Nasal immunization with a recombinant HIV gp120 and nanoemulsion adjuvant produces Th1 polarized responses and neutralizing antibodies to primary HIV type 1 isolates

AIDS Research and Human Retroviruses

Volumn 24, Issue 2, 2008, Pages 271-281

  Bielinska, Anna U ^a   Janczak, Katarzyna W ^a   Landers, Jeffrey J ^a   Markovitz, David M ^b   Montefiori, David C ^c   Baker Jr , James R ^a,d  

^a UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c DUKE UNIVERSITY MEDICAL CENTER   (United States)

^d UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; GLYCOPROTEIN GP 120; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; NEUTRALIZING ANTIBODY; WATER OIL CREAM;

ANIMAL EXPERIMENT; ARTICLE; CELL PROLIFERATION; CELLULAR IMMUNITY; CONTROLLED STUDY; FEMALE; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IMMUNIZATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; SEROTYPE; TH1 CELL;

ADJUVANTS, IMMUNOLOGIC; ADMINISTRATION, INTRANASAL; ANIMALS; CELL PROLIFERATION; CROSS REACTIONS; EMULSIONS; FEMALE; GUINEA PIGS; HIV ANTIBODIES; HIV ENVELOPE PROTEIN GP120; HIV-1; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; INTERFERON TYPE II; LUNG; MICE; T-LYMPHOCYTES, CYTOTOXIC; VACCINES, SYNTHETIC; VAGINA;

EID: 39549118132     PISSN: 08892229     EISSN: None     Source Type: Journal    
DOI: 10.1089/aid.2007.0148     Document Type: Article

References (84)

1. Burton DR: A vaccine for HIV type 1: The antibody perspective. Proc Natl Acad Sci USA 1997;94:10018-10023.
2. Burton DR, Desrosiers RC, Doms RW, et al.: HIV vaccine design and the neutralizing antibody problem. Nat Immunol 2004;5:233-236.
3. Letvin NL: Progress and obstacles in the development of an AIDS vaccine. Nat Rev Immunol 2006;6:930-939.
4. Srivastava IK, Stamatatos L, Legg H, et al.: Purification and characterization of oligomeric envelope glycoprotein from a primary R5 subtype B human immunodeficiency virus. J Virol 2002;76:2835-2847.
5. Barnett SW, Lu S, Srivastava I, et al.: The ability of an oligomeric human immunodeficiency virus type 1 (HIV-1) envelope antigen to elicit neutralizing antibodies against primary HIV-1 isolates is improved following partial deletion of the second hypervariable region. J Virol 2001;75:5526-5540.
6. Spearman P: Current progress in the development of HIV vaccines. Curr Pharm Des 2006;12:1147-1167.
7. Cohen J: Public health: AIDS vaccine still alive as booster after second failure in Thailand. Science 2003;302:1309a-1310.
8. McMichael AJ: HIV vaccines. Annu Rev Immunol 2006;24:227-255.
9. Takahashi, Nakagawa Y, Pendleton CD, et al.: Induction of broadly cross-reactive cytotoxic T cells recognizing an HIV-1 envelope determinant. Science 1992;255:333-336.
10. Baba TW, Liska V, Hofmann-Lehmann R, et al.: Human neutralizing monoclonal antibodies of the IgG1 subtype protect against mucosal simian-human immunodeficiency virus infection. Nat Med 2000;6:200-206.
11. Betts MR, Nason MC, West SM, et al.: HIV nonprogressors preferentially maintain highly functional HIV-specific CD8+ T cells. Blood 2006;107:4781-4789.
12. Grundner C, Li Y, Louder M, et al.: Analysis of the neutralizing antibody response elicited in rabbits by repeated inoculation with trimeric HIV-1 envelope glycoproteins. Virology 2005;331:33-46.
13. Koup RA, Safrit JT, Cao Y, et al.: Temporal association of cellular immune responses with the initial control of viremia in primary human immunodeficiency virus type 1 syndrome. J Virol 1994;68:4650-4655.
14. Nabel GJ: Challenges and opportunities for development of an AIDS vaccine. Nature 2001;410:1002-1007.
15. Ogg GS, Jin X, Bonhoeffer S, et al.: Quantitation of HIV-1-specific cytotoxic T lymphocytes and plasma load of viral RNA. Science 1998;279:2103-2106.
16. Rosenberg ES, Altfeld M, Poon SH, et al.: Immune control of HIV-1 after early treatment of acute infection. Nature 2000;407:523-526.
17. Catanzaro AT, Koup RA, Roederer M, et al.: Phase 1 safety and immunogenicity evaluation of a multiclade HIV-1 candidate vaccine delivered by a replication-defective recombinant adenovirus vector. J Infect Dis 2006;194:1638-1649.
18. Graham BS, Koup RA, Roederer M, et al.: Phase 1 safety and immunogenicity evaluation of a multiclade HIV-1 DNA candidate vaccine. J Infect Dis 2006;194:1650-1660.
19. Neutra MR and Kozlowski PA: Mucosal vaccines: The promise and the challenge. Nat Rev Immunol 2006;6:148-158.
20. Pantaleo G and Koup RA: Correlates of immune protection in HIV-1 infection: What we know, what we don't know, what we should know. Nat Med 2004;10:806-810.
21. Shu Y, Winfrey S, Yang Z-y, et al.: Efficient protein boosting after plasmid DNA or recombinant adenovirus immunization with HIV-1 vaccine constructs. Vaccine 2007;25:1398-1408.
22. Goepfert PA, Horton H, McElrath MJ, et al.: High-dose recombinant canarypox vaccine expressing HIV-1 protein, in seronegative human subjects. J Infect Dis 2005;192:1249-1259.
23. Lu X, Wu S, Blackwell CE, Humphreys RE, von Hofe E, and Xu M: Suppression of major histocompatibility complex class II-associated invariant chain enhances the potency of an HIV gp120 DNA vaccine. Immunology 2007;120:207-216.
24. Mazzoli S, Trabaironi D, Caputo SL, et al.: HIV-specific mucosal and cellular immunity in HIV-seronegative partners of HIV-seropositive individuals. Nat Med 1997;3:1250-1257.
25. Vajdy M, Singh M, Kazzaz J, et al.: Mucosal and systemic anti-HIV responses in rhesus macaques following combinations of intranasal and parenteral immunizations. AIDS Res Hum Retroviruses 2004;20:1269-1281.
26. Vajdy M, Srivastava I, Polo J, Donnelly J, O'Hagan D, and Singh M: Mucosal adjuvants and delivery systems for protein-, DNA- and RNA-based vaccines. Immunol Cell Biol 2004;82:617-627.
27. Balmelli C, Demotz S, Acha-Orbea H, De Grandi P, and Nardelli-Haefliger D: Trachea, lung, and tracheobronchial lymph nodes are the major sites where antigen-presenting cells are detected after nasal vaccination of mice with human papillomavirus type 16 virus-like particles. J Virol 2002;76:12596-12602.
28. Gallichan WS, Woolstencroft RN, Guarasci T, McCluskie MJ, Davis HL, and Rosenthal KL: Intranasal immunization with CpG oligodeoxynucleotides as an adjuvant dramatically increases IgA and protection against herpes simplex virus-2 in the genital tract. J Immunol 2001;166:3451-3457.
29. Takada A, Matsushita S, Ninomiya A, Kawaoka Y, and Kida H: Intranasal immunization with formalin-inactivated virus vaccine induces a broad spectrum of heterosubtypic immunity against influenza A virus infection in mice. Vaccine 2003;21:3212-3218.
30. Yasuda Y, Isaka M, Taniguchi T, et al.: Frequent nasal administrations of recombinant cholera toxin B subunit (rCTB)-containing tetanus and diphtheria toxoid vaccines induced antigen-specific serum and mucosal immune responses in the presence of anti-rCTB antibodies. Vaccine 2003;21:2954-2963.
31. Akagi T, Kawamura M, Ueno M, Hiraishi K, Adachi M, Serizawa T, Akashi M, and Baba M: Mucosal immunization with inactivated HIV-1-capturing nanospheres induces a significant HIV-1-specific vaginal antibody response in mice. J Med Virol 2003;69:163-172.
32. Dumais N, Patrick A, Moss RB, Davis HL, and Rosenthal KL: Mucosal immunization with inactivated human immunodeficiency virus plus CpG oligodeoxynucleotides induces genital immune responses and protection against intravaginal challenge. J Infect Dis 2002;186:1098-1105.
33. 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;20:1949-1955.
34. Gherardi MM and Esteban M: Recombinant poxviruses as mucosal vaccine vectors. J Gen Virol 2005;86:2925-2936.
35. Golding B, Eller N, Levy L, et al.: Mucosal immunity in mice immunized with HIV-1 peptide conjugated to Brucella abortus. Vaccine 2002;20:1445-1450.
36. Joseph J, Saubi N, Pezzat E, and Gatell JM: Progress towards an HIV vaccine based on recombinant Bacillus Calamette-Guerin: Failures and challenges. Expert Rev Vaccines 2006;5:827-838.
37. Buonaguro L, Tornesello ML, Tagliamonte M, et al.: Baculovirus-derived human immunodeficiency virus type 1 virus-like particles activate dendritic cells and induce ex vivo T-cell responses. J Virol 2006;80:9134-9143.
38. Lundholm P, Leandersson A-C, Christensson B, Bratt G, Sandstrom E, and Wahren B: DNA mucosal HIV vaccine in humans. Virus Res 2002;82:141-145.
39. Singh M, Vajdy M, Gardner J, Briones M, and O'Hagan D: Mucosal immunization with HIV-1 gag DNA on cationic microparticles prolongs gene expression and enhances local and systemic immunity. Vaccine 2001;20:594-602.
40. Albu DI, Jones-Trower A, Woron AM, Stellrecht K, Broder CC, and Metzger DW: Intranasal vaccination using interleukin-12 and cholera toxin subunit B as adjuvants to enhance mucosal and systemic immunity to human immunodeficiency virus type 1 glycoproteins. J Virol 2003;77:5589-5597.
41. Bradney CP, Sempowski GD, Liao H-X, Haynes BF, and Staats HF: Cytokines as adjuvants for the induction of anti-human immunodeficiency virus peptide immunoglobulin G (IgG) and IgA antibodies in serum and mucosal secretions after nasal immunization. J Virol 2002;76:517-524.
42. Wu HY and Russell MW: Induction of mucosal immunity by intranasal application of a streptococcal surface protein antigen with the cholera toxin B subunit. Infect Immun 1993;61:314-322.
43. Donnelly S, Loscher CE, Lynch MA, and Mills KHG: Whole-cell but not acellular pertussis vaccines induce convulsive activity in mice: Evidence of a role for toxin-induced interleukin-1 beta in a new murine model for analysis of neuronal side effects of vaccination. Infect Immun 2001;69:4217-4223.
44. Mutsch M, Zhou W, Rhodes P, et al.: Use of the inactivated intranasal influenza vaccine and the risk of Bell's palsy in Switzerland. N Engl J Med 2004;350:896-903.
45. van Ginkel FW, Jackson RJ, Yuki Y, and McGhee JR: Cutting edge: The mucosal adjuvant cholera toxin redirects vaccine proteins into olfactory tissues. 2000;165:4778-4782.
46. Belyakov IM, Ahlers J, and Berzofsky JA: Mucosal AIDS vaccines: Current status and future. Expert Rev Vaccines 2004;3:S65-73.
47. Eriksson K and Holmgren J: Recent advances in mucosal vaccines and adjuvants. Curr Opin Immunol 2002;14:666-672.
48. Yuki Y and Kiyono H: New generation of mucosal adjuvants for the induction of protective immunity. Rev Med Virol 2003;13:293-310. US Patent No. 6,015,832, 2000.
49. Hamouda T, Myc A, Donovan B, Shih AY, Reuter JD, and Baker JRJ: A novel surfactant nanoemulsion with a unique non-irritant topical antimicrobial activity against bacteria, enveloped viruses and fungi. Microbiol Res 2001;156:1-7.
50. Myc A, Kukowska-Latallo JF, Bielinska AU, et al.: Development of immune response that protects mice from viral pneumonitis after a single intranasal immunization with influenza A virus and nanoemulsion. Vaccine 2003;21:3801-3814.
51. Bielinska AU, Janczak KW, Landers JJ, et al.: Mucosal immunization with a novel nanoemulsion-based recombinant anthrax protective antigen vaccine protects against Bacillus anthracis spore challenge. Infect Immun 2007;75:4020-4029.
52. Moldoveanu Z, Love-Homan L, Huang WQ, and Krieg AM: CpG DNA, a novel immune enhancer for systemic and mucosal immunization with influenza virus. Vaccine 1998;16:1216-1224.
53. Li M, Gao F, Mascola JR, et al.: Human immunodeficiency virus type 1 env clones from acute and early subtype B infections for standardized assessments of vaccine-elicited neutralizing antibodies. J Virol 2005;79:10108-10125.
54. Montefiori DC: Evaluating neutralizing antibodies against HIV, SIV and SHIV in luciferase reporter gene assays. In: Current Protocols in Immunology (Coligan J, Kruisbeek A, Margulies D, Shevach E, Strober W, and Coico R, eds.). John Wiley & Sons, New York, 2004, pp. 12.11.11-12.11.15.
55. Mascola JR: Defining the protective antibody response to HIV-1. Curr Mol Med 2003;3:209-216.
56. Kwong PD, Wyatt R, Robinson J, Sweet RW, Sodroski J, and Hendrickson WA: Structure of an HIV gp120 envelope glycoprotein in complex with the CD4 receptor and a neutralizing human antibody. Nature 1998;393:648-659.
57. Holmgren J and Czerkinsky C: Mucosal immunity and vaccines. Nat Med 2005;11(4 Suppl.):S45-53.
58. O'Hagan DT, Ugozzoli M, Barackman J, et al.: Microparticles in MF59, a potent adjuvant combination for a recombinant protein vaccine against HIV-1. Vaccine 2000;18:1793-1801.
59. Vajdy M and Singh M: Intranasal delivery of vaccines against HIV. Expert Opin Drug Deliv 2006;3:247-259.
60. Varona-Santos JT, Vazquez-Padron RI, and Moreno-Fierros L: Production of a short recombinant C4V3 HIV-1 immunogen that induces strong anti-HIV responses by systemic and mucosal routes without the need of adjuvants. Viral Immunol 2006;19:237-249.
61. 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;54:189-201.
62. Mascola JR, Sambor A, Beaudry K, et al.: Neutralizing antibodies elicited by immunization of monkeys with DNA plasmids and recombinant adenoviral vectors expressing human immunodeficiency virus type 1 proteins. J Virol 2005;79:771-779.
63. Wu L, Kong W-p, and Nabel GJ: Enhanced breadth of CD4 T-cell immunity by DNA prime and adenovirus boost immunization to human immunodeficiency virus Env and Gag immunogens. J Virol 2005;79:8024-8031.
64. Holmgren J, Adamsson J, Anjuere F, et al.: Mucosal adjuvants and anti-infection and anti-immunopathology vaccines based on cholera toxin, cholera toxin B subunit and CpG DNA. Immunol Lett 2005;97:181-188.
65. Johansson E-L, Wassen L, Holmgren J, Jertborn M, and Rudin A: Nasal and vaginal vaccinations have differential effects on antibody responses in vaginal and cervical secretions in humans. Infect Immun 2001;69:7481-7486.
66. Kozlowski PA, Cu-Uvin S, Neutra MR, and Flanigan TP: Comparison of the oral, rectal, and vaginal immunization routes for induction of antibodies in rectal and genital tract secretions of women. Infect Immun 1997;65:1387-1394.
67. Johansson E-L, Rask C, Fredriksson M, Eriksson K, Czerkinsky C, and Holmgren J: Antibodies and antibody-secreting cells in the female genital tract after vaginal or intranasal immunization with cholera toxin B subunit or conjugates. Infect Immun 1998;66:514-520.
68. Mestecky J: Humoral immune responses to the human immunodeficiency virus type-1 (HIV-1) in the genital tract compared to other mucosal sites. J Reprod Immunol 2006;72:1-17.
69. Russell MW and Mestecky J: Humoral immune responses to microbial infections in the genital tract. Microbes Infect 2002;4:667-677.
70. Li Y, Svehla K, Mathy NL, Voss G, Mascola JR, and Wyatt R: Characterization of antibody responses elicited by human immunodeficiency virus type 1 primary isolate trimeric and monomeric envelope glycoproteins in selected adjuvants. J Virol 2006;80:1414-1426.
71. Mascola JR, D'Souza P, Gilbert P, et al.: Recommendations for the design and use of standard virus panels to assess neutralizing antibody responses elicited by candidate human immunodeficiency virus type 1 vaccines. J Virol 2005;79:10103-10107.
72. Goodenow MM and Collman RG: HIV-1 coreceptor preference is distinct from target cell tropism: A dual-parameter nomenclature to define viral phenotypes. J Leukoc Biol 2006;80:965-972.
73. Gorse GJ, Corey L, Patel GB, et al.: HIV-1MN recombinant glycoprotein gp160 vaccine-induced cellular and humoral immunity boosted with HIV-1MN recombinant glycoprotein120 vaccine. National Institute of Allergy and Infectious Diseases AIDS Vaccine Evaluation Group. AIDS Res Hum Retroviruses 1999;15:115-132.
74. Wrin T, Loh TP, Vennari JC, Schuitemaker H, and Nunberg JH: Adaptation to persistent growth in the H9 cell line renders a primary isolate of human immunodeficiency virus type 1 sensitive to neutralization by vaccine sera. J Virol 1995;69:39-48.
75. Andrianov AM and Veresov VG: Determination of structurally conservative amino acids of the HIV-1 protein gp120 V3 loop as promising targets for drug design by protein engineering approaches. Biochemistry (Moscow) 2006;V71:906-914.
76. Carmichael A, Jin X, and Sissons P: Analysis of the human env-specific cytotoxic T-lymphocyte (CTL) response in natural human immunodeficiency virus type 1 infection: Low prevalence of broadly cross-reactive env-specific CTL. J Virol 1996;70:8468-8476.
77. Bradley LM, Dalton DK, and Croft M: A direct role for IFN-gamma in regulation of Th1 cell development. J Immunol 1996;157:1350-1358.
78. Mosmann TR: T lymphocyte subsets, cytokines, and effector functions. Ann NY Acad Sci 1992;664:89-92.
79. Kornbluth RS and Stone GW: Immunostimulatory combinations: Designing the next generation of vaccine adjuvants. J Leukoc Biol 2006;80:1084-1102.
80. Hartmann G, Weeratna RD, Ballas ZK, et al.: Delineation of a CpG phosphorothioate oligodeoxynucleotide for activating primate immune responses in vitro and in vivo. J Immunol 2000;164:1617-1624.
81. Klinman DM, Xie H, and Ivins BE: CpG oligonucleotides improve the protective immune response induced by the licensed anthrax vaccine. Ann NY Acad Sci 2006;1082:137-150.
82. Kojima Y, Xin K-Q, Ooki T, et al.: Adjuvant effect of multi-CpG motifs on an HIV-1 DNA vaccine. Vaccine 2002;20:2857-2865.
83. VanCott TC, Kaminski RW, Mascola JR, et al.: HIV-1 neutralizing antibodies in the genital and respiratory tracts of mice intranasally immunized with oligomeric gp160. J Immunol 1998;160:2000-2012.
84. Greene S, Fortier A, Dijkstra J, et al.: Liposomal vaccines. Adv Exp Med Biol 1995;383:83-92.