)61418-1. [DOI] [PubMed] [Google Scholar]
  34. Kim D., Lewis D. L., Graziadei L., Neer E. J., Bar-Sagi D., Clapham D. E. G-protein beta gamma-subunits activate the cardiac muscarinic K+-channel via phospholipase A2. Nature. 1989 Feb 9;337(6207):557–560. doi: 10.1038/337557a0. [DOI] [PubMed] [Google Scholar]
  35. Kishimoto T., Kanatani H. Cytoplasmic factor responsible for germinal vesicle breakdown and meiotic maturation in starfish oocyte. Nature. 1976 Mar 25;260(5549):321–322. doi: 10.1038/260321a0. [DOI] [PubMed] [Google Scholar]
  36. Kishimoto T. Microinjection and cytoplasmic transfer in starfish oocytes. Methods Cell Biol. 1986;27:379–394. doi: 10.1016/s0091-679x(08)60359-3. [DOI] [PubMed] [Google Scholar]
  37. Kishimoto T., Usui N., Kanatani H. Breakdown of starfish ovarian follicle induced by maturation-promoting factor. Dev Biol. 1984 Jan;101(1):28–34. doi: 10.1016/0012-1606(84)90113-1. [DOI] [PubMed] [Google Scholar]
  38. Kobayashi H., Golsteyn R., Poon R., Stewart E., Gannon J., Minshull J., Smith R., Hunt T. Cyclins and their partners during Xenopus oocyte maturation. Cold Spring Harb Symp Quant Biol. 1991;56:437–447. doi: 10.1101/sqb.1991.056.01.051. [DOI] [PubMed] [Google Scholar]
  39. Kohnken R. E., Hildebrandt J. D. G protein subunit interactions. Studies with biotinylated G protein subunits. J Biol Chem. 1989 Dec 5;264(34):20688–20696. [PubMed] [Google Scholar]
  40. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  41. Leberer E., Dignard D., Harcus D., Thomas D. Y., Whiteway M. The protein kinase homologue Ste20p is required to link the yeast pheromone response G-protein beta gamma subunits to downstream signalling components. EMBO J. 1992 Dec;11(13):4815–4824. doi: 10.1002/j.1460-2075.1992.tb05587.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Leberer E., Dignard D., Hougan L., Thomas D. Y., Whiteway M. Dominant-negative mutants of a yeast G-protein beta subunit identify two functional regions involved in pheromone signalling. EMBO J. 1992 Dec;11(13):4805–4813. doi: 10.1002/j.1460-2075.1992.tb05586.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Lee R. H., Lieberman B. S., Lolley R. N. A novel complex from bovine visual cells of a 33,000-dalton phosphoprotein with beta- and gamma-transducin: purification and subunit structure. Biochemistry. 1987 Jun 30;26(13):3983–3990. doi: 10.1021/bi00387a036. [DOI] [PubMed] [Google Scholar]
  44. Lee R. H., Ting T. D., Lieberman B. S., Tobias D. E., Lolley R. N., Ho Y. K. Regulation of retinal cGMP cascade by phosducin in bovine rod photoreceptor cells. Interaction of phosducin and transducin. J Biol Chem. 1992 Dec 15;267(35):25104–25112. [PubMed] [Google Scholar]
  45. Linder M. E., Ewald D. A., Miller R. J., Gilman A. G. Purification and characterization of Go alpha and three types of Gi alpha after expression in Escherichia coli. J Biol Chem. 1990 May 15;265(14):8243–8251. [PubMed] [Google Scholar]
  46. Linder M. E., Pang I. H., Duronio R. J., Gordon J. I., Sternweis P. C., Gilman A. G. Lipid modifications of G protein subunits. Myristoylation of Go alpha increases its affinity for beta gamma. J Biol Chem. 1991 Mar 5;266(7):4654–4659. [PubMed] [Google Scholar]
  47. Logothetis D. E., Kurachi Y., Galper J., Neer E. J., Clapham D. E. The beta gamma subunits of GTP-binding proteins activate the muscarinic K+ channel in heart. Nature. 1987 Jan 22;325(6102):321–326. doi: 10.1038/325321a0. [DOI] [PubMed] [Google Scholar]
  48. Mangels L. A., Neubig R. R., Hamm H. E., Gnegy M. E. Calmodulin binding distinguishes between beta gamma subunits of activated G proteins and transducin. Biochem J. 1992 May 1;283(Pt 3):683–690. doi: 10.1042/bj2830683. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Masui Y., Clarke H. J. Oocyte maturation. Int Rev Cytol. 1979;57:185–282. doi: 10.1016/s0074-7696(08)61464-3. [DOI] [PubMed] [Google Scholar]
  50. Meijer L., Arion D. Negative control of cdc2 kinase activation by cAMP in starfish oocytes. Cold Spring Harb Symp Quant Biol. 1991;56:591–598. doi: 10.1101/sqb.1991.056.01.067. [DOI] [PubMed] [Google Scholar]
  51. Meijer L., Dostmann W., Genieser H. G., Butt E., Jastorff B. Starfish oocyte maturation: evidence for a cyclic AMP-dependent inhibitory pathway. Dev Biol. 1989 May;133(1):58–66. doi: 10.1016/0012-1606(89)90296-0. [DOI] [PubMed] [Google Scholar]
  52. Meijer L., Zarutskie P. Starfish oocyte maturation: 1-methyladenine triggers a drop of cAMP concentration related to the hormone-dependent period. Dev Biol. 1987 Jun;121(2):306–315. doi: 10.1016/0012-1606(87)90166-7. [DOI] [PubMed] [Google Scholar]
  53. Miyazaki S. I., Ohmori H., Sasaki S. Potassium rectifications of the starfish oocyte membrane and their changes during oocyte maturation. J Physiol. 1975 Mar;246(1):55–78. doi: 10.1113/jphysiol.1975.sp010880. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Moriarty T. M., Gillo B., Carty D. J., Premont R. T., Landau E. M., Iyengar R. Beta gamma subunits of GTP-binding proteins inhibit muscarinic receptor stimulation of phospholipase C. Proc Natl Acad Sci U S A. 1988 Dec;85(23):8865–8869. doi: 10.1073/pnas.85.23.8865. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Mumby S. M., Casey P. J., Gilman A. G., Gutowski S., Sternweis P. C. G protein gamma subunits contain a 20-carbon isoprenoid. Proc Natl Acad Sci U S A. 1990 Aug;87(15):5873–5877. doi: 10.1073/pnas.87.15.5873. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Muntz K. H., Sternweis P. C., Gilman A. G., Mumby S. M. Influence of gamma subunit prenylation on association of guanine nucleotide-binding regulatory proteins with membranes. Mol Biol Cell. 1992 Jan;3(1):49–61. doi: 10.1091/mbc.3.1.49. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Murakami T., Simonds W. F., Spiegel A. M. Site-specific antibodies directed against G protein beta and gamma subunits: effects on alpha and beta gamma subunit interaction. Biochemistry. 1992 Mar 24;31(11):2905–2911. doi: 10.1021/bi00126a009. [DOI] [PubMed] [Google Scholar]
  58. Navon S. E., Fung B. K. Characterization of transducin from bovine retinal rod outer segments. Participation of the amino-terminal region of T alpha in subunit interaction. J Biol Chem. 1987 Nov 15;262(32):15746–15751. [PubMed] [Google Scholar]
  59. Neer E. J., Pulsifer L., Wolf L. G. The amino terminus of G protein alpha subunits is required for interaction with beta gamma. J Biol Chem. 1988 Jun 25;263(18):8996–8970. [PubMed] [Google Scholar]
  60. Otto J. J., Schroeder T. E. Assembly-disassembly of actin bundles in starfish oocytes: an analysis of actin-associated proteins in the isolated cortex. Dev Biol. 1984 Feb;101(2):263–273. doi: 10.1016/0012-1606(84)90140-4. [DOI] [PubMed] [Google Scholar]
  61. Peaucellier G., Andersen A. C., Kinsey W. H. Protein tyrosine phosphorylation during meiotic divisions of starfish oocytes. Dev Biol. 1990 Apr;138(2):391–399. doi: 10.1016/0012-1606(90)90205-w. [DOI] [PubMed] [Google Scholar]
  62. Pelech S. L., Tombes R. M., Meijer L., Krebs E. G. Activation of myelin basic protein kinases during echinoderm oocyte maturation and egg fertilization. Dev Biol. 1988 Nov;130(1):28–36. doi: 10.1016/0012-1606(88)90410-1. [DOI] [PubMed] [Google Scholar]
  63. Phillips W. J., Cerione R. A. Labeling of the beta gamma subunit complex of transducin with an environmentally sensitive cysteine reagent. Use of fluorescence spectroscopy to monitor transducin subunit interactions. J Biol Chem. 1991 Jun 15;266(17):11017–11024. [PubMed] [Google Scholar]
  64. Picard A., Labbé J. C., Barakat H., Cavadore J. C., Dorée M. Okadaic acid mimics a nuclear component required for cyclin B-cdc2 kinase microinjection to drive starfish oocytes into M phase. J Cell Biol. 1991 Oct;115(2):337–344. doi: 10.1083/jcb.115.2.337. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Pitcher J. A., Inglese J., Higgins J. B., Arriza J. L., Casey P. J., Kim C., Benovic J. L., Kwatra M. M., Caron M. G., Lefkowitz R. J. Role of beta gamma subunits of G proteins in targeting the beta-adrenergic receptor kinase to membrane-bound receptors. Science. 1992 Aug 28;257(5074):1264–1267. doi: 10.1126/science.1325672. [DOI] [PubMed] [Google Scholar]
  66. Pondaven P., Meijer L., Beach D. Activation of M-phase-specific histone H1 kinase by modification of the phosphorylation of its p34cdc2 and cyclin components. Genes Dev. 1990 Jan;4(1):9–17. doi: 10.1101/gad.4.1.9. [DOI] [PubMed] [Google Scholar]
  67. Ruderman J., Luca F., Shibuya E., Gavin K., Boulton T., Cobb M. Control of the cell cycle in early embryos. Cold Spring Harb Symp Quant Biol. 1991;56:495–502. doi: 10.1101/sqb.1991.056.01.056. [DOI] [PubMed] [Google Scholar]
  68. Sadler S. E., Maller J. L. Inhibition of Xenopus oocyte adenylate cyclase by progesterone: a novel mechanism of action. Adv Cyclic Nucleotide Protein Phosphorylation Res. 1985;19:179–194. [PubMed] [Google Scholar]
  69. Sanghera J. S., Paddon H. B., Pelech S. L. Role of protein phosphorylation in the maturation-induced activation of a myelin basic protein kinase from sea star oocytes. J Biol Chem. 1991 Apr 15;266(11):6700–6707. [PubMed] [Google Scholar]
  70. Sawada M. T., Someno T., Hoshi M., Sawada H. Participation of 650-kDa protease (20 S proteasome) in starfish oocyte maturation. Dev Biol. 1992 Apr;150(2):414–418. doi: 10.1016/0012-1606(92)90252-c. [DOI] [PubMed] [Google Scholar]
  71. Schroeder T. E., Otto J. J. Cyclic assembly-disassembly of cortical microtubules during maturation and early development of starfish oocytes. Dev Biol. 1984 Jun;103(2):493–503. doi: 10.1016/0012-1606(84)90336-1. [DOI] [PubMed] [Google Scholar]
  72. Schroeder T. E., Stricker S. A. Morphological changes during maturation of starfish oocytes: surface ultrastructure and cortical actin. Dev Biol. 1983 Aug;98(2):373–384. doi: 10.1016/0012-1606(83)90366-4. [DOI] [PubMed] [Google Scholar]
  73. Schägger H., von Jagow G. Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal Biochem. 1987 Nov 1;166(2):368–379. doi: 10.1016/0003-2697(87)90587-2. [DOI] [PubMed] [Google Scholar]
  74. Shilling F., Chiba K., Hoshi M., Kishimoto T., Jaffe L. A. Pertussis toxin inhibits 1-methyladenine-induced maturation in starfish oocytes. Dev Biol. 1989 Jun;133(2):605–608. doi: 10.1016/0012-1606(89)90063-8. [DOI] [PubMed] [Google Scholar]
  75. Simoncini L., Moody W. J. Changes in voltage-dependent currents and membrane area during maturation of starfish oocytes: species differences and similarities. Dev Biol. 1990 Mar;138(1):194–201. doi: 10.1016/0012-1606(90)90189-p. [DOI] [PubMed] [Google Scholar]
  76. Simonds W. F., Goldsmith P. K., Codina J., Unson C. G., Spiegel A. M. Gi2 mediates alpha 2-adrenergic inhibition of adenylyl cyclase in platelet membranes: in situ identification with G alpha C-terminal antibodies. Proc Natl Acad Sci U S A. 1989 Oct;86(20):7809–7813. doi: 10.1073/pnas.86.20.7809. [DOI] [PMC free article] [PubMed] [Google Scholar]
  77. Smith L. D. The induction of oocyte maturation: transmembrane signaling events and regulation of the cell cycle. Development. 1989 Dec;107(4):685–699. doi: 10.1242/dev.107.4.685. [DOI] [PubMed] [Google Scholar]
  78. Spiegel A. M., Backlund P. S., Jr, Butrynski J. E., Jones T. L., Simonds W. F. The G protein connection: molecular basis of membrane association. Trends Biochem Sci. 1991 Sep;16(9):338–341. doi: 10.1016/0968-0004(91)90139-m. [DOI] [PubMed] [Google Scholar]
  79. Sternweis P. C., Robishaw J. D. Isolation of two proteins with high affinity for guanine nucleotides from membranes of bovine brain. J Biol Chem. 1984 Nov 25;259(22):13806–13813. [PubMed] [Google Scholar]
  80. Tadenuma H., Chiba K., Takahashi K., Hoshi M., Katada T. Purification and characterization of a GTP-binding protein serving as pertussis toxin substrate in starfish oocytes. Arch Biochem Biophys. 1991 Nov 1;290(2):411–417. doi: 10.1016/0003-9861(91)90560-6. [DOI] [PubMed] [Google Scholar]
  81. Tadenuma H., Takahashi K., Chiba K., Hoshi M., Katada T. Properties of 1-methyladenine receptors in starfish oocyte membranes: involvement of pertussis toxin-sensitive GTP-binding protein in the receptor-mediated signal transduction. Biochem Biophys Res Commun. 1992 Jul 15;186(1):114–121. doi: 10.1016/s0006-291x(05)80782-x. [DOI] [PubMed] [Google Scholar]
  82. Tang W. J., Gilman A. G. Type-specific regulation of adenylyl cyclase by G protein beta gamma subunits. Science. 1991 Dec 6;254(5037):1500–1503. doi: 10.1126/science.1962211. [DOI] [PubMed] [Google Scholar]
  83. Tang W. J., Krupinski J., Gilman A. G. Expression and characterization of calmodulin-activated (type I) adenylylcyclase. J Biol Chem. 1991 May 5;266(13):8595–8603. [PubMed] [Google Scholar]
  84. Taussig R., Quarmby L. M., Gilman A. G. Regulation of purified type I and type II adenylylcyclases by G protein beta gamma subunits. J Biol Chem. 1993 Jan 5;268(1):9–12. [PubMed] [Google Scholar]
  85. Witchel H. J., Steinhardt R. A. 1-Methyladenine can consistently induce a fura-detectable transient calcium increase which is neither necessary nor sufficient for maturation in oocytes of the starfish Asterina miniata. Dev Biol. 1990 Oct;141(2):393–398. doi: 10.1016/0012-1606(90)90393-w. [DOI] [PubMed] [Google Scholar]
  86. Yatani A., Codina J., Brown A. M., Birnbaumer L. Direct activation of mammalian atrial muscarinic potassium channels by GTP regulatory protein Gk. Science. 1987 Jan 9;235(4785):207–211. doi: 10.1126/science.2432660. [DOI] [PubMed] [Google Scholar]
  87. Yatani A., Mattera R., Codina J., Graf R., Okabe K., Padrell E., Iyengar R., Brown A. M., Birnbaumer L. The G protein-gated atrial K+ channel is stimulated by three distinct Gi alpha-subunits. Nature. 1988 Dec 15;336(6200):680–682. doi: 10.1038/336680a0. [DOI] [PubMed] [Google Scholar]
  88. Yoshikuni M., Ishikawa K., Isobe M., Goto T., Nagahama Y. Characterization of 1-methyladenine binding in starfish oocyte cortices. Proc Natl Acad Sci U S A. 1988 Mar;85(6):1874–1877. doi: 10.1073/pnas.85.6.1874. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES