Minimally Mutated HIV-1 Broadly Neutralizing Antibodies to Guide Reductionist Vaccine Design
Abstract
An optimal HIV vaccine should induce broadly neutralizing antibodies (bnAbs) that neutralize diverse viral strains and subtypes. However, potent bnAbs develop in only a small fraction of HIV-infected individuals, all contain rare features such as extensive mutation, insertions, deletions, and/or long complementarity-determining regions, and some are polyreactive, casting doubt on whether bnAbs to HIV can be reliably induced by vaccination. We engineered two potent VRC01-class bnAbs that minimized rare features. According to a quantitative features frequency analysis, the set of features for one of these minimally mutated bnAbs compared favorably with all 68 HIV bnAbs analyzed and was similar to antibodies elicited by common vaccines. This same minimally mutated bnAb lacked polyreactivity in four different assays. We then divided the minimal mutations into spatial clusters and dissected the epitope components interacting with those clusters, by mutational and crystallographic analyses coupled with neutralization assays. Finally, by synthesizing available data, we developed a working-concept boosting strategy to select the mutation clusters in a logical order following a germline-targeting prime. We have thus developed potent HIV bnAbs that may be more tractable vaccine goals compared to existing bnAbs, and we have proposed a strategy to elicit them. This reductionist approach to vaccine design,more »
- Authors:
-
[4];
more »
- The Scripps Research Inst., La Jolla, CA (United States); Univ. of Washington, Seattle, WA (United States)
- The Scripps Research Inst., La Jolla, CA (United States); International AIDS Vaccine Initiative, New York, NY (United States)
- The Scripps Research Inst., La Jolla, CA (United States); Univ. of Toronto, ON (Canada)
- The Scripps Research Inst., La Jolla, CA (United States)
- Fred Hutchinson Cancer Research Center, Seattle, WA (United States)
- Univ. of Chicago, IL (United States)
- The Scripps Research Inst., La Jolla, CA (United States); Massachusetts General Hospital, Cambridge, MA (United States). Ragon Inst.
- The Scripps Research Inst., La Jolla, CA (United States); Univ. of Washington, Seattle, WA (United States); Massachusetts General Hospital, Cambridge, MA (United States). Ragon Inst.
- Publication Date:
- Research Org.:
- Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)
- Sponsoring Org.:
- International AIDS Vaccine Initiative Neutralizing Antibody Consortium and Center; Bill and Melinda Gates Foundation; The Collaboration for AIDS Vaccine Discovery (CAVD); Bayer Science and Education Foundation; National Institute of Allergy and Infectious Diseases (NIAID); USDOE Office of Science (SC), Basic Energy Sciences (BES); National Cancer Institute (NCI); National Institute of General Medical Sciences (NIGMS)
- OSTI Identifier:
- 1357641
- Grant/Contract Number:
- P01AI081625; CHAVI-ID 1UM1 AI100663; P01 AI110657; R01 AI084817; AC02-06CH11357; Y1-CO-1020; Y1-GM-1104
- Resource Type:
- Accepted Manuscript
- Journal Name:
- PLoS Pathogens
- Additional Journal Information:
- Journal Volume: 12; Journal Issue: 8; Journal ID: ISSN 1553-7374
- Publisher:
- Public Library of Science
- Country of Publication:
- United States
- Language:
- ENGLISH
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Antibodies; HIV; Insertion mutation; Deletion mutation; Crystal structure; Microbial mutation; Antigens; Sequence databases
Citation Formats
Jardine, Joseph G., Sok, Devin, Julien, Jean-Philippe, Briney, Bryan, Sarkar, Anita, Liang, Chi-Hui, Scherer, Erin A., Henry Dunand, Carole J., Adachi, Yumiko, Diwanji, Devan, Hsueh, Jessica, Jones, Meaghan, Kalyuzhniy, Oleksandr, Kubitz, Michael, Spencer, Skye, Pauthner, Matthias, Saye-Francisco, Karen L., Sesterhenn, Fabian, Wilson, Patrick C., Galloway, Denise M., Stanfield, Robyn L., Wilson, Ian A., Burton, Dennis R., and Schief, William R. Minimally Mutated HIV-1 Broadly Neutralizing Antibodies to Guide Reductionist Vaccine Design. United States: N. p., 2016.
Web. doi:10.1371/journal.ppat.1005815.
Jardine, Joseph G., Sok, Devin, Julien, Jean-Philippe, Briney, Bryan, Sarkar, Anita, Liang, Chi-Hui, Scherer, Erin A., Henry Dunand, Carole J., Adachi, Yumiko, Diwanji, Devan, Hsueh, Jessica, Jones, Meaghan, Kalyuzhniy, Oleksandr, Kubitz, Michael, Spencer, Skye, Pauthner, Matthias, Saye-Francisco, Karen L., Sesterhenn, Fabian, Wilson, Patrick C., Galloway, Denise M., Stanfield, Robyn L., Wilson, Ian A., Burton, Dennis R., & Schief, William R. Minimally Mutated HIV-1 Broadly Neutralizing Antibodies to Guide Reductionist Vaccine Design. United States. https://doi.org/10.1371/journal.ppat.1005815
Jardine, Joseph G., Sok, Devin, Julien, Jean-Philippe, Briney, Bryan, Sarkar, Anita, Liang, Chi-Hui, Scherer, Erin A., Henry Dunand, Carole J., Adachi, Yumiko, Diwanji, Devan, Hsueh, Jessica, Jones, Meaghan, Kalyuzhniy, Oleksandr, Kubitz, Michael, Spencer, Skye, Pauthner, Matthias, Saye-Francisco, Karen L., Sesterhenn, Fabian, Wilson, Patrick C., Galloway, Denise M., Stanfield, Robyn L., Wilson, Ian A., Burton, Dennis R., and Schief, William R. Thu .
"Minimally Mutated HIV-1 Broadly Neutralizing Antibodies to Guide Reductionist Vaccine Design". United States. https://doi.org/10.1371/journal.ppat.1005815. https://www.osti.gov/servlets/purl/1357641.
@article{osti_1357641,
title = {Minimally Mutated HIV-1 Broadly Neutralizing Antibodies to Guide Reductionist Vaccine Design},
author = {Jardine, Joseph G. and Sok, Devin and Julien, Jean-Philippe and Briney, Bryan and Sarkar, Anita and Liang, Chi-Hui and Scherer, Erin A. and Henry Dunand, Carole J. and Adachi, Yumiko and Diwanji, Devan and Hsueh, Jessica and Jones, Meaghan and Kalyuzhniy, Oleksandr and Kubitz, Michael and Spencer, Skye and Pauthner, Matthias and Saye-Francisco, Karen L. and Sesterhenn, Fabian and Wilson, Patrick C. and Galloway, Denise M. and Stanfield, Robyn L. and Wilson, Ian A. and Burton, Dennis R. and Schief, William R.},
abstractNote = {An optimal HIV vaccine should induce broadly neutralizing antibodies (bnAbs) that neutralize diverse viral strains and subtypes. However, potent bnAbs develop in only a small fraction of HIV-infected individuals, all contain rare features such as extensive mutation, insertions, deletions, and/or long complementarity-determining regions, and some are polyreactive, casting doubt on whether bnAbs to HIV can be reliably induced by vaccination. We engineered two potent VRC01-class bnAbs that minimized rare features. According to a quantitative features frequency analysis, the set of features for one of these minimally mutated bnAbs compared favorably with all 68 HIV bnAbs analyzed and was similar to antibodies elicited by common vaccines. This same minimally mutated bnAb lacked polyreactivity in four different assays. We then divided the minimal mutations into spatial clusters and dissected the epitope components interacting with those clusters, by mutational and crystallographic analyses coupled with neutralization assays. Finally, by synthesizing available data, we developed a working-concept boosting strategy to select the mutation clusters in a logical order following a germline-targeting prime. We have thus developed potent HIV bnAbs that may be more tractable vaccine goals compared to existing bnAbs, and we have proposed a strategy to elicit them. This reductionist approach to vaccine design, guided by antibody and antigen structure, could be applied to design candidate vaccines for other HIV bnAbs or protective Abs against other pathogens.},
doi = {10.1371/journal.ppat.1005815},
journal = {PLoS Pathogens},
number = 8,
volume = 12,
place = {United States},
year = {Thu Aug 25 00:00:00 EDT 2016},
month = {Thu Aug 25 00:00:00 EDT 2016}
}
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