• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of embojLink to Publisher's site
EMBO J. Dec 15, 1994; 13(24): 6099–6106.
PMCID: PMC395589

A role for Hsp90 in cell cycle control: Wee1 tyrosine kinase activity requires interaction with Hsp90.

Abstract

Wee1 protein kinase regulates the length of G2 phase by carrying out the inhibitory tyrosyl phosphorylation of Cdc2-cyclin B kinase. Mutations were isolated that suppressed the G2 cell cycle arrest caused by overproduction of Wee1. One class of swo (suppressor of wee1 overproduction) mutation, exemplified by swo1-26, also caused a temperature sensitive lethal phenotype in a wee1+ background. The swo1+ gene encodes a member of the Hsp90 family of stress proteins. Swo1 is essential for viability at all temperatures. Swo1 coimmunoprecipitates with Wee1, showing that the two proteins interact. The swo1-26 mutant undergoes premature mitosis when grown at a semi-permissive temperature. These data strongly indicate that formation of active Wee1 tyrosine kinase requires interaction with Swo1, perhaps in a manner analogous to the previously demonstrated interaction between Hsp90 and v-src tyrosine kinase. These observations demonstrate a unexpected role for Hsp90 in cell cycle control.

Full text

Full text is available as a scanned copy of the original print version. Get a printable copy (PDF file) of the complete article (2.5M), or click on a page image below to browse page by page. Links to PubMed are also available for Selected References.

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Alfa CE, Booher R, Beach D, Hyams JS. Fission yeast cyclin: subcellular localisation and cell cycle regulation. J Cell Sci Suppl. 1989;12:9–19. [PubMed]
  • Alfa CE, Ducommun B, Beach D, Hyams JS. Distinct nuclear and spindle pole body population of cyclin-cdc2 in fission yeast. Nature. 1990 Oct 18;347(6294):680–682. [PubMed]
  • Amin J, Ananthan J, Voellmy R. Key features of heat shock regulatory elements. Mol Cell Biol. 1988 Sep;8(9):3761–3769. [PMC free article] [PubMed]
  • Bohen SP, Yamamoto KR. Isolation of Hsp90 mutants by screening for decreased steroid receptor function. Proc Natl Acad Sci U S A. 1993 Dec 1;90(23):11424–11428. [PMC free article] [PubMed]
  • Borkovich KA, Farrelly FW, Finkelstein DB, Taulien J, Lindquist S. hsp82 is an essential protein that is required in higher concentrations for growth of cells at higher temperatures. Mol Cell Biol. 1989 Sep;9(9):3919–3930. [PMC free article] [PubMed]
  • Brugge JS. Interaction of the Rous sarcoma virus protein pp60src with the cellular proteins pp50 and pp90. Curr Top Microbiol Immunol. 1986;123:1–22. [PubMed]
  • Carr AM, MacNeill SA, Hayles J, Nurse P. Molecular cloning and sequence analysis of mutant alleles of the fission yeast cdc2 protein kinase gene: implications for cdc2+ protein structure and function. Mol Gen Genet. 1989 Jul;218(1):41–49. [PubMed]
  • Coleman TR, Tang Z, Dunphy WG. Negative regulation of the wee1 protein kinase by direct action of the nim1/cdr1 mitotic inducer. Cell. 1993 Mar 26;72(6):919–929. [PubMed]
  • Cutforth T, Rubin GM. Mutations in Hsp83 and cdc37 impair signaling by the sevenless receptor tyrosine kinase in Drosophila. Cell. 1994 Jul 1;77(7):1027–1036. [PubMed]
  • Dunphy WG. The decision to enter mitosis. Trends Cell Biol. 1994 Jun;4(6):202–207. [PubMed]
  • Dunphy WG, Kumagai A. The cdc25 protein contains an intrinsic phosphatase activity. Cell. 1991 Oct 4;67(1):189–196. [PubMed]
  • Enoch T, Carr AM, Nurse P. Fission yeast genes involved in coupling mitosis to completion of DNA replication. Genes Dev. 1992 Nov;6(11):2035–2046. [PubMed]
  • Fikes JD, Becker DM, Winston F, Guarente L. Striking conservation of TFIID in Schizosaccharomyces pombe and Saccharomyces cerevisiae. Nature. 1990 Jul 19;346(6281):291–294. [PubMed]
  • Gould KL, Nurse P. Tyrosine phosphorylation of the fission yeast cdc2+ protein kinase regulates entry into mitosis. Nature. 1989 Nov 2;342(6245):39–45. [PubMed]
  • Jakob U, Buchner J. Assisting spontaneity: the role of Hsp90 and small Hsps as molecular chaperones. Trends Biochem Sci. 1994 May;19(5):205–211. [PubMed]
  • Lee MS, Ogg S, Xu M, Parker LL, Donoghue DJ, Maller JL, Piwnica-Worms H. cdc25+ encodes a protein phosphatase that dephosphorylates p34cdc2. Mol Biol Cell. 1992 Jan;3(1):73–84. [PMC free article] [PubMed]
  • Lindquist S, Craig EA. The heat-shock proteins. Annu Rev Genet. 1988;22:631–677. [PubMed]
  • Lundgren K, Walworth N, Booher R, Dembski M, Kirschner M, Beach D. mik1 and wee1 cooperate in the inhibitory tyrosine phosphorylation of cdc2. Cell. 1991 Mar 22;64(6):1111–1122. [PubMed]
  • MacNeill SA, Nurse P. Mutational analysis of the fission yeast p34cdc2 protein kinase gene. Mol Gen Genet. 1993 Jan;236(2-3):415–426. [PubMed]
  • McGowan CH, Russell P. Human Wee1 kinase inhibits cell division by phosphorylating p34cdc2 exclusively on Tyr15. EMBO J. 1993 Jan;12(1):75–85. [PMC free article] [PubMed]
  • Maundrell K. Thiamine-repressible expression vectors pREP and pRIP for fission yeast. Gene. 1993 Jan 15;123(1):127–130. [PubMed]
  • Millar JB, McGowan CH, Lenaers G, Jones R, Russell P. p80cdc25 mitotic inducer is the tyrosine phosphatase that activates p34cdc2 kinase in fission yeast. EMBO J. 1991 Dec;10(13):4301–4309. [PMC free article] [PubMed]
  • Moreno S, Klar A, Nurse P. Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol. 1991;194:795–823. [PubMed]
  • Murray AW. Cell-cycle control: turning on mitosis. Curr Biol. 1993 May 1;3(5):291–293. [PubMed]
  • Nurse P. Genetic control of cell size at cell division in yeast. Nature. 1975 Aug 14;256(5518):547–551. [PubMed]
  • Nurse P. Universal control mechanism regulating onset of M-phase. Nature. 1990 Apr 5;344(6266):503–508. [PubMed]
  • Parker LL, Atherton-Fessler S, Piwnica-Worms H. p107wee1 is a dual-specificity kinase that phosphorylates p34cdc2 on tyrosine 15. Proc Natl Acad Sci U S A. 1992 Apr 1;89(7):2917–2921. [PMC free article] [PubMed]
  • Parker LL, Walter SA, Young PG, Piwnica-Worms H. Phosphorylation and inactivation of the mitotic inhibitor Wee1 by the nim1/cdr1 kinase. Nature. 1993 Jun 24;363(6431):736–738. [PubMed]
  • Russell P, Nurse P. cdc25+ functions as an inducer in the mitotic control of fission yeast. Cell. 1986 Apr 11;45(1):145–153. [PubMed]
  • Russell P, Nurse P. The mitotic inducer nim1+ functions in a regulatory network of protein kinase homologs controlling the initiation of mitosis. Cell. 1987 May 22;49(4):569–576. [PubMed]
  • Russell P, Nurse P. Negative regulation of mitosis by wee1+, a gene encoding a protein kinase homolog. Cell. 1987 May 22;49(4):559–567. [PubMed]
  • Shaknovich R, Shue G, Kohtz DS. Conformational activation of a basic helix-loop-helix protein (MyoD1) by the C-terminal region of murine HSP90 (HSP84). Mol Cell Biol. 1992 Nov;12(11):5059–5068. [PMC free article] [PubMed]
  • Yamazaki M, Akaogi K, Miwa T, Imai T, Soeda E, Yokoyama K. Nucleotide sequence of a full-length cDNA for 90 kDa heat-shock protein from human peripheral blood lymphocytes. Nucleic Acids Res. 1989 Sep 12;17(17):7108–7108. [PMC free article] [PubMed]
  • Tang Z, Coleman TR, Dunphy WG. Two distinct mechanisms for negative regulation of the Wee1 protein kinase. EMBO J. 1993 Sep;12(9):3427–3436. [PMC free article] [PubMed]
  • Thuriaux P, Nurse P, Carter B. Mutants altered in the control co-ordinating cell division with cell growth in the fission yeast Schizosaccharomyces pombe. Mol Gen Genet. 1978 May 3;161(2):215–220. [PubMed]
  • Wiech H, Buchner J, Zimmermann R, Jakob U. Hsp90 chaperones protein folding in vitro. Nature. 1992 Jul 9;358(6382):169–170. [PubMed]
  • Wu L, Russell P. Nim1 kinase promotes mitosis by inactivating Wee1 tyrosine kinase. Nature. 1993 Jun 24;363(6431):738–741. [PubMed]
  • Xu Y, Lindquist S. Heat-shock protein hsp90 governs the activity of pp60v-src kinase. Proc Natl Acad Sci U S A. 1993 Aug 1;90(15):7074–7078. [PMC free article] [PubMed]

Articles from The EMBO Journal are provided here courtesy of The European Molecular Biology Organization

Formats:

Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...

Links

  • Gene
    Gene
    Gene links
  • Gene (nucleotide)
    Gene (nucleotide)
    Records in Gene identified from shared sequence links
  • GEO Profiles
    GEO Profiles
    Related GEO records
  • HomoloGene
    HomoloGene
    HomoloGene links
  • MedGen
    MedGen
    Related information in MedGen
  • Nucleotide
    Nucleotide
    Published Nucleotide sequences
  • Pathways + GO
    Pathways + GO
    Pathways, annotations and biological systems (BioSystems) that cite the current article.
  • Protein
    Protein
    Published protein sequences
  • PubMed
    PubMed
    PubMed citations for these articles

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...