p53 status dictates responses of B lymphomas to monotherapy with proteasome inhibitors

Blood

Volumn 109, Issue 11, 2007, Pages 4936-4943

  Yu, Duonan ^a   Carroll, Martin ^b   Thomas Tikhonenko, Andrei ^a,c  

^a UNIVERSITY OF PENNSYLVANIA SCHOOL OF VETERINARY MEDICINE   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BORTEZOMIB; EPOXOMICIN; PROTEASOME INHIBITOR; PROTEIN MDM2; PROTEIN P53; TAMOXIFEN;

ALLELE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BURKITT LYMPHOMA; CONTROLLED STUDY; ENZYME INHIBITION; GENE FUSION; GENE OVEREXPRESSION; LYMPHOMA; MOUSE; NONHUMAN; ONCOGENE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN FUNCTION; TUMOR REGRESSION;

EID: 34249736408     PISSN: 00064971     EISSN: 00064971     Source Type: Journal    
DOI: 10.1182/blood-2006-10-050294     Document Type: Article

References (74)

1. Evan GI, Vousden KH. Proliferation, cell cycle and apoptosis in cancer. Nature. 2001;411:342-348.
2. Lowe SW, Cepero E, Evan G. Intrinsic tumour suppression. Nature. 2004;432:307-315.
3. Bullock AN, Fersht AR. Rescuing the function of mutant p53. Nat Rev Cancer. 2001;1:68-76.
4. Bower M. Acquired immunodeficiency syndrome-related systemic non-Hodgkin's lymphoma. Br J Hematol. 2001;112:863-873.
5. Carbone A. Emerging pathways in the development of AIDS-related lymphomas. Lancet Oncol. 2003;4:22-29.
6. Sanchez-Beato M, Sanchez-Aguilera A, Piris MA. Cell cycle deregulation in B-cell lymphomas. Blood. 2003;101:1220-1235.
7. Hudis CA, Schmitz N. Dose-dense chemotherapy in breast cancer and lymphoma. Semin. Oncol. 2004;31:19-26.
8. Wang W, Rastinejad F, El Deiry WS. Restoring p53-dependent tumor suppression. Cancer Biol Ther. 2003;2:41-49.
9. Freedman DA, Levine AJ. Nuclear export is required for degradation of endogenous p53 by MDM2 and human papillomavirus E6. Mol Cell Biol. 1998;18:7288-7293.
10. Roth J, Dobbelstein M, Freedman DA, Shenk T, Levine AJ. 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. 1998;17:554-564.
11. Tao W, Levine AJ. Nucleocytoplasmic shuttling of oncoprotein Hdm2 is required for Hdm2-mediated degradation of p53. Proc Natl Acad Sci U S A. 1999;96:3077-3080.
12. Geyer RK, Yu ZK, Maki CG. The MDM2 RING-finger domain is required to promote p53 nuclear export. Nat Cell Biol. 2000;2:569-573.
13. Momand J, Zambetti GP, Olson DC, George D, Levine AJ. The mdm-2 oncogene product forms a complex with the p53 protein and inhibits p53-mediated transactivation. Cell. 1992;69:1237-1245.
14. Oliner JD, Pietenpol JA, Thiagalingam S, et al. Oncoprotein MDM2 conceals the activation domain of tumour suppressor p53. Nature. 1993;362:857-860.
15. Haupt Y, Maya R, Kazaz A, Oren M. Mdm2 promotes the rapid degradation of p53. Nature. 1997;387:296-299.
16. Honda R, Tanaka H, Yasuda H. Oncoprotein MDM2 is a ubiquitin ligase E3 for tumor suppressor p53. FEBS Lett. 1997;420:25-27.
17. Kubbutat MH, Jones SN, Vousden KH. Regulation of p53 stability by Mdm2. Nature. 1997;387:299-303.
18. Grossman SR, Deato ME, Brignone C, et al. Polyubiquitination of p53 by a ubiquitin ligase activity of p300. Science. 2003;300:342-344.
19. Dornan D, Wertz I, Shimizu H, et al. The ubiquitin ligase COP1 is a critical negative regulator of p53. Nature. 2004;429:86-92.
20. Scheffner M, Werness BA, Huibregtse JM, Levine AJ, Howley PM. The E6 oncoprotein encoded by human papillomavirus types 16 and 18 promotes the degradation of p53. Cell. 1990;63:1129-1136.
21. Yang Y, Li CC, Weissman AM. Regulating the p53 system through ubiquitination. Oncogene. 2004;23:2096-2106.
22. Michael D, Oren M. The p53-Mdm2 module and the ubiquitin system. Semin Cancer Biol. 2003;13:49-58.
23. Capoulade C, Bressac-de Paillerets B, Lefrere I, et al. Overexpression of MDM2, due to enhanced translation, results in inactivation of wild-type p53 in Burkitt's lymphoma cells. Oncogene. 1998;16:1603-1610.
24. Pomerantz J, Schreiber-Agus N, Liegeois NJ, et al. The Ink4a tumor suppressor gene product, p19Arf, interacts with MDM2 and neutralizes MDM2's inhibition of p53. Cell. 1998;92:713-723.
25. 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.
26. Kamijo T, Weber JD, Zambetti G, et al. Functional and physical interactions of the ARF tumor suppressor with p53 and Mdm2. Proc Natl Acad Sci U S A. 1998; 95:8292-8297.
27. Stott FJ, Bates S, James MC, et al. The alternative product from the human CDKN2A locus, p14(ARF), participates in a regulatory feedback loop with p53 and MDM2. EMBO J. 1998;17:5001-5014.
28. Zindy F, Eischen CM, Randle DH, et al. Myc signaling via the ARF tumor suppressor regulates p53-dependent apoptosis and immortalization. Genes Dev. 1998;12:2424-2433.
29. 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.
30. Schmitt CA, McCurrach ME, de Stanchina E, Wallace-Brodeur RR, Lowe SW. INK4a/ARF mutations accelerate lymphomagenesis and promote chemoresistance by disabling p53. Genes Dev. 1999;13:2670-2677.
31. Wilda M, Bruch J, Harder L, et al. Inactivation of the ARF-MDM-2-p53 pathway in sporadic Burkitt's lymphoma in children. Leukemia. 2004;18:584-588.
32. Christophorou MA, Martin-Zanca D, Soucek L, et al. Temporal dissection of p53 function in vitro and in vivo. Nat Genet. 2005;37:718-726.
33. Christophorou MA, Ringshausen I, Finch AJ, Brown-Swigart L, Evan GI. The pathological response to DNA damage does not contribute to p53-mediated tumour suppression. Nature. 2006;443:214-217.
34. Martins CP, Brown-Swigart L, Evan GI. Modeling the therapeutic efficacy of p53 restoration in tumors. Cell. 2006;127:1323-1334.
35. Ringshausen I, O'Shea CC, Finch AJ, Swigart LB, Evan GI. Mdm2 is critically and continuously required to suppress lethal p53 activity in vivo. Cancer Cell. 2006;10:501-514.
36. Yu D, Thomas-Tikhonenko A. A non-transgenic mouse model for B-cell lymphoma: in vivo infection of p53-null bone marrow progenitors by a Myc retrovirus is sufficient for tumorigenesis. Oncogene. 2002;21:1922-1927.
37. Yu D, Allman D, Goldscmidt M, et al. Oscillation between B-lymphoid and myeloid lineages in Myc-induced hematopoietic tumors following spontaneous silencing/reactivation of the EBF/ Pax5 pathway. Blood. 2003;101:1950-1955.
38. Yu D, Dews M, Park A, Tobias JW, Thomas-Tikhonenko A. Inactivation of Myc in two-hit B-lymphomas causes dormancy with elevated levels of interleukin-10 receptor and CD20: implications for adjuvant therapies. Cancer Res. 2005;65:5454-5461.
39. Yu D, Cozma D, Park A, Thomas-Tikhonenko A. Functional validation of genes implicated in lymphomagenesis: an in vivo selection assay using a Myc-induced B-cell tumor. Ann N Y Acad Sci. 2005;1059:145-159.
40. Amaravadi RK, Yu D, Lum JJ, et al. Autophagy inhibition enhances therapy-induced apoptosis in a Myc-induced model of lymphoma. J Clin Invest. 2007;117:326-336.
41. Etscheid BG, Foster SA, Galloway DA. The E6 protein of human papillomavirus type 16 functions as a transcriptional repressor in a mechanism independent of the tumor suppressor protein, p53. Virology. 1994;205:583-585.
42. Picard D, Khursheed B, Garabedian MJ, et al. Reduced levels of hsp90 compromise steroid receptor action in vivo. Nature. 1990;348:166-168.
43. Han J, Flemington C, Houghton AB, et al. Expression of bbc3, a pro-apoptotic BH3-only gene, is regulated by diverse cell death and survival signals. Proc Natl Acad Sci U S A.2001;98:11318-11323.
44. Nakano K, Vousden KH. PUMA, a novel proapoptotic gene, is induced by p53. Mol Cell. 2001;7:683-694.
45. Yu J, Zhang L, Hwang PM, Kinzler KW, Vogelstein B. PUMA induces the rapid apoptosis of colorectal cancer cells. Mol Cell. 2001;7:673-682.
46. Oda E, Ohki R, Murasawa H, et al. Noxa, a BH3-only member of the Bcl-2 family and candidate mediator of p53-induced apoptosis. Science. 2000;288:1053-1058.
47. Alarcon R, Koumenis C, Geyer RK, Maki CG, Giaccia AJ. Hypoxia induces p53 accumulation through MDM2 down-regulation and inhibition of E6-mediated degradation. Cancer Res. 1999;59:6046-6051.
48. Meng L, Mohan R, Kwok BH, et al. Epoxomicin, a potent and selective proteasome inhibitor, exhibits in vivo antiinflammatory activity. Proc Natl Acad Sci U S A. 1999;96:10403-10408.
49. Lindsten K, Menendez-Benito V, Masucci MG, Dantuma NP. A transgenic mouse model of the ubiquitin/proteasome system. Nat Biotechnol. 2003;21:897-902.
50. Adams J. Proteasome inhibition in cancer: development of PS-341. Semin Oncol. 2001;28:613-619.
51. Lindstrom MS, Klangby U, Wiman KG. p14ARF homozygous deletion or MDM2 overexpression in Burkitt lymphoma lines carrying wild type p53. Oncogene. 2001;20:2171-2177.
52. Gaidano G, Ballerini P, Gong JZ, et al. p53 mutations in human lymphoid malignancies: association with Burkitt lymphoma and chronic lymphocytic leukemia. Proc Natl Acad Sci U S A. 1991;88:5413-5417.
53. Camus S, Higgins M, Lane DP, Lain S. Differences in the ubiquitination of p53 by Mdm2 and the HPV protein E6. FEBS Lett. 2003;536:220-224.
54. Reisman D, Elkind NB, Roy B, Beamon J, Rotter V. c-Myc trans-activates the p53 promoter through a required downstream CACGTG motif. Cell Growth Differ. 1993;4:57-65.
55. Adams JM, Harris AW, Pinkert CA, et al. The c-myc oncogene driven by immunoglobulin enhancers induces lymphoid malignancy in transgenic mice. Nature. 1985;318:533-538.
56. Alt JR, Greiner TC, Cleveland JL, Eischen CM. Mdm2 haplo-insufficiency profoundly inhibits Myc-induced lymphomagenesis. EMBO J. 2003;22:1442-1450.
57. Hemann MT, Bric A, Teruya-Feldstein J, et al. Evasion of the p53 tumour surveillance network by tumour-derived MYC mutants. Nature. 2005;436:807-811.
58. Adams J. The proteasome: a suitable antineo-plastic target. Nat Rev Cancer. 2004;4:349-360.
59. Lopes UG, Erhardt P, Yao R, Cooper GM. p53-dependent induction of apoptosis by proteasome inhibitors. J Biol Chem. 1997;272:12893-12896.
60. Dietrich C, Bartsch T, Schanz F, Oesch F, Wieser RJ. p53-dependent cell cycle arrest induced by N-acetyl-L-leucinyl-L-leucinyl-L-norleucinal in platelet-derived growth factor-stimulated human fibroblasts. Proc Natl Acad Sci U S A. 1996;93:10815-10819.
61. Chen F, Chang D, Goh M, Klibanov SA, Ljungman M. Role of p53 in cell cycle regulation and apoptosis following exposure to proteasome inhibitors. Cell Growth Differ. 2000;11:239-246.
62. Meng LH, Zhang H, Hayward L, et al. Tetrandrine induces early G1 arrest in human colon carcinoma cells by down-regulating the activity and inducing the degradation of G1-S-specific cyclin-dependent kinases and by inducing p53 and p21Cip1. Cancer Res. 2004;64:9086-9092.
63. Matta H, Chaudhary PM. The proteasome inhibitor bortezomib (PS-341) inhibits growth and induces apoptosis in primary effusion lymphoma cells. Cancer Biol Ther. 2005;4:77-82.
64. Nasr R, El-Sabban ME, Karam JA, et al. Efficacy and mechanism of action of the proteasome inhibitor PS-341 in T-cell lymphomas and HTLV-I associated adult T-cell leukemia/lymphoma. Oncogene. 2005;24:419-430.
65. Pei XY, Dai Y, Grant S. Synergistic induction of oxidative injury and apoptosis in human multiple myeloma cells by the proteasome inhibitor bortezomib and histone deacetylase inhibitors. Clin Cancer Res. 2004;10:3839-3852.
66. Williams SA, McConkey DJ. The proteasome inhibitor bortezomib stabilizes a novel active form of p53 in human LNCaP-Pro5 prostate cancer cells. Cancer Res. 2003;63:7338-7344.
67. Perez-Galan P, Roue G, Villamor N, et al. The proteasome inhibitor bortezomib induces apoptosis in mantle cell lymphoma through generation of ROS species and Noxa activation independent of p53 status. Blood. 2005;107:257-264.
68. Yin D, Zhou H, Kumagai T, et al. Proteasome inhibitor PS-341 causes cell growth arrest and apoptosis in human glioblastoma multiforme (GBM). Oncogene. 2005;24:344-354.
69. An WG, Hwang SG, Trepel JB, Blagosklonny MV. Protease inhibitor-induced apoptosis: accumulation of wt p53, p21WAF1/CIP1, and induction of apoptosis are independent markers of proteasome inhibition. Leukemia. 2000;14:1276-1283.
70. Yu J, Tiwari S, Steiner P, Zhang L. Differential apoptotic response to the proteasome inhibitor Bortezomib [VELCADE™, PS-341] in Bax-deficient and p21-deficient colon cancer cells. Cancer Biol Ther. 2003;2:694-699.
71. Herrmann JL, Briones F Jr, Brisbay S, Logothetis CJ, McDonnell TJ. Prostate carcinoma cell death resulting from inhibition of proteasome activity is independent of functional Bcl-2 and p53. Oncogene. 1998;17:2889-2899.
72. Kamat AM, Karashima T, Davis DW, et al. The proteasome inhibitor bortezomib synergizes with gemcitabine to block the growth of human 253JB-V bladder tumors in vivo. Mol Cancer Ther. 2004;3:279-290.
73. Xue W, Zender L, Miething C, et al. Senescence and tumour clearance is triggered by p53 restoration in murine liver carcinomas. Nature. 2007;445:656-660.
74. Ventura A, Kirsch DG, McLaughlin ME, et al. Restoration of p53 function leads to tumour regression in vivo. Nature. 2007;445:661-665.