CD4 + Th2 cells are directly regulated by IL-10 during allergic airway inflammation

Mucosal Immunology

Volumn 10, Issue 1, 2017, Pages 150-161

  Coomes, S M ^a   Kannan, Y ^a   Pelly, V S ^a   Entwistle, L J ^a   Guidi, R ^a   Perez Lloret, J ^a   Nikolov, N ^a   Muller W ^b   Wilson, M S ^a  

^a THE FRANCIS CRICK INSTITUTE   (United Kingdom)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; INTERLEUKIN 10; INTERLEUKIN 10 RECEPTOR; GRANZYME; HOUSE DUST ALLERGEN;

ALLERGIC AIRWAY INFLAMMATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD4+ T LYMPHOCYTE; CELL DEATH; CELL SURVIVAL; CONTROLLED STUDY; DISEASE EXACERBATION; FEMALE; GENE; GENE EXPRESSION REGULATION; GRANZYME B GENE; HOUSE DUST ALLERGY; IMMUNOREGULATION; IN VITRO STUDY; IN VIVO STUDY; LYMPHOCYTE DIFFERENTIATION; MOUSE; NONHUMAN; SIGNAL TRANSDUCTION; TH2 CELL; ANIMAL; C57BL MOUSE; CELL CULTURE; CELL DIFFERENTIATION; DISEASE MODEL; GENETICS; HUMAN; HYPERSENSITIVITY; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; KNOCKOUT MOUSE; LYMPHOCYTE ACTIVATION; METABOLISM; PYROGLYPHIDAE;

ANIMALS; ANTIGENS, DERMATOPHAGOIDES; CELL DIFFERENTIATION; CELL SURVIVAL; CELLS, CULTURED; DISEASE MODELS, ANIMAL; FEMALE; GRANZYMES; HUMANS; HYPERSENSITIVITY; IMMUNE TOLERANCE; INTERLEUKIN-10; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PYROGLYPHIDAE; RECEPTORS, INTERLEUKIN-10; SIGNAL TRANSDUCTION; TH2 CELLS;

EID: 85011049504     PISSN: 19330219     EISSN: 19353456     Source Type: Journal    
DOI: 10.1038/mi.2016.47     Document Type: Article

References (44)

1. Moore, K.W., O'Garra, A., de Waal Malefyt, R., Vieira, P. &Mosmann, T.R. Interleukin-10. Annu. Rev. Immunol. 11, 165-190 (1993).
2. Hawrylowicz, C.M. Regulatory T cells and IL-10 in allergic inflammation. J. Exp. Med. 202, 1459-1463 (2005).
3. Borish, L., Aarons, A., Rumbyrt, J., Cvietusa, P., Negri, J. &Wenzel, S. Interleukin-10 regulation in normal subjects and patients with asthma. J. Allergy Clin. Immunol. 97, 1288-1296 (1996).
4. John, M. et al. Inhaled corticosteroids increase interleukin-10 but reduce macrophage inflammatory protein-1alpha, granulocyte-macrophage colony-stimulating factor, and interferon-gamma release from alveolar macrophages in asthma. Am. J. Respir. Crit. Care Med. 157, 256-262 (1998).
5. Lim, S., Crawley, E., Woo, P. &Barnes, P.J. Haplotype associated with low interleukin-10 production in patients with severe asthma. Lancet 352, 113 (1998).
6. Wilson, M.S. et al. IL-13Ralpha2 and IL-10 coordinately suppress airway inflammation, airway-hyperreactivity, and fibrosis in mice. J. Clin. Invest. 117, 2941-2951 (2007).
7. Grunig, G., Corry, D.B., Leach, M.W., Seymour, B.W., Kurup, V.P. &Rennick, D.M. Interleukin-10 is a natural suppressor of cytokine production and inflammation in a murine model of allergic bronchopulmonary aspergillosis. J. Exp. Med. 185, 1089-1099 (1997).
8. Tournoy, K.G., Kips, J.C. &Pauwels, R.A. Endogenous interleukin-10 suppresses allergen-induced airway inflammation and nonspecific airway responsiveness. Clin. Exp. Allergy 30, 775-783 (2000).
9. Radinger, M., Johansson, A.K., Sitkauskiene, B., Sjostrand,M. &Lotvall, J. Eotaxin-2 regulates newly produced and CD34 airway eosinophils after allergen exposure. J. Allergy Clin. Immunol. 113, 1109-1116 (2004).
10. Akdis, C.A., Blesken, T., Akdis, M., Wuthrich, B. &Blaser, K. Role of interleukin 10 in specific immunotherapy. J. Clin. Invest. 102, 98-106 (1998).
11. Jutel, M. et al. IL-10 and TGF-beta cooperate in the regulatory T cell response to mucosal allergens in normal immunity and specific immunotherapy. Eur. J. Immunol. 33, 1205-1214 (2003).
12. de Waal Malefyt, R. et al. Interleukin 10 (IL-10) and viral IL-10 strongly reduce antigen-specific human T cell proliferation by diminishing the antigen-presenting capacity of monocytes via downregulation of class II major histocompatibility complex expression. J. Exp. Med. 174, 915-924 (1991).
13. Fiorentino, D.F. et al. IL-10 acts on the antigen-presenting cell to inhibit cytokine production by Th1 cells. J. Immunol. 146, 3444-3451 (1991).
14. Kamanaka, M. et al. Memory/effector (CD45RB(lo)) CD4 T cells are controlled directly by IL-10 and cause IL-22-dependent intestinal pathology. J. Exp. Med. 208, 1027-1040 (2011).
15. Huber, S. et al. Th17 cells express interleukin-10 receptor and are controlled by Foxp3(-) and Foxp3+ regulatory CD4+ T cells in an interleukin-10-dependent manner. Immunity 34, 554-565 (2011).
16. Chaudhry, A. et al. Interleukin-10 signaling in regulatory T cells is required for suppression of Th17 cell-mediated inflammation. Immunity 34, 566-578 (2011).
17. Schandene, L. et al. B7/CD28-dependent IL-5 production by human resting T cells is inhibited by IL-10. J. Immunol. 152, 4368-4374 (1994).
18. Barrat, F.J. et al. 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, 603-616 (2002).
19. Pils, M.C. et al. Monocytes/macrophages and/or neutrophils are the target of IL-10 in the LPS endotoxemia model. Eur. J. Immunol. 40, 443-448 (2010).
20. Wang, S.B., Deng, Y.Q., Ren, J., Xiao, B.K., Liu, Z. &Tao, Z.Z. Exogenous interleukin-10 alleviates allergic inflammation but inhibits local interleukin-10 expression in a mouse allergic rhinitis model. BMC Immunol. 15, 9 (2014).
21. Finbloom, D.S. &Winestock, K.D. IL-10 induces the tyrosine phosphorylation of tyk2 and Jak1 and the differential assembly of STAT1 alpha and STAT3 complexes in human T cells and monocytes. J. Immunol. 155, 1079-1090 (1995).
22. Mohrs, M., Shinkai, K., Mohrs, K. &Locksley, R.M. Analysis of type 2 immunity in vivo with a bicistronic IL-4 reporter. Immunity 15, 303-311 (2001).
23. Maynard, C.L. et al. Regulatory T cells expressing interleukin 10 develop from Foxp3+ and Foxp3-precursor cells in the absence of interleukin 10. Nat. Immunol. 8, 931-941 (2007).
24. Devadas, S. et al. Granzyme B is critical for T cell receptor-induced cell death of type 2 helper T cells. Immunity 25, 237-247 (2006).
25. Ichiba, M., Nakajima, K., Yamanaka, Y., Kiuchi, N. &Hirano, T. Autoregulation of the Stat3 gene through cooperation with a cAMPresponsive element-binding protein. J. Biol. Chem. 273, 6132-6138 (1998).
26. Stritesky,G.L. et al. The transcription factor STAT3 is required for T helper 2 cell development. Immunity 34, 39-49 (2011).
27. Zhu, J. et al. Conditional deletion of Gata3 shows its essential function in T(H)1-T(H)2 responses. Nat. Immunol. 5, 1157-1165 (2004).
28. Shoemaker, J., Saraiva, M. &O'Garra, A. GATA-3 directly remodels the IL-10 locus independently of IL-4 in CD4+ T cells. J. Immunol. 176, 3470-3479 (2006).
29. Chang, H.D. et al. Expression of IL-10 in Th memory lymphocytes is conditional on IL-12 or IL-4, unless the IL-10 gene is imprinted by GATA-3. Eur. J. Immunol. 37, 807-817 (2007).
30. Guo, L., Huang, Y., Chen, X., Hu-Li, J., Urban, J.F. Jr. &Paul, W.E. Innate immunological function of T2 cells in vivo. Nat. Immunol. 16, 1051-9 (2015).
31. Bohm, L. et al. IL-10 and regulatory T cells cooperate in allergen-specific immunotherapy to ameliorate allergic asthma. J. Immunol. 194, 887-897 (2015).
32. Stanic, B. et al. IL-10-overexpressing B cells regulate innate and adaptive immune responses. J. Allergy Clin. Immunol. 135, 771-780.e8 (2015).
33. Mumm, J.B. et al. IL-10 elicits IFNgamma-dependent tumor immune surveillance. Cancer Cell 20, 781-796 (2011).
34. Altin, J.A., Goodnow, C.C. &Cook, M.C. IL-10+ CTLA-4+ Th2 inhibitory cells form in a Foxp3-independent, IL-2-dependent manner from Th2 effectors during chronic inflammation. J. Immunol. 188, 5478-5488 (2012).
35. Xu, X. et al. Activation-induced T helper cell death contributes to Th1/Th2 polarization following murine Schistosoma japonicum infection. J. Biomed. Biotechnol. 2010, 202397 (2010).
36. van de Berg, P.J., van Leeuwen, E.M., ten Berge, I.J. &van Lier, R. Cytotoxic human CD4(+) T cells. Curr. Opin. Immunol. 20, 339-343 (2008).
37. McHugh, R.S. et al. CD4(+)CD25(+) immunoregulatory T cells: gene expression analysis reveals a functional role for the glucocorticoid-induced TNF receptor. Immunity 16, 311-323 (2002).
38. Steidler, L. et al. Treatment of murine colitis by Lactococcus lactis secreting interleukin-10. Science 289, 1352-1355 (2000).
39. Mohrs, K., Wakil, A.E., Killeen, N., Locksley, R.M. &Mohrs, M. A two-step process for cytokine production revealed by IL-4 dual-reporter mice. Immunity 23, 419-429 (2005).
40. Wan, Y.S.Y. &Flavell, R.A. Identifying Foxp3-expressing suppressor Tcells with a bicistronic reporter. Proc. Natl. Acad. Sci. USA 102, 5126-5131 (2005).
41. Bolger, A.M., Lohse, M. &Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114-2120 (2014).
42. Kim, D., Pertea, G., Trapnell, C., Pimentel, H., Kelley, R. &Salzberg, S.L. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 14, R36 (2013).
43. Anders, S., Theodor Pyl, P. &Huber, W. HTSeq-A Python framework to work with high-throughput sequencing data. Bioinformatics 131, 166-169 (2015).
44. Robinson, M.D., McCarthy, D.J. &Smyth, G.K. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139-140 (2010).