Intersubunit disulfide isomerization controls membrane fusion of human T-cell leukemia virus Env

Journal of Virology

Volumn 82, Issue 14, 2008, Pages 7135-7143

  Li, Kejun ^a   Zhang, Shujing ^a   Kronqvist, Malin ^a   Wallin, Michael ^a   Ekström, Maria ^a   Derse, David ^b   Garoff, Henrik ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MUTANT PROTEIN; VIRUS ENVELOPE PROTEIN; VIRUS VECTOR; DISULFIDE; DITHIOTHREITOL; REDUCING AGENT;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DISULFIDE BOND; HUMAN T CELL LEUKEMIA VIRUS; ISOMERIZATION; MEMBRANE FUSION; MURINE LEUKEMIA VIRUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN MOTIF; AMINO ACID SUBSTITUTION; ANIMAL; CELL LINE; GENETICS; HAMSTER; HUMAN; HUMAN T CELL LEUKEMIA VIRUS 1; METABOLISM; MISSENSE MUTATION; PHYSIOLOGY; RAT; VIRUS ENTRY;

HUMAN IMMUNODEFICIENCY VIRUS; HUMAN T-LYMPHOTROPIC VIRUS 1; MURINE LEUKEMIA VIRUS; RATTUS;

AMINO ACID SUBSTITUTION; ANIMALS; CELL LINE; CRICETINAE; DISULFIDES; DITHIOTHREITOL; GENE PRODUCTS, ENV; HUMAN T-LYMPHOTROPIC VIRUS 1; HUMANS; MUTATION, MISSENSE; RATS; REDUCING AGENTS; VIRUS INTERNALIZATION;

EID: 47049126218     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00448-08     Document Type: Article

References (52)

1. Bae, Y., S. M. Kingsman, and A. J. Kingsman. 1997. Functional dissection of the Moloney murine leukemia virus envelope protein gp70. J. Virol. 71:2092-2099.
2. Barnett, A. L., and J. M. Cunningham. 2001. Receptor binding transforms the surface subunit of the mammalian C-type retrovirus envelope protein from an inhibitor to an activator of fusion. J. Virol. 75:9096-9105.
3. Barnett, A. L., R. A. Davey, and J. M. Cunningham. 2001. Modular organization of the Friend murine leukemia virus envelope protein underlies the mechanism of infection. Proc. Natl. Acad. Sci. USA 98:4113-4118.
4. Brighty, D. W., and S. R. Jassal. 2001. The synthetic peptide P-197 inhibits human T-cell leukemia virus type 1 envelope-mediated syncytium formation by a mechanism that is independent of Hsc70. J. Virol. 75:10472-10478.
5. Bullough, P. A., F. M. Hughson, J. J. Skehel, and D. C. Wiley. 1994. Structure of influenza haemagglutinin at the pH of membrane fusion. Nature 371:37-43.
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. Carr, C. M., C. Chaudhry, and P. S. Kim. 1997. Influenza hemagglutinin is spring-loaded by a metastable native conformation. Proc. Natl. Acad. Sci. USA 94:14306-14313.
8. Carrington, C. V., R. A. Weiss, and T. F. Schulz. 1994. A truncated HTLV-I envelope protein, lacking the hydrophobic membrane anchor domain, is associated with cellular membranes and virions. Virology 202:61-69.
9. Center, R. J., B. Kobe, K. A. Wilson, T. Teh, G. J. Hewlett, B. E. Kemp, and P. Poumbourios. 1998. Crystallization of a trimeric human T cell leukemia virus type 1 gp21 ectodomain fragment as a chimera with maltose-binding protein. Protein Sci. 7:1612-1619.
10. Derse, D., S. A. Hill, P. A. Lloyd, H. Chung, and B. A. Morse. 2001. Examining human T-lymphotropic virus type 1 infection and replication by cell-free infection with recombinant virus vectors. J. Virol. 75:8461-8468.
11. Fass, D., and P. S. Kim. 1995. Dissection of a retrovirus envelope protein reveals structural similarity to influenza hemagglutinin. Curr. Biol. 5:1377-1383.
12. Ferrari, D. M., and H. D. Soling. 1999. The protein disulphide-isomerase family: unravelling a string of folds. Biochem. J. 339:1-10.
13. 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.
14. Gu, J., S. Parthasarathi, A. Varela-Echavarria, Y. Ron, and J. P. Dougherty. 1995. Mutations of conserved cysteine residues in the CWLC motif of the oncoretrovirus SU protein affect maturation and translocation. Virology 206:885-893.
15. Hattori, S., T. Kiyokawa, K. Imagawa, F. Shimizu, E. Hashimura, M. Seiki, and M. Yoshida. 1984. Identification of gag and env gene products of human T-cell leukemia virus (HTLV). Virology 136:338-347.
16. Hoshino, H., M. Shimoyama, M. Miwa, and T. Sugimura. 1983. Detection of lymphocytes producing a human retrovirus associated with adult T-cell leukemia by syncytia induction assay. Proc. Natl. Acad. Sci. USA 80:7337-7341.
17. Hunter, E. 1997. Viral entry and receptors, p. 71-119. In J. M. Coffin, S. H. Hughes, and H. E. Varmus (ed.), Retroviruses. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
18. Jinno, A., Y. Haraguchi, H. Shiraki, and H. Hoshino. 1999. Inhibition of cell-free human T-cell leukemia virus type 1 infection at a postbinding step by the synthetic peptide derived from an ectodomain of the gp21 transmembrane glycoprotein. J. Virol. 73:9683-9689.
19. Jones, J. S., and R. Risser. 1993. Cell fusion induced by the murine leukemia virus envelope glycoprotein. J. Virol. 67:67-74.
20. 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.
21. 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.
22. Kobe, B., R. J. Center, B. E. Kemp, and P. Poumbourios. 1999. Crystal structure of human T cell leukemia virus type 1 gp21 ectodomain crystallized as a maltose-binding protein chimera reveals structural evolution of retroviral transmembrane proteins. Proc. Natl. Acad. Sci. USA 96:4319-4324.
23. Lavillette, D., B. Boson, S. J. Russell, and F. L. Cosset. 2001. Activation of membrane fusion by murine leukemia viruses is controlled in cis or in trans by interactions between the receptor-binding domain and a conserved disulfide loop of the carboxy terminus of the surface glycoprotein. J. Virol. 75:3685-3695.
24. Lavillette, D., M. Maurice, C. Roche, S. J. Russell, M. Sitbon, and F. L. Cosset. 1998. A proline-rich motif downstream of the receptor binding domain modulates conformation and fusogenicity of murine retroviral envelopes. J. Virol. 72:9955-9965.
25. Lavillette, D., A. Ruggieri, S. J. Russell, and F. L. Cosset. 2000. Activation of a cell entry pathway common to type C mammalian retroviruses by soluble envelope fragments. J. Virol. 74:295-304.
26. Leamnson, R. N., and M. S. Halpern. 1976. Subunit structure of the glycoprotein complex of avian tumor virus. J. Virol. 18:956-968.
27. Li, K., S. Zhang, M. Kronqvist, M. Ekström, M. Wallin, and H. Garoff. 2007. The conserved His8 of the Moloney murine leukemia virus Env SU subunit directs the activity of the SU-TM disulphide bond isomerase. Virology 361:149-160.
28. Li, K. J., and H. Garoff. 1996. Production of infectious recombinant Moloney murine leukemia virus particles in BHK cells using Semliki Forest virus-derived RNA expression vectors. Proc. Natl. Acad. Sci. USA 93:11658-11663.
29. Liljestrom, P., and H. Garoff. 1991. A new generation of animal cell expression vectors based on the Semliki Forest virus replicon. Biotechnology 9:1356-1361.
30. Maerz, A. L., R. J. Center, B. E. Kemp, B. Kobe, and P. Poumbourios. 2000. Functional implications of the human T-lymphotropic virus type 1 transmembrane glycoprotein helical hairpin structure. J. Virol. 74:6614-6621.
31. 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.
32. Mazurov, D., G. Heidecker, and D. Derse. 2006. HTLV-1 Gag protein associates with CD82 tetraspanin microdomains at the plasma membrane. Virology 346:194-204.
33. Miyamoto, K., N. Tomita, A. Ishii, T. Nishizaki, K. Kitajima, T. Tanaka, T. Nakamura, S. Watanabe, and T. Oda. 1984. Transformation of ATLA-negative leukocytes by blood components from anti-ATLA-positive donors in vitro. Int. J. Cancer 33:721-725.
34. Mothes, W., A. L. Boerger, S. Narayan, J. M. Cunningham, and J. A. Young. 2000. Retroviral entry mediated by receptor priming and low pH triggering of an envelope glycoprotein. Cell 103:679-689.
35. Nagy, K., P. Clapham, R. Cheingsong-Popov, and R. A. Weiss. 1983. Human T-cell leukemia virus type I: induction of syncytia and inhibition by patients' sera. Int. J. Cancer 32:321-328.
36. Opstelten, D. J., M. Wallin, and H. Garoff. 1998. Moloney murine leukemia virus envelope protein subunits, gp70 and Pr15E, form a stable disulfide-linked complex. J. Virol. 72:6537-6545.
37. Paine, E., R. Gu, and L. Ratner. 1994. Structure and expression of the human T-cell leukemia virus type 1 envelope protein. Virology 199:331-338.
38. Pinon, J. D., S. M. Kelly, N. C. Price, J. U. Flanagan, and D. W. Brighty. 2003. An antiviral peptide targets a coiled-coil domain of the human T-cell leukemia virus envelope glycoprotein. J. Virol. 77:3281-3290.
39. 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.
40. Pinter, A., R. Kopelman, Z. Li, S. C. Kayman, and D. A. Sanders. 1997. Localization of the labile disulfide bond between SU and TM of the murine leukemia virus envelope protein complex to a highly conserved CWLC motif in SU that resembles the active-site sequence of thiol-disulfide exchange enzymes. J. Virol. 71:8073-8077.
41. Popovic, M., P. S. Sarin, M. Robert-Gurroff, V. S. Kalyanaraman, D. Mann, J. Minowada, and R. C. Gallo. 1983. Isolation and transmission of human retrovirus (human T-cell leukemia virus). Science 219:856-859.
42. Rice, N. R., R. M. Stephens, D. Couez, J. Deschamps, R. Kettmann, A. Burny, and R. V. Gilden. 1984. The nucleotide sequence of the env gene and post-env region of bovine leukemia virus. Virology 138:82-93.
43. Schneider, J., N. Yamamoto, Y. Hinuma, and G. Hunsmann. 1984. Sera from adult T-cell leukemia patients react with envelope and core polypeptides of adult T-cell leukemia virus. Virology 132:1-11.
44. Seiki, M., S. Hattori, Y. Hirayama, and M. Yoshida. 1983. Human adult T-cell leukemia virus: complete nucleotide sequence of the provirus genome integrated in leukemia cell DNA. Proc. Natl. Acad. Sci. USA 80:3618-3622.
45. Seiki, M., T. Watanabe, A. Komuro, I. Miyoshi, M. Hayami, and M. Yoshida. 1984. Characterization of simian retrovirus genome related to human T-cell leukemia virus type I. Princess Takamatsu Symp. 15:241-249.
46. Skehel, J. J., and D. C. Wiley. 2000. Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin. Annu. Rev. Biochem. 69:531-569.
47. Smith, J. G., W. Mothes, S. C. Blacklow, and J. M. Cunningham. 2004. The mature avian leukosis virus subgroup A envelope glycoprotein is metastable, and refolding induced by the synergistic effects of receptor binding and low pH is coupled to infection. J. Virol. 78:1403-1410.
48. Wallin, M., M. Ekstrom, and H. Garoff. 2005. The fusion-controlling disulfide bond isomerase in retrovirus env is triggered by protein destabilization. J. Virol. 79:1678-1685.
49. Wallin, M., M. Ekstrom, and H. Garoff. 2004. Isomerization of the intersubunit disulphide-bond in Env controls retrovirus fusion. EMBO J. 23:54-65.
50. White, J., K. Matlin, and A. Helenius. 1981. Cell fusion by Semliki Forest, influenza, and vesicular stomatitis viruses. J. Cell Biol. 89:674-679.
51. Yamamoto, N., M. Okada, Y. Koyanagi, M. Kannagi, and Y. Hinuma. 1982. Transformation of human leukocytes by cocultivation with an adult T cell leukemia virus producer cell line. Science 217:737-739.
52. Zavorotinskaya, T., Z. Qian, J. Franks, and L. M. Albritton. 2004. A point mutation in the binding subunit of a retroviral envelope protein arrests virus entry at hemifusion. J. Virol. 78:473-481.