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Mapping the immunogenic landscape of near-native HIV-1 envelope trimers in non-human primates.

Cottrell CA, van Schooten J, Bowman CA, Yuan M, Oyen D, Shin M, Morpurgo R, van der Woude P, van Breemen M, Torres JL, Patel R, Gross J, Sewall LM, Copps J, Ozorowski G, Nogal B, Sok D, Rakasz EG, Labranche C, Vigdorovich V, Christley S, Carnathan DG, Sather DN, Montefiori D, Silvestri G, Burton DR, Moore JP, Wilson IA, Sanders RW, Ward AB, van Gils MJ
PLoS Pathog 16 e1008753 (2020)
Related entries: 6vn0, 6vo1, 6vor, 6vos, 6vsr

Cited: 41 times
EuropePMC logo PMID: 32866207

Abstract

The induction of broad and potent immunity by vaccines is the key focus of research efforts aimed at protecting against HIV-1 infection. Soluble native-like HIV-1 envelope glycoproteins have shown promise as vaccine candidates as they can induce potent autologous neutralizing responses in rabbits and non-human primates. In this study, monoclonal antibodies were isolated and characterized from rhesus macaques immunized with the BG505 SOSIP.664 trimer to better understand vaccine-induced antibody responses. Our studies reveal a diverse landscape of antibodies recognizing immunodominant strain-specific epitopes and non-neutralizing neo-epitopes. Additionally, we isolated a subset of mAbs against an epitope cluster at the gp120-gp41 interface that recognize the highly conserved fusion peptide and the glycan at position 88 and have characteristics akin to several human-derived broadly neutralizing antibodies.

Reviews citing this publication (4)

  1. Inducing broad-based immunity against viruses with pandemic potential. Sette A, Saphire EO. Immunity 55 738-748 (2022)
  2. HIV vaccinology: 2021 update. Lee JH, Crotty S. Semin Immunol 51 101470 (2021)
  3. Strategies for induction of HIV-1 envelope-reactive broadly neutralizing antibodies. Williams WB, Wiehe K, Saunders KO, Haynes BF. J Int AIDS Soc 24 Suppl 7 e25831 (2021)
  4. Structure-guided envelope trimer design in HIV-1 vaccine development: a narrative review. Derking R, Sanders RW. J Int AIDS Soc 24 Suppl 7 e25797 (2021)

Articles citing this publication (37)

  1. Visualization of the HIV-1 Env glycan shield across scales. Berndsen ZT, Chakraborty S, Wang X, Cottrell CA, Torres JL, Diedrich JK, López CA, Yates JR, van Gils MJ, Paulson JC, Gnanakaran S, Ward AB. Proc Natl Acad Sci U S A 117 28014-28025 (2020)
  2. Site-Specific Steric Control of SARS-CoV-2 Spike Glycosylation. Allen JD, Chawla H, Samsudin F, Zuzic L, Shivgan AT, Watanabe Y, He WT, Callaghan S, Song G, Yong P, Brouwer PJM, Song Y, Cai Y, Duyvesteyn HME, Malinauskas T, Kint J, Pino P, Wurm MJ, Frank M, Chen B, Stuart DI, Sanders RW, Andrabi R, Burton DR, Li S, Bond PJ, Crispin M. Biochemistry 60 2153-2169 (2021)
  3. Targeting HIV Env immunogens to B cell follicles in nonhuman primates through immune complex or protein nanoparticle formulations. Martin JT, Cottrell CA, Antanasijevic A, Carnathan DG, Cossette BJ, Enemuo CA, Gebru EH, Choe Y, Viviano F, Fischinger S, Tokatlian T, Cirelli KM, Ueda G, Copps J, Schiffner T, Menis S, Alter G, Schief WR, Crotty S, King NP, Baker D, Silvestri G, Ward AB, Irvine DJ. NPJ Vaccines 5 72 (2020)
  4. Cryo-ET of Env on intact HIV virions reveals structural variation and positioning on the Gag lattice. Mangala Prasad V, Leaman DP, Lovendahl KN, Croft JT, Benhaim MA, Hodge EA, Zwick MB, Lee KK. Cell 185 641-653.e17 (2022)
  5. Enhancing glycan occupancy of soluble HIV-1 envelope trimers to mimic the native viral spike. Derking R, Allen JD, Cottrell CA, Sliepen K, Seabright GE, Lee WH, Aldon Y, Rantalainen K, Antanasijevic A, Copps J, Yasmeen A, Cupo A, Cruz Portillo VM, Poniman M, Bol N, van der Woude P, de Taeye SW, van den Kerkhof TLGM, Klasse PJ, Ozorowski G, van Gils MJ, Moore JP, Ward AB, Crispin M, Sanders RW. Cell Rep 35 108933 (2021)
  6. A multiclade env-gag VLP mRNA vaccine elicits tier-2 HIV-1-neutralizing antibodies and reduces the risk of heterologous SHIV infection in macaques. Zhang P, Narayanan E, Liu Q, Tsybovsky Y, Boswell K, Ding S, Hu Z, Follmann D, Lin Y, Miao H, Schmeisser H, Rogers D, Falcone S, Elbashir SM, Presnyak V, Bahl K, Prabhakaran M, Chen X, Sarfo EK, Ambrozak DR, Gautam R, Martin MA, Swerczek J, Herbert R, Weiss D, Misamore J, Ciaramella G, Himansu S, Stewart-Jones G, McDermott A, Koup RA, Mascola JR, Finzi A, Carfi A, Fauci AS, Lusso P. Nat Med 27 2234-2245 (2021)
  7. Disassembly of HIV envelope glycoprotein trimer immunogens is driven by antibodies elicited via immunization. Turner HL, Andrabi R, Cottrell CA, Richey ST, Song G, Callaghan S, Anzanello F, Moyer TJ, Abraham W, Melo M, Silva M, Scaringi N, Rakasz EG, Sattentau QJ, Irvine DJ, Burton DR, Ward AB. Sci Adv 7 eabh2791 (2021)
  8. Neutralizing Antibody Responses Induced by HIV-1 Envelope Glycoprotein SOSIP Trimers Derived from Elite Neutralizers. Schorcht A, van den Kerkhof TLGM, Cottrell CA, Allen JD, Torres JL, Behrens AJ, Schermer EE, Burger JA, de Taeye SW, Torrents de la Peña A, Bontjer I, Gumbs S, Ozorowski G, LaBranche CC, de Val N, Yasmeen A, Klasse PJ, Montefiori DC, Moore JP, Schuitemaker H, Crispin M, van Gils MJ, Ward AB, Sanders RW. J Virol 94 e01214-20 (2020)
  9. Polyclonal antibody responses to HIV Env immunogens resolved using cryoEM. Antanasijevic A, Sewall LM, Cottrell CA, Carnathan DG, Jimenez LE, Ngo JT, Silverman JB, Groschel B, Georgeson E, Bhiman J, Bastidas R, LaBranche C, Allen JD, Copps J, Perrett HR, Rantalainen K, Cannac F, Yang YR, de la Peña AT, Rocha RF, Berndsen ZT, Baker D, King NP, Sanders RW, Moore JP, Crotty S, Crispin M, Montefiori DC, Burton DR, Schief WR, Silvestri G, Ward AB. Nat Commun 12 4817 (2021)
  10. Antibodies from primary humoral responses modulate the recruitment of naive B cells during secondary responses. Tas JMJ, Koo JH, Lin YC, Xie Z, Steichen JM, Jackson AM, Hauser BM, Wang X, Cottrell CA, Torres JL, Warner JE, Kirsch KH, Weldon SR, Groschel B, Nogal B, Ozorowski G, Bangaru S, Phelps N, Adachi Y, Eskandarzadeh S, Kubitz M, Burton DR, Lingwood D, Schmidt AG, Nair U, Ward AB, Schief WR, Batista FD. Immunity 55 1856-1871.e6 (2022)
  11. Antibody responses induced by SHIV infection are more focused than those induced by soluble native HIV-1 envelope trimers in non-human primates. van Schooten J, van Haaren MM, Li H, McCoy LE, Havenar-Daughton C, Cottrell CA, Burger JA, van der Woude P, Helgers LC, Tomris I, Labranche CC, Montefiori DC, Ward AB, Burton DR, Moore JP, Sanders RW, Crotty S, Shaw GM, van Gils MJ. PLoS Pathog 17 e1009736 (2021)
  12. Broad and ultra-potent cross-clade neutralization of HIV-1 by a vaccine-induced CD4 binding site bovine antibody. Heydarchi B, Fong DS, Gao H, Salazar-Quiroz NA, Edwards JM, Gonelli CA, Grimley S, Aktepe TE, Mackenzie C, Wales WJ, van Gils MJ, Cupo A, Rouiller I, Gooley PR, Moore JP, Sanders RW, Montefiori D, Sethi A, Purcell DFJ. Cell Rep Med 3 100635 (2022)
  13. Hitting the sweet spot: exploiting HIV-1 glycan shield for induction of broadly neutralizing antibodies. Wagh K, Hahn BH, Korber B. Curr Opin HIV AIDS 15 267-274 (2020)
  14. Neutralizing Antibodies Induced by First-Generation gp41-Stabilized HIV-1 Envelope Trimers and Nanoparticles. Kumar S, Lin X, Ngo T, Shapero B, Sou C, Allen JD, Copps J, Zhang L, Ozorowski G, He L, Crispin M, Ward AB, Wilson IA, Zhu J. mBio 12 e0042921 (2021)
  15. Nucleic acid delivery of immune-focused SARS-CoV-2 nanoparticles drives rapid and potent immunogenicity capable of single-dose protection. Konrath KM, Liaw K, Wu Y, Zhu X, Walker SN, Xu Z, Schultheis K, Chokkalingam N, Chawla H, Du J, Tursi NJ, Moore A, Adolf-Bryfogle J, Purwar M, Reuschel EL, Frase D, Sullivan M, Fry B, Maricic I, Andrade VM, Iffland C, Crispin M, Broderick KE, Humeau LMPF, Patel A, Smith TRF, Pallesen J, Weiner DB, Kulp DW. Cell Rep 38 110318 (2022)
  16. A combined adjuvant approach primes robust germinal center responses and humoral immunity in non-human primates. Phung I, Rodrigues KA, Marina-Zárate E, Maiorino L, Pahar B, Lee WH, Melo M, Kaur A, Allers C, Fahlberg M, Grasperge BF, Dufour JP, Schiro F, Aye PP, Lopez PG, Torres JL, Ozorowski G, Eskandarzadeh S, Kubitz M, Georgeson E, Groschel B, Nedellec R, Bick M, Kaczmarek Michaels K, Gao H, Shen X, Carnathan DG, Silvestri G, Montefiori DC, Ward AB, Hangartner L, Veazey RS, Burton DR, Schief WR, Irvine DJ, Crotty S. Nat Commun 14 7107 (2023)
  17. Addressing IGHV Gene Structural Diversity Enhances Immunoglobulin Repertoire Analysis: Lessons From Rhesus Macaque. Kaduk M, Corcoran M, Karlsson Hedestam GB. Front Immunol 13 818440 (2022)
  18. Antibodies from Rabbits Immunized with HIV-1 Clade B SOSIP Trimers Can Neutralize Multiple Clade B Viruses by Destabilizing the Envelope Glycoprotein. van Haaren MM, McCoy LE, Torres JL, Lee W, Cottrell CA, Copps JL, van der Woude P, Yasmeen A, de Taeye SW, Torrents de la Peña A, Moore JP, Burton DR, Klasse PJ, Ward AB, Sanders RW, van Gils MJ. J Virol 95 e0009421 (2021)
  19. Antibody elicited by HIV-1 immunogen vaccination in macaques displaces Env fusion peptide and destroys a neutralizing epitope. Abernathy ME, Gristick HB, Vielmetter J, Keeffe JR, Gnanapragasam PNP, Lee YE, Escolano A, Gautam R, Seaman MS, Martin MA, Nussenzweig MC, Bjorkman PJ. NPJ Vaccines 6 126 (2021)
  20. Convergent HIV-1 Evolution upon Targeted Destabilization of the gp120-gp41 Interface. Torrents de la Peña A, Del Moral Sánchez I, Burger JA, Bontjer I, Isik G, Eggink D, van Gils MJ, Sanders RW. J Virol 95 e0053221 (2021)
  21. Fine-mapping the immunodominant antibody epitopes on consensus sequence-based HIV-1 envelope trimer vaccine candidates. Reiss EIMM, van Haaren MM, van Schooten J, Claireaux MAF, Maisonnasse P, Antanasijevic A, Allen JD, Bontjer I, Torres JL, Lee WH, Ozorowski G, Vázquez Bernat N, Kaduk M, Aldon Y, Burger JA, Chawla H, Aartse A, Tolazzi M, Gao H, Mundsperger P, Crispin M, Montefiori DC, Karlsson Hedestam GB, Scarlatti G, Ward AB, Le Grand R, Shattock R, Dereuddre-Bosquet N, Sanders RW, van Gils MJ. NPJ Vaccines 7 152 (2022)
  22. From structure to sequence: Antibody discovery using cryoEM. Antanasijevic A, Bowman CA, Kirchdoerfer RN, Cottrell CA, Ozorowski G, Upadhyay AA, Cirelli KM, Carnathan DG, Enemuo CA, Sewall LM, Nogal B, Zhao F, Groschel B, Schief WR, Sok D, Silvestri G, Crotty S, Bosinger SE, Ward AB. Sci Adv 8 eabk2039 (2022)
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  24. HIV-1 neutralizing antibodies elicited in humans by a prefusion-stabilized envelope trimer form a reproducible class targeting fusion peptide. Wang S, Matassoli F, Zhang B, Liu T, Shen CH, Bylund T, Johnston T, Henry AR, Teng IT, Tripathi P, Becker JE, Changela A, Chaudhary R, Cheng C, Gaudinski M, Gorman J, Harris DR, Lee M, Morano NC, Novik L, O'Dell S, Olia AS, Parchment DK, Rawi R, Roberts-Torres J, Stephens T, Tsybovsky Y, Wang D, Van Wazer DJ, Zhou T, Doria-Rose NA, Koup RA, Shapiro L, Douek DC, McDermott AB, Kwong PD. Cell Rep 42 112755 (2023)
  25. High-resolution mapping of the neutralizing and binding specificities of polyclonal sera post-HIV Env trimer vaccination. Dingens AS, Pratap P, Malone K, Hilton SK, Ketas T, Cottrell CA, Overbaugh J, Moore JP, Klasse PJ, Ward AB, Bloom JD. Elife 10 (2021)
  26. Highly mutated antibodies capable of neutralizing N276 glycan-deficient HIV after a single immunization with an Env trimer. Lee JH, Nakao C, Appel M, Le A, Landais E, Kalyuzhniy O, Hu X, Liguori A, Mullen TM, Groschel B, Abbott RK, Sok D, Schief WR, Crotty S. Cell Rep 38 110485 (2022)
  27. IMGT® Biocuration and Analysis of the Rhesus Monkey IG Loci. Nguefack Ngoune V, Bertignac M, Georga M, Papadaki A, Albani A, Folch G, Jabado-Michaloud J, Giudicelli V, Duroux P, Lefranc MP, Kossida S. Vaccines (Basel) 10 394 (2022)
  28. Immune Repertoire Analysis on High-Performance Computing Using VDJServer V1: A Method by the AIRR Community. Christley S, Stervbo U, Cowell LG, AIRR Community. Methods Mol Biol 2453 439-446 (2022)
  29. Immunofocusing and enhancing autologous Tier-2 HIV-1 neutralization by displaying Env trimers on two-component protein nanoparticles. Brouwer PJM, Antanasijevic A, de Gast M, Allen JD, Bijl TPL, Yasmeen A, Ravichandran R, Burger JA, Ozorowski G, Torres JL, LaBranche C, Montefiori DC, Ringe RP, van Gils MJ, Moore JP, Klasse PJ, Crispin M, King NP, Ward AB, Sanders RW. NPJ Vaccines 6 24 (2021)
  30. Increasing sensitivity of antibody-antigen interactions using photo-cross-linking. Torrents de la Peña A, Sewall LM, de Paiva Froes Rocha R, Jackson AM, Pratap PP, Bangaru S, Cottrell CA, Mohanty S, Shaw AC, Ward AB. Cell Rep Methods 3 100509 (2023)
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  32. Mapping Neutralizing Antibody Epitope Specificities to an HIV Env Trimer in Immunized and in Infected Rhesus Macaques. Zhao F, Joyce C, Burns A, Nogal B, Cottrell CA, Ramos A, Biddle T, Pauthner M, Nedellec R, Qureshi H, Mason R, Landais E, Briney B, Ward AB, Burton DR, Sok D. Cell Rep 32 108122 (2020)
  33. Modulating the quantity of HIV Env-specific CD4 T cell help promotes rare B cell responses in germinal centers. Lee JH, Hu JK, Georgeson E, Nakao C, Groschel B, Dileepan T, Jenkins MK, Seumois G, Vijayanand P, Schief WR, Crotty S. J Exp Med 218 (2021)
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  36. The Glycan Hole Area of HIV-1 Envelope Trimers Contributes Prominently to the Induction of Autologous Neutralization. Schorcht A, Cottrell CA, Pugach P, Ringe RP, Han AX, Allen JD, van den Kerkhof TLGM, Seabright GE, Schermer EE, Ketas TJ, Burger JA, van Schooten J, LaBranche CC, Ozorowski G, de Val N, Bader DLV, Schuitemaker H, Russell CA, Montefiori DC, van Gils MJ, Crispin M, Klasse PJ, Ward AB, Moore JP, Sanders RW. J Virol 96 e0155221 (2022)
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Related citations provided by authors (1)

  1. Mapping the immunogenic landscape of native HIV-1 envelope trimers in non-human primates. Cottrell CA, van Schooten J, Bowman CA, Yuan M, Oyen D, Shin M, Morpurgo R, van der Woude P, van Breemen M, Torres JL, Patel R, Gross J, Sewall LM, Copps J, Ozorowski G, Sok D, Rakasz EG, Labranche C, Vigdorovich V, Christley S, Sather DN, Montefiori D, Moore JP, Burton DR, Wilson IA, Sanders RW, Ward AB, van Gils MJ Biorxiv - (2020)

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