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Originally published In Press as doi:10.1074/jbc.M101885200 on April 25, 2001

J. Biol. Chem., Vol. 276, Issue 26, 23572-23580, June 29, 2001
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BCR-ABL and Interleukin 3 Promote Haematopoietic Cell Proliferation and Survival through Modulation of Cyclin D2 and p27Kip1 Expression*

Yelena Paradaabc, Lolita Banerjiabc, Janet Glassfordabd, Nicholas C. Leaef, Manuel Colladoa, Carmen Rivasg, John L. Lewisgh, Myrtle Y. Gordongi, N. Shaun B. Thomasej, and Eric W.-F. Lamabk

From the a Ludwig Institute for Cancer Research and Section of Virology and Cell Biology, Imperial College School of Medicine at St Mary's, Norfolk Place, London W2 1PG, United Kingdom, the b CRC Labs and Section of Cancer Cell Biology, Imperial College School of Medicine at Hammersmith Hospital, Du Cane Road, London W12 ONN, United Kingdom, the g LRF Centre for Adult Leukaemia, Department of Haematology, Royal Postgraduate Medical School, Imperial College School of Medicine at Hammersmith's Campus, London W12 0NN, United Kingdom, and the e Department of Haematological Medicine, Guy's, King's, St. Thomas' School of Medicine, Rayne Institute, Leukaemia Sciences, Coldharbour Lane, London SE5 9NU, United Kingdom

Although it is evident that BCR-ABL can rescue cytokine-deprived hematopoietic progenitor cells from cell cycle arrest and apoptosis, the exact mechanism of action of BCR/ABL and interleukin (IL)-3 to promote proliferation and survival has not been established. Using the pro-B cell line BaF3 and a BaF3 cell line stably overexpressing BCR-ABL (BaF3-p210), we investigated the proliferative signals derived from BCR-ABL and IL-3. The results indicate that both IL-3 and BCR-ABL target the expression of cyclin Ds and down-regulation of p27Kip1 to mediate pRB-related pocket protein phosphorylation, E2F activation, and thus S phase progression. These findings were further confirmed in a BaF3 cell line (TonB.210) where the BCR-ABL expression is inducible by doxycyclin and by using the drug STI571 to inactivate BCR-ABL activity in BaF3-p210. To establish the functional significance of cyclin D2 and p27Kip1 expression in response to IL-3 and BCR-ABL expression, we studied the effects of ectopic expression of cyclin D2 and p27Kip1 on cell proliferation and survival. Our results demonstrate that both cyclin D2 and p27Kip1 have a role in BaF3 cell proliferation and survival, as ectopic expression of cyclin D2 is sufficient to abolish the cell cycle arrest and apoptosis induced by IL-3 withdrawal or by BCR-ABL inactivation, while overexpression of p27Kip1 can cause cell cycle arrest and apoptosis in the BaF3 cells. Furthermore, our data also suggest that cyclin D2 functions upstream of p27Kip1, cyclin E, and cyclin D3, and therefore, plays an essential part in integrating the signals from IL-3 and BCR-ABL with the pRB/E2F pathway.

* The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

c Contributed equally to the results of this study.

d Supported by the Leukemia Research Fund.

f Supported by the Sir Charles Wolfson Trust.

h Supported by the Leukemia Research Fund.

i Supported by the Leukemia Research Fund.

j Supported by the Leukemia Research Fund and the Sir Charles Wolfson Trust.

k Supported by the Leukemia Research Fund. To whom correspondence should be addressed: CRC Labs and Section of Cancer Cell Biology, Imperial College School of Medicine at Hammersmith Hospital, Du Cane Road, London W12 ONN, United Kingdom. Tel.: 44-020-8383-5834; Fax: 44-20-8383-5830; E-mail: eric.lam@ic.ac.uk.

Copyright © 2001 by The American Society for Biochemistry and Molecular Biology, Inc.
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