ArticleScience (New York, N.Y.)2021
Recapitulation of HIV-1 Env-antibody coevolution in macaques leading to neutralization breadth.
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Article in Science (New York, N.Y.), 2021. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 79 papers.
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79citing papers in PubMed
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Who cites it
79 citing papers in PubMed, 94 citations in OpenAlex.
- Deletions in variable region 1 of the HIV envelope accelerate V3-glycan bNAb induction in SHIV-infected rhesus macaques.Proceedings of the National Academy of Sciences of the United States of America · 2026Article
- Priming of Multiple HIV Neutralizing B Cell Precursors in Humans.medRxiv : the preprint server for health sciences · 2026Article
- Vaccine elicitation of HIV broadly neutralizing antibodies from genome-edited B cells in non-human primates and derived lymphoid organoids.Gene therapy · 2026Article
- Apex-guided HIV vaccination: liposome-displayed Env trimers elicit PG9-like cross-neutralizing antibodies.Signal transduction and targeted therapy · 2026Article
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- Scientific synergy between prophylactic and therapeutic HIV vaccines-prevention and cure.NPJ vaccines · 2026Article
- Induction of broadly neutralizing HIV antibodies by a two-step mechanism informs vaccine design.Science (New York, N.Y.) · 2026Article
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- Genotypic challenges in implementing broadly neutralizing antibody-based long-acting HIV-1 therapies.Communications medicine · 2026Review
- Deep mining of the human antibody repertoire identifies frequent and genetically diverse CDRH3 topologies targetable by vaccination.Proceedings of the National Academy of Sciences of the United States of America · 2026Article
- Structural and genetic signatures of two classes of HCV E2 neutralizing face antibodies from non-human primates immunized with a recombinant E1E2.NPJ vaccines · 2026Article
- Germline-targeting HIV immunogen induces cross-neutralizing antibodies in outbred macaques.Immunity · 2026Article
- Early clonal dominance at priming sets the trajectory for broad HIV serum neutralization.bioRxiv : the preprint server for biology · 2026Article
- Predicting viral sensitivity to antibodies using genetic sequences and antibody similarities.PLoS computational biology · 2026Article
- Env-antibody coevolution identifies B cell priming as the principal bottleneck to HIV V2 apex broadly neutralizing antibody development.Science immunology · 2026Article
- Rapidly acquired HIV-1 neutralization breadth in a rhesus V2 apex knockin mouse model after a single bolus immunization.Science immunology · 2026Article
- Functional Convergence of Genetically Diverse B-Cell Receptors in Simian-HIV Infected Rhesus Macaques.bioRxiv : the preprint server for biology · 2026Article
- Experimental evolution in an era of molecular manipulation.Nature reviews. Genetics · 2026Review
- Accelerating Innovation: Advancing Opportunities in HIV Vaccine Development.Current HIV research · 2026Review
19 more citing papers are in PubMed but not listed here.
Corrections and comments
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Authors and funding
57 authors at 7 institutions in 1 country.
Ryan S Roark *Departments of Medicine and Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.ORCID https://orcid.org/0000-0003-0586-103X
Hui Li *Departments of Medicine and Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.ORCID https://orcid.org/0000-0001-7231-8219
Wilton B Williams *Duke Human Vaccine Institute, Duke University School of Medicine, Durham, NC 27710, USA.ORCID https://orcid.org/0000-0002-2970-7259
Hema Chug *Laboratory of Molecular Medicine, Boston Children's Hospital and Harvard Medical School, Boston, MA 02115, USA.ORCID https://orcid.org/0000-0002-9889-7076
Rosemarie D Mason *Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.ORCID https://orcid.org/0000-0001-7123-4902
Jason Gorman *Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.ORCID https://orcid.org/0000-0002-3775-6560
Shuyi WangDepartments of Medicine and Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.ORCID https://orcid.org/0000-0001-6831-9323
Fang-Hua LeeDepartments of Medicine and Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.ORCID https://orcid.org/0000-0003-1853-1902
Juliette RandoDepartments of Medicine and Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.ORCID https://orcid.org/0000-0002-1742-9255
Mattia BonsignoriDuke Human Vaccine Institute, Duke University School of Medicine, Durham, NC 27710, USA.ORCID https://orcid.org/0000-0003-2973-2101
Kwan-Ki HwangDuke Human Vaccine Institute, Duke University School of Medicine, Durham, NC 27710, USA.ORCID https://orcid.org/0000-0002-3903-6997
Kevin O SaundersDuke Human Vaccine Institute, Duke University School of Medicine, Durham, NC 27710, USA.ORCID https://orcid.org/0000-0001-7399-7954
Kevin WieheDuke Human Vaccine Institute, Duke University School of Medicine, Durham, NC 27710, USA.ORCID https://orcid.org/0000-0001-9933-9618
M Anthony MoodyDuke Human Vaccine Institute, Duke University School of Medicine, Durham, NC 27710, USA.ORCID https://orcid.org/0000-0002-3890-5855
Peter T HraberTheoretical Biology and Biophysics, Los Alamos National Laboratory, Los Alamos, NM 87545, USA.ORCID https://orcid.org/0000-0002-2920-4897
Kshitij WaghTheoretical Biology and Biophysics, Los Alamos National Laboratory, Los Alamos, NM 87545, USA.ORCID https://orcid.org/0000-0001-7552-6582
Elena E GiorgiTheoretical Biology and Biophysics, Los Alamos National Laboratory, Los Alamos, NM 87545, USA.
Ronnie M RussellDepartments of Medicine and Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.ORCID https://orcid.org/0000-0003-1484-4207
Frederic Bibollet-RucheDepartments of Medicine and Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.
Weimin LiuDepartments of Medicine and Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.
Jesse ConnellDepartments of Medicine and Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.ORCID https://orcid.org/0000-0002-9393-3074
Andrew G SmithDepartments of Medicine and Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.
Julia DeVotoDepartments of Medicine and Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.
Alexander I MurphyDepartments of Medicine and Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.ORCID https://orcid.org/0000-0003-3866-960X
Jessica SmithDepartments of Medicine and Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.
Wenge DingDepartments of Medicine and Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.
Chengyan ZhaoDepartments of Medicine and Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.
Neha ChohanDepartments of Medicine and Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.ORCID https://orcid.org/0000-0002-2665-4622
Maho OkumuraDepartments of Medicine and Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.
Christina RosarioDepartments of Medicine and Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.ORCID https://orcid.org/0000-0002-2508-4226
Yu DingDepartments of Medicine and Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.ORCID https://orcid.org/0000-0003-1521-2383
Emily LindemuthDepartments of Medicine and Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.ORCID https://orcid.org/0000-0001-5721-0787
Anya M BauerDepartments of Medicine and Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.
Katharine J BarDepartments of Medicine and Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.ORCID https://orcid.org/0000-0002-9773-0071
David AmbrozakVaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.
Cara W ChaoVaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.
Gwo-Yu ChuangVaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.
Hui GengVaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.
Bob C LinVaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.
Mark K LouderVaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.ORCID https://orcid.org/0000-0001-7540-9263
Richard NguyenVaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.ORCID https://orcid.org/0000-0003-2453-3461
Baoshan ZhangVaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.
Mark G LewisBioqual, Inc., Rockville, MD 20850, USA.ORCID https://orcid.org/0000-0001-7852-0135
Donald D RaymondLaboratory of Molecular Medicine, Boston Children's Hospital and Harvard Medical School, Boston, MA 02115, USA.ORCID https://orcid.org/0000-0003-4154-6141
Nicole A Doria-RoseVaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.ORCID https://orcid.org/0000-0002-5731-3054
Chaim A SchrammVaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.
Daniel C DouekVaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.
Mario RoedererVaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.ORCID https://orcid.org/0000-0001-7448-7040
Thomas B KeplerDepartment of Microbiology, Boston University School of Medicine, Boston, MA 02118, USA.ORCID https://orcid.org/0000-0002-1383-6865
Garnett KelsoeDuke Human Vaccine Institute, Duke University School of Medicine, Durham, NC 27710, USA.ORCID https://orcid.org/0000-0002-8770-040X
John R MascolaVaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.ORCID https://orcid.org/0000-0002-5293-4695
Peter D KwongVaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.ORCID https://orcid.org/0000-0003-3560-232X
Bette T KorberTheoretical Biology and Biophysics, Los Alamos National Laboratory, Los Alamos, NM 87545, USA.ORCID https://orcid.org/0000-0002-2026-5757
Stephen C HarrisonLaboratory of Molecular Medicine, Boston Children's Hospital and Harvard Medical School, Boston, MA 02115, USA.ORCID https://orcid.org/0000-0001-7215-9393
Barton F HaynesDuke Human Vaccine Institute, Duke University School of Medicine, Durham, NC 27710, USA.ORCID https://orcid.org/0000-0002-7643-9023
Beatrice H HahnDepartments of Medicine and Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.ORCID https://orcid.org/0000-0002-9400-9887
George M ShawDepartments of Medicine and Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA. shawg@pennmedicine.upenn.edu.ORCID https://orcid.org/0000-0002-2338-4532
University of Pennsylvania · USNational Institutes of Health · USDuke University · USLos Alamos National Laboratory · USBoston Children's Hospital · USBioqual · USBoston University · US
Funding
Virus biology scientific research support componentUM1AI100645 · NIAID · DUKE UNIVERSITY · PI HAYNES, BARTON F. · 2012 to 2018
$204.7MNonhuman primate studies for development of a prototype HIV vaccine that induces broadly neutralizing antibodiesUM1AI144371 · NIAID · DUKE UNIVERSITY · PI HAYNES, BARTON F. · 2019 to 2025
$190.4MVirus & Reservoirs CoreP30AI045008 · NIAID · UNIVERSITY OF PENNSYLVANIA · PI DAVID S METZGER · 1999 to 2026
$78.6MViral TestingU42OD021458 · OD · UNIVERSITY OF PUERTO RICO MED SCIENCES · PI Armando Gil Burgos-Rodriguez, Marcos Lopez · 2016 to 2026
$45.1MVirus and Antibody Gene Sequencing CoreP01AI131251 · NIAID · UNIVERSITY OF PENNSYLVANIA · PI Kevin Wiehe · 2017 to 2026
$40.7MTranslational Science InitiativeP40OD012217 · OD · UNIVERSITY OF PUERTO RICO MED SCIENCES · PI CARLOS A SARIOL · 2012 to 2026
$40.4MNeutralization Mechanisms Of Anti-HIV-1 Monoclonal AntibodiesZIAAI005022 · NIAID · NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES · PI ZHOU, TONGQING · 2009 to 2025
$24.6MHost Genomic Factors in Infectious Disease Susceptibility ZIAAI005066 · NIAID · NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES · PI DOUEK, DANIEL CESAR · 2009 to 2025
$17.9MThe Genome Analysis CoreZICAI005133 · NIAID · NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES · PI DOUEK, DANIEL CESAR · 2019 to 2025
$16.9MTRD #3: An automated and streamlined pipeline for in-situ molecular microscopyP41GM103310 · NIGMS · SCRIPPS RESEARCH INSTITUTE, THE · PI DE MARCO, ALEX, KIEFT, JEFFREY S · 2012 to 2021
$14.7MOverall EvaluationP41GM103403 · NIGMS · CORNELL UNIVERSITY · PI EALICK, STEVEN E · 2012 to 2017
$14.3MT Cell Immune Responses To HIV And Other PathogensZIAAI005033 · NIAID · NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES · PI DOUEK, DANIEL CESAR · 2009 to 2025
$11.4MNIAID NIH HHS P01 AI131251NIAID NIH HHS P30 AI045008NIAID NIH HHS R01 AI050529NIAID NIH HHS R01 AI128832NIAID NIH HHS R01 AI131331NIAID NIH HHS R01 AI140897NIAID NIH HHS R01 AI160607NIAID NIH HHS R01 AI165080NIAID NIH HHS R37 AI050529NIAID NIH HHS R37 AI140897NIAID NIH HHS R37 AI150590NIAID NIH HHS R61 AI161818NIAID NIH HHS T32 AI007632NIAID NIH HHS UM1 AI100645NIAID NIH HHS UM1 AI144371NIGMS NIH HHS P41 GM103310NIGMS NIH HHS P41 GM103403NIH HHS P40 OD012217NIH HHS U42 OD021458
Abstract
Neutralizing antibodies elicited by HIV-1 coevolve with viral envelope proteins (Env) in distinctive patterns, in some cases acquiring substantial breadth. We report that primary HIV-1 envelope proteins-when expressed by simian-human immunodeficiency viruses in rhesus macaques-elicited patterns of Env-antibody coevolution very similar to those in humans, including conserved immunogenetic, structural, and chemical solutions to epitope recognition and precise Env-amino acid substitutions, insertions, and deletions leading to virus persistence. The structure of one rhesus antibody, capable of neutralizing 49% of a 208-strain panel, revealed a V2 apex mode of recognition like that of human broadly neutralizing antibodies (bNAbs) PGT145 and PCT64-35S. Another rhesus antibody bound the CD4 binding site by CD4 mimicry, mirroring human bNAbs 8ANC131, CH235, and VRC01. Virus-antibody coevolution in macaques can thus recapitulate developmental features of human bNAbs, thereby guiding HIV-1 immunogen design.
Indexed as
Broadly Neutralizing AntibodiesHIV AntibodiesAnimalsBinding SitesBiological CoevolutionCD4 AntigensCryoelectron MicroscopyEpitopesHIV-1HIV Envelope Protein gp120HIV InfectionsHumansMacaca mulattaMolecular MimicrySimian Immunodeficiency VirusVirus ReplicationBroadly Neutralizing AntibodiesCD4 AntigensEpitopesHIV AntibodiesHIV Envelope Protein gp120
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