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. 1997 Apr;17(4):1904–1912. doi: 10.1128/mcb.17.4.1904

The casein kinase II beta subunit binds to Mos and inhibits Mos activity.

M Chen 1, D Li 1, E G Krebs 1, J A Cooper 1
PMCID: PMC232037  PMID: 9121438

Abstract

Mos is a germ cell-specific serine/threonine kinase and is required for Xenopus oocyte maturation. Active Mos stimulates a mitogen-activated protein kinase (MAPK) by directly phosphorylating and activating MAPK kinase (MKK). We report here that the Xenopus homolog of the beta subunit of casein kinase II (CKII beta) binds to and regulates Mos. The Mos-interacting region of CKII beta was mapped to the C terminus. Mos bound to CKII beta in somatic cells ectopically expressing Mos and CKII beta as well as in unfertilized Xenopus eggs. CKII beta inhibited Mos-mediated MAPK activation in rabbit reticulocyte lysates and repressed MKK activation by v-Mos in a coupled kinase assay. In addition, microinjection of CKII beta mRNA into Xenopus oocytes inhibited progesterone-induced meiotic maturation and MAPK activation, presumably by binding of CKII beta to Mos and thereby inhibiting MAPK activation. Moreover, this inhibitory phenotype could be rescued by another protein that binds to CKII beta, CKII alpha. The ability of ectopic CKII beta to inhibit meiotic maturation and the detection of a complex between endogenous Mos and CKII beta suggest that CKII beta may act as an inhibitor of Mos during oocyte maturation, perhaps setting a threshold beyond which Mos protein must accumulate before it can activate the MAPK pathway.

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Selected References

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  1. Alessi D. R., Saito Y., Campbell D. G., Cohen P., Sithanandam G., Rapp U., Ashworth A., Marshall C. J., Cowley S. Identification of the sites in MAP kinase kinase-1 phosphorylated by p74raf-1. EMBO J. 1994 Apr 1;13(7):1610–1619. doi: 10.1002/j.1460-2075.1994.tb06424.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Allende J. E., Allende C. C. Protein kinases. 4. Protein kinase CK2: an enzyme with multiple substrates and a puzzling regulation. FASEB J. 1995 Mar;9(5):313–323. doi: 10.1096/fasebj.9.5.7896000. [DOI] [PubMed] [Google Scholar]
  3. Ball J., McCarter J. A., Sunderland S. M. Evidence for helper independent murine sarcoma virus. I. Segregation of replication-defective and transformation-defective viruses. Virology. 1973 Nov;56(1):268–284. doi: 10.1016/0042-6822(73)90305-x. [DOI] [PubMed] [Google Scholar]
  4. Bartel P., Chien C. T., Sternglanz R., Fields S. Elimination of false positives that arise in using the two-hybrid system. Biotechniques. 1993 Jun;14(6):920–924. [PubMed] [Google Scholar]
  5. Bidwai A. P., Reed J. C., Glover C. V. Phosphorylation of calmodulin by the catalytic subunit of casein kinase II is inhibited by the regulatory subunit. Arch Biochem Biophys. 1993 Jan;300(1):265–270. doi: 10.1006/abbi.1993.1037. [DOI] [PubMed] [Google Scholar]
  6. Bilger A., Fox C. A., Wahle E., Wickens M. Nuclear polyadenylation factors recognize cytoplasmic polyadenylation elements. Genes Dev. 1994 May 1;8(9):1106–1116. doi: 10.1101/gad.8.9.1106. [DOI] [PubMed] [Google Scholar]
  7. Boldyreff B., Meggio F., Pinna L. A., Issinger O. G. Casein kinase-2 structure-function relationship: creation of a set of mutants of the beta subunit that variably surrogate the wildtype beta subunit function. Biochem Biophys Res Commun. 1992 Oct 15;188(1):228–234. doi: 10.1016/0006-291x(92)92374-7. [DOI] [PubMed] [Google Scholar]
  8. Boldyreff B., Meggio F., Pinna L. A., Issinger O. G. Reconstitution of normal and hyperactivated forms of casein kinase-2 by variably mutated beta-subunits. Biochemistry. 1993 Nov 30;32(47):12672–12677. doi: 10.1021/bi00210a016. [DOI] [PubMed] [Google Scholar]
  9. 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]
  10. Cobb M. H., Boulton T. G., Robbins D. J. Extracellular signal-regulated kinases: ERKs in progress. Cell Regul. 1991 Dec;2(12):965–978. doi: 10.1091/mbc.2.12.965. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Colledge W. H., Carlton M. B., Udy G. B., Evans M. J. Disruption of c-mos causes parthenogenetic development of unfertilized mouse eggs. Nature. 1994 Jul 7;370(6484):65–68. doi: 10.1038/370065a0. [DOI] [PubMed] [Google Scholar]
  12. Cooper J. A. MAP kinase pathways. Straight and narrow or tortuous and intersecting? Curr Biol. 1994 Dec 1;4(12):1118–1121. doi: 10.1016/s0960-9822(00)00251-7. [DOI] [PubMed] [Google Scholar]
  13. Daar I., Paules R. S., Vande Woude G. F. A characterization of cytostatic factor activity from Xenopus eggs and c-mos-transformed cells. J Cell Biol. 1991 Jul;114(2):329–335. doi: 10.1083/jcb.114.2.329. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. 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]
  15. Feilotter H. E., Hannon G. J., Ruddell C. J., Beach D. Construction of an improved host strain for two hybrid screening. Nucleic Acids Res. 1994 Apr 25;22(8):1502–1503. doi: 10.1093/nar/22.8.1502. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Ferrell J. E., Jr Tripping the switch fantastic: how a protein kinase cascade can convert graded inputs into switch-like outputs. Trends Biochem Sci. 1996 Dec;21(12):460–466. doi: 10.1016/s0968-0004(96)20026-x. [DOI] [PubMed] [Google Scholar]
  17. 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]
  18. Fields S., Sternglanz R. The two-hybrid system: an assay for protein-protein interactions. Trends Genet. 1994 Aug;10(8):286–292. doi: 10.1016/0168-9525(90)90012-u. [DOI] [PubMed] [Google Scholar]
  19. Fox C. A., Sheets M. D., Wickens M. P. Poly(A) addition during maturation of frog oocytes: distinct nuclear and cytoplasmic activities and regulation by the sequence UUUUUAU. Genes Dev. 1989 Dec;3(12B):2151–2162. doi: 10.1101/gad.3.12b.2151. [DOI] [PubMed] [Google Scholar]
  20. Gietz R. D., Graham K. C., Litchfield D. W. Interactions between the subunits of casein kinase II. J Biol Chem. 1995 Jun 2;270(22):13017–13021. doi: 10.1074/jbc.270.22.13017. [DOI] [PubMed] [Google Scholar]
  21. 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]
  22. Gotoh Y., Matsuda S., Takenaka K., Hattori S., Iwamatsu A., Ishikawa M., Kosako H., Nishida E. Characterization of recombinant Xenopus MAP kinase kinases mutated at potential phosphorylation sites. Oncogene. 1994 Jul;9(7):1891–1898. [PubMed] [Google Scholar]
  23. Gotoh Y., Nishida E., Matsuda S., Shiina N., Kosako H., Shiokawa K., Akiyama T., Ohta K., Sakai H. In vitro effects on microtubule dynamics of purified Xenopus M phase-activated MAP kinase. Nature. 1991 Jan 17;349(6306):251–254. doi: 10.1038/349251a0. [DOI] [PubMed] [Google Scholar]
  24. Gurdon J. B. Injected nuclei in frog oocytes: fate, enlargement, and chromatin dispersal. J Embryol Exp Morphol. 1976 Dec;36(3):523–540. [PubMed] [Google Scholar]
  25. Haccard O., Lewellyn A., Hartley R. S., Erikson E., Maller J. L. Induction of Xenopus oocyte meiotic maturation by MAP kinase. Dev Biol. 1995 Apr;168(2):677–682. doi: 10.1006/dbio.1995.1112. [DOI] [PubMed] [Google Scholar]
  26. Haccard O., Sarcevic B., Lewellyn A., Hartley R., Roy L., Izumi T., Erikson E., Maller J. L. Induction of metaphase arrest in cleaving Xenopus embryos by MAP kinase. Science. 1993 Nov 19;262(5137):1262–1265. doi: 10.1126/science.8235656. [DOI] [PubMed] [Google Scholar]
  27. Hashimoto N., Watanabe N., Furuta Y., Tamemoto H., Sagata N., Yokoyama M., Okazaki K., Nagayoshi M., Takeda N., Ikawa Y. Parthenogenetic activation of oocytes in c-mos-deficient mice. Nature. 1994 Jul 7;370(6484):68–71. doi: 10.1038/370068a0. [DOI] [PubMed] [Google Scholar]
  28. Huang C. Y., Ferrell J. E., Jr Dependence of Mos-induced Cdc2 activation on MAP kinase function in a cell-free system. EMBO J. 1996 May 1;15(9):2169–2173. [PMC free article] [PubMed] [Google Scholar]
  29. Kanki J. P., Donoghue D. J. Progression from meiosis I to meiosis II in Xenopus oocytes requires de novo translation of the mosxe protooncogene. Proc Natl Acad Sci U S A. 1991 Jul 1;88(13):5794–5798. doi: 10.1073/pnas.88.13.5794. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Kirschner M. The cell cycle then and now. Trends Biochem Sci. 1992 Aug;17(8):281–285. doi: 10.1016/0968-0004(92)90435-c. [DOI] [PubMed] [Google Scholar]
  31. Kosako H., Gotoh Y., Nishida E. Requirement for the MAP kinase kinase/MAP kinase cascade in Xenopus oocyte maturation. EMBO J. 1994 May 1;13(9):2131–2138. doi: 10.1002/j.1460-2075.1994.tb06489.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Krek W., Maridor G., Nigg E. A. Casein kinase II is a predominantly nuclear enzyme. J Cell Biol. 1992 Jan;116(1):43–55. doi: 10.1083/jcb.116.1.43. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Kusk M., Bendixen C., Dunø M., Westergaard O., Thomsen B. Genetic dissection of intersubunit contacts within human protein kinase CK2. J Mol Biol. 1995 Nov 10;253(5):703–711. doi: 10.1006/jmbi.1995.0584. [DOI] [PubMed] [Google Scholar]
  34. Kyriakis J. M., App H., Zhang X. F., Banerjee P., Brautigan D. L., Rapp U. R., Avruch J. Raf-1 activates MAP kinase-kinase. Nature. 1992 Jul 30;358(6385):417–421. doi: 10.1038/358417a0. [DOI] [PubMed] [Google Scholar]
  35. Litchfield D. W., Lozeman F. J., Cicirelli M. F., Harrylock M., Ericsson L. H., Piening C. J., Krebs E. G. Phosphorylation of the beta subunit of casein kinase II in human A431 cells. Identification of the autophosphorylation site and a site phosphorylated by p34cdc2. J Biol Chem. 1991 Oct 25;266(30):20380–20389. [PubMed] [Google Scholar]
  36. Litchfield D. W., Lozeman F. J., Piening C., Sommercorn J., Takio K., Walsh K. A., Krebs E. G. Subunit structure of casein kinase II from bovine testis. Demonstration that the alpha and alpha' subunits are distinct polypeptides. J Biol Chem. 1990 May 5;265(13):7638–7644. [PubMed] [Google Scholar]
  37. Lorca T., Cruzalegui F. H., Fesquet D., Cavadore J. C., Méry J., Means A., Dorée M. Calmodulin-dependent protein kinase II mediates inactivation of MPF and CSF upon fertilization of Xenopus eggs. Nature. 1993 Nov 18;366(6452):270–273. doi: 10.1038/366270a0. [DOI] [PubMed] [Google Scholar]
  38. Lorenz P., Pepperkok R., Ansorge W., Pyerin W. Cell biological studies with monoclonal and polyclonal antibodies against human casein kinase II subunit beta demonstrate participation of the kinase in mitogenic signaling. J Biol Chem. 1993 Feb 5;268(4):2733–2739. [PubMed] [Google Scholar]
  39. Lüscher B., Litchfield D. W. Biosynthesis of casein kinase II in lymphoid cell lines. Eur J Biochem. 1994 Mar 1;220(2):521–526. doi: 10.1111/j.1432-1033.1994.tb18651.x. [DOI] [PubMed] [Google Scholar]
  40. Mansour S. J., Matten W. T., Hermann A. S., Candia J. M., Rong S., Fukasawa K., Vande Woude G. F., Ahn N. G. Transformation of mammalian cells by constitutively active MAP kinase kinase. Science. 1994 Aug 12;265(5174):966–970. doi: 10.1126/science.8052857. [DOI] [PubMed] [Google Scholar]
  41. Marin O., Meggio F., Boldyreff B., Issinger O. G., Pinna L. A. Dissection of the dual function of the beta-subunit of protein kinase CK2 ('casein kinase-2'): a synthetic peptide reproducing the carboxyl-terminal domain mimicks the positive but not the negative effects of the whole protein. FEBS Lett. 1995 Apr 17;363(1-2):111–114. doi: 10.1016/0014-5793(95)00295-k. [DOI] [PubMed] [Google Scholar]
  42. Marshall C. J. MAP kinase kinase kinase, MAP kinase kinase and MAP kinase. Curr Opin Genet Dev. 1994 Feb;4(1):82–89. doi: 10.1016/0959-437x(94)90095-7. [DOI] [PubMed] [Google Scholar]
  43. 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]
  44. Maxwell S. A., Arlinghaus R. B. Serine kinase activity associated with Maloney murine sarcoma virus-124-encoded p37mos. Virology. 1985 May;143(1):321–333. doi: 10.1016/0042-6822(85)90119-9. [DOI] [PubMed] [Google Scholar]
  45. Mayer B. J., Baltimore D. Mutagenic analysis of the roles of SH2 and SH3 domains in regulation of the Abl tyrosine kinase. Mol Cell Biol. 1994 May;14(5):2883–2894. doi: 10.1128/mcb.14.5.2883. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Mizushima S., Nagata S. pEF-BOS, a powerful mammalian expression vector. Nucleic Acids Res. 1990 Sep 11;18(17):5322–5322. doi: 10.1093/nar/18.17.5322. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Murray A. W., Kirschner M. W. Dominoes and clocks: the union of two views of the cell cycle. Science. 1989 Nov 3;246(4930):614–621. doi: 10.1126/science.2683077. [DOI] [PubMed] [Google Scholar]
  48. Nasmyth K., Hunt T. Cell cycle. Dams and sluices. Nature. 1993 Dec 16;366(6456):634–635. doi: 10.1038/366634a0. [DOI] [PubMed] [Google Scholar]
  49. 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]
  50. Okazaki K., Nishizawa M., Furuno N., Yasuda H., Sagata N. Differential occurrence of CSF-like activity and transforming activity of Mos during the cell cycle in fibroblasts. EMBO J. 1992 Jul;11(7):2447–2456. doi: 10.1002/j.1460-2075.1992.tb05309.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Oskarsson M., McClements W. L., Blair D. G., Maizel J. V., Vande Woude G. F. Properties of a normal mouse cell DNA sequence (sarc) homologous to the src sequence of Moloney sarcoma virus. Science. 1980 Mar 14;207(4436):1222–1224. doi: 10.1126/science.6243788. [DOI] [PubMed] [Google Scholar]
  52. Papkoff J., Verma I. M., Hunter T. Detection of a transforming gene product in cells transformed by Moloney murine sarcoma virus. Cell. 1982 Jun;29(2):417–426. doi: 10.1016/0092-8674(82)90158-1. [DOI] [PubMed] [Google Scholar]
  53. Paules R. S., Buccione R., Moschel R. C., Vande Woude G. F., Eppig J. J. Mouse Mos protooncogene product is present and functions during oogenesis. Proc Natl Acad Sci U S A. 1989 Jul;86(14):5395–5399. doi: 10.1073/pnas.86.14.5395. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Pelech S. L., Sanghera J. S. MAP kinases: charting the regulatory pathways. Science. 1992 Sep 4;257(5075):1355–1356. doi: 10.1126/science.1382311. [DOI] [PubMed] [Google Scholar]
  55. Pinna L. A. Casein kinase 2: an 'eminence grise' in cellular regulation? Biochim Biophys Acta. 1990 Sep 24;1054(3):267–284. doi: 10.1016/0167-4889(90)90098-x. [DOI] [PubMed] [Google Scholar]
  56. Posada J., Cooper J. A. Requirements for phosphorylation of MAP kinase during meiosis in Xenopus oocytes. Science. 1992 Jan 10;255(5041):212–215. doi: 10.1126/science.1313186. [DOI] [PubMed] [Google Scholar]
  57. 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]
  58. 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]
  59. Propst F., Vande Woude G. F. Expression of c-mos proto-oncogene transcripts in mouse tissues. Nature. 1985 Jun 6;315(6019):516–518. doi: 10.1038/315516a0. [DOI] [PubMed] [Google Scholar]
  60. Resing K. A., Mansour S. J., Hermann A. S., Johnson R. S., Candia J. M., Fukasawa K., Vande Woude G. F., Ahn N. G. Determination of v-Mos-catalyzed phosphorylation sites and autophosphorylation sites on MAP kinase kinase by ESI/MS. Biochemistry. 1995 Feb 28;34(8):2610–2620. doi: 10.1021/bi00008a027. [DOI] [PubMed] [Google Scholar]
  61. Roussou I., Draetta G. The Schizosaccharomyces pombe casein kinase II alpha and beta subunits: evolutionary conservation and positive role of the beta subunit. Mol Cell Biol. 1994 Jan;14(1):576–586. doi: 10.1128/mcb.14.1.576. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. 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]
  63. Sagata N., Oskarsson M., Copeland T., Brumbaugh J., Vande Woude G. F. Function of c-mos proto-oncogene product in meiotic maturation in Xenopus oocytes. Nature. 1988 Oct 6;335(6190):519–525. doi: 10.1038/335519a0. [DOI] [PubMed] [Google Scholar]
  64. 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]
  65. Selfors L. M., Stern M. J. MAP kinase function in C. elegans. Bioessays. 1994 May;16(5):301–304. doi: 10.1002/bies.950160502. [DOI] [PubMed] [Google Scholar]
  66. 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]
  67. 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]
  68. 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]
  69. 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]
  70. Singh B., al-Bagdadi F., Liu J. X., Arlinghaus R. B. Use of antipeptide antibodies to probe the catalytic activity of p37v-mos. Virology. 1990 Oct;178(2):535–542. doi: 10.1016/0042-6822(90)90351-q. [DOI] [PubMed] [Google Scholar]
  71. Stigare J., Buddelmeijer N., Pigon A., Egyhazi E. A majority of casein kinase II alpha subunit is tightly bound to intranuclear components but not to the beta subunit. Mol Cell Biochem. 1993 Dec 8;129(1):77–85. doi: 10.1007/BF00926578. [DOI] [PubMed] [Google Scholar]
  72. Teitz T., Eli D., Penner M., Bakhanashvili M., Naiman T., Timme T. L., Wood C. M., Moses R. E., Canaani D. Expression of the cDNA for the beta subunit of human casein kinase II confers partial UV resistance on xeroderma pigmentosum cells. Mutat Res. 1990 Jul;236(1):85–97. doi: 10.1016/0921-8777(90)90036-5. [DOI] [PubMed] [Google Scholar]
  73. Thomas G. MAP kinase by any other name smells just as sweet. Cell. 1992 Jan 10;68(1):3–6. doi: 10.1016/0092-8674(92)90199-m. [DOI] [PubMed] [Google Scholar]
  74. Turner D. L., Weintraub H. Expression of achaete-scute homolog 3 in Xenopus embryos converts ectodermal cells to a neural fate. Genes Dev. 1994 Jun 15;8(12):1434–1447. doi: 10.1101/gad.8.12.1434. [DOI] [PubMed] [Google Scholar]
  75. Vojtek A. B., Hollenberg S. M., Cooper J. A. Mammalian Ras interacts directly with the serine/threonine kinase Raf. Cell. 1993 Jul 16;74(1):205–214. doi: 10.1016/0092-8674(93)90307-c. [DOI] [PubMed] [Google Scholar]
  76. Wang X. M., Yew N., Peloquin J. G., Vande Woude G. F., Borisy G. G. Mos oncogene product associates with kinetochores in mammalian somatic cells and disrupts mitotic progression. Proc Natl Acad Sci U S A. 1994 Aug 30;91(18):8329–8333. doi: 10.1073/pnas.91.18.8329. [DOI] [PMC free article] [PubMed] [Google Scholar]
  77. Waskiewicz A. J., Cooper J. A. Mitogen and stress response pathways: MAP kinase cascades and phosphatase regulation in mammals and yeast. Curr Opin Cell Biol. 1995 Dec;7(6):798–805. doi: 10.1016/0955-0674(95)80063-8. [DOI] [PubMed] [Google Scholar]
  78. Watanabe N., Vande Woude G. F., Ikawa Y., Sagata N. Specific proteolysis of the c-mos proto-oncogene product by calpain on fertilization of Xenopus eggs. Nature. 1989 Nov 30;342(6249):505–511. doi: 10.1038/342505a0. [DOI] [PubMed] [Google Scholar]
  79. Yang Y., Herrmann C. H., Arlinghaus R. B., Singh B. Inhibition of v-Mos kinase activity by protein kinase A. Mol Cell Biol. 1996 Mar;16(3):800–809. doi: 10.1128/mcb.16.3.800. [DOI] [PMC free article] [PubMed] [Google Scholar]
  80. Yew N., Mellini M. L., Vande Woude G. F. Meiotic initiation by the mos protein in Xenopus. Nature. 1992 Feb 13;355(6361):649–652. doi: 10.1038/355649a0. [DOI] [PubMed] [Google Scholar]
  81. Zheng C. F., Guan K. L. Activation of MEK family kinases requires phosphorylation of two conserved Ser/Thr residues. EMBO J. 1994 Mar 1;13(5):1123–1131. doi: 10.1002/j.1460-2075.1994.tb06361.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

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