A Germline-Targeting Chimpanzee SIV Envelope Glycoprotein Elicits a New Class of V2-Apex Directed Cross-Neutralizing Antibodies

Bibollet-Ruche, Frederic; Russell, Ronnie M.; Ding, Wenge; Liu, Weimin; Li, Yingying; Wagh, Kshitij; Wrapp, Daniel; Habib, Rumi; Skelly, Ashwin N.; Roark, Ryan S.; Sherrill-Mix, Scott; Wang, Shuyi; Rando, Juliette; Lindemuth, Emily; Cruickshank, Kendra; Park, Younghoon; Baum, Rachel; Carey, John W.; Connell, Andrew Jesse; Li, Hui; Giorgi, Elena E.; Song, Ge S.; Ding, Shilei; Finzi, Andrés; Newman, Amanda; Hernandez, Giovanna E.; Machiele, Emily; Cain, Derek W.; Mansouri, Katayoun; Lewis, Mark G.; Montefiori, David C.; Wiehe, Kevin J.; Alam, S. Munir; Teng, I-Ting; Kwong, Peter D.; Andrabi, Raiees; Verkoczy, Laurent; Burton, Dennis R.; Korber, Bette T.; Saunders, Kevin O.; Haynes, Barton F.; Edwards, Robert J.; Shaw, George M.; Hahn, Beatrice H.

doi:10.1128/mbio.03370-22

A Germline-Targeting Chimpanzee SIV Envelope Glycoprotein Elicits a New Class of V2-Apex Directed Cross-Neutralizing Antibodies

Journal Article · Wed Jan 11 00:00:00 EST 2023 · mBio (Online)

DOI:https://doi.org/10.1128/mbio.03370-22· OSTI ID:2470552

Bibollet-Ruche, Frederic ^[1]; Russell, Ronnie M. ^[1]; Ding, Wenge ^[1]; Liu, Weimin ^[1]; Li, Yingying ^[1]; Wagh, Kshitij ^[2]; ^[3]; Habib, Rumi ^[4]; ^[4]; Roark, Ryan S. ^[1]; Sherrill-Mix, Scott ^[1]; Wang, Shuyi ^[1]; Rando, Juliette ^[1]; Lindemuth, Emily ^[1]; Cruickshank, Kendra ^[1]; Park, Younghoon ^[1]; Baum, Rachel ^[1]; Carey, John W. ^[1]; Connell, Andrew Jesse ^[1]; Li, Hui ^[1] more »

University of Pennsylvania, Philadelphia, PA (United States)
Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)
Duke University School of Medicine, Durham, NC (United States)
University of Pennsylvania, Philadelphia, PA (United States); The Wistar Institute, Philadelphia, PA (United States)
The Scripps Research Institute, La Jolla, CA (United States)
Centre de Recherche du CHUM, Montreal, QC (Canada); Univ. of Montreal, QC (Canada)
Bioqual, Inc., Rockville, MD (United States)
National Institutes of Health (NIH), Bethesda, MD (United States)
San Diego Biomedical Research Institute, CA (United States)
The Scripps Research Institute, La Jolla, CA (United States); Ragon Institute of MGH, Harvard and MIT, Cambridge, MA (United States)

HIV-1 and its SIV precursors share a broadly neutralizing antibody (bNAb) epitope in variable loop 2 (V2) at the envelope glycoprotein (Env) trimer apex. Here, we tested the immunogenicity of germ line-targeting versions of a chimpanzee SIV (SIVcpz) Env in human V2-apex bNAb heavy-chain precursor-expressing knock-in mice and as chimeric simian-chimpanzee immunodeficiency viruses (SCIVs) in rhesus macaques (RMs). Trimer immunization of knock-in mice induced V2-directed NAbs, indicating activation of V2-apex bNAb precursor-expressing mouse B cells. SCIV infection of RMs elicited high-titer viremia, potent autologous tier 2 neutralizing antibodies, and rapid sequence escape in the canonical V2-apex epitope. Six of seven animals also developed low-titer heterologous plasma breadth that mapped to the V2-apex. Antibody cloning from two of these animals identified multiple expanded lineages with long heavy chain third complementarity determining regions that cross-neutralized as many as 7 of 19 primary HIV-1 strains, but with low potency. Negative stain electron microscopy (NSEM) of members of the two most cross-reactive lineages confirmed V2 targeting but identified an angle of approach distinct from prototypical V2-apex bNAbs, with antibody binding either requiring or inducing an occluded-open trimer. Probing with conformation-sensitive, nonneutralizing antibodies revealed that SCIV-expressed, but not wild-type SIVcpz Envs, as well as a subset of primary HIV-1 Envs, preferentially adopted a more open trimeric state. These results reveal the existence of a cryptic V2 epitope that is exposed in occluded-open SIVcpz and HIV-1 Env trimers and elicits cross-neutralizing responses of limited breadth and potency.

View Accepted Manuscript (DOE)

Research Organization:: Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)

Sponsoring Organization:: Canada Research Chair on Retroviral Entry; Canadian Institutes of Health Research (CIHR); National Institutes of Health (NIH); USDOE

Grant/Contract Number:: 89233218CNA000001

OSTI ID:: 2470552

Journal Information:: mBio (Online), Journal Name: mBio (Online) Journal Issue: 1 Vol. 14; ISSN 2150-7511

Publisher:: American Society for Microbiology (ASM)Copyright Statement

Country of Publication:: United States

Language:: English

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