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Title: Plasma IgG to Linear Epitopes in the V2 and V3 Regions of HIV-1 gp120 Correlate with a Reduced Risk of Infection in the RV144 Vaccine Efficacy Trial

Abstract

Neutralizing and non-neutralizing antibodies to linear epitopes on HIV-1 envelope glycoproteins have potential to mediate antiviral effector functions that could be beneficial to vaccine-induced protection. Here, plasma IgG responses were assessed in three HIV-1 gp120 vaccine efficacy trials (RV144, Vax003, Vax004) and in HIV-1- infected individuals by using arrays of overlapping peptides spanning the entire consensus gp160 of all major genetic subtypes and circulating recombinant forms (CRFs) of the virus. In RV144, where 31.2% efficacy against HIV-1 infection was seen, dominant responses targeted the C1, V2, V3 and C5 regions of gp120. An analysis of RV144 case-control samples showed that IgG to V2 CRF01_AE significantly inversely correlated with infection risk (OR= 0.54, p=0.0042), as did the response to other V2 subtypes (OR=0.60-0.63, p=0.016-0.025). The response to V3 CRF01_AE also inversely correlated with infection risk but only in vaccine recipients who had lower levels of other antibodies, especially Env-specific plasma IgA (OR=0.49, p=0.007) and neutralizing antibodies (OR=0.5, p=0.008). Responses to C1 and C5 showed no significant correlation with infection risk. In Vax003 and Vax004, where no significant protection was seen, serum IgG responses targeted the same epitopes as in RV144 with the exception of an additional C1 reactivity in Vax003 andmore » infrequent V2 reactivity in Vax004. In HIV-1 infected subjects, dominant responses targeted the V3 and C5 regions of gp120, as well as the immunodominant domain, heptad repeat 1 (HR-1) and membrane proximal external region (MPER) of gp41. These results highlight the presence of several dominant linear B cell epitopes on the HIV-1 envelope glycoproteins. They also generate the hypothesis that IgG to linear epitopes in the V2 and V3 regions of gp120 are part of a complex interplay of immune responses that contributed to protection in RV144.« less

Authors:
 [1];  [2];  [2];  [3];  [3];  [4];  [4];  [2];  [1];  [5];  [5];  [5];  [4];  [4];  [6];  [7];  [7];  [7];  [8];  [9] more »;  [10];  [10];  [11];  [12];  [12];  [12];  [13];  [4];  [1];  [1];  [1];  [4] « less
+ Show Author Affiliations
  1. Fred Hutchinson Cancer Research Center, Seattle, WA (United States)
  2. National Institutes of Health (NIH), Bethesda, MD (United States)
  3. Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)
  4. Duke University, Durham, NC (United States)
  5. PT Peptide Technologies GmbH, Berlin (Germany)
  6. Santa Clara Univesity, Santa Clara, CA (United States)
  7. Global Solutions for Infectious Diseases, South San Francisco, CA (United States)
  8. US Army Medical Component, AFRIMS, Bangkok (Thailand)
  9. Ministry of Public Health, Nonthaburi (Thailand)
  10. Mahidol University, Bangkok (Thailand)
  11. Sanofi Pasteur, Swiftwater, PA (United States)
  12. Walter Reed Army Institute of Research, Silver Spring, MD (United States)
  13. Veterans Affairs New York Harbor Healthcare System, New York, NY (United States); New York University (NYU), NY (United States)
Publication Date:
Research Org.:
Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) US Department of Defense; New York University School of Medicine; Bill & Melinda Gates Foundation; Henry M. Jackson Foundation
OSTI Identifier:
1627640
Grant/Contract Number:  
AC52-06NA25396; W81XWH-07-2-0067; 692526; 38619
Resource Type:
Accepted Manuscript
Journal Name:
PLoS ONE
Additional Journal Information:
Journal Volume: 8; Journal Issue: 9; Journal ID: ISSN 1932-6203
Publisher:
Public Library of Science
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; HIV vaccines; medical risk factors; HIV-1; antibodies; vaccine development; viral vaccines; medicine and health sciences; immune response

Citation Formats

Gottardo, Raphael, Bailer, Robert T., Korber, Bette T., Gnanakaran, S., Phillips, Joshua, Shen, Xiaoying, Tomaras, Georgia D., Turk, Ellen, Imholte, Gregory, Eckler, Larry, Wenschuh, Holger, Zerweck, Johannes, Greene, Kelli, Gao, Hongmei, Berman, Phillip W., Francis, Donald, Sinangil, Faruk, Lee, Carter, Nitayaphan, Sorachai, Rerks-Ngarm, Supachai, Kaewkungwal, Jaranit, Pitisuttithum, Punnee, Tartaglia, James, Robb, Merlin L., Michael, Nelson L., Kim, Jerome H., Zolla-Pazner, Susan, Haynes, Barton F., Mascola, John R., Self, Steve, Gilbert, Peter, and Montefiori, David C. Plasma IgG to Linear Epitopes in the V2 and V3 Regions of HIV-1 gp120 Correlate with a Reduced Risk of Infection in the RV144 Vaccine Efficacy Trial. United States: N. p., 2013. Web. doi:10.1371/journal.pone.0075665.
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Gottardo, Raphael, Bailer, Robert T., Korber, Bette T., Gnanakaran, S., Phillips, Joshua, Shen, Xiaoying, Tomaras, Georgia D., Turk, Ellen, Imholte, Gregory, Eckler, Larry, Wenschuh, Holger, Zerweck, Johannes, Greene, Kelli, Gao, Hongmei, Berman, Phillip W., Francis, Donald, Sinangil, Faruk, Lee, Carter, Nitayaphan, Sorachai, Rerks-Ngarm, Supachai, Kaewkungwal, Jaranit, Pitisuttithum, Punnee, Tartaglia, James, Robb, Merlin L., Michael, Nelson L., Kim, Jerome H., Zolla-Pazner, Susan, Haynes, Barton F., Mascola, John R., Self, Steve, Gilbert, Peter, & Montefiori, David C. Plasma IgG to Linear Epitopes in the V2 and V3 Regions of HIV-1 gp120 Correlate with a Reduced Risk of Infection in the RV144 Vaccine Efficacy Trial. United States. https://doi.org/10.1371/journal.pone.0075665
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Gottardo, Raphael, Bailer, Robert T., Korber, Bette T., Gnanakaran, S., Phillips, Joshua, Shen, Xiaoying, Tomaras, Georgia D., Turk, Ellen, Imholte, Gregory, Eckler, Larry, Wenschuh, Holger, Zerweck, Johannes, Greene, Kelli, Gao, Hongmei, Berman, Phillip W., Francis, Donald, Sinangil, Faruk, Lee, Carter, Nitayaphan, Sorachai, Rerks-Ngarm, Supachai, Kaewkungwal, Jaranit, Pitisuttithum, Punnee, Tartaglia, James, Robb, Merlin L., Michael, Nelson L., Kim, Jerome H., Zolla-Pazner, Susan, Haynes, Barton F., Mascola, John R., Self, Steve, Gilbert, Peter, and Montefiori, David C. Thu . "Plasma IgG to Linear Epitopes in the V2 and V3 Regions of HIV-1 gp120 Correlate with a Reduced Risk of Infection in the RV144 Vaccine Efficacy Trial". United States. https://doi.org/10.1371/journal.pone.0075665. https://www.osti.gov/servlets/purl/1627640.
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@article{osti_1627640,
title = {Plasma IgG to Linear Epitopes in the V2 and V3 Regions of HIV-1 gp120 Correlate with a Reduced Risk of Infection in the RV144 Vaccine Efficacy Trial},
author = {Gottardo, Raphael and Bailer, Robert T. and Korber, Bette T. and Gnanakaran, S. and Phillips, Joshua and Shen, Xiaoying and Tomaras, Georgia D. and Turk, Ellen and Imholte, Gregory and Eckler, Larry and Wenschuh, Holger and Zerweck, Johannes and Greene, Kelli and Gao, Hongmei and Berman, Phillip W. and Francis, Donald and Sinangil, Faruk and Lee, Carter and Nitayaphan, Sorachai and Rerks-Ngarm, Supachai and Kaewkungwal, Jaranit and Pitisuttithum, Punnee and Tartaglia, James and Robb, Merlin L. and Michael, Nelson L. and Kim, Jerome H. and Zolla-Pazner, Susan and Haynes, Barton F. and Mascola, John R. and Self, Steve and Gilbert, Peter and Montefiori, David C.},
abstractNote = {Neutralizing and non-neutralizing antibodies to linear epitopes on HIV-1 envelope glycoproteins have potential to mediate antiviral effector functions that could be beneficial to vaccine-induced protection. Here, plasma IgG responses were assessed in three HIV-1 gp120 vaccine efficacy trials (RV144, Vax003, Vax004) and in HIV-1- infected individuals by using arrays of overlapping peptides spanning the entire consensus gp160 of all major genetic subtypes and circulating recombinant forms (CRFs) of the virus. In RV144, where 31.2% efficacy against HIV-1 infection was seen, dominant responses targeted the C1, V2, V3 and C5 regions of gp120. An analysis of RV144 case-control samples showed that IgG to V2 CRF01_AE significantly inversely correlated with infection risk (OR= 0.54, p=0.0042), as did the response to other V2 subtypes (OR=0.60-0.63, p=0.016-0.025). The response to V3 CRF01_AE also inversely correlated with infection risk but only in vaccine recipients who had lower levels of other antibodies, especially Env-specific plasma IgA (OR=0.49, p=0.007) and neutralizing antibodies (OR=0.5, p=0.008). Responses to C1 and C5 showed no significant correlation with infection risk. In Vax003 and Vax004, where no significant protection was seen, serum IgG responses targeted the same epitopes as in RV144 with the exception of an additional C1 reactivity in Vax003 and infrequent V2 reactivity in Vax004. In HIV-1 infected subjects, dominant responses targeted the V3 and C5 regions of gp120, as well as the immunodominant domain, heptad repeat 1 (HR-1) and membrane proximal external region (MPER) of gp41. These results highlight the presence of several dominant linear B cell epitopes on the HIV-1 envelope glycoproteins. They also generate the hypothesis that IgG to linear epitopes in the V2 and V3 regions of gp120 are part of a complex interplay of immune responses that contributed to protection in RV144.},
doi = {10.1371/journal.pone.0075665},
journal = {PLoS ONE},
number = 9,
volume = 8,
place = {United States},
year = {Thu Sep 26 00:00:00 EDT 2013},
month = {Thu Sep 26 00:00:00 EDT 2013}
}
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journal, July 2012

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Randomized, Double‐Blind, Placebo‐Controlled Efficacy Trial of a Bivalent Recombinant Glycoprotein 120 HIV‐1 Vaccine among Injection Drug Users in Bangkok, Thailand
journal, December 2006

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Humoral Immune Responses to Homologous Envelope Peptides in Vaccinees and Lab Workers Infected with HIV
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Magnitude and Breadth of the Neutralizing Antibody Response in the RV144 and Vax003 HIV-1 Vaccine Efficacy Trials
journal, May 2012

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Broad and Potent Neutralizing Antibodies from an African Donor Reveal a New HIV-1 Vaccine Target
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Antibody-Dependent Cellular Cytotoxicity against Primary HIV-Infected CD4 + T Cells Is Directly Associated with the Magnitude of Surface IgG Binding
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Two Distinct Broadly Neutralizing Antibody Specificities of Different Clonal Lineages in a Single HIV-1-Infected Donor: Implications for Vaccine Design
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Conserved and Exposed Epitopes on Intact, Native, Primary Human Immunodeficiency Virus Type 1 Virions of Group M
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Nature of Nonfunctional Envelope Proteins on the Surface of Human Immunodeficiency Virus Type 1
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The Role of Antibodies in HIV Vaccines
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Map of Sequential B Cell Epitopes of the HIV-1 Transmembrane Protein Using Human Antibodies as Probe
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Differences in the antibody response to human immunodeficiency virus-1 envelope glycoprotein (gp160) in infected laboratory workers and vaccinees.
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Analysis of Memory B Cell Responses and Isolation of Novel Monoclonal Antibodies with Neutralizing Breadth from HIV-1-Infected Individuals
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Anti-V3 Monoclonal Antibodies Display Broad Neutralizing Activities against Multiple HIV-1 Subtypes
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Analysis of V2 Antibody Responses Induced in Vaccinees in the ALVAC/AIDSVAX HIV-1 Vaccine Efficacy Trial
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HIV-1 rational vaccine design: molecular details of b12–gp120 complex structure
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  • Phogat, Sanjay K.; Kaminsky, Stephen M.; Koff, Wayne C.
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osDesign: AnRPackage for the Analysis, Evaluation, and Design of Two-Phase and Case-Control Studies
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Mass Spectrometric Characterization of a Discontinuous Epitope of the HIV Envelope Protein HIV-gp120 Recognized by the Human Monoclonal Antibody 1331A
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Secretory IgA Specific for a Conserved Epitope on gp41 Envelope Glycoprotein Inhibits Epithelial Transcytosis of HIV-1
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Intraepithelial Cell Neutralization of HIV-1 Replication by IgA
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