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Review

Novel prime-boost vaccine strategies against HIV-1

ORCID Icon & ORCID Icon
Pages 765-779 | Received 23 Jan 2019, Accepted 02 Jul 2019, Published online: 09 Jul 2019

References

  • UNAIDS. Miles to go. Switzerland: Geneva; 2018.
  • UNAIDS data. Switzerland: Geneva; 2018.
  • Fauci AS. An HIV vaccine is essential for ending the HIV/AIDS pandemic. JAMA. 2017;318(16):1535–1536.
  • Eisinger RW, Fauci AS. Ending the HIV/AIDS pandemic. Emerg Infect Dis. 2018;24(3):413–416.
  • Institute for Health Metrics and Evaluation. Financing Global Health. Funding universal health coverage and the unfinished HIV/AIDS agenda. Seattle WA, USA: University of Washington; 2017.
  • UNAIDS. Fact sheet – World AIDS Day 2018.
  • Harmon TM, Fisher KA, McGlynn MG, et al. Exploring the potential health impact and cost-effectiveness of AIDS vaccine within a comprehensive HIV/AIDS response in low- and middle-income countries. PLoS One. 2016;11(1):e0146387.
  • Dimitrov D, Kublin JG, Ramsey S, et al. Are clade specific HIV vaccines a necessity? An analysis based on mathematical models. EBioMedicine. 2015;2(12):2062–2069.
  • de Montigny S, Adamson BJS, Masse BR, et al. Projected effectiveness and added value of HIV vaccination campaigns in South Africa: a modeling study. Sci Rep. 2018;8(1):6066.
  • Hsu DC, O’Connell RJ. Progress in HIV vaccine development. Hum Vaccin Immunother. 2017;13(5):1018–1030.
  • Stephenson KE, D’Couto HT, Barouch DH. New concepts in HIV-1 vaccine development. Curr Opin Immunol. 2016;41:39–46.
  • Alayo QA, Provine NM, Penaloza-MacMaster P. Novel concepts for HIV vaccine vector design. mSphere. 2017;2(6):e00415–e17.
  • Excler JL, Robb ML, Kim JH. HIV-1 vaccines: challenges and new perspectives. Hum Vaccin Immunother. 2014;10(6):1734–1746.
  • Excler JL, Robb ML, Kim JH. Prospects for a globally effective HIV-1 vaccine. Vaccine. 2015;33(Suppl 4):D4–D12.
  • Excler JL, Tomaras GD, Russell ND. Novel directions in HIV-1 vaccines revealed from clinical trials. Curr Opin HIV AIDS. 2013;8(5):421–431.
  • Gao Y, McKay PF, Mann JFS. Advances in HIV-1 vaccine development. Viruses. 2018;10(4):167.
  • Kardani K, Bolhassani A, Shahbazi S. Prime-boost vaccine strategy against viral infections: mechanisms and benefits. Vaccine. 2016;34(4):413–423.
  • Lu S. Heterologous prime-boost vaccination. Curr Opin Immunol. 2009;21(3):346–351.
  • Ramshaw IA, Ramsay AJ. The prime-boost strategy: exciting prospects for improved vaccination. Immunol Today. 2000;21(4):163–165.
  • Excler JL, Plotkin S. The prime-boost concept applied to HIV preventive vaccines. AIDS. 1997;11(Suppl A):S127–S137.
  • Plotkin SA. Vaccines: correlates of vaccine-induced immunity. Clin Infect Dis. 2008;47(3):401–409.
  • Streeck H, D’Souza MP, Littman DR, et al. Harnessing CD4(+) T cell responses in HIV vaccine development. Nat Med. 2013;19(2):143–149.
  • Havenar-Daughton C, Carnathan DG, Torrents de la Pena A, et al. Direct probing of germinal center responses reveals immunological features and bottlenecks for neutralizing antibody responses to HIV env trimer. Cell Rep. 2016;17(9):2195–2209.
  • Khurana S, Coyle EM, Dimitrova M, et al. Heterologous prime-boost vaccination with MF59-adjuvanted H5 vaccines promotes antibody affinity maturation towards the hemagglutinin HA1 domain and broad H5N1 cross-clade neutralization. PLoS One. 2014;9(4):e95496.
  • Gamble LJ, Matthews QL. Current progress in the development of a prophylactic vaccine for HIV-1. Drug Des Devel Ther. 2010;5:9–26.
  • Hemelaar J, Elangovan R, Yun J, et al. Global and regional molecular epidemiology of HIV-1, 1990-2015: a systematic review, global survey, and trend analysis. Lancet Infect Dis. 2019;19(2):143–155.
  • Phanuphak N, Lo YR, Shao Y, et al. HIV epidemic in Asia: implications for HIV vaccine and other prevention trials. AIDS Res Hum Retroviruses. 2015;31(11):1060–1076.
  • McCoy LE. The expanding array of HIV broadly neutralizing antibodies. Retrovirology. 2018;15(1):70.
  • Sok D, Burton DR. Recent progress in broadly neutralizing antibodies to HIV. Nat Immunol. 2018;19(11):1179–1188.
  • 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.
  • 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.
  • Alter G, Barouch D. Immune correlate-guided HIV vaccine design. Cell Host Microbe. 2018;24(1):25–33.
  • 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.
  • Robb ML, Rerks-Ngarm S, Nitayaphan S, et al. Risk behaviour and time as covariates for efficacy of the HIV vaccine regimen ALVAC-HIV (vCP1521) and AIDSVAX B/E: a post-hoc analysis of the Thai phase 3 efficacy trial RV 144. Lancet Infect Dis. 2012;12(7):531–537.
  • Montefiori DC, Karnasuta C, Huang Y, et al. Magnitude and breadth of the neutralizing antibody response in the RV144 and Vax003 HIV-1 vaccine efficacy trials. J Infect Dis. 2012;206(3):431–441.
  • Rerks-Ngarm S, Paris RM, Chunsutthiwat S, et al. Extended evaluation of the virologic, immunologic, and clinical course of volunteers who acquired HIV-1 infection in a phase III vaccine trial of ALVAC-HIV and AIDSVAX B/E. J Infect Dis. 2013;207(8):1195–1205.
  • 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.
  • Vasan S, Rerks-Ngarm S, Gilbert P, et al. Letter to the editor on: the RV144 vaccine regimen was not associated with enhancement of infection. Hum Vaccin Immunother. 2015;11(4):1036–1037.
  • O’Connell RJ, Excler JL. HIV vaccine efficacy and immune correlates of risk. Curr HIV Res. 2013;11(6):450–463.
  • Kim JH, Excler JL, Michael NL. Lessons from the RV144 thai phase III HIV-1 vaccine trial and the search for correlates of protection. Annu Rev Med. 2015;66:423–437.
  • Corey L, Gilbert PB, Tomaras GD, et al. Immune correlates of vaccine protection against HIV-1 acquisition. Sci Transl Med. 2015;7(310):310rv317.
  • Tomaras GD, Plotkin SA. Complex immune correlates of protection in HIV-1 vaccine efficacy trials. Immunol Rev. 2017;275(1):245–261.
  • Rolland M, Edlefsen PT, Larsen BB, et al. Increased HIV-1 vaccine efficacy against viruses with genetic signatures in Env V2. Nature. 2012;490(7420):417–420.
  • Zolla-Pazner S, deCamp AC, Cardozo T, et al. Analysis of V2 antibody responses induced in vaccinees in the ALVAC/AIDSVAX HIV-1 vaccine efficacy trial. PLoS One. 2013;8(1):e53629.
  • Zolla-Pazner S, Decamp A, Gilbert PB, et al. Vaccine-induced IgG antibodies to V1V2 regions of multiple HIV-1 subtypes correlate with decreased risk of HIV-1 infection. PLoS One. 2014;9(2):e87572.
  • Liao HX, Bonsignori M, Alam SM, et al. 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.
  • Chung AW, Ghebremichael M, Robinson H, et al. Polyfunctional Fc-effector profiles mediated by IgG subclass selection distinguish RV144 and VAX003 vaccines. Sci Transl Med. 2014;6(228):228ra238.
  • 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.
  • Yates NL, Liao HX, Fong Y, et al. Vaccine-induced env V1-V2 IgG3 correlates with lower HIV-1 infection risk and declines soon after vaccination. Sci Transl Med. 2014;6(228):228ra239.
  • Perez LG, Martinez DR, deCamp AC, et al. V1V2-specific complement activating serum IgG as a correlate of reduced HIV-1 infection risk in RV144. PLoS One. 2017;12(7):e0180720.
  • Liu P, Yates NL, Shen X, et al. Infectious virion capture by HIV-1 gp120-specific IgG from RV144 vaccinees. J Virol. 2013;87(14):7828–7836.
  • Fahrbach KM, Malykhina O, Stieh DJ, et al. Differential binding of IgG and IgA to mucus of the female reproductive tract. PLoS One. 2013;8(10):e76176.
  • Gunn B, Schneider J, Shansab M, et al. Enhanced binding of antibodies generated during chronic HIV infection to mucus component MUC16. Mucosal Immunol. 2016;9(6):1549–1558.
  • Wines BD, Billings H, McLean MR, et al. Antibody functional assays as measures of Fc receptor-mediated immunity to HIV – new technologies and their impact on the HIV vaccine field. Curr HIV Res. 2017;15(3):202–215.
  • Huang Y, Ferrari G, Alter G, et al. Diversity of antiviral IgG effector activities observed in HIV-infected and vaccinated subjects. J Immunol. 2016;197(12):4603–4612.
  • Tomaras GD, Ferrari G, Shen X, et al. Vaccine-induced plasma IgA specific for the C1 region of the HIV-1 envelope blocks binding and effector function of IgG. Proc Natl Acad Sci U S A. 2013;110(22):9019–9024.
  • Gottardo R, Bailer RT, Korber BT, et al. Plasma IgG to linear epitopes in the V2 and V3 regions of HIV-1 gp120 correlate with a reduced risk of infection in the RV144 vaccine efficacy trial. PLoS One. 2013;8(9):e75665.
  • Zolla-Pazner S, Edlefsen PT, Rolland M, et al. Vaccine-induced human antibodies specific for the third variable region of HIV-1 gp120 impose immune pressure on infecting viruses. EBioMedicine. 2014;1(1):37–45.
  • Lin L, Finak G, Ushey K, et al. COMPASS identifies T-cell subsets correlated with clinical outcomes. Nat Biotechnol. 2015;33(6):610–616.
  • Rerks-Ngarm S, Pitisuttithum P, Excler JL, et al. Randomized, double-blind evaluation of late boost strategies for HIV-uninfected vaccine recipients in the RV144 HIV vaccine efficacy trial. J Infect Dis. 2017;215(8):1255–1263.
  • Akapirat S, Karnasuta C, Vasan S, et al. Characterization of HIV-1 gp120 antibody specificities induced in anogenital secretions of RV144 vaccine recipients after late boost immunizations. PLoS One. 2018;13(4):e0196397.
  • Easterhoff D, Moody MA, Fera D, et al. Boosting of HIV envelope CD4 binding site antibodies with long variable heavy third complementarity determining region in the randomized double blind RV305 HIV-1 vaccine trial. PLoS Pathog. 2017;13(2):e1006182.
  • Shen X, Moodie Z, McMillan A, et al. V1V2 IgG and antibody Fc effector functions in a subtype C ALVAC-HIV and bivalent subtype C gp120/MF59 HIV-1 vaccine trial in South Africa (HIVR4P 2018, abstract OA02.03). AIDS Res Hum Retroviruses. 2018;34(S1):17.
  • Bekker LG, Moodie Z, Grunenberg N, et al. Subtype C ALVAC-HIV and bivalent subtype C gp120/MF59 HIV-1 vaccine in low-risk, HIV-uninfected, South African adults: a phase 1/2 trial. Lancet HIV. 2018;5(7):e366–e378.
  • Gray GE, Andersen-Nissen E, Grunenberg N, et al. HVTN 097: evaluation of the RV144 vaccine regimen in HIV uninfected South African adults (HIVR4P 2014, abstract). AIDS Res Hum Retroviruses. 2014;30(S1):A33–A34.
  • Fleming L, Andersen-Nissen E, Fiore-Gartland A, et al. Systems analysis of the innate and adaptive immune responses to the RV144 ALVAC HIV vaccine in a South African HIV uninfected cohort (HIVR4P 2018, abstract P26.03). AIDS Res Hum Retroviruses. 2018;34(S1):378.
  • Cohen K, Malahleha M, Laher F, et al. Increase in env-specific binding antibody and CD4+ T Cell-responses after month 30 boost of gp120/MF59 delivered alone or with ALVAC-HIV (HIVR4P 2018, abstract PD03.05LB). AIDS Res Hum Retroviruses. 2018;34(S1):90.
  • Barouch DH. A step forward for HIV vaccines. Lancet HIV. 2018;5(7):e338–e339.
  • Vaccari M, Gordon SN, Fourati S, et al. Adjuvant-dependent innate and adaptive immune signatures of risk of SIVmac251 acquisition. Nat Med. 2016;22(7):762–770.
  • Moody MA, Santra S, Vandergrift NA, et al. Toll-like receptor 7/8 (TLR7/8) and TLR9 agonists cooperate to enhance HIV-1 envelope antibody responses in rhesus macaques. J Virol. 2014;88(6):3329–3339.
  • Fouts TR, Bagley K, Prado IJ, et al. Balance of cellular and humoral immunity determines the level of protection by HIV vaccines in rhesus macaque models of HIV infection. Proc Natl Acad Sci U S A. 2015;112(9):E992–E999.
  • Beck Z, Matyas GR, Jalah R, et al. Differential immune responses to HIV-1 envelope protein induced by liposomal adjuvant formulations containing monophosphoryl lipid A with or without QS21. Vaccine. 2015;33(42):5578–5587.
  • Chea LS, Amara RR. Immunogenicity and efficacy of DNA/MVA HIV vaccines in rhesus macaque models. Expert Rev Vaccines. 2017;16(10):973–985.
  • Amara RR, Villinger F, Altman JD, et al. Control of a mucosal challenge and prevention of AIDS by a multiprotein DNA/MVA vaccine. Vaccine. 2002;20(15):1949–1955.
  • Hanke T, McMichael AJ, Mwau M, et al. Development of a DNA-MVA/HIVA vaccine for Kenya. Vaccine. 2002;20(15):1995–1998.
  • Hanke T, Goonetilleke N, McMichael AJ, et al. Clinical experience with plasmid DNA- and modified vaccinia virus Ankara-vectored human immunodeficiency virus type 1 clade A vaccine focusing on T-cell induction. J Gen Virol. 2007;88(Pt 1):1–12.
  • Kent S, De Rose R, Rollman E. Drug evaluation: DNA/MVA prime-boost HIV vaccine. Curr Opin Invest Drugs. 2007;8(2):159–167.
  • Iyer SS, Amara RR. DNA/MVA vaccines for HIV/AIDS. Vaccines (Basel). 2014;2(1):160–178.
  • Garcia-Arriaza J, Esteban M. Enhancing poxvirus vectors vaccine immunogenicity. Hum Vaccin Immunother. 2014;10(8):2235–2244.
  • Viegas EO, Tembe N, Nilsson C, et al. Intradermal HIV-1 DNA immunization using needle-free zetajet injection followed by HIV-modified vaccinia virus ankara vaccination is safe and immunogenic in mozambican young adults: a phase I randomized controlled trial. AIDS Res Hum Retroviruses. 2018;34(2):193–205.
  • Ake JA, Schuetz A, Pegu P, et al. Safety and immunogenicity of PENNVAX-G DNA prime administered by biojector 2000 or CELLECTRA electroporation device with modified vaccinia ankara-CMDR boost. J Infect Dis. 2017;216(9):1080–1090.
  • Hinkula J, Petkov S, Ljungberg K, et al. HIVIS-DNA or HIVISopt-DNA priming followed by CMDR vaccinia-based boosts induce both humoral and cellular murine immune responses to HIV. Heliyon. 2017;3(6):e00339.
  • Joachim A, Bauer A, Joseph S, et al. Boosting with subtype C CN54rgp140 protein adjuvanted with glucopyranosyl lipid adjuvant after priming with HIV-DNA and HIV-MVA is safe and enhances immune responses: a phase I trial. PLoS One. 2016;11(5):e0155702.
  • Nilsson C, Godoy-Ramirez K, Hejdeman B, et al. Broad and potent cellular and humoral immune responses after a second late HIV-modified vaccinia virus ankara vaccination in HIV-DNA-primed and HIV-modified vaccinia virus Ankara-boosted Swedish vaccinees. AIDS Res Hum Retroviruses. 2014;30(3):299–311.
  • Munseri PJ, Kroidl A, Nilsson C, et al. Priming with a simplified intradermal HIV-1 DNA vaccine regimen followed by boosting with recombinant HIV-1 MVA vaccine is safe and immunogenic: a phase IIa randomized clinical trial. PLoS One. 2015;10(4):e0119629.
  • Joachim A, Munseri PJ, Nilsson C, et al. Three-year durability of immune responses induced by HIV-DNA and HIV-modified vaccinia virus ankara and effect of a late HIV-modified vaccinia virus ankara boost in tanzanian volunteers. AIDS Res Hum Retroviruses. 2017;33(8):880–888.
  • Frahm N, Fiore-Gartland A, Malhi H, et al. Increased breadth of T-cell responses after mosaic HIV vaccination in humans (HVTN 106) (HIVR4P 2018, abstract OA07.01). AIDS Res Hum Retroviruses. 2018;34(S1):31.
  • Goepfert P, Casapia M, Elizaga M, et al. HVTN114: a Phase 1 trial to evaluate late boosts with AIDSVAX B/E of participants previously vaccinated with MVA/HIV62B in DNA/MVA or MVA regimens (HIVR4P 2018, abstract P05.14LB). AIDS Res Hum Retroviruses. 2018;34(S1):184.
  • Pissani F, Schulte B, Eller MA, et al. Modulation of vaccine-induced CD4 T cell functional profiles by changes in components of HIV vaccine regimens in humans. J Virol. 2018;92(23):e01143–e18.
  • Viegas EO, Kroidl A, Munseri PJ, et al. Optimizing the immunogenicity of HIV prime-boost DNA-MVA-rgp140/GLA vaccines in a phase II randomized factorial trial design. PLoS One. 2018;13(11):e0206838.
  • Excler JL, Rida W, Priddy F, et al. AIDS vaccines and preexposure prophylaxis: is synergy possible? AIDS Res Hum Retroviruses. 2011;27(6):669–680.
  • McNicholl JM. Combining biomedical preventions for HIV: vaccines with pre-exposure prophylaxis, microbicides or other HIV preventions. Hum Vaccin Immunother. 2016;12(12):3202–3211.
  • Harari A, Bart PA, Stohr W, et al. An HIV-1 clade C DNA prime, NYVAC boost vaccine regimen induces reliable, polyfunctional, and long-lasting T cell responses. J Exp Med. 2008;205(1):63–77.
  • Bart PA, Huang Y, Karuna ST, et al. HIV-specific humoral responses benefit from stronger prime in phase Ib clinical trial. J Clin Invest. 2014;124(11):4843–4856.
  • Garcia-Arriaza J, Perdiguero B, Heeney J, et al. Head-to-head comparison of poxvirus NYVAC and ALVAC vectors expressing identical HIV-1 clade C immunogens in prime-boost combination with env protein in nonhuman primates. J Virol. 2015;89(16):8525–8539.
  • Kibler KV, Asbach B, Perdiguero B, et al. Replication-competent NYVAC-KC yields improved immunogenicity to HIV-1 antigens in rhesus macaques, compared to non-replicating NYVAC. J Virol. 2019;93(3):e01513–e18.
  • Asbach B, Kibler KV, Kostler J, et al. Priming with a potent HIV-1 DNA vaccine frames the quality of immune responses prior to a poxvirus and protein boost. J Virol. 2019;93(3):e01529–e18.
  • Paris RM, Kim JH, Robb ML, et al. Prime-boost immunization with poxvirus or adenovirus vectors as a strategy to develop a protective vaccine for HIV-1. Expert Rev Vaccines. 2010;9(9):1055–1069.
  • Frahm N, DeCamp AC, Friedrich DP, et al. Human adenovirus-specific T cells modulate HIV-specific T cell responses to an Ad5-vectored HIV-1 vaccine. J Clin Invest. 2012;122(1):359–367.
  • Ondondo B, Abdul-Jawad S, Bridgeman A, et al. Characterization of T-cell responses to conserved regions of the HIV-1 proteome in BALB/c mice. Clin Vaccine Immunol. 2014;21(11):1565–1572.
  • Fausther-Bovendo H, Kobinger GP. Pre-existing immunity against Ad vectors: humoral, cellular, and innate response, what’s important? Hum Vaccin Immunother. 2014;10(10):2875–2884.
  • Barouch DH, Alter G, Broge T, et al. Protective efficacy of adenovirus/protein vaccines against SIV challenges in rhesus monkeys. Science. 2015;349(6245):320–324.
  • Barouch DH, Stephenson KE, Borducchi EN, et al. Protective efficacy of a global HIV-1 mosaic vaccine against heterologous SHIV challenges in rhesus monkeys. Cell. 2013;155(3):531–539.
  • Barouch DH, Liu J, Li H, et al. Vaccine protection against acquisition of neutralization-resistant SIV challenges in rhesus monkeys. Nature. 2012;482(7383):89–93.
  • Barouch DH, Tomaka FL, Wegmann F, et al. Evaluation of a mosaic HIV-1 vaccine in a multicentre, randomised, double-blind, placebo-controlled, phase 1/2a clinical trial (APPROACH) and in rhesus monkeys (NHP 13-19). Lancet. 2018;392(10143):232–243.
  • Stieh DJ, Callewaert K, Sarnecki M, et al. Primary analysis of TRAVERSE: a Phase 1/2a study to assess safety/tolerability and immunogenicity of 2 different prime/boost HIV vaccine regimens (HIVR4P 2018, abstract OA02.06LB). AIDS Res Hum Retroviruses. 2018;34(S1):18.
  • Omosa-Manyonyi G, Mpendo J, Ruzagira E, et al. A Phase I double blind, placebo-controlled, randomized study of the safety and immunogenicity of an adjuvanted HIV-1 gag-pol-nef fusion protein and adenovirus 35 Gag-RT-int-nef vaccine in healthy HIV-uninfected African Adults. PLoS One. 2015;10(5):e0125954.
  • Ratto-Kim S, Currier JR, Cox JH, et al. Heterologous prime-boost regimens using rAd35 and rMVA vectors elicit stronger cellular immune responses to HIV proteins than homologous regimens. PLoS One. 2012;7(9):e45840.
  • Nyombayire J, Anzala O, Gazzard B, et al. First-in-human evaluation of the safety and immunogenicity of an intranasally administered replication-competent sendai virus-vectored HIV Type 1 gag vaccine: induction of potent T-cell or antibody responses in prime-boost regimens. J Infect Dis. 2017;215(1):95–104.
  • Crank MC, Wilson EM, Novik L, et al. Safety and Immunogenicity of a rAd35-EnvA prototype HIV-1 vaccine in combination with rAd5-EnvA in healthy adults (VRC 012). PLoS One. 2016;11(11):e0166393.
  • Walsh SR, Moodie Z, Fiore-Gartland AJ, et al. Vaccination with heterologous HIV-1 envelope sequences and heterologous adenovirus vectors increases T-cell responses to conserved regions: HVTN 083. J Infect Dis. 2016;213(4):541–550.
  • Parks CL, Picker LJ, King CR. Development of replication-competent viral vectors for HIV vaccine delivery. Curr Opin HIV AIDS. 2013;8(5):402–411.
  • Excler JL, Parks CL, Ackland J, et al. Replicating viral vectors as HIV vaccines: summary report from the IAVI-sponsored satellite symposium at the AIDS vaccine 2009 conference. Biologicals. 2010;38(4):511–521.
  • Stephenson KE, Keefer MC, Bunce CA, et al. First-in-human randomized controlled trial of an oral, replicating adenovirus 26 vector vaccine for HIV-1. PLoS One. 2018;13(11):e0205139.
  • Malherbe DC, Mendy J, Vang L, et al. Combination adenovirus and protein vaccines prevent infection or reduce viral burden after heterologous clade c simian-human immunodeficiency virus mucosal challenge. J Virol. 2018;92:2.
  • 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.
  • Gray GE, Allen M, Moodie Z, et al. Safety and efficacy of the HVTN 503/Phambili study of a clade-B-based HIV-1 vaccine in South Africa: a double-blind, randomised, placebo-controlled test-of-concept phase 2b study. Lancet Infect Dis. 2011;11(7):507–515.
  • Hu H, Eller MA, Zafar S, et al. Preferential infection of human Ad5-specific CD4 T cells by HIV in Ad5 naturally exposed and recombinant Ad5-HIV vaccinated individuals. Proc Natl Acad Sci U S A. 2014;111(37):13439–13444.
  • Auclair S, Liu F, Niu Q, et al. Distinct susceptibility of HIV vaccine vector-induced CD4 T cells to HIV infection. PLoS Pathog. 2018;14(2):e1006888.
  • Churchyard GJ, Morgan C, Adams E, et al. A phase IIA randomized clinical trial of a multiclade HIV-1 DNA prime followed by a multiclade rAd5 HIV-1 vaccine boost in healthy adults (HVTN204). PLoS One. 2011;6(8):e21225.
  • Hammer SM, Sobieszczyk ME, Janes H, et al. Efficacy trial of a DNA/rAd5 HIV-1 preventive vaccine. N Engl J Med. 2013;369(22):2083–2092.
  • Enama ME, Ledgerwood JE, Novik L, et al. Phase I randomized clinical trial of VRC DNA and rAd5 HIV-1 vaccine delivery by intramuscular (i.m.), subcutaneous (s.c.) and intradermal (i.d.) administration (VRC 011). PLoS One. 2014;9(3):e91366.
  • Mpendo J, Mutua G, Nyombayire J, et al. A Phase I double blind, placebo-controlled, randomized study of the safety and immunogenicity of electroporated HIV DNA with or without interleukin 12 in prime-boost combinations with an Ad35 HIV vaccine in healthy HIV-seronegative African Adults. PLoS One. 2015;10(8):e0134287.
  • Clarke DK, Cooper D, Egan MA, et al. Recombinant vesicular stomatitis virus as an HIV-1 vaccine vector. Springer Semin Immunopathol. 2006;28(3):239–253.
  • Fauci AS, Marovich MA, Dieffenbach CW, et al. Immunology. Immune activation with HIV vaccines. Science. 2014;344(6179):49–51.
  • Fuchs JD, Frank I, Elizaga ML, et al. First-in-human evaluation of the safety and immunogenicity of a recombinant vesicular stomatitis virus human immunodeficiency Virus-1 gag vaccine (HVTN 090). Open Forum Infect Dis. 2015;2:3. ofv082
  • Elizaga ML, Li SS, Kochar NK, et al. Safety and tolerability of HIV-1 multiantigen pDNA vaccine given with IL-12 plasmid DNA via electroporation, boosted with a recombinant vesicular stomatitis virus HIV Gag vaccine in healthy volunteers in a randomized, controlled clinical trial. PLoS One. 2018;13(9):e0202753.
  • Li SS, Kochar NK, Elizaga M, et al. DNA priming increases frequency of T-cell responses to a vesicular stomatitis virus HIV vaccine with specific enhancement of CD8(+) T-cell responses by interleukin-12 plasmid DNA. Clin Vaccine Immunol. 2017;24(11):e00263–e17.
  • Pialoux G, Gahery-Segard H, Sermet S, et al. Lipopeptides induce cell-mediated anti-HIV immune responses in seronegative volunteers. AIDS. 2001;15(10):1239–1249.
  • Levy Y, Thiebaut R, Montes M, et al. Dendritic cell-based therapeutic vaccine elicits polyfunctional HIV-specific T-cell immunity associated with control of viral load. Eur J Immunol. 2014;44(9):2802–2810.
  • Frey SE, Peiperl L, McElrath MJ, et al. Phase I/II randomized trial of safety and immunogenicity of LIPO-5 alone, ALVAC-HIV (vCP1452) alone, and ALVAC-HIV (vCP1452) prime/LIPO-5 boost in healthy, HIV-1-uninfected adult participants. Clin Vaccine Immunol. 2014;21(11):1589–1599.
  • Dereuddre-Bosquet N, Baron ML, Contreras V, et al. HIV specific responses induced in nonhuman primates with ANRS HIV-Lipo-5 vaccine combined with rMVA-HIV prime or boost immunizations. Vaccine. 2015;33(20):2354–2359.
  • Malm M, Sikut R, Krohn K, et al. GTU-multihiv DNA vaccine results in protection in a novel P815 tumor challenge model. Vaccine. 2007;25(17):3293–3301.

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