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Molecular and Cellular Biology, April 2002, p. 2025-2036, Vol. 22, No. 7
0270-7306/02/$04.00+0     DOI: 10.1128/MCB.22.7.2025-2036.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.

Control of Cell Cycle Exit and Entry by Protein Kinase B-Regulated Forkhead Transcription Factors

Geert J. P. L. Kops,1 Rene H. Medema,2 Janet Glassford,3,{dagger} Marieke A. G. Essers,1 Pascale F. Dijkers,4 Paul J. Coffer,4 Eric W.-F. Lam,3,{dagger} and Boudewijn M. T. Burgering1*

Department of Physiological Chemistry and Center for Biomedical Genetics,1 Department of Pulmonary Diseases, University Medical Center Utrecht, 3584 CG Utrecht,4 Department of Molecular Biology, Netherlands Cancer Institute, Amsterdam, The Netherlands,2 Ludwig Institute for Cancer Research and Section of Virology and Cell Biology, Imperial College School of Medicine at St. Mary's Campus, London, United Kingdom3

Received 19 September 2001/ Returned for modification 22 October 2001/ Accepted 21 December 2001

AFX-like Forkhead transcription factors, which are controlled by phosphatidylinositol 3-kinase (PI3K)/protein kinase B (PKB) signaling, are involved in regulating cell cycle progression and cell death. Both cell cycle arrest and induction of apoptosis are mediated in part by transcriptional regulation of p27kip1. Here we show that the Forkheads AFX (FOXO4) and FKHR-L1 (FOXO3a) also directly control transcription of the retinoblastoma-like p130 protein and cause upregulation of p130 protein expression. Detailed analysis of p130 regulation demonstrates that following Forkhead-induced cell cycle arrest, cells enter G0 and become quiescent. This is shown by a change in phosphorylation of p130 to G0-specific forms and increased p130/E2F-4 complex formation. Most importantly, long-term Forkhead activation causes a sustained but reversible inhibition of proliferation without a marked increase in apoptosis. As for the activity of the Forkheads, we also show that protein levels of p130 are controlled by endogenous PI3K/PKB signaling upon cell cycle reentry. Surprisingly, not only nontransformed cells, but also cancer cells such as human colon carcinoma cells, are forced into quiescence by Forkhead activation. We therefore propose that Forkhead inactivation by PKB signaling in quiescent cells is a crucial step in cell cycle reentry and contributes to the processes of transformation and regeneration.

* Corresponding author. Mailing address: Department of Physiological Chemistry and Center for Biomedical Genetics, University Medical Center Utrecht, Stratenum, Universiteitsweg 100, 3584 CG Utrecht, The Netherlands. Phone: 31 30 253 8918. Fax: 331 30 253 9035. E-mail: b.m.t.burgering{at}med.uu.nl.

{dagger} Present address: CRC Labs and Section of Cancer Cell Biology, Imperial College School of Medicine at Hammersmith Hospital, London, United Kingdom.

Molecular and Cellular Biology, April 2002, p. 2025-2036, Vol. 22, No. 7
0022-538X/02/$04.00+0     DOI: 10.1128/MCB.22.7.2025-2036.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.



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