Chemokine receptor CCR6-dependent accumulation of γδ T cells in injured liver restricts hepatic inflammation and fibrosis

Hepatology

Volumn 59, Issue 2, 2014, Pages 630-642

  Hammerich, Linda ^a   Bangen, Jörg M ^a   Govaere, Olivier ^b   Zimmermann, Henning W ^a   Gassler, Nikolaus ^a   Huss, Sebastian ^c   Liedtke, Christian ^a   Prinz, Immo ^d   Lira, Sergio A ^e   Luedde, Tom ^a   Roskams, Tania ^b   Trautwein, Christian ^a   Heymann, Felix ^a   Tacke, Frank ^a  

^a UNIVERSITY HOSPITAL RWTH AACHEN   (Germany)

^b DEPARTMENT OF IMAGING AND PATHOLOGY   (Belgium)

^c UNIVERSITY OF BONN   (Germany)

^d HANNOVER MEDICAL SCHOOL   (Germany)

^e MOUNT SINAI MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CCR6; FAS LIGAND; INTERLEUKIN 17; INTERLEUKIN 22; MACROPHAGE INFLAMMATORY PROTEIN 3ALPHA;

ADOPTIVE TRANSFER; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD4+ T LYMPHOCYTE; CELL INFILTRATION; CHRONIC LIVER DISEASE; CONTROLLED STUDY; DISEASE SEVERITY; GAMMA DELTA T LYMPHOCYTE; HEPATITIS; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LIVER CELL; LIVER FIBROSIS; LIVER INJURY; LIVER PARENCHYMA; MACROPHAGE; MONONUCLEAR CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; UPREGULATION;

ANIMALS; APOPTOSIS; CASE-CONTROL STUDIES; CELL MOVEMENT; CHEMOKINE CCL20; DISEASE MODELS, ANIMAL; FEMALE; HEPATITIS; HUMANS; INTERLEUKIN-17; LIVER CIRRHOSIS; LIVER DISEASES; MALE; MICE, INBRED C57BL; MICE, KNOCKOUT; RECEPTORS, ANTIGEN, T-CELL, GAMMA-DELTA; RECEPTORS, CCR6; T-LYMPHOCYTES; T-LYMPHOCYTES, REGULATORY; TH17 CELLS; UP-REGULATION;

EID: 84893650001     PISSN: 02709139     EISSN: 15273350     Source Type: Journal    
DOI: 10.1002/hep.26697     Document Type: Article

References (29)

1. Bataller R, Brenner DA. Liver fibrosis. J Clin Invest 2005;115:209-218.
2. Zimmermann HW, Tacke F. Modification of chemokine pathways and immune cell infiltration as a novel therapeutic approach in liver inflammation and fibrosis. Inflamm Allergy Drug Targets 2011;10:509-536.
3. Shields PL, Morland CM, Salmon M, Qin S, Hubscher SG, Adams DH. Chemokine and chemokine receptor interactions provide a mechanism for selective T cell recruitment to specific liver compartments within hepatitis C-infected liver. J Immunol 1999;163:6236-6243.
4. Oo YH, Banz V. CXCR3 dependent recruitment and CCR6 mediated positioning of Th-17 cells in the inflamed liver. J Hepatol 2012;57:1044-1051.
5. Bonacchi A, Petrai I, Defranco RM, Lazzeri E, Annunziato F, Efsen E, et al. The chemokine CCL21 modulates lymphocyte recruitment and fibrosis in chronic hepatitis C. Gastroenterology 2003;125:1060-1076.
6. Racanelli V, Rehermann B. The liver as an immunological organ. Hepatology 2006;43:S54-S62.
7. Wang X, Sun R, Wei H, Tian Z. High-mobility group box 1 (HMGB1)-Toll-like receptor (TLR)4-interleukin (IL)-23-IL-17A axis in drug-induced damage-associated lethal hepatitis: interaction of gammadelta T cells with macrophages. Hepatology 2013;57:373-384.
8. Zhao N, Hao J, Ni Y, Luo W, Liang R, Cao G, et al. Vgamma4 gammadelta T cell-derived IL-17A negatively regulates NKT cell function in Con A-induced fulminant hepatitis. J Immunol 2011;187:5007-5014.
9. Cook DN, Prosser DM, Forster R, Zhang J, Kuklin NA, Abbondanzo SJ, et al. CCR6 mediates dendritic cell localization, lymphocyte homeostasis, and immune responses in mucosal tissue. Immunity 2000;12:495-503.
10. Villares R, Cadenas V, Lozano M, Almonacid L, Zaballos A, Martinez AC, Varona R. CCR6 regulates EAE pathogenesis by controlling regulatory CD4+ T-cell recruitment to target tissues. Eur J Immunol 2009;39:1671-1681.
11. Turner JE, Paust HJ, Steinmetz OM, Peters A, Riedel JH, Erhardt A, et al. CCR6 recruits regulatory T cells and Th17 cells to the kidney in glomerulonephritis. J Am Soc Nephrol 2010;21:974-985.
12. Haas JD, Gonzalez FH, Schmitz S, Chennupati V, Fohse L, Kremmer E, et al. CCR6 and NK1.1 distinguish between IL-17A and IFN-gamma-producing gammadelta effector T cells. Eur J Immunol 2009;39:3488-3497.
13. Sutton CE, Lalor SJ, Sweeney CM, Brereton CF, Lavelle EC, Mills KH. Interleukin-1 and IL-23 induce innate IL-17 production from gammadelta T cells, amplifying Th17 responses and autoimmunity. Immunity 2009;31:331-341.
14. Shimizu Y, Murata H, Kashii Y, Hirano K, Kunitani H, Higuchi K, Watanabe A. CC-chemokine receptor 6 and its ligand macrophage inflammatory protein 3alpha might be involved in the amplification of local necroinflammatory response in the liver. Hepatology 2001;34:311-319.
15. Zimmermann HW, Seidler S, Nattermann J, Gassler N, Hellerbrand C, Zernecke A, et al. Functional contribution of elevated circulating and hepatic non-classical CD14CD16 monocytes to inflammation and human liver fibrosis. PLoS One 2010;5:e11049.
16. Haas JD, Ravens S, Duber S, Sandrock I, Oberdorfer L, Kashani E, et al. Development of interleukin-17-producing gammadelta T cells is restricted to a functional embryonic wave. Immunity 2012;37:48-59.
17. Baeck C, Wehr A, Karlmark KR, Heymann F, Vucur M, Gassler N, et al. Pharmacological inhibition of the chemokine CCL2 (MCP-1) diminishes liver macrophage infiltration and steatohepatitis in chronic hepatic injury. Gut 2012;61:416-426.
18. Yamazaki T, Yang XO, Chung Y, Fukunaga A, Nurieva R, Pappu B, et al. CCR6 regulates the migration of inflammatory and regulatory T cells. J Immunol 2008;181:8391-8401.
19. Meng F, Wang K, Aoyama T, Grivennikov SI, Paik Y, Scholten D, et al. Interleukin-17 signaling in inflammatory, Kupffer, and hepatic stellate cells exacerbates liver fibrosis in mice. Gastroenterology 2012;143:765-776.
20. Radaeva S, Sun R, Jaruga B, Nguyen VT, Tian Z, Gao B. Natural killer cells ameliorate liver fibrosis by killing activated stellate cells in NKG2D-dependent and tumor necrosis factor-related apoptosis-inducing ligand-dependent manners. Gastroenterology 2006;130:435-452.
21. Kong X, Feng D, Wang H, Hong F, Bertola A, Wang FS, Gao B. Interleukin-22 induces hepatic stellate cell senescence and restricts liver fibrosis in mice. Hepatology 2012;56:1150-1159.
22. Karlmark KR, Zimmermann HW, Roderburg C, Gassler N, Wasmuth HE, Luedde T, et al. The fractalkine receptor CX3CR1 protects against liver fibrosis by controlling differentiation and survival of infiltrating hepatic monocytes. Hepatology 2010;52:1769-1782.
23. Wasmuth HE, Lammert F, Zaldivar MM, Weiskirchen R, Hellerbrand C, Scholten D, et al. Antifibrotic effects of CXCL9 and its receptor CXCR3 in livers of mice and humans. Gastroenterology 2009;137:309-319, 319.e1-3.
24. Novobrantseva TI, Majeau GR, Amatucci A, Kogan S, Brenner I, Casola S, et al. Attenuated liver fibrosis in the absence of B cells. J Clin Invest 2005;115:3072-3082.
25. Martin B, Hirota K, Cua DJ, Stockinger B, Veldhoen M. Interleukin-17-producing gammadelta T cells selectively expand in response to pathogen products and environmental signals. Immunity 2009;31:321-330.
26. Turner JE, Krebs C, Tittel AP, Paust HJ, Meyer-Schwesinger C, Bennstein SB, et al. IL-17A production by renal gammadelta T cells promotes kidney injury in crescentic GN. J Am Soc Nephrol 2012;23:1486-1495.
27. Mielke LA, Jones SA, Raverdeau M, Higgs R, Stefanska A, Groom JR, et al. Retinoic acid expression associates with enhanced IL-22 production by gammadelta T cells and innate lymphoid cells and attenuation of intestinal inflammation. J Exp Med 2013;210:1117-1124.
28. Laggner U, Di Meglio P, Perera GK, Hundhausen C, Lacy KE, Ali N, et al. Identification of a novel proinflammatory human skin-homing Vgamma9Vdelta2 T cell subset with a potential role in psoriasis. J Immunol 2011;187:2783-2793.
29. Hammerich L, Heymann F, Tacke F. Role of IL-17 and Th17 cells in liver diseases. Clin Dev Immunol 2011;2011:345803.