Apoptosis Triggered by Myc-Induced Suppression of Bcl-X_L or Bcl-2 Is Bypassed during Lymphomagenesis

REFERENCES

• Adams, J. M., A. W. Harris, C. A. Pinkert, L. M. Corcoran, W. S. Alexander, S. Cory, R. D. Palmiter, and R. L. Brinster. 1985. The c-myc oncogene driven by immunoglobulin enhancers induces lymphoid malignancy in transgenic mice. Nature 318:533–538.
   PubMed Web of Science ®Google Scholar
• Akashi, K., M. Kondo, U. von Freeden-Jeffry, R. Murray, and I. L. Weissman. 1997. Bcl-2 rescues T lymphopoiesis in interleukin-7 receptor-deficient mice. Cell 89:1033–1041.
   PubMed Web of Science ®Google Scholar
• Alitalo, K., P. Koskinen, T. P. Makela, K. Saksela, L. Sistonen, and R. Winqvist. 1987. myc oncogenes: activation and amplification. Biochim. Biophys. Acta 907:1–32.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Attardi, L. D., and T. Jacks. 1999. The role of p53 in tumour suppression: lessons from mouse models. Cell. Mol. Life Sci. 55:48–63.
   PubMed Web of Science ®Google Scholar
• Bissonnette, R. P., F. Echeverri, A. Mahboubi, and D. R. Green. 1992. Apoptotic cell death induced by c-myc is inhibited by bcl-2. Nature 359:552–554.
   PubMed Web of Science ®Google Scholar
• Capoulade, C., B. Bressac-de Paillerets, I. Lefrere, M. Ronsin, J. Feunteun, T. Tursz, and J. Wiels. 1998. Overexpression of MDM2, due to enhanced translation, results in inactivation of wild-type p53 in Burkitt's lymphoma cells. Oncogene 16:1603–1610.
   PubMed Web of Science ®Google Scholar
• Conzen, S. D., K. Gottlob, E. S. Kandel, P. Khanduri, A. J. Wagner, M. O'Leary, and N. Hay. 2000. Induction of cell cycle progression and acceleration of apoptosis are two separable functions of c-Myc: transrepression correlates with acceleration of apoptosis. Mol. Cell. Biol. 20:6008–6018.
   PubMedGoogle Scholar
• Donehower, L. A., M. Harvey, B. L. Slagle, M. J. McArthur, C. A. Montgomery Jr., J. S. Butel, and A. Bradley. 1992. Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumours. Nature 356:215–221.
   PubMed Web of Science ®Google Scholar
• Eilers, M., S. Schirm, and J. M. Bishop. 1991. The MYC protein activates transcription of the alpha-prothymosin gene. EMBO J. 10:133–141.
   PubMed Web of Science ®Google Scholar
• Eischen, C. M., J. D. Weber, M. F. Roussel, C. J. Sherr, and J. L. Cleveland. 1999. Disruption of the ARF-Mdm2–p53 tumor suppressor pathway in Myc-induced lymphomagenesis. Genes Dev. 13:2658–2669.
   PubMed Web of Science ®Google Scholar
• Evan, G. I., A. H. Wyllie, C. S. Gilbert, T. D. Littlewood, H. Land, M. Brooks, C. M. Waters, L. Z. Penn, and D. C. Hancock. 1992. Induction of apoptosis in fibroblasts by c-myc protein. Cell 69:119–128.
   PubMed Web of Science ®Google Scholar
• Fanidi, A., E. A. Harrington, and G. I. Evan. 1992. Cooperative interaction between c-myc and bcl-2 proto-oncogenes. Nature 359:554–556.
   PubMed Web of Science ®Google Scholar
• Finke, J., R. Fritzen, P. Ternes, P. Trivedi, K. J. Bross, W. Lange, R. Mertelsmann, and G. Dolken. 1992. Expression of bcl-2 in Burkitt's lymphoma cell lines: induction by latent Epstein-Barr virus genes. Blood 80:459–469.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Grillot, D. A., R. Merino, J. C. Pena, W. C. Fanslow, F. D. Finkelman, C. B. Thompson, and G. Nune. 1996. Bcl-x exhibits regulated expression during B cell development and activation and modulates lymphocyte survival in transgenic mice. J. Exp. Med. 183:381–391.
   PubMed Web of Science ®Google Scholar
• Gross, A., J. M. McDonnell, and S. J. Korsmeyer. 1999. BCL-2 family members and the mitochondria in apoptosis. Genes Dev. 13:1899–1911.
   PubMed Web of Science ®Google Scholar
• Hainaut, P., T. Soussi, B. Shomer, M. Hollstein, M. Greenblatt, E. Hovig, C. C. Harris, and R. Montesano. 1997. Database of p53 gene somatic mutations in human tumors and cell lines: updated compilation and future prospects. Nucleic Acids Res. 25:151–157.
   PubMed Web of Science ®Google Scholar
• Harrington, E. A., M. R. Bennett, A. Fanidi, and G. I. Evan. 1994. c-Myc-induced apoptosis in fibroblasts is inhibited by specific cytokines. EMBO J. 13:3286–3295.
   PubMed Web of Science ®Google Scholar
• Harris, A. W., C. A. Pinkert, M. Crawford, W. Y. Langdon, R. L. Brinster, and J. M. Adams. 1988. The E mu-myc transgenic mouse. A model for high-incidence spontaneous lymphoma and leukemia of early B cells. J. Exp. Med. 167:353–371.
   PubMedGoogle Scholar
• Honda, R., H. Tanaka, and H. Yasuda. 1997. Oncoprotein MDM2 is a ubiquitin ligase E3 for tumor suppressor p53. FEBS Lett. 420:25–27.
   PubMed Web of Science ®Google Scholar
• Honda, R., and H. Yasuda. 1999. Association of p19(ARF) with Mdm2 inhibits ubiquitin ligase activity of Mdm2 for tumor suppressor p53. EMBO J. 18:22–27.
   PubMed Web of Science ®Google Scholar
• Hsu, B., M. C. Marin, A. K. el-Naggar, L. C. Stephens, S. Brisbay, and T. J. McDonnell. 1995. Evidence that c-myc mediated apoptosis does not require wild-type p53 during lymphomagenesis. Oncogene 11:175–179.
   PubMedGoogle Scholar
• Hueber, A. O., and G. I. Evan. 1998. Traps to catch unwary oncogenes. Trends Genet. 14:364–367.
   PubMedGoogle Scholar
• Jacobs, J. J., B. Scheijen, J. W. Voncken, K. Kieboom, A. Berns, and M. van Lohuizen. 1999. Bmi-1 collaborates with c-Myc in tumorigenesis by inhibiting c-Myc-induced apoptosis via INK4a/ARF. Genes Dev. 13:2678–2690.
   PubMed Web of Science ®Google Scholar
• Jacobsen, K. A., V. S. Prasad, C. L. Sidman, and D. G. Osmond. 1994. Apoptosis and macrophage-mediated deletion of precursor B cells in the bone marrow of E mu-myc transgenic mice. Blood 84:2784–2794.
   PubMedGoogle Scholar
• Juin, P., A. O. Hueber, T. Littlewood, and G. Evan. 1999. c-Myc-induced sensitization to apoptosis is mediated through cytochrome c release. Genes Dev. 13:1367–1381.
   PubMed Web of Science ®Google Scholar
• Kamijo, T., F. Zindy, M. F. Roussel, D. E. Quelle, J. R. Downing, R. A. Ashmun, G. Grosveld, and C. J. Sherr. 1997. Tumor suppression at the mouse INK4a locus mediated by the alternative reading frame product p19ARF. Cell 91:649–659.
   PubMed Web of Science ®Google Scholar
• Kataoka, M., S. Wiehle, F. Spitz, G. Schumacher, J. A. Roth, and R. J. Cristiano. 2000. Down-regulation of bcl-2 is associated with p16INK4-mediated apoptosis in non-small cell lung cancer cells. Oncogene 19:1589–1595.
   PubMedGoogle Scholar
• Kinoshita, T., T. Yokota, K. Arai, and A. Miyajima. 1995. Regulation of Bcl-2 expression by oncogenic Ras protein in hematopoietic cells. Oncogene 10:2207–2212.
   PubMed Web of Science ®Google Scholar
• Klangby, U., I. Okan, K. P. Magnusson, M. Wendland, P. Lind, and K. G. Wiman. 1998. p16/INK4a and p15/INK4b gene methylation and absence of p16/INK4a mRNA and protein expression in Burkitt's lymphoma. Blood 91:1680–1687.
   PubMed Web of Science ®Google Scholar
• Kondo, M., K. Akashi, J. Domen, K. Sugamura, and I. L. Weissman. 1997. Bcl-2 rescues T lymphopoiesis, but not B or NK cell development, in common gamma chain-deficient mice. Immunity 7:155–162.
   PubMed Web of Science ®Google Scholar
• Korsmeyer, S. J.. 1999. BCL-2 gene family and the regulation of programmed cell death. Cancer Res. 59 (Suppl.):1693s–1700s.
   PubMedGoogle Scholar
• Lagasse, E., and I. L. Weissman. 1997. Enforced expression of Bcl-2 in monocytes rescues macrophages and partially reverses osteopetrosis in op/op mice. Cell 89:1021–1031.
   PubMed Web of Science ®Google Scholar
• Lilly, M., J. Sandholm, J. J. Cooper, P. J. Koskinen, and A. Kraft. 1999. The PIM-1 serine kinase prolongs survival and inhibits apoptosis-related mitochondrial dysfunction in part through a bcl-2-dependent pathway. Oncogene 18:4022–4031.
   PubMed Web of Science ®Google Scholar
• Littlewood, T. D., D. C. Hancock, P. S. Danielian, M. G. Parker, and G. I. Evan. 1995. A modified oestrogen receptor ligand-binding domain as an improved switch for the regulation of heterologous proteins. Nucleic Acids Res. 23:1686–1690.
   PubMed Web of Science ®Google Scholar
• Mateyak, M. K., A. J. Obaya, S. Adachi, and J. M. Sedivy. 1997. Phenotypes of c-Myc-deficient rat fibroblasts isolated by targeted homologous recombination. Cell Growth Differ. 8:1039–1048.
   PubMedGoogle Scholar
• McDonnell, T. J., and S. J. Korsmeyer. 1991. Progression from lymphoid hyperplasia to high-grade malignant lymphoma in mice transgenic for the t(14; 18). Nature 349:254–256.
   PubMed Web of Science ®Google Scholar
• Meijerink, J. P., E. J. Mensink, K. Wang, T. W. Sedlak, A. W. Sloetjes, T. de Witte, G. Waksman, and S. J. Korsmeyer. 1998. Hematopoietic malignancies demonstrate loss-of-function mutations of BAX. Blood 91:2991–2997.
   PubMed Web of Science ®Google Scholar
• Merino, R., L. Ding, D. J. Veis, S. J. Korsmeyer, and G. Nune. 1994. Developmental regulation of the Bcl-2 protein and susceptibility to cell death in B lymphocytes. EMBO J. 13:683–691.
   PubMed Web of Science ®Google Scholar
• Minn, A. J., L. H. Boise, and C. B. Thompson. 1996. Expression of Bcl-xL and loss of p53 can cooperate to overcome a cell cycle checkpoint induced by mitotic spindle damage. Genes Dev. 10:2621–2631.
   PubMed Web of Science ®Google Scholar
• Miyashita, T., S. Krajewski, M. Krajewska, H. G. Wang, H. K. Lin, D. A. Liebermann, B. Hoffman, and J. C. Reed. 1994. Tumor suppressor p53 is a regulator of bcl-2 and bax gene expression in vitro and in vivo. Oncogene 9:1799–1805.
   PubMed Web of Science ®Google Scholar
• Momand, J., G. P. Zambetti, D. C. Olson, D. George, and A. J. Levine. 1992. The mdm-2 oncogene product forms a complex with the p53 protein and inhibits p53-mediated transactivation. Cell 69:1237–1245.
   PubMed Web of Science ®Google Scholar
• Motoyama, N., F. Wang, K. A. Roth, H. Sawa, K. I. Nakayama, K. Nakayama, I. Negishi, S. Senju, Q. Zhang, S. Fujii, and D. Y. Loh. 1995. Massive cell death of immature hematopoietic cells and neurons in Bcl-x-deficient mice. Science 267:1506–1510.
   PubMed Web of Science ®Google Scholar
• Nakayama, K., I. Negishi, K. Kuida, H. Sawa, and D. Y. Loh. 1994. Targeted disruption of Bcl-2 alpha beta in mice: occurrence of gray hair, polycystic kidney disease, and lymphocytopenia. Proc. Natl. Acad. Sci. USA 91:3700–3704.
   PubMed Web of Science ®Google Scholar
• Newcomb, E. W.. 1995. P53 gene mutations in lymphoid diseases and their possible relevance to drug resistance. Leukoc. Lymphoma 17:211–221.
   PubMed Web of Science ®Google Scholar
• Packham, G., and J. L. Cleveland. 1995. c-Myc and apoptosis. Biochim. Biophys. Acta 1242:11–28.
   PubMed Web of Science ®Google Scholar
• Packham, G., E. L. White, C. M. Eischen, H. Yang, E. Parganas, J. N. Ihle, D. A. Grillot, G. P. Zambetti, G. Nunez, and J. L. Cleveland. 1998. Selective regulation of Bcl-XL by a Jak kinase-dependent pathway is bypassed in murine hematopoietic malignancies. Genes Dev. 12:2475–2487.
   PubMed Web of Science ®Google Scholar
• Quelle, D. E., F. Zindy, R. A. Ashmun, and C. J. Sherr. 1995. Alternative reading frames of the INK4a tumor suppressor gene encode two unrelated proteins capable of inducing cell cycle arrest. Cell 83:993–1000.
   PubMed Web of Science ®Google Scholar
• Rampino, N., H. Yamamoto, Y. Ionov, Y. Li, H. Sawai, J. C. Reed, and M. Perucho. 1997. Somatic frameshift mutations in the BAX gene in colon cancers of the microsatellite mutator phenotype. Science 275:967–969.
   PubMed Web of Science ®Google Scholar
• Reed, J. C., T. Miyashita, S. Takayama, H. G. Wang, T. Sato, S. Krajewski, C. Aime-Sempe, S. Bodrug, S. Kitada, and M. Hanada. 1996. BCL-2 family proteins: regulators of cell death involved in the pathogenesis of cancer and resistance to therapy. J. Cell. Biochem. 60:23–32.
   PubMed Web of Science ®Google Scholar
• Roth, J., M. Dobbelstein, D. A. Freedman, T. Shenk, and A. J. Levine. 1998. Nucleo-cytoplasmic shuttling of the hdm2 oncoprotein regulates the levels of the p53 protein via a pathway used by the human immunodeficiency virus rev protein. EMBO J. 17:554–564.
   PubMed Web of Science ®Google Scholar
• Sanchez-Garcia, I., and G. Grut. 1995. Tumorigenic activity of the BCR-ABL oncogenes is mediated by BCL2. Proc. Natl. Acad. Sci. USA 92:5287–5291.
   PubMed Web of Science ®Google Scholar
• Santoni-Rugiu, E., J. Falck, N. Mailand, J. Bartek, and J. Lukas. 2000. Involvement of Myc activity in a G1/S-promoting mechanism parallel to the pRb/E2F pathway. Mol. Cell. Biol. 20:3497–3509.
   PubMed Web of Science ®Google Scholar
• Schmitt, C. A., M. E. McCurrach, E. de Stanchina, R. R. Wallace-Brodeur, and S. W. Lowe. 1999. INK4a/ARF mutations accelerate lymphomagenesis and promote chemoresistance by disabling p53. Genes Dev. 13:2670–2677.
   PubMed Web of Science ®Google Scholar
• Sherr, C. J., and J. D. Weber. 2000. The ARF/p53 pathway. Curr. Opin. Genet. Dev. 10:94–99.
   PubMed Web of Science ®Google Scholar
• Strasser, A., A. W. Harris, M. L. Bath, and S. Cory. 1990. Novel primitive lymphoid tumours induced in transgenic mice by cooperation between myc and bcl-2. Nature 348:331–333.
   PubMed Web of Science ®Google Scholar
• Strasser, A., A. W. Harris, and S. Cory. 1993. E mu-bcl-2 transgene facilitates spontaneous transformation of early pre-B and immunoglobulin-secreting cells but not T cells. Oncogene 8:1–9.
   PubMedGoogle Scholar
• Tao, W., and A. J. Levine. 1999. P19(ARF) stabilizes p53 by blocking nucleo-cytoplasmic shuttling of Mdm2. Proc. Natl. Acad. Sci. USA 96:6937–6941.
   PubMed Web of Science ®Google Scholar
• Taylor, D., P. Badiani, and K. Weston. 1996. A dominant interfering Myb mutant causes apoptosis in T cells. Genes Dev. 10:2732–2744.
   PubMed Web of Science ®Google Scholar
• Veis, D. J., C. M. Sorenson, J. R. Shutter, and S. J. Korsmeyer. 1993. Bcl-2-deficient mice demonstrate fulminant lymphoid apoptosis, polycystic kidneys, and hypopigmented hair. Cell 75:229–240.
   PubMed Web of Science ®Google Scholar
• Weber, J. D., L. J. Taylor, M. F. Roussel, C. J. Sherr, and D. Bar-Sagi. 1999. Nucleolar Arf sequesters Mdm2 and activates p53. Nat. Cell Biol. 1:20–26.
   PubMed Web of Science ®Google Scholar
• Weston, K.. 1999. Reassessing the role of C-MYB in tumorigenesis. Oncogene 18:3034–3038.
   PubMedGoogle Scholar
• Zindy, F., C. M. Eischen, D. H. Randle, T. Kamijo, J. L. Cleveland, C. J. Sherr, and M. F. Roussel. 1998. Myc signaling via the ARF tumor suppressor regulates p53-dependent apoptosis and immortalization. Genes Dev. 12:2424–2433.
   PubMed Web of Science ®Google Scholar