Kinetic analyses of the surface-transmembrane disulfide bond isomerization-controlled fusion activation pathway in moloney murine leukemia virus

Journal of Virology

Volumn 79, Issue 22, 2005, Pages 13856-13864

  Wallin, Michael ^a   Löving, Robin ^a   Ekström, Maria ^a   Li, Kejun ^a   Garoff, Henrik ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTEINE; ENVELOPE PROTEIN; THIOL;

ALKYLATION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING KINETICS; CONTROLLED STUDY; DISSOCIATION; DISULFIDE BOND; GENE FUSION; ISOMERIZATION; MEMBRANE FUSION; MOLONEY LEUKEMIA ONCOVIRUS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN MOTIF; RECEPTOR BINDING; VIRUS ACTIVATION; VIRUS ENVELOPE;

3T3 CELLS; ANIMALS; BINDING SITES; CYSTEINE; DISULFIDES; ISOMERISM; KINETICS; MICE; MOLONEY MURINE LEUKEMIA VIRUS; RECEPTORS, VIRUS; VIRAL ENVELOPE PROTEINS; VIRAL FUSION PROTEINS;

ANIMALIA; MOLONEY MURINE LEUKEMIA VIRUS;

EID: 27644493609     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.79.22.13856-13864.2005     Document Type: Article

References (48)

1. Blumenthal, R., D. P. Sarkar, S. Durell, D. E. Howard, and S. J. Morris. 1996. Dilation of the influenza hemagglutinin fusion pore revealed by the kinetics of individual cell-cell fusion events. J. Cell Biol. 135:63-71.
2. 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.
3. 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.
4. 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.
5. Chan, D. C., D. Fass, J. M. Berger, and P. S. Kim. 1997. Core structure of gp41 from the HIV envelope glycoprotein. Cell 89:263-273.
6. Chen, B., E. M. Vogan, H. Gong, J. J. Skehel, D. C. Wiley, and S. C. Harrison. 2005. Structure of an unliganded simian immunodeficiency virus gp120 core. Nature 433:834-841.
7. Chernomordik, L. V., and M. M. Kozlov. 2003. Protein-lipid interplay in fusion and fission of biological membranes. Annu. Rev. Biochem. 72:175-207.
8. Chernomordik, L. V., E. Leikina, V. Frolov, P. Bronk, and J. Zimmerberg. 1997. An early stage of membrane fusion mediated by the low pH conformation of influenza hemagglutinin depends upon membrane lipids. J. Cell Biol. 136:81-93.
9. Danieli, T., S. L. Pelletier, Y. I. Henis, and J. M. White. 1996. Membrane fusion mediated by the influenza virus hemagglutinin requires the concerted action of at least three hemagglutinin trimers. J. Cell Biol. 133:559-569.
10. Earp, L. J., S. E. Delos, R. C. Netter, P. Bates, and J. M. White. 2003. The avian retrovirus avian sarcoma/leukosis virus subtype A reaches the lipid mixing stage of fusion at neutral pH. J. Virol. 77:3058-3066.
11. Fass, D., S. C. Harrison, and P. S. Kim. 1996. Retrovirus envelope domain at 1.7 angstrom resolution. Nat. Struct. Biol 3:465-469.
12. Forster, F., O. Medalia, N. Zauberman, W. Baumeister, and D. Fass. 2005. Retrovirus envelope protein complex structure in situ studied by cryo-electron tomography. Proc. Natl. Acad. Sci. USA 102:4729-4734.
13. Hernandez, L. D., R. J. Peters, S. E. Delos, J. A. Young, D. A. Agard, and J. M. White. 1997. Activation of a retroviral membrane fusion protein: soluble receptor-induced liposome binding of the ALSV envelope glycoprotein. J. Cell Biol. 139:1455-1464.
14. 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, N.Y.
15. Jiang, S., K. Lin, N. Strick, and A. R. Neurath. 1993. HIV-1 inhibition by a peptide. Nature 365:113.
16. 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.
17. Kemble, G. W., T. Danieli, J. M. White, Y. I. Henis, D. L. Bodian, J. Rose, and I. A. Wilson. 1994. Lipid-anchored influenza hemagglutinin promotes hemifusion, not complete fusion. Cell 76:383-391.
18. Klement, V., W. P. Rowe, J. W. Hartley, and W. E. Pugh. 1969. Mixed culture cytopathogenicity: a new test for growth of murine leukemia viruses in tissue culture. Proc. Natl. Acad. Sci. USA 63:753-758.
19. 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.
20. Leamnson, R. N., and M. S. Halpern. 1976. Subunit structure of the glycoprotein complex of avian tumor virus. J. Virol. 18:956-968.
21. Leikina, E., C. Ramos, I. Markovic, J. Zimmerberg, and L. V. Chernomordik. 2002. Reversible stages of the low-pH-triggered conformational change in influenza virus hemagglutinin. EMBO J. 21:5701-5710.
22. Maeda, T., K. Kawasaki, and S. Ohnishi. 1981. Interaction of influenza virus hemagglutinin with target membrane lipids is a key step in virus-induced hemolysis and fusion at pH 5.2. Proc. Natl. Acad. Sci. USA 78:4133-4137.
23. Markosyan, R. M., P. Bates, F. S. Cohen, and G. B. Melikyan. 2004. A study of low pH-induced refolding of Env of avian sarcoma and leukosis virus into a six-helix bundle. Biophys. J. 87:3291-3298.
24. Markosyan, R. M., F. S. Cohen, and G. B. Melikyan. 2003. HIV-1 envelope proteins complete their folding into six-helix bundles immediately after fusion pore formation. Mol. Biol. Cell. 14:926-938.
25. Markovic, I., E. Leikina, M. Zhukovsky, J. Zimmerberg, and L. V. Chernomordik. 2001. Synchronized activation and refolding of influenza hemagglutinin in multimeric fusion machines. J. Cell Biol. 155:833-844.
26. Matsuyama, S., S. E. Delos, and J. M. White. 2004. Sequential roles of receptor binding and low pH in forming prehairpin and hairpin conformations of a retroviral envelope glycoprotein. J. Virol. 78:8201-8209.
27. Melikyan, G. B., R. J. Barnard, R. M. Markosyan, J. A. Young, and F. S. Cohen. 2004. Low pH is required for avian sarcoma and leukosis virus Env-induced hemifusion and fusion pore formation but not for pore growth. J. Virol. 78:3753-3762.
28. Melikyan, G. B., S. A. Brener, D. C. Ok, and F. S. Cohen. 1997. Inner but not outer membrane leaflets control the transition from glycosylphosphatidylinositol-anchored influenza hemagglutinin-induced hemifusion to full fusion. J. Cell Biol. 136:995-1005.
29. Melikyan, G. B., R. M. Markosyan, S. A. Brener, Y. Rozenberg, and F. S. Cohen. 2000. Role of the cytoplasmic tail of ecotropic Moloney murine leukemia virus Env protein in fusion pore formation. J. Virol. 74:447-455.
30. Melikyan, G. B., R. M. Markosyan, H. Hemmati, M. K. Delmedico, D. M. Lambert, and F. S. Cohen. 2000. Evidence that the transition of HIV-1 gp41 into a six-helix bundle, not the bundle configuration, induces membrane fusion. J. Cell Biol 151:413-423.
31. 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.
32. Netter, R. C., S. M. Amberg, J. W. Balliet, M. J. Biscone, A. Vermeulen, L. J. Earp, J. M. White, and P. Bates. 2004. Heptad repeat 2-based peptides inhibit avian sarcoma and leukosis virus subgroup a infection and identify a fusion intermediate. J. Virol. 78:13430-13439.
33. 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.
34. 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.
35. Pizzato, M., S. A. Marlow, E. D. Blair, and Y. Takeuchi. 1999. Initial binding of murine leukemia virus particles to cells does not require specific Env-receptor interaction. J. Virol. 73:8599-8611.
36. Portis, J. L., F. J. McAtee, and L. H. Evans. 1985. Infectious entry of murine retroviruses into mouse cells: evidence of a postadsorption step inhibited by acidic pH. J. Virol. 55:806-812.
37. Qiao, H., R. T. Armstrong, G. B. Melikyan, F. S. Cohen, and J. M. White. 1999. A specific point mutant at position 1 of the influenza hemagglutinin fusion peptide displays a hemifusion phenotype. Mol. Biol. Cell. 10:2759-2769.
38. Sattentau, Q. J., and J. P. Moore. 1991. Conformational changes induced in the human immunodeficiency virus envelope glycoprotein by soluble CD4 binding. J. Exp. Med. 174:407-415.
39. 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.
40. 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.
41. 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.
42. Wallin, M., M. Ekstrom, and H. Garoff. 2004. Isomerization of the intersubunit disulphide-bond in Env controls retrovirus fusion. EMBO J. 23:54-65.
43. Weissenhorn, W., A. Dessen, S. C. Harrison, J. J. Skehel, and D. C. Wiley. 1997. Atomic structure of the ectodomain from HIV-1 gp41. Nature 387: 426-430.
44. White, J., K. Matlin, and A. Helenius. 1981. Cell fusion by Semliki Forest, influenza, and vesicular stomatitis viruses. J. Cell Biol. 89:674-679.
45. Wild, C. T., D. C. Shugars, T. K. Greenwell, C. B. McDanal, and T. J. Matthews. 1994. Peptides corresponding to a predictive alpha-helical domain of human immunodeficiency virus type 1 gp41 are potent inhibitors of virus infection. Proc. Natl. Acad. Sci. USA 91:9770-9774.
46. Wilson, I. A., J. J. Skehel, and D. C. Wiley. 1981. Structure of the haemagglutinin membrane glycoprotein of influenza virus at 3 Å resolution. Nature 289:366-373.
47. Zarling, D. A., and I. Keshet. 1979. Fusion activity of virions of murine leukemia virus. Virology 95:185-196.
48. 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.