Metallothioneins negatively regulate IL-27-induced type 1 regulatory T-cell differentiation

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 19, 2013, Pages 7802-7807

  Wu, Chuan ^a   Pot, Caroline ^a,b,c   Apetoh, Lionel ^a,d,e   Thalhamer, Theresa ^a,g   Zhu, Bing ^a   Murugaiyan, Gopal ^a   Xiao, Sheng ^a   Lee, Youjin ^a   Rangachari, Manu ^a   Yosef, Nir ^a,f   Kuchroo, Vijay K ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b GENEVA UNIVERSITY HOSPITALS   (Switzerland)

^c UNIVERSITY OF GENEVA   (Switzerland)

^d INSERM   (France)

^e UNIVERSITÉ DE BOURGOGNE   (France)

^f BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^g UNIVERSITY OF SALZBURG   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 10; INTERLEUKIN 27; METALLOTHIONEIN I; METALLOTHIONEIN II; STAT1 PROTEIN; STAT3 PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL DIFFERENTIATION; CELL MATURATION; CONTROLLED STUDY; ENCEPHALOMYELITIS; HUMAN; HUMAN CELL; LYMPHOCYTE PROLIFERATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REGULATORY T LYMPHOCYTE;

ANIMALS; CELL DIFFERENTIATION; CELL SEPARATION; CELLS, CULTURED; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; HUMANS; INTERLEUKIN-10; INTERLEUKIN-17; METALLOTHIONEIN; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PHOSPHORYLATION; STAT1 TRANSCRIPTION FACTOR; STAT3 TRANSCRIPTION FACTOR; T-LYMPHOCYTES, REGULATORY;

EID: 84877321163     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1211776110     Document Type: Article

References (30)

1. Apetoh L, et al. (2010) The aryl hydrocarbon receptor interacts with c-Maf to promote the differentiation of type 1 regulatory T cells induced by IL-27. Nat Immunol 11(9): 854-861.
2. Fitzgerald DC, et al. (2007) Suppression of autoimmune inflammation of the central nervous system by interleukin 10 secreted by interleukin 27-stimulated T cells. Nat Immunol 8(12): 1372-1379.
3. Roncarolo MG, et al. (2006) Interleukin-10-secreting type 1 regulatory T cells in rodents and humans. Immunol Rev 212: 28-50.
4. Xie Y, et al. (2009) Tumor apoptotic bodies inhibit CTL responses and antitumor immunity via membrane-bound transforming growth factor-beta1 inducing CD8+ T-cell anergy and CD4+ Tr1 cell responses. Cancer Res 69(19): 7756-7766.
5. Awasthi A, et al. (2007) A dominant function for interleukin 27 in generating interleukin 10-producing anti-inflammatory T cells. Nat Immunol 8(12): 1380-1389.
6. Stumhofer JS, 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(9): 937-945.
7. Pot C, et al. (2009) Cutting edge: IL-27 induces the transcription factor c-Maf, cytokine IL-21, and the costimulatory receptor ICOS that coordinately act together to promote differentiation of IL-10-producing Tr1 cells. J Immunol 183(2): 797-801.
8. Hamer DH (1986) Metallothionein. Annu Rev Biochem 55: 913-951.
9. Ghoshal K, et al. (2001) Influenza virus infection induces metallothionein gene expression in the mouse liver and lung by overlapping but distinct molecular mechanisms. Mol Cell Biol 21(24): 8301-8317.
10. Lee DK, Carrasco J, Hidalgo J, Andrews GK (1999) Identification of a signal transducer and activator of transcription (STAT) binding site in the mouse metallothionein-I promoter involved in interleukin-6-induced gene expression. Biochem J 337(Pt 1): 59-65.
11. McGeachy MJ, et al. (2007) TGF-beta and IL-6 drive the production of IL-17 and IL-10 by T cells and restrain T(H)-17 cell-mediated pathology. Nat Immunol 8(12): 1390-1397.
12. Lee Y, et al. (2012) Induction and molecular signature of pathogenic TH17 cells. Nat Immunol 13(10): 991-999.
13. Barrat FJ, et al. (2002) In vitro generation of interleukin 10-producing regulatory CD4 (+) T cells is induced by immunosuppressive drugs and inhibited by T helper type 1 (Th1)- and Th2-inducing cytokines. J Exp Med 195(5): 603-616.
14. Wang H, et al. (2011) IL-27 induces the differentiation of Tr1-like cells from human naive CD4+ T cells via the phosphorylation of STAT1 and STAT3. Immunol Lett 136(1): 21-28.
15. Saraiva M, et al. (2009) Interleukin-10 production by Th1 cells requires interleukin- 12-induced STAT4 transcription factor and ERK MAP kinase activation by high antigen dose. Immunity 31(2): 209-219.
16. Kamanaka M, et al. (2006) Expression of interleukin-10 in intestinal lymphocytes detected by an interleukin-10 reporter knockin tiger mouse. Immunity 25(6): 941-952.
17. Langrish CL, et al. (2005) IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J Exp Med 201(2): 233-240.
18. Stromnes IM, Goverman JM (2006) Active induction of experimental allergic encephalomyelitis. Nat Protoc 1(4): 1810-1819.
19. Furlan R, et al. (1999) Caspase-1 regulates the inflammatory process leading to autoimmune demyelination. J Immunol 163(5): 2403-2409.
20. Lai Y, Yip GW, Bay BH (2011) Targeting metallothionein for prognosis and treatment of breast cancer. Recent Patents Anticancer Drug Discov 6(2): 178-185.
21. Abdel-Mageed AB, Agrawal KC (1998) Activation of nuclear factor kappaB: Potential role in metallothionein-mediated mitogenic response. Cancer Res 58(11): 2335-2338.
22. Cano-Gauci DF, Sarkar B (1996) Reversible zinc exchange between metallothionein and the estrogen receptor zinc finger. FEBS Lett 386(1): 1-4.
23. Kitabayashi C, et al. (2010) Zinc suppresses Th17 development via inhibition of STAT3 activation. Int Immunol 22(5): 375-386.
24. Xu J, et al. (2009) c-Maf regulates IL-10 expression during Th17 polarization. J Immunol 182(10): 6226-6236.
25. Chen Z, et al. (2006) Selective regulatory function of Socs3 in the formation of IL- 17-secreting T cells. Proc Natl Acad Sci USA 103(21): 8137-8142.
26. Youn J, et al. (2002) Metallothionein suppresses collagen-induced arthritis via induction of TGF-beta and down-regulation of proinflammatory mediators. Clin Exp Immunol 129(2): 232-239.
27. Espejo C, Penkowa M, Demestre M, Montalban X, Martínez- Cáceres EM (2005) Timecourse expression of CNS inflammatory, neurodegenerative tissue repair markers and metallothioneins during experimental autoimmune encephalomyelitis. Neuroscience 132(4): 1135-1149.
28. Penkowa M, Hidalgo J (2003) Treatment with metallothionein prevents demyelination and axonal damage and increases oligodendrocyte precursors and tissue repair during experimental autoimmune encephalomyelitis. J Neurosci Res 72(5): 574-586.
29. Penkowa M, Espejo C, Martínez-Cáceres EM, Montalban X, Hidalgo J (2003) Increased demyelination and axonal damage in metallothionein I+II-deficient mice during experimental autoimmune encephalomyelitis. Cell Mol Life Sci 60(1): 185-197.
30. Penkowa M, et al. (2001) Altered inflammatory response and increased neurodegeneration in metallothionein I+II deficient mice during experimental autoimmune encephalomyelitis. J Neuroimmunol 119(2): 248-260.