Natural killer cells and Helicobacter pylori infection: Bacterial antigens and interleukin-12 act synergistically to induce gamma interferon production

Infection and Immunity

Volumn 73, Issue 3, 2005, Pages 1482-1490

  Yun, Cheol H ^a,b   Lundgren, Anna ^a   Azem, Josef ^a   Sjöling, Åsa ^a   Holmgren, Jan ^a   Svennerholm, Ann Mari ^a   Lundin, B Samuel ^a  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b International Vaccine Institute   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ANTIGEN; BACTERIUM LYSATE; GAMMA INTERFERON; INTERLEUKIN 12 RECEPTOR BETA2; INTERLEUKIN 12;

ARTICLE; CELL INFILTRATION; CYTOKINE PRODUCTION; CYTOKINE RELEASE; CYTOTOXICITY; DUODENUM MUCOSA; EPITHELIUM CELL; HELICOBACTER INFECTION; HELICOBACTER PYLORI; HUMAN; HUMAN CELL; IMMUNE RESPONSE; LYMPHOCYTE ACTIVATION; NATURAL KILLER CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; STOMACH MUCOSA; T LYMPHOCYTE; ADULT; BIOSYNTHESIS; CYTOLOGY; DRUG POTENTIATION; IMMUNOLOGY; INTESTINE MUCOSA; MICROBIOLOGY; MIDDLE AGED; PATHOGENICITY;

ADULT; ANTIGENS, BACTERIAL; DRUG SYNERGISM; GASTRIC MUCOSA; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; HUMANS; INTERFERON TYPE II; INTERLEUKIN-12; INTESTINAL MUCOSA; KILLER CELLS, NATURAL; LYMPHOCYTE ACTIVATION; MIDDLE AGED;

EID: 15544378838     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.73.3.1482-1490.2005     Document Type: Article

References (55)

1. 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.
2. + T cells. J. Immunol. 169:3232-3241.
3. Bauditz, J., M. Ortner, M. Bierbaum, G. Niedobitek, H. Lochs, and S. Schreiber. 1999. Production of IL-12 in gastritis relates to infection with Helicobacter pylori. Clin. Exp. Immunol. 117:316-323.
4. Bauer, S., V. Groh, J. Wu, A. Steinle, J. H. Phillips, L. L. Lanier, and T. Spies. 1999. Activation of NK cells and T cells by NKG2D, a receptor for stress-inducible MICA. Science 285:727-729.
5. Blaser, M. J. 1999. Hypothesis: the changing relationships of Helicobacter pylori and humans: implications for health and disease. J. Infect. Dis. 179:1523-1530.
6. Boehm, U., T. Klamp, M. Groot, and J. C. Howard. 1997. Cellular responses to interferon-gamma. Annu. Rev. Immunol. 15:749-795.
7. Bream, J. H., R. E. Curiel, C. R. Yu, C. E. Egwuagu, M. J. Grusby, T. M. Aune, and H. A. Young. 2003. IL-4 synergistically enhances both IL-2- and IL-12-induced IFN-gamma expression in murine NK cells. Blood 102:207-214.
8. bright natural killer cell subsets: characterization of distinct functional responses to interleukin-2 and the c-kit ligand. Eur. J. Immunol. 27:354-360.
9. Cerwenka, A., and L. L. Lanier. 2001. Natural killer cells, viruses and cancer. Nat. Rev. Immunol. 1:41-49.
10. Chakir, H., A. A. Camilucci, L. G. Filion, and J. R. Webb. 2000. Differentiation of murine NK cells into distinct subsets based on variable expression of the IL-12R beta 2 subunit. J. Immunol. 165:4985-4993.
11. Cooper, M. A., T. A. Fehniger, and M. A. Caligiuri. 2001. The biology of human natural killer-cell subsets. Trends Immunol. 22:633-640.
12. bright subset. Blood 97:3146-3151.
13. DeBlaker-Hohe, D. F., A. Yamauchi, C. R. Yu, J. A. Horvath-Arcidiacono, and E. T. Bloom. 1995. IL-12 synergizes with IL-2 to induce lymphokine-activated cytotoxicity and perforin and granzyme gene expression in fresh human NK cells. Cell Immunol. 165:33-43.
14. Eckenberg, R., J. L. Moreau, O. Melnyk, and J. Theze. 2000. IL-2R beta agonist P1-30 acts in synergy with IL-2, IL-4, IL-9, and IL-15: biological and molecular effects. J. Immunol. 165:4312-4318.
15. 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.
16. Favre-Felix, N., M. Martin, E. Maraskovsky, A. Fromentin, M. Moutet, E. Solary, F. Martin, and B. Bonnette. 2000. Flt3 ligand lessens the growth of tumors obtained after colon cancer cell injection in rats but does not restore tumor-suppressed dendritic cell function. Int. J. Cancer 86:827-834.
17. Fukao, T., S. Matsuda, and S. Koyasu. 2000. Synergistic effects of IL-4 and IL-18 on IL-12-dependent IFN-gamma production by dendritic cells. J. Immunol. 164:64-71.
18. Gherardi, M. M., J. C. Ramirez, and M. Esteban. 2003. 1L-12 and 1L-18 act in synergy to clear vaccinia virus infection: involvement of innate and adaptive components of the immune system. J. Gen. Virol. 84:1961-1972.
19. Gilfillan, S., E. L. Ho, M. Cella, W. M. Yokoyama, and M. Colonna. 2002. NKG2D recruits two distinct adapters to trigger NK cell activation and costimulation. Nat. Immunol. 3:1150-1155.
20. Gobert, A. P., J. C. Bambou, C. Werts, V. Balloy, M. Chignard, A. P. Moran, and R. L. Ferrero. 2004. Heticobacter pylori heat shock protein 60 mediates interleukin-6 production by macrophages via a toll-like receptor (TLR)-2-, TLR-4-, and myeloid differentiation factor 88-independent mechanism. J. Biol. Chem. 279:245-250.
21. Hafsi, N., P. Voland, S. Schwendy, R. Rad, W. Reindl, M. Gerhard, and C. Prinz. 2004. Human dendritic cells respond to Heticobacter pylori, promoting NK cell and Th1-effector responses in vitro. J. Immunol. 173:1249-1257.
22. Hamlet, A. K., K. I. Erlandsson, L. Olbe, A. M. Svennerholm, V. E. Backman, and A. B. Pettersson. 1995. A simple, rapid, and highly reliable capsule-based 14C urea breath test for diagnosis of Helicobacter pylori infection. Scand. J. Gastroenterol. 30:1058-1063.
23. Hayakawa, Y., J. M. Kelly, J. A. Westwood, P. K. Darcy, A. Diefenbach, D. Raulet, and M. J. Smyth. 2002. Cutting edge: tumor rejection mediated by NKG2D receptor-ligand interaction is dependent upon perforin. J. Immunol. 169:5377-5381.
24. Herberman, R. B. 2002. Cancer immunotherapy with natural killer cells. Semin. Oncol. 29:27-30.
25. Hida, N., T. Shimoyama, Jr., P. Neville, M. F. Dixon, A. T. Axon, T. Shimoyama, Sr., and J. E. Crabtree. 1999. Increased expression of IL-10 and IL-12 (p40) mRNA in Helicobacter pylori infected gastric mucosa: relation to bacterial cag status and peptic ulceration. J. Clin. Pathol. 52:658-664.
26. Hornung, V., S. Rothenfusser, S. Britsch, A. Krug, B. Jahrsdorfer, T. Giese, S. Endres, and G. Hartmann. 2002. Quantitative expression of toll-like receptor 1-10 mRNA in cellular subsets of human peripheral blood mononuclear cells and sensitivity to CpG oligodeoxynucleotides. J. Immunol. 168:4531-4537.
27. Inohara, N., and G. Nunez. 2003. NODs: intracellular proteins involved in inflammation and apoptosis. Nat. Rev. Immunol. 3:371-382.
28. bright NK cells. Eur. J. Immunol. 31:3121-3127.
29. Kelly, J. M., P. K. Darcy, J. L. Markby, D. I. Godfrey, K. Takeda, H. Yagita, and M. J. Smyth. 2002. Induction of tumor-specific T cell memory by NK cell-mediated tumor rejection. Nat. Immunol. 3:83-90.
30. Kirby, A. C., U. Yrlid, and M. J. Wick. 2002. The innate immune response differs in primary and secondary Salmonella infection. J. Immunol. 169:4450-4459.
31. + T cells in humans. Infect. Immun. 70:5622-5627.
32. Mandelboim, O., P. Malik, D. M. Davis, C. H. Jo, J. E. Boyson, and J. L. Strominger. 1999. Human CD16 as a lysis receptor mediating direct natural killer cell cytotoxicity. Proc. Natl. Acad. Sci. USA 96:5640-5644.
33. McQueen, K. L., and P. Parham. 2002. Variable receptors controlling activation and inhibition of NK cells. Curr. Opin. Immunol. 14:615-621.
34. + T cell responses. Nat. Immunol. 3:189-195.
35. Muzio, M., D. Bosisio, N. Polentarutti, G. D'Amico, A. Stoppacciaro, R. Mancinelli, C. van't Veer, G. Penton-Rol, L. P. Ruco, P. Allavena, and A. Mantovani. 2000. Differential expression and regulation of toll-like receptors (TLR) in human leukocytes: selective expression of TLR3 in dendritic cells. J. Immunol. 164:5998-6004.
36. Obonyo, M., D. G. Guiney, J. Harwood, J. Fierer, and S. P. Cole. 2002. Role of gamma Interferon in Helicobacter pylori induction of inflammatory mediators during murine infection. Infect. Immun. 70:3295-3299.
37. Ogura, K., S. Maeda, M. Nakao, T. Watanabe, M. Tada, T. Kyutoku, H. Yoshida, Y. Shiratori, and M. Omata. 2000. Virulence factors of Helicobacter pylori responsible for gastric diseases in Mongolian gerbil. J. Exp. Med. 192:1601-1610.
38. Okamoto, M., S. Kato, K. Oizumi, M. Kinoshita, Y. Inoue, K. Hoshino, S. Akira, A. N. McKenzie, H. A. Young, and T. Hoshino. 2002. Interieukin 18 (IL-18) in synergy with IL-2 induces lethal lung injury in mice: a potential role for cytokines, chemokines, and natural killer cells in the pathogenesis of interstitial pneumonia. Blood 99:1289-1298.
39. +dim natural killer cells in patients with chronic myelogenous leukemia progressively decrease in number, respond less to stimuli that recruit elonogenic natural killer cells, and exhibit decreased proliferation on a per cell basis. Blood 88:2279-2287.
40. Raghavan, S., M. Hjulstrom, J. Holmgren, and A. M. Svennerholm. 2002. Protection against experimental Helicobaaer pylori infection after immunization with inactivated H. pylori whole-cell vaccines. Infect. Immun. 70:6383-6388.
41. bright natural killer cells in the human early pregnancy decidua. Int. Immunol. 5:559-563.
42. Semino-Mora, C., S. Q. Doi, A. Marty, V. Simko, I. Carlstedt, and A. Dubois. 2003. Intracellular and interstitial expression of Helicobacter pylori virulence genes in gastric precancerous intestinal metaplasia and adenocarcinoma. J. Infect. Dis. 187:1165-1177.
43. Smith, M. F., Jr., A. Mitchell, G. Li, S. Ding, A. M. Fitzmaurke, K. Ryan, S. Crowe, and J. B. Goldberg. 2003. Toll-like receptor (TLR) 2 and TLR5, but not TLR4, are required for Helicobacter pylori-induced NF-kappa B activation and chemokine expression by epithelial cells. J. Biol. Chem. 278:32552-32560.
44. Smyth, M. J., D. I. Godfrey, and J. A. Trapani. 2001. A fresh look at tumor, immunosurveillance and immunotherapy. Nat. Immunol. 2:293-299.
45. Soloski, M. J. 2001. Recognition of tumor cells by the innate immune system. Curr. Opin. Immunol. 13:154-162.
46. + lymphocytes in Helicobacterpylori gastritis display a Th1 phenotype. Infect. Immun. 66:5543-5546.
47. Stromberg, E., A. Lundgren, A. Edebo, S. Lundin, A. M. Svennerholm, and C. Lindholm. 2003. Increased frequency of activated T-cells in the Helicobacter pylori-infected antrum and duodenum. FEMS Immunol. Med. Microbiol. 36:159-168.
48. Su, R. C., S. K. Kung, J. Gariepy, B. H. Barber, and R. G. Miller. 1998. NK cells can recognize different forms of class I MHC. J. Immunol. 161:755-766.
49. Suzuki, T., M. Ito, N. Hayasaki, A. Ishihara, T. Ando, K. Ina, and K. Kusugami. 2003. Cytotoxic molecules expressed by intraepithelial lymphocytes may be involved in the pathogenesis of acute gastric mucosal lesions. J. Gastroenterol. 38:216-221.
50. Tarkkanen, J., T. U. Kosunen, and E. Saksela. 1993. Contact of lymphocytes with Helicobacter pylori augments natural killer cell activity and induces production of gamma interferon. Infect. Immun. 61:3012-3016.
51. Van Tol, E. A., H. W. Verspaget, A. S. Pena, C. V. Kraemer, and C. B. Lamers. 1992. The CD56 adhesion molecule is the major determinant for detecting non-major histocompatibility complex-restricted cytotoxic mononuclear cells from the intestinal lamina propria. Eur. J. Immunol. 22:23-29.
52. Westphal, O., and K. Jann. 1965. Bacterial lipopolysaccharide: extraction with phenol-water and further applications of the procedure, p. 83-92. In R. Whitler (ed.). Methods in carbohydrate chemistry. Academic Press. New York, N.Y.
53. Wu, C., J. Ferrante, M. K. Gately, and J. Magram. 1997. Characterization of IL-12 receptor β1 chain (IL-12Rβ1)-deficient mice: IL-12Rβ1 is an essential component of the functional mouse IL-12 receptor. J. Immunol. 159:1658-1665.
54. Wu, C., X. Wang, M. Gadina, J. J. O'Shea, D. H. Presky, and J. Magram. 2000. IL-12 receptor beta 2 (IL-12R beta 2)-deficient mice are defective in IL-12-mediated signaling despite the presence of high affinity IL-12 binding sites. J. Immunol. 165:6221-6228.
55. Xing, Z., A. Zganiacz, J. Wang, and S. K. Sharma. 2001. Enhanced protection against fatal mycobacterial infection in SCID beige mice by reshaping innate immunity with IFN-gamma transgene. J. Immunol. 167:375-383.