Human T-cell leukemia virus type 1 tax and cell cycle progression: Role of cyclin D-cdk and p110Rb

Molecular and Cellular Biology

Volumn 18, Issue 6, 1998, Pages 3620-3632

  Neuveut, Christine ^a   Low, Kenneth G ^b   Maldarelli, Frank ^a   Schmitt, Iris ^c   Majone, Franca ^d   Grassmann, Ralph ^c   Jeang, Kuan Teh ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY HOSPITAL ERLANGEN   (Germany)

^d UNIVERSITY OF PADOVA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE; PROTEIN P16; RETINOBLASTOMA PROTEIN; TAX PROTEIN; TRANSCRIPTION FACTOR E2F;

ARTICLE; CELL CYCLE; CELL DIFFERENTIATION; HUMAN; HUMAN CELL; HUMAN T CELL LEUKEMIA VIRUS 1; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; T LYMPHOCYTE;

ANIMALIA; DNA VIRUSES; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN T-LYMPHOTROPIC VIRUS 1;

EID: 0031814142     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.18.6.3620     Document Type: Article

References (93)

1. Alexandre, C., P. Charnay, and B. Verrier. 1991. Transactivation of Krox-20 and Krox-24 promoters by the HTLV-1 Tax protein through common regulatory elements. Oncogene 6:1851-1857.
2. Arnold, A., H. G. Kim, R. D. Gaz, R. L. Eddy, Y. Fukushima, M. G. Byers, T. B. Shows, and H. M. Kronenberg. 1989. Molecular cloning and chromosomal mapping of DNA rearranged with the parathyroid hormone gene in a parathyroid adenoma. J. Clin. Invest. 83:2034-2040.
3. Arroyo, M., S. Bagchi, and P. Raychaudhuri. 1993. Association of the human papillomavirus type 16 E7 protein with the S-phase-specific E2F-cyclin A complex. Mol. Cell. Biol. 13:6537-6546.
4. Ballard, D. W., E. Bohnlein, J. W. Lowenthal, Y. Wano, B. R. Franza, and W. C. Greene. 1988. HTLV-I tax induces cellular proteins that activate the kappa B element in the IL-2 receptor alpha gene. Science 241:1652-1655.
5. Boyer, S. N., D. E. Wazer, and V. Band. 1996. E7 protein of human papilloma virus-16 induces degradation of retinoblastoma protein through the ubiquitin-proteasome pathway. Cancer Res. 56:4620-4624.
6. Brady, J., K. T. Jeang, J. Duvall, and G. Khoury. 1987. Identification of p40x-responsive regulatory sequences within the human T-cell leukemia virus type I long terminal repeat. J. Virol. 61:2175-2181.
7. Brauweiler, A., J. E. Garrus, J. C. Reed, and J. K. Nyborg. 1997. Repression of bax gene expression by the HTLV-1 Tax protein: implications for suppression of apoptosis in virally infected cells. Virology 231:135-140.
8. Buckley, M. F., K. J. Sweeney, J. A. Hamilton, R. L. Sini, D. L. Manning, R. I. Nicholson, A. deFazio, C. K. Watts, E. A. Musgrove, and R. L. Sutherland. 1993. Expression and amplification of cyclin genes in human breast cancer. Oncogene 8:2127-2133.
9. Chan, F. K., J. Zhang, L. Cheng, D. N. Shapiro, and A. Winoto. 1995. Identification of human and mouse p19, a novel CDK4 and CDK6 inhibitor with homology to p16ink4. Mol. Cell. Biol. 15:2682-2688.
10. Chen, I. S., D. J. Slamon, J. D. Rosenblatt, N. P. Shah, S. G. Quan, and W. Wachsman. 1985. The x gene is essential for HTLV replication. Science 229:54-58.
11. DeCaprio, J. A., J. W. Ludlow, J. Figge, J. Y. Shew, C. M. Huang, W. H. Lee, E. Marsilio, E. Paucha, and D. M. Livingston. 1988. SV40 large tumor antigen forms a specific complex with the product of the retinoblastoma susceptibility gene. Cell 54:275-283.
12. DeGregori, J., G. Leone, K. Ohtani, A. Miron, and J. R. Nevins. 1995. E2F-1 accumulation bypasses a G1 arrest resulting from the inhibition of G1 cyclin-dependent kinase activity. Genes Dev. 9:2873-2887.
13. Diehl, J. A., F. Zindy, and C. J. Sherr. 1997. Inhibition of cyclin D1 phosphorylation on threonine-286 prevents its rapid degradation via the ubiquitin-proteasome pathway. Genes Dev. 11:957-972.
14. Dowdy, S. F., P. W. Hinds, K. Louie, S. I. Reed, A. Arnold, and R. A. Weinberg, 1993. Physical interaction of the retinoblastoma protein with human D cyclins. Cell 73:499-511.
15. Dyson, N., P. M. Howley, K. Munger, and E. Harlow. 1989. The human papilloma virus-16 E7 oncoprotein is able to bind to the retinoblastoma gene product. Science 243:934-937.
16. Earl, P. L., N. Cooper, and B. Moss. 1991. Preparation of cell culture and vaccinia virus stocks, p. 16.16.1-16.16.7. In F. M. Ausubel, R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl (ed.), Current protocols in molecular biology. Greene Publishing Associates and Wiley-Interscience, New York, N.Y.
17. Elroy-Stein, O., T. R. Fuerst, and B. Moss. 1989. Cap-independent translation of mRNA conferred by encephalomyocarditis virus 5′ sequence improves the performance of the vaccinia virus/bacteriophage T7 hybrid expression system. Proc. Natl. Acad. Sci. USA 86:6126-6130.
18. Elroy-Stein, O., and B. Moss. 1991. Gene expression using vaccinia/T7 RNA polymerase hybrid system, p. 16.19.1-16.19.9. In F. M. Ausubel, R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl (ed.), Current protocols in molecular biology. Greene Publishing Associates and Wiley-Interscience, New York, N.Y.
19. Erikson, J., J. Finan, Y. Tsujimoto, P. C. Nowell, and C. M. Croce. 1984. The chromosome 14 breakpoint in neoplastic B cells with the t(11;14) translocation involves the immunoglobulin heavy chain locus. Proc. Natl. Acad. Sci. USA 81:4144-4148.
20. Ewen, M. E., H. K. Sluss, C. J. Sherr, H. Matsushime, J. Kato, and D. M. Livingston. 1993. Functional interactions of the retinoblastoma protein with mammalian D-type cyclins. Cell 73:487-497.
21. Faha, B., E. Harlow, and E. Lees. 1993. The adenovirus E1A-associated kinase consists of cyclin E-p33cdk2 and cyclin A-p33cdk2. J. Virol. 67:2456-2465.
22. Felber, B. K., H. Paskalis, C. Kleinman-Ewing, F. Wong-Staal, and G. N. Pavlakis. 1985. The pX protein of HTLV-I is a transcriptional activator of its long terminal repeats. Science 229:675-679.
23. Franklin, A. A., and J. K. Nyborg. 1995. Mechanisms of Tax regulation of human T cell leukemia virus type I gene expression. J. Biomed. Sci. 2:17-29.
24. Fujii, M., T. Niki, T. Mori, T. Matsuda, M. Matsui, N. Nomura, and M. Seiki. 1991. HTLV-1 Tax induces expression of various immediate early serum responsive genes. Oncogene 6:1023-1029.
25. Fujii, M., P. Sassone-Corsi, and I. M. Verma. 1988. c-fos promoter trans-activation by the tax1 protein of human T-cell leukemia virus type I. Proc. Natl. Acad. Sci. USA 85:8526-3530.
26. Gorman, C. M., L. F. Moffat, and B. H. Howard. 1982. Recombinant genomes which express chloramphenicol acetyltransferase in mammalian cells. Mol. Cell. Biol. 2:1044-1051.
27. Grana, X., and E. P. Reddy. 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.
28. Grassmann, R., S. Berchtold, I. Radant, M. Alt, B. Fleckenstein, J. G. Sodroski, W. A. Haseltine, and U. Ramstedt. 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.
29. Grossman, W. J., J. T. Kimata, F. H. Wong, M. Zutter, T. J. Ley, and L. Ratner. 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.
30. Gu, W., J. W. Schneider, G. Condorelli, S. Kaushal, V. Mahdavi, and B. Nadal-Ginard. 1993. Interaction of myogenic factors and the retinoblastoma protein mediates muscle cell commitment and differentiation. Cell 72:309-324.
31. Guan, K. L., C. W. Jenkins, Y. Li, M. A. Nichols, X. Wu, C. L. O'Keefe, A. G. Matera, and Y. Xiong. 1994. Growth suppression by p18, a p16INK4/MTS1-and p14INK4B/MTS2-related CDK6 inhibitor, correlates with wild-type pRb function. Genes Dev. 8:2939-2952.
32. Hannon, G. J., and D. Beach. 1994. p15INK4B is a potential effector of TGF-beta-induced cell cycle arrest. Nature 371:257-261.
33. Hinds, P. W., and R. A. Weinberg. 1994. Tumor suppressor genes. Curr. Opin. Genet. Dev. 4:135-141.
34. Hirai, H., M. F. Roussel, J. Y. Kato, R. A. Ashmun, and C. J. Sherr. 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.
35. Hirama, T., and H. P. Koeffler. 1995. Role of the cyclin-dependent kinase inhibitors in the development of cancer. Blood 86:841-854.
36. Hollsberg, P., and D. A. Hafler. 1993. Seminars in medicine of the Beth Israel Hospital, Boston. Pathogenesis ot diseases induced by human lymphotropic virus type I infection. N. Engl. J. Med. 328:1173-1182.
37. Hunter, T., and J. Pines. 1994. Cyclins and cancer. II: cyclin D and CDK inhibitors come of age. Cell 79:573-582.
38. Inoue, J., M. Seiki, T. Taniguchi, S. Tsuru, and M. Yoshida. 1986. Induction of interleukin 2 receptor gene expression by p40x encoded by human T-cell leukemia virus type 1. EMBO J. 5:2883-2888.
39. Jeang, K. T., P. R. Shank, and A. Kumar. 1988. Transcriptional activation of homologous viral long terminal repeats by the human immunodeficiency virus type 1 or the human T-cell leukemia virus type I tat proteins occurs in the absence of de novo protein synthesis. Proc. Natl. Acad. Sci. USA 85: 8291-8295.
40. Jeang, K. T., S. G. Widen, O. J. Semmes IV, and S. H. Wilson. 1990. HTLV-I trans-activator protein, tax, is a trans-repressor of the human beta-polymerase gene. Science 247:1082-1084.
41. Jiang, W., S. M. Kahn, N. Tomita, Y. J. Zhang, S. H. Lu, and I. B. Weinstein. 1992. Amplification and expression of the human cyclin D gene in esophageal cancer. Cancer Res. 52:2980-2983.
42. Jin, D. Y., H. Teramoto, C. Z. Giam, R. F. Chun, J. S. Gutkind, and K. T. Jeang. 1997. A human suppressor of c-Jun N-terminal kinase 1 activation by tumor necrosis factor alpha. J. Biol. Chem. 272:25816-25823.
43. Johnson, D. G., J. K. Schwarz, W. D. Cress, and J. R. Nevins. 1993. Expression of transcription factor E2F1 induces quiescent cells to enter S phase. Nature 365:349-352.
44. 1 growth arrest pathway in cells expressing the human papillomavirus type 16 E7 oncoprotein. J. Virol. 71:2905-2912.
45. Kato, J., H. Matsushime, S. W. Hiebert, M. E. Ewen, and C. J. Sherr. 1993. Direct binding of cyclin D to the retinoblastoma gene product (pRb) and pRb phosphorylation by the cyclin D-dependent kinase CDK4. Genes Dev. 7:331-342.
46. Kato, J. Y., and C. J. Sherr. 1993. Inhibition of granulocyte differentiation by G1 cyclins D2 and D3 but not D1. Proc. Natl. Acad. Sci. USA 90:11513-11517.
47. Khatib, Z. A., H. Matsushime, M. Valentine, D. N. Shapiro, C. J. Sherr, and A. T. Look. 1993. Coamplification of the CDK4 gene with MDM2 and GLI in human sarcomas. Cancer Res. 53:5535-5541.
48. Lammie, G. A., and G. Peters. 1991. Chromosome 11q13 abnormalities in human cancer. Cancer Cells 3:413-420.
49. Low, K. G., L. F. Dorner, D. B. Fernando, J. Grossman, K. T. Jeang, and M. J. Comb. 1997. Human T-cell leukemia virus type 1 Tax releases cell cycle arrest induced by p161NK4a. J. Virol. 71:1956-1962.
50. Martelli, F., C. Cenciarelli, G. Santarelli, B. Polikar, A. Felsani, and M. Caruso. 1994. MyoD induces retinoblastoma gene expression during myogenic differentiation. Oncogene 9:3579-3590.
51. Matsushime, H., D. E. Quelle, S. A. Shurtleff, M. Shibuya, C. J. Sherr, and J. Y. Kato. 1994. D-type cyclin-dependent kinase activity in mammalian cells. Mol. Cell. Biol. 14:2066-2076.
52. Matsushime, H., M. F. Roussel, R. A. Ashmun, and C. J. Sherr. 1991. Colony-stimulating factor 1 regulates novel cyclins during the G1 phase of the cell cycle. Cell 65:701-713.
53. McIntyre, M. C., M. N. Ruesch, and L. A. Laimins. 1996. Human papillomavirus E7 oncoproteins bind a single form of cyclin E in a complex with cdk2 and p107. Virology 215:73-82.
54. Miyatake, S., M. Seik, M. Yoshida, and K. Arai. 1988. T-cell activation signals and human T-cell leukemia virus type I-encoded p40x protein activate the mouse granulocyte-macrophage colony-stimulating factor gene through a common DNA element. Mol. Cell. Biol. 8:5581-5587.
55. Morgan, D. O. 1995. Principles of CDK regulation. Nature 374:131-134.
56. Moss, B., O. Elroy-Stein, T. Mizukami, W. A. Alexander, and T. R. Fuerst. 1990. Product review. New mammalian expression vectors. Nature 348:91-92.
57. Motokura, T., T. Bloom, H. G. Kim, H. Juppner, J. V. Ruderman, H. M. Kronenberg, and A. Arnold. 1991. A novel cyclin encoded by a bc11-linked candidate oncogene. Nature 350:512-515.
58. Murray, A. 1994. Cell cycle checkpoints. Curr. Opin. Cell. Biol. 6:872-876.
59. Nerenberg, M., S. H. Hinrichs, R. K. Reynolds, G. Khoury, and G. Jay. 1987. The tat gene of human T-lymphotropic virus type 1 induces mesenchymal tumors in transgenic mice. Science 237:1324-1329.
60. Neuveut, C. Unpublished data.
61. Neuveut, C., D. Y. Jin, O. J. Semmes, F. Diella, R. Callahan, and K. T. Jeang. 1997. Divergent subcellular locations of HTLV-1 Tax and INT-6: a contrast between in vitro protein-protein binding and intracellular protein colocalizatron. J. Biomed. Sci. 4:229-234.
62. Nevins, J. R. 1992. E2F: a link between the Rb tumor suppressor protein and viral oncoproteins. Science 258:424-429.
63. Ohtani, K., M. Nakamura, S. Saito, K. Nagata, K. Sugamura, and Y. Hinuma. 1989. Electroporation: application to human lymphoid cell lines for stable introduction of a transactivator gene of human T-cell leukemia virus type I. Nucleic Acids Res. 17:1589-1604.
64. Peter, M., and I. Herskowitz. 1994. Joining the complex: cyclin-dependent kinase inhibitory proteins and the cell cycle. Cell 79:181-184.
65. Peters, G. 1994. The D-type cyclins and their role in tumorigenesis. J. Cell. Sci. Suppl. 18:89-96.
66. Pozzarti, R., J. Vogel, and G. Jay. 1990. The human T-lymphotropic virus type I tax gene can cooperate with the ras oncogene to induce neoplastic transformation of cells. Mol. Cell. Biol. 10:413-417.
67. Qin, X. Q., D. M. Livingston, W. Kaelin, Jr., and P. D. Adams. 1994 Deregulated transcription factor E2F-1 expression leads to S-phase entry and p53-mediated apoptosis. Proc. Natl. Acad. Sci. USA 91:10918-10922.
68. Rao, S. S., C. Chu, and D. S. Kohtz, 1994. Ectopic expression of cyclin D1 prevents activation of gene transcription by myogenic basic helix-loop-helix regulators. Mol. Cell. Biol. 14:5259-5267.
69. 1/S phase transition by expression of cyclins D1 and E with an inducible system. Mol. Cell. Biol. 14:1669-1679.
70. Ruben, S., H. Poteat, T. H. Tan, K. Kawakami, R. Roeder, W. Haseltine, and C. A. Rosen. 1988. Cellular transcription factors and regulation of IL-2 receptor gene expression by HTLV-I tax gene product. Science 241:89-92.
71. 1-to-S-phase transition in human lymphocytes by the human T-cell leukemia/lymphotropic virus type 1 Tax protein. J. Virol. 72:633-640.
72. -/- muscle cells. Science 264:1467-1471.
73. Semmes, O. J., J. F. Barret, C. V. Dang, and K. T. Jeang. 1996. Human T-cell leukemia virus type I tax masks c-Myc function through a cAMP-dependent pathway. J. Biol. Chem. 271:9730-9738.
74. Sherr, C. J. 1994. G1 phase progression: cycling on cue. Cell 79:551-555.
75. Sherr, C. J. 1995. D-type cyclins. Trends Biochem. Sci. 20:187-190.
76. Sherr, C. J., and J. M. Roberts. 1995. Inhibitors of mammalian G1 cyclin-dependent kinases. Genes Dev. 9:1149-1163.
77. Siekevitz, M., M. B. Feinberg, N. Holbrook, F. Wong-Staal, and W. C. Greene. 1987. Activation of interleukin 2 and interleukin 2 receptor (Tac) promoter expression by the trans-activator (tat) gene product of human T-cell leukemia virus, type I. Proc. Natl. Acad. Sci. USA 84:5389-5393.
78. Skapek, S. X., J. Rhee, D. B. Spicer, and A. B. Lassar. 1995. Inhibition of myogenic differentiation in proliferating myoblasts by cyclin D1-dependent kinase. Science 267:1022-1024.
79. Slansky, J. E., and P. J. Farnham. 1996. Introduction to the E2F family: protein structure and gene regulation. Curr. Top. Microbiol. Immunol. 208: 1-30.
80. Sodroski, J., C. Rosen, W. C. Goh, and W. Haseltine. 1985. A transcriptional activator protein encoded by the x-lor region of the human T-cell leukemia virus. Science 228:1430-1434.
81. Steiner, P., A. Philipp, J. Lukas, D. Godden-Kent, M. Pagano, S. Mittnacht, J. Bartek, and M. Eilers. 1995. Identification of a Myc-dependent step during the formation of active G1 cyclin-cdk complexes. EMBO J. 14:4814-4826.
82. Sugamora, K. Personal communication.
83. Suzuki, T., S. Kitao, H. Matsushime, and M. Yoshida. 1996. HTLV-1 Tax protein interacts with cyclin-dependent kinase inhibitor p16INK4A and counteracts its inhibitory activity towards CDK4. EMBO J. 15:1607-1614.
84. Tam, S. W., A. M. Theodoras, J. W. Shay, G. F. Draetta, and M. Pagano. 1994. Differential expression and regulation of cyclin D1 protein in normal and tumor human cells: association with Cdk4 is required for cyclin D1 function in G1 progression. Oncogene 9:2663-2674.
85. Tommasino, M., J. P. Adamczewski, F. Carlotti, C. F. Barth, R. Manetti, M. Contorni, F. Cavalieri, T. Hunt, and L. Crawford. 1993. HPV16 E7 protein associates with the protein kinase p33CDK2 and cyclin A. Oncogene 8:195-202.
86. Trihn, D., K. T. Jeang, and O. J. Semmes. 1997. HTLV-1 Tax and cytokeratin-Tax-expressing cells show morphological changes in keratin-containing cytoskeletal networks. J. Biomed. Sci. 4:47-53.
87. Tsujimoto, Y., J. Yunis, L. Onorato-Showe, J. Erikson, P. C. Nowell, and C. M. Croce. 1984. Molecular cloning of the chromosomal breakpoint of B-cell lymphomas and leukemias with the t(11;14) chromosome translocation. Science 224:1403-1406.
88. Uittenbogaard, M. N., H. A. Giebler, D. Reisman, and J. K. Nyborg. 1995. Transcriptional repression of p53 by human T-cell leukemia virus type I Tax protein. J. Biol. Chem. 270:28503-28506.
89. Wang, J., and B. Nadal-Ginard. 1995. Regulation of cyclins and p34CDC2 expression during terminal differentiation of C2C12 myocytes. Biochem. Biophys. Res. Commun. 206:82-88.
90. Weber, F., E. Meinl, K. Drexler, A. Czlonkowska, S. Huber, H. Fickenscher, I. Muller-Fleckenstein, B. Fleckenstein, H. Wekerle, and R. Hohlfeld. 1993. Transformation of human T-cell clones by herpesvirus saimiri: intact antigen recognition by autonomously growing myelin basic protein-specific T cells. Proc. Natl. Acad. Sci. USA 90:11049-11053.
91. Weinberg, R. A. 1996. E2F and cell proliferation: a world turned upside down. Cell 85:457-459.
92. Whyte, P., K. J. Buchkovich, J. M. Horowitz, S. H. Friend, M. Raybuck, R. A. Weinberg, and E. Harlow. 1988. Association between an oncogene and an anti-oncogene: the adenovirus E1A proteins bind to the retinoblastoma gene product. Nature 334:124-129.
93. Yoshida, M. 1993. HTLV-1 Tax: regulation of gene expression and disease. Trends Microbiol. 1:131-135.