A neutralizing antibody target in early HIV-1 infection was recapitulated in rhesus macaques immunized with the transmitted/founder envelope sequence
Transmitted/founder (T/F) HIV-1 envelope proteins (Envs) from infected individuals that developed neutralization breadth are likely to possess inherent features desirable for vaccine immunogen design. To explore this premise, we conducted an immunization study in rhesus macaques (RM) using T/F Env s...
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| Published in | PLoS pathogens Vol. 18; no. 5; p. e1010488 |
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| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
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United States
Public Library of Science
03.05.2022
Public Library of Science (PLoS) |
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| Abstract | Transmitted/founder (T/F) HIV-1 envelope proteins (Envs) from infected individuals that developed neutralization breadth are likely to possess inherent features desirable for vaccine immunogen design. To explore this premise, we conducted an immunization study in rhesus macaques (RM) using T/F Env sequences from two human subjects, one of whom developed potent and broad neutralizing antibodies (Z1800M) while the other developed little to no neutralizing antibody responses (R66M) during HIV-1 infection. Using a DNA/MVA/protein immunization protocol, 10 RM were immunized with each T/F Env. Within each T/F Env group, the protein boosts were administered as either monomeric gp120 or stabilized trimeric gp140 protein. All vaccination regimens elicited high titers of antigen-specific IgG, and two animals that received monomeric Z1800M Env gp120 developed autologous neutralizing activity. Using early Env escape variants isolated from subject Z1800M as guides, the serum neutralizing activity of the two immunized RM was found to be dependent on the gp120 V5 region. Interestingly, the exact same residues of V5 were also targeted by a neutralizing monoclonal antibody (nmAb) isolated from the subject Z1800M early in infection. Glycan profiling and computational modeling of the Z1800M Env gp120 immunogen provided further evidence that the V5 loop is exposed in this T/F Env and was a dominant feature that drove neutralizing antibody targeting during infection and immunization. An expanded B cell clonotype was isolated from one of the neutralization-positive RM and nmAbs corresponding to this group demonstrated V5-dependent neutralization similar to both the RM serum and the human Z1800M nmAb. The results demonstrate that neutralizing antibody responses elicited by the Z1800M T/F Env in RM converged with those in the HIV-1 infected human subject, illustrating the potential of using immunogens based on this or other T/F Envs with well-defined immunogenicity as a starting point to drive breadth. |
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| AbstractList | Transmitted/founder (T/F) HIV-1 envelope proteins (Envs) from infected individuals that developed neutralization breadth are likely to possess inherent features desirable for vaccine immunogen design. To explore this premise, we conducted an immunization study in rhesus macaques (RM) using T/F Env sequences from two human subjects, one of whom developed potent and broad neutralizing antibodies (Z1800M) while the other developed little to no neutralizing antibody responses (R66M) during HIV-1 infection. Using a DNA/MVA/protein immunization protocol, 10 RM were immunized with each T/F Env. Within each T/F Env group, the protein boosts were administered as either monomeric gp120 or stabilized trimeric gp140 protein. All vaccination regimens elicited high titers of antigen-specific IgG, and two animals that received monomeric Z1800M Env gp120 developed autologous neutralizing activity. Using early Env escape variants isolated from subject Z1800M as guides, the serum neutralizing activity of the two immunized RM was found to be dependent on the gp120 V5 region. Interestingly, the exact same residues of V5 were also targeted by a neutralizing monoclonal antibody (nmAb) isolated from the subject Z1800M early in infection. Glycan profiling and computational modeling of the Z1800M Env gp120 immunogen provided further evidence that the V5 loop is exposed in this T/F Env and was a dominant feature that drove neutralizing antibody targeting during infection and immunization. An expanded B cell clonotype was isolated from one of the neutralization-positive RM and nmAbs corresponding to this group demonstrated V5-dependent neutralization similar to both the RM serum and the human Z1800M nmAb. The results demonstrate that neutralizing antibody responses elicited by the Z1800M T/F Env in RM converged with those in the HIV-1 infected human subject, illustrating the potential of using immunogens based on this or other T/F Envs with well-defined immunogenicity as a starting point to drive breadth. Transmitted/founder (T/F) HIV-1 envelope proteins (Envs) from infected individuals that developed neutralization breadth are likely to possess inherent features desirable for vaccine immunogen design. To explore this premise, we conducted an immunization study in rhesus macaques (RM) using T/F Env sequences from two human subjects, one of whom developed potent and broad neutralizing antibodies (Z1800M) while the other developed little to no neutralizing antibody responses (R66M) during HIV-1 infection. Using a DNA/MVA/protein immunization protocol, 10 RM were immunized with each T/F Env. Within each T/F Env group, the protein boosts were administered as either monomeric gp120 or stabilized trimeric gp140 protein. All vaccination regimens elicited high titers of antigen-specific IgG, and two animals that received monomeric Z1800M Env gp120 developed autologous neutralizing activity. Using early Env escape variants isolated from subject Z1800M as guides, the serum neutralizing activity of the two immunized RM was found to be dependent on the gp120 V5 region. Interestingly, the exact same residues of V5 were also targeted by a neutralizing monoclonal antibody (nmAb) isolated from the subject Z1800M early in infection. Glycan profiling and computational modeling of the Z1800M Env gp120 immunogen provided further evidence that the V5 loop is exposed in this T/F Env and was a dominant feature that drove neutralizing antibody targeting during infection and immunization. An expanded B cell clonotype was isolated from one of the neutralization-positive RM and nmAbs corresponding to this group demonstrated V5-dependent neutralization similar to both the RM serum and the human Z1800M nmAb. The results demonstrate that neutralizing antibody responses elicited by the Z1800M T/F Env in RM converged with those in the HIV-1 infected human subject, illustrating the potential of using immunogens based on this or other T/F Envs with well-defined immunogenicity as a starting point to drive breadth. A subset of HIV-1 infected individuals generates antibodies that neutralize many different viral strains. However, this process requires years of infection and has proved difficult to achieve through vaccination. The envelope proteins of the infecting HIV-1 virus likely contain features that drive neutralization breadth within an individual. To explore this, we immunized rhesus macaques using envelope proteins from two HIV-1 infected human subjects that developed either high or low neutralizing antibody levels during infection. Several animals developed neutralizing antibodies when immunized with the envelope protein derived from the high neutralizing individual. Using viral escape variants that emerged in this infected individual over time, we mapped the targets of vaccine-elicited neutralizing antibodies to a distinct loop region of the envelope protein, which was also targeted by neutralizing monoclonal antibodies isolated from both the infected individual and the immunized rhesus macaques. Modeling of the envelope protein used in the vaccine demonstrated why this loop is vulnerable to antibody attack in infection and vaccination. By recapitulating the early HIV-1 human neutralizing antibody responses in a nonhuman primate immunization model, we demonstrate remarkable similarities as well as the potential of using this approach as a starting point to drive neutralizing antibody breadth, one of the ultimate goals of vaccine design. |
| Audience | Academic |
| Author | Shen, Xiaoying Wang, Shiyu Welbourn, Sarah Gangadhara, Sailaja Wright, Elizabeth R Burton, Samantha Karita, Etienne Zhang, Lu Peters, Tiffany Bosinger, Steven E Charles, Tysheena Eisel, Nathan Gnanakaran, Sandrasegaram Price, Matt A Yang, Jie E Upadhyay, Amit A Williams, Danielle Khan, Salar Thompson, Justin Kilembe, William Amara, Rama R Williams, LaTonya D Chakraborty, Srirupa Smith, S Abigail Gleinich, Anne S Mopuri, Rohini Ferrebee, Courtney Tomaras, Georgia D Qin, Zhaohui Derdeyn, Cynthia A Yagnik, Bhrugu Azadi, Parastoo |
| AuthorAffiliation | 1 Yerkes National Primate Research Center, Emory University, Atlanta, Georgia, United States of America Vaccine Research Center, UNITED STATES 10 Projet San Francisco, Kigali, Rwanda 3 Department of Biochemistry, University of Wisconsin-Madison, Madison, Wisconsin, United States of America 2 Theoretical Biology and Biophysics Group, Center for Nonlinear Studies, Los Alamos National Laboratory, Los Alamos, New Mexico, United States of America 11 Department of Pathology and Laboratory Medicine, Emory University, Atlanta, Georgia, United States of America 9 Center for Family Health Research in Zambia (CFHRZ), Lusaka, Zambia 6 International AIDS Vaccine Initiative, New York city, New York, United States of America 7 Department of Biostatistics and Bioinformatics, Rollins School of Public Health, Emory University, Atlanta, Georgia, United States of America 8 Department of Surgery, Duke University, Durham, North Carolina, United States of America 12 Department of Microbiology and Immunology, Emory Uni |
| AuthorAffiliation_xml | – name: 4 Complex Carbohydrate Research Center, University of Georgia, Athens, Georgia, United States of America – name: 6 International AIDS Vaccine Initiative, New York city, New York, United States of America – name: 8 Department of Surgery, Duke University, Durham, North Carolina, United States of America – name: 12 Department of Microbiology and Immunology, Emory University, Atlanta, Georgia, United States of America – name: 1 Yerkes National Primate Research Center, Emory University, Atlanta, Georgia, United States of America – name: 2 Theoretical Biology and Biophysics Group, Center for Nonlinear Studies, Los Alamos National Laboratory, Los Alamos, New Mexico, United States of America – name: 5 Department of Epidemiology and Biostatistics, University of California San Francisco, San Francisco, California, United States of America – name: 10 Projet San Francisco, Kigali, Rwanda – name: 3 Department of Biochemistry, University of Wisconsin-Madison, Madison, Wisconsin, United States of America – name: 9 Center for Family Health Research in Zambia (CFHRZ), Lusaka, Zambia – name: 7 Department of Biostatistics and Bioinformatics, Rollins School of Public Health, Emory University, Atlanta, Georgia, United States of America – name: 11 Department of Pathology and Laboratory Medicine, Emory University, Atlanta, Georgia, United States of America – name: Vaccine Research Center, UNITED STATES |
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A surname: Price fullname: Price, Matt A organization: International AIDS Vaccine Initiative, New York city, New York, United States of America – sequence: 17 givenname: Shiyu surname: Wang fullname: Wang, Shiyu organization: Department of Biostatistics and Bioinformatics, Rollins School of Public Health, Emory University, Atlanta, Georgia, United States of America – sequence: 18 givenname: Zhaohui surname: Qin fullname: Qin, Zhaohui organization: Department of Biostatistics and Bioinformatics, Rollins School of Public Health, Emory University, Atlanta, Georgia, United States of America – sequence: 19 givenname: Xiaoying surname: Shen fullname: Shen, Xiaoying organization: Department of Surgery, Duke University, Durham, North Carolina, United States of America – sequence: 20 givenname: LaTonya D surname: Williams fullname: Williams, LaTonya D organization: Department of Surgery, Duke University, Durham, North Carolina, United States of America – sequence: 21 givenname: Nathan surname: 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| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/35503780$$D View this record in MEDLINE/PubMed https://www.osti.gov/servlets/purl/2342060$$D View this record in Osti.gov |
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| CitedBy_id | crossref_primary_10_1371_journal_ppat_1011452 crossref_primary_10_1371_journal_ppat_1011717 |
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| DocumentTitleAlternate | Convergence of neutralizing antibody targeting in HIV-1 infection and vaccination |
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| Notes | new_version ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 89233218CNA000001; DMR-1720415 National Science Foundation (NSF) LA-UR-22-22584 USDOE Laboratory Directed Research and Development (LDRD) Program USDOE National Nuclear Security Administration (NNSA) Current address: American Type Culture Collection, Manassas, Virginia, United States of America Current address: Department of Medicine, Emory University, Decatur, Georgia, United States of America Current address: Taconic Biosciences, Rensselaer, New York, United States of America The authors have declared that no competing interests exist. |
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| OpenAccessLink | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9106183/ |
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| Publisher | Public Library of Science Public Library of Science (PLoS) |
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| SubjectTerms | AIDS Vaccines Amino acids Animals Antibodies Antibodies, Neutralizing Antigens BASIC BIOLOGICAL SCIENCES Binding sites Biology and life sciences Care and treatment Chemical bonds Computer applications Deoxyribonucleic acid Development and progression DNA env Gene Products, Human Immunodeficiency Virus Genetic aspects Glycan Glycoprotein gp120 Health aspects HIV HIV Antibodies HIV Envelope Protein gp120 HIV infection HIV Infections - prevention & control HIV-1 Human immunodeficiency virus Humans Immune response Immunization Immunogenicity Immunoglobulin G Infections Macaca mulatta Medicine and health sciences Monoclonal antibodies Neutralization Neutralizing Plasma Process controls Proteins Research and Analysis Methods Vaccination Vaccines Viral proteins Virus research |
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| Title | A neutralizing antibody target in early HIV-1 infection was recapitulated in rhesus macaques immunized with the transmitted/founder envelope sequence |
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