The current and future role of nanovaccines in HIV-1 vaccine development

References

• Ng’uni T, Chasara C, Ndhlovu ZM. Major scientific hurdles in HIV vaccine development: historical perspective and future directions. Front Immunol. 2020;11:590780.
   PubMed Web of Science ®Google Scholar
• Hsu DC, O’Connell RJ. Progress in HIV vaccine development. Hum Vaccin Immunother. 2017;13(5):1018–1030.
   PubMed Web of Science ®Google Scholar
• Hemelaar J. The origin and diversity of the HIV-1 pandemic. Trends Mol Med. 2012;18(3):182–192.
   PubMed Web of Science ®Google Scholar
• Ventura JD. Human immunodeficiency virus 1 (HIV-1): viral latency, the reservoir, and the cure. Yale J Biol Med. 2020;93(4):549–560.
   PubMed Web of Science ®Google Scholar
• Rios A. Fundamental challenges to the development of a preventive HIV vaccine. Curr Opin Virol. 2018;29:26–32.
   PubMed Web of Science ®Google Scholar
• Amanna IJ, Slifka MK. Successful vaccines. Curr Top Microbiol Immunol. 2020;428:1–30.
   PubMed Web of Science ®Google Scholar
• Klasse PJ, Ozorowski G, Sanders RW, et al. Env exceptionalism: why are HIV-1 Env glycoproteins atypical immunogens? Cell Host Microbe. 2020;27(4):507–518.
   PubMed Web of Science ®Google Scholar
• Del Moral-Sanchez I, Sliepen K. Strategies for inducing effective neutralizing antibody responses against HIV-1. Expert Rev Vaccines. 2019;18(11):1127–1143.
   PubMed Web of Science ®Google Scholar
• Zhu P, Chertova E, Bess J Jr, et al. Electron tomography analysis of envelope glycoprotein trimers on HIV and simian immunodeficiency virus virions. Proc Natl Acad Sci U S A. 2003;100(26):15812–15817.
   PubMed Web of Science ®Google Scholar
• Schiller J, Chackerian B. Why HIV virions have low numbers of envelope spikes: implications for vaccine development. Plos Pathog. 2014;10(8):e1004254.
   PubMed Web of Science ®Google Scholar
• Crispin M, Ward AB, Wilson IA. Structure and immune recognition of the HIV glycan shield. Annu Rev Biophys. 2018;47:499–523.
   PubMed Web of Science ®Google Scholar
• Stefic K, Bouvin-Pley M, Braibant M, et al. Impact of HIV-1 diversity on its sensitivity to neutralization. Vaccines (Basel). 2019;7(3).
   PubMed Web of Science ®Google Scholar
• Pauthner MG, Hangartner L. Broadly neutralizing antibodies to highly antigenically variable viruses as templates for vaccine design. Curr Top Microbiol Immunol. 2020;428:31–87.
   PubMed Web of Science ®Google Scholar
• Doria-Rose NA, Schramm CA, Gorman J, et al. Developmental pathway for potent V1V2-directed HIV-neutralizing antibodies. Nature. 2014;509(7498):55–62.
   PubMed Web of Science ®Google Scholar
• Liao HX, Lynch R, Zhou T, et al. Co-evolution of a broadly neutralizing HIV-1 antibody and founder virus. Nature. 2013;496(7446):469–476.
   PubMed Web of Science ®Google Scholar
• Haynes BF, Burton DR, Mascola JR. Multiple roles for HIV broadly neutralizing antibodies. Sci Transl Med. 2019;11(516).
   Web of Science ®Google Scholar
• Excler JL, Ake J, Robb ML, et al. Nonneutralizing functional antibodies: a new “old” paradigm for HIV vaccines. Clin Vaccine Immunol. 2014;21(8):1023–1036.
   PubMed Web of Science ®Google Scholar
• Rerks-Ngarm S, Pitisuttithum P, Nitayaphan S, et al. Vaccination with ALVAC and AIDSVAX to prevent HIV-1 infection in Thailand. N Engl J Med. 2009;361(23):2209–2220.
   PubMed Web of Science ®Google Scholar
• Haynes BF, Gilbert PB, McElrath MJ, et al. Immune-correlates analysis of an HIV-1 vaccine efficacy trial. N Engl J Med. 2012;366(14):1275–1286.
   PubMed Web of Science ®Google Scholar
• Su B, Dispinseri S, Iannone V, et al. Update on Fc-mediated antibody functions against HIV-1 beyond neutralization. Front Immunol. 2019;10:2968.
   PubMed Web of Science ®Google Scholar
• Korber B, Fischer W. T cell-based strategies for HIV-1 vaccines. Hum Vaccin Immunother. 2020;16(3):713–722.
   PubMed Web of Science ®Google Scholar
• Hel Z, Nacsa J, Tryniszewska E, et al. Containment of simian immunodeficiency virus infection in vaccinated macaques: correlation with the magnitude of virus-specific pre- and postchallenge CD4+ and CD8+ T cell responses. J Immunol. 2002;169(9):4778–4787.
   PubMed Web of Science ®Google Scholar
• Ostrowski MA, Justement SJ, Ehler L, et al. The role of CD4+ T cell help and CD40 ligand in the in vitro expansion of HIV-1-specific memory cytotoxic CD8+ T cell responses. J Immunol. 2000;165(11):6133–6141.
   PubMed Web of Science ®Google Scholar
• Shedlock DJ, Shen H. Requirement for CD4 T cell help in generating functional CD8 T cell memory. Science. 2003;300(5617):337–339.
   PubMed Web of Science ®Google Scholar
• Ahrends T, Busselaar J, Severson TM, et al. CD4(+) T cell help creates memory CD8(+) T cells with innate and help-independent recall capacities. Nat Commun. 2019;10(1):5531.
   PubMedGoogle Scholar
• Mothe B, Brander C. HIV T-cell vaccines. Adv Exp Med Biol. 2018;1075:31–51.
   PubMed Web of Science ®Google Scholar
• Mothe B, Llano A, Ibarrondo J, et al. Definition of the viral targets of protective HIV-1-specific T cell responses. J Transl Med. 2011;9:208.
   PubMed Web of Science ®Google Scholar
• Letourneau S, Im EJ, Mashishi T, et al. Design and pre-clinical evaluation of a universal HIV-1 vaccine. plos One. 2007;2(10):e984.
   PubMed Web of Science ®Google Scholar
• Borthwick N, Ahmed T, Ondondo B, et al. Vaccine-elicited human T cells recognizing conserved protein regions inhibit HIV-1. Mol Ther. 2014;22(2):464–475.
   PubMed Web of Science ®Google Scholar
• Duerr A, Huang Y, Buchbinder S, et al. Extended follow-up confirms early vaccine-enhanced risk of HIV acquisition and demonstrates waning effect over time among participants in a randomized trial of recombinant adenovirus HIV vaccine (Step Study). J Infect Dis. 2012;206(2):258–266.
   PubMed Web of Science ®Google Scholar
• McElrath MJ, De Rosa SC, Moodie Z, et al. HIV-1 vaccine-induced immunity in the test-of-concept step study: a case-cohort analysis. Lancet. 2008;372(9653):1894–1905.
   PubMed Web of Science ®Google Scholar
• Buchbinder SP, Mehrotra DV, Duerr A, et al. Efficacy assessment of a cell-mediated immunity HIV-1 vaccine (the step study): a double-blind, randomised, placebo-controlled, test-of-concept trial. Lancet. 2008;372(9653):1881–1893.
   PubMed Web of Science ®Google Scholar
• Korber BT, Letvin NL, Haynes BF. T-cell vaccine strategies for human immunodeficiency virus, the virus with a thousand faces. J Virol. 2009;83(17):8300–8314.
   PubMed Web of Science ®Google Scholar
• Fischer W, Perkins S, Theiler J, et al. Polyvalent vaccines for optimal coverage of potential T-cell epitopes in global HIV-1 variants. Nat Med. 2007;13(1):100–106.
   PubMed Web of Science ®Google Scholar
• Barouch DH, O’Brien KL, Simmons NL, et al. Mosaic HIV-1 vaccines expand the breadth and depth of cellular immune responses in rhesus monkeys. Nat Med. 2010;16(3):319–323.
   PubMed Web of Science ®Google Scholar
• Santra S, Liao HX, Zhang R, et al. Mosaic vaccines elicit CD8+ T lymphocyte responses that confer enhanced immune coverage of diverse HIV strains in monkeys. Nat Med. 2010;16(3):324–328.
   PubMed Web of Science ®Google Scholar
• Nkolola JP, Bricault CA, Cheung A, et al. Characterization and immunogenicity of a novel mosaic M HIV-1 gp140 trimer. J Virol. 2014;88(17):9538–9552.
   PubMed Web of Science ®Google Scholar
• Excler JL, Kim JH. Novel prime-boost vaccine strategies against HIV-1. Expert Rev Vaccines. 2019;18(8):765–779.
   PubMed Web of Science ®Google Scholar
• Haynes BF, Kelsoe G, Harrison SC, et al. B-cell-lineage immunogen design in vaccine development with HIV-1 as a case study. Nat Biotechnol. 2012;30(5):423–433.
   PubMed Web of Science ®Google Scholar
• Kang CY, Gao Y. Killed whole-HIV vaccine; employing a well established strategy for antiviral vaccines. AIDS Res Ther. 2017;14(1):47.
   PubMedGoogle Scholar
• Doll TA, Raman S, Dey R, et al. Nanoscale assemblies and their biomedical applications. J R Soc Interface. 2013;10(80):20120740.
   PubMed Web of Science ®Google Scholar
• Kelly HG, Kent SJ, Wheatley AK. Immunological basis for enhanced immunity of nanoparticle vaccines. Expert Rev Vaccines. 2019;18(3):269–280.
   PubMed Web of Science ®Google Scholar
• Zaheer T, Pal K, Zaheer I. Topical review on nano-vaccinology: biochemical promises and key challenges. Process Biochem. 2021;100:237-244.
   PubMed Web of Science ®Google Scholar
• Facciola A, Visalli G, Lagana P, et al. The new era of vaccines: the “nanovaccinology.” Eur Rev Med Pharmacol Sci. 2019;23(16):7163–7182.
   PubMed Web of Science ®Google Scholar
• Irvine DJ, Read BJ. Shaping humoral immunity to vaccines through antigen-displaying nanoparticles. Curr Opin Immunol. 2020;65:1–6./mixed-citation>
   PubMed Web of Science ®Google Scholar
• Karch CP, Burkhard P. Vaccine technologies: from whole organisms to rationally designed protein assemblies. Biochem Pharmacol. 2016;120:1–14.
   PubMed Web of Science ®Google Scholar
• Butkovich N, Li E, Ramirez A, et al. Advancements in protein nanoparticle vaccine platforms to combat infectious disease. Wiley Interdiscip Rev Nanomed Nanobiotechnol. 2020;13:e1681.
   PubMed Web of Science ®Google Scholar
• Roldao A, Mellado MC, Castilho LR, et al. Virus-like particles in vaccine development. Expert Rev Vaccines. 2010;9(10):1149–1176.
   PubMed Web of Science ®Google Scholar
• Donaldson B, Lateef Z, Walker GF, et al. Virus-like particle vaccines: immunology and formulation for clinical translation. Expert Rev Vaccines. 2018;17(9):833–849.
   PubMed Web of Science ®Google Scholar
• Weis F, Beckers M, von der Hocht I, et al. Elucidation of the viral disassembly switch of tobacco mosaic virus. EMBO Rep. 2019;20(11):e48451.
   PubMed Web of Science ®Google Scholar
• Zhang X, Meining W, Fischer M, et al. X-ray structure analysis and crystallographic refinement of lumazine synthase from the hyperthermophile aquifex aeolicus at 1.6 A resolution: determinants of thermostability revealed from structural comparisons. J Mol Biol. 2001;306(5):1099–1114.
   PubMed Web of Science ®Google Scholar
• Karch CP, Matyas GR, Burkhard P, et al. Self-assembling protein nanoparticles: implications for HIV-1 vaccine development. Nanomedicine (Lond). 2018;13(17):2121–2125.
   PubMed Web of Science ®Google Scholar
• El Bissati K, Zhou Y, Paulillo SM, et al. Engineering and characterization of a novel self assembling protein for toxoplasma peptide vaccine in HLA-A*11:01, HLA-A*02:01 and HLA-B*07:02 transgenic mice. Sci Rep. 2020;10(1):16984.
   PubMed Web of Science ®Google Scholar
• Karch CP, Li J, Kulangara C, et al. Vaccination with self-adjuvanted protein nanoparticles provides protection against lethal influenza challenge. Nanomedicine. 2017;13(1):241–251.
   PubMed Web of Science ®Google Scholar
• Kaba SA, Karch CP, Seth L, et al. Self-assembling protein nanoparticles with built-in flagellin domains increases protective efficacy of a Plasmodium falciparum based vaccine. Vaccine. 2018;36(6):906–914.
   PubMed Web of Science ®Google Scholar
• Nisini R, Poerio N, Mariotti S, et al. The multirole of liposomes in therapy and prevention of infectious diseases. Front Immunol. 2018;9(155):1–29.
   PubMedGoogle Scholar
• Alving CR, Beck Z, Matyas GR, et al. Liposomal adjuvants for human vaccines. Expert Opin Drug Deliv. 2016;13(6):807–816.
   PubMed Web of Science ®Google Scholar
• Filipczak N, Pan J, Yalamarty SSK, et al. Recent advancements in liposome technology. Adv Drug Deliv Rev. 2020;156:4-22.
   PubMed Web of Science ®Google Scholar
• Alving CR, Peachman KK, Matyas GR, et al. Army liposome formulation (ALF) family of vaccine adjuvants. Expert Rev Vaccines. 2020;19(3):279–292.
   PubMed Web of Science ®Google Scholar
• Corthesy B, Bioley G. Lipid-based particles: versatile delivery systems for mucosal vaccination against infection. Front Immunol. 2018;9:1-20.
   Web of Science ®Google Scholar
• Kim J, Eygeris Y, Gupta M, et al. Self-assembled mRNA vaccines. Adv Drug Deliv Rev. 2021;170:83–112.
   PubMed Web of Science ®Google Scholar
• Tejeda-Mansir A, Garcia-Rendon A, Guerrero-German P. Plasmid-DNA lipid and polymeric nanovaccines: a new strategic in vaccines development. Biotechnol Genet Eng Rev. 2019;35(1):46–68.
   PubMed Web of Science ®Google Scholar
• Kraft JC, Freeling JP, Wang Z, et al. Emerging research and clinical development trends of liposome and lipid nanoparticle drug delivery systems. J Pharm Sci. 2014;103(1):29–52.
   PubMed Web of Science ®Google Scholar
• Samaridou E, Heyes J, Lutwyche P. Lipid nanoparticles for nucleic acid delivery: current perspectives. Adv Drug Deliv Rev. 2020;154-155:37–63.
   PubMed Web of Science ®Google Scholar
• Karch CP, Bai H, Torres OB, et al. Design and characterization of a self-assembling protein nanoparticle displaying HIV-1 Env V1V2 loop in a native-like trimeric conformation as vaccine antigen. Nanomedicine. 2019;16:206–216.
   PubMed Web of Science ®Google Scholar
• Shao S, Huang WC, Lin C, et al. An engineered biomimetic MPER peptide vaccine induces weakly HIV neutralizing antibodies in mice. Ann Biomed Eng. 2020;48(7):1991–2001.
   PubMed Web of Science ®Google Scholar
• Ingale J, Stano A, Guenaga J, et al. High-density array of well-ordered HIV-1 spikes on synthetic liposomal nanoparticles efficiently activate B cells. Cell Rep. 2016;15(9):1986–1999.
   PubMed Web of Science ®Google Scholar
• Brouwer PJM, Antanasijevic A, Berndsen Z, et al. Enhancing and shaping the immunogenicity of native-like HIV-1 envelope trimers with a two-component protein nanoparticle. Nat Commun. 2019;10(1):4272.
   PubMedGoogle Scholar
• Sanders RW, Derking R, Cupo A, et al. 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. 2013;9(9):e1003618.
   PubMed Web of Science ®Google Scholar
• Sok D, Burton DR. Recent progress in broadly neutralizing antibodies to HIV. Nat Immunol. 2018;19(11):1179–1188.
   PubMed Web of Science ®Google Scholar
• Sanders RW, Moore JP. Native-like Env trimers as a platform for HIV-1 vaccine design. Immunol Rev. 2017;275(1):161–182.
   PubMed Web of Science ®Google Scholar
• Escolano A, Dosenovic P, Nussenzweig MC. Progress toward active or passive HIV-1 vaccination. J Exp Med. 2017;214(1):3–16.
   PubMed Web of Science ®Google Scholar
• Dey AK, Cupo A, Ozorowski G, et al. cGMP production and analysis of BG505 SOSIP.664, an extensively glycosylated, trimeric HIV-1 envelope glycoprotein vaccine candidate. Biotechnol Bioeng. 2018;115(4):885–899.
   PubMed Web of Science ®Google Scholar
• Sliepen K, Ozorowski G, Burger JA, et al. Presenting native-like HIV-1 envelope trimers on ferritin nanoparticles improves their immunogenicity. Retrovirology. 2015;12(82):1–5.
   PubMedGoogle Scholar
• He L, De Val N, Morris CD, et al. Presenting native-like trimeric HIV-1 antigens with self-assembling nanoparticles. Nat Commun. 2016;7(12041):1–36.
   Google Scholar
• Antanasijevic A, Ueda G, Brouwer PJM, et al. Structural and functional evaluation of de novo-designed, two-component nanoparticle carriers for HIV Env trimer immunogens. PLoS Pathog. 2020;16(8):e1008665.
   PubMed Web of Science ®Google Scholar
• Karch CP, Paquin-Proulx D, Eller MA, et al. Impact of the expression system on the immune responses to self-assembling protein nanoparticles (SAPNs) displaying HIV-1 V1V2 loop. Nanomedicine. 2020;29(102255):1–13.
   PubMedGoogle Scholar
• Bachmann MF, Zinkernagel RM. Neutralizing antiviral B cell responses. Annu Rev Immunol. 1997;15:235–270.
   PubMed Web of Science ®Google Scholar
• Vogelstein B, Dintzis RZ, Dintzis HM. Specific cellular stimulation in the primary immune response: a quantized model. Proc Natl Acad Sci U S A. 1982;79(2):395–399.
   PubMed Web of Science ®Google Scholar
• Dobrovolskaia MA, Aggarwal P, Hall JB, et al. Preclinical studies to understand nanoparticle interaction with the immune system and its potential effects on nanoparticle biodistribution. Mol Pharm. 2008;5(4):487–495.
   PubMed Web of Science ®Google Scholar
• Brinkkemper M, Sliepen K. Nanoparticle vaccines for inducing HIV-1 neutralizing antibodies. Vaccines (Basel). 2019;7(3):1–14.
   PubMed Web of Science ®Google Scholar
• Crooks ET, Osawa K, Tong T, et al. Effects of partially dismantling the CD4 binding site glycan fence of HIV-1 envelope glycoprotein trimers on neutralizing antibody induction. Virology. 2017;505:193–209.
   PubMed Web of Science ®Google Scholar
• Crooks ET, Tong T, Chakrabarti B, et al. Vaccine-elicited tier 2 HIV-1 neutralizing antibodies bind to quaternary epitopes involving glycan-deficient patches proximal to the CD4 binding site. PLoS Pathog. 2015;11(5):e1004932.
   PubMed Web of Science ®Google Scholar
• Kim M, Qiao Z, Yu J, et al. Immunogenicity of recombinant human immunodeficiency virus type 1-like particles expressing gp41 derivatives in a pre-fusion state. Vaccine. 2007;25(27):5102–5114.
   PubMed Web of Science ®Google Scholar
• Wagner R, Deml L, Schirmbeck R, et al. Construction, expression, and immunogenicity of chimeric HIV-1 virus-like particles. Virology. 1996;220(1):128–140.
   PubMed Web of Science ®Google Scholar
• Griffiths JC, Harris SJ, Layton GT, et al. Hybrid human immunodeficiency virus Gag particles as an antigen carrier system: induction of cytotoxic T-cell and humoral responses by a Gag: V3fusion. J Virol. 1993;67(6):3191–3198.
   PubMed Web of Science ®Google Scholar
• Tagliamonte M, Visciano ML, Tornesello ML, et al. HIV-Gag VLPs presenting trimeric HIV-1 gp140 spikes constitutively expressed in stable double transfected insect cell line. Vaccine. 2011;29(31):4913–4922.
   PubMed Web of Science ®Google Scholar
• Buonaguro L, Buonaguro FM, Tornesello ML, et al. High efficient production of Pr55(gag) virus-like particles expressing multiple HIV-1 epitopes, including a gp120 protein derived from an Ugandan HIV-1 isolate of subtype A. Antiviral Res. 2001;49(1):35–47.
   PubMed Web of Science ®Google Scholar
• Chen CW, Saubi N, Joseph-Munne J. Design concepts of virus-like particle-based HIV-1 vaccines. Front Immunol. 2020;11(573157):1–8.
   Google Scholar
• Deml L, Schirmbeck R, Reimann J, et al. Recombinant human immunodeficiency Pr55gag virus-like particles presenting chimeric envelope glycoproteins induce cytotoxic T-cells and neutralizing antibodies. Virology. 1997;235(1):26–39.
   PubMed Web of Science ®Google Scholar
• Haffar OK, Smithgall MD, Moran PA, et al. HIV-specific humoral and cellular immunity in rabbits vaccinated with recombinant human immunodeficiency virus-like gag-env particles. Virology. 1991;183(2):487–495.
   PubMed Web of Science ®Google Scholar
• Buonaguro L, Racioppi L, Tornesello ML, et al. Induction of neutralizing antibodies and cytotoxic T lymphocytes in Balb/c mice immunized with virus-like particles presenting a gp120 molecule from a HIV-1 isolate of clade A. Antiviral Res. 2002;54(3):189–201.
   PubMed Web of Science ®Google Scholar
• Rovinski B, Rodrigues L, Cao SX, et al. Induction of HIV type 1 neutralizing and env-CD4 blocking antibodies by immunization with genetically engineered HIV type 1-like particles containing unprocessed gp160 glycoproteins. AIDS Res Hum Retroviruses. 1995;11(10):1187–1195.
   PubMed Web of Science ®Google Scholar
• Kang CY, Luo L, Wainberg MA, et al. Development of HIV/AIDS vaccine using chimeric gag-env virus-like particles. Biol Chem. 1999;380(3):353–364.
   PubMed Web of Science ®Google Scholar
• Pastori C, Tudor D, Diomede L, et al. Virus like particle based strategy to elicit HIV-protective antibodies to the alpha-helic regions of gp41. Virology. 2012;431(1–2):1–11.
   PubMed Web of Science ®Google Scholar
• Zhai Y, Zhong Z, Zariffard M, et al. Bovine papillomavirus-like particles presenting conserved epitopes from membrane-proximal external region of HIV-1 gp41 induced mucosal and systemic antibodies. Vaccine. 2013;31(46):5422–5429.
   PubMed Web of Science ®Google Scholar
• Demchuk AM, Patel TR. The biomedical and bioengineering potential of protein nanocompartments. Biotechnol Adv. 2020;41(107547):1–21.
   PubMedGoogle Scholar
• Sliepen K, Han BW, Bontjer I, et al. Structure and immunogenicity of a stabilized HIV-1 envelope trimer based on a group-M consensus sequence. Nat Commun. 2019;10(1):2355.
   PubMed Web of Science ®Google Scholar
• Georgiev IS, Joyce MG, Chen RE, et al. Two-component ferritin nanoparticles for multimerization of diverse trimeric antigens. ACS Infect Dis. 2018;4(5):788–796.
   PubMed Web of Science ®Google Scholar
• Ladenstein R, Morgunova E. Second career of a biosynthetic enzyme: lumazine synthase as a virus-like nanoparticle in vaccine development. Biotechnol Rep (Amst). 2020;27(e00494):1–21.
   PubMedGoogle Scholar
• Jardine J, Julien JP, Menis S, et al. Rational HIV immunogen design to target specific germline B cell receptors. Science. 2013;340(6133):711–716.
   PubMed Web of Science ®Google Scholar
• Jardine JG, Ota T, Sok D, et al. HIV-1 VACCINES. Priming a broadly neutralizing antibody response to HIV-1 using a germline-targeting immunogen. Science. 2015;349(6244):156–161.
   PubMed Web of Science ®Google Scholar
• Gao Y, Wijewardhana C, Mann JFS. Virus-like particle, liposome, and polymeric particle-based vaccines against HIV-1. Front Immunol. 2018;9:345.
   PubMed Web of Science ®Google Scholar
• Zwick MB, Labrijn AF, Wang M, et al. Broadly neutralizing antibodies targeted to the membrane-proximal external region of human immunodeficiency virus type 1 glycoprotein gp41. J Virol. 2001;75(22):10892–10905.
   PubMed Web of Science ®Google Scholar
• Muster T, Steindl F, Purtscher M, et al. A conserved neutralizing epitope on gp41 of human immunodeficiency virus type 1. J Virol. 1993;67(11):6642–6647.
   PubMed Web of Science ®Google Scholar
• Caillat C, Guilligay D, Sulbaran G, et al. Neutralizing antibodies targeting HIV-1 gp41. Viruses. 2020;12(11):1–19.
   PubMed Web of Science ®Google Scholar
• Matyas GR, Wieczorek L, Beck Z, et al. Neutralizing antibodies induced by liposomal HIV-1 glycoprotein 41 peptide simultaneously bind to both the 2F5 or 4E10 epitope and lipid epitopes. AIDS. 2009;23(16):2069–2077.
   PubMed Web of Science ®Google Scholar
• Lai RP, Hock M, Radzimanowski J, et al. A fusion intermediate gp41 immunogen elicits neutralizing antibodies to HIV-1. J Biol Chem. 2014;289(43):29912–29926.
   PubMed Web of Science ®Google Scholar
• Bomsel M, Tudor D, Drillet AS, et al. Immunization with HIV-1 gp41 subunit virosomes induces mucosal antibodies protecting nonhuman primates against vaginal SHIV challenges. Immunity. 2011;34(2):269–280.
   PubMed Web of Science ®Google Scholar
• Leroux-Roels G, Maes C, Clement F, et al. Randomized phase I: safety, immunogenicity and mucosal antiviral activity in young healthy women vaccinated with HIV-1 Gp41 P1 peptide on virosomes. Plos One. 2013;8(2):e55438.
   PubMed Web of Science ®Google Scholar
• Dubrovskaya V, Tran K, Ozorowski G, et al. Vaccination with glycan-modified HIV NFL envelope trimer-liposomes elicits broadly neutralizing antibodies to multiple sites of vulnerability. Immunity. 2019;51(5):915–929 e917.
   PubMed Web of Science ®Google Scholar
• Pardi N, Hogan MJ, Weissman D. Recent advances in mRNA vaccine technology. Curr Opin Immunol. 2020;65:14–20.
   PubMed Web of Science ®Google Scholar
• Pardi N, LaBranche CC, Ferrari G, et al. Characterization of HIV-1 nucleoside-modified mRNA vaccines in rabbits and rhesus macaques. Mol Ther Nucleic Acids. 2019;15:36–47.
   PubMedGoogle Scholar
• Saunders KO, Pardi N, Parks R, et al. Lipid nanoparticle encapsulated nucleoside-modified mRNA vaccines elicit polyfunctional HIV-1 antibodies comparable to proteins in nonhuman primates. NPJ Vaccines. 2021;6(1):50.
   PubMed Web of Science ®Google Scholar
• Lewis GK, Ackerman ME, Scarlatti G, et al. Knowns and unknowns of assaying antibody-dependent cell-mediated cytotoxicity against HIV-1. Front Immunol. 2019;10(1025):1–12.
   Google Scholar
• Sips M, Krykbaeva M, Diefenbach TJ, et al. Fc receptor-mediated phagocytosis in tissues as a potent mechanism for preventive and therapeutic HIV vaccine strategies. Mucosal Immunol. 2016;9(6):1584–1595.
   PubMed Web of Science ®Google Scholar
• Mujib S, Liu J, Rahman A, et al. Comprehensive cross-clade characterization of antibody-mediated recognition, complement-mediated lysis, and cell-mediated cytotoxicity of HIV-1 envelope-specific antibodies toward eradication of the HIV-1 reservoir. J Virol. 2017;91:16.
   Web of Science ®Google Scholar
• Tay MZ, Liu P, Williams LD, et al. Antibody-mediated internalization of infectious HIV-1 virions differs among antibody isotypes and subclasses. PLoS Pathog. 2016;12(8):e1005817.
   PubMed Web of Science ®Google Scholar
• von Bredow B, Arias JF, Heyer LN, et al. Comparison of antibody-dependent cell-mediated cytotoxicity and virus neutralization by HIV-1 env-specific monoclonal antibodies. J Virol. 2016;90(13):6127–6139.
   PubMed Web of Science ®Google Scholar
• Hessell AJ, Jaworski JP, Epson E, et al. Early short-term treatment with neutralizing human monoclonal antibodies halts SHIV infection in infant macaques. Nat Med. 2016;22(4):362–368.
   PubMed Web of Science ®Google Scholar
• Liu J, Ghneim K, Sok D, et al. Antibody-mediated protection against SHIV challenge includes systemic clearance of distal virus. Science. 2016;353(6303):1045–1049.
   PubMed Web of Science ®Google Scholar
• Parsons MS, Lee WS, Kristensen AB, et al. Fc-dependent functions are redundant to efficacy of anti-HIV antibody PGT121 in macaques. J Clin Invest. 2019;129(1):182–191.
   PubMed Web of Science ®Google Scholar
• Asokan M, Dias J, Liu C, et al. Fc-mediated effector function contributes to the in vivo antiviral effect of an HIV neutralizing antibody. Proc Natl Acad Sci U S A. 2020;117(31):18754–18763.
   PubMed Web of Science ®Google Scholar
• Wang P, Gajjar MR, Yu J, et al. Quantifying the contribution of Fc-mediated effector functions to the antiviral activity of anti-HIV-1 IgG1 antibodies in vivo. Proc Natl Acad Sci U S A. 2020;117(30):18002–18009.
   PubMed Web of Science ®Google Scholar
• Yang L, Song Y, Li X, et al. HIV-1 virus-like particles produced by stably transfected Drosophila S2 cells: a desirable vaccine component. J Virol. 2012;86(14):7662–7676.
   PubMed Web of Science ®Google Scholar
• Zhao C, Ao Z, Yao X. Current advances in virus-like particles as a vaccination approach against HIV infection. Vaccines (Basel). 2016;4(1):1–20.
   PubMed Web of Science ®Google Scholar
• Franco D, Liu W, Gardiner DF, et al. CD40L-containing virus-like particle as a candidate HIV-1 vaccine targeting dendritic cells. J Acquir Immune Defic Syndr. 2011;56(5):393–400.
   PubMed Web of Science ®Google Scholar
• Zhang R, Zhang S, Li M, et al. Incorporation of CD40 ligand into SHIV virus-like particles (VLP) enhances SHIV-VLP-induced dendritic cell activation and boosts immune responses against HIV. Vaccine. 2010;28(31):5114–5127.
   PubMed Web of Science ®Google Scholar
• Kwa S, Lai L, Gangadhara S, et al. CD40L-adjuvanted DNA/modified vaccinia virus Ankara simian immunodeficiency virus SIV239 vaccine enhances SIV-specific humoral and cellular immunity and improves protection against a heterologous SIVE660 mucosal challenge. J Virol. 2014;88(17):9579–9589.
   PubMed Web of Science ®Google Scholar
• Gangadhara S, Kwon YM, Jeeva S, et al. Vaccination with combination DNA and virus-like particles enhances humoral and cellular immune responses upon boost with recombinant modified vaccinia virus ankara expressing human immunodeficiency virus envelope proteins. Vaccines (Basel). 2017;5(4):1–14.
   PubMed Web of Science ®Google Scholar
• Huang X, Zhu Q, Huang X, et al. In vivo electroporation in DNA-VLP prime-boost preferentially enhances HIV-1 envelope-specific IgG2a, neutralizing antibody and CD8 T cell responses. Vaccine. 2017;35(16):2042–2051.
   PubMed Web of Science ®Google Scholar
• Poteet E, Lewis P, Li F, et al. A novel prime and boost regimen of HIV virus-like particles with TLR4 adjuvant MPLA induces Th1 oriented immune responses against HIV. PLoS One. 2015;10(8):e0136862.
   PubMed Web of Science ®Google Scholar
• Iyer SS, Gangadhara S, Victor B, et al. Virus-like particles displaying trimeric simian immunodeficiency virus (SIV) envelope gp160 enhance the breadth of DNA/modified vaccinia virus ankara SIV vaccine-induced antibody responses in rhesus macaques. J Virol. 2016;90(19):8842–8854.
   PubMed Web of Science ®Google Scholar
• Pillay S, Shephard EG, Meyers AE, et al. HIV-1 subtype C chimaeric VLPs boost cellular immune responses in mice. J Immune Based Ther Vaccines. 2010;8(7):1–6.
   PubMedGoogle Scholar
• Moyo N, Wee EG, Korber B, et al. Tetravalent immunogen assembled from conserved regions of HIV-1 and delivered as mRNA Demonstrates potent preclinical T-cell immunogenicity and breadth. Vaccines (Basel). 2020;8(3):1–10.
   Web of Science ®Google Scholar
• Moyo N, Vogel AB, Buus S, et al. Efficient induction of T cells against conserved HIV-1 regions by Mosaic vaccines delivered as self-amplifying mRNA. Mol Ther Methods Clin Dev. 2019;12:32–46.
   PubMed Web of Science ®Google Scholar
• Ahmad N, Khan MA, Owais M. Liposome mediated antigen delivery leads to induction of CD8+ T lymphocyte and antibody responses against the V3 loop region of HIV gp120. Cell Immunol. 2001;210(1):49–55.
   PubMed Web of Science ®Google Scholar
• Steers NJ, Peachman KK, McClain S, et al. Liposome-encapsulated HIV-1 Gag p24 containing lipid A induces effector CD4+ T-cells, memory CD8+ T-cells, and pro-inflammatory cytokines. Vaccine. 2009;27(49):6939–6949.
   PubMed Web of Science ®Google Scholar
• Hanke T. Aiming for protective T-cell responses: a focus on the first generation conserved-region HIVconsv vaccines in preventive and therapeutic clinical trials. Expert Rev Vaccines. 2019;18(10):1029–1041.
   PubMed Web of Science ®Google Scholar
• Rao M, Alving CR. Adjuvants for HIV vaccines. Curr Opin HIV AIDS. 2016;11(6):585–592.
   PubMed Web of Science ®Google Scholar
• Ratnapriya S, Perez-Greene E, Schifanella L, et al. Adjuvant-mediated enhancement of the immune response to HIV vaccines. FEBS J. 2021:1–18.
   PubMed Web of Science ®Google Scholar
• Alving CR, Peachman KK, Rao M, et al. Adjuvants for human vaccines. Curr Opin Immunol. 2012;24(3):310–315.
   PubMed Web of Science ®Google Scholar
• Kasturi SP, Rasheed MAU, Havenar-Daughton C, et al. 3M-052, a synthetic TLR-7/8 agonist, induces durable HIV-1 envelope-specific plasma cells and humoral immunity in nonhuman primates. Sci Immunol. 2020;5:48.
   Web of Science ®Google Scholar