Toxoplasma gondii prevents chromatin remodeling initiated by TLR-triggered macrophage activation

Journal of Immunology

Volumn 182, Issue 1, 2009, Pages 489-497

  Leng, Jin ^a   Butcher, Barbara A ^a   Egan, Charlotte E ^a   Abi Abdallah, Delbert S ^a   Denkers, Eric Y ^a  

^a Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; DNA DIRECTED RNA POLYMERASE; HISTONE H3; LIGAND; LIPOPOLYSACCHARIDE; PROTEIN C JUN; TOLL LIKE RECEPTOR; TRANSCRIPTION FACTOR RELA; TUMOR NECROSIS FACTOR ALPHA; AUTACOID; HISTONE; RNA POLYMERASE II;

ACETYLATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CONTROLLED STUDY; CYTOKINE PRODUCTION; FEMALE; INFLAMMATION; MACROPHAGE ACTIVATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; TOXOPLASMA GONDII; TOXOPLASMOSIS; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CELL CULTURE; DRUG ANTAGONISM; ENZYMOLOGY; GENETICS; HUMAN; IMMUNOLOGY; MACROPHAGE; METABOLISM; PARASITOLOGY; PHOSPHORYLATION; PHYSIOLOGY; PROTEIN TRANSPORT; TOXOPLASMA;

ACETYLATION; ANIMALS; CELLS, CULTURED; CHROMATIN ASSEMBLY AND DISASSEMBLY; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; FEMALE; HISTONES; HUMANS; INFLAMMATION MEDIATORS; LIPOPOLYSACCHARIDES; MACROPHAGE ACTIVATION; MACROPHAGES; MICE; MICE, INBRED C57BL; PHOSPHORYLATION; PROMOTER REGIONS, GENETIC; PROTEIN TRANSPORT; PROTO-ONCOGENE PROTEINS C-JUN; RNA POLYMERASE II; TOLL-LIKE RECEPTORS; TOXOPLASMA; TRANSCRIPTION FACTOR RELA; TUMOR NECROSIS FACTOR-ALPHA;

EID: 59849096943     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.182.1.489     Document Type: Article

References (60)

1. Alexander, J., and C. A. Hunter. 1998. Immunoregulation during toxoplasmosis. Chem. Immunol. 70: 81-102.
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: 569-588.
3. + T cells and accompanied by overproduction of IL-12, IFN-γ, and TNF-α. J. Immunol. 157: 798-805.
4. Butcher, B. A., L. Kim, P. F. Johnson, and E. Y. Denkers. 2001. Toxoplasma gondii tachyzoites inhibit proinflammatory cytokine induction in infected macrophages by preventing nuclear translocation of the transcription factor NF-κB. J. Immunol. 167: 2193-2201.
5. Lee, C. W., S. Bennouna, and E. Y. Denkers. 2006. Screening for Toxoplasma gondii regulated transcriptional responses in LPS-activated macrophages. Infect. Immun. 74: 1916-1923.
6. Luder, C. G. K., M. Algner, C. Lang, N. Bleicher, and U. Gross. 2003. Reduced expression of the inducible nitric oxide synthase after infection with Toxoplasma gondii facilitates parasite replication in activated murine macrophages. Intl. J. Parasitol. 33: 833-844.
7. Lang, C., U. Gross, and C. G. Luder. 2007. Subversion of innate and adaptive immune responses by Toxoplasma gondii. Parasitol Res. 100: 191-203.
8. Denkers, E. Y., L. Kim, and B. A. Butcher. 2003. In the belly of the beast: subversion of macrophage proinflammatory signaling cascades during Toxoplasma gondii infection. Cell. Microbiol. 5: 75-83.
9. Kim, L., B. A. Butcher, and E. Y. Denkers. 2004. Toxoplasma gondii interferes with lipopolysaccharide-induced mitogen-activated protein kinase activation by mechanisms distinct from endotoxin tolerance. J. Immunol. 172: 3003-3010.
10. Shapira, S., O. Harb, J. Margarit, M. Matrajt, J. Han, A. Hoffmann, B. Freedman, M. J. May, D. S. Roos, and C. A. Hunter. 2005. Initiation and termination of NFκB signaling by the intracellular protozoan parasite Toxoplasma gondii. J. Cell Sci. 118: 3501-3508.
11. Butcher, B. A., L. Kim, A. Panopoulos, S. S. Watowich, P. J. Murray, and E. Y. Denkers. 2005. Cutting edge: IL-10-independent STAT3 activation by Toxoplasma gondii mediates suppression of IL-12 and TNF-α in host macrophages. J. Immunol. 174: 3148-3152.
12. Saeij, J. P., S. Coller, J. P. Boyle, M. E. Jerome, M. W. White, and J. C. Boothroyd. 2007. Toxoplasma co-opts host gene expression by injection of a polymorphic kinase homologue. Nature 445: 324-327.
13. Denkers, E. Y., B. A. Butcher, L. Del Rio, and L. Kim. 2004. Manipulation of mitogen-activated protein kinase/nuclear factor-κB-signaling cascades during intracellular Toxoplasma gondii infection. Immunol. Rev. 201: 191-205.
14. Butcher, B. A., and E. Y. Denkers. 2002. Mechanism of entry determines ability of Toxoplasma gondii to inhibit macrophage proinflammatory cytokine production. Infect. Immun. 70: 5216-5224.
15. Falvo, J. V., B. M. Brinkman, A. V. Tsytsykova, E. Y. Tsai, T. P. Yao, A. L. Kung, and A. E. Goldfeld. 2000. A stimulus-specific role for CREB-binding protein (CBP) in T cell receptor-activated tumor necrosis factor α gene expression. Proc. Natl. Acad. Sci. USA 97: 3925-3929.
16. Falvo, J. V., A. M. Uglialoro, B. M. Brinkman, M. Merika, B. S. Parekh, E. Y. Tsai, H. C. King, A. D. Morielli, E. G. Peralta, T. Maniatis, et al. 2000. Stimulus-specific assembly of enhancer complexes on the tumor necrosis factor α gene promoter. Mol. Cell. Biol. 20: 2239-2247.
17. Tsai, E. Y., J. V. Falvo, A. V. Tsytsykova, A. K. Barczak, A. M. Reimold, L. H. Glimcher, M. J. Fenton, D. C. Gordon, I. F. Dunn, and A. E. Goldfeld. 2000. A lipopolysaccharide-specific enhancer complex involving Ets, Elk-1, Sp1, and CREB binding protein and p300 is recruited to the tumor necrosis factor α promoter in vivo. Mol. Cell. Biol. 20: 6084-6094.
18. Goldfeld, A. E., and T. Maniatis. 1989. Coordinate viral induction of tumor necrosis factor α and interferon β in human B cells and monocytes. Proc. Natl. Acad. Sci. USA 86: 1490-1494.
19. Tsytsykova, A. V., and A. E. Goldfeld. 2002. Inducer-specific enhanceosome formation controls tumor necrosis factor α gene expression in T lymphocytes. Mol. Cell. Biol. 22: 2620-2631.
20. Kuprash, D. V., I. A. Udalova, R. L. Turetskaya, D. Kwiatkowski, N. R. Rice, and S. A. Nedospasov. 1999. Similarities and differences between human and murine TNF promoters in their response to lipopolysaccharide. J. Immunol. 162: 4045-4052.
21. Osman, F., N. Jarrous, Y. Ben-Asouli, and R. Kaempfer. 1999. A cis-acting element in the 3′-untranslated region of human TNF-α mRNA renders splicing dependent on the activation of protein kinase PKR. Genes Dev. 13: 3280-3293.
22. Dumitru, C. D., J. D. Ceci, C. Tsatsanis, D. Kontoyiannis, K. Stamatakis, J. H. Lin, C. Patriotis, N. A. Jenkins, N. G. Copeland, G. Kollias, and P. N. Tsichlis. 2000. TNF-α induction by LPS is regulated posttranscriptionally via a Tpl2/ERK-dependent pathway. Cell 103: 1071-1083.
23. Lee, J. Y., N. A. Kim, A. Sanford, and K. E. Sullivan. 2003. Histone acetylation and chromatin conformation are regulated separately at the TNF-α promoter in monocytes and macrophages. J. Leukocyte Biol. 73: 862-871.
24. Garrett, S., K. Dietzmann-Maurer, L. Song, and K. E. Sullivan. 2008. Polarization of primary human monocytes by IFN-γ induces chromatin changes and recruits RNA PolII to the TNF-α promoter. J. Immunol. 180: 5257-5266.
25. Sullivan, K. E., A. B. Reddy, K. Dietzmann, A. R. Suriano, V. P. Kocieda, M. Stewart, and M. Bhatia. 2007. Epigenetic regulation of tumor necrosis factor α. Mol. Cell. Biol. 27: 5147-5160.
26. Shivaswamy, S., A. Bhinge, Y. Zhao, S. Jones, M. Hirst, and V. R. Iyer. 2008. Dynamic remodeling of individual nucleosomes across a eukaryotic genome in response to transcriptional perturbation. PLoS Biol. 6: e65.
27. Berger, S. L. 2007. The complex language of chromatin regulation during transcription. Nature 447: 407-412.
28. Ait-Si-Ali, S., S. Ramirez, F. X. Barre, F. Dkhissi, L. Magnaghi-Jaulin, J. A. Girault, P. Robin, M. Knibiehler, L. L. Pritchard, B. Ducommun, et al. 1998. Histone acetyltransferase activity of CBP is controlled by cycle-dependent kinases and oncoprotein E1A. Nature 396: 184-186.
29. Martinez-Balbas, M. A., A. J. Bannister, K. Martin, P. Haus-Seuffert, M. Meisterernst, and T. Kouzarides. 1998. The acetyltransferase activity of CBP stimulates transcription. EMBO J. 17: 2886-2893.
30. Li, B., M. Carey, and J. L. Workman. 2007. The role of chromatin during transcription. Cell 128: 707-719.
31. Dyson, M. H., S. Thomson, M. Inagaki, H. Goto, S. J. Arthur, K. Nightingale, F. J. Iborra, and L. C. Mahadevan. 2005. MAP kinase-mediated phosphorylation of distinct pools of histone H3 at S10 or S28 via mitogen- and stress-activated kinase 1/2. J. Cell Sci. 118: 2247-2259.
32. Soloaga, A., S. Thomson, G. R. Wiggin, N. Rampersaud, M. H. Dyson, C. A. Hazzalin, L. C. Mahadevan, and J. S. Arthur. 2003. MSK2 and MSK1 mediate the mitogen- and stress-induced phosphorylation of histone H3 and HMG-14. EMBO J. 22: 2788-2797.
33. Rosenberger, C. M., and B. B. Finlay. 2003. Phagocyte sabotage: disruption of macrophage signalling by bacterial pathogens. Nat. Rev. Mol. Cell Biol. 4: 385-396.
34. Sacks, D., and A. Sher. 2002. Evasion of innate immunity by parasitic protozoa. Nat. Immunol. 3: 1041-1047.
35. Muegge, K. 2002. Preparing the target for the bullet. Nat. Immunol. 3: 16-17.
36. Cheung, P., C. D. Allis, and P. Sassone-Corsi. 2000. Signaling to chromatin through histone modifications. Cell 103: 263-271.
37. Jenuwein, T., and C. D. Allis. 2001. Translating the histone code. Science 293: 1074-1080.
38. Saccani, S., S. Pantano, and G. Natoli. 2002. p38-Dependent marking of inflammatory genes for increased NF-κB recruitment. Nat. Immunol. 3: 69-75.
39. Hamon, M. A., E. Batsche, B. Regnault, T. N. Tham, S. Seveau, C. Muchardt, and P. Cossart. 2007. Histone modifications induced by a family of bacterial toxins. Proc. Natl. Acad. Sci. USA 104: 13467-13472.
40. Wang, Y., H. M. Curry, B. S. Zwilling, and W. P. Lafuse. 2005. Mycobacteria inhibition of IFN-γ induced HLA-DR gene expression by up-regulating histone deacetylation at the promoter region in human THP-1 monocytic cells. J. Immunol. 174: 5687-5694.
41. Pennini, M. E., R. K. Pai, D. C. Schultz, W. H. Boom, and C. V. Harding. 2006. Mycobacterium tuberculosis 19-kDa lipoprotein inhibits IFN-γ-induced chromatin remodeling of MHC2TA by TLR2 and MAPK signaling. J. Immunol. 176: 4323-4330.
42. Arbibe, L., D. W. Kim, E. Batsche, T. Pedron, B. Mateescu, C. Muchardt, C. Parsot, and P. J. Sansonetti. 2007. An injected bacterial effector targets chromatin access for transcription factor NF-κB to alter transcription of host genes involved in immune responses. Nat. Immunol. 8: 47-56.
43. Cheung, P., K. G. Tanner, W. L. Cheung, P. Sassone-Corsi, J. M. Denu, and C. D. Allis. 2000. Synergistic coupling of histone H3 phosphorylation and acetylation in response to epidermal growth factor stimulation. Mol. Cell 5: 905-915.
44. Lo, W. S., R. C. Trievel, J. R. Rojas, L. Duggan, J. Y. Hsu, C. D. Allis, R. Marmorstein, and S. L. Berger. 2000. Phosphorylation of serine 10 in histone H3 is functionally linked in vitro and in vivo to Gcn5-mediated acetylation at lysine 14. Mol. Cell 5: 917-926.
45. Zhang, X., J. P. Edwards, and D. M. Mosser. 2006. Dynamic and transient remodeling of the macrophage IL-10 promoter during transcription. J. Immunol. 177: 1282-1288.
46. Shapira, S. S., K. Speirs, A. Gerstein, J. Caamano, and C. A. Hunter. 2002. Suppression of NF-κB activation by infection with Toxoplasma gondii. J. Infect. Dis. 185: S66-S72.
47. Ravindran, S., and J. C. Boothroyd. 2008. Secretion of proteins into host cells by Apicomplexan parasites. Traffic 9: 647-656.
48. Gilbert, L. A., S. Ravindran, J. M. Turetzky, J. C. Boothroyd, and P. J. Bradley. 2007. Toxoplasma gondii targets a protein phosphatase 2C to the nuclei of infected host cells. Eukaryot. Cell 6: 73-83.
49. Laliberte, J., and V. B. Carruthers. 2008. Host cell manipulation by the human pathogen Toxoplasma gondii. Cell. Mol. Life Sci. 65: 1900-1915.
50. Debierre-Grockiego, F., M. A. Campos, N. Azzouz, J. Schmidt, U. Bieker, M. G. Resende, D. S. Mansur, R. Weingart, R. R. Schmidt, D. T. Golenbock, et al. 2007. Activation of TLR2 and TLR4 by glycosylphosphatidylinositols derived from Toxoplasma gondii. J. Immunol. 179: 1129-1137.
51. Yarovinsky, F., D. Zhang, J. F. Anderson, G. L. Bannenberg, C. N. Serhan, M. S. Hayden, S. Hieny, F. S. Sutterwala, R. A. Flavell, S. Ghosh, and A. Sher. 2005. TLR11 activation of dendritic cells by a protozoan profilin-like protein. Science 308: 1626-1629.
52. Plattner, F., F. Yarovinsky, S. Romero, D. Didry, M. F. Carlier, A. Sher, and D. Soldati-Favre. 2008. Toxoplasma profilin is essential for host cell invasion and TLR dependent induction of interleukin-12. Cell Host Microbes 14: 77-87.
53. Wichroski, M. J., and G. E. Ward. 2003. Biosynthesis of glycosylphosphatidylinositol is essential to the survival of the protozoan parasite Toxoplasma gondii. Eukaryot. Cell 2: 1132-1136.
54. Mukherjee, S., G. Keitany, Y. Li, Y. Wang, H. L. Ball, E. J. Goldsmith, and K. Orth. 2006. Yersinia YopJ acetylates and inhibits kinase activation by blocking phosphorylation. Science 312: 1211-1214.
55. 2-terminal kinase. J. Biol. Chem. 272: 15920-15927.
56. Ruckdeschel, K., O. Mannel, K. Richter, C. A. Jacobi, K. Trulzsch, B. Rouot, and J. Heesemann. 2001. Yersinia outer protein P of Yersinia enterocolitica simultaneously blocks the nuclear factor-κB pathway and exploits lipopolysaccharide signaling to trigger apoptosis. J. Immunol. 166: 1823-1831.
57. Viboud, G. I., and J. B. Bliska. 2005. Yersinia outer proteins: role in modulation of host cell signaling responses and pathogenesis. Annu. Rev. Microbiol. 59: 69-89.
58. Park, J. M., F. R. Greten, Z.-W. Li, and M. Karin. 2002. Macrophage apoptosis by anthrax lethal factor through p38 MAP kinase inhibition. Science 297: 2048-2051.
59. Kim, S. K., A. E. Fouts, and J. C. Boothroyd. 2007. Toxoplasma gondii dysregulates IFN-γ-inducible gene expression in human fibroblasts: insights from a genome-wide transcriptional profiling. J. Immunol. 178: 5154-5165.
60. Luder, C. G. K., W. Walter, B. Beuerle, M. J. Maeurer, and U. Gross. 2001. Toxoplasma gondii down-regulates MHC class II gene expression and antigen presentation by murine macrophages via interference with nuclear translocation of STAT1a. Eur. J. Immunol. 31: 1475-1484.