Journal of Experimental Medicine, Vol 183, 811-820, Copyright © 1996 by Rockefeller University Press

ARTICLES

Tyrosyl phosphorylation and DNA binding activity of signal transducers and activators of transcription (STAT) proteins in hematopoietic cell lines transformed by Bcr/Abl

N Carlesso, DA Frank and JD Griffin
Division of Hematologic Malignancies, Dana-Farber Cancer Institute, Boston, Massachusetts 02115, USA.

Bcr/Abl is a chimeric oncogene that can cause both acute and chronic human leukemias. Bcr/Abl-encoded proteins exhibit elevated kinase activity compared to c-Abl, but the mechanisms of transformation are largely unknown. Some of the biological effects of Bcr/Abl overlap with those of hematopoietic cytokines, particularly interleukin 3 (IL-3). Such effects include mitogenesis, enhanced survival, and enhanced basophilic differentiation. Therefore, it has been suggested that p210Bcr/Abl and the IL-3 receptor may activate some common signal transduction pathways. An important pathway for IL-3 signaling involves activation of the Janus family kinases (JAKs) and subsequent tyrosyl phosphorylation of STAT proteins (signal transducers and activators of transcription). This pathway directly links growth factor receptors to gene transcription. We analyzed JAK activation, STAT protein phosphorylation, and the formation of specific DNA-binding complexes containing STAT proteins, in a series of leukemia cell lines transformed by Bcr/Abl or other oncogenes. We also examined these events in cell lines transformed by a temperature sensitive (ts) mutant of Bcr/Abl, where the kinase activity of Abl could be regulated. STAT1 and STAT5 were found to be constitutively phosphorylated in 32D, Ba/F3, and TF-1 cells transformed by Bcr/Abl, but not in the untransformed parental cell lines in the absence of IL-3. Phosphorylation of STAT1 and STAT5 was also observed in the human leukemia cell lines K562 and BV173, which express the Bcr/Abl oncogene, but not in several Bcr/Abl- negative leukemia cell lines. Phosphorylation of STAT1 and STAT5 was directly due to the tyrosine kinase activity of Bcr/Abl since it could be activated or deactivated by temperature shifting of cells expressing the Bcr/Abl ts mutant. DNA-STAT complexes were detected in all Bcr/Abl- transformed cell lines and they were supershifted by antibodies against STAT1 and STAT5. DNA-STAT complexes in 32Dp210Bcr/Abl cells were similar, but not identical, to those formed after IL-3 stimulation. It is interesting to note that JAK kinases (JAK1, JAK2, JAK3, and Tyk2) were not consistently activated in Bcr/Abl-positive cells. These data suggest that STATs can be activated directly by Bcr/Abl, possibly bypassing JAK family kinase activation. Overall, our results suggest a novel mechanism that could contribute to some of the major biological effects of Bcr/Abl transformation.
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• Kaplan, M. H., Daniel, C., Schindler, U., Grusby, M. J. (1998). Stat Proteins Control Lymphocyte Proliferation by Regulating p27Kip1 Expression. Mol. Cell. Biol. 18: 1996-2003 [Abstract] [Full Text]  
• Nelson, K. L., Rogers, J. A., Bowman, T. L., Jove, R., Smithgall, T. E. (1998). Activation of STAT3 by the c-Fes Protein-tyrosine Kinase. J. Biol. Chem. 273: 7072-7077 [Abstract] [Full Text]  
• Ichiba, M., Nakajima, K., Yamanaka, Y., Kiuchi, N., Hirano, T. (1998). Autoregulation of the Stat3 Gene through Cooperation with a cAMP-responsive Element-binding Protein. J. Biol. Chem. 273: 6132-6138 [Abstract] [Full Text]  
• Yamamura, Y., Senda, H., Kageyama, Y., Matsuzaki, T., Noda, M., Ikawa, Y. (1998). Erythropoietin and Friend Virus gp55 Activate Different JAK/STAT Pathways through the Erythropoietin Receptor in Erythroid Cells. Mol. Cell. Biol. 18: 1172-1180 [Abstract] [Full Text]  
• Okuda, K., Smith, L., Griffin, J. D., Foster, R. (1997). Signaling Functions of the Tyrosine Residues in the beta c Chain of the Granulocyte-Macrophage Colony-Stimulating Factor Receptor. Blood 90: 4759-4766 [Abstract] [Full Text]  
• Saharinen, P., Ekman, N., Sarvas, K., Parker, P., Alitalo, K., Silvennoinen, O. (1997). The Bmx Tyrosine Kinase Induces Activation of the Stat Signaling Pathway, Which Is Specifically Inhibited by Protein Kinase Cdelta. Blood 90: 4341-4353 [Abstract] [Full Text]  
• Luo, G., Yu-Lee, L.-y. (1997). Transcriptional Inhibition by Stat5. DIFFERENTIAL ACTIVITIES AT GROWTH-RELATED VERSUS DIFFERENTIATION-SPECIFIC PROMOTERS. J. Biol. Chem. 272: 26841-26849 [Abstract] [Full Text]  
• Tenen, D. G., Hromas, R., Licht, J. D., Zhang, D.-E. (1997). Transcription Factors, Normal Myeloid Development, and Leukemia. Blood 90: 489-519 [Full Text]  
• Nielsen, M., Kaltoft, K., Nordahl, M., Ropke, C., Geisler, C., Mustelin, T., Dobson, P., Svejgaard, A., Odum, N. (1997). Constitutive activation of a slowly migrating isoform of Stat3 in mycosis fungoides: Tyrphostin AG490 inhibits Stat3 activation and growth of mycosis fungoides tumor cell lines. Proc. Natl. Acad. Sci. USA 94: 6764-6769 [Abstract] [Full Text]  
• Barber, D. L., Mason, J. M., Fukazawa, T., Reedquist, K. A., Druker, B. J., Band, H., D'Andrea, A. D. (1997). Erythropoietin and Interleukin-3 Activate Tyrosine Phosphorylation of CBL and Association With CRK Adaptor Proteins. Blood 89: 3166-3174 [Abstract] [Full Text]  
• Selleri, C., Sato, T., Del Vecchio, L., Luciano, L., Barrett, A. J., Rotoli, B., Young, N. S., Maciejewski, J. P. (1997). Involvement of Fas-Mediated Apoptosis in the Inhibitory Effects of Interferon-alpha in Chronic Myelogenous Leukemia. Blood 89: 957-964 [Abstract] [Full Text]  
• Herrada, G, Wolgemuth, D. (1997). The mouse transcription factor Stat4 is expressed in haploid male germ cells and is present in the perinuclear theca of spermatozoa. J. Cell Sci. 110: 1543-1553 [Abstract]  
• Ilaria, R. L. Jr., Van Etten, R. A. (1996). P210 and P190BCR/ABL Induce the Tyrosine Phosphorylation and DNA Binding Activity of Multiple Specific STAT Family Members. J. Biol. Chem. 271: 31704-31710 [Abstract] [Full Text]  
• Lionberger, J. M., Wilson, M. B., Smithgall, T. E. (2000). Transformation of Myeloid Leukemia Cells to Cytokine Independence by Bcr-Abl Is Suppressed by Kinase-defective Hck. J. Biol. Chem. 275: 18581-18585 [Abstract] [Full Text]  
• Daniel, C., Salvekar, A., Schindler, U. (2000). A Gain-of-function Mutation in STAT6. J. Biol. Chem. 275: 14255-14259 [Abstract] [Full Text]  
• Gesbert, F., Sellers, W. R., Signoretti, S., Loda, M., Griffin, J. D. (2000). BCR/ABL Regulates Expression of the Cyclin-dependent Kinase Inhibitor p27Kip1 through the Phosphatidylinositol 3-Kinase/AKT Pathway. J. Biol. Chem. 275: 39223-39230 [Abstract] [Full Text]  
• Nguyen, M. H.-H., Ho, J. M.-Y., Beattie, B. K., Barber, D. L. (2001). TEL-JAK2 Mediates Constitutive Activation of the Phosphatidylinositol 3'-Kinase/Protein Kinase B Signaling Pathway. J. Biol. Chem. 276: 32704-32713 [Abstract] [Full Text]  

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