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Title: Crystal structure, conformational fixation and entry-related interactions of mature ligand-free HIV-1 Env

Journal Article · · Nature Structural & Molecular Biology
DOI:https://doi.org/10.1038/nsmb.3051· OSTI ID:1245840
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  1. National Inst. of Health (NIH), Bethesda, MD (United States). National Inst. of Allergy and Infectious Diseases. Vaccine Research Center
  2. San Diego Biomedical Research Inst., San Diego, CA (United States)
  3. Univ. of Washington, Seattle, WA (United States). Dept. of Medicinal Chemistry
  4. Yale Univ., New Haven, CT (United States). School of Medicine. Dept. of Microbial Pathogenesis
  5. Weill Cornell Medical College of Cornell Univ., New York, NY (United States). Dept. of Physiology and Biophysics
  6. Columbia Univ., New York, NY (United States). Dept. of Biochemistry & Molecular Biophysics. Dept. of Systems Biology
  7. National Inst. of Health (NIH), Bethesda, MD (United States). National Inst. of Allergy and Infectious Diseases. Vaccine Research Center; Duke Univ., Durham, NC (United States). Medical Center. Dept. of Biochemistry
  8. Frederick National Lab. for Cancer Research, Frederick, MD (United States). Leidos Biomedical Research. Cancer Research Technology Program. Electron Microscopy Lab.
  9. New York Univ. (NYU), NY (United States). School of Medicine
  10. Duke Univ., Durham, NC (United States). Medical Center. Dept. of Biochemistry. Dept. of Chemistry. Dept. of Computer Science
  11. Victor Chang Cardiac Research Inst., Darlinghurst, NSW (Australia). Structural and Computational Biology Division
  12. New York Univ. (NYU), NY (United States). School of Medicine; New York Veterans Affairs Harbor Healthcare System, New York, NY (United States)
  13. Johns Hopkins Univ., Baltimore, MD (United States). Dept. of Biology
  14. National Inst. of Health (NIH), Bethesda, MD (United States). National Inst. of Allergy and Infectious Diseases. Vaccine Research Center; Columbia Univ., New York, NY (United States). Dept. of Biochemistry & Molecular Biophysics
  15. National Inst. of Health (NIH), Bethesda, MD (United States). National Inst. of Allergy and Infectious Diseases. Lab. of Immunoregulation
  16. Yale Univ., New Haven, CT (United States). School of Medicine. Dept. of Microbial Pathogenesis; Tufts Univ., Boston, MA (United States). School of Medicine. Dept. of Molecular Biology and Microbiology
+ Show Author Affiliations

As the sole viral antigen on the HIV-1–virion surface, trimeric Env is a focus of vaccine efforts. In this paper, we present the structure of the ligand-free HIV-1–Env trimer, fix its conformation and determine its receptor interactions. Epitope analyses revealed trimeric ligand-free Env to be structurally compatible with broadly neutralizing antibodies but not poorly neutralizing ones. We coupled these compatibility considerations with binding antigenicity to engineer conformationally fixed Envs, including a 201C 433C (DS) variant specifically recognized by broadly neutralizing antibodies. DS-Env retained nanomolar affinity for the CD4 receptor, with which it formed an asymmetric intermediate: a closed trimer bound by a single CD4 without the typical antigenic hallmarks of CD4 induction. Finally, antigenicity-guided structural design can thus be used both to delineate mechanism and to fix conformation, with DS-Env trimers in virus-like-particle and soluble formats providing a new generation of vaccine antigens.

Research Organization:
National Institutes of Health (NIH), Bethesda, MD (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Basic Energy Sciences (BES); National Inst. of Health (NIH) (United States); National Science Foundation (NSF); Bill and Melinda Gates Foundation (United States); Australian Research Council (Australia)
Contributing Organization:
San Diego Biomedical Research Inst., San Diego, CA (United States); Univ. of Washington, Seattle, WA (United States); Yale Univ., New Haven, CT (United States); Weill Cornell Medical College of Cornell Univ., New York, NY (United States); Columbia Univ., New York, NY (United States); Duke Univ., Durham, NC (United States); Frederick National Lab. for Cancer Research, Frederick, MD (United States); New York Univ. (NYU), NY (United States); Victor Chang Cardiac Research Inst., Darlinghurst, NSW (Australia); New York Veterans Affairs Harbor Healthcare System, New York, NY (United States); Johns Hopkins Univ., Baltimore, MD (United States); Tufts Univ., Boston, MA (United States)
Grant/Contract Number:
W-31-109-Eng-38; HHSN261200800001E; P01-AI100151; P01-AI104722; R01-AI93278; R21-AI100696; R21-AI112389; R33-AI84714; P01-GM56550; R01-GM78031; R01-GM98859; PO1-HL59725; MCB-1157506; OPP1033102; DP130102219
OSTI ID:
1245840
Journal Information:
Nature Structural & Molecular Biology, Vol. 22, Issue 7; ISSN 1545-9993
Publisher:
Nature Publishing GroupCopyright Statement
Country of Publication:
United States
Language:
ENGLISH
Citation Metrics:
Cited by: 259 works
Citation information provided by
Web of Science

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Open and closed structures reveal allostery and pliability in the HIV-1 envelope spike journal July 2017
Global site-specific N-glycosylation analysis of HIV envelope glycoprotein journal March 2017
Structures of HIV-1 Env V1V2 with broadly neutralizing antibodies reveal commonalities that enable vaccine design journal December 2015
Iterative structure-based improvement of a fusion-glycoprotein vaccine against RSV journal August 2016
Quaternary contact in the initial interaction of CD4 with the HIV-1 envelope trimer journal February 2017
Structure-based design of native-like HIV-1 envelope trimers to silence non-neutralizing epitopes and eliminate CD4 binding journal November 2017
Structural characterization of a highly-potent V3-glycan broadly neutralizing antibody bound to natively-glycosylated HIV-1 envelope journal March 2018
Capturing the inherent structural dynamics of the HIV-1 envelope glycoprotein fusion peptide journal February 2019
A sequestered fusion peptide in the structure of an HIV-1 transmitted founder envelope trimer journal February 2019
Difficult-to-neutralize global HIV-1 isolates are neutralized by antibodies targeting open envelope conformations journal July 2019
Disruption of the HIV-1 Envelope allosteric network blocks CD4-induced rearrangements journal January 2020
Structural basis of coreceptor recognition by HIV-1 envelope spike journal December 2018
A dynamic three-step mechanism drives the HIV-1 pre-fusion reaction journal August 2018
Insights into the molecular mechanism underlying CD4-dependency and neutralization sensitivity of HIV-1: a comparative molecular dynamics study on gp120s from isolates with different phenotypes journal January 2018
Opening dynamics of HIV-1 gp120 upon receptor binding is dictated by a key hydrophobic core journal January 2019
Cryo-EM structure of a CD4-bound open HIV-1 envelope trimer reveals structural rearrangements of the gp120 V1V2 loop journal October 2016
Stabilization of the V2 loop improves the presentation of V2 loop–associated broadly neutralizing antibody epitopes on HIV-1 envelope trimers journal February 2019
Influence of protein fold stability on immunogenicity and its implications for vaccine design journal March 2017
Native-like Env trimers as a platform for HIV-1 vaccine design journal January 2017
Germline-targeting immunogens journal January 2017
Cryo-EM structure of a native, fully glycosylated, cleaved HIV-1 envelope trimer journal March 2016
Structural basis for antibody-mediated neutralization of Lassa virus journal June 2017
Conformational Engineering of HIV-1 Env Based on Mutational Tolerance in the CD4 and PG16 Bound States journal March 2019
Monoclonal Antibody 2C6 Targets a Cross-Clade Conformational Epitope in gp41 with Highly Active Antibody-Dependent Cell Cytotoxicity journal June 2019
The Tryptophan-Rich Motif of HIV-1 gp41 Can Interact with the N-Terminal Deep Pocket Site: New Insights into the Structure and Function of gp41 and Its Inhibitors journal October 2019
Influences on the Design and Purification of Soluble, Recombinant Native-Like HIV-1 Envelope Glycoprotein Trimers journal August 2015
Native Conformation and Canonical Disulfide Bond Formation Are Interlinked Properties of HIV-1 Env Glycoproteins journal December 2015
The Polar Region of the HIV-1 Envelope Protein Determines Viral Fusion and Infectivity by Stabilizing the gp120-gp41 Association journal January 2019
Structural and Computational Biology in the Design of Immunogenic Vaccine Antigens journal January 2015
Exploiting glycan topography for computational design of Env glycoprotein antigenicity journal April 2018
Minimally Mutated HIV-1 Broadly Neutralizing Antibodies to Guide Reductionist Vaccine Design journal August 2016
Similarities and differences between native HIV-1 envelope glycoprotein trimers and stabilized soluble trimer mimetics journal July 2019
In silico Analysis of HIV-1 Env-gp120 Reveals Structural Bases for Viral Adaptation in Growth-Restrictive Cells journal February 2016
Advances in HIV-1 Vaccine Development journal April 2018
HIV-1 Env trimer opens through an asymmetric intermediate in which individual protomers adopt distinct conformations journal March 2018
HIV-1 Envelope and MPER Antibody Structures in Lipid Assemblies journal April 2020
Presenting native-like trimeric HIV-1 antigens with self-assembling nanoparticles journal June 2016
HIV envelope V3 region mimic embodies key features of a broadly neutralizing antibody lineage epitope journal March 2018
Common helical V1V2 conformations of HIV-1 Envelope expose the α4β7 binding site on intact virions journal October 2018
Envelope residue 375 substitutions in simian–human immunodeficiency viruses enhance CD4 binding and replication in rhesus macaques journal May 2016
Structural basis for membrane anchoring of HIV-1 envelope spike journal June 2016
Complete functional mapping of infection- and vaccine-elicited antibodies against the fusion peptide of HIV journal July 2018
Quantification of the Resilience and Vulnerability of HIV-1 Native Glycan Shield at Atomistic Detail journal January 2020
Relationships Between HIV-Mediated Chemokine Coreceptor Signaling, Cofilin Hyperactivation, Viral Tropism Switch and HIV-Mediated CD4 Depletion journal January 2020
Associating HIV-1 envelope glycoprotein structures with states on the virus observed by smFRET journal April 2019
Epitope-based vaccine design yields fusion peptide-directed antibodies that neutralize diverse strains of HIV-1 journal June 2018
Targeted selection of HIV-specific antibody mutations by engineering B cell maturation journal December 2019
Rationally Designed Vaccines Targeting the V2 Region of HIV-1 gp120 Induce a Focused, Cross-Clade-Reactive, Biologically Functional Antibody Response journal September 2016
Maternal Binding and Neutralizing IgG Responses Targeting the C-Terminal Region of the V3 Loop Are Predictive of Reduced Peripartum HIV-1 Transmission Risk journal February 2017
Exploitation of glycosylation in enveloped virus pathobiology journal October 2019
Soluble Prefusion Closed DS-SOSIP.664-Env Trimers of Diverse HIV-1 Strains journal December 2017
The Chimpanzee SIV Envelope Trimer: Structure and Deployment as an HIV Vaccine Template journal May 2019
Stoichiometric Analyses of Soluble CD4 to Native-like HIV-1 Envelope by Single-Molecule Fluorescence Spectroscopy journal October 2019
VRC34-Antibody Lineage Development Reveals How a Required Rare Mutation Shapes the Maturation of a Broad HIV-Neutralizing Lineage journal April 2020
Tyrosine-sulfated V2 peptides inhibit HIV-1 infection via coreceptor mimicry journal August 2016
Protein and Glycan Mimicry in HIV Vaccine Design journal May 2019
Model Building and Refinement of a Natively Glycosylated HIV-1 Env Protein by High-Resolution Cryoelectron Microscopy journal October 2015
Microsecond Dynamics and Network Analysis of the HIV-1 SOSIP Env Trimer Reveal Collective Behavior and Conserved Microdomains of the Glycan Shield journal October 2017
Developability Assessment of Physicochemical Properties and Stability Profiles of HIV-1 BG505 SOSIP.664 and BG505 SOSIP.v4.1-GT1.1 gp140 Envelope Glycoprotein Trimers as Candidate Vaccine Antigens journal July 2019
Uncleaved prefusion-optimized gp140 trimers derived from analysis of HIV-1 envelope metastability journal June 2016
Determinants of Tenascin-C and HIV-1 envelope binding and neutralization journal July 2019
Identification and specificity of broadly neutralizing antibodies against HIV journal January 2017
HIV-1 vaccine design through minimizing envelope metastability journal November 2018
Structure/Function Studies Involving the V3 Region of the HIV-1 Envelope Delineate Multiple Factors That Affect Neutralization Sensitivity journal October 2015
Chemical Cross-Linking Stabilizes Native-Like HIV-1 Envelope Glycoprotein Trimer Antigens journal January 2016
Differential Antibody Responses to Conserved HIV-1 Neutralizing Epitopes in the Context of Multivalent Scaffolds and Native-Like gp140 Trimers journal February 2017
Stabilizing HIV-1 envelope glycoprotein trimers to induce neutralizing antibodies journal September 2018
Human Antibodies that Recognize Novel Immunodominant Quaternary Epitopes on the HIV-1 Env Protein journal July 2016
Thermostability of Well-Ordered HIV Spikes Correlates with the Elicitation of Autologous Tier 2 Neutralizing Antibodies journal August 2016
Receptor Activation of HIV-1 Env Leads to Asymmetric Exposure of the gp41 Trimer journal December 2016
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Related Subjects

59 BASIC BIOLOGICAL SCIENCES
60 APPLIED LIFE SCIENCES
Computational biology and bioinformatics
Immunology
Viral membrane fusion
X-ray crystallography