HTLV-1 tax protein interacts with cyclin-dependent kinase inhibitor p16INK4A and counteracts its inhibitory activity towards CDK4

EMBO Journal

Volumn 15, Issue 7, 1996, Pages 1607-1614

  Suzuki, Takeshi ^a   Kitao, Saori ^a   Matsushime, Hitoshi ^a   Yoshida, Mitsuaki ^a  

^a UNIVERSITY OF TOKYO   (Japan)

Author keywords

Adult T cell leukemia; Cell cycle inhibitor; HTLV 1; Tax protein; Tumor suppressor gene

Indexed keywords

ANKYRIN; CELL PROTEIN; CYCLIN DEPENDENT KINASE; ENZYME INHIBITOR; REGULATOR PROTEIN; TAX PROTEIN;

ARTICLE; CELL CYCLE; CELL CYCLE G1 PHASE; CELL GROWTH; ENZYME INHIBITION; HUMAN; HUMAN CELL; HUMAN T CELL LEUKEMIA VIRUS 1; PRIORITY JOURNAL; T LYMPHOCYTE;

ANIMALS; BASE SEQUENCE; BINDING SITES; CARRIER PROTEINS; CELL CYCLE; CELL LINE; CELL TRANSFORMATION, VIRAL; CYCLIN-DEPENDENT KINASE 4; CYCLIN-DEPENDENT KINASE INHIBITOR P16; CYCLIN-DEPENDENT KINASES; DNA PRIMERS; ENZYME INHIBITORS; GENE PRODUCTS, TAX; HTLV-I INFECTIONS; HUMAN T-LYMPHOTROPIC VIRUS 1; HUMANS; MICE; MICE, TRANSGENIC; MOLECULAR SEQUENCE DATA; PROTO-ONCOGENE PROTEINS; SIGNAL TRANSDUCTION; T-LYMPHOCYTES;

HTLV; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN T-LYMPHOTROPIC VIRUS 1; MUS MUSCULUS;

EID: 0029923745     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1002/j.1460-2075.1996.tb00505.x     Document Type: Article

References (61)

1. Baldin, V., Lukas, J., Marcote, M.J., Pagano, M. and Draetta, G. (1993) Cyclin D1 is a nuclear protein required for cell cycle progression in G1. Genes Dev., 7, 812-821.
2. Beg, A.A. and Baldwin, A.S., Jr (1993) The IκB proteins: multifunctional regulators of Rel/NF-κB transcription factors. Genes Dev., 7. 2064-2070
3. Beraud, C., Sun, S., Ganchi, P., Ballard, D.W. and Greene, W.C. (1994) Human T-cell leukemia virus type 1 Tax associates with and is negatively regulated by the NF-κB2 p100 gene product: implication for viral latency. Mol. Cell. Biol, 14, 1374-1382.
4. Cannon-Albright, L.A. et al (1992) Assignment of a locus for familial melanoma, MLM, to chromosome 9p13-p22. Science, 258, 1148-1152.
5. Cesarman, E., Chadburn, A., Inghirami, G., Gaidano, G. and Knowles, D.M. (1992) Structural and functional analysis of oncogenes and tumor suppressor genes in adult T-cell leukemia/lymphoma shows frequent p53 mutations. Blood, 80, 3205-3216.
6. Chan, F.K., Zhang, J , Cheng, L., Shapiro, D.N. and Winoto, A. (1995) Identification of human and mouse p19, a novel CDK4 and CDK6 inhibitor with homology to p16ink4. Mol. Cell. Biol., 15, 2682-2688.
7. Dowdy, S F., Hinds, P.W., Louis, K., Reed, S.I., Arnord, A. and Weinberg, R A. (1993) Physical interactions of the retinoblastoma protein with human cyclins. Cell, 73, 499-511.
8. Dyson, N, Howley, P.M., Munger, K. and Harlow, E. (1989) The human papilloma virus-16E7 oncoprotein is able to bind to the retinoblastoma gene product. Science, 243, 934-937.
9. Ewen, M.E., Sluss, H.K., Sherr, C.J., Matsushime, H., Kato, J. and Livingston, D.M. (1993) Functional interaction of the retinoblastoma protein with mammalian D-type cyclins. Cell, 73, 487-497.
10. SRF causes the aberrant induction of cellular immediate early genes through CArG boxes. Genes Dev., 6, 2066-2076.
11. Grana, X. and Reddy, E.P. (1995) Cell cycle control in mammalian cells: role of cyclins, cyclin dependent kinases (CDKs), growth suppressor genes and cyclin-dependent kinase inhibitors (CKIs). Oncogene, 11, 211-219.
12. Grassmann, R., Berchtold, S., Radam, I., Alt, M., Fleckenstein, B., Sodroski, J.G., Haseltine, W.A. and Ramstedt, U. (1992) Role of human T-cell leukemia virus type 1 X region proteins in immortalization of primary human lymphocytes in culture. J. Virol., 66, 4570-4575.
13. Grossman, W.L. Kimata, J.T., Wong, F.H., Zutter, M., Ley, T.J. and Ratner, L. (1995) Development of leukemia in mice transgenic for the tax gene of human T-cell leukemia virus type I. Proc. Natl Acad. Sci. USA, 92, 1057-1061.
14. INK4B/MTS2-related CDK6 inhibitor, correlates with wild-type pRb function. Genes Dev., 8, 2939-2952.
15. INK4B is a potential effector of TGF-beta-induced cell cycle arrest Nature, 371, 257-261.
16. Hinds, P.W. and Weinberg, R.A. (1994) Tumor suppressor genes. Curr. Opin. Genet. Dev., 4, 135-141.
17. Hirai, H., Fujisawa, J., Suzuki, T., Ueda, K., Muramatsu, M., Tsuboi, A., Arai, N. and Yoshida, M. (1992) Transcriptional activator Tax of HTLV-1 binds to the NF-κB precursor p105. Oncogene, 7, 1737-1742.
18. Hirai, H, Suzuki, T., Fujisawa, J., Inoue, J. and Yoshida, M. (1994) Tax protein of human T-cell leukemia virus type I binds to the ankyrin motifs of inhibitory factor kappa B and induces nuclear translocation of transcription factor NF-κB proteins for transcriptional activation. Proc. Natl Acad. Sci. USA, 91, 3584-3588.
19. Hirai, H., Roussel, M.F., Kato, J.Y., Ashmun, R.A. and Sherr, C.J. (1995) Novel INK4 proteins, p19 and p18, are specific inhibitors of the cyclin D-dependent kinases CDK4 and CDK6. Mol. Cell. Biol., 15, 2672-2681.
20. Hollsberg, P., Ausubel, L.J and Hafler, D.A. (1994) Human T cell lymphotropic virus type I-induced T cell activation. Resistance to TGF-beta 1-induced suppression. J. Immunol., 153, 566-573.
21. Hunter, T. and Pines, J. (1994) Cyclins and cancer. II. Cyclin D and CDK inhibitors come of age Cell, 79, 573-582.
22. Kamb, A. et al (1994a) A cell cycle regulator potentially involved in genesis of many tumor types. Science, 264, 436-440.
23. Kamb, A. et al. (1994b) Analysis of the p16INK4A gene (CDKN2) as a candidate for the chromosome 9p melanoma susceptibility locus. Nature Genetics, 8, 23-26.
24. Khatib, Z.A., Matsushime, H., Valentine, M., Shapiro, D.N., Sherr, C.J. and Look, A.T. (1993) Coamplification of the CDK4 gene with MDM2 and GL1 in human sarcomas. Cancer Res., 53, 5535-5541.
25. x) encoded by a unique sequence pX of human T-cell leukemia virus type I. Gann, 75, 747-751.
26. Koh, J., Enders, G.H., Dynlacht, B.D. and Harlow, E. (1995) Tumour-derived p16 alleles encoding proteins defective in cell-cycle inhibition. Nature, 375, 506-510.
27. Lanoix, J., Lacoste, J., Pepin, N., Rice, N. and Hiscott, J. (1994) Overproduction of NFκB2 (lyt-I0) and c-Rel: a mechanism for HTLV-1 Tax-mediated trans-activation via the NF-κB signaling pathway. Oncogene, 9, 841-852.
28. Lukas, J., Parry, D., Aagaard, L., Mann, D J., Bartkova, J., Strauss, M., Peters, G. and Bartek, J. (1995) Retinoblastoma-protein-dependent cell-cycle inhibition by the tumour suppressor p16. Nature, 375, 503-506.
29. Lux, S.E., John, K.M. and Bennett, V. (1990) Analysis of cDNA for human erythrocyte ankyrin indicates a repeated structure with homology to tissue-differentiation and cell-cycle control proteins. Nature, 344, 36-42.
30. Matsushime, H., Quelle, D.E., Shurtleff, S.A., Shibuya, M., Sherr, C J. and Kato, J.-Y. (1994) D-type cyclin-dependent kinase activity in mammalian cells. Mol. Cell. Biol., 14, 2066-2076.
31. Medema, R H., Herrera, R.E., Lam, F. and Weinberg, R.A. (1995) Growth suppression by p16ink4 requires functional retinoblastoma protein. Proc. Natl Acad. Sci. USA, 92, 6289-6293
32. Meyerson, M. and Harlow, E. (1994) Identification of a G1 kinase activity for cdk6, a novel cyclin D partner. Mol. Cell. Biol., 14, 2077-2086.
33. Murakami, T., Hirai, H., Suzuki, T., Fujisawa, J. and Yoshida, M. (1995) HTLV-1 Tax enhances NF-κB2 expression and binds to the products p52 and p100, but does not suppress the inhibitory function of p100. Virology, 206, 1066-1074.
34. Nerenberg, M., Hinrichs, S.H., Reynolds, R.K., Khoury, G. and Jay, G. (1987) The tat gene of human T lymphotropic virus type I induces mesenchymal tumors in transgenic mice. Science, 237, 1324-1329.
35. Nevins, J.R (1992) E2F a link between the Rb tumor suppressor protein and viral oncoproteins. Science, 258, 424-429.
36. Nobon, T., Miura, K., Wu, D.J., Lots, A., Takabayashi, K. and Carson, D.A (1994) Deletions of the cyclin-dependent kinase-4 inhibitor gene in multiple human cancers. Nature, 368, 753-756.
37. Ogawa, S et al (1994) Homozygous loss of the cyclin-dependent kinase 4-inhibitor (p16) gene in human leukemias. Blood, 84, 2431-2435.
38. Ohtani, K., Nakamura, M., Saito, K., Nagata, K., Sugamura, K. and Hinuma, Y. (1989) Electroporation: application to human lymphoid cell lines for stable induction of a transactivator gene of human T-cell leukemia virus type I. Nucleic Acids Res., 17, 1589-1604.
39. Okamoto, A. et al. (1994) Mutations and altered expression of p16Ink4 in human cancer. Proc. Natl Acad. Sci. USA, 91, 11045-11049.
40. INK4 protein is restricted to the subset of lung cancer lines that retains wild type RB. Oncogene, 9, 3375-3378.
41. INK4/MTS1 tumour suppressor gene product. EMBO J., 14, 503-511.
42. Pines, J. (1993) Cyclins and cyclin-dependent kinases: take your partners. Trends Biochem. Sci., 18, 195-197.
43. Poeisz, B.J., Ruscetti, R.W., Gazdar, A.R. Bunn, P.A., Minna, J.D and Gallo, R.C. (1980) Detection and isolation of the C retrovirus from fresh and cultured lymphocytes of a patient with T cell lymphoma. Proc. Natl Acad. Sci. USA, 77, 7415-7419.
44. Quelle, D.E., Ashmun, R.A., Shurtleff, S.A., Kato, J., Bar-Sagi, D, Roussel, M.F. and Sherr, C.J. (1993) Overexpression of mouse D-type cyclins accelerates G1 phase in rodent fibroblasts. Genes Dev., 7, 1559-1571.
45. Resnitzky, D., Gossen, M., Bujard, H. and Reed, S.I. (1994) Acceleration of the G1 to S phase transition by expression of cyclins D1 and E with an inducible system. Mol. Cell. Biol., 14, 1669-1679.
46. Schmidt, E.E., Ichimura, K , Reifenberger, G. and Collins, V.P. (1994) CDKN2 (p16/MTS1) gene deletion or CDK4 amplification occurs in the majority of glioblastomas. Cancer Res., 54, 6321-6324.
47. Serrano, M., Hannon, G.J. and Beach, D. (1993) A new regulatory motif in cell-cycle control causing specific inhibition of cyclin D/CDK4. Nature, 366, 704-707.
48. Serrano, M., Gomez-Lahoz, E., DePinho, R.A., Beach, D. and Bar-Sagi, D. (1995) Inhibition of Ras-induced proliferation and cellular transformation by p16Ink4. Science, 267, 249-252.
49. Sheaff, R J. and Roberts, J.M. (1995) Tumor suppression. Lessons in p16 from phylum Falconium. Curr. Biol., 5, 28-31.
50. Sherr, C.J. (1994) G1 progression: cycling on cue. Cell, 79, 1059-1065.
51. Sherr, C.J. and Roberts, J.M. (1995) Inhibitors of mammalian G1 cyclin-dependent kinases. Genes Dev., 9, 1149-1163.
52. Smith, D.B. and Johnson, K.S. (1988) Single-step purification of polypeptides expressed in Escherichia coli as fusions with glutathione S-transferase. Gene, 67, 31-40.
53. Suzuki, T., Fujisawa, J.I., Toita, M. and Yoshida, M. (1993a) The trans-activator tax of human T-cell leukemia virus type 1 (HTLV-1) interacts with cAMP-responsive element (CRE) binding and CRE modulator proteins that bind to the 21-base-pair enhancer of HTLV-1. Proc. Natl Acad. Sci. USA, 90, 610-614.
54. Suzuki, T., Hirai, H., Fujisawa, J., Fujita, T. and Yoshida, M. (1993b) A trans-activator Tax of human T-cell leukemia virus type 1 binds to NF-κB p50 and serum response factor (SRF) and associates with enhancer DNAs of the NF-κB site and CArG box. Oncogene, 8, 2391-2397.
55. Suzuki, T., Hirai, H and Yoshida, M. (1994) Tax protein of HTLV-1 interacts with the Rel homology domain of NF-κB p65 and c-Rel proteins bound to the NH-κB binding site and activates transcription. Oncogene, 9, 3099-3105.
56. Suzuki, T, Hirai, H., Murakami, T. and Yoshida, M. (1995) Tax protein of HTLV-1 destabilizes the complexes of NF-κB and IκB-α and induces nuclear translocation of NF-κB for transcriptional activation. Oncogene, 10, 1199-1207.
57. Watanabe, M., Muramatsu, M., Hirai, H., Suzuki, T., Fujisawa, J., Yoshida, M., Arai, K. and Arai, N. (1993) HTLV-1 encoded Tax in association with NF-κB precursor p105 enhances nuclear localization of NF-κB p50 and p65 in transfected cells. Oncogene, 8, 2949-2958.
58. Whyte, P., Williamson, N.M. and Harlow, E. (1989) Cellular targets for transformation by the adenovirus E1A proteins. Cell, 56, 67-75
59. Yoshida, M. (1993) HTLV-1 Tax: regulation of gene expression and disease. Trends Microbiol., 1, 131-135.
60. Yoshida, M., Miyoshi, I and Hinuma, Y. (1982) Isolation and characterization of retrovirus from cell lines of human adult T-cell leukemia and its implication in the disease. Proc. Natl Acad. Sci. USA, 79, 2031-2035
61. Zhao, L.J. and Giam, C.Z. (1992) Human T-cell lymphotropic virus type I (HTLV-I) transcriptional activator, Tax, enhances CREB binding to HTLV-I 21-base-pair repeats by protein-protein interaction. Proc. Natl Acad. Sci. USA, 89, 7070-7074.