Vaccine-induced protection against Helicobacter pylori in mice lacking both antibodies and interleukin-4

Infection and Immunity

Volumn 71, Issue 6, 2003, Pages 3628-3633

  Garhart, Christine A ^a   Nedrud, John G ^a   Heinzel, Frederick P ^b,c   Sigmund, Norma E ^a   Czinn, Steven J ^a,b  

^a CASE WESTERN RESERVE UNIVERSITY   (United States)

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c LOUIS STOKES CLEVELAND VA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; INTERLEUKIN 4; INTERLEUKIN 5;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE; CONTROLLED STUDY; HELICOBACTER INFECTION; HELICOBACTER PYLORI; HUMORAL IMMUNITY; IMMUNIZATION; KNOCKOUT MOUSE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTECTION; TH2 CELL; VACCINATION;

ANIMALS; ANTIBODIES, BACTERIAL; BACTERIAL VACCINES; GASTRITIS; HELICOBACTER PYLORI; IMMUNIZATION; INTERLEUKIN-4; INTERLEUKIN-5; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PHENOTYPE; TH2 CELLS;

EID: 0038443031     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.71.6.3628-3633.2003     Document Type: Article

References (49)

1. Aebischer, T., S. Laforsch, R. Hurwitz, F. Brombacher, and T. F. Meyer. 2001. Immunity against Helicobacter pylori: significance of interleukin-4 receptor α chain status and gender of infected mice. Infect. Immun. 69:556-558.
2. Akhiani, A. A., J. Pappo, Z. Kabok, K. Schon, W. Gao, L. E. Franzen, and N. Lycke. 2002. Protection against Helicobacter pylori infection following immunization is IL-12-dependent and mediated by Th1 cells. J. Immunol. 169:6977-6984.
3. Bamford, K. B., X. Fan, S. E. Crowe, J. F. Leary, W. K. Gourley, G. K. Luthra, E. G. Brooks, D. Y. Graham, V. E. Reyes, and P. B. Ernst. 1998. Lymphocytes in the human gastric mucosa during Helicobacter pylori have a T helper cell 1 phenotype. Gastroenterology 114:482-492.
4. Beckmann, M. P., K. A. Schooley, B. Gallis, T. Vanden Bos, D. Friend, A. R. Alpert, R. Raunio, K. S. Prickett, P. E. Baker, and L. S. Park. 1990. Monoclonal antibodies block murine IL-4 receptor function. J. Immunol. 144:4212-4217.
5. Blanchard, T. G., S. J. Czinn, R. W. Redline, N. Sigmund, G. Harriman, and J. G. Nedrud. 1999. Antibody-independent protective mucosal immunity to gastric Helicobacter infection in mice. Cell. Immunol. 191:74-80.
6. Blaser, M. J. 1990. Helicobacter pylori and the pathogenesis of gastroduodenal inflammation. J. Infect. Dis. 161:626-633.
7. Burstein, H. J., and A. K. Abbas. 1993. In vivo role of interleukin 4 in T cell tolerance induced by aqueous protein antigen. J. Exp. Med. 177:457-463.
8. Chen, W., D. Shu, and V. S. Chadwick. 1999. Helicobacter pylori infection in interleukin-4-deficient and transgenic mice. Scand. J. Gastroenterol. 34:987-992.
9. Clarke, C. J., A. D. Wilson, N. A. Williams, and C. R. Stokes. 1991. Mucosal priming of T-lymphocyte responses to fed protein antigens using cholera toxin as an adjuvant. Immunology 72:323-328.
10. Del Giudice, G., A. Covacci, J. L. Telford, C. Montecucco, and R. Rappuoli. 2001. The design of vaccines against Helicobacter pylori and their development. Annu. Rev. Immunol. 19:523-563.
11. D'Elios, M. M., M. Manghetti, M. De Carli, F. Costa, C. T. Baldari, D. Burroni, J. L. Telford, S. Romagnani, and G. Del Prete. 1997. T helper 1 effector cells specific for Helicobacter pylori in the gastric antrum of patients with peptic ulcer disease. J. Immunol. 158:962-967.
12. Ermak, T. H., P. J. Giannasca, R. Nichols, G. A. Myers, J. Nedrud, R. Weltzin, C. K. Lee, H. Kleanthous, and T. P. Monath. 1998. Immunization of mice with urease vaccine affords protection against Helicobacter pylori infection in the absence of antibodies and is mediated by MHC class II-restricted responses. J. Exp. Med, 188:2277-2288.
13. Ernst, P. B., and B. D. Gold. 2000. The disease spectrum of Helicobacter pylori: the immunopathogenesis of gastroduodenal ulcer and gastric cancer. Annu. Rev. Microbiol. 54:615-640.
14. Garhart, C. A. 2002. Ph.D. thesis. Case Western Reserve University, Cleveland, Ohio.
15. Garhart, C. A., F. P. Heinzel, S. J. Czinn, and J. G. Nedrud. 2003. Vaccine-induced reduction of Helicobacter pylori colonization in mice is interleukin-12 dependent, but gamma interferon and inducible nitric oxide synthase independent. Infect. Immun. 71:910-921.
16. Garhart, C. A., R. W. Redline, J. G. Nedrud, and S. J. Czinn. 2002. Clearance of Helicobacter pylori infection and resolution of postimmunization gastritis in a kinetic study of prophylactically immunized mice. Infect. Immun. 70:3529-3538.
17. Gottwein, J. M., T. G. Blanchard, O. S. Targoni, J. C. Eisenberg, B. M. Zagorski, R. W. Redline, J. G. Nedrud, M. Tary-Lehmann, P. V. Lehmann, and S. J. Czinn. 2001. Protective anti-Helicobacter immunity is induced with aluminum hydroxide or complete Freund's adjuvant by systemic immunization. J. Infect. Dis. 184:308-314.
18. Guy, B., C. Hessler, S. Fourage, J. Haensler, E. Vialon-Lafay, B. Rokbi, and M.-J. Q. Millet. 1998. Systemic immunization with urease protects mice against Helicobacterpylori infection. Vaccine 16:850-856.
19. Guy, B., C. Hessler, S. Fourage, B. Rokbi, and M.-J. Q. Millet. 1999. Comparison between targeted and untargeted systemic immunizations with adjuvanted urease to cure Helicobacter pylori infection in mice. Vaccine 17:1130-1135.
20. Heinzel, F., M. Sadick, B. Holaday, R. Coffman, and R. Locksley. 1989. Reciprocal expression of interferon γ or interleukin 4 during the resolution or progression of murine leishmaniasis. J. Exp. Med. 169:59-72.
21. Heinzel, F. P., R. M. Rerko, F. Ahmed, and E. Pearlman. 1995. Endogenous IL-12 is required for control of Th2 cytokine responses capable of exacerbating leishmaniasis in normally resistant mice. J. Immunol. 155:730-739.
22. Hornquist, E., and N. Lycke. 1993. Cholera toxin adjuvant greatly promotes antigen priming of T cells. Eur. J. Immunol. 23:2136-2143.
23. Ibraghimov, A., and J. Pappo. 2000. The immune response against Helicobacter pylori - a direct linkage to the development of gastroduodenal disease. Microbes Infect. 2:1073-1077.
24. Kamradt, A. E., M. Greiner, P. Ghiara, and S. H. Kaufmann. 2000. Helicobacter pylori infection in wild-type and cytokine-deficient C57BL/6 and BALB/c mouse mutants. Microbes Infect. 2:593-597.
25. Kitamura, D., J. Roes, R. Kühn, and K. Rajewsky. 1991. A B cell-deficient mouse by targeted disruption of the membrane exon of the immunoglobulin μ chain gene. Nature 350:423-426.
26. Kleanthous, H., G. A. Myers, K. M. Georgakopoulos, T. J. Tibbitts, J. W. Ingrassia, H. L. Gray, R. Ding, Z.-Z. Zhang, W. Lei, R. Nichols, C. K. Lee, T. H. Ermak, and T. P. Monath. 1998. Rectal and intranasal immunizations with recombinant urease induce distinct local and serum immune responses in mice and protect against Helicobacter pylori infection. Infect. Immun. 66:2879-2886.
27. Kopf, M., F. Brombacher, P. D. Hodgkin, A. J. Ramsay, E. A. Milbourne, W. J. Dai, K. S. Ovington, C. A. Behm, G. Kohler, I. G. Young, and K. I. Matthaei. 1996. IL-5-deficient mice have a developmental defect in CD5+ B-1 cells and lack eosinophilia but have normal antibody and cytotoxic T cell responses. Immunity 4:15-24.
28. Kopf, M., G. Le Gros, M. Bachmann, M. C. Lamers, H. Bluethmann, and G. Kohler. 1993. Disruption of the murine IL-4 gene blocks Th2 cytokine responses. Nature 362:245-248.
29. Kühn, R., K. Rajewsky, and W. Müller. 1991. Generation and analysis of interleukin-4 deficient mice. Science 254:707-710,
30. Kurono, Y., M. Yamamoto, K. Fujihashi, S. Kodama, M. Suzuki, G. Mogi, J. R. McGhee, and H. Kiyono. 1999. Nasal immunization induces Haemophilus influenzae-specific Th1 and Th2 responses with mucosal IgA and systemic IgG antibodies for protective immunity. J. Infect. Dis. 180:122-132.
31. Lee, A., J. O'Rourke, M. C. De Ungria, B. Robertson, G. Daskalopoulos, and M. F. Dixon. 1997. A standardized mouse model of Helicobacter pylori infection: introducing the Sydney strain. Gastroenterology 112:1386-1397.
32. Lindholm, C., M. Quiding-Jarbrink, H. Lonroth, A. Hamlet, and A.-M. Svennerholm. 1998. Local cytokine response in Helicobacter pylori-infected subjects. Infect. Immun. 66:5964-5971.
33. + T cells specific for subunit A of Helicobacter pylori urease reduces H. pylori stomach colonization in mice in the absence of interleukin-4 (IL-4)/IL-13 receptor signaling. Infect. Immun. 69:1714-1721.
34. Marinaro, M., H. F. Staats, T. Hiroi, R. J. Jackson, M. Coste, P. N. Boyaka, N. Okahashi, M. Yamamoto, H. Kiyono, H. Bluethmann, K. Fujihashi, and J. R. McGheee. 1995. Mucosal adjuvant effect of cholera toxin in mice results from induction of T helper (Th2) cells and IL-4. J. Immunol. 155:4621-4629.
35. Mohammadi, M., S. Czinn, R. Redline, and J. Nedrud. 1996. Helicobacter-specific cell-mediated immune responses display a predominant TH1 phenotype and promote a DTH response in the stomachs of mice. J. Immunol. 156:4729-4738.
36. Mohammadi, M., J. Nedrud, R. Redline, N. Lycke, and S. Czinn. 1997. Murine CD4 T cell responses to Helicobacter infection: TH1 cells enhance gastritis and TH2 cells reduce bacterial load. Gastroenterology 113:1848-1857.
37. Mohammadi, M., R. Redline, J. Nedrud, and S. Czinn. 1996. Role of the host in pathogenesis of Helicobacter-associated gastritis: H. felis infection of inbred and congenic mouse strains. Infect. Immun. 64:238-245.
38. + Th2 cells producing IL-6 and IL-10 are associated with mucosal immunoglobulin A responses. Infect. Immun. 64:1516-1525.
39. Parsonnet, J., G. D. Friedman, D. P. Vandersteen, Y. Chang, J. H. Vogelman, N. Orentreich, and R. K. Sibley. 1991. Helicobacter pylori infection and the risk of gastric carcinoma. N. Engl. J. Med. 325:1127-1131.
40. Radcliff, F. J., S. L. Hazell, T. Kolesnikow, C. Doidge, and A. Lee. 1997. Catalase, a novel antigen for Helicobacterpylori vaccination. Infect. Immun. 65:4668-4674.
41. Rizzo, L. V., R. A. Morawetz, N. E. Miller-Rivero, R. Choi, B. Wiggert, C. C. Chan, H. C. Morse III, R. B. Nussenblatt, and R. R. Caspi. 1999. IL-4 and IL-10 are both required for the induction of oral tolerance. J. Immunol. 162:2613-2622.
42. Sakagami, T., M. Dixon, J. O'Rourke, R. Howlett, F. Alderuccio, J. Vella, T. Shimoyama, and A. Lee. 1996. Atrophic gastric changes in both H. felis and H. pylori infected mice are host dependent and separate from antral gastritis. Gut 39:639-648.
43. Saldinger, P., N. Porta, P. Launois, J. Louis, G. Waanders, H. Bouzourene, P. Michetti, A. Blum, and I. Corthesy-Theulaz. 1998. Immunization of BALB/c mice with Helicobacter urease B induces a T helper 2 response absent in Helicobacter infection. Gastroenterology 115:891-897.
44. Smythies, L. E., K. B. Waites, J. R. Lindsey, P. R. Harris, P. Ghiara, and P. D. Smith. 2000. Helicobacter pylori-induced mucosal inflammation is Th1 mediated and exacerbated in IL-4, but not IFN-gamma, gene-deficient mice. J. Immunol. 165:1022-1029.
45. Sutton, P., J. Wilson, T. Kosaka, I. Wolowczuk, and A. Lee. 2000. Therapeutic immunization against Helicobacter pylori infection in the absence of antibodies. Immunol. Cell Biol. 78:28-30.
46. Vajdy, M., M. H. Kosco-Vilbois, M. Kopf, G. Kohler, and N. Lycke. 1995. Impaired mucosal immune responses in interleukin 4-targeted mice. J. Exp. Med. 181:41-53.
47. Warren, J. R. 1983. Unidentified curved bacilli on gastric epithelium in active chronic gastritis. Lancet i:1273.
48. 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.
49. Yamaoka, Y., M. Kita, T. Kodama, N. Sawai, and J. Imanishi. 1996. Helicobacter pylori caga gene and expression of cytokine messenger RNA in gastric mucosa. Gastroenterology 110:1744-1752.