Home LiteratureArticle Details
PMID: 9724639 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

A link between MAP kinase and p34(cdc2)/cyclin B during oocyte maturation: p90(rsk) phosphorylates and inactivates the p34(cdc2) inhibitory kinase Myt1.

The EMBO journal ·Vol. 17 ·No. 17 ·1998-09-01 ·Pages 5037-47

Palmer A, Gavin AC, Nebreda AR

Abstract

M-phase entry in eukaryotic cells is driven by activation of MPF, a regulatory factor composed of cyclin B and the protein kinase p34(cdc2). In G2-arrested Xenopus oocytes, there is a stock of p34(cdc2)/cyclin B complexes (pre-MPF) which is maintained in an inactive state by p34(cdc2) phosphorylation on Thr14 and Tyr15. This suggests an important role for the p34(cdc2) inhibitory kinase(s) such as Wee1 and Myt1 in regulating the G2-->M transition during oocyte maturation. MAP kinase (MAPK) activation is required for M-phase entry in Xenopus oocytes, but its precise contribution to the activation of pre-MPF is unknown. Here we show that the C-terminal regulatory domain of Myt1 specifically binds to p90(rsk), a protein kinase that can be phosphorylated and activated by MAPK. p90(rsk) in turn phosphorylates the C-terminus of Myt1 and down-regulates its inhibitory activity on p34(cdc2)/cyclin B in vitro. Consistent with these results, Myt1 becomes phosphorylated during oocyte maturation, and activation of the MAPK-p90(rsk) cascade can trigger some Myt1 phosphorylation prior to pre-MPF activation. We found that Myt1 preferentially associates with hyperphosphorylated p90(rsk), and complexes can be detected in immunoprecipitates from mature oocytes. Our results suggest that during oocyte maturation MAPK activates p90(rsk) and that p90(rsk) in turn down-regulates Myt1, leading to the activation of p34(cdc2)/cyclin B.

MeSH Terms
Animals CDC2 Protein Kinase/metabolism Calcium-Calmodulin-Dependent Protein Kinases/metabolism Cell Differentiation Cyclin B/metabolism Enzyme Activation Models, Biological Oocytes/cytology,metabolism Phosphorylation Protein Binding Protein Serine-Threonine Kinases/antagonists & inhibitors Protein-Tyrosine Kinases/antagonists & inhibitors Ribosomal Protein S6 Kinases/metabolism Signal Transduction Xenopus Xenopus Proteins
Chemicals
Cyclin B Xenopus Proteins MYT1 kinase, Xenopus Protein-Tyrosine Kinases Protein Serine-Threonine Kinases Ribosomal Protein S6 Kinases Calcium-Calmodulin-Dependent Protein Kinases CDC2 Protein Kinase
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Palmer A
European Molecular Biology Laboratory, Meyerhofstrasse 1, 69117 Heidelberg, Germany.
Gavin A C
Nebreda A R
References (62)
62 references, click to expand
  1. Inactivation of the p34cdc2-cyclin B complex by the human WEE1 tyrosine kinase.
    Science. 1992 Sep 25;257(5078):1955-7 PMID: 1384126
  2. Cell cycle extracts.
    Methods Cell Biol. 1991;36:581-605 PMID: 1839804
  3. Phosphorylation and activation of human cdc25-C by cdc2--cyclin B and its involvement in the self-amplification of MPF at mitosis.
    EMBO J. 1993 Jan;12(1):53-63 PMID: 8428594
  4. Human Wee1 kinase inhibits cell division by phosphorylating p34cdc2 exclusively on Tyr15.
    EMBO J. 1993 Jan;12(1):75-85 PMID: 8428596
  5. Mos stimulates MAP kinase in Xenopus oocytes and activates a MAP kinase kinase in vitro.
    Mol Cell Biol. 1993 Apr;13(4):2546-53 PMID: 8384311
  6. 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):1979-86 PMID: 8387916
  7. The protein kinase mos activates MAP kinase kinase in vitro and stimulates the MAP kinase pathway in mammalian somatic cells in vivo.
    FEBS Lett. 1993 Oct 25;333(1-2):183-7 PMID: 8224161
  8. 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):781-90 PMID: 8241566
  9. Two distinct mechanisms for negative regulation of the Wee1 protein kinase.
    EMBO J. 1993 Sep;12(9):3427-36 PMID: 7504624
  10. Elimination of cdc2 phosphorylation sites in the cdc25 phosphatase blocks initiation of M-phase.
    Mol Biol Cell. 1993 Dec;4(12):1337-50 PMID: 7513216
  11. Requirement for the MAP kinase kinase/MAP kinase cascade in Xenopus oocyte maturation.
    EMBO J. 1994 May 1;13(9):2131-8 PMID: 8187766
  12. Evidence that inactive p42 mitogen-activated protein kinase and inactive Rsk exist as a heterodimer in vivo.
    Proc Natl Acad Sci U S A. 1994 Jun 7;91(12):5480-4 PMID: 8202512
  13. Membrane localization of the kinase which phosphorylates p34cdc2 on threonine 14.
    Mol Biol Cell. 1994 Mar;5(3):273-82 PMID: 8049520
  14. Cell cycle regulation of the p34cdc2 inhibitory kinases.
    Mol Biol Cell. 1994 Sep;5(9):989-1001 PMID: 7841526
  15. Principles of CDK regulation.
    Nature. 1995 Mar 9;374(6518):131-4 PMID: 7877684
  16. Cdc2 regulatory factors.
    Curr Opin Cell Biol. 1994 Dec;6(6):877-82 PMID: 7880537
  17. Polyadenylation of c-mos mRNA as a control point in Xenopus meiotic maturation.
    Nature. 1995 Apr 6;374(6522):511-6 PMID: 7700377
  18. Induction of Xenopus oocyte meiotic maturation by MAP kinase.
    Dev Biol. 1995 Apr;168(2):677-82 PMID: 7729598
  19. Cell cycle regulation of a Xenopus Wee1-like kinase.
    Mol Biol Cell. 1995 Jan;6(1):119-34 PMID: 7749193
  20. Cell cycle regulation of human WEE1.
    EMBO J. 1995 May 15;14(10):2166-75 PMID: 7774574
  21. Biochemical and biological analysis of Mek1 phosphorylation site mutants.
    Mol Biol Cell. 1995 Mar;6(3):237-45 PMID: 7612960
  22. Myt1: a membrane-associated inhibitory kinase that phosphorylates Cdc2 on both threonine-14 and tyrosine-15.
    Science. 1995 Oct 6;270(5233):86-90 PMID: 7569953
  23. Initiation of Xenopus oocyte maturation by activation of the mitogen-activated protein kinase cascade.
    J Biol Chem. 1995 Oct 27;270(43):25898-904 PMID: 7592777
  24. PD 098059 is a specific inhibitor of the activation of mitogen-activated protein kinase kinase in vitro and in vivo.
    J Biol Chem. 1995 Nov 17;270(46):27489-94 PMID: 7499206
  25. Comparison of the specificities of p70 S6 kinase and MAPKAP kinase-1 identifies a relatively specific substrate for p70 S6 kinase: the N-terminal kinase domain of MAPKAP kinase-1 is essential for peptide phosphorylation.
    FEBS Lett. 1995 Nov 20;375(3):289-93 PMID: 7498520
  26. Newly synthesized protein(s) must associate with p34cdc2 to activate MAP kinase and MPF during progesterone-induced maturation of Xenopus oocytes.
    EMBO J. 1995 Nov 15;14(22):5597-607 PMID: 8521817
  27. Evidence for two catalytically active kinase domains in pp90rsk.
    Mol Cell Biol. 1996 Mar;16(3):1212-9 PMID: 8622665
  28. p21ras-induced meiotic maturation of Xenopus oocytes in the absence of protein synthesis: MPF activation is preceded by activation of MAP and S6 kinases.
    Oncogene. 1993 Feb;8(2):467-77 PMID: 8381222
  29. Cytoplasmic control of nuclear behavior during meiotic maturation of frog oocytes.
    J Exp Zool. 1971 Jun;177(2):129-45 PMID: 5106340
  30. Oocyte maturation.
    Int Rev Cytol. 1979;57:185-282 PMID: 385540
  31. Purification and characterization of a protein kinase from Xenopus eggs highly specific for ribosomal protein S6.
    J Biol Chem. 1986 Jan 5;261(1):350-5 PMID: 3941081
  32. Regulation of MPF activity in vitro.
    Cell. 1988 Apr 22;53(2):185-95 PMID: 2834064
  33. A Xenopus ribosomal protein S6 kinase has two apparent kinase domains that are each similar to distinct protein kinases.
    Proc Natl Acad Sci U S A. 1988 May;85(10):3377-81 PMID: 3368449
  34. Insulin-stimulated MAP-2 kinase phosphorylates and activates ribosomal protein S6 kinase II.
    Nature. 1988 Aug 25;334(6184):715-8 PMID: 2842685
  35. Function of c-mos proto-oncogene product in meiotic maturation in Xenopus oocytes.
    Nature. 1988 Oct 6;335(6190):519-25 PMID: 2971141
  36. The product of the mos proto-oncogene as a candidate "initiator" for oocyte maturation.
    Science. 1989 Aug 11;245(4918):643-6 PMID: 2474853
  37. Sequence and expression of chicken and mouse rsk: homologs of Xenopus laevis ribosomal S6 kinase.
    Mol Cell Biol. 1989 Sep;9(9):3850-9 PMID: 2779569
  38. Cyclin B in Xenopus oocytes: implications for the mechanism of pre-MPF activation.
    EMBO J. 1991 Jan;10(1):177-82 PMID: 1824935
  39. The cdc25 protein controls tyrosine dephosphorylation of the cdc2 protein in a cell-free system.
    Cell. 1991 Mar 8;64(5):903-14 PMID: 1825803
  40. Dephosphorylation and activation of a p34cdc2/cyclin B complex in vitro by human CDC25 protein.
    Nature. 1991 May 16;351(6323):242-5 PMID: 1828290
  41. Mitogen-activated Swiss mouse 3T3 RSK kinases I and II are related to pp44mpk from sea star oocytes and participate in the regulation of pp90rsk activity.
    Proc Natl Acad Sci U S A. 1991 Jun 1;88(11):4981-5 PMID: 2052581
  42. Regulation of the cdc25 protein during the cell cycle in Xenopus extracts.
    Cell. 1992 Jul 10;70(1):139-51 PMID: 1623517
  43. Periodic changes in phosphorylation of the Xenopus cdc25 phosphatase regulate its activity.
    Mol Biol Cell. 1992 Aug;3(8):927-39 PMID: 1392080
  44. MAPKAP kinase-2; a novel protein kinase activated by mitogen-activated protein kinase.
    EMBO J. 1992 Nov;11(11):3985-94 PMID: 1327754
  45. Phosphorylation of Drosophila Jun by the MAP kinase rolled regulates photoreceptor differentiation.
    EMBO J. 1996 Aug 1;15(15):3943-50 PMID: 8670899
  46. Purification and molecular cloning of Plx1, a Cdc25-regulatory kinase from Xenopus egg extracts.
    Science. 1996 Sep 6;273(5280):1377-80 PMID: 8703070
  47. Regulatory roles of cyclin dependent kinase phosphorylation in cell cycle control.
    Curr Opin Cell Biol. 1996 Dec;8(6):795-804 PMID: 8939679
  48. Regulation and interaction of pp90(rsk) isoforms with mitogen-activated protein kinases.
    J Biol Chem. 1996 Nov 22;271(47):29773-9 PMID: 8939914
  49. The human Myt1 kinase preferentially phosphorylates Cdc2 on threonine 14 and localizes to the endoplasmic reticulum and Golgi complex.
    Mol Cell Biol. 1997 Feb;17(2):571-83 PMID: 9001210
  50. The protein kinase C inhibitors Ro 318220 and GF 109203X are equally potent inhibitors of MAPKAP kinase-1beta (Rsk-2) and p70 S6 kinase.
    FEBS Lett. 1997 Feb 3;402(2-3):121-3 PMID: 9037179
  51. Mitogen-activated protein kinase activation down-regulates a mechanism that inactivates cyclin B-cdc2 kinase in G2-arrested oocytes.
    Mol Biol Cell. 1997 Feb;8(2):249-61 PMID: 9190205
  52. Regulation of Xenopus Cdc25 protein.
    Methods Enzymol. 1997;283:564-71 PMID: 9251048
  53. Human Myt1 is a cell cycle-regulated kinase that inhibits Cdc2 but not Cdk2 activity.
    J Biol Chem. 1997 Aug 29;272(35):22300-6 PMID: 9268380
  54. XSmad2 directly activates the activin-inducible, dorsal mesoderm gene XFKH1 in Xenopus embryos.
    EMBO J. 1997 Dec 15;16(24):7411-21 PMID: 9405370
  55. Analysis of the early embryonic cell cycles of Xenopus; regulation of cell cycle length by Xe-wee1 and Mos.
    Development. 1998 Jan;125(2):237-48 PMID: 9486797
  56. Meiotic maturation in Xenopus requires polyadenylation of multiple mRNAs.
    EMBO J. 1998 Jun 1;17(11):3168-75 PMID: 9606198
  57. 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):5794-8 PMID: 1648231
  58. On the synthesis and destruction of A- and B-type cyclins during oogenesis and meiotic maturation in Xenopus laevis.
    J Cell Biol. 1991 Aug;114(4):755-65 PMID: 1831203
  59. The cdc25 protein contains an intrinsic phosphatase activity.
    Cell. 1991 Oct 4;67(1):189-96 PMID: 1655274
  60. cdc25 is a specific tyrosine phosphatase that directly activates p34cdc2.
    Cell. 1991 Oct 4;67(1):197-211 PMID: 1913817
  61. Determination of phosphoamino acid composition by acid hydrolysis of protein blotted to Immobilon.
    Methods Enzymol. 1991;201:21-7 PMID: 1719341
  62. Activation of extracellular signal-regulated kinase, ERK2, by p21ras oncoprotein.
    EMBO J. 1992 Feb;11(2):569-74 PMID: 1371463
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
1998-09-01
Pages
5037-47
Language
English
Region
England
NLM ID
8208664
PMCID
PMC1170831
Subset
IM
Corrections
ErratumIn
-
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com