Interleukin-18 (IL-18) enhances innate IL-12-mediated resistance to Toxoplasma gondii

Infection and Immunity

Volumn 68, Issue 12, 2000, Pages 6932-6938

  Cai, Guifang ^a   Kastelein, Robert ^b   Hunter, Christopher A ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b MERCK RESEARCH LABORATORIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 12; INTERLEUKIN 18;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOTOXICITY TEST; INFECTION RESISTANCE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; SCID MOUSE; TOXOPLASMA GONDII; TOXOPLASMOSIS;

ANIMALS; INTERFERON TYPE II; INTERLEUKIN-12; INTERLEUKIN-18; KILLER CELLS, NATURAL; MICE; MICE, SCID; TOXOPLASMOSIS, ANIMAL;

EID: 0034445617     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.68.12.6932-6938.2000     Document Type: Article

References (59)

1. Altare, F., A. Durandy, D. Lammas, J.-F. Emile, S. Lamharnedi, F. L. Deist, P. Drysdale, E. Jouanguy, R. Döffinger, F. Bernaudin, O. Jeppsson, J. A. Gollob, E. Meinl, A. W. Segal, A. Fischer, D. Kumararatne, and J.-L. Casanova. 1998. Impairment of mycobacterial immunity in human interleukin-12 receptor deficiency. Science 280:1432-1435.
2. Bazan, J. F., J. C. Timans, and R. Kastelein. 1996. A newly defined interleukin-1? Nature 379:591-591.
3. Bohn, E., A. Sing, R. Zumbihl, C. Biefeldt, H. Okamura, M. Kurimoto, J. Heesemann, and J. B. Autenrieth. 1998. IL-18 (IFN-γ-inducing factor) regulates early cytokine production in, and promotes resolution of, bacterial infection in mice. J. Immunol. 160:299-307.
4. Cai, G., R. A. Kastelein, and C. A. Hunter. 1999. IL-10 enhances NK cell proliferation, cytotoxicity and production of IFN-γ when combined with IL-18. Eur. J. Immunol. 29:2658-2665.
5. Coughlin, C. M., K. E. Salhany, M. Wysocka, E. Aruga, H. Kurzawa, A. E. Chang, C. A. Hunter, J. C. Fox, G. Trinchieri, and W. M. F. Lee. 1998. Interleukin-12 and interleukin-18 synergistically induce murine tumor regression which involves inhibition of angiogenesis. J. Clin. Investig. 101: 1441-1452.
6. Dao, T., W. Z. Mehal, and I. N. Crispe. 1998. IL-18 augements perforin-dependent cytotoxicity of liver NK-T cells. J. Immunol. 161:2217-2222.
7. de Jong, R., F. Altare, I.-A. Haagen, D. G. Elferink, T. Boer, P. J. van Breda Vriesman, P. J. Kabel, J. M. T. Draaisma, J. T. van Dissel, F. P. Kroon, J.-L. Casanova, and T. H. M. Ottenhoff. 1998. Severe mycobacterial and Salmonella infections in interleukin-12 receptor-deficient patients. Science 280: 1435-1438.
8. Dybing, J. K., N. Walters, and D. W. Pascual. 1999. Role of endogenous interleukin-18 in resolving wild-type and attenuated Salmonella typhimurium infections. Infect. Immun. 67:6242-6248.
9. Elhofy, A., and K. L. Bost. 1999. Limited interleukin-18 response in Salmonella-infected murine macrophages and in Salmonella-infected mice. Infect. Immun. 67:5021-5026.
10. + T cell response by IFN-γ in IL-12-deficient mice during Toxoplasma gondii infection. J. Immunol. 162:5449-5454.
11. Fehniger, T. A., M. H. Shah, M. J. Turner, J. B. VanDeusen, S. P. Whitman, M. A. Cooper, K. Suzuki, M. Wechser, F. Goodsaid, and M. A. Caligiuri. 1999. Differential cytokine and chemokine gene expression by human NK cells following activation with IL-18 or IL-15 in combination with IL-12: implications for the innate immune response. J. Immunol. 162:4511-4520.
12. Fukao, T., S. Matsuda, and S. Koyasu. 2000. Synergistic effects of IL-4 and IL-18 on IL-12-dependent IFN-γ production by dendritic cells. J. Immunol. 164:64-71.
13. Gazzinelli, R. T., E. Y. Denkers, and A. Sher. 1993. Host resistance to Toxoplasma gondii: model for studying the selective induction of cell-mediated immunity by intracellular parasites. Infect. Agents Dis. 2:139-149.
14. Gazzinelli, R. T., I. Eltourn, T. A. Wynn, and A. Sher. 1993. Acute cerebral toxoplasmosis is induced by in vivo neutralization of TNF-α and correlates with the down-regulated expressin of inducible nitric oxide synthase and other markers of macrophage activation. J. Immunol. 151:3672-3681.
15. Gazzinelli, R. T., S. Hieny, T. A. Wynn, S. Wolf, and A. Sher. 1993. Interleukin-12 is required for the T-lymphocyte-independent induction of interferon α by an intracellular parasite and induces resistance in T-cell deficient hosts. Proc. Natl. Acad. Sci. USA 90:6115-6119.
16. Ghayur, T., S. Banerjee, M. Hugunin, D. Butler, L. Herzog, A. Carter, L. Quintal, L. Sekut, R. Talanian, M. Paskind, W. Wong, R. Kamen, D. Tracey, and H. Allen. 1997. Caspase-1 processes IFN-γ-inducing factor and regulates LPS-induced IFN-γ production. Nature 386:619-623.
17. Gu, Y., K. Kuida, H. Tsutsui, G. Ku, K. Hsiao, M. A. Fleming, N. Hayashi, K. Higashino, H. Okamura, K. Nakanishi, M. Kurimoto, T. Tanimoto, R. A. Flavell, V. Sato, M. W. Harding, D. J. Livington, and M. S. S. Su. 1997. Activation of interferon-γ inducing factor mediated by interleukin-1β converting enzyme. Science 275:206-209.
18. Hashimoto, W., T. Osaki, H. Okamura, P. D. Robbins, M. Kurimoto, S. Nagata, M. T. Lotze, and H. Tahara. 1999. Differential antitumor effects of administration of recombinant IL-18 or recombinant IL-12 are mediated primarily by Fas-Fas ligand- and perforin-induced tumor apoptosis, respectively. J. Immunol. 163:583-589.
19. Hunter, C. A., E. Candolfi, C. S. Subauste, V. V. Cleave, and J. S. Remington. 1995. Studies on the role of interleukin-12 in acute murine toxoplasmosis. Immunology 84:16-20.
20. Hunter, C. A., R. Chizzonite, and J. S. Remington. 1995. IL-1β is required for IL-12 to induce production of IFN-γ by NK cells, a role for IL-1β in the T-cell-independent mechanism of resistance against intracellular pathogens. J. Immunol. 155:4347-4354.
21. Hunter, C. A., L. Ellis-Neyer, K. E. Gabriel, M. K. Kennedy, K. H. Grabstein, P. S. Linsley, and J. S. Remington. 1997. The role of the CD28/B7 interaction in the regulation of NK cell responses during infection with Toxoplasma gondii. J. Immunol. 158:2285-2293.
22. Hunter, C. A., C. S. Subauste, V. H. Van Cleave, and J. S. Remington. 1994. Production of gamma interferon by natural killer cells from Toxoplasma gondii-infected SCID mice: regulation by interleukin-10, interleukin-12, and tumor necrosis factor alpha. Infect. Immun. 62:2818-2824.
23. Hunter, C. A., J. C. Timans, P. Pisacane, S. Menon, G. Cai, W. Walker, M. Aste-Amezaga, R. Chizzonite, J. F. Bazan, and R. A. Kastelein. 1997. Comparison of the effects of interleukin-1α, interleukin-1β and interferon-γ-inducing factor on the production of interferon-γ by natural killer. Eur. J. Immunol. 27:2787-2792.
24. Hyodo, Y., K. Matsui, N. Hayashi, H. Tsutsui, S. Kashiwamura, H. Yamauchi, K. Hiroishi, K. Takeda, Y. Tagawa, Y. Iwakura, N. Kayagaki, M. Kurimoto, H. Okamura, T. Hada, H. Yagita, S. Akira, K. Nakanishi, and K. Higashino. 1999. IL-18 up-regulates perforin-mediated NK activity without increasing perform messenger RNA expression by binding to constitutively expressed IL-18 receptor. J. Immunol. 162:1662-1668.
25. Johnson, L. L. 1992. A protective role for endogenous tumor necrosis factor in Toxoplasma gondii infection. Infect. Immun. 60:1979-1983.
26. Kanakaraj, P., K. Ngo, Y. Wu, A. Angulo, P. Ghazal, C. A. Harris, J. J. Siekierka, P. A. Peterson, and W.-P. Fung-Leung. 1999. Defective interleukin (IL)-18-mediated natural killer and T helper cell type 1 responses in IL-1 receptor-associated kinase (IRAK)-deficient mice. J. Exp. Med 189:1129-1138.
27. Kaplan, M. H., A. L. Wurster, and M. J. Grusby. 1998. A signal transducer and activator of transcription (Stat)4-independent pathway for the development of T helper type 1 cells. J. Exp. Med. 188:1191-1196.
28. Kim, Y.-M., R. V. Talanian, J. Li, and T. R. Billiar. 1998. Nitric oxide prevents IL-1β and IFN-γ-inducing factor (IL-18) release from macrophages by inhibiting caspase-1 (IL-1β-converting enzyme). J. Immunol. 161:4122-4128.
29. Kohka, H., T. Yoshino, H. Iwagaki, I. Sakuma, T. Tanimoto, Y. Matsuo, M. Kurimoto, K. Orita, T. Akagi, and N. Tanaka. 1998. Interleukin-18/interferon-gamma-inducing factor, a novel cytokine, up-regulates ICAM-1 (CD54) expression in KG-1 cells. J. Leukoc. Biol. 64:519-527.
30. Mastroeni, P., S. Clare, S. Khan, J. A. Harrison, C. E. Hormaeche, H. Okamura, M. Kurimoto, and G. Dougan. 1999. Interleukin 18 contributes to host resistance and gamma interferon production in mice infected with virulent Salmonella typhimurium. Infect. Immun. 67:478-483.
31. Matsumoto, S., K. Tsuji-Takayama, Y. Aizawa, K. Koide, M. Takeuchi, T. Ohta, and M. Kurimoto. 1997. Interleukin-18 activates NF-κB in murine T helper type 1 cells. Biochem. Biophys. Res. Commun. 234:454-457.
32. Micallef, M. J., T. Tanimoto, K. Kohno, M. Ikeda, and M. Kurimoto. 1997. Interleukin 18 induces the sequential activation of natural killer cells and cytotoxic T lymphocytes to protect syngeneic mice from transplantation with Meth A sarcoma. Cancer Res. 57:4557-4563.
33. Monteleone, G., F. Trapasso, T. Parrello, L. Biancone, A. Stella, R. Iuliano, F. Luzza, A. Fusco, and F. Pallone. 1999. Bioactive IL-18 expression is up-regulated in Crohn's disease. J. Immunol. 163:143-147.
34. Munder, M., M. Mallo, K. Eichmann, and M. Modolell. 1998. Murine macrophages secrete interferon γ upon combined stimulation with interleukin (IL)-12 and IL-18: a novel pathway of autocrine macrophage activation. J. Exp. Med. 187:2103-2108.
35. Nagai, H., I. Hara, T. Horikawa, M. Fujii, M. Kurimoto, S. Kamidono, and M. Ichihashi. 2000. Antitumor effects on mouse melanoma elicited by local secretion of interleukin-12 and their enhancement by treatment with interleukin-18. Cancer Investig. 18:206-213.
36. Ohkusu, K., T. Yoshimoto, K. Takeda, T. Ogura, S.-I. Kashiwamura, Y. Iwakura, S. Akira, H. Okamura, and K. Nakanishi. 2000. Potentiality of interleukin-18 as a useful reagent for treatment and prevention of Leishmania major infection. Infect. Immun. 68:2449-2456.
37. Okamura, H., H. Tsutsui, S. Kashiwamura, T. Yoshimoto, and K. Nakanishi. 1998. Interleukin-18: a novel cytokine that augments both innate and acquired immunity. Adv. Immunol. 70:281-312.
38. Okamura, H., H. Tsutsui, T. Komatsu, M. Yutsudo, A. Hakura, T. Tanimoto, K. Torigoe, T. Okura, Y. Nukata, K. Hattori, K. Akita, M. Namba, F. Tanabe, K. Konishi, S. Fukuda, and M. Kurimoto. 1995. Cloning of a new cytokine that induces IFN-γ production by T cells. Nature 378:88-91.
39. Osaki, T., H. Okamnra, Q. Cai, P. D. Robbins, M. Kurimoto, M. T. Lotze, and H. Tahara. 1998. IFN-γ-inducing factor/IL-18 administration mediates IFN-γ-and IL-12-independent antitumor effects. J. Immunol. 160:1742-1749.
40. Oxenius, A., U. Karrer, R. M. Zinkernagel, and H. Hengartner. 1999. IL-12 is not required for induction of type 1 cytokine responses in viral infections. J. Immunol. 162:965-973.
41. Pirhonen, J., T. Sareneva, M. Kurimoto, I. Julkunen, and S. Matikainen. 1999. Virus infection activates IL-1 beta and IL-18 production in human macrophages by a caspase-1-dependent pathway. J. Immunol. 162:7322-7329.
42. Pizarro, T. T., M. H. Michie, M. Bentz, J. Woraratanadharm, M. F. Smith, E. Foley, C. A. Moskaluk, S. J. Bickston, and F. Cominelli. 1999. IL-18, a novel immunoregulatory cytokine, is up-regulated in Crohn's disease: expression and localization in intestinal mucosal cells. J. Immunol. 162:6829-6835.
43. Qureshi, M. H., T. Zhang, Y. Koguchi, K. Nakashima, H. Okamura, M. Kurimoto, and K. Kawakami. 1999. Combined effects of IL-12 and IL-18 on the clinical course and local cytokine production in murine pulmonary infection with Cryptococcus neoformans. Eur. J. Immunol. 29:643-649.
44. Sander, B., I. Höidén, U. Andersson, E. Möller, and J. S. Abrams. 1993. Similar frequencies and kinetics of cytokine producing cells in murine peripheral blood and spleen. J. Immunol. Methods 166:201-214.
45. Scharton-Kersten, T., P. Caspar, A. Sher, and E. Y. Denkers. 1996. Toxoplasma gondii: evidence for interleukin-12-dependent and -independent pathways of interferon-γ production induced by an attenuated parasite strain. Exp. Parasitol. 84:102-114.
46. Scharton-Kersten, T. M., T. A. Wynn, E. Y. Denkers, S. Bala, E. Grunvald, S. Hieny, R. T. Gazzinelli, and A. Sher. 1996. In the absence of endogenous IFN-gamma, mice develop unimpaired IL-12 responses to Toxoplasma gondii while failing to control acute infection. J. Immunol. 157:4045-4054.
47. Sharma, S. D., J. M. Hofflin, and J. S. Remington. 1985. In vivo recombinant interleukin 2 administration enhances survival against a lethal challenge with Toxoplasma gondii. J. Immunol. 135:4160-4163.
48. Sugawara, I., H. Yamada, H. Kaneko, S. Mizumo, K. Takeda, and S. Akira. 1999. Role of interleukin-18 (IL-18) in mycobacterial infection in IL-18-gene-disrupted mice. Infect. Immun. 67:2585-2589.
49. Suzuki, Y., F. K. Conley, and J. S. Remington. 1989. Importance of endogenous IFN-γ for the prevention of toxoplasmic encephalitis in mice. J. Immunol. 143:2045-2050.
50. Suzuki, Y., M. A. Orellana, R. D. Schreiber, and J. S. Remington. 1988. Interferon-γ: the major mediator of resistance against Toxoplasma gondii. Science 240:516-518.
51. Takeda, K., H. Tsutsui, T. Yoshimoto, O. Adachi, N. Yoshida, T. Kishimoto, H. Okamura, K. Nakanishi, and S. Akira. 1998. Defective NK cell activity and Th1 response in IL-18-deficient mice. Immunity 8:383-390.
52. Thomassen, E., T. A. Bird, B. R. Renshaw, M. K. Kennedy, and J. E. Sims. 1998. Binding of interleukin-18 to the interleukin-1 receptor homologous receptor IL-1Rrp1 leads to activation of signaling pathways similar to those used by interleukin-1. J. Interferon Cytokine Res. 18:1077-1088.
53. Trinchieri, G. 1989. Biology of natural killer cells. Adv. Immunol. 47:187-376.
54. Walker, W., M. Aste-Amezaga, R. A. Kastelein, G. Trinchieri, and C. A. Hunter. 1999. IL-18 and CD28 use distinct molecular mechanisms to enhance NK cell production of IL-12-induced IFNγ J. Immunol. 162:5894-5901.
55. Wei, X, B. P. Leung, W. Niedbala, D. Piedrafita, G. Feng, M. Sweet, L. Dobbie, A. J. H. Smith, and F. Y. Liew. 1999. Altered immune responses and susceptibility to Leishmania major and Staphylococcus aureus infection in IL-18-deficient mice. J. Immunol. 163:2821-2828.
56. + T cells: evidence for two distinct pathways for promoter activation. Eur. J. Immunol. 29:548-555.
57. Yoshimoto, T., H. Okamura, Y.-I. Tagawa, Y. Iwakura, and K. Nakanishi. 1997. Interleukin-18 together with interleukin-12 inhibits IgE production by induction of interferon-γ production from activated B cells. Proc. Natl. Acad. Sci. USA 94:3948-3953.
58. Yoshimoto, T., K. Takeda, Y. Tanaka, K. Ohkusu, S.-I. Kashiwamura, H. Okamura, S. Akira, and K. Nakanishi. 1998. IL-12 up-regulates IL-18 receptor expression on T cells, Th1 cells, and B cells: synergism with IL-18 for IFN-γ production. J. Immunol. 161:3400-3407.
59. Zhang, T., K. Kawakami, M. H. Qureshi, H. Okamura, M. Kurimoto, and A. Saito. 1997. Interleukin-12 (IL-12) and IL-18 synergistically induce the fungicidal activity of murine peritoneal exudate cells against Cryptococcus neoformans through production of gamma interferon by natural killer cells. Infect. Immun. 65:3594-3599.