Both lymphotoxin-α and TNF are crucial for control of Toxoplasma gondii in the central nervous system

Journal of Immunology

Volumn 170, Issue 12, 2003, Pages 6172-6182

  Schlüter, Dirk ^a   Kwok, Lai Yu ^a   Lütjen, Sonja ^a,b   Soltek, Sabine ^a   Hoffmann, Sigrid ^a   Körner, Heinrich ^a,c   Deckert, Martina ^b  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b UNIVERSITY OF COLOGNE   (Germany)

^c UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 2; INTERLEUKIN 4; LYMPHOTOXIN; MESSENGER RNA; NITRIC OXIDE SYNTHASE; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR RECEPTOR 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY TITER; ARTICLE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BONE MARROW; CENTRAL NERVOUS SYSTEM; CHIMERA; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENCEPHALITIS; FEMALE; GENOTYPE; HISTOPATHOLOGY; HUMAN; HUMAN CELL; IMMUNITY; INFECTION CONTROL; MALE; MOUSE; NONHUMAN; PARASITE; PERITONEUM MACROPHAGE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SPLEEN; SURVIVAL; T LYMPHOCYTE; TOXOPLASMA GONDII; TOXOPLASMOSIS; WILD TYPE;

EID: 0037604804     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.170.12.6172     Document Type: Article

References (51)

1. Dubey, J. P. 1997. Bradyzoite-induced murine toxoplasmosis: stage conversion, pathogenesis, and tissue cyst formation in mice red bradyzoites of different strains of Toxoplasma gondii. J. Eukaryotic Microbiol. 44:592.
2. Schlüter, D., J. Löhler, M. Deckert, H. Hof, and G. Schwendemann. 1991. Toxoplasma encephalitis of immunocompetent and nude mice: immunohistochemical characterisation of Toxoplasma antigen, infiltrates and major histocompatibility complex gene products. J. Neuroimmunol. 31:185.
3. + T lymphocytes is required to reactivate chronic infection with Toxoplasma gondii. J. Immunol. 149:175.
4. Suzuki, Y., F. K. Conley, and J. S. Remington. 1989. Importance of endogenous IFN-γ for prevention of toxoplasmic encephalitis in mice. J. Imnumol. 143:2045.
5. Schlüter, D., N. Kaefer, H. Hof, O. D. Wiestler, and M. Deckert-Schlüter. 1997. Expression pattern and cellular origin of cytokines in the normal and Toxoplasma gondii-infected murine brain. Am. J. Pathol. 150:1021.
6. Deckert-Schlüter, M., A. Rang, D. Weiner, S. Huang, O. D. Wiestler, H. Hof, and D. Schlüter. 1996. Interferon-γ receptor-deficiency renders mice highly susceptible to toxoplasmosis by decreased macrophage activation. Lab. Invest. 75:827.
7. Schlüter, D., M. Deckert-Schlater, G. Schwendemann, H. Brunner, and H. Hof. 1993. Expression of major histocompatibility complex class II antigens and levels of interferon-γ, tumour necrosis factor, and interleukin-6 in cerebrospinal fluid and serum in Toxoplasma gondii-infected SCID and immunocompetent C.B-17 mice. Immunology 78:430.
8. 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.
9. + T lymphocytes in IFN-γ production and protective immunity induced by an attenuated Toxoplasma gondii vaccine. J. Immunol. 146:286.
10. Waldeland, H., and J. K. Frenkel. 1983. Live and killed vaccines against toxoplasmosis in mice. J. Parasitol. 69:60.
11. Sayles, P. C., and L. L. Johnson. 1996. Intact immune defenses are required for mice to resist the ts-4 vaccine strain of Toxoplasma gondii. Infect. Immun. 64:3088.
12. Sousa, C. R., S. Hieny, T. Scharton-Kersten, D. Jankovic, H. Charest, R. N. Germain, and A. Sher. 1997. In vivo microbial stimulation induces rapid CD40 ligand-independent production of interleukin 12 by dendritic cells and their redistribution to T cell areas. J. Exp. Med. 186:1819.
13. Suzuki, Y., Q. Yang, S. Yang, N. Nguyen, S. Lim, O. Liesenfeld, T. Kojima, and J. S. Remington. 1996. IL-4 is protective against development of toxoplasmic encephalitis. J. Immunol. 157:2564.
14. Kang, H., J. S. Remington, and Y. Suzuki. 2000. Decreased resistance of B cell-deficient mice to infection with Toxoplasma gondii despite unimpaired expression of IFN-γ, TNF-α, and inducible nitric oxide synthase. J. Immunol. 164:2629.
15. Gazzinelli, R. T., I. Eltoum, 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 expression of inducible nitric oxide synthase and other markers of macrophage activation. J. Immunol. 151:3672.
16. Johnson, L. L. 1992. A protective role for endogenous tumor necrosis factor in Toxoplasma gondii infection. Infect. Immun. 60:1979.
17. Chang, H. R., G. E. Grau, and J. C. Pechere. 1990. Role of TNF and IL-1 in infections with Toxoplasma gondii. Immunology 69:33.
18. Langermans, J. A., M. E. Van der Hulst, P. H. Nibbering, P. S. Hiemstra, L. Fransen, and R. Van Furth. 1992. IFN-γ-induced L-arginine-dependent toxoplasmastatic activity in murine peritoneal macrophages is mediated by endogenous tumor necrosis factor-α. J. Immunol. 148:568.
19. Chao, C. C., S. Hu, G. Gekker, W. J. Novick Jr., J. S. Remington, and P. K. Peterson. 1993. Effects of cytokines on multiplication of Toxoplasma gondii in microglial cells. J. Immunol. 150:3404.
20. Däubener, W., B. Spors, C. Hucke, R. Adam, M. Stins, K. S. Kim, and H. Schroten. 2001. Restriction of Toxoplasma gondii growth in human brain microvascular endothelial cells by activation of indoleamine 2,3-dioxygenase. Infect. Immun. 69:6527.
21. Chaves, A. C., I. P. Ceravolo, J. A. Gomes, C. L. Zani, A. J. Romanha, and R. T. Gazzinelli. 2001. IL-4 and IL-13 regulate the induction of indoleamine 2,3-dioxygenase activity and the control of Toxoplasma gondii replication in human fibroblasts activated with IFN-γ. Eur. J. Immunol. 31:333.
22. Nagineni, C. N., K. Pardhasaradhi, M. C. Martins, B. Detrick, and J. J. Hooks. 1996. Mechanisms of interferon-induced inhibition of Toxoplasma gondii replication in human retinal pigment epithelial cells. Infect. Immun. 64:4188.
23. Habara-Ohkubo, A., T. Shirahata, O. Takikawa, and R. Yoshida. 1993. Establishment of an antitoxoplasma state by stable expression of mouse indoleamine 2,3-dioxygenase. Infect. Immun. 61:1810.
24. Yap, G. S., T. Scharton-Kersten, H. Charest, and A. Sher. 1998. Decreased resistance of TNF receptor p55- and p75-deficient mice to chronic toxoplasmosis despite normal activation of inducible nitric oxide synthase in vivo. J. Immunol. 160:1340.
25. Deckert-Schlüter, M., H. Bluethmann, A. Rang, H. Hof, and D. Schlüter. 1998. Crucial role of TNF receptor type 1 (p55), but not of TNF receptor type 2 (p75), in murine toxoplasmosis. J. Immunol. 160:3427.
26. Loetscher, H., R. Gentz, M. Zulauf, A. Lustig, H. Tabuchi, E. J. Schlaeger, M. Brockhaus, H. Gallati, M. Manneberg, and W. Lesslauer. 1991. Recombinant 55-kDa tumor necrosis factor (TNF) receptor: stoichiometry of binding to TNF α and TNF β and inhibition of TNF activity. J. Biol. Chem. 266:18324.
27. Crowe, P. D., T. L. VanArsdale, B. N. Walter, C. F. Ware, C. Hession, B. Ehrenfels, J. L. Browning, W. S. Din, R. G. Goodwin, and C. A. Smith. 1994. A lymphotoxin-β-specific receptor. Science 264:707.
28. Roach, D. R., H. Briscoe, B. Saunders, M. P. France, S. Riminton, and W. J. Britton. 2001. Secreted lymphotoxin-α is essential for the control of an intracellular bacterial infection. J. Exp. Med. 193:239.
29. Magez, S., B. Stijlemans, G. Caljon, H. P. Eugster, and P. De Baetselier. 2002. Control of experimental Trypanosoma brucei infections occurs independently of lymphotoxin-α induction. Infect. Immun. 70:1342.
30. Engwerda, C. R., T. L. Mynott, S. Sawhney, J. B. De Souza, Q. D. Bickle. and P. M. Kaye. 2002. Locally up-regulated lymphotoxin a, not systemic tumor necrosis factor α, is the principle mediator of murine cerebral malaria. J. Exp. Med. 195:1371.
31. Körner, H., M. Cook, D. S. Riminton, F. A. Lemekert, R. M. Hoek, B. Ledermann, F. Köntgen, B. Fazekas de St. Groth, and J. D. Sedgwick. 1997. Distinct roles for lymphotoxin-α and tumor necrosis factor in organogenesis and spatial organization of lymphoid tissue. Eur. J. Immunol. 27:2600.
32. Riminton, D., H. Körner, D. H. Strickland, F. A. Lemckert, J. D. Pollard, and J. D. Sedgwick. 1998. Challenging cytokine redundancy: inflammatory cell movement and clinical course of experimental autoimmune encephalomyelitis are normal in lymphotoxin-deficient, but not tumor necrosis factor-deficient, mice. J. Exp. Med. 187:1517.
33. Schlüter, D., A. Hein, R. Dorries, and M. Deckert-Schlüter. 1995. Different subsets of T cells in conjunction with natural killer cells, macrophages, and activated microglia participate in the intracerebral immune response to Toxoplasma gondii in athymic nude and immunocompetent rats. Am. J. Pathol. 146:999.
34. Deckert, M., S. Soltek, G. Geginat, S. Lutjen, M. Montesinos-Rongen, H. Hof, and D. Schlüter. 2001. Endogenous interleukin-10 is required for prevention of a hyperinflammatory intracerebral immune response in Listeria monocytogenes meningoencephalitis. Infect. Immun. 69:4561.
35. Deckert-Schlüter, M., S. Albrecht, H. Hof, O. D. Wiestler, and D. Schlüter. 1995. Dynamics of the intracerebral and splenic cytokine mRNA production in Toxoplasma gondii-resistant and -susceptible congenic strains of mice. Immunology 85:408.
36. Silva, N. M., C. V. Rodrigues, M. M. Santoro, L. F. Reis, J. I. Alvarez-Leite, and R. T. Gazzinelli. 2002. Expression of indoleamine 2,3-dioxygenase, tryptophan degradation, and kynurenine formation during in vivo infection with Toxoplasma gondii: induction by endogenous γ interferon and requirement of interferon regulatory factor 1. Infect. Immun. 70:859.
37. + T cells: selective analysis in CD45-congenic normal and Toxoplasma gondii-infected bone marrow chimeras. Brain Pathol. 11:44.
38. Alexopoulou, L., M. Pasparakis, and G. Kollias. 1998. Complementation of lymphotoxin α knockout mice with tumor necrosis factor-expressing transgenes rectifies defective splenic structure and function. J. Exp. Med. 188:745.
39. Scharton-Kersten, T. M., G. Yap, J. Magram, and A. Sher. 1997. Inducible nitric oxide is essential for host control of persistent but not acute infection with the intracellular pathogen Toxoplasma gondii. J. Exp. Med. 185:1261.
40. Wilhelm, P., U. Ritter, S. Labbow, N. Donhäuser, M. Röllinghoff, C. Bogdan, and H. Körner. 2001. Rapidly fatal leishmaniasis in resistant C57BL/6 mice lacking TNF. J. Immunol. 166:4012.
41. Pasparakis, M., L. Alexopoulou, M. Grell, K. Pfizenmaier, H. Bluethmann, and G. Kollias. 1997. Peyer's patch organogenesis is intact yet formation of B lymphocyte follicles is defective in peripheral lymphoid organs of mice deficient for tumor necrosis factor and its 55-kDa receptor. [Published erratum appears in 1997 Proc. Natl. Acad. Sci. USA 94:9510.]. Proc. Natl. Acad. Sci. USA 94:6319.
42. Matsumoto, M., S. Mariathasan, M. H. Nahm, F. Baranyay, J. J. Peschon, and D. D. Chaplin. 1996. Role of lymphotoxin and the type I TNF receptor in the formation of germinal centers. Science 271:1289.
43. De Togni, P., J. Goellner, N. H. Ruddle, P. R. Streeter, A. Fick, S. Mariathasan, S. C. Smith, R. Carlson, L. P. Shornick, J. Strauss-Schoenberger, et al. 1994. Abnormal development of peripheral lymphoid organs in mice deficient in lymphotoxin. Science 264:703.
44. Banks, T. A., B. T. Rouse, M. K. Kerley, P. J. Blair, V. L. Godfrey, N. A. Kuklin, D. M. Bouley, J. Thomas, S. Kanangat, and M. L. Mucenski. 1995. Lympho-toxin-α-deficient mice: effects on secondary lymphoid organ development and humoral immune responsiveness. J. Immunol. 155:1685.
45. Gazzinelli, R. T., M. Wysocka, S. Hayashi, E. Y. Denkers, S. Hieny, P. Caspar, G. Trinchieri, and A. Sher. 1994. Parasite-induced IL-12 stimulates early IFN-γ synthesis and resistance during acute infection with Toxoplasma gondii. J. Immunol. 153:2533.
46. Fu, Y. X., G. Huang, M. Matsumoto, H. Molina, and D. D. Chaplin. 1997. Independent signals regulate development of primary and secondary follicle structure in spleen and mesenteric lymph node. Proc. Natl. Acad. Sci. USA 94:5739.
47. Fu, Y. X., and D. D. Chaplin. 1999. Development and maturation of secondary lymphoid tissues. Annu. Rev. Immunol. 17:399.
48. Matsumoto, M., Y. X. Fu, H. Molina, and D. D. Chaplin. 1997. Lymphotoxin-α-deficient and TNF receptor-1-deficient mice define developmental and functional characteristics of germinal centers. Immunol. Rev. 156:137.
49. Müller, M., H. P. Eugster, M. Le Hir, A. Shakhov, F. Di Padova, C. Maurer, V. F. Quesniaux, and B. Ryffel. 1996. Correction or transfer of immunodeficiency due to TNF-LTα deletion by bone marrow transplantation. Mol. Med. 2:247.
50. Yap, G. S., and A. Sher. 1999. Effector cells of both nonhemopoietic and hemopoietic origin are required for interferon (IFN)-γ- and tumor necrosis factor (TNF)-α-dependent host resistance to the intracellular pathogen Toxoplasma gondii. J. Exp. Med. 189:1083.
51. Wilhelm, P., D. S. Riminton, U. Ritter, F. A. Lemckert, C. Scheidig, R. Hoek, J. D. Sedgwick, and H. Körner. 2002. Membrane lymphotoxin contributes to anti-leishmanial immunity by controlling structural integrity of lymphoid organs. Eur. J. Immunol. 32:1993.