Regulation of CCL20 expression in astrocytes by IL-6 and IL-17

GLIA

Volumn 60, Issue 5, 2012, Pages 771-781

  Meares, Gordon P ^a   Ma, Xiangyu ^b   Qin, Hongwei ^a   Benveniste, Etty N ^a  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^b SHANDONG UNIVERSITY   (China)

Author keywords

Central nervous system; Chemotaxis; Glia; Inflammation; Interleukin; NF kappaB; STAT3

Indexed keywords

HISTONE H3; HISTONE H4; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 17; INTERLEUKIN 6; INTERLEUKIN 6 RECEPTOR; MACROPHAGE INFLAMMATORY PROTEIN 3ALPHA; PROTEIN P300; STAT3 PROTEIN;

ANIMAL CELL; ARTICLE; ASTROCYTE; CELL MIGRATION; CELL STIMULATION; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; HISTONE ACETYLATION; IMMUNOPRECIPITATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; T LYMPHOCYTE;

ANIMALS; ASTROCYTES; CELL MOVEMENT; CHEMOKINE CCL20; GENE EXPRESSION REGULATION; HUMANS; INTERLEUKIN-17; INTERLEUKIN-6; MICE; PRIMARY CELL CULTURE; RECEPTORS, INTERLEUKIN-6;

EID: 84858079448     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.22307     Document Type: Article

References (89)

1. Ambrosini E, Columba-Cabezas S, Serafini B, Muscella A, Aloisi F. 2003. Astrocytes are the major intracerebral source of macrophage inflammatory protein-3alpha/CCL20 in relapsing experimental autoimmune encephalomyelitis and in vitro. Glia 41: 290-300.
2. Ambrosini E, Remoli ME, Giacomini E, Rosicarelli B, Serafini B, Lande R, Aloisi F, Coccia EM. 2005. Astrocytes produce dendritic cell-attracting chemokines in vitro and in multiple sclerosis lesions. J Neuropathol Exp Neurol 64: 706-715.
3. Azuma H, Moriyama T, Ikeda H, Oshima M, Okuno A, Sekiguchi S. 2000. Analysis of soluble interleukin 6 receptor in cerebrospinal fluid in inflammatory and non-inflammatory conditions. Cytokine 12: 160-164.
4. Baba M, Imai T, Nishimura M, Kakizaki M, Takagi S, Hieshima K, Nomiyama H, Yoshie O. 1997. Identification of CCR6, the specific receptor for a novel lymphocyte-directed CC chemokine LARC. J Biol Chem 272: 14893-14898.
5. Battaglia F, Delfino S, Merello E, Puppo M, Piva R, Varesio L, Bosco MC. 2008. Hypoxia transcriptionally induces macrophage-inflammatory protein-3alpha/CCL-20 in primary human mononuclear phagocytes through nuclear factor (NF)-kappaB. J Leukoc Biol 83: 648-662.
6. Bettelli E, Carrier Y, Gao W, Korn T, Strom TB, Oukka M, Weiner HL, Kuchroo VK. 2006. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 441: 235-238.
7. Brambilla R, Persaud T, Hu X, Karmally S, Shestopalov VI, Dvoriantchikova G, Ivanov D, Nathanson L, Barnum SR, Bethea JR. 2009. Transgenic inhibition of astroglial NF-kappa B improves functional outcome in experimental autoimmune encephalomyelitis by suppressing chronic central nervous system inflammation. J Immunol 182: 2628-2640.
8. Butzkueven H, Emery B, Cipriani T, Marriott MP, Kilpatrick TJ. 2006. Endogenous leukemia inhibitory factor production limits autoimmune demyelination and oligodendrocyte loss. Glia 53: 696-703.
9. Butzkueven H, Zhang JG, Soilu-Hanninen M, Hochrein H, Chionh F, Shipham KA, Emery B, Turnley AM, Petratos S, Ernst M, Bartlett PF, Kilpatrick TJ. 2002. LIF receptor signaling limits immune-mediated demyelination by enhancing oligodendrocyte survival. Nat Med 8: 613-619.
10. Cao W, Yang Y, Wang Z, Liu A, Fang L, Wu F, Hong J, Shi Y, Leung S, Dong C, Zhang JZ. 2011. Leukemia inhibitory factor inhibits T helper 17 cell differentiation and confers treatment effects of neural progenitor cell therapy in autoimmune disease. Immunity 35: 273-284.
11. Chabaud M, Fossiez F, Taupin JL, Miossec P. 1998. Enhancing effect of IL-17 on IL-1-induced IL-6 and leukemia inhibitory factor production by rheumatoid arthritis synoviocytes and its regulation by Th2 cytokines. J Immunol 161: 409-414.
12. Chabaud M, Page G, Miossec P. 2001. Enhancing effect of IL-1, IL-17, and TNF-alpha on macrophage inflammatory protein-3alpha production in rheumatoid arthritis: Regulation by soluble receptors and Th2 cytokines. J Immunol 167: 6015-6020.
13. Comerford I, Bunting M, Fenix K, Haylock-Jacobs S, Litchfield W, Harata-Lee Y, Turvey M, Brazzatti J, Gregor C, Nguyen P, Kara E, McColl SR. 2010. An immune paradox: How can the same chemokine axis regulate both immune tolerance and activation?: CCR6/CCL20: A chemokine axis balancing immunological tolerance and inflammation in autoimmune disease. Bioessays 32: 1067-1076.
14. Desgeorges A, Gabay C, Silacci P, Novick D, Roux-Lombard P, Grau G, Dayer JM, Vischer T, Guerne PA. 1997. Concentrations and origins of soluble interleukin 6 receptor-alpha in serum and synovial fluid. J Rheumatol 24: 1510-1516.
15. Egwuagu CE. 2009. STAT3 in CD4+ T helper cell differentiation and inflammatory diseases. Cytokine 47: 149-156.
16. Emery B, Cate HS, Marriott M, Merson T, Binder MD, Snell C, Soo PY, Murray S, Croker B, Zhang JG, Alexander WS, Cooper H, Butzkueven H, Kilpatrick TJ. 2006. Suppressor of cytokine signaling 3 limits protection of leukemia inhibitory factor receptor signaling against central demyelination. Proc Natl Acad Sci USA 103: 7859-7864.
17. Farina C, Aloisi F, Meinl E. 2007. Astrocytes are active players in cerebral innate immunity. Trends Immunol 28: 138-145.
18. Farré D, Roset R, Huerta M, Adsuara JE, Roselló L, Albà MM, Messeguer X. 2003. Identification of patterns in biological sequences at the ALGGEN server: PROMO and MALGEN. Nucleic Acids Res 31: 3651-3653.
19. Fossiez F, Djossou O, Chomarat P, Flores-Romo L, Ait-Yahia S, Maat C, Pin JJ, Garrone P, Garcia E, Saeland S, Blanchard D, Gaillard C, Das Mahapatra B, Rouvier E, Golstein P, Banchereau J, Lebecque S. 1996. T cell interleukin-17 induces stromal cells to produce proinflammatory and hematopoietic cytokines. J Exp Med 183: 2593-2603.
20. Fujiie S, Hieshima K, Izawa D, Nakayama T, Fujisawa R, Ohyanagi H, Yoshie O. 2001. Proinflammatory cytokines induce liver and activation-regulated chemokine/macrophage inflammatory protein-3alpha/CCL20 in mucosal epithelial cells through NF-kappaB [correction of NK-kappaB]. Int Immunol 13: 1255-1263.
21. Gabay C. 2006. Interleukin-6 and chronic inflammation. Arthritis Res Ther 8 (Suppl 2): S3.
22. Gaffen SL. 2008. An overview of IL-17 function and signaling. Cytokine 43: 402-407.
23. Gaffen SL. 2009. Structure and signalling in the IL-17 receptor family. Nat Rev Immunol 9: 556-567.
24. Gijbels K, Van Damme J, Proost P, Put W, Carton H, Billiau A. 1990. Interleukin 6 production in the central nervous system during experimental autoimmune encephalomyelitis. Eur J Immunol 20: 233-235.
25. Glass CK, Saijo K, Winner B, Marchetto MC, Gage FH. 2010. Mechanisms underlying inflammation in neurodegeneration. Cell 140: 918-934.
26. Grivennikov S, Karin M. 2010. Dangerous liaisons: STAT3 and NF-B collaboration and crosstalk in cancer. Cytokine Growth Factor Rev 21: 11-19.
27. Haroon F, Drogemuller K, Handel U, Brunn A, Reinhold D, Nishanth G, Mueller W, Trautwein C, Ernst M, Deckert M, Schluter D. 2011. Gp130-dependent astrocytic survival is critical for the control of autoimmune central nervous system inflammation. J Immunol 186: 6521-6531.
28. Harper EG, Guo C, Rizzo H, Lillis JV, Kurtz SE, Skorcheva I, Purdy D, Fitch E, Iordanov M, Blauvelt A. 2009. Th17 cytokines stimulate CCL20 expression in keratinocytes in vitro and in vivo: Implications for psoriasis pathogenesis. J Invest Dermatol 129: 2175-2183.
29. Harrington LE, Hatton RD, Mangan PR, Turner H, Murphy TL, Murphy KM, Weaver CT. 2005. Interleukin 17-producing CD4+ effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat Immunol 6: 1123-1132.
30. Hartupee J, Liu C, Novotny M, Li X, Hamilton T. 2007. IL-17 enhances chemokine gene expression through mRNA stabilization. J Immunol 179: 4135-4141.
31. Heinrich PC, Behrmann I, Haan S, Hermanns HM, Muller-Newen G, Schaper F. 2003. Principles of interleukin (IL)-6-type cytokine signalling and its regulation. Biochem J 374: 1-20.
32. Henness S, Johnson CK, Ge Q, Armour CL, Hughes JM, Ammit AJ. 2004. IL-17A augments TNF-alpha-induced IL-6 expression in airway smooth muscle by enhancing mRNA stability. J Allergy Clin Immunol 114: 958-964.
33. Henness S, van Thoor E, Ge Q, Armour CL, Hughes JM, Ammit AJ. 2006. IL-17A acts via p38 MAPK to increase stability of TNF-alpha-induced IL-8 mRNA in human ASM. Am J Physiol Lung Cell Mol Physiol 290: L1283-L1290.
34. Hirata T, Osuga Y, Takamura M, Kodama A, Hirota Y, Koga K, Yoshino O, Harada M, Takemura Y, Yano T, Taketani Y. 2010. Recruitment of CCR6-expressing Th17 cells by CCL 20 secreted from IL-1 beta-, TNF-alpha-, and IL-17A-stimulated endometriotic stromal cells. Endocrinology 151: 5468-5476.
35. Hirota K, Yoshitomi H, Hashimoto M, Maeda S, Teradaira S, Sugimoto N, Yamaguchi T, Nomura T, Ito H, Nakamura T, Sakaguchi N, Sakaguchi S. 2007. Preferential recruitment of CCR6-expressing Th17 cells to inflamed joints via CCL20 in rheumatoid arthritis and its animal model. J Exp Med 204: 2803-2812.
36. Hurst SM, Wilkinson TS, McLoughlin RM, Jones S, Horiuchi S, Yamamoto N, Rose-John S, Fuller GM, Topley N, Jones SA. 2001. IL-6 and its soluble receptor orchestrate a temporal switch in the pattern of leukocyte recruitment seen during acute inflammation. Immunity 14: 705-714.
37. Imaizumi Y, Sugita S, Yamamoto K, Imanishi D, Kohno T, Tomonaga M, Matsuyama T. 2002. Human T cell leukemia virus type-I Tax activates human macrophage inflammatory protein-3 alpha/CCL20 gene transcription via the NF-kappa B pathway. Int Immunol 14: 147-155.
38. Izikson L, Klein RS, Charo IF, Weiner HL, Luster AD. 2000. Resistance to experimental autoimmune encephalomyelitis in mice lacking the CC chemokine receptor (CCR)2. J Exp Med 192: 1075-1080.
39. Kang Z, Altuntas CZ, Gulen MF, Liu C, Giltiay N, Qin H, Liu L, Qian W, Ransohoff RM, Bergmann C, Stohlman S, Tuohy VK, Li X. 2010. Astrocyte-restricted ablation of interleukin-17-induced Act1-mediated signaling ameliorates autoimmune encephalomyelitis. Immunity 32: 414-425.
40. Kao CY, Huang F, Chen Y, Thai P, Wachi S, Kim C, Tam L, Wu R. 2005. Up-regulation of CC chemokine ligand 20 expression in human airway epithelium by IL-17 through a JAK-independent but MEK/NF-kappaB-dependent signaling pathway. J Immunol 175: 6676-6685.
41. Kochi Y, Okada Y, Suzuki A, Ikari K, Terao C, Takahashi A, Yamazaki K, Hosono N, Myouzen K, Tsunoda T, Kamatani N, Furuichi T, Ikegawa S, Ohmura K, Mimori T, Matsuda F, Iwamoto T, Momohara S, Yamanaka H, Yamada R, Kubo M, Nakamura Y, Yamamoto K. 2010. A regulatory variant in CCR6 is associated with rheumatoid arthritis susceptibility. Nat Genet 42: 515-519.
42. Laurence A, Tato CM, Davidson TS, Kanno Y, Chen Z, Yao Z, Blank RB, Meylan F, Siegel R, Hennighausen L, Shevach EM, O'Shea JJ. 2007. Interleukin-2 signaling via STAT5 constrains T helper 17 cell generation. Immunity 26: 371-381.
43. Lee H, Herrmann A, Deng JH, Kujawski M, Niu G, Li Z, Forman S, Jove R, Pardoll DM, Yu H. 2009. Persistently activated Stat3 maintains constitutive NF-kappaB activity in tumors. Cancer Cell 15: 283-293.
44. Liang SC, Long AJ, Bennett F, Whitters MJ, Karim R, Collins M, Goldman SJ, Dunussi-Joannopoulos K, Williams CM, Wright JF, Fouser LA. 2007. An IL-17F/A heterodimer protein is produced by mouse Th17 cells and induces airway neutrophil recruitment. J Immunol 179: 7791-7799.
45. Liston A, Kohler RE, Townley S, Haylock-Jacobs S, Comerford I, Caon AC, Webster J, Harrison JM, Swann J, Clark-Lewis I, Korner H, McColl SR. 2009. Inhibition of CCR6 function reduces the severity of experimental autoimmune encephalomyelitis via effects on the priming phase of the immune response. J Immunol 182: 3121-3130.
46. Liu X, Lee YS, Yu CR, Egwuagu CE. 2008. Loss of STAT3 in CD4+ T cells prevents development of experimental autoimmune diseases. J Immunol 180: 6070-6076.
47. Lock C, Hermans G, Pedotti R, Brendolan A, Schadt E, Garren H, Langer-Gould A, Strober S, Cannella B, Allard J, Klonowski P, Austin A, Lad N, Kaminski N, Galli SJ, Oksenberg JR, Raine CS, Heller R, Steinman L. 2002. Gene-microarray analysis of multiple sclerosis lesions yields new targets validated in autoimmune encephalomyelitis. Nat Med 8: 500-508.
48. Lust JA, Donovan KA, Kline MP, Greipp PR, Kyle RA, Maihle NJ. 1992. Isolation of an mRNA encoding a soluble form of the human interleukin-6 receptor. Cytokine 4: 96-100.
49. Ma X, Reynolds SL, Baker BJ, Li X, Benveniste EN, Qin H. 2010. IL-17 enhancement of the IL-6 signaling cascade in astrocytes. J Immunol 184: 4898-4906.
50. Mackiewicz A, Schooltink H, Heinrich PC, Rose-John S. 1992. Complex of soluble human IL-6-receptor/IL-6 up-regulates expression of acute-phase proteins. J Immunol 149: 2021-2027.
51. Mangan PR, Harrington LE, O'Quinn DB, Helms WS, Bullard DC, Elson CO, Hatton RD, Wahl SM, Schoeb TR, Weaver CT. 2006. Transforming growth factor-beta induces development of the T(H)17 lineage. Nature 441: 231-234.
52. Matsui T, Akahoshi T, Namai R, Hashimoto A, Kurihara Y, Rana M, Nishimura A, Endo H, Kitasato H, Kawai S, Takagishi K, Kondo H. 2001. Selective recruitment of CCR6-expressing cells by increased production of MIP-3 alpha in rheumatoid arthritis. Clin Exp Immunol 125: 155-161.
53. Meares GP, Zmijewska AA, Jope RS. 2004. Heat shock protein-90 dampens and directs signaling stimulated by insulin-like growth factor-1 and insulin. FEBS Lett 574: 181-186.
54. Messeguer X, Escudero R, Farré D, Núñez O, Martínez J, Albà MM. 2002. PROMO: Detection of known transcription regulatory elements using species-tailored searches. Bioinformatics 18: 333-334.
55. Mullberg J, Schooltink H, Stoyan T, Gunther M, Graeve L, Buse G, Mackiewicz A, Heinrich PC, Rose-John S. 1993. The soluble interleukin-6 receptor is generated by shedding. Eur J Immunol 23: 473-480.
56. Murakami M, Okuyama Y, Ogura H, Asano S, Arima Y, Tsuruoka M, Harada M, Kanamoto M, Sawa Y, Iwakura Y, Takatsu K, Kamimura D, Hirano T. 2011. Local microbleeding facilitates IL-6- and IL-17-dependent arthritis in the absence of tissue antigen recognition by activated T cells. J Exp Med 208: 103-114.
57. Ogura H, Murakami M, Okuyama Y, Tsuruoka M, Kitabayashi C, Kanamoto M, Nishihara M, Iwakura Y, Hirano T. 2008. Interleukin-17 promotes autoimmunity by triggering a positive-feedback loop via interleukin-6 induction. Immunity 29: 628-636.
58. Oh JW, Schwiebert LM, Benveniste EN. 1999. Cytokine regulation of CC and CXC chemokine expression by human astrocytes. J Neurovirol 5: 82-94.
59. Onishi RM, Gaffen SL. 2010. Interleukin-17 and its target genes: Mechanisms of interleukin-17 function in disease. Immunology 129: 311-321.
60. Pedranzini L, Dechow T, Berishaj M, Comenzo R, Zhou P, Azare J, Bornmann W, Bromberg J. 2006. Pyridone 6, a pan-Janus-activated kinase inhibitor, induces growth inhibition of multiple myeloma cells. Cancer Res 66: 9714-9721.
61. Pierce JW, Schoenleber R, Jesmok G, Best J, Moore SA, Collins T, Gerritsen ME. 1997. Novel inhibitors of cytokine-induced IkappaBalpha phosphorylation and endothelial cell adhesion molecule expression show anti-inflammatory effects in vivo. J Biol Chem 272: 21096-21103.
62. Qin H, Niyongere SA, Lee SJ, Baker BJ, Benveniste EN. 2008. Expression and functional significance of SOCS-1 and SOCS-3 in astrocytes. J Immunol 181: 3167-3176.
63. Quintana A, Müller M, Frausto RF, Ramos R, Getts DR, Sanz E, Hofer MJ, Krauthausen M, King NJ, Hidalgo J, Campbell IL. 2009. Site-specific production of IL-6 in the central nervous system retargets and enhances the inflammatory response in experimental autoimmune encephalomyelitis. J Immunol 183: 2079-2088.
64. Reboldi A, Coisne C, Baumjohann D, Benvenuto F, Bottinelli D, Lira S, Uccelli A, Lanzavecchia A, Engelhardt B, Sallusto F. 2009. 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 10: 514-523.
65. Ruddy MJ, Wong GC, Liu XK, Yamamoto H, Kasayama S, Kirkwood KL, Gaffen SL. 2004. Functional cooperation between interleukin-17 and tumor necrosis factor-alpha is mediated by CCAAT/enhancer-binding protein family members. J Biol Chem 279: 2559-2567.
66. Scheller J, Chalaris A, Schmidt-Arras D, Rose-John S. 2011. The pro- and anti-inflammatory properties of the cytokine interleukin-6. Biochim Biophys Acta 1813: 878-888.
67. Seidel HM, Milocco LH, Lamb P, Darnell JE, Stein RB, Rosen J. 1995. Spacing of palindromic half sites as a determinant of selective STAT (signal transducers and activators of transcription) DNA binding and transcriptional activity. Proc Natl Acad Sci USA 92: 3041-3045.
68. Serafini B, Columba-Cabezas S, Di Rosa F, Aloisi F. 2000. Intracerebral recruitment and maturation of dendritic cells in the onset and progression of experimental autoimmune encephalomyelitis. Am J Pathol 157: 1991-2002.
69. Shahrara S, Pickens SR, Mandelin AM, Karpus WJ, Huang Q, Kolls JK, Pope RM. 2010. IL-17-mediated monocyte migration occurs partially through CC chemokine ligand 2/monocyte chemoattractant protein-1 induction. J Immunol 184: 4479-4487.
70. Silver JS, Hunter CA. 2010. gp130 at the nexus of inflammation, autoimmunity, and cancer. J Leukoc Biol 88: 1145-1156.
71. Simpson JE, Newcombe J, Cuzner ML, Woodroofe MN. 1998. Expression of monocyte chemoattractant protein-1 and other beta-chemokines by resident glia and inflammatory cells in multiple sclerosis lesions. J Neuroimmunol 84: 238-249.
72. Sofroniew MV, Vinters HV. 2010. Astrocytes: Biology and pathology. Acta Neuropathol 119: 7-35.
73. Sugita S, Kohno T, Yamamoto K, Imaizumi Y, Nakajima H, Ishimaru T, Matsuyama T. 2002. Induction of macrophage-inflammatory protein-3alpha gene expression by TNF-dependent NF-kappaB activation. J Immunol 168: 5621-5628.
74. Sun D, Novotny M, Bulek K, Liu C, Li X, Hamilton T. 2011. Treatment with IL-17 prolongs the half-life of chemokine CXCL1 mRNA via the adaptor TRAF5 and the splicing-regulatory factor SF2 (ASF). Nat Immunol 12: 853-860.
75. Taga T, Hibi M, Hirata Y, Yamasaki K, Yasukawa K, Matsuda T, Hirano T, Kishimoto T. 1989. Interleukin-6 triggers the association of its receptor with a possible signal transducer, gp130. Cell 58: 573-581.
76. van Loo G, De Lorenzi R, Schmidt H, Huth M, Mildner A, Schmidt-Supprian M, Lassmann H, Prinz MR, Pasparakis M. 2006. Inhibition of transcription factor NF-kappaB in the central nervous system ameliorates autoimmune encephalomyelitis in mice. Nat Immunol 7: 954-961.
77. Van Wagoner NJ, Benveniste EN. 1999. Interleukin-6 expression and regulation in astrocytes. J Neuroimmunol 100: 124-139.
78. Van Wagoner NJ, Oh JW, Repovic P, Benveniste EN. 1999. Interleukin-6 (IL-6) production by astrocytes: Autocrine regulation by IL-6 and the soluble IL-6 receptor. J Neurosci 19: 5236-5244.
79. Varesio L, Battaglia F, Raggi F, Ledda B, Bosco MC. 2010. Macrophage-inflammatory protein-3alpha/CCL-20 is transcriptionally induced by the iron chelator desferrioxamine in human mononuclear phagocytes through nuclear factor (NF)-kappaB. Mol Immunol 47: 685-693.
80. Webb A, Johnson A, Fortunato M, Platt A, Crabbe T, Christie MI, Watt GF, Ward SG, Jopling LA. 2008. Evidence for PI-3K-dependent migration of Th17-polarized cells in response to CCR2 and CCR6 agonists. J Leukoc Biol 84: 1202-1212.
81. Wegenka UM, Buschmann J, Lutticken C, Heinrich PC, Horn F. 1993. Acute-phase response factor, a nuclear factor binding to acute-phase response elements, is rapidly activated by interleukin-6 at the posttranslational level. Mol Cell Biol 13: 276-288.
82. Wilson EH, Weninger W, Hunter CA. 2010. Trafficking of immune cells in the central nervous system. J Clin Invest 120: 1368-1379.
83. Wright JF, Bennett F, Li B, Brooks J, Luxenberg DP, Whitters MJ, Tomkinson KN, Fitz LJ, Wolfman NM, Collins M, Dunussi-Joannopoulos K, Chatterjee-Kishore M, Carreno BM. 2008. The human IL-17F/IL-17A heterodimeric cytokine signals through the IL-17RA/IL-17RC receptor complex. J Immunol 181: 2799-2805.
84. Yamazaki T, Yang XO, Chung Y, Fukunaga A, Nurieva R, Pappu B, Martin-Orozco N, Kang HS, Ma L, Panopoulos AD, Craig S, Watowich SS, Jetten AM, Tian Q, Dong C. 2008. CCR6 regulates the migration of inflammatory and regulatory T cells. J Immunol 181: 8391-8401.
85. Yang J, Liao X, Agarwal MK, Barnes L, Auron PE, Stark GR. 2007. Unphosphorylated STAT3 accumulates in response to IL-6 and activates transcription by binding to NFkappaB. Genes Dev 21: 1396-1408.
86. Yao Z, Fanslow WC, Seldin MF, Rousseau AM, Painter SL, Comeau MR, Cohen JI, Spriggs MK. 1995. Herpesvirus Saimiri encodes a new cytokine, IL-17, which binds to a novel cytokine receptor. Immunity 3: 811-821.
87. Yu H, Pardoll D, Jove R. 2009. STATs in cancer inflammation and immunity: A leading role for STAT3. Nat Rev Cancer 9: 798-809.
88. Zhang D, Hu X, Qian L, O'Callaghan JP, Hong JS. 2010. Astrogliosis in CNS pathologies: Is there a role for microglia? Mol Neurobiol 41: 232-241.
89. Zhao X, Laver T, Hong SW, Twitty GBJr, Devos A, Devos M, Benveniste EN, Nozell SE. 2011. An NF-kappaB p65-cIAP2 link is necessary for mediating resistance to TNF-alpha induced cell death in gliomas. J Neurooncol 102: 367-381.