1887

Abstract

Several alterations in the mechanism of cell cycle control have been observed in human T-lymphotropic virus type I (HTLV-I)-infected cells. Here, it is reported that HTLV-I-infected cells both in their immortalized and transformed phase do not undergo apoptosis following ionizing radiation (IR) treatment. However, when IL-2 withdrawal is combined with genotoxic stress, HTLV-I-infected T-cells in their immortalized phase (IL-2-dependent) undergo apoptosis where as their transformed counterparts (IL-2-independent) do not. These results suggest that, during the transformation process, the HTLV-I-infected T-cells become less sensitive to cell death signals through the acquisition of constitutive activation of the IL-2 receptor pathway. The expression of bcl-2 and bcl-XL proteins, which are known to increase cell survival mediated by IL-2, as well as of p21waf1 and p53, was not substantially different in immortalized and transformed cells following IR. All together, these findings suggest that activation of alternative anti-apoptotic pathways, regulated by IL-2, might be responsible for the differential cell death response observed in immortalized versus transformed HTLV-I-infected T-cells.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-80-7-1575
1999-07-01
2024-04-26
Loading full text...

Full text loading...

/deliver/fulltext/jgv/80/7/0801575a.html?itemId=/content/journal/jgv/10.1099/0022-1317-80-7-1575&mimeType=html&fmt=ahah

References

  1. Akagi T., Shimotohno K. 1993; Proliferative response of Tax1-transduced primary human T-cells to anti-CD3 antibody stimulation by an interleukin-2-independent pathway. Journal of Virology 67:1211–1217
    [Google Scholar]
  2. Akagi T., Ono H., Tsuchida N., Shimotohno K. 1997; Aberrant expression and function of p53 in T-cells immortalized by HTLV-I Tax 1. FEBS Letters 406:263–266
    [Google Scholar]
  3. Boise L. H., Minn A. J., June C. H., Lindsten T., Thompson C. B. 1995; Growth factors can enhance lymphocyte survival without committing the cell to undergo cell division. Proceedings of the National Academy of Sciences, USA 92:5491–5495
    [Google Scholar]
  4. Cereseto A., Diella F., Cara A., Mulloy J. C., Grassman R., Franchini G., Klotman M.E. 1996; p53 functional impairment and high p21waf1/cip1 expression in human T-cell lymphotropic/leukemia virus type (HTLV-I) transformed T-cell. Blood 88:1551–1560
    [Google Scholar]
  5. Cereseto A., Washington Parks R., 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 (in press)
    [Google Scholar]
  6. Collins M., Marvel J., Malde P., Lopez-Rivas A. 1992; Interleukin 3 protects murine bone marrow cells from apoptosis induced by DNA damaging agents. Journal of Experimental Medicine 176:1043–1051
    [Google Scholar]
  7. De Rossi A., Aldovini A., Franchini G., Mann D., Gallo R. C., Wong Staal F. 1985; Clonal selection of T lymphocytes infected by cell-free human T-cell leukemia/lymphoma virus type 1: parameters of virus integration and expression. Virology 143:640–645
    [Google Scholar]
  8. Firpo E. J., Koff A., Solomon M. J., Roberts J. M. 1994; Inactivation of a Cdk2 inhibitor during interleukin 2-induced proliferation of human T lymphocytes. Molecular and Cellular Biology 14:4889–4901
    [Google Scholar]
  9. Franchini G. 1995; Molecular mechanisms of human T-cell leukemia/lymphotropic virus type I infection. Blood 86:3619–3639
    [Google Scholar]
  10. Franchini G., Mann D. L., Popovic M., Zicht R. R., Gallo R. C., Wong-Staal F. 1985; HTLV-I infection of T and B cells of a patient with adult T-cell leukemia-lymphoma (ATLL) and transmission of HTLV-I from B cells to normal T-cells. Leukemia Research 9:1305–1314
    [Google Scholar]
  11. Franchini G., Cereseto A., Tryniszewska E., Rivadeneira E., Kislyakova T., Mulloy J. C., Takemoto S., Casareto L., Nicot C., Trovato R. 1999; Telomerase activation, rearrangement, and inhibition of cell-cycle inhibitors in human T-cells immortalized or transformed by HTLV-I. In HTLV-I Pathogenesis Charlottesville: University of Virginia Press;
    [Google Scholar]
  12. Gallo R. C. 1986; The first human retrovirus. Scientific American 255:88–98
    [Google Scholar]
  13. Grassman R., Dengler C., Muller-Fleckenstein I., Fleckenstein B., McGuire K., Dokhelar M. C., Sodroski J. G., Haseltine W. A. 1989; Transformation to continuous growth of primary human T-lymphocytes by human T-cell leukemia virus type I X-region genes transduced by herpesvirus saimiri vector. Proceedings of the National Academy of Sciences, USA 86:3351–3355
    [Google Scholar]
  14. Hahn B., Gallo R. C., Franchini G., Popovic M., Aoki T., Salahuddin S. Z., Markham P. D., Wong-Staal F. 1984; Clonal selection of human T-cell leukemia virus-infected cells in vivo and in vitro. Molecular Biology and Medicine 2:29–36
    [Google Scholar]
  15. Hinuma Y., Nagata K., Hanaoka M., Nakai M., Matsumoto T., Kinoshita K. I., Shirakawa S., Miyoshi I. 1981; Adult T-cell leukemia antigen in an ATL cell line and detection of antibodies to the antigen in human sera. Proceedings ofthe National Academy ofSciences, USA 78:6476–6480
    [Google Scholar]
  16. Jin D. Y., Spencer F., Jeang K. T. 1998; Human T-cell leukemia virus type 1 oncoprotein Tax targets the human mitotic checkpoint protein MAD1. Cell 93:1–20
    [Google Scholar]
  17. Levkau B., Koyama H., Raines E. W., Clurman B. E., Herren B., Orth K., Roberts J. M., Ross R. 1998; Cleavage of p21c1p1/waf1 and p27k1p1 mediates apoptosis in endothelial cells through activation of cdk2: role of a caspase cascade. Molecular Cell 1:553–563
    [Google Scholar]
  18. Low K. G., Dorner L. F., Fernando D. B., Grossman J., Jeang K.-T., Comb M. J. 1997; Human T-cell leukemia virus type 1 tax releases cell cycle arrest induced by p16INK4a. Journal of Virology 71:1956–1962
    [Google Scholar]
  19. Markham P. D., Salahuddin S. Z., Kalyanaraman V. S., Popovic M., Sarin P., Gallo R. C. 1983; Infection and transformation of fresh human umbilical cord blood cells by multiple sources of human T-cell leukemia-lymphoma virus (HTLV). International Journal of Cancer 31:413–420
    [Google Scholar]
  20. Migone T. S., Lin J. X., Cereseto A., Mulloy J. C., O’Shea J. J., Franchini G., Leonard W. J. 1995; Constitutively activated JAK-STAT pathway in T-cells transformed with HTLV-I. Science 269:79–81
    [Google Scholar]
  21. Migone T. S., Cacalano N. A., Taylor N., Yi T., Waldmann T. A., Johnston J. A. 1998; Recruitment of SH2-containing protein tyrosine phosphatase SHP-1 to the interleukin 2 receptor; loss ofSHP-1 expression in human T-lymphotropic virus type I-transformed T cells. Proceedings of the National Academy of Sciences, USA 95:3845–3850
    [Google Scholar]
  22. Miyoshi I., Kubonishi I., Yoshimoto S., Akagi T., Ohtsuki Y., Shiraishi Y., Nagata K., Hinuma Y. 1981; Type C virus particles in a cord T-cell line derived by co-cultivating normal human cord leukocytes and human leukaemic T-cells. Nature 294:770–771
    [Google Scholar]
  23. Mor F., Cohen I. R. 1996; IL-2 rescues antigen-specific T cells from radiation or dexamethasone-induced apoptosis. Correlation with induction of bcl-2. Journal of Immunology 156:515–522
    [Google Scholar]
  24. Mulloy J. C., Kislyakova T., Cereseto A., Casareto L., Lo Monico A., Fullen J., Lorenzi M. V., Cara A., Nicot C., Giam C. Z., Franchini G. 1998; Human T-cell lymphotropic/leukemia virus type 1 Tax abrogates p53-induced cell cycle arrest and apoptosis through its CREB/ATL functional domain. Journal of Virology 72:8852–8860
    [Google Scholar]
  25. Murphy E. L., Hanchard B., Figueroa J. P., Gibbs W. N., Lofters W. S., Campbell M., Goedert J. J., Blattner W. A. 1989; Modeling the risk of adult T-cell leukemia/lymphoma in persons infected with human T-lymphotropic virus type I. International Journal of Cancer 43:250–253
    [Google Scholar]
  26. Nourse J., Firpo E., Flanagan W. M., Coats S., Polyak K., Lee M. H., Massague J., Crabtree G. R., Roberts J. M. 1994; Interleukin-2-mediated elimination of p27K1p1 cyclin-dependent kinase inhibitor prevented by rapamycin. Nature 372:570–573
    [Google Scholar]
  27. Patchen M. L., MacVittie T. J., Williams J. L., Schwartz G. N., Souza L. M. 1991; Administration of interleukin-6 stimulates multilineage hematopoiesis and accelerates recovery from radiation-induced hematopoietic depression. Blood 77:472–480
    [Google Scholar]
  28. Pise-Masison C. A., Choi K.-S., Radonovich M., Dittmer J., Kim S.-J., Brady J. N. 1998a; Inhibition of p53 transactivation function by the human T-cell lymphotropic virus type 1 Tax protein. Journal of Virology 72:1165–1170
    [Google Scholar]
  29. Pise-Masison C. A., Radonovich M., Sakaguchi K., Appella E., Brady J. N. 1998b; Phosphorylation of p53: a novel pathway for p53 inactivation in human T-cell lymphotropic virus type 1-transformed cells. Journal of Virology 72:6348–6355
    [Google Scholar]
  30. Poiesz B. J., Ruscetti F. W., Gazdar A. F., Bunn P. A., Minna J. D., Gallo R. C. 1980; Detection and isolation of type C retrovirus particles from fresh and cultured lymphocytes of a patient with cutaneous T-cell lymphoma. Proceedings of the National Academy of Sciences, USA 77:7415–7419
    [Google Scholar]
  31. Popovic M., Lange-Wantzin G., Sarin P. S., Mann D., Gallo R. C. 1983; Transformation of human umbilical cord blood T-cells by human T-cell leukemia/lymphoma virus. Proceedings of the National Academy of Sciences, USA 80:5402–5406
    [Google Scholar]
  32. Sachs L., Lotem J. 1993; Control of programmed cell death in normal andleukemic cells:newimplications for therapy. Blood 82:15–21
    [Google Scholar]
  33. Seki H., Iwai K., Kanegane H., Konno A., Ohta K., Ohta K., Yachie A., Taniguchi N., Miyawaki T. 1995; Differential protective action of cytokines on radiation-induced apoptosis of peripheral lymphocyte subpopulation. Cellular Immunology 163:30–36
    [Google Scholar]
  34. Sherr C. J., Roberts J. M. 1995; Inhibitors of mammalian G1 cyclin-dependent kinases. Genes and Development 9:1149–1163
    [Google Scholar]
  35. Suzuki T., Kitao S., Matsushime H., Yoshida M. 1996; HTLV-1 Tax protein interacts with cyclin-dependent kinase inhibitor p16lNK4A and counteracts its inhibitory activity towards CDK4. European Molecular Biology Organization Journal 15:1607–1614
    [Google Scholar]
  36. Takemoto S., Mulloy J. C., Cereseto A., Migone T. S., Patel B. K. R., Matsuoka M., Yamaguchi K., Takatsuki K., Kamihira S., White J. D., Leonard W. J., Waldmann T., Franchini G. 1997; Proliferation of adult T-cell leukemia/lymphoma cells is associated with the constitutive activation of JAK/STAT proteins. Proceedings of the National Academy of Sciences, USA 94:13897–13902
    [Google Scholar]
  37. Wattel E., Vartanian J. P., Pannetier C., Wain-Hobson S. 1995; Clonal expansion of human T-cell leukemia virus type I-infected cells in asymptomatic and symptomatic carriers without malignancy. Journal of Virology 69:2863–2868
    [Google Scholar]
  38. Xu X., Kang S. H., Heidenreich O., Okerholm M., O’Shea J. J., Nerenberg M. I. 1995; Constitutive activation of different Jak tyrosine kinases in human T-cell leukemia virus type 1 (HTLV-1) tax protein or virus-transformed cells. Journal of Clinical Investigation 961548–1555
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-80-7-1575
Loading
/content/journal/jgv/10.1099/0022-1317-80-7-1575
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error