New developments in an old strategy: heterologous vector primes and envelope protein boosts in HIV vaccine design

References

• Belshe RB, Graham BS, Keefer MC, et al. Neutralizing antibodies to HIV-1 in seronegative volunteers immunized with recombinant gp120 from the MN strain of HIV-1. NIAID AIDS vaccine clinical trials network. JAMA. 1994;272(6):475–480.
   PubMed Web of Science ®Google Scholar
• Flynn NM, Forthal DN, Harro CD, et al. Placebo-controlled phase 3 trial of a recombinant glycoprotein 120 vaccine to prevent HIV-1 infection. J Infect Dis. 2005;191(5):654–665.
   PubMed Web of Science ®Google Scholar
• Pitisuttithum P, Gilbert P, Gurwith M, et al. 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. 2006;194(12):1661–1671.
   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
• 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.
   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
• Cheng C, Wang L, Gall JG, et al. Decreased pre-existing Ad5 capsid and Ad35 neutralizing antibodies increase HIV-1 infection risk in the step trial independent of vaccination. PLoS One. 2012;7(4):e33969.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Nitayaphan S, Pitisuttithum P, Karnasuta C, et al. Safety and immunogenicity of an HIV subtype B and E prime-boost vaccine combination in HIV-negative Thai adults. J Infect Dis. 2004;190(4):702–706.
   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
• 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.
   PubMed Web of Science ®Google Scholar
• Pollara J, Bonsignori M, Moody MA, et al. HIV-1 vaccine-induced C1 and V2 Env-specific antibodies synergize for increased antiviral activities. J Virol. 2014;88(14):7715–7726.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Mascola JR. Defining the protective antibody response for HIV-1. Curr Mol Med. 2003;3(3):209–216.
   PubMed Web of Science ®Google Scholar
• Wang B, Ugen KE, Srikantan V, et al. Gene inoculation generates immune responses against human immunodeficiency virus type 1. Proc Natl Acad Sci U S A. 1993;90(9):4156–4160.
   PubMed Web of Science ®Google Scholar
• Boyer JD, Wang B, Ugen KE, et al. In vivo protective anti-HIV immune responses in non-human primates through DNA immunization. J Med Primatol. 1996;25(3):242–250.
   PubMed Web of Science ®Google Scholar
• Lu S, Arthos J, Montefiori DC, et al. Simian immunodeficiency virus DNA vaccine trial in macaques. J Virol. 1996;70(6):3978–3991.
   PubMed Web of Science ®Google Scholar
• MacGregor RR, Boyer JD, Ugen KE, et al. First human trial of a DNA-based vaccine for treatment of human immunodeficiency virus type 1 infection: safety and host response. J Infect Dis. 1998;178(1):92–100.
   PubMed Web of Science ®Google Scholar
• Liu MA. DNA vaccines: a review. J Intern Med. 2003;253(4):402–410.
   PubMed Web of Science ®Google Scholar
• Kong WP, Wu L, Wallstrom TC, et al. Expanded breadth of the T-cell response to mosaic human immunodeficiency virus type 1 envelope DNA vaccination. J Virol. 2009;83(5):2201–2215.
   PubMed Web of Science ®Google Scholar
• Kothe DL, Li Y, Decker JM, et al. Ancestral and consensus envelope immunogens for HIV-1 subtype C. Virology. 2006;352(2):438–449.
   PubMed Web of Science ®Google Scholar
• Kulkarni V, Valentin A, Rosati M, et al. Altered response hierarchy and increased T-cell breadth upon HIV-1 conserved element DNA vaccination in macaques. PLoS One. 2014;9(1):e86254.
   PubMed Web of Science ®Google Scholar
• Kulkarni V, Valentin A, Rosati M, et al. HIV-1 conserved elements p24CE DNA vaccine induces humoral immune responses with broad epitope recognition in macaques. PLoS One. 2014;9(10):e111085.
   PubMed Web of Science ®Google Scholar
• Pal R, Kalyanaraman VS, Nair BC, et al. Immunization of rhesus macaques with a polyvalent DNA prime/protein boost human immunodeficiency virus type 1 vaccine elicits protective antibody response against simian human immunodeficiency virus of R5 phenotype. Virology. 2006;348(2):341–353.
   PubMed Web of Science ®Google Scholar
• Rollman E, Brave A, Boberg A, et al. The rationale behind a vaccine based on multiple HIV antigens. Microbes Infect. 2005;7(14):1414–1423.
   PubMed Web of Science ®Google Scholar
• Wang S, Kennedy JS, West K, et al. Cross-subtype antibody and cellular immune responses induced by a polyvalent DNA prime-protein boost HIV-1 vaccine in healthy human volunteers. Vaccine. 2008;26(31):3947–3957.
   PubMed Web of Science ®Google Scholar
• Widera G, Austin M, Rabussay D, et al. Increased DNA vaccine delivery and immunogenicity by electroporation in vivo. J Immunol. 2000;164(9):4635–4640.
   PubMed Web of Science ®Google Scholar
• Hutnick NA, Myles DJ, Ferraro B, et al. Intradermal DNA vaccination enhanced by low-current electroporation improves antigen expression and induces robust cellular and humoral immune responses. Hum Gene Ther. 2012;23(9):943–950.
   PubMed Web of Science ®Google Scholar
• Jalah R, Patel V, Kulkarni V, et al. IL-12 DNA as molecular vaccine adjuvant increases the cytotoxic T cell responses and breadth of humoral immune responses in SIV DNA vaccinated macaques. Hum Vaccin Immunother. 2012;8(11):1620–1629.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Vasan S, Hurley A, Schlesinger SJ, et al. In vivo electroporation enhances the immunogenicity of an HIV-1 DNA vaccine candidate in healthy volunteers. PLoS One. 2011;6(5):e19252.
   PubMed Web of Science ®Google Scholar
• Kichaev G, Mendoza JM, Amante D, et al. Electroporation mediated DNA vaccination directly to a mucosal surface results in improved immune responses. Hum Vaccin Immunother. 2013;9(10):2041–2048.
   PubMed Web of Science ®Google Scholar
• Hutnick NA, Myles DJ, Bian CB, et al. Selected approaches for increasing HIV DNA vaccine immunogenicity in vivo. Curr Opin Virol. 2011;1(4):233–240.
   PubMed Web of Science ®Google Scholar
• Chong SY, Egan MA, Kutzler MA, et al. Comparative ability of plasmid IL-12 and IL-15 to enhance cellular and humoral immune responses elicited by a SIVgag plasmid DNA vaccine and alter disease progression following SHIV(89.6P) challenge in rhesus macaques. Vaccine. 2007;25(26):4967–4982.
   PubMed Web of Science ®Google Scholar
• Kalams SA, Parker S, Jin X, et al. Safety and immunogenicity of an HIV-1 gag DNA vaccine with or without IL-12 and/or IL-15 plasmid cytokine adjuvant in healthy, HIV-1 uninfected adults. PLoS One. 2012;7(1):e29231.
   PubMed Web of Science ®Google Scholar
• Kutzler MA, Wise MC, Hutnick NA, et al. Chemokine-adjuvanted electroporated DNA vaccine induces substantial protection from simian immunodeficiency virus vaginal challenge. Mucosal Immunol. 2015;19:13–23.
   PubMed Web of Science ®Google Scholar
• Oynebraten I, Hinkula J, Fredriksen AB, et al. Increased generation of HIV-1 gp120-reactive CD8+ T cells by a DNA vaccine construct encoding the chemokine CCL3. PLoS One. 2014;9(8):e104814.
   Google Scholar
• Villarreal DO, Svoronos N, Wise MC, et al. Molecular adjuvant IL-33 enhances the potency of a DNA vaccine in a lethal challenge model. Vaccine. 2015;33(35):4313–4320.
   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
• Garrod T, Grubor-Bauk B, Yu S, et al. Encoded novel forms of HSP70 or a cytolytic protein increase DNA vaccine potency. Hum Vaccin Immunother. 2014;10(9):2679–2683.
   PubMed Web of Science ®Google Scholar
• Kulkarni V, Rosati M, Valentin A, et al. Vaccination with Vaxfectin((R)) adjuvanted SIV DNA induces long-lasting humoral immune responses able to reduce SIVmac251 Viremia. Hum Vaccin Immunother. 2013;9(10):2069–2080.
   PubMed Web of Science ®Google Scholar
• Johnson JA, Barouch DH, Baden LR. Nonreplicating vectors in HIV vaccines. Curr Opin HIV AIDS. 2013;8(5):412–420.
   PubMed Web of Science ®Google Scholar
• Robert-Guroff M. Replicating and non-replicating viral vectors for vaccine development. Curr Opin Biotechnol. 2007;18(6):546–556.
   PubMed Web of Science ®Google Scholar
• Patterson LJ, Kuate S, Daltabuit-Test M, et al. Replicating adenovirus-simian immunodeficiency virus (SIV) vectors efficiently prime SIV-specific systemic and mucosal immune responses by targeting myeloid dendritic cells and persisting in rectal macrophages, regardless of immunization route. Clin Vaccine Immunol. 2012;19(5):629–637.
   PubMed Web of Science ®Google Scholar
• Tatsis N, Fitzgerald JC, Reyes-Sandoval A, et al. Adenoviral vectors persist in vivo and maintain activated CD8+ T cells: implications for their use as vaccines. Blood. 2007;110(6):1916–1923.
   PubMed Web of Science ®Google Scholar
• Appledorn DM, Patial S, McBride A, et al. Adenovirus vector-induced innate inflammatory mediators, MAPK signaling, as well as adaptive immune responses are dependent upon both TLR2 and TLR9 in vivo. J Immunol. 2008;181(3):2134–2144.
   PubMed Web of Science ®Google Scholar
• Yang TC, Millar J, Groves T, et al. On the role of CD4+ T cells in the CD8+ T-cell response elicited by recombinant adenovirus vaccines. Mol Ther. 2007;15(5):997–1006.
   PubMed Web of Science ®Google Scholar
• Liu J, O’Brien KL, Lynch DM, et al. Immune control of an SIV challenge by a T-cell-based vaccine in rhesus monkeys. Nature. 2009;457(7225):87–91.
   PubMed Web of Science ®Google Scholar
• Barouch DH, Kik SV, Weverling GJ, et al. International seroepidemiology of adenovirus serotypes 5, 26, 35, and 48 in pediatric and adult populations. Vaccine. 2011;29(32):5203–5209.
   PubMed Web of Science ®Google Scholar
• Teigler JE, Iampietro MJ, Barouch DH. Vaccination with adenovirus serotypes 35, 26, and 48 elicits higher levels of innate cytokine responses than adenovirus serotype 5 in rhesus monkeys. J Virol. 2012;86(18):9590–9598.
   PubMed Web of Science ®Google Scholar
• Tan WG, Jin HT, West EE, et al. Comparative analysis of simian immunodeficiency virus gag-specific effector and memory CD8+ T cells induced by different adenovirus vectors. J Virol. 2013;87(3):1359–1372.
   PubMed Web of Science ®Google Scholar
• Penaloza-MacMaster P, Provine NM, Ra J, et al. Alternative serotype adenovirus vaccine vectors elicit memory T cells with enhanced anamnestic capacity compared to Ad5 vectors. J Virol. 2013;87(3):1373–1384.
   PubMed Web of Science ®Google Scholar
• Colloca S, Barnes E, Folgori A, et al. Vaccine vectors derived from a large collection of simian adenoviruses induce potent cellular immunity across multiple species. Sci Transl Med. 2012;4(115):115ra112.
   Web of Science ®Google Scholar
• Keefer MC, Gilmour J, Hayes P, et al. A phase I double blind, placebo-controlled, randomized study of a multigenic HIV-1 adenovirus subtype 35 vector vaccine in healthy uninfected adults. PLoS One. 2012;7(8):e41936.
   PubMed Web of Science ®Google Scholar
• Barouch DH, Liu J, Peter L, et al. Characterization of humoral and cellular immune responses elicited by a recombinant adenovirus serotype 26 HIV-1 Env vaccine in healthy adults (IPCAVD 001). J Infect Dis. 2013;207(2):248–256.
   PubMed Web of Science ®Google Scholar
• Baden LR, Liu J, Li H, et al. Induction of HIV-1-specific mucosal immune responses following intramuscular recombinant adenovirus serotype 26 HIV-1 vaccination of humans. J Infect Dis. 2015;211(4):518–528.
   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
• Tatsis N, Lasaro MO, Lin SW, et al. Adenovirus vector-induced immune responses in nonhuman primates: responses to prime boost regimens. J Immunol. 2009;182(10):6587–6599.
   PubMed Web of Science ®Google Scholar
• Cervasi B, Carnathan DG, Sheehan KM, et al. Immunological and virological analyses of rhesus macaques immunized with chimpanzee adenoviruses expressing the simian immunodeficiency virus Gag/Tat fusion protein and challenged intrarectally with repeated low doses of SIVmac. J Virol. 2013;87(17):9420–9430.
   PubMed Web of Science ®Google Scholar
• Abbink P, Maxfield LF, Ng’ang’a D, et al. Construction and evaluation of novel rhesus monkey adenovirus vaccine vectors. J Virol. 2015;89(3):1512–1522.
   PubMed Web of Science ®Google Scholar
• Quinn KM, Da Costa A, Yamamoto A, et al. Comparative analysis of the magnitude, quality, phenotype, and protective capacity of simian immunodeficiency virus gag-specific CD8+ T cells following human-, simian-, and chimpanzee-derived recombinant adenoviral vector immunization. J Immunol. 2013;190(6):2720–2735.
   PubMed Web of Science ®Google Scholar
• Gaydos CA, Gaydos JC. Adenovirus vaccines in the U.S. military. Mil Med. 1995;160(6):300–304.
   PubMed Web of Science ®Google Scholar
• Khurana S, Coyle EM, Manischewitz J, et al. Oral priming with replicating adenovirus serotype 4 followed by subunit H5N1 vaccine boost promotes antibody affinity maturation and expands H5N1 cross-clade neutralization. PLoS One. 2015;10(1):e0115476.
   PubMed Web of Science ®Google Scholar
• Crosby CM, Nehete P, Sastry KJ, et al. Amplified and persistent immune responses generated by single-cycle replicating adenovirus vaccines. J Virol. 2015;89(1):669–675.
   PubMed Web of Science ®Google Scholar
• Jacobs BL, Langland JO, Kibler KV, et al. Vaccinia virus vaccines: past, present and future. Antiviral Res. 2009;84(1):1–13.
   PubMed Web of Science ®Google Scholar
• Collier LH. The development of a stable smallpox vaccine. J Hyg (Lond). 1955;53(1):76–101.
   PubMedGoogle Scholar
• Pastoret PP, Vanderplasschen A. Poxviruses as vaccine vectors. Comp Immunol Microbiol Infect Dis. 2003;26(5–6):343–355.
   PubMed Web of Science ®Google Scholar
• Gomez CE, Perdiguero B, Garcia-Arriaza J, et al. Poxvirus vectors as HIV/AIDS vaccines in humans. Hum Vaccin Immunother. 2012;8(9):1192–1207.
   PubMed Web of Science ®Google Scholar
• Mayr A, Stickl H, Muller HK, et al. [The smallpox vaccination strain MVA: marker, genetic structure, experience gained with the parenteral vaccination and behavior in organisms with a debilitated defence mechanism (author’s transl)]. Zentralbl Bakteriol B. 1978;167(5–6):375–390.
   PubMedGoogle Scholar
• Volz A, Sutter G. Protective efficacy of modified vaccinia virus Ankara in preclinical studies. Vaccine. 2013;31(39):4235–4240.
   PubMed Web of Science ®Google Scholar
• Gomez CE, Najera JL, Krupa M, et al. MVA and NYVAC as vaccines against emergent infectious diseases and cancer. Curr Gene Ther. 2011;11(3):189–217.
   PubMed Web of Science ®Google Scholar
• Tameris MD, Hatherill M, Landry BS, et al. Safety and efficacy of MVA85A, a new tuberculosis vaccine, in infants previously vaccinated with BCG: a randomised, placebo-controlled phase 2b trial. Lancet. 2013;381(9871):1021–1028.
   PubMed Web of Science ®Google Scholar
• Garcia-Arriaza J, Esteban M. Enhancing poxvirus vectors vaccine immunogenicity. Hum Vaccin Immunother. 2014;10(8):2235–2244.
   PubMed Web of Science ®Google Scholar
• Kibler KV, Gomez CE, Perdiguero B, et al. Improved NYVAC-based vaccine vectors. PLoS One. 2011;6(11):e25674.
   Google Scholar
• Quakkelaar ED, Redeker A, Haddad EK, et al. Improved innate and adaptive immunostimulation by genetically modified HIV-1 protein expressing NYVAC vectors. PLoS One. 2011;6(2):e16819.
   Google Scholar
• Mooij P, Koopman G, Drijfhout JW, et al. Synthetic long peptide booster immunization in rhesus macaques primed with replication-competent NYVAC-C-KC induces a balanced CD4/CD8 T-cell and antibody response against the conserved regions of HIV-1. J Gen Virol. 2015;96(Pt 6):1478–1483.
   PubMed Web of Science ®Google Scholar
• Franchini G, Gurunathan S, Baglyos L, et al. Poxvirus-based vaccine candidates for HIV: two decades of experience with special emphasis on canarypox vectors. Expert Rev Vaccines. 2004;3(4 Suppl):S75–S88.
   PubMedGoogle Scholar
• Kahn JO, Sinangil F, Baenziger J, et al. Clinical and immunologic responses to human immunodeficiency virus (HIV) type 1SF2 gp120 subunit vaccine combined with MF59 adjuvant with or without muramyl tripeptide dipalmitoyl phosphatidylethanolamine in non-HIV-infected human volunteers. J Infect Dis. 1994;170(5):1288–1291.
   PubMed Web of Science ®Google Scholar
• Montefiori DC, Graham BS, Zhou J, et al. V3-specific neutralizing antibodies in sera from HIV-1 gp160-immunized volunteers block virus fusion and act synergistically with human monoclonal antibody to the conformation-dependent CD4 binding site of gp120. NIH-NIAID AIDS vaccine clinical trials network. J Clin Invest. 1993;92(2):840–847.
   PubMed Web of Science ®Google Scholar
• Schwartz DH, Gorse G, Clements ML, et al. Induction of HIV-1-neutralising and syncytium-inhibiting antibodies in uninfected recipients of HIV-1IIIB rgp120 subunit vaccine. Lancet. 1993;342(8863):69–73.
   PubMed Web of Science ®Google Scholar
• Teigler JE, Phogat S, Franchini G, et al. The canarypox virus vector ALVAC induces distinct cytokine responses compared to the vaccinia virus-based vectors MVA and NYVAC in rhesus monkeys. J Virol. 2014;88(3):1809–1814.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Hansen SG, Ford JC, Lewis MS, et al. Profound early control of highly pathogenic SIV by an effector memory T-cell vaccine. Nature. 2011;473(7348):523–527.
   PubMed Web of Science ®Google Scholar
• Hansen SG, Piatak M Jr., Ventura AB, et al. Immune clearance of highly pathogenic SIV infection. Nature. 2013;502(7469):100–104.
   PubMed Web of Science ®Google Scholar
• Bogers WM, Oostermeijer H, Mooij P, et al. Potent immune responses in rhesus macaques induced by nonviral delivery of a self-amplifying RNA vaccine expressing HIV type 1 envelope with a cationic nanoemulsion. J Infect Dis. 2015;211(6):947–955.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Ishii H, Matano T. Development of an AIDS vaccine using Sendai virus vectors. Vaccine. 2015;33(45):6061–6065.
   Google Scholar
• Virnik K, Hockenbury M, Ni Y, et al. Live attenuated rubella vectors expressing SIV and HIV vaccine antigens replicate and elicit durable immune responses in rhesus macaques. Retrovirology. 2013;10:99.
   PubMed Web of Science ®Google Scholar
• Rosati M, Alicea C, Kulkarni V, et al. Recombinant rubella vectors elicit SIV Gag-specific T cell responses with cytotoxic potential in rhesus macaques. Vaccine. 2015;33(18):2167–2174.
   PubMed Web of Science ®Google Scholar
• Martins MA, Bonaldo MC, Rudersdorf RA, et al. Immunogenicity of seven new recombinant yellow fever viruses 17D expressing fragments of SIVmac239 Gag, Nef, and Vif in Indian rhesus macaques. PLoS One. 2013;8(1):e54434.
   PubMed Web of Science ®Google Scholar
• Dunkel A, Shen S, LaBranche CC, et al. A bivalent, chimeric rabies virus expressing simian immunodeficiency virus envelope induces multifunctional antibody responses. AIDS Res Hum Retroviruses. 2015;31(11):1126–1138.
   PubMed Web of Science ®Google Scholar
• Deal CE, Balazs AB. Vectored antibody gene delivery for the prevention or treatment of HIV infection. Curr Opin HIV AIDS. 2015;10(3):190–197.
   PubMed Web of Science ®Google Scholar
• Yu Y, Fu L, Shi Y, et al. Elicitation of HIV-1 neutralizing antibodies by presentation of 4E10 and 10E8 epitopes on Norovirus P particles. Immunol Lett. 2015;168(2):271–278.
   Web of Science ®Google Scholar
• Liu C, Du S, Li C, et al. Immunogenicity analysis following human immunodeficiency virus recombinant DNA and recombinant vaccinia virus Tian Tan prime-boost immunization. Sci China Life Sci. 2013;56(6):531–540.
   PubMed Web of Science ®Google Scholar
• Barouch DH, Picker LJ. Novel vaccine vectors for HIV-1. Nat Rev Microbiol. 2014;12(11):765–771.
   PubMed Web of Science ®Google Scholar
• Hansen SG, Sacha JB, Hughes CM, et al. Cytomegalovirus vectors violate CD8+ T cell epitope recognition paradigms. Science. 2013;340(6135):1237874.
   PubMed Web of Science ®Google Scholar
• Geall AJ, Mandl CW, Ulmer JB. RNA: the new revolution in nucleic acid vaccines. Semin Immunol. 2013;25(2):152–159.
   PubMed Web of Science ®Google Scholar
• Burton DR, Mascola JR. Antibody responses to envelope glycoproteins in HIV-1 infection. Nat Immunol. 2015;16(6):571–576.
   PubMed Web of Science ®Google Scholar
• Lewis GK, Finzi A, DeVico AL, et al. Conformational masking and receptor-dependent unmasking of highly conserved Env epitopes recognized by non-neutralizing antibodies that mediate potent ADCC against HIV-1. Viruses. 2015;7(9):5115–5132.
   PubMed Web of Science ®Google Scholar
• Shingai M, Donau OK, Plishka RJ, et al. Passive transfer of modest titers of potent and broadly neutralizing anti-HIV monoclonal antibodies block SHIV infection in macaques. J Exp Med. 2014;211(10):2061–2074.
   PubMed Web of Science ®Google Scholar
• Baum LL, Cassutt KJ, Knigge K, et al. HIV-1 gp120-specific antibody-dependent cell-mediated cytotoxicity correlates with rate of disease progression. J Immunol. 1996;157(5):2168–2173.
   PubMed Web of Science ®Google Scholar
• Forthal DN, Gilbert PB, Landucci G, et al. Recombinant gp120 vaccine-induced antibodies inhibit clinical strains of HIV-1 in the presence of Fc receptor-bearing effector cells and correlate inversely with HIV infection rate. J Immunol. 2007;178(10):6596–6603.
   PubMed Web of Science ®Google Scholar
• Gomez-Roman VR, Patterson LJ, Venzon D, et al. Vaccine-elicited antibodies mediate antibody-dependent cellular cytotoxicity correlated with significantly reduced acute viremia in rhesus macaques challenged with SIVmac251. J Immunol. 2005;174(4):2185–2189.
   PubMed Web of Science ®Google Scholar
• Xiao P, Zhao J, Patterson LJ, et al. Multiple vaccine-elicited nonneutralizing antienvelope antibody activities contribute to protective efficacy by reducing both acute and chronic viremia following simian/human immunodeficiency virus SHIV89.6P challenge in rhesus macaques. J Virol. 2010;84(14):7161–7173.
   PubMed Web of Science ®Google Scholar
• Dugast AS, Chan Y, Hoffner M, et al. Lack of protection following passive transfer of polyclonal highly functional low-dose non-neutralizing antibodies. PLoS One. 2014;9(5):e97229.
   Google Scholar
• Florese RH, Van Rompay KK, Aldrich K, et al. Evaluation of passively transferred, nonneutralizing antibody-dependent cellular cytotoxicity-mediating IgG in protection of neonatal rhesus macaques against oral SIVmac251 challenge. J Immunol. 2006;177(6):4028–4036.
   PubMed Web of Science ®Google Scholar
• Santra S, Tomaras GD, Warrier R, et al. Human non-neutralizing HIV-1 envelope monoclonal antibodies limit the number of founder viruses during SHIV mucosal infection in rhesus macaques. PLoS Pathog. 2015;11(8):e1005042.
   PubMed 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
• Hessell AJ, Hangartner L, Hunter M, et al. Fc receptor but not complement binding is important in antibody protection against HIV. Nature. 2007;449(7158):101–104.
   PubMed Web of Science ®Google Scholar
• Haynes BF, Montefiori DC. Aiming to induce broadly reactive neutralizing antibody responses with HIV-1 vaccine candidates. Expert Rev Vaccines. 2006;5(3):347–363.
   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
• 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
• Santra S, Muldoon M, Watson S, et al. Breadth of cellular and humoral immune responses elicited in rhesus monkeys by multi-valent mosaic and consensus immunogens. Virology. 2012;428(2):121–127.
   PubMed Web of Science ®Google Scholar
• Kovacs JM, Nkolola JP, Peng H, et al. HIV-1 envelope trimer elicits more potent neutralizing antibody responses than monomeric gp120. Proc Natl Acad Sci U S A. 2012;109(30):12111–12116.
   PubMed Web of Science ®Google Scholar
• Sundling C, Forsell MN, O’Dell S, et al. Soluble HIV-1 Env trimers in adjuvant elicit potent and diverse functional B cell responses in primates. J Exp Med. 2010;207(9):2003–2017.
   PubMed Web of Science ®Google Scholar
• Wieczorek L, Krebs SJ, Kalyanaraman V, et al. Comparable antigenicity and immunogenicity of oligomeric forms of a novel, acute HIV-1 subtype C gp145 envelope for use in preclinical and clinical vaccine research. J Virol. 2015;89(15):7478–7493.
   PubMed Web of Science ®Google Scholar
• Bricault CA, Kovacs JM, Nkolola JP, et al. A multivalent clade C HIV-1 Env trimer cocktail elicits a higher magnitude of neutralizing antibodies than any individual component. J Virol. 2015;89(5):2507–2519.
   PubMed Web of Science ®Google 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
• Sanders RW, Vesanen M, Schuelke N, et al. Stabilization of the soluble, cleaved, trimeric form of the envelope glycoprotein complex of human immunodeficiency virus type 1. J Virol. 2002;76(17):8875–8889.
   PubMed Web of Science ®Google Scholar
• Ringe RP, Sanders RW, Yasmeen A, et al. Cleavage strongly influences whether soluble HIV-1 envelope glycoprotein trimers adopt a native-like conformation. Proc Natl Acad Sci U S A. 2013;110(45):18256–18261.
   PubMed Web of Science ®Google Scholar
• Julien JP, Lee JH, Ozorowski G, et al. Design and structure of two HIV-1 clade C SOSIP.664 trimers that increase the arsenal of native-like Env immunogens. Proc Natl Acad Sci U S A. 2015;112(38):11947–11952.
   PubMed Web of Science ®Google Scholar
• Sanders RW, Van Gils MJ, Derking R, et al. HIV-1 VACCINES. HIV-1 neutralizing antibodies induced by native-like envelope trimers. Science. 2015;349(6244):aac4223.
   PubMed Web of Science ®Google Scholar
• Pancera M, Zhou T, Druz A, et al. Structure and immune recognition of trimeric pre-fusion HIV-1 Env. Nature. 2014;514(7523):455–461.
   PubMed Web of Science ®Google Scholar
• Wu X, Zhou T, Zhu J, et al. Focused evolution of HIV-1 neutralizing antibodies revealed by structures and deep sequencing. Science. 2011;333(6049):1593–1602.
   PubMed Web of Science ®Google Scholar
• Kong L, Torrents De La Pena A, Deller MC, et al. Complete epitopes for vaccine design derived from a crystal structure of the broadly neutralizing antibodies PGT128 and 8ANC195 in complex with an HIV-1 Env trimer. Acta Crystallogr D Biol Crystallogr. 2015;71(Pt 10):2099–2108.
   PubMedGoogle Scholar
• Ward AB, Wilson IA. Insights into the trimeric HIV-1 envelope glycoprotein structure. Trends Biochem Sci. 2015;40(2):101–107.
   PubMed Web of Science ®Google Scholar
• Sattentau QJ. Immunogen design to focus the B-cell repertoire. Curr Opin HIV AIDS. 2014;9(3):217–223.
   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
• Mann JK, Ndung’u T. HIV-1 vaccine immunogen design strategies. Virol J. 2015;12:3.
   PubMed Web of Science ®Google Scholar
• McGuire AT, Hoot S, Dreyer AM, et al. Engineering HIV envelope protein to activate germline B cell receptors of broadly neutralizing anti-CD4 binding site antibodies. J Exp Med. 2013;210(4):655–663.
   PubMed Web of Science ®Google Scholar
• Sun C, Chen Z, Tang X, et al. Mucosal priming with a replicating-vaccinia virus-based vaccine elicits protective immunity to simian immunodeficiency virus challenge in rhesus monkeys. J Virol. 2013;87(10):5669–5677.
   PubMed Web of Science ®Google Scholar
• Joachim A, Nilsson C, Aboud S, et al. Potent functional antibody responses elicited by HIV-I DNA priming and boosting with heterologous HIV-1 recombinant MVA in healthy Tanzanian adults. PLoS One. 2015;10(4):e0118486.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Zagury D, Bernard J, Cheynier R, et al. A group specific anamnestic immune reaction against HIV-1 induced by a candidate vaccine against AIDS. Nature. 1988;332(6166):728–731.
   PubMed Web of Science ®Google Scholar
• Hu SL, Klaniecki J, Dykers T, et al. Neutralizing antibodies against HIV-1 BRU and SF2 isolates generated in mice immunized with recombinant vaccinia virus expressing HIV-1 (BRU) envelope glycoproteins and boosted with homologous gp160. AIDS Res Hum Retroviruses. 1991;7(7):615–620.
   PubMed Web of Science ®Google Scholar
• Cooney EL, McElrath MJ, Corey L, et al. Enhanced immunity to human immunodeficiency virus (HIV) envelope elicited by a combined vaccine regimen consisting of priming with a vaccinia recombinant expressing HIV envelope and boosting with gp160 protein. Proc Natl Acad Sci U S A. 1993;90(5):1882–1886.
   PubMed Web of Science ®Google Scholar
• Vaine M, Wang S, Hackett A, et al. Antibody responses elicited through homologous or heterologous prime-boost DNA and protein vaccinations differ in functional activity and avidity. Vaccine. 2010;28(17):2999–3007.
   PubMed Web of Science ®Google Scholar
• Pissani F, Malherbe DC, Schuman JT, et al. Improvement of antibody responses by HIV envelope DNA and protein co-immunization. Vaccine. 2014;32(4):507–513.
   PubMed Web of Science ®Google Scholar
• Wise MC, Hutnick NA, Pollara J, et al. An enhanced synthetic multiclade DNA prime induces improved cross-clade-reactive functional antibodies when combined with an adjuvanted protein boost in nonhuman primates. J Virol. 2015;89(18):9154–9166.
   PubMed Web of Science ®Google Scholar
• Li J, Valentin A, Kulkarni V, et al. HIV/SIV DNA vaccine combined with protein in a co-immunization protocol elicits highest humoral responses to envelope in mice and macaques. Vaccine. 2013;31(36):3747–3755.
   PubMed Web of Science ®Google Scholar
• Jalah R, Kulkarni V, Patel V, et al. DNA and protein co-immunization improves the magnitude and longevity of humoral immune responses in macaques. PLoS One. 2014;9(3):e91550.
   PubMed Web of Science ®Google Scholar
• Patel V, Jalah R, Kulkarni V, et al. DNA and virus particle vaccination protects against acquisition and confers control of viremia upon heterologous simian immunodeficiency virus challenge. Proc Natl Acad Sci U S A. 2013;110(8):2975–2980.
   PubMed Web of Science ®Google Scholar
• Spearman P, Lally MA, Elizaga M, et al. A trimeric, V2-deleted HIV-1 envelope glycoprotein vaccine elicits potent neutralizing antibodies but limited breadth of neutralization in human volunteers. J Infect Dis. 2011;203(8):1165–1173.
   PubMed Web of Science ®Google Scholar
• Cox JH, Ferrari MG, Earl P, et al. Inclusion of a CRF01_AE HIV envelope protein boost with a DNA/MVA prime-boost vaccine: impact on humoral and cellular immunogenicity and viral load reduction after SHIV-E challenge. Vaccine. 2012;30(10):1830–1840.
   PubMed Web of Science ®Google Scholar
• Hulot SL, Korber B, Giorgi EE, et al. Comparison of Immunogenicity in rhesus macaques of transmitted-founder, HIV-1 group M consensus, and trivalent mosaic envelope vaccines formulated as a DNA prime, NYVAC, and envelope protein boost. J Virol. 2015;89(12):6462–6480.
   PubMed Web of Science ®Google Scholar
• Hidajat R, Xiao P, Zhou Q, et al. Correlation of vaccine-elicited systemic and mucosal nonneutralizing antibody activities with reduced acute viremia following intrarectal simian immunodeficiency virus SIVmac251 challenge of rhesus macaques. J Virol. 2009;83(2):791–801.
   PubMed Web of Science ®Google Scholar
• Xiao P, Patterson LJ, Kuate S, et al. Replicating adenovirus-simian immunodeficiency virus (SIV) recombinant priming and envelope protein boosting elicits localized, mucosal IgA immunity in rhesus macaques correlated with delayed acquisition following a repeated low-dose rectal SIV(mac251) challenge. J Virol. 2012;86(8):4644–4657.
   PubMed Web of Science ®Google Scholar
• Barouch DH, Alter G, Broge T, et al. HIV-1 vaccines. Protective efficacy of adenovirus/protein vaccines against SIV challenges in rhesus monkeys. Science. 2015;349(6245):320–324.
   PubMed Web of Science ®Google Scholar
• Gordon SN, Doster MN, Kines RC, et al. Antibody to the gp120 V1/V2 loops and CD4+ and CD8+ T cell responses in protection from SIVmac251 vaginal acquisition and persistent viremia. J Immunol. 2014;193(12):6172–6183.
   PubMed Web of Science ®Google Scholar
• Moody MA. Modulation of HIV-1 immunity by adjuvants. Curr Opin HIV AIDS. 2014;9(3):242–249.
   PubMed Web of Science ®Google Scholar
• Lee S, Nguyen MT. Recent advances of vaccine adjuvants for infectious diseases. Immune Netw. 2015;15(2):51–57.
   PubMed Web of Science ®Google Scholar
• Barnett SW, Burke B, Sun Y, et al. Antibody-mediated protection against mucosal simian-human immunodeficiency virus challenge of macaques immunized with alphavirus replicon particles and boosted with trimeric envelope glycoprotein in MF59 adjuvant. J Virol. 2010;84(12):5975–5985.
   PubMed Web of Science ®Google Scholar
• Wecker M, Gilbert P, Russell N, et al. Phase I safety and immunogenicity evaluations of an alphavirus replicon HIV-1 subtype C gag vaccine in healthy HIV-1-uninfected adults. Clin Vaccine Immunol. 2012;19(10):1651–1660.
   PubMed Web of Science ®Google Scholar
• Burton SL, Kilgore KM, Smith SA, et al. Breakthrough of SIV strain smE660 challenge in SIV strain mac239-vaccinated rhesus macaques despite potent autologous neutralizing antibody responses. Proc Natl Acad Sci U S A. 2015;112(34):10780–10785.
   PubMed Web of Science ®Google Scholar
• Iyer SS, Gangadhara S, Victor B, et al. Codelivery of envelope protein in alum with MVA vaccine induces CXCR3-biased CXCR5+ and CXCR5- CD4 T cell responses in rhesus macaques. J Immunol. 2015;195(3):994–1005.
   PubMed Web of Science ®Google Scholar
• Honda K, Littman DR. The microbiome in infectious disease and inflammation. Annu Rev Immunol. 2012;30:759–795.
   PubMed Web of Science ®Google Scholar
• Salas JT, Chang TL. Microbiome in human immunodeficiency virus infection. Clin Lab Med. 2014;34(4):733–745.
   PubMed Web of Science ®Google Scholar
• Williams WB, Liao HX, Moody MA, et al. HIV-1 VACCINES. Diversion of HIV-1 vaccine-induced immunity by gp41-microbiota cross-reactive antibodies. Science. 2015;349(6249):aab1253.
   PubMed Web of Science ®Google Scholar
• Tuero I, Mohanram V, Musich T, et al. Mucosal B cells are associated with delayed SIV acquisition in vaccinated female but not male rhesus macaques following SIVmac251 rectal challenge. PLoS Pathog. 2015;11(8):e1005101.
   PubMed Web of Science ®Google Scholar
• Klein SL. Sex influences immune responses to viruses, and efficacy of prophylaxis and treatments for viral diseases. Bioessays. 2012;34(12):1050–1059.
   PubMed Web of Science ®Google Scholar
• Addo MM, Altfeld M. Sex-based differences in HIV type 1 pathogenesis. J Infect Dis. 2014;209(Suppl 3):S86–S92.
   PubMed Web of Science ®Google Scholar
• Boesch AW, Alter G, Ackerman ME. Prospects for engineering HIV-specific antibodies for enhanced effector function and half-life. Curr Opin HIV AIDS. 2015;10(3):160–169.
   PubMed Web of Science ®Google Scholar