Journal of Neuroimmunology
Volume 222, Issue 1 , Pages 19-28 , May 2010

NF-κB1 contributes to T cell-mediated control of Toxoplasma gondii in the CNS

Received 17 November 2009 ,Revised 18 December 2009 ,Accepted 18 December 2009.

References 

  1. Artis D, Kane CM, Fiore J, Zaph C, Shapira S, Joyce K, et al. Dendritic cell-intrinsic expression of NF-kappa B1 is required to promote optimal Th2 cell differentiation. J Immunol. 2005;174:7154–7159
  2. Artis D, Shapira S, Mason N, Speirs KM, Goldschmidt M, Caamano J, et al. Differential requirement for NF-kappa B family members in control of helminth infection and intestinal inflammation. J Immunol. 2002;169:4481–4487
  3. Artis D, Speirs K, Joyce K, Goldschmidt M, Caamano J, Hunter CA, et al. NF-kappa B1 is required for optimal CD4+ Th1 cell development and resistance to Leishmania major. J Immunol. 2003;170:1995–2003
  4. Barber DL, Wherry EJ, Masopust D, Zhu B, Allison JP, Sharpe AH, et al. Restoring function in exhausted CD8 T cells during chronic viral infection. Nature. 2006;439:682–687
  5. Beinke S, Ley SC. Functions of NF-kappaB1 and NF-kappaB2 in immune cell biology. Biochem J. 2004;382:393–409
  6. Blanchard N, Gonzalez F, Schaeffer M, Joncker NT, Cheng T, Shastri AJ, et al. Immunodominant, protective response to the parasite Toxoplasma gondii requires antigen processing in the endoplasmic reticulum. Nat Immunol. 2008;9:937–944
  7. Butcher BA, Kim L, Johnson PF, Denkers EY. Toxoplasma gondii tachyzoites inhibit proinflammatory cytokine induction in infected macrophages by preventing nuclear translocation of the transcription factor NF-kappa B. J Immunol. 2001;167:2193–2201
  8. Caamano J, Alexander J, Craig L, Bravo R, Hunter CA. The NF-kappa B family member RelB is required for innate and adaptive immunity to Toxoplasma gondii. J Immunol. 1999;163:4453–4461
  9. Caamano J, Tato C, Cai G, Villegas EN, Speirs K, Craig L, et al. Identification of a role for NF-kappa B2 in the regulation of apoptosis and in maintenance of T cell-mediated immunity to Toxoplasma gondii. J Immunol. 2000;165:5720–5728
  10. Cao S, Zhang X, Edwards JP, Mosser DM. NF-kappaB1 (p50) homodimers differentially regulate pro- and anti-inflammatory cytokines in macrophages. J Biol Chem. 2006;281:26041–26050
  11. Corn RA, Aronica MA, Zhang F, Tong Y, Stanley SA, Kim SR, et al. T cell-intrinsic requirement for NF-kappa B induction in postdifferentiation IFN-gamma production and clonal expansion in a Th1 response. J Immunol. 2003;171:1816–1824
  12. Deckert-Schluter M, Bluethmann H, Rang A, Hof H, Schluter D. Crucial role of TNF receptor type 1 (p55), but not of TNF receptor type 2 (p75), in murine toxoplasmosis. J Immunol. 1998;160:3427–3436
  13. Gazzinelli R, Xu Y, Hieny S, Cheever A, Sher A. Simultaneous depletion of CD4+ and CD8+ T lymphocytes is required to reactivate chronic infection with Toxoplasma gondii. J Immunol. 1992;149:175–180
  14. Gazzinelli RT, Eltoum I, Wynn TA, Sher A. Acute cerebral toxoplasmosis is induced by in vivo neutralization of TNF-alpha and correlates with the down-regulated expression of inducible nitric oxide synthase and other markers of macrophage activation. J Immunol. 1993;151:3672–3681
  15. Gazzinelli RT, Wysocka M, Hayashi S, Denkers EY, Hieny S, Caspar P, et al. Parasite-induced IL-12 stimulates early IFN-gamma synthesis and resistance during acute infection with Toxoplasma gondii. J Immunol. 1994;153:2533–2543
  16. Hill DE, Chirukandoth S, Dubey JP. Biology and epidemiology of Toxoplasma gondii in man and animals. Anim. Health Res. Rev. 2005;6:41–61
  17. Hilliard B, Samoilova EB, Liu TS, Rostami A, Chen Y. Experimental autoimmune encephalomyelitis in NF-kappa B-deficient mice: roles of NF-kappa B in the activation and differentiation of autoreactive T cells. J Immunol. 1999;163:2937–2943
  18. Hilliard BA, Mason N, Xu L, Sun J, Lamhamedi-Cherradi SE, Liou HC, et al. Critical roles of c-Rel in autoimmune inflammation and helper T cell differentiation. J Clin Invest. 2002;110:843–850
  19. Hunter CA, Remington JS. Immunopathogenesis of toxoplasmic encephalitis. J Infect Dis. 1994;170:1057–1067
  20. Karin M, Yamamoto Y, Wang QM. The IKK NF-kappa B system: a treasure trove for drug development. Nat Rev Drug Discov. 2004;3:17–26
  21. Li Q, Verma IM. NF-kappaB regulation in the immune system. Nat Rev Immunol. 2002;2:725–734
  22. Lieberman LA, Banica M, Reiner SL, Hunter CA. STAT1 plays a critical role in the regulation of antimicrobial effector mechanisms, but not in the development of Th1-type responses during toxoplasmosis. J Immunol. 2004;172:457–463
  23. Liu CH, Fan YT, Dias A, Esper L, Corn RA, Bafica A, et al. Cutting edge: dendritic cells are essential for in vivo IL-12 production and development of resistance against Toxoplasma gondii infection in mice. J Immunol. 2006;177:31–35
  24. Luft BJ, Remington JS. AIDS commentary. Toxoplasmic encephalitis. J Infect Dis. 1988;157:1–6
  25. Luft BJ, Remington JS. Toxoplasmic encephalitis in AIDS. Clin Infect Dis. 1992;15:211–222
  26. Mason N, Aliberti J, Caamano JC, Liou HC, Hunter CA. Cutting edge: identification of c-Rel-dependent and -independent pathways of IL-12 production during infectious and inflammatory stimuli. J Immunol. 2002;168:2590–2594
  27. Mason NJ, Artis D, Hunter CA. New lessons from old pathogens: what parasitic infections have taught us about the role of nuclear factor-kappaB in the regulation of immunity. Immunol Rev. 2004;201:48–56
  28. Mason NJ, Liou HC, Hunter CA. T cell-intrinsic expression of c-Rel regulates Th1 cell responses essential for resistance to Toxoplasma gondii. J Immunol. 2004;172:3704–3711
  29. May MJ, Ghosh S. Rel/NF-kappa B and I kappa B proteins: an overview. Semin Cancer Biol. 1997;8:63–73
  30. Sander B, Cardell S, Heremans H, Andersson U, Moller G. Detection of individual interleukin 4- and gamma interferon-producing murine spleen cells after activation with T-cell mitogens. Scand J Immunol. 1989;30:315–320
  31. Sanjabi S, Hoffmann A, Liou HC, Baltimore D, Smale ST. Selective requirement for c-Rel during IL-12 P40 gene induction in macrophages. Proc Natl Acad Sci U S A. 2000;97:12705–12710
  32. Scanga CA, Aliberti J, Jankovic D, Tilloy F, Bennouna S, Denkers EY, et al. Cutting edge: MyD88 is required for resistance to Toxoplasma gondii infection and regulates parasite-induced IL-12 production by dendritic cells. J Immunol. 2002;168:5997–6001
  33. Scharton-Kersten T, Denkers EY, Gazzinelli R, Sher A. Role of IL12 in induction of cell-mediated immunity to Toxoplasma gondii. Res Immunol. 1995;146:539–545
  34. Scharton-Kersten TM, Wynn TA, Denkers EY, Bala S, Grunvald E, Hieny S, et al. In the absence of endogenous IFN-gamma, mice develop unimpaired IL-12 responses to Toxoplasma gondii while failing to control acute infection. J Immunol. 1996;157:4045–4054
  35. Scharton-Kersten TM, Yap G, Magram J, Sher A. Inducible nitric oxide is essential for host control of persistent but not acute infection with the intracellular pathogen Toxoplasma gondii. J Exp Med. 1997;185:1261–1273
  36. Schluter D, Deckert-Schluter M, Lorenz E, Meyer T, Rollinghoff M, Bogdan C. Inhibition of inducible nitric oxide synthase exacerbates chronic cerebral toxoplasmosis in Toxoplasma gondii-susceptible C57BL/6 mice but does not reactivate the latent disease in T. gondii-resistant BALB/c mice. J Immunol. 1999;162:3512–3518
  37. Scholzen T, Gerdes J. The Ki-67 protein: from the known and the unknown. J Cell Physiol. 2000;182:311–322
  38. Schwarz EM, Badorff C, Hiura TS, Wessely R, Badorff A, Verma IM, et al. NF-kappaB-mediated inhibition of apoptosis is required for encephalomyocarditis virus virulence: a mechanism of resistance in p50 knockout mice. J Virol. 1998;72:5654–5660
  39. Sha WC, Liou HC, Tuomanen EI, Baltimore D. Targeted disruption of the p50 subunit of NF-kappa B leads to multifocal defects in immune responses. Cell. 1995;80:321–330
  40. Shapira S, Harb OS, Margarit J, Matrajt M, Han J, Hoffmann A, et al. Initiation and termination of NF-kappaB signaling by the intracellular protozoan parasite Toxoplasma gondii. J Cell Sci. 2005;118:3501–3508
  41. Shapira S, Speirs K, Gerstein A, Caamano J, Hunter CA. Suppression of F-kappaB activation by infection with Toxoplasma gondii. J Infect Dis. 2002;185(Suppl 1):S66–S72
  42. Sibley LD, Adams LB, Fukutomi Y, Krahenbuhl JL. Tumor necrosis factor-alpha triggers antitoxoplasmal activity of IFN-gamma primed macrophages. J Immunol. 1991;147:2340–2345
  43. Snapper CM, Zelazowski P, Rosas FR, Kehry MR, Tian M, Baltimore D, et al. B cells from p50/NF-kappa B knockout mice have selective defects in proliferation, differentiation, germ-line CH transcription, and Ig class switching. J Immunol. 1996;156:183–191
  44. Sriskantharajah S, Belich MP, Papoutsopoulou S, Janzen J, Tybulewicz V, Seddon B, et al. Proteolysis of NF-kappaB1 p105 is essential for T cell antigen receptor-induced proliferation. Nat. Immunol. 2009;10:38–47
  45. Suzuki Y, Conley FK, Remington JS. Importance of endogenous IFN-gamma for prevention of toxoplasmic encephalitis in mice. J Immunol. 1989;143:2045–2050
  46. Suzuki Y, Orellana MA, Schreiber RD, Remington JS. Interferon-gamma: the major mediator of resistance against Toxoplasma gondii. Science. 1988;240:516–518
  47. Tato CM, Hunter CA. Host–pathogen interactions: subversion and utilization of the NF-kappa B pathway during infection. Infect. Immun. 2002;70:3311–3317
  48. Tato CM, Mason N, Artis D, Shapira S, Caamano JC, Bream JH, et al. Opposing roles of NF-kappaB family members in the regulation of NK cell proliferation and production of IFN-gamma. Int Immunol. 2006;18:505–513
  49. Tato CM, Villarino A, Caamano JH, Boothby M, Hunter CA. Inhibition of NF-kappa B activity in T and NK cells results in defective effector cell expansion and production of IFN-gamma required for resistance to Toxoplasma gondii. J Immunol. 2003;170:3139–3146
  50. Taylor GA, Feng CG, Sher A. p47 GTPases: regulators of immunity to intracellular pathogens. Nat Rev Immunol. 2004;4:100–109
  51. Wilson EH, Hunter CA. The role of astrocytes in the immunopathogenesis of toxoplasmic encephalitis. Int J Parasitol. 2004;34:543–548
  52. Wilson EH, Wille-Reece U, Dzierszinski F, Hunter CA. A critical role for IL-10 in limiting inflammation during toxoplasmic encephalitis. J Neuroimmunol. 2005;165:63–74
  53. Yap GS, Scharton-Kersten T, Charest H, Sher A. 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. 1998;160:1340–1345
  54. Zhang G, Ghosh S. Toll-like receptor-mediated NF-kappaB activation: a phylogenetically conserved paradigm in innate immunity. J Clin Invest. 2001;107:13–19

PII: S0165-5728(10)00002-0

doi: 10.1016/j.jneuroim.2009.12.009

Journal of Neuroimmunology
Volume 222, Issue 1 , Pages 19-28 , May 2010