IL-33 promotes innate IFN-γ production and modulates dendritic cell response in LCMV-induced hepatitis in mice

European Journal of Immunology

Volumn 45, Issue 11, 2015, Pages 3052-3063

  Liang, Yuejin ^a   Jie, Zuliang ^a   Hou, Lifei ^a   Yi, Panpan ^a,b   Wang, Wei ^a   Kwota, Zakari ^a   Salvato, Maria ^c   de Waal Malefyt, Rene ^d   Soong, Lynn ^a   Sun, Jiaren ^a  

^a University of Texas Medical Branch School of Medicine   (United States)

^b CENTRAL SOUTH UNIVERSITY   (China)

^c UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^d MERCK RESEARCH LABORATORIES   (United States)

Author keywords

Dendritic cell; IFN ; IL 33; Innate lymphoid cell; LCMV; Viral hepatitis; T cell

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 17; INTERLEUKIN 33; IL33 PROTEIN, MOUSE;

ADAPTIVE IMMUNITY; ADOPTIVE TRANSFER; ARTICLE; CYTOKINE PRODUCTION; DENDRITIC CELL; GAMMA DELTA T LYMPHOCYTE; INNATE IMMUNITY; LIVER INJURY; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; LYMPHOID CELL; NATURAL KILLER CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; VIRUS HEPATITIS; WILD TYPE; ANIMAL; ARENAVIRUS INFECTION; BIOSYNTHESIS; C57BL MOUSE; DEFICIENCY; DISEASE MODEL; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HEPATITIS; IMMUNOLOGY; KNOCKOUT MOUSE; MOUSE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; T LYMPHOCYTE SUBPOPULATION; VIROLOGY;

ADOPTIVE TRANSFER; ANIMALS; ARENAVIRIDAE INFECTIONS; DENDRITIC CELLS; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HEPATITIS; IMMUNITY, INNATE; INTERFERON-GAMMA; INTERLEUKIN-33; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; T-LYMPHOCYTE SUBSETS;

EID: 84951570165     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201545696     Document Type: Article

References (52)

1. Medzhitov, R. and Janeway, C. A., Jr., Innate immune recognition and control of adaptive immune responses. Semin. Immunol. 1998. 10: 351-353.
2. Saito, T., Owen, D. M., Jiang, F., Marcotrigiano, J. and Gale, M., Jr., Innate immunity induced by composition-dependent RIG-I recognition of hepatitis C virus RNA. Nature 2008. 454: 523-527.
3. Seong, S. Y. and Matzinger, P., Hydrophobicity: an ancient damage-associated molecular pattern that initiates innate immune responses. Nat. Rev. Immunol. 2004. 4: 469-478.
4. Schmitz, J., Owyang, A., Oldham, E., Song, Y., Murphy, E., McClanahan, T. K., Zurawski, G. et al., IL-33, an interleukin-1-like cytokine that signals via the IL-1 receptor-related protein ST2 and induces T helper type 2-associated cytokines. Immunity 2005. 23: 479-490.
5. Oboki, K., Ohno, T., Kajiwara, N., Arae, K., Morita, H., Ishii, A., Nambu, A. et al., IL-33 is a crucial amplifier of innate rather than acquired immunity. Proc. Natl. Acad. Sci. USA 2010. 107: 18581-18586.
6. Bonilla, W. V., Frohlich, A., Senn, K., Kallert, S., Fernandez, M., Johnson, S., Kreutzfeldt, M. et al., The alarmin interleukin-33 drives protective antiviral CD8 T cell responses. Science 2012. 335: 984-989.
7. Liang, Y., Jie, Z., Hou, L., Aguilar-Valenzuela, R., Vu, D., Soong, L. and Sun, J., IL-33 induces nuocytes and modulates liver injury in viral hepatitis. J. Immunol. 2013. 190: 5666-5675.
8. Bonneville, M., O'Brien, R. L. and Born, W. K., Gammadelta T cell effector functions: a blend of innate programming and acquired plasticity. Nat. Rev. Immunol. 2010. 10: 467-478.
9. Hayday, A. C., Gammadelta T cells and the lymphoid stress-surveillance response. Immunity 2009. 31: 184-196.
10. Jost, S. and Altfeld, M., Control of human viral infections by natural killer cells. Annu. Rev. Immunol. 2013. 31: 163-194.
11. Probst, H. C. and van den Broek, M., Priming of CTLs by lymphocytic choriomeningitis virus depends on dendritic cells. J. Immunol. 2005. 174: 3920-3924.
12. Bhardwaj, N., Seder, R. A., Reddy, A. and Feldman, M. V., IL-12 in conjunction with dendritic cells enhances antiviral CD8+ CTL responses in vitro. J. Clin. Invest. 1996. 98: 715-722.
13. KleinJan, A., Klein Wolterink, R. G., Levani, Y., de Bruijn, M. J., Hoogsteden, H. C., van Nimwegen, M. and Hendriks, R. W., Enforced expression of Gata3 in T cells and group 2 innate lymphoid cells increases susceptibility to allergic airway inflammation in mice. J. Immunol. 2014. 192: 1385-1394.
14. Monticelli, L. A., Sonnenberg, G. F., Abt, M. C., Alenghat, T., Ziegler, C. G., Doering, T. A., Angelosanto, J. M. et al., Innate lymphoid cells promote lung-tissue homeostasis after infection with influenza virus. Nat. Immunol. 2011. 12: 1045-1054.
15. Arshad, M. I., Piquet-Pellorce, C., L'Helgoualc'h, A., Rauch, M., Patrat-Delon, S., Ezan, F., Lucas-Clerc, C. et al., TRAIL but not FasL and TNFalpha, regulates IL-33 expression in murine hepatocytes during acute hepatitis. Hepatology 2012. 56: 2353-2362.
16. Hou, L., Jie, Z., Desai, M., Liang, Y., Soong, L., Wang, T. and Sun, J., Early IL-17 production by intrahepatic T cells is important for adaptive immune responses in viral hepatitis. J. Immunol. 2013. 190: 621-629.
17. Ribot, J. C., deBarros, A., Pang, D. J., Neves, J. F., Peperzak, V., Roberts, S. J., Girardi, M. et al., CD27 is a thymic determinant of the balance between interferon-gamma- and interleukin 17-producing gammadelta T cell subsets. Nat. Immunol. 2009. 10: 427-436.
18. Bai, H., Cheng, J., Gao, X., Joyee, A. G., Fan, Y., Wang, S., Jiao, L. et al., IL-17/Th17 promotes type 1 T cell immunity against pulmonary intracellular bacterial infection through modulating dendritic cell function. J. Immunol. 2009. 183: 5886-5895.
19. Michel, M. L., Pang, D. J., Haque, S. F., Potocnik, A. J., Pennington, D. J. and Hayday, A. C., Interleukin 7 (IL-7) selectively promotes mouse and human IL-17-producing gammadelta cells. Proc. Natl. Acad. Sci. USA 2012. 109: 17549-17554.
20. Reis e Sousa, C., Dendritic cells in a mature age. Nat. Rev. Immunol. 2006. 6: 476-483.
21. Curtsinger, J. M., Lins, D. C. and Mescher, M. F., Signal 3 determines tolerance versus full activation of naive CD8 T cells: dissociating proliferation and development of effector function. J. Exp. Med. 2003. 197: 1141-1151.
22. Wang, J., Cai, Y., Ji, H., Feng, J., Ayana, D. A., Niu, J. and Jiang, Y., Serum IL-33 levels are associated with liver damage in patients with chronic hepatitis B. J. Interferon. Cytokine Res. 2012. 32: 248-253.
23. Wang, J., Zhao, P., Guo, H., Sun, X., Jiang, Z., Xu, L., Feng, J. et al., Serum IL-33 levels are associated with liver damage in patients with chronic hepatitis C. Mediat. Inflamm. 2012. 2012: 1-7.
24. Baumann, C., Bonilla, W. V., Frohlich, A., Helmstetter, C., Peine, M., Hegazy, A. N., Pinschewer, D. D. et al., T-bet- and STAT4-dependent IL-33 receptor expression directly promotes antiviral Th1 cell responses. Proc. Natl. Acad. Sci. USA 2015. 112: 4056-4061.
25. Toka, F. N., Kenney, M. A. and Golde, W. T., Rapid and transient activation of gammadelta T cells to IFN-gamma production, NK cell-like killing, and antigen processing during acute virus infection. J. Immunol. 2011. 186: 4853-4861.
26. Wang, T., Scully, E., Yin, Z., Kim, J. H., Wang, S., Yan, J., Mamula, M. et al., IFN-gamma-producing gamma delta T cells help control murine West Nile virus infection. J. Immunol. 2003. 171: 2524-2531.
27. Fang, H., Welte, T., Zheng, X., Chang, G. J., Holbrook, M. R., Soong, L. and Wang, T., gammadelta T cells promote the maturation of dendritic cells during West Nile virus infection. FEMS Immunol. Med. Microbiol. 2010. 59: 71-80.
28. Luzina, I. G., Pickering, E. M., Kopach, P., Kang, P. H., Lockatell, V., Todd, N. W., Papadimitriou, J. C. et al., Full-length IL-33 promotes inflammation but not Th2 response in vivo in an ST2-independent fashion. J. Immunol. 2012. 189: 403-410.
29. Bourgeois, E., Van, L. P., Samson, M., Diem, S., Barra, A., Roga, S., Gombert, J. M. et al., The pro-Th2 cytokine IL-33 directly interacts with invariant NKT and NK cells to induce IFN-gamma production. Eur. J. Immunol. 2009. 39: 1046-1055.
30. Nabekura, T., Girard, J. P. and Lanier, L. L., IL-33 receptor ST2 amplifies the expansion of NK cells and enhances host defense during mouse cytomegalovirus infection. J. Immunol. 2015. 194: 5948-5952.
31. Pandya, A. D., Al-Jaderi, Z., Hoglund, R. A., Holmoy, T., Harbo, H. F., Norgauer, J. and Maghazachi, A. A., Identification of human NK17/NK1 cells. PLoS One 2011. 6: e26780.
32. Waggoner, S. N., Cornberg, M., Selin, L. K. and Welsh, R. M., Natural killer cells act as rheostats modulating antiviral T cells. Nature 2011. 481: 394-398.
33. Jiang, H. R., Milovanovic, M., Allan, D., Niedbala, W., Besnard, A. G., Fukada, S. Y., Alves-Filho, J. C. et al., IL-33 attenuates EAE by suppressing IL-17 and IFN-gamma production and inducing alternatively activated macrophages. Eur. J. Immunol. 2012. 42: 1804-1814.
34. Pellegrini, M., Calzascia, T., Toe, J. G., Preston, S. P., Lin, A. E., Elford, A. R., Shahinian, A. et al., IL-7 engages multiple mechanisms to overcome chronic viral infection and limit organ pathology. Cell 2011. 144: 601-613.
35. Jie, Z., Liang, Y., Hou, L., Dong, C., Iwakura, Y., Soong, L., Cong, Y. et al., Intrahepatic innate lymphoid cells secrete IL-17A and IL-17F that are crucial for T cell priming in viral infection. J. Immunol. 2014. 192: 3289-3300.
36. Schnell, F. J., Sundholm, S., Crumley, S., Iversen, P. L. and Mourich, D. V., Lymphocytic choriomeningitis virus infection in FVB mouse produces hemorrhagic disease. PLoS Pathog. 2012. 8: e1003073.
37. Liu, Y., Munker, S., Mullenbach, R. and Weng, H. L., IL-13 signaling in liver fibrogenesis. Front. Immunol. 2012. 3: 1-7.
38. Spits, H., Artis, D., Colonna, M., Diefenbach, A., Di Santo, J. P., Eberl, G., Koyasu, S. et al., Innate lymphoid cells-a proposal for uniform nomenclature. Nat. Rev. Immunol. 2013. 13: 145-149.
39. Kapsenberg, M. L., Dendritic-cell control of pathogen-driven T-cell polarization. Nat. Rev. Immunol. 2003. 3: 984-993.
40. Walsh, K. P. and Mills, K. H., Dendritic cells and other innate determinants of T helper cell polarisation. Trends Immunol. 2013. 34: 521-530.
41. Iwasaki, A. and Medzhitov, R., Regulation of adaptive immunity by the innate immune system. Science 2010. 327: 291-295.
42. Freeman, B. E., Hammarlund, E., Raue, H. P. and Slifka, M. K., Regulation of innate CD8+ T-cell activation mediated by cytokines. Proc. Natl. Acad. Sci. USA 2012. 109: 9971-9976.
43. Nambu, A., Nakae, S. and Iwakura, Y., IL-1beta, but not IL-1alpha, is required for antigen-specific T cell activation and the induction of local inflammation in the delayed-type hypersensitivity responses. Int. Immunol. 2006. 18: 701-712.
44. Ben-Sasson, S. Z., Hu-Li, J., Quiel, J., Cauchetaux, S., Ratner, M., Shapira, I., Dinarello, C. A. et al., IL-1 acts directly on CD4 T cells to enhance their antigen-driven expansion and differentiation. Proc. Natl. Acad. Sci. USA 2009. 106: 7119-7124.
45. Bottcher, J. P., Schanz, O., Garbers, C., Zaremba, A., Hegenbarth, S., Kurts, C., Beyer, M. et al., IL-6 trans-signaling-dependent rapid development of cytotoxic CD8+ T cell function. Cell Rep. 2014. 8: 1318-1327.
46. Besnard, A. G., Togbe, D., Guillou, N., Erard, F., Quesniaux, V. and Ryffel, B., IL-33-activated dendritic cells are critical for allergic airway inflammation. Eur. J. Immunol. 2011. 41: 1675-1686.
47. Mayuzumi, N., Matsushima, H. and Takashima, A., IL-33 promotes DC development in BM culture by triggering GM-CSF production. Eur. J. Immunol. 2009. 39: 3331-3342.
48. Louten, J., Rankin, A. L., Li, Y., Murphy, E. E., Beaumont, M., Moon, C., Bourne, P. et al., Endogenous IL-33 enhances Th2 cytokine production and T-cell responses during allergic airway inflammation. Int. Immunol. 2011. 23: 307-315.
49. Welsh, R. M. and Seedhom, M. O., Lymphocytic choriomeningitis virus (LCMV): propagation, quantitation, and storage. Curr. Protoc. Microbiol. 2008. 15: Unit 15A 1-11.
50. Quah, B. J. and Parish, C. R., The use of carboxyfluorescein diacetate succinimidyl ester (CFSE) to monitor lymphocyte proliferation. J. Vis. Exp. 2010. 44: 1-3.
51. Vargas-Inchaustegui, D. A., Xin, L. and Soong, L., Leishmania braziliensis infection induces dendritic cell activation, ISG15 transcription, and the generation of protective immune responses. J. Immunol. 2008. 180: 7537-7545.
52. Neill, D. R., Wong, S. H., Bellosi, A., Flynn, R. J., Daly, M., Langford, T. K., Bucks, C. et al., Nuocytes represent a new innate effector leukocyte that mediates type-2 immunity. Nature 2010. 464: 1367-1370.