Recapitulation of HIV-1 Env-antibody coevolution in macaques leading to neutralization breadth.


Journal

Science (New York, N.Y.)
ISSN: 1095-9203
Titre abrégé: Science
Pays: United States
ID NLM: 0404511

Informations de publication

Date de publication:
08 01 2021
Historique:
received: 10 06 2020
accepted: 09 11 2020
pubmed: 21 11 2020
medline: 17 2 2021
entrez: 20 11 2020
Statut: ppublish

Résumé

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.

Identifiants

pubmed: 33214287
pii: science.abd2638
doi: 10.1126/science.abd2638
pmc: PMC8040783
mid: NIHMS1679978
pii:
doi:

Substances chimiques

Broadly Neutralizing Antibodies 0
CD4 Antigens 0
Epitopes 0
HIV Antibodies 0
HIV Envelope Protein gp120 0

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, N.I.H., Intramural

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : NIAID NIH HHS
ID : UM1 AI100645
Pays : United States
Organisme : NIGMS NIH HHS
ID : P41 GM103403
Pays : United States
Organisme : NIAID NIH HHS
ID : T32 AI007632
Pays : United States
Organisme : NIAID NIH HHS
ID : R37 AI050529
Pays : United States
Organisme : NIAID NIH HHS
ID : R37 AI150590
Pays : United States
Organisme : NIAID NIH HHS
ID : P30 AI045008
Pays : United States
Organisme : NIAID NIH HHS
ID : R01 AI140897
Pays : United States
Organisme : NIAID NIH HHS
ID : P01 AI131251
Pays : United States
Organisme : NIAID NIH HHS
ID : R01 AI128832
Pays : United States
Organisme : NIH HHS
ID : U42 OD021458
Pays : United States
Organisme : NIGMS NIH HHS
ID : P41 GM103310
Pays : United States
Organisme : NIAID NIH HHS
ID : R61 AI161818
Pays : United States
Organisme : NIAID NIH HHS
ID : R01 AI131331
Pays : United States
Organisme : NIAID NIH HHS
ID : R01 AI160607
Pays : United States
Organisme : NIAID NIH HHS
ID : R01 AI165080
Pays : United States
Organisme : NIAID NIH HHS
ID : R01 AI050529
Pays : United States
Organisme : NIAID NIH HHS
ID : UM1 AI144371
Pays : United States
Organisme : NIH HHS
ID : P40 OD012217
Pays : United States

Informations de copyright

Copyright © 2021, American Association for the Advancement of Science.

Références

Nucleic Acids Res. 2004 Jul 1;32(Web Server issue):W615-9
pubmed: 15215462
Nat Methods. 2015 Oct;12(10):943-6
pubmed: 26280328
J Virol. 2010 Dec;84(24):12995-3003
pubmed: 20881050
J Virol. 2005 Apr;79(8):5232-7
pubmed: 15795308
Nat Commun. 2019 Feb 13;10(1):721
pubmed: 30760721
mBio. 2015 Apr 21;6(2):
pubmed: 25900654
Viruses. 2015 Oct 21;7(10):5443-75
pubmed: 26506369
J Virol. 2000 Jan;74(1):254-63
pubmed: 10590113
Front Immunol. 2017 Oct 27;8:1407
pubmed: 29163486
N Engl J Med. 2016 Jun 2;374(22):2120-30
pubmed: 27192360
J Immunol Methods. 2012 Dec 14;386(1-2):10-21
pubmed: 22955212
J Struct Biol. 2007 Jan;157(1):38-46
pubmed: 16859925
Cell Rep. 2018 Jun 12;23(11):3249-3261
pubmed: 29898396
J Gen Virol. 1979 Jan;42(1):1-26
pubmed: 215703
J Struct Biol. 2009 Apr;166(1):95-102
pubmed: 19263523
Front Immunol. 2014 Apr 22;5:170
pubmed: 24795717
Cell Rep. 2018 Oct 23;25(4):893-908.e7
pubmed: 30355496
Nature. 1995 Jan 12;373(6510):123-6
pubmed: 7816094
PLoS Pathog. 2016 Jan 14;12(1):e1005369
pubmed: 26766578
Bioinformatics. 2006 Feb 15;22(4):438-44
pubmed: 16357034
Science. 2005 Jun 24;308(5730):1906-8
pubmed: 15860590
Nature. 2019 Jun;570(7762):468-473
pubmed: 31142836
PLoS Pathog. 2016 Dec 13;12(12):e1006114
pubmed: 27959955
Structure. 2011 May 11;19(5):691-9
pubmed: 21565703
Annu Rev Immunol. 2020 Apr 26;38:673-703
pubmed: 32340576
Sci Transl Med. 2019 Oct 30;11(516):
pubmed: 31666399
Nat Methods. 2017 Mar;14(3):290-296
pubmed: 28165473
J Struct Biol. 2016 Jan;193(1):1-12
pubmed: 26592709
J Struct Biol. 2015 Nov;192(2):216-21
pubmed: 26278980
Nature. 2002 Dec 12;420(6916):678-82
pubmed: 12478295
Immunity. 2015 Nov 17;43(5):959-73
pubmed: 26588781
Sci Immunol. 2017 Jan 27;2(7):
pubmed: 28783671
Virology. 2006 Feb 5;345(1):44-55
pubmed: 16242749
J Immunol Methods. 2014 Jul;409:131-46
pubmed: 24291345
Front Immunol. 2016 Sep 21;7:372
pubmed: 27708645
J Struct Biol. 2009 May;166(2):205-13
pubmed: 19374019
Science. 2011 Nov 25;334(6059):1097-103
pubmed: 21998254
Nat Protoc. 2013 Oct;8(10):1907-15
pubmed: 24030440
J Virol. 2019 Mar 5;93(6):
pubmed: 30567996
J Virol. 2013 Feb;87(3):1554-68
pubmed: 23175357
Nature. 2014 Oct 23;514(7523):455-61
pubmed: 25296255
Cell. 1986 Jun 6;45(5):637-48
pubmed: 2423250
Nat Commun. 2017 Nov 23;8(1):1732
pubmed: 29170366
Science. 2019 Dec 6;366(6470):
pubmed: 31806786
Nature. 1998 Jun 18;393(6686):705-11
pubmed: 9641684
Immunity. 2017 Jun 20;46(6):1073-1088.e6
pubmed: 28636956
J Virol. 2016 Mar 28;90(8):4017-4031
pubmed: 26842476
Cell. 2016 Apr 7;165(2):449-63
pubmed: 26949186
J Virol. 2010 Feb;84(3):1439-52
pubmed: 19939925
Cell Host Microbe. 2019 Jan 9;25(1):59-72.e8
pubmed: 30629920
J Virol. 2015 Oct 14;90(1):76-91
pubmed: 26468542
Nature. 1995 Jan 12;373(6510):117-22
pubmed: 7529365
J Virol. 2009 Feb;83(3):1240-59
pubmed: 19019969
J Exp Med. 2005 May 2;201(9):1407-19
pubmed: 15867093
PLoS Pathog. 2013;9(5):e1003342
pubmed: 23658524
J Virol. 2013 May;87(9):4882-94
pubmed: 23408621
J Exp Med. 2009 Jun 8;206(6):1253-72
pubmed: 19487423
Science. 2015 Jul 10;349(6244):191-5
pubmed: 26113642
J Immunol Methods. 2008 Jan 1;329(1-2):112-24
pubmed: 17996249
Sci Transl Med. 2017 Mar 15;9(381):
pubmed: 28298420
Proc Natl Acad Sci U S A. 2014 Jul 15;111(28):10275-80
pubmed: 24982157
Retrovirology. 2018 Sep 5;15(1):61
pubmed: 30185183
Virology. 2010 Jan 20;396(2):213-25
pubmed: 19913270
Commun Biol. 2018 Sep 5;1:134
pubmed: 30272013
Curr Protoc Cytom. 2010 Jul;Chapter 9:Unit 9.34
pubmed: 20578108
Elife. 2020 Oct 21;9:
pubmed: 33084569
Proc Natl Acad Sci U S A. 2011 Dec 13;108(50):20125-9
pubmed: 22123961
Acta Crystallogr D Biol Crystallogr. 2010 Apr;66(Pt 4):486-501
pubmed: 20383002
Science. 2011 Sep 16;333(6049):1633-7
pubmed: 21764753
PLoS Pathog. 2016 May 24;12(5):e1005674
pubmed: 27219002
PLoS Pathog. 2013 Sep;9(9):e1003618
pubmed: 24068931
Immunity. 2016 Jul 19;45(1):31-45
pubmed: 27438765
J Virol. 2011 Oct;85(19):9998-10009
pubmed: 21795340
Nat Protoc. 2009;4(3):372-84
pubmed: 19247287
Cell. 2014 Jul 31;158(3):481-91
pubmed: 25065977
Trends Microbiol. 2003 Dec;11(12):543-6
pubmed: 14659685
Virology. 2006 Jun 20;350(1):34-47
pubmed: 16616287
J Virol. 2007 Feb;81(3):1424-32
pubmed: 17121806
Immunity. 2015 Sep 15;43(3):591-604
pubmed: 26362266
Acta Crystallogr D Biol Crystallogr. 2004 Dec;60(Pt 12 Pt 1):2126-32
pubmed: 15572765
Immunity. 2017 Nov 21;47(5):990-1003.e9
pubmed: 29166592
Structure. 2019 Jan 2;27(1):196-206.e6
pubmed: 30471922
Cell Host Microbe. 2020 Apr 8;27(4):507-518
pubmed: 32272076
PLoS Pathog. 2009 May;5(5):e1000414
pubmed: 19424423
Cell Host Microbe. 2018 Jun 13;23(6):759-765.e6
pubmed: 29861171
Nat Commun. 2016 Dec 20;7:13642
pubmed: 27995928
AIDS. 2014 Jan 14;28(2):163-9
pubmed: 24361678
Acta Crystallogr D Biol Crystallogr. 2010 Feb;66(Pt 2):125-32
pubmed: 20124692
Nature. 2003 Mar 20;422(6929):307-12
pubmed: 12646921
Immunity. 2019 Mar 19;50(3):677-691.e13
pubmed: 30876875
Proc Natl Acad Sci U S A. 2016 Jun 14;113(24):E3413-22
pubmed: 27247400
Immunity. 2018 May 15;48(5):855-871
pubmed: 29768174
Viruses. 2020 Jan 31;12(2):
pubmed: 32023860
J Virol. 2018 Mar 28;92(8):
pubmed: 29367243
J Virol. 2014 Mar;88(5):2489-507
pubmed: 24352443
Curr HIV Res. 2018;16(1):21-28
pubmed: 29173180
Proc Natl Acad Sci U S A. 2008 May 27;105(21):7552-7
pubmed: 18490657
Science. 2019 Dec 6;366(6470):
pubmed: 31672916
Cell Rep. 2017 Dec 26;21(13):3681-3690
pubmed: 29281818
J Virol. 2003 Apr;77(8):5037-8
pubmed: 12663814
Immunity. 2013 Aug 22;39(2):245-58
pubmed: 23911655
Cell Rep. 2019 May 21;27(8):2426-2441.e6
pubmed: 31116986
J Struct Biol. 2005 Jul;151(1):41-60
pubmed: 15890530
Nat Methods. 2017 Apr;14(4):331-332
pubmed: 28250466
Immunity. 2014 Dec 18;41(6):909-18
pubmed: 25526306
Nat Biotechnol. 2012 May 07;30(5):423-33
pubmed: 22565972
Sci Transl Med. 2017 Mar 15;9(381):
pubmed: 28298421
Genome Res. 1998 Mar;8(3):175-85
pubmed: 9521921
J Appl Crystallogr. 2007 Aug 1;40(Pt 4):658-674
pubmed: 19461840
J Virol. 2016 May 12;90(11):5231-5245
pubmed: 26984721
Nature. 2014 May 1;509(7498):55-62
pubmed: 24590074
Cell Rep. 2017 Apr 25;19(4):719-732
pubmed: 28445724
AIDS. 2018 Mar 13;32(5):555-563
pubmed: 29239895
J Virol Methods. 2009 Jun;158(1-2):171-9
pubmed: 19428587
Cell Rep. 2018 Feb 13;22(7):1798-1809
pubmed: 29444432
J Virol. 2012 Jul;86(14):7496-507
pubmed: 22553329
J Exp Med. 2009 Jun 8;206(6):1273-89
pubmed: 19487424
Nat Struct Mol Biol. 2016 Jan;23(1):81-90
pubmed: 26689967
Cell. 2019 Jul 25;178(3):567-584.e19
pubmed: 31348886
PLoS Pathog. 2012;8(5):e1002721
pubmed: 22693447
Nat Med. 2015 Nov;21(11):1332-6
pubmed: 26457756
Sci Transl Med. 2016 Apr 27;8(336):336ra62
pubmed: 27122615
Cell Rep. 2020 Apr 7;31(1):107488
pubmed: 32268107
Science. 2013 May 10;340(6133):751-6
pubmed: 23661761
Nat Commun. 2019 Jul 1;10(1):2898
pubmed: 31263112
Nat Immunol. 2018 Nov;19(11):1179-1188
pubmed: 30333615
Nature. 2013 Apr 25;496(7446):469-76
pubmed: 23552890
Nat Med. 1997 Feb;3(2):205-11
pubmed: 9018240
J Synchrotron Radiat. 2004 Jan 1;11(Pt 1):53-5
pubmed: 14646133
Science. 2010 Aug 13;329(5993):856-61
pubmed: 20616233
Curr Protoc Immunol. 2005 Jan;Chapter 12:Unit 12.11
pubmed: 18432938
J Struct Biol. 2012 Dec;180(3):519-30
pubmed: 23000701

Auteurs

Ryan S Roark (RS)

Departments of Medicine and Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.

Hui Li (H)

Departments of Medicine and Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.

Wilton B Williams (WB)

Duke Human Vaccine Institute, Duke University School of Medicine, Durham, NC 27710, USA.
Department of Medicine, Duke University School of Medicine, Durham, NC 27710, USA.

Hema Chug (H)

Laboratory of Molecular Medicine, Boston Children's Hospital and Harvard Medical School, Boston, MA 02115, USA.

Rosemarie D Mason (RD)

Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.

Jason Gorman (J)

Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.

Shuyi Wang (S)

Departments of Medicine and Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.

Fang-Hua Lee (FH)

Departments of Medicine and Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.

Juliette Rando (J)

Departments of Medicine and Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.

Mattia Bonsignori (M)

Duke Human Vaccine Institute, Duke University School of Medicine, Durham, NC 27710, USA.
Department of Medicine, Duke University School of Medicine, Durham, NC 27710, USA.

Kwan-Ki Hwang (KK)

Duke Human Vaccine Institute, Duke University School of Medicine, Durham, NC 27710, USA.

Kevin O Saunders (KO)

Duke Human Vaccine Institute, Duke University School of Medicine, Durham, NC 27710, USA.
Departments of Immunology and Surgery, Duke University School of Medicine, Durham, NC 27710, USA.

Kevin Wiehe (K)

Duke Human Vaccine Institute, Duke University School of Medicine, Durham, NC 27710, USA.
Department of Medicine, Duke University School of Medicine, Durham, NC 27710, USA.

M Anthony Moody (MA)

Duke Human Vaccine Institute, Duke University School of Medicine, Durham, NC 27710, USA.
Departments of Pediatrics and Immunology, Duke University School of Medicine, Durham, NC 27710, USA.

Peter T Hraber (PT)

Theoretical Biology and Biophysics, Los Alamos National Laboratory, Los Alamos, NM 87545, USA.

Kshitij Wagh (K)

Theoretical Biology and Biophysics, Los Alamos National Laboratory, Los Alamos, NM 87545, USA.

Elena E Giorgi (EE)

Theoretical Biology and Biophysics, Los Alamos National Laboratory, Los Alamos, NM 87545, USA.

Ronnie M Russell (RM)

Departments of Medicine and Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.

Frederic Bibollet-Ruche (F)

Departments of Medicine and Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.

Weimin Liu (W)

Departments of Medicine and Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.

Jesse Connell (J)

Departments of Medicine and Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.

Andrew G Smith (AG)

Departments of Medicine and Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.

Julia DeVoto (J)

Departments of Medicine and Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.

Alexander I Murphy (AI)

Departments of Medicine and Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.

Jessica Smith (J)

Departments of Medicine and Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.

Wenge Ding (W)

Departments of Medicine and Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.

Chengyan Zhao (C)

Departments of Medicine and Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.

Neha Chohan (N)

Departments of Medicine and Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.

Maho Okumura (M)

Departments of Medicine and Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.

Christina Rosario (C)

Departments of Medicine and Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.

Yu Ding (Y)

Departments of Medicine and Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.

Emily Lindemuth (E)

Departments of Medicine and Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.

Anya M Bauer (AM)

Departments of Medicine and Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.

Katharine J Bar (KJ)

Departments of Medicine and Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.

David Ambrozak (D)

Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.

Cara W Chao (CW)

Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.

Gwo-Yu Chuang (GY)

Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.

Hui Geng (H)

Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.

Bob C Lin (BC)

Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.

Mark K Louder (MK)

Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.

Richard Nguyen (R)

Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.

Baoshan Zhang (B)

Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.

Mark G Lewis (MG)

Bioqual, Inc., Rockville, MD 20850, USA.

Donald D Raymond (DD)

Laboratory of Molecular Medicine, Boston Children's Hospital and Harvard Medical School, Boston, MA 02115, USA.

Nicole A Doria-Rose (NA)

Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.

Chaim A Schramm (CA)

Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.

Daniel C Douek (DC)

Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.

Mario Roederer (M)

Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.

Thomas B Kepler (TB)

Department of Microbiology, Boston University School of Medicine, Boston, MA 02118, USA.
Department of Mathematics and Statistics, Boston University, Boston, MA 02215, USA.

Garnett Kelsoe (G)

Duke Human Vaccine Institute, Duke University School of Medicine, Durham, NC 27710, USA.
Departments of Immunology and Surgery, Duke University School of Medicine, Durham, NC 27710, USA.

John R Mascola (JR)

Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.

Peter D Kwong (PD)

Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.

Bette T Korber (BT)

Theoretical Biology and Biophysics, Los Alamos National Laboratory, Los Alamos, NM 87545, USA.

Stephen C Harrison (SC)

Laboratory of Molecular Medicine, Boston Children's Hospital and Harvard Medical School, Boston, MA 02115, USA.
Howard Hughes Medical Institute, Harvard Medical School, Boston, MA 02115, USA.

Barton F Haynes (BF)

Duke Human Vaccine Institute, Duke University School of Medicine, Durham, NC 27710, USA.
Department of Medicine, Duke University School of Medicine, Durham, NC 27710, USA.

Beatrice H Hahn (BH)

Departments of Medicine and Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.

George M Shaw (GM)

Departments of Medicine and Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA. shawg@pennmedicine.upenn.edu.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH