Envelope is a major viral determinant of the distinct in vitro cellular transformation tropism of human T-cell leukemia virus type 1 (HTLV-1) and HTLV-2

Journal of Virology

Volumn 79, Issue 23, 2005, Pages 14536-14545

  Xie, Li ^a   Green, Patrick L ^a,b  

^a OHIO STATE UNIVERSITY   (United States)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; CD8 ANTIGEN; GAG PROTEIN; INTERLEUKIN 2; PROTEIN P19; REX PROTEIN; TAX PROTEIN; VIRUS ENVELOPE PROTEIN;

ARTICLE; CELL TRANSFORMATION; CELL TYPE; CONTROLLED STUDY; DISEASE ASSOCIATION; EMBRYO; HUMAN; HUMAN CELL; HUMAN T CELL LEUKEMIA VIRUS 1; HUMAN T CELL LEUKEMIA VIRUS 2; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN FUNCTION; RETROVIRUS; T LYMPHOCYTE; VIRUS ENVELOPE; VIRUS INFECTION; VIRUS RECOMBINANT; VIRUS STRAIN; WILD TYPE;

CD4-POSITIVE T-LYMPHOCYTES; CELL TRANSFORMATION, VIRAL; CELLS, CULTURED; GENE PRODUCTS, ENV; HUMAN T-LYMPHOTROPIC VIRUS 1; HUMAN T-LYMPHOTROPIC VIRUS 2; HUMANS; RECOMBINATION, GENETIC; TERMINAL REPEAT SEQUENCES;

HTLV; HUMAN T-LYMPHOTROPIC VIRUS 1; HUMAN T-LYMPHOTROPIC VIRUS 2;

EID: 27744464429     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.79.23.14536-14545.2005     Document Type: Article

References (77)

1. Akagi, T., Y. Hoshida, T. Yoshino, N. Teramoto, E. Kondo, K. Hayashi, and K. Takahashi. 1992. Infectivity of human T-lymphotropic virus type I to human nervous tissue cells in vitro. Acta Neuropathol. (Berlin) 84:147-152.
2. Arni, S., S. Ilangumaran, G. van Echten-Decfcert, K. Sandhoff, M. Poincelet, A. Briol, E. Rungger-Brandle, and D. C. Hoessli. 1996. Differential regulation of Src-family protein tyrosine kinases in GPI domains of T lymphocyte plasma membranes. Biochem. Biophys. Res. Commun. 225:801-807.
3. Boral, A. L., S. A. Okenquist, and J. Lenz. 1989. Identification of the SL3-3 virus enhancer core as a T-lymphoma cell-specific element. J. Virol. 63:76-84.
4. Cann, A. J., Y. Koyanagi, and I. S. Y. Chen. 1988. High efficiency transfection of primary human lymphocytes and studies of gene expression. Oncogene 3:123-128.
5. Chatis, P. A., C. A. Holland, J. W. Hartley, W. P. Rowe, and N. Hopkins. 1983. Role for the 3′ end of the genome in determining disease specificity of Friend and Moloney murine leukemia viruses. Proc. Natl. Acad. Sci. USA 80:4408-4411.
6. Chatis, P. A., C. A. Holland, J. E. Silver, T. N. Fredrickson, and N. Hopkins. 1984. A 3′ end fragment encompassing the transcriptional enhancers of nondefective Friend virus confers erythroleukemogenicity of Moloney leukemia virus. J. Virol. 52:248-254.
7. Chen, I. Y., J. McLaughlin, J. C. Gasson, S. C. Clark, and D. W. Golde. 1983. Molecular characterization of genome of a novel human T-cell leukaemia virus. Nature 305:502-505.
8. Cinek, T., and V. Horejsi. 1992. The nature of large noncovalent complexes containing glycosyl-phosphatidylinositol-anchored membrane glycoproteins and protein tyrosine kinases. J. Immunol. 149:2262-2270.
9. Clarke, M. F., E. P. Gelmann, and M. S. Reitz, Jr. 1983. Homology of human T-cell leukaemia virus envelope gene with class I HLA gene. Nature 305:60-62.
10. Collins, N. D., G. C. Newbound, B. Albrecht, J. Beard, L. Ratner, and M. D. Lairmore. 1998. Selective ablation of human T-cell lymphotropic virus type 1 p12I reduces viral infectivity in vivo. Blood 91:4701-4707.
11. Coskun, A. K., and R. E. Sutton. 2005. Expression of glucose transporter 1 confers susceptibility to human T-cell leukemia virus envelope-mediated fusion. J. Virol. 79:4150-4158.
12. Daenke, S., S. A. McCracken, and S. Booth. 1999. Human T-cell leukaemia/lymphoma virus type 1 syncytium formation is regulated in a cell-specific manner by ICAM-1, ICAM-3 and VCAM-1 and can be inhibited by antibodies to integrin beta2 or beta7. J. Gen. Virol. 80:1429-1436.
13. Datta, S., N. H. Kothari, and H. Fan. 2000. In vivo genomic footprinting of the human T-cell leukemia virus type 1 (HTLV-1) long terminal repeat enhancer sequences in HTLV-1-infected human T-cell lines with different levels of Tax 1 activity. J. Virol. 74:8277-8285.
14. Doms, R. W. 2000. Beyond receptor expression: the influence of receptor conformation, density, and affinity in HIV-1 infection. Virology 276:229-237.
15. Duc Dodon, M., A. Bernard, and L. Gazzolo. 1989. Peripheral T-lymphocyte activation by human T-cell leukemia virus type 1 interferes with the CD2 but not with the CD3/TCR pathway. J. Virol. 63:5413-5419.
16. Edinger, A. L., A. Amedee, K. Miller, B. J. Doranz, M. Endres, M. Sharron, M. Samson, Z. H. Lu, J. E. Clements, M. Murphey-Corb, S. C. Peiper, M. Parmentier, C. C. Broder, and R. W. Doms. 1997. Differential utilization of CCR5 by macrophage and T cell tropic simian immunodeficiency virus strains. Proc. Natl. Acad. Sci. USA 94:4005-4010.
17. 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.
18. Feuer, G., and P. L. Green. 2005. Comparative biology of human T-cell lymphotropic virus type 1 (HTLV-1) and HTLV-2. Oncogene 24:5996-6004.
19. Fujisawa, J., M. Seiki, T. Kiyokawa, and M. Yoshida. 1985. Functional activation of the long terminal repeat of human T-cell leukemia virus type I by a trans-acting factor. Proc. Natl. Acad. Sci. USA 82:2277-2281.
20. Fukudome, K., M. Furuse, T. Imai, M. Nishimura, S. Takagi, Y. Hinuma, and O. Yoshie. 1992. Identification of membrane antigen C33 recognized by monoclonal antibodies inhibitory to human T-cell leukemia virus type 1 (HTLV-1)-induced syncytium formation: altered glycosylation of C33 antigen in HTLV-1-positive T cells. J. Virol. 66:1394-1401.
21. Gazzolo, L., and M. Duc Dodon. 1987. Direct activation of resting T lymphocytes by human T-lymphotropic virus type I. Nature 326:714-717.
22. Green, P. L., and I. S. Y. Chen. 1994. Molecular features of the human T-cell leukemia virus: mechanisms of transformation and leukemogenicity, p. 227-311. In J. A Levy (ed.), The Retroviridae, vol. 3. Plenum Press, New York, N.Y.
23. Green, P. L., and I. S. Y. Chen. 2001. Human T-cell leukemia virus types 1 and 2, p. 1941-1969. In D. M. Knipe, P. Howley, D. Griffin, R. Lamb, M. Martin, and S. Straus (ed.), Virology, 4th ed. Lippincott Williams & Wilkins, Philidelphia, Pa.
24. Green, P. L., T. M. Ross, I. S. Y. Chen, and S, Pettiford. 1995. Human T-cell leukemia virus type II nucleotide sequences between env and the last exon of tax/rex are not required for viral replication or cellular transformation. J. Virol. 69:387-394.
25. Gwynn, S. R., F. C. Hankenson, A. S. Lauring, J. L. Rohn, and J. Overbaugh. 2000. Feline leukemia virus envelope sequences that affect T-cell tropism and syncytium formation are not part of known receptor-binding domains. J. Virol. 74:5754-5761.
26. Hattori, T., T. Uchiyama, T. Toibana, K. Takatsuki, and H. Uchino. 1981. Surface phenotype of Japanese adult T-cell leukemia cells characterized by monoclonal antibodies. Blood 58:645-647.
27. Hildreth, J. E., A. Subramanium, and R. A. Hampton. 1997. Human T-cell lymphotropic virus type 1 (HTLV-1)-induced syncytium formation mediated by vascular cell adhesion molecule-1: evidence for involvement of cell adhesion molecules in HTLV-1 biology. J. Virol. 71:1173-1180.
28. Hjelle, B., O. Appenzeller, R. Mills, S. Alexander, N. Torrez-Martinez, R. Jahnke, and G. Ross. 1992. Chronic neurodegenerative disease associated with HTLV-II infection. Lancet 339:645-646.
29. Ho, D. D., T. R. Rota, and M. S. Hirsch. 1984. Infection of human endothelial cells by human T-lymphotropic virus type I. Proc. Natl. Acad. Sci. USA 81:7588-7590.
30. Hoffman, P. M., S. Dhib-Jalbut, J. A. Mikovits, D. S. Robbins, A. L. Wolf, G. K. Bergey, N. C. Lohrey, O. S. Weislow, and F. W. Ruscetti. 1984. Human T-cell leukemia virus type I infection of monocytes and microglial cells in primary human cultures. Proc. Natl. Acad. Sci. USA 89:11784-11788.
31. Hoxie, J. A., D. M. Matthews, and D. B. Cines. 1984. Infection of human endothelial cells by human T-cell leukemia virus type I. Proc. Natl. Acad. Sci. USA 81:7591-7595.
32. Ijichi, S., M. B. Ramundo, H. Takahashi, and W. W. Hall. 1992. In vivo cellular tropism of human T-cell leukemia virus type II (HTLV-II). J Exp. Med. 176:293-296.
33. Janes, P. W., S. C. Ley, A. I. Magee, and P. S. Kabouridis. 2000. The role of lipid rafts in T cell antigen receptor (TCR) signalling. Semin. Immunol. 12:23-34.
34. Kalyanaraman, V. S., M. G. Sarngadharan, M. Robert-Guroff, I. Miyoshi, D. Blayney, D. Golde, and R. C. Gallo. 1982. A new subtype of human T-cell leukemia virus (HTLV-II) associated with a T-cell variant of hairy cell leukemia. Science 218:571-573.
35. Kehn, K., R. Berro, C. de la Fuente, K. Strouss, E. Ghedin, S. Dadgar, M. E. Bottazzi, A. Pumfery, and F. Kashanchi. 2004. Mechanisms of HTLV-1 transformation. Front. Biosci. 9:2347-2372.
36. Kimata, J. T., T. J. Palker, and L. Ratner. 1993. The mitogenic activity of human T-cell leukemia virus type I is T-cell associated and requires the CD2/LFA-3 activation pathway. J. Virol. 67:3134-3141.
37. Kimata, J. T., and L. Ratner. 1991. Temporal regulation of viral and cellular gene expression during human T-lymphotropic virus type I-mediated lymphocyte immortalization. J. Virol. 65:4398-41407.
38. Kimata, J. T., F. H. Wong, J. J. Wang, and L. Ratner. 1994. Construction and characterization of infectious human T-cell leukemia virus type I molecular clones. Virology 204:656-664.
39. Kohtz, D. S., A. Altman, J. D. Kohtz, and S. Puszkin. 1988. Immunological and structural homology between human T-cell leukemia virus type I envelope glycoprotein and a region of human interleukin-2 implicated in binding the beta receptor. J. Virol. 62:659-662.
40. Lairmore, M. D., R. B. Lai, and P. T. Kaumaya. 1995. Evaluation of immunodominant epitopes of human T-lymphotropic virus type 1 (HTLV-I) using synthetic peptides. Biomed. Pept. Proteins Nucleic Acids 1:117-122.
41. + cells. Virology 210:441-447.
42. Li, Y., E. Golemis, J. W. Hartley, and N. Hopkins. 1987. Disease specificity of nondefective Friend and Moloney murine leukemia viruses is controlled by a small number of nucleotides. J. Virol. 61:693-700.
43. Maeda, N., W. Fu, A. Ortin, M. de las Heras, and H. Fan. 2005. Roles of the Ras-MEK-mitogen-activated protein kinase and phosphatidylinositol 3-kinase-Akt-mTOR pathways in Jaagsiekte sheep retrovirus-induced transformation of rodent fibroblast and epithelial cell lines. J. Virol. 79:4440-4450.
44. Maeda, N., M. Palmarini, C. Murgia, and H. Fan. 2001. Direct transformation of rodent fibroblasts by jaagsiekte sheep retrovirus DNA. Proc. Natl. Acad. Sci. USA 98:4449-4454.
45. Manel, N., F. J. Kim, S. Kinet, N. Taylor, M. Sitbon, and J. L. Battini. 2003. The ubiquitous glucose transporter GLUT-1 is a receptor for HTLV. Cell 115:449-459.
46. Manel, N., S. Kinet, J. L. Battini, F. J. Kim, N. Taylor, and M. Sitbon. 2003. The HTLV receptor is an early T-cell activation marker whose expression requires de novo protein synthesis. Blood 101:1913-1918.
47. Manel, N., N. Taylor, S. Kinet, F. J. Kim, L. Swainson, M. Lavanva, J. L. Battini, and M. Sitbon. 2004. HTLV envelopes and their receptor GLUT1, the ubiquitous glucose transporter: a new vision on HTLV infection? Front. Biosci. 9:3218-3241.
48. Moore, J. P., A. Trkola, and T. Dragic. 1997. Co-receptors for HIV-1 entry. Curr. Opin. Immunol. 9:551-562.
49. Nagai, M., M. B. Brennan, J. A. Sakai, C. A. Mora, and S. Jacobson. 2001. CD8(+) T cells are an in vivo reservoir for human T-cell lymphotropic virus type I. Blood 98:1858-1861.
50. Nath, M. D., F. W. Ruscetti, C. Petrow-Sadowski, and K. S. Jones. 2003. Regulation of the cell-surface expression of an HTLV-I binding protein in human T cells during immune activation. Blood 101:3085-3092.
51. + T lymphocytes. J. Virol. 70:2101-2106.
52. Nishigaki, K., D. Thompson, C. Hanson, T. Yugawa, and S. Ruscetti. 2001. The envelope glycoprotein of Friend spleen focus-forming virus covalently interacts with and constitutively activates a truncated form of the receptor tyrosine kinase Stk. J. Virol. 75:7893-7903.
53. Niyogi, K., and J. E. Hildreth. 2001. Characterization of new syncytium-inhibiting monoclonal antibodies implicates lipid rafts in human T-cell leukemia virus type 1 syncytium formation. J. Virol. 75:7351-7361.
54. Oliff, A., K. Signorelli, and L. Collins. 1984. The envelope gene and long terminal repeat sequences contribute to the pathogenic phenotype of helper-independent Friend viruses. J. Virol. 51:788-794.
55. Persaud, D., J. L. Munoz, S. L. Tarsis, E. S. Parks, and W. P. Parks. 1995. Time course and cytokine dependence of human T-cell lymphotropic virus type 1 T-lymphocyte transformation as revealed by a microtiter infectivity assay. J. Virol. 69:6297-6303.
56. Poon, B., and I. S. Y. Chen. 1998. Identification of a domain within the human T-cell leukemia virus type 2 envelope required for syncytium induction and replication. J. Virol. 72:1959-1966.
57. Richardson, J. H., A. J. Edwards, J. K. Cruickshank, P. Rudge, and A. G. Dalgleish. 1990. In vivo cellular tropism of human T-cell leukemia virus type 1. J. Virol. 64:5682-5687.
58. Richardson, J. H., P. Hollsberg, A. Windhagen, L. A. Child, D. A. Hafler, and A. M. Lever. 1997. Variable immortalizing potential and frequent virus latency in blood-derived T-cell clones infected with human T-cell leukemia virus type I. Blood 89:3303-3314.
59. + T-lymphocytes by human T-cell leukemia virus type 1 Tax mutants expressed in a functional molecular clone. J. Virol. 73:4856-4865.
60. Rosenblatt, J. D., D. W. Golde, W. Wachsman, A. Jacobs, G. Schmidt, S. Quan, J. C. Gasson, and I. S. Y. Chen. 1986. A second HTLV-II isolate associated with atypical hairy-cell leukemia. N. Engl. J. Med. 315:372-377.
61. Ross, T. M., M. Narayan, Z. Y. Fang, A. C. Minella, and P. L. Green. 2000. Tax transactivation of both NFκB and CREB/ATF is essential for human T-cell leukemia virus type 2-mediated transformation of primary human T cells. J. Virol. 74:2655-2662.
62. Ross, T. M., S. M. Pettiford, and P. L. Green. 1996. The tax gene of human T-cell leukemia virus type 2 is essential for transformation of human T lymphocytes. J. Virol. 70:5194-5202.
63. Rulli, K., T. Yugawa, C. Hanson, D. Thompson, S. Ruscetti, and K. Nishigaki. 2004. Ex vivo and in vivo biological effects of a truncated form of the receptor tyrosine kinase Stk when activated by interaction with the Friend spleen focus-forming virus envelope glycoprotein or by point mutation. J. Virol. 78:4573-4581.
64. Sagara, Y., C. Ishida, Y. Inoue, H. Shiraki, and Y. Maeda. 1998. 71-Kilodalton heat shock cognate protein acts as a cellular receptor for syncytium formation induced by human T-cell lymphotropic virus type 1. J. Virol. 72:535-541.
65. Silver, J. E., and T. N. Fredrickson. 1983. A new gene that controls the type of leukemia induced by Friend murine leukemia virus. J. Exp. Med. 158:493-505.
66. Simons, K., and E. Ikonen. 1997. Functional rafts in cell membranes. Nature 387:569-572.
67. Sommerfelt, M. A., B. P. Williams, P. R. Clapham, E. Solomon, P. N. Goodfellow, and R. A. Weiss. 1988. Human T cell leukemia viruses use a receptor determined by human chromosome 17. Science 242:1557-1559.
68. Sutton, R. E., and D. R. Littman. 1996. Broad host range of human T-cell leukemia virus type 1 demonstrated with an improved pseudotyping system. J. Virol. 70:7322-7326.
69. Trejo, S. R., and L. Ratner. 2000. The HTLV receptor is a widely expressed protein. Virology 268:41-48.
70. Viard, M., I. Parolini, M. Sargiacomo, K. Fecchi, C. Kamoni, S. Ablan, F. W. Ruscetti, J. M. Wang, and R. Blumenthal. 2002. Role of cholesterol in human immunodeficiency virus type 1 envelope protein-mediated fusion with host cells. J. Virol. 76:11584-11595.
71. Wang, T.-G., J. Ye, M. Lairmore, and P. L. Green. 2000. In vitro cellular tropism of human T-cell leukemia virus type 2. AIDS Res. Hum. Retroviruses 16:1661-1668.
72. Wielgosz, M. M., D. A. Rauch, K. S. Jones, F. W. Ruscetti, and L. Ratner. 2005. Cholesterol dependence of HTLV-1 infection. AIDS Res. Hum. Retroviruses 21:43-50.
73. Wycuff, D. R., and S. J. Marriott. 2005. The HTLV-1 Tax oncoprotein: hypertasking at the molecular level. Front. Biosci. 10:620-642.
74. Yamada, Y. 1983. Phenotypic and functional analysis of leukemic cells from 16 patients with adult T-cell leukemia/lymphoma. Blood 61: 192-199.
75. Yamada, Y., S. Kamihira, T. Amagasaki, K. Kinoshita, M. Kusano, S. Chiyoda, E. Yawo, S. Ikeda, J. Suzuyama, and M. Ichimaru. 1985. Adult T cell leukemia with atypical surface phenotypes: clinical correlation. J. Clin. Oncol. 3:782-788.
76. Ye, J., L. Xie, and P. L. Green. 2003. Tax and overlapping Rex sequences do not confer the distinct transformation tropisms of HTLV-1 and HTLV-2. J. Virol. 77:7728-7735.
77. Yoshida, M. 2001. Multiple viral strategies of HTLV-1 for dysregulation of cell growth control. Annu. Rev. Immunol. 19:475-496.