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Title: A Neutralizing Antibody Recognizing Primarily N-Linked Glycan Targets the Silent Face of the HIV Envelope

Abstract

Virtually the entire surface of the HIV-1-envelope trimer is recognized by neutralizing antibodies, except for a highly glycosylated region at the center of the “silent face” on the gp120 subunit. From an HIV-1-infected donor, #74, we identified antibody VRC-PG05, which neutralized 27% of HIV-1 strains. The crystal structure of the antigen-binding fragment of VRC-PG05 in complex with gp120 revealed an epitope comprised primarily of N-linked glycans from N262, N295, and N448 at the silent face center. Furthermore, somatic hypermutation occurred preferentially at antibody residues that interacted with these glycans, suggesting somatic development of glycan recognition. Resistance to VRC-PG05 in donor #74 involved shifting of glycan-N448 to N446 or mutation of glycan-proximal residue E293. HIV-1 neutralization can thus be achieved at the silent face center by glycan-recognizing antibody; along with other known epitopes, the VRC-PG05 epitope completes coverage by neutralizing antibody of all major exposed regions of the prefusion closed trimer.

Authors:
 [1];  [1];  [2];  [1];  [3];  [1];  [1];  [4];  [1];  [2];  [1];  [5];  [1];  [1];  [1];  [1];  [1];  [1];  [6];  [1] more »;  [1];  [7];  [7];  [7];  [7];  [8];  [9];  [10];  [11];  [12];  [13];  [1];  [12];  [14];  [15];  [15];  [15];  [15];  [15];  [15];  [15];  [15];  [15];  [15];  [15];  [15];  [15];  [15];  [15];  [15];  [15];  [15];  [15];  [15];  [15];  [15];  [15];  [15];  [15];  [15];  [15];  [15];  [15] « less
+ Show Author Affiliations
  1. National Inst. of Health (NIH), Bethesda, MD (United States). National Inst. of Allergy and Infectious Diseases (NIAID)
  2. Frederick National Lab. for Cancer Research, MD (United States)
  3. National Inst. of Health (NIH), Bethesda, MD (United States). National Inst. of Allergy and Infectious Diseases (NIAID); Vanderbilt Univ., Nashville, TN (United States)
  4. National Inst. of Health (NIH), Bethesda, MD (United States). National Inst. of Allergy and Infectious Diseases (NIAID) and National Inst. of Diabetes, Digestive and Kidney Diseases (NIDDK)
  5. Walter Reed Army Inst. of Research, Silver Spring, MD (United States); Henry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, MD (United States)
  6. Rockefeller Univ., New York, NY (United States). Aaron Diamond AIDS Research Center
  7. Academia Sinica, Taipei (Taiwan)
  8. National Inst. of Health (NIH), Bethesda, MD (United States), National Human Genome Research Inst. (NHGRI)
  9. National Inst. of Health (NIH), Bethesda, MD (United States). National Inst. of Diabetes, Digestive and Kidney Diseases (NIDDK)
  10. The Scripps Research Inst., La Jolla, CA (United States); Ragon Inst., Cambridge, MA (United States)
  11. Walter Reed Army Inst. of Research, Silver Spring, MD (United States)
  12. National Inst. of Health (NIH), Bethesda, MD (United States). National Inst. of Allergy and Infectious Diseases (NIAID); Columbia Univ., New York, NY (United States)
  13. Academia Sinica, Taipei (Taiwan); The Scripps Research Inst., La Jolla, CA (United States)
  14. National Inst. of Health (NIH), Bethesda, MD (United States). National Inst. of Allergy and Infectious Diseases (NIAID); Rockefeller Univ., New York, NY (United States). Aaron Diamond AIDS Research Center
  15. NIH Intramural Sequencing Center (NISC), Bethesda, MD (United States). Comparative Sequencing Program
Publication Date:
Research Org.:
Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)
Sponsoring Org.:
National Institute of Allergy and Infectious Diseases (NIAID); National Human Genome Research Institute (NHGRI); National Institutes of Health (NIH); International AIDS Vaccine Initiative’s (IAVI’s) Neutralizing Antibody Consortium; Frederick National Laboratory for Cancer Research; USDOE Office of Science (SC), Basic Energy Sciences (BES); Academia Sinica; Ministry of Science and Technology
Contributing Org.:
NISC Comparative Sequencing Program
OSTI Identifier:
1506497
Grant/Contract Number:  
R21 AI108399; HHSN261200800001E; W-31-109-Eng-38; R01 AI131722; 106-0210- 01-15-02; 104-0210-01-09-02; 103-2321-B-001-004; R01 AI072155
Resource Type:
Accepted Manuscript
Journal Name:
Immunity
Additional Journal Information:
Journal Volume: 48; Journal Issue: 3; Journal ID: ISSN 1074-7613
Publisher:
Cell Press
Country of Publication:
United States
Language:
ENGLISH
Subject:
59 BASIC BIOLOGICAL SCIENCES; broadly neutralizing antibody; crystal structure; glycan cluster; glycan recognition; glycopeptide epitope; HIV silent face; HIV vaccine; prefusion-closed Env trimer; viral escape

Citation Formats

Zhou, Tongqing, Zheng, Anqi, Baxa, Ulrich, Chuang, Gwo-Yu, Georgiev, Ivelin S., Kong, Rui, O’Dell, Sijy, Shahzad-ul-Hussan, Syed, Shen, Chen-Hsiang, Tsybovsky, Yaroslav, Bailer, Robert T., Gift, Syna K., Louder, Mark K., McKee, Krisha, Rawi, Reda, Stevenson, Catherine H., Stewart-Jones, Guillaume B. E., Taft, Justin D., Waltari, Eric, Yang, Yongping, Zhang, Baoshan, Shivatare, Sachin S., Shivatare, Vidya S., Lee, Chang-Chun D., Wu, Chung-Yi, Mullikin, James C., Bewley, Carole A., Burton, Dennis R., Polonis, Victoria R., Shapiro, Lawrence, Wong, Chi-Huey, Mascola, John R., Kwong, Peter D., Wu, Xueling, Benjamin, Betty, Blakesley, Robert, Bouffard, Gerry, Brooks, Shelise, Coleman, Holly, Dekhtyar, Mila, Gregory, Michael, Guan, Xiaobin, Gupta, Jyoti, Han, Joel, Hargrove, April, Ho, Shiling, Legaspi, Richelle, Maduro, Quino, Masiello, Cathy, Maskeri, Baishali, McDowell, Jenny, Montemayor, Casandra, Mullikin, James, Park, Morgan, Riebow, Nancy, Schandler, Karen, Schmidt, Brian, Sison, Christina, Stantripop, Mal, Thomas, James, Thomas, Pam, Vemulapalli, Meg, and Young, Alice. A Neutralizing Antibody Recognizing Primarily N-Linked Glycan Targets the Silent Face of the HIV Envelope. United States: N. p., 2018. Web. doi:10.1016/j.immuni.2018.02.013.
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Zhou, Tongqing, Zheng, Anqi, Baxa, Ulrich, Chuang, Gwo-Yu, Georgiev, Ivelin S., Kong, Rui, O’Dell, Sijy, Shahzad-ul-Hussan, Syed, Shen, Chen-Hsiang, Tsybovsky, Yaroslav, Bailer, Robert T., Gift, Syna K., Louder, Mark K., McKee, Krisha, Rawi, Reda, Stevenson, Catherine H., Stewart-Jones, Guillaume B. E., Taft, Justin D., Waltari, Eric, Yang, Yongping, Zhang, Baoshan, Shivatare, Sachin S., Shivatare, Vidya S., Lee, Chang-Chun D., Wu, Chung-Yi, Mullikin, James C., Bewley, Carole A., Burton, Dennis R., Polonis, Victoria R., Shapiro, Lawrence, Wong, Chi-Huey, Mascola, John R., Kwong, Peter D., Wu, Xueling, Benjamin, Betty, Blakesley, Robert, Bouffard, Gerry, Brooks, Shelise, Coleman, Holly, Dekhtyar, Mila, Gregory, Michael, Guan, Xiaobin, Gupta, Jyoti, Han, Joel, Hargrove, April, Ho, Shiling, Legaspi, Richelle, Maduro, Quino, Masiello, Cathy, Maskeri, Baishali, McDowell, Jenny, Montemayor, Casandra, Mullikin, James, Park, Morgan, Riebow, Nancy, Schandler, Karen, Schmidt, Brian, Sison, Christina, Stantripop, Mal, Thomas, James, Thomas, Pam, Vemulapalli, Meg, & Young, Alice. A Neutralizing Antibody Recognizing Primarily N-Linked Glycan Targets the Silent Face of the HIV Envelope. United States. https://doi.org/10.1016/j.immuni.2018.02.013
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Zhou, Tongqing, Zheng, Anqi, Baxa, Ulrich, Chuang, Gwo-Yu, Georgiev, Ivelin S., Kong, Rui, O’Dell, Sijy, Shahzad-ul-Hussan, Syed, Shen, Chen-Hsiang, Tsybovsky, Yaroslav, Bailer, Robert T., Gift, Syna K., Louder, Mark K., McKee, Krisha, Rawi, Reda, Stevenson, Catherine H., Stewart-Jones, Guillaume B. E., Taft, Justin D., Waltari, Eric, Yang, Yongping, Zhang, Baoshan, Shivatare, Sachin S., Shivatare, Vidya S., Lee, Chang-Chun D., Wu, Chung-Yi, Mullikin, James C., Bewley, Carole A., Burton, Dennis R., Polonis, Victoria R., Shapiro, Lawrence, Wong, Chi-Huey, Mascola, John R., Kwong, Peter D., Wu, Xueling, Benjamin, Betty, Blakesley, Robert, Bouffard, Gerry, Brooks, Shelise, Coleman, Holly, Dekhtyar, Mila, Gregory, Michael, Guan, Xiaobin, Gupta, Jyoti, Han, Joel, Hargrove, April, Ho, Shiling, Legaspi, Richelle, Maduro, Quino, Masiello, Cathy, Maskeri, Baishali, McDowell, Jenny, Montemayor, Casandra, Mullikin, James, Park, Morgan, Riebow, Nancy, Schandler, Karen, Schmidt, Brian, Sison, Christina, Stantripop, Mal, Thomas, James, Thomas, Pam, Vemulapalli, Meg, and Young, Alice. Tue . "A Neutralizing Antibody Recognizing Primarily N-Linked Glycan Targets the Silent Face of the HIV Envelope". United States. https://doi.org/10.1016/j.immuni.2018.02.013. https://www.osti.gov/servlets/purl/1506497.
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@article{osti_1506497,
title = {A Neutralizing Antibody Recognizing Primarily N-Linked Glycan Targets the Silent Face of the HIV Envelope},
author = {Zhou, Tongqing and Zheng, Anqi and Baxa, Ulrich and Chuang, Gwo-Yu and Georgiev, Ivelin S. and Kong, Rui and O’Dell, Sijy and Shahzad-ul-Hussan, Syed and Shen, Chen-Hsiang and Tsybovsky, Yaroslav and Bailer, Robert T. and Gift, Syna K. and Louder, Mark K. and McKee, Krisha and Rawi, Reda and Stevenson, Catherine H. and Stewart-Jones, Guillaume B. E. and Taft, Justin D. and Waltari, Eric and Yang, Yongping and Zhang, Baoshan and Shivatare, Sachin S. and Shivatare, Vidya S. and Lee, Chang-Chun D. and Wu, Chung-Yi and Mullikin, James C. and Bewley, Carole A. and Burton, Dennis R. and Polonis, Victoria R. and Shapiro, Lawrence and Wong, Chi-Huey and Mascola, John R. and Kwong, Peter D. and Wu, Xueling and Benjamin, Betty and Blakesley, Robert and Bouffard, Gerry and Brooks, Shelise and Coleman, Holly and Dekhtyar, Mila and Gregory, Michael and Guan, Xiaobin and Gupta, Jyoti and Han, Joel and Hargrove, April and Ho, Shiling and Legaspi, Richelle and Maduro, Quino and Masiello, Cathy and Maskeri, Baishali and McDowell, Jenny and Montemayor, Casandra and Mullikin, James and Park, Morgan and Riebow, Nancy and Schandler, Karen and Schmidt, Brian and Sison, Christina and Stantripop, Mal and Thomas, James and Thomas, Pam and Vemulapalli, Meg and Young, Alice},
abstractNote = {Virtually the entire surface of the HIV-1-envelope trimer is recognized by neutralizing antibodies, except for a highly glycosylated region at the center of the “silent face” on the gp120 subunit. From an HIV-1-infected donor, #74, we identified antibody VRC-PG05, which neutralized 27% of HIV-1 strains. The crystal structure of the antigen-binding fragment of VRC-PG05 in complex with gp120 revealed an epitope comprised primarily of N-linked glycans from N262, N295, and N448 at the silent face center. Furthermore, somatic hypermutation occurred preferentially at antibody residues that interacted with these glycans, suggesting somatic development of glycan recognition. Resistance to VRC-PG05 in donor #74 involved shifting of glycan-N448 to N446 or mutation of glycan-proximal residue E293. HIV-1 neutralization can thus be achieved at the silent face center by glycan-recognizing antibody; along with other known epitopes, the VRC-PG05 epitope completes coverage by neutralizing antibody of all major exposed regions of the prefusion closed trimer.},
doi = {10.1016/j.immuni.2018.02.013},
journal = {Immunity},
number = 3,
volume = 48,
place = {United States},
year = {Tue Mar 13 00:00:00 EDT 2018},
month = {Tue Mar 13 00:00:00 EDT 2018}
}
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