Sequential roles of receptor binding and low pH in forming prehairpin and hairpin conformations of a retroviral envelope glycoprotein

Journal of Virology

Volumn 78, Issue 15, 2004, Pages 8201-8209

  Matsuyama, Shutoku ^a,c   Delos, Sue Ellen ^a   White, Judith M ^a,b  

^a UNIVERSITY OF VIRGINIA   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CHLORPROMAZINE; LYSOPHOSPHATIDYLCHOLINE; VIRUS ENVELOPE PROTEIN; VIRUS FUSION PROTEIN;

ARTICLE; AVIAN SARCOMA VIRUS; CONTROLLED STUDY; HIGH TEMPERATURE; LEUKEMIA VIRUS; NONHUMAN; PH; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FOLDING; RECEPTOR BINDING; RETROVIRUS; VIRION; VIRUS ENVELOPE; WESTERN BLOTTING;

GENE PRODUCTS, ENV; HYDROGEN-ION CONCENTRATION; MEMBRANE FUSION; PROTEIN CONFORMATION; PROTEIN SUBUNITS; RECEPTORS, VIRUS; RETROVIRIDAE; RETROVIRIDAE PROTEINS; TEMPERATURE;

EID: 3242713988     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.78.15.8201-8209.2004     Document Type: Article

References (63)

1. Aguilar, H. C., W. F. Anderson, and P. M. Cannon. 2003. Cytoplasmic tail of Moloney murine leukemia virus envelope protein influences the conformation of the extracellular domain: implications for mechanism of action of the R peptide. J. Virol. 77:1281-1291.
2. Bates, P., J. A. T. Young, and H. E. Varmus. 1993. A receptor for subgroup A Rous sarcoma virus is related to the low density lipoprotein receptor. Cell 74:1043-1051.
3. Bayer, N., D. Schober, E. Prchla, R. F. Murphy, D. Blaas, and R. Fuchs. 1998. Effect of bafilomycin A1 and nocodazole on endocytic transport in HeLa cells: implications for viral uncoating and infection. J. Virol. 72:9645-9655.
4. 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.
5. Bobkova, M., J. Stitz, M. Engelstadter, K. Cichutek, and C. J. Buchholz. 2002. Identification of R-peptides in envelope proteins of C-type retroviruses. J. Gen. Virol. 83:2241-2246.
6. Bosch, B. J., R. van der Zee, C. A. de Haan, and P. J. Rottier. 2003. The coronavirus spike protein is a class I virus fusion protein: structural and functional characterization of the fusion core complex. J. Virol. 77:8801-8811.
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. Chazal, N., G. Singer, C. Aiken, M.-L. Hammarskjold, and D. Rekosh. 2001. Human immunodeficiency virus type 1 particles pseudotyped with envelope proteins that fuse at low pH no longer require Nef for optimal infectivity. J. Virol. 75:4014-4018.
9. Chernomordik, L. V., and M. M. Kozlov. 2003. Protein-lipid interplay in fusion and fission of biological membranes. Annu. Rev. Biochem. 72:175-207.
10. +-, GTP-, and pH-dependent fusion of biological membranes. FEBS Lett. 318:71-76.
11. Clague, M. J., S. Urbe, F. Aniento, and J. Gruenberg. 1994. Vacuolar ATPase activity is required for endosomal carrier vesicle formation. J. Biol. Chem. 269:21-24.
12. Colman, P. M., and M. C. Lawrence. 2003. The structural biology of type I viral membrane fusion. Nat. Rev. Mol. Cell. Biol. 4:309-319.
13. Daniell, 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.
14. Delos, S. E., and J. M. White. 2000. Critical role for the cysteines flanking the internal fusion peptide of avian sarcoma/leukosis virus envelope glycoprotein. J. Virol. 74:9738-9741.
15. Diaz-Griffero, F., S. A. Hoschander, and J. Brojatsch. 2002. Endocytosis is a critical step in entry of subgroup B avian leukosis viruses. J. Virol. 76:12866-12876.
16. Dutch, R. E., S. B. Joshi, and R. A. Lamb. 1998. Membrane fusion promoted by increasing surface densities of the paramyxovirus F and HN proteins: comparison of fusion reactions mediated by simian virus 5 F, human parainfluenza virus type 3 F, and influenza virus HA. J. Virol. 72:7745-7753.
17. Dutch, R. E., and R. A. Lamb. 2001. Deletion of the cytoplasmic tail of the fusion protein of the paramyxovirus simian virus 5 affects fusion pore enlargement. J. Virol. 75:5363-5369.
18. Earp, L. E., 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.
19. Earp, L. J., S. E. Delos, H. E. Park, and J. M. White. The many mechanisms of viral membrane fusion proteins. In M. Marsh (ed.), Current topics in microbiology and immunology. Membrane trafficking in viral replication, in press. Springer Verlag, New York, N.Y.
20. Eckert, D. M., and P. S. Kim. 2001. Mechanisms of viral membrane fusion and its inhibition. Annu. Rev. Biochem. 70:777-810.
21. Edwards, T. G., S. Wyss, J. D. Reeves, S. Zolla-Pazner, J. A. Hoxie, R. W. Doms, and F. Baribaud. 2002. Truncation of the cytoplasmic domain induces exposure of conserved regions in the ectodomain of human immunodeficiency virus type 1 envelope protein. J. Virol. 76:2683-2691.
22. Furuta, R. A., C. T. Wild, Y. Weng, and C. D. Weiss. 1998. Capture of an early fusion-active conformation of HIV-1 gp41. Nat. Struct. Biol. 5:276-279.
23. Gallagher, T. M., C. Escarmis, and M. J. Buchmeier. 1991. Alteration of the pH dependence of coronavirus-induced cell fusion: effect of mutations in the spike glycoprotein. J. Virol. 65:1916-1928.
24. Gallaher, W. R. 1996. Similar structural models of the transmembrane proteins of Ebola and avian sarcoma viruses. Cell 85:477-478.
25. Gilbert, J., D. Mason, and J. White. 1990. Fusion of Rous sarcoma virus with host cells does not require low pH. J. Virol. 64:5106-5113.
26. Gilbert, J. M., L. D. Hernandez, J. W. Balliet, P. Bates, and J. M. White. 1995. Receptor-induced conformational changes in the subgroup A avian leukosis and sarcoma virus envelope glycoprotein. J. Virol. 69:7410-7415.
27. Gunther-Ausborn, S., A. Praetor, and T. Stegmann. 1995. Inhibition of influenza-induced membrane fusion by lysophosphatidylcholine. J. Biol. Chem. 270:29279-29285.
28. Hernandez, L. D., R. R. Peters, S. E. Delos, J. A. T. 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.
29. Hernandez, L. D., and J. M. White. 1998. Mutational analysis of the candidate internal fusion peptide of the avian leukosis and sarcoma virus subgroup A envelope glycoprotein. J. Virol. 72:3259-3267.
30. Kim, F. J., N. Manel, Y. Boublik, J. L. Battini, and M. Sitbon. 2003. Human T-cell leukemia virus type 1 envelope-mediated syncytium formation can be activated in resistant mammalian cell lines by a carboxy-terminal truncation of the envelope cytoplasmic domain. J. Virol. 77:963-969.
31. Kozerski, C., E. Ponimaskin, B. Schroth-Diez, M. F. Schmidt, and A. Herrmann. 2000. Modification of the cytoplasmic domain of influenza virus hemagglutinin affects enlargement of the fusion pore. J. Virol. 74:7529-7537.
32. Lakadamyali, M., M. J. Rust, H. P. Babcock, and X. Zhuang. 2003. Visualizing infection of individual influenza viruses. Proc. Natl. Acad. Sci. USA 100:9280-9285.
33. Leikina, E., and L. V. Chernomordik. 2000. Reversible merger of membranes at the early stage of influenza hemagglutinin-mediated fusion. Mol. Biol. Cell 11:2359-2371.
34. Li, M., C. Yang, and R. W. Compans. 2001. Mutations in the cytoplasmic tail of murine leukemia virus envelope protein suppress fusion inhibition by R peptide. J. Virol. 75:2337-2344.
35. Lin, X., C. A. Derdeyn, R. Blumenthal, J. West, and E. Hunter. 2003. Progressive truncations C terminal to the membrane-spanning domain of simian immunodeficiency virus Env reduce fusogenicity and increase concentration dependence of Env for fusion. J. Virol. 77:7067-7077.
36. 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.
37. 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.
38. Markosyan, R. M., F. S. Cohen, and G. B. Melikyan. 2000. The lipid-anchored ectodomain of influenza virus hemagglutinin (GPI-HA) is capable of inducing nonenlarging fusion pores. Mol. Biol. Cell 11:1143-1152.
39. 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.
40. Markovic, I., H. Pulyaeva, A. Sokoloff, and L. V. Chernomordik. 1998. Membrane fusion mediated by baculovirus gp64 involves assembly of stable gp64 trimers into multiprotein aggregates. J. Cell Biol. 143:1155-1166.
41. McGinnes, L. W., T. Sergel, H. Chen, L. Hamo, S. Schwertz, D. Li, and T. G. Morrison. 2001. Mutational analysis of the membrane proximal heptad repeat of the Newcastle disease virus fusion protein. Virology 289:343-352.
42. Melikyan, G. B., S. Lin, M. G. Roth, and F. S. Cohen. 1999. Amino acid sequence requirements of the transmembrane and cytoplasmic domains of influenza virus hemagglutinin for viable membrane fusion. Mol. Biol. Cell 10:1821-1836.
43. 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.
44. 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.
45. 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.
46. Narayan, S., R. J. Barnard, and J. A. Young. 2003. Two retroviral entry pathways distinguished by lipid raft association of the viral receptor and differences in viral infectivity. J. Virol. 77:1977-1983.
47. Paterson, R. G., C. J. Russell, and R. A. Lamb. 2000. Fusion protein of the paramyxovirus SV5: destabilizing and stabilizing mutants of fusion activation. Virology 270:17-30.
48. Picard-Maureau, M., G. Jarmy, A. Berg, A. Rethwilm, and D. Lindemann. 2003. Foamy virus envelope glycoprotein-mediated entry involves a pH-dependent fusion process. J. Virol. 77:4722-4730.
49. Ragheb, J. A., and W. F. Anderson. 1994. pH-independent murine leukemia virus ecotropic envelope-mediated cell fusion: implications for the role of the R peptide and p12E TM in viral entry. J. Virol. 68:3220-3231.
50. Ross, S. R., J. J. Schofield, C. J. Farr, and M. Bucan. 2002. Mouse transferrin receptor 1 is the cell entry receptor for mouse mammary tumor virus. Proc. Natl. Acad. Sci. USA 99:12386-12390.
51. Ruigrok, R. W., S. R. Martin, S. A. Wharton, J. J. Skehel, P. M. Bayley, and D. C. Wiley. 1986. Conformational changes in the hemagglutinin of influenza virus which accompany heat-induced fusion of virus with liposomes. Virology 155:484-497.
52. Russell, C. J., T. S. Jardetzky, and R. A. Lamb. 2001. Membrane fusion machines of paramyxoviruses: capture of intermediates of fusion. EMBO J. 20:4024-4034.
53. Salzwedel, K., J. T. West, and H. E. 1999. A conserved tryptophan-rich motif in the membrane-proximal region of the human immunodeficiency virus type 1 gp41 ectodomain is important for Env-mediated fusion and virus infectivity. J. Virol. 73:2469-2480.
54. Sanders, D. A. 2003. Ancient viruses in the fight against HIV. Drug Discov. Today 8:287-291.
55. Seth, S., A. Vincent, and R. W. Compans. 2003. Activation of fusion by the SER virus F protein: a low-pH-dependent paramyxovirus entry process. J. Virol. 77:6520-6527.
56. Seth, S., A. Vincent, and R. W. Compans. 2003. Mutations in the cytoplasmic domain of a paramyxovirus fusion glycoprotein rescue syncytium formation and eliminate the hemagglutinin-neuraminidase protein requirement for membrane fusion. J. Virol. 77:167-178.
57. 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.
58. Stegmann, T. 1993. Influenza hemagglutinin-mediated membrane fusion does not involve inverted phase lipid intermediates. J. Biol. Chem. 268:1716-1722.
59. Taylor, G. M., and D. A. Sanders. 1999. The role of the membrane-spanning domain sequence in glycoprotein-mediated membrane fusion. Mol. Biol. Cell 10:2803-2815.
60. Taylor, G. M., and D. A. Sanders. 2003. Structural criteria for regulation of membrane fusion and virion incorporation by the murine leukemia virus TM cytoplasmic domain. Virology 312:295-305.
61. Tobiume, M., J. E. Lineberger, C. A. Lundquist, M. D. Miller, and C. Aiken. 2003. Nef does not affect the efficiency of human immunodeficiency virus type 1 fusion with target cells. J. Virol. 77:10645-10650.
62. Tonelli, M., R. J. Peters, T. L. James, and D. A. Agard. 2001. The solution structure of the viral binding domain of Tva, the cellular receptor for subgroup A avian leukosis and sarcoma virus. FEBS Lett. 509:161-168.
63. Wilson, I. A., J. J. Skehel, and D. C. Wiley. 1981. Structure of the haemagglutinin membrane glycoprotein of influenza virus at 3 A resolution. Nature 289:366-372.