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Retrovirus envelope domain at 1.7 Å resolution

Abstract

We report the crystal structure of an extraviral segment of a retrovirus envelope protein, the Moloney murine leukemia virus (MoMuLV) transmembrane (TM) subunit. This segment, which comprises a region of the MoMuLVTM protein analogous to that contained within the X-ray crystal structure of low-pH converted influenza hemagglutinin, contains a trimeric coiled coil, with a hydrophobic cluster at its base and a strand that packs in an antiparallel orientation against the coiled coil. This structure gives the first high-resolution insight into the retrovirus surface and serves as a model for a wide range of viral fusion proteins; key residues in this structure are conserved among C- and D-type retroviruses and the filovirus ebola.

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References

  1. Hunter, E. & Swanstrom, R. Retrovirus envelope glycoproteins. Curr. Top. Microbiol. Immun. 157, 187–253 (1990).

    CAS  Google Scholar 

  2. Pinter, A., Lieman-Hurwitz, J. & Fleissner, E. The nature of the association between the murine leukemia virus envelope proteins. Virology 91, 345–351 (1978).

    Article  CAS  PubMed  Google Scholar 

  3. Fass, D & Kim, P.S. Dissection of a retrovirus envelope protein reveals structural similarity to influenza hemagglutinin. Curr. Biol. 5, 1377–1383 (1995).

    Article  CAS  PubMed  Google Scholar 

  4. Chambers, P., Pringle, C.R. & Easton, A.J. Heptad repeat sequences are located adjacent to hydrophobic regions in several types of virus fusion glycoproteins. J. Gen. Virol. 71, 3075–3080 (1990).

    Article  CAS  PubMed  Google Scholar 

  5. Delwart, E.L, Mosialos, G. & Gilmore, T. Retroviral envelope glycoproteins contain a “leucinezipper”-like repeat. AIDS Res. Human Retroviruses 6, 703–706 (1990).

    Article  CAS  Google Scholar 

  6. Cianciolo, G.J., Copeland, T.D., Oroszlan, S. & Snyderman, R. Inhibition of lymphocyte proliferation by a synthetic peptide homologous to retroviral envelope proteins. Science 230, 453–55 (1985).

    Article  CAS  PubMed  Google Scholar 

  7. Ogasawara, M. et al. Human INF-γ production is inhibited by a synthetic peptide homologous to retoviral envelope protein. J. Immunol. 141, 614–619 (1988).

    CAS  PubMed  Google Scholar 

  8. Volchkov, V.E., Blinov, V.M. & Netesov, S.V. The envelope glycoprotein of Ebola virus contains an immunosuppressive-like domain similar to oncogenic retroviruses. FEBS Letters 305, 181–184 (1992).

    Article  CAS  PubMed  Google Scholar 

  9. Feldman, H., Will, C., Schikore, M., Slenczka, W. & Klenk, H.-D. Glycosylation and oligomerization of the spike protein of Marburg virus. Virology 182, 353–356 (1991).

    Article  Google Scholar 

  10. Jones, T.A., Zou, J.-Y., Cowan, S.W. & Kjeldgaard, M. Improved methods for binding protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A47, 110–119 (1991).

    Article  CAS  Google Scholar 

  11. Harbury, P.B., Zhang, T., Kim, P.S. & Alber, T. A switch between two-, three-, and four-stranded coiled coils in GCN4 leucine zipper mutants. Science 262, 1401–1407 (1993).

    Article  CAS  PubMed  Google Scholar 

  12. Lumb, K.J. & Kim, P.S. A buried polar interaction imparts structural uniqueness in a designed heterodimeric coiled coil. Biochem. 34, 8642–8648 (1995).

    Article  CAS  Google Scholar 

  13. Rey, F.A., Heinz, F.X., Mandl, C., Kunz, C. & Harrison, S.C. The envelope glycoprotein from tick–borne encephalitis virus at 2 Å resolution. Nature 375, 291–298 (1995).

    Article  CAS  PubMed  Google Scholar 

  14. Wilson, I.A., Skehel, J.J. & Wiley, D.C. Structure of the haemagglutinin membrane glycoprotein of influenza virus at 3 Å resolution. Nature 289, 366–373 (1981).

    Article  CAS  PubMed  Google Scholar 

  15. Bullough, P.A., Hughson, F.M., Skehel, J.J. & Wiley, D.C. Structure of influenza haemagglutinin atthepH of membrane fusion. Nature 371, 37–43 (1994).

    Article  CAS  PubMed  Google Scholar 

  16. Bullough, P.A. et al Crystals of a fragment of influenza haemagglutinin in the low pH induced conformation. J. Mol. Biol. 236, 1262–1265 (1994).

    Article  CAS  PubMed  Google Scholar 

  17. Hughson, F.M. Structural characterization of viral fusion proteins. Curr. Biol. 5, 265–274 (1995).

    Article  CAS  PubMed  Google Scholar 

  18. Harbury, P.B., Kim, P.S. & Alber, T. Crystal structure of an isoleucine-zipper trimer. Nature 371, 80–83 (1994).

    Article  CAS  PubMed  Google Scholar 

  19. Carr, C.M. & Kim, P.S. A spring-loaded mechanism for the conformational change of influenza hemagglutinin. Cell 73, 823–832 (1993).

    Article  CAS  PubMed  Google Scholar 

  20. Blum, M., Metcalf, P., Harrison, S.C. & Wiley, D.C. A system for collection and on-line integration of X-ray diffraction data from a multiwire area detector. J. Appl. Crystallogr. 20, 235–242 (1987).

    Article  CAS  Google Scholar 

  21. CCP4, a Suite of Programs for Protein Crystallography (SERC (UK) Collaborative Computing Project No. 4, Daresbury Laboratory, Warrington, 1979).

  22. Van Duyne, G.D., Standaert, R.F., Karplus, P.A., Schreiber, S.L. & Clardy, J. Atomic structures of the human immunophilin FKBP-12 complexes with FK506 and rapamycin. J. Mol. Biol. 229, 105–124 (1993).

    Article  CAS  PubMed  Google Scholar 

  23. Brünger, A.T. X-PLOR (Version 3.1:) A System for X-ray Crystallography and NMR (Yale Univ. Press, New Haven, 1992).

    Google Scholar 

  24. Stegmann, T., Delfino, J.M., Richards, F.M. & Helenius, A. The HA2 subunit of influenza hemagglutinin inserts into the target membrane prior to fusion. J. Biol. Chem. 266, 18404–18410 (1991).

    CAS  PubMed  Google Scholar 

  25. Tsurudome, M. et al. Lipid interactions of the hemagglutinin HA2NH2-terminal segment during influenza virus-induced membrane fusion. J. Biol. Chem. 267, 20225–20232 (1992).

    CAS  PubMed  Google Scholar 

  26. Pinter, A. & Honnen, W.J. Topography of murine leukemia virus envelope proteins: characterization of transmembrane components. J. Virol. 46, 1056–1060 (1983).

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Weast, R.C., Ed., CRC Handbook of Chemistry and Physics (CRC Press, Inc. Boca Raton, Florida, 1980), p. F–216.

  28. Kraulis, P. MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr. 24, 924–950 (1991).

    Article  Google Scholar 

  29. White, J.M. & Wilson, I.A. Anti-peptide antibodies detect steps in a protein conformational change: low-pH activation of the influenza virus hemagglutinin. J. Cell. Biol. 105, 2887–2896 (1987).

    Article  CAS  PubMed  Google Scholar 

  30. Kemble, G.W., Bodian, D.L., Rose, J., Wilson, I.A. & White, J.M. Intermonomer disulfide bonds impair the fusion activity of influenza virus hemagglutinin. J. Virol. 66, 4940–4950 (1992).

    CAS  PubMed  PubMed Central  Google Scholar 

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Fass, D., Harrison, S. & Kim, P. Retrovirus envelope domain at 1.7 Å resolution. Nat Struct Mol Biol 3, 465–469 (1996). https://doi.org/10.1038/nsb0596-465

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