Astrocyte-Restricted Ablation of Interleukin-17-Induced Act1-Mediated Signaling Ameliorates Autoimmune Encephalomyelitis

Immunity

Volumn 32, Issue 3, 2010, Pages 414-425

  Kang, Zizhen ^a   Altuntas, Cengiz Zubeyir ^a   Gulen, Muhammet Fatih ^a   Liu, Caini ^a   Giltiay, Natalia ^a   Qin, Hongwei ^b   Liu, Liping ^a   Qian, Wen ^a   Ransohoff, Richard M ^a   Bergmann, Cornelia ^a   Stohlman, Stephen ^a   Tuohy, Vincent K ^a   Li, Xiaoxia ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

Cellimmuno; Molimmuno

Indexed keywords

GENE PRODUCT; INTERLEUKIN 17; PROTEIN ACT1; UNCLASSIFIED DRUG;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CENTRAL NERVOUS SYSTEM DISEASE; CONTROLLED STUDY; DISEASE COURSE; DISEASE SEVERITY; ENDOTHELIUM CELL; GENE DELETION; GENE INDUCTION; LYMPHOCYTE; MACROPHAGE; MICROGLIA; MOUSE; NERVE CELL; NERVOUS SYSTEM INFLAMMATION; NEUROECTODERM; NEUTROPHIL; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; ASTROCYTES; CELL SURVIVAL; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; GENE EXPRESSION REGULATION; INTERLEUKIN-17; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; SIGNAL TRANSDUCTION; T-LYMPHOCYTES, HELPER-INDUCER;

EID: 77949973725     PISSN: 10747613     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.immuni.2010.03.004     Document Type: Article

References (61)

1. Agrawal A., Dillon S., Denning T.L., Pulendran B. ERK1-/- mice exhibit Th1 cell polarization and increased susceptibility to experimental autoimmune encephalomyelitis. J. Immunol. 2006, 176:5788-5796.
2. Aloisi F. Immune function of microglia. Glia 2001, 36:165-179.
3. Awane M., Andres P.G., Li D.J., Reinecker H.C. NF-kappa B-inducing kinase is a common mediator of IL-17-, TNF-alpha-, and IL-1 beta-induced chemokine promoter activation in intestinal epithelial cells. J. Immunol. 1999, 162:5337-5344.
4. Bauer M., Brakebusch C., Coisne C., Sixt M., Wekerle H., Engelhardt B., Fässler R. Beta1 integrins differentially control extravasation of inflammatory cell subsets into the CNS during autoimmunity. Proc. Natl. Acad. Sci. USA 2009, 106:1920-1925.
5. Becher B., Bechmann I., Greter M. Antigen presentation in autoimmunity and CNS inflammation: How T lymphocytes recognize the brain. J. Mol. Med. 2006, 84:532-543.
6. Bettelli E., Sullivan B., Szabo S.J., Sobel R.A., Glimcher L.H., Kuchroo V.K. Loss of T-bet, but not STAT1, prevents the development of experimental autoimmune encephalomyelitis. J. Exp. Med. 2004, 200:79-87.
7. Boillée S., Yamanaka K., Lobsiger C.S., Copeland N.G., Jenkins N.A., Kassiotis G., Kollias G., Cleveland D.W. Onset and progression in inherited ALS determined by motor neurons and microglia. Science 2006, 312:1389-1392.
8. Butti E., Bergami A., Recchia A., Brambilla E., Del Carro U., Amadio S., Cattalini A., Esposito M., Stornaiuolo A., Comi G., et al. IL4 gene delivery to the CNS recruits regulatory T cells and induces clinical recovery in mouse models of multiple sclerosis. Gene Ther. 2008, 15:504-515.
9. Carson M.J. Microglia as liaisons between the immune and central nervous systems: functional implications for multiple sclerosis. Glia 2002, 40:218-231.
10. Claudio E., Sønder S.U., Saret S., Carvalho G., Ramalingam T.R., Wynn T.A., Chariot A., Garcia-Perganeda A., Leonardi A., Paun A., et al. The adaptor protein CIKS/Act1 is essential for IL-25-mediated allergic airway inflammation. J. Immunol. 2009, 182:1617-1630.
11. Croitoru-Lamoury J., Guillemin G.J., Boussin F.D., Mognetti B., Gigout L.I., Chéret A., Vaslin B., Le Grand R., Brew B.J., Dormont D. Expression of chemokines and their receptors in human and simian astrocytes: Evidence for a central role of TNF alpha and IFN gamma in CXCR4 and CCR5 modulation. Glia 2003, 41:354-370.
12. Cua D.J., Sherlock J., Chen Y., Murphy C.A., Joyce B., Seymour B., Lucian L., To W., Kwan S., Churakova T., et al. Interleukin-23 rather than interleukin-12 is the critical cytokine for autoimmune inflammation of the brain. Nature 2003, 421:744-748.
13. Das M.P., Nicholson L.B., Greer J.M., Kuchroo V.K. Autopathogenic T helper cell type 1 (Th1) and protective Th2 clones differ in their recognition of the autoantigenic peptide of myelin proteolipid protein. J. Exp. Med. 1997, 186:867-876.
14. Das Sarma J., Ciric B., Marek R., Sadhukhan S., Caruso M.L., Shafagh J., Fitzgerald D.C., Shindler K.S., Rostami A. Functional interleukin-17 receptor A is expressed in central nervous system glia and upregulated in experimental autoimmune encephalomyelitis. J. Neuroinflammation 2009, 6:14.
15. Dong Y., Benveniste E.N. Immune function of astrocytes. Glia 2001, 36:180-190.
16. 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.
17. Gold R., Linington C., Lassmann H. Understanding pathogenesis and therapy of multiple sclerosis via animal models: 70 years of merits and culprits in experimental autoimmune encephalomyelitis research. Brain 2006, 129:1953-1971.
18. Gonzalez-García I., Zhao Y., Ju S., Gu Q., Liu L., Kolls J.K., Lu B. IL-17 signaling-independent central nervous system autoimmunity is negatively regulated by TGF-beta. J. Immunol. 2009, 182:2665-2671.
19. Graus-Porta D., Blaess S., Senften M., Littlewood-Evans A., Damsky C., Huang Z., Orban P., Klein R., Schittny J.C., Müller U. Beta1-class integrins regulate the development of laminae and folia in the cerebral and cerebellar cortex. Neuron 2001, 31:367-379.
20. Haak S., Croxford A.L., Kreymborg K., Heppner F.L., Pouly S., Becher B., Waisman A. IL-17A and IL-17F do not contribute vitally to autoimmune neuro-inflammation in mice. J. Clin. Invest. 2009, 119:61-69.
21. Halonen S.K., Woods T., McInnerney K., Weiss L.M. Microarray analysis of IFN-gamma response genes in astrocytes. J. Neuroimmunol. 2006, 175:19-30.
22. Harrington L.E., Hatton R.D., Mangan P.R., Turner H., Murphy T.L., Murphy K.M., Weaver C.T. Interleukin 17-producing CD4+ effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat. Immunol. 2005, 6:1123-1132.
23. Inoue D., Numasaki M., Watanabe M., Kubo H., Sasaki T., Yasuda H., Yamaya M., Sasaki H. IL-17A promotes the growth of airway epithelial cells through ERK-dependent signaling pathway. Biochem. Biophys. Res. Commun. 2006, 347:852-858.
24. 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.
25. Jovanovic D.V., Di Battista J.A., Martel-Pelletier J., Jolicoeur F.C., He Y., Zhang M., Mineau F., Pelletier J.P. IL-17 stimulates the production and expression of proinflammatory cytokines, IL-beta and TNF-alpha, by human macrophages. J. Immunol. 1998, 160:3513-3521.
26. Kano A., Wolfgang M.J., Gao Q., Jacoby J., Chai G.X., Hansen W., Iwamoto Y., Pober J.S., Flavell R.A., Fu X.Y. Endothelial cells require STAT3 for protection against endotoxin-induced inflammation. J. Exp. Med. 2003, 198:1517-1525.
27. Kebir H., Kreymborg K., Ifergan I., Dodelet-Devillers A., Cayrol R., Bernard M., Giuliani F., Arbour N., Becher B., Prat A. Human TH17 lymphocytes promote blood-brain barrier disruption and central nervous system inflammation. Nat. Med. 2007, 13:1173-1175.
28. Kleinschek M.A., Owyang A.M., Joyce-Shaikh B., Langrish C.L., Chen Y., Gorman D.M., Blumenschein W.M., McClanahan T., Brombacher F., Hurst S.D., et al. IL-25 regulates Th17 function in autoimmune inflammation. J. Exp. Med. 2007, 204:161-170.
29. Kolls J.K., Lindén A. Interleukin-17 family members and inflammation. Immunity 2004, 21:467-476.
30. Komiyama Y., Nakae S., Matsuki T., Nambu A., Ishigame H., Kakuta S., Sudo K., Iwakura Y. IL-17 plays an important role in the development of experimental autoimmune encephalomyelitis. J. Immunol. 2006, 177:566-573.
31. Korn T., Bettelli E., Oukka M., Kuchroo V.K. IL-17 and Th17 cells. Annu. Rev. Immunol. 2009, 27:485-517.
32. Kroenke M.A., Carlson T.J., Andjelkovic A.V., Segal B.M. IL-12- and IL-23-modulated T cells induce distinct types of EAE based on histology, CNS chemokine profile, and response to cytokine inhibition. J. Exp. Med. 2008, 205:1535-1541.
33. Lees J.R., Golumbek P.T., Sim J., Dorsey D., Russell J.H. Regional CNS responses to IFN-gamma determine lesion localization patterns during EAE pathogenesis. J. Exp. Med. 2008, 205:2633-2642.
34. Leonardi A., Chariot A., Claudio E., Cunningham K., Siebenlist U. CIKS, a connection to Ikappa B kinase and stress-activated protein kinase. Proc. Natl. Acad. Sci. USA 2000, 97:10494-10499.
35. Li X., Commane M., Nie H., Hua X., Chatterjee-Kishore M., Wald D., Haag M., Stark G.R. Act1, an NF-kappa B-activating protein. Proc. Natl. Acad. Sci. USA 2000, 97:10489-10493.
36. 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-beta induces development of the T(H)17 lineage. Nature 2006, 441:231-234.
37. McFarland H.F., Martin R. Multiple sclerosis: A complicated picture of autoimmunity. Nat. Immunol. 2007, 8:913-919.
38. Novatchkova M., Leibbrandt A., Werzowa J., Neubüser A., Eisenhaber F. The STIR-domain superfamily in signal transduction, development and immunity. Trends Biochem. Sci. 2003, 28:226-229.
39. Park H., Li Z., Yang X.O., Chang S.H., Nurieva R., Wang Y.H., Wang Y., Hood L., Zhu Z., Tian Q., Dong C. A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat. Immunol. 2005, 6:1133-1141.
40. Qian Y., Zhao Z., Jiang Z., Li X. Role of NF kappa B activator Act1 in CD40-mediated signaling in epithelial cells. Proc. Natl. Acad. Sci. USA 2002, 99:9386-9391.
41. Qian Y., Qin J., Cui G., Naramura M., Snow E.C., Ware C.F., Fairchild R.L., Omori S.A., Rickert R.C., Scott M., et al. Act1, a negative regulator in CD40- and BAFF-mediated B cell survival. Immunity 2004, 21:575-587.
42. Qian Y., Liu C., Hartupee J., Altuntas C.Z., Gulen M.F., Jane-Wit D., Xiao J., Lu Y., Giltiay N., Liu J., et al. The adaptor Act1 is required for interleukin 17-dependent signaling associated with autoimmune and inflammatory disease. Nat. Immunol. 2007, 8:247-256.
43. Ramírez F., Mason D. Induction of resistance to active experimental allergic encephalomyelitis by myelin basic protein-specific Th2 cell lines generated in the presence of glucocorticoids and IL-4. Eur. J. Immunol. 2000, 30:747-758.
44. Ransohoff R.M. Immunology: In the beginning. Nature 2009, 462:41-42.
45. Reboldi A., Coisne C., Baumjohann D., Benvenuto F., Bottinelli D., Lira S., Uccelli A., Lanzavecchia A., Engelhardt B., Sallusto F. C-C chemokine receptor 6-regulated entry of TH-17 cells into the CNS through the choroid plexus is required for the initiation of EAE. Nat. Immunol. 2009, 10:514-523.
46. Sixt M., Engelhardt B., Pausch F., Hallmann R., Wendler O., Sorokin L.M. Endothelial cell laminin isoforms, laminins 8 and 10, play decisive roles in T cell recruitment across the blood-brain barrier in experimental autoimmune encephalomyelitis. J. Cell Biol. 2001, 153:933-946.
47. Sospedra M., Martin R. Immunology of multiple sclerosis. Annu. Rev. Immunol. 2005, 23:683-747.
48. Steinman L. Multiple sclerosis: A two-stage disease. Nat. Immunol. 2001, 2:762-764.
49. Steinman L. A rush to judgment on Th17. J. Exp. Med. 2008, 205:1517-1522.
50. Steinman L. Shifting therapeutic attention in MS to osteopontin, type 1 and type 2 IFN. Eur. J. Immunol. 2009, 39:2358-2360.
51. Stromnes I.M., Goverman J.M. Active induction of experimental allergic encephalomyelitis. Nat. Protoc. 2006, 1:1810-1819.
52. Stromnes I.M., Cerretti L.M., Liggitt D., Harris R.A., Goverman J.M. Differential regulation of central nervous system autoimmunity by T(H)1 and T(H)17 cells. Nat. Med. 2008, 14:337-342.
53. Sutton C.E., Lalor S.J., Sweeney C.M., Brereton C.F., Lavelle E.C., Mills K.H. Interleukin-1 and IL-23 induce innate IL-17 production from gammadelta T cells, amplifying Th17 responses and autoimmunity. Immunity 2009, 31:331-341.
54. Swaidani S., Bulek K., Kang Z., Liu C., Lu Y., Yin W., Aronica M., Li X. The critical role of epithelial-derived Act1 in IL-17- and IL-25-mediated pulmonary inflammation. J. Immunol. 2009, 182:1631-1640.
55. Toy D., Kugler D., Wolfson M., Vanden Bos T., Gurgel J., Derry J., Tocker J., Peschon J. Cutting edge: Interleukin 17 signals through a heteromeric receptor complex. J. Immunol. 2006, 177:36-39.
56. Trajkovic V., Stosic-Grujicic S., Samardzic T., Markovic M., Miljkovic D., Ramic Z., Mostarica Stojkovic M. Interleukin-17 stimulates inducible nitric oxide synthase activation in rodent astrocytes. J. Neuroimmunol. 2001, 119:183-191.
57. Tronche F., Kellendonk C., Kretz O., Gass P., Anlag K., Orban P.C., Bock R., Klein R., Schütz G. Disruption of the glucocorticoid receptor gene in the nervous system results in reduced anxiety. Nat. Genet. 1999, 23:99-103.
58. Veldhoen M., Hocking R.J., Atkins C.J., Locksley R.M., Stockinger B. TGFbeta in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells. Immunity 2006, 24:179-189.
59. Weaver A., Goncalves da Silva A., Nuttall R.K., Edwards D.R., Shapiro S.D., Rivest S., Yong V.W. An elevated matrix metalloproteinase (MMP) in an animal model of multiple sclerosis is protective by affecting Th1/Th2 polarization. FASEB J. 2005, 19:1668-1670.
60. Wohler J.E., Smith S.S., Zinn K.R., Bullard D.C., Barnum S.R. Gammadelta T cells in EAE: early trafficking events and cytokine requirements. Eur. J. Immunol. 2009, 39:1516-1526.
61. 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.