Disruption of the ARF-Mdm2-p53 tumor suppressor pathway in Myc-induced lymphomagenesis

Genes and Development

Volumn 13, Issue 20, 1999, Pages 2658-2669

  Eischen, Christine M ^a   Weber, Jason D ^a   Roussel, Martine F ^a,b   Sherr, Charles J ^a,b   Cleveland, John L ^a,b  

^a ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^b UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

Apoptosis; ARF; B cell lymphoma; Mdm2; Myc; P53

Indexed keywords

MYC PROTEIN; PROTEIN MDM2; PROTEIN P19; PROTEIN P53; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; B CELL LYMPHOMA; CANCER INHIBITION; CONTROLLED STUDY; EMBRYO; FIBROBLAST; GENE DISRUPTION; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; LYMPHOMA; MOUSE; NONHUMAN; ONCOGENE C MYC; PRIORITY JOURNAL;

ANIMALS; APOPTOSIS; B-LYMPHOCYTES; CELLS, CULTURED; ENHANCER ELEMENTS (GENETICS); FEMALE; GENES, MYC; GENES, P53; HEMATOPOIETIC STEM CELLS; IMMUNOGLOBULIN HEAVY CHAINS; LYMPHOMA, B-CELL; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MUTATION; NUCLEAR PROTEINS; PROTEINS; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-MDM2; TUMOR SUPPRESSOR PROTEIN P14ARF;

EID: 0033569422     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.13.20.2658     Document Type: Article

References (79)

1. Adams, J.M. and S. Cory. 1992. Oncogene cooperation in leukaemogenesis. Cancer Surveys 15: 119-141.
2. 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.
3. 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.
4. Alkema, M.J., H. Jacobs, M. van Lohuizen, and A. Berns. 1997. Perturbation of B and T cell development and predisposition to lymphomagenesis in Eμ-bmi-1 transgenic mice require the Bmi-1 RING finger. Oncogene 15: 899-910.
5. Askew, D.S., R.A. Ashmun, B.C. Simmons, and J.L. Cleveland. 1991. Constitutive c-myc expression in an IL3-dependent myeloid cell line suppresses cell cycle arrest and accelerates apoptosis. Oncogene 6: 1915-1922.
6. Barak, Y., T. Juven, R. Haffner, and M. Oren. 1993. Mdm2 expression is induced by wild type p53 activity. EMBO J. 12: 461-468.
7. ARF links pRB and p53. Nature 395: 124-125.
8. Borzillo, G.V. and C.J. Sherr. 1989. Early pre-B-cell transformation induced by the v-fms oncogene in long-term mouse bone marrow cultures. Mol. Cell. Biol. 9: 3973-3981.
9. Chen, J., V. Marechal, and A.J. Levine. 1993. Mapping of the p53 and mdm-2 interaction domains. Mol. Cell. Biol. 13: 4107-4114.
10. ARF tumor suppressor. Genes & Dev. 12: 2434-2442.
11. 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.
12. Eilers, M., S. Schirm, and J.M. Bishop. 1991. The Myc protein activates transcription of the α-prothymosin gene. EMBO J. 10: 133-141.
13. Evan, G.I., A.H. Wyllie, C.S. Gilbert, T.D. Littlewood, H. Land, M. Brooks, C.M. Water, L.Z. Penn, and D.C. Hancock. 1992. Induction of apoptosis in fibroblasts by c-myc protein. Cell 69: 119-128.
14. Evan, G.I., L. Brown, M. Whyte, and E. Harrington. 1995. Apoptosis and the cell cycle. Curr. Opin. Cell. Biol. 7: 825-834.
15. Fakharzadeh, S.S., S.P. Trusko, and D.L. George. 1991. Tumorigenic potential associated with enhanced expression of a gene that is amplified in a mouse tumor cell line. EMBO J. 10: 1565-1569.
16. Frazier, M.W., X. He, J. Wang, Z. Gu, J.L. Cleveland, and G.P. Zambetti. 1998. Activation of c-myc gene expression by tumor-derived p53 mutants requires a discrete C-terminal domain. Mol. Cell. Biol. 18: 3735-3743.
17. Fukusawa, K., T. Choi, R. Kuriyama, S. Rulong, and G.F. Vande Woude. 1996. Abnormal centrosome amplification in the absence of p53. Science 271: 1744-1747.
18. Giaccia, A.J. and M.B. Kastan. 1998. The complexity of p53 modulation: Emerging patterns from divergent signals. Genes & Dev. 12: 2973-2983.
19. Grossman, S.R., Perez, A.L. Kung, M. Joseph, C. Mansur, Z.X. Xiao, S. Kumar, P.M. Howley, and D.M. Livingston. 1998. p300/MDM2 complexes participate in MDM2-mediated p53 degradation. Mol. Cell 2: 405-415.
20. Harvey, D.M. and A.J. Levine. 1991. p53 alteration is a common event in the spontaneous immortalization of primary BALB/c murine embryo fibroblasts. Genes & Dev. 5: 2375-2385.
21. Harvey, M., M.J. McArthur, C.A. Montgomery Jr., J.A. Butel, A. Bradley, and L.A. Donehower. 1993a. Spontaneous and carcinogen-induced tumorigenesis in p53-deficient mice. Nat. Genet. 5: 225-229.
22. Harvey, M., A.T. Sands, R.S. Weiss, M.E. Hegi, R.W. Wiseman, P. Pantazis, B.C. Giovanella, M.A. Tainsky, A. Bradley, and L.A. Donehower. 1993b. In vitro growth characteristics of embryo fibroblasts isolated from p53-deficient mice. Oncogene 8: 2457-2467.
23. Haupt, Y., W.S. Alexander, G. Barri, S.P. Klinken, and J.M. Adams. 1991. Novel zinc finger gene implicated as myc collaborator by retovirally accelerated lymphomagenesis in Eμ-myc transgenic mice. Cell 65: 753-763.
24. Haupt, Y., R. Maya, A. Kazaz, and M. Oren. 1997. Mdm2 promotes the rapid degradation of p53. Nature 387: 296-299.
25. 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.
26. ARF with Mdm2 inhibits ubiquitin ligase activity of MDM2 for tumor suppressor p53. EMBO J. 18: 22-27.
27. Honda, R., H. Tanaka, and H. Yasuda. 1997. Oncoprotein MDM2 is a ubiquitin ligase E3 for tumor suppressor p53. FEBS Lett. 420: 25-27.
28. Hsieh, J.-K., F.S.G. Chan, D.J. O'Connor, S. Mittnacht, S. Zhong, and X. Lu. 1999. RB regulates the stability of the apoptotic function of p53 via MDM2. Mol. Cell 3: 181-193.
29. 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.
30. Jacks, T., L. Remington, B.O. Williams, E.M. Schmitt, S. Halachmi, R.T. Bronson, and R.A. Weinberg. 1994. Tumor spectrum analysis in p53-mutant mice. Curr. Biol. 4: 1-7.
31. Jacobs, J.J.L., K. Kieboom, S. Marino, R.A. DePinho, and M. van Lohuizen. 1999. The oncogene and Polycomb-group gene bmi-1 regulates cell proliferation and senescence through the ink4a locus. Nature 397: 164-168.
32. Jacobs, J.J.L., 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. (This issue).
33. 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 Eμ-myc transgenic mice. Blood 84: 2784-2794.
34. Jonkers, J. and A. Berns. 1996. Retroviral insertional mutagenesis as a strategy to identify cancer genes. Biochim. Biophys. Acta 1287: 29-57.
35. 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.
36. ARF. Cell 91: 649-659.
37. Kamijo, T., J.D. Weber, G. Zambetti, F. Zindy, M.F. Roussel, and C.J. Sherr. 1998. Functional and physical interactions of the ARF tumor suppressor with p53 and Mdm2. Proc. Natl. Acad. Sci. 95: 8292-8297.
38. Kamijo, T., S. Bodner, E. van de Kamp, D.H. Randle, and C.J. Sherr. 1999a. Tumor spectrum in ARF-deficient mice. Cancer Res. 59: 2217-2222.
39. Kamijo, T., E. van de Kamp, M.J. Chong, F. Zindy, A.J. Diehl, C.J. Sherr, and P. McKinnon. 1999b. Loss of the ARF tumor suppressor reverses premature replicative arrest but not radiation hypersensitivity arising from disabled Atm function. Cancer Res. 59: 2464-2469.
40. Ko, L.J. and C. Prives. 1996. p53: Puzzle and paradigm. Genes & Dev. 10: 1054-1072.
41. Kubbutat, M.H., S.N. Jones, and K.H. Vousden. 1997. Regulation of p53 stability by Mdm2. Nature 387: 299-303.
42. Levine, A.J. 1997. p53, the cellular gatekeeper for growth and division. Cell 88: 323-331.
43. Levy, N., E. Yonish-Rouach, M. Oren, and A. Kimchi. 1993. Complementation by wild-type p53 of interleukin-6 effects on M1 cells: Induction of cell cycle exit and cooperativity with c-myc suppression. Mol. Cell. Biol. 13: 7942-7952.
44. Littlewood, T.D., D.C. Hancock, P.S. Danielian, M.G. Parker, and G.I. Evan. 1995. A modified estrogen receptor ligand-binding domain as an improved switch for the regulation of heterologous proteins. Nucleic Acids Res. 23: 1686-1690.
45. Lundgren, K., R. Montes de Oca Luna, Y.B. McNeill, E.P. Emerick, B. Spencer, C.R. Barfield, G. Lozano, M.P. Rosenberg, and C.A. Finlay. 1997. Targeted expression of MDM2 uncouples S phase from mitosis and inhibits mammary gland development independent of p53. Genes & Dev. 11: 714-725.
46. Martin, K., D. Trouche, C. Hagemeier, T.S. Sorensen, N.B. LaThangue, and T. Kouzarides. 1995. Stimulation of E2F1/ DP1 transcriptional activity by mdm2 oncoprotein. Nature 375: 691-694.
47. 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.
48. McMasters, K.M., R. Montes de Oca Luna, J.R. Pena, and G. Lozano. 1996. Mdm2 deletion does not alter growth characteristics of p53-deficient embryo fibroblasts. Oncogene 13: 1731-1736.
49. 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.
50. Oliner, J.D., J.A. Pietenpol, S. Thiagalingam, J. Gyuris, K.W. Kinzler, and B. Vogelstein. 1993. Oncoprotein MDM2 conceals the activation domain of tumour suppressor p53. Nature 362: 857-860.
51. Olson, D.C., V. Marechal, J. Momand, J. Chen, C. Romocki, and A.J. Levine. 1993. Identification and characterization of multiple mdm-2 protein and mdm-2-p53 protein complexes. Oncogene 8: 2353-2360.
52. Packham, G. and J.L. Cleveland. 1995. c-Myc and apoptosis. Biochim. Biophys. Acta Rev. Cancer 1242: 11-29.
53. ARF links the tumour suppressor p53 to ras. Nature 395: 125-126.
54. ARF, interacts with MDM2 and neutralizes MDM2's inhibition of p53. Cell 92: 713-723.
55. Prives, C. 1998. Signaling to p53: Breaking the MDM2-p53 circuit. Cell 95: 5-8.
56. INK4b genes. Oncogene 11: 635-645.
57. Quelle, D.E., F. Zindy, R.A. Ashmun, and C.J. Sherr. 1995b. Alternative reading frames of the INK4a tumor suppressor gene encode two unrelated proteins capable of inducing cell cycle arrest. Cell 83: 993-1000.
58. ARF induces p53-dependent apoptosis during Abelson virus-mediated pre-B cell transformation. Proc. Natl. Acad. Sci. 95: 13194-13199.
59. Roth, J., M. Dobbelstein, D. Freedman, T. Shenk, and A.J. Levine. 1998. Nucleocytoplasmic 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.
60. Roussel, M.F., A.M. Theodoras, M. Pagano, and C.J. Sherr. 1995. Rescue of defective mitogenic signaling by D-type cyclins. Proc. Natl. Acad. Sci. 92: 6837-6841.
61. Sakamuro, D., V. Eviner, K.J. Elliott, L. Showe, E. White, and G.C. Prendergast. 1995. c-Myc induces apoptosis in epithelial cells by both p53-dependent and p53-independent mechanisms. Oncogene 11: 2411-2418.
62. Schmitt, C.A., M.E. McCurrach, E. de Stanchina, and S.W. Lowe. 1999. Impact of Ink4a/ARF and p53 mutations during lymphoma development and therapy. Genes & Dev. (This issue).
63. Serrano, M., G.J. Hannon, and D. Beach. 1993. A new regulatory motif in cell cycle control causing specific inhibition of cyclin D/CDK4. Nature 366: 704-707.
64. Sherr, C.J. 1998. Tumor surveillance via the ARF-p53 pathway. Genes & Dev. 12: 2984-2991.
65. Sidman, C.L., J.D. Marshall, and A.W. Harris. 1988. Genetic studies on Eμ-myc transgenic mice. Curr. Top Microbiol. Immunol. 141: 94-99.
66. ARF, participates in a regulatory feedback loop with p53 and MDM2. EMBO J. 17: 5001-5014.
67. 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.
68. ARF stabilizes p53 by blocking nucleo-cytoplasmic shuttling of Mdm2. Proc. Natl. Acad. Sci. 96: 6937-6941.
69. Van Lohuizen, M., S. Verbeek, B. Scheijen, E. Wientjens, H. Van der Gulden, and A. Berns. 1991. Identification of cooperating oncogenes in Eμ-myc transgenic mice by provirus tagging. Cell 65: 737-752.
70. Verbeek, S., M. van Lohuizen, M. van der Valk, J. Domen, G. Kraal, and A. Berns. 1991. Mice bearing the Eμ-myc and Eμ-pim-1 transgenes develop pre-B-cell leukemia prenatally. Mol. Cell. Biol. 11: 1176-1179.
71. Weber, J.D., L.J. Taylor, M.F. Roussel, C.J. Sherr, and D. BarSagi. 1999. Nucleolar Arf sequesters Mdm2 and activates p53. Nat. Cell Biol. 1: 20-26.
72. Whitlock, C.A. and O.N. Witte. 1987. Long-term culture of murine bone marrow precursors of B lymphocytes. Methods Enzymol. 150: 275-286.
73. Wu, X., J.H. Bayle, D. Olson, and A.J. Levine. 1993. The p53-mdm-2 autoregulatory feedback loop. Genes & Dev. 7: 1126-1132.
74. Xiao, Z.X., J. Chen, A. Levine, N. Modjtahedi, J. Xing, W.R. Sellers, and D.M. Livingston. 1995. Interactions between the retinoblastoma protein and the oncoprotein mdm2. Nature 375: 694-697.
75. Zeng, X., L. Chen, C.A. Jost, R. Maya, D. Keller, X. Wang, W.G. Kaelin Jr., M. Oren, J. Chen, and H. Lu. 1999. MDM2 suppresses p73 function without promoting p73 degradation. Mol. Cell. Biol. 19: 3257-3266.
76. Zhang, Y. and Y. Xiong. 1999. Mutations in human ARF exon 2 disrupt its nucleolar localization and impair its ability to block nuclear export of MDM2 and p53. Mol. Cell 3: 579-591.
77. Zhang, Y., Y. Xiong, and W.G. Yarbrough. 1998. ARF promotes MDM2 degradation and stabilizes p53: ARF-INK4a locus deletion impairs both the Rb and p53 tumor suppressor pathways. Cell 92: 725-734.
78. INK4a tumor suppressor versus other INK4 family members during mouse development and aging. Oncogene 15: 203-211.
79. Zindy, F., C.M. Eischen, D. 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.