Staged induction of HIV-1 glycan–dependent broadly neutralizing antibodies
Abstract
A preventive HIV-1 vaccine should induce HIV-1–specific broadly neutralizing antibodies (bnAbs). However, bnAbs generally require high levels of somatic hypermutation (SHM) to acquire breadth, and current vaccine strategies have not been successful in inducing bnAbs. Because bnAbs directed against a glycosylated site adjacent to the third variable loop (V3) of the HIV-1 envelope protein require limited SHM, the V3-glycan epitope is an attractive vaccine target. By studying the cooperation among multiple V3-glycan B cell lineages and their coevolution with autologous virus throughout 5 years of infection, we identify key events in the ontogeny of a V3- glycan bnAb. Two autologous neutralizing antibody lineages selected for virus escape mutations and consequently allowed initiation and affinity maturation of a V3-glycan bnAb lineage. The nucleotide substitution required to initiate the bnAb lineage occurred at a low-probability site for activation-induced cytidine deaminase activity. Cooperation of B cell lineages and an improbable mutation critical for bnAb activity defined the necessary events leading to breadth in this V3- glycan bnAb lineage. These findings may, in part, explain why initiation of V3-glycan bnAbs is rare, and suggest an immunization strategy for inducing similar V3-glycan bnAbs.
- Authors:
-
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- Duke Univ. School of Medicine, Durham, NC (United States); Duke Human Vaccine Inst., Durham, NC (United States)
- Univ. of Pennsylvania, Philadelphia, PA (United States). Perelman School of Medicine
- Brigham and Women's Hospital (Harvard Medical School), Boston, MA (United States)
- Memorial Sloan Kettering Cancer Center, New York, NY (United States)
- Duke Human Vaccine Inst., Durham, NC (United States)
- Duke Human Vaccine Inst., Durham, NC (United States); Duke Univ. Schoole of Medicine, Durham, NC (United States)
- National Inst. of Health (NIH), Bethesda, MD (United States)
- National Inst. of Communicable Diseases, Johannesburg (South Africa)
- Univ. of Alabama, Burmingham, AL (United States)
- Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
- Kamuzu Central Hospital, Lilongwe (Malawi). Univ. of North Carolina Project
- Univ. of North Carolina, Chapel Hill, NC (United States)
- Boston Univ., MA (United States)
- Publication Date:
- Research Org.:
- Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)
- Sponsoring Org.:
- National Institutes of Health (NIH); USDOE
- OSTI Identifier:
- 1406204
- Report Number(s):
- LA-UR-16-25421
Journal ID: ISSN 1946-6234
- Grant/Contract Number:
- AC52-06NA25396
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Science Translational Medicine
- Additional Journal Information:
- Journal Volume: 9; Journal Issue: 381; Journal ID: ISSN 1946-6234
- Publisher:
- AAAS
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 60 APPLIED LIFE SCIENCES; Biological Science
Citation Formats
Bonsignori, Mattia, Kreider, Edward F., Fera, Daniela, Meyerhoff, R. Ryan, Bradley, Todd, Wiehe, Kevin, Alam, S. Munir, Aussedat, Baptiste, Walkowicz, William E., Hwang, Kwan-Ki, Saunders, Kevin O., Zhang, Ruijun, Gladden, Morgan A., Monroe, Anthony, Kumar, Amit, Xia, Shi-Mao, Cooper, Melissa, Louder, Mark K., McKee, Krisha, Bailer, Robert T., Pier, Brendan W., Jette, Claudia A., Kelsoe, Garnett, Williams, Wilton B., Morris, Lynn, Kappes, John, Wagh, Kshitij, Kamanga, Gift, Cohen, Myron S., Hraber, Peter T., Montefiori, David C., Trama, Ashley, Liao, Hua-Xin, Kepler, Thomas B., Moody, M. Anthony, Gao, Feng, Danishefsky, Samuel J., Mascola, John R., Shaw, George M., Hahn, Beatrice H., Harrison, Stephen C., Korber, Bette T., and Haynes, Barton F. Staged induction of HIV-1 glycan–dependent broadly neutralizing antibodies. United States: N. p., 2017.
Web. doi:10.1126/scitranslmed.aai7514.
Bonsignori, Mattia, Kreider, Edward F., Fera, Daniela, Meyerhoff, R. Ryan, Bradley, Todd, Wiehe, Kevin, Alam, S. Munir, Aussedat, Baptiste, Walkowicz, William E., Hwang, Kwan-Ki, Saunders, Kevin O., Zhang, Ruijun, Gladden, Morgan A., Monroe, Anthony, Kumar, Amit, Xia, Shi-Mao, Cooper, Melissa, Louder, Mark K., McKee, Krisha, Bailer, Robert T., Pier, Brendan W., Jette, Claudia A., Kelsoe, Garnett, Williams, Wilton B., Morris, Lynn, Kappes, John, Wagh, Kshitij, Kamanga, Gift, Cohen, Myron S., Hraber, Peter T., Montefiori, David C., Trama, Ashley, Liao, Hua-Xin, Kepler, Thomas B., Moody, M. Anthony, Gao, Feng, Danishefsky, Samuel J., Mascola, John R., Shaw, George M., Hahn, Beatrice H., Harrison, Stephen C., Korber, Bette T., & Haynes, Barton F. Staged induction of HIV-1 glycan–dependent broadly neutralizing antibodies. United States. https://doi.org/10.1126/scitranslmed.aai7514
Bonsignori, Mattia, Kreider, Edward F., Fera, Daniela, Meyerhoff, R. Ryan, Bradley, Todd, Wiehe, Kevin, Alam, S. Munir, Aussedat, Baptiste, Walkowicz, William E., Hwang, Kwan-Ki, Saunders, Kevin O., Zhang, Ruijun, Gladden, Morgan A., Monroe, Anthony, Kumar, Amit, Xia, Shi-Mao, Cooper, Melissa, Louder, Mark K., McKee, Krisha, Bailer, Robert T., Pier, Brendan W., Jette, Claudia A., Kelsoe, Garnett, Williams, Wilton B., Morris, Lynn, Kappes, John, Wagh, Kshitij, Kamanga, Gift, Cohen, Myron S., Hraber, Peter T., Montefiori, David C., Trama, Ashley, Liao, Hua-Xin, Kepler, Thomas B., Moody, M. Anthony, Gao, Feng, Danishefsky, Samuel J., Mascola, John R., Shaw, George M., Hahn, Beatrice H., Harrison, Stephen C., Korber, Bette T., and Haynes, Barton F. Wed .
"Staged induction of HIV-1 glycan–dependent broadly neutralizing antibodies". United States. https://doi.org/10.1126/scitranslmed.aai7514. https://www.osti.gov/servlets/purl/1406204.
@article{osti_1406204,
title = {Staged induction of HIV-1 glycan–dependent broadly neutralizing antibodies},
author = {Bonsignori, Mattia and Kreider, Edward F. and Fera, Daniela and Meyerhoff, R. Ryan and Bradley, Todd and Wiehe, Kevin and Alam, S. Munir and Aussedat, Baptiste and Walkowicz, William E. and Hwang, Kwan-Ki and Saunders, Kevin O. and Zhang, Ruijun and Gladden, Morgan A. and Monroe, Anthony and Kumar, Amit and Xia, Shi-Mao and Cooper, Melissa and Louder, Mark K. and McKee, Krisha and Bailer, Robert T. and Pier, Brendan W. and Jette, Claudia A. and Kelsoe, Garnett and Williams, Wilton B. and Morris, Lynn and Kappes, John and Wagh, Kshitij and Kamanga, Gift and Cohen, Myron S. and Hraber, Peter T. and Montefiori, David C. and Trama, Ashley and Liao, Hua-Xin and Kepler, Thomas B. and Moody, M. Anthony and Gao, Feng and Danishefsky, Samuel J. and Mascola, John R. and Shaw, George M. and Hahn, Beatrice H. and Harrison, Stephen C. and Korber, Bette T. and Haynes, Barton F.},
abstractNote = {A preventive HIV-1 vaccine should induce HIV-1–specific broadly neutralizing antibodies (bnAbs). However, bnAbs generally require high levels of somatic hypermutation (SHM) to acquire breadth, and current vaccine strategies have not been successful in inducing bnAbs. Because bnAbs directed against a glycosylated site adjacent to the third variable loop (V3) of the HIV-1 envelope protein require limited SHM, the V3-glycan epitope is an attractive vaccine target. By studying the cooperation among multiple V3-glycan B cell lineages and their coevolution with autologous virus throughout 5 years of infection, we identify key events in the ontogeny of a V3- glycan bnAb. Two autologous neutralizing antibody lineages selected for virus escape mutations and consequently allowed initiation and affinity maturation of a V3-glycan bnAb lineage. The nucleotide substitution required to initiate the bnAb lineage occurred at a low-probability site for activation-induced cytidine deaminase activity. Cooperation of B cell lineages and an improbable mutation critical for bnAb activity defined the necessary events leading to breadth in this V3- glycan bnAb lineage. These findings may, in part, explain why initiation of V3-glycan bnAbs is rare, and suggest an immunization strategy for inducing similar V3-glycan bnAbs.},
doi = {10.1126/scitranslmed.aai7514},
journal = {Science Translational Medicine},
number = 381,
volume = 9,
place = {United States},
year = {Wed Mar 15 00:00:00 EDT 2017},
month = {Wed Mar 15 00:00:00 EDT 2017}
}
Web of Science
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HIV Envelope Glycoform Heterogeneity and Localized Diversity Govern the Initiation and Maturation of a V2 Apex Broadly Neutralizing Antibody Lineage
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Multivalent Antigen Presentation Enhances the Immunogenicity of a Synthetic Three-Component HIV-1 V3 Glycopeptide Vaccine
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Correction for Anthony et al., “Cooperation between Strain-Specific and Broadly Neutralizing Responses Limited Viral Escape and Prolonged the Exposure of the Broadly Neutralizing Epitope”
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Maternal Broadly Neutralizing Antibodies Can Select for Neutralization-Resistant, Infant-Transmitted/Founder HIV Variants
journal, April 2020
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journal, September 2018
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Star nanoparticles delivering HIV-1 peptide minimal immunogens elicit near-native envelope antibody responses in nonhuman primates
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Somatic hypermutation to counter a globally rare viral immunotype drove off-track antibodies in the CAP256-VRC26 HIV-1 V2-directed bNAb lineage
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Cooperation between somatic mutation and germline-encoded residues enables antibody recognition of HIV-1 envelope glycans
journal, December 2019
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Beyond Hot Spots: Biases in Antibody Somatic Hypermutation and Implications for Vaccine Design
journal, August 2018
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Techniques to Study Antigen-Specific B Cell Responses
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Advances in HIV-1 Vaccine Development
journal, April 2018
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Gp120 V5 Is Targeted by the First Wave of Sequential Neutralizing Antibodies in SHIVSF162P3N-Infected Rhesus Macaques
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