In the belly of the beast: Subversion of macrophage proinflammatory signalling cascades during Toxoplasma gondii infection

Cellular Microbiology

Volumn 5, Issue 2, 2003, Pages 75-83

  Denkers, Eric Y ^a   Kim, Leesun ^a   Butcher, Barbara A ^a  

^a Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 12; LIPOPOLYSACCHARIDE; STAT1 PROTEIN; TRANSCRIPTION FACTOR; TUMOR NECROSIS FACTOR ALPHA;

CELL ACTIVITY; CELL NUCLEUS; CELL TRANSFER; CYTOKINE PRODUCTION; HOST PARASITE INTERACTION; IMMUNITY; INFLAMMATION; MACROPHAGE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SHORT SURVEY; SIGNAL TRANSDUCTION; TOXOPLASMA GONDII; TOXOPLASMOSIS;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; ANTIGENS, DIFFERENTIATION; CELL NUCLEUS; DNA-BINDING PROTEINS; INTERLEUKIN-12; LIPOPOLYSACCHARIDES; MACROPHAGES; MYELOID DIFFERENTIATION FACTOR 88; NF-KAPPA B; RECEPTORS, CCR5; RECEPTORS, IMMUNOLOGIC; SIGNAL TRANSDUCTION; STAT1 TRANSCRIPTION FACTOR; TOXOPLASMA; TOXOPLASMOSIS; TRANS-ACTIVATORS; TUMOR NECROSIS FACTOR-ALPHA;

BACTERIA (MICROORGANISMS); PROTOZOA; TOXOPLASMA; TOXOPLASMA GONDII;

EID: 0037303310     PISSN: 14625814     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1462-5822.2003.00258.x     Document Type: Short Survey

References (85)

1. Aderem, A., and Underhill, D.M. (1999) Mechanisms of phagocytosis in macrophages. Annu Rev Immunol 17: 593-623.
2. Aliberti, J., Reis e Sousa, C., Schito, M., Hieny, S., Wells, T., Huffnage, G.B., and Sher, A. (2000) CCR5 provides a signal for microbial induced production of IL-12 by CD8α+ dendritic cells. Nature Immunol 1: 83-87.
3. Blank, J.L., Gerwins, P., Elliot, E.M., Sather, S., and Johnson, G.L. (1996) Molecular cloning of mitogen-activated protein/ERKkinase kinases (MEKK) 2 and 3. J Biol Chem 271: 5361-5368.
4. Bogdan, C., and Rollinghoff, M. (1998) The immune response to Leishmania: mechanisms of parasite control and evasion. Int J Parasitol 28: 121-124.
5. Bogdan, C., and Rollinghoff, M. (1999) How do protozoan parasites survive inside macrophages? Parasitol Today 15: 22-28.
6. Bohuslav, J., Kravchenko, V.V., Parry, G.C.N., Erlich, J.H., Gerdankis, S., Mackman, N., and Ulevitch, R.J. (1998) Regulation of an essential innate immune response by the p50 subunit of NF-κB. J Clin Invest 102: 1645-1652.
7. Bowie, A., Kiss-Toth, E., Symons, J.A., Smith, G.L., Dower, S.K., and O'Niell, L.A. (2000) A46R and A52R from vaccinia virus are antagonists of host IL-1 and Toll-like receptor signaling. Proc Natl Acad Sci USA 97: 10162-10167.
8. Braun, M.C., and Kelsall, B.L. (2001) Regulation of interleukin-12 production by G-protein-coupled receptors. Microbes Infect 3: 99-107.
9. Briggs, L.J., Stein, D., Goltz, J., Corrigan, V.C., Efthymiadis, A., Hubner, S., and Jans, D.A. (1998) The cAMP-dependent protein kinase site (Ser312) enhances dorsal nuclear import through facilitating nuclear localization sequence/importin interaction. J Biol Chem 273: 22745-22752.
10. Brown, K., Park, S., Kanno, T., Franzoso, G., and Siebenlist, U. (1993) Mutual regulation of the transcriptional factor NF-κB and its inhibitor, IκB-α. Proc Nat Acad Sci USA 90: 2532-2536.
11. Burleigh, B.A., and Andrews, N.W. (1995) The mechanisms of Trypanosoma cruzi invasion of mammalian cells. Annu Rev Micro 49: 175-200.
12. Butcher, B.A., and Denkers, E.Y. (2002) Mechanism of entry determines ability of Toxoplasma gondii to inhibit macrophage proinflammatory cytokine production. Infect Immun 70: 5216-5224.
13. Butcher, B.A., Kim, L., Johnson, P.F., and Denkers, E.Y. (2001) Toxoplasma gondii tachyzoites inhibit proinflammatory cytokine induction in infected macrophages by preventing nuclear translocation of the transcription factor NFκB. J Immunol 167: 2193-2201.
14. Caamano, J., and Hunter, C.A. (2002) NF-kB family of transcription factors: central regulators of innate and adaptive immune functions. Clin Micro Rev 15: 414-429.
15. Caamano, J., Alexander, J., Craig, L., Bravo, R., and Hunter, C.A. (1999) The NF-kB family member RelB is required for innate and adaptive immunity to Toxoplasma gondii. J Immunol 163: 4453-4461.
16. 2 in the regulation of apoptosis and in maintenance of T cell-mediated immunity to Toxoplasma gondii. J Immunol 165: 5720-5728.
17. Campos, M.A.S., Almeida, I.C., Takeuchi, O., Akira, S., Valente, E.P., Procópio, D.O., et al. (2001) Activation of Toll-Like Receptor-2 by glycosylphosphatidylinositol anchors from a protozoan parasite. J Immunol 167: 416-423.
18. Carrera, L., Gazzinelli, R.T., Badolato, R., Hieny, S., Muller, W., Kuhn, R., and Sacks, D.L. (1996) Leishmania promastigotes selectively inhibit interleukin 12 induction in bone marrow-derived macrophages from susceptible and resistant mice. J Exp Med 183: 515-526.
19. Collazo, C.M., Yap, G.S., Sempowski, G.D., Lusby, K.C., Tessarollo, L., Vande Woude, G.F., Sher, A., and Taylor, G.A. (2001) Inactivation of LRG-47 and IRG-47 reveals a family of interferon-γ-inducible genes with essential, pathogen-specific roles in resistance to infection. J Exp Med 194: 181-187.
20. Collier-Hyams, L.S., Zeng, H., Sun, J., Tomlinson, A.D., Bao, Z.Q., Chen, H., Madara, J.L., Orth, K., and Neish, A.S. (2002) Cutting edge: Salmonella AvrA effector inhibits the key proinflammatory, anti-apoptotic NF-κB pathway. J Immunol 169: 2486-2850.
21. Dang, C.V., and Lee, W.M. (1989) Nuclear and nucleolar targeting sequences of c-erb-A, c-myb, N-myc, p53, HSP70, and HIV tat proteins. J Biol Chem 264: 18019-18023.
22. Denkers, E.Y., and Gazzinelli, R.T. (1998) Regulation and function of T cell-mediated immunity during Toxoplasma gondii infection. Clin Microbiol Rev 11: 569-588.
23. Desjardins, M., and Descoteaux, A. (1997) Inhibition of phagolysosomal biogenesis by the Leishmania lipophosphoglycan. J Exp Med 185: 2061-2068.
24. Dhib-Jalbut, S., Xia, J., Rangaviggulaa, H., Fang, Y.Y., and Lee, T. (1999) Failure of measles virus to activate nuclear factor-kappa B in neuronal cells: implications on the immune response to viral infections in the central nervous system. J Immunol 162: 4024-4029.
25. Dobbin, C.A., Smith, N.C., and Johnson, A.M. (2002) Heat shock protein 70 is a potential virulence factor in murine Toxoplasma gondii infection via immunomodulation of host NF-kB and nitric oxide. J Immunol 169: 958-965.
26. Feinstein, D.L., Galea, E., Aquino, D.A., Li, G.C., Xu, H., and Reis, D.J. (1996) Heat shock protein 70 suppresses astroglial-inducible nitric-oxide synthase expression by decreasing NFkappaB activation. J Biol Chem 271: 17724-17732.
27. Feinstein, D.L., Galea, E., and Reis, D.J. (1997) Suppression of glial nitric oxide synthase induction by heat shock: effects on proteolytic degradation of IkappaB-alpha. Nitric Oxide 1: 167-176.
28. Gazzinelli, R.T., Hieny, S., Wynn, T., Wolf, S., and Sher, A. (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: 6115-6119.
29. + T cells and accompanied by overproduction of IL-12, IFN-γ, and TNF-α. J Immunol 157: 798-805.
30. Gorlich, D., and Mattaj, I.W. (1996) Nucleocytoplasmic transport. Science 271: 1513-1518.
31. Gorlich, D., Vogel, F., Mills, A.D., Hartmann, E., and Laskey, R. (1995) Distinct functions for the two importin subunits in nuclear protein import. Nature 377: 246-248.
32. Gustin, K.E., and Sarnow, P. (2001) Effects of poliovirus infection on nucleo-cytoplasmic trafficking and nuclear pore complex composition. EMBO J 20: 240-249.
33. + T cells through IL-12 produced by Listeria-induced macrophages. Science 260: 547-549.
34. Hunter, C.A., and Remington, J.S. (1994) Regulation of IL-12 and TNF-α induced NK cell production of IFN-γ by IL-1β and TGF-β. Eur Cytokine Network 5: 145.
35. Janeway, J., C.A., and Medzhitov, R. (2002) Innate immune recognition. Annu Rev Immunol 20: 197-216.
36. Joiner, K.A., Fuhrman, S.A., Miettinen, H.M., Kasper, L.H., and Mellman, I. (1990) Toxoplasma gondii: fusion competence of parasitophorous vacuoles in Fc receptor-transfected fibroblasts. Science 249: 641-646.
37. Kalinski, P., Hilkens, C.M.U., Wierenga, E.A., and Kapsenberg, M.L. (1999) T-cell priming by type-1 and type-2 polarized dendritic cells: the concept of a third signal. Immunol Today 20: 561-567.
38. Karin, M., and Ben-Neriah, Y. (2000) Phosphorylation meets ubiquitination: the control of NF-kB activity. Annu Rev Immunol 18: 621-663.
39. Kaye, P.M. (1995) Costimulation and the regulation of antimicrobial immunity. Immunol Today 16: 423-427.
40. Lee, F.S., Hagler, J., Chen, Z.J., and Maniatis, T. (1997) Activation of the IκBα kinase complex by MEKK1, a kinase of the JNK pathway. Cell 88: 213-222.
41. + 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: 597-607.
42. Liesenfeld, O., Kang, H., Park, D., Nguyen, T.A., Parkhe, C.V., Watanabe, H., et al. (1999) TNF-α, nitric oxide and IFN-γ are all critical for development of necrosis in the small intestine and early mortality in genetically susceptible mice infected perorally with Toxoplasma gondii. Parasite Immunol 21: 365-376.
43. Locksley, R.M. (1993) Interleukin 12 in host defense against microbial pathogens. Proc Natl Acad. Sci. USA 90: 5879-5880.
44. Luder, C.G.K., Lang, T., Beurle, B., and Gross, U. (1998) Down-regulation of MHC class II molecules and inability to up-regulate class I molecules in murine macrophages after infection with Toxoplasma gondii. Clin Exp Immunol 112: 308-316.
45. Luder, C.G.K., Walter, W., Beuerle, B., Maeurer, M.J., and Gross, U. (2001) Toxoplasma gondii down-regulates MHC class II gene expression and antigen presentation by murine macrophages via interference with nuclear translocation of STAT1α. Eur J Immunol 31: 1475-1484.
46. MacMicking, J.D., Nathan, C., Hom, G., Chartrain, N., Fletcher, D.S., Trumbauer, M., et al. (1995) Altered responses to bacterial infection and endotoxic shock in mice lacking inducible nitric oxide synthase. Cell 81: 641-650.
47. MacMicking, J., Xie, Q., and Nathan, C. (1997) Nitric oxide and macrophage function. Annu Rev Immunol 15: 323-350.
48. Malanin, N.L., Boldin, M.R., Kovalenko, A.V., and Wallach, D. (1997) MAP3K-related kinase involved in NF-κB induction by TNF, CD95 and IL-1. Nature 385: 540-544.
49. Maniatis, T. (1999) A ubiquitin ligase complex essential for the NF-kappaB, Wnt/Wingless, and Hedgehog signaling pathways. Genes Dev 13: 505-510.
50. Mason, N., Aliberti, J., Caamano, J.C., Liou, H.C., and Hunter, C.A. (2002) Identification of c-Rel-dependent and - independent pathways of IL-12 production during infectious and inflammatory stimuli. J Immunol 168: 2590-2594.
51. Matzinger, P. (2002) The danger model: a renewed sense of self. Science 296: 301-305.
52. McMahon-Pratt, D., Kima, P.E., and Soong, L. (1998) Leishmania amastigote target antigens: the challenge of a stealthy intracellular parasite. Parasitol Today 14: 31-34.
53. Melchoir, F., Paschal, B., Evans, J., and Gerace, L. (1993) Inhibition of nuclear protein import by nonhydrolyzable analogues of GTP and identification of the small GTPase Ran/TC4 as an essential transport factor. J Cell Biol 123: 1649-1659.
54. + T lymphocytes synergize with murine intestinal epithelial cells to enhance proinflammatory response against an intracellular pathogen. J Immunol 168: 2988-2996.
55. Mordue, D.G., Hakansson, S., Niesman, I., and Sibley, L.D. (1999) Toxoplasma gondii resides in a vacuole that avoids fusion with host cell endocytic and exocytic vesicular trafficking pathways. Exp Parasitol 92: 87-99.
56. c-rel. Mol Cel Biol 11: 5867-5877.
57. Nakielny, S., and Dreyfuss, G. (1999) Transport of proteins in and out of the nucleus. Cell 99: 677-690.
58. Neyer, L.E., Grunig, G., Fort, M., Remington, J.S., Rennick, D., and Hunter, C.A. (1997) Role of interleukin-10 in regulation of T-cell-dependent and T-cell-independent mechanisms of resistance to Toxoplasma gondii. Infect Immun 65: 1675-1682.
59. Orth, K., Palmer, L.E.B.Z.Q., Stewart, S., Rudolph, A.E., Bliska, J.B., and Dixon, J.E. (1999) Inhibition of the mitogen-activated protein kinase kinase superfamily by a Yersinia effector. Science 285: 1920-1923.
60. Revilla, Y., Callejo, M., Rodriquez, J.M., Culebras, E., Nogal, M.L., Sala, M.L., Vinuela, E., and Fresno, M. (1998) Inhibition of nuclear factor kB activation by a virus-encoded IκB-like protein. J Biol Chem 273: 5405-5411.
61. Roff, M., Thompson, J., Rodriguez, M.S., Jacque, J.-M., Baleux, F., Arenzana-Seisdedos, F., and Hay, R. (1996) Role of IκBα ubiquitination in signal-induced activation of NF-kB in vivo. J Biol Chem 271: 7844-7850.
62. Ruckdeschel, K., Mannel, O., Richter, K., Jacobi, C.A., Trulzsch, K., Rouot, B., and Heesemann, J. (2001) Yersinia outer membrane protein P of Yersinia enterocolitica simulataneously blocks the nuclear factor-kappa B pathway and exploits lipopolysaccharide signaling to trigger apoptosis in macrophages. J Immunol 166: 1823-1831.
63. Saccani, S., Pantano, S., and Natoli, G. (2001) Two waves of nuclear factor kB recruitment to target promoters. J Exp Med 193: 1351-1359.
64. Sanjabi, S., Hoffmann, A., Liou, H.C., Baltimore, D., and Smale, S.T. (2000) Selective requirement for c-Rel during IL-12 P40 gene induction in macrophages. Proc Natl Acad Sci USA 97: 12705-12710.
65. Scanga, C.A., Aliberti, J., Jankovic, D., Tilloy, F., Bennouna, S., Denkers, E.Y., Medzhitov, R., and Sher, A. (2002) Cutting edge: MyD88 is required for resistance to Toxoplasma gondii infection and regulates parasite-induced IL-12 production by dendritic cells. J Immunol 168: 5997-6001.
66. Scharton-Kersten, T.M., Wynn, T.A., Denkers, E.Y., Bala, S., Showe, L., Grunvald, E., et al. (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: 4045-4054.
67. Scharton-Kersten, T., Yap, G., Magram, J., and Sher, A. (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: 1-13.
68. Sen, R., and Baltimore, D. (1986) Inducibility of the immunoglobulin enhancer-binding protein NF-κB by posttranslational mechanisms. Cell 47: 921-928.
69. Shanley, T.P., Ryan, M.A., Eaves-Pyles, T., and Wong, H.R. (2000) Heat shock inhibits phosphorylation of I-kappaBalpha. Shock 14: 447-450.
70. Shapira, S.S., Speirs, K., Gerstein, A., Caamano, J., and Hunter, C.A. (2002) Suppression of NF-kB activation by infection with Toxoplasma gondii. J Infect Dis 185: S66-S72.
71. Snyder, Y.M., Guthrie, L., Evans, G.F., and Zuckerman, S.H. (1992) Transcriptional inhibition of endotoxin-induced monokine synthesis following heat shock in murine peritoneal macrophages. J Leukoc Biol 51: 181-187.
72. Spencer, E., Jiang, J., and Chen, Z.J. (1999) Signal-induced ubiquitination of I kappa B alpha by the F-box protein Slimb/beta-TrCP. Genes Dev 13: 284-294.
73. Suzuki, Y., Sher, A., Yap, G., Park, D., Ellis Neyer, L., Liesenfeld, O., et al. (2000) IL-10 is required for prevention of necrosis in the small intestine and mortality in both genetically resistant BALB/c and susceptible C57BL/6 mice following peroral infection with Toxoplasma gondii. J Immunol 164: 5375-5382.
74. Tato, C.M., and Hunter, C.A. (2002) Host-pathogen interactions: subversion and utilization of the NF-kB pathway during infection. Infect Immun 70: 3311-3317.
75. Taylor, G.A., Collazo, C.M., Yap, G.S., Nguyen, K., Gregorio, T.A., Taylor, L.S. et al. (2000) Pathogen-specific loss of host resistance in mice lacking the IFN-γ-inducible gene IGTP. Proc Natl Acad Sci USA 97: 751-755.
76. Vayssier, M., Favatier, F., Pinot, F., Bachelet, M., and Polla, B.S. (1998) Tobacco smoke induces coordinate activation of HSF and inhibition of NFkappaB in human monocytes: effects on TNFalpha release. Biochem Biophys Res Commun 252: 249-256.
77. Vazquez-Torres, A., and Fang, F.C. (2001) Oxygen-dependent anti-Salmonella activity of macrophages. Trends Microbiol 9: 29-33.
78. Welch, W.J., and Feramisco, J.R. (1984) Nuclear and nucleolar localization of the 72,000-dalton heat shock protein in heat-shocked mammalian cells. J Biol Chem 259: 4501-4513.
79. Winston, J.T., Strack, P., Beer-Romero, P., Chu, C.Y., Elledge, S.J., and Harper, J.W. (1999) The SCFbeta-TRCP-ubiquitin ligase complex associates specifically with phosphorylated destruction motifs in IkappaBalpha and beta-catenin and stimulates IkappaBalpha ubiquitination in vitro. Genes Dev 13: 270-283.
80. Wong, H.R., Ryan, M., and Wispe, J.R. (1997a) The heat shock response inhibits inducible nitric oxide synthase gene expression by blocking Iκ-B degradation and NF-κB nuclear translocation. Biochem Biophys Res Com 231: 257-263.
81. Wong, H.R., Ryan, M., and Wispe, J.R. (1997b) Stress response decreases NF-κB nuclear translocation and increases I-κBα expression in A549 cells. J Clin Invest 99: 2423-2428.
82. Yap, G.S., Scharton-Kersten, T., Charest, H., and Sher, A. (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: 1340-1345.
83. Yap, G.S., and Sher, A. (1999a) Cell-mediated immunity to Toxoplasma gondii: initiation, regulation and effector function. Immunobiology 201: 240-247.
84. Yap, G.S., and Sher, A. (1999b) 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: 1083-1091.
85. Ziegler-Heitbrock, L.H.W., Petersmann, I., and Frankenberger, M. (1997) p50 (NF-κB1) is upregulated in LPS tolerant P388D1 murine macrophages. Immunobiol 198: 73-80.