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Title: Structure and immune recognition of trimeric pre-fusion HIV-1 Env

Abstract

The human immunodeficiency virus type 1 (HIV-1) envelope (Env) spike, comprising three gp120 and three gp41 subunits, is a conformational machine that facilitates HIV-1 entry by rearranging from a mature unliganded state, through receptor-bound intermediates, to a post-fusion state. As the sole viral antigen on the HIV-1 virion surface, Env is both the target of neutralizing antibodies and a focus of vaccine efforts. Here we report the structure at 3.5 Å resolution for an HIV-1 Env trimer captured in a mature closed state by antibodies PGT122 and 35O22. This structure reveals the pre-fusion conformation of gp41, indicates rearrangements needed for fusion activation, and defines parameters of immune evasion and immune recognition. Pre-fusion gp41 encircles amino- and carboxy-terminal strands of gp120 with four helices that form a membrane-proximal collar, fastened by insertion of a fusion peptide-proximal methionine into a gp41-tryptophan clasp. Spike rearrangements required for entry involve opening the clasp and expelling the termini. In conclusion, N-linked glycosylation and sequence-variable regions cover the pre-fusion closed spike; we used chronic cohorts to map the prevalence and location of effective HIV-1-neutralizing responses, which were distinguished by their recognition of N-linked glycan and tolerance for epitope-sequence variation.

Authors:
 [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [2];  [1];  [1];  [3];  [4] more »;  [1];  [2];  [5];  [6];  [5];  [1];  [1] « less
+ Show Author Affiliations
  1. National Inst. of Health (NIH), Bethesda, MD (United States). National Inst. of Allergy and Infectious Diseases, Vaccine Research Center, Lab. of Immunoregulation
  2. National Health Lab. Service (NHLS), Johannesburg (South Africa). National Inst. for Communicable Diseases, Center for HIV and STIs; Univ. of the Witwatersrand, Johannesburg (South Africa); Univ. of KwaZulu-Natal, Durban (South Africa). Centre for the AIDS Programme of Research in South Africa (CAPRISA)
  3. Univ. of North Carolina, Chapel Hill, NC (United States). Dept. of Medicine, Epidemiology, Microbiology and Immunology
  4. Duke Univ., Durham, NC (United States). School of Medicine, Human Vaccine Inst., Dept. of Medicine, Surgery, Pediatrics and Immunology; Duke Univ., Durham, NC (United States). Center for HIV/AIDS Vaccine Immunology-Immunogen Discovery
  5. Yale Univ., New Haven, CT (United States). School of Medicine, Dept. of Microbial Pathogenesis
  6. Cornell Univ., Ithaca, NY (United States). Weill Cornell Medical College, Dept. of Physiology and Biophysics
Publication Date:
Research Org.:
Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)
Sponsoring Org.:
National Institutes of Health (NIH); USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1165315
Grant/Contract Number:  
W-31-109-Eng-38
Resource Type:
Accepted Manuscript
Journal Name:
Nature (London)
Additional Journal Information:
Journal Name: Nature (London); Journal Volume: 514; Journal Issue: 7523; Journal ID: ISSN 0028-0836
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
ENGLISH
Subject:
59 BASIC BIOLOGICAL SCIENCES; 60 APPLIED LIFE SCIENCES; HIV infections; X-ray crystallography; Protein vaccines; Protein function predictions

Citation Formats

Pancera, Marie, Zhou, Tongqing, Druz, Aliaksandr, Georgiev, Ivelin S., Soto, Cinque, Gorman, Jason, Huang, Jinghe, Acharya, Priyamvada, Chuang, Gwo-Yu, Ofek, Gilad, Stewart-Jones, Guillaume B. E., Stuckey, Jonathan, Bailer, Robert T., Joyce, M. Gordon, Louder, Mark K., Tumba, Nancy, Yang, Yongping, Zhang, Baoshan, Cohen, Myron S., Haynes, Barton F., Mascola, John R., Morris, Lynn, Munro, James B., Blanchard, Scott C., Mothes, Walther, Connors, Mark, and Kwong, Peter D. Structure and immune recognition of trimeric pre-fusion HIV-1 Env. United States: N. p., 2014. Web. doi:10.1038/nature13808.
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Pancera, Marie, Zhou, Tongqing, Druz, Aliaksandr, Georgiev, Ivelin S., Soto, Cinque, Gorman, Jason, Huang, Jinghe, Acharya, Priyamvada, Chuang, Gwo-Yu, Ofek, Gilad, Stewart-Jones, Guillaume B. E., Stuckey, Jonathan, Bailer, Robert T., Joyce, M. Gordon, Louder, Mark K., Tumba, Nancy, Yang, Yongping, Zhang, Baoshan, Cohen, Myron S., Haynes, Barton F., Mascola, John R., Morris, Lynn, Munro, James B., Blanchard, Scott C., Mothes, Walther, Connors, Mark, & Kwong, Peter D. Structure and immune recognition of trimeric pre-fusion HIV-1 Env. United States. https://doi.org/10.1038/nature13808
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Pancera, Marie, Zhou, Tongqing, Druz, Aliaksandr, Georgiev, Ivelin S., Soto, Cinque, Gorman, Jason, Huang, Jinghe, Acharya, Priyamvada, Chuang, Gwo-Yu, Ofek, Gilad, Stewart-Jones, Guillaume B. E., Stuckey, Jonathan, Bailer, Robert T., Joyce, M. Gordon, Louder, Mark K., Tumba, Nancy, Yang, Yongping, Zhang, Baoshan, Cohen, Myron S., Haynes, Barton F., Mascola, John R., Morris, Lynn, Munro, James B., Blanchard, Scott C., Mothes, Walther, Connors, Mark, and Kwong, Peter D. Wed . "Structure and immune recognition of trimeric pre-fusion HIV-1 Env". United States. https://doi.org/10.1038/nature13808. https://www.osti.gov/servlets/purl/1165315.
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@article{osti_1165315,
title = {Structure and immune recognition of trimeric pre-fusion HIV-1 Env},
author = {Pancera, Marie and Zhou, Tongqing and Druz, Aliaksandr and Georgiev, Ivelin S. and Soto, Cinque and Gorman, Jason and Huang, Jinghe and Acharya, Priyamvada and Chuang, Gwo-Yu and Ofek, Gilad and Stewart-Jones, Guillaume B. E. and Stuckey, Jonathan and Bailer, Robert T. and Joyce, M. Gordon and Louder, Mark K. and Tumba, Nancy and Yang, Yongping and Zhang, Baoshan and Cohen, Myron S. and Haynes, Barton F. and Mascola, John R. and Morris, Lynn and Munro, James B. and Blanchard, Scott C. and Mothes, Walther and Connors, Mark and Kwong, Peter D.},
abstractNote = {The human immunodeficiency virus type 1 (HIV-1) envelope (Env) spike, comprising three gp120 and three gp41 subunits, is a conformational machine that facilitates HIV-1 entry by rearranging from a mature unliganded state, through receptor-bound intermediates, to a post-fusion state. As the sole viral antigen on the HIV-1 virion surface, Env is both the target of neutralizing antibodies and a focus of vaccine efforts. Here we report the structure at 3.5 Å resolution for an HIV-1 Env trimer captured in a mature closed state by antibodies PGT122 and 35O22. This structure reveals the pre-fusion conformation of gp41, indicates rearrangements needed for fusion activation, and defines parameters of immune evasion and immune recognition. Pre-fusion gp41 encircles amino- and carboxy-terminal strands of gp120 with four helices that form a membrane-proximal collar, fastened by insertion of a fusion peptide-proximal methionine into a gp41-tryptophan clasp. Spike rearrangements required for entry involve opening the clasp and expelling the termini. In conclusion, N-linked glycosylation and sequence-variable regions cover the pre-fusion closed spike; we used chronic cohorts to map the prevalence and location of effective HIV-1-neutralizing responses, which were distinguished by their recognition of N-linked glycan and tolerance for epitope-sequence variation.},
doi = {10.1038/nature13808},
journal = {Nature (London)},
number = 7523,
volume = 514,
place = {United States},
year = {Wed Oct 08 00:00:00 EDT 2014},
month = {Wed Oct 08 00:00:00 EDT 2014}
}
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    • DOI: 10.1186/s12977-016-0279-4

    Buffering deleterious polymorphisms in highly constrained parts of HIV-1 envelope by flexible regions
    journal, July 2016

    Enhanced antibody-mediated neutralization of HIV-1 variants that are resistant to fusion inhibitors
    journal, September 2016

    Sequential trafficking of Env and Gag to HIV-1 T cell virological synapses revealed by live imaging
    journal, January 2019

    Optimal Sequential Immunization Can Focus Antibody Responses against Diversity Loss and Distraction
    journal, January 2017

    Coevolution Analysis of HIV-1 Envelope Glycoprotein Complex
    journal, November 2015

    Heterogeneous Evolution of HIV-1 CRF01_AE in Men Who Have Sex with Men (MSM) and Other Populations in China
    journal, December 2015

    Human Antibodies that Recognize Novel Immunodominant Quaternary Epitopes on the HIV-1 Env Protein
    journal, July 2016

    Antigenic characterization of the human immunodeficiency virus (HIV-1) envelope glycoprotein precursor incorporated into nanodiscs
    journal, February 2017

    Identification of variant HIV envelope proteins with enhanced affinities for precursors to anti-gp41 broadly neutralizing antibodies
    journal, September 2019

    Comprehensive Antigenic Map of a Cleaved Soluble HIV-1 Envelope Trimer
    journal, March 2015

    Human Non-neutralizing HIV-1 Envelope Monoclonal Antibodies Limit the Number of Founder Viruses during SHIV Mucosal Infection in Rhesus Macaques
    journal, August 2015

    Cryo-electron Microscopy Structure of the Native Prototype Foamy Virus Glycoprotein and Virus Architecture
    journal, July 2016

    Thermostability of Well-Ordered HIV Spikes Correlates with the Elicitation of Autologous Tier 2 Neutralizing Antibodies
    journal, August 2016

    Sequential and Simultaneous Immunization of Rabbits with HIV-1 Envelope Glycoprotein SOSIP.664 Trimers from Clades A, B and C
    journal, September 2016

    Structure and Recognition of a Novel HIV-1 gp120-gp41 Interface Antibody that Caused MPER Exposure through Viral Escape
    journal, January 2017

    Receptor Activation of HIV-1 Env Leads to Asymmetric Exposure of the gp41 Trimer
    journal, December 2016

    Experimental Estimation of the Effects of All Amino-Acid Mutations to HIV’s Envelope Protein on Viral Replication in Cell Culture
    journal, December 2016

    Mapping Polyclonal HIV-1 Antibody Responses via Next-Generation Neutralization Fingerprinting
    journal, January 2017

    Targeted N-glycan deletion at the receptor-binding site retains HIV Env NFL trimer integrity and accelerates the elicited antibody response
    journal, September 2017

    Broadly resistant HIV-1 against CD4-binding site neutralizing antibodies
    journal, June 2019

    Carbohydrates in Cyberspace
    journal, June 2015

    Structure-Guided Redesign Improves NFL HIV Env Trimer Integrity and Identifies an Inter-Protomer Disulfide Permitting Post-Expression Cleavage
    journal, July 2018

    • Yang, Lifei; Sharma, Shailendra Kumar; Cottrell, Christopher
    • Frontiers in Immunology, Vol. 9
    • DOI: 10.3389/fimmu.2018.01631

    Cross Type Neutralizing Antibodies Detected in a Unique HIV-2 Infected Individual From India
    journal, December 2018

    • Vidyavijayan, K. K.; Cheedarala, Narayanaiah; Babu, Hemalatha
    • Frontiers in Immunology, Vol. 9
    • DOI: 10.3389/fimmu.2018.02841

    In silico Analysis of HIV-1 Env-gp120 Reveals Structural Bases for Viral Adaptation in Growth-Restrictive Cells
    journal, February 2016

    Super Potent Bispecific Llama VHH Antibodies Neutralize HIV via a Combination of gp41 and gp120 Epitopes
    journal, June 2019

    • Strokappe, Nika M.; Hock, Miriam; Rutten, Lucy
    • Antibodies, Vol. 8, Issue 2
    • DOI: 10.3390/antib8020038

    Engineering and Characterization of a Fluorescent Native-Like HIV-1 Envelope Glycoprotein Trimer
    journal, October 2015

    • Sliepen, Kwinten; van Montfort, Thijs; Ozorowski, Gabriel
    • Biomolecules, Vol. 5, Issue 4
    • DOI: 10.3390/biom5042919

    Protein Crystallography in Vaccine Research and Development
    journal, June 2015

    • Malito, Enrico; Carfi, Andrea; Bottomley, Matthew
    • International Journal of Molecular Sciences, Vol. 16, Issue 12
    • DOI: 10.3390/ijms160613106

    Structure-Based Reverse Vaccinology Failed in the Case of HIV Because it Disregarded Accepted Immunological Theory
    journal, September 2016

    • Van Regenmortel, Marc
    • International Journal of Molecular Sciences, Vol. 17, Issue 9
    • DOI: 10.3390/ijms17091591

    Antiviral Therapy by HIV-1 Broadly Neutralizing and Inhibitory Antibodies
    journal, November 2016

    • Zhang, Zhiqing; Li, Shaowei; Gu, Ying
    • International Journal of Molecular Sciences, Vol. 17, Issue 11
    • DOI: 10.3390/ijms17111901

    HIV Vaccination: A Roadmap among Advancements and Concerns
    journal, April 2018

    • Trovato, Maria; D’Apice, Luciana; Prisco, Antonella
    • International Journal of Molecular Sciences, Vol. 19, Issue 4
    • DOI: 10.3390/ijms19041241

    Overview of the Structure–Function Relationships of Mannose-Specific Lectins from Plants, Algae and Fungi
    journal, January 2019

    • Barre, Annick; Bourne, Yves; Van Damme, Els
    • International Journal of Molecular Sciences, Vol. 20, Issue 2
    • DOI: 10.3390/ijms20020254

    Structural Basis for Epitopes in the gp120 Cluster A Region that Invokes Potent Effector Cell Activity
    journal, January 2019

    • Tolbert, William; Sherburn, Rebekah; Van, Verna
    • Viruses, Vol. 11, Issue 1
    • DOI: 10.3390/v11010069

    Identification of HIV-1 Envelope Mutations that Enhance Entry Using Macaque CD4 and CCR5
    journal, February 2020

    • Roop, Jeremy I.; Cassidy, Noah A.; Dingens, Adam S.
    • Viruses, Vol. 12, Issue 2
    • DOI: 10.3390/v12020241

    Current Peptide and Protein Candidates Challenging HIV Therapy beyond the Vaccine Era
    journal, September 2017

    • Chupradit, Koollawat; Moonmuang, Sutpirat; Nangola, Sawitree
    • Viruses, Vol. 9, Issue 10
    • DOI: 10.3390/v9100281

    Current Advances in Virus-Like Particles as a Vaccination Approach against HIV Infection
    journal, January 2016

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