Molecular mechanisms associated with the regulation of apoptosis by the two alternatively spliced products of c-Myb

Molecular and Cellular Biology

Volumn 23, Issue 18, 2003, Pages 6631-6645

  Kumar, Atul ^a,b   Baker, Stacey J ^a   Lee, Clement M ^a   Reddy, E Premkumar ^a  

^a TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MONTEFIORE MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; COMPLEMENTARY DNA; GLUTATHIONE TRANSFERASE; INTERLEUKIN 3; MESSENGER RNA; PROTEIN C MYB;

ALTERNATIVE RNA SPLICING; ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DEATH; MOUSE; NONHUMAN; ONCOGENE C MYB; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

ALTERNATIVE SPLICING; ANIMALS; APOPTOSIS; BONE MARROW CELLS; CASPASES; CELLS, CULTURED; CYTOCHROME C GROUP; ENZYME ACTIVATION; GENE EXPRESSION REGULATION; GLUTATHIONE TRANSFERASE; INTERLEUKIN-3; MICE; MUTATION; MYELOID CELLS; OLIGONUCLEOTIDES, ANTISENSE; PROTEIN ISOFORMS; PROTO-ONCOGENE PROTEINS C-MYB; TRANS-ACTIVATION (GENETICS);

ANIMALIA; MURINAE;

EID: 0043192766     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.23.18.6631-6645.2003     Document Type: Article

References (68)

1. Arends, M. J., R. G. Morris, and A. H. Wyllie. 1990. Apoptosis. The role of the endonuclease. Am. J. Pathol. 136:593-608.
2. Askew, D. S., R. A. Ashmun, B. C. Simmons, and J. L. Cleveland. 1991. Constitutive c-myc expression in an IL-3-dependent myeloid cell line suppresses cell cycle arrest and accelerates apoptosis. Oncogene 6:1915-1922.
3. Baker, S. J., and E. P. Reddy. 1998. Modulation of life and death by the TNF receptor superfamily. Oncogene 17:3261-3270.
4. Bergmann, A., J. Agapite, and H. Steller. 1998. Mechanisms and control of programmed cell death in invertebrates. Oncogene 17:3215-3223.
5. Biedenkapp, H., U. Borgmeyer, A. E. Sippel, and K. H. Klempnauer. 1988. Viral myb oncogene encodes a sequence-specific DNA-binding activity. Nature 335:835-837.
6. Bies, J., R. Mukhopadhyaya, J. Pierce, and L. Wolff. 1995. Only late, nonmitotic stages of granulocyte differentiation in 32Dcl3 cells are blocked by ectopic expression of murine c-myb and its truncated forms. Cell Growth Differ. 6:59-68.
7. Bourette, R. P., G. M. Myles, K. Carlberg, A. R. Chen, and L. R. Rohrschneider. 1995. Uncoupling of the proliferation and differentiation signals mediated by the murine macrophage colony-stimulating factor receptor expressed in myeloid FDC-P1 cells. Cell Growth Differ. 6:631-645.
8. Clarke, M. F., J. F. Kukowska-Latallo, E. Westin, M. Smith, and E. V. Prochownik. 1988. Constitutive expression of a c-myb cDNA blocks Friend murine erythroleukemia cell differentiation. Mol Cell. Biol. 8:884-892.
9. Cleveland, J. L., M. Dean, N. Rosenberg, J. Y. Wang, and U. R. Rapp. 1989. Tyrosine kinase oncogenes abrogate interleukin-3 dependence of murine myeloid cells through signaling pathways involving c-myc: conditional regulation of c-myc transcription by temperature-sensitive v-abl. Mol Cell. Biol. 9:5685-5695.
10. Danish, R., O. el-Awar, B. L. Weber, J. Langmore, L. A. Turka, J. J. Ryan, and M. F. Clarke. 1992. c-myb effects on kinetic events during MEL cell differentiation. Oncogene 7:901-907.
11. Dasgupta, P., and E. P. Reddy. 1989. Identification of alternatively spliced transcripts for human c-myb: molecular cloning and sequence analysis of human c-myb exon 9A sequences. Oncogene 4:1419-1423.
12. Dean, M., J. L. Cleveland, U. R. Rapp, and J. N. Ihle. 1987. Role of myc in the abrogation of IL-3 dependence of myeloid FDC-P1 cells. Oncogene Res. 1:279-296.
13. Dean, M., R. A. Levine, W. Ran, M. S. Kindy, G. E. Sonenshein, and J. Campisi. 1986. Regulation of c-myc transcription and mRNA abundance by serum growth factors and cell contact. J. Biol. Chem. 261:9161-9166.
14. Dexter, T. M., J. Garland, D. Scott, E. Scolnick, and D. Metcalf. 1980. Growth of factor-dependent hemopoietic precursor cell lines. J. Exp. Med. 152:1036-1047.
15. Dragovich, T., C. M. Rudin, and C. B. Thompson. 1998. Signal transduction pathways that regulate cell survival and cell death. Oncogene 17:3207-3213.
16. Dubendorff, J. W., L. J. Whittaker, J. T. Eltman, and J. S. Lipsick. 1992. Carboxy-terminal elements of c-Myb negatively regulate transcriptional activation in cis and in trans. Genes Dev. 6:2524-2535.
17. Dudek, H., and E. P. Reddy. 1989. Identification of two translational products for c-myb. Oncogene 4:1061-1066.
18. Dudek, H., R. V. Tantravahi, V. N. Rao, E. S. Reddy, and E. P. Reddy. 1992. Myb and Ets proteins cooperate in transcriptional activation of the mim-1 promoter. Proc. Natl. Acad. Sci. USA 89:1291-1295.
19. Favier, D., and T. J. Gonda. 1994. Detection of proteins that bind to the leucine zipper motif of c-Myb. Oncogene 9:305-311.
20. Fiskum, G., S. W. Craig, G. L. Decker, and A. L. Lehninger. 1980. The cytoskeleton of digitonin-treated rat hepatocytes. Proc. Natl. Acad. Sci. USA 77:3430-3434.
21. Frampton, J., T. Ramqvist, and T. Graf. 1996. v-Myb of E26 leukemia virus up-regulates bcl-2 and suppresses apoptosis in myeloid cells. Genes Dev. 10:2720-2731.
22. Gaozza, E., S. J. Baker, R. K. Vora, and E. P. Reddy. 1997. AATYK: a novel tyrosine kinase induced during growth arrest and apoptosis of myeloid cells. Oncogene 15:3127-3135.
23. Gonda, T. J., and D. Metcalf. 1984. Expression of myb, myc and fos protooncogenes during the differentiation of a murine myeloid leukaemia. Nature 310:249-251.
24. Greenberger, J. S., R. J. Eckner, M. Sakakeeny, P. Marks, D. Reid, G. Nabel, A. Hapel, J. N. Ihle, and K. C. Humphries. 1983. Interleukin 3-dependent hematopoietic progenitor cell lines. Fed. Proc. 42:2762-2771.
25. Gross, A., J. M. McDonnell, and S. J. Korsmeyer. 1999. BCL-2 family members and the mitochondria in apoptosis. Genes Dev. 13:1899-1911.
26. Ho, S. N., H. D. Hunt, R. M. Horton, J. K. Pullen, and L. R. Pease. 1989. Site-directed mutagenesis by overlap extension with the polymerase chain reaction. Gene. 77:51-59.
27. Ihle, J. N., and D. Askew. 1989. Origins and properties of hematopoietic growth factor-dependent cell lines. Int. J. Cell Cloning 7:68-91.
28. Kanei-Ishii, C., E. M. MacMillan, T. Nomura, A. Sarai, R. G. Ramsay, S. Aimoto, S. Ishii, and T. J. Gonda. 1992. Transactivation and transformation by Myb are negatively regulated by a leucine-zipper structure. Proc. Natl. Acad. Sci. USA 89:3088-3092.
29. Kluck, R. M., E. Bossy-Wetzel, D. R. Green, and D. D. Newmeyer. 1997. The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science. 275:1132-1136.
30. Kuehl, W. M., T. P. Bender, J. Stafford, D. McClinton, S. Segal, and E. Dmitrovsky. 1988. Expression and function of the c-myb oncogene during hematopoietic differentiation. Curr. Top. Microbiol. Immunol. 141:318-323.
31. Kumar, A., C. M. Lee, and E. P. Reddy. 2003. c-Myc is essential but not sufficient for c-Myb-mediated block of granulocytic differentiation. J. Biol. Chem. 278:11480-11488.
32. Landschulz, W. H., P. F. Johnson, and S. L. McKnight. 1988. The leucine zipper: a hypothetical structure common to a new class of DNA binding proteins. Science 240:1759-1764.
33. Lazebnik, Y. A., A. Takahashi, R. D. Moir, R. D. Goldman, G. G. Poirier, S. H. Kaufmann, and W. C. Earnshaw. 1995. Studies of the lamin proteinase reveal multiple parallel biochemical pathways during apoptotic execution. Proc. Natl. Acad. Sci. USA 92:9042-9046.
34. Leopold, L. H., S. K. Shore, T. A. Newkirk, R. M. Reddy, and E. P. Reddy. 1995. Multi-unit ribozyme-mediated cleavage of bcr-abl mRNA in myeloid leukemias. Blood 85:2162-2170.
35. Liu, X., C. N. Kim, J. Yang, R. Jemmerson, and X. Wang. 1996. Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell 86:147-157.
36. McClinton, D., J. Stafford, L. Brents, T. P. Bender, and W. M. Kuehl. 1990. Differentiation of mouse erythroleukemia cells is blocked by late up-regulation of a c-myb transgene. Mol Cell. Biol. 10:705-710.
37. Migliaccio, G., A. R. Migliaccio, V. Broudy, B. Kreider, G. Rovera, and J. W. Adamson. 1989. Selection of lineage-restricted cell lines immortalized at different stages of hematopoietic differentiation from the murine cell line 32 D. Prog. Clin. Biol. Res. 183-196.
38. Ness, S. A., A. Marknell, and T. Graf. 1989. The v-myb oncogene product binds to and activates the promyelocyte-specific mim-1 gene. Cell 59:1115-1125.
39. Nomura, T., N. Sakai, A. Sarai, T. Sudo, C. Kanei-Ishii, R. G. Ramsay, D. Favier, T. J. Gonda, and S. Ishii. 1993. Negative autoregulation of c-Myb activity by homodimer formation through the leucine zipper. J. Biol. Chem. 268:21914-21923.
40. Nordeen, S. K. 1988. Luciferase reporter gene vectors for analysis of promoters and enhancers. BioTechniques 6:454-458.
41. Oh, I. H., and E. P. Reddy. 1997. Murine A-myb gene encodes a transcription factor, which cooperates with Ets-2 and exhibits distinctive biochemical and biological activities from c-myb. J. Biol. Chem. 272:21432-21443.
42. Oh, I. H., and E. P. Reddy. 1999. The myb gene family in cell growth, differentiation and apoptosis. Oncogene 18:3017-3033.
43. Packham, G., and J. L. Cleveland. 1994. Ornithine decarboxylase is a mediator of c-Myc-induced apoptosis. Mol. Cell. Biol. 14:5741-5747.
44. Patel, G., B. Kreider, G. Rovera, and E. P. Reddy. 1993. v-myb blocks granulocyte colony-stimulating factor-induced myeloid cell differentiation but not proliferation. Mol. Cell. Biol. 13:2269-2276.
45. Patel, G., R. Tantravahi, I. H. Oh, and E. P. Reddy. 1996. Transcriptional activation potential of normal and tumor-associated myb isoforms does not correlate with their ability to block GCSF-induced terminal differentiation of murine myeloid precursor cells. Oncogene 13:1197-1208.
46. Prendergast, G. C. 1999. Mechanisms of apoptosis by c-Myc. Oncogene 18:2967-2987.
47. Ramsay, R. G., K. Ikeda, R. A. Rifkind, and P. A. Marks. 1986. Changes in gene expression associated with induced differentiation of erythroleukemia: protooncogenes, globin genes, and cell division. Proc. Natl. Acad. Sci. USA 83:6849-6853.
48. Rathmell, J. C., and C. B. Thompson. 1999. The central effectors of cell death in the immune system. Annu. Rev. Immunol. 17:781-828.
49. Rodriguez-Tarduchy, G., M. Collins, and A. Lopez-Rivas. 1990. Regulation of apoptosis in interleukin-3-dependent hemopoietic cells by interleukin-3 and calcium ionophores. EMBO J. 9:2997-3002.
50. Rosson, D., D. Dugan, and E. P. Reddy. 1987. Aberrant splicing events that are induced by proviral integration: implications for myb oncogene activation. Proc. Natl. Acad. Sci. USA 84:3171-3175.
51. Rovera, G., B. Kreider, N. Shirsat, D. Venturelli, G. Naso, and F. Mavilio. 1989. Alteration of the program of terminal differentiation caused by oncogenes in the hemopoietic progenitor cell line 32D C13 (G). Ann. N. Y. Acad. Sci. 567:154-164.
52. Sakura, H., C. Kanei-Ishii, T. Nagase, H. Nakagoshi, T. J. Gonda, and S. Ishii. 1989. Delineation of three functional domains of the transcriptional activator encoded by the c-myb protooncogene. Proc. Natl. Acad. Sci. USA 86:5758-5762.
53. 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 94:3296-3301.
54. Selvakumaran, M., H. K. Lin, R. T. Sjin, J. C. Reed, D. A. Liebermann, B. Hoffman. 1994. The novel primary response gene MyD118 and the protooncogenes myb, myc, and bcl-2 modulate transforming growth factor beta 1-induced apoptosis of myeloid leukemia cells. Mol Cell. Biol. 14:2352-2360.
55. Shen-Ong, G. L. 1987. Alternative internal splicing in c-myb RNAs occurs commonly in normal and tumor cells. EMBO J. 6:4035-4039.
56. Shimizu, T., C. X. Cao, R. G. Shao, and Y. Pommier. 1998. Lamin B phosphorylation by protein kinase calpha and proteolysis during apoptosis in human leukemia HL60 cells. J. Biol. Chem. 273:8669-8674.
57. t Hoen, P. A., B. S. Rosema, J. N. Commandeur, N. P. Vermeulen, M. Manoharan, T. J. van Berkel, E. A. Biessen, and M. K. Bösterbosch. 2002. Selection of effective antisense oligodeoxynucleotides with a green fluorescent protein-based assay. Discovery of selective and potent inhibitors of glutathione S-transferase Mu expression. Eur. J. Biochem. 269:2574-2583.
58. Tavner, F. J., R. Simpson, S. Tashiro, D. Favier, N. A. Jenkins, D. J. Gilbert, N. G. Copeland, E. M. Macmillan, J. Lutwyche, R. A. Keough, S. Ishii, and T. J. Gonda. 1998. Molecular cloning reveals that the p160 Myb-binding protein is a novel, predominantly nucleolar protein which may play a role in transactivation by Myb. Mol. Cell. Biol. 18:989-1002.
59. Taylor, D., P. Badiani, and K. Weston. 1996. A dominant interfering Myb mutant causes apoptosis in T cells. Genes Dev. 10:2732-2744.
60. Todokoro, K., R. J. Watson, H. Higo, H. Amanuma, S. Kuramochi, H. Yanagisawa, and Y. Ikawa. 1988. Down-regulation of c-myb gene expression is a prerequisite for erythropoietin-induced erythroid differentiation. Proc. Natl. Acad. Sci. USA 85:8900-8904.
61. 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.
62. Varadhachary, A. S., and P. Salgame. 1998. CD95 mediated T cell apoptosis and its relevance to immune deviation. Oncogene 17:3271-3276.
63. Westin, E. H., R. C. Gallo, S. K. Arya, A. Eva, L. M. Souza, M. A. Baluda, S. A. Aaronson, and F. Wong-Staal. 1982. Differential expression of the amv gene in human hematopoietic cells. Proc. Natl. Acad. Sci. USA 79:2194-2198.
64. Weston, K., and J. M. Bishop. 1989. Transcriptional activation by the v-myb oncogene and its cellular progenitor, c-myb. Cell 58:85-93.
65. Williams, G. T., C. A. Smith, E. Spooncer, T. M. Dexter, and D. R. Taylor. 1990. Haemopoietic colony stimulating factors promote cell survival by suppressing apoptosis. Nature 343:76-79.
66. Woo, C. H., L. Sopchak, and J. S. Lipsick. 1998. Overexpression of an alternatively spliced form of c-Myb results in increases in transactivation and transforms avian myelomonoblasts. J. Virol. 72:6813-6821.
67. Yang, J., X. Liu, K. Bhalla, C. N. Kim, A. M. Ibrado, J. Cai, T. I. Peng, D. P. Jones, and X. Wang. 1997. Prevention of apoptosis by Bcl-2: release of cytochrome c from mitochondria blocked. Science. 275:1129-1132.
68. Ymer, S., W. Q. Tucker, C. J. Sanderson, A. J. Hapel, H. D. Campbell, and I. G. Young. 1985. Constitutive synthesis of interleukin-3 by leukaemia cell line WEHI-3B is due to retroviral insertion near the gene. Nature 317:255-258.