IL-17A plays a critical role in the pathogenesis of liver fibrosis through hepatic stellate cell activation

Journal of Immunology

Volumn 191, Issue 4, 2013, Pages 1835-1844

  Tan, Zhongming ^a,b,c,d   Qian, Xiaofeng ^a,b   Jiang, Runqiu ^a,b   Liu, Qianghui ^a,b   Wang, Youjing ^a,b   Chen, Chen ^a,b   Wang, Xuehao ^a,b   Ryffel, Bernhard ^c,d   Sun, Beicheng ^a,b  

^a NANJING MEDICAL UNIVERSITY   (China)

^b BEIJING HOSPITAL   (China)

^c UNIVERSITÉ D'ORLÉANS   (France)

^d UNIVERSITY OF CAPE TOWN   (South Africa)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; COLLAGEN; CYTOKINE; INTERLEUKIN 17; INTERLEUKIN 17 RECEPTOR; INTERLEUKIN 6; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; RETINOID RELATED ORPHAN RECEPTOR GAMMA; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CHEMOTAXIS; CHRONIC HEPATITIS; CLINICAL ARTICLE; CONTROLLED STUDY; ENZYME INHIBITION; GENE EXPRESSION; HEPATITIS B; HUMAN; HUMAN CELL; HUMAN TISSUE; INFLAMMATION; INFLAMMATORY INFILTRATE; LIVER CELL CARCINOMA; LIVER CIRRHOSIS; LIVER FIBROSIS; LIVER HEMANGIOMA; LIVER NECROSIS; LIVER RESECTION; MALE; MOUSE; NEUTROPHIL; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; STELLATE CELL; T LYMPHOCYTE;

ACTINS; ADULT; ANIMALS; CARBON TETRACHLORIDE POISONING; CARCINOMA, HEPATOCELLULAR; COLLAGEN; CYTOKINES; DRUG-INDUCED LIVER INJURY; FEMALE; GENE EXPRESSION REGULATION; HEMANGIOMA; HEPATECTOMY; HEPATIC STELLATE CELLS; HEPATITIS B, CHRONIC; HEPATITIS, ANIMAL; HUMANS; INTERLEUKIN-17; LIVER CIRRHOSIS; LIVER NEOPLASMS; MALE; MAP KINASE SIGNALING SYSTEM; MICE; MICE, KNOCKOUT; MIDDLE AGED; NEUTROPHILS; NUCLEAR RECEPTOR SUBFAMILY 1, GROUP F, MEMBER 3; PROTEIN KINASE INHIBITORS; RECEPTORS, INTERLEUKIN-17; RECOMBINANT PROTEINS; TH17 CELLS; TRANSFORMING GROWTH FACTOR BETA;

EID: 84881393577     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1203013     Document Type: Article

References (48)

1. Friedman, S. L. 2003. Liver fibrosis - from bench to bedside. J. Hepatol. 38 (Suppl. 1): S38-S53.
2. Liu, C., M. D. Gaça, E. S. Swenson, V. F. Vellucci, M. Reiss, and R. G. Wells. 2003. Smads 2 and 3 are differentially activated by transforming growth factorbeta (TGF-beta ) in quiescent and activated hepatic stellate cells. Constitutive nuclear localization of Smads in activated cells is TGF-beta-independent. J. Biol. Chem. 278: 11721-11728.
3. Bioulac-Sage, P., M. E. Lafon, J. Saric, and C. Balabaud. 1990. Nerves and perisinusoidal cells in human liver. J. Hepatol. 10: 105-112.
4. Cassiman, D., and T. Roskams. 2002. Beauty is in the eye of the beholder: emerging concepts and pitfalls in hepatic stellate cell research. J. Hepatol. 37: 527-535.
5. Roulot, D., A. M. Sevcsik, T. Coste, A. D. Strosberg, and S. Marullo. 1999. Role of transforming growth factor beta type II receptor in hepatic fibrosis: studies of human chronic hepatitis C and experimental fibrosis in rats. Hepatology 29: 1730-1738.
6. Hammerich, L., F. Heymann, and F. Tacke. 2011. Role of IL-17 and Th17 cells in liver diseases. Clin. Dev. Immunol. 2011: 345803.
7. Miossec, P., T. Korn, and V. K. Kuchroo. 2009. Interleukin-17 and type 17 helper T cells. N. Engl. J. Med. 361: 888-898.
8. Gasse, P., N. Riteau, R. Vacher, M. L. Michel, A. Fautrel, F. di Padova, L. Fick, S. Charron, V. Lagente, G. Eberl, et al. 2011. IL-1 and IL-23 mediate early IL-17A production in pulmonary inflammation leading to late fibrosis. PLoS ONE 6: e23185.
9. Cortez, D. M., M. D. Feldman, S. Mummidi, A. J. Valente, B. Steffensen, M. Vincenti, J. L. Barnes, and B. Chandrasekar. 2007. IL-17 stimulates MMP-1 expression in primary human cardiac fibroblasts via p38 MAPK- and ERK1/2- dependent C/EBP-beta, NF-kappaB, and AP-1 activation. Am. J. Physiol. Heart Circ. Physiol. 293: H3356-H3365.
10. Lafdil, F., A. M. Miller, S. H. Ki, and B. Gao. 2010. Th17 cells and their associated cytokines in liver diseases. Cell. Mol. Immunol. 7: 250-254.
11. Ye, P., F. H. Rodriguez, S. Kanaly, K. L. Stocking, J. Schurr, P. Schwarzenberger, P. Oliver, W. Huang, P. Zhang, J. Zhang, et al. 2001. Requirement of interleukin 17 receptor signaling for lung CXC chemokine and granulocyte colony-stimulating factor expression, neutrophil recruitment, and host defense. J. Exp. Med. 194: 519-527.
12. Lochner, M., L. Peduto, M. Cherrier, S. Sawa, F. Langa, R. Varona, D. Riethmacher, M. Si-Tahar, J. P. Di Santo, and G. Eberl. 2008. In vivo equilibrium of proinflammatory IL-17+ and regulatory IL-10+ Foxp3+ RORgamma t+ T cells. J. Exp. Med. 205: 1381-1393.
13. Le Pabic, H., D. Bonnier, U. M. Wewer, A. Coutand, O. Musso, G. Baffet, B. Clément, and N. Théret. 2003. ADAM12 in human liver cancers: TGF-betaregulated expression in stellate cells is associated with matrix remodeling. Hepatology 37: 1056-1066.
14. Cowley, S., H. Paterson, P. Kemp, and C. J. Marshall. 1994. Activation of MAP kinase kinase is necessary and sufficient for PC12 differentiation and for transformation of NIH 3T3 cells. Cell 77: 841-852.
15. Cuenda, A., J. Rouse, Y. N. Doza, R. Meier, P. Cohen, T. F. Gallagher, P. R. Young, and J. C. Lee. 1995. SB 203580 is a specific inhibitor of a MAP kinase homologue which is stimulated by cellular stresses and interleukin-1. FEBS Lett. 364: 229-233.
16. Schnyder-Candrian, S., D. Togbe, I. Couillin, I. Mercier, F. Brombacher, V. Quesniaux, F. Fossiez, B. Ryffel, and B. Schnyder. 2006. Interleukin-17 is a negative regulator of established allergic asthma. J. Exp. Med. 203: 2715-2725.
17. Loo, D. T. 2011. In situ detection of apoptosis by the TUNEL assay: an overview of techniques. Methods Mol. Biol. 682: 3-13.
18. Suzuki, S., L. H. Toledo-Pereyra, F. J. Rodriguez, and D. Cejalvo. 1993. Neutrophil infiltration as an important factor in liver ischemia and reperfusion injury. Modulating effects of FK506 and cyclosporine. Transplantation 55: 1265-1272.
19. Doz, E., N. Noulin, E. Boichot, I. Guénon, L. Fick, M. Le Bert, V. Lagente, B. Ryffel, B. Schnyder, V. F. Quesniaux, and I. Couillin. 2008. Cigarette smokeinduced pulmonary inflammation is TLR4/MyD88 and IL-1R1/MyD88 signaling dependent. J. Immunol. 180: 1169-1178.
20. Tan, Z., R. Jiang, X. Wang, Y. Wang, L. Lu, Q. Liu, S. G. Zheng, B. Sun, and B. Ryffel. 2013. RORγt+IL-17+ neutrophils play a critical role in hepatic ischemia-reperfusion injury. J. Mol. Cell Biol. 5: 143-146.
21. Jovanovic, D. V., J. A. Di Battista, J. Martel-Pelletier, F. C. Jolicoeur, Y. He, M. Zhang, F. Mineau, and J. P. Pelletier. 1998. IL-17 stimulates the production and expression of proinflammatory cytokines, IL-beta and TNF-alpha, by human macrophages. J. Immunol. 160: 3513-3521.
22. Lamkanfi, M., L. V. Walle, and T. D. Kanneganti. 2011. Deregulated inflammasome signaling in disease. Immunol. Rev. 243: 163-173.
23. Pappu, R., V. Ramirez-Carrozzi, N. Ota, W. Ouyang, and Y. Hu. 2010. The IL-17 family cytokines in immunity and disease. J. Clin. Immunol. 30: 185-195.
24. Lemmers, A., C. Moreno, T. Gustot, R. Maréchal, D. Degré, P. Demetter, P. de Nadai, A. Geerts, E. Quertinmont, V. Vercruysse, et al. 2009. The interleukin-17 pathway is involved in human alcoholic liver disease. Hepatology 49: 646-657.
25. Mantovani, A., M. A. Cassatella, C. Costantini, and S. Jaillon. 2011. Neutrophils in the activation and regulation of innate and adaptive immunity. Nat. Rev. Immunol. 11: 519-531.
26. Cua, D. J., and C. M. Tato. 2010. Innate IL-17-producing cells: the sentinels of the immune system. Nat. Rev. Immunol. 10: 479-489.
27. Ajibade, A. A., Q. Wang, J. Cui, J. Zou, X. Xia, M. Wang, Y. Tong, W. Hui, D. Liu, B. Su, et al. 2012. TAK1 negatively regulates NF-κB and p38 MAP kinase activation in Gr-1+CD11b+ neutrophils. Immunity 36: 43-54.
28. Roderfeld, M., A. Geier, C. G. Dietrich, E. Siewert, B. Jansen, C. Gartung, and E. Roeb. 2006. Cytokine blockade inhibits hepatic tissue inhibitor of metalloproteinase-1 expression and up-regulates matrix metalloproteinase-9 in toxic liver injury. Liver Int. 26: 579-586.
29. Lisbonne, M., A. L'Helgoualc'h, G. Nauwelaers, B. Turlin, C. Lucas, A. Herbelin, C. Piquet-Pellorce, and M. Samson. 2011. Invariant natural killer T-cell-deficient mice display increased CCl- -induced hepatitis associated with CXCL1 overexpression and neutrophil infiltration. Eur. J. Immunol. 41: 1720-1732.
30. Ather, J. L., K. Ckless, R. Martin, K. L. Foley, B. T. Suratt, J. E. Boyson, K. A. Fitzgerald, R. A. Flavell, S. C. Eisenbarth, and M. E. Poynter. 2011. Serum amyloid A activates the NLRP3 inflammasome and promotes Th17 allergic asthma in mice. J. Immunol. 187: 64-73.
31. Fujino, S., A. Andoh, S. Bamba, A. Ogawa, K. Hata, Y. Araki, T. Bamba, and Y. Fujiyama. 2003. Increased expression of interleukin 17 in inflammatory bowel disease. Gut 52: 65-70.
32. Chabaud, M., P. Garnero, J. M. Dayer, P. A. Guerne, F. Fossiez, and P. Miossec. 2000. Contribution of interleukin 17 to synovium matrix destruction in rheumatoid arthritis. Cytokine 12: 1092-1099.
33. Sadik, C. D., N. D. Kim, E. Alekseeva, and A. D. Luster. 2011. IL-17RA signaling amplifies antibody-induced arthritis. PLoS One 6: e26342.
34. Kolls, J. K., and A. Lindén. 2004. Interleukin-17 family members and inflammation. Immunity 21: 467-476.
35. Wilson, M. S., S. K. Madala, T. R. Ramalingam, B. R. Gochuico, I. O. Rosas, A. W. Cheever, and T. A. Wynn. 2010. Bleomycin and IL-1beta-mediated pulmonary fibrosis is IL-17A dependent. J. Exp. Med. 207: 535-552.
36. Sharma, A. K., D. J. LaPar, Y. Zhao, L. Li, C. L. Lau, I. L. Kron, Y. Iwakura, M. D. Okusa, and V. E. Laubach. 2011. Natural killer T cell-derived IL-17 mediates lung ischemia-reperfusion injury. Am. J. Respir. Crit. Care Med. 183: 1539-1549.
37. Hamada, S., M. Umemura, T. Shiono, K. Tanaka, A. Yahagi, M. D. Begum, K. Oshiro, Y. Okamoto, H. Watanabe, K. Kawakami, et al. 2008. IL-17A produced by gammadelta T cells plays a critical role in innate immunity against listeria monocytogenes infection in the liver. J. Immunol. 181: 3456-3463.
38. Chang, Y., J. Nadigel, N. Boulais, J. Bourbeau, F. Maltais, D. H. Eidelman, and Q. Hamid. 2011. CD8 positive T cells express IL-17 in patients with chronic obstructive pulmonary disease. Respir. Res. 12: 43.
39. Takahashi, N., I. Vanlaere, R. de Rycke, A. Cauwels, L. A. Joosten, E. Lubberts, W. B. van den Berg, and C. Libert. 2008. IL-17 produced by Paneth cells drives TNF-induced shock. J. Exp. Med. 205: 1755-1761.
40. Moran, E. M., R. Heydrich, C. T. Ng, T. P. Saber, J. McCormick, J. Sieper, H. Appel, U. Fearon, and D. J. Veale. 2011. IL-17A expression is localised to both mononuclear and polymorphonuclear synovial cell infiltrates. PLoS One 6: e24048.
41. Li, L., L. Huang, A. L. Vergis, H. Ye, A. Bajwa, V. Narayan, R. M. Strieter, D. L. Rosin, and M. D. Okusa. 2010. IL-17 produced by neutrophils regulates IFN-gamma-mediated neutrophil migration in mouse kidney ischemia-reperfusion injury. J. Clin. Invest. 120: 331-342.
42. Meng, F., K. Wang, T. Aoyama, S. I. Grivennikov, Y. Paik, D. Scholten, M. Cong, K. Iwaisako, X. Liu, M. Zhang, et al. 2012. Interleukin-17 signaling in inflammatory, Kupffer cells, and hepatic stellate cells exacerbates liver fibrosis in mice. Gastroenterology 143:765-776.e761-763.
43. Mi, S., Z. Li, H. Z. Yang, H. Liu, J. P. Wang, Y. G. Ma, X. X. Wang, H. Z. Liu, W. Sun, and Z. W. Hu. 2011. Blocking IL-17A promotes the resolution of pulmonary inflammation and fibrosis via TGF-beta1-dependent and -independent mechanisms. J. Immunol. 187: 3003-3014.
44. Pearson, G., F. Robinson, T. Beers Gibson, B. E. Xu, M. Karandikar, K. Berman, and M. H. Cobb. 2001. Mitogen-activated protein (MAP) kinase pathways: regulation and physiological functions. Endocr. Rev. 22: 153-183.
45. Rahman, M. S., A. Yamasaki, J. Yang, L. Shan, A. J. Halayko, and A. S. Gounni. 2006. IL-17A induces eotaxin-1/CC chemokine ligand 11 expression in human airway smooth muscle cells: role of MAPK (Erk1/2, JNK, and p38) pathways. J. Immunol. 177: 4064-4071.
46. Saleh, A., L. Shan, A. J. Halayko, S. Kung, and A. S. Gounni. 2009. Critical role for STAT3 in IL-17A-mediated CCL11 expression in human airway smooth muscle cells. J. Immunol. 182: 3357-3365.
47. Schnabl, B., C. A. Bradham, B. L. Bennett, A. M. Manning, B. Stefanovic, and D. A. Brenner. 2001. TAK1/JNK and p38 have opposite effects on rat hepatic stellate cells. Hepatology 34: 953-963.
48. Valente, A. J., T. Yoshida, J. D. Gardner, N. Somanna, P. Delafontaine, and B. Chandrasekar. 2012. Interleukin-17A stimulates cardiac fibroblast proliferation and migration via negative regulation of the dual-specificity phosphatase MKP-1/DUSP-1. Cell. Signal. 24: 560-568.