Glucopyranosyl lipid a adjuvant significantly enhances HIV specific T and B cell responses elicited by a DNA-MVA-protein vaccine regimen

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  McKay, Paul F ^a   Cope, Alethea V ^a   Mann, Jamie F S ^a   Joseph, Sarah ^b   Esteban, Mariano ^c   Tatoud, Roger ^a   Carter, Darrick ^d   Reed, Steven G ^d   Weber, Jonathan ^a   Shattock, Robin J ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b MRC CLINICAL TRIALS UNIT   (United Kingdom)

^c CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

^d INFECTIOUS DISEASE RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA VACCINE; GAG PROTEIN; GLUCOPYRANOSYL LIPID A; IMMUNOGLOBULIN G; LIPID A DERIVATIVE; NEF PROTEIN; POL PROTEIN; UNCLASSIFIED DRUG; VACCINIA VACCINE; VIRUS ENVELOPE PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY RESPONSE; ANTIGEN SPECIFICITY; ARTICLE; B LYMPHOCYTE; CONTROLLED STUDY; DRUG EFFICACY; FEMALE; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOGENICITY; MALE; MOUSE; MUCOSAL IMMUNITY; NONHUMAN; QUADRICEPS FEMORIS MUSCLE; RABBIT; T LYMPHOCYTE; VACCINATION; VIRUS IMMUNITY;

ADJUVANTS, IMMUNOLOGIC; AIDS VACCINES; ANIMALS; ANTIBODIES, VIRAL; B-LYMPHOCYTES; CELLS, CULTURED; CYTOKINES; ENV GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; FEMALE; HIV INFECTIONS; HUMANS; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; LIPID A; MALE; MICE; MICE, INBRED BALB C; PLASMIDS; RABBITS; SPLEEN; T-LYMPHOCYTES; VACCINATION; VACCINE POTENCY; VACCINES, DNA; VIRAL VACCINES;

EID: 84899877379     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0084707     Document Type: Article

References (55)

1. Hurwitz JL, Zhan X, Brown SA, Bonsignori M, Stambas J, et al. (2007) A Multi-Vector, Multi-Envelope HIV-1 Vaccine. J Pediatr Pharmacol Ther 12: 68-76.
2. Rerks-Ngarm S, Pitisuttithum P, Nitayaphan S, Kaewkungwal J, Chiu J, et al. (2009) Vaccination with ALVAC and AIDSVAX to prevent HIV-1 infection in Thailand. N Engl J Med 361: 2209-2220.
3. Amara RR, Smith JM, Staprans SI, Montefiori DC, Villinger F, et al. (2002) Critical role for Env as well as Gag-Pol in control of a simian-human immunodeficiency virus 89.6P challenge by a DNA prime/recombinant modified vaccinia virus Ankara vaccine. J Virol 76: 6138-6146. (Pubitemid 34556309)
4. Hanke T, Samuel RV, Blanchard TJ, Neumann VC, Allen TM, et al. (1999) Effective induction of simian immunodeficiency virus-specific cytotoxic T lymphocytes in macaques by using a multiepitope gene and DNA primemodified vaccinia virus Ankara boost vaccination regimen. J Virol 73: 7524- 7532.
5. Lu S (2009) Heterologous prime-boost vaccination. Curr Opin Immunol 21: 346-351.
6. Yang ZY, Wyatt LS, Kong WP, Moodie Z, Moss B, et al. (2003) Overcoming immunity to a viral vaccine by DNA priming before vector boosting. J Virol 77: 799-803. (Pubitemid 36005022)
7. Cox KS, Clair JH, Prokop MT, Sykes KJ, Dubey SA, et al. (2008) DNA gag/ adenovirus type 5 (Ad5) gag and Ad5 gag/Ad5 gag vaccines induce distinct Tcell response profiles. J Virol 82: 8161-8171.
8. Asmuth DM, Brown EL, DiNubile MJ, Sun X, del Rio C, et al. (2010) Comparative cell-mediated immunogenicity of DNA/DNA, DNA/adenovirus type 5 (Ad5), or Ad5/Ad5 HIV-1 clade B gag vaccine prime-boost regimens. J Infect Dis 201: 132-141.
9. Thorner AR, Lemckert AA, Goudsmit J, Lynch DM, Ewald BA, et al. (2006) Immunogenicity of heterologous recombinant adenovirus prime-boost vaccine regimens is enhanced by circumventing vector cross-reactivity. J Virol 80: 12009-12016. (Pubitemid 44904350)
10. Zak DE, Andersen-Nissen E, Peterson ER, Sato A, Hamilton MK, et al. (2012) Merck Ad5/HIV induces broad innate immune activation that predicts CD8(+) T-cell responses but is attenuated by preexisting Ad5 immunity. Proc Natl Acad Sci U S A 109: E3503-3512.
11. McKay PF, Barouch DH, Santra S, Sumida SM, Jackson SS, et al. (2004) Recruitment of different subsets of antigen-presenting cells selectively modulates DNA vaccine-elicited CD4+ and CD8+ T lymphocyte responses. Eur J Immunol 34: 1011-1020. (Pubitemid 39255979)
12. Barouch DH, McKay PF, Sumida SM, Santra S, Jackson SS, et al. (2003) Plasmid chemokines and colony-stimulating factors enhance the immunogenicity of DNA priming-viral vector boosting human immunodeficiency virus type 1 vaccines. J Virol 77: 8729-8735. (Pubitemid 36936084)
13. Kalams SA, Parker S, Jin X, Elizaga M, Metch B, et al. (2012) 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 7: e29231.
14. Park SH, Song MY, Nam HJ, Im SJ, Sung YC (2010) Codelivery of IL-7 Augments Multigenic HCV DNA Vaccine-induced Antibody as well as Broad T Cell Responses in Cynomolgus Monkeys. Immune Netw 10: 198-205.
15. Hallengard D, Applequist SE, Nystrom S, Maltais AK, Marovich M, et al. (2012) Immunization with multiple vaccine modalities induce strong HIVspecific cellular and humoral immune responses. Viral Immunol 25: 423-432.
16. Lu S, Wang S, Grimes-Serrano JM (2008) Current progress of DNA vaccine studies in humans. Expert Rev Vaccines 7: 175-191. (Pubitemid 351357954)
17. Harari A, Bart PA, StohrW, Tapia G, Garcia M, et al. (2008) An HIV-1 clade C DNA prime, NYVAC boost vaccine regimen induces reliable, polyfunctional, and long-lasting T cell responses. J Exp Med 205: 63-77. (Pubitemid 351185716)
18. Chahroudi A, Garber DA, Reeves P, Liu L, Kalman D, et al. (2006) Differences and similarities in viral life cycle progression and host cell physiology after infection of human dendritic cells with modified vaccinia virus Ankara and vaccinia virus. J Virol 80: 8469-8481. (Pubitemid 44384859)
19. Kastenmuller W, Drexler I, Ludwig H, Erfle V, Peschel C, et al. (2006) Infection of human dendritic cells with recombinant vaccinia virus MVA reveals general persistence of viral early transcription but distinct maturation-dependent cytopathogenicity. Virology 350: 276-288. (Pubitemid 43928113)
20. Bomsel M, Tudor D, Drillet AS, Alfsen A, Ganor Y, et al. (2011) Immunization with HIV-1 gp41 subunit virosomes induces mucosal antibodies protecting nonhuman primates against vaginal SHIV challenges. Immunity 34: 269-280.
21. Lambert SL, Yang CF, Liu Z, Sweetwood R, Zhao J, et al. (2012) Molecular and cellular response profiles induced by the TLR4 agonist-based adjuvant Glucopyranosyl Lipid A. PLoS One 7: e51618.
22. Xiao L, Kim J, Lim M, Dai B, Yang L, et al. (2012) A TLR4 agonist synergizes with dendritic cell-directed lentiviral vectors for inducing antigen-specific immune responses. Vaccine 30: 2570-2581.
23. Arias MA, Van Roey GA, Tregoning JS, Moutaftsi M, Coler RN, et al. (2012) Glucopyranosyl Lipid Adjuvant (GLA), a Synthetic TLR4 agonist, promotes potent systemic and mucosal responses to intranasal immunization with HIVgp140. PLoS One 7: e41144.
24. Hahn BH, Shaw GM, Taylor ME, Redfield RR, Markham PD, et al. (1986) Genetic variation in HTLV-III/LAV over time in patients with AIDS or at risk for AIDS. Science 232: 1548-1553. (Pubitemid 16061564)
25. Mansky LM (1998) Retrovirus mutation rates and their role in genetic variation. J Gen Virol 79 (Pt 6): 1337-1345.
26. Montefiori DC, Safrit JT, Lydy SL, Barry AP, Bilska M, et al. (2001) Induction of neutralizing antibodies and gag-specific cellular immune responses to an R5 primary isolate of human immunodeficiency virus type 1 in rhesus macaques. J Virol 75: 5879-5890. (Pubitemid 32553118)
27. Santra S, Barouch DH, Kuroda MJ, Schmitz JE, Krivulka GR, et al. (2002) Prior vaccination increases the epitopic breadth of the cytotoxic T-lymphocyte response that evolves in rhesus monkeys following a simian-human immuno-deficiency virus infection. J Virol 76: 6376-6381. (Pubitemid 34556333)
28. Barouch DH, Craiu A, Santra S, Egan MA, Schmitz JE, et al. (2001) Elicitation of high-frequency cytotoxic T-lymphocyte responses against both dominant and subdominant simian-human immunodeficiency virus epitopes by DNA vaccination of rhesus monkeys. J Virol 75: 2462-2467. (Pubitemid 32147585)
29. Jalah R, Patel V, Kulkarni V, Rosati M, Alicea C, et al. (2012) 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 8.
30. Khawaja G, Buronfosse T, Jamard C, Guerret S, Zoulim F, et al. (2012) Enhanced magnitude and breadth of neutralizing humoral response to a DNA vaccine targeting the DHBV envelope protein delivered by in vivo electroporation. Virology 425: 61-69.
31. Ferraro B, Cisper NJ, Talbott KT, Philipson-Weiner L, Lucke CE, et al. (2011) Co-delivery of PSA and PSMA DNA vaccines with electroporation induces potent immune responses. Hum Vaccin 7 Suppl: 120-127.
32. Brave A, Hinkula J, Cafaro A, Eriksson LE, Srivastava IK, et al. (2007) Candidate HIV-1 gp140DeltaV2, Gag and Tat vaccines protect against experimental HIV-1/MuLV challenge. Vaccine 25: 6882-6890. (Pubitemid 47391106)
33. Bielinska AU, Janczak KW, Landers JJ, Markovitz DM, Montefiori DC, et al. (2008) Nasal immunization with a recombinant HIV gp120 and nanoemulsion adjuvant produces Th1 polarized responses and neutralizing antibodies to primary HIV type 1 isolates. AIDS Res Hum Retroviruses 24: 271-281. (Pubitemid 351282102)
34. Otero M, Calarota SA, Felber B, Laddy D, Pavlakis G, et al. (2004) Resiquimod is a modest adjuvant for HIV-1 gag-based genetic immunization in a mouse model. Vaccine 22: 1782-1790. (Pubitemid 38455417)
35. Lycke N (2012) Recent progress in mucosal vaccine development: potential and limitations. Nat Rev Immunol 12: 592-605.
36. Alving CR, Peachman KK, Rao M, Reed SG (2012) Adjuvants for human vaccines. Curr Opin Immunol 24: 310-315.
37. Rodenburg CM, Li Y, Trask SA, Chen Y, Decker J, et al. (2001) Near full-length clones and reference sequences for subtype C isolates of HIV type 1 from three different continents. AIDS Res Hum Retroviruses 17: 161-168. (Pubitemid 32099300)
38. Su L, Graf M, Zhang Y, von Briesen H, Xing H, et al. (2000) Characterization of a virtually full-length human immunodeficiency virus type 1 genome of a prevalent intersubtype (C/B′) recombinant strain in China. J Virol 74: 11367-11376. (Pubitemid 32224007)
39. Cranage MP, Fraser CA, Stevens Z, Huting J, Chang M, et al. (2010) Repeated vaginal administration of trimeric HIV-1 clade C gp140 induces serum and mucosal antibody responses. Mucosal Immunol 3: 57-68.
40. Krashias G, Simon AK, Wegmann F, Kok WL, Ho LP, et al. (2010) Potent adaptive immune responses induced against HIV-1 gp140 and influenza virus HA by a polyanionic carbomer. Vaccine 28: 2482-2489.
41. Barouch DH, Yang ZY, Kong WP, Korioth-Schmitz B, Sumida SM, et al. (2005) A human T-cell leukemia virus type 1 regulatory element enhances the immunogenicity of human immunodeficiency virus type 1 DNA vaccines in mice and nonhuman primates. J Virol 79: 8828-8834. (Pubitemid 40934793)
42. Gomez CE, Najera JL, Jimenez V, Bieler K, Wild J, et al. (2007) Generation and immunogenicity of novel HIV/AIDS vaccine candidates targeting HIV-1 Env/Gag-Pol-Nef antigens of clade C. Vaccine 25: 1969-1992. (Pubitemid 46227680)
43. Gomez CE, Perdiguero B, Jimenez V, Filali-Mouhim A, Ghneim K, et al. (2012) Systems analysis of MVA-C induced immune response reveals its significance as a vaccine candidate against HIV/AIDS of clade C. PLoS One 7: e35485.
44. Baldwin SL, Shaverdian N, Goto Y, Duthie MS, Raman VS, et al. (2009) Enhanced humoral and Type 1 cellular immune responses with Fluzone adjuvanted with a synthetic TLR4 agonist formulated in an emulsion. Vaccine 27: 5956-5963.
45. Anderson RC, Fox CB, Dutill TS, Shaverdian N, Evers TL, et al. (2010) Physicochemical characterization and biological activity of synthetic TLR4 agonist formulations. Colloids Surf B Biointerfaces 75: 123-132.
46. Roederer M, Nozzi JL, Nason MC (2011) SPICE: exploration and analysis of post-cytometric complex multivariate datasets. Cytometry A 79: 167-174.
47. Da'Dara AA, Skelly PJ, Walker CM, Harn DA (2003) A DNA-prime/protein- boost vaccination regimen enhances Th2 immune responses but not protection following Schistosoma mansoni infection. Parasite Immunol 25: 429-437. (Pubitemid 38058020)
48. Fox CB, Baldwin SL, Vedvick TS, Angov E, Reed SG (2012) Effects on immunogenicity by formulations of emulsion-based adjuvants for malaria vaccines. Clin Vaccine Immunol 19: 1633-1640.
49. Gomes R, Teixeira C, Oliveira F, Lawyer PG, Elnaiem DE, et al. (2012) KSAC, a defined Leishmania antigen, plus adjuvant protects against the virulence of L. major transmitted by its natural vector Phlebotomus duboscqi. PLoS Negl Trop Dis 6: e1610.
50. Falivene J, Del Medico Zajac MP, Pascutti MF, Rodriguez AM, Maeto C, et al. (2012) Improving the MVA vaccine potential by deleting the viral gene coding for the IL-18 binding protein. PLoS One 7: e32220.
51. Mann JF, McKay PF, Arokiasamy S, Patel RK, Tregoning JS, et al. (2013) Mucosal application of gp140 encoding DNA polyplexes to different tissues results in altered immunological outcomes in mice. PLoS One 8: e67412.
52. Mann JF, Stieh D, Klein K, de Stegmann DS, Cranage MP, et al. (2012) Transferrin conjugation confers mucosal molecular targeting to a model HIV-1 trimeric gp140 vaccine antigen. J Control Release 158: 240-249.
53. Catanzaro AT, Roederer M, Koup RA, Bailer RT, Enama ME, et al. (2007) Phase I clinical evaluation of a six-plasmid multiclade HIV-1 DNA candidate vaccine. Vaccine 25: 4085-4092. (Pubitemid 46616987)
54. Chen H, Xu X, Lin HH, Chen SH, Forsman A, et al. (2008) Mapping the immune response to the outer domain of a human immunodeficiency virus-1 clade C gp120. J Gen Virol 89: 2597-2604.
55. Wu L, Kong WP, Nabel GJ (2005) Enhanced breadth of CD4 T-cell immunity by DNA prime and adenovirus boost immunization to human immuno-deficiency virus Env and Gag immunogens. J Virol 79: 8024-8031. (Pubitemid 40853506)