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Molecular and Cellular Biology, December 2000, p. 9138-9148, Vol. 20, No. 24
0270-7306/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.

Forkhead Transcription Factor FKHR-L1 Modulates Cytokine-Dependent Transcriptional Regulation of p27KIP1

Pascale F. Dijkers,1 Rene H. Medema,2 Cornelieke Pals,1 Lolita Banerji,3 N. Shaun B. Thomas,4 Eric W.-F. Lam,3 Boudewijn M. T. Burgering,5 Jan A. M. Raaijmakers,1 Jan-Willem J. Lammers, Leo Koenderman,1 and Paul J. Coffer1,*

Departments of Pulmonary Diseases1 and Hematology,2 University Medical Center, 3584 CX Utrecht, and Department of Physiological Chemistry and Center for Biomedical Genetics, University of Utrecht, 3584 CG Utrecht,5 The Netherlands, and Ludwig Institute for Cancer Research and Section of Virology and Cell Biology, Imperial College School of Medicine, St. Mary's Campus,3 and Department of Haematological Medicine, Guy's, King's and St. Thomas' School of Medicine and Dentistry, King's Denmark Hill Campus,4 London, United Kingdom

Received 12 May 2000/Returned for modification 21 June 2000/Accepted 12 September 2000

Interleukin-3 (IL-3), IL-5, and granulocyte-macrophage colony-stimulating factor regulate the survival, proliferation, and differentiation of hematopoietic lineages. Phosphatidylinositol 3-kinase (PI3K) has been implicated in the regulation of these processes. Here we investigate the molecular mechanism by which PI3K regulates cytokine-mediated proliferation and survival in the murine pre-B-cell line Ba/F3. IL-3 was found to repress the expression of the cyclin-dependent kinase inhibitor p27KIP1 through activation of PI3K, and this occurs at the level of transcription. This transcriptional regulation occurs through modulation of the forkhead transcription factor FKHR-L1, and IL-3 inhibited FKHR-L1 activity in a PI3K-dependent manner. We have generated Ba/F3 cell lines expressing a tamoxifen-inducible active FKHR-L1 mutant [FKHR-L1(A3):ER*]. Tamoxifen-mediated activation of FKHR-L1(A3):ER* resulted in a striking increase in p27KIP1 promoter activity and mRNA and protein levels as well as induction of the apoptotic program. The level of p27KIP1 appears to be critical in the regulation of cell survival since mere ectopic expression of p27KIP1 was sufficient to induce Ba/F3 apoptosis. Moreover, cell survival was increased in cytokine-starved bone marrow-derived stem cells from p27KIP1 null-mutant mice compared to that in cells from wild-type mice. Taken together, these observations indicate that inhibition of p27KIP1 transcription through PI3K-induced FKHR-L1 phosphorylation provides a novel mechanism of regulating cytokine-mediated survival and proliferation.

* Corresponding author. Mailing address: Department of Pulmonary Diseases, University Medical Center, Heidelberglaan 100, 3584 CX Utrecht, The Netherlands. Phone: 31-30-2507134. Fax: 31-30-2505414. E-mail: P.Coffer{at}hli.azu.nl.

Molecular and Cellular Biology, December 2000, p. 9138-9148, Vol. 20, No. 24
0270-7306/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.


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