Structural basis for Epstein–Barr virus host cell tropism mediated by gp42 and gHgL entry glycoproteins

Sathiyamoorthy, Karthik; Hu, Yao Xiong; Möhl, Britta S.; Chen, Jia; Longnecker, Richard; Jardetzky, Theodore S.

doi:10.1038/ncomms13557

Title: Structural basis for Epstein–Barr virus host cell tropism mediated by gp42 and gHgL entry glycoproteins

Journal Article · Thu Dec 08 04:00:00 UTC 2016 · Nature Communications

DOI: https://doi.org/10.1038/ncomms13557 · OSTI ID:1339648

^[1]; Hu, Yao Xiong ^[1]; Möhl, Britta S. ^[2]; Chen, Jia ^[2]; Longnecker, Richard ^[2]; Jardetzky, Theodore S. ^[1]

Stanford Univ. School of Medicine, CA (United States). Dept. of Structural Biology
Northwestern Univ., Chicago, IL (United States). Feinberg School of Medicine. Dept. of Microbiology and Immunology

Herpesvirus entry into host cells is mediated by multiple virally encoded receptor binding and membrane fusion glycoproteins. Despite their importance in host cell tropism and associated disease pathology, the underlying and essential interactions between these viral glycoproteins remain poorly understood. For Epstein–Barr virus (EBV), gHgL/gp42 complexes bind HLA class II to activate membrane fusion with B cells, but gp42 inhibits fusion and entry into epithelial cells. To clarify the mechanism by which gp42 controls the cell specificity of EBV infection, in this paper we determined the structure of gHgL/gp42 complex bound to an anti-gHgL antibody (E1D1). The critical regulator of EBV tropism is the gp42 N-terminal domain, which tethers the HLA-binding domain to gHgL by wrapping around the exterior of three gH domains. Both the gp42 N-terminal domain and E1D1 selectively inhibit epithelial-cell fusion; however, they engage distinct surfaces of gHgL. Finally, these observations clarify key determinants of EBV host cell tropism.

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Research Organization:: SLAC National Accelerator Lab., Menlo Park, CA (United States); Stanford Univ. School of Medicine, CA (United States); Northwestern Univ., Chicago, IL (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22); USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23); National Inst. of Health (NIH) (United States). National Inst. of Allergy and Infectious Diseases (NIAID). National Cancer Inst. (NCI). National Inst. of General Medical Sciences (NIGMS); Michigan Economic Development Corporation (United States); Michigan Technology Tri-Corridor (United States)

Grant/Contract Number:: AC02-76SF00515; AC02-06CH11357

OSTI ID:: 1339648

Journal Information:: Nature Communications, Journal Name: Nature Communications Vol. 7; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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EBV glycoproteins: where are we now? Hutt-Fletcher, Lindsey M. Future Virology, Vol. 10, Issue 10 https://doi.org/10.2217/fvl.15.80	journal	October 2015
Herpes Virus Fusion and Entry: A Story with Many Characters Eisenberg, Roselyn J.; Atanasiu, Doina; Cairns, Tina M. Viruses, Vol. 4, Issue 5 https://doi.org/10.3390/v4050800	journal	May 2012
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A site of varicella-zoster virus vulnerability identified by structural studies of neutralizing antibodies bound to the glycoprotein complex gHgL Xing, Yi; Oliver, Stefan L.; Nguyen, TuongVi Proceedings of the National Academy of Sciences, Vol. 112, Issue 19 https://doi.org/10.1073/pnas.1501176112	journal	April 2015
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The Large Groove Found in the gH/gL Structure Is an Important Functional Domain for Epstein-Barr Virus Fusion Chen, J.; Jardetzky, T. S.; Longnecker, R. Journal of Virology, Vol. 87, Issue 7 https://doi.org/10.1128/JVI.03245-12	journal	January 2013
Fusion of Epstein-Barr Virus with Epithelial Cells Can Be Triggered by v 5 in Addition to v 6 and v 8, and Integrin Binding Triggers a Conformational Change in Glycoproteins gHgL Chesnokova, L. S.; Hutt-Fletcher, L. M. Journal of Virology, Vol. 85, Issue 24 https://doi.org/10.1128/JVI.05580-11	journal	September 2011
Mutational Analyses of Epstein-Barr Virus Glycoprotein 42 Reveal Functional Domains Not Involved in Receptor Binding but Required for Membrane Fusion Silva, A. L.; Omerovic, J.; Jardetzky, T. S. Journal of Virology, Vol. 78, Issue 11 https://doi.org/10.1128/JVI.78.11.5946-5956.2004	journal	May 2004
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Overview of the CCP4 suite and current developments. Winn, Martyn D.; Ballard, Charles C.; Cowtan, Kevin D. Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.52322	text	January 2011
Improvement of molecular-replacement models with Sculptor. Bunkóczi, Gábor; Read, Randy J. International Union of Crystallography (IUCr) https://doi.org/10.17863/cam.52324	journalarticle	January 2011
Iterative model building, structure refinement and density modification with the PHENIX AutoBuild wizard. Terwilliger, Thomas C.; Grosse-Kunstleve, Ralf W.; Afonine, Pavel V. International Union of Crystallography (IUCr) https://doi.org/10.17863/cam.52329	journalarticle	January 2008
EBV glycoproteins: where are we now? Hutt-Fletcher, Lindsey M. Future Virology, Vol. 10, Issue 10 https://doi.org/10.2217/fvl.15.80	journal	October 2015
Herpes Virus Fusion and Entry: A Story with Many Characters Eisenberg, Roselyn J.; Atanasiu, Doina; Cairns, Tina M. Viruses, Vol. 4, Issue 5 https://doi.org/10.3390/v4050800	journal	May 2012
Collaboration gets the most out of software Morin, Andrew; Eisenbraun, Ben; Key, Jason eLife, Vol. 2 https://doi.org/10.7554/eLife.01456	journal	September 2013

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Epstein Barr Virus Associated Lymphomas and Epithelia Cancers in Humans Ayee, Richmond; Ofori, Maame Ekua; Wright, Edward Journal of Cancer, Vol. 11, Issue 7 https://doi.org/10.7150/jca.37282	journal	January 2020
Epstein-Barr Virus and the Human Leukocyte Antigen Complex Li, Qingxue; Cohen, Jeffrey I. Current Clinical Microbiology Reports, Vol. 6, Issue 3 https://doi.org/10.1007/s40588-019-00120-9	journal	July 2019
Ephrin receptor A2 is a functional entry receptor for Epstein–Barr virus Chen, Jia; Sathiyamoorthy, Karthik; Zhang, Xianming Nature Microbiology, Vol. 3, Issue 2 https://doi.org/10.1038/s41564-017-0081-7	journal	January 2018
Sequence Variation of Epstein-Barr Virus: Viral Types, Geography, Codon Usage, and Diseases Correia, Samantha; Bridges, Ray; Wegner, Fanny Journal of Virology, Vol. 92, Issue 22 https://doi.org/10.1128/jvi.01132-18	journal	August 2018
Computer-Aided Design of an Epitope-Based Vaccine against Epstein-Barr Virus Alonso-Padilla, Julio; Lafuente, Esther M.; Reche, Pedro A. Journal of Immunology Research, Vol. 2017 https://doi.org/10.1155/2017/9363750	journal	January 2017
A conserved Eph family receptor-binding motif on the gH/gL complex of Kaposi’s sarcoma-associated herpesvirus and rhesus monkey rhadinovirus Großkopf, Anna K.; Ensser, Armin; Neipel, Frank PLOS Pathogens, Vol. 14, Issue 2 https://doi.org/10.1371/journal.ppat.1006912	journal	February 2018
Progress in EBV Vaccines van Zyl, Dwain G.; Mautner, Josef; Delecluse, Henri-Jacques Frontiers in Oncology, Vol. 9 https://doi.org/10.3389/fonc.2019.00104	journal	February 2019
Human MHC-II with Shared Epitope Motifs Are Optimal Epstein-Barr Virus Glycoprotein 42 Ligands—Relation to Rheumatoid Arthritis Trier, Nicole; Izarzugaza, Jose; Chailyan, Anna International Journal of Molecular Sciences, Vol. 19, Issue 1 https://doi.org/10.3390/ijms19010317	journal	January 2018

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