Expression of constitutively active Raf-1 in the mitochondria restores antiapoptotic and leukemogenic potential of a transformation-deficient BCR/ABL mutant

Journal of Experimental Medicine

Volumn 187, Issue 12, 1998, Pages 1995-2007

  Salomoni, Paolo ^a,b   Wasik, Mariusz A ^c   Riedel, Richard F ^a   Reiss, Krzysztof ^a   Choi, John K ^c   Skorski, Tomasz ^a   Calabretta, Bruno ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b UNIVERSITY OF MODENA AND REGGIO EMILIA   (Italy)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Apoptosis; Oncogene; Phosphorylation; Signal transduction

Indexed keywords

GROWTH FACTOR; INTERLEUKIN 3; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN TYROSINE KINASE; RAF PROTEIN; RAS PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; ENZYME ACTIVITY; GENETIC TRANSFECTION; HEMATOPOIETIC CELL; LEUKEMOGENESIS; MALE; MITOCHONDRION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMYELOCYTE; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SCID MOUSE; SIGNAL TRANSDUCTION;

ANIMALS; APOPTOSIS; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CELL COMPARTMENTATION; FUSION PROTEINS, BCR-ABL; HEMATOPOIETIC STEM CELLS; INTERLEUKIN-3; LEUKEMIA, EXPERIMENTAL; MICE; MITOCHONDRIA; MUTATION; ONCOGENES; PROTO-ONCOGENE PROTEINS C-RAF; RAS PROTEINS; SIGNAL TRANSDUCTION;

EID: 0032526544     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.187.12.1995     Document Type: Article

References (52)

1. Clark, S.S., J. McLaughlin, M. Timmonis, A.M. Pendergast, Y. Ben-Neriah, L. Dow, G. Rovera, S.D. Smith, and O.N. Witte. 1988. Expression of a distinctive bcr-abl oncogene in Ph1-positive acute lymphoblastic leukemia (ALL). Science. 239:775-779.
2. Shtivelman, E., B. Lifshitz, R.P. Gale, B.A. Roe, and E. Canaani. 1986. Alternative splicing of RNAs transcribed from the human abl gene and from bcr-abl fused gene. Cell. 47:277-286.
3. bcr/abl protein. Proc. Natl. Acad. Sci. USA. 85:9312-9316.
4. Lugo, T.G., A.M. Pendergast, A.J. Muller, and O.N. Witte. 1990. Tyrosine kinase activity and transformation potency of bcr/abl oncogenic products. Science. 247:1079-1082.
5. Gishizki, M.L., and O.N. Witte. 1992. Initiation of deregulated growth of multipotent progenitor cells by bcr-abl in vitro. Science. 256:836-839.
6. bcr/abl gene of the Philadelphia chromosome. Science. 247: 824-830.
7. Heisterkamp, N., G. Jenster, J.T. Hoeve, D. Zovich, P.K. Pattengale, and J. Graffen. 1990. Acute leukemia in bcr/abl transgenic mice. Nature. 344:251-253.
8. McWhirter, J.R., D.L. Glasso, and J.Y. Wang. 1993. A colied-coil oligomerization domain ot Bcr is essential for the transforming function of Bcr-Abl oncoproteins. Mol. Cell. Biol. 13:7587-7595.
9. Pendergast, A.M., A.J. Muller, M.H. Havlik, Y. Maru, and O.N. Witte. 1991. BCR sequences essential for transformation by the BCR/ABL oncogene bind to the ABL SH2 regulatory domain in a non-phosphotyrosine-dependent manner. Cell. 66:161-171.
10. McWhirter, J.R., and J.Y. Wang. 1997. Effect of Bcr sequences on the cellular function of the Bcr-Abl oncoprotein. Oncogene. 15:1625-1634.
11. McGahon, A., R. Bissonnette, M. Schmitt, K.M. Cotter, D.R. Green, and T.G. Cotter. 1994. BCR/ABL maintains resistance of chronic myelogenous leukemia cells to apoptotic cell death. Blood. 83:1179-1187.
12. Bedi, A., B.A. Zehnbauer, J.P. Barber, S.J. Sharkis, and R.J. Jones. 1994. Inhibition of apoptosis by BCR/ABL in chronic myeloid leukemia. Blood. 83:2038-2044.
13. Cortez, D., L. Kadlec, and A.M. Pendergast. 1995. Structural and signalling requirements for BCR-ABL-mediated transformation and inhibition of apoptosis. Mol. Cell. Biol. 15: 5531-5541.
14. Kroemer, G. 1997. The proto-oncogene Bcl-2 and its role in regulating apoptosis. Nat. Med. 3:614-620.
15. Sanchez-Garcia, I., and G. Grütz. 1995. Tumorigenic activity of the BCR/ABL oncogenes is mediated by Bcl-2. Proc. Natl. Acad. Sci. USA. 92:5287-5291.
16. Zhu, J., P.M. Nabissa, B. Hoffman, D.A. Lieberman, and S.K. Shore. 1996. Activated abl oncogenes and apoptosis: differing responses of transformed myeloid progenitor cell lines. Blood. 87:4368-4375.
17. Reed, J.C. 1994. Bcl-2 and the regulation of programmed cell death. J. Cell. Biol. 124:1-6.
18. Yang, E., and S.J. Korsmeyer. 1996. Molecular thanatopsis: a discourse on the BCL-2 family and cell death. Blood. 88: 386-401.
19. Tanaka, S., K. Saito, and J.C. Reed. 1993. Structure-function analysis of the Bcl-2 oncoprotein. Addition of a heterologous transmembrane domain to portions of the Bcl-2 beta protein restores function as a regulator of cell survival. J. Biol. Chem. 268:10920-10926.
20. L. Cell. 87:619-628.
21. Oltvai, Z., and S. Korsmeyer. 1994. Checkpoints of dueling dimers foil death wishes. Cell. 79:189-192.
22. Sedlak, T.W., Z.N. Oltvai, E. Yang, K. Wang, L.H. Boise, C.B. Thompson, and S.J. Korsmeyer. 1995. Multiple Bcl-2 family members demonstrate selective dimerizations with Bax. Proc. Natl. Acad. Sci. USA. 92:7834-7838.
23. Strack, P.R., M.W. Frey, C.J. Rizzo, B. Cordova, H.J. George, R. Meade, S.P. Ho, J. Corman, R. Tricht, and B.D. Korant. 1996. Apoptosis mediated by HIV proteases is preceded by cleavage of Bcl-2. Proc. Natl. Acad. Sci. USA. 93: 9571-9576.
24. Cheng, E.H.Y., D.G. Kirsch, R.J. Clem, R. Ravi, M.B. Kastan, A. Bedi, K. Ueno, and J.M. Hardwick. 1997. Conversion of Bcl-2 to a Bax-like death effector by caspases. Science. 278:1966-1968.
25. Haldar, S., N. Jena, and C.M. Croce. 1995. Inactivation of Bcl-2 by phosphoryation. Proc. Natl. Acad. Sci. USA. 92: 4507-4511.
26. Ito, T., X. Deng, B. Can, and S.W. May. 1997. Bcl-2 phosphorylation required for anti-apoptosis function. J. Biol. Chem. 272:11671-11673.
27. L. Mol. Cell. Biol. 17:7040-7046.
28. Muslin, A.J., J.W. Tanner, P.M. Allen, and A.S. Shaw. 1996. Interaction of 14-3-3 with signaling molecules is mediated by the recognition of phosphoserine. Cell. 84:889-897.
29. Kinoshita, T., T. Yokata, K. Arai, and A. Miyajima. 1995. Suppression of apoptotic death in hematopoietic cells by signalling through the IL-3/GM-CSF receptors. EMBO (Eur. Mol. Biol. Organ.) J. 14:266-275.
30. Cortez, D., G. Stoica, J.H. Pierce, and A.M. Pendergast. 1996. The BCR-ABL tyrosine kinase inhibits apoptosis by activating a Ras-dependent signaling pathway. Oncogene. 13: 2589-2594.
31. Cleveland, J.L., J. Troppmair, G. Packham, D.S. Askew, P. Lloyd, M. Gonzales-Garcia, G. Nunez. J.N. Ihle, and U.R. Rapp. 1994. v-Raf suppresses apoptosis and promotes growth of interleukin-3-dependent myeloid cells. Oncogene. 9:2217-2226.
32. Weissinger, E.M., U. Eissner, C. Grammer, S. Fackler, B. Haefner, L.S. Yoon, K.S. Lu, A. Bazarov, J.M. Sedivy, H. Mischak, and W. Kolch. 1997. Inhibition of the Rat-1 kinase by cyclic AMP agonists causes apoptosis of v-abl-transformed cells. Mol. Cell. Biol. 17:3229-3241.
33. Skorski, T., M. Nieborowska-Skorska, C. Szczylik, P. Kanakaraj, D. Perrotti, G. Zon, A. Gewirtz, B. Perussia, and B. Calabretta. 1995. c-Raf-1 serine/threonine kinase is required in BCR/ABL-dependent and normal hematopoiesis. Cancer Res. 55:2275-2278.
34. Wang, H.-G., T. Miyashita, S. Takayama, T. Sato, T. Torigol, S. Krajewski, S. Tanaka, L. Hovey, III, J. Troppmair, U. Rapp, and J. Reed. 1994. Apoptosis regulation by interaction of bcl-2 protein and Raf-1 kinase. Oncogene. 9:2751-2756.
35. Wang, H.-G., U.R. Rapp, and J. Reed. 1996. Bcl-2 targets the protein kinase Raf-1 to mitochondria. Cell. 87:629-638.
36. Olivier, R., I. Otter, L. Monney, M. Wartmann, and C. Borner. 1997. Bcl-2 does not require Raf kinase activity for its death-protective function. Biochem. J. 324:75-83.
37. Hase, T., V. Muller, H. Riezman, and G. Schatz. 1984. The 70-kd protein of the yeast mitochondrial outer membrane is targeted and anchored via its extreme amino terminus. EMBO (Eur. Mol. Biol. Organ.) J. 3:3157-3164.
38. Valtieri, M., D.J. Tweardy, D. Caracciolo, K. Johnson, F. Mavilio, S. Altmann, D. Santoli, and G. Rovera. 1987. Cytokine-dependent granulocytic differentiation: regulation of proliferative and differentiative responses in a murine progenitor cell line. J. Immunol. 138:3829-3835.
39. bcr/abl: implication for RAS-dependent Philadelphia chromosome positive cell growth. J. Exp. Med. 179: 1855-1865.
40. Fabian, J.R., I.O. Daar, and D.K. Morrison. 1993. Critical tyrosine residues regulate the enzymatic and biological activity of Raf-1 kinase. Mol. Cell. Biol. 13:7170-7179.
41. Fabian, J.R., D.K. Morrison, and I.O. Daar. 1993. Requirement for Raf and MAP kinase function during the meiotic maturation of Xenopus oocytes. J. Cell. Biol. 122:645-652.
42. Salomoni, P., D. Perrotti, R. Martinez, C. Franceschi, and B. Calabretta. 1997. Resistance to apoptosis in CTLL-2 cells constitutively expressing C-Myb is associated with induction of BCL-2 expression and Myb-dependent regulation of bcl-2 promoter activity. Proc. Natl. Acad. Sci. USA. 96:3296-331.
43. bcr/abl transformation of murine myeloid cells. Blood. 82:1838-1847.
44. Marais, R., Y. Light, H.F. Paterson, and C.J. Marshall. 1995. Ras recruits Raf-1 to the plasma membrane for activation by tyrosine phosphorylation. EMBO (Eur. Mol. Biol. Organ.) J. 14:3136-3145.
45. Blagosklomy, M., T. Schulte, P. Nguyen, J. Trepel, and L. Neckers. 1996. Taxol-induced apoptosis and phosphorylation of Bcl-2 protein involves c-Raf-1 and represents a novel c-Raf-1 signal transduction pathway. Cancer Res. 56:1851-1854.
46. Morrison, D.K., and R.E. Cutler. 1997. The complexity of Raf-1 regulation. Curr. Opin. Cell Biol. 9:174-179.
47. Skorski, T., M. Nieborowska-Skorska, P. Wlodarski, G. Zon, R. Iozzo, and B. Calabretta. 1996. Antisense oligodeoxynucleotide combination therapy of primary chronic myelogenous leukemia blast crisis in SCID mice. Blood. 88: 1005-1012.
48. Kantarjan, H.M., A. Deisseroth, R. Kurzrok, Z. Esrov, and M. Talpaz. 1993. Chronic myelogenous leukemia: a concise update. Blood. 82:691-703.
49. Skorski, T., A. Bellacosa, M. Nieborowska-Skorska, M. Majewski, R. Martinez, J.K. Choi, R. Trotta, P. Wlodarski, D. Perrotti, T.O. Chan, et al. 1997. Transformation of hematopoietic cells by BCR/ABL requires activation of a PI-3k/ Akt-dependent pathway. EMBO (Eur. Mol. Biol. Organ.) J. 16:6151-6161.
50. Datta, S.R., H. Dudek, X. Tao, S. Masters, H. Fu, Y. Gotoh, and M. Greenberg. 1997. Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell. 91:231-241.
51. del Peso, L., M. Gonzalez-Garcia, C. Page, R. Herrera, and G. Nunez. 1997. Interleukin-3-induced phosphorylation of BAD through the protein kinase Akt. Science. 278:687-689.
52. Ahmed, N.N., H.L. Grimes, A. Bellacosa, T.O. Chan, and P.N. Tsichlis. 1997. Transduction of IL-2 anti-apoptotic and proliferative signals via Akt. Proc. Natl. Acad. Sci. USA. 94: 3627-3632.