Mucosal and Systemic Immune Responses to a Human Immunodeficiency Virus Type 1 Epitope Induced upon Vaginal Infection with a Recombinant Influenza A Virus

Journal of Virology

Volumn 78, Issue 2, 2004, Pages 1020-1025

  Garulli, Bruno ^a,e   Kawaoka, Yoshihiro ^b,c,d   Castrucci, Maria R ^a  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

^c UNIVERSITY OF TOKYO   (Japan)

^d JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^e SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ENVELOPE PROTEIN; EPITOPE; GLYCOPROTEIN GP 160; PROGESTERONE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN SPECIFICITY; ARTICLE; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; FEMALE; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMORAL IMMUNITY; IMMUNE RESPONSE; IMMUNIZATION; IMMUNOLOGICAL MEMORY; INFLUENZA VIRUS A; LYMPH NODE; MOUSE; MUCOSAL IMMUNITY; NONHUMAN; PRIORITY JOURNAL; SEXUALLY TRANSMITTED DISEASE; SPLEEN; VACCINIA VIRUS; VAGINITIS; VIRUS RECOMBINANT;

AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES, VIRAL; EPITOPES; FEMALE; HIV ENVELOPE PROTEIN GP160; HIV-1; HUMANS; IMMUNOLOGIC MEMORY; INFLUENZA A VIRUS; INFLUENZA VACCINES; LYMPH NODES; MICE; MICE, INBRED BALB C; MOLECULAR SEQUENCE DATA; SPLEEN; T-LYMPHOCYTES, CYTOTOXIC; VACCINES, SYNTHETIC; VAGINA;

EID: 0347949562     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.78.2.1020-1025.2004     Document Type: Article

References (54)

1. Barnett, S. W., J. M. Klinger, B. Doe, C. M. Walker, L. Hansen, A. M. Duliege, and F. M. Sinangil. 1998. Prime-boost immunization strategies against HIV. AIDS Res. Hum. Retrovir. 14(Suppl. 3):299-309.
2. Belyakov, I. M., M. A. Derby, J. D. Ahlers, B. L. Kelsall, P. Earl, B. Moss, W. Strober, and J. A. Berzofsky. 1998. Mucosal immunization with HIV-1 peptide vaccine induces mucosal and systemic cytotoxic T lymphocytes and protective immunity in mice against intrarectal recombinant HIV-vaccinia challenge. Proc. Natl. Acad. Sci. USA 95:1709-1714.
3. Belyakov, I. M., L. S. Wyatt, J. D. Ahlers, P. Earl, C. D. Pendleton, B. L. Kelsall, W. Strober, B. Moss, and J. A. Berzofsky. 1998. Induction of mucosal cytotoxic T-lymphocyte response by intrarectal immunization with a replication-deficient recombinant vaccinia virus expressing human immunodeficiency virus 89.6 envelope protein. J. Virol. 72:8264-8272.
4. Belyakov, I. M., J. D. Ahlers, J. D. Clements, W. Strober, and J. A. Berzofsky. 2000. Interplay of cytokines and adjuvants in the regulation of mucosal and systemic HIV-specific CTL. J. Immunol. 165:6454-6462.
5. Belyakov, I. M., Z. Hel, B. Kelsall, V. A. Kuznetsov, J. D. Ahlers, J. Nacsa, D. I. Watkins, T. M. Allen, A. Sette, J. Altman, R. Woodward, P. D. Markham, J. D. Clements, G. Franchini, W. Strober, and J. A. Berzofsky. 2001. Mucosal AIDS vaccine reduces disease and viral load in gut reservoir and blood after mucosal infection of macaques. Nat. Med. 7:1320-1326.
6. Bhardwaj, N., A. Bender, N. Gonzales, L. K. Bui, M. C. Garrett, and R. M. Steinman. 1994. Influenza virus-infected dendritic cells stimulate strong proliferative and cytolytic responses from human CD8+ T cells. J. Clin. Investig. 94:797-807.
7. Bienestock, J., A. D. Defus, M. McDermott. S. Mirski, K. Rosenthal, and A. Tagliabue. 1992. The mucosal immunologic network: compartmentalization of lymphocytes, natural killer cells and mast cells. Ann. N. Y. Acad. Sci. 409:164-170.
8. Bodmer, H. C., R. M. Pemberton, J. B. Rothbard, and B. A. Askonas. 1988. Enhanced recognition of a modified peptide antigen by cytotoxic T cells specific for influenza nucleoprotein. Cell 512:253-258.
9. Bomsel, M., M. Heyman, H. Hocini, S. Lagaye, L. Belec, C. Dupont, and C. Desgranges. 1998. Intracellular neutralization of HIV transcytosis across tight epithelial barriers by anti-HIV envelope protein dIgA or IgM. Immunity 9:277-287.
10. Castrucci, M. R., P. Bilsel, and Y. Kawaoka. 1992. Attenuation of influenza A virus by insertion of a foreign epitope into the neuraminidase. J. Virol. 66:4647-4653.
11. Castrucci, M. R., S. Hou, P. C. Doherty, and Y. Kawaoka. 1994. Protection against lethal lymphocytic choriomeningitis virus (LCMV) infection by immunization of mice with an influenza virus containing an LCMV epitope recognized by cytotoxic T lymphocytes. J. Virol. 68:3486-3490.
12. Cella, M., M. Salio, Y. Sakakibara, H. Langen, I. Julkunen, and A. Lanzavecchia. 1999. Maturation, activation, and protection of dendritic cells induced by double-stranded RNA. J. Exp. Med. 189:821-829.
13. Devito, C., K. Broliden, R. Kaul, L. Svensson, K. Johansen, P. Kiama, J. Kimani, L. Lopalco, S. Piconi, J. J. Bwayo, F. Plummer, M. Clerici, and J. Hinkula. 2000. Mucosal and plasma IgA from HIV-1-exposed uninfected individuals inhibit HIV-1 transcytosis across human epithelial cells. J. Immunol. 165:5170-5176.
14. Earl, P. L., S. Koenig, and B. Moss. 1991. Biological and immunological properties of human immunodeficiency virus type 1 envelope glycoprotein: analysis of proteins with truncations and deletions expressed by recombinant vaccinia viruses. J. Virol. 65:31-41.
15. Enami, M., W. Luytjes, M. Krystal, and P. Palese. 1990. Introduction of site-specific mutations into the genome of influenza virus. Proc. Natl. Acad. Sci. USA 87:3802-3805.
16. Eo, S. K., M. Gierynska, A. A. Kamar, and B. T. Rouse. 2001. Prime-boost immunization with DNA vaccine: mucosal route of administration changes the rules. J. Immunol. 166:5473-5479.
17. Ferko, B., J. Stasakova, S. Sereinig, J. Romanova, D. Katinger, B. Niebler, H. Katinger, and A. Egorov. 2001. Hyperattenuated recombinant influenza A virus nonstructural-protein-encoding vectors induce human immunodeficiency virus type 1 Nef-specific systemic and mucosal immune responses in mice. J. Virol. 75:8899-8908.
18. Gallichan, W. S., and K. L. Rosenthal. 1996. Long-lived cytotoxic T lymphocyte memory in mucosal tissues after mucosal but not systemic immunization. J. Exp. Med. 184:1879-1890.
19. Gallichan, W. S., and K. L. Rosenthal. 1998. Long-term immunity and protection against herpes simplex virus type 2 in the murine female genital tract after mucosal but not systemic immunization. J. Infect. Dis. 177:1155-1161.
20. Gallichan, W. S., R. N. Woolstenencroft, 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.
21. Gherardi, M. M., J. L. Najera, E. Perez-Jimenez, S. Guerra, A. Garcia-Sastre, and M. Esteban. 2003. Prime-boost immunization schedules based on influenza virus and vaccinia virus vectors potentiate cellular immune responses against human immunodeficiency virus Env protein systemically and in the genitorectal draining lymph nodes. J. Virol. 77:7048-7057.
22. Gonzalo, R. M., D. Rodriguez, A. Garcia-Sastre, J. R. Rodriguez, P. Palese, and M. Esteban. 1999. Enhanced CD8+ T cell response to HIV-1 Env by combined immunization with influenza and vaccinia virus recombinants. Vaccine 17:887-892.
23. Haglund, K., I. Leiner, K. Kerksiek, L. Buonocore, E. Pamer, and J. K. Rose. 2002. Robust recall and long-term memory T-cell responses induced by prime-boost regimens with heterologous live viral vectors expressing human immunodeficiency virus type 1 Gag and Env proteins. J. Virol. 76:7506-7517.
24. Hamajima, K., Y. Hoshino, K. Q. Xin, F. Hayashi, K. Tadokoro, and K. Okuda. 2002. Systemic and mucosal immune responses in mice after rectal and vaginal immunization with HIV-DNA vaccine. Clin. Immunol. 102:12-18.
25. Heeney, J. L., G. Koopman, B. Rosenwirth, W. Bogers, J. Van Dijk, I. Nieuwenhuis, H. Niphuis, P. ten Haaft, T. Hanke, G. Rhodes, P. Berglund, A. Burny, F. Bex, G. Sutter, and P. Liljestrom. 2000. A vaccine strategy utilizing a combination of three different chimeric vectors which share specific vaccine antigens. J. Med. Primatol. 29:268-273.
26. Kiyono, H., C. J. Miller, Y. Lu, T. Lehner, M. Cranage, Y. T. Huang, S. Kawabata, M. Marthas, B. Roberts, J. G. Nedrud, M. E. Lamm, L. Bergmeier, R. Brooks, L. Tao, and J. R. McGhee. 1995. The common mucosal immune system for the reproductive tract: basic principles applied toward an AIDS vaccine. Adv. Drug Deliv. Rev. 18:23-51.
27. Klavinskis, L. S., C. Barnfield, L. Gao, and S. Parker. 1999. Intranasal immunization with plasmid DNA-lipid complexes elicits mucosal immunity in the female genital and rectal tracts. J. Immunol. 162:254-262.
28. Kozlowski, P. A., S. Cu-Uvin, M. R. Neutra, and T. P. Flanigan. 1997. Comparison of the oral, rectal, and vaginal immunization routes for induction of antibodies in rectal and genital tract secretions. Infect. Immun. 65:1387-1394.
29. Lehner, T., Y. Wang, M. Cranage, L. A. Bergmeier, E. Mitchell, L. Tao, G. Hall, M. Dennis, N. Cook, R. Brookes, L. Klavinskis, I. Jones, C. Doyle, and R. Wards. 1996. Protective mucosal immunity elicited by targeted iliac lymph node immunization with a subunit SIV envelope and core vaccine in macaques. Nat. Med. 2:767-775.
30. Lehner, T., L. Bergmeier, Y. Wang, L. Tao, and E. Mitchell. 1999. A rational basis for mucosal vaccination against HIV infection. Immunol. Rev. 170: 183-196.
31. Li, S., V. Polonis, H. Isobe, H. Zaghouani, R. Guinea, T. Moran, C. Bona, and P. Palese. 1993. Chimeric influenza virus induces neutralizing antibodies and cytotoxic T cells against human immunodeficiency virus type 1. J. Virol. 67:6659-6666.
32. Li, S., M. Rodrigues, D. Rodriguez, J. R. Rodriguez, M. Esteban, P. Palese, R. S. Nussenzweig, and F. Zavala. 1993. Priming with recombinant influenza virus followed by administration of recombinant vaccinia virus induces CD8+ T-cell-mediated protective immunity against malaria. Proc. Natl. Acad. Sci. USA 90:5214-5218.
33. Marx, P. A., A. I. Spira, A. Gettie, P. J. Dailey, R. S. Veazey, A. A. Lackner, C. J. Mahoney, C. J. Miller, L. E. Claypool, D. D. Ho, and N. J. Alexander. 1996. Progesterone implants enhance SIV vaginal transmission and early virus load. Nat. Med. 2:1084-1089.
34. McDermott, M. R., and J. Bienenstock. 1979. Evidence for a common mucosal immunologic system. I. Migration of B immunoblasts into intestinal, respiratory and genital tissues. J. Immunol. 122:1892-1898.
35. Menge, A. C., S. M. Michalek, M. W. Russell, and J. Mestecky. 1993. Immune response of the female rat genital tract after oral and local immunization with keyhole limpet hemocyanin conjugated to the cholera toxin B subunit. Infect. Immun. 61:2162-2171.
36. Mitchell, E. A., L. A. Bergmeier, C. Doyle, R. Brooks, L. A. Hussain, Wang, Y., and T. Lehner. 1998. Homing of mononuclear cells from iliac lymph nodes to the genital and rectal mucosa in non-human primates. Eur. J. Immunol. 28:3066-3074.
37. Murali-Krishna, K., J. D. Altman, M. Suresh, D. Sourdive, A. Zajac, J. Miller, J. Slansky, and R. Ahmed. 1998. Counting antigen-specific CD8 T cells: a reevaluation of bystander activation during viral infection. Immunity 8:177-187.
38. Murata, K., A. Garcia-Sastre, M. Tsuji, M. Rodrigues, D. Rodriguez, J. R. Rodriguez, R. S. Nussenzweig, P. Palese, M. Esteban, and F. Zavala. 1996. Characterization of in vivo primary and secondary CD8+ T cell responses induced by recombinant influenza and vaccinia virus. Cell. Immunol. 173: 96-107.
39. Murphy, B. R., and M. L. Clements. 1989. The systemic and mucosal immune response of humans to influenza A virus. Curr. Top. Microbiol. Immunol. 146:107-116.
40. Muster, T., B. Ferko, A. Klima, M. Purtscher, A. Trkola, P. Schulz, A. Grassauer, O. G. Engelhardt, A. Garcia-Sastre, P. Palese, and H. Katinger. 1995. Mucosal model of immunization against human immunodeficiency virus type 1 with a chimeric influenza virus. J. Virol. 69: 6678-6686.
41. Nakaya, Y., H. Zheng, and A. Garcia-Sastre. 2003. Enhanced cellular immune responses to SIV Gag by immunization with influenza and vaccinia virus recombinants. Vaccine 21:2097-2106.
42. Parr, E. L., J. J. Bozzola, and M. B. Parr. 1998. Immunity to vaginal infection by herpes simplex virus type 2 in adult mice: characterization of the immunoglobulins in vaginal mucus. J. Reprod. Immunol. 38:15-30.
43. Parr, M. B., L. Kepple, M. R. McDermott, M. D. Drew, J. J. Bozzola, and E. L. Parr. 1994. A mouse model for studies of mucosal immunity to vaginal infection by herpes simplex virus type 2. Lab. Investig. 70:369-379.
44. Rayevskaya, M. V., and F. R. Frankel. 2001. Systemic immunity and mucosal immunity are induced against human immunodeficiency virus Gag protein in mice by a new hyperattenuated strain of Listeria monocytogenes. J. Virol. 75:2786-2791.
45. Shirai, M., C. D. Pendleton, and J. A. Berzofsky. 1992. Broad recognition of cytotoxic T cell epitopes from the HIV-1 envelope protein with multiple class I histocompatibility molecules. J. Immunol. 148:1657-1667.
46. Staats, H. F., R. J. Jackson, M. Marinaro, I. Takahashi, H. Kiyono, and J. R. McGhee. 1994. Mucosal immunity to infection with implications for vaccine development. Curr. Opin. Immunol. 6:572-583.
47. Staczek, J., H. E. Gilleland, Jr., L. B. Gilleland, N. Harty, A. Garcia-Sastre, O. G. Engelhardt, and P. Palese. 1998. A chimeric influenza virus expressing an epitope of outer membrane protein F of Pseudomonas aeruginosa affords protection against challenge with P. aeruginosa in a murine model of chronic pulmonary infection. Infect. Immun. 66:3990-3994.
48. Topham, D. J., M. R. Castrucci, F. S. Wingo, G. T. Belz, and P. C. Doherty. 2001. The role of antigen in the localization of naive, acutely activated, and memory CD8+ T cells to the lung during influenza pneumonia. J. Immunol. 167:6983-6990.
49. Tuffrey, M., and D. Taylor-Robinson. 1981. Progesterone as a key factor in the development of a mouse model for genital tract infection with Chlamydia trachomatis. FEMS Microbiol. Lett. 12:111-115.
50. Vajdy, M., J. Gardner, J. Neidleman, L. Cuadra, C. Greer, S. Perri, D. O'Hagan, and J. M. Polo. 2001. Human immunodeficiency virus type 1 Gag-specific vaginal immunity and protection after local immunizations with Sindbis virus-based replicon particles. J. Infect. Dis. 184:1613-1616.
51. Wassen, L., K. Schon, J. Holmgren, M. Jertborn, and N. Lycke. 1996. Local intravaginal vaccination of the female genital tract. Scand. J. Immunol. 44:408-414.
52. Webster, R. G., L. E. Brown, and D. C. Jackson. 1983. Change in antigenicity of the hemagglutinin molecule of H3 influenza virus at acidic pH. Virology 126:587-599.
53. Wu, H. Y., S. Abdu, D. Stinson, and M. W. Russell. 2000. Generation of female genital tract antibody responses by local and central (common) mucosal immunization. Infect. Immun. 68:5539-5545.
54. Zdenek, H., W. P. Tsai, A. Thornton, J. Nacsa, L. Giuliani, E. Tryniszewska, M. Poudyal, D. Venzon, X. Wang, J. Altman, D. I. Watkins, W. Lu, A. von Gegerfelt, B. K. Felber, J. Tartaglia, G. N. Pavlakis, and G. Franchini. 2001. Potentiation of simian immunodeficiency virus (SIV)-specific CD4+ and CD8+ T cell responses by a DNA-SIV and NYVAC-SIV prime/boost regimen. J. Immunol. 167:7180-7191.