Enhancement of mucosal immunization with virus-like particles of simian immunodeficiency virus

Journal of Virology

Volumn 77, Issue 6, 2003, Pages 3615-3623

  Kang, Sang Moo ^a   Compans, Richard W ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLERA TOXIN; DNA; GAMMA INTERFERON; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G2A; IMMUNOLOGICAL ADJUVANT; INTERLEUKIN 4; NEUTRALIZING ANTIBODY; RANTES; VIRUS ENVELOPE PROTEIN;

ADOLESCENT; ANIMAL CELL; ANIMAL TISSUE; ANTIBODY RESPONSE; ANTIBODY SPECIFICITY; ANTIBODY TITER; ARTICLE; CELLULAR IMMUNITY; CONTROLLED STUDY; CPG ISLAND; CYTOTOXIC T LYMPHOCYTE; FEMALE; HUMORAL IMMUNITY; IMMUNE RESPONSE; IMMUNIZATION; LYMPH NODE; MOUSE; MUCOSAL IMMUNITY; NONHUMAN; PRIORITY JOURNAL; SIMIAN IMMUNODEFICIENCY VIRUS; SPLEEN; TH1 CELL; VIRUS PARTICLE;

ADJUVANTS, IMMUNOLOGIC; ADMINISTRATION, INTRANASAL; ANIMALS; ANTIBODIES, VIRAL; CHOLERA TOXIN; FEMALE; HUMANS; IMMUNIZATION; IMMUNOGLOBULIN A, SECRETORY; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED BALB C; NEUTRALIZATION TESTS; OLIGODEOXYRIBONUCLEOTIDES; RANTES; SAIDS VACCINES; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; T-LYMPHOCYTES, CYTOTOXIC; VIRION;

EID: 0037333412     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.77.6.3615-3623.2003     Document Type: Article

References (77)

1. Bauer, M., V. Redecke, J. W. Ellwart, B. Scherer, J. P. Kremer, H. Wagner, and G. B. Lipford. 2001. Bacterial CpG-DNA triggers activation and maturation of human CD11c-, CD123+ dendritic cells. J. Immunol. 166:5000-5007.
2. Behl, C., J. B. Davis, R. Lesley, and D. Schubert. 1994. Hydrogen peroxide mediates amyloid beta protein toxicity. Cell 77:817-827.
3. Bonecchi, R., G. Bianchi, P. P. Bordignon, D. D'Ambrosio, R. Lang, A. Borsatti, S. Sozzani, P. Allavena, P. A. Gray, A. Mantovani, and F. Sinigaglia. 1998. Differential expression of chemokine receptors and chemotactic responsiveness of type 1 T helper cells (Th1s) and Th2s. J. Exp. Med. 187: 129-134.
4. Bowen, J. C., S. K. Nair, R. Reddy, and B. T. Rouse. 1994. Cholera toxin acts as a potent adjuvant for the induction of cytotoxic T-lymphocyte responses with non-replicating antigens. Immunology 81:338-342.
5. Brander, C., T. Wyss-Coray, D. Mauri, F. Bettens, and W. J. Pichler. 1993. Carrier-mediated uptake and presentation of a major histocompatibility complex class I-restricted peptide. Eur. J. Immunol. 23:3217-3223.
6. Chackerian, B., D. R. Lowy, and J. T. Schiller. 2001. Conjugation of a self-antigen to papillomavirus-like particles allows for efficient induction of protective autoantibodies. J. Clin. Investig. 108:415-423.
7. Chu, R. S., O. S. Targoni, A. M. Krieg, P. V. Lehmann, and C. V. Harding. 1997. CpG oligodeoxynucleotides act as adjuvants that switch on T helper 1 (Th1) immunity. J. Exp. Med. 186:1623-1631.
8. Coffman, R. L., K. Varkila, P. Scott, and R. Chatelain. 1991. Role of cytokines in the differentiation of CD4+ T-cell subsets in vivo. Immunol. Rev. 123:189-207.
9. Davis, H. L., R. Weeratna, T. J. Waldschmidt, L. Tygrett, J. Schorr, A. M. Krieg, and R. Weeranta. 1998. CpG DNA is a potent enhancer of specific immunity in mice immunized with recombinant hepatitis B surface antigen. J. Immunol. 160:870-876.
10. Decker, T., and M. L. Lohmann-Matthes. 1988. A quick and simple method for the quantitation of lactate dehydrogenase release in measurements of cellular cytotoxicity and tumor necrosis factor (TNF) activity. J. Immunol. Methods 115:61-69.
11. Deml, L., G. Kratochwil, N. Osterrieder, R. Knuchel, H. Wolf, and R. Wagner. 1997. Increased incorporation of chimeric human immunodeficiency virus type 1 gp120 proteins into Pr55gag virus-like particles by an Epstein-Barr virus gp220/350-derived transmembrane domain. Virology 235: 10-25.
12. Edinger, A. L., M. Ahuja, T. Sung, K. C. Baxter, B. Haggarty, R. W. Doms, and J. A. Hoxie. 2000. Characterization and epitope mapping of neutralizing monoclonal antibodies produced by immunization with oligomeric simian immunodeficiency virus envelope protein. J. Virol. 74:7922-7935.
13. Gallichan, W. S., R. N. Woolstencroft, T. Guarasci, M. J. McCluskie, H. L. Davis, and K. L. Rosenthal. 2001. Intranasal immunization with CpG oligodeoxynucleotides as an adjuvant dramatically increases IgA and protection against herpes simplex virus-2 in the genital tract. J. Immunol. 166:3451-3457.
14. Gomez, R. S., J. E. da Costa, T. M. Lorentz, A. Garrocho Ade, and J. A. Nogueira-Machado. 1994. Chemoluminescence generation and MTT dye reduction by polymorphonuclear leukocytes from periodontal disease patients. J. Periodontal Res. 29:109-112.
15. Haffar, O., J. Garrigues, B. Travis, P. Moran, J. Zarling, and S.-L. Hu. 1990. Human immunodeficiency virus-like, nonreplicating, gag-env particles assemble in a recombinant vaccinia virus expression system. J. Virol. 64:2653-2659.
16. Hameleers, D. M., I. van der Ven, J. Biewenga, and T. Sminia. 1991. Mucosal and systemic antibody formation in the rat after intranasal administration of three different antigens. Immunol. Cell Biol. 69:119-125.
17. Hemmi, H., O. Takeuchi, T. Kawai, T. Kaisho, S. Sato, H. Sanjo, M. Matsumoto, K. Hoshino, H. Wagner, K. Takeda, and S. Akira. 2000. A Toll-like receptor recognizes bacterial DNA. Nature 408:740-745.
18. Horner, A. A., S. K. Datta, K. Takabayashi, I. M. Belyakov, T. Hayashi, N. Cinman, M. D. Nguyen, J. H. Van Uden, J. A. Berzofsky, D. D. Richman, and E. Raz. 2001. Immunostimulatory DNA-based vaccines elicit multifaceted immune responses against HIV at systemic and mucosal sites. J. Immunol. 167:1584-1591.
19. Horner, A. A., A. Ronaghy, P. M. Cheng, M. D. Nguyen, H. J. Cho, D. Broide, and E. Raz. 1998. Immunostimulatory DNA is a potent mucosal adjuvant. Cell. Immunol. 190:77-82.
20. Isaka, M., Y. Yasuda, M. Mizokami, S. Kozuka, T. Taniguchi, K. Matano, J. Maeyama, K. Mizuno, K. Morokuma, K. Ohkuma, N. Goto, and K. Tochikubo. 2001. Mucosal immunization against hepatitis B virus by intranasal co-administration of recombinant hepatitis B surface antigen and recombinant cholera toxin B subunit as an adjuvant. Vaccine 19:1460-1466.
21. Johansson, E. L., C. Rask, M. Fredriksson, K. Eriksson, C. Czerkinsky, and J. Holmgren. 1998. Antibodies and antibody-secreting cells in the female genital tract after vaginal or intranasal immunization with cholera toxin B subunit or conjugates. Infect. Immun. 66:514-520.
22. Jones, D. H., B. W. McBride, M. A. Roff, and G. H. Farrar. 1995. Efficient purification and rigorous characterisation of a recombinant gp120 for HIV vaccine studies. Vaccine 13:991-999.
23. Jones, D. H., B. W. McBride, M. A. Roff, V. Maloney, and G. H. Farrar. 1994. Purification and characterization of simian immunodeficiency virus (SIVmac) envelope glycoprotein gp130 from virus-infected cells. Vaccine 12:250-258.
24. Jones, T. R., N. Obaldia III, R. A. Gramzinski, Y. Charoenvit, N. Kolodny, S. Kitov, H. L. Davis, A. M. Krieg, and S. L. Hoffman. 1999. Synthetic oligodeoxynucleotides containing CpG motifs enhance immunogenicity of a peptide malaria vaccine in Aotus monkeys Vaccine 17:3065-3071.
25. Kadowaki, N., S. Antonenko, S. Ho, M. C. Rissoan, V. Soumelis, S. A. Porcelli, L. L. Lanier, and Y. J. Liu. 2001. Distinct cytokine profiles of neonatal natural killer T cells after expansion with subsets of dendritic cells. J. Exp. Med. 193:1221-1226.
26. Kameyoshi, Y., A. Dorschner, A. I. Mallet, E. Christophers, and J. M. Schroder. 1992. Cytokine RANTES released by thrombin-stimulated platelets is a potent attractant for human cosinophils. J. Exp. Med. 176:587-592.
27. Klinman, D. M., A. K. Yi, S. L. Beaucage, J. Conover, and A. M. Krieg. 1996. CpG motifs present in bacteria DNA rapidly induce lymphocytes to secrete interleukin 6, interleukin 12, and interferon gamma. Proc. Natl. Acad. Sci. USA 93:2879-2883.
28. Korzeniewski, C., and D. M. Callewaert. 1983. An enzyme-release assay for natural cytotoxicity. J. Immunol. Methods 64:313-320.
29. Krausslich, H. G., C. Ochsenbauer, A. M. Traenckner, K. Mergener, M. Facke, H. R. Gelderblom, and V. Bosch. 1993. Analysis of protein expression and virus-like particle formation in mammalian cell lines stably expressing HIV-1 gag and env gene products with or without active HIV proteinase. Virology. 192:605-617.
30. Krieg, A. M., A. K. Yi, S. Matson, T. J. Waldschmidt, G. A. Bishop, R. Teasdale, G. A. Koretzky, and D. M. Klinman. 1995. CpG motifs in bacterial DNA trigger direct B-cell activation. Nature 374:546-549.
31. Kuper, C. F., P. J. Koornstra, D. M. Hameleers, J. Biewenga, B. J. Spit, A. M. Duijvestijn, P. J. Breda Vriesman, and T. Sminia. 1992. The role of nasopharyngeal lymphoid tissue. Immunol. Today 13:219-224.
32. + T cells while decreasing IL-2 release and NF-AT induction. Int. Immunol. 6:1333-1343.
33. Lagranderie, M., N. Winter, A. M. Balazuc, B. Gicquel, and M. Gheorghiu. 1998. A cocktail of Mycobacterium bovis BCG recombinants expressing the SIV Nef, Env, and Gag antigens induces antibody and cytotoxic responses in mice vaccinated by different mucosal routes. AIDS Res. Hum. Retroviruses 14:1625-1633.
34. Lian, T., T. Bui, and R. J. Ho. 1999. Formulation of HIV-envelope protein with lipid vesicles expressing ganglioside GM1 associated to cholera toxin B enhances mucosal immune responses. Vaccine 18:604-611.
35. Lillard, J. W., Jr., P. N. Boyaka, D. D. Taub, and J. R. McGhee. 2001. RANTES potentiates antigen -specific mucosal immune responses. J. Immunol. 166:162-169.
36. Lim, E. M., M. Lagranderie, R. Le Grand, J. Rauzier, M. Gheorghiu, B. Gicquel, and N. Winter. 1997. Recombinant Mycobacterium bovis BCG producing the N-terminal half of SIVmac251 Env antigen induces neutralizing antibodies and cytotoxic T lymphocyte responses in mice and guinea pigs. AIDS Res. Hum. Retroviruses 13:1573-1581.
37. Lipford, G. B., M. Bauer, C. Blank, R. Reiter, H. Wagner, and K. Heeg. 1997. CpG-containing synthetic oligonucleotides promote B and cytotoxic T cell responses to protein antigen: a new class of vaccine adjuvants. Eur. J. Immunol. 27:2340-2344.
38. Matsukura, S., F. Kokubu, H. Kubo, T. Tomita, H. Tokunaga, M. Kadokura, T. Yamamoto, Y. Kuroiwa, T. Ohno, H. Suzaki, and M. Adachi. 1998. Expression of RANTES by normal airway epithelial cells after influenza virus A infection. Am. J. Respir. Cell Mol. Biol. 18:255-264.
39. McCluskie, M. J., and H. L. Davis. 1998. CpG DNA is a potent enhancer of systemic and mucosal immune responses against hepatitis B surface antigen with intranasal administration to mice. J. Immunol. 161:4463-4466.
40. McCluskie, M. J., R. D. Weeratna, and H. L. Davis. 2000. Intranasal immunization of mice with CpG DNA induces strong systemic and mucosal responses that are influenced by other mucosal adjuvants and antigen distribution. Mol. Med. 6:867-877.
41. McCluskie, M. J., R. D. Weeratna, and H. L. Davis. 2001. The potential of oligodeoxynucleotides as mucosal and parenteral adjuvants. Vaccine 19: 2657-2660.
42. Meyer, D., and J. V. Torres. 1999. Induction of cytotoxic and helper T cell responses by modified simian immunodeficiency virus hypervariable epitope constructs. Viral Immunol. 12:117-129.
43. Moldoveanu, Z., L. Love-Homan, W. Q. Huang, and A. M. Krieg. 1998. CpG DNA, a novel immune enhancer for systemic and mucosal immunization with influenza virus. Vaccine 16:1216-1224.
44. Moldoveanu, Z., A. N. Vzorov, W. Q. Huang, J. Mestecky, and R. W. Compans. 1999. Induction of immune responses to SIV antigens by mucosally administered vaccines. AIDS Res. Hum. Retroviruses. 15:1469-1476.
45. Montefiori, D. C., J. T. Safrit, S. L. Lydy, A. P. Barry, M. Bilska, H. T. T. Vo, M. Klein, J. Tartaglia, H. L. Robinson, and B. Rovinski. 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.
46. Morris, C. B., E. Cheng, A. Thanawastien, L. Cardenas-Freytag, and J. D. Clements. 2000. Effectiveness of intranasal immunization with HIV-gp160 and an HIV-1 env CTL epitope peptide (E7) in combination with the mucosal adjuvant LT(R192G). Vaccine 18:1944-1951.
47. Munoz, E., A. M. Zubiaga, M. Merrow, N. P. Sauter, and B. T. Huber. 1990. Cholera toxin discriminates between T helper 1 and 2 cells in T cell receptor-mediated activation: role of cAMP in T cell proliferation. J. Exp. Med. 172:95-103.
48. Neote, K., D. DiGregorio, J. Y. Mak, R. Horuk, and T. J. Schall. 1993. Molecular cloning, functional expression, and signaling characteristics of a C-C chemokine receptor. Cell 72:415-425.
49. Niks, M., M. Otto, B. Busova, and J. Stefanovic. 1990. Quantification of proliferative and suppressive responses of human T lymphocytes following ConA stimulation. J. Immunol. Methods 126:263-271.
50. Notka, F., C. Stahl-Hennig, U. Dittmer, H. Wolf, and R. Wagner. 1999. Accelerated clearance of SHIV in rhesus monkeys by virus-like particle vaccines is dependent on induction of neutralizing antibodies. Vaccine 18: 291-301.
51. Oliva, A., A. L. Kinter, M. Vaccarezza, A. Rubbert, A. Catanzaro, S. Moir, J. Monaco, L. Ehler, S. Mizell, R. Jackson, Y. Li, J. W. Romano, and A. S. Fauci. 1998. Natural killer cells from human immunodeficiency virus (HIV)-infected individuals are an important source of CC-chemokines and suppress HIV-1 entry and replication in vitro. J. Clin. Investig. 102:223-231.
52. Olszewska-Pazdrak, B., A. Casola, T. Saito, R. Alam, S. E. Crowe, F. Mei, P. L. Ogra, and R. P. Garofalo. 1998. Cell-specific expression of RANTES, MCP-1, and MIP-1α by lower airway epithelial cells and eosinophils infected with respiratory syncytial virus. J. Virol. 72:4756-4764.
53. + cytotoxic T cells after administration of a virus-like particle vaccine in rhesus macaques. AIDS Res. Hum. Retroviruses 16:273-282.
54. Porgador, A., H. F. Staats, B. Faiola, E. Gilboa, and T. J. Palker. 1997. Intranasal immunization with CTL epitope peptides from HIV-1 or ovalbumin and the mucosal adjuvant cholera toxin induces peptide-specific CTLs and protection against tumor development in vivo. J. Immunol. 158:834-841.
55. Roman, M., E. Martin-Orozco, J. S. Goodman, M. D. Nguyen, Y. Sato, A. Ronaghy, R. S. Kornbluth, D. D. Richman, D. A. Carson, and E. Raz. 1997. Immunostimulatory DNA sequences function as T helper-1-promoting adjuvants. Nat. Med. 3:849-854.
56. Rudzik, O., R. L. Clancy, D. Y. Perey, J. Bienenstock, and D. P. Singal. 1975. The distribution of a rabbit thymic antigen and membrane immunoglobulins in lymphoid tissue, with special reference to mucosal lymphocytes. J. Immunol. 114:1-4.
57. Saito, T., R. W. Deskin, A. Casola, H. Haeberle, B. Olszewska, P. B. Ernst, R. Alam, P. L. Ogra, and R. Garofalo. 1997. Respiratory syncytial virus induces selective production of the chemokine RANTES by upper airway epithelial cells. J. Infect. Dis. 175:497-504.
58. Schall, T. J., K. Bacon, K. J. Toy, and D. V. Goeddel. 1990. Selective attraction of monocytes and T lymphocytes of the memory phenotype by cytokine RANTES. Nature 347:669-671.
59. Shi, Y. F., B. M. Sahai, and D. R. Green. 1989. Cyclosporin A inhibits activation-induced cell death in T-cell hybridomas and thymocytes. Nature 339:625-626.
60. Simmons, C. P., P. Mastroeni, R. Fowler, M. Ghaem-Maghami, N. Lycke, M. Pizza, R. Rappuoli, and G. Dougan. 1999. MHC class I-restricted cytotoxic lymphocyte responses induced by enterotoxin-based mucosal adjuvants. J. Immunol. 163:6502-6510.
61. Sparwasser, T., E. S. Koch, R. M. Vabulas, K. Heeg, G. B. Lipford, J. W. Ellwart, and H. Wagner. 1998. Bacterial DNA and immunostimulatory CpG oligonucleotides trigger maturation and activation of murine dendritic cells. Eur. J. Immunol. 28:2045-2054.
62. Spit, B. J., E. G. Hendriksen, J. P. Bruijntjes, and C. F. Kuper. 1989. Nasal lymphoid tissue in the rat. Cell Tissue Res. 255:193-198.
63. Stacey, K. J., D. P. Sester, M. J. Sweet, and D. A. Hume. 2000. Macrophage activation by immunostimulatory DNA. Curr. Top. Microbiol. Immunol. 247:41-58.
64. Taub, D. D., J. R. Ortaldo, S. M. Turcovski-Corrales, M. L. Key, D. L. Longo, and W. J. Murphy. 1996. Beta chemokines costimulate lymphocyte cytolysis, proliferation, and lymphokine production. J. Leukoc. Biol. 59:81-89.
65. Tilney, N. L. 1971. Patterns of lymphatic drainage in the adult laboratory rat. J. Anat. 109:369-383.
66. Tochikubo, K., M. Isaka, Y. Yasuda, S. Kozuka, K. Matano, Y. Miura, and T. Taniguchi. 1998. Recombinant cholera toxin B subunit acts as an adjuvant for the mucosal and systemic responses of mice to mucosally co-administered bovine serum albumin. Vaccine 16:150-155.
67. van der Ven, I., and T. Sminia. 1993. The development and structure of mouse nasal-associated lymphoid tissue: an immuno- and enzyme-histochemical study. Reg. Immunol. 5:69-75.
68. Vzorov, A. N., and R. W. Compans. 1996. Assembly and release of SIV env proteins with full-length or truncated cytoplasmic domains. Virology 221: 22-33.
69. Wagner, R., V. J. Teeuwsen, L. Deml, F. Notka, A. G. Haaksma, S. S. Jhagjhoorsingh, H. Niphuis, H. Wolf, and J. L. Heeney. 1998. Cytotoxic T cells and neutralizing antibodies induced in rhesus monkeys by virus-like particle HIV vaccines in the absence of protection from SHIV infection. Virology 245:65-74.
70. Wu, H. Y., H. H. Nguyen, and M. W. Russell. 1997. Nasal lymphoid tissue (NALT) as a mucosal immune inductive site. Scand. J. Immunol. 46:506-513.
71. Xu-Amano, J., R. J. Jackson, K. Fujihashi, H. Kiyono, H. F. Staats, and J. R. McGhee. 1994. Helper Th1 and Th2 cell responses following mucosal or systemic immunization with cholera toxin. Vaccine 12:903-911.
72. Xu-Amano, J., H. Kiyono, R. J. Jackson, H. F. Staats, K. Fujihashi, P. D. Burrows, C. O. Elson, S. Pillai, and J. R. McGhee. 1993. Helper T cell subsets for immunoglobulin A responses: oral immunization with tetanus toxoid and cholera toxin as adjuvant selectively induces Th2 cells in mucosa associated tissues. J. Exp. Med. 178:1309-1320.
73. Yamshchikov, G. V., G. D. Ritter, M. Vey, and R. W. Compans. 1995. Assembly of SIV virus-like particles containing envelope proteins using a baculovirus expression system. Virology 214:50-58.
74. Yang, S. K., L. Eckmann, A. Panja, and M. F. Kagnoff. 1997. Differential and regulated expression of C-X-C, C-C, and C-chemokines by human colon epithelial cells. Gastroenterology 113:1214-1223.
75. Yao, Q., F. M. Kuhlmann, R. Eller, R. W. Compans, and C. Chen. 2000. Production and characterization of simian-human immunodeficiency virus-like particles. AIDS Res. Hum. Retroviruses 16:227-236.
76. Yao, Q., V. Vuong, M. Li, and R. W. Compans. 2002. Intranasal immunization with SIV virus-like particles (VLPs) elicits systemic and mucosal immunity. Vaccine 20:2537-2545.
77. + cytotoxic T lymphocytes in rhesus monkeys. J. Immunol. 151:5096-5105.