Exploration of a Sequential Gp140-Gp145 Immunization Regimen with Heterologous Envs to Induce a Protective Cross-Reactive HIV Neutralizing Antibody Response In Non-human Primates

Alter G, Barouch D (2018) Immune correlate-guided HIV vaccine design. Cell Host Microbe 24:25–33 Barban V, Munoz-Jordan JL, Santiago GA, Mantel N, Girerd Y, Gulia S, Claude J-B, Lang J (2012) Broad neutralization of wild-type dengue virus isolates following immunization in monkeys with a tetravalent dengue vaccine based on chimeric yellow fever 17D/dengue viruses. Virology 429:91–98 Barouch DH, Alter G, Broge T, Linde C, Ackerman ME, Brown EP, Borducchi EN, Smith KM, Nkolola JP, Liu J (2015) Protective efficacy of adenovirus/protein vaccines against SIV challenges in rhesus monkeys. Science 349:320–324 Barouch DH, Stephenson KE, Borducchi EN, Smith K, Stanley K, McNally AG, Liu J, Abbink P, Maxfield LF, Seaman MS (2013) Protective efficacy of a global HIV-1 mosaic vaccine against heterologous SHIV challenges in rhesus monkeys. Cell 155:531–539 Binley JM, Sanders RW, Clas B, Schuelke N, Master A, Guo Y, Kajumo F, Anselma DJ, Maddon PJ, Olson WC (2000) A recombinant human immunodeficiency virus type 1 envelope glycoprotein complex stabilized by an intermolecular disulfide bond between the gp120 and gp41 subunits is an antigenic mimic of the trimeric virion-associated structure. J Virol 74:627–643 Burton DR, Mascola JR (2015) Antibody responses to envelope glycoproteins in HIV-1 infection. Nat Immunol 16:571–576 de Taeye SW, Moore JP, Sanders RW (2016) HIV-1 envelope trimer design and immunization strategies to induce broadly neutralizing antibodies. Trends Immunol 37:221–232 Doria-Rose NA, Klein RM, Manion MM, O’Dell S, Phogat A, Chakrabarti B, Hallahan CW, Migueles SA, Wrammert J, Ahmed R (2009) Frequency and phenotype of human immunodeficiency virus envelope-specific B cells from patients with broadly cross-neutralizing antibodies. J Virol 83:188–199 Emmer KL, Wieczorek L, Tuyishime S, Molnar S, Polonis VR, Ertl HC (2016) Antibody responses to prime-boost vaccination with an HIV-1 gp145 Env protein and chimpanzee adenovirus vectors expressing HIV-1 gp140. AIDS (London, England) 30:2405 Flynn NM, Forthal DN, Harro CD, Judson FN, Mayer KH, Para MF, rgp HIVVSG (2005) Placebo-controlled phase 3 trial of a recombinant glycoprotein 120 vaccine to prevent HIV-1 infection. J Infect Dis 191:654–665 Georgiev IS, Joyce MG, Yang Y, Sastry M, Zhang B, Baxa U, Chen RE, Druz A, Lees CR, Narpala S (2015) Single-chain soluble BG505. SOSIP gp140 trimers as structural and antigenic mimics of mature closed HIV-1 Env. J Virol 89:5318–5329 He L, De Val N, Morris CD, Vora N, Thinnes TC, Kong L, Azadnia P, Sok D, Zhou B, Burton DR (2016) Presenting native-like trimeric HIV-1 antigens with self-assembling nanoparticles. Nat Commun 7:1–15 He L, Kumar S, Allen JD, Huang D, Lin X, Mann CJ, Saye-Francisco KL, Copps J, Sarkar A, Blizard GS (2018) HIV-1 vaccine design through minimizing envelope metastability. Science advances 4:eaau6769 Hessell AJ, Malherbe DC, Pissani F, McBurney S, Krebs SJ, Gomes M, Pandey S, Sutton WF, Burwitz BJ, Gray M, Robins H, Park BS, Sacha JB, LaBranche CC, Fuller DH, Montefiori DC, Stamatatos L, Sather DN, Haigwood NL (2016) Achieving potent autologous neutralizing antibody responses against tier 2 HIV-1 viruses by strategic selection of envelope immunogens. J Immunol 196:3064–3078 Huang J, Ofek G, Laub L, Louder MK, Doria-Rose NA, Longo NS, Imamichi H, Bailer RT, Chakrabarti B, Sharma SK (2012) Broad and potent neutralization of HIV-1 by a gp41-specific human antibody. Nature 491:406–412 Julien J-P, Cupo A, Sok D, Stanfield RL, Lyumkis D, Deller MC, Klasse P-J, Burton DR, Sanders RW, Moore JP (2013a) Crystal structure of a soluble cleaved HIV-1 envelope trimer. Science 342:1477–1483 Julien J-P, Lee JH, Cupo A, Murin CD, Derking R, Hoffenberg S, Caulfield MJ, King CR, Marozsan AJ, Klasse PJ (2013b) Asymmetric recognition of the HIV-1 trimer by broadly neutralizing antibody PG9. Proc Natl Acad Sci 110:4351–4356 Klasse P, LaBranche CC, Ketas TJ, Ozorowski G, Cupo A, Pugach P, Ringe RP, Golabek M, van Gils MJ, Guttman M (2016) Sequential and simultaneous immunization of rabbits with HIV-1 envelope glycoprotein SOSIP. 664 trimers from clades A, B and C. PLoS Pathog 12:e1005864 Kong L, He L, De Val N, Vora N, Morris CD, Azadnia P, Sok D, Zhou B, Burton DR, Ward AB (2016) Uncleaved prefusion-optimized gp140 trimers derived from analysis of HIV-1 envelope metastability. Nat Commun 7:1–15 Lee JH, Ozorowski G, Ward AB (2016) Cryo-EM structure of a native, fully glycosylated, cleaved HIV-1 envelope trimer. Science 351:1043–1048 Lin Y, Böker A, He J, Sill K, Xiang H, Abetz C, Li X, Wang J, Emrick T, Long S (2005) Self-directed self-assembly of nanoparticle/copolymer mixtures. Nature 434:55–59 Liu L, Hao Y, Luo Z, Huang Y, Hu X, Liu Y, Shao Y (2012) Broad HIV-1 neutralizing antibody response induced by heterologous gp140/gp145 DNA prime-vaccinia boost immunization. Vaccine 30:4135–4143 Montefiori DC (2005) Evaluating neutralizing antibodies against HIV, SIV, and SHIV in luciferase reporter gene assays. Curr Protoc Immuno 64:12–11 Moore PL, Gray ES, Sheward D, Madiga M, Ranchobe N, Lai Z, Honnen WJ, Nonyane M, Tumba N, Hermanus T (2011) Potent and broad neutralization of HIV-1 subtype C by plasma antibodies targeting a quaternary epitope including residues in the V2 loop. J Virol 85:3128–3141 Pancera M, Zhou T, Druz A, Georgiev IS, Soto C, Gorman J, Huang J, Acharya P, Chuang G-Y, Ofek G (2014) Structure and immune recognition of trimeric pre-fusion HIV-1 Env. Nature 514:455–461 Pantaleo G, Koup RA (2004) Correlates of immune protection in HIV-1 infection: what we know, what we don’t know, what we should know. Nat Med 10:806–810 Pauthner M, Havenar-Daughton C, Sok D, Nkolola JP, Bastidas R, Boopathy AV, Carnathan DG, Chandrashekar A, Cirelli KM, Cottrell CA (2017) Elicitation of robust tier 2 neutralizing antibody responses in nonhuman primates by HIV envelope trimer immunization using optimized approaches. Immunity 46:1073–1088 Pitisuttithum P, Gilbert P, Gurwith M, Heyward W, Martin M, van Griensven F, Hu D, Tappero JW, Group BVE (2006) Randomized, double-blind, placebo-controlled efficacy trial of a bivalent recombinant glycoprotein 120 HIV-1 vaccine among injection drug users in Bangkok, Thailand. J infect Dis 194:1661–1671 Sanders R, Van Gils M, Derking R, Sok D, Ketas T, Burger J, Ozorowski G, Cupo A, Simonich C, Goo L (2015) HIV-1 vaccines. HIV-1 neutralizing antibodies induced by native-like envelope trimers. Science 349:aac4223 Sanders RW, Derking R, Cupo A, Julien J-P, Yasmeen A, de Val N, Kim HJ, Blattner C, de la Peña AT, Korzun J (2013) A next-generation cleaved, soluble HIV-1 Env trimer, BG505 SOSIP 664. gp140, expresses multiple epitopes for broadly neutralizing but not non-neutralizing antibodies. PLoS pathog 9:e1003618 Sanders RW, Moore JP (2017) Native-like Env trimers as a platform for HIV-1 vaccine design. Immunol Rev 275:161–182 Sanders RW, Schiffner L, Master A, Kajumo F, Guo Y, Dragic T, Moore JP, Binley JM (2000) Variable-loop-deleted variants of the human immunodeficiency virus type 1 envelope glycoprotein can be stabilized by an intermolecular disulfide bond between the gp120 and gp41 subunits. J Virol 74:5091–5100 Sanders RW, Vesanen M, Schuelke N, Master A, Schiffner L, Kalyanaraman R, Paluch M, Berkhout B, Maddon PJ, Olson WC (2002) Stabilization of the soluble, cleaved, trimeric form of the envelope glycoprotein complex of human immunodeficiency virus type 1. J Virol 76:8875–8889 Saunders KO, Verkoczy LK, Jiang C, Zhang J, Parks R, Chen H, Housman M, Bouton-Verville H, Shen X, Trama AM (2017) Vaccine induction of heterologous tier 2 HIV-1 neutralizing antibodies in animal models. Cell Rep 21:3681–3690 Saunders KO, Wiehe K, Tian M, Acharya P, Bradley T, Alam SM, Go EP, Scearce R, Sutherland L, Henderson R (2019) Targeted selection of HIV-specific antibody mutations by engineering B cell maturation. Science 366:eaay7199 Scheid JF, Mouquet H, Feldhahn N, Seaman MS, Velinzon K, Pietzsch J, Ott RG, Anthony RM, Zebroski H, Hurley A (2009) Broad diversity of neutralizing antibodies isolated from memory B cells in HIV-infected individuals. Nature 458:636–640 Scheid JF, Mouquet H, Ueberheide B, Diskin R, Klein F, Oliveira TY, Pietzsch J, Fenyo D, Abadir A, Velinzon K (2011) Sequence and structural convergence of broad and potent HIV antibodies that mimic CD4 binding. Science 333:1633–1637 Sharma SK, de Val N, Bale S, Guenaga J, Tran K, Feng Y, Dubrovskaya V, Ward AB, Wyatt RT (2015) Cleavage-independent HIV-1 Env trimers engineered as soluble native spike mimetics for vaccine design. Cell Rep 11:539–550 Simek MD, Rida W, Priddy FH, Pung P, Carrow E, Laufer DS, Lehrman JK, Boaz M, Tarragona-Fiol T, Miiro G (2009) Human immunodeficiency virus type 1 elite neutralizers: individuals with broad and potent neutralizing activity identified by using a high-throughput neutralization assay together with an analytical selection algorithm. J Virol 83:7337–7348 Sliepen K, Ozorowski G, Burger JA, van Montfort T, Stunnenberg M, LaBranche C, Montefiori DC, Moore JP, Ward AB, Sanders RW (2015) Presenting native-like HIV-1 envelope trimers on ferritin nanoparticles improves their immunogenicity. Retrovirology 12:1–5 Tian R-R, Zhang M-X, Zhang L-T, Zhang X-L, Zheng H-Y, Zhu L, Pang W, Zhang G-H, Zheng Y-T (2015) High immune activation and abnormal expression of cytokines contribute to death of SHIV89. 6-infected Chinese rhesus macaques. Adv Virol 160:1953–1966 Tokatlian T, Read BJ, Jones CA, Kulp DW, Menis S, Chang JY, Steichen JM, Kumari S, Allen JD, Dane EL (2019) Innate immune recognition of glycans targets HIV nanoparticle immunogens to germinal centers. Science 363:649–654 Walker LM, Phogat SK, Chan-Hui P-Y, Wagner D, Phung P, Goss JL, Wrin T, Simek MD, Fling S, Mitcham JL (2009) Broad and potent neutralizing antibodies from an African donor reveal a new HIV-1 vaccine target. Science 326:285–289 Wang W, Liu Z, Zhou X, Guo Z, Zhang J, Zhu P, Yao S, Zhu M (2019) Ferritin nanoparticle-based SpyTag/SpyCatcher-enabled click vaccine for tumor immunotherapy . Nanomed: Nanotechnol Biol Med 16:69–78 Ward AB, Wilson IA (2017) The HIV-1 envelope glycoprotein structure: nailing down a moving target. Immunol Rev 275:21–32 Wu X, Yang Z-Y, Li Y, Hogerkorp C-M, Schief WR, Seaman MS, Zhou T, Schmidt SD, Wu L, Xu L (2010) Rational design of envelope identifies broadly neutralizing human monoclonal antibodies to HIV-1. Science 329:856–861