Toxoplasma gondii and Schistosoma mansoni synergize to promote hepatocyte dysfunction associated with high levels of plasma TNF-α and early death in C57BL/6 mice

Journal of Immunology

Volumn 163, Issue 4, 1999, Pages 2089-2097

  Marshall, Anthony J ^a   Rosa Brunet, Laura ^a   Van Gessel, Yvonne ^a   Alcaraz, Ana ^a   Bliss, Susan K ^a   Pearce, Edward J ^a   Denkers, Eric Y ^a  

^a Cornell University ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; GAMMA INTERFERON; IMMUNOGLOBULIN E; NITRIC OXIDE; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; FEMALE; IMMUNE RESPONSE; LIVER CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCHISTOSOMA MANSONI; SCHISTOSOMIASIS; TOXOPLASMA GONDII; TOXOPLASMOSIS;

EID: 0344131392     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (48)

1. Rosa Brunet, L., F. D. Finkelman, A. W. Cheever, M. A. Kopf, and E. J. Pearce. 1997. IL-4 protects against TNF-α-mediated cachexia and death during acute schistosomiasis. J. Immunol 159:777.
2. Denkers, E. Y., and R. T. Gazzinelli. 1998. Regulation and function of T cell-mediated immunity during Toxoplasma gondii infection. Clin. Microbiol. Rev. 11:569.
3. Scharton-Kersten. T., E. Y. Denkers, R. T. Gazzinelli, and A. Sher. 1995. Role of IL-12 in the induction of cell-mediated immunity to Toxoplasma gondii. Res. Immunol. 146:539.
4. + T cells to enhance priming for IFN-γ production and diminishes IL-4 inhibition of such priming. Proc. Natl. Acad. Sci. USA 90:10188.
5. Scott, P. 1993. IL-12: initiation cytokine for cell-mediated immunity. Science 260:496.
6. Saavedra, R., F. de Meuter, J.-L. Decourt, and P. Herion. 1991. Human T cell clone identifies a potentially protective 54-kDa protein antigen of Toxoplasma gondii cloned and expressed in Escherichia coli. J. Immunol. 147:1975.
7. Sibley, L. D., L. B. Adams, A. Y. Fukutomi, and J. L. Krahenbuhl. 1991. Tumor necrosis factor-α triggers antitoxoplasmal activity in IFN-γ primed macrophages. J. Immunol. 147:2340.
8. 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.
9. Gazzinelli, R. T., I. P. Oswald, S. Hieny, S. James, and A. Sher. 1992. The microbicidal activity of interferon-γ-treated macrophages against Trypanosoma cruzi involves an L-arginine-dependent, nitrogen oxide-mediated mechanism inhibitable by interleukin-10 and transforming growth factor-β. Eur. J. Immunol. 22:2501.
10. Denkers, E. Y., T. Scharton-Kersten, R. T. Gazzinelli, G. Yap, H. Charest, and A. Sher. 1997. Cell-mediated immunity to Toxoplasma gondii: redundant and required mechanisms as revealed by studies in gene knockout mice. In Medical Intelligence Unit: Host Response to Intracellutar Pathogens. S. H. E. Kaufmann, ed. R.G. Landes Company. Austin, p. 167.
11. Scharton-Kersten, T. M., T. A. Wynn, E. Y. Denkers, S. Bala, L. Showe, E. Grunvald, S. Hieny, R. T. Gazzinelli, and A. Sher. 1996. In the absence of endogenous IFN-γ mice develop unimpaired IL-12 responses to Toxoplasma gondii while failing to control acute infection. J. Immunol. 157:4045.
12. 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.
13. 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.
14. + T lymphocytes in IFN-γ production and protective immunity induced by an attenuated T. gondii vaccine. J. Immunol. 146:286.
15. Johnson, L. L. 1992. A protective role for endogenous tumor necrosis factor in Toxoplasma gondii infection. Infect. Immun. 60:1979.
16. 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.
17. Deckert-Schluter, M., H. Bluethmann, A. Rang, H. Hof, and D. Schluter. 1998. Crucial role for TNF receptor type 1 (p55), but not TNF receptor type 2 (p75), in murine toxoplasmosis. J. Immunol. 160:3427.
18. + T cells and accompanied by overproduction of IL-12, IFN-γ, and TNF-α. J. Immunol. 157:798.
19. Neyer, L. E., G. Grunig, M. Fort, J. S. Remington, D. Rennick, and C. A. Hunter. 1997. Role of interleukin-10 in regulation of T-cell-dependent and T-cell-independent mechanisms of resistance to Toxoplasma gondii. Infect. Immun. 65:1675.
20. Marshall, A. J., and E. Y. Denkers. 1998. Toxoplasma gondii triggers granulocyte-dependent, cytokine-mediated lethal shock in D-galactosamine sensitized mice. Infect. Immun. 66:1325.
21. Abbas, A. K., K. M. Murphy, and A. Sher. 1996. Functional diversity of helper T lymphocytes. Nature 383:787.
22. Gajewski, T. F., and F. W. Fitch. 1988. Anti-proliferative effect of IFN-γ in immunoregulation. I. IFN-γ inhibits the proliferation of Th2 but not Th1 murine helper T lymphocyte clones. J. Immunol. 140:4245.
23. + T cell-dependent, IFN-γ-mediated necrosis of the small intestine with genetic susceptibility of mice to peroral infection with Toxoplasma gondii. J. Exp. Med. 184:597.
24. Donehower, L. A., R. C. Bohannon, R. J. Ford, and R. A. Gibss. 1990. The use of primers from highly conserved pol regions to identify uncharacterized retroviruses by the polymerase chain reaction. J. Virol. Methods 28:33.
25. Gazzineili, R. T., S. Hieny, T. Wynn, S. Wolf, and A. Sher. 1993. IL-12 is required for the T-cell independent induction of IFN-γ by an intracellular parasite and induces resistance in T-cell-deficient hosts. Proc. Natl. Acad. Sci. USA 90: 6115.
26. Prince, J. B., K. L. Auer, J. Huskinson, S. F. Parmley, F. G. Araujo, and J. S. Remington. 1990. Cloning, expression, and cDNA sequence of surface antigen P22 from Toxoplasma gondii. Mol. Biochem. Parasitol. 43:97.
27. Pearce, E., P. Scott and A. Sher. 1999. Immune regulation in parasitic infection and disease. In Fundamental Immunology. W. E. Paul, ed. Lippincott-Raven. Philadelphia, p. 1271.
28. Scharton-Kersten, T., 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. 185:1.
29. Kloetzel, K., P. Chieffi, J. Faleiros, and T. Filho. 1977. Mortality and other parameters of concomitant infections in albino mice: the Schistosoma-Toxoplasma model. Trop. Geog. Med. 29:407.
30. Actor, J. K., M. A. Marshall, I. A. Eltoum, R. M. Buller, J. A. Berzofsky, and A. Sher. 1994. Increased susceptibility of mice infected with Schistosoma mansoni to recombinant vaccinia virus: association of viral persistence with egg granuloma formation. Eur. J. Immunol. 24:3050.
31. Actor, J. K., M. Shirai, M. C. Kullberg, R. M. Buller, A. Sher, and J. A. Berzofsky. 1993. Helminth infection results in decreased virus-specific CD8+ cytotoxic T-cell and Th1 cytokine responses as well as delayed virus clearance. Proc. Natl. Acad. Sci. USA 90:948.
32. Kullberg, M. C., E. J. Pearce, S. A. Hieny, and A. Sher. 1992. Infection with Schistosoma mansoni alters Th1/Th2 cytokine responses to a non-parasite antigen. J. Immunol. 148:3264.
33. Sabin, E. A., M. I. Araujo, E. M. Carvalho, and E. J. Pearce. 1996. Impairment of tetanus toxoid-specific Th1-like immune responses in humans infected with Schistosoma mansoni. J. Infect. Dis. 173:269.
34. Liesenfeld, O., J. C. Kosek, and Y. Suzuki. 1997. γ-interferon induces Fas-dependent apoptosis of Peyer's patch T cells in mice following peroral infection with Toxoplasma gondii. Infect. Immun. 65:4682.
35. Gately, M., L. Renzetti, H. Magram, A. Stern, L. Adorini, U. Gubler, and D. H. Presky. 1998. The interleukin-12/interleukin-12-receptor system. Annu. Rev. Immunol. 16:495.
36. James, S., J. Glaven, S. Goldenberg, M. Meltzer, and E. Pearce. 1990. Tumor necrosis factor (TNF) as a mediator of macrophage helminthotoxic activity. Parasite Immunol. 12:1.
37. Neta, R., T. Sayers, and J. Oppenheim. 1992. Relationship of TNF to interleukins. In Tumor Necrosis Factors: Structure, Function, and Mechanisms of Action. B. Aggarwal and J. Vilcek, ed. Marcel-Dekker, Inc. New York, p. 499.
38. Boros, D. 1994. The role of cytokines in formation of the schistosome egg granuloma. Immunobiology 191:441.
39. Bradham, C., J. Plumpe, M. Manns, D. Brenner, and C. Trautwein. 1998. Mechanisms of hepatic toxicity. I. TNF-induced liver injury. Am. J. Physiol. 275:G387.
40. Leist, M., F. Gantner, I. Bohlinger, G. Tiegs, P. Germann, and A. Wendel. 1995. Tumor necrosis factor-induced hepatocyte apoptosis precedes liver failure in experimental murine shock models. Am. J. Pathol. 146:1220.
41. Kim, Y., R. Talanian, and T. Billiar. 1997. Nitric oxide inhibits apoptosis by preventing increases in caspase-3-like activity via two distinct mechanisms. J. Biol. Chem. 272:31138.
42. Khan, I. A., J. D. Schwartzman, T. Matsuura, and L. H. Kasper. 1997. A dichotomous role for nitric oxide during acute Toxoplasma gondii infection in mice. Proc. Natl. Acad. Sci. USA 94:13955.
43. Doenhoff, M. J., R. Musallam, J. Bain, and A. McGregor. 1979. Schisiosoma mansoni infection in T-cell deprived mice, and the ameliorating effect of administering homologous chronic infection serum. I. Pathogenesis. Am. J. Trop. Med. Hyg. 28:260.
44. Doenhoff, M., S. Pearson, D. Dunne, Q. Bickle, and S. Lucas. 19981. Immunological control of hepatotoxicity and parasite egg excretion in Schistosoma mansoni infections: stage specificity of the reactivity of immune serum in T-cell deprived mice. Trans. R. Soc. Trop. Med. Hyg. 75:41.
45. Byram, J., and F. Von Lichtenberg. 1977. Altered schistosome granuloma formation in nude mice. Am. J. Trop. Med. Hyg. 26:944.
46. Dunne, D., F. M. Jones, and M. J. Doenhoff. 1991. The purification, characterization, serological activity and hepatotoxic properties of two cationic glycoproteins from Schistosoma mansoni eggs. Parasitology 103:225.
47. Mahmoud, A., G. Strickland, and K. Warren. 1977. Toxoplasmosis and the host-parasite relationship in murine schistosomiasis mansoni. J. Infect. Dis. 135:408.
48. Wynn, T. A., and A. W. Cheever. 1995. Cytokine regulation of granuloma formation in schistosomiasis. Curr. Opin. Immunol. 7:505.