BATF2 inhibits immunopathological Th17 responses by suppressing Il23a expression during Trypanosoma cruzi infection

Journal of Experimental Medicine

Volumn 214, Issue 5, 2017, Pages 1313-1331

  Kitada, Shoko ^a,b,d   Kayama, Hisako ^a,b,d   Okuzaki, Daisuke ^c   Koga, Ritsuko ^e   Kobayashi, Masao ^a   Arima, Yasunobu ^f   Kumanogoh, Atsushi ^a   Murakami, Masaaki ^f   Ikawa, Masahito ^c   Takeda, Kiyoshi ^a,b,d  

^a OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b OSAKA UNIVERSITY   (Japan)

^c OSAKA UNIVERSITY   (Japan)

^d JAPAN AGENCY FOR MEDICAL RESEARCH AND DEVELOPMENT   (Japan)

^e KYUSHU UNIVERSITY   (Japan)

^f HOKKAIDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 23; PROTEIN BATF2; PROTEIN C JUN; PROTEIN DERIVATIVE; UNCLASSIFIED DRUG; BASIC LEUCINE ZIPPER TRANSCRIPTION FACTOR; BATF2 PROTEIN, MOUSE; IL23A PROTEIN, MOUSE; INTERLEUKIN 23P19;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; CHAGAS DISEASE; IMMUNOPATHOLOGY; INNATE IMMUNITY; LIVER CELL; MOUSE; NONHUMAN; PARASITE LOAD; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SPLEEN CELL; TH17 CELL; ANIMAL; C57BL MOUSE; FEMALE; IMMUNOLOGY; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; PHYSIOLOGY; TRYPANOSOMA CRUZI;

ANIMALS; BASIC-LEUCINE ZIPPER TRANSCRIPTION FACTORS; CHAGAS DISEASE; FEMALE; IMMUNITY, INNATE; INTERLEUKIN-23 SUBUNIT P19; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PROTO-ONCOGENE PROTEINS C-JUN; TH17 CELLS; TRYPANOSOMA CRUZI;

EID: 85021856033     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20161076     Document Type: Article

References (43)

1. Ahern, P.P., C. Schiering, S. Buonocore, M.J. McGeachy, D.J. Cua, K.J. Maloy, and F. Powrie. 2010. Interleukin-23 drives intestinal inflammation through direct activity on T cells. Immunity. 33:279-288. http ://dx .doi .org/10 .1016/j .immuni .2010 .08 .010
2. Barreto-de-Albuquerque, J., D. Silva-dos-Santos, A.R. Pérez, L.R. Berbert, E. de Santana-van-Vliet, D.A. Farias-de-Oliveira, O.C. Moreira, E. Roggero, C.E. de Carvalho-Pinto, J. Jurberg, et al. 2015. Trypanosoma cruzi infection through the oral route promotes a severe infection in mice: New disease form from an old infection? PLoS Negl. Trop. Dis. 9:e0003849. http ://dx .doi .org/10 .1371/journal .pntd .0003849
3. Bermejo, D.A., S.W. Jackson, M. Gorosito-Serran, E.V. Acosta-Rodriguez, M.C. Amezcua-Vesely, B.D. Sather, A.K. Singh, S. Khim, J. Mucci, D. Liggitt, et al. 2013. Trypanosoma cruzi trans-sialidase initiates a program independent of the transcription factors RORγt and Ahr that leads to IL-17 production by activated B cells. Nat. Immunol. 14:514-522. http ://dx .doi .org/10 .1038/ni .2569
4. Bonney, K.M., J.M. Taylor, E.B. Thorp, C.L. Epting, and D.M. Engman. 2015. Depletion of regulatory T cells decreases cardiac parasitosis and inflammation in experimental Chagas disease. Parasitol. Res. 114:1167-1178. http ://dx .doi .org/10 .1007/s00436-014-4300-3
5. Caldas, S., I.S. Caldas, L.F. Diniz, W.G. Lima, R.P. Oliveira, A.B. Cecílio, I. Ribeiro, A. Talvani, and M.T. Bahia. 2012. Real-time PCR strategy for parasite quantification in blood and tissue samples of experimental Trypanosoma cruzi infection. Acta Trop. 123:170-177. http ://dx .doi .org/10 .1016/j .actatropica .2012 .05 .002
6. Cencig, S., N. Coltel, C. Truyens, and Y. Carlier. 2011. Parasitic loads in tissues of mice infected with Trypanosoma cruzi and treated with AmBisome. PLoS Negl. Trop. Dis. 5:e1216. http ://dx .doi .org/10 .1371/journal .pntd .0001216
7. Chmielewski, S., A. Olejnik, K. Sikorski, J. Pelisek, K. Blaszczyk, C. Aoqui, H. Nowicka, A. Zernecke, U. Heemann, J. Wesoly, et al. 2014. STAT1-dependent signal integration between IFNγ and TLR4 in vascular cells reflect pro-atherogenic responses in human atherosclerosis. PLoS One. 9:e113318. http ://dx .doi .org/10 .1371/journal .pone .0113318
8. Cobb, D., and R.B. Smeltz. 2012. Regulation of proinflammatory Th17 responses during Trypanosoma cruzi infection by IL-12 family cytokines. J. Immunol. 188:3766-3773. http ://dx .doi .org/10 .4049/jimmunol .1103478
9. Cobb, D., D. Hambright, and R.B. Smeltz. 2010. T-bet-independent effects of IL-12 family cytokines on regulation of Th17 responses to experimental T. cruzi infection. J. Leukoc. Biol. 88:965-971. http ://dx .doi .org/10 .1189/jlb .0410238
10. Cua, D.J., and C.M. Tato. 2010. Innate IL-17-producing cells: The sentinels of the immune system. Nat. Rev. Immunol. 10:479-489. http ://dx .doi .org/10 .1038/nri2800
11. da Matta Guedes, P.M., F.R. Gutierrez, F.L. Maia, C.M. Milanezi, G.K. Silva, W.R. Pavanelli, and J.S. Silva. 2010. IL-17 produced during Trypanosoma cruzi infection plays a central role in regulating parasiteinduced myocarditis. PLoS Negl. Trop. Dis. 4:e604. http ://dx .doi .org/10 .1371/journal .pntd .0000604
12. Erdmann, H., C. Roßnagel, J. Böhme, Y. Iwakura, T. Jacobs, U.E. Schaible, and C. Hölscher. 2013. IL-17A promotes macrophage effector mechanisms against Trypanosoma cruzi by trapping parasites in the endolysosomal compartment. Immunobiology. 218:910-923. http ://dx .doi .org/10 .1016/j .imbio .2012 .10 .005
13. Findlay, E.G., R. Greig, J.S. Stumhofer, J.C. Hafalla, J.B. de Souza, C.J. Saris, C.A. Hunter, E.M. Riley, and K.N. Couper. 2010. Essential role for IL-27 receptor signaling in prevention of Th1-mediated immunopathology during malaria infection. J. Immunol. 185:2482-2492. http ://dx .doi .org/10 .4049/jimmunol .0904019
14. Gaffen, S.L., R. Jain, A.V. Garg, and D.J. Cua. 2014. The IL-23-IL-17 immune axis: From mechanisms to therapeutic testing. Nat. Rev. Immunol. 14:585-600. http ://dx .doi .org/10 .1038/nri3707
15. Gazzinelli, R.T., and E.Y. Denkers. 2006. Protozoan encounters with Tolllike receptor signalling pathways: Implications for host parasitism. Nat. Rev. Immunol. 6:895-906. http ://dx .doi .org/10 .1038/nri1978
16. Guo, S., D. Cobb, and R.B. Smeltz. 2009. T-bet inhibits the in vivo differentiation of parasite-specific CD4+ Th17 cells in a T cell-intrinsic manner. J. Immunol. 182:6179-6186. http ://dx .doi .org/10 .4049/jimmunol .0803821
17. Hall, A.O., D.P. Beiting, C. Tato, B. John, G. Oldenhove, C.G. Lombana, G.H. Pritchard, J.S. Silver, N. Bouladoux, J.S. Stumhofer, et al. 2012. The cytokines interleukin 27 and interferon-γ promote distinct Treg cell populations required to limit infection-induced pathology. Immunity. 37:511-523. http ://dx .doi .org/10 .1016/j .immuni .2012 .06 .014
18. Hamano, S., K. Himeno, Y. Miyazaki, K. Ishii, A. Yamanaka, A. Takeda, M. Zhang, H. Hisaeda, T.W. Mak, A. Yoshimura, and H. Yoshida. 2003. WSX-1 is required for resistance to Trypanosoma cruzi infection by regulation of proinflammatory cytokine production. Immunity. 19:657-667. http ://dx .doi .org/10 .1016/S1074-7613(03)00298-X
19. Kawai, T., and S. Akira. 2011. Toll-like receptors and their crosstalk with other innate receptors in infection and immunity. Immunity. 34:637-650. http ://dx .doi .org/10 .1016/j .immuni .2011 .05 .006
20. Kayama, H., and K. Takeda. 2010. The innate immune response to Trypanosoma cruzi infection. Microbes Infect. 12:511-517. http ://dx .doi .org/10 .1016/j .micinf .2010 .03 .005
21. Kayama, H., V.R. Ramirez-Carrozzi, M. Yamamoto, T. Mizutani, H. Kuwata, H. Iba, M. Matsumoto, K. Honda, S.T. Smale, and K. Takeda. 2008. Classspecific regulation of pro-inflammatory genes by MyD88 pathways and IκBζ. J. Biol. Chem. 283:12468-12477 (published errata appear in J. Biol. Chem. 2015. 290:4815 and 22446). http ://dx .doi .org/10 .1074/jbc .M709965200
22. Kayama, H., R. Koga, K. Atarashi, M. Okuyama, T. Kimura, T.W. Mak, S. Uematsu, S. Akira, H. Takayanagi, K. Honda, et al. 2009. NFATc1 mediates Toll-like receptor-independent innate immune responses during Trypanosoma cruzi infection. PLoS Pathog. 5:e1000514. http ://dx .doi .org/10 .1371/journal .ppat .1000514
23. Kolaczkowska, E., and P. Kubes. 2013. Neutrophil recruitment and function in health and inflammation. Nat. Rev. Immunol. 13:159-175. http ://dx .doi .org/10 .1038/nri3399
24. H17 differentiation by preventing Runx1-mediated activation of the gene encoding RORγt. Nat. Immunol. 12:96-104. http ://dx .doi .org/10 .1038/ni .1969
25. Leon, J.S., K. Wang, and D.M. Engman. 2003. Captopril ameliorates myocarditis in acute experimental Chagas disease. Circulation. 107:2264-2269. http ://dx .doi .org/10 .1161/01 .CIR .0000062690 .79456 .D0
26. Liu, W., X. Ouyang, J. Yang, J. Liu, Q. Li, Y. Gu, M. Fukata, T. Lin, J.C. He, M. Abreu, et al. 2009. AP-1 activated by Toll-like receptors regulates expression of IL-23 p19. J. Biol. Chem. 284:24006-24016. http ://dx .doi .org/10 .1074/jbc .M109 .025528
27. Liu, X., S. Ren, X. Qu, C. Ge, K. Cheng, and R.C. Zhao. 2015. Mesenchymal stem cells inhibit Th17 cells differentiation via IFN-γ-mediated SOCS3 activation. Immunol. Res. 61:219-229. http ://dx .doi .org/10 .1007/s12026-014-8612-2
28. McGeachy, M.J., and S.J. McSorley. 2012. Microbial-induced Th17: Superhero or supervillain? J. Immunol. 189:3285-3291. http ://dx .doi .org/10 .4049/jimmunol .1201834
29. McGeachy, M.J., Y. Chen, C.M. Tato, A. Laurence, B. Joyce-Shaikh, W.M. Blumenschein, T.K. McClanahan, J.J. O'Shea, and D.J. Cua. 2009. The interleukin 23 receptor is essential for the terminal differentiation of interleukin 17-producing effector T helper cells in vivo. Nat. Immunol. 10:314-324. http ://dx .doi .org/10 .1038/ni .1698
30. Mise-Omata, S., E. Kuroda, J. Niikura, U. Yamashita, Y. Obata, and T.S. Doi. 2007. A proximal kappaB site in the IL-23 p19 promoter is responsible for RelA-and c-Rel-dependent transcription. J. Immunol. 179:6596-6603. http ://dx .doi .org/10 .4049/jimmunol .179 .10 .6596
31. Miyazaki, Y., S. Hamano, S. Wang, Y. Shimanoe, Y. Iwakura, and H. Yoshida. 2010. IL-17 is necessary for host protection against acute-phase Trypanosoma cruzi infection. J. Immunol. 185:1150-1157. http ://dx .doi .org/10 .4049/jimmunol .0900047
32. Mühlbauer, M., P.M. Chilton, T.C. Mitchell, and C. Jobin. 2008. Impaired Bcl3 up-regulation leads to enhanced lipopolysaccharide-induced interleukin (IL)-23P19 gene expression in IL-10(-/-) mice. J. Biol. Chem. 283:14182-14189. http ://dx .doi .org/10 .1074/jbc .M709029200
33. Murphy, T.L., R. Tussiwand, and K.M. Murphy. 2013. Specificity through cooperation: BATF-IRF interactions control immune-regulatory networks. Nat. Rev. Immunol. 13:499-509. http ://dx .doi .org/10 .1038/nri3470
34. Rangachari, M., N. Mauermann, R.R. Marty, S. Dirnhofer, M.O. Kurrer, V. Komnenovic, J.M. Penninger, and U. Eriksson. 2006. T-bet negatively regulates autoimmune myocarditis by suppressing local production of interleukin 17. J. Exp. Med. 203:2009-2019. http ://dx .doi .org/10 .1084/jem .20052222
35. Rodrigues, M.M., A.C. Oliveira, and M. Bellio. 2012. The immune response to Trypanosoma cruzi: Role of Toll-like receptors and perspectives for vaccine development. J. Parasitol. Res. 2012:507874. http ://dx .doi .org/10 .1155/2012/507874
36. Roy, S., R. Guler, S.P. Parihar, S. Schmeier, B. Kaczkowski, H. Nishimura, J.W. Shin, Y. Negishi, M. Ozturk, R. Hurdayal, et al. 2015. Batf2/Irf1 induces inflammatory responses in classically activated macrophages, lipopolysaccharides, and mycobacterial infection. J. Immunol. 194:6035-6044. http ://dx .doi .org/10 .4049/jimmunol .1402521
37. Sheikh, S.Z., K. Matsuoka, T. Kobayashi, F. Li, T. Rubinas, and S.E. Plevy. 2010. Cutting edge: IFN-γ is a negative regulator of IL-23 in murine macrophages and experimental colitis. J. Immunol. 184:4069-4073. http ://dx .doi .org/10 .4049/jimmunol .0903600
38. Stumhofer, J.S., A. Laurence, E.H. Wilson, E. Huang, C.M. Tato, L.M. Johnson, A.V. Villarino, Q. Huang, A. Yoshimura, D. Sehy, et al. 2006. Interleukin 27 negatively regulates the development of interleukin 17-producing T helper cells during chronic inflammation of the central nervous system. Nat. Immunol. 7:937-945. http ://dx .doi .org/10 .1038/ni1376
39. Su, Z.Z., S.G. Lee, L. Emdad, I.V. Lebdeva, P. Gupta, K. Valerie, D. Sarkar, and P.B. Fisher. 2008. Cloning and characterization of SARI (suppressor of AP-1, regulated by IFN). Proc. Natl. Acad. Sci. USA. 105:20906-20911. http ://dx .doi .org/10 .1073/pnas .0807975106
40. Tagawa, Y., K. Sekikawa, and Y. Iwakura. 1997. Suppression of concanavalin A-induced hepatitis in IFN-gamma(-/-) mice, but not in TNF-alpha(-/-) mice: Role for IFN-gamma in activating apoptosis of hepatocytes. J. Immunol. 159:1418-1428
41. Tussiwand, R., W.L. Lee, T.L. Murphy, M. Mashayekhi, W. Kc, J.C. Albring, A.T. Satpathy, J.A. Rotondo, B.T. Edelson, N.M. Kretzer, et al. 2012. Compensatory dendritic cell development mediated by BATF-IRF interactions. Nature. 490:502-507. http ://dx .doi .org/10 .1038/nature11531
42. Villarino, A., L. Hibbert, L. Lieberman, E. Wilson, T. Mak, H. Yoshida, R.A. Kastelein, C. Saris, and C.A. Hunter. 2003. The IL-27R (WSX-1) is required to suppress T cell hyperactivity during infection. Immunity. 19:645-655. http ://dx .doi .org/10 .1016/S1074-7613(03)00300-5
43. Yoshimura, T., A. Takeda, S. Hamano, Y. Miyazaki, I. Kinjyo, T. Ishibashi, A. Yoshimura, and H. Yoshida. 2006. Two-sided roles of IL-27: Induction of Th1 differentiation on naive CD4+ T cells versus suppression of proinflammatory cytokine production including IL-23-induced IL-17 on activated CD4+ T cells partially through STAT3-dependent mechanism. J. Immunol. 177:5377-5385. http ://dx .doi .org/10 .4049/jimmunol .177 .8 .5377 Downloaded from jem.rupress.org on July 7, 2017