HTLV-I p30 inhibits multiple S phase entry checkpoints, decreases cyclin E-CDK2 interactions and delays cell cycle progression

Molecular Cancer

Volumn 9, Issue , 2010, Pages

  Baydoun, Hicham H ^a   Pancewicz, Joanna ^a   Bai, XueTao ^a   Nicot, Christophe ^a  

^a UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHECKPOINT KINASE 1; CYCLIN DEPENDENT KINASE 2; CYCLIN E; PROTEIN P30; RETINOBLASTOMA PROTEIN; TRANSCRIPTION FACTOR DP1; CDK2 PROTEIN, HUMAN; VIRUS PROTEIN;

ARTICLE; CELL CYCLE G1 PHASE; CELL CYCLE PROGRESSION; CELL CYCLE S PHASE; HUMAN; HUMAN CELL; HUMAN T CELL LEUKEMIA VIRUS 1; PROTEIN BINDING; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; CELL CYCLE; CELL LINE; FLOW CYTOMETRY; GENETICS; HELA CELL; IMMUNOPRECIPITATION; METABOLISM; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

HUMAN T-LYMPHOTROPIC VIRUS 1;

BLOTTING, WESTERN; CELL CYCLE; CELL LINE; CYCLIN E; CYCLIN-DEPENDENT KINASE 2; FLOW CYTOMETRY; HELA CELLS; HUMAN T-LYMPHOTROPIC VIRUS 1; HUMANS; IMMUNOPRECIPITATION; PROTEIN BINDING; RETROVIRIDAE PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; S PHASE;

EID: 78649923779     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/1476-4598-9-302     Document Type: Article

References (55)

1. Sherr CJ, Roberts JM. Living with or without cyclins and cyclin-dependent kinases. Genes Dev 2004, 18:2699-2711. 10.1101/gad.1256504, 15545627.
2. van den Heuvel S, Dyson NJ. Conserved functions of the pRB and E2F families. Nat Rev Mol Cell Biol 2008, 9:713-724. 10.1038/nrm2469, 18719710.
3. Zhang HS, Gavin M, Dahiya A, Postigo AA, Ma D, Luo RX, Harbour JW, Dean DC. Exit from G1 and S phase of the cell cycle is regulated by repressor complexes containing HDAC-Rb-hSWI/SNF and Rb-hSWI/SNF. Cell 2000, 101:79-89. 10.1016/S0092-8674(00)80625-X, 10778858.
4. Lees E, Faha B, Dulic V, Reed SI, Harlow E. Cyclin E/cdk2 and cyclin A/cdk2 kinases associate with p107 and E2F in a temporally distinct manner. Genes Dev 1992, 6:1874-1885. 10.1101/gad.6.10.1874, 1398067.
5. Dulic V, Lees E, Reed SI. Association of human cyclin E with a periodic G1-S phase protein kinase. Science 1992, 257:1958-1961. 10.1126/science.1329201, 1329201.
6. Hinds PW, Mittnacht S, Dulic V, Arnold A, Reed SI, Weinberg RA. Regulation of retinoblastoma protein functions by ectopic expression of human cyclins. Cell 1992, 70:993-1006. 10.1016/0092-8674(92)90249-C, 1388095.
7. Sheaff RJ, Groudine M, Gordon M, Roberts JM, Clurman BE. Cyclin E-CDK2 is a regulator of p27Kip1. Genes Dev 1997, 11:1464-1478. 10.1101/gad.11.11.1464, 9192873.
8. Vlach J, Hennecke S, Amati B. Phosphorylation-dependent degradation of the cyclin-dependent kinase inhibitor p27. EMBO J 1997, 16:5334-5344. 10.1093/emboj/16.17.5334, 1170165, 9311993.
9. Harbour JW, Dean DC. The Rb/E2F pathway: expanding roles and emerging paradigms. Genes Dev 2000, 14:2393-2409. 10.1101/gad.813200, 11018009.
10. Yu Q, Sicinski P. Mammalian cell cycles without cyclin E-CDK2. Cell Cycle 2004, 3:292-295. 10.4161/cc.3.1.594, 14726682.
11. Le Cam L, Polanowska J, Fabbrizio E, Olivier M, Philips A, Ng EE, Classon M, Geng Y, Sardet C. Timing of cyclin E gene expression depends on the regulated association of a bipartite repressor element with a novel E2F complex. EMBO J 1999, 18:1878-1890. 10.1093/emboj/18.7.1878, 1171273, 10202151.
12. Poiesz BJ, Ruscetti FW, Gazdar AF, Bunn PA, Minna JD, Gallo RC. Detection and isolation of type C retrovirus particles from fresh and cultured lymphocytes of a patient with cutaneous T-cell lymphoma. Proc Natl Acad Sci USA 1980, 77:7415-7419. 10.1073/pnas.77.12.7415, 350514, 6261256.
13. Hinuma Y, Nagata K, Hanaoka M, Nakai M, Matsumoto T, Kinoshita KI, Shirakawa S, Miyoshi I. Adult T-cell leukemia: antigen in an ATL cell line and detection of antibodies to the antigen in human sera. Proc Natl Acad Sci USA 1981, 78(10):6476-80. 10.1073/pnas.78.10.6476, 349062, 7031654.
14. Gessain A, Barin F, Vernant JC, Gout O, Maurs L, Calender A, de The G. Antibodies to human T-lymphotropic virus type-I in patients with tropical spastic paraparesis. Lancet 1985, 2:407-410. 10.1016/S0140-6736(85)92734-5, 2863442.
15. Osame M, Matsumoto M, Usuku K, Izumo S, Ijichi N, Amitani H, Tara M, Igata A. Chronic progressive myelopathy associated with elevated antibodies to human T-lymphotropic virus type I and adult T-cell leukemialike cells. Ann Neurol 1987, 21:117-122. 10.1002/ana.410210203, 2881513.
16. Franchini G, Nicot C, Johnson JM. Seizing of T cells by human T-cell leukemia/lymphoma virus type 1. Adv Cancer Res 2003, 89:69-132. full_text, 14587871.
17. Marriott SJ, Semmes OJ. Impact of HTLV-I Tax on cell cycle progression and the cellular DNA damage repair response. Oncogene 2005, 24:5986-5995. 10.1038/sj.onc.1208976, 16155605.
18. Neuveut C, Jeang KT. Cell cycle dysregulation by HTLV-I: role of the tax oncoprotein. Front Biosci 2002, 7:d157-d163. 10.2741/neuveut, 11779707.
19. Lemoine FJ, Marriott SJ. Accelerated G(1) phase progression induced by the human T cell leukemia virus type I (HTLV-I) Tax oncoprotein. J Biol Chem 2001, 276:31851-31857. 10.1074/jbc.M105195200, 11435441.
20. de la Fuente C, Deng L, Santiago F, Arce L, Wang L, Kashanchi F. Gene expression array of HTLV type 1-infected T cells: Up-regulation of transcription factors and cell cycle genes. AIDS Res Hum Retroviruses 2000, 16:1695-1700. 10.1089/08892220050193164, 11080812.
21. Schmitt I, Rosin O, Rohwer P, Gossen M, Grassmann R. Stimulation of cyclin-dependent kinase activity and G1- to S-phase transition in human lymphocytes by the human T-cell leukemia/lymphotropic virus type 1 Tax protein. J Virol 1998, 72:633-640. 109417, 9420268.
22. Cereseto A, Diella F, Mulloy JC, Cara A, Michieli P, Grassmann R, Franchini G, Klotman ME. p53 functional impairment and high p21waf1/cip1 expression in human T-cell lymphotropic/leukemia virus type I-transformed T cells. Blood 1996, 88:1551-1560.
23. Suzuki T, Kitao S, Matsushime H, Yoshida M. HTLV-1 Tax protein interacts with cyclin-dependent kinase inhibitor p16INK4A and counteracts its inhibitory activity towards CDK4. EMBO J 1996, 15:1607-1614. 450070, 8612584.
24. Liu M, Yang L, Zhang L, Liu B, Merling R, Xia Z, Giam CZ. Human T-cell leukemia virus type 1 infection leads to arrest in the G1 phase of the cell cycle. J Virol 2008, 82:8442-8455. 10.1128/JVI.00091-08, 2519625, 18596104.
25. Kuo YL, Giam CZ. Activation of the anaphase promoting complex by HTLV-1 tax leads to senescence. EMBO J 2006, 25:1741-1752. 10.1038/sj.emboj.7601054, 1440834, 16601696.
26. Bellon M, Baydoun HH, Yao Y, Nicot C. HTLV-I Tax-dependent and -independent events associated with immortalization of human primary T lymphocytes. Blood 2010, 115:2441-2448. 10.1182/blood-2009-08-241117, 20093405.
27. Silic-Benussi M, Cavallari I, Zorzan T, Rossi E, Hiraragi H, Rosato A, Horie K, Saggioro D, Lairmore MD, Willems L, Chieco-Bianchi L, D'Agostino DM, Ciminale V. Suppression of tumor growth and cell proliferation by p13II, a mitochondrial protein of human T cell leukemia virus type 1. Proc Natl Acad Sci USA 2004, 101:6629-6634. 10.1073/pnas.0305502101, 404096, 15100416.
28. Taylor JM, Ghorbel S, Nicot C. Genome wide analysis of human genes transcriptionally and post-transcriptionally regulated by the HTLV-I protein p30. BMC Genomics 2009, 10:311. 10.1186/1471-2164-10-311, 2723137, 19602286.
29. Datta A, Silverman L, Phipps AJ, Hiraragi H, Ratner L, Lairmore MD. Human T-lymphotropic virus type-1 p30 alters cell cycle G2 regulation of T lymphocytes to enhance cell survival. Retrovirology 2007, 4:49. 10.1186/1742-4690-4-49, 1937004, 17634129.
30. Taylor JM, Brown M, Nejmeddine M, Kim KJ, Ratner L, Lairmore M, Nicot C. Novel role for interleukin-2 receptor-Jak signaling in retrovirus transmission. J Virol 2009, 83:11467-11476. 10.1128/JVI.00952-09, 2772716, 19726513.
31. Fukumoto R, Dundr M, Nicot C, Adams A, Valeri VW, Samelson LE, Franchini G. Inhibition of T-cell receptor signal transduction and viral expression by the linker for activation of T cells-interacting p12(I) protein of human T-cell leukemia/lymphoma virus type 1. J Virol 2007, 81:9088-9099. 10.1128/JVI.02703-06, 1951423, 17582004.
32. Ding W, Kim SJ, Nair AM, Michael B, Boris-Lawrie K, Tripp A, Feuer G, Lairmore MD. Human T-cell lymphotropic virus type 1 p12I enhances interleukin-2 production during T-cell activation. J Virol 2003, 77:11027-11039. 10.1128/JVI.77.20.11027-11039.2003, 225008, 14512551.
33. Nicot C, Mulloy JC, Ferrari MG, Johnson JM, Fu K, Fukumoto R, Trovato R, Fullen J, Leonard WJ, Franchini G. HTLV-1 p12(I) protein enhances STAT5 activation and decreases the interleukin-2 requirement for proliferation of primary human peripheral blood mononuclear cells. Blood 2001, 98:823-829. 10.1182/blood.V98.3.823, 11468184.
34. Arnold J, Zimmerman B, Li M, Lairmore MD, Green PL. Human T-cell leukemia virus type-1 antisense-encoded gene, Hbz, promotes T-lymphocyte proliferation. Blood 2008, 112:3788-3797. 10.1182/blood-2008-04-154286, 2572803, 18689544.
35. Nicot C, Dundr M, Johnson JM, Fullen JR, Alonzo N, Fukumoto R, Princler GL, Derse D, Misteli T, Franchini G. HTLV-1-encoded p30II is a post-transcriptional negative regulator of viral replication. Nat Med 2004, 10:197-201. 10.1038/nm984, 14730358.
36. Sinha-Datta U, Datta A, Ghorbel S, Dodon MD, Nicot C. Human T-cell lymphotrophic virus type I rex and p30 interactions govern the switch between virus latency and replication. J Biol Chem 2007, 282:14608-14615. 10.1074/jbc.M611219200, 17360706.
37. Baydoun HH, Bellon M, Nicot C. HTLV-1 Yin and Yang: Rex and p30 master regulators of viral mRNA trafficking. AIDS Rev 2008, 10:195-204. 2666328, 19092975.
38. Datta A, Sinha-Datta U, Dhillon NK, Buch S, Nicot C. The HTLV-I p30 interferes with TLR4 signaling and modulates the release of pro- and anti-inflammatory cytokines from human macrophages. J Biol Chem 2006, 281:23414-23424. 10.1074/jbc.M600684200, 16785240.
39. Zhang W, Nisbet JW, Albrecht B, Ding W, Kashanchi F, Bartoe JT, Lairmore MD. Human T-lymphotropic virus type 1 p30(II) regulates gene transcription by binding CREB binding protein/p300. J Virol 2001, 75:9885-9895. 10.1128/JVI.75.20.9885-9895.2001, 114560, 11559821.
40. Zhang W, Nisbet JW, Bartoe JT, Ding W, Lairmore MD. Human T-lymphotropic virus type 1 p30(II) functions as a transcription factor and differentially modulates CREB-responsive promoters. J Virol 2000, 74:11270-11277. 10.1128/JVI.74.23.11270-11277.2000, 113231, 11070026.
41. Welcker M, Singer J, Loeb KR, Grim J, Bloecher A, Gurien-West M, Clurman BE, Roberts JM. Multisite phosphorylation by Cdk2 and GSK3 controls cyclin E degradation. Mol Cell 2003, 2:381-92.
42. Gjoerup O, Lukas J, Bartek J, Willumsen BM. Rac and Cdc42 Are Potent Stimulators of E2F-dependent Transcription Capable of Promoting Retinoblastoma Susceptibility Gene Product Hyperphosphorylation. J Biol Chem 1998, 273:18812-18818. 10.1074/jbc.273.30.18812, 9668055.
43. Bellon M, Baydoun HH, Yao Y, Nicot C. HTLV-I Tax-dependent and -independent events associated with immortalization of human primary T lymphocytes. Blood 2010, 115(12):2441-2448. 10.1182/blood-2009-08-241117, 20093405.
44. Blais A, Dynlacht BD. E2F-associated chromatin modifiers and cell cycle control. Curr Opin Cell Biol 2007, 19:658-662. 10.1016/j.ceb.2007.10.003, 18023996.
45. Lemasson I, Thebault S, Sardet C, Devaux C, Mesnard JM. Activation of E2F-mediated transcription by human T-cell leukemia virus type I Tax protein in a p16(INK4A)-negative T-cell line. J Biol Chem 1998, 273:23598-23604. 10.1074/jbc.273.36.23598, 9722600.
46. Gu Y, Rosenblatt J, Morgan DO. Cell cycle regulation of CDK2 activity by phosphorylation of Thr160 and Tyr15. EMBO J 1992, 11:3995-4005. 556910, 1396589.
47. Cereseto A, Washington Parks R, Rivadeneira E, Franchini G. Limiting amounts of p27Kip1 correlates with constitutive activation of cyclin E-CDK2 complex in HTLV-I-transformed T-cells. Oncogene 1999, 18(15):2441-2450. 10.1038/sj.onc.1202567, 10229195.
48. Yamamoto B, Li M, Kesic M, Younis I, Lairmore MD, Green PL. Human T-cell leukemia virus type 2 post-transcriptional control protein p28 is required for viral infectivity and persistence in vivo. Retrovirology 2008, 5:38. 10.1186/1742-4690-5-38, 2405800, 18474092.
49. Furukawa Y, Osame M, Kubota R, Tara M, Yoshida M. Human T-cell leukemia virus type-1 (HTLV-1) Tax is expressed at the same level in infected cells of HTLV-1-associated myelopathy or tropical spastic paraparesis patients as in asymptomatic carriers but at a lower level in adult T-cell leukemia cells. Blood 1995, 85:1865-1870.
50. Mortreux F, Leclercq I, Gabet AS, Leroy A, Westhof E, Gessain A, Wain-Hobson S, Wattel E. Somatic mutation in human T-cell leukemia virus type 1 provirus and flanking cellular sequences during clonal expansion in vivo. J Natl Cancer Inst 2001, 93(5):367-77. 10.1093/jnci/93.5.367, 11238698.
51. Kim SJ, Ding W, Albrecht B, Green PL, Lairmore MD. A conserved calcineurin-binding motif in human T lymphotropic virus type 1 p12I functions to modulate nuclear factor of activated T cell activation. J Biol Chem 2003, 278:15550-15557. 10.1074/jbc.M210210200, 12601010.
52. Albrecht B, Lairmore MD. Critical role of human T-lymphotropic virus type 1 accessory proteins in viral replication and pathogenesis. Microbiol Mol Biol Rev 2002, 66:396-406. 10.1128/MMBR.66.3.396-406.2002, 120794, 12208996.
53. Johnson JM, Nicot C, Fullen J, Ciminale V, Casareto L, Mulloy JC, Jacobson S, Franchini G. Free major histocompatibility complex class I heavy chain is preferentially targeted for degradation by human T-cell leukemia/lymphotropic virus type 1 p12(I) protein. J Virol 2001, 75:6086-6094. 10.1128/JVI.75.13.6086-6094.2001, 114324, 11390610.
54. Albrecht B, Collins ND, Burniston MT, Nisbet JW, Ratner L, Green PL, Lairmore MD. Human T-lymphotropic virus type 1 open reading frame I p12(I) is required for efficient viral infectivity in primary lymphocytes. J Virol 2000, 74:9828-9835. 10.1128/JVI.74.21.9828-9835.2000, 102019, 11024109.
55. Fukumoto R, Andresen V, Bialuk I, Cecchinato V, Walser JC, Valeri VW, Nauroth JM, Gessain A, Nicot C, Franchini G. In vivo genetic mutations define predominant functions of the human T-cell leukemia/lymphoma virus p12I protein. Blood 2009, 113:3726-3734. 10.1182/blood-2008-04-146928, 2670790, 18791162.