nature.com

Specific interaction between 14-3-3 isoforms and the human CDC25B phosphatase - Oncogene

  • ️Ducommun, Bernard
  • ️Tue Mar 07 2000
  • Original Paper
  • Published: 07 March 2000

Oncogene volume 19, pages 1257–1265 (2000)Cite this article

Abstract

CDC25 dual-specificity phosphatases are essential regulators that activate cyclin-dependent kinases (CDKs) at critical stages of the cell cycle. In human cells, CDC25A and C are involved in the control of G1/S and G2/M respectively, whereas CDC25B is proposed to act both in S phase and G2/M. Evidence for an interaction between CDC25 phosphatases and members of the 14-3-3 protein family has been obtained in vitro and in vivo in several organisms. On the basis of the work performed with CDC25C, it has been proposed that phosphorylation is required to mediate the interaction with 14-3-3. Here we have examined the molecular basis of the interaction between CDC25B phosphatases and 14-3-3 proteins. We show that in the two-hybrid assay all three splice variants of CDC25B interact similarly and strongly with 14-3-3η, β and ζ proteins, but poorly with ε and Θ. In vitro, CDC25B interacts at a low level with 14-3-3β, ε, ζ, η, and Θ isoforms. This interaction is not increased upon phosphorylation of CDC25B by CHK1 and is not abolished by dephosphorylation. In contrast, a specific, strong interaction between CDC25B and 14-3-3ζ and η isoforms is revealed by a deletion of 288 residues in the amino-terminal region of CDC25B. This interaction requires the integrity of Ser 323, although it is independent of phosphorylation. Thus, interaction between 14-3-3 proteins and CDC25B is regulated in a manner that is different from that with CDC25C. We propose that, in addition to a low affinity binding site that is available for all 14-3-3 isoforms, post-translational modification of CDC25B in vivo exposes a high-affinity binding site that is specific for the ζ and η14-3-3 isoforms.

This is a preview of subscription content, access via your institution

Access options

Subscribe to this journal

Receive 50 print issues and online access

$259.00 per year

only $5.18 per issue

Buy this article

  • Purchase on SpringerLink
  • Instant access to full article PDF

Prices may be subject to local taxes which are calculated during checkout

Additional access options:

Similar content being viewed by others

Abbreviations

MBP:

Maltose binding protein

CHK1:

checkpoint kinase 1

References

  • Aitken A . 1995 Trends Biochem Sci 20: 95–97

  • Baldin V . 1999 Progress in Cell Cycle Research, Vol 4 L Meijer, A Jézéquel and B Ducommun eds New York, USA Plenum Press In press

    Google Scholar 

  • Baldin V, Cans C, Superti-Furga G and Ducommun B . 1997 Oncogene 14: 2485–2495

  • Blomberg I and Hoffman I . 1999 Mol Cell Biol 19: 6183–6194

  • Chen L, Liu TH and Walworth NC . 1999 Genes Dev 13: 675–685

  • Clarke PR, Hoffmann I, Draetta G and Karsenti E . 1993 Mol Biol Cell 4: 397–411

  • Conklin DS, Galaktionov K and Beach D . 1995 Proc Natl Acad Sci USA 92: 7892–7896

  • Dalal SN, Schweitzer CM and DeCaprio JA . 1999 Mol Cell Biol 19: 4465–4479

  • Descombes P and Nigg EA . 1998 EMBO J 17: 1328–1335

  • Furnari B, Rhind N and Russell P . 1997 Science 277: 1495–1497

  • Gabrielli BG, De Souza CPC, Tonks ID, Clarck JM, Hatward NK and Ellem KAO . 1996 J Cell Sci 109: 1081–1093

  • Galaktionov K and Beach D . 1991 Cell 67: 1181–1194

  • Garner-Hamrick PA and Fischer C . 1998 Int J Cancer 76: 720–728

  • Gautier J, Solomon MJ, Booher RN, Bazan JF and Kirschner MW . 1991 Cell 67: 197–211

  • Hoffman I, Draetta I and Karsenti G . 1994 EMBO J 13: 4302–4310

  • Hoffmann I, Clarke P, Marcote MJ, Karsenti E and Draetta G . 1993 EMBO J 12: 53–63

  • Jessus C and Beach D . 1992 Cell 68: 323–332

  • Jinno S, Suto K, Nagata A, Igashari M, Kanaoka Y, Nojima H and Okayama H . 1994 EMBO J 13: 1549–1556

  • Jones DH, Ley S and Aitken A . 1995 FEBS Lett 368: 55–58

  • Kumagai A and Dunphy WG . 1999 Genes Dev 13: 1067–1072

  • Kumagai A and Dunphy WG . 1996 Science 273: 1377–1380

  • Kumagai A, Guo Z, Emami KH, Wang SX and Dunphy WG . 1998a J Cell Biol 142: 1559–1569

  • Kumagai A, Yakowec PS and Dunphy WG . 1998b Mol Biol Cell 9: 345–354

  • Lammer C, Wagerer S, Saffrich R, Mertens D, Ansorge W and Hoffman I . 1998 J Cell Sci 111: 2445–2453

  • Lopez-Girona A, Furnari B, Mondesert O and Russell P . 1999 Nature 397: 172–175

  • Matsuoka S, Huang M and Elledge SJ . 1998 Science 282: 1893–1897

  • Mueller PR, Coleman TR, Kumagai A and Dunphy WG . 1995 Science 270: 86–90

  • Nagata A, Igarashi M, Jinno S, Suto K and Okayama H . 1991 New Biol 3: 959–968

  • Nigg E . 1995 BioEssays 17: 471–480

  • Peng CY, Graves PR, Ogg S, Thoma RS, Byrnes MJ III, Wu Z, Stephenson MT and Piwnica-Worms H . 1998 Cell Growth Differ 9: 197–208

  • Peng CY, Graves PR, Thoma RS, Wu Z, Shaw AS and Piwnica-Worms H . 1997 Science 277: 1501–1505

  • Petosa C, Masters SC, Bankston LA, Pohl J, Wang B, Fu H and Liddington RC . 1998 J Biol Chem 273: 16305–16310

  • Russell P and Nurse P . 1986 Cell 45: 145–153

  • Russell P and Nurse P . 1987 Cell 49: 559–567

  • Sadhu K, Reed SI, Richardson H and Russell P . 1990 Proc Natl Acad Sci USA 87: 5139–5143

  • Sanchez Y, Wong C, Thoma RS, Richman R, Wu Z, Piwnica-Worms H and Elledge S . 1997 Science 277: 1497–1501

  • Smith D and Johnson K . 1988 Gene 67: 31–40

  • Superti-Furga G, Berges G, Picard D and Busslinger M . 1991 Proc Natl Acad Sci USA 88: 5144–5118

  • Walworth NC and Bernards R . 1996 Science 271: 353–356

  • Weiss A and Schlessinger J . 1998 Cell 94: 277–280

  • Xu X and Burke SP . 1996 J Biol Chem 271: 5118–5124

  • Yang J, Winkler K, Yoshida M and Kornbluth S . 1999 EMBO J 18: 2174–2183

  • Zheng XF and Ruderman JV . 1993 Cell 75: 155–164

Download references

Acknowledgements

We gratefully acknowledge M Yaffe, H Robertson and H Yasuda for the gift plasmids, M Knibiehler for technical assistance, D Mathieu for reagents, and to J Smith and J Hyams for critical reading of the manuscript. This work was supported by the CNRS, l'Université Paul Sabatier, l'Association pour la Recherche sur le Cancer, l'Association Pour la Recherche sur l'Ataxie Télangiectasie, la Ligue Nationale Contre le Cancer and la Ligue Contre le Cancer comité de la Haute-Garonne and comité des Yvelines.

Author information

Authors and Affiliations

  1. LBCMCP–CNRS, Université Paul Sabatier, 118 Route de Narbonne, Toulouse cedex, 31062, France

    Valérie Mils, Véronique Baldin, Françoise Goubin, Isabelle Pinta & Bernard Ducommun

  2. UMR 146 CNRS/Institut Curie-Recherche, Laboratoire d'Oncogenèse Rétrovirale & Moléculaire, Bat 110, Centre Universitaire, 91405, Orsay, France

    Catherine Papin & Alain Eychene

  3. Department of Biochemistry, The Chinese University of Hong Kong Shatin, N.T., Hong Kong

    Mary Waye

Authors

  1. Valérie Mils

    You can also search for this author in PubMed Google Scholar

  2. Véronique Baldin

    You can also search for this author in PubMed Google Scholar

  3. Françoise Goubin

    You can also search for this author in PubMed Google Scholar

  4. Isabelle Pinta

    You can also search for this author in PubMed Google Scholar

  5. Catherine Papin

    You can also search for this author in PubMed Google Scholar

  6. Mary Waye

    You can also search for this author in PubMed Google Scholar

  7. Alain Eychene

    You can also search for this author in PubMed Google Scholar

  8. Bernard Ducommun

    You can also search for this author in PubMed Google Scholar

About this article

Cite this article

Mils, V., Baldin, V., Goubin, F. et al. Specific interaction between 14-3-3 isoforms and the human CDC25B phosphatase. Oncogene 19, 1257–1265 (2000). https://doi.org/10.1038/sj.onc.1203419

Download citation

  • Received: 06 July 1999

  • Revised: 20 December 1999

  • Accepted: 20 December 1999

  • Published: 07 March 2000

  • Issue Date: 02 March 2000

  • DOI: https://doi.org/10.1038/sj.onc.1203419

Keywords