Combined loss of PUMA and p21 accelerates c-MYC-driven lymphoma development considerably less than loss of one allele of p53

Oncogene

Volumn 35, Issue 29, 2016, Pages 3866-3871

  Valente, L J ^a,b,c   Grabow, S ^a,b   Vandenberg, C J ^a,b   Strasser, A ^a,b   Janic, A ^a,b  

^a WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; PROTEIN P21; PROTEIN P53; PUMA PROTEIN; APOPTOSIS REGULATORY PROTEIN; CDKN1A PROTEIN, MOUSE; CYCLIN DEPENDENT KINASE INHIBITOR 1A; MYC PROTEIN; MYC PROTEIN, MOUSE; PMAIP1 PROTEIN, MOUSE; PROTEIN BCL 2; PUMA PROTEIN, MOUSE; TUMOR SUPPRESSOR PROTEIN;

ALLELE; ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CARCINOGENESIS; CELL AGING; CELL CYCLE ARREST; CELL SELECTION; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; DNA DAMAGE; FEMALE; GENE OVEREXPRESSION; LATENT PERIOD; LYMPHOMA; MALE; MOUSE; NONHUMAN; ONCOGENE C MYC; PRE B LYMPHOCYTE; PRIORITY JOURNAL; PROTEIN DEPLETION; WESTERN BLOTTING; ANIMAL; B LYMPHOCYTE; CELL CULTURE; GENETICS; HETEROZYGOSITY LOSS; KAPLAN MEIER METHOD; KNOCKOUT MOUSE; METABOLISM; MUTATION; PATHOLOGY; TRANSGENIC MOUSE;

ANIMALS; APOPTOSIS REGULATORY PROTEINS; B-LYMPHOCYTES; BLOTTING, WESTERN; CELLS, CULTURED; CYCLIN-DEPENDENT KINASE INHIBITOR P21; KAPLAN-MEIER ESTIMATE; LOSS OF HETEROZYGOSITY; LYMPHOMA; MICE, KNOCKOUT; MICE, TRANSGENIC; MUTATION; PRECURSOR CELLS, B-LYMPHOID; PROTO-ONCOGENE PROTEINS C-BCL-2; PROTO-ONCOGENE PROTEINS C-MYC; TUMOR SUPPRESSOR PROTEIN P53; TUMOR SUPPRESSOR PROTEINS;

EID: 84949309449     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2015.457     Document Type: Article

References (46)

1. Lane DP. p53, guardian of the genome. Nature 1992; 358: 15-16.
2. Levine AJ. p53, the cellular gatekeeper for growth and division. Cell 1997; 88: 323-331.
3. Vogelstein B, Lane D, Levine AJ. Surfing the p53 network. Nature 2000; 408: 307-310.
4. Vousden KH, Lane DP. p53 in health and disease. Nat Rev Mol Cell Biol 2007; 8: 275-283.
5. Donehower LA, Harvey M, Slagle BL, McArthur MJ, Montgomery CAJ, Butel JS et al. Mice deficient for p53 are developmentally normal but are susceptible to spontaneous tumours. Nature 1992; 356: 215-221.
6. Jacks T, Remington L, Williams BO, Schmitt EM, Halachmi S, Bronson RT et al. Tumor spectrum analysis in p53-mutant mice. Curr Biol 1994; 4: 1-7.
7. Lowe SW, Sherr CJ. Tumor suppression by Ink4a-Arf: progress and puzzles. Curr Opin Genet Dev 2003; 13: 77-83.
8. Kamijo T, Weber JD, Zambetti G, Zindy F, Roussel MF, Sherr CJ. Functional and physical interactions of the ARF tumor suppressor with p53 and Mdm2. Proc Natl Acad Sci US A 1998; 95: 8292-8297.
9. Pomerantz J, Schreiber-Agus N, Liégeois NJ, Silverman A, Alland L, Chin L et al. The Ink4a tumor suppressor gene product, p19Arf, interacts with MDM2 and neutralizes MDM2's inhibition of p53. Cell 1998; 92: 713-723.
10. Zhang Y, Xiong Y, Yarbrough WG. ARF promotes MDM2 degradation and stabilizes p53: ARF-INK4a locus deletion impairs both the Rb and p53 tumor suppression pathways. Cell 1998; 92: 725-734.
11. Michalak EM, Jansen ES, Happo L, Cragg MS, Tai L, Smyth GK et al. Puma and to a lesser extent Noxa are suppressors of Myc-induced lymphomagenesis. Cell Death Differ 2009; 16: 684-696.
12. Garrison SP, Jeffers JR, Yang C, Nilsson JA, Hall MA, Rehg JE et al. Selection against PUMA gene expression in Myc-driven B-cell lymphomagenesis. Mol Cell Biol 2008; 28: 5391-5402.
13. Adams JM, Harris AW, Pinkert CA, Corcoran LM, Alexander WS, Cory S et al. The c-myc oncogene driven by immunoglobulin enhancers induces lymphoid malignancy in transgenic mice. Nature 1985; 318: 533-538.
14. Eischen CM, Weber JD, Roussel MF, Sherr CJ, Cleveland JL. Disruption of the ARF-Mdm2-p53 tumor suppressor pathway in Myc-induced lymphomagenesis. Genes Dev 1999; 13: 2658-2669.
15. Villunger A, Michalak EM, Coultas L, Mullauer F, Bock G, Ausserlechner MJ et al. p53-and drug-induced apoptotic responses mediated by BH3-only proteins puma and noxa. Science 2003; 302: 1036-1038.
16. Jeffers JR, Parganas E, Lee Y, Yang C, Wang J, Brennan J et al. Puma is an essential mediator of p53-dependent and-independent apoptotic pathways. Cancer Cell 2003; 4: 321-328.
17. Hanahan D, Weinberg RA. The hallmarks of cancer. Cell 2000; 100: 57-70.
18. Deng C, Zhang P, Harper JW, Elledge SJ, Leder P. Mice lacking p21CIP1/WAF1 undergo normal development, but are defective in G1 checkpoint control. Cell 1995; 82: 675-684.
19. Newbold A, Salmon JM, Martin BP, Stanley K, Johnstone RW. The role of p21(waf1/cip1) and p27(Kip1) in HDACi-mediated tumor cell death and cell cycle arrest in the Emu-myc model of B-cell lymphoma. Oncogene 2014; 33: 5415-5423.
20. Patino-Garcia A, Sotillo-Pineiro E, Sierrasesumaga-Ariznabarreta L. p21WAF1 mutation is not a predominant alteration in pediatric bone tumors. Pediatr Res 1998; 43: 393-395.
21. McKenzie KE, Siva A, Maier S, Runnebaum IB, Seshadri R, Sukumar S. Altered WAF1 genes do not play a role in abnormal cell cycle regulation in breast cancers lacking p53 mutations. Clin Cancer Res 1997; 3: 1669-1673.
22. Shiohara M, el-Deiry WS, Wada M, Nakamaki T, Takeuchi S, Yang R et al. Absence of WAF1 mutations in a variety of human malignancies. Blood 1994; 84: 3781-3784.
23. Jackson RJ, Adnane J, Coppola D, Cantor A, Sebti SM, Pledger WJ. Loss of the cell cycle inhibitors p21(Cip1) and p27(Kip1) enhances tumorigenesis in knockout mouse models. Oncogene 2002; 21: 8486-8497.
24. Topley GI, Okuyama R, Gonzales JG, Conti C, Dotto GP. p21(WAF1/Cip1) functions as a suppressor of malignant skin tumor formation and a determinant of keratinocyte stem-cell potential. Proc Natl Acad Sci USA 1999; 96: 9089-9094.
25. Adnane J, Jackson RJ, Nicosia SV, Cantor AB, Pledger WJ, Sebti SM. Loss of p21WAF1/CIP1 accelerates Ras oncogenesis in a transgenic/knockout mammary cancer model. Oncogene 2000; 19: 5338-5347.
26. Yang WC, Mathew J, Velcich A, Edelmann W, Kucherlapati R, Lipkin M et al. Targeted inactivation of the p21(WAF1/cip1) gene enhances Apc-initiated tumor formation and the tumor-promoting activity of a Western-style high-risk diet by altering cell maturation in the intestinal mucosal. Cancer Res 2001; 61: 565-569.
27. Wang YA, Elson A, Leder P. Loss of p21 increases sensitivity to ionizing radiation and delays the onset of lymphoma in atm-deficient mice. Proc Natl Acad Sci USA 1997; 94: 14590-14595.
28. Martin-Caballero J, Flores JM, Garcia-Palencia P, Serrano M. Tumor susceptibility of p21(Waf1/Cip1)-deficient mice. Cancer Res 2001; 61: 6234-6238.
29. Bearss DJ, Lee RJ, Troyer DA, Pestell RG, Windle JJ. Differential effects of p21 (WAF1/CIP1) deficiency on MMTV-ras and MMTV-myc mammary tumor properties. Cancer Res 2002; 62: 2077-2084.
30. Martins CP, Berns A. Loss of p27(Kip1) but not p21(Cip1) decreases survival and synergizes with MYC in murine lymphomagenesis. EMBO J 2002; 21: 3739-3748.
31. Barboza JA, Liu G, Ju Z, El-Naggar AK, Lozano G. p21 delays tumor onset by preservation of chromosomal stability. Proc Natl Acad Sci USA 2006; 103: 19842-19847.
32. Post SM, Quintas-Cardama A, Terzian T, Smith C, Eischen CM, Lozano G. p53-dependent senescence delays Emu-myc-induced B-cell lymphomagenesis. Oncogene 2010; 29: 1260-1269.
33. Valente LJ, Gray DH, Michalak EM, Pinon-Hofbauer J, Egle A, Scott CL et al. p53 efficiently suppresses tumor development in the complete absence of its cellcycle inhibitory and proapoptotic effectors p21, Puma, and Noxa. Cell Rep 2013; 3: 1339-1345.
34. Li T, Kon N, Jiang L, Tan M, Ludwig T, Zhao Y et al. Tumor suppression in the absence of p53-mediated cell-cycle arrest, apoptosis, and senescence. Cell 2012; 149: 1269-1283.
35. Aubrey BJ, Kelly GL, Kueh AJ, Brennan MS, O'Connor L, Milla L et al. An inducible lentiviral guide rna platform enables the identification of tumor-essential genes and tumor-promoting mutations in vivo. Cell Rep 2015; 10: 1422-1432.
36. Harris AW, Pinkert CA, Crawford M, Langdon WY, Brinster RL, Adams JM. The E?-myc transgenic mouse: a model for high-incidence spontaneous lymphoma and leukemia of early B cells. J Exp Med 1988; 167: 353-371.
37. Langdon WY, Harris AW, Cory S, Adams JM. The c-myc oncogene perturbs B lymphocyte development in E?-myc transgenic mice. Cell 1986; 47: 11-18.
38. Strasser A, Elefanty AG, Harris AW, Cory S. Progenitor tumours from Em-bcl-2-myc transgenic mice have lymphomyeloid differentiation potential and reveal developmental differences in cell survival. EMBO J 1996; 15: 3823-3834.
39. Strasser A, Harris AW, Bath ML, Cory S. Novel primitive lymphoid tumours induced in transgenic mice by cooperation between myc and bcl-2. Nature 1990; 348: 331-333.
40. Nakano K, Vousden KH. PUMA, a novel proapoptotic gene, is induced by p53. Mol Cell 2001; 7: 683-694.
41. Jiang D, Brady CA, Johnson TM, Lee EY, Park EJ, Scott MP et al. Full p53 transcriptional activation potential is dispensable for tumor suppression in diverse lineages. Proc Natl Acad Sci USA 2011; 108: 17123-17128.
42. Hoffman B, Liebermann DA. Apoptotic signaling by c-MYC. Oncogene 2008; 27: 6462-6472.
43. Bieging KT, Attardi LD. Deconstructing p53 transcriptional networks in tumor suppression. Trends Cell Biol 2012; 22: 97-106.
44. Riley T, Sontag E, Chen P, Levine A. Transcriptional control of human p53-regulated genes. Nat Rev Mol Cell Biol 2008; 9: 402-412.
45. Brady CA, Jiang D, Mello SS, Johnson TM, Jarvis LA, Kozak MM et al. Distinct p53 transcriptional programs dictate acute DNA-damage responses and tumor suppression. Cell 2011; 145: 571-583.
46. Brugarolas J, Chandrasekaran C, Gordon JI, Beach D, Jacks T, Hannon GJ. Radiation-induced cell cycle arrest compromised by p21 deficiency. Nature 1995; 377: 552-557.