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Title: Diverse specificity and effector function among human antibodies to HIV-1 envelope glycoprotein epitopes exposed by CD4 binding

Abstract

The HIV-1 envelope glycoprotein (Env) undergoes conformational transitions consequent to CD4 binding and coreceptor engagement during viral entry. The physical steps in this process are becoming defined, but less is known about their significance as targets of antibodies potentially protective against HIV-1 infection. Here we probe the functional significance of transitional epitope exposure by characterizing 41 human mAbs specific for epitopes exposed on trimeric Env after CD4 engagement. These mAbs recognize three epitope clusters: cluster A, the gp120 face occluded by gp41 in trimeric Env; cluster B, a region proximal to the coreceptor-binding site (CoRBS) and involving the V1/V2 domain; and cluster C, the coreceptor-binding site. The mAbs were evaluated functionally by antibody-dependent, cell-mediated cytotoxicity (ADCC) and for neutralization of Tiers 1 and 2 pseudoviruses. All three clusters included mAbs mediating ADCC. However, there was a strong potency bias for cluster A, which harbors at least three potent ADCC epitopes whose cognate mAbs have electropositive paratopes. Cluster A epitopes are functional ADCC targets during viral entry in an assay format using virion-sensitized target cells. In contrast, only cluster C contained epitopes that were recognized by neutralizing mAbs. There was significant diversity in breadth and potency that correlated with epitope finemore » specificity. In contrast, ADCC potency had no relationship with neutralization potency or breadth for any epitope cluster. In conclusion, Fc-mediated effector function and neutralization coselect with specificity in anti-Env antibody responses, but the nature of selection is distinct for these two antiviral activities.« less

Authors:
 [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [2];  [3];  [4];  [1];  [1];  [1]
+ Show Author Affiliations
  1. Univ. of Maryland School of Medicine, Baltimore, MD (United States)
  2. Tulane Univ., New Orleans, LA (United States)
  3. Harvard Medical School, Boston, MA (United States)
  4. Profectus Biosciences, Inc., Baltimore, MD (United States)
Publication Date:
Research Org.:
SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1136677
Report Number(s):
SLAC-REPRINT-2014-212
Journal ID: ISSN 0027-8424
Grant/Contract Number:  
AC02-76SF00515
Resource Type:
Accepted Manuscript
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Volume: 110; Journal Issue: 1; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences, Washington, DC (United States)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Guan, Yongjun, Pazgier, Marzena, Sajadi, Mohammad M., Kamin-Lewis, Roberta, Al-Darmarki, Salma, Flinko, Robin, Lovo, Elena, Wu, Xueji, Robinson, James E., Seaman, Michael S., Fouts, Timothy R., Gallo, Robert C., DeVico, Anthony L., and Lewis, George K. Diverse specificity and effector function among human antibodies to HIV-1 envelope glycoprotein epitopes exposed by CD4 binding. United States: N. p., 2012. Web. doi:10.1073/pnas.1217609110.
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Guan, Yongjun, Pazgier, Marzena, Sajadi, Mohammad M., Kamin-Lewis, Roberta, Al-Darmarki, Salma, Flinko, Robin, Lovo, Elena, Wu, Xueji, Robinson, James E., Seaman, Michael S., Fouts, Timothy R., Gallo, Robert C., DeVico, Anthony L., & Lewis, George K. Diverse specificity and effector function among human antibodies to HIV-1 envelope glycoprotein epitopes exposed by CD4 binding. United States. https://doi.org/10.1073/pnas.1217609110
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Guan, Yongjun, Pazgier, Marzena, Sajadi, Mohammad M., Kamin-Lewis, Roberta, Al-Darmarki, Salma, Flinko, Robin, Lovo, Elena, Wu, Xueji, Robinson, James E., Seaman, Michael S., Fouts, Timothy R., Gallo, Robert C., DeVico, Anthony L., and Lewis, George K. Thu . "Diverse specificity and effector function among human antibodies to HIV-1 envelope glycoprotein epitopes exposed by CD4 binding". United States. https://doi.org/10.1073/pnas.1217609110. https://www.osti.gov/servlets/purl/1136677.
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@article{osti_1136677,
title = {Diverse specificity and effector function among human antibodies to HIV-1 envelope glycoprotein epitopes exposed by CD4 binding},
author = {Guan, Yongjun and Pazgier, Marzena and Sajadi, Mohammad M. and Kamin-Lewis, Roberta and Al-Darmarki, Salma and Flinko, Robin and Lovo, Elena and Wu, Xueji and Robinson, James E. and Seaman, Michael S. and Fouts, Timothy R. and Gallo, Robert C. and DeVico, Anthony L. and Lewis, George K.},
abstractNote = {The HIV-1 envelope glycoprotein (Env) undergoes conformational transitions consequent to CD4 binding and coreceptor engagement during viral entry. The physical steps in this process are becoming defined, but less is known about their significance as targets of antibodies potentially protective against HIV-1 infection. Here we probe the functional significance of transitional epitope exposure by characterizing 41 human mAbs specific for epitopes exposed on trimeric Env after CD4 engagement. These mAbs recognize three epitope clusters: cluster A, the gp120 face occluded by gp41 in trimeric Env; cluster B, a region proximal to the coreceptor-binding site (CoRBS) and involving the V1/V2 domain; and cluster C, the coreceptor-binding site. The mAbs were evaluated functionally by antibody-dependent, cell-mediated cytotoxicity (ADCC) and for neutralization of Tiers 1 and 2 pseudoviruses. All three clusters included mAbs mediating ADCC. However, there was a strong potency bias for cluster A, which harbors at least three potent ADCC epitopes whose cognate mAbs have electropositive paratopes. Cluster A epitopes are functional ADCC targets during viral entry in an assay format using virion-sensitized target cells. In contrast, only cluster C contained epitopes that were recognized by neutralizing mAbs. There was significant diversity in breadth and potency that correlated with epitope fine specificity. In contrast, ADCC potency had no relationship with neutralization potency or breadth for any epitope cluster. In conclusion, Fc-mediated effector function and neutralization coselect with specificity in anti-Env antibody responses, but the nature of selection is distinct for these two antiviral activities.},
doi = {10.1073/pnas.1217609110},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 1,
volume = 110,
place = {United States},
year = {Thu Dec 13 00:00:00 EST 2012},
month = {Thu Dec 13 00:00:00 EST 2012}
}
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    • Journal of Virology, Vol. 93, Issue 3
    • DOI: 10.1128/jvi.01823-18

    Structural basis for the recognition of complex-type N-glycans by Endoglycosidase S
    journal, May 2018

    Lack of ADCC Breadth of Human Nonneutralizing Anti-HIV-1 Antibodies
    journal, April 2017

    • Bruel, Timothée; Guivel-Benhassine, Florence; Lorin, Valérie
    • Journal of Virology, Vol. 91, Issue 8
    • DOI: 10.1128/jvi.02440-16

    Concurrent Exposure of Neutralizing and Non-neutralizing Epitopes on a Single HIV-1 Envelope Structure
    journal, July 2019

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

    HIV Nef and Vpu protect HIV-infected CD4+ T cells from antibody-mediated cell lysis through down-modulation of CD4 and BST2
    journal, January 2014

    Stabilizing Exposure of Conserved Epitopes by Structure Guided Insertion of Disulfide Bond in HIV-1 Envelope Glycoprotein
    journal, October 2013

    HIV / AIDS Vaccines: 2018
    journal, October 2018

    • Robinson, Harriet L.
    • Clinical Pharmacology & Therapeutics, Vol. 104, Issue 6
    • DOI: 10.1002/cpt.1208

    The Antibodiome—Mapping the Humoral Immune Response to HIV
    journal, March 2019

    • Butler, Audrey L.; Fischinger, Stephanie; Alter, Galit
    • Current HIV/AIDS Reports, Vol. 16, Issue 2
    • DOI: 10.1007/s11904-019-00432-x

    Antibody-dependent cellular cytotoxicity targeting CD4-inducible epitopes predicts mortality in HIV-infected infants
    journal, September 2019

    A stamp on the envelope
    journal, October 2014

    Initiation of HIV neutralizing B cell lineages with sequential envelope immunizations
    journal, November 2017

    Structural basis for the recognition of complex-type N-glycans by Endoglycosidase S
    journal, May 2018

    Structural basis of mammalian high-mannose N-glycan processing by human gut Bacteroides
    journal, February 2020

    Molecular basis for epitope recognition by non-neutralizing anti-gp41 antibody F240
    journal, November 2016

    • Gohain, Neelakshi; Tolbert, William D.; Orlandi, Chiara
    • Scientific Reports, Vol. 6, Issue 1
    • DOI: 10.1038/srep36685

    Adaption of human antibody λ and κ light chain architectures to CDR repertoires
    journal, March 2019

    • van der Kant, Rob; Bauer, Joschka; Karow-Zwick, Anne R.
    • Protein Engineering, Design and Selection, Vol. 32, Issue 3
    • DOI: 10.1093/protein/gzz012

    Incomplete Downregulation of CD4 Expression Affects HIV-1 Env Conformation and Antibody-Dependent Cellular Cytotoxicity Responses
    journal, April 2018

    • Prévost, Jérémie; Richard, Jonathan; Medjahed, Halima
    • Journal of Virology, Vol. 92, Issue 13
    • DOI: 10.1128/jvi.00484-18

    Boosting with AIDSVAX B/E Enhances Env Constant Region 1 and 2 Antibody-Dependent Cellular Cytotoxicity Breadth and Potency
    journal, November 2019

    • Easterhoff, David; Pollara, Justin; Luo, Kan
    • Journal of Virology, Vol. 94, Issue 4
    • DOI: 10.1128/jvi.01120-19

    Uninfected Bystander Cells Impact the Measurement of HIV-Specific Antibody-Dependent Cellular Cytotoxicity Responses
    journal, March 2018

    • Richard, Jonathan; Prévost, Jérémie; Baxter, Amy E.
    • mBio, Vol. 9, Issue 2
    • DOI: 10.1128/mbio.00358-18

    Antibody-Dependent Cellular Cytotoxicity-Competent Antibodies against HIV-1-Infected Cells in Plasma from HIV-Infected Subjects
    journal, December 2019

    Development of prophylactic vaccines against HIV-1
    journal, January 2013

    • Schiffner, Torben; Sattentau, Quentin J.; Dorrell, Lucy
    • Retrovirology, Vol. 10, Issue 1
    • DOI: 10.1186/1742-4690-10-72

    HIV Nef and Vpu protect HIV-infected CD4+ T cells from antibody-mediated cell lysis through down-modulation of CD4 and BST2
    journal, January 2014

    Highlights from the 2014 International Symposium on HIV & Emerging Infectious Diseases (ISHEID): from cART management to the end of the HIV pandemic
    journal, January 2014

    • Lafeuillade, Alain; Wainberg, Mark; Gougeon, Marie-Lise
    • AIDS Research and Therapy, Vol. 11, Issue 1
    • DOI: 10.1186/1742-6405-11-28

    Systems serology: profiling vaccine induced humoral immunity against HIV
    journal, December 2017

    Stabilizing Exposure of Conserved Epitopes by Structure Guided Insertion of Disulfide Bond in HIV-1 Envelope Glycoprotein
    journal, October 2013

    Herpes Simplex Virus 2 (HSV-2) Infected Cell Proteins Are among the Most Dominant Antigens of a Live-Attenuated HSV-2 Vaccine
    journal, February 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

    Epitope Specificity of Human Immunodeficiency Virus-1 Antibody Dependent Cellular Cytotoxicity [ADCC] Responses
    journal, November 2013

    Antibody Functional Assays as Measures of Fc Receptor-Mediated Immunity to HIV - New Technologies and their Impact on the HIV Vaccine Field
    journal, July 2017

    Preparation and Evaluation of the Fully Humanized Monoclonal Antibody GD-mAb Against Respiratory Syncytial Virus
    journal, July 2019

    • Tian, Puyuan; Wang, Yuqing; Liu, Hui
    • Frontiers in Cellular and Infection Microbiology, Vol. 9
    • DOI: 10.3389/fcimb.2019.00275

    A New Scientific Paradigm may be Needed to Finally Develop an HIV Vaccine
    journal, March 2015

    Natural Killer (NK) Cell Education Differentially Influences HIV Antibody-Dependent NK Cell Activation and Antibody-Dependent Cellular Cytotoxicity
    journal, August 2017

    • Bernard, Nicole F.; Kiani, Zahra; Tremblay-McLean, Alexandra
    • Frontiers in Immunology, Vol. 8
    • DOI: 10.3389/fimmu.2017.01033

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

    Induction of Fc-Mediated Effector Functions Against a Stabilized Inner Domain of HIV-1 gp120 Designed to Selectively Harbor the A32 Epitope Region
    journal, April 2019

    • Visciano, Maria L.; Gohain, Neelakshi; Sherburn, Rebekah
    • Frontiers in Immunology, Vol. 10
    • DOI: 10.3389/fimmu.2019.00677

    Knowns and Unknowns of Assaying Antibody-Dependent Cell-Mediated Cytotoxicity Against HIV-1
    journal, May 2019

    • Lewis, George K.; Ackerman, Margaret E.; Scarlatti, Gabriella
    • Frontiers in Immunology, Vol. 10
    • DOI: 10.3389/fimmu.2019.01025

    Concurrent Exposure of Neutralizing and Non-neutralizing Epitopes on a Single HIV-1 Envelope Structure
    journal, July 2019

    A Sample-Sparing Multiplexed ADCP Assay
    journal, August 2019

    Antibody-Dependent Cellular Cytotoxicity (ADCC)-Mediating Antibodies Constrain Neutralizing Antibody Escape Pathway
    journal, December 2019

    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

    Quantifying Anti-HIV Envelope-Specific Antibodies in Plasma from HIV Infected Individuals
    journal, May 2019

    • Kant, Sanket; Zhang, Ningyu; Routy, Jean-Pierre
    • Viruses, Vol. 11, Issue 6
    • DOI: 10.3390/v11060487
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