Native structure of a retroviral envelope protein and its conformational change upon interaction with the target cell

Journal of Structural Biology

Volumn 197, Issue 2, 2017, Pages 172-180

  Riedel, Christiane ^a,b   Vasishtan, Daven ^a   Siebert, C Alistair ^a   Whittle, Cathy ^a   Lehmann, Maik J ^c   Mothes, Walther ^d   Grünewald, Kay ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF VETERINARY MEDICINE   (Austria)

^c UNIVERSITY OF APPLIED SCIENCES BINGEN   (Germany)

^d YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Electron cryo tomography; Env; Murine leukemia virus; Retroviridae; Sub volume averaging; Virus entry

Indexed keywords

CELL MEMBRANE PROTEIN; MEMBRANE LIPID; VIRUS ENVELOPE PROTEIN; YELLOW FLUORESCENT PROTEIN;

ANIMAL CELL; ARTICLE; BILAYER MEMBRANE; BINDING SITE; CELL MEMBRANE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ELECTRON TOMOGRAPHY; HOST CELL; LIPID COMPOSITION; MEMBRANE STRUCTURE; MURINE LEUKEMIA VIRUS; NONHUMAN; PROLINE RICH PROTEIN DOMAIN; PROTEIN BINDING; PROTEIN CONFORMATION; RAT; RETROVIRIDAE; STRUCTURE ANALYSIS; TARGET CELL; VIRUS CELL INTERACTION; VIRUS ENVELOPE; CRYOELECTRON MICROSCOPY; PHYSIOLOGY; PROCEDURES; ULTRASTRUCTURE;

BINDING SITES; CRYOELECTRON MICROSCOPY; LEUKEMIA VIRUS, MURINE; PROTEIN CONFORMATION; VIRAL ENVELOPE PROTEINS;

EID: 85002777084     PISSN: 10478477     EISSN: 10958657     Source Type: Journal    
DOI: 10.1016/j.jsb.2016.06.017     Document Type: Article

References (40)

1. Albritton, L.M., Kim, J.W., Tseng, L., Cunningham, J.M., Envelope-binding domain in the cationic amino acid transporter determines the host range of ecotropic murine retroviruses. J. Virol. 67 (1993), 2091–2096.
2. Albritton, L.M., Tseng, L., Scadden, D., Cunningham, J.M., A putative murine ecotropic retrovirus receptor gene encodes a multiple membrane-spanning protein and confers susceptibility to virus infection. Cell 57 (1989), 659–666.
3. Apellániz, B., Huarte, N., Largo, E., Nieva, J.L., The three lives of viral fusion peptides. Chem. Phys. Lipids 181 (2014), 40–55, 10.1016/j.chemphyslip.2014.03.003.
4. Aydin, H., Cook, J.D., Lee, J.E., Crystal structures of beta- and gammaretrovirus fusion proteins reveal a role for electrostatic stapling in viral entry. J. Virol. 88 (2014), 143–153, 10.1128/JVI.02023-13.
5. Bae, Y., Kingsman, S., Kingsman, A., Functional dissection of the Moloney murine leukemia virus envelope protein gp70. J. Virol. 71 (1997), 2092–2099.
6. Bartesaghi, A., Merk, A., Borgnia, M.J., Milne, J.L.S., Subramaniam, S., Prefusion structure of trimeric HIV-1 envelope glycoprotein determined by cryo-electron microscopy. Nat. Struct. Mol. Biol. 20 (2013), 1352–1357, 10.1038/nsmb.2711.
7. Blumenthal, R., Durell, S., Viard, M., HIV entry and envelope glycoprotein-mediated fusion. J. Biol. Chem. 287 (2012), 40841–40849, 10.1074/jbc.R112.406272.
8. Caffrey, M., HIV envelope: challenges and opportunities for development of entry inhibitors. Trends Microbiol. 19 (2011), 191–197, 10.1016/j.tim.2011.02.001.
9. Davey, R.A., Zuo, Y., Cunningham, J.M., Identification of a receptor-binding pocket on the envelope protein of friend murine leukemia virus. J. Virol. 73 (1999), 3758–3763.
10. Fass, D., Davey, R.A., Hamson, C.A., Kim, P.S., Cunningham, J.M., Berger, J.M., Structure of a murine leukemia virus receptor-binding glycoprotein at 2.0 Å resolution. Science 277 (1997), 1662–1666.
11. Fass, D., Harrison, S.C., Kim, P.S., Retrovirus envelope domain at 1.7 Å resolution. Nat. Struct. Biol. 3 (1996), 465–469, 10.1038/nsb0596-465.
12. Fernández, J.J., Li, S., Crowther, R.A., CTF determination and correction in electron cryotomography. Ultramicroscopy 106 (2006), 587–596, 10.1016/j.ultramic.2006.02.004.
13. Fischer, H., Polikarpov, I., Craievich, A.F., Average protein density is a molecular-weight-dependent function. Protein Sci. 13 (2004), 2825–2828, 10.1110/ps.04688204.
14. Förster, F., Medalia, O., Zauberman, N., Baumeister, W., Fass, D., Retrovirus envelope protein complex structure in situ studied by cryo-electron tomography. Proc. Natl. Acad. Sci. U.S.A. 102 (2005), 4729–4734, 10.1073/pnas.0409178102.
15. Henderson, R., Sali, A., Baker, M.L., Carragher, B., Devkota, B., Downing, K.H., Egelman, E.H., Feng, Z., Frank, J., Grigorieff, N., Jiang, W., Ludtke, S.J., Medalia, O., Penczek, P.A., Rosenthal, P.B., Rossmann, M.G., Schmid, M.F., Schröder, G.F., Steven, A.C., Stokes, D.L., Westbrook, J.D., Wriggers, W., Yang, H., Young, J., Berman, H.M., Chiu, W., Kleywegt, G.J., Lawson, C.L., Outcome of the first electron microscopy validation task force meeting. Structure 20 (2012), 205–214, 10.1016/j.str.2011.12.014.
16. Heumann, J.M., Hoenger, A., Mastronarde, D.N., Clustering and variance maps for cryo-electron tomography using wedge-masked differences. J. Struct. Biol. 175 (2011), 288–299, 10.1016/j.jsb.2011.05.011.
17. Huiskonen, J.T., Hepojoki, J., Laurinmäki, P., Vaheri, A., Lankinen, H., Butcher, S.J., Grünewald, K., Electron cryotomography of Tula hantavirus suggests a unique assembly paradigm for enveloped viruses. J. Virol. 84 (2010), 4889–4897, 10.1128/JVI.00057-10.
18. Kayman, S.C., Kopelman, R., Projan, S., Kinney, D.M., Pinter, A., Mutational analysis of N-linked glycosylation sites of Friend murine leukemia virus envelope protein. J. Virol. 65 (1991), 5323–5332.
19. Kayman, S.C., Park, H., Saxon, M., Pinter, A., The Hypervariable Domain of the Murine Leukemia Virus Surface Protein Tolerates Large Insertions and Deletions, Enabling Development of a Retroviral Particle Display System. J. Virol. 73 (1999), 1802–1808.
20. Kayman, S.C., Park, H., Saxon, M., Pinter, A., The hypervariable domain of the murine leukemia virus surface protein tolerates large insertions and deletions, enabling development of a retroviral particle display system. J. Virol. 73 (1999), 1802–1808.
21. Kelley, L.A., Mezulis, S., Yates, C.M., Wass, M.N., Sternberg, M.J.E., The Phyre2 web portal for protein modeling, prediction and analysis. Nat. Protoc. 10 (2015), 845–858.
22. Kremer, J.R., Mastronarde, D.N., McIntosh, J.R., Computer visualization of three-dimensional image data using IMOD. J. Struct. Biol. 116 (1996), 71–76, 10.1006/jsbi.1996.0013.
23. Lehmann, M.J., Sherer, N.M., Marks, C.B., Pypaert, M., Mothes, W., Actin- and myosin-driven movement of viruses along filopodia precedes their entry into cells. J. Cell Biol. 170 (2005), 317–325, 10.1083/jcb.200503059.
24. Li, X., Mooney, P., Zheng, S., Booth, C.R., Braunfeld, M.B., Gubbens, S., Agard, D.A., Cheng, Y., Electron counting and beam-induced motion correction enable near-atomic-resolution single-particle cryo-EM. Nat. Methods 10 (2013), 584–590, 10.1038/nmeth.2472.
25. MacKrell, A.J., Soong, N.W., Curtis, C.M., Anderson, W.F., Identification of a subdomain in the Moloney murine leukemia virus envelope protein involved in receptor binding. J. Virol. 70 (1996), 1768–1774.
26. Maurer, U.E., Zeev-Ben-Mordehai, T., Pandurangan, A.P., Cairns, T.M., Hannah, B.P., Whitbeck, J.C., Eisenberg, R.J., Cohen, G.H., Topf, M., Huiskonen, J.T., Grünewald, K., The structure of herpesvirus fusion glycoprotein B-bilayer complex reveals the protein-membrane and lateral protein-protein interaction. Structure 21 (2013), 1396–1405, 10.1016/j.str.2013.05.018.
27. Melikyan, G.B., HIV entry: a game of hide-and-fuse?. Curr. Opin. Virol. 4 (2014), 1–7, 10.1016/j.coviro.2013.09.004.
28. Nicastro, D., Schwartz, C., Pierson, J., Gaudette, R., Porter, M.E., McIntosh, J.R., The molecular architecture of axonemes revealed by cryoelectron tomography. Science 313 (2006), 944–948, 10.1126/science.1128618.
29. Opstelten, D.J., Wallin, M., Garoff, H., Moloney murine leukemia virus envelope protein subunits, gp70 and Pr15E, form a stable disulfide-linked complex. J. Virol. 72 (1998), 6537–6545.
30. Pettersen, E.F., Goddard, T.D., Huang, C.C., Couch, G.S., Greenblatt, D.M., Meng, E.C., Ferrin, T.E., UCSF Chimera–a visualization system for exploratory research and analysis. J. Comput. Chem. 25 (2004), 1605–1612, 10.1002/jcc.20084.
31. Pinter, A., Honnen, W.J., O-linked glycosylation of retroviral envelope gene products. J. Virol. 62 (1988), 1016–1021.
32. Pinter, A., Kopelman, R., Li, Z., Kayman, S., Sanders, D., 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 (1997), 8073–8077.
33. Sandberg, K., Mastronarde, D.N., Beylkin, G., A fast reconstruction algorithm for electron microscope tomography. J. Struct. Biol. 144 (2003), 61–72, 10.1016/j.jsb.2003.09.013.
34. Sherer, N.M., Lehmann, M.J., Jimenez-Soto, L.F., Ingmundson, A., Horner, S.M., Cicchetti, G., Allen, P.G., Pypaert, M., Cunningham, J.M., Mothes, W., Visualization of Retroviral Replication in Living Cells Reveals Budding into Multivesicular Bodies. Traffic 4 (2003), 785–801, 10.1034/j.1600-0854.2003.00135.x.
35. Sougrat, R., Bartesaghi, A., Lifson, J.D., Bennett, A.E., Bess, J.W., Zabransky, D.J., Subramaniam, S., Electron tomography of the contact between T cells and SIV/HIV-1: implications for viral entry. PLoS Pathog., 3, 2007, e63, 10.1371/journal.ppat.0030063.
36. Wu, S.-R., Sjöberg, M., Wallin, M., Lindqvist, B., Ekström, M., Hebert, H., Koeck, P.J.B., Garoff, H., Turning of the receptor-binding domains opens up the murine leukaemia virus Env for membrane fusion. EMBO J. 27 (2008), 2799–2808, 10.1038/emboj.2008.187.
37. Yeager, M., Wilson-Kubalek, E.M., Weiner, S.G., Brown, P.O., Rein, A., Supramolecular organization of immature and mature murine leukemia virus revealed by electron cryo-microscopy: Implications for retroviral assembly mechanisms. Proc. Natl. Acad. Sci. 95 (1998), 7299–7304, 10.1073/pnas.95.13.7299.
38. Yoshimoto, T., Yoshimoto, E., Meruelo, D., Identification of amino acid residues critical for infection with ecotropic murine leukemia retrovirus. J. Virol. 67 (1993), 1310–1314.
39. Zavorotinskaya, T., Albritton, L.M., A hydrophobic patch in ecotropic murine leukemia virus envelope protein is the putative binding site for a critical tyrosine residue on the cellular receptor. J. Virol. 73 (1999), 10164–10172.
40. Zeev-Ben-Mordehai, T., Vasishtan, D., Siebert, C.A., Grünewald, K., The full-length cell-cell fusogen EFF-1 is monomeric and upright on the membrane. Nat. Commun., 5, 2014, 3912, 10.1038/ncomms4912.