HIV Envelope Glycoform Heterogeneity and Localized Diversity Govern the Initiation and Maturation of a V2 Apex Broadly Neutralizing Antibody Lineage

Landais, Elise; Murrell, Ben; Briney, Bryan; Murrell, Sasha; Rantalainen, Kimmo; Berndsen, Zachary T.; Ramos, Alejandra; Wickramasinghe, Lalinda; Smith, Melissa Laird; Eren, Kemal; de Val, Natalia; Wu, Mengyu; Cappelletti, Audrey; Umotoy, Jeffrey; Lie, Yolanda; Wrin, Terri; Algate, Paul; Chan-Hui, Po-Ying; Karita, Etienne; Ward, Andrew B.; Wilson, Ian A.; Burton, Dennis R.; Smith, Davey; Pond, Sergei L.  Kosakovsky; Poignard, Pascal

doi:10.1016/j.immuni.2017.11.002

Title: HIV Envelope Glycoform Heterogeneity and Localized Diversity Govern the Initiation and Maturation of a V2 Apex Broadly Neutralizing Antibody Lineage

Journal Article · 21 November 2017 · Immunity

DOI: https://doi.org/10.1016/j.immuni.2017.11.002 · OSTI ID:1483019

Landais, Elise ^[1]; Murrell, Ben ^[2]; Briney, Bryan ^[3]; Murrell, Sasha ^[3]; Rantalainen, Kimmo ^[3]; Berndsen, Zachary T. ^[3]; Ramos, Alejandra ^[1]; Wickramasinghe, Lalinda ^[1]; Smith, Melissa Laird ^[4]; Eren, Kemal ^[2]; de Val, Natalia ^[5]; Wu, Mengyu ^[3]; Cappelletti, Audrey ^[6]; Umotoy, Jeffrey ^[1]; Lie, Yolanda ^[7]; Wrin, Terri ^[7]; Algate, Paul ^[8]; Chan-Hui, Po-Ying ^[8]; Karita, Etienne ^[9]; Ward, Andrew B. ^[3] more »

The Scripps Research Inst., La Jolla, CA (United States); International AIDS Vaccine Initiative, New York, NY (United States)
Univ. of California, San Diego, CA (United States)
The Scripps Research Inst., La Jolla, CA (United States)
Icahn School of Medicine and Icahn Inst. for Genomics and Multiscale Biology at Mount Sinai, New York, NY (United States)
The Scripps Research Inst., La Jolla, CA (United States); Leidos Biomedical Inc., Bethesda, MD (United States)
The Scripps Research Inst., La Jolla, CA (United States); Univ. Grenoble Alpes (France)
Monogram Biosciences Inc., San Francisco, CA (United States)
Theraclone Sciences, Inc., Seattle, WA (United States); OncoResponse Inc, Seattle WA (United States)
Rwanda-Zambia HIV Research Group, Kigali (Rwanda)
The Scripps Research Inst., La Jolla, CA (United States); Massachusetts Inst. of Technology and Harvard, Cambridge, MA (United States)
Univ. of California, San Diego, CA (United States); Veterans Affairs Healthcare System, San Diego, CA (United States)
Univ. of California, San Diego, CA (United States); Temple Univ., Philadelphia, PA (United States)
The Scripps Research Inst., La Jolla, CA (United States); International AIDS Vaccine Initiative, New York, NY (United States); Univ. Grenoble Alpes (France)

Understanding how broadly neutralizing antibodies (bnAbs) to HIV envelope (Env) develop during natural infection can help guide the rational design of an HIV vaccine. Here, we described a bnAb lineage targeting the Env V2 apex and the Ab-Env co-evolution that led to development of neutralization breadth. The lineage Abs bore an anionic heavy chain complementarity-determining region 3 (CDRH3) of 25 amino acids, among the shortest known for this class of Abs, and achieved breadth with only 10% nucleotide somatic hypermutation and no insertions or deletions. The data suggested a role for Env glycoform heterogeneity in the activation of the lineage germline B cell. Finally, we showed that localized diversity at key V2 epitope residues drove bnAb maturation toward breadth, mirroring the Env evolution pattern described for another donor who developed V2-apex targeting bnAbs. Furthermore, these findings suggest potential strategies for vaccine approaches based on germline-targeting and serial immunogen design.

View Journal Article

Cite

Export

Save

Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States)

Sponsoring Organization:: USDOE Office of Science (SC); Center for HIV/AIDS Vaccine Immunology and Immunogen Discovery; National Inst. of Allergy and Infectious Diseases (NIH/NIAID); International AIDS Vaccine Initiative Neutralizing Antibody Consortium through the Collaboration for AIDS Vaccine Discovery

Grant/Contract Number:: AC02-06CH11357; U19AI090970; UM1AI100663; R00AI120851; T15LM007092; U01GM110749; OPP1084519; OPP1115782

OSTI ID:: 1483019

Alternate ID(s):: OSTI ID: 1498319

Journal Information:: Immunity, Vol. 47, Issue 5; ISSN 1074-7613

Publisher:: Cell PressCopyright Statement

Country of Publication:: United States

Language:: ENGLISH

Citation Metrics:

Cited by: 68 works

Citation information provided by
Web of Science

References (89)

PHENIX: a comprehensive Python-based system for macromolecular structure solution Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221 https://doi.org/10.1107/S0907444909052925	journal	January 2010
Identification of Common Features in Prototype Broadly Neutralizing Antibodies to HIV Envelope V2 Apex to Facilitate Vaccine Design Andrabi, Raiees; Voss, James E.; Liang, Chi-Hui Immunity, Vol. 43, Issue 5 https://doi.org/10.1016/j.immuni.2015.10.014	journal	November 2015
Composition and Antigenic Effects of Individual Glycan Sites of a Trimeric HIV-1 Envelope Glycoprotein Behrens, Anna-Janina; Vasiljevic, Snezana; Pritchard, Laura K. Cell Reports, Vol. 14, Issue 11 https://doi.org/10.1016/j.celrep.2016.02.058	journal	March 2016
Viral variants that initiate and drive maturation of V1V2-directed HIV-1 broadly neutralizing antibodies Bhiman, Jinal N.; Anthony, Colin; Doria-Rose, Nicole A. Nature Medicine, Vol. 21, Issue 11 https://doi.org/10.1038/nm.3963	journal	October 2015
Two Distinct Broadly Neutralizing Antibody Specificities of Different Clonal Lineages in a Single HIV-1-Infected Donor: Implications for Vaccine Design Bonsignori, Mattia; Montefiori, David C.; Wu, Xueling Journal of Virology, Vol. 86, Issue 8 https://doi.org/10.1128/JVI.07163-11	journal	February 2012
Maturation Pathway from Germline to Broad HIV-1 Neutralizer of a CD4-Mimic Antibody Bonsignori, Mattia; Zhou, Tongqing; Sheng, Zizhang Cell, Vol. 165, Issue 2 https://doi.org/10.1016/j.cell.2016.02.022	journal	April 2016
Staged induction of HIV-1 glycan–dependent broadly neutralizing antibodies Bonsignori, Mattia; Kreider, Edward F.; Fera, Daniela Science Translational Medicine, Vol. 9, Issue 381 https://doi.org/10.1126/scitranslmed.aai7514	journal	March 2017
Human Peripheral Blood Antibodies with Long HCDR3s Are Established Primarily at Original Recombination Using a Limited Subset of Germline Genes Briney, Bryan S.; Willis, Jordan R.; Crowe, James E. PLoS ONE, Vol. 7, Issue 5 https://doi.org/10.1371/journal.pone.0036750	journal	May 2012
Clonify: unseeded antibody lineage assignment from next-generation sequencing data Briney, Bryan; Le, Khoa; Zhu, Jiang Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep23901	journal	April 2016
Tailored Immunogens Direct Affinity Maturation toward HIV Neutralizing Antibodies Briney, Bryan; Sok, Devin; Jardine, Joseph G. Cell, Vol. 166, Issue 6 https://doi.org/10.1016/j.cell.2016.08.005	journal	September 2016
Broadly Neutralizing Antibodies to HIV and Their Role in Vaccine Design Burton, Dennis R.; Hangartner, Lars Annual Review of Immunology, Vol. 34, Issue 1 https://doi.org/10.1146/annurev-immunol-041015-055515	journal	May 2016
A Blueprint for HIV Vaccine Discovery Burton, Dennis R.; Ahmed, Rafi; Barouch, Dan H. Cell Host & Microbe, Vol. 12, Issue 4 https://doi.org/10.1016/j.chom.2012.09.008	journal	October 2012
Virus-like Particles Identify an HIV V1V2 Apex-Binding Neutralizing Antibody that Lacks a Protruding Loop Cale, Evan M.; Gorman, Jason; Radakovich, Nathan A. Immunity, Vol. 46, Issue 5 https://doi.org/10.1016/j.immuni.2017.04.011	journal	May 2017
Global site-specific N-glycosylation analysis of HIV envelope glycoprotein Cao, Liwei; Diedrich, Jolene K.; Kulp, Daniel W. Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/ncomms14954	journal	March 2017
Variable Loop Glycan Dependency of the Broad and Potent HIV-1-Neutralizing Antibodies PG9 and PG16 Doores, Katie J.; Burton, Dennis R. Journal of Virology, Vol. 84, Issue 20 https://doi.org/10.1128/JVI.00552-10	journal	August 2010
Breadth of Human Immunodeficiency Virus-Specific Neutralizing Activity in Sera: Clustering Analysis and Association with Clinical Variables Doria-Rose, N. A.; Klein, R. M.; Daniels, M. G. Journal of Virology, Vol. 84, Issue 3 https://doi.org/10.1128/JVI.01482-09	journal	November 2009
Developmental pathway for potent V1V2-directed HIV-neutralizing antibodies Doria-Rose, Nicole A.; Schramm, Chaim A.; Gorman, Jason Nature, Vol. 509, Issue 7498 https://doi.org/10.1038/nature13036	journal	March 2014
New Member of the V1V2-Directed CAP256-VRC26 Lineage That Shows Increased Breadth and Exceptional Potency Doria-Rose, Nicole A.; Bhiman, Jinal N.; Roark, Ryan S. Journal of Virology, Vol. 90, Issue 1 https://doi.org/10.1128/JVI.01791-15	journal	October 2015
Mapping Polyclonal HIV-1 Antibody Responses via Next-Generation Neutralization Fingerprinting Doria-Rose, Nicole A.; Altae-Tran, Han R.; Roark, Ryan S. PLOS Pathogens, Vol. 13, Issue 1 https://doi.org/10.1371/journal.ppat.1006148	journal	January 2017
Immunization for HIV-1 Broadly Neutralizing Antibodies in Human Ig Knockin Mice Dosenovic, Pia; von Boehmer, Lotta; Escolano, Amelia Cell, Vol. 161, Issue 7 https://doi.org/10.1016/j.cell.2015.06.003	journal	June 2015
Search and clustering orders of magnitude faster than BLAST Edgar, Robert C. Bioinformatics, Vol. 26, Issue 19, p. 2460-2461 https://doi.org/10.1093/bioinformatics/btq461	journal	August 2010
Coot model-building tools for molecular graphics Emsley, Paul; Cowtan, Kevin Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12, p. 2126-2132 https://doi.org/10.1107/S0907444904019158	journal	November 2004
Sequential Immunization Elicits Broadly Neutralizing Anti-HIV-1 Antibodies in Ig Knockin Mice Escolano, Amelia; Steichen, Jon M.; Dosenovic, Pia Cell, Vol. 166, Issue 6 https://doi.org/10.1016/j.cell.2016.07.030	journal	September 2016
Ending AIDS — Is an HIV Vaccine Necessary? Fauci, Anthony S.; Marston, Hilary D. New England Journal of Medicine, Vol. 370, Issue 6 https://doi.org/10.1056/NEJMp1313771	journal	February 2014
Cooperation of B Cell Lineages in Induction of HIV-1-Broadly Neutralizing Antibodies Gao, Feng; Bonsignori, Mattia; Liao, Hua-Xin Cell, Vol. 158, Issue 3 https://doi.org/10.1016/j.cell.2014.06.022	journal	July 2014
Structures of HIV-1 Env V1V2 with broadly neutralizing antibodies reveal commonalities that enable vaccine design Gorman, Jason; Soto, Cinque; Yang, Max M. Nature Structural & Molecular Biology, Vol. 23, Issue 1 https://doi.org/10.1038/nsmb.3144	journal	December 2015
Neutralizing Antibody Responses in Acute Human Immunodeficiency Virus Type 1 Subtype C Infection Gray, E. S.; Moore, P. L.; Choge, I. A. Journal of Virology, Vol. 81, Issue 12 https://doi.org/10.1128/JVI.00239-07	journal	April 2007
Structure-Guided Redesign Increases the Propensity of HIV Env To Generate Highly Stable Soluble Trimers Guenaga, Javier; Dubrovskaya, Viktoriya; de Val, Natalia Journal of Virology, Vol. 90, Issue 6 https://doi.org/10.1128/JVI.02652-15	journal	December 2015
Prevalence of broadly neutralizing antibody responses during chronic HIV-1 infection Hraber, Peter; Seaman, Michael S.; Bailer, Robert T. AIDS, Vol. 28, Issue 2 https://doi.org/10.1097/QAD.0000000000000106	journal	January 2014
ETE: a python Environment for Tree Exploration Huerta-Cepas, Jaime; Dopazo, Joaquín; Gabaldón, Toni BMC Bioinformatics, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2105-11-24	journal	January 2010
HIV-1 broadly neutralizing antibody precursor B cells revealed by germline-targeting immunogen Jardine, J. G.; Kulp, D. W.; Havenar-Daughton, C. Science, Vol. 351, Issue 6280 https://doi.org/10.1126/science.aad9195	journal	March 2016
Crystal Structure of a Soluble Cleaved HIV-1 Envelope Trimer Julien, J. -P.; Cupo, A.; Sok, D. Science, Vol. 342, Issue 6165 https://doi.org/10.1126/science.1245625	journal	October 2013
Linking Crystallographic Model and Data Quality Karplus, P. A.; Diederichs, K. Science, Vol. 336, Issue 6084 https://doi.org/10.1126/science.1218231	journal	May 2012
MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability Katoh, K.; Standley, D. M. Molecular Biology and Evolution, Vol. 30, Issue 4 https://doi.org/10.1093/molbev/mst010	journal	January 2013
MAFFT version 5: improvement in accuracy of multiple sequence alignment Katoh, K. Nucleic Acids Research, Vol. 33, Issue 2 https://doi.org/10.1093/nar/gki198	journal	January 2005
Accelerated cryo-EM structure determination with parallelisation using GPUs in RELION-2 Kimanius, Dari; Forsberg, Björn O.; Scheres, Sjors HW eLife, Vol. 5 https://doi.org/10.7554/eLife.18722	journal	November 2016
Somatic Mutations of the Immunoglobulin Framework Are Generally Required for Broad and Potent HIV-1 Neutralization Klein, Florian; Diskin, Ron; Scheid, Johannes F. Cell, Vol. 153, Issue 1 https://doi.org/10.1016/j.cell.2013.03.018	journal	March 2013
Fusion peptide of HIV-1 as a site of vulnerability to neutralizing antibody Kong, R.; Xu, K.; Zhou, T. Science, Vol. 352, Issue 6287 https://doi.org/10.1126/science.aae0474	journal	May 2016
Rapid Sequencing of Complete env Genes from Primary HIV-1 Samples Laird Smith, Melissa; Murrell, Ben; Eren, Kemal Virus Evolution, Vol. 2, Issue 2 https://doi.org/10.1093/ve/vew018	journal	July 2016
Broadly Neutralizing Antibody Responses in a Large Longitudinal Sub-Saharan HIV Primary Infection Cohort Landais, Elise; Huang, Xiayu; Havenar-Daughton, Colin PLOS Pathogens, Vol. 12, Issue 1 https://doi.org/10.1371/journal.ppat.1005369	journal	January 2016
Model Building and Refinement of a Natively Glycosylated HIV-1 Env Protein by High-Resolution Cryoelectron Microscopy Lee, Jeong Hyun; de Val, Natalia; Lyumkis, Dmitry Structure, Vol. 23, Issue 10 https://doi.org/10.1016/j.str.2015.07.020	journal	October 2015
Co-evolution of a broadly neutralizing HIV-1 antibody and founder virus Liao, Hua-Xin; Lynch, Rebecca; Zhou, Tongqing Nature, Vol. 496, Issue 7446 https://doi.org/10.1038/nature12053	journal	April 2013
Early Antibody Lineage Diversification and Independent Limb Maturation Lead to Broad HIV-1 Neutralization Targeting the Env High-Mannose Patch MacLeod, Daniel T.; Choi, Nancy M.; Briney, Bryan Immunity, Vol. 44, Issue 5 https://doi.org/10.1016/j.immuni.2016.04.016	journal	May 2016
PANDAseq: paired-end assembler for illumina sequences Masella, Andre P.; Bartram, Andrea K.; Truszkowski, Jakub M. BMC Bioinformatics, Vol. 13, Issue 1 https://doi.org/10.1186/1471-2105-13-31	journal	January 2012
Phaser crystallographic software McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D. Journal of Applied Crystallography, Vol. 40, Issue 4 https://doi.org/10.1107/S0021889807021206	journal	July 2007
Structure of HIV-1 gp120 V1/V2 domain with broadly neutralizing antibody PG9 McLellan, Jason S.; Pancera, Marie; Carrico, Chris Nature, Vol. 480, Issue 7377 https://doi.org/10.1038/nature10696	journal	November 2011
[20] Processing of X-ray diffraction data collected in oscillation mode Otwinowski, Zbyszek; Minor, Wladek Macromolecular Crystallography Part A, 307-326 https://doi.org/10.1016/S0076-6879(97)76066-X	book	January 1997
Systematic analysis of the in situ crosstalk of tyrosine modifications reveals no additional natural selection on multiply modified residues Pan, Zhicheng; Liu, Zexian; Cheng, Han Scientific Reports, Vol. 4, Issue 1 https://doi.org/10.1038/srep07331	journal	December 2014
Crystal Structure of PG16 and Chimeric Dissection with Somatically Related PG9: Structure-Function Analysis of Two Quaternary-Specific Antibodies That Effectively Neutralize HIV-1 Pancera, M.; McLellan, J. S.; Wu, X. Journal of Virology, Vol. 84, Issue 16 https://doi.org/10.1128/JVI.00966-10	journal	June 2010
Mapping the complete glycoproteome of virion-derived HIV-1 gp120 provides insights into broadly neutralizing antibody binding Panico, Maria; Bouché, Laura; Binet, Daniel Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep32956	journal	September 2016
Structure and function of broadly reactive antibody PG16 reveal an H3 subdomain that mediates potent neutralization of HIV-1 Pejchal, R.; Walker, L. M.; Stanfield, R. L. Proceedings of the National Academy of Sciences, Vol. 107, Issue 25 https://doi.org/10.1073/pnas.1004600107	journal	June 2010
A Potent and Broad Neutralizing Antibody Recognizes and Penetrates the HIV Glycan Shield Pejchal, R.; Doores, K. J.; Walker, L. M. Science, Vol. 334, Issue 6059 https://doi.org/10.1126/science.1213256	journal	October 2011
UCSF Chimera?A visualization system for exploratory research and analysis Pettersen, Eric F.; Goddard, Thomas D.; Huang, Conrad C. Journal of Computational Chemistry, Vol. 25, Issue 13 https://doi.org/10.1002/jcc.20084	journal	January 2004
Leginon: a system for fully automated acquisition of 1000 electron micrographs a day Potter, C. S.; Chu, H.; Frey, B. Ultramicroscopy, Vol. 77, Issue 3-4 https://doi.org/10.1016/S0304-3991(99)00043-1	journal	July 1999
FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments Price, Morgan N.; Dehal, Paramvir S.; Arkin, Adam P. PLoS ONE, Vol. 5, Issue 3 https://doi.org/10.1371/journal.pone.0009490	journal	March 2010
Determinants of HIV-1 broadly neutralizing antibody induction Rusert, Peter; Kouyos, Roger D.; Kadelka, Claus Nature Medicine, Vol. 22, Issue 11 https://doi.org/10.1038/nm.4187	journal	September 2016
A Next-Generation Cleaved, Soluble HIV-1 Env Trimer, BG505 SOSIP.664 gp140, Expresses Multiple Epitopes for Broadly Neutralizing but Not Non-Neutralizing Antibodies Sanders, Rogier W.; Derking, Ronald; Cupo, Albert PLoS Pathogens, Vol. 9, Issue 9, Article No. e1003618 https://doi.org/10.1371/journal.ppat.1003618	journal	September 2013
Development of an HIV-1 Reference Panel of Subtype B Envelope Clones Isolated From the Plasma of Recently Infected Individuals Schweighardt, Becky; Liu, Yang; Huang, Wei JAIDS Journal of Acquired Immune Deficiency Syndromes, Vol. 46, Issue 1 https://doi.org/10.1097/QAI.0b013e318074eb5a	journal	January 2007
Tiered Categorization of a Diverse Panel of HIV-1 Env Pseudoviruses for Assessment of Neutralizing Antibodies Seaman, M. S.; Janes, H.; Hawkins, N. Journal of Virology, Vol. 84, Issue 3 https://doi.org/10.1128/JVI.02108-09	journal	November 2009
Effects of Darwinian Selection and Mutability on Rate of Broadly Neutralizing Antibody Evolution during HIV-1 Infection Sheng, Zizhang; Schramm, Chaim A.; Connors, Mark PLOS Computational Biology, Vol. 12, Issue 5 https://doi.org/10.1371/journal.pcbi.1004940	journal	May 2016
Human Immunodeficiency Virus Type 1 Elite Neutralizers: Individuals with Broad and Potent Neutralizing Activity Identified by Using a High-Throughput Neutralization Assay together with an Analytical Selection Algorithm Simek, M. D.; Rida, W.; Priddy, F. H. Journal of Virology, Vol. 83, Issue 14 https://doi.org/10.1128/JVI.00110-09	journal	May 2009
The Effects of Somatic Hypermutation on Neutralization and Binding in the PGT121 Family of Broadly Neutralizing HIV Antibodies Sok, Devin; Laserson, Uri; Laserson, Jonathan PLoS Pathogens, Vol. 9, Issue 11 https://doi.org/10.1371/journal.ppat.1003754	journal	November 2013
Recombinant HIV envelope trimer selects for quaternary-dependent antibodies targeting the trimer apex Sok, Devin; van Gils, Marit J.; Pauthner, Matthias Proceedings of the National Academy of Sciences, Vol. 111, Issue 49 https://doi.org/10.1073/pnas.1415789111	journal	November 2014
HIV Vaccine Design to Target Germline Precursors of Glycan-Dependent Broadly Neutralizing Antibodies Steichen, Jon M.; Kulp, Daniel W.; Tokatlian, Talar Immunity, Vol. 45, Issue 3 https://doi.org/10.1016/j.immuni.2016.08.016	journal	September 2016
Induction of HIV Neutralizing Antibody Lineages in Mice with Diverse Precursor Repertoires Tian, Ming; Cheng, Cheng; Chen, Xuejun Cell, Vol. 166, Issue 6 https://doi.org/10.1016/j.cell.2016.07.029	journal	September 2016
Prevalence of cross-reactive HIV-1-neutralizing activity in HIV-1-infected patients with rapid or slow disease progression van Gils, Marit J.; Euler, Zelda; Schweighardt, Becky AIDS, Vol. 23, Issue 18 https://doi.org/10.1097/QAD.0b013e32833243e7	journal	January 2009
Broad and Potent Neutralizing Antibodies from an African Donor Reveal a New HIV-1 Vaccine Target Walker, L. M.; Phogat, S. K.; Chan-Hui, P. -Y. Science, Vol. 326, Issue 5950 https://doi.org/10.1126/science.1178746	journal	September 2009
Broad neutralization coverage of HIV by multiple highly potent antibodies Walker, Laura M.; Huber, Michael; Doores, Katie J. Nature, Vol. 477, Issue 7365 https://doi.org/10.1038/nature10373	journal	September 2011
Predominant Autoantibody Production by Early Human B Cell Precursors Wardemann, H. Science, Vol. 301, Issue 5638 https://doi.org/10.1126/science.1086907	journal	September 2003
Gctf: Real-time CTF determination and correction Zhang, Kai Journal of Structural Biology, Vol. 193, Issue 1 https://doi.org/10.1016/j.jsb.2015.11.003	journal	January 2016
MotionCor2: anisotropic correction of beam-induced motion for improved cryo-electron microscopy Zheng, Shawn Q.; Palovcak, Eugene; Armache, Jean-Paul Nature Methods, Vol. 14, Issue 4 https://doi.org/10.1038/nmeth.4193	journal	February 2017
UCSF Chimera?A visualization system for exploratory research and analysis Pettersen, Eric F.; Goddard, Thomas D.; Huang, Conrad C. Journal of Computational Chemistry, Vol. 25, Issue 13 https://doi.org/10.1002/jcc.20084	journal	January 2004
B Cell Liaison Confounds HIV-1 Evolution McHeyzer-Williams, Michael G. Cell, Vol. 158, Issue 3 https://doi.org/10.1016/j.cell.2014.07.018	journal	July 2014
Sequential Immunization Elicits Broadly Neutralizing Anti-HIV-1 Antibodies in Ig Knockin Mice Escolano, Amelia; Steichen, Jon M.; Dosenovic, Pia Cell, Vol. 166, Issue 6 https://doi.org/10.1016/j.cell.2016.07.030	journal	September 2016
Composition and Antigenic Effects of Individual Glycan Sites of a Trimeric HIV-1 Envelope Glycoprotein Behrens, Anna-Janina; Vasiljevic, Snezana; Pritchard, Laura K. Cell Reports, Vol. 14, Issue 11 https://doi.org/10.1016/j.celrep.2016.02.058	journal	March 2016
Identification of Common Features in Prototype Broadly Neutralizing Antibodies to HIV Envelope V2 Apex to Facilitate Vaccine Design Andrabi, Raiees; Voss, James E.; Liang, Chi-Hui Immunity, Vol. 43, Issue 5 https://doi.org/10.1016/j.immuni.2015.10.014	journal	November 2015
HIV Immunology Goes Out On a Limb Doria-Rose, Nicole A.; Mascola, John R. Immunity, Vol. 44, Issue 5 https://doi.org/10.1016/j.immuni.2016.05.004	journal	May 2016
Co-evolution of a broadly neutralizing HIV-1 antibody and founder virus Liao, Hua-Xin; Lynch, Rebecca; Zhou, Tongqing Nature, Vol. 496, Issue 7446 https://doi.org/10.1038/nature12053	journal	April 2013
Systematic analysis of the in situ crosstalk of tyrosine modifications reveals no additional natural selection on multiply modified residues Pan, Zhicheng; Liu, Zexian; Cheng, Han Scientific Reports, Vol. 4, Issue 1 https://doi.org/10.1038/srep07331	journal	December 2014
Recombinant HIV envelope trimer selects for quaternary-dependent antibodies targeting the trimer apex Sok, Devin; van Gils, Marit J.; Pauthner, Matthias Proceedings of the National Academy of Sciences, Vol. 111, Issue 49 https://doi.org/10.1073/pnas.1415789111	journal	November 2014
MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability Katoh, K.; Standley, D. M. Molecular Biology and Evolution, Vol. 30, Issue 4 https://doi.org/10.1093/molbev/mst010	journal	January 2013
Broad and Potent Neutralizing Antibodies from an African Donor Reveal a New HIV-1 Vaccine Target Walker, L. M.; Phogat, S. K.; Chan-Hui, P. -Y. Science, Vol. 326, Issue 5950 https://doi.org/10.1126/science.1178746	journal	September 2009
HIV-1 broadly neutralizing antibody precursor B cells revealed by germline-targeting immunogen Jardine, J. G.; Kulp, D. W.; Havenar-Daughton, C. Science, Vol. 351, Issue 6280 https://doi.org/10.1126/science.aad9195	journal	March 2016
Fusion peptide of HIV-1 as a site of vulnerability to neutralizing antibody Kong, R.; Xu, K.; Zhou, T. Science, Vol. 352, Issue 6287 https://doi.org/10.1126/science.aae0474	journal	May 2016
Staged induction of HIV-1 glycan–dependent broadly neutralizing antibodies Bonsignori, Mattia; Kreider, Edward F.; Fera, Daniela Science Translational Medicine, Vol. 9, Issue 381 https://doi.org/10.1126/scitranslmed.aai7514	journal	March 2017
ETE: a python Environment for Tree Exploration Huerta-Cepas, Jaime; Dopazo, Joaquín; Gabaldón, Toni BMC Bioinformatics, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2105-11-24	journal	January 2010
Correction: The Effects of Somatic Hypermutation on Neutralization and Binding in the PGT121 Family of Broadly Neutralizing HIV Antibodies Sok, Devin; Laserson, Uri; Laserson, Jonathan PLoS Pathogens, Vol. 9, Issue 12 https://doi.org/10.1371/annotation/f1f8c791-61e9-45c6-a455-92c6dadf9f06	journal	December 2013
Effects of Darwinian Selection and Mutability on Rate of Broadly Neutralizing Antibody Evolution during HIV-1 Infection Sheng, Zizhang; Schramm, Chaim A.; Connors, Mark PLOS Computational Biology, Vol. 12, Issue 5 https://doi.org/10.1371/journal.pcbi.1004940	journal	May 2016
Broadly Neutralizing Antibody Responses in a Large Longitudinal Sub-Saharan HIV Primary Infection Cohort Landais, Elise; Huang, Xiayu; Havenar-Daughton, Colin PLOS Pathogens, Vol. 12, Issue 1 https://doi.org/10.1371/journal.ppat.1005369	journal	January 2016

Cited By (30)

Stabilization of the V2 loop improves the presentation of V2 loop–associated broadly neutralizing antibody epitopes on HIV-1 envelope trimers de Taeye, Steven W.; Go, Eden P.; Sliepen, Kwinten Journal of Biological Chemistry, Vol. 294, Issue 14 https://doi.org/10.1074/jbc.ra118.005396	journal	February 2019
Long-read amplicon denoising Kumar, Venkatesh; Vollbrecht, Thomas; Chernyshev, Mark Nucleic Acids Research, Vol. 47, Issue 18 https://doi.org/10.1093/nar/gkz657	journal	August 2019
Antibody responses to viral infections: a structural perspective across three different enveloped viruses Murin, Charles D.; Wilson, Ian A.; Ward, Andrew B. Nature Microbiology, Vol. 4, Issue 5 https://doi.org/10.1038/s41564-019-0392-y	journal	March 2019
Positive Selection at Key Residues in the HIV Envelope Distinguishes Broad and Strain-Specific Plasma Neutralizing Antibodies Mabvakure, Batsirai M.; Scheepers, Cathrine; Garrett, Nigel Journal of Virology, Vol. 93, Issue 6 https://doi.org/10.1128/jvi.01685-18	journal	December 2018
Strategies for inducing effective neutralizing antibody responses against HIV-1 del Moral-Sánchez, Iván; Sliepen, Kwinten Expert Review of Vaccines, Vol. 18, Issue 11 https://doi.org/10.1080/14760584.2019.1690458	journal	November 2019
Ancestral sequences from an elite neutralizer proximal to the development of neutralization resistance as a potential source of HIV vaccine immunogens Mesa, Kathryn A.; Yu, Bin; Wrin, Terri PLOS ONE, Vol. 14, Issue 4 https://doi.org/10.1371/journal.pone.0213409	journal	April 2019
An MPER antibody neutralizes HIV-1 using germline features shared among donors Zhang, Lei; Irimia, Adriana; He, Lingling Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-12973-1	journal	November 2019
Defining HIV-1 Envelope N-Glycan Microdomains through Site-Specific Heterogeneity Profiles Hargett, Audra A.; Wei, Qing; Knoppova, Barbora Journal of Virology, Vol. 93, Issue 1 https://doi.org/10.1128/jvi.01177-18	journal	October 2018
The expanding array of HIV broadly neutralizing antibodies McCoy, Laura E. Retrovirology, Vol. 15, Issue 1 https://doi.org/10.1186/s12977-018-0453-y	journal	October 2018
Insights into the Structural Basis of Antibody Affinity Maturation from Next-Generation Sequencing Mishra, Arjun K.; Mariuzza, Roy A. Frontiers in Immunology, Vol. 9 https://doi.org/10.3389/fimmu.2018.00117	journal	February 2018
De novo Inference of Diversity Genes and Analysis of Non-canonical V(DD)J Recombination in Immunoglobulins Safonova, Yana; Pevzner, Pavel A. Frontiers in Immunology, Vol. 10 https://doi.org/10.3389/fimmu.2019.00987	journal	May 2019
Advances in HIV-1 Vaccine Development Gao, Yong; McKay, Paul; Mann, Jamie Viruses, Vol. 10, Issue 4 https://doi.org/10.3390/v10040167	journal	April 2018
Exploiting B Cell Receptor Analyses to Inform on HIV-1 Vaccination Strategies Kreer, Christoph; Gruell, Henning; Mora, Thierry Vaccines, Vol. 8, Issue 1 https://doi.org/10.3390/vaccines8010013	journal	January 2020
Broadly neutralizing antibodies: What is needed to move from a rare event in HIV-1 infection to vaccine efficacy? Subbaraman, Harini; Schanz, Merle; Trkola, Alexandra Retrovirology, Vol. 15, Issue 1 https://doi.org/10.1186/s12977-018-0433-2	journal	July 2018
Development of broadly neutralizing antibodies in HIV-1 infected elite neutralizers Landais, Elise; Moore, Penny L. Retrovirology, Vol. 15, Issue 1 https://doi.org/10.1186/s12977-018-0443-0	journal	September 2018
Glycoengineering HIV-1 Env creates ‘supercharged’ and ‘hybrid’ glycans to increase neutralizing antibody potency, breadth and saturation Crooks, Ema T.; Grimley, Samantha L.; Cully, Michelle PLOS Pathogens, Vol. 14, Issue 5 https://doi.org/10.1371/journal.ppat.1007024	journal	May 2018
Immunodominance and Antigenic Variation of Influenza Virus Hemagglutinin: Implications for Design of Universal Vaccine Immunogens Zost, Seth J.; Wu, Nicholas C.; Hensley, Scott E. The Journal of Infectious Diseases, Vol. 219, Issue Supplement_1 https://doi.org/10.1093/infdis/jiy696	journal	April 2019
Full-Length Envelope Analyzer (FLEA): A tool for longitudinal analysis of viral amplicons Eren, Kemal; Weaver, Steven; Ketteringham, Robert PLOS Computational Biology, Vol. 14, Issue 12 https://doi.org/10.1371/journal.pcbi.1006498	journal	December 2018
Recent progress in broadly neutralizing antibodies to HIV Sok, Devin; Burton, Dennis R. Nature Immunology, Vol. 19, Issue 11 https://doi.org/10.1038/s41590-018-0235-7	journal	October 2018
Somatic hypermutation to counter a globally rare viral immunotype drove off-track antibodies in the CAP256-VRC26 HIV-1 V2-directed bNAb lineage Sacks, David; Bhiman, Jinal N.; Wiehe, Kevin PLOS Pathogens, Vol. 15, Issue 9 https://doi.org/10.1371/journal.ppat.1008005	journal	September 2019
Broadly neutralizing antibodies: What is needed to move from a rare event in HIV-1 infection to vaccine efficacy? Subbaraman, Harini; Schanz, Merle; Trkola, Alexandra BioMed Central https://doi.org/10.5167/uzh-166638	text	January 2018
Identification of Antibodies Targeting the H3N2 Hemagglutinin Receptor Binding Site Following Vaccination of Humans Zost, Seth J.; Lee, Juhye; Gumina, Megan E. SSRN Electronic Journal https://doi.org/10.2139/ssrn.3417940	journal	January 2019
De novo inference of diversity genes and analysis of non-canonical V(DD)J recombination in immunoglobulins Safonova, Yana; Pevzner, Pavel A. arXiv https://doi.org/10.48550/arxiv.1901.02483	preprint	January 2019
The Chimpanzee SIV Envelope Trimer: Structure and Deployment as an HIV Vaccine Template Andrabi, Raiees; Pallesen, Jesper; Allen, Joel D. Cell Reports, Vol. 27, Issue 8 https://doi.org/10.1016/j.celrep.2019.04.082	journal	May 2019
Long-read amplicon denoising Kumar, Venkatesh; Vollbrecht, Thomas; Chernyshev, Mark Nucleic Acids Research, Vol. 47, Issue 18 https://doi.org/10.1093/nar/gkz657	journal	August 2019
Positive Selection at Key Residues in the HIV Envelope Distinguishes Broad and Strain-Specific Plasma Neutralizing Antibodies Mabvakure, Batsirai M.; Scheepers, Cathrine; Garrett, Nigel Journal of Virology, Vol. 93, Issue 6 https://doi.org/10.1128/jvi.01685-18	journal	December 2018
Stabilizing HIV-1 envelope glycoprotein trimers to induce neutralizing antibodies Torrents de la Peña, Alba; Sanders, Rogier W. Retrovirology, Vol. 15, Issue 1 https://doi.org/10.1186/s12977-018-0445-y	journal	September 2018
The expanding array of HIV broadly neutralizing antibodies McCoy, Laura E. Retrovirology, Vol. 15, Issue 1 https://doi.org/10.1186/s12977-018-0453-y	journal	October 2018
Glycoengineering HIV-1 Env creates ‘supercharged’ and ‘hybrid’ glycans to increase neutralizing antibody potency, breadth and saturation Crooks, Ema T.; Grimley, Samantha L.; Cully, Michelle PLOS Pathogens, Vol. 14, Issue 5 https://doi.org/10.1371/journal.ppat.1007024	journal	May 2018
V2-Specific Antibodies in HIV-1 Vaccine Research and Natural Infection: Controllers or Surrogate Markers Duerr, Ralf; Gorny, Miroslaw K. Vaccines, Vol. 7, Issue 3 https://doi.org/10.3390/vaccines7030082	journal	August 2019

Similar Records

Co-evolution of HIV Envelope and Apex-Targeting Neutralizing Antibody Lineage Provides Benchmarks for Vaccine Design

Journal Article · 2018 · Cell Reports · OSTI ID:1454274

Rantalainen, Kimmo; Berndsen, Zachary T.; Murrell, Sasha; +11 more

Vaccination with Glycan-Modified HIV NFL Envelope Trimer-Liposomes Elicits Broadly Neutralizing Antibodies to Multiple Sites of Vulnerability

Journal Article · 2019 · Immunity · OSTI ID:1577147

Dubrovskaya, Viktoriya; Tran, Karen; Ozorowski, Gabriel; +25 more

A Broadly Neutralizing Antibody Targets the Dynamic HIV Envelope Trimer Apex via a Long, Rigidified, and Anionic β-Hairpin Structure

Journal Article · 2017 · Immunity · OSTI ID:1399607

Lee, Jeong Hyun; Andrabi, Raiees; Su, Ching-Yao; +15 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES

Title: HIV Envelope Glycoform Heterogeneity and Localized Diversity Govern the Initiation and Maturation of a V2 Apex Broadly Neutralizing Antibody Lineage

Citation Formats

References (89)

Cited By (30)

Similar Records

Related Subjects