Viral Envelope Evolution in Simian–HIV-Infected Neonate and Adult-Dam Pairs of Rhesus Macaques

Giorgi, Elena E.; Li, Hui; Hora, Bhavna; Shaw, George M.; Wagh, Kshitij; Williams, Wilton B.

doi:10.3390/v16071014

Viral Envelope Evolution in Simian–HIV-Infected Neonate and Adult-Dam Pairs of Rhesus Macaques

Journal Article · Tue Jun 25 04:00:00 EDT 2024 · Viruses

DOI:https://doi.org/10.3390/v16071014· OSTI ID:2470525

^[1]; Li, Hui ^[2]; Hora, Bhavna ^[3]; Shaw, George M. ^[2]; Wagh, Kshitij ^[4]; ^[3]

Fred Hutchinson Cancer Center, Seattle, WA (United States)
Univ. of Pennsylvania, Philadelphia, PA (United States)
Duke Univ. School of Medicine, Durham, NC (United States)
Los Alamos National Laboratory (LANL), Los Alamos, NM (United States); Duke Univ. School of Medicine, Durham, NC (United States)

We recently demonstrated that Simian–HIV (SHIV)-infected neonate rhesus macaques (RMs) generated heterologous HIV-1 neutralizing antibodies (NAbs) with broadly-NAb (bNAb) characteristics at a higher frequency compared with their corresponding dam. Here, we characterized genetic diversity in Env sequences from four neonate or adult/dam RM pairs: in two pairs, neonate and dam RMs made heterologous HIV-1 NAbs; in one pair, neither the neonate nor the dam made heterologous HIV-1 NAbs; and in another pair, only the neonate made heterologous HIV-1 NAbs. Phylogenetic and sequence diversity analyses of longitudinal Envs revealed that a higher genetic diversity, within the host and away from the infecting SHIV strain, was correlated with heterologous HIV-1 NAb development. We identified 22 Env variable sites, of which 9 were associated with heterologous HIV-1 NAb development; 3/9 sites had mutations previously linked to HIV-1 Env bNAb development. These data suggested that viral diversity drives heterologous HIV-1 NAb development, and the faster accumulation of viral diversity in neonate RMs may be a potential mechanism underlying bNAb induction in pediatric populations. Moreover, these data may inform candidate Env immunogens to guide precursor B cells to bNAb status via vaccination by the Env-based selection of bNAb lineage members with the appropriate mutations associated with neutralization breadth.

View Accepted Manuscript (DOE)

Research Organization:: Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: 89233218CNA000001

OSTI ID:: 2470525

Journal Information:: Viruses, Journal Name: Viruses Journal Issue: 7 Vol. 16; ISSN 1999-4915

Publisher:: MDPICopyright Statement

Country of Publication:: United States

Language:: English

References (37)

Strategies for induction of HIV‐1 envelope‐reactive broadly neutralizing antibodies Williams, Wilton B.; Wiehe, Kevin; Saunders, Kevin O. Journal of the International AIDS Society, Vol. 24, Issue S7 https://doi.org/10.1002/jia2.25831	journal	November 2021
Identification and characterization of conserved and variable regions in the envelope gene of HTLV-III/LAV, the retrovirus of AIDS Starcich, Bruno R.; Hahn, Beatrice H.; Shaw, George M. Cell, Vol. 45, Issue 5 https://doi.org/10.1016/0092-8674(86)90778-6	journal	June 1986
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
Holes in the Glycan Shield of the Native HIV Envelope Are a Target of Trimer-Elicited Neutralizing Antibodies McCoy, Laura E.; van Gils, Marit J.; Ozorowski, Gabriel Cell Reports, Vol. 16, Issue 9 https://doi.org/10.1016/j.celrep.2016.07.074	journal	August 2016
Completeness of HIV-1 Envelope Glycan Shield at Transmission Determines Neutralization Breadth Wagh, Kshitij; Kreider, Edward F.; Li, Yingying Cell Reports, Vol. 25, Issue 4 https://doi.org/10.1016/j.celrep.2018.09.087	journal	October 2018
Neonatal SHIV infection in rhesus macaques elicited heterologous HIV-1-neutralizing antibodies Hora, Bhavna; Li, Hui; Shen, Xiaoying Cell Reports, Vol. 42, Issue 3 https://doi.org/10.1016/j.celrep.2023.112255	journal	March 2023
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
Functional Relevance of Improbable Antibody Mutations for HIV Broadly Neutralizing Antibody Development Wiehe, Kevin; Bradley, Todd; Meyerhoff, R. Ryan Cell Host & Microbe, Vol. 23, Issue 6 https://doi.org/10.1016/j.chom.2018.04.018	journal	June 2018
HIV-1 Neutralizing Antibody Signatures and Application to Epitope-Targeted Vaccine Design Bricault, Christine A.; Yusim, Karina; Seaman, Michael S. Cell Host & Microbe, Vol. 25, Issue 1 https://doi.org/10.1016/j.chom.2018.12.001	journal	January 2019
Virological features associated with the development of broadly neutralizing antibodies to HIV-1 Moore, Penny L.; Williamson, Carolyn; Morris, Lynn Trends in Microbiology, Vol. 23, Issue 4 https://doi.org/10.1016/j.tim.2014.12.007	journal	April 2015
Immunological mechanisms of inducing HIV immunity in infants Fouda, Genevieve G.; De Paris, Kristina; Levy, Ofer Vaccine, Vol. 38, Issue 3 https://doi.org/10.1016/j.vaccine.2019.11.011	journal	January 2020
The antigenic structure of the HIV gp120 envelope glycoprotein Wyatt, Richard; Kwong, Peter D.; Desjardins, Elizabeth Nature, Vol. 393, Issue 6686 https://doi.org/10.1038/31514	journal	June 1998
HIV-1 evades antibody-mediated neutralization through conformational masking of receptor-binding sites Kwong, Peter D.; Doyle, Michael L.; Casper, David J. Nature, Vol. 420, Issue 6916 https://doi.org/10.1038/nature01188	journal	December 2002
Antibody neutralization and escape by HIV-1 Wei, Xiping; Decker, Julie M.; Wang, Shuyi Nature, Vol. 422, Issue 6929 https://doi.org/10.1038/nature01470	journal	March 2003
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
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
B-cell–lineage immunogen design in vaccine development with HIV-1 as a case study Haynes, Barton F.; Kelsoe, Garnett; Harrison, Stephen C. Nature Biotechnology, Vol. 30, Issue 5 https://doi.org/10.1038/nbt.2197	journal	May 2012
Tracking HIV-1 recombination to resolve its contribution to HIV-1 evolution in natural infection Song, Hongshuo; Giorgi, Elena E.; Ganusov, Vitaly V. Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-04217-5	journal	May 2018
Strategies for HIV-1 vaccines that induce broadly neutralizing antibodies Haynes, Barton F.; Wiehe, Kevin; Borrow, Persephone Nature Reviews Immunology, Vol. 23, Issue 3 https://doi.org/10.1038/s41577-022-00753-w	journal	August 2022
IQ-TREE 2: New Models and Efficient Methods for Phylogenetic Inference in the Genomic Era Minh, Bui Quang; Schmidt, Heiko A.; Chernomor, Olga Molecular Biology and Evolution, Vol. 37, Issue 5 https://doi.org/10.1093/molbev/msaa015	journal	February 2020
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
What Are the Most Powerful Immunogen Design Vaccine Strategies?: Reverse Vaccinology 2.0 Shows Great Promise Burton, Dennis R. Cold Spring Harbor Perspectives in Biology, Vol. 9, Issue 11 https://doi.org/10.1101/cshperspect.a030262	journal	February 2017
The HIV-1 envelope glycoprotein structure: nailing down a moving target Ward, Andrew B.; Wilson, Ian A. Immunological Reviews, Vol. 275, Issue 1 https://doi.org/10.1111/imr.12507	journal	January 2017
Antibody-virus co-evolution in HIV infection: paths for HIV vaccine development Bonsignori, Mattia; Liao, Hua-Xin; Gao, Feng Immunological Reviews, Vol. 275, Issue 1 https://doi.org/10.1111/imr.12509	journal	January 2017
Developing an HIV vaccine Haynes, Barton F.; Burton, Dennis R. Science, Vol. 355, Issue 6330 https://doi.org/10.1126/science.aan0662	journal	March 2017
Recapitulation of HIV-1 Env-antibody coevolution in macaques leading to neutralization breadth Roark, Ryan S.; Li, Hui; Williams, Wilton B. Science, Vol. 371, Issue 6525 https://doi.org/10.1126/science.abd2638	journal	November 2020
Nonprogressing HIV-infected children share fundamental immunological features of nonpathogenic SIV infection Muenchhoff, Maximilian; Adland, Emily; Karimanzira, Owen Science Translational Medicine, Vol. 8, Issue 358 https://doi.org/10.1126/scitranslmed.aag1048	journal	September 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
Multiple roles for HIV broadly neutralizing antibodies Haynes, Barton F.; Burton, Dennis R.; Mascola, John R. Science Translational Medicine, Vol. 11, Issue 516 https://doi.org/10.1126/scitranslmed.aaz2686	journal	October 2019
New SHIVs and Improved Design Strategy for Modeling HIV-1 Transmission, Immunopathogenesis, Prevention, and Cure Li, Hui; Wang, Shuyi; Lee, Fang-Hua Journal of Virology, Vol. 95, Issue 11 https://doi.org/10.1128/JVI.00071-21	journal	May 2021
Simian-Human Immunodeficiency Virus SHIV.CH505-Infected Infant and Adult Rhesus Macaques Exhibit Similar Env-Specific Antibody Kinetics, despite Distinct T-Follicular Helper and Germinal Center B Cell Landscapes Nelson, Ashley N.; Goswami, Ria; Dennis, Maria Journal of Virology, Vol. 93, Issue 15 https://doi.org/10.1128/JVI.00168-19	journal	May 2019
HIV-1 Subtype C-Infected Children with Exceptional Neutralization Breadth Exhibit Polyclonal Responses Targeting Known Epitopes Ditse, Zanele; Muenchhoff, Maximilian; Adland, Emily Journal of Virology, Vol. 92, Issue 17 https://doi.org/10.1128/JVI.00878-18	journal	June 2018
Global Panel of HIV-1 Env Reference Strains for Standardized Assessments of Vaccine-Elicited Neutralizing Antibodies deCamp, A.; Hraber, P.; Bailer, R. T. Journal of Virology, Vol. 88, Issue 5 https://doi.org/10.1128/JVI.02853-13	journal	December 2013
HIV-Specific Probabilistic Models of Protein Evolution Nickle, David C.; Heath, Laura; Jensen, Mark A. PLoS ONE, Vol. 2, Issue 6 https://doi.org/10.1371/journal.pone.0000503	journal	June 2007
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
The Neutralizing Antibody Response to the HIV-1 Env Protein Moore, Penny L. Current HIV Research, Vol. 16, Issue 1 https://doi.org/10.2174/1570162X15666171124122044	journal	April 2018
Longitudinal Antigenic Sequences and Sites from Intra-Host Evolution (LASSIE) Identifies Immune-Selected HIV Variants Hraber, Peter; Korber, Bette; Wagh, Kshitij Viruses, Vol. 7, Issue 10 https://doi.org/10.3390/v7102881	journal	October 2015

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60 APPLIED LIFE SCIENCES
NAb selection pressures on HIV-1 Env
antibody–virus coevolution
dam–neonate infection pairs
macaque SHIV infection
neonatal SHIV immunity
viral Env evolution

Viral Envelope Evolution in Simian–HIV-Infected Neonate and Adult-Dam Pairs of Rhesus Macaques

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