Crystal structure of the prefusion surface glycoprotein of the prototypic arenavirus LCMV

Nature Structural and Molecular Biology

Volumn 23, Issue 6, 2016, Pages 513-521

  Hastie, Kathryn M ^a   Igonet, Sébastien ^a,e   Sullivan, Brian M ^a   Legrand, Pierre ^b   Zandonatti, Michelle A ^a   Robinson, James E ^c   Garry, Robert F ^c   Rey, Félix A ^d   Oldstone, Michael B ^a   Saphire, Erica Ollmann ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b SYNCHROTRON SOLEIL   (France)

^c TULANE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d INSTITUT PASTEUR   (France)

^e Present Address: Calixar   (France)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; MEMBRANE PROTEIN; PROTEIN SUBUNIT; SIGNAL PEPTIDE; VIRUS ENVELOPE PROTEIN;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; EBOLAVIRUS; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MEMBRANE FUSION; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN STRUCTURE; RECEPTOR BINDING; STOICHIOMETRY; ANIMAL; CELL LINE; CHEMISTRY; DROSOPHILA; GLYCOSYLATION; HUMAN; LYMPHOCYTIC CHORIOMENINGITIS; METABOLISM; MOLECULAR MODEL; PHYSIOLOGY; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; PROTEIN SUBUNIT; VIROLOGY; VIRUS ENTRY; X RAY CRYSTALLOGRAPHY;

ANIMALS; CELL LINE; CRYSTALLOGRAPHY, X-RAY; DROSOPHILA; GLYCOSYLATION; HUMANS; LYMPHOCYTIC CHORIOMENINGITIS; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MEMBRANE GLYCOPROTEINS; MODELS, MOLECULAR; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; PROTEIN SORTING SIGNALS; PROTEIN SUBUNITS; VIRAL ENVELOPE PROTEINS; VIRUS INTERNALIZATION;

EID: 84964270228     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.3210     Document Type: Article

References (69)

1. Stephensen, C. B. et al. Prevalence of serum antibodies against lymphocytic choriomeningitis virus in selected populations from two U. S. cities. J. Med. Virol. 38, 27-31 (1992).
2. Childs, J. E. et al. Human-rodent contact and infection with lymphocytic choriomeningitis and Seoul viruses in an inner-city population. Am. J. Trop. Med. Hyg. 44, 117-121 (1991).
3. Ambrosio, A. M., Feuillade, M. R., Gamboa, G. S.&Maiztegui, J. I. Prevalence of lymphocytic choriomeningitis virus infection in a human population of Argentina. Am. J. Trop. Med. Hyg. 50, 381-386 (1994).
4. Marrie, T. J.&Saron, M. F. Seroprevalence of lymphocytic choriomeningitis virus in Nova Scotia. Am. J. Trop. Med. Hyg. 58, 47-49 (1998).
5. Lledó, L., Gegúndez, M. I., Saz, J. V., Bahamontes, N.&Beltrán, M. Lymphocytic choriomeningitis virus infection in a province of Spain: Analysis of sera from the general population and wild rodents. J. Med. Virol. 70, 273-275 (2003).
6. Riera, L. et al. Serological study of the lymphochoriomeningitis virus (LCMV) in an inner city of Argentina. J. Med. Virol. 76, 285-289 (2005).
7. Buchmeier, M., de la Torre, J. C.&Peters, C. J. Arenaviridae: The Viruses and their Replication (Lippincott-Raven, 2007).
8. Fischer, S. A. et al. Transmission of lymphocytic choriomeningitis virus by organ transplantation. N. Engl. J. Med. 354, 2235-2249 (2006).
9. Jamieson, D. J., Kourtis, A. P., Bell, M.&Rasmussen, S. A. Lymphocytic choriomeningitis virus: An emerging obstetric pathogen? Am. J. Obstet. Gynecol. 194, 1532-1536 (2006).
10. Armstrong, C.&Lillie, R. D. Experimental lymphocytic choriomeningitis of monkeys and mice produced by a virus encountered in studies of the 1933 St. Louis epidemic. Public Health Rep. 49, 1019-1027 (1934).
11. Oldstone, M. B. Lessons learned and concepts formed from study of the pathogenesis of the two negative-strand viruses lymphocytic choriomeningitis and influenza. Proc. Natl. Acad. Sci. USA 110, 4180-4183 (2013).
12. Pauken, K. E.&Wherry, E. J. Overcoming T cell exhaustion in infection and cancer. Trends Immunol. 36, 265-276 (2015).
13. Zinkernagel, R. M. Lymphocytic choriomeningitis virus and immunology. Curr. Top. Microbiol. Immunol. 263, 1-5 (2002).
14. Gourley, T. S., Wherry, E. J., Masopust, D.&Ahmed, R. Generation and maintenance of immunological memory. Semin. Immunol. 16, 323-333 (2004).
15. Eichler, R. et al. Identification of Lassa virus glycoprotein signal peptide as a trans-acting maturation factor. EMBO Rep. 4, 1084-1088 (2003).
16. York, J., Romanowski, V., Lu, M.&Nunberg, J. H. The signal peptide of the Junín arenavirus envelope glycoprotein is myristoylated and forms an essential subunit of the mature G1-G2 complex. J. Virol. 78, 10783-10792 (2004).
17. Eichler, R., Lenz, O., Strecker, T.&Garten, W. Signal peptide of Lassa virus glycoprotein GP-C exhibits an unusual length. FEBS Lett. 538, 203-206 (2003).
18. Froeschke, M., Basler, M., Groettrup, M.&Dobberstein, B. Long-lived signal peptide of lymphocytic choriomeningitis virus glycoprotein pGP-C. J. Biol. Chem. 278, 41914-41920 (2003).
19. Kunz, S., Edelmann, K. H., de la Torre, J. C., Gorney, R.&Oldstone, M. B. Mechanisms for lymphocytic choriomeningitis virus glycoprotein cleavage, transport, and incorporation into virions. Virology 314, 168-178 (2003).
20. Saunders, A. A. et al. Mapping the landscape of the lymphocytic choriomeningitis virus stable signal peptide reveals novel functional domains. J. Virol. 81, 5649-5657 (2007).
21. Schrempf, S., Froeschke, M., Giroglou, T., von Laer, D.&Dobberstein, B. Signal peptide requirements for lymphocytic choriomeningitis virus glycoprotein C maturation and virus infectivity. J. Virol. 81, 12515-12524 (2007).
22. York, J.&Nunberg, J. H. Role of the stable signal peptide of Junín arenavirus envelope glycoprotein in pH-dependent membrane fusion. J. Virol. 80, 7775-7780 (2006).
23. York, J.&Nunberg, J. H. Distinct requirements for signal peptidase processing and function in the stable signal peptide subunit of the Junín virus envelope glycoprotein. Virology 359, 72-81 (2007).
24. Cao, W. et al. Identification of alpha-dystroglycan as a receptor for lymphocytic choriomeningitis virus and Lassa fever virus. Science 282, 2079-2081 (1998).
25. Inamori, K. et al. Dystroglycan function requires xylosyl-and glucuronyltransferase activities of LARGE. Science 335, 93-96 (2012).
26. Kanagawa, M. et al. Molecular recognition by LARGE is essential for expression of functional dystroglycan. Cell 117, 953-964 (2004).
27. Kunz, S. et al. Posttranslational modification of alpha-dystroglycan, the cellular receptor for arenaviruses, by the glycosyltransferase LARGE is critical for virus binding. J. Virol. 79, 14282-14296 (2005).
28. Jae, L. T. et al. Lassa virus entry requires a trigger-induced receptor switch. Science 344, 1506-1510 (2014).
29. Spiropoulou, C. F., Kunz, S., Rollin, P. E., Campbell, K. P.&Oldstone, M. B. New World arenavirus clade C, but not clade A and B viruses, utilizes alpha-dystroglycan as its major receptor. J. Virol. 76, 5140-5146 (2002).
30. Flanagan, M. L. et al. New world clade B arenaviruses can use transferrin receptor 1 (TfR1)-dependent and-independent entry pathways, and glycoproteins from human pathogenic strains are associated with the use of TfR1. J. Virol. 82, 938-948 (2008).
31. Radoshitzky, S. R. et al. Transferrin receptor 1 is a cellular receptor for New World haemorrhagic fever arenaviruses. Nature 446, 92-96 (2007).
32. Eschli, B. et al. Identification of an N-terminal trimeric coiled-coil core within arenavirus glycoprotein 2 permits assignment to class I viral fusion proteins. J. Virol. 80, 5897-5907 (2006).
33. Igonet, S. et al. X-ray structure of the arenavirus glycoprotein GP2 in its postfusion hairpin conformation. Proc. Natl. Acad. Sci. USA 108, 19967-19972 (2011).
34. Parsy, M. L., Harlos, K., Huiskonen, J. T.&Bowden, T. A. Crystal structure of Venezuelan hemorrhagic fever virus fusion glycoprotein reveals a class 1 postfusion architecture with extensive glycosylation. J. Virol. 87, 13070-13075 (2013).
35. Abraham, J., Corbett, K. D., Farzan, M., Choe, H.&Harrison, S. C. Structural basis for receptor recognition by New World hemorrhagic fever arenaviruses. Nat. Struct. Mol. Biol. 17, 438-444 (2010).
36. Bowden, T. A. et al. Unusual molecular architecture of the machupo virus attachment glycoprotein. J. Virol. 83, 8259-8265 (2009).
37. Mahmutovic, S. et al. Molecular basis for antibody-mediated neutralization of New World hemorrhagic fever mammarenaviruses. Cell Host Microbe 18, 705-713 (2015).
38. Cohen-Dvashi, H., Cohen, N., Israeli, H.&Diskin, R. Molecular mechanism for LAMP1 recognition by Lassa virus. J. Virol. 89, 7584-7592 (2015).
39. Klewitz, C., Klenk, H. D.&ter Meulen, J. Amino acids from both N-terminal hydrophobic regions of the Lassa virus envelope glycoprotein GP-2 are critical for pH-dependent membrane fusion and infectivity. J. Gen. Virol. 88, 2320-2328 (2007).
40. Welch, B. D. et al. Structure of the cleavage-activated prefusion form of the parainfluenza virus 5 fusion protein. Proc. Natl. Acad. Sci. USA 109, 16672-16677 (2012).
41. Rey, F. A., Heinz, F. X., Mandl, C., Kunz, C.&Harrison, S. C. The envelope glycoprotein from tick-borne encephalitis virus at 2 A resolution. Nature 375, 291-298 (1995).
42. Kanai, R. et al. Crystal structure of west nile virus envelope glycoprotein reveals viral surface epitopes. J. Virol. 80, 11000-11008 (2006).
43. Modis, Y., Ogata, S., Clements, D.&Harrison, S. C. A ligand-binding pocket in the dengue virus envelope glycoprotein. Proc. Natl. Acad. Sci. USA 100, 6986-6991 (2003).
44. Modis, Y., Ogata, S., Clements, D.&Harrison, S. C. Variable surface epitopes in the crystal structure of dengue virus type 3 envelope glycoprotein. J. Virol. 79, 1223-1231 (2005).
45. Kunz, S., Sevilla, N., Rojek, J. M.&Oldstone, M. B. Use of alternative receptors different than alpha-dystroglycan by selected isolates of lymphocytic choriomeningitis virus. Virology 325, 432-445 (2004).
46. Oldstone, M. B.&Campbell, K. P. Decoding arenavirus pathogenesis: essential roles for alpha-dystroglycan-virus interactions and the immune response. Virology 411, 170-179 (2011).
47. Oldstone, M. B. A. Biology and pathogenesis of lymphocytic choriomeningitis virus infection. Curr. Top. Microbiol. Immunol. 263, 83-117 (2002).
48. Sevilla, N. et al. Immunosuppression and resultant viral persistence by specific viral targeting of dendritic cells. J. Exp. Med. 192, 1249-1260 (2000).
49. Sullivan, B. M. et al. Point mutation in the glycoprotein of lymphocytic choriomeningitis virus is necessary for receptor binding, dendritic cell infection, and long-term persistence. Proc. Natl. Acad. Sci. USA 108, 2969-2974 (2011).
50. Smelt, S. C. et al. Differences in affinity of binding of lymphocytic choriomeningitis virus strains to the cellular receptor alpha-dystroglycan correlate with viral tropism and disease kinetics. J. Virol. 75, 448-457 (2001).
51. Teng, M. N., Borrow, P., Oldstone, M. B.&de la Torre, J. C. A single amino acid change in the glycoprotein of lymphocytic choriomeningitis virus is associated with the ability to cause growth hormone deficiency syndrome. J. Virol. 70, 8438-8443 (1996).
52. Li, S. et al. Acidic pH-induced conformations and LAMP1 binding of the Lassa virus glycoprotein spike. PLoS Pathog. 12, e1005418 (2016).
53. Burns, J. W.&Buchmeier, M. J. Protein-protein interactions in lymphocytic choriomeningitis virus. Virology 183, 620-629 (1991).
54. Mukhopadhyay, S., Kuhn, R. J.&Rossmann, M. G. A structural perspective of the flavivirus life cycle. Nat. Rev. Microbiol. 3, 13-22 (2005).
55. Baker, N. A., Sept, D., Joseph, S., Holst, M. J.&McCammon, J. A. Electrostatics of nanosystems: Application to microtubules and the ribosome. Proc. Natl. Acad. Sci. USA 98, 10037-10041 (2001).
56. Kabsch, W. Xds. Acta Crystallogr. D Biol. Crystallogr. 66, 125-132 (2010).
57. Vonrhein, C., Blanc, E., Roversi, P.&Bricogne, G. Automated structure solution with autoSHARP. Methods Mol. Biol. 364, 215-230 (2007).
58. Cowtan, K. The Buccaneer software for automated model building. 1. Tracing protein chains. Acta Crystallogr. D Biol. Crystallogr. 62, 1002-1011 (2006).
59. Cowtan, K. Completion of autobuilt protein models using a database of protein fragments. Acta Crystallogr. D Biol. Crystallogr. 68, 328-335 (2012).
60. Emsley, P.&Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132 (2004).
61. Adams, P. D. et al. PHENIX: A comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221 (2010).
62. Wen, J., Arakawa, T.&Philo, J. S. Size-exclusion chromatography with on-line light-scattering, absorbance, and refractive index detectors for studying proteins and their interactions. Anal. Biochem. 240, 155-166 (1996).
63. Folta-Stogniew, E. Oligomeric states of proteins determined by size-exclusion chromatography coupled with light scattering, absorbance, and refractive index detectors. Methods Mol. Biol. 328, 97-112 (2006).
64. Sánchez, A. B.&de la Torre, J. C. Rescue of the prototypic Arenavirus LCMV entirely from plasmid. Virology 350, 370-380 (2006).
65. Kunz, S., Calder, L.&Oldstone, M. B. Electron microscopy of an alpha-dystroglycan fragment containing receptor sites for lymphocytic choriomeningitis virus and laminin, and use of the receptoid body as a reagent to neutralize virus. Virology 325, 207-215 (2004).
66. Kunz, S., Sevilla, N., McGavern, D. B., Campbell, K. P.&Oldstone, M. B. Molecular analysis of the interaction of LCMV with its cellular receptor ?-dystroglycan. J. Cell Biol. 155, 301-310 (2001).
67. Parekh, B. S.&Buchmeier, M. J. Proteins of lymphocytic choriomeningitis virus: Antigenic topography of the viral glycoproteins. Virology 153, 168-178 (1986).
68. Bruns, M., Cihak, J., Müller, G.&Lehmann-Grube, F. Lymphocytic choriomeningitis virus. VI. Isolation of a glycoprotein mediating neutralization. Virology 130, 247-251 (1983).
69. Battegay, M. et al. Quantification of lymphocytic choriomeningitis virus with an immunological focus assay in 24-or 96-well plates. J. Virol. Methods 33, 191-198 (1991).