Toxoplasma gondii TgIST co-opts host chromatin repressors dampening STAT1-dependent gene regulation and IFN-γ-mediated host defenses

Journal of Experimental Medicine

Volumn 213, Issue 9, 2016, Pages 1779-1798

  Gay, Gabrielle ^a   Braun, Laurence ^a   Brenier Pinchart, Marie Pierre ^a   Vollaire, Julien ^c   Josserand, Véronique ^c   Bertini, Rose Laurence ^a   Varesano, Aurélie ^a   Touquet, Bastien ^b   De Bock, Pieter Jan ^d   Coute, Yohann ^d   Tardieux, Isabelle ^b   Bougdour, Alexandre ^a   Hakimi, Mohamed Ali ^a  

^a INSTITUTE FOR ADVANCED BIOSCIENCES   (France)

^b UNIV GRENOBLE ALPES   (France)

^c IAB Grenoble   (France)

^d DIF   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ENZYME; GAMMA INTERFERON; INTERFERON REGULATORY FACTOR 1; INTERLEUKIN 12; INTERLEUKIN 1BETA; INTERLEUKIN 6; NUCLEOSOME REMODELING DEACETYLASE; STAT1 PROTEIN; TOXOPLASMA GONDII INHIBITOR OF STAT1; UNCLASSIFIED DRUG; CHROMATIN; IRF1 PROTEIN, MOUSE; PROTOZOAL PROTEIN; STAT1 PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; BINDING SITE; CONTROLLED STUDY; ECTOPIC EXPRESSION; GENE CONTROL; GENE EXPRESSION; GENE LOCUS; GENETIC TRANSCRIPTION; HOST RESISTANCE; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; TOXOPLASMOSIS; ANIMAL; ANTAGONISTS AND INHIBITORS; BAGG ALBINO MOUSE; CHROMATIN; GENE EXPRESSION REGULATION; MACROPHAGE; MONOCYTE; PHOSPHORYLATION; PHYSIOLOGY; PROMOTER REGION; TOXOPLASMA;

ANIMALS; CHROMATIN; GENE EXPRESSION REGULATION; INTERFERON REGULATORY FACTOR-1; INTERFERON-GAMMA; MACROPHAGES; MICE; MICE, INBRED BALB C; MONOCYTES; PHOSPHORYLATION; PROMOTER REGIONS, GENETIC; PROTOZOAN PROTEINS; STAT1 TRANSCRIPTION FACTOR; TOXOPLASMA;

EID: 84984850905     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20160340     Document Type: Article

References (51)

1. Bekpen, C., J.P. Hunn, C. Rohde, I. Parvanova, L. Guethlein, D.M. Dunn, E. Glowalla, M. Leptin, and J.C. Howard. 2005. The interferon-inducible p47 (IRG) GTPases in vertebrates: loss of the cell autonomous resistance mechanism in the human lineage. Genome Biol. 6:R92. http://dx.doi.org/10.1186/gb -2005-6-11-r92
2. Bougdour, A., E. Durandau, M.-P. Brenier-Pinchart, P. Ortet, M. Barakat, S. Kieffer, A. Curt-Varesano, R.-L. Curt-Bertini, O. Bastien, Y. Coute, et al. 2013. Host cell subversion by Toxoplasma GRA16, an exported dense granule protein that targets the host cell nucleus and alters gene expression. Cell Host Microbe. 13:489-500. http://dx.doi.org/10.1016/j.chom.2013.03.002
3. Braun, L., M.-P. Brenier-Pinchart, M. Yogavel, A. Curt-Varesano, R.-L. Curt-Bertini, T. Hussain, S. Kieffer-Jaquinod, Y. Coute, H. Pelloux, I. Tardieux, et al. 2013. A Toxoplasma dense granule protein, GRA24, modulates the early immune response to infection by promoting a direct and sustained host p38 MAPK activation. J. Exp. Med. 210:2071-2086. http://dx.doi.org/10.1084/jem.20130103
4. Chinnadurai, G. 2002. CtBP, an unconventional transcriptional corepressor in development and oncogenesis. Mol. Cell. 9:213-224. http://dx.doi.org/10.1016/S1097-2765(02)00443-4
5. Coffey, M.J., B.E. Sleebs, A.D. Uboldi, A. Garnham, M. Franco, N.D. Marino, M.W. Panas, D.J. Ferguson, M. Enciso, M.T. O'Neill, et al. 2015. An aspartyl protease defines a novel pathway for export of Toxoplasma proteins into the host cell. eLife. 4:e10809. http://dx.doi.org/10.7554/eLife.10809
6. Collazo, C.M., G.S. Yap, S. Hieny, P. Caspar, C.G. Feng, G.A. Taylor, and A. Sher. 2002. The function of gamma interferon-inducible GTP-binding protein IGTP in host resistance to Toxoplasma gondii is Stat1 dependent and requires expression in both hematopoietic and nonhematopoietic cellular compartments. Infect. Immun. 70:6933-6939. http://dx.doi.org/10.1128/IAI.70.12.6933-6939.2002
7. Curt-Varesano, A., L. Braun, C. Ranquet, M.-A. Hakimi, and A. Bougdour. 2016. The aspartyl protease TgASP5 mediates the export of the Toxoplasma GRA16 and GRA24 effectors into host cells. Cell. Microbiol. 18:151-167. http://dx.doi.org/10.1111/cmi.12498
8. Dunay, I.R., R.A. Damatta, B. Fux, R. Presti, S. Greco, M. Colonna, and L.D. Sibley. 2008. Gr1+ inflammatory monocytes are required for mucosal resistance to the pathogen Toxoplasma gondii. Immunity. 29:306-317. http://dx.doi.org/10.1016/j.immuni.2008.05.019
9. Etheridge, R.D., A. Alaganan, K. Tang, H.J. Lou, B.E. Turk, and L.D. Sibley. 2014. The Toxoplasma pseudokinase ROP5 forms complexes with ROP18 and ROP17 kinases that synergize to control acute virulence in mice. Cell Host Microbe. 15:537-550. http://dx.doi.org/10.1016/j.chom.2014.04.002
10. Gavrilescu, L.C., B.A. Butcher, L. Del Rio, G.A. Taylor, and E.Y. Denkers. 2004. STAT1 is essential for antimicrobial effector function but dispensable for gamma interferon production during Toxoplasma gondii infection. Infect. Immun. 72:1257-1264. http://dx.doi.org/10.1128/IAI.72.3.1257-1264.2004
11. Hakimi, M.-A., and A. Bougdour. 2015. Toxoplasma's ways of manipulating the host transcriptome via secreted effectors. Curr. Opin. Microbiol. 26:24-31. http://dx.doi.org/10.1016/j.mib.2015.04.003
12. Honda, K., and T. Taniguchi. 2006. IRFs: master regulators of signalling by Toll-like receptors and cytosolic pattern-recognition receptors. Nat. Rev. Immunol. 6:644-658. http://dx.doi.org/10.1038/nri1900
13. Howard, J.C., J.P. Hunn, and T. Steinfeldt. 2011. The IRG protein-based resistance mechanism in mice and its relation to virulence in Toxoplasma gondii. Curr. Opin. Microbiol. 14:414-421. http://dx.doi.org/10.1016/j.mib.2011.07.002
14. 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. http://dx.doi.org/10.4049/jimmunol.178.8.5154
15. Krämer, O.H., and T. Heinzel. 2010. Phosphorylation-acetylation switch in the regulation of STAT1 signaling. Mol. Cell. Endocrinol. 315:40-48. http://dx.doi.org/10.1016/j.mce.2009.10.007
16. Kravets, E., D. Degrandi, Q. Ma, T.-O. Peulen, V. Klümpers, S. Felekyan, R. Kühnemuth, S. Weidtkamp-Peters, C.A. Seidel, and K. Pfeffer. 2016. Guanylate binding proteins directly attack Toxoplasma gondii via supramolecular complexes. eLife. 5:e11479. http://dx.doi.org/10.7554/eLife.11479
17. Lang, C., A. Hildebrandt, F. Brand, L. Opitz, H. Dihazi, and C.G.K. Lüder. 2012. Impaired chromatin remodelling at STAT1-regulated promoters leads to global unresponsiveness of Toxoplasma gondii-infected macrophages to IFN-γ. PLoS Pathog. 8:e1002483. http://dx.doi.org/10.1371/journal.ppat.1002483
18. Liu, B., S. Mink, K.A. Wong, N. Stein, C. Getman, P.W. Dempsey, H. Wu, and K. Shuai. 2004. PIAS1 selectively inhibits interferon-inducible genes and is important in innate immunity. Nat. Immunol. 5:891-898. http://dx.doi.org/10.1038/ni1104
19. Lüder, C.G., C. Lang, M. Giraldo-Velasquez, M. Algner, J. Gerdes, and U. Gross. 2003. Toxoplasma gondii inhibits MHC class II expression in neural antigen-presenting cells by down-regulating the class II transactivator CII TA. J. Neuroimmunol. 134:12-24. http://dx.doi.org/10.1016/S0165-5728(02)00320-X
20. Martens, S., I. Parvanova, J. Zerrahn, G. Griffiths, G. Schell, G. Reichmann, and J.C. Howard. 2005. Disruption of Toxoplasma gondii parasitophorous vacuoles by the mouse p47-resistance GTPases. PLoS Pathog. 1:e24. http://dx.doi.org/10.1371/journal.ppat.0010024
21. Matsumura, Y., R. Nakaki, T. Inagaki, A. Yoshida, Y. Kano, H. Kimura, T. Tanaka, S. Tsutsumi, M. Nakao, T. Doi, et al. 2015. H3K4/H3K9me3 bivalent chromatin domains targeted by lineage-specific DNA methylation pauses adipocyte differentiation. Mol. Cell. 60:584-596. http://dx.doi.org/10.1016/j.molcel.2015.10.025
22. McKendry, R., J. John, D. Flavell, M. Müller, I.M. Kerr, and G.R. Stark. 1991. High-frequency mutagenesis of human cells and characterization of a mutant unresponsive to both alpha and gamma interferons. Proc. Natl. Acad. Sci. USA. 88:11455-11459. http://dx.doi.org/10.1073/pnas.88.24.11455
23. Meira, C.S., V.L. Pereira-Chioccola, J.E. Vidal, C.C.B. de Mattos, G. Motoie, T.A. Costa-Silva, R. Gava, F.B. Frederico, and L.C. de Mattos. Toxoplasma Groups. 2014. Cerebral and ocular toxoplasmosis related with IFN-γ, TNF-α, and IL-10 levels. Front. Microbiol. 5:492.
24. Melo, M.B., K.D.C. Jensen, and J.P.J. Saeij. 2011. Toxoplasma gondii effectors are master regulators of the inflammatory response. Trends Parasitol. 27:487-495. http://dx.doi.org/10.1016/j.pt.2011.08.001
25. Pereira-Chioccola, V.L., J.E. Vidal, and C. Su. 2009. Toxoplasma gondii infection and cerebral toxoplasmosis in HIV-infected patients. Future Microbiol. 4:1363-1379. http://dx.doi.org/10.2217/fmb.09.89
26. Rakesh, K., and D.K. Agrawal. 2005. Controlling cytokine signaling by constitutive inhibitors. Biochem. Pharmacol. 70:649-657. http://dx.doi.org/10.1016/j.bcp.2005.04.042
27. Ramana, C.V., M. Chatterjee-Kishore, H. Nguyen, and G.R. Stark. 2000. Complex roles of Stat1 in regulating gene expression. Oncogene. 19:2619-2627. http://dx.doi.org/10.1038/sj.onc.1203525
28. + monocytes is essential for control of acute toxoplasmosis. J. Exp. Med. 201:1761-1769. http://dx.doi.org/10.1084/jem.20050054
29. Robertson, A.G., M. Bilenky, A. Tam, Y. Zhao, T. Zeng, N. Thiessen, T. Cezard, A.P. Fejes, E.D. Wederell, R. Cullum, et al. 2008. Genome-wide relationship between histone H3 lysine 4 mono- and tri-methylation and transcription factor binding. Genome Res. 18:1906-1917. http://dx.doi.org/10.1101/gr.078519.108
30. Rosowski, E.E., and J.P.J. Saeij. 2012. Toxoplasma gondii clonal strains all inhibit STAT1 transcriptional activity but polymorphic effectors differentially modulate IFNγ induced gene expression and STAT1 phosphorylation. PLoS One. 7:e51448. http://dx.doi.org/10.1371/journal.pone.0051448
31. Rosowski, E.E., Q.P. Nguyen, A. Camejo, E. Spooner, and J.P.J. Saeij. 2014. Toxoplasma gondii inhibits gamma interferon (IFN-γ)- and IFN-β- induced host cell STAT1 transcriptional activity by increasing the association of STAT1 with DNA. Infect. Immun. 82:706-719. http://dx.doi.org/10.1128/IAI.01291-13
32. Sadzak, I., M. Schiff, I. Gattermeier, R. Glinitzer, I. Sauer, A. Saalmüller, E. Yang, B. Schaljo, and P. Kovarik. 2008. Recruitment of Stat1 to chromatin is required for interferon-induced serine phosphorylation of Stat1 transactivation domain. Proc. Natl. Acad. Sci. USA. 105:8944-8949. http://dx.doi.org/10.1073/pnas.0801794105
33. Saeij, J.P.J., 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. http://dx.doi.org/10.1038/nature05395
34. Sakamoto, S., R. Potla, and A.C. Larner. 2004. Histone deacetylase activity is required to recruit RNA polymerase II to the promoters of selected interferon-stimulated early response genes. J. Biol. Chem. 279:40362-40367. http://dx.doi.org/10.1074/jbc. M406400200
35. Scallan, E., R.M. Hoekstra, B.E. Mahon, T.F. Jones, and P.M. Griffin. 2015. An assessment of the human health impact of seven leading foodborne pathogens in the United States using disability adjusted life years. Epidemiol. Infect. 143:2795-2804. http://dx.doi.org/10.1017/S0950268814003185
36. 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. 185:1261-1274. http://dx.doi.org/10.1084/jem.185.7.1261
37. Schneider, A.G., D.S. Abi Abdallah, B.A. Butcher, and E.Y. Denkers. 2013. Toxoplasma gondii triggers phosphorylation and nuclear translocation of dendritic cell STAT1 while simultaneously blocking IFNγ-induced STAT1 transcriptional activity. PLoS One. 8:e60215. http://dx.doi.org/10.1371/journal.pone.0060215
38. 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 gamma interferon and requirement of interferon regulatory factor 1. Infect. Immun. 70:859-868. http://dx.doi.org/10.1128/IAI.70.2.859-868.2002
39. Stark, G.R., and J.E. Darnell Jr. 2012. The JAK-STAT pathway at twenty. Immunity. 36:503-514. http://dx.doi.org/10.1016/j.immuni.2012.03.013
40. Sturge, C.R., and F. Yarovinsky. 2014. Complex immune cell interplay in the gamma interferon response during Toxoplasma gondii infection. Infect. Immun. 82:3090-3097. http://dx.doi.org/10.1128/IAI.01722-14
41. Sullivan, W.J. Jr., and V. Jeffers. 2012. Mechanisms of Toxoplasma gondii persistence and latency. FEMS Microbiol. Rev. 36:717-733. http://dx.doi.org/10.1111/j.1574-6976.2011.00305.x
42. Tahk, S., B. Liu, V. Chernishof, K.A. Wong, H. Wu, and K. Shuai. 2007. Control of specificity and magnitude of NF-κB and STAT1-mediated gene activation through PIASy and PIAS1 cooperation. Proc. Natl. Acad. Sci. USA. 104:11643-11648. http://dx.doi.org/10.1073/pnas.0701877104
43. Voigt, P., W.-W. Tee, and D. Reinberg. 2013. A double take on bivalent promoters. Genes Dev. 27:1318-1338. http://dx.doi.org/10.1101/gad.219626.113
44. Wojciak, J.M., M.A. Martinez-Yamout, H.J. Dyson, and P.E. Wright. 2009. Structural basis for recruitment of CBP/p300 coactivators by STAT1 and STAT2 transactivation domains. EMBO J. 28:948-958. http://dx.doi.org/10.1038/emboj.2009.30
45. Xue, Y., J. Wong, G.T. Moreno, M.K. Young, J. Côté, and W. Wang. 1998. NURD, a novel complex with both ATP-dependent chromatinremodeling and histone deacetylase activities. Mol. Cell. 2:851-861. http://dx.doi.org/10.1016/S1097-2765(00)80299-3
46. Yamamoto, M., D.M. Standley, S. Takashima, H. Saiga, M. Okuyama, H. Kayama, E. Kubo, H. Ito, M. Takaura, T. Matsuda, et al. 2009. A single polymorphic amino acid on Toxoplasma gondii kinase ROP16 determines the direct and strain-specific activation of Stat3. J. Exp. Med. 206:2747-2760. http://dx.doi.org/10.1084/jem.20091703
47. Yamamoto, M., M. Okuyama, J.S. Ma, T. Kimura, N. Kamiyama, H. Saiga, J. Ohshima, M. Sasai, H. Kayama, T. Okamoto, et al. 2012. A cluster of interferon-γ-inducible p65 GTPases plays a critical role in host defense against Toxoplasma gondii. Immunity. 37:302-313. http://dx.doi.org/10.1016/j.immuni.2012.06.009
48. 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. 189:1083-1092. http://dx.doi.org/10.1084/jem.189.7.1083
49. Yarovinsky, F. 2014. Innate immunity to Toxoplasma gondii infection. Nat. Rev. Immunol. 14:109-121. http://dx.doi.org/10.1038/nri3598
50. Zhao, Y., D.J.P. Ferguson, D.C. Wilson, J.C. Howard, L.D. Sibley, and G.S. Yap. 2009. Virulent Toxoplasma gondii evade immunity-related GTPasemediated parasite vacuole disruption within primed macrophages. J. Immunol. 182:3775-3781. http://dx.doi.org/10.4049/jimmunol.0804190
51. Zimmermann, S., P.J. Murray, K. Heeg, and A.H. Dalpke. 2006. Induction of suppressor of cytokine signaling-1 by Toxoplasma gondii contributes to immune evasion in macrophages by blocking IFN-γ signaling. J. Immunol. 176:1840-1847. http://dx.doi.org/10.4049/jimmunol.176.3.1840