Active Akt and Functional p53 Modulate Apoptosis in Abelson Virus-Transformed Pre-B Cells

Journal of Virology

Volumn 78, Issue 4, 2004, Pages 1636-1644

  Gong, Li ^a,c   Unnikrishnan, Indira ^b,d   Raghavan, Anuradha ^b   Parmar, Kalindi ^b,e   Rosenberg, Naomi ^a,b  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b TUFTS UNIVERSITY   (United States)

^c Entelos Inc   (United States)

^d THOMAS JEFFERSON UNIVERSITY   (United States)

^e BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABELSON KINASE; PROTEIN KINASE B; PROTEIN P53; PROTEIN SH2; PROTEIN TYROSINE KINASE;

ABELSON MURINE LEUKEMIA ONCOVIRUS; ANIMAL CELL; APOPTOSIS; ARTICLE; CELL TRANSFORMATION; CONTROLLED STUDY; CORRELATION ANALYSIS; GENE ACTIVITY; GENE CONTROL; GENE FUNCTION; MOUSE; MUTANT; NONHUMAN; PHENOTYPE; PRE B LYMPHOCYTE; PRIORITY JOURNAL; PROTEIN DOMAIN; SIGNAL TRANSDUCTION; TEMPERATURE DEPENDENCE; VIRUS PATHOGENESIS;

ABELSON MURINE LEUKEMIA VIRUS; ANIMALS; APOPTOSIS; B-LYMPHOCYTES; BONE MARROW CELLS; CELL LINE, TRANSFORMED; CELL TRANSFORMATION, VIRAL; HUMANS; MICE; ONCOGENE PROTEINS V-ABL; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; SRC HOMOLOGY DOMAINS; TUMOR SUPPRESSOR PROTEIN P53;

EID: 0842347727     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.78.4.1636-1644.2004     Document Type: Article

References (56)

1. Amarante-Mendes, G. P., A. J. McGahon, W. K. Nishioka, D. E. Afar, O. N. Witte, and D. R. Green. 1998. Bcl-2-independent Bcr-Abl-mediated resistance to apoptosis: protection is correlated with up regulation of Bcl-XL. Oncogene 16:1383-1390.
2. Banerjee, A., and P. Rothman. 1998. IL-7 reconstitutes multiple aspects of v-Abl-mediated signaling. J. Immunol. 161:4611-4617.
3. Brunet, A., A. Bonni, M. J. Zigmond, M. Z. Lin, P. Juo, L. S. Hu, M. J. Anderson, K. C. Arden, J. Blenis, and M. E. Greenberg. 1999. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96:857-868.
4. Chen, Q., J. Turner, A. J. Watson, and C. Dive. 1997. v-Abl protein tyrosine kinase (PTK) mediated suppression of apoptosis is associated with the up-regulation of Bcl-XL. Oncogene 15:2249-2254.
5. Chen, Y. Y., and N. Rosenberg. 1992. Lymphoid cells transformed by Abelson virus require the v-abl protein tyrosine kinase only during early G1. Proc. Natl. Acad. Sci. USA 89:6683-6687.
6. Chen, Y.-Y., L. C. Wang, M. S. Huang, and N. Rosenberg. 1994. An active v-abl protein tyrosine kinase blocks immunoglobulin light-chain gene rearrangement. Genes Dev. 8:688-697.
7. Chesebro, B., K. Wehrly, M. Cloyd, W. Britt, J. Portis, J. Collins, and J. Nishio. 1981. Characterization of mouse monoclonal antibodies specific for Friend murine leukemia virus-induced erythroleukemia cells: Friend-specific and FMR-specific antigens. Virology 112:131-144.
8. Cortez, D., L. Kadlec, and A. M. Pendergast. 1995. Structural and signaling requirements for BCR-ABL-mediated transformation and inhibition of apoptosis. Mol. Cell. Biol. 15:5531-5541.
9. Cortez, D., G. Reuther, and A. M. Pendergast. 1997. The Bcr-Abl tyrosine kinase activates mitogenic signaling pathways and stimulates G1-to-S phase transition in hematopoietic cells. Oncogene 15:2333-2342.
10. Datta, S. R., A. Brunet, and M. E. Greenberg. 1999. Cellular survival: a play in three Akts. Genes Dev. 13:2905-2927.
11. Datta, S. R., H. Dudek, X. Tao, S. Masters, H. Fu, Y. Gotoh, and M. E. Greenberg. 1997. Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell 91:231-241.
12. 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.
13. DuBridge, R. B., P. Tang, H. C. Hsai, P.-M. Leong, J. H. Miller, and M. P. Calos. 1987. Analysis of mutation in human cells by using an Epstein-Barr virus shuttle system. Mol. Cell. Biol. 7:379-387.
14. Engelman, A., and N. Rosenberg. 1990. bcr/abl and src but not myc and ras replace v-abl in lymphoid transformation. Mol. Cell. Biol. 10:4365-4369.
15. Engelman, A., and N. Rosenberg. 1987. Isolation of temperature-sensitive Abelson virus mutants by site-directed mutagenesis. Proc. Natl. Acad. Sci. USA 84:8021-8025.
16. Engelman, A., and N. Rosenberg. 1990. Temperature-sensitive mutants of Abelson murine leukemia virus deficient in protein tyrosine kinase activity. J. Virol. 64:4242-4251.
17. Franke, T. F., S. I. Yang, T. O. Chan, K. Datta, A. Kazlauskas, D. K. Morrison, D. R. Kaplan, and P. N. Tsichlis. 1995. The protein kinase encoded by Akt proto-oncogene is a target of the PDGF activated PI 3-kinase. Cell 81:727-736.
18. Gottlieb, T. M., J. F. M. Leal, R. Seger, Y. Taya, and M. Oren. 2002. Cross-talk between Akt, p53 and Mdm2: possible implications for the regulation of apoptosis. Oncogene 21:1299-1303.
19. Hawley, R. G., F. H. Lieu, A. Z. Fong, and T. S. Hawley. 1994. Versatile retroviral vectors for potential use in gene therapy. Gene Ther. 1:136-138.
20. BCR/ABL is not required for the transformation of hematopoietic factor-dependent cells. Blood 86:3897-3904.
21. Jenab-Wolcott, J., D. Rodriguez-Correa, A. Reitmair, T. Mak, and N. Rosenberg. 2000. The absence of Msh2 alters Abelson virus pre-B-cell transformation by influencing p53 mutation. Mol. Cell. Biol. 20:8373-8381.
22. Joneson, T., M. A. White, M. H. Wigler, and D. Bar-Sagi. 1996. Stimulation of membrane ruffling and MAP kinase activation by distinct effectors of RAS. Science 271:810-812.
23. Kohn, A. D., F. Takeuchi, and R. A. Roth. 1996. Akt, a pleckstrin homology domain containing kinase, is activated primarily by phosphorylation. J. Biol. Chem. 271:21920-21926.
24. Mainville, C., K. Parmar, I. Unnikrishnan, G. D. Raffel, L. Gong, and N. Rosenberg. 2001. Alteration of the FLVRES motif in the v-Abl SH2 domain confers a temperature-sensitive transformation phenotype. J. Virol. 75:1816-1823.
25. Majewski, M., M. Nieborowska-Skorska, P. Salomoni, A. Slupianek K. Reiss, R. Trotta, B. Calabretta, and T. Skorski. 1999. Activation of mitochondrial Raf-1 is involved in the antiapoptotic effects of Akt. Cancer Res. 59:2815-2819.
26. Marshall, C. 1996. Ras effectors. Curr. Opin. Cell Biol. 8:197-204.
27. Morgenstern, J. P., and H. Land. 1990. Advanced mammalian gene transfer: high titre retroviral vectors with multiple drug selection markers and a complementary helper-free packaging cell line. Nucleic Acids Res. 18:3587.
28. Muljo, S. A., and M. S. Schlissel. 2003. A small molecule Abl kinase inhibitor induces differentiation of Abelson virus-transformed pre-B cell lines. Nat. Immunol. 4:31-37.
29. Muller, A. J., J. C. Young, A. M. Pendergast, M. Pondel, N. R. Landau, D. R. Littman, and O. N. Witte. 1991. BCR first exon sequences specifically activate the BCR/ABL tyrosine kinase oncogene of Philadelphia chromosome-positive human leukemias. Mol. Cell. Biol. 11:1785-1792.
30. Owen, P. J., P. Musk, C. A. Evans, and A. D. Whetton. 1993. Cellular signaling events elicated by v-abl associated with growth factor independence in an interluekin-3-dependent cell line. J. Biol. Chem. 268:15696-15703.
31. Pendergast, A. M., M. L. Gishizky, M. H. Havlik, and O. N. Witte. 1993. SH1 domain autophosphorylation of P210 BCR/ABL is required for transformation but not growth factor independence. Mol. Cell. Biol. 13:1728-1736.
32. Arf induces p53-dependent apoptosis during Abelson virus-mediated pre-B cell transformation. Proc. Natl. Acad. Sci. USA 95:13194-13199.
33. Raffel, G. D., K. Parmar, and N. Rosenberg. 1996. In vivo association of v-Abl with Shc mediated by a non-phosphotyrosine-dependent SH2 interaction. J. Biol. Chem. 271:4640-4645.
34. Rameh, L. E., and L. C. Cantley. 1999. The role of phosphoinositide 3-kinase lipid products in cell function. J. Biol. Chem. 274:8347-8350.
35. Reid, S., R. Cross, and E. Snow. 1996. Combined Hoechst 33342 and merocyanin 540 staining to examine murine B cell cycle stage, viability and apoptosis. J. Immunol. Methods 192:43-54.
36. Reynolds, F. H., Jr., S. Oroszlan, and J. R. Stephenson. 1982. Abelson murine leukemia virus P120: identification and characterization of tyrosine phosphorylation sites. J. Virol. 44:1097-1101.
37. Rosenberg, N., and O. N. Witte. 1988. The viral and cellular forms of the Abelson (abl) oncogene. Adv. Virus Res. 35:39-81.
38. Salomoni, P., M. A. Wasik, R. F. Riedel, K. Reiss, J. K. Choi, T. Skorski, and B. Calabretta. 1998. Expression of constitutively active Raf-1 in the mitochondria restores antiapoptotic and leukemogenic potential of a transformation-deficient BCR/ABL mutant. J. Exp. Med. 187:1995-2007.
39. Sanchez-Garcia, I., and G. Grutz. 1995. Tumorigenic activity of the BCR-ABL oncogenes is mediated by BCL2. Proc. Natl. Acad. Sci. USA 92:5287-5291.
40. Sawyers, C. L., W. Callahan, and O. N. Witte. 1992. Dominant negative myc blocks transformation by abl oncogenes. Cell 70:901-910.
41. Sawyers, C. L., J. McLaughlin, and O. N. Witte. 1995. Genetic requirement for ras in the transformation of fibroblasts and hematopoietic cells by the bcr-abl oncogene. J. Exp. Med. 181:307-313.
42. Sherr, C. J. 2001. The Ink4a/ARF network in tumour suppression. Nat. Rev. Mol. Cell Biol. 2:731-737.
43. Skorski, T., A. Bellacosa, M. Nieborowska-Skorska, M. Majewski, R. Martinez, J. K. Choi, R. Trotta, P. Wlodarski, D. Perrotti, T. O. Chan, M. A. Wasik, P. N. Tsichlis, and B. Calabretta. 1997. Transformation of hematopoietic cells by BCR/ABL requires activation of a PI-3K/Akt-dependent pathway. EMBO J. 16:6151-6161.
44. Skorski, T., P. Kanakaraj, M. R. Neiborowska-Skorska, M. Z., S. C. Wen, G. Zon, A. M. Gerwitz, P. Perussia, and B. Calabretta. 1995. Phosphatidylinositol-3 kinase activity is regulated by BCR/ABL and is required for growth of Philadelphia chromosome-positive cells. Blood 2:726-736.
45. Skorski, T., M. Nieborowska-Skorska, C. Szcylik, P. Kanakaraj, D. Perrotti, G. Zon, A. Gerwirtz, B. Perussia, and B. Calabretta. 1995. c-Raf-1 serine/ threonine kinase is required in BCR/ABL-dependent and normal hamatopoiesis. Cancer Res. 55:2275-2278.
46. Tang, X., C. P. Downes, A. D. Whetton, and P. J. Owen-Lych. 2000. Role of phosphatidylinositol 3-kinase and specific protein kinase B isoforms in the suppression of apoptosis mediated by the Abelson protein-tyrosine kinase. J. Biol. Chem. 275:13142-13148.
47. Thome, K., A. Radfar, and N. Rosenberg. 1997. Mutation of Tp53 contributes to the malignant phenotype of Abelson virus-transformed lymphoid cells. J. Virol. 77:8149-8156.
48. Unnikrishnan, I., A. Radfar, J. Jenab-Wolcott, and N. Rosenberg. 1999. p53 mediates apoptotic crisis in primary Abelson murine leukemia virus-transformed pre-B cells. Mol. Cell. Biol. 19:4825-4831.
49. Unnikrishnan, I., and N. Rosenberg. 2003. Absence of p53 complements defects in Abelson murine leukemia virus signaling. J. Virol. 77:6208-6215.
50. Van Parijs, L., Y. Refaeli, J. D. Lord, B. H. Nelson, A. K. Abbas, and D. Baltimore. 1999. Uncoupling IL-2 signals that regulate T cell proliferation, survival, and Fas-mediated activation induced cell death. Immunity 11:281-288.
51. Weissinger, E. M., G. Eissner, C. Grammer, A. Fackler, B. Haefner, L. S. Yoon, K. S. Lu, A. Bazarov, J. M. Sedivy, H. Mischak, and W. Kolch. 1997. Inhibition of the Raf-1 kinase by cyclin AMP agonists causes apoptosis of v-abl-transformed cells. Mol. Cell. Biol. 17:3229-3241.
52. White, Q. P., C. Nicolette, A. Minden, A. Polverino, L. Vanaelst, M. Karin, and M. H. Wigler. 1995. Multiple ras functions can contribute to mammalian-cell transformation. Cell 80:533-541.
53. Zhu, J., P. M. Nabissa, B. Hoffman, D. A. Liebermann, and S. K. Shore. 1996. Activated abl oncogenes and apoptosis: differing response of transformed myeloid progenitor cells. Blood 87:4368-4375.
54. Zou, X., and K. Calame. 1999. Signaling pathways activated by oncogenic forms of Abl tyrosine kinase. J. Biol. Chem. 274:18141-18144.
55. Zou, X., F. Cong, M. Coutts, G. Cattoretti, S. P. Goff, and K. Calame. 2000. p53 deficiency increases transformation by v-Abl and rescues the ability of a C-terminally truncated v-Abl mutant to induce pre-B lymphoma in vivo. Mol. Cell. Biol. 20:628-633.
56. Zou, X., S. Rudchenko, K.-K. Wong, and K. Calame. 1997. Induction of c-myc transcription by the v-Abl tyrosine kinase requires Ras, Raf1, and cyclin-dependent kinases. Genes Dev. 11:654-662.