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Title: Epitope-based vaccine design yields fusion peptide-directed antibodies that neutralize diverse strains of HIV-1

Abstract

A central goal of HIV-1 vaccine research is the elicitation of antibodies capable of neutralizing diverse primary isolates of HIV-1. Here we show that focusing the immune response to exposed N-terminal residues of the fusion peptide, a critical component of the viral entry machinery and the epitope of antibodies elicited by HIV-1 infection, through immunization with fusion peptide-coupled carriers and prefusion stabilized envelope trimers, induces cross-clade neutralizing responses. In mice, these immunogens elicited monoclonal antibodies capable of neutralizing up to 31% of a cross-clade panel of 208 HIV-1 strains. Crystal and cryoelectron microscopy structures of these antibodies revealed fusion peptide conformational diversity as a molecular explanation for the cross-clade neutralization. Immunization of guinea pigs and rhesus macaques induced similarly broad fusion peptide-directed neutralizing responses, suggesting translatability. In conclusion, the N terminus of the HIV-1 fusion peptide is thus a promising target of vaccine efforts aimed at eliciting broadly neutralizing antibodies.

Authors:
 [1];  [2];  [1];  [1];  [1]; ORCiD logo [1]; ORCiD logo [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [3];  [1] more »;  [1];  [3];  [1];  [1];  [1];  [4];  [1];  [1];  [1];  [1]; ORCiD logo [1];  [5];  [1];  [1];  [1];  [1];  [1]; ORCiD logo [6];  [1];  [7];  [1];  [1];  [3];  [1];  [1];  [8];  [8];  [1];  [1];  [9];  [3];  [3];  [1];  [10] « less
+ Show Author Affiliations
  1. National Inst. of Health (NIH), Bethesda, MD (United States)
  2. National Inst. of Health (NIH), Bethesda, MD (United States); Simons Electron Microscopy Center, New York, NY (United States)
  3. Simons Electron Microscopy Center, New York, NY (United States)
  4. Vanderbilt Univ., Nashville, TN (United States)
  5. Univ. of California, San Francisco, CA (United States)
  6. Columbia Univ., New York, NY (United States)
  7. Frederick National Lab for Cancer Research, Frederick, MD (United States)
  8. GenScript USA, Piscataway, NJ (United States)
  9. National Inst. of Health (NIH), Bethesda, MD (United States) ; Columbia Univ., New York, NY (United States)
  10. National Inst. of Health (NIH), Bethesda, MD (United States); Columbia Univ., New York, NY (United States)
Publication Date:
Research Org.:
Argonne National Laboratory (ANL), Argonne, IL (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES); National Institutes of Health (NIH); Simons Foundation; National Institute of General Medical Sciences; Agouron Institute
OSTI Identifier:
1467705
Grant/Contract Number:  
W-31-109-Eng-38; HHSN261200800001E; R01 AI131722; SF349247; GM103310; F00316; OD019994
Resource Type:
Accepted Manuscript
Journal Name:
Nature Medicine
Additional Journal Information:
Journal Volume: 24; Journal Issue: 6; Journal ID: ISSN 1078-8956
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
ENGLISH
Subject:
60 APPLIED LIFE SCIENCES; HIV infections; vaccines; viral infection

Citation Formats

Xu, Kai, Acharya, Priyamvada, Kong, Rui, Cheng, Cheng, Chuang, Gwo-Yu, Liu, Kevin, Louder, Mark K., O’Dell, Sijy, Rawi, Reda, Sastry, Mallika, Shen, Chen-Hsiang, Zhang, Baoshan, Zhou, Tongqing, Asokan, Mangaiarkarasi, Bailer, Robert T., Chambers, Michael, Chen, Xuejun, Choi, Chang W., Dandey, Venkata P., Doria-Rose, Nicole A., Druz, Aliaksandr, Eng, Edward T., Farney, S. Katie, Foulds, Kathryn E., Geng, Hui, Georgiev, Ivelin S., Gorman, Jason, Hill, Kurt R., Jafari, Alexander J., Kwon, Young D., Lai, Yen-Ting, Lemmin, Thomas, McKee, Krisha, Ohr, Tiffany Y., Ou, Li, Peng, Dongjun, Rowshan, Ariana P., Sheng, Zizhang, Todd, John-Paul, Tsybovsky, Yaroslav, Viox, Elise G., Wang, Yiran, Wei, Hui, Yang, Yongping, Zhou, Amy F., Chen, Rui, Yang, Lu, Scorpio, Diana G., McDermott, Adrian B., Shapiro, Lawrence, Carragher, Bridget, Potter, Clinton S., Mascola, John R., and Kwong, Peter D. Epitope-based vaccine design yields fusion peptide-directed antibodies that neutralize diverse strains of HIV-1. United States: N. p., 2018. Web. doi:10.1038/s41591-018-0042-6.
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Xu, Kai, Acharya, Priyamvada, Kong, Rui, Cheng, Cheng, Chuang, Gwo-Yu, Liu, Kevin, Louder, Mark K., O’Dell, Sijy, Rawi, Reda, Sastry, Mallika, Shen, Chen-Hsiang, Zhang, Baoshan, Zhou, Tongqing, Asokan, Mangaiarkarasi, Bailer, Robert T., Chambers, Michael, Chen, Xuejun, Choi, Chang W., Dandey, Venkata P., Doria-Rose, Nicole A., Druz, Aliaksandr, Eng, Edward T., Farney, S. Katie, Foulds, Kathryn E., Geng, Hui, Georgiev, Ivelin S., Gorman, Jason, Hill, Kurt R., Jafari, Alexander J., Kwon, Young D., Lai, Yen-Ting, Lemmin, Thomas, McKee, Krisha, Ohr, Tiffany Y., Ou, Li, Peng, Dongjun, Rowshan, Ariana P., Sheng, Zizhang, Todd, John-Paul, Tsybovsky, Yaroslav, Viox, Elise G., Wang, Yiran, Wei, Hui, Yang, Yongping, Zhou, Amy F., Chen, Rui, Yang, Lu, Scorpio, Diana G., McDermott, Adrian B., Shapiro, Lawrence, Carragher, Bridget, Potter, Clinton S., Mascola, John R., & Kwong, Peter D. Epitope-based vaccine design yields fusion peptide-directed antibodies that neutralize diverse strains of HIV-1. United States. https://doi.org/10.1038/s41591-018-0042-6
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Xu, Kai, Acharya, Priyamvada, Kong, Rui, Cheng, Cheng, Chuang, Gwo-Yu, Liu, Kevin, Louder, Mark K., O’Dell, Sijy, Rawi, Reda, Sastry, Mallika, Shen, Chen-Hsiang, Zhang, Baoshan, Zhou, Tongqing, Asokan, Mangaiarkarasi, Bailer, Robert T., Chambers, Michael, Chen, Xuejun, Choi, Chang W., Dandey, Venkata P., Doria-Rose, Nicole A., Druz, Aliaksandr, Eng, Edward T., Farney, S. Katie, Foulds, Kathryn E., Geng, Hui, Georgiev, Ivelin S., Gorman, Jason, Hill, Kurt R., Jafari, Alexander J., Kwon, Young D., Lai, Yen-Ting, Lemmin, Thomas, McKee, Krisha, Ohr, Tiffany Y., Ou, Li, Peng, Dongjun, Rowshan, Ariana P., Sheng, Zizhang, Todd, John-Paul, Tsybovsky, Yaroslav, Viox, Elise G., Wang, Yiran, Wei, Hui, Yang, Yongping, Zhou, Amy F., Chen, Rui, Yang, Lu, Scorpio, Diana G., McDermott, Adrian B., Shapiro, Lawrence, Carragher, Bridget, Potter, Clinton S., Mascola, John R., and Kwong, Peter D. Mon . "Epitope-based vaccine design yields fusion peptide-directed antibodies that neutralize diverse strains of HIV-1". United States. https://doi.org/10.1038/s41591-018-0042-6. https://www.osti.gov/servlets/purl/1467705.
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@article{osti_1467705,
title = {Epitope-based vaccine design yields fusion peptide-directed antibodies that neutralize diverse strains of HIV-1},
author = {Xu, Kai and Acharya, Priyamvada and Kong, Rui and Cheng, Cheng and Chuang, Gwo-Yu and Liu, Kevin and Louder, Mark K. and O’Dell, Sijy and Rawi, Reda and Sastry, Mallika and Shen, Chen-Hsiang and Zhang, Baoshan and Zhou, Tongqing and Asokan, Mangaiarkarasi and Bailer, Robert T. and Chambers, Michael and Chen, Xuejun and Choi, Chang W. and Dandey, Venkata P. and Doria-Rose, Nicole A. and Druz, Aliaksandr and Eng, Edward T. and Farney, S. Katie and Foulds, Kathryn E. and Geng, Hui and Georgiev, Ivelin S. and Gorman, Jason and Hill, Kurt R. and Jafari, Alexander J. and Kwon, Young D. and Lai, Yen-Ting and Lemmin, Thomas and McKee, Krisha and Ohr, Tiffany Y. and Ou, Li and Peng, Dongjun and Rowshan, Ariana P. and Sheng, Zizhang and Todd, John-Paul and Tsybovsky, Yaroslav and Viox, Elise G. and Wang, Yiran and Wei, Hui and Yang, Yongping and Zhou, Amy F. and Chen, Rui and Yang, Lu and Scorpio, Diana G. and McDermott, Adrian B. and Shapiro, Lawrence and Carragher, Bridget and Potter, Clinton S. and Mascola, John R. and Kwong, Peter D.},
abstractNote = {A central goal of HIV-1 vaccine research is the elicitation of antibodies capable of neutralizing diverse primary isolates of HIV-1. Here we show that focusing the immune response to exposed N-terminal residues of the fusion peptide, a critical component of the viral entry machinery and the epitope of antibodies elicited by HIV-1 infection, through immunization with fusion peptide-coupled carriers and prefusion stabilized envelope trimers, induces cross-clade neutralizing responses. In mice, these immunogens elicited monoclonal antibodies capable of neutralizing up to 31% of a cross-clade panel of 208 HIV-1 strains. Crystal and cryoelectron microscopy structures of these antibodies revealed fusion peptide conformational diversity as a molecular explanation for the cross-clade neutralization. Immunization of guinea pigs and rhesus macaques induced similarly broad fusion peptide-directed neutralizing responses, suggesting translatability. In conclusion, the N terminus of the HIV-1 fusion peptide is thus a promising target of vaccine efforts aimed at eliciting broadly neutralizing antibodies.},
doi = {10.1038/s41591-018-0042-6},
journal = {Nature Medicine},
number = 6,
volume = 24,
place = {United States},
year = {Mon Jun 04 00:00:00 EDT 2018},
month = {Mon Jun 04 00:00:00 EDT 2018}
}
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