Affinity for the Interface Underpins Potency of Antibodies Operating In Membrane Environments.

HIV-1 antibody antibody engineering antibody-membrane interaction aromatic grafting membrane biophysics protein-membrane interaction site-selective chemical modification

Journal

Cell reports
ISSN: 2211-1247
Titre abrégé: Cell Rep
Pays: United States
ID NLM: 101573691

Informations de publication

Date de publication:
18 08 2020
Historique:
received: 04 05 2020
revised: 02 07 2020
accepted: 23 07 2020
entrez: 20 8 2020
pubmed: 20 8 2020
medline: 29 5 2021
Statut: ppublish

Résumé

The contribution of membrane interfacial interactions to recognition of membrane-embedded antigens by antibodies is currently unclear. This report demonstrates the optimization of this type of antibodies via chemical modification of regions near the membrane but not directly involved in the recognition of the epitope. Using the HIV-1 antibody 10E8 as a model, linear and polycyclic synthetic aromatic compounds are introduced at selected sites. Molecular dynamics simulations predict the favorable interactions of these synthetic compounds with the viral lipid membrane, where the epitope of the HIV-1 glycoprotein Env is located. Chemical modification of 10E8 with aromatic acetamides facilitates the productive and specific recognition of the native antigen, partially buried in the crowded environment of the viral membrane, resulting in a dramatic increase of its capacity to block viral infection. These observations support the harnessing of interfacial affinity through site-selective chemical modification to optimize the function of antibodies that target membrane-proximal epitopes.

Identifiants

pubmed: 32814041
pii: S2211-1247(20)31022-6
doi: 10.1016/j.celrep.2020.108037
pmc: PMC7861656
mid: NIHMS1663757
pii:
doi:

Substances chimiques

Antibodies, Neutralizing 0
Membrane Lipids 0

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

108037

Subventions

Organisme : Wellcome Trust
ID : 107457/Z/15/Z
Pays : United Kingdom
Organisme : NIAID NIH HHS
ID : R01 AI143563
Pays : United States
Organisme : Medical Research Council
ID : MC_UU_12010/UNIT PROGRAMS G0902418
Pays : United Kingdom
Organisme : Medical Research Council
ID : MC_UU_12025
Pays : United Kingdom
Organisme : Medical Research Council
ID : MC_UU_00008/9
Pays : United Kingdom
Organisme : Medical Research Council
ID : MC_UU_12010/9
Pays : United Kingdom
Organisme : Wellcome Trust
Pays : United Kingdom

Informations de copyright

Copyright © 2020 The Author(s). Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of Interests A patent application covering several aspects of this work has been filled by Kyushu University/UPV-EHU/CSIC/FBB, listing E.R., R.S.-E., A.O., J.L.N., and J.M.M.C. as inventors.

Références

Nat Commun. 2019 Nov 26;10(1):5389
pubmed: 31772165
Nat Protoc. 2010 Jun;5(6):1033-41
pubmed: 20539279
J Virol. 1994 Nov;68(11):7433-47
pubmed: 7933127
J Virol. 2003 Jun;77(12):6965-78
pubmed: 12768015
J Am Chem Soc. 2019 May 22;141(20):8005-8013
pubmed: 30974939
Cell Rep. 2020 Apr 28;31(4):107583
pubmed: 32348769
Nat Chem. 2016 Feb;8(2):103-13
pubmed: 26791892
Virology. 2008 Aug 1;377(2):364-78
pubmed: 18539308
PLoS Pathog. 2017 Feb 22;13(2):e1006212
pubmed: 28225819
Nat Struct Biol. 1996 Oct;3(10):842-8
pubmed: 8836100
FEBS Lett. 2011 Nov 16;585(22):3533-7
pubmed: 22020218
Cell. 2020 Jun 25;181(7):1695
pubmed: 32589960
Cancer Cell. 2018 Nov 12;34(5):792-806.e5
pubmed: 30449325
Biophys J. 2005 Mar;88(3):1818-27
pubmed: 15596514
Mol Cell. 2000 Nov;6(5):1233-42
pubmed: 11106760
Cell Host Microbe. 2019 Nov 13;26(5):623-637.e8
pubmed: 31653484
J Virol. 2009 Jul;83(14):7337-48
pubmed: 19439467
Antimicrob Agents Chemother. 2002 Jun;46(6):1896-905
pubmed: 12019106
J Biol Chem. 2016 Aug 12;291(33):16948-62
pubmed: 27311714
AIDS Res Hum Retroviruses. 2001 Dec 10;17(18):1757-65
pubmed: 11788027
Nature. 2012 Nov 15;491(7424):406-12
pubmed: 23151583
Sci Immunol. 2017 Jan 27;2(7):
pubmed: 28783671
MAbs. 2019 Feb/Mar;11(2):265-296
pubmed: 30526315
Biochim Biophys Acta. 2013 Mar;1828(3):1094-101
pubmed: 23274277
J Virol. 2015 Dec;89(23):11975-89
pubmed: 26378169
PLoS Pathog. 2013 Feb;9(2):e1003184
pubmed: 23468626
Nat Rev Immunol. 2018 May;18(5):297-308
pubmed: 29379211
Nat Rev Drug Discov. 2017 Sep;16(9):787-810
pubmed: 28706220
Sci Rep. 2016 Dec 01;6:38177
pubmed: 27905530
J Comput Chem. 2005 Dec;26(16):1781-802
pubmed: 16222654
J Virol. 2010 Apr;84(7):3382-95
pubmed: 20089658
J Phys Chem B. 1998 Apr 30;102(18):3586-616
pubmed: 24889800
J Comput Chem. 2008 Aug;29(11):1859-65
pubmed: 18351591
Annu Rev Biophys Biomol Struct. 1999;28:319-65
pubmed: 10410805
Science. 2016 Mar 4;351(6277):1043-8
pubmed: 26941313
J Biol Chem. 2017 Mar 31;292(13):5571-5583
pubmed: 28213514
Nature. 2003 Mar 20;422(6929):307-12
pubmed: 12646921
Biochemistry. 1998 Oct 20;37(42):14713-8
pubmed: 9778346
Immunity. 2019 Mar 19;50(3):677-691.e13
pubmed: 30876875
Anal Sci. 2019 Jan 10;35(1):5-27
pubmed: 30318491
Nat Commun. 2019 Jan 8;10(1):78
pubmed: 30622256
MAbs. 2013 Jan-Feb;5(1):22-33
pubmed: 23211638
J Phys Chem B. 2010 Jun 17;114(23):7830-43
pubmed: 20496934
Cell Metab. 2019 Mar 5;29(3):611-626.e5
pubmed: 30581119
J Am Chem Soc. 2016 Jun 29;138(25):7946-50
pubmed: 27254476
Int Rev Cell Mol Biol. 2017;331:289-383
pubmed: 28325214
Immunity. 2016 Jan 19;44(1):21-31
pubmed: 26777395
Science. 2014 Nov 7;346(6210):759-63
pubmed: 25298114
Cell Rep. 2018 Feb 13;22(7):1798-1809
pubmed: 29444432
Proc Natl Acad Sci U S A. 2008 Apr 8;105(14):5525-30
pubmed: 18378908
J Virol. 2001 Dec;75(24):12198-208
pubmed: 11711611
J Biol Chem. 2001 Aug 31;276(35):32395-8
pubmed: 11432876
Sci Rep. 2016 Sep 28;6:34190
pubmed: 27678107
J Virol. 2018 Mar 28;92(8):
pubmed: 29386285
Nat Biotechnol. 2005 Oct;23(10):1289-93
pubmed: 16170312
Biochemistry. 1998 Oct 13;37(41):14563-74
pubmed: 9772185
Nat Microbiol. 2018 Jun;3(6):670-677
pubmed: 29736037

Auteurs

Edurne Rujas (E)

Instituto Biofisika (CSIC, UPV/EHU) and Department of Biochemistry and Molecular Biology, University of the Basque Country (UPV/EHU), PO Box 644, 48080 Bilbao, Spain; Program in Molecular Medicine, The Hospital for Sick Children Research Institute, Toronto, ON M5G 0A4, Canada.

Sara Insausti (S)

Instituto Biofisika (CSIC, UPV/EHU) and Department of Biochemistry and Molecular Biology, University of the Basque Country (UPV/EHU), PO Box 644, 48080 Bilbao, Spain.

Daniel P Leaman (DP)

Department of Immunology and Microbiology, The Scripps Research Institute, La Jolla, CA 92037, USA.

Pablo Carravilla (P)

Instituto Biofisika (CSIC, UPV/EHU) and Department of Biochemistry and Molecular Biology, University of the Basque Country (UPV/EHU), PO Box 644, 48080 Bilbao, Spain; Institute of Applied Optics and Biophysics Friedrich-Schiller-University Jena, Max-Wien Platz 4, 07743 Jena, Germany; Leibniz Institute of Photonic Technology e.V., Albert-Einstein-Straße 9, 07745 Jena, Germany.

Saul González-Resines (S)

Department of Chemistry, University of Bath, Claverton Down, Bath BA2 7AX, UK.

Valérie Monceaux (V)

Institut Pasteur, Unité HIV Inflammation et Persistance, 28 rue du Docteur Roux, 75724 Paris Cedex 15, France.

Rubén Sánchez-Eugenia (R)

Instituto Biofisika (CSIC, UPV/EHU) and Department of Biochemistry and Molecular Biology, University of the Basque Country (UPV/EHU), PO Box 644, 48080 Bilbao, Spain.

Miguel García-Porras (M)

Instituto Biofisika (CSIC, UPV/EHU) and Department of Biochemistry and Molecular Biology, University of the Basque Country (UPV/EHU), PO Box 644, 48080 Bilbao, Spain.

Ibon Iloro (I)

Proteomics Platform, CIC bioGUNE, Parque Tecnológico de Vizcaya, 48160 Derio, Spain.

Lei Zhang (L)

Department of Immunology and Microbiology, The Scripps Research Institute, La Jolla, CA 92037, USA.

Félix Elortza (F)

Proteomics Platform, CIC bioGUNE, Parque Tecnológico de Vizcaya, 48160 Derio, Spain.

Jean-Philippe Julien (JP)

Program in Molecular Medicine, The Hospital for Sick Children Research Institute, Toronto, ON M5G 0A4, Canada; Department of Biochemistry, University of Toronto, Toronto, ON M5S 1A8, Canada; Department of Immunology, University of Toronto, Toronto, ON M5S 1A8, Canada.

Asier Saéz-Cirión (A)

Institut Pasteur, Unité HIV Inflammation et Persistance, 28 rue du Docteur Roux, 75724 Paris Cedex 15, France.

Michael B Zwick (MB)

Department of Immunology and Microbiology, The Scripps Research Institute, La Jolla, CA 92037, USA.

Christian Eggeling (C)

Institute of Applied Optics and Biophysics Friedrich-Schiller-University Jena, Max-Wien Platz 4, 07743 Jena, Germany; Leibniz Institute of Photonic Technology e.V., Albert-Einstein-Straße 9, 07745 Jena, Germany.

Akio Ojida (A)

Department of Chemical Biology, School of Pharmaceutical Sciences, Kyushu University, Fukuoka 819-0395, Japan.

Carmen Domene (C)

Department of Chemistry, University of Bath, Claverton Down, Bath BA2 7AX, UK; Department of Chemistry, University of Oxford, Oxford OX1 3TF, UK.

Jose M M Caaveiro (JMM)

Laboratory of Global Health Care, School of Pharmaceutical Sciences, Kyushu University, Fukuoka 819-0395, Japan. Electronic address: jose@phar.kyushu-u.ac.jp.

José L Nieva (JL)

Instituto Biofisika (CSIC, UPV/EHU) and Department of Biochemistry and Molecular Biology, University of the Basque Country (UPV/EHU), PO Box 644, 48080 Bilbao, Spain. Electronic address: joseluis.nieva@ehu.es.

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