The receptor complex associated with human T-cell lymphotropic virus type 3 (HTLV-3) Env-mediated binding and entry is distinct from, but overlaps with, the receptor complexes of HTLV-1 and HTLV-2

Journal of Virology

Volumn 83, Issue 10, 2009, Pages 5244-5255

  Jones, Kathryn S ^a   Huang, Ying K ^b   Chevalier, Sébastien A ^c   Afonso, Philippe V ^c   Petrow Sadowski, Cari ^a   Bertolette, Daniel C ^b   Gessain, Antoine ^c   Ruscetti, Francis W ^b   Mahieux, Renaud ^c,d,e  

^a SAIC FREDERICK INC   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

^c INSTITUT PASTEUR   (France)

^d GEORGE WASHINGTON UNIVERSITY MEDICAL CENTER   (United States)

^e University Lyon i   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; CD8 ANTIGEN; GLUCOSE TRANSPORTER 1; NEUROPILIN 1; PROTEOHEPARAN SULFATE; VIRUS ENVELOPE PROTEIN; VIRUS GLYCOPROTEIN; VIRUS RECEPTOR; HUMAN T CELL LEUKEMIA VIRUS ANTIGEN;

ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL DEGENERATION; CELL MATURATION; CELL MEMBRANE PERMEABILITY; CELL MOTION; CONTROLLED STUDY; DRUG BINDING; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN T CELL LEUKEMIA VIRUS 1; HUMAN T CELL LEUKEMIA VIRUS 2; NONHUMAN; PLANT GROWTH; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; RETROVIRUS; STEM CELL; T LYMPHOCYTE; VIRUS ATTACHMENT; VIRUS ENTRY; VIRUS ENVELOPE; VIRUS TYPING; AMINO ACID SEQUENCE; CELL LINE; GENETIC TRANSDUCTION; GENETICS; HUMAN; METABOLISM; MOLECULAR GENETICS; PHYLOGENY; PHYSIOLOGY; SEQUENCE ALIGNMENT; VIROLOGY;

HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN T-LYMPHOTROPIC VIRUS 1; HUMAN T-LYMPHOTROPIC VIRUS 2; HUMAN T-LYMPHOTROPIC VIRUS 3;

AMINO ACID SEQUENCE; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE; DELTARETROVIRUS; DELTARETROVIRUS ANTIGENS; GENE PRODUCTS, ENV; GLUCOSE TRANSPORTER TYPE 1; HEPARAN SULFATE PROTEOGLYCANS; HUMANS; MOLECULAR SEQUENCE DATA; PHYLOGENY; PROTEIN BINDING; RECEPTORS, VIRUS; SEQUENCE ALIGNMENT; TRANSDUCTION, GENETIC; VIRUS ATTACHMENT;

EID: 65349156269     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02285-08     Document Type: Article

References (56)

1. Battini, J. L., J. M. Heard, and O. Danos. 1992. Receptor choice determinants in the envelope glycoproteins of amphotropic, xenotropic, and polytropic murine leukemia viruses. J. Virol. 66:1468-1475.
2. Battini, J. L., J. E. Rasko, and A. D. Miller. 1999. A human cell-surface receptor for xenotropic and polytropic murine leukemia viruses: possible role in G protein-coupled signal transduction. Proc. Natl. Acad. Sci. USA 96:1385-1390.
3. Boomer, S., M. Eiden, C. C. Burns, and J. Overbaugh. 1997. Three distinct envelope domains, variably present in subgroup B feline leukemia virus recombinants, mediate Pit1 and Pit2 receptor recognition. J. Virol. 71:8116-8123.
4. Bruder, D., M. Probst-Kepper, A. M. Westendorf, R. Geffers, S. Beissert, K. Loser, H. von Boehmer, J. Buer, and W. Hansen. 2004. Neuropilin-1: a surface marker of regulatory T cells. Eur. J. Immunol. 34:623-630.
5. Calattini, S., E. Betsem, S. Bassot, S. A. Chevalier, R. Mahieux, A. Froment, and A. Gessain. 1999. A new HTLV-3 strain in a Pygmy from Cameroon with a peculiar HTLV serology. J. Infect. Dis. 199:561-564.
6. Calattini, S., S. A. Chevalier, R. Duprez, P. Afonso, A. Froment, A. Gessain, and R. Mahieux. 2006. Human T-cell lymphotropic virus type 3: complete nucleotide sequence and characterization of the human tax3 protein. J. Virol. 80:9876-9888.
7. Calattini, S., S. A. Chevalier, R. Duprez, S. Bassot, A. Froment, R. Mahieux, and A. Gessain. 2005. Discovery of a new human T-cell lymphotropic virus (HTLV-3) in Central Africa. Retrovirology 2:30.
8. Chevalier, S. A., N. L. Ko, S. Calattini, A. Mallet, M. C. Prevost, K. Kehn, J. N. Brady, F. Kashanchi, A. Gessain, and R. Mahieux. 2008. Construction and characterization of a human T-cell lymphotropic virus type 3 infectious molecular clone. J. Virol. 82:6747-6752.
9. Chevalier, S. A., M. Walic, S. Calattini, A. Mallet, M. C. Prevost, A. Gessain, and R. Mahieux. 2007. Construction and characterization of a full-length infectious simian T-cell lymphotropic virus type 3 molecular clone. J. Virol. 81:6276-6285. (Pubitemid 46878034)
10. Davey, R. A., Y. Zuo, and J. M. Cunningham. 1999. Identification of a receptor-binding pocket on the envelope protein of Friend murine leukemia virus. J. Virol. 73:3758-3763. (Pubitemid 29189819)
11. Delamarre, L., A. R. Rosenberg, C. Pique, D. Pham, and M. C. Dokhelar. 1997. A novel human T-leukemia virus type 1 cell-to-cell transmission assay permits definition of SU glycoprotein amino acids important for infectivity. J. Virol. 71:259-266. (Pubitemid 26412287)
12. Dooneief, G., R. Marlink, K. Bell, K. Marder, B. Renjifo, Y. Stern, and R. Mayeux. 1996. Neurologic consequences of HTLV-II infection in injectiondrug users. Neurology 46:1556-1560.
13. 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.
14. Gemeniano, M., O. Mpanju, D. R. Salomon, M. V. Eiden, and C. A. Wilson. 2006. The infectivity and host range of the ecotropic porcine endogenous retrovirus, PERV-C, is modulated by residues in the C-terminal region of its surface envelope protein. Virology 346:108-117.
15. Gessain, A., F. Barin, J. C. Vernant, O. Gout, L. Maurs, A. Calender, and G. de The. 1985. Antibodies to human T-lymphotropic virus type-I in patients with tropical spastic paraparesis. Lancet ii:407-410. (Pubitemid 15231248)
16. Ghez, D., Y. Lepelletier, S. Lambert, J. M. Fourneau, V. Blot, S. Janvier, B. Arnulf, P. M. van Endert, N. Heveker, C. Pique, and O. Hermine. 2006. Neuropilin-1 is involved in human T-cell lymphotropic virus type 1 entry. J. Virol. 80:6844-6854. (Pubitemid 44025184)
17. Goubau, P., M. Van Brussel, A. M. Vandamme, H. F. Liu, and J. Desmyter. 1994. A primate T-lymphotropic virus, PTLV-L, different from human T-lymphotropic viruses types I and II, in a wild-caught baboon (Papio hamadryas). Proc. Natl. Acad. Sci. USA 91:2848-2852. (Pubitemid 24984857)
18. Heard, J. M., and O. Danos. 1991. An amino-terminal fragment of the Friend murine leukemia virus envelope glycoprotein binds the ecotropic receptor. J. Virol. 65:4026-4032.
19. Hishizawa, M., K. Imada, T. Kitawaki, M. Ueda, N. Kadowaki, and T. Uchiyama. 2004. Depletion and impaired interferon-alpha-producing capacity of blood plasmacytoid dendritic cells in human T-cell leukaemia virus type I-infected individuals. Br. J. Haematol. 125:568-575. (Pubitemid 38747958)
20. 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.
21. 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.
22. Jassal, S. R., R. G. Pohler, and D. W. Brighty. 2001. Human T-cell leukemia virus type 1 receptor expression among syncytium-resistant cell lines revealed by a novel surface glycoprotein-immunoadhesin. J. Virol. 75:8317-8328. (Pubitemid 32743704)
23. Jin, Q., L. Agrawal, Z. Vanhorn-Ali, and G. Alkhatib. 2006. GLUT-1-independent infection of the glioblastoma/astroglioma U87 cells by the human T cell leukemia virus type 1. Virology 353:99-110.
24. Johnston, E. R., L. M. Albritton, and K. Radke. 2002. Envelope proteins containing single amino acid substitutions support a structural model of the receptor-binding domain of bovine leukemia virus surface protein. J. Virol. 76:10861-10872. (Pubitemid 35176203)
25. Jones, K. S., S. Akel, C. Petrow-Sadowski, Y. Huang, D. C. Bertolette, and F. W. Ruscetti. 2005. Induction of human T cell leukemia virus type I receptors on quiescent naive T lymphocytes by TGF-beta. J. Immunol. 174:4262-4270. (Pubitemid 40396007)
26. Jones, K. S., K. Fugo, C. Petrow-Sadowski, Y. Huang, D. C. Bertolette, I. Lisinski, S. W. Cushman, S. Jacobson, and F. W. Ruscetti. 2006. Human T-cell leukemia virus type 1 (HTLV-1) and HTLV-2 use different receptor complexes to enter T cells. J. Virol. 80:8291-8302. (Pubitemid 44384843)
27. Jones, K. S., M. Nath, C. Petrow-Sadowski, A. C. Baines, M. Dambach, Y. Huang, and F. W. Ruscetti. 2002. Similar regulation of cell surface human T-cell leukemia virus type 1 (HTLV-1) surface binding proteins in cells highly and poorly transduced by HTLV-1-pseudotyped virions. J. Virol. 76:12723-12734. (Pubitemid 35386957)
28. + T cells. J. Virol. 79:12692-12702.
29. Jones, K. S., C. Petrow-Sadowski, Y. K. Huang, D. C. Bertolette, and F. W. Ruscetti. 2008. Cell-free HTLV-1 infects dendritic cells leading to transmission and transformation of CD4(+) T cells. Nat. Med. 14:429-436.
30. Kalyanaraman, V. S., M. G. Sarngadharan, M. Robert-Guroff, I. Miyoshi, 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.
31. Kim, F. J., N. Manel, E. N. Garrido, C. Valle, M. Sitbon, and J. L. Battini. 2004. HTLV-1 and -2 envelope SU subdomains and critical determinants in receptor binding. Retrovirology 1:41.
32. Kim, F. J., I. Seiliez, C. Denesvre, D. Lavillette, F. L. Cosset, and M. Sitbon. 2000. Definition of an amino-terminal domain of the human T-cell leukemia virus type 1 envelope surface unit that extends the fusogenic range of an ecotropic murine leukemia virus. J. Biol. Chem. 275:23417-23420. (Pubitemid 30624619)
33. Koyanagi, Y., Y. Itoyama, N. Nakamura, K. Takamatsu, J. Kira, T. Iwamasa, I. Goto, and N. Yamamoto. 1993. In vivo infection of human T-cell leukemia virus type I in non-T cells. Virology 196:25-33.
34. 165. Blood [Epub ahead of print.]
35. Liegeois, F., B. Lafay, W. M. Switzer, S. Locatelli, E. Mpoudi-Ngole, S. Loul, W. Heneine, E. Delaporte, and M. Peeters. 2008. Identification and molecular characterization of new STLV-1 and STLV-3 strains in wild-caught nonhuman primates in Cameroon. Virology 371:405-417.
36. Macatonia, S. E., J. K. Cruickshank, P. Rudge, and S. C. Knight. 1992. Dendritic cells from patients with tropical spastic paraparesis are infected with HTLV-1 and stimulate autologous lymphocyte proliferation. AIDS Res. Hum. Retrovir. 8:1699-1706.
37. Mahieux, R., and A. Gessain. 2008. The human HTLV-3 and HTLV-4 retroviruses: new members of the HTLV family. Pathol. Biol. (Paris) 57:161-166.
38. Mahieux, R., J. Pecon-Slattery, and A. Gessain. 1997. Molecular characterization and phylogenetic analyses of a new, highly divergent simian T-cell lymphotropic virus type 1 (STLV-1marc1) in Macaca arctoides. J. Virol. 71:6253-6258. (Pubitemid 27304975)
39. 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.
40. 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.
41. 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.
42. Osame, M., K. Usuku, S. Izumo, N. Ijichi, H. Amitani, A. Igata, M. Matsumoto, and M. Tara. 1986. HTLV-I associated myelopathy, a new clinical entity. Lancet i:1031-1032. (Pubitemid 16102987)
43. 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.
44. Pinon, J. D., P. J. Klasse, S. R. Jassal, S. Welson, J. Weber, D. W. Brighty, and Q. J. Sattentau. 2003. Human T-cell leukemia virus type 1 envelope glycoprotein gp46 interacts with cell surface heparan sulfate proteoglycans. J. Virol. 77:9922-9930. (Pubitemid 37122073)
45. Poiesz, B. J., F. W. Ruscetti, A. F. Gazdar, P. A. Bunn, J. D. Minna, and R. C. Gallo. 1980. 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 77:7415-7419.
46. 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.
47. Rosenberg, A. R., L. Delamarre, A. Preira, and M. C. Dokhelar. 1998. Analysis of functional conservation in the surface and transmembrane glycoprotein subunits of human T-cell leukemia virus type 1 (HTLV-1) and HTLV-2. J. Virol. 72:7609-7614. (Pubitemid 28377897)
48. Sarris, M., K. G. Andersen, F. Randow, L. Mayr, and A. G. Betz. 2008. Neuropilin-1 expression on regulatory T cells enhances their interactions with dendritic cells during antigen recognition. Immunity 28:402-413.
49. Takenouchi, N., K. S. Jones, I. Lisinski, K. Fugo, K. Yao, S. W. Cushman, F. W. Ruscetti, and S. Jacobson. 2007. GLUT1 is not the primary binding receptor but is associated with cell-to-cell transmission of human T-cell leukemia virus type 1. J. Virol. 81:1506-1510. (Pubitemid 46167872)
50. Vander Kooi, C. W., M. A. Jusino, B. Perman, D. B. Neau, H. D. Bellamy, and D. J. Leahy. 2007. Structural basis for ligand and heparin binding to neuropilin B domains. Proc. Natl. Acad. Sci. USA 104:6152-6157.
51. Van Dooren, S., L. Meertens, P. Lemey, A. Gessain, and A. M. Vandamme. 2005. Full-genome analysis of a highly divergent simian T-cell lymphotropic virus type 1 strain in Macaca arctoides. J. Gen. Virol. 86:1953-1959. (Pubitemid 40916378)
52. von Wronski, M. A., N. Raju, R. Pillai, N. J. Bogdan, E. R. Marinelli, P. Nanjappan, K. Ramalingam, T. Arunachalam, S. Eaton, K. E. Linder, F. Yan, S. Pochon, M. F. Tweedle, and A. D. Nunn. 2006. Tuftsin binds neuropilin- 1 through a sequence similar to that encoded by exon 8 of vascular endothelial growth factor. J. Biol. Chem. 281:5702-5710. (Pubitemid 43847668)
53. Wolfe, N. D., W. Heneine, J. K. Carr, A. D. Garcia, V. Shanmugam, U. Tamoufe, J. N. Torimiro, A. T. Prosser, M. Lebreton, E. Mpoudi-Ngole, F. E. McCutchan, D. L. Birx, T. M. Folks, D. S. Burke, and W. M. Switzer. 2005. Emergence of unique primate T-lymphotropic viruses among central African bushmeat hunters. Proc. Natl. Acad. Sci. USA 102:7994-7999.
54. Xie, L., and P. L. Green. 2005. 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. J. Virol. 79:14536-14545. (Pubitemid 41636252)
55. Yoshida, M., I. Miyoshi, and Y. Hinuma. 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.
56. Zhang, Y., J. C. Rassa, M. E. deObaldia, L. M. Albritton, and S. R. Ross. 2003. Identification of the receptor binding domain of the mouse mammary tumor virus envelope protein. J. Virol. 77:10468-10478.