Activation of the anaphase promoting complex by HTLV-1 tax leads to senescence

EMBO Journal

Volumn 25, Issue 8, 2006, Pages 1741-1752

  Kuo, Yu Liang ^a   Giam, Chou Zen ^a  

^a UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

Author keywords

Anaphase promoting complex; Cyclin dependent kinase inhibitor; HTLV 1 Tax; Senescence; Skp1 Cullin F box

Indexed keywords

ANAPHASE PROMOTING COMPLEX; CYCLIN A; CYCLIN B1; CYCLIN DEPENDENT KINASE INHIBITOR 1; CYCLIN DEPENDENT KINASE INHIBITOR 1B; PROTEIN P53; RETINOBLASTOMA PROTEIN; S PHASE KINASE ASSOCIATED PROTEIN 2; SMALL INTERFERING RNA; TAX PROTEIN;

ARTICLE; CELL CYCLE; CELL CYCLE ARREST; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL CYCLE PROGRESSION; CELL CYCLE S PHASE; CELL STRAIN 3T3; CELL SYNCHRONIZATION; CELL TRANSFORMATION; CONTROLLED STUDY; FLOW CYTOMETRY; GENE ACTIVATION; HELA CELL; HUMAN; HUMAN CELL; HUMAN T CELL LEUKEMIA VIRUS 1; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; REAL TIME POLYMERASE CHAIN REACTION; SENESCENCE; T CELL LEUKEMIA; UBIQUITINATION;

ANIMALS; CELL AGING; CELL CYCLE; CELL LINE; CELL TRANSFORMATION, VIRAL; CYCLIN A; CYCLIN B; CYCLIN-DEPENDENT KINASE INHIBITOR P21; CYCLIN-DEPENDENT KINASE INHIBITOR P27; ENZYME ACTIVATION; GENE PRODUCTS, TAX; HUMANS; MICE; NEOPLASM PROTEINS; POLYUBIQUITIN; S-PHASE KINASE-ASSOCIATED PROTEINS; TUMOR SUPPRESSOR PROTEIN P53; UBIQUITIN-PROTEIN LIGASE COMPLEXES;

HUMAN T-LYMPHOTROPIC VIRUS 1;

EID: 33646164424     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/sj.emboj.7601054     Document Type: Article

References (38)

1. Akagi T, Ono H, Shimotohno K (1996) Expression of cell-cycle regulatory genes in HTLV-I infected T-cell lines: possible involvement of Taxi in the altered expression of cyclin D2, p18Ink4 and p21Waf1/Cip1/Sdi1. Oncogene 12: 1645-1652
2. Bashir T, Dorrello NV, Amador V, Guardavaccaro D, Pagano M (2004) Control of the SCF(Skp2-Cks1) ubiquitin ligase by the APC/C(Cdh1) ubiquitin ligase. Nature 428: 190-193
3. Bornstein G, Bloom J, Sitry-Shevah D, Nakayama K, Pagano M, Hershko A (2003) Role of the SCFSkp2 ubiquitin ligase in the degradation of p21Cip1 in S phase. J Biol Chem 278: 25752-25757
4. Carrano AC, Eytan E, Hershko A, Pagano M (1999) SKP2 is required for ubiquitin-mediated degradation of the CDK inhibitor p27. Nat Cell Biol 1: 193-199
5. Cereseto A, Washington PR, Rivadeneira E, Franchini G (1999) Limiting amounts of p27Kip1 correlates with constitutive activation of cyclin E-CDK2 complex in HTLV-I-transformed T-cells. Oncogene 18: 2441-2450
6. Chang BD, Broude EV, Dokmanovic M, Zhu H, Ruth A, Xuan Y, Kandel ES, Lausch E, Christov K, Roninson IB (1999) A senescence-like phenotype distinguishes tumor cells that undergo terminal proliferation arrest after exposure to anticancer agents. Cancer Res 59: 3761-3767
7. Chin L, Artandi SE, Shen Q, Tam A, Lee SL, Gottlieb GJ, Greider CW, DePinho RA (1999) p53 deficiency rescues the adverse effects of telomere loss and cooperates with telomere dysfunction to accelerate carcinogenesis. Cell 97: 527-538
8. Chowdhury IH, Farhadi A, Wang XF, Robb ML, Birx DL, Kim JH (2003) Human T-cell leukemia virus type 1 Tax activates cyclin-dependent kinase inhibitor p21/Waf1/Cip1 expression through a p53-independent mechanism: inhibition of cdk2. Int J Cancer 107: 603-611
9. Chu ZL, Di Donato JA, Hawiger J, Ballard DW (1998) The tax oncoprotein of human T-cell leukemia virus type 1 associates with and persistently activates IkappaB kinases containing IKKalpha and IKKbeta. J Biol Chem 273: 15891-15894
10. de la Fuente C, Wang L, Wang D, Deng L, Wu K, Li H, Stein LD, Denny T, Coffman F, Kehn K, Baylor S, Maddukuri A, Pumfery A, Kashanchi F (2003) Paradoxical effects of a stress signal on proand anti-apoptotic machinery in HTLV-1 Tax expressing cells. Mol Cell Biochem 245: 99-113
11. Dimri GP, Lee X, Basile G, Acosta M, Scott G, Roskelley C, Medrano EE, Linskens M, Rubelj I, Pereira-Smith O (1995) A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc Natl Acad Sci USA 92: 9363-9367
12. Ferbeyre G, de Stanchina E, Lin AW, Querido E, McCurrach ME, Hannon GJ, Lowe SW (2002) Oncogenic ras and p53 cooperate to induce cellular senescence. Mol Cell Biol 22: 3497-3508
13. Franchini G, Wong-Staal F, Gallo RC (1984) Human T-cell leukemia virus (HTLV-I) transcripts in fresh and cultured cells of patients with adult T-cell leukemia. Proc Natl Acad Sci USA 81: 6207-6211
14. Fu DX, Kuo YL, Liu B, Jeang KT, Giam CZ (2003) Human T-lymphotropic virus type I tax activates I-kappa B kinase by inhibiting I-kappa B kinase-associated serine/threonine protein phosphatase 2A. J Biol Chem 278: 1487-1493
15. Ganoth D, Bornstein G, Ko TK, Larsen B, Tyers M, Pagano M, Hershko A (2001) The cell-cycle regulatory protein Cks1 is required for SCF(Skp2)-mediated ubiquitinylation of p27. Nat Cell Biol 3: 321-324
16. Hara T, Kamura T, Nakayama K, Oshikawa K, Hatakeyama S, Nakayama K (2001) Degradation of p27(Kip1) at the G(0)-G(1) transition mediated by a Skp2-independent ubiquitination pathway. J Biol Chem 276: 48937-48943
17. Helt AM, Galloway DA (2003) Mechanisms by which DNA tumor virus oncoproteins target the Rb family of pocket proteins. Carcinogenesis 24: 159-169
18. Jeang KT, Giam CZ, Majone F, Aboud M (2004) Life, death, and tax: role of HTLV-I oncoprotein in genetic instability and cellular transformation. J Biol Chem 279: 31991-31994
19. Jin DY, Giordano V, Kibler KV, Nakano H, Jeang KT (1999) Role of adapter function in oncoprotein-mediated activation of NF-kappaB. Human T-cell leukemia virus type I Tax interacts directly with IkappaB kinase gamma. J Biol Chem 274: 17402-17405
20. Kawata S, Ariumi Y, Shimotohno K (2003) p21(Waf1/Cip1/Sdi1) prevents apoptosis as well as stimulates growth in cells transformed or immortalized by human T-cell leukemia virus type 1-encoded tax. J Virol 77: 7291-7299
21. Korber B, Okayama A, Donnelly R, Tachibana N, Essex M (1991) Polymerase chain reaction analysis of defective human T-cell leukemia virus type I proviral genomes in leukemic cells of patients with adult T-cell leukemia. J Virol 65: 5471-5476
22. Liang MH, Geisbert T, Yao Y, Hinrichs SH, Giam CZ (2002) Human T-lymphotropic virus type 1 oncoprotein tax promotes S-phase entry but blocks mitosis. J Virol 76: 4022-4033
23. Lim MS, Adamson A, Lin Z, Perez-Ordonez B, Jordan RC, Tripp S, Perkins SL, Elenitoba-Johnson KS (2002) Expression of Skp2, a p27(Kip1) ubiquitin ligase, in malignant lymphoma: correlation with p27(Kip1) and proliferation index. Blood 100: 2950-2956
24. Liu B, Hong S, Tang Z, Yu H, Giam CZ (2005) HTLV-I Tax directly binds the Cdc20-associated anaphase-promoting complex and activates it ahead of schedule. Proc Natl Acad Sci USA 102: 63-68
25. Liu B, Liang MH, Kuo YL, Liao W, Boros I, Kleinberger T, Blancato J, Giam CZ (2003) Human T-lymphotropic virus type 1 oncoprotein tax promotes unscheduled degradation of Pds1p/securin and Clb2p/cyclin B1 and causes chromosomal instability. Mol Cell Biol 23: 5269-5281
26. Nakayama K, Nagahama H, Minamishima YA, Matsumoto M, Nakamichi I, Kitagawa K, Shirane M, Tsunematsu R, Tsukiyama T, Ishida N, Kitagawa M, Nakayama K, Hatakeyama S (2000) Targeted disruption of Skp2 results in accumulation of cyclin E and p27(Kip1), polyploidy and centrosome overduplication. EMBO J 19: 2069-2081
27. Nakayama K, Nagahama H, Minamishima YA, Miyake S, Ishida N, Hatakeyama S, Kitagawa M, Iemura S, Natsume T, Nakayama KI (2004) Skp2-mediated degradation of p27 regulates progression into mitosis. Dev Cell 6: 661-672
28. Naldini L, Blomer U, Gallay P, Ory D, Mulligan R, Gage FH, Verma IM, Trono D (1996) In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science 272: 263-267
29. Scheffner M, Werness BA, Huibregtse JM, Levine AJ, Howley PM (1990) The E6 oncoprotein encoded by human papillomavirus types 16 and 18 promotes the degradation of p53. Cell 63: 1129-1136
30. Serrano M, Lin AW, McCurrach ME, Beach D, Lowe SW (1997) Oncogenic ras provokes premature cell senescence associated with accumulation of p53 and p16INK4a. Cell 88: 593-602
31. Sun SC, Ballard DW (1999) Persistent activation of NF-kappaB by the tax transforming protein of HTLV-1: hijacking cellular IkappaB kinases. Oncogene 18: 6948-6958
32. Swanson C, Ross J, Jackson PK (2000) Nuclear accumulation of cyclin E/Cdk2 triggers a concentration-dependent switch for the destruction of p27Xic1. Proc Natl Acad Sci USA 97: 7796-7801
33. Wei W, Ayad NG, Wan Y, Zhang GJ, Kirschner MW, Kaelin Jr WG (2004) Degradation of the SCF component Skp2 in cell-cycle phase G1 by the anaphase-promoting complex. Nature 428: 194-198
34. Wells SI, Aronow BJ, Wise TM, Williams SS, Couget JA, Howley PM (2003) Transcriptome signature of irreversible senescence in human papillomavirus-positive cervical cancer cells. Proc Natl Acad Sci USA 100: 7093-7098
35. Wells SI, Francis DA, Karpova AY, Dowhanick JJ, Benson JD, Howley PM (2000) Papillomavirus E2 induces senescence in HPV-positive cells via pRB- and p21 (CIP)-dependent pathways. EMBO J 19: 5762-5771
36. Xiao G, Sun SC (2000) Activation of IKKalpha and IKKbeta through their fusion with HTLV-I tax protein. Oncogene 19: 5198-5203
37. Yamaoka S, Courtois G, Bessia C, Whiteside ST, Weil R, Agou F, Kirk HE, Kay RJ, Israel A (1998) Complementation cloning of NEMO, a component of the IkappaB kinase complex essential for NF-kappaB activation. Cell 93: 1231-1240
38. Zhu XH, Nguyen H, Halicka HD, Traganos F, Koff A (2004) Noncatalytic requirement for cyclin A-cdk2 in p27 turnover. Mol Cell Biol 24: 6058-6066