Skip to main content
PMC home page
The EMBO Journal logoLink to The EMBO Journal
. 1998 Oct 1;17(19):5627–5637. doi: 10.1093/emboj/17.19.5627

The kinase Eg2 is a component of the Xenopus oocyte progesterone-activated signaling pathway.

T Andrésson 1, J V Ruderman 1
PMCID: PMC1170891  PMID: 9755163

Abstract

Quiescent Xenopus oocytes are activated by progesterone, which binds to an unidentified surface-associated receptor. Progesterone activates a poorly understood signaling pathway that results in the translational activation of mRNA encoding Mos, a MAP kinase kinase kinase necessary for the activation of MAP kinase and MPF, the resumption of meiosis, and maturation of the oocyte into the sperm-responsive egg. We have designed a screen to identify early signaling proteins based on the premise that some of these proteins would be phosphorylated or otherwise modified within minutes of progesterone addition. This screen has revealed Eg2, a Ser/Thr kinase. We find that Eg2 is phosphorylated soon after progesterone stimulation and provide evidence that it functions in the signaling pathway. Overexpression of Eg2 via mRNA microinjection shortens the time between progesterone stimulation and the appearance of new Mos protein, accelerates activation of MAP kinase and advances entry into the meiotic cell cycle. Finally, overexpression of Eg2 dramatically reduces the concentration of progesterone needed to trigger oocyte activation. These results argue that the kinase Eg2 is a component of the progesterone-activated signaling pathway that releases frog oocytes from cell cycle arrest.

Full Text

The Full Text of this article is available as a PDF (510.1 KB).

Selected References

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

  1. Ballantyne S., Bilger A., Astrom J., Virtanen A., Wickens M. Poly (A) polymerases in the nucleus and cytoplasm of frog oocytes: dynamic changes during oocyte maturation and early development. RNA. 1995 Mar;1(1):64–78. [PMC free article] [PubMed] [Google Scholar]
  2. Ballantyne S., Daniel D. L., Jr, Wickens M. A dependent pathway of cytoplasmic polyadenylation reactions linked to cell cycle control by c-mos and CDK1 activation. Mol Biol Cell. 1997 Aug;8(8):1633–1648. doi: 10.1091/mbc.8.8.1633. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Beato M., Sánchez-Pacheco A. Interaction of steroid hormone receptors with the transcription initiation complex. Endocr Rev. 1996 Dec;17(6):587–609. doi: 10.1210/edrv-17-6-587. [DOI] [PubMed] [Google Scholar]
  4. Chan C. S., Botstein D. Isolation and characterization of chromosome-gain and increase-in-ploidy mutants in yeast. Genetics. 1993 Nov;135(3):677–691. doi: 10.1093/genetics/135.3.677. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cheatham L., Monfar M., Chou M. M., Blenis J. Structural and functional analysis of pp70S6k. Proc Natl Acad Sci U S A. 1995 Dec 5;92(25):11696–11700. doi: 10.1073/pnas.92.25.11696. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Chen M., Cooper J. A. Ser-3 is important for regulating Mos interaction with and stimulation of mitogen-activated protein kinase kinase. Mol Cell Biol. 1995 Sep;15(9):4727–4734. doi: 10.1128/mcb.15.9.4727. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Chen M., Cooper J. A. The beta subunit of CKII negatively regulates Xenopus oocyte maturation. Proc Natl Acad Sci U S A. 1997 Aug 19;94(17):9136–9140. doi: 10.1073/pnas.94.17.9136. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Chen M., Li D., Krebs E. G., Cooper J. A. The casein kinase II beta subunit binds to Mos and inhibits Mos activity. Mol Cell Biol. 1997 Apr;17(4):1904–1912. doi: 10.1128/mcb.17.4.1904. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Coleman T. R., Dunphy W. G. Cdc2 regulatory factors. Curr Opin Cell Biol. 1994 Dec;6(6):877–882. doi: 10.1016/0955-0674(94)90060-4. [DOI] [PubMed] [Google Scholar]
  10. Cork R. J., Robinson K. R. Second messenger signalling during hormone-induced Xenopus oocyte maturation. Zygote. 1994 Nov;2(4):289–299. doi: 10.1017/s0967199400002112. [DOI] [PubMed] [Google Scholar]
  11. Daar I., Yew N., Vande Woude G. F. Inhibition of mos-induced oocyte maturation by protein kinase A. J Cell Biol. 1993 Mar;120(5):1197–1202. doi: 10.1083/jcb.120.5.1197. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Deshpande A. K., Kung H. F. Insulin induction of Xenopus laevis oocyte maturation is inhibited by monoclonal antibody against p21 ras proteins. Mol Cell Biol. 1987 Mar;7(3):1285–1288. doi: 10.1128/mcb.7.3.1285. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Evans J. P., Kay B. K. Biochemical fractionation of oocytes. Methods Cell Biol. 1991;36:133–148. doi: 10.1016/s0091-679x(08)60275-7. [DOI] [PubMed] [Google Scholar]
  14. Fabian J. R., Morrison D. K., Daar I. O. Requirement for Raf and MAP kinase function during the meiotic maturation of Xenopus oocytes. J Cell Biol. 1993 Aug;122(3):645–652. doi: 10.1083/jcb.122.3.645. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Ferrell J. E., Jr, Machleder E. M. The biochemical basis of an all-or-none cell fate switch in Xenopus oocytes. Science. 1998 May 8;280(5365):895–898. doi: 10.1126/science.280.5365.895. [DOI] [PubMed] [Google Scholar]
  16. Ferrell J. E., Jr, Wu M., Gerhart J. C., Martin G. S. Cell cycle tyrosine phosphorylation of p34cdc2 and a microtubule-associated protein kinase homolog in Xenopus oocytes and eggs. Mol Cell Biol. 1991 Apr;11(4):1965–1971. doi: 10.1128/mcb.11.4.1965. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Finidori-Lepicard J., Schorderet-Slatkine S., Hanoune J., Baulieu E. E. Progesterone inhibits membrane-bound adenylate cyclase in Xenopus laevis oocytes. Nature. 1981 Jul 16;292(5820):255–257. doi: 10.1038/292255a0. [DOI] [PubMed] [Google Scholar]
  18. Freeman R. S., Pickham K. M., Kanki J. P., Lee B. A., Pena S. V., Donoghue D. J. Xenopus homolog of the mos protooncogene transforms mammalian fibroblasts and induces maturation of Xenopus oocytes. Proc Natl Acad Sci U S A. 1989 Aug;86(15):5805–5809. doi: 10.1073/pnas.86.15.5805. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Gard D. L., Hafezi S., Zhang T., Doxsey S. J. Centrosome duplication continues in cycloheximide-treated Xenopus blastulae in the absence of a detectable cell cycle. J Cell Biol. 1990 Jun;110(6):2033–2042. doi: 10.1083/jcb.110.6.2033. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Gard D. L. Organization, nucleation, and acetylation of microtubules in Xenopus laevis oocytes: a study by confocal immunofluorescence microscopy. Dev Biol. 1991 Feb;143(2):346–362. doi: 10.1016/0012-1606(91)90085-h. [DOI] [PubMed] [Google Scholar]
  21. Gebauer F., Richter J. D. Synthesis and function of Mos: the control switch of vertebrate oocyte meiosis. Bioessays. 1997 Jan;19(1):23–28. doi: 10.1002/bies.950190106. [DOI] [PubMed] [Google Scholar]
  22. Glover D. M., Leibowitz M. H., McLean D. A., Parry H. Mutations in aurora prevent centrosome separation leading to the formation of monopolar spindles. Cell. 1995 Apr 7;81(1):95–105. doi: 10.1016/0092-8674(95)90374-7. [DOI] [PubMed] [Google Scholar]
  23. Gopalan G., Chan C. S., Donovan P. J. A novel mammalian, mitotic spindle-associated kinase is related to yeast and fly chromosome segregation regulators. J Cell Biol. 1997 Aug 11;138(3):643–656. doi: 10.1083/jcb.138.3.643. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Gotoh Y., Masuyama N., Dell K., Shirakabe K., Nishida E. Initiation of Xenopus oocyte maturation by activation of the mitogen-activated protein kinase cascade. J Biol Chem. 1995 Oct 27;270(43):25898–25904. doi: 10.1074/jbc.270.43.25898. [DOI] [PubMed] [Google Scholar]
  25. Gotoh Y., Moriyama K., Matsuda S., Okumura E., Kishimoto T., Kawasaki H., Suzuki K., Yahara I., Sakai H., Nishida E. Xenopus M phase MAP kinase: isolation of its cDNA and activation by MPF. EMBO J. 1991 Sep;10(9):2661–2668. doi: 10.1002/j.1460-2075.1991.tb07809.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Grazzini E., Guillon G., Mouillac B., Zingg H. H. Inhibition of oxytocin receptor function by direct binding of progesterone. Nature. 1998 Apr 2;392(6675):509–512. doi: 10.1038/33176. [DOI] [PubMed] [Google Scholar]
  27. Hershko A. Roles of ubiquitin-mediated proteolysis in cell cycle control. Curr Opin Cell Biol. 1997 Dec;9(6):788–799. doi: 10.1016/s0955-0674(97)80079-8. [DOI] [PubMed] [Google Scholar]
  28. Huang C. Y., Ferrell J. E., Jr Ultrasensitivity in the mitogen-activated protein kinase cascade. Proc Natl Acad Sci U S A. 1996 Sep 17;93(19):10078–10083. doi: 10.1073/pnas.93.19.10078. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Katzenellenbogen J. A., O'Malley B. W., Katzenellenbogen B. S. Tripartite steroid hormone receptor pharmacology: interaction with multiple effector sites as a basis for the cell- and promoter-specific action of these hormones. Mol Endocrinol. 1996 Feb;10(2):119–131. doi: 10.1210/mend.10.2.8825552. [DOI] [PubMed] [Google Scholar]
  30. Kimura M., Kotani S., Hattori T., Sumi N., Yoshioka T., Todokoro K., Okano Y. Cell cycle-dependent expression and spindle pole localization of a novel human protein kinase, Aik, related to Aurora of Drosophila and yeast Ipl1. J Biol Chem. 1997 May 23;272(21):13766–13771. doi: 10.1074/jbc.272.21.13766. [DOI] [PubMed] [Google Scholar]
  31. Korn L. J., Siebel C. W., McCormick F., Roth R. A. Ras p21 as a potential mediator of insulin action in Xenopus oocytes. Science. 1987 May 15;236(4803):840–843. doi: 10.1126/science.3554510. [DOI] [PubMed] [Google Scholar]
  32. Lane H. A., Morley S. J., Dorée M., Kozma S. C., Thomas G. Identification and early activation of a Xenopus laevis p70s6k following progesterone-induced meiotic maturation. EMBO J. 1992 May;11(5):1743–1749. doi: 10.1002/j.1460-2075.1992.tb05226.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Lim P. S., Jenson A. B., Cowsert L., Nakai Y., Lim L. Y., Jin X. W., Sundberg J. P. Distribution and specific identification of papillomavirus major capsid protein epitopes by immunocytochemistry and epitope scanning of synthetic peptides. J Infect Dis. 1990 Dec;162(6):1263–1269. doi: 10.1093/infdis/162.6.1263. [DOI] [PubMed] [Google Scholar]
  34. Liu X. J., Sorisky A., Zhu L., Pawson T. Molecular cloning of an amphibian insulin receptor substrate 1-like cDNA and involvement of phosphatidylinositol 3-kinase in insulin-induced Xenopus oocyte maturation. Mol Cell Biol. 1995 Jul;15(7):3563–3570. doi: 10.1128/mcb.15.7.3563. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Maller J. L., Koontz J. W. A study of the induction of cell division in amphibian oocytes by insulin. Dev Biol. 1981 Jul 30;85(2):309–316. doi: 10.1016/0012-1606(81)90262-1. [DOI] [PubMed] [Google Scholar]
  36. Maller J. L., Krebs E. G. Progesterone-stimulated meiotic cell division in Xenopus oocytes. Induction by regulatory subunit and inhibition by catalytic subunit of adenosine 3':5'-monophosphate-dependent protein kinase. J Biol Chem. 1977 Mar 10;252(5):1712–1718. [PubMed] [Google Scholar]
  37. Mangelsdorf D. J., Thummel C., Beato M., Herrlich P., Schütz G., Umesono K., Blumberg B., Kastner P., Mark M., Chambon P. The nuclear receptor superfamily: the second decade. Cell. 1995 Dec 15;83(6):835–839. doi: 10.1016/0092-8674(95)90199-x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Masui Y. Relative roles of the pituitary, follicle cells, and progesterone in the induction of oocyte maturation in Rana pipiens. J Exp Zool. 1967 Dec;166(3):365–375. doi: 10.1002/jez.1401660309. [DOI] [PubMed] [Google Scholar]
  39. Matten W. T., Copeland T. D., Ahn N. G., Vande Woude G. F. Positive feedback between MAP kinase and Mos during Xenopus oocyte maturation. Dev Biol. 1996 Nov 1;179(2):485–492. doi: 10.1006/dbio.1996.0277. [DOI] [PubMed] [Google Scholar]
  40. Matten W., Daar I., Vande Woude G. F. Protein kinase A acts at multiple points to inhibit Xenopus oocyte maturation. Mol Cell Biol. 1994 Jul;14(7):4419–4426. doi: 10.1128/mcb.14.7.4419. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. McGrew L. L., Richter J. D. Translational control by cytoplasmic polyadenylation during Xenopus oocyte maturation: characterization of cis and trans elements and regulation by cyclin/MPF. EMBO J. 1990 Nov;9(11):3743–3751. doi: 10.1002/j.1460-2075.1990.tb07587.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Migliaccio A., Di Domenico M., Castoria G., de Falco A., Bontempo P., Nola E., Auricchio F. Tyrosine kinase/p21ras/MAP-kinase pathway activation by estradiol-receptor complex in MCF-7 cells. EMBO J. 1996 Mar 15;15(6):1292–1300. [PMC free article] [PubMed] [Google Scholar]
  43. Migliaccio A., Piccolo D., Castoria G., Di Domenico M., Bilancio A., Lombardi M., Gong W., Beato M., Auricchio F. Activation of the Src/p21ras/Erk pathway by progesterone receptor via cross-talk with estrogen receptor. EMBO J. 1998 Apr 1;17(7):2008–2018. doi: 10.1093/emboj/17.7.2008. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Moritz M., Braunfeld M. B., Sedat J. W., Alberts B., Agard D. A. Microtubule nucleation by gamma-tubulin-containing rings in the centrosome. Nature. 1995 Dec 7;378(6557):638–640. doi: 10.1038/378638a0. [DOI] [PubMed] [Google Scholar]
  45. Morley S. J., Pain V. M. Hormone-induced meiotic maturation in Xenopus oocytes occurs independently of p70s6k activation and is associated with enhanced initiation factor (eIF)-4F phosphorylation and complex formation. J Cell Sci. 1995 Apr;108(Pt 4):1751–1760. doi: 10.1242/jcs.108.4.1751. [DOI] [PubMed] [Google Scholar]
  46. Muslin A. J., MacNicol A. M., Williams L. T. Raf-1 protein kinase is important for progesterone-induced Xenopus oocyte maturation and acts downstream of mos. Mol Cell Biol. 1993 Jul;13(7):4197–4202. doi: 10.1128/mcb.13.7.4197. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Nebreda A. R., Hunt T. The c-mos proto-oncogene protein kinase turns on and maintains the activity of MAP kinase, but not MPF, in cell-free extracts of Xenopus oocytes and eggs. EMBO J. 1993 May;12(5):1979–1986. doi: 10.1002/j.1460-2075.1993.tb05847.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Neer E. J., Schmidt C. J., Nambudripad R., Smith T. F. The ancient regulatory-protein family of WD-repeat proteins. Nature. 1994 Sep 22;371(6495):297–300. doi: 10.1038/371297a0. [DOI] [PubMed] [Google Scholar]
  49. Nishizawa M., Furuno N., Okazaki K., Tanaka H., Ogawa Y., Sagata N. Degradation of Mos by the N-terminal proline (Pro2)-dependent ubiquitin pathway on fertilization of Xenopus eggs: possible significance of natural selection for Pro2 in Mos. EMBO J. 1993 Oct;12(10):4021–4027. doi: 10.1002/j.1460-2075.1993.tb06080.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Nishizawa M., Okazaki K., Furuno N., Watanabe N., Sagata N. The 'second-codon rule' and autophosphorylation govern the stability and activity of Mos during the meiotic cell cycle in Xenopus oocytes. EMBO J. 1992 Jul;11(7):2433–2446. doi: 10.1002/j.1460-2075.1992.tb05308.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Oakley B. R., Oakley C. E., Yoon Y., Jung M. K. Gamma-tubulin is a component of the spindle pole body that is essential for microtubule function in Aspergillus nidulans. Cell. 1990 Jun 29;61(7):1289–1301. doi: 10.1016/0092-8674(90)90693-9. [DOI] [PubMed] [Google Scholar]
  52. Paris J., Philippe M. Poly(A) metabolism and polysomal recruitment of maternal mRNAs during early Xenopus development. Dev Biol. 1990 Jul;140(1):221–224. doi: 10.1016/0012-1606(90)90070-y. [DOI] [PubMed] [Google Scholar]
  53. Posada J., Sanghera J., Pelech S., Aebersold R., Cooper J. A. Tyrosine phosphorylation and activation of homologous protein kinases during oocyte maturation and mitogenic activation of fibroblasts. Mol Cell Biol. 1991 May;11(5):2517–2528. doi: 10.1128/mcb.11.5.2517. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Posada J., Yew N., Ahn N. G., Vande Woude G. F., Cooper J. A. Mos stimulates MAP kinase in Xenopus oocytes and activates a MAP kinase kinase in vitro. Mol Cell Biol. 1993 Apr;13(4):2546–2553. doi: 10.1128/mcb.13.4.2546. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Roghi C., Giet R., Uzbekov R., Morin N., Chartrain I., Le Guellec R., Couturier A., Dorée M., Philippe M., Prigent C. The Xenopus protein kinase pEg2 associates with the centrosome in a cell cycle-dependent manner, binds to the spindle microtubules and is involved in bipolar mitotic spindle assembly. J Cell Sci. 1998 Mar;111(Pt 5):557–572. doi: 10.1242/jcs.111.5.557. [DOI] [PubMed] [Google Scholar]
  56. Roy L. M., Haccard O., Izumi T., Lattes B. G., Lewellyn A. L., Maller J. L. Mos proto-oncogene function during oocyte maturation in Xenopus. Oncogene. 1996 May 16;12(10):2203–2211. [PubMed] [Google Scholar]
  57. Sadler S. E., Maller J. L. Identification of a steroid receptor on the surface of Xenopus oocytes by photoaffinity labeling. J Biol Chem. 1982 Jan 10;257(1):355–361. [PubMed] [Google Scholar]
  58. Sadler S. E., Maller J. L. Progesterone inhibits adenylate cyclase in Xenopus oocytes. Action on the guanine nucleotide regulatory protein. J Biol Chem. 1981 Jun 25;256(12):6368–6373. [PubMed] [Google Scholar]
  59. Sadler S. E., Schechter A. L., Tabin C. J., Maller J. L. Antibodies to the ras gene product inhibit adenylate cyclase and accelerate progesterone-induced cell division in Xenopus laevis oocytes. Mol Cell Biol. 1986 Feb;6(2):719–722. doi: 10.1128/mcb.6.2.719. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Sagata N., Daar I., Oskarsson M., Showalter S. D., Vande Woude G. F. The product of the mos proto-oncogene as a candidate "initiator" for oocyte maturation. Science. 1989 Aug 11;245(4918):643–646. doi: 10.1126/science.2474853. [DOI] [PubMed] [Google Scholar]
  61. Sagata N., Watanabe N., Vande Woude G. F., Ikawa Y. The c-mos proto-oncogene product is a cytostatic factor responsible for meiotic arrest in vertebrate eggs. Nature. 1989 Nov 30;342(6249):512–518. doi: 10.1038/342512a0. [DOI] [PubMed] [Google Scholar]
  62. Sagata N. What does Mos do in oocytes and somatic cells? Bioessays. 1997 Jan;19(1):13–21. doi: 10.1002/bies.950190105. [DOI] [PubMed] [Google Scholar]
  63. Schuetz A. W. Action of hormones on germinal vesicle breakdown in frog (Rana pipiens) oocytes. J Exp Zool. 1967 Dec;166(3):347–354. doi: 10.1002/jez.1401660307. [DOI] [PubMed] [Google Scholar]
  64. Sheets M. D., Fox C. A., Hunt T., Vande Woude G., Wickens M. The 3'-untranslated regions of c-mos and cyclin mRNAs stimulate translation by regulating cytoplasmic polyadenylation. Genes Dev. 1994 Apr 15;8(8):926–938. doi: 10.1101/gad.8.8.926. [DOI] [PubMed] [Google Scholar]
  65. Sheets M. D., Wu M., Wickens M. Polyadenylation of c-mos mRNA as a control point in Xenopus meiotic maturation. Nature. 1995 Apr 6;374(6522):511–516. doi: 10.1038/374511a0. [DOI] [PubMed] [Google Scholar]
  66. Shibuya E. K., Morris J., Rapp U. R., Ruderman J. V. Activation of the Xenopus oocyte mitogen-activated protein kinase pathway by Mos is independent of Raf. Cell Growth Differ. 1996 Feb;7(2):235–241. [PubMed] [Google Scholar]
  67. Shibuya E. K., Polverino A. J., Chang E., Wigler M., Ruderman J. V. Oncogenic ras triggers the activation of 42-kDa mitogen-activated protein kinase in extracts of quiescent Xenopus oocytes. Proc Natl Acad Sci U S A. 1992 Oct 15;89(20):9831–9835. doi: 10.1073/pnas.89.20.9831. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Shibuya E. K., Ruderman J. V. Mos induces the in vitro activation of mitogen-activated protein kinases in lysates of frog oocytes and mammalian somatic cells. Mol Biol Cell. 1993 Aug;4(8):781–790. doi: 10.1091/mbc.4.8.781. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. 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]
  70. Stearns T., Evans L., Kirschner M. Gamma-tubulin is a highly conserved component of the centrosome. Cell. 1991 May 31;65(5):825–836. doi: 10.1016/0092-8674(91)90390-k. [DOI] [PubMed] [Google Scholar]
  71. Stebbins-Boaz B., Richter J. D. Translational control during early development. Crit Rev Eukaryot Gene Expr. 1997;7(1-2):73–94. doi: 10.1615/critreveukargeneexpr.v7.i1-2.50. [DOI] [PubMed] [Google Scholar]
  72. Stukenberg P. T., Lustig K. D., McGarry T. J., King R. W., Kuang J., Kirschner M. W. Systematic identification of mitotic phosphoproteins. Curr Biol. 1997 May 1;7(5):338–348. doi: 10.1016/s0960-9822(06)00157-6. [DOI] [PubMed] [Google Scholar]
  73. Terada Y., Tatsuka M., Suzuki F., Yasuda Y., Fujita S., Otsu M. AIM-1: a mammalian midbody-associated protein required for cytokinesis. EMBO J. 1998 Feb 2;17(3):667–676. doi: 10.1093/emboj/17.3.667. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Verde F., Berrez J. M., Antony C., Karsenti E. Taxol-induced microtubule asters in mitotic extracts of Xenopus eggs: requirement for phosphorylated factors and cytoplasmic dynein. J Cell Biol. 1991 Mar;112(6):1177–1187. doi: 10.1083/jcb.112.6.1177. [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. Waskiewicz A. J., Cooper J. A. Evolutionary conservation of Xenopus laevis mitogen-activated protein kinase activation and function. Cell Growth Differ. 1993 Dec;4(12):965–973. [PubMed] [Google Scholar]
  76. Wehling M. Specific, nongenomic actions of steroid hormones. Annu Rev Physiol. 1997;59:365–393. doi: 10.1146/annurev.physiol.59.1.365. [DOI] [PubMed] [Google Scholar]
  77. Wickens M., Anderson P., Jackson R. J. Life and death in the cytoplasm: messages from the 3' end. Curr Opin Genet Dev. 1997 Apr;7(2):220–232. doi: 10.1016/s0959-437x(97)80132-3. [DOI] [PubMed] [Google Scholar]
  78. Yanai A., Arama E., Kilfin G., Motro B. ayk1, a novel mammalian gene related to Drosophila aurora centrosome separation kinase, is specifically expressed during meiosis. Oncogene. 1997 Jun 19;14(24):2943–2950. doi: 10.1038/sj.onc.1201144. [DOI] [PubMed] [Google Scholar]
  79. Zheng Y., Wong M. L., Alberts B., Mitchison T. Nucleation of microtubule assembly by a gamma-tubulin-containing ring complex. Nature. 1995 Dec 7;378(6557):578–583. doi: 10.1038/378578a0. [DOI] [PubMed] [Google Scholar]
  80. de Moor C. H., Richter J. D. The Mos pathway regulates cytoplasmic polyadenylation in Xenopus oocytes. Mol Cell Biol. 1997 Nov;17(11):6419–6426. doi: 10.1128/mcb.17.11.6419. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The EMBO Journal are provided here courtesy of Nature Publishing Group

RESOURCES