Analysis of TGF-β1 and TGF-β3 as regulators of encephalitogenic Th17 cells: Implications for multiple sclerosis

Brain, Behavior, and Immunity

Volumn 46, Issue , 2015, Pages 44-49

  Lee, Priscilla W ^a   Yang, Yuhong ^b   Racke, Michael K ^b   Lovett Racke, Amy E ^b  

^a OHIO STATE UNIVERSITY   (United States)

^b THE OHIO STATE UNIVERSITY WEXNER MEDICAL CENTER   (United States)

Author keywords

Experimental autoimmune encephalomyelitis; GM CSF; IL 23R; Multiple sclerosis; T cell encephalitogenicity; TGF 1; TGF 3; Th17 cells

Indexed keywords

GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 12; INTERLEUKIN 17; INTERLEUKIN 23 RECEPTOR; INTERLEUKIN 4; INTERLEUKIN 6; MYELIN; T LYMPHOCYTE RECEPTOR; TRANSFORMING GROWTH FACTOR BETA1; TRANSFORMING GROWTH FACTOR BETA3;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; LYMPHOCYTE DIFFERENTIATION; MOUSE; MULTIPLE SCLEROSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TH1 CELL; TH17 CELL; TH2 CELL; TRANSGENIC MOUSE; ANIMAL; CELL DIFFERENTIATION; DRUG EFFECTS; IMMUNOLOGY; METABOLISM;

ADOPTIVE TRANSFER; ANIMALS; CELL DIFFERENTIATION; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; INTERFERON-GAMMA; INTERLEUKIN-17; MICE; MICE, TRANSGENIC; TH17 CELLS; TRANSFORMING GROWTH FACTOR BETA1; TRANSFORMING GROWTH FACTOR BETA3;

EID: 84928826568     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2014.12.007     Document Type: Article

References (37)

1. Acosta-Rodriguez E.V., Rivino L., Geginat J., Jarrossay D., Gattorno M., Lanzavecchia A., Sallusto F., Napolitani G. Interleukins 1β and 6 but not transforming growth factor-β are essential for the differentiation of interleukin 17-producing human T helper cells. Nat. Immunol. 2007, 8:639-646. 10.1038/ni1467.
2. Ando D.G., Clayton J., Kono D., Urban J.L., Sercarz E.E. Encephalitogenic T cells in the B10.PL model of experimental allergic encephalomyelitis (EAE) are of the Th-1 lymphokine subtype. Cell. Immunol. 1989, 124:132-143.
3. Becher B., Durell B.G., Noelle R.J. IL-23 produced by CNS-resident cells controls T cell encephalitogenicity during the effector phase of experimental autoimmune encephalomyelitis. J. Clin. Invest. 2003, 112:1186-1191. 10.1172/JCI19079.
4. Bettelli E., Carrier Y., Gao W., Korn T., Strom T.B., Oukka M., Weiner H.L., Kuchroo V.K. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 2006, 441:235-238. 10.1038/nature04753.
5. Codarri L., Gyülvészi G., Tosevski V., Hesske L., Fontana A., Magnenat L., Suter T., Becher B. RORγt drives production of the cytokine GM-CSF in helper T cells, which is essential for the effector phase of autoimmune neuroinflammation. Nat. Immunol. 2011, 12:560-567. 10.1038/ni.2027.
6. Cua D.J., Sherlock J., Chen Y., Murphy C.A., Joyce B., Seymour B., Lucian L., To W., Kwan S., Churakova T., Zurawski S., Wiekowski M., Lira S.A., Gorman D., Kastelein R.A., Sedgwick J.D. Interleukin-23 rather than interleukin-12 is the critical cytokine for autoimmune inflammation of the brain. Nature 2003, 421:744-748. 10.1038/nature01355.
7. Das Jyoti., Ren G., Zhang L., Roberts A.I., Zhao X., Bothwell A.L.M., Van Kaer L., Shi Y., Das G. Transforming growth factor beta is dispensable for the molecular orchestration of Th17 cell differentiation. J. Exp. Med. 2009, 206:2407-2416. 10.1084/jem.20082286.
8. El-Behi M., Ciric B., Dai H., Yan Y., Cullimore M., Safavi F., Zhang G.-X., Dittel B.N., Rostami A. The encephalitogenicity of T(H)17 cells is dependent on IL-1- and IL-23-induced production of the cytokine GM-CSF. Nat. Immunol. 2011, 12:568-575. 10.1038/ni.2031.
9. Evans H.G., Suddason T., Jackson I., Taams L.S., Lord G.M. Optimal induction of T helper 17 cells in humans requires T cell receptor ligation in the context of Toll-like receptor-activated monocytes. Proc. Natl. Acad. Sci. USA 2007, 104:17034-17039. 10.1073/pnas.0708426104.
10. Ferber I.A., Brocke S., Taylor-Edwards C., Ridgway W., Dinisco C., Steinman L., Dalton D., Fathman C.G. Mice with a disrupted IFN-gamma gene are susceptible to the induction of experimental autoimmune encephalomyelitis (EAE). J. Immunol. 1996, 156:5-7.
11. Ghoreschi K., Laurence A., Yang X.-P., Tato C.M., McGeachy M.J., Konkel J.E., Ramos H.L., Wei L., Davidson T.S., Bouladoux N., Grainger J.R., Chen Q., Kanno Y., Watford W.T., Sun H.-W., Eberl G., Shevach E.M., Belkaid Y., Cua D.J., Chen W., O'Shea J.J. Generation of pathogenic T(H)17 cells in the absence of TGF-β signalling. Nature 2010, 467:967-971. 10.1038/nature09447.
12. Gocke A.R., Cravens P.D., Ben L.-H., Hussain R.Z., Northrop S.C., Racke M.K., Lovett-Racke A.E. T-bet regulates the fate of Th1 and Th17 lymphocytes in autoimmunity. J. Immunol. 2007, 178:1341-1348.
13. Gorelik L., Fields P.E., Flavell R.A. Cutting edge: TGF-beta inhibits Th type 2 development through inhibition of GATA-3 expression. J. Immunol. 2000, 165:4773-4777.
14. Gorelik L., Constant S., Flavell R.A. Mechanism of transforming growth factor beta-induced inhibition of T helper type 1 differentiation. J. Exp. Med. 2002, 195:1499-1505.
15. Goverman J., Woods A., Larson L., Weiner L.P., Hood L. Transgenic mice that express a myelin basic protein-specific T cell receptor develop spontaneous autoimmunity. Cell 1993, 72:551-560.
16. Huss D.J., Winger R.C., Peng H., Yang Y., Racke M.K., Lovett-Racke A.E. TGF-beta enhances effector Th1 cell activation but promotes self-regulation via IL-10. J. Immunol. 2010, 184:5628-5636. 10.4049/jimmunol.1000288.
17. Huss D.J., Winger R.C., Cox G.M., Guerau-de-Arellano M., Yang Y., Racke M.K., Lovett-Racke A.E. TGF-β signaling via Smad4 drives IL-10 production in effector Th1 cells and reduces T-cell trafficking in EAE. Eur. J. Immunol. 2011, 41:2987-2996. 10.1002/eji.201141666.
18. Jäger A., Dardalhon V., Sobel R.A., Bettelli E., Kuchroo V.K. Th1, Th17, and Th9 effector cells induce experimental autoimmune encephalomyelitis with different pathological phenotypes. J. Immunol. 2009, 183:7169-7177. 10.4049/jimmunol.0901906.
19. Johns L.D., Sriram S. Experimental allergic encephalomyelitis: neutralizing antibody to TGFβ1 enhances the clinical severity of the disease. J. Neuroimmunol. 1993, 47:1-7. 10.1016/0165-5728(93)90278-7.
20. Langrish C.L., Chen Y., Blumenschein W.M., Mattson J., Basham B., Sedgwick J.D., McClanahan T., Kastelein R.A., Cua D.J. IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J. Exp. Med. 2005, 201:233-240. 10.1084/jem.20041257.
21. Lee Y., Awasthi A., Yosef N., Quintana F.J., Xiao S., Peters A., Wu C., Kleinewietfeld M., Kunder S., Hafler D.A., Sobel R.A., Regev A., Kuchroo V.K. Induction and molecular signature of pathogenic TH17 cells. Nat. Immunol. 2012, 13:991-999. 10.1038/ni.2416.
22. Lovett-Racke A.E., Rocchini A.E., Choy J., Northrop S.C., Hussain R.Z., Ratts R.B., Sikder D., Racke M.K. Silencing T-bet defines a critical role in the differentiation of autoreactive T lymphocytes. Immunity 2004, 21:719-731. 10.1016/j.immuni.2004.09.010.
23. Mangan P.R., Harrington L.E., O'Quinn D.B., Helms W.S., Bullard D.C., Elson C.O., Hatton R.D., Wahl S.M., Schoeb T.R., Weaver C.T. Transforming growth factor-β induces development of the TH17 lineage. Nature 2006, 441:231-234. 10.1038/nature04754.
24. McGeachy M.J., Bak-Jensen K.S., Chen Y., Tato C.M., Blumenschein W., McClanahan T., Cua D.J. 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. 2007, 8:1390-1397. 10.1038/ni1539.
25. McQualter J.L., Darwiche R., Ewing C., Onuki M., Kay T.W., Hamilton J.A., Reid H.H., Bernard C.C.A. Granulocyte macrophage colony-stimulating factor: a new putative therapeutic target in multiple sclerosis. J. Exp. Med. 2001, 194:873-882. 10.1084/jem.194.7.873.
26. Mukasa R., Balasubramani A., Lee Y.K., Whitley S.K., Weaver B.T., Shibata Y., Crawford G.E., Hatton R.D., Weaver C.T. Epigenetic instability of cytokine and transcription factor gene loci underlies plasticity of the T helper 17 cell lineage. Immunity 2010, 32:616-627. 10.1016/j.immuni.2010.04.016.
27. Olsson T., Zhi W.W., Höjeberg B., Kostulas V., Jiang Y.P., Anderson G., Ekre H.P., Link H. Autoreactive T lymphocytes in multiple sclerosis determined by antigen-induced secretion of interferon-gamma. J. Clin. Invest. 1990, 86:981-985. 10.1172/JCI114800.
28. Pelfrey C.M., Rudick R.A., Cotleur A.C., Lee J.C., Tary-Lehmann M., Lehmann P.V. Quantification of self-recognition in multiple sclerosis by single-cell analysis of cytokine production. J. Immunol. 2000, 165:1641-1651.
29. Ponomarev E.D., Shriver L.P., Maresz K., Pedras-Vasconcelos J., Verthelyi D., Dittel B.N. GM-CSF production by autoreactive T cells is required for the activation of microglial cells and the onset of experimental autoimmune encephalomyelitis. J. Immunol. 2007, 178:39-48.
30. Racke M.K., Dhib-Jalbut S., Cannella B., Albert P.S., Raine C.S., McFarlin D.E. Prevention and treatment of chronic relapsing experimental allergic encephalomyelitis by transforming growth factor-beta 1. J. Immunol. 1991, 146:3012-3017.
31. Racke M.K., Siram S., Carlino J., Cannella B., Raine C.S., McFarlin D.E. Long-term treatment of chronic relapsing experimental allergic encephalomyelitis by transforming growth factor-β2. J. Neuroimmunol. 1993, 46:175-183. 10.1016/0165-5728(93)90247-V.
32. Santarlasci V., Maggi L., Capone M., Frosali F., Querci V., De Palma R., Liotta F., Cosmi L., Maggi E., Romagnani S., Annunziato F. TGF-β indirectly favors the development of human Th17 cells by inhibiting Th1 cells. Eur. J. Immunol. 2009, 39:207-215. 10.1002/eji.200838748.
33. Sun J.B., Olsson T., Wang W.Z., Xiao B.G. Autoreactive T and B cells responding to myelin proteolipid protein in multiple sclerosis and controls. Eur. J. Immunol. 1991, 21:1461-1468.
34. Waldburger K.E., Hastings R.C., Schaub R.G., Goldman S.J., Leonard J.P. Adoptive transfer of experimental allergic encephalomyelitis after in vitro treatment with recombinant murine interleukin-12. Preferential expansion of interferon-gamma-producing cells and increased expression of macrophage-associated inducible nitric oxide synthase as immunomodulatory mechanisms. Am. J. Pathol. 1996, 148:375-382.
35. Wilson N.J., Boniface K., Chan J.R., McKenzie B.S., Blumenschein W.M., Mattson J.D., Basham B., Smith K., Chen T., Morel F., Lecron J.-C., Kastelein R.A., Cua D.J., McClanahan T.K., Bowman E.P., de Waal Malefyt R. Development, cytokine profile and function of human interleukin 17-producing helper T cells. Nat. Immunol. 2007, 8:950-957. 10.1038/ni1497.
36. Yang Y., Weiner J., Liu Y., Smith A.J., Huss D.J., Winger R., Peng H., Cravens P.D., Racke M.K., Lovett-Racke A.E. T-bet is essential for encephalitogenicity of both Th1 and Th17 cells. J. Exp. Med. 2009, 206:1549-1564. 10.1084/jem.20082584.
37. Yoshida Y., Yoshimi R., Yoshii H., Kim D., Dey A., Xiong H., Munasinghe J., Yazawa I., O'Donovan M.J., Maximova O.A., Sharma S., Zhu J., Wang H., Morse H.C., Ozato K. The transcription factor IRF8 activates integrin-mediated TGF-β signaling and promotes neuroinflammation. Immunity 2014, 40:187-198. 10.1016/j.immuni.2013.11.022.