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

doi:10.1128/MCB.20.24.9138-9148.2000

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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 p27^KIP1

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, anddifferentiation of hematopoietic lineages. Phosphatidylinositol3-kinase (PI3K) has been implicated in the regulation of theseprocesses. Here we investigate the molecular mechanism by whichPI3K regulates cytokine-mediated proliferation and survival inthe murine pre-B-cell line Ba/F3. IL-3 was found to repress theexpression of the cyclin-dependent kinase inhibitor p27^KIP1 through activation of PI3K, and this occurs at the level of transcription.This transcriptional regulation occurs through modulation of theforkhead transcription factor FKHR-L1, and IL-3 inhibited FKHR-L1activity in a PI3K-dependent manner. We have generated Ba/F3 celllines expressing a tamoxifen-inducible active FKHR-L1 mutant [FKHR-L1(A3):ER*].Tamoxifen-mediated activation of FKHR-L1(A3):ER* resulted in astriking increase in p27^KIP1 promoter activity and mRNA and protein levels as well as inductionof the apoptotic program. The level of p27^KIP1 appears to be critical in the regulation of cell survival sincemere ectopic expression of p27^KIP1 was sufficient to induce Ba/F3 apoptosis. Moreover, cell survivalwas increased in cytokine-starved bone marrow-derived stem cellsfrom p27^KIP1 null-mutant mice compared to that in cells from wild-type mice.Taken together, these observations indicate that inhibition ofp27^KIP1 transcription through PI3K-induced FKHR-L1 phosphorylation providesa novel mechanism of regulating cytokine-mediated survival andproliferation.

^* Corresponding author. Mailing address: Department of Pulmonary Diseases, University Medical Center, Heidelberglaan 100, 3584CX 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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Bakker, W. J., Blazquez-Domingo, M., Kolbus, A., Besooyen, J., Steinlein, P., Beug, H., Coffer, P. J., Lowenberg, B., von Lindern, M., van Dijk, T. B. (2004). FoxO3a regulates erythroid differentiation and induces BTG1, an activator of protein arginine methyl transferase 1. J. Cell Biol. 164: 175-184 [Abstract] [Full Text]
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Wang, X., Chen, L., Maures, T. J., Herrington, J., Carter-Su, C. (2004). SH2-B Is a Positive Regulator of Nerve Growth Factor-mediated Activation of the Akt/Forkhead Pathway in PC12 Cells. J. Biol. Chem. 279: 133-141 [Abstract] [Full Text]
Li, L., Ren, C. H., Tahir, S. A., Ren, C., Thompson, T. C. (2003). Caveolin-1 Maintains Activated Akt in Prostate Cancer Cells through Scaffolding Domain Binding Site Interactions with and Inhibition of Serine/Threonine Protein Phosphatases PP1 and PP2A. Mol. Cell. Biol. 23: 9389-9404 [Abstract] [Full Text]
Sunters, A., Fernandez de Mattos, S., Stahl, M., Brosens, J. J., Zoumpoulidou, G., Saunders, C. A., Coffer, P. J., Medema, R. H., Coombes, R. C., Lam, E. W.-F. (2003). FoxO3a Transcriptional Regulation of Bim Controls Apoptosis in Paclitaxel-treated Breast Cancer Cell Lines. J. Biol. Chem. 278: 49795-49805 [Abstract] [Full Text]
Tsai, W.-C., Bhattacharyya, N., Han, L.-Y., Hanover, J. A., Rechler, M. M. (2003). Insulin Inhibition of Transcription Stimulated by the Forkhead Protein Foxo1 Is Not Solely due to Nuclear Exclusion. Endocrinology 144: 5615-5622 [Abstract] [Full Text]
Christian, S. L., Lee, R. L., McLeod, S. J., Burgess, A. E., Li, A. H. Y., Dang-Lawson, M., Lin, K. B. L., Gold, M. R. (2003). Activation of the Rap GTPases in B Lymphocytes Modulates B Cell Antigen Receptor-induced Activation of Akt but Has No Effect on MAPK Activation. J. Biol. Chem. 278: 41756-41767 [Abstract] [Full Text]
Crossley, L. J. (2003). Neutrophil activation by fMLP regulates FOXO (forkhead) transcription factors by multiple pathways, one of which includes the binding of FOXO to the survival factor Mcl-1. J. Leukoc. Biol. 74: 583-592 [Abstract] [Full Text]
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Birkenkamp, K. U., Coffer, P. J. (2003). FOXO Transcription Factors as Regulators of Immune Homeostasis: Molecules to Die for?. J. Immunol. 171: 1623-1629 [Full Text]
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Tang, T. T.-L., Lasky, L. A. (2003). The Forkhead Transcription Factor FOXO4 Induces the Down-regulation of Hypoxia-inducible Factor 1{alpha} by a von Hippel-Lindau Protein-independent Mechanism. J. Biol. Chem. 278: 30125-30135 [Abstract] [Full Text]
Perrot, V., Rechler, M. M. (2003). Characterization of Insulin Inhibition of Transactivation by a C-terminal Fragment of the Forkhead Transcription Factor Foxo1 in Rat Hepatoma Cells. J. Biol. Chem. 278: 26111-26119 [Abstract] [Full Text]
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Komatsu, N., Watanabe, T., Uchida, M., Mori, M., Kirito, K., Kikuchi, S., Liu, Q., Tauchi, T., Miyazawa, K., Endo, H., Nagai, T., Ozawa, K. (2003). A Member of Forkhead Transcription Factor FKHRL1 Is a Downstream Effector of STI571-induced Cell Cycle Arrest in BCR-ABL-expressing Cells. J. Biol. Chem. 278: 6411-6419 [Abstract] [Full Text]
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