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Vaccine Elicitation of High Mannose-Dependent Neutralizing Antibodies against the V3-Glycan Broadly Neutralizing Epitope in Nonhuman Primates.

Saunders KO, Nicely NI, Wiehe K, Bonsignori M, Meyerhoff RR, Parks R, Walkowicz WE, Aussedat B, Wu NR, Cai F, Vohra Y, Park PK, Eaton A, Go EP, Sutherland LL, Scearce RM, Barouch DH, Zhang R, Von Holle T, Overman RG, Anasti K, Sanders RW, Moody MA, Kepler TB, Korber B, Desaire H, Santra S, Letvin NL, Nabel GJ, Montefiori DC, Tomaras GD, Liao HX, Alam SM, Danishefsky SJ, Haynes BF
Cell Rep 18 2175-2188 (2017)
Cited: 49 times
EuropePMC logo PMID: 28249163

Abstract

Induction of broadly neutralizing antibodies (bnAbs) that target HIV-1 envelope (Env) is a goal of HIV-1 vaccine development. A bnAb target is the Env third variable loop (V3)-glycan site. To determine whether immunization could induce antibodies to the V3-glycan bnAb binding site, we repetitively immunized macaques over a 4-year period with an Env expressing V3-high mannose glycans. Env immunizations elicited plasma antibodies that neutralized HIV-1 expressing only high-mannose glycans-a characteristic shared by early bnAb B cell lineage members. A rhesus recombinant monoclonal antibody from a vaccinated macaque bound to the V3-glycan site at the same amino acids as broadly neutralizing antibodies. A structure of the antibody bound to glycan revealed that the three variable heavy-chain complementarity-determining regions formed a cavity into which glycan could insert and neutralized multiple HIV-1 isolates with high-mannose glycans. Thus, HIV-1 Env vaccination induced mannose-dependent antibodies with characteristics of V3-glycan bnAb precursors.

Articles - 5iie mentioned but not cited (2)

  1. Vaccine Elicitation of High Mannose-Dependent Neutralizing Antibodies against the V3-Glycan Broadly Neutralizing Epitope in Nonhuman Primates. Saunders KO, Nicely NI, Wiehe K, Bonsignori M, Meyerhoff RR, Parks R, Walkowicz WE, Aussedat B, Wu NR, Cai F, Vohra Y, Park PK, Eaton A, Go EP, Sutherland LL, Scearce RM, Barouch DH, Zhang R, Von Holle T, Overman RG, Anasti K, Sanders RW, Moody MA, Kepler TB, Korber B, Desaire H, Santra S, Letvin NL, Nabel GJ, Montefiori DC, Tomaras GD, Liao HX, Alam SM, Danishefsky SJ, Haynes BF. Cell Rep 18 2175-2188 (2017)
  2. Fab-dimerized glycan-reactive antibodies are a structural category of natural antibodies. Williams WB, Meyerhoff RR, Edwards RJ, Li H, Manne K, Nicely NI, Henderson R, Zhou Y, Janowska K, Mansouri K, Gobeil S, Evangelous T, Hora B, Berry M, Abuahmad AY, Sprenz J, Deyton M, Stalls V, Kopp M, Hsu AL, Borgnia MJ, Stewart-Jones GBE, Lee MS, Bronkema N, Moody MA, Wiehe K, Bradley T, Alam SM, Parks RJ, Foulger A, Oguin T, Sempowski GD, Bonsignori M, LaBranche CC, Montefiori DC, Seaman M, Santra S, Perfect J, Francica JR, Lynn GM, Aussedat B, Walkowicz WE, Laga R, Kelsoe G, Saunders KO, Fera D, Kwong PD, Seder RA, Bartesaghi A, Shaw GM, Acharya P, Haynes BF. Cell 184 2955-2972.e25 (2021)


Reviews citing this publication (10)

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Articles citing this publication (37)

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  2. Vaccine Induction of Heterologous Tier 2 HIV-1 Neutralizing Antibodies in Animal Models. Saunders KO, Verkoczy LK, Jiang C, Zhang J, Parks R, Chen H, Housman M, Bouton-Verville H, Shen X, Trama AM, Scearce R, Sutherland L, Santra S, Newman A, Eaton A, Xu K, Georgiev IS, Joyce MG, Tomaras GD, Bonsignori M, Reed SG, Salazar A, Mascola JR, Moody MA, Cain DW, Centlivre M, Zurawski S, Zurawski G, Erickson HP, Kwong PD, Alam SM, Levy Y, Montefiori DC, Haynes BF. Cell Rep 21 3681-3690 (2017)
  3. Functional Relevance of Improbable Antibody Mutations for HIV Broadly Neutralizing Antibody Development. Wiehe K, Bradley T, Meyerhoff RR, Hart C, Williams WB, Easterhoff D, Faison WJ, Kepler TB, Saunders KO, Alam SM, Bonsignori M, Haynes BF. Cell Host Microbe 23 759-765.e6 (2018)
  4. Neutralization-guided design of HIV-1 envelope trimers with high affinity for the unmutated common ancestor of CH235 lineage CD4bs broadly neutralizing antibodies. LaBranche CC, Henderson R, Hsu A, Behrens S, Chen X, Zhou T, Wiehe K, Saunders KO, Alam SM, Bonsignori M, Borgnia MJ, Sattentau QJ, Eaton A, Greene K, Gao H, Liao HX, Williams WB, Peacock J, Tang H, Perez LG, Edwards RJ, Kepler TB, Korber BT, Kwong PD, Mascola JR, Acharya P, Haynes BF, Montefiori DC. PLoS Pathog 15 e1008026 (2019)
  5. Synthetic Three-Component HIV-1 V3 Glycopeptide Immunogens Induce Glycan-Dependent Antibody Responses. Cai H, Orwenyo J, Giddens JP, Yang Q, Zhang R, LaBranche CC, Montefiori DC, Wang LX. Cell Chem Biol 24 1513-1522.e4 (2017)
  6. Co-immunization of DNA and Protein in the Same Anatomical Sites Induces Superior Protective Immune Responses against SHIV Challenge. Felber BK, Lu Z, Hu X, Valentin A, Rosati M, Remmel CAL, Weiner JA, Carpenter MC, Faircloth K, Stanfield-Oakley S, Williams WB, Shen X, Tomaras GD, LaBranche CC, Montefiori D, Trinh HV, Rao M, Alam MS, Vandergrift NA, Saunders KO, Wang Y, Rountree W, Das J, Alter G, Reed SG, Aye PP, Schiro F, Pahar B, Dufour JP, Veazey RS, Marx PA, Venzon DJ, Shaw GM, Ferrari G, Ackerman ME, Haynes BF, Pavlakis GN. Cell Rep 31 107624 (2020)
  7. Lipid nanoparticle encapsulated nucleoside-modified mRNA vaccines elicit polyfunctional HIV-1 antibodies comparable to proteins in nonhuman primates. Saunders KO, Pardi N, Parks R, Santra S, Mu Z, Sutherland L, Scearce R, Barr M, Eaton A, Hernandez G, Goodman D, Hogan MJ, Tombacz I, Gordon DN, Rountree RW, Wang Y, Lewis MG, Pierson TC, Barbosa C, Tam Y, Matyas GR, Rao M, Beck Z, Shen X, Ferrari G, Tomaras GD, Montefiori DC, Weissman D, Haynes BF. NPJ Vaccines 6 50 (2021)
  8. Difficult-to-neutralize global HIV-1 isolates are neutralized by antibodies targeting open envelope conformations. Han Q, Jones JA, Nicely NI, Reed RK, Shen X, Mansouri K, Louder M, Trama AM, Alam SM, Edwards RJ, Bonsignori M, Tomaras GD, Korber B, Montefiori DC, Mascola JR, Seaman MS, Haynes BF, Saunders KO. Nat Commun 10 2898 (2019)
  9. Multivalent Antigen Presentation Enhances the Immunogenicity of a Synthetic Three-Component HIV-1 V3 Glycopeptide Vaccine. Cai H, Zhang R, Orwenyo J, Giddens J, Yang Q, LaBranche CC, Montefiori DC, Wang LX. ACS Cent Sci 4 582-589 (2018)
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  12. Oligomannose Glycopeptide Conjugates Elicit Antibodies Targeting the Glycan Core Rather than Its Extremities. Nguyen DN, Xu B, Stanfield RL, Bailey JK, Horiya S, Temme JS, Leon DR, LaBranche CC, Montefiori DC, Costello CE, Wilson IA, Krauss IJ. ACS Cent Sci 5 237-249 (2019)
  13. Maternal Broadly Neutralizing Antibodies Can Select for Neutralization-Resistant, Infant-Transmitted/Founder HIV Variants. Martinez DR, Tu JJ, Kumar A, Mangold JF, Mangan RJ, Goswami R, Giorgi EE, Chen J, Mengual M, Douglas AO, Heimsath H, Saunders KO, Nicely NI, Eudailey J, Hernandez G, Morgan-Asiedu PK, Wiehe K, Haynes BF, Moody MA, LaBranche C, Montefiori DC, Gao F, Permar SR. mBio 11 e00176-20 (2020)
  14. Neonatal Rhesus Macaques Have Distinct Immune Cell Transcriptional Profiles following HIV Envelope Immunization. Han Q, Bradley T, Williams WB, Cain DW, Montefiori DC, Saunders KO, Parks RJ, Edwards RW, Ferrari G, Mueller O, Shen X, Wiehe KJ, Reed S, Fox CB, Rountree W, Vandergrift NA, Wang Y, Sutherland LL, Santra S, Moody MA, Permar SR, Tomaras GD, Lewis MG, Van Rompay KKA, Haynes BF. Cell Rep 30 1553-1569.e6 (2020)
  15. Automated Design by Structure-Based Stabilization and Consensus Repair to Achieve Prefusion-Closed Envelope Trimers in a Wide Variety of HIV Strains. Rawi R, Rutten L, Lai YT, Olia AS, Blokland S, Juraszek J, Shen CH, Tsybovsky Y, Verardi R, Yang Y, Zhang B, Zhou T, Chuang GY, Kwong PD, Langedijk JPM. Cell Rep 33 108432 (2020)
  16. Signature-Ion-Triggered Mass Spectrometry Approach Enabled Discovery of N- and O-Linked Glycosylated Neuropeptides in the Crustacean Nervous System. Cao Q, Yu Q, Liu Y, Chen Z, Li L. J Proteome Res 19 634-643 (2020)
  17. Synthetic HIV V3 Glycopeptide Immunogen Carrying a N334 N-Glycan Induces Glycan-Dependent Antibodies with Promiscuous Site Recognition. Cai H, Zhang RS, Orwenyo J, Giddens J, Yang Q, LaBranche CC, Montefiori DC, Wang LX. J Med Chem 61 10116-10125 (2018)
  18. HIV DNA-Adenovirus Multiclade Envelope Vaccine Induces gp41 Antibody Immunodominance in Rhesus Macaques. Han Q, Williams WB, Saunders KO, Seaton KE, Wiehe KJ, Vandergrift N, Von Holle TA, Trama AM, Parks RJ, Luo K, Gurley TC, Kepler TB, Marshall DJ, Montefiori DC, Sutherland LL, Alam MS, Whitesides JF, Bowman CM, Permar SR, Graham BS, Mascola JR, Seed PC, Van Rompay KKA, Tomaras GD, Moody MA, Haynes BF. J Virol 91 e00923-17 (2017)
  19. HIV vaccine delayed boosting increases Env variable region 2-specific antibody effector functions. Easterhoff D, Pollara J, Luo K, Janus B, Gohain N, Williams LD, Tay MZ, Monroe A, Peachman K, Choe M, Min S, Lusso P, Zhang P, Go EP, Desaire H, Bonsignori M, Hwang KK, Beck C, Kakalis M, O'Connell RJ, Vasan S, Kim JH, Michael NL, Excler JL, Robb ML, Rerks-Ngarm S, Kaewkungwal J, Pitisuttithum P, Nitayaphan S, Sinangil F, Tartaglia J, Phogat S, Wiehe K, Saunders KO, Montefiori DC, Tomaras GD, Moody MA, Arthos J, Rao M, Joyce MG, Ofek G, Ferrari G, Haynes BF. JCI Insight 5 131437 (2020)
  20. Star nanoparticles delivering HIV-1 peptide minimal immunogens elicit near-native envelope antibody responses in nonhuman primates. Francica JR, Laga R, Lynn GM, Mužíková G, Androvič L, Aussedat B, Walkowicz WE, Padhan K, Ramirez-Valdez RA, Parks R, Schmidt SD, Flynn BJ, Tsybovsky Y, Stewart-Jones GBE, Saunders KO, Baharom F, Petrovas C, Haynes BF, Seder RA. PLoS Biol 17 e3000328 (2019)
  21. Modeling Immunity with Rosetta: Methods for Antibody and Antigen Design. Schoeder CT, Schmitz S, Adolf-Bryfogle J, Sevy AM, Finn JA, Sauer MF, Bozhanova NG, Mueller BK, Sangha AK, Bonet J, Sheehan JH, Kuenze G, Marlow B, Smith ST, Woods H, Bender BJ, Martina CE, Del Alamo D, Kodali P, Gulsevin A, Schief WR, Correia BE, Crowe JE, Meiler J, Moretti R. Biochemistry 60 825-846 (2021)
  22. Neutralizing Antibody Responses following Long-Term Vaccination with HIV-1 Env gp140 in Guinea Pigs. Bricault CA, Kovacs JM, Badamchi-Zadeh A, McKee K, Shields JL, Gunn BM, Neubauer GH, Ghantous F, Jennings J, Gillis L, Perry J, Nkolola JP, Alter G, Chen B, Stephenson KE, Doria-Rose N, Mascola JR, Seaman MS, Barouch DH. J Virol 92 e00369-18 (2018)
  23. Immunogenicity of NYVAC Prime-Protein Boost Human Immunodeficiency Virus Type 1 Envelope Vaccination and Simian-Human Immunodeficiency Virus Challenge of Nonhuman Primates. Saunders KO, Santra S, Parks R, Yates NL, Sutherland LL, Scearce RM, Balachandran H, Bradley T, Goodman D, Eaton A, Stanfield-Oakley SA, Tartaglia J, Phogat S, Pantaleo G, Esteban M, Gomez CE, Perdiguero B, Jacobs B, Kibler K, Korber B, Montefiori DC, Ferrari G, Vandergrift N, Liao HX, Tomaras GD, Haynes BF. J Virol 92 e02035-17 (2018)
  24. Cooperation between somatic mutation and germline-encoded residues enables antibody recognition of HIV-1 envelope glycans. Wu NR, Nicely NI, Lee EM, Reed RK, Watts BE, Cai F, Walkowicz WE, Aussedat B, Jones JA, Eaton A, Trama AM, Alam SM, Montefiori DC, Haynes BF, Saunders KO. PLoS Pathog 15 e1008165 (2019)
  25. Serum alpha-mannosidase as an additional barrier to eliciting oligomannose-specific HIV-1-neutralizing antibodies. Bruxelle JF, Kirilenko T, Qureshi Q, Lu N, Trattnig N, Kosma P, Pantophlet R. Sci Rep 10 7582 (2020)
  26. A Derivative of the D5 Monoclonal Antibody That Targets the gp41 N-Heptad Repeat of HIV-1 with Broad Tier-2-Neutralizing Activity. Rubio AA, Filsinger Interrante MV, Bell BN, Brown CL, Bruun TUJ, LaBranche CC, Montefiori DC, Kim PS. J Virol 95 e0235020 (2021)
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  29. The Impact of Sustained Immunization Regimens on the Antibody Response to Oligomannose Glycans. Nguyen DN, Redman RL, Horiya S, Bailey JK, Xu B, Stanfield RL, Temme JS, LaBranche CC, Wang S, Rodal AA, Montefiori DC, Wilson IA, Krauss IJ. ACS Chem Biol 15 789-798 (2020)
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  35. Predicting Antibody Neutralization Efficacy in Hypermutated Epitopes Using Monte Carlo Simulations. Amengual-Rigo P, Carrillo J, Blanco J, Guallar V. Polymers (Basel) 12 E2392 (2020)
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