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Engineering well-expressed, V2-immunofocusing HIV-1 envelope glycoprotein membrane trimers for use in heterologous prime-boost vaccine regimens

Engineering well-expressed, V2-immunofocusing HIV-1 envelope glycoprotein membrane trimers for use in heterologous prime-boost vaccine regimens
Engineering well-expressed, V2-immunofocusing HIV-1 envelope glycoprotein membrane trimers for use in heterologous prime-boost vaccine regimens

HIV-1 vaccine immunofocusing strategies may be able to induce broadly-reactive neutralizing antibodies (NAbs). Here, we engineered a panel of diverse, membrane-resident native HIV-1 trimers vulnerable to two broad targets-the V2 apex and fusion peptide (FP). Selection criteria included i) high expression and ii) infectious function, so that trimer neutralization sensitivity can be profiled in pseudovirus (PV) assays. Initially, we boosted the expression of 17 candidate trimers by truncating gp41 and introducing a gp120-gp41 SOS disulfide to prevent gp120 shedding. "Repairs" were made to fill glycan holes and eliminate other strain-specific aberrations. A new neutralization assay allowed PV infection when our standard assay was insufficient. Trimers with exposed V3 loops, a target of non-NAbs, were discarded. To try to increase V2-sensitivity, we removed clashing glycans and modified the C-strand. Notably, a D167N mutation improved V2-sensitivity in several cases. Glycopeptide analysis of JR-FL trimers revealed near complete sequon occupation and that filling the N197 glycan hole was well-tolerated. In contrast, sequon optimization and inserting/removing glycans at other positions frequently had global "ripple" effects on glycan maturation and sequon occupation throughout the gp120 outer domain and gp41. V2 MAb CH01 selectively bound to trimers with small high mannose glycans near the base of the V1 loop, thereby avoiding clashes. Knocking in a rare N49 glycan was found to perturb gp41 glycans, increasing FP NAb sensitivity-and sometimes improving expression. Finally, a biophysical analysis of VLPs revealed that i) ~25% of particles bear Env spikes, ii) spontaneous particle budding is high and only increases 4-fold upon Gag transfection, and iii) Env+ particles express ~30-40 spikes. Taken together, we identified 7 diverse trimers with a range of sensitivities to two targets to allow rigorous testing of immunofocusing vaccine concepts.

AIDS Vaccines/immunology, Broadly Neutralizing Antibodies/immunology, Epitopes/immunology, HIV Antibodies/immunology, HIV Envelope Protein gp120/immunology, HIV Envelope Protein gp41/immunology, HIV-1/immunology, Humans
1553-7366
Crooks, Emma T
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Almanza, Francisco
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D'Addabbo, Alessio
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Duggan, Erika
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Zhang, Jinsong
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Wagh, Kshitij
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Mou, Huihui
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Allen, Joel D
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Thomas, Alyssa
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Osawa, Keiko
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Korber, Bette T
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Tsybovsky, Yaroslav
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Cale, Evan
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Nolan, John
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Crispin, Max
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Verkoczy, Laurent K
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Binley, James M
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Crooks, Emma T
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Almanza, Francisco
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D'Addabbo, Alessio
ae2358c9-d733-4c7f-aaf3-b8b52b7cb810
Duggan, Erika
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Zhang, Jinsong
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Wagh, Kshitij
80b12c7f-2218-47ff-9eac-1d009be67a55
Mou, Huihui
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Allen, Joel D
c89d5569-7659-4835-b535-c9586e956b3a
Thomas, Alyssa
d8348a9c-9183-49bd-b394-8069a2fa6add
Osawa, Keiko
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Korber, Bette T
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Tsybovsky, Yaroslav
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Cale, Evan
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Nolan, John
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Crispin, Max
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Verkoczy, Laurent K
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Binley, James M
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Crooks, Emma T, Almanza, Francisco, D'Addabbo, Alessio, Duggan, Erika, Zhang, Jinsong, Wagh, Kshitij, Mou, Huihui, Allen, Joel D, Thomas, Alyssa, Osawa, Keiko, Korber, Bette T, Tsybovsky, Yaroslav, Cale, Evan, Nolan, John, Crispin, Max, Verkoczy, Laurent K and Binley, James M (2021) Engineering well-expressed, V2-immunofocusing HIV-1 envelope glycoprotein membrane trimers for use in heterologous prime-boost vaccine regimens. PLOS Pathogens, 17 (10), [e1009807]. (doi:10.1371/journal.ppat.1009807).

Record type: Article

Abstract

HIV-1 vaccine immunofocusing strategies may be able to induce broadly-reactive neutralizing antibodies (NAbs). Here, we engineered a panel of diverse, membrane-resident native HIV-1 trimers vulnerable to two broad targets-the V2 apex and fusion peptide (FP). Selection criteria included i) high expression and ii) infectious function, so that trimer neutralization sensitivity can be profiled in pseudovirus (PV) assays. Initially, we boosted the expression of 17 candidate trimers by truncating gp41 and introducing a gp120-gp41 SOS disulfide to prevent gp120 shedding. "Repairs" were made to fill glycan holes and eliminate other strain-specific aberrations. A new neutralization assay allowed PV infection when our standard assay was insufficient. Trimers with exposed V3 loops, a target of non-NAbs, were discarded. To try to increase V2-sensitivity, we removed clashing glycans and modified the C-strand. Notably, a D167N mutation improved V2-sensitivity in several cases. Glycopeptide analysis of JR-FL trimers revealed near complete sequon occupation and that filling the N197 glycan hole was well-tolerated. In contrast, sequon optimization and inserting/removing glycans at other positions frequently had global "ripple" effects on glycan maturation and sequon occupation throughout the gp120 outer domain and gp41. V2 MAb CH01 selectively bound to trimers with small high mannose glycans near the base of the V1 loop, thereby avoiding clashes. Knocking in a rare N49 glycan was found to perturb gp41 glycans, increasing FP NAb sensitivity-and sometimes improving expression. Finally, a biophysical analysis of VLPs revealed that i) ~25% of particles bear Env spikes, ii) spontaneous particle budding is high and only increases 4-fold upon Gag transfection, and iii) Env+ particles express ~30-40 spikes. Taken together, we identified 7 diverse trimers with a range of sensitivities to two targets to allow rigorous testing of immunofocusing vaccine concepts.

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Accepted/In Press date: 7 October 2021
Published date: 22 October 2021
Keywords: AIDS Vaccines/immunology, Broadly Neutralizing Antibodies/immunology, Epitopes/immunology, HIV Antibodies/immunology, HIV Envelope Protein gp120/immunology, HIV Envelope Protein gp41/immunology, HIV-1/immunology, Humans

Identifiers

Local EPrints ID: 453008
URI: http://eprints.soton.ac.uk/id/eprint/453008
ISSN: 1553-7366
PURE UUID: 72020fab-54bc-444e-a210-886c5ba9fa7e
ORCID for Alessio D'Addabbo: ORCID iD orcid.org/0000-0003-2542-6465
ORCID for Joel D Allen: ORCID iD orcid.org/0000-0003-2547-968X
ORCID for Max Crispin: ORCID iD orcid.org/0000-0002-1072-2694

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Date deposited: 07 Jan 2022 14:23
Last modified: 17 Mar 2024 04:09

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Contributors

Author: Emma T Crooks
Author: Francisco Almanza
Author: Erika Duggan
Author: Jinsong Zhang
Author: Kshitij Wagh
Author: Huihui Mou
Author: Joel D Allen ORCID iD
Author: Alyssa Thomas
Author: Keiko Osawa
Author: Bette T Korber
Author: Yaroslav Tsybovsky
Author: Evan Cale
Author: John Nolan
Author: Max Crispin ORCID iD
Author: Laurent K Verkoczy
Author: James M Binley

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