Skip to content
2000
image of Current Approaches for Assessments of Neutralizing, Binding, and Effector Functions of Antibodies on the Path to Antibody-Mediated Prevention Strategies for HIV-1

Abstract

Robust assay technologies and reference reagents are essential components in efforts to develop safe and effective antibody-mediated prevention strategies for HIV-1. Here, we describe current approaches used to conduct standardized assessments of neutralizing, binding, and Fc receptor-mediated effector functions of vaccine-elicited antibodies, with an emphasis on recent developments that enable early precursors and intermediates of broadly neutralizing antibodies (bnAbs) to be monitored. We also describe how these assay technologies were adapted to facilitate clinical evaluations of passively delivered bnAbs for HIV-1 prevention.

This is an open access article published under CC BY 4.0 https://creativecommons.org/licenses/by/4.0/legalcode.
Loading

Article metrics loading...

/content/journals/chr/10.2174/011570162X363301250314034023
2025-03-27
2025-10-18
Loading full text...

Full text loading...

/deliver/fulltext/chr/10.2174/011570162X363301250314034023/BMS-CHIVR-2024-HT10-6091-8.html?itemId=/content/journals/chr/10.2174/011570162X363301250314034023&mimeType=html&fmt=ahah

References

  1. Haynes B.F. Wiehe K. Borrow P. Saunders K.O. Korber B. Wagh K. McMichael A.J. Kelsoe G. Hahn B.H. Alt F. Shaw G.M. Strategies for HIV-1 vaccines that induce broadly neutralizing antibodies. Nat. Rev. Immunol. 2023 23 3 142 158 10.1038/s41577‑022‑00753‑w 35962033
    [Google Scholar]
  2. Kwong P.D. Mascola J.R. HIV-1 vaccines based on antibody identification, B cell ontogeny, and epitope structure. Immunity 2018 48 5 855 871 10.1016/j.immuni.2018.04.029 29768174
    [Google Scholar]
  3. Sanders R.W. van Gils M.J. Derking R. Sok D. Ketas T.J. Burger J.A. Ozorowski G. Cupo A. Simonich C. Goo L. Arendt H. Kim H.J. Lee J.H. Pugach P. Williams M. Debnath G. Moldt B. van Breemen M.J. Isik G. Medina-Ramírez M. Back J.W. Koff W.C. Julien J.P. Rakasz E.G. Seaman M.S. Guttman M. Lee K.K. Klasse P.J. LaBranche C. Schief W.R. Wilson I.A. Overbaugh J. Burton D.R. Ward A.B. Montefiori D.C. Dean H. Moore J.P. HIV-1 neutralizing antibodies induced by native-like envelope trimers. Science 2015 349 6244 aac4223 10.1126/science.aac4223 26089353
    [Google Scholar]
  4. Pauthner M.G. Nkolola J.P. Havenar-Daughton C. Murrell B. Reiss S.M. Bastidas R. Prévost J. Nedellec R. von Bredow B. Abbink P. Cottrell C.A. Kulp D.W. Tokatlian T. Nogal B. Bianchi M. Li H. Lee J.H. Butera S.T. Evans D.T. Hangartner L. Finzi A. Wilson I.A. Wyatt R.T. Irvine D.J. Schief W.R. Ward A.B. Sanders R.W. Crotty S. Shaw G.M. Barouch D.H. Burton D.R. Vaccine-induced protection from homologous tier 2 SHIV challenge in nonhuman primates depends on serum-neutralizing antibody titers. Immunity 2019 50 1 241 252.e6 10.1016/j.immuni.2018.11.011 30552025
    [Google Scholar]
  5. Hahn W.O. Parks K.R. Shen M. Ozorowski G. Janes H. Ballweber-Fleming L. Woodward Davis A.S. Duplessis C. Tomai M. Dey A.K. Sagawa Z.K. De Rosa S.C. Seese A. Kallur Siddaramaiah L. Stamatatos L. Lee W.H. Sewall L.M. Karlinsey D. Turner H.L. Rubin V. Furth S. MacPhee K. Duff M. Corey L. Keefer M.C. Edupuganti S. Frank I. Maenza J. Baden L.R. Hyrien O. Sanders R.W. Moore J.P. Ward A.B. Tomaras G.D. Montefiori D.C. Rouphael N. McElrath M.J. Use of 3M-052-AF with Alum adjuvant in HIV trimer vaccine induces human autologous neutralizing antibodies. J. Exp. Med. 2024 221 10 e20240604 10.1084/jem.20240604 39235529
    [Google Scholar]
  6. Leggat D.J. Cohen K.W. Willis J.R. Fulp W.J. deCamp A.C. Kalyuzhniy O. Cottrell C.A. Menis S. Finak G. Ballweber-Fleming L. Srikanth A. Plyler J.R. Schiffner T. Liguori A. Rahaman F. Lombardo A. Philiponis V. Whaley R.E. Seese A. Brand J. Ruppel A.M. Hoyland W. Yates N.L. Williams L.D. Greene K. Gao H. Mahoney C.R. Corcoran M.M. Cagigi A. Taylor A. Brown D.M. Ambrozak D.R. Sincomb T. Hu X. Tingle R. Georgeson E. Eskandarzadeh S. Alavi N. Lu D. Mullen T.M. Kubitz M. Groschel B. Maenza J. Kolokythas O. Khati N. Bethony J. Crotty S. Roederer M. Karlsson Hedestam G.B. Tomaras G.D. Montefiori D. Diemert D. Koup R.A. Laufer D.S. McElrath M.J. McDermott A.B. Schief W.R. Vaccination induces HIV broadly neutralizing antibody precursors in humans. Science 2022 378 6623 eadd6502 10.1126/science.add6502 36454825
    [Google Scholar]
  7. Steichen J.M. Lin Y.C. Havenar-Daughton C. Pecetta S. Ozorowski G. Willis J.R. Toy L. Sok D. Liguori A. Kratochvil S. Torres J.L. Kalyuzhniy O. Melzi E. Kulp D.W. Raemisch S. Hu X. Bernard S.M. Georgeson E. Phelps N. Adachi Y. Kubitz M. Landais E. Umotoy J. Robinson A. Briney B. Wilson I.A. Burton D.R. Ward A.B. Crotty S. Batista F.D. Schief W.R. A generalized HIV vaccine design strategy for priming of broadly neutralizing antibody responses. Science 2019 366 6470 eaax4380 10.1126/science.aax4380 31672916
    [Google Scholar]
  8. Steichen J.M. Kulp D.W. Tokatlian T. Escolano A. Dosenovic P. Stanfield R.L. McCoy L.E. Ozorowski G. Hu X. Kalyuzhniy O. Briney B. Schiffner T. Garces F. Freund N.T. Gitlin A.D. Menis S. Georgeson E. Kubitz M. Adachi Y. Jones M. Mutafyan A.A. Yun D.S. Mayer C.T. Ward A.B. Burton D.R. Wilson I.A. Irvine D.J. Nussenzweig M.C. Schief W.R. HIV vaccine design to target germline precursors of glycan-dependent broadly neutralizing antibodies. Immunity 2016 45 3 483 496 10.1016/j.immuni.2016.08.016 27617678
    [Google Scholar]
  9. Mu Z. Wiehe K. Saunders K.O. Henderson R. Cain D.W. Parks R. Martik D. Mansouri K. Edwards R.J. Newman A. Lu X. Xia S.M. Eaton A. Bonsignori M. Montefiori D. Han Q. Venkatayogi S. Evangelous T. Wang Y. Rountree W. Korber B. Wagh K. Tam Y. Barbosa C. Alam S.M. Williams W.B. Tian M. Alt F.W. Pardi N. Weissman D. Haynes B.F. mRNA-encoded HIV-1 Env trimer ferritin nanoparticles induce monoclonal antibodies that neutralize heterologous HIV-1 isolates in mice. Cell Rep. 2022 38 11 110514 10.1016/j.celrep.2022.110514 35294883
    [Google Scholar]
  10. Andrabi R. Pallesen J. Allen J.D. Song G. Zhang J. de Val N. Gegg G. Porter K. Su C.Y. Pauthner M. Newman A. Bouton-Verville H. Garces F. Wilson I.A. Crispin M. Hahn B.H. Haynes B.F. Verkoczy L. Ward A.B. Burton D.R. The Chimpanzee SIV envelope trimer: Structure and deployment as an HIV vaccine template. Cell Rep. 2019 27 8 2426 2441.e6 10.1016/j.celrep.2019.04.082 31116986
    [Google Scholar]
  11. Saunders K.O. Verkoczy L.K. Jiang C. Zhang J. Parks R. Chen H. Housman M. Bouton-Verville H. Shen X. Trama A.M. Scearce R. Sutherland L. Santra S. Newman A. Eaton A. Xu K. Georgiev I.S. Joyce M.G. Tomaras G.D. Bonsignori M. Reed S.G. Salazar A. Mascola J.R. Moody M.A. Cain D.W. Centlivre M. Zurawski S. Zurawski G. Erickson H.P. Kwong P.D. Alam S.M. Levy Y. Montefiori D.C. Haynes B.F. Vaccine induction of heterologous tier 2 HIV-1 neutralizing antibodies in animal models. Cell Rep. 2017 21 13 3681 3690 10.1016/j.celrep.2017.12.028 29281818
    [Google Scholar]
  12. Saunders K.O. Wiehe K. Tian M. Acharya P. Bradley T. Alam S.M. Go E.P. Scearce R. Sutherland L. Henderson R. Hsu A.L. Borgnia M.J. Chen H. Lu X. Wu N.R. Watts B. Jiang C. Easterhoff D. Cheng H.L. McGovern K. Waddicor P. Chapdelaine-Williams A. Eaton A. Zhang J. Rountree W. Verkoczy L. Tomai M. Lewis M.G. Desaire H.R. Edwards R.J. Cain D.W. Bonsignori M. Montefiori D. Alt F.W. Haynes B.F. Targeted selection of HIV-specific antibody mutations by engineering B cell maturation. Science 2019 366 6470 eaay7199 10.1126/science.aay7199 31806786
    [Google Scholar]
  13. Lin Y.R. Parks K.R. Weidle C. Naidu A.S. Khechaduri A. Riker A.O. Takushi B. Chun J.H. Borst A.J. Veesler D. Stuart A. Agrawal P. Gray M. Pancera M. Huang P.S. Stamatatos L. HIV-1 VRC01 germline-targeting immunogens select distinct epitope-specific B cell receptors. Immunity 2020 53 4 840 851.e6 10.1016/j.immuni.2020.09.007 33053332
    [Google Scholar]
  14. Steichen J.M. Phung I. Salcedo E. Ozorowski G. Willis J.R. Baboo S. Liguori A. Cottrell C.A. Torres J.L. Madden P.J. Ma K.M. Sutton H.J. Lee J.H. Kalyuzhniy O. Allen J.D. Rodriguez O.L. Adachi Y. Mullen T.M. Georgeson E. Kubitz M. Burns A. Barman S. Mopuri R. Metz A. Altheide T.K. Diedrich J.K. Saha S. Shields K. Schultze S.E. Smith M.L. Schiffner T. Burton D.R. Watson C.T. Bosinger S.E. Crispin M. Yates J.R. III Paulson J.C. Ward A.B. Sok D. Crotty S. Schief W.R. Vaccine priming of rare HIV broadly neutralizing antibody precursors in nonhuman primates. Science 2024 384 6697 eadj8321 10.1126/science.adj8321 38753769
    [Google Scholar]
  15. Caniels T.G. Medina-Ramírez M. Zhang J. Sarkar A. Kumar S. LaBranche A. Derking R. Allen J.D. Snitselaar J.L. Capella-Pujol J. Sánchez I.M. Yasmeen A. Diaz M. Aldon Y. Bijl T.P.L. Venkatayogi S. Martin Beem J.S. Newman A. Jiang C. Lee W.H. Pater M. Burger J.A. van Breemen M.J. de Taeye S.W. Rantalainen K. LaBranche C. Saunders K.O. Montefiori D. Ozorowski G. Ward A.B. Crispin M. Moore J.P. Klasse P.J. Haynes B.F. Wilson I.A. Wiehe K. Verkoczy L. Sanders R.W. Germline-targeting HIV-1 Env vaccination induces VRC01-class antibodies with rare insertions. Cell Rep. Med. 2023 4 4 101003 10.1016/j.xcrm.2023.101003 37044090
    [Google Scholar]
  16. Briney B. Sok D. Jardine J.G. Kulp D.W. Skog P. Menis S. Jacak R. Kalyuzhniy O. de Val N. Sesterhenn F. Le K.M. Ramos A. Jones M. Saye-Francisco K.L. Blane T.R. Spencer S. Georgeson E. Hu X. Ozorowski G. Adachi Y. Kubitz M. Sarkar A. Wilson I.A. Ward A.B. Nemazee D. Burton D.R. Schief W.R. Tailored immunogens direct affinity maturation toward HIV neutralizing antibodies. Cell 2016 166 6 1459 1470.e11 10.1016/j.cell.2016.08.005 27610570
    [Google Scholar]
  17. Escolano A. Steichen J.M. Dosenovic P. Kulp D.W. Golijanin J. Sok D. Freund N.T. Gitlin A.D. Oliveira T. Araki T. Lowe S. Chen S.T. Heinemann J. Yao K.H. Georgeson E. Saye-Francisco K.L. Gazumyan A. Adachi Y. Kubitz M. Burton D.R. Schief W.R. Nussenzweig M.C. Sequential immunization elicits broadly neutralizing anti-HIV-1 antibodies in Ig knockin mice. Cell 2016 166 6 1445 1458.e12 10.1016/j.cell.2016.07.030 27610569
    [Google Scholar]
  18. Cottrell C.A. Hu X. Lee J.H. Skog P. Luo S. Flynn C.T. McKenney K.R. Hurtado J. Kalyuzhniy O. Liguori A. Willis J.R. Landais E. Raemisch S. Chen X. Baboo S. Himansu S. Diedrich J.K. Duan H. Cheng C. Schiffner T. Bader D.L.V. Kulp D.W. Tingle R. Georgeson E. Eskandarzadeh S. Alavi N. Lu D. Sincomb T. Kubitz M. Mullen T.M. Yates J.R. III Paulson J.C. Mascola J.R. Alt F.W. Briney B. Sok D. Schief W.R. Heterologous prime-boost vaccination drives early maturation of HIV broadly neutralizing antibody precursors in humanized mice. Sci. Transl. Med. 2024 16 748 eadn0223 10.1126/scitranslmed.adn0223 38753806
    [Google Scholar]
  19. Corey L. Gilbert P.B. Juraska M. Montefiori D.C. Morris L. Karuna S.T. Edupuganti S. Mgodi N.M. deCamp A.C. Rudnicki E. Huang Y. Gonzales P. Cabello R. Orrell C. Lama J.R. Laher F. Lazarus E.M. Sanchez J. Frank I. Hinojosa J. Sobieszczyk M.E. Marshall K.E. Mukwekwerere P.G. Makhema J. Baden L.R. Mullins J.I. Williamson C. Hural J. McElrath M.J. Bentley C. Takuva S. Gomez Lorenzo M.M. Burns D.N. Espy N. Randhawa A.K. Kochar N. Piwowar-Manning E. Donnell D.J. Sista N. Andrew P. Kublin J.G. Gray G. Ledgerwood J.E. Mascola J.R. Cohen M.S. Two randomized trials of neutralizing antibodies to prevent HIV-1 acquisition. N. Engl. J. Med. 2021 384 11 1003 1014 10.1056/NEJMoa2031738 33730454
    [Google Scholar]
  20. Gilbert P.B. Huang Y. deCamp A.C. Karuna S. Zhang Y. Magaret C.A. Giorgi E.E. Korber B. Edlefsen P.T. Rossenkhan R. Juraska M. Rudnicki E. Kochar N. Huang Y. Carpp L.N. Barouch D.H. Mkhize N.N. Hermanus T. Kgagudi P. Bekker V. Kaldine H. Mapengo R.E. Eaton A. Domin E. West C. Feng W. Tang H. Seaton K.E. Heptinstall J. Brackett C. Chiong K. Tomaras G.D. Andrew P. Mayer B.T. Reeves D.B. Sobieszczyk M.E. Garrett N. Sanchez J. Gay C. Makhema J. Williamson C. Mullins J.I. Hural J. Cohen M.S. Corey L. Montefiori D.C. Morris L. Neutralization titer biomarker for antibody-mediated prevention of HIV-1 acquisition. Nat. Med. 2022 28 9 1924 1932 10.1038/s41591‑022‑01953‑6 35995954
    [Google Scholar]
  21. Gelderblom H.C. Corey L. Barouch D.H. The potential of broadly neutralizing antibodies for HIV prevention. J. Int. AIDS Soc. 2024 27 5 e26257 10.1002/jia2.26257 38757844
    [Google Scholar]
  22. Kong R. Louder M.K. Wagh K. Bailer R.T. deCamp A. Greene K. Gao H. Taft J.D. Gazumyan A. Liu C. Nussenzweig M.C. Korber B. Montefiori D.C. Mascola J.R. Improving neutralization potency and breadth by combining broadly reactive HIV-1 antibodies targeting major neutralization epitopes. J. Virol. 2015 89 5 2659 2671 10.1128/JVI.03136‑14 25520506
    [Google Scholar]
  23. Wagh K. Bhattacharya T. Williamson C. Robles A. Bayne M. Garrity J. Rist M. Rademeyer C. Yoon H. Lapedes A. Gao H. Greene K. Louder M.K. Kong R. Karim S.A. Burton D.R. Barouch D.H. Nussenzweig M.C. Mascola J.R. Morris L. Montefiori D.C. Korber B. Seaman M.S. Optimal combinations of broadly neutralizing antibodies for prevention and treatment of HIV-1 Clade C infection. PLoS Pathog. 2016 12 3 e1005520 10.1371/journal.ppat.1005520 27028935
    [Google Scholar]
  24. Wagh K. Seaman M.S. Zingg M. Fitzsimons T. Barouch D.H. Burton D.R. Connors M. Ho D.D. Mascola J.R. Nussenzweig M.C. Ravetch J. Gautam R. Martin M.A. Montefiori D.C. Korber B. Potential of conventional & bispecific broadly neutralizing antibodies for prevention of HIV-1 subtype A, C & D infections. PLoS Pathog. 2018 14 3 e1006860 10.1371/journal.ppat.1006860 29505593
    [Google Scholar]
  25. Miner MD Corey L Montefiori D Broadly neutralizing monoclonal antibodies for HIV prevention. J. Int AIDS Soc. 2021 24 7 e25829 10.1002/jia2.25829
    [Google Scholar]
  26. Ko S.Y. Pegu A. Rudicell R.S. Yang Z. Joyce M.G. Chen X. Wang K. Bao S. Kraemer T.D. Rath T. Zeng M. Schmidt S.D. Todd J.P. Penzak S.R. Saunders K.O. Nason M.C. Haase A.T. Rao S.S. Blumberg R.S. Mascola J.R. Nabel G.J. Enhanced neonatal Fc receptor function improves protection against primate SHIV infection. Nature 2014 514 7524 642 645 10.1038/nature13612 25119033
    [Google Scholar]
  27. Zalevsky J. Chamberlain A.K. Horton H.M. Karki S. Leung I.W.L. Sproule T.J. Lazar G.A. Roopenian D.C. Desjarlais J.R. Enhanced antibody half-life improves in vivo activity. Nat. Biotechnol. 2010 28 2 157 159 10.1038/nbt.1601 20081867
    [Google Scholar]
  28. Haynes B.F. Gilbert P.B. McElrath M.J. Zolla-Pazner S. Tomaras G.D. Alam S.M. Evans D.T. Montefiori D.C. Karnasuta C. Sutthent R. Liao H.X. DeVico A.L. Lewis G.K. Williams C. Pinter A. Fong Y. Janes H. DeCamp A. Huang Y. Rao M. Billings E. Karasavvas N. Robb M.L. Ngauy V. de Souza M.S. Paris R. Ferrari G. Bailer R.T. Soderberg K.A. Andrews C. Berman P.W. Frahm N. De Rosa S.C. Alpert M.D. Yates N.L. Shen X. Koup R.A. Pitisuttithum P. Kaewkungwal J. Nitayaphan S. Rerks-Ngarm S. Michael N.L. Kim J.H. Immune-correlates analysis of an HIV-1 vaccine efficacy trial. N. Engl. J. Med. 2012 366 14 1275 1286 10.1056/NEJMoa1113425 22475592
    [Google Scholar]
  29. Gray G.E. Bekker L.G. Laher F. Malahleha M. Allen M. Moodie Z. Grunenberg N. Huang Y. Grove D. Prigmore B. Kee J.J. Benkeser D. Hural J. Innes C. Lazarus E. Meintjes G. Naicker N. Kalonji D. Nchabeleng M. Sebe M. Singh N. Kotze P. Kassim S. Dubula T. Naicker V. Brumskine W. Ncayiya C.N. Ward A.M. Garrett N. Kistnasami G. Gaffoor Z. Selepe P. Makhoba P.B. Mathebula M.P. Mda P. Adonis T. Mapetla K.S. Modibedi B. Philip T. Kobane G. Bentley C. Ramirez S. Takuva S. Jones M. Sikhosana M. Atujuna M. Andrasik M. Hejazi N.S. Puren A. Wiesner L. Phogat S. Diaz Granados C. Koutsoukos M. Van Der Meeren O. Barnett S.W. Kanesa-Thasan N. Kublin J.G. McElrath M.J. Gilbert P.B. Janes H. Corey L. Vaccine efficacy of ALVAC-HIV and bivalent subtype C gp120–MF59 in adults. N. Engl. J. Med. 2021 384 12 1089 1100 10.1056/NEJMoa2031499 33761206
    [Google Scholar]
  30. Gray GE Mngadi K Lavreys L Nijs S Gilbert PB Hural J Hyrien O Juraska M Luedtke A Mann P McElrath MJ Odhiambo JA Stieh DJ van Duijn J Takalani AN Willems W Tapley A Tomaras GD Van Hoof J Schuitemaker H Swann E Barouch DH Kublin JG Corey L Pau MG Buchbinder S Tomaka F Mosaic HIV-1 vaccine regimen in southern African women (Imbokodo/HVTN 705/HPX2008): a randomised, double-blind, placebo-controlled, phase 2b trial. Lancet. Infect. Dis 2024 19 S1473 10.1016/S1473‑3099(24)00358‑X
    [Google Scholar]
  31. Anklesaria P. Russell N.D. Iterative hypothesis testing in HIV vaccine research: Moving towards success. J. Int. AIDS Soc. 2023 26 5 e26102 10.1002/jia2.26102 37195222
    [Google Scholar]
  32. Neidich S.D. Fong Y. Li S.S. Geraghty D.E. Williamson B.D. Young W.C. Goodman D. Seaton K.E. Shen X. Sawant S. Zhang L. deCamp A.C. Blette B.S. Shao M. Yates N.L. Feely F. Pyo C.W. Ferrari G. Frank I. Karuna S.T. Swann E.M. Mascola J.R. Graham B.S. Hammer S.M. Sobieszczyk M.E. Corey L. Janes H.E. McElrath M.J. Gottardo R. Gilbert P.B. Tomaras G.D. Antibody Fc effector functions and IgG3 associate with decreased HIV-1 risk. J. Clin. Invest. 2019 129 11 4838 4849 10.1172/JCI126391 31589165
    [Google Scholar]
  33. Kenny A. van Duijn J. Dintwe O. Heptinstall J. Burnham R. Sawant S. Zhang L. Mielke D. Khuzwayo S. Omar F.L. Stanfield-Oakley S. Keyes T. Dunn B. Goodman D. Fong Y. Benkeser D. Zou R. Hural J. Hyrien O. Juraska M. Luedtke A. van der Laan L. Giorgi E.E. Magaret C. Carpp L.N. Pattacini L. van de Kerkhof T. Korber B. Willems W. Fisher L.H. Schuitemaker H. Swann E. Kublin J.G. Pau M.G. Buchbinder S. Tomaka F. Nijs S. Lavreys L. Gelderblom H.C. Corey L. Mngadi K. Gray G.E. Borducchi E. Hendriks J. Seaton K.E. Zolla-Pazner S. Barouch D.H. Ferrari G. De Rosa S.C. McElrath M.J. Andersen-Nissen E. Stieh D.J. Tomaras G.D. Gilbert P.B. Allagappen J. Andriesen J. Ayres A. Baral S. Bekker L-G. Besethi A. Borremans C. Braams E. Brackett C. Brumskine W. Chilengi R. Choi R. Dubula T. Dumas J.S. Dunn B. Etikala R. Euler Z. Everett S. Garrett N. Gelderblom H. Gill K. Gillespie K. Goedhart D. Goosmann E. Grant S. Hands E. Haynes B. Herringer B. Hoosain Z. Hosseinipour M. Hunidzarira P. Hutter J. Inambao M. Innes C. Keyes T. Kilembe W. Kotze P. Kotze S. Laher F. Laszlo I. Lazarus E. Liao H-X. Lin Y. Lu H. Lucas J. Malahleha M. McNair T. Meerts P. Mgaga Z. Montlha M. Mosito B. Moultrie A. Mudrak S. Oriol-Mathieu V. Sarzotti-Kelsoe M. Mathebula M.T. Matoga M. McClennen R. Mda P. Meerts P. Naicker V. Naidoo L. Okkers C-A. Omarjee S. Pasmans H. Philip T. Pinter A. Pitsi A. Ramos O. Randhawa A. Roels S. Rohith S. Rutten L. Sadoff J. Salinas G. Salzgeber Y. Scheppler L. Schwedhelm K. Schuller N. Sharak A. Stanfield-Oakley S. Sopher C. Tafatatha T. Takuva S.G. Tang C. Vandebosch A. Viegas E. Voillet V. Wegmann F. Weijtens M. Wilcox S. Williams A. Yu C. Yu P-C. Yuan O. Zhang X. Immune correlates analysis of the Imbokodo (HVTN 705/HPX2008) efficacy trial of a mosaic HIV-1 vaccine regimen evaluated in Southern African people assigned female sex at birth: A two-phase case-control study. EBioMedicine 2024 108 105320 Epub ahead of print 10.1016/j.ebiom.2024.105320 39236556
    [Google Scholar]
  34. Montefiori D.C. Measuring HIV neutralization in a luciferase reporter gene assay. Methods Mol. Biol. 2009 485 395 405 10.1007/978‑1‑59745‑170‑3_26 19020839
    [Google Scholar]
  35. Kabat D. Kozak S.L. Wehrly K. Chesebro B. Differences in CD4 dependence for infectivity of laboratory-adapted and primary patient isolates of human immunodeficiency virus type 1. J. Virol. 1994 68 4 2570 2577 10.1128/jvi.68.4.2570‑2577.1994 8139036
    [Google Scholar]
  36. Platt E.J. Wehrly K. Kuhmann S.E. Chesebro B. Kabat D. Effects of CCR5 and CD4 cell surface concentrations on infections by macrophagetropic isolates of human immunodeficiency virus type 1. J. Virol. 1998 72 4 2855 2864 10.1128/JVI.72.4.2855‑2864.1998 9525605
    [Google Scholar]
  37. Wei X. Decker J.M. Liu H. Zhang Z. Arani R.B. Kilby J.M. Saag M.S. Wu X. Shaw G.M. Kappes J.C. Emergence of resistant human immunodeficiency virus type 1 in patients receiving fusion inhibitor (T-20) monotherapy. Antimicrob. Agents Chemother. 2002 46 6 1896 1905 10.1128/AAC.46.6.1896‑1905.2002 12019106
    [Google Scholar]
  38. Wei X. Decker J.M. Wang S. Hui H. Kappes J.C. Wu X. Salazar-Gonzalez J.F. Salazar M.G. Kilby J.M. Saag M.S. Komarova N.L. Nowak M.A. Hahn B.H. Kwong P.D. Shaw G.M. Antibody neutralization and escape by HIV-1. Nature 2003 422 6929 307 312 10.1038/nature01470 12646921
    [Google Scholar]
  39. Richman D.D. Wrin T. Little S.J. Petropoulos C.J. Rapid evolution of the neutralizing antibody response to HIV type 1 infection. Proc. Natl. Acad. Sci. USA 2003 100 7 4144 4149 10.1073/pnas.0630530100 12644702
    [Google Scholar]
  40. Gilbert P. Wang M. Wrin T. Petropoulos C. Gurwith M. Sinangil F. D’Souza P. Rodriguez-Chavez I.R. DeCamp A. Giganti M. Berman P.W. Self S.G. Montefiori D.C. Magnitude and breadth of a nonprotective neutralizing antibody response in an efficacy trial of a candidate HIV-1 gp120 vaccine. J. Infect. Dis. 2010 202 4 595 605 10.1086/654816 20608874
    [Google Scholar]
  41. Sarzotti-Kelsoe M. Bailer R.T. Turk E. Lin C. Bilska M. Greene K.M. Gao H. Todd C.A. Ozaki D.A. Seaman M.S. Mascola J.R. Montefiori D.C. Optimization and validation of the TZM-bl assay for standardized assessments of neutralizing antibodies against HIV-1. J. Immunol. Methods 2014 409 131 146 10.1016/j.jim.2013.11.022 24291345
    [Google Scholar]
  42. Ozaki D.A. Gao H. Todd C.A. Greene K.M. Montefiori D.C. Sarzotti-Kelsoe M. International technology transfer of a GCLP-compliant HIV-1 neutralizing antibody assay for human clinical trials. PLoS One 2012 7 1 e30963 10.1371/journal.pone.0030963 22303476
    [Google Scholar]
  43. Todd C.A. Greene K.M. Yu X. Ozaki D.A. Gao H. Huang Y. Wang M. Li G. Brown R. Wood B. D’Souza M.P. Gilbert P. Montefiori D.C. Sarzotti-Kelsoe M. Development and implementation of an international proficiency testing program for a neutralizing antibody assay for HIV-1 in TZM-bl cells. J. Immunol. Methods 2012 375 1-2 57 67 10.1016/j.jim.2011.09.007 21968254
    [Google Scholar]
  44. Fenyö E.M. Heath A. Dispinseri S. Holmes H. Lusso P. Zolla-Pazner S. Donners H. Heyndrickx L. Alcami J. Bongertz V. Jassoy C. Malnati M. Montefiori D. Moog C. Morris L. Osmanov S. Polonis V. Sattentau Q. Schuitemaker H. Sutthent R. Wrin T. Scarlatti G. International network for comparison of HIV neutralization assays: The NeutNet report. PLoS One 2009 4 2 e4505 10.1371/journal.pone.0004505 19229336
    [Google Scholar]
  45. Heyndrickx L. Heath A. Sheik-Khalil E. Alcami J. Bongertz V. Jansson M. Malnati M. Montefiori D. Moog C. Morris L. Osmanov S. Polonis V. Ramaswamy M. Sattentau Q. Tolazzi M. Schuitemaker H. Willems B. Wrin T. Fenyö E.M. Scarlatti G. International network for comparison of HIV neutralization assays: The NeutNet report II. PLoS One 2012 7 5 e36438 10.1371/journal.pone.0036438 22590544
    [Google Scholar]
  46. Mascola J.R. D’Souza P. Gilbert P. Hahn B.H. Haigwood N.L. Morris L. Petropoulos C.J. Polonis V.R. Sarzotti M. Montefiori D.C. Recommendations for the design and use of standard virus panels to assess neutralizing antibody responses elicited by candidate human immunodeficiency virus type 1 vaccines. J. Virol. 2005 79 16 10103 10107 10.1128/JVI.79.16.10103‑10107.2005 16051803
    [Google Scholar]
  47. Montefiori D.C. Roederer M. Morris L. Seaman M.S. Neutralization tiers of HIV-1. Curr. Opin. HIV AIDS 2018 13 2 128 136 10.1097/COH.0000000000000442 29266013
    [Google Scholar]
  48. Seaman M.S. Janes H. Hawkins N. Grandpre L.E. Devoy C. Giri A. Coffey R.T. Harris L. Wood B. Daniels M.G. Bhattacharya T. Lapedes A. Polonis V.R. McCutchan F.E. Gilbert P.B. Self S.G. Korber B.T. Montefiori D.C. Mascola J.R. Tiered categorization of a diverse panel of HIV-1 Env pseudoviruses for assessment of neutralizing antibodies. J. Virol. 2010 84 3 1439 1452 10.1128/JVI.02108‑09 19939925
    [Google Scholar]
  49. Rademeyer C. Korber B. Seaman M.S. Giorgi E.E. Thebus R. Robles A. Sheward D.J. Wagh K. Garrity J. Carey B.R. Gao H. Greene K.M. Tang H. Bandawe G.P. Marais J.C. Diphoko T.E. Hraber P. Tumba N. Moore P.L. Gray G.E. Kublin J. McElrath M.J. Vermeulen M. Middelkoop K. Bekker L.G. Hoelscher M. Maboko L. Makhema J. Robb M.L. Abdool Karim S. Abdool Karim Q. Kim J.H. Hahn B.H. Gao F. Swanstrom R. Morris L. Montefiori D.C. Williamson C. Features of recently transmitted HIV-1 Clade C viruses that impact antibody recognition: Implications for active and passive immunization. PLoS Pathog. 2016 12 7 e1005742 10.1371/journal.ppat.1005742 27434311
    [Google Scholar]
  50. Li M. Gao F. Mascola J.R. Stamatatos L. Polonis V.R. Koutsoukos M. Voss G. Goepfert P. Gilbert P. Greene K.M. Bilska M. Kothe D.L. Salazar-Gonzalez J.F. Wei X. Decker J.M. Hahn B.H. Montefiori D.C. Human immunodeficiency virus type 1 env clones from acute and early subtype B infections for standardized assessments of vaccine-elicited neutralizing antibodies. J. Virol. 2005 79 16 10108 10125 10.1128/JVI.79.16.10108‑10125.2005 16051804
    [Google Scholar]
  51. deCamp A. Hraber P. Bailer R.T. Seaman M.S. Ochsenbauer C. Kappes J. Gottardo R. Edlefsen P. Self S. Tang H. Greene K. Gao H. Daniell X. Sarzotti-Kelsoe M. Gorny M.K. Zolla-Pazner S. LaBranche C.C. Mascola J.R. Korber B.T. Montefiori D.C. Global panel of HIV-1 Env reference strains for standardized assessments of vaccine-elicited neutralizing antibodies. J. Virol. 2014 88 5 2489 2507 10.1128/JVI.02853‑13 24352443
    [Google Scholar]
  52. Hraber P. Rademeyer C. Williamson C. Seaman M.S. Gottardo R. Tang H. Greene K. Gao H. LaBranche C. Mascola J.R. Morris L. Montefiori D.C. Korber B. Panels of HIV-1 subtype C Env reference strains for standardized neutralization assessments. J. Virol. 2017 91 19 e00991-17 10.1128/JVI.00991‑17 28747500
    [Google Scholar]
  53. Hraber P. Seaman M.S. Bailer R.T. Mascola J.R. Montefiori D.C. Korber B.T. Prevalence of broadly neutralizing antibody responses during chronic HIV-1 infection. AIDS 2014 28 2 163 169 10.1097/QAD.0000000000000106 24361678
    [Google Scholar]
  54. Hraber P. Korber B.T. Lapedes A.S. Bailer R.T. Seaman M.S. Gao H. Greene K.M. McCutchan F. Williamson C. Kim J.H. Tovanabutra S. Hahn B.H. Swanstrom R. Thomson M.M. Gao F. Harris L. Giorgi E. Hengartner N. Bhattacharya T. Mascola J.R. Montefiori D.C. Impact of clade, geography, and age of the epidemic on HIV-1 neutralization by antibodies. J. Virol. 2014 88 21 12623 12643 10.1128/JVI.01705‑14 25142591
    [Google Scholar]
  55. Huang Y. Gilbert P.B. Montefiori D.C. Self S.G. Simultaneous evaluation of the magnitude and breadth of a left- and right-censored multivariate response, with application to HIV vaccine development. Stat. Biopharm. Res. 2009 1 1 81 91 10.1198/sbr.2009.0008 20072667
    [Google Scholar]
  56. Bunnik E.M. Euler Z. Welkers M.R.A. Boeser-Nunnink B.D.M. Grijsen M.L. Prins J.M. Schuitemaker H. Adaptation of HIV-1 envelope gp120 to humoral immunity at a population level. Nat. Med. 2010 16 9 995 997 10.1038/nm.2203 20802498
    [Google Scholar]
  57. Mkhize N.N. Yssel A.E.J. Kaldine H. van Dorsten R.T. Woodward Davis A.S. Beaume N. Matten D. Lambson B. Modise T. Kgagudi P. York T. Westfall D.H. Giorgi E.E. Korber B. Anthony C. Mapengo R.E. Bekker V. Domin E. Eaton A. Deng W. DeCamp A. Huang Y. Gilbert P.B. Gwashu-Nyangiwe A. Thebus R. Ndabambi N. Mielke D. Mgodi N. Karuna S. Edupuganti S. Seaman M.S. Corey L. Cohen M.S. Hural J. McElrath M.J. Mullins J.I. Montefiori D. Moore P.L. Williamson C. Morris L. Neutralization profiles of HIV-1 viruses from the VRC01 Antibody Mediated Prevention (AMP) trials. PLoS Pathog. 2023 19 6 e1011469 10.1371/journal.ppat.1011469 37384759
    [Google Scholar]
  58. Wu X. Yang Z.Y. Li Y. Hogerkorp C.M. Schief W.R. Seaman M.S. Zhou T. Schmidt S.D. Wu L. Xu L. Longo N.S. McKee K. O’Dell S. Louder M.K. Wycuff D.L. Feng Y. Nason M. Doria-Rose N. Connors M. Kwong P.D. Roederer M. Wyatt R.T. Nabel G.J. Mascola J.R. Rational design of envelope identifies broadly neutralizing human monoclonal antibodies to HIV-1. Science 2010 329 5993 856 861 10.1126/science.1187659 20616233
    [Google Scholar]
  59. Zhou T. Georgiev I. Wu X. Yang Z.Y. Dai K. Finzi A. Do Kwon Y. Scheid J.F. Shi W. Xu L. Yang Y. Zhu J. Nussenzweig M.C. Sodroski J. Shapiro L. Nabel G.J. Mascola J.R. Kwong P.D. Structural basis for broad and potent neutralization of HIV-1 by antibody VRC01. Science 2010 329 5993 811 817 10.1126/science.1192819 20616231
    [Google Scholar]
  60. LaBranche C.C. McGuire A.T. Gray M.D. Behrens S. Zhou T. Sattentau Q.J. Peacock J. Eaton A. Greene K. Gao H. Tang H. Perez L.G. Saunders K.O. Mascola J.R. Haynes B.F. Stamatatos L. Montefiori D.C. Mascola J.R. Haynes B.F. Stamatatos L. Montefiori D.C. HIV-1 envelope glycan modifications that permit neutralization by germline-reverted VRC01-class broadly neutralizing antibodies. PLoS Pathog. 2018 14 11 e1007431 10.1371/journal.ppat.1007431 30395637
    [Google Scholar]
  61. Zhou T. Zhu J. Wu X. Moquin S. Zhang B. Acharya P. Georgiev I.S. Altae-Tran H.R. Chuang G.Y. Joyce M.G. Do Kwon Y. Longo N.S. Louder M.K. Luongo T. McKee K. Schramm C.A. Skinner J. Yang Y. Yang Z. Zhang Z. Zheng A. Bonsignori M. Haynes B.F. Scheid J.F. Nussenzweig M.C. Simek M. Burton D.R. Koff W.C. Mullikin J.C. Connors M. Shapiro L. Nabel G.J. Mascola J.R. Kwong P.D. Multidonor analysis reveals structural nlms, genetic determinants, and maturation pathway for HIV-1 neutralization by VRC01-class antibodies. Immunity 2013 39 2 245 258 10.1016/j.immuni.2013.04.012 23911655
    [Google Scholar]
  62. Bonsignori M. Scott E. Wiehe K. Easterhoff D. Alam S.M. Hwang K.K. Cooper M. Xia S.M. Zhang R. Montefiori D.C. Henderson R. Nie X. Kelsoe G. Moody M.A. Chen X. Joyce M.G. Kwong P.D. Connors M. Mascola J.R. McGuire A.T. Stamatatos L. Medina-Ramírez M. Sanders R.W. Saunders K.O. Kepler T.B. Haynes B.F. Inference of the HIV-1 VRC01 antibody lineage unmutated common ancestor reveals alternative pathways to overcome a key glycan barrier. Immunity 2018 49 6 1162 1174.e8 10.1016/j.immuni.2018.10.015 30552024
    [Google Scholar]
  63. McGuire A.T. Gray M.D. Dosenovic P. Gitlin A.D. Freund N.T. Petersen J. Correnti C. Johnsen W. Kegel R. Stuart A.B. Glenn J. Seaman M.S. Schief W.R. Strong R.K. Nussenzweig M.C. Stamatatos L. Specifically modified Env immunogens activate B-cell precursors of broadly neutralizing HIV-1 antibodies in transgenic mice. Nat. Commun. 2016 7 1 10618 10.1038/ncomms10618 26907590
    [Google Scholar]
  64. Parks K.R. MacCamy A.J. Trichka J. Gray M. Weidle C. Borst A.J. Khechaduri A. Takushi B. Agrawal P. Guenaga J. Wyatt R.T. Coler R. Seaman M. LaBranche C. Montefiori D.C. Veesler D. Pancera M. McGuire A. Stamatatos L. Overcoming steric restrictions of VRC01 HIV-1 neutralizing antibodies through immunization. Cell Rep. 2019 29 10 3060 3072.e7 10.1016/j.celrep.2019.10.071 31801073
    [Google Scholar]
  65. Medina-Ramírez M. Garces F. Escolano A. Skog P. de Taeye S.W. Del Moral-Sanchez I. McGuire A.T. Yasmeen A. Behrens A.J. Ozorowski G. van den Kerkhof T.L.G.M. Freund N.T. Dosenovic P. Hua Y. Gitlin A.D. Cupo A. van der Woude P. Golabek M. Sliepen K. Blane T. Kootstra N. van Breemen M.J. Pritchard L.K. Stanfield R.L. Crispin M. Ward A.B. Stamatatos L. Klasse P.J. Moore J.P. Nemazee D. Nussenzweig M.C. Wilson I.A. Sanders R.W. Design and crystal structure of a native-like HIV-1 envelope trimer that engages multiple broadly neutralizing antibody precursors in vivo. J. Exp. Med. 2017 214 9 2573 2590 10.1084/jem.20161160 28847869
    [Google Scholar]
  66. Caniels T.G. Medina-Ramìrez M. Zhang S. Kratochvil S. Xian Y. Koo J.H. Derking R. Samsel J. van Schooten J. Pecetta S. Lamperti E. Yuan M. Carrasco M.R. del Moral Sánchez I. Allen J.D. Bouhuijs J.H. Yasmeen A. Ketas T.J. Snitselaar J.L. Bijl T.P.L. Martin I.C. Torres J.L. Cupo A. Shirreff L. Rogers K. Mason R.D. Roederer M. Greene K.M. Gao H. Silva C.M. Baken I.J.L. Tian M. Alt F.W. Pulendran B. Seaman M.S. Crispin M. van Gils M.J. Montefiori D.C. McDermott A.B. Villinger F.J. Koup R.A. Moore J.P. Klasse P.J. Ozorowski G. Batista F.D. Wilson I.A. Ward A.B. Sanders R.W. Germline-targeting HIV vaccination induces neutralizing antibodies to the CD4 binding site. Sci. Immunol. 2024 9 98 eadk9550 10.1126/sciimmunol.adk9550 39213338
    [Google Scholar]
  67. Bonsignori M. Zhou T. Sheng Z. Chen L. Gao F. Joyce M.G. Ozorowski G. Chuang G.Y. Schramm C.A. Wiehe K. Alam S.M. Bradley T. Gladden M.A. Hwang K.K. Iyengar S. Kumar A. Lu X. Luo K. Mangiapani M.C. Parks R.J. Song H. Acharya P. Bailer R.T. Cao A. Druz A. Georgiev I.S. Kwon Y.D. Louder M.K. Zhang B. Zheng A. Hill B.J. Kong R. Soto C. Mullikin J.C. Douek D.C. Montefiori D.C. Moody M.A. Shaw G.M. Hahn B.H. Kelsoe G. Hraber P.T. Korber B.T. Boyd S.D. Fire A.Z. Kepler T.B. Shapiro L. Ward A.B. Mascola J.R. Liao H.X. Kwong P.D. Haynes B.F. Maturation pathway from germline to broad HIV-1 neutralizer of a CD4-mimic antibody. Cell 2016 165 2 449 463 10.1016/j.cell.2016.02.022 26949186
    [Google Scholar]
  68. LaBranche C.C. Henderson R. Hsu A. Behrens S. Chen X. Zhou T. Wiehe K. Saunders K.O. Alam S.M. Bonsignori M. Borgnia M.J. Sattentau Q.J. Eaton A. Greene K. Gao H. Liao H.X. Williams W.B. Peacock J. Tang H. Perez L.G. Edwards R.J. Kepler T.B. Korber B.T. Kwong P.D. Mascola J.R. Acharya P. Haynes B.F. Montefiori D.C. Neutralization-guided design of HIV-1 envelope trimers with high affinity for the unmutated common ancestor of CH235 lineage CD4bs broadly neutralizing antibodies. PLoS Pathog. 2019 15 9 e1008026 10.1371/journal.ppat.1008026 31527908
    [Google Scholar]
  69. Saunders K.O. Counts J. Thakur B. Stalls V. Edwards R. Manne K. Lu X. Mansouri K. Chen Y. Parks R. Barr M. Sutherland L. Bal J. Havill N. Chen H. Machiele E. Jamieson N. Hora B. Kopp M. Janowska K. Anasti K. Jiang C. Van Itallie E. Venkatayogi S. Eaton A. Henderson R. Barbosa C. Alam S.M. Santra S. Weissman D. Moody M.A. Cain D.W. Tam Y.K. Lewis M. Williams W.B. Wiehe K. Montefiori D.C. Acharya P. Haynes B.F. Vaccine induction of CD4-mimicking HIV-1 broadly neutralizing antibody precursors in macaques. Cell 2024 187 1 79 94.e24 10.1016/j.cell.2023.12.002 38181743
    [Google Scholar]
  70. Liao H.X. Lynch R. Zhou T. Gao F. Alam S.M. Boyd S.D. Fire A.Z. Roskin K.M. Schramm C.A. Zhang Z. Zhu J. Shapiro L. Mullikin J.C. Gnanakaran S. Hraber P. Wiehe K. Kelsoe G. Yang G. Xia S.M. Montefiori D.C. Parks R. Lloyd K.E. Scearce R.M. Soderberg K.A. Cohen M. Kamanga G. Louder M.K. Tran L.M. Chen Y. Cai F. Chen S. Moquin S. Du X. Joyce M.G. Srivatsan S. Zhang B. Zheng A. Shaw G.M. Hahn B.H. Kepler T.B. Korber B.T.M. Kwong P.D. Mascola J.R. Haynes B.F. Co-evolution of a broadly neutralizing HIV-1 antibody and founder virus. Nature 2013 496 7446 469 476 10.1038/nature12053 23552890
    [Google Scholar]
  71. Bonsignori M. Kreider E.F. Fera D. Meyerhoff R.R. Bradley T. Wiehe K. Alam S.M. Aussedat B. Walkowicz W.E. Hwang K.K. Saunders K.O. Zhang R. Gladden M.A. Monroe A. Kumar A. Xia S.M. Cooper M. Louder M.K. McKee K. Bailer R.T. Pier B.W. Jette C.A. Kelsoe G. Williams W.B. Morris L. Kappes J. Wagh K. Kamanga G. Cohen M.S. Hraber P.T. Montefiori D.C. Trama A. Liao H.X. Kepler T.B. Moody M.A. Gao F. Danishefsky S.J. Mascola J.R. Shaw G.M. Hahn B.H. Harrison S.C. Korber B.T. Haynes B.F. Staged induction of HIV-1 glycan–dependent broadly neutralizing antibodies. Sci. Transl. Med. 2017 9 381 eaai7514 10.1126/scitranslmed.aai7514 28298420
    [Google Scholar]
  72. Tomaras G.D. Yates N.L. Liu P. Qin L. Fouda G.G. Chavez L.L. Decamp A.C. Parks R.J. Ashley V.C. Lucas J.T. Cohen M. Eron J. Hicks C.B. Liao H.X. Self S.G. Landucci G. Forthal D.N. Weinhold K.J. Keele B.F. Hahn B.H. Greenberg M.L. Morris L. Karim S.S.A. Blattner W.A. Montefiori D.C. Shaw G.M. Perelson A.S. Haynes B.F. Initial B-cell responses to transmitted human immunodeficiency virus type 1: virion-binding immunoglobulin M (IgM) and IgG antibodies followed by plasma anti-gp41 antibodies with ineffective control of initial viremia. J. Virol. 2008 82 24 12449 12463 10.1128/JVI.01708‑08 18842730
    [Google Scholar]
  73. Yates N.L. deCamp A.C. Korber B.T. Liao H.X. Irene C. Pinter A. Peacock J. Harris L.J. Sawant S. Hraber P. Shen X. Rerks-Ngarm S. Pitisuttithum P. Nitayapan S. Berman P.W. Robb M.L. Pantaleo G. Zolla-Pazner S. Haynes B.F. Alam S.M. Montefiori D.C. Tomaras G.D. HIV-1 envelope glycoproteins from diverse clades differentiate antibody responses and durability among vaccinees. J. Virol. 2018 92 8 e01843-17 10.1128/JVI.01843‑17 29386288
    [Google Scholar]
  74. Shen X. Dennison S.M. Liu P. Gao F. Jaeger F. Montefiori D.C. Verkoczy L. Haynes B.F. Alam S.M. Tomaras G.D. Prolonged exposure of the HIV-1 gp41 membrane proximal region with L669S substitution. Proc. Natl. Acad. Sci. USA 2010 107 13 5972 5977 10.1073/pnas.0912381107 20231447
    [Google Scholar]
  75. Shen X. Parks R.J. Montefiori D.C. Kirchherr J.L. Keele B.F. Decker J.M. Blattner W.A. Gao F. Weinhold K.J. Hicks C.B. Greenberg M.L. Hahn B.H. Shaw G.M. Haynes B.F. Tomaras G.D. in vivo gp41 antibodies targeting the 2F5 monoclonal antibody epitope mediate human immunodeficiency virus type 1 neutralization breadth. J. Virol. 2009 83 8 3617 3625 10.1128/JVI.02631‑08 19193787
    [Google Scholar]
  76. Moyo-Gwete T. Scheepers C. Makhado Z. Kgagudi P. Mzindle N.B. Ziki R. Madzorera S. Manamela N.P. Ayres F. Lambson B.E. Richardson S.I. Morris L. Moore P.L. Enhanced neutralization potency of an identical HIV neutralizing antibody expressed as different isotypes is achieved through genetically distinct mechanisms. Sci. Rep. 2022 12 1 16473 10.1038/s41598‑022‑20141‑7 36182959
    [Google Scholar]
  77. Scheepers C. Richardson S.I. Moyo-Gwete T. Moore P.L. Antibody class-switching as a strategy to improve HIV-1 neutralization. Trends Mol. Med. 2022 28 11 979 988 10.1016/j.molmed.2022.08.010 36117072
    [Google Scholar]
  78. Scheepers C. Bekker V. Anthony C. Richardson S.I. Oosthuysen B. Moyo T. Kgagudi P. Kitchin D. Nonyane M. York T. Mielke D. Mabvakure B.M. Sheng Z. Lambson B.E. Ismail A. Garrett N.J. Abdool Karim S.S. Shapiro L. Williamson C. Morris L. Moore P.L. Antibody isotype switching as a mechanism to counter HIV neutralization escape. Cell Rep. 2020 33 8 108430 10.1016/j.celrep.2020.108430 33238131
    [Google Scholar]
  79. Yates N.L. Liao H.X. Fong Y. deCamp A. Vandergrift N.A. Williams W.T. Alam S.M. Ferrari G. Yang Z. Seaton K.E. Berman P.W. Alpert M.D. Evans D.T. O’Connell R.J. Francis D. Sinangil F. Lee C. Nitayaphan S. Rerks-Ngarm S. Kaewkungwal J. Pitisuttithum P. Tartaglia J. Pinter A. Zolla-Pazner S. Gilbert P.B. Nabel G.J. Michael N.L. Kim J.H. Montefiori D.C. Haynes B.F. Tomaras G.D. Vaccine-induced Env V1-V2 IgG3 correlates with lower HIV-1 infection risk and declines soon after vaccination. Sci. Transl. Med. 2014 6 228 228ra39 10.1126/scitranslmed.3007730 24648342
    [Google Scholar]
  80. Chung A.W. Kumar M.P. Arnold K.B. Yu W.H. Schoen M.K. Dunphy L.J. Suscovich T.J. Frahm N. Linde C. Mahan A.E. Hoffner M. Streeck H. Ackerman M.E. McElrath M.J. Schuitemaker H. Pau M.G. Baden L.R. Kim J.H. Michael N.L. Barouch D.H. Lauffenburger D.A. Alter G. Dissecting polyclonal vaccine-induced humoral immunity against HIV using systems serology. Cell 2015 163 4 988 998 10.1016/j.cell.2015.10.027 26544943
    [Google Scholar]
  81. Nyanhete T.E. Edwards R.J. LaBranche C.C. Mansouri K. Eaton A. Dennison S.M. Saunders K.O. Goodman D. Janowska K. Spreng R.L. Zhang L. Mudrak S.V. Hope T.J. Hora B. Bradley T. Georgiev I.S. Montefiori D.C. Acharya P. Tomaras G.D. Polyclonal broadly neutralizing antibody activity characterized by CD4 binding site and V3-glycan antibodies in a subset of HIV-1 virus controllers. Front. Immunol. 2021 12 670561 10.3389/fimmu.2021.670561 35003053
    [Google Scholar]
  82. Li K. Dodds M. Spreng R.L. Abraha M. Huntwork R.H.C. Dahora L.C. Nyanhete T. Dutta S. Wille-Reece U. Jongert E. Ewer K.J. Hill A.V.S. Jin C. Hill J. Pollard A.J. Munir Alam S. Tomaras G.D. Dennison S.M. A tool for evaluating heterogeneity in avidity of polyclonal antibodies. Front. Immunol. 2023 14 1049673 10.3389/fimmu.2023.1049673 36875126
    [Google Scholar]
  83. Seaton K.E. Huang Y. Karuna S. Heptinstall J.R. Brackett C. Chiong K. Zhang L. Yates N.L. Sampson M. Rudnicki E. Juraska M. deCamp A.C. Edlefsen P.T. Mullins J.I. Williamson C. Rossenkhan R. Giorgi E.E. Kenny A. Angier H. Randhawa A. Weiner J.A. Rojas M. Sarzotti-Kelsoe M. Zhang L. Sawant S. Ackerman M.E. McDermott A.B. Mascola J.R. Hural J. McElrath M.J. Andrew P. Hidalgo J.A. Clark J. Laher F. Orrell C. Frank I. Gonzales P. Edupuganti S. Mgodi N. Corey L. Morris L. Montefiori D. Cohen M.S. Gilbert P.B. Tomaras G.D. Pharmacokinetic serum concentrations of VRC01 correlate with prevention of HIV-1 acquisition. EBioMedicine 2023 93 104590 10.1016/j.ebiom.2023.104590 37300931
    [Google Scholar]
  84. Huang Y. Zhang L. Eaton A. Mkhize N.N. Carpp L.N. Rudnicki E. DeCamp A. Juraska M. Randhawa A. McDermott A. Ledgerwood J. Andrew P. Karuna S. Edupuganti S. Mgodi N. Cohen M. Corey L. Mascola J. Gilbert P.B. Morris L. Montefiori D.C. Prediction of serum HIV-1 neutralization titers of VRC01 in HIV-uninfected Antibody Mediated Prevention (AMP) trial participants. Hum. Vaccin. Immunother. 2022 18 1 1908030 10.1080/21645515.2021.1908030 34213402
    [Google Scholar]
  85. Huang Y. Zhang Y. Bailer R. Grunenberg N. Carpp L.N. Seaton K. Mayer K.H. Ledgerwood J. Corey L. Mascola J. Montefiori D. Gilbert P.B. Brief report: Prediction of serum HIV-1 neutralization titers after passive administration of VRC01. J. Acquir. Immune Defic. Syndr. 2020 83 4 434 439 10.1097/QAI.0000000000002272 31855881
    [Google Scholar]
  86. Walsh S.R. Gay C.L. Karuna S.T. Hyrien O. Skalland T. Mayer K.H. Sobieszczyk M.E. Baden L.R. Goepfert P.A. del Rio C. Pantaleo G. Andrew P. Karg C. He Z. Lu H. Paez C.A. Baumblatt J.A.G. Polakowski L.L. Chege W. Anderson M.A. Janto S. Han X. Huang Y. Dumond J. Ackerman M.E. McDermott A.B. Flach B. Piwowar-Manning E. Seaton K. Tomaras G.D. Montefiori D.C. Gama L. Mascola J.R. Safety and pharmacokinetics of VRC07-523LS administered via different routes and doses (HVTN 127/HPTN 087): A phase I randomized clinical trial. PLoS Med. 2024 21 6 e1004329 10.1371/journal.pmed.1004329 38913710
    [Google Scholar]
  87. Sobieszczyk M.E. Mannheimer S. Paez C.A. Yu C. Gamble T. Theodore D.A. Chege W. Yacovone M. Hanscom B. Heptinstall J. Seaton K.E. Zhang L. Miner M.D. Eaton A. Weiner J.A. Mayer K. Kalams S. Stephenson K. Julg B. Caskey M. Nussenzweig M. Gama L. Barouch D.H. Ackerman M.E. Tomaras G.D. Huang Y. Montefiori D. Safety, tolerability, pharmacokinetics, and immunological activity of dual-combinations and triple-combinations of anti-HIV monoclonal antibodies PGT121, PGDM1400, 10-1074, and VRC07-523LS administered intravenously to HIV-uninfected adults: A phase 1 randomised trial. Lancet HIV 2023 10 10 e653 e662 10.1016/S2352‑3018(23)00140‑6 37802566
    [Google Scholar]
  88. Song S. Yang L. Trepicchio W.L. Wyant T. Understanding the supersensitive anti-drug antibody assay: Unexpected high anti-drug antibody incidence and its clinical relevance. J. Immunol. Res. 2016 2016 1 8 10.1155/2016/3072586 27340678
    [Google Scholar]
  89. Bharadwaj P. Riekofski C. Lin S. Seaman M.S. Garber D.A. Montefiori D. Sarzotti-Kelsoe M. Ackerman M.E. Weiner J.A. Implementation of a three-tiered approach to identify and characterize anti-drug antibodies raised against HIV-specific broadly neutralizing antibodies. J. Immunol. Methods 2020 479 112764 10.1016/j.jim.2020.112764 32070674
    [Google Scholar]
  90. Seaman M.S. Bilska M. Ghantous F. Eaton A. LaBranche C.C. Greene K. Gao H. Weiner J.A. Ackerman M.E. Garber D.A. Rosenberg Y.J. Sarzotti-Kelsoe M. Montefiori D.C. Optimization and qualification of a functional anti-drug antibody assay for HIV-1 bnAbs. J. Immunol. Methods 2020 479 112736 10.1016/j.jim.2020.112736 31917969
    [Google Scholar]
  91. Westfall D.H. Deng W. Pankow A. Murrell H. Chen L. Zhao H. Williamson C. Rolland M. Murrell B. Mullins J.I. Optimized SMRT-UMI protocol produces highly accurate sequence datasets from diverse populations: Application to HIV-1 quasispecies. Virus Evol. 2024 10 1 veae019 10.1093/ve/veae019 38765465
    [Google Scholar]
  92. Juraska M. Bai H. deCamp A.C. Magaret C.A. Li L. Gillespie K. Carpp L.N. Giorgi E.E. Ludwig J. Molitor C. Hudson A. Williamson B.D. Espy N. Simpkins B. Rudnicki E. Shao D. Rossenkhan R. Edlefsen P.T. Westfall D.H. Deng W. Chen L. Zhao H. Bhattacharya T. Pankow A. Murrell B. Yssel A. Matten D. York T. Beaume N. Gwashu-Nyangiwe A. Ndabambi N. Thebus R. Karuna S.T. Morris L. Montefiori D.C. Hural J.A. Cohen M.S. Corey L. Rolland M. Gilbert P.B. Williamson C. Mullins J.I. Prevention efficacy of the broadly neutralizing antibody VRC01 depends on HIV-1 envelope sequence features. Proc. Natl. Acad. Sci. USA 2024 121 4 e2308942121 10.1073/pnas.2308942121 38241441
    [Google Scholar]
  93. Bar-On Y. Gruell H. Schoofs T. Pai J.A. Nogueira L. Butler A.L. Millard K. Lehmann C. Suárez I. Oliveira T.Y. Karagounis T. Cohen Y.Z. Wyen C. Scholten S. Handl L. Belblidia S. Dizon J.P. Vehreschild J.J. Witmer-Pack M. Shimeliovich I. Jain K. Fiddike K. Seaton K.E. Yates N.L. Horowitz J. Gulick R.M. Pfeifer N. Tomaras G.D. Seaman M.S. Fätkenheuer G. Caskey M. Klein F. Nussenzweig M.C. Safety and antiviral activity of combination HIV-1 broadly neutralizing antibodies in viremic individuals. Nat. Med. 2018 24 11 1701 1707 10.1038/s41591‑018‑0186‑4 30258217
    [Google Scholar]
  94. Capparelli E.V. Ajibola G. Maswabi K. Holme M.P. Bennett K. Powis K.M. Moyo S. Mohammed T. Maphorisa C. Hughes M.D. Seaton K.E. Tomaras G.D. Mosher S. Taylor A. O’Connell S. Narpala S. Mcdermott A. Caskey M. Gama L. Lockman S. Jean-Philippe P. Makhema J. Kuritzkes D.R. Lichterfeld M. Shapiro R.L. Safety and pharmacokinetics of intravenous 10-1074 and VRC01LS in young children. J. Acquir. Immune Defic. Syndr. 2022 91 2 182 188 10.1097/QAI.0000000000003033 36094485
    [Google Scholar]
  95. Cohen Y.Z. Butler A.L. Millard K. Witmer-Pack M. Levin R. Unson-O’Brien C. Patel R. Shimeliovich I. Lorenzi J.C.C. Horowitz J. Walsh S.R. Lin S. Weiner J.A. Tse A. Sato A. Bennett C. Mayer B. Seaton K.E. Yates N.L. Baden L.R. deCamp A.C. Ackerman M.E. Seaman M.S. Tomaras G.D. Nussenzweig M.C. Caskey M. Safety, pharmacokinetics, and immunogenicity of the combination of the broadly neutralizing anti-HIV-1 antibodies 3BNC117 and 10-1074 in healthy adults: A randomized, phase 1 study. PLoS One 2019 14 8 e0219142 10.1371/journal.pone.0219142 31393868
    [Google Scholar]
  96. Julg B. Stephenson K.E. Wagh K. Tan S.C. Zash R. Walsh S. Ansel J. Kanjilal D. Nkolola J. Walker-Sperling V.E.K. Ophel J. Yanosick K. Borducchi E.N. Maxfield L. Abbink P. Peter L. Yates N.L. Wesley M.S. Hassell T. Gelderblom H.C. deCamp A. Mayer B.T. Sato A. Gerber M.W. Giorgi E.E. Gama L. Koup R.A. Mascola J.R. Monczor A. Lupo S. Rolle C.P. Arduino R. DeJesus E. Tomaras G.D. Seaman M.S. Korber B. Barouch D.H. Safety and antiviral activity of triple combination broadly neutralizing monoclonal antibody therapy against HIV-1: A phase 1 clinical trial. Nat. Med. 2022 28 6 1288 1296 10.1038/s41591‑022‑01815‑1 35551291
    [Google Scholar]
  97. Kerwin B.A. Bennett C. Brodsky Y. Clark R. Floyd J.A. Gillespie A. Mayer B.T. McClure M. Siska C. Seaman M.S. Seaton K.E. Shaver J. Tomaras G.D. Yates N.L. Ketchem R.R. Framework mutations of the 10-1074 bnAb increase conformational stability, manufacturability, and stability while preserving full neutralization activity. J. Pharm. Sci. 2020 109 1 233 246 10.1016/j.xphs.2019.07.009 31348937
    [Google Scholar]
  98. Mayer K.H. Seaton K.E. Huang Y. Grunenberg N. Isaacs A. Allen M. Ledgerwood J.E. Frank I. Sobieszczyk M.E. Baden L.R. Rodriguez B. Van Tieu H. Tomaras G.D. Deal A. Goodman D. Bailer R.T. Ferrari G. Jensen R. Hural J. Graham B.S. Mascola J.R. Corey L. Montefiori D.C. Safety, pharmacokinetics, and immunological activities of multiple intravenous or subcutaneous doses of an anti-HIV monoclonal antibody, VRC01, administered to HIV-uninfected adults: Results of a phase 1 randomized trial. PLoS Med. 2017 14 11 e1002435 10.1371/journal.pmed.1002435 29136037
    [Google Scholar]
  99. Mendoza P. Gruell H. Nogueira L. Pai J.A. Butler A.L. Millard K. Lehmann C. Suárez I. Oliveira T.Y. Lorenzi J.C.C. Cohen Y.Z. Wyen C. Kümmerle T. Karagounis T. Lu C.L. Handl L. Unson-O’Brien C. Patel R. Ruping C. Schlotz M. Witmer-Pack M. Shimeliovich I. Kremer G. Thomas E. Seaton K.E. Horowitz J. West A.P. Jr Bjorkman P.J. Tomaras G.D. Gulick R.M. Pfeifer N. Fätkenheuer G. Seaman M.S. Klein F. Caskey M. Nussenzweig M.C. Combination therapy with anti-HIV-1 antibodies maintains viral suppression. Nature 2018 561 7724 479 484 10.1038/s41586‑018‑0531‑2 30258136
    [Google Scholar]
  100. Stephenson K.E. Julg B. Tan C.S. Zash R. Walsh S.R. Rolle C.P. Monczor A.N. Lupo S. Gelderblom H.C. Ansel J.L. Kanjilal D.G. Maxfield L.F. Nkolola J. Borducchi E.N. Abbink P. Liu J. Peter L. Chandrashekar A. Nityanandam R. Lin Z. Setaro A. Sapiente J. Chen Z. Sunner L. Cassidy T. Bennett C. Sato A. Mayer B. Perelson A.S. deCamp A. Priddy F.H. Wagh K. Giorgi E.E. Yates N.L. Arduino R.C. DeJesus E. Tomaras G.D. Seaman M.S. Korber B. Barouch D.H. Safety, pharmacokinetics and antiviral activity of PGT121, a broadly neutralizing monoclonal antibody against HIV-1: A randomized, placebo-controlled, phase 1 clinical trial. Nat. Med. 2021 27 10 1718 1724 10.1038/s41591‑021‑01509‑0 34621054
    [Google Scholar]
  101. Wesley M.S. Chiong K.T. Seaton K.E. Arocena C.A. Sawant S. Hare J. Hernandez K. Rojas M. Heptinstall J. Beaumont D. Crisafi K. Nkolola J. Barouch D.H. Sarzotti-Kelsoe M. Tomaras G.D. Yates N.L. Validation of a triplex pharmacokinetic assay for simultaneous quantitation of HIV-1 broadly neutralizing antibodies PGT121, PGDM1400, and VRC07-523-LS. Front. Immunol. 2021 12 709994 10.3389/fimmu.2021.709994 34504492
    [Google Scholar]
  102. Wang P. Gajjar M.R. Yu J. Padte N.N. Gettie A. Blanchard J.L. Russell-Lodrigue K. Liao L.E. Perelson A.S. Huang Y. Ho D.D. Quantifying the contribution of Fc-mediated effector functions to the antiviral activity of anti–HIV-1 IgG1 antibodies in vivo. Proc. Natl. Acad. Sci. USA 2020 117 30 18002 18009 10.1073/pnas.2008190117 32665438
    [Google Scholar]
  103. Asokan M. Dias J. Liu C. Maximova A. Ernste K. Pegu A. McKee K. Shi W. Chen X. Almasri C. Promsote W. Ambrozak D.R. Gama L. Hu J. Douek D.C. Todd J.P. Lifson J.D. Fourati S. Sekaly R.P. Crowley A.R. Ackerman M.E. Ko S.H. Kilam D. Boritz E.A. Liao L.E. Best K. Perelson A.S. Mascola J.R. Koup R.A. Fc-mediated effector function contributes to the in vivo antiviral effect of an HIV neutralizing antibody. Proc. Natl. Acad. Sci. USA 2020 117 31 18754 18763 10.1073/pnas.2008236117 32690707
    [Google Scholar]
  104. Bournazos S. Klein F. Pietzsch J. Seaman M.S. Nussenzweig M.C. Ravetch J.V. Broadly neutralizing anti-HIV-1 antibodies require Fc effector functions for in vivo activity. Cell 2014 158 6 1243 1253 10.1016/j.cell.2014.08.023 25215485
    [Google Scholar]
  105. Bradley T. Pollara J. Santra S. Vandergrift N. Pittala S. Bailey-Kellogg C. Shen X. Parks R. Goodman D. Eaton A. Balachandran H. Mach L.V. Saunders K.O. Weiner J.A. Scearce R. Sutherland L.L. Phogat S. Tartaglia J. Reed S.G. Hu S.L. Theis J.F. Pinter A. Montefiori D.C. Kepler T.B. Peachman K.K. Rao M. Michael N.L. Suscovich T.J. Alter G. Ackerman M.E. Moody M.A. Liao H.X. Tomaras G. Ferrari G. Korber B.T. Haynes B.F. Pentavalent HIV-1 vaccine protects against simian-human immunodeficiency virus challenge. Nat. Commun. 2017 8 1 15711 10.1038/ncomms15711 28593989
    [Google Scholar]
  106. Santra S. Tomaras G.D. Warrier R. Nicely N.I. Liao H.X. Pollara J. Liu P. Alam S.M. Zhang R. Cocklin S.L. Shen X. Duffy R. Xia S.M. Schutte R.J. Pemble C.W. IV Dennison S.M. Li H. Chao A. Vidnovic K. Evans A. Klein K. Kumar A. Robinson J. Landucci G. Forthal D.N. Montefiori D.C. Kaewkungwal J. Nitayaphan S. Pitisuttithum P. Rerks-Ngarm S. Robb M.L. Michael N.L. Kim J.H. Soderberg K.A. Giorgi E.E. Blair L. Korber B.T. Moog C. Shattock R.J. Letvin N.L. Schmitz J.E. Moody M.A. Gao F. Ferrari G. Shaw G.M. Haynes B.F. Human non-neutralizing HIV-1 envelope monoclonal antibodies limit the number of founder viruses during SHIV mucosal infection in Rhesus Macaques. PLoS Pathog. 2015 11 8 e1005042 10.1371/journal.ppat.1005042 26237403
    [Google Scholar]
  107. Tuyishime M. Garrido C. Jha S. Moeser M. Mielke D. LaBranche C. Montefiori D. Haynes B.F. Joseph S. Margolis D.M. Ferrari G. Improved killing of HIV-infected cells using three neutralizing and non-neutralizing antibodies. J. Clin. Invest. 2020 130 10 5157 5170 10.1172/JCI135557 32584790
    [Google Scholar]
  108. Sneller M.C. Blazkova J. Justement J.S. Shi V. Kennedy B.D. Gittens K. Tolstenko J. McCormack G. Whitehead E.J. Schneck R.F. Proschan M.A. Benko E. Kovacs C. Oguz C. Seaman M.S. Caskey M. Nussenzweig M.C. Fauci A.S. Moir S. Chun T.W. Combination anti-HIV antibodies provide sustained virological suppression. Nature 2022 606 7913 375 381 10.1038/s41586‑022‑04797‑9 35650437
    [Google Scholar]
  109. Margolis D.M. Koup R.A. Ferrari G. HIV antibodies for treatment of HIV infection Immunol. Rev. 2017 275 1 313 323 10.1111/imr.12506 28133794
    [Google Scholar]
  110. Pollara J Hart L Brewer F Pickeral J Packard BZ Hoxie JA Komoriya A Ochsenbauer C Kappes JC Roederer M Huang Y Weinhold KJ Tomaras GD Haynes BF Montefiori DC Ferrari G High-throughput quantitative analysis of HIV-1 and SIV-specific ADCC-mediating antibody responses. Cytometry 2011 79 8 603 10.1002/cyto.a.21084
    [Google Scholar]
  111. Felber B.K. Lu Z. Hu X. Valentin A. Rosati M. Remmel C.A.L. Weiner J.A. Carpenter M.C. Faircloth K. Stanfield-Oakley S. Williams W.B. Shen X. Tomaras G.D. LaBranche C.C. Montefiori D. Trinh H.V. Rao M. Alam M.S. Vandergrift N.A. Saunders K.O. Wang Y. Rountree W. Das J. Alter G. Reed S.G. Aye P.P. Schiro F. Pahar B. Dufour J.P. Veazey R.S. Marx P.A. Venzon D.J. Shaw G.M. Ferrari G. Ackerman M.E. Haynes B.F. Pavlakis G.N. Co-immunization of DNA and protein in the same anatomical sites induces superior protective immune responses against SHIV challenge. Cell Rep. 2020 31 6 107624 10.1016/j.celrep.2020.107624 32402293
    [Google Scholar]
  112. Pollara J. Bonsignori M. Moody M.A. Liu P. Alam S.M. Hwang K.K. Gurley T.C. Kozink D.M. Armand L.C. Marshall D.J. Whitesides J.F. Kaewkungwal J. Nitayaphan S. Pitisuttithum P. Rerks-Ngarm S. Robb M.L. O’Connell R.J. Kim J.H. Michael N.L. Montefiori D.C. Tomaras G.D. Liao H.X. Haynes B.F. Ferrari G. HIV-1 vaccine-induced C1 and V2 Env-specific antibodies synergize for increased antiviral activities. J. Virol. 2014 88 14 7715 7726 10.1128/JVI.00156‑14 24807721
    [Google Scholar]
  113. Bonsignori M. Pollara J. Moody M.A. Alpert M.D. Chen X. Hwang K.K. Gilbert P.B. Huang Y. Gurley T.C. Kozink D.M. Marshall D.J. Whitesides J.F. Tsao C.Y. Kaewkungwal J. Nitayaphan S. Pitisuttithum P. Rerks-Ngarm S. Kim J.H. Michael N.L. Tomaras G.D. Montefiori D.C. Lewis G.K. DeVico A. Evans D.T. Ferrari G. Liao H.X. Haynes B.F. Antibody-dependent cellular cytotoxicity-mediating antibodies from an HIV-1 vaccine efficacy trial target multiple epitopes and preferentially use the VH1 gene family. J. Virol. 2012 86 21 11521 11532 10.1128/JVI.01023‑12 22896626
    [Google Scholar]
  114. Liao H.X. Bonsignori M. Alam S.M. McLellan J.S. Tomaras G.D. Moody M.A. Kozink D.M. Hwang K.K. Chen X. Tsao C.Y. Liu P. Lu X. Parks R.J. Montefiori D.C. Ferrari G. Pollara J. Rao M. Peachman K.K. Santra S. Letvin N.L. Karasavvas N. Yang Z.Y. Dai K. Pancera M. Gorman J. Wiehe K. Nicely N.I. Rerks-Ngarm S. Nitayaphan S. Kaewkungwal J. Pitisuttithum P. Tartaglia J. Sinangil F. Kim J.H. Michael N.L. Kepler T.B. Kwong P.D. Mascola J.R. Nabel G.J. Pinter A. Zolla-Pazner S. Haynes B.F. Vaccine induction of antibodies against a structurally heterogeneous site of immune pressure within HIV-1 envelope protein variable regions 1 and 2. Immunity 2013 38 1 176 186 10.1016/j.immuni.2012.11.011 23313589
    [Google Scholar]
  115. Easterhoff D. Pollara J. Luo K. Tolbert W.D. Young B. Mielke D. Jha S. O’Connell R.J. Vasan S. Kim J. Michael N.L. Excler J.L. Robb M.L. Rerks-Ngarm S. Kaewkungwal J. Pitisuttithum P. Nitayaphan S. Sinangil F. Tartaglia J. Phogat S. Kepler T.B. Alam S.M. Wiehe K. Saunders K.O. Montefiori D.C. Tomaras G.D. Moody M.A. Pazgier M. Haynes B.F. Ferrari G. Boosting with AIDSVAX B/E enhances Env constant region 1 and 2 antibody-dependent cellular cytotoxicity breadth and potency. J. Virol. 2020 94 4 e01120-19 10.1128/JVI.01120‑19 31776278
    [Google Scholar]
  116. Fisher L. Zinter M. Stanfield-Oakley S. Carpp L.N. Edwards R.W. Denny T. Moodie Z. Laher F. Bekker L.G. McElrath M.J. Gilbert P.B. Corey L. Tomaras G. Pollara J. Ferrari G. Vaccine-induced antibodies mediate higher antibody-dependent cellular cytotoxicity after interleukin-15 pretreatment of natural killer effector cells. Front. Immunol. 2019 10 2741 10.3389/fimmu.2019.02741 31827470
    [Google Scholar]
  117. Mielke D. Stanfield-Oakley S. Borate B. Fisher L.H. Faircloth K. Tuyishime M. Greene K. Gao H. Williamson C. Morris L. Ochsenbauer C. Tomaras G. Haynes B.F. Montefiori D. Pollara J. deCamp A.C. Ferrari G. Selection of HIV envelope strains for standardized assessments of vaccine-elicited antibody-dependent cellular cytotoxicity-mediating antibodies. J. Virol. 2022 96 2 e01643-21 10.1128/JVI.01643‑21 34730393
    [Google Scholar]
  118. Dieter Mielke E.E.G. A higher proportion of recent compared to historic HIV viruses are resistant to antibody dependent cellular cytotoxicity mediated by monoclonal antibodies. J. Int. AIDS Soc. 2024 Oct;27 Suppl 5 Suppl 5 e26351 10.1002/jia2.26351
    [Google Scholar]
  119. Ackerman M.E. Das J. Pittala S. Broge T. Linde C. Suscovich T.J. Brown E.P. Bradley T. Natarajan H. Lin S. Sassic J.K. O’Keefe S. Mehta N. Goodman D. Sips M. Weiner J.A. Tomaras G.D. Haynes B.F. Lauffenburger D.A. Bailey-Kellogg C. Roederer M. Alter G. Route of immunization defines multiple mechanisms of vaccine-mediated protection against SIV. Nat. Med. 2018 24 10 1590 1598 10.1038/s41591‑018‑0161‑0 30177821
    [Google Scholar]
  120. Barouch D.H. Alter G. Broge T. Linde C. Ackerman M.E. Brown E.P. Borducchi E.N. Smith K.M. Nkolola J.P. Liu J. Shields J. Parenteau L. Whitney J.B. Abbink P. Ng’ang’a D.M. Seaman M.S. Lavine C.L. Perry J.R. Li W. Colantonio A.D. Lewis M.G. Chen B. Wenschuh H. Reimer U. Piatak M. Lifson J.D. Handley S.A. Virgin H.W. Koutsoukos M. Lorin C. Voss G. Weijtens M. Pau M.G. Schuitemaker H. Protective efficacy of adenovirus/protein vaccines against SIV challenges in rhesus monkeys. Science 2015 349 6245 320 324 10.1126/science.aab3886 26138104
    [Google Scholar]
  121. Li S.S. Gilbert P.B. Tomaras G.D. Kijak G. Ferrari G. Thomas R. Pyo C.W. Zolla-Pazner S. Montefiori D. Liao H.X. Nabel G. Pinter A. Evans D.T. Gottardo R. Dai J.Y. Janes H. Morris D. Fong Y. Edlefsen P.T. Li F. Frahm N. Alpert M.D. Prentice H. Rerks-Ngarm S. Pitisuttithum P. Kaewkungwal J. Nitayaphan S. Robb M.L. O’Connell R.J. Haynes B.F. Michael N.L. Kim J.H. McElrath M.J. Geraghty D.E. FCGR2C polymorphisms associate with HIV-1 vaccine protection in RV144 trial. J. Clin. Invest. 2014 124 9 3879 3890 10.1172/JCI75539 25105367
    [Google Scholar]
  122. Li S.S. Gilbert P.B. Carpp L.N. Pyo C.W. Janes H. Fong Y. Shen X. Neidich S.D. Goodman D. deCamp A. Cohen K.W. Ferrari G. Hammer S.M. Sobieszczyk M.E. Mulligan M.J. Buchbinder S.P. Keefer M.C. DeJesus E. Novak R.M. Frank I. McElrath M.J. Tomaras G.D. Geraghty D.E. Peng X. Fc gamma receptor polymorphisms modulated the vaccine effect on HIV-1 risk in the HVTN 505 HIV vaccine trial. J. Virol. 2019 93 21 e02041-18 10.1128/JVI.02041‑18 31434737
    [Google Scholar]
  123. Boesch A.W. Brown E.P. Cheng H.D. Ofori M.O. Normandin E. Nigrovic P.A. Alter G. Ackerman M.E. Highly parallel characterization of IgG Fc binding interactions. MAbs 2014 6 4 915 927 10.4161/mabs.28808 24927273
    [Google Scholar]
  124. Brown E.P. Dowell K.G. Boesch A.W. Normandin E. Mahan A.E. Chu T. Barouch D.H. Bailey-Kellogg C. Alter G. Ackerman M.E. Multiplexed Fc array for evaluation of antigen-specific antibody effector profiles. J. Immunol. Methods 2017 443 33 44 10.1016/j.jim.2017.01.010 28163018
    [Google Scholar]
  125. Brown E.P. Weiner J.A. Lin S. Natarajan H. Normandin E. Barouch D.H. Alter G. Sarzotti-Kelsoe M. Ackerman M.E. Optimization and qualification of an Fc Array assay for assessments of antibodies against HIV-1/SIV. J. Immunol. Methods 2018 455 24 33 10.1016/j.jim.2018.01.013 29395167
    [Google Scholar]
  126. Yates N.L. Stacey A.R. Nolen T.L. Vandergrift N.A. Moody M.A. Montefiori D.C. Weinhold K.J. Blattner W.A. Borrow P. Shattock R. Cohen M.S. Haynes B.F. Tomaras G.D. HIV-1 gp41 envelope IgA is frequently elicited after transmission but has an initial short response half-life. Mucosal Immunol. 2013 6 4 692 703 10.1038/mi.2012.107 23299618
    [Google Scholar]
  127. Seaton K.E. Ballweber L. Lan A. Donathan M. Hughes S. Vojtech L. Moody M.A. Liao H.X. Haynes B.F. Galloway C.G. Richardson B.A. Karim S.A. Dezzutti C.S. McElrath M.J. Tomaras G.D. Hladik F. HIV-1 specific IgA detected in vaginal secretions of HIV uninfected women participating in a microbicide trial in Southern Africa are primarily directed toward gp120 and gp140 specificities. PLoS One 2014 9 7 e101863 10.1371/journal.pone.0101863 25054205
    [Google Scholar]
  128. Archary D. Seaton K.E. Passmore J.S. Werner L. Deal A. Dunphy L.J. Arnold K.B. Yates N.L. Lauffenburger D.A. Bergin P. Liebenberg L.J. Samsunder N. Mureithi M.W. Altfeld M. Garrett N. Abdool Karim Q. Abdool Karim S.S. Morris L. Tomaras G.D. Distinct genital tract HIV-specific antibody profiles associated with tenofovir gel. Mucosal Immunol. 2016 9 3 821 833 10.1038/mi.2015.145 26813340
    [Google Scholar]
  129. Seaton K.E. Deal A. Han X. Li S.S. Clayton A. Heptinstall J. Duerr A. Allen M.A. Shen X. Sawant S. Yates N.L. Spearman P. Churchyard G. Goepfert P.A. Maenza J. Gray G. Pantaleo G. Polakowski L. Robinson H.L. Grant S. Randhawa A.K. Huang Y. Morgan C. Grunenberg N. Karuna S. Gilbert P.B. McElrath M.J. Huang Y. Tomaras G.D. NIAID HIV Vaccine Trials Network (HVTN) 076, 088, 086, 096, 097, 205 Study Teams. Meta-analysis of HIV-1 vaccine elicited mucosal antibodies in humans. NPJ Vaccines 2021 6 1 56 10.1038/s41541‑021‑00305‑8 33859204
    [Google Scholar]
  130. Arunachalam P.S. Charles T.P. Joag V. Bollimpelli V.S. Scott M.K.D. Wimmers F. Burton S.L. Labranche C.C. Petitdemange C. Gangadhara S. Styles T.M. Quarnstrom C.F. Walter K.A. Ketas T.J. Legere T. Jagadeesh Reddy P.B. Kasturi S.P. Tsai A. Yeung B.Z. Gupta S. Tomai M. Vasilakos J. Shaw G.M. Kang C.Y. Moore J.P. Subramaniam S. Khatri P. Montefiori D. Kozlowski P.A. Derdeyn C.A. Hunter E. Masopust D. Amara R.R. Pulendran B. T cell-inducing vaccine durably prevents mucosal SHIV infection even with lower neutralizing antibody titers. Nat. Med. 2020 26 6 932 940 10.1038/s41591‑020‑0858‑8 32393800
    [Google Scholar]
/content/journals/chr/10.2174/011570162X363301250314034023
Loading
/content/journals/chr/10.2174/011570162X363301250314034023
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error
Please enter a valid_number test