Neuroprotection effect of interleukin (IL)-17 secreted by reactive astrocytes is emerged from a high-level IL-17-containing environment during acute neuroinflammation

Clinical and Experimental Immunology

Volumn 175, Issue 2, 2014, Pages 268-284

  Hu, M H ^a,b   Zheng, Q F ^a,b   Jia, X Z ^a,b   Li, Y ^a,b   Dong, Y C ^a,b   Wang, C Y ^a,b   Lin, Q Y ^a,b   Zhang, F Y ^a,b   Zhao, R B ^a   Xu, H W ^a,b   Zhou, J H ^c   Yuan, H P ^a   Zhang, W H ^a   Ren, H ^a,b  

^a HARBIN MEDICAL UNIVERSITY   (China)

^b Key Laboratory of Heilongjiang Province   (China)

^c INSTITUTE OF PLANT PROTECTION   (China)

Author keywords

Autoimmune response; Experimental autoimmune uveitis; Interleukin 17; Neuroinflammation; Neuroprotection; Primary neurone culture

Indexed keywords

CILIARY NEUROTROPHIC FACTOR; GAMMA INTERFERON; INTERLEUKIN 17; INTERLEUKIN 17F; INTERLEUKIN 23P19; INTERLEUKIN 6; JANUS KINASE; NERVE GROWTH FACTOR; RETINOID RELATED ORPHAN RECEPTOR GAMMA; TRANSCRIPTION FACTOR FOXP3; TRANSCRIPTION FACTOR GATA 3; TRANSCRIPTION FACTOR T BET; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; ASTROCYTE; CALCIUM CELL LEVEL; CYTOKINE RELEASE; IMMUNE RESPONSE; NERVOUS SYSTEM INFLAMMATION; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION;

AUTOIMMUNE RESPONSE; EXPERIMENTAL AUTOIMMUNE UVEITIS; INTERLEUKIN-17; NEUROINFLAMMATION; NEUROPROTECTION; PRIMARY NEURONE CULTURE;

ANIMALS; ANTIBODIES, BLOCKING; APOPTOSIS; ASTROCYTES; AUTOIMMUNITY; INFLAMMATION; INTERFERON-GAMMA; INTERLEUKIN-17; JANUS KINASES; LEUKOCYTES, MONONUCLEAR; NEURONS; RATS; RATS, INBRED LEW; RATS, WISTAR; RNA, MESSENGER; STAT TRANSCRIPTION FACTORS; TETRADECANOYLPHORBOL ACETATE; UVEITIS;

EID: 84891589688     PISSN: 00099104     EISSN: 13652249     Source Type: Journal    
DOI: 10.1111/cei.12219     Document Type: Article

References (48)

1. Lucas SM, Rothwell NJ, Gibson RM. The role of inflammation in CNS injury and disease. Br J Pharmacol 2006; 147 (Suppl. 1):S232-240.
2. Markiewicz I, Lukomska B. The role of astrocytes in the physiology and pathology of the central nervous system. Acta Neurobiol Exp (Warsaw) 2006; 66:343-358.
3. Amadi-Obi A, Yu CR, Liu X etal. TH17 cells contribute to uveitis and scleritis and are expanded by IL-2 and inhibited by IL-27/STAT1. Nat Med 2007; 13:711-718.
4. Zhang X, Angkasekwinai P, Dong C, Tang H. Structure and function of interleukin-17 family cytokines. Protein Cell 2011; 2:26-40.
5. Liang SC, Long AJ, Bennett F etal. An IL-17F/A heterodimer protein is produced by mouse Th17 cells and induces airway neutrophil recruitment. J Immunol 2007; 179:7791-7799.
6. Gaffen SL. Structure and signalling in the IL-17 receptor family. Nat Rev Immunol 2009; 9:556-567.
7. Linden A, Laan M, Anderson GP. Neutrophils, interleukin-17A and lung disease. Eur Respir J 2005; 25:159-172.
8. Miossec P, Kolls JK. Targeting IL-17 and TH17 cells in chronic inflammation. Nat Rev Drug Discov 2012; 11:763-776.
9. Horai R, Caspi RR. Cytokines in autoimmune uveitis. J Interferon Cytokine Res 2011; 31:733-744.
10. Becher B, Segal BM. T(H)17 cytokines in autoimmune neuro-inflammation. Curr Opin Immunol 2011; 23:707-712.
11. Tzartos JS, Friese MA, Craner MJ etal. Interleukin-17 production in central nervous system-infiltrating T cells and glial cells is associated with active disease in multiple sclerosis. Am J Pathol 2008; 172:146-155.
12. Chien YH, Zeng X, Prinz I. The natural and the inducible: interleukin (IL)-17-producing gammadelta T cells. Trends Immunol 2013; 34:151-154.
13. Monteiro M, Almeida CF, Agua-Doce A, Graca L. Induced IL-17-producing invariant NKT cells require activation in presence of TGF-beta and IL-1beta. J Immunol 2013; 190:805-811.
14. Dong Y, Benveniste EN. Immune function of astrocytes. Glia 2001; 36:180-190.
15. Ma X, Reynolds SL, Baker BJ, Li X, Benveniste EN, Qin H. IL-17 enhancement of the IL-6 signaling cascade in astrocytes. J Immunol 2010; 184:4898-4906.
16. Chisholm SP, Cervi AL, Nagpal S, Lomax AE. Interleukin-17A increases neurite outgrowth from adult postganglionic sympathetic neurons. J Neurosci 2012; 32:1146-1155.
17. Hymowitz SG, Filvaroff EH, Yin JP etal. IL-17s adopt a cystine knot fold: structure and activity of a novel cytokine, IL-17F, and implications for receptor binding. EMBO J 2001; 20:5332-5341.
18. Ke Y, Liu K, Huang GQ etal. Anti-inflammatory role of IL-17 in experimental autoimmune uveitis. J Immunol 2009; 182:3183-3190.
19. Liberto CM, Albrecht PJ, Herx LM, Yong VW, Levison SW. Pro-regenerative properties of cytokine-activated astrocytes. J Neurochem 2004; 89:1092-1100.
20. John GR, Lee SC, Brosnan CF. Cytokines: powerful regulators of glial cell activation. Neuroscientist 2003; 9:10-22.
21. D'Mello SR, Galli C, Ciotti T, Calissano P. Induction of apoptosis in cerebellar granule neurons by low potassium: inhibition of death by insulin-like growth factor I and cAMP. Proc Natl Acad Sci USA 1993; 90:10989-10993.
22. Liesi P, Dahl D, Vaheri A. Laminin is produced by early rat astrocytes in primary culture. J Cell Biol 1983; 96:920-924.
23. Bilimoria PM, Bonni A. Cultures of cerebellar granule neurons. CSH Protoc 2008; 2008:pdb prot5107.
24. Jia X, Hu M, Wang C etal. Coordinated gene expression of Th17- and Treg-associated molecules correlated with resolution of the monophasic experimental autoimmune uveitis. Mol Vis 2011; 17:1493-1507.
25. Agarwal RK, Caspi RR. Rodent models of experimental autoimmune uveitis. Methods Mol Med 2004; 102:395-419.
26. Li J, Gong Q, Zhong S etal. Neutralization of the extracellular HMGB1 released by ischaemic damaged renal cells protects against renal ischaemia-reperfusion injury. Nephrol Dial Transplant 2011; 26:469-478.
27. Redmond L, Kashani AH, Ghosh A. Calcium regulation of dendritic growth via CaM kinase IV and CREB-mediated transcription. Neuron 2002; 34:999-1010.
28. Duncan RS, Hwang SY, Koulen P. Differential inositol 1, 4, 5-trisphosphate receptor signaling in a neuronal cell line. Int J Biochem Cell Biol 2007; 39:1852-1862.
29. Gao Y, Flori L, Lecardonnel J etal. Transcriptome analysis of porcine PBMCs after in vitro stimulation by LPS or PMA/ionomycin using an expression array targeting the pig immune response. BMC Genomics 2010; 11:292.
30. Annunziato L, Amoroso S, Pannaccione A etal. Apoptosis induced in neuronal cells by oxidative stress: role played by caspases and intracellular calcium ions. Toxicol Lett 2003; 139:125-133.
31. Zhang R, Qian J, Guo J, Yuan YF, Xue K. Suppression of experimental autoimmune uveoretinitis by anti-IL-17 antibody. Curr Eye Res 2009; 34:297-303.
32. Carr AJ, Vugler AA, Yu L etal. The expression of retinal cell markers in human retinal pigment epithelial cells and their augmentation by the synthetic retinoid fenretinide. Mol Vis 2011; 17:1701-1715.
33. Barber AC, Hippert C, Duran Y etal. Repair of the degenerate retina by photoreceptor transplantation. Proc Natl Acad Sci USA 2013; 110:354-359.
34. Marwaha AK, Leung NJ, McMurchy AN, Levings MK. TH17 cells in autoimmunity and immunodeficiency: protective or pathogenic? Front Immunol 2012; 3:129.
35. Domingues HS, Mues M, Lassmann H, Wekerle H, Krishnamoorthy G. Functional and pathogenic differences of Th1 and Th17 cells in experimental autoimmune encephalomyelitis. PLOS ONE 2010; 5:e15531.
36. Ogawa A, Andoh A, Araki Y, Bamba T, Fujiyama Y. Neutralization of interleukin-17 aggravates dextran sulfate sodium-induced colitis in mice. Clin Immunol 2004; 110:55-62.
37. Yang XO, Chang SH, Park H etal. Regulation of inflammatory responses by IL-17F. J Exp Med 2008; 205:1063-1075.
38. Zenewicz LA, Yancopoulos GD, Valenzuela DM, Murphy AJ, Stevens S, Flavell RA. Innate and adaptive interleukin-22 protects mice from inflammatory bowel disease. Immunity 2008; 29:947-957.
39. Dobolyi A, Vincze C, Pal G, Lovas G. The neuroprotective functions of transforming growth factor beta proteins. Int J Mol Sci 2012; 13:8219-8258.
40. Peng YP, Qiu YH, Lu JH, Wang JJ. Interleukin-6 protects cultured cerebellar granule neurons against glutamate-induced neurotoxicity. Neurosci Lett 2005; 374:192-196.
41. Stockinger B, Veldhoen M. Differentiation and function of Th17 T cells. Curr Opin Immunol 2007; 19:281-286.
42. Pierson E, Simmons SB, Castelli L, Goverman JM. Mechanisms regulating regional localization of inflammation during CNS autoimmunity. Immunol Rev 2012; 248:205-215.
43. von Toerne C, Sieg C, Kaufmann U, Diedrichs-Mohring M, Nelson PJ, Wildner G. Effector T cells driving monophasic vs. relapsing/remitting experimental autoimmune uveitis show unique pathway signatures. Mol Immunol 2010; 48:272-280.
44. Kaufmann U, Diedrichs-Mohring M, Wildner G. Dynamics of intraocular IFN-gamma, IL-17 and IL-10-producing cell populations during relapsing and monophasic rat experimental autoimmune uveitis. PLOS ONE 2012; 7:e49008.
45. Price AE, Reinhardt RL, Liang HE, Locksley RM. Marking and quantifying IL-17A-producing cells in vivo. PLOS ONE 2012; 7:e39750.
46. Fang XX, Jiang XL, Han XH, Peng YP, Qiu YH. Neuroprotection of interleukin-6 against NMDA-induced neurotoxicity is mediated by JAK/STAT3, MAPK/ERK, and PI3K/AKT signaling pathways. Cell Mol Neurobiol 2013; 33:241-251.
47. Siffrin V, Radbruch H, Glumm R etal. In vivo imaging of partially reversible th17 cell-induced neuronal dysfunction in the course of encephalomyelitis. Immunity 2010; 33:424-436.
48. Allaman I, Belanger M, Magistretti PJ. Astrocyte-neuron metabolic relationships: for better and for worse. Trends Neurosci 2011; 34:76-87.