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Title: Visualization of the HIV-1 Env glycan shield across scales

Abstract

The dense array of N-linked glycans on the HIV-1 envelope glycoprotein (Env), known as the “glycan shield,” is a key determinant of immunogenicity, yet intrinsic heterogeneity confounds typical structure–function analysis. Here, we present an integrated approach of single-particle electron cryomicroscopy (cryo-EM), computational modeling, and site-specific mass spectrometry (MS) to probe glycan shield structure and behavior at multiple levels. We found that dynamics lead to an extensive network of interglycan interactions that drive the formation of higher-order structure within the glycan shield. This structure defines diffuse boundaries between buried and exposed protein surface and creates a mapping of potentially immunogenic sites on Env. Analysis of Env expressed in different cell lines revealed how cryo-EM can detect subtle changes in glycan occupancy, composition, and dynamics that impact glycan shield structure and epitope accessibility. Importantly, this identified unforeseen changes in the glycan shield of Env obtained from expression in the same cell line used for vaccine production. Finally, by capturing the enzymatic deglycosylation of Env in a time-resolved manner, we found that highly connected glycan clusters are resistant to digestion and help stabilize the prefusion trimer, suggesting the glycan shield may function beyond immune evasion.

Authors:
ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [1]; ORCiD logo [1]; ORCiD logo [1];  [1]; ORCiD logo [2]; ORCiD logo [1];  [3]; ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [1]
+ Show Author Affiliations
  1. The Scripps Research Inst., La Jolla, CA (United States)
  2. Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
  3. Univ. of Amsterdam (Netherlands)
Publication Date:
Research Org.:
Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)
Sponsoring Org.:
National Institutes of Health (NIH); National Institute of Allergy and Infectious Diseases (NIAID); Bill and Melinda Gates Foundation
OSTI Identifier:
1762730
Report Number(s):
LA-UR-19-30964
Journal ID: ISSN 0027-8424
Grant/Contract Number:  
89233218CNA000001; UM1 AI100663; UM1 AI144462; AI113867; P41GM103533; OPP1100639; OPP1115782; OPP1196345/INV-008813; UM1 AI100645; UM1 AI144371
Resource Type:
Accepted Manuscript
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Volume: 117; Journal Issue: 45; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences
Country of Publication:
United States
Language:
English
Subject:
60 APPLIED LIFE SCIENCES; HIV-1; glycoprotein; cryo-EM; molecular modeling; vaccine

Citation Formats

Berndsen, Zachary T., Chakraborty, Srirupa, Wang, Xiaoning, Cottrell, Christopher A., Torres, Jonathan L., Diedrich, Jolene K., López, Cesar A., Yates III, John R., van Gils, Marit J., Paulson, James C., Gnanakaran, Sandrasegaram, and Ward, Andrew B. Visualization of the HIV-1 Env glycan shield across scales. United States: N. p., 2020. Web. doi:10.1073/pnas.2000260117.
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Berndsen, Zachary T., Chakraborty, Srirupa, Wang, Xiaoning, Cottrell, Christopher A., Torres, Jonathan L., Diedrich, Jolene K., López, Cesar A., Yates III, John R., van Gils, Marit J., Paulson, James C., Gnanakaran, Sandrasegaram, & Ward, Andrew B. Visualization of the HIV-1 Env glycan shield across scales. United States. https://doi.org/10.1073/pnas.2000260117
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Berndsen, Zachary T., Chakraborty, Srirupa, Wang, Xiaoning, Cottrell, Christopher A., Torres, Jonathan L., Diedrich, Jolene K., López, Cesar A., Yates III, John R., van Gils, Marit J., Paulson, James C., Gnanakaran, Sandrasegaram, and Ward, Andrew B. Thu . "Visualization of the HIV-1 Env glycan shield across scales". United States. https://doi.org/10.1073/pnas.2000260117. https://www.osti.gov/servlets/purl/1762730.
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@article{osti_1762730,
title = {Visualization of the HIV-1 Env glycan shield across scales},
author = {Berndsen, Zachary T. and Chakraborty, Srirupa and Wang, Xiaoning and Cottrell, Christopher A. and Torres, Jonathan L. and Diedrich, Jolene K. and López, Cesar A. and Yates III, John R. and van Gils, Marit J. and Paulson, James C. and Gnanakaran, Sandrasegaram and Ward, Andrew B.},
abstractNote = {The dense array of N-linked glycans on the HIV-1 envelope glycoprotein (Env), known as the “glycan shield,” is a key determinant of immunogenicity, yet intrinsic heterogeneity confounds typical structure–function analysis. Here, we present an integrated approach of single-particle electron cryomicroscopy (cryo-EM), computational modeling, and site-specific mass spectrometry (MS) to probe glycan shield structure and behavior at multiple levels. We found that dynamics lead to an extensive network of interglycan interactions that drive the formation of higher-order structure within the glycan shield. This structure defines diffuse boundaries between buried and exposed protein surface and creates a mapping of potentially immunogenic sites on Env. Analysis of Env expressed in different cell lines revealed how cryo-EM can detect subtle changes in glycan occupancy, composition, and dynamics that impact glycan shield structure and epitope accessibility. Importantly, this identified unforeseen changes in the glycan shield of Env obtained from expression in the same cell line used for vaccine production. Finally, by capturing the enzymatic deglycosylation of Env in a time-resolved manner, we found that highly connected glycan clusters are resistant to digestion and help stabilize the prefusion trimer, suggesting the glycan shield may function beyond immune evasion.},
doi = {10.1073/pnas.2000260117},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 45,
volume = 117,
place = {United States},
year = {Thu Oct 22 00:00:00 EDT 2020},
month = {Thu Oct 22 00:00:00 EDT 2020}
}
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Factors limiting the immunogenicity of HIV-1 gp120 envelope glycoproteins
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Differential processing of HIV envelope glycans on the virus and soluble recombinant trimer
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The core trisaccharide of an N-linked glycoprotein intrinsically accelerates folding and enhances stability
journal, February 2009

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Structure-based model of allostery predicts coupling between distant sites
journal, March 2012

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Nonrandom distribution of gp120 N-linked glycosylation sites important for infectivity of human immunodeficiency virus type 1.
journal, March 1992

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journal, September 2001

SWISS-MODEL: homology modelling of protein structures and complexes
journal, May 2018

  • Waterhouse, Andrew; Bertoni, Martino; Bienert, Stefan
  • Nucleic Acids Research, Vol. 46, Issue W1
  • DOI: 10.1093/nar/gky427

Effects of glycosylation on protein structure and dynamics in ribonuclease B and some of its individual glycoforms
journal, November 1993

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    Works referencing / citing this record:

    Quantification of the Resilience and Vulnerability of HIV-1 Native Glycan Shield at Atomistic Detail
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    • Chakraborty, Srirupa; Berndsen, Zachary T.; Hengartner, Nicolas W.
    • SSRN Electronic Journal
    • DOI: 10.2139/ssrn.3606299
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