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Title: Fusion peptide of HIV-1 as a site of vulnerability to neutralizing antibody

Abstract

The HIV-1 fusion peptide, comprising 15 to 20 hydrophobic residues at the N terminus of the Env-gp41 subunit, is a critical component of the virus-cell entry machinery. In this paper, we report the identification of a neutralizing antibody, N123-VRC34.01, which targets the fusion peptide and blocks viral entry by inhibiting conformational changes in gp120 and gp41 subunits of Env required for entry. Crystal structures of N123-VRC34.01 liganded to the fusion peptide, and to the full Env trimer, revealed an epitope consisting of the N-terminal eight residues of the gp41 fusion peptide and glycan N88 of gp120, and molecular dynamics showed that the N-terminal portion of the fusion peptide can be solvent-exposed. Finally, these results reveal the fusion peptide to be a neutralizing antibody epitope and thus a target for vaccine design.

Authors:
 [1];  [1];  [1];  [1];  [2];  [1];  [3];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [4];  [1] more »;  [1];  [5];  [1];  [1];  [1];  [1];  [6];  [5];  [7];  [8];  [4];  [3];  [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
  2. Univ. of California, San Francisco, CA (United States). Dept. of Pharmaceutical Chemistry
  3. The Scripps Research Inst., La Jolla, CA (United States). Dept. of Integrative Structural and Computational Biology. Center for HIV/AIDS Vaccine Immunology and Immunogen Discovery. Neutralizing Antibody Center. International AIDS Vaccine Initiative
  4. National Inst. of Health (NIH), Bethesda, MD (United States). National Inst. of Allergy and Infectious Diseases. Lab. of Immunoregulation. HIV-Specific Immunity Section
  5. Yale Univ., New Haven, CT (United States). School of Medicine. Dept. of Microbial Pathogenesis
  6. Weill Cornell Medical College of Cornell Univ., New York, NY (United States). Dept. of Physiology and Biophysics
  7. The Scripps Research Inst., La Jolla, CA (United States). Center for HIV/AIDS Vaccine Immunology and Immunogen Discovery. International AIDS Vaccine Initiative Neutralizing Antibody Center. Dept. of Immunology and Microbial Science; Massachusetts Inst. of Technology and Harvard Univ., Boston, MA (United States). Ragon Inst. of Massachusetts General Hospital
  8. International AIDS Vaccine Initiative, New York, NY (United States)
Publication Date:
Research Org.:
National Institutes of Health (NIH), Bethesda, MD (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES); National Inst. of Health (NIH) (United States); International AIDS Vaccine Initiative’s (IAVI) Neutralizing Antibody Consortium (United States)
Contributing Org.:
Univ. of California, San Francisco, CA (United States); The Scripps Research Inst., La Jolla, CA (United States); Yale Univ., New Haven, CT (United States); Weill Cornell Medical College of Cornell Univ., New York, NY (United States); Massachusetts Inst. of Technology and Harvard Univ., Boston, MA (United States); International AIDS Vaccine Initiative, New York, NY (United States)
OSTI Identifier:
1257468
Grant/Contract Number:  
W-31-109-Eng-38; R01GM079238; P01GM56550; R01GM116654
Resource Type:
Accepted Manuscript
Journal Name:
Science
Additional Journal Information:
Journal Volume: 352; Journal Issue: 6287; Journal ID: ISSN 0036-8075
Publisher:
AAAS
Country of Publication:
United States
Language:
ENGLISH
Subject:
59 BASIC BIOLOGICAL SCIENCES; 60 APPLIED LIFE SCIENCES

Citation Formats

Kong, Rui, Xu, Kai, Zhou, Tongqing, Acharya, Priyamvada, Lemmin, Thomas, Liu, Kevin, Ozorowski, Gabriel, Soto, Cinque, Taft, Justin D., Bailer, Robert T., Cale, Evan M., Chen, Lei, Choi, Chang W., Chuang, Gwo-Yu, Doria-Rose, Nicole A., Druz, Aliaksandr, Georgiev, Ivelin S., Gorman, Jason, Huang, Jinghe, Joyce, M. Gordon, Louder, Mark K., Ma, Xiaochu, McKee, Krisha, O'Dell, Sijy, Pancera, Marie, Yang, Yongping, Blanchard, Scott C., Mothes, Walther, Burton, Dennis R., Koff, Wayne C., Connors, Mark, Ward, Andrew B., Kwong, Peter D., and Mascola, John R. Fusion peptide of HIV-1 as a site of vulnerability to neutralizing antibody. United States: N. p., 2016. Web. doi:10.1126/science.aae0474.
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Kong, Rui, Xu, Kai, Zhou, Tongqing, Acharya, Priyamvada, Lemmin, Thomas, Liu, Kevin, Ozorowski, Gabriel, Soto, Cinque, Taft, Justin D., Bailer, Robert T., Cale, Evan M., Chen, Lei, Choi, Chang W., Chuang, Gwo-Yu, Doria-Rose, Nicole A., Druz, Aliaksandr, Georgiev, Ivelin S., Gorman, Jason, Huang, Jinghe, Joyce, M. Gordon, Louder, Mark K., Ma, Xiaochu, McKee, Krisha, O'Dell, Sijy, Pancera, Marie, Yang, Yongping, Blanchard, Scott C., Mothes, Walther, Burton, Dennis R., Koff, Wayne C., Connors, Mark, Ward, Andrew B., Kwong, Peter D., & Mascola, John R. Fusion peptide of HIV-1 as a site of vulnerability to neutralizing antibody. United States. https://doi.org/10.1126/science.aae0474
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Kong, Rui, Xu, Kai, Zhou, Tongqing, Acharya, Priyamvada, Lemmin, Thomas, Liu, Kevin, Ozorowski, Gabriel, Soto, Cinque, Taft, Justin D., Bailer, Robert T., Cale, Evan M., Chen, Lei, Choi, Chang W., Chuang, Gwo-Yu, Doria-Rose, Nicole A., Druz, Aliaksandr, Georgiev, Ivelin S., Gorman, Jason, Huang, Jinghe, Joyce, M. Gordon, Louder, Mark K., Ma, Xiaochu, McKee, Krisha, O'Dell, Sijy, Pancera, Marie, Yang, Yongping, Blanchard, Scott C., Mothes, Walther, Burton, Dennis R., Koff, Wayne C., Connors, Mark, Ward, Andrew B., Kwong, Peter D., and Mascola, John R. Fri . "Fusion peptide of HIV-1 as a site of vulnerability to neutralizing antibody". United States. https://doi.org/10.1126/science.aae0474. https://www.osti.gov/servlets/purl/1257468.
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@article{osti_1257468,
title = {Fusion peptide of HIV-1 as a site of vulnerability to neutralizing antibody},
author = {Kong, Rui and Xu, Kai and Zhou, Tongqing and Acharya, Priyamvada and Lemmin, Thomas and Liu, Kevin and Ozorowski, Gabriel and Soto, Cinque and Taft, Justin D. and Bailer, Robert T. and Cale, Evan M. and Chen, Lei and Choi, Chang W. and Chuang, Gwo-Yu and Doria-Rose, Nicole A. and Druz, Aliaksandr and Georgiev, Ivelin S. and Gorman, Jason and Huang, Jinghe and Joyce, M. Gordon and Louder, Mark K. and Ma, Xiaochu and McKee, Krisha and O'Dell, Sijy and Pancera, Marie and Yang, Yongping and Blanchard, Scott C. and Mothes, Walther and Burton, Dennis R. and Koff, Wayne C. and Connors, Mark and Ward, Andrew B. and Kwong, Peter D. and Mascola, John R.},
abstractNote = {The HIV-1 fusion peptide, comprising 15 to 20 hydrophobic residues at the N terminus of the Env-gp41 subunit, is a critical component of the virus-cell entry machinery. In this paper, we report the identification of a neutralizing antibody, N123-VRC34.01, which targets the fusion peptide and blocks viral entry by inhibiting conformational changes in gp120 and gp41 subunits of Env required for entry. Crystal structures of N123-VRC34.01 liganded to the fusion peptide, and to the full Env trimer, revealed an epitope consisting of the N-terminal eight residues of the gp41 fusion peptide and glycan N88 of gp120, and molecular dynamics showed that the N-terminal portion of the fusion peptide can be solvent-exposed. Finally, these results reveal the fusion peptide to be a neutralizing antibody epitope and thus a target for vaccine design.},
doi = {10.1126/science.aae0474},
journal = {Science},
number = 6287,
volume = 352,
place = {United States},
year = {Fri May 13 00:00:00 EDT 2016},
month = {Fri May 13 00:00:00 EDT 2016}
}
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    An HIV-1 antibody from an elite neutralizer implicates the fusion peptide as a site of vulnerability
    journal, November 2016

    • van Gils, Marit J.; van den Kerkhof, Tom L. G. M.; Ozorowski, Gabriel
    • Nature Microbiology, Vol. 2, Issue 2
    • DOI: 10.1038/nmicrobiol.2016.199

    Monoclonal Antibody 2C6 Targets a Cross-Clade Conformational Epitope in gp41 with Highly Active Antibody-Dependent Cell Cytotoxicity
    journal, June 2019

    • Sojar, Hakimuddin; Baron, Sarah; Sullivan, Jonathan T.
    • Journal of Virology, Vol. 93, Issue 17
    • DOI: 10.1128/jvi.00772-19

    Antibody-virus co-evolution in HIV infection: paths for HIV vaccine development
    journal, January 2017

    • Bonsignori, Mattia; Liao, Hua-Xin; Gao, Feng
    • Immunological Reviews, Vol. 275, Issue 1
    • DOI: 10.1111/imr.12509

    The HIV-1 envelope glycoprotein structure: nailing down a moving target
    journal, January 2017

    • Ward, Andrew B.; Wilson, Ian A.
    • Immunological Reviews, Vol. 275, Issue 1
    • DOI: 10.1111/imr.12507

    Structural basis for broad neutralization of ebolaviruses by an antibody targeting the glycoprotein fusion loop
    journal, September 2018

    Extensive dissemination and intraclonal maturation of HIV Env vaccine-induced B cell responses
    journal, November 2019

    • Phad, Ganesh E.; Pushparaj, Pradeepa; Tran, Karen
    • Journal of Experimental Medicine, Vol. 217, Issue 2
    • DOI: 10.1084/jem.20191155

    Native-like Env trimers as a platform for HIV-1 vaccine design
    journal, January 2017

    • Sanders, Rogier W.; Moore, John P.
    • Immunological Reviews, Vol. 275, Issue 1
    • DOI: 10.1111/imr.12481

    Conformational Plasticity in the HIV-1 Fusion Peptide Facilitates Recognition by Broadly Neutralizing Antibodies
    journal, June 2019

    Protein and Glycan Mimicry in HIV Vaccine Design
    journal, May 2019

    • Seabright, Gemma E.; Doores, Katie J.; Burton, Dennis R.
    • Journal of Molecular Biology, Vol. 431, Issue 12
    • DOI: 10.1016/j.jmb.2019.04.016

    Peptide-Based Vaccines: Current Progress and Future Challenges
    journal, December 2019

    Identification of a novel broadly HIV-1-neutralizing antibody from a CRF01_AE-infected Chinese donor
    journal, November 2018

    HIV envelope V3 region mimic embodies key features of a broadly neutralizing antibody lineage epitope
    journal, March 2018

    Structural characterization of a highly-potent V3-glycan broadly neutralizing antibody bound to natively-glycosylated HIV-1 envelope
    journal, March 2018

    • Barnes, Christopher O.; Gristick, Harry B.; Freund, Natalia T.
    • Nature Communications, Vol. 9, Issue 1
    • DOI: 10.1038/s41467-018-03632-y

    Structure of a cleavage-independent HIV Env recapitulates the glycoprotein architecture of the native cleaved trimer
    journal, May 2018

    Selection of immunoglobulin elbow region mutations impacts interdomain conformational flexibility in HIV-1 broadly neutralizing antibodies
    journal, February 2019

    Improvement of antibody functionality by structure-guided paratope engraftment
    journal, February 2019

    Capturing the inherent structural dynamics of the HIV-1 envelope glycoprotein fusion peptide
    journal, February 2019

    Antibody responses to viral infections: a structural perspective across three different enveloped viruses
    journal, March 2019

    Conformational Heterogeneity of the HIV Envelope Glycan Shield
    journal, June 2017

    Preclinical Development of a Fusion Peptide Conjugate as an HIV Vaccine Immunogen
    journal, February 2020

    HIV-1 anchor inhibitors and membrane fusion inhibitors target distinct but overlapping steps in virus entry
    journal, April 2019

    • Eggink, Dirk; Bontjer, Ilja; de Taeye, Steven W.
    • Journal of Biological Chemistry, Vol. 294, Issue 15
    • DOI: 10.1074/jbc.ra119.007360

    Strategies for inducing effective neutralizing antibody responses against HIV-1
    journal, November 2019

    Antibodyomics: bioinformatics technologies for understanding B-cell immunity to HIV-1
    journal, January 2017

    • Kwong, Peter D.; Chuang, Gwo-Yu; DeKosky, Brandon J.
    • Immunological Reviews, Vol. 275, Issue 1
    • DOI: 10.1111/imr.12480

    Identification and specificity of broadly neutralizing antibodies against HIV
    journal, January 2017

    • McCoy, Laura E.; Burton, Dennis R.
    • Immunological Reviews, Vol. 275, Issue 1
    • DOI: 10.1111/imr.12484

    Ontogeny-based immunogens for the induction of V2-directed HIV broadly neutralizing antibodies
    journal, January 2017

    • Moore, Penny L.; Gorman, Jason; Doria-Rose, Nicole A.
    • Immunological Reviews, Vol. 275, Issue 1
    • DOI: 10.1111/imr.12501

    Antibody-virus co-evolution in HIV infection: paths for HIV vaccine development
    journal, January 2017

    • Bonsignori, Mattia; Liao, Hua-Xin; Gao, Feng
    • Immunological Reviews, Vol. 275, Issue 1
    • DOI: 10.1111/imr.12509

    HIV-1 vaccine design through minimizing envelope metastability
    journal, November 2018

    AIDS Vaccine Research Subcommittee (AVRS) Consultation: Early-Life Immunization Strategies against HIV Acquisition
    journal, August 2019

    Reverse Immunology Approach to Define a New HIV-gp41-Neutralizing Epitope
    journal, March 2019

    • Dorgham, Karim; Pietrancosta, Nicolas; Affoune, Amel
    • Journal of Immunology Research, Vol. 2019
    • DOI: 10.1155/2019/9804584

    Development of broadly neutralizing antibodies in HIV-1 infected elite neutralizers
    journal, September 2018

    The expanding array of HIV broadly neutralizing antibodies
    journal, October 2018

    Star nanoparticles delivering HIV-1 peptide minimal immunogens elicit near-native envelope antibody responses in nonhuman primates
    journal, June 2019

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

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

    Complete functional mapping of infection- and vaccine-elicited antibodies against the fusion peptide of HIV
    journal, July 2018

    Identification of a novel HIV-1-neutralizing antibody from a CRF07_BC-infected Chinese donor
    journal, June 2017

    Neutralizing Monoclonal Antibodies to Fight HIV-1: On the Threshold of Success
    journal, January 2017

    • Jaworski, Juan Pablo; Vendrell, Alejandrina; Chiavenna, Sebastián Matias
    • Frontiers in Immunology, Vol. 7
    • DOI: 10.3389/fimmu.2016.00661

    Env-Specific Antibodies in Chronic Infection versus in Vaccination
    journal, September 2017

    Increasing the Clinical Potential and Applications of Anti-HIV Antibodies
    journal, November 2017

    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

    Driving HIV-1 into a Vulnerable Corner by Taking Advantage of Viral Adaptation and Evolution
    journal, March 2017

    Development of Protein- and Peptide-Based HIV Entry Inhibitors Targeting gp120 or gp41
    journal, August 2019

    • Pu, Jing; Wang, Qian; Xu, Wei
    • Viruses, Vol. 11, Issue 8, p. 705
    • DOI: 10.3390/v11080705
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