Intrahepatic IL-8 producing Foxp3+CD4+ regulatory T cells and fibrogenesis in chronic hepatitis C

Journal of Hepatology

Volumn 59, Issue 2, 2013, Pages 229-235

  Langhans, Bettina ^a   Krämer, Benjamin ^a   Louis, Marcell ^a   Nischalke, Hans Dieter ^a   Hüneburg, Robert ^a   Staratschek Jox, Andrea ^a   Odenthal, Margarethe ^b   Manekeller, Steffen ^a   Schepke, Michael ^c   Kalff, Jörg ^a   Fischer, Hans Peter ^a   Schultze, Joachim L ^a   Spengler, Ulrich ^a  

^a UNIVERSITY OF BONN   (Germany)

^b UNIVERSITY OF COLOGNE   (Germany)

^c Helios Kliniken   (Germany)

Author keywords

Fibrogenesis; Hepatic stellate cells; Hepatitis C virus; IL 8; Regulatory; T cells

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; CD4 ANTIGEN; GELATINASE A; INTERLEUKIN 8; MONOCYTE CHEMOTACTIC PROTEIN 1; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA1;

ADULT; AGED; ARTICLE; CLINICAL ARTICLE; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FIBROGENESIS; FLOW CYTOMETRY; HEPATITIS C; HUMAN; HUMAN CELL; HUMAN TISSUE; IN SITU HYBRIDIZATION; LIVER FIBROSIS; MALE; MICROARRAY ANALYSIS; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; UPREGULATION;

ALPHA-SMA; ALPHA-SMOOTH MUSCLE ACTIN; CCL2; CHEMOKINE LIGAND 2; FIBROGENESIS; FORKHEAD BOX P3; FOXP3; GARP; GLYCOPROTEIN A REPETITIONS PREDIMONANT; HCV; HEPATIC STELLATE CELLS; HEPATITIS C VIRUS; HSC; IL-8; MATRIX METALLOPROTEINASES 2; MESSENGER RNA; MMP2; MRNA; PRIMARY HUMAN HEPATIC STELLATE CELLS; REAL-TIME POLYMERASE CHAIN REACTION; REGULATORY CD4(+) T CELLS; REGULATORY T CELLS; RT-PCR; T EFFECTOR CELLS; TEFFS; TIMP1; TISSUE INHIBITOR OF METALLOPROTEINASES 1; TREGS;

ADAPTIVE IMMUNITY; ADULT; AGED; BIOLOGICAL MARKERS; DISEASE PROGRESSION; FEMALE; FIBROSIS; FORKHEAD TRANSCRIPTION FACTORS; HEPATIC STELLATE CELLS; HEPATITIS C, CHRONIC; HUMANS; INTERLEUKIN-8; LIVER; MALE; MIDDLE AGED; T-LYMPHOCYTES, REGULATORY; UP-REGULATION; YOUNG ADULT;

EID: 84880255313     PISSN: 01688278     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jhep.2013.04.011     Document Type: Article

References (49)

1. L.B. Dustin, and C.M. Rice Flying under the radar: the immunobiology of hepatitis C Annu Rev Immunol 25 2007 71 99
2. B. Rehermann, and C. Hepatitis Virus versus innate and adaptive immune responses: a tale of coevolution and coexistence J Clin Invest 119 2009 1745 1754
3. E.M. Shevach From vanilla to 28 flavors: multiple varieties of T regulatory cells Immunity 25 2006 195 201
4. M. Stassen, H. Jonuleit, C. Muller, M. Klein, C. Richter, and T. Bopp Differential regulatory capacity of CD25+ T regulatory cells and preactivated CD25+ T regulatory cells on development, functional activation, and proliferation of Th2 cells J Immunol 173 2004 267 274
5. M.A. Claassen, R.J. de Knegt, H.W. Tilanus, H.L. Janssen, and A. Boonstra Abundant numbers of regulatory T cells localize to the liver of chronic hepatitis C infected patients and limit the extent of fibrosis J Hepatol 52 2010 315 321
6. H. Ebinuma, N. Nakamoto, Y. Li, D.A. Price, E. Gostick, and B.L. Levine Identification and in vitro expansion of functional antigen-specific CD25+ FoxP3+ regulatory T cells in hepatitis C virus infection J Virol 82 2008 5043 5053
7. K. Sugimoto, F. Ikeda, J. Stadanlick, F.A. Nunes, H.J. Alter, and K.M. Chang Suppression of HCV-specific T cells without differential hierarchy demonstrated ex vivo in persistent HCV infection Hepatology 38 2003 1437 1448
8. R. Cabrera, Z. Tu, Y. Xu, R.J. Firpi, H.R. Rosen, and C. Liu An immunomodulatory role for CD4(+)CD25(+) regulatory T lymphocytes in hepatitis C virus infection Hepatology 40 2004 1062 1071
9. S.M. Rushbrook, S.M. Ward, E. Unitt, S.L. Vowler, M. Lucas, and P. Klenerman Regulatory T cells suppress in vitro proliferation of virus-specific CD8+ T cells during persistent hepatitis C virus infection J Virol 79 2005 7852 7859
10. B. Langhans, I. Braunschweiger, S. Arndt, W. Schulte, J. Satoguina, and L.E. Layland Core-specific adaptive regulatory T-cells in different outcomes of hepatitis C Clin Sci (Lond) 119 2011 97 109
11. B. Langhans, H.D. Nischalke, S. Arndt, I. Braunschweiger, J. Nattermann, and T. Sauerbruch Ribavirin exerts differential effects on functions of Cd4+ Th1, Th2, and regulatory T cell clones in hepatitis C PLoS One 7 2012 e42094
12. Y. Benjamini, D. Drai, G. Elmer, N. Kafkafi, and I. Golani Controlling the false discovery rate in behavior genetics research Behav Brain Res 125 2001 279 284
13. A. Boyum Separation of leukocytes from blood and bone marrow. Introduction Scand J Clin Lab Invest Suppl 97 1968 7
14. M. Coenen, H.D. Nischalke, B. Kramer, B. Langhans, A. Glassner, and D. Schulte Hepatitis C virus core protein induces fibrogenic actions of hepatic stellate cells via toll-like receptor 2 Lab Invest 91 2011 1375 1382
15. R. Mori, Q. Wang, K.D. Danenberg, J.K. Pinski, and P.V. Danenberg Both beta-actin and GAPDH are useful reference genes for normalization of quantitative RT-PCR in human FFPE tissue samples of prostate cancer Prostate 68 2008 1555 1560
16. L. Weglarz, I. Molin, A. Orchel, B. Parfiniewicz, and Z. Dzierzewicz Quantitative analysis of the level of p53 and p21(WAF1) mRNA in human colon cancer HT-29 cells treated with inositol hexaphosphate Acta Biochim Pol 53 2006 349 356
17. X.J. Ji, C.J. Ma, J.M. Wang, X.Y. Wu, T. Niki, and M. Hirashima HCV-infected hepatocytes drive CD4(+) CD25(+) Foxp3(+) regulatory T-cell development through the Tim-3/Gal-9 pathway Eur J Immunol 43 2012 458 467
18. J.P. Moorman, J.M. Wang, Y. Zhang, X.J. Ji, C.J. Ma, and X.Y. Wu Tim-3 pathway controls regulatory and effector T cell balance during hepatitis C virus infection J Immunol 189 2012 755 766
19. R. Wang, L. Kozhaya, F. Mercer, A. Khaitan, H. Fujii, and D. Unutmaz Expression of GARP selectively identifies activated human FOXP3+ regulatory T cells Proc Natl Acad Sci U S A 106 2009 13439 13444
20. T. Boettler, H.C. Spangenberg, C. Neumann-Haefelin, E. Panther, S. Urbani, and C. Ferrari T cells with a CD4+CD25+ regulatory phenotype suppress in vitro proliferation of virus-specific CD8+ T cells during chronic hepatitis C virus infection J Virol 79 2005 7860 7867
21. F. Bolacchi, A. Sinistro, C. Ciaprini, F. Demin, M. Capozzi, and F.C. Carducci Increased hepatitis C virus (HCV)-specific CD4+CD25+ regulatory T lymphocytes and reduced HCV-specific CD4+ T cell response in HCV-infected patients with normal versus abnormal alanine aminotransferase levels Clin Exp Immunol 144 2006 188 196
22. J.P. Wang, Y. Zhang, X. Wei, J. Li, X.P. Nan, and H.T. Yu Circulating Toll-like receptor (TLR) 2, TLR4, and regulatory T cells in patients with chronic hepatitis C APMIS 118 2010 261 270
23. A. Ulsenheimer, J.T. Gerlach, N.H. Gruener, M.C. Jung, C.A. Schirren, and W. Schraut Detection of functionally altered hepatitis C virus-specific CD4 T cells in acute and chronic hepatitis C Hepatology 37 2003 1189 1198
24. A. Perrella, L. Vitiello, L. Atripaldi, P. Conti, C. Sbreglia, and S. Altamura Elevated CD4+/CD25+ T cell frequency and function during acute hepatitis C presage chronic evolution Gut 55 2006 1370 1371
25. M.H. Heeg, A. Ulsenheimer, N.H. Gruner, R. Zachoval, M.C. Jung, and J.T. Gerlach FOXP3 expression in hepatitis C virus-specific CD4+ T cells during acute hepatitis C Gastroenterology 137 2009 1280 1288 e1281-e1286
26. S. Smyk-Pearson, L. Golden-Mason, J. Klarquist, J.R. Burton Jr., I.A. Tester, and C.C. Wang Functional suppression by FoxP3+CD4+CD25(high) regulatory T cells during acute hepatitis C virus infection J Infect Dis 197 2008 46 57
27. N. Muhanna, S. Doron, O. Wald, A. Horani, A. Eid, and O. Pappo Activation of hepatic stellate cells after phagocytosis of lymphocytes: a novel pathway of fibrogenesis Hepatology 48 2008 963 977
28. I.F. Charo, and R.M. Ransohoff The many roles of chemokines and chemokine receptors in inflammation N Engl J Med 354 2006 610 621
29. A. Rot, and U.H. von Andrian Chemokines in innate and adaptive host defense: basic chemokinese grammar for immune cells Annu Rev Immunol 22 2004 891 928
30. T. Masumoto, K. Ohkubo, K. Yamamoto, T. Ninomiya, M. Abe, and S.M. Akbar Serum IL-8 levels and localization of IL-8 in liver from patients with chronic viral hepatitis Hepatogastroenterology 45 1998 1630 1634
31. K. Shimoda, N.A. Begum, K. Shibuta, M. Mori, H.L. Bonkovsky, and B.F. Banner Interleukin-8 and hIRH (SDF1-alpha/PBSF) mRNA expression and histological activity index in patients with chronic hepatitis C Hepatology 28 1998 108 115
32. S. Mahmood, M. Sho, Y. Yasuhara, M. Kawanaka, G. Niiyama, and K. Togawa Clinical significance of intrahepatic interleukin-8 in chronic hepatitis C patients Hepatol Res 24 2002 413 419
33. T. Asselah, I. Bieche, I. Laurendeau, V. Paradis, D. Vidaud, and C. Degott Liver gene expression signature of mild fibrosis in patients with chronic hepatitis C Gastroenterology 129 2005 2064 2075
34. J.K. Oem, C. Jackel-Cram, Y.P. Li, H.N. Kang, Y. Zhou, and L.A. Babiuk Hepatitis C virus non-structural protein-2 activates CXCL-8 transcription through NF-kappaB Arch Virol 153 2008 293 301
35. J. Wagoner, M. Austin, J. Green, T. Imaizumi, A. Casola, and A. Brasier Regulation of CXCL-8 (interleukin-8) induction by double-stranded RNA signaling pathways during hepatitis C virus infection J Virol 81 2007 309 318
36. A.M. Wertheimer, S.J. Polyak, R. Leistikow, and H.R. Rosen Engulfment of apoptotic cells expressing HCV proteins leads to differential chemokine expression and STAT signaling in human dendritic cells Hepatology 45 2007 1422 1432
37. A. Balasubramanian, N. Munshi, M.J. Koziel, Z. Hu, T.J. Liang, and J.E. Groopman Structural proteins of Hepatitis C virus induce interleukin 8 production and apoptosis in human endothelial cells J Gen Virol 86 2005 3291 3301
38. H. Kadoya, M. Nagano-Fujii, L. Deng, N. Nakazono, and H. Hotta Nonstructural proteins 4A and 4B of hepatitis C virus transactivate the interleukin 8 promoter Microbiol Immunol 49 2005 265 273
39. Y. Hoshida, N. Kato, H. Yoshida, Y. Wang, M. Tanaka, and T. Goto Hepatitis C virus core protein and hepatitis activity are associated through transactivation of interleukin-8 J Infect Dis 192 2005 266 275
40. M. Radkowski, A. Bednarska, A. Horban, J. Stanczak, J. Wilkinson, and D.M. Adair Infection of primary human macrophages with hepatitis C virus in vitro: induction of tumour necrosis factor-alpha and interleukin 8 J Gen Virol 85 2004 47 59
41. H.W. Zimmermann, S. Seidler, N. Gassler, J. Nattermann, T. Luedde, and C. Trautwein Interleukin-8 is activated in patients with chronic liver diseases and associated with hepatic macrophage accumulation in human liver fibrosis PLoS One 6 2011 e21381
42. H.E. Wasmuth, and R. Weiskirchen Pathogenesis of liver fibrosis: modulation of stellate cells by chemokines Z Gastroenterol 48 2010 38 45
43. J. Napoli, G.A. Bishop, and G.W. McCaughan Increased intrahepatic messenger RNA expression of interleukins 2, 6, and 8 in human cirrhosis Gastroenterology 107 1994 789 798
44. N. Sturm, M.A. Thelu, X. Camous, G. Dimitrov, M. Ramzan, and T. Dufeu-Duchesne Characterization and role of intra-hepatic regulatory T cells in chronic hepatitis C pathogenesis J Hepatol 53 2010 25 35
45. S.M. Ward, B.C. Fox, P.J. Brown, J. Worthington, S.B. Fox, and R.W. Chapman Quantification and localisation of FOXP3+ T lymphocytes and relation to hepatic inflammation during chronic HCV infection J Hepatol 47 2007 316 324
46. M.E. Himmel, S.Q. Crome, S. Ivison, C. Piccirillo, T.S. Steiner, and M.K. Levings Human CD4+ FOXP3+ regulatory T cells produce CXCL8 and recruit neutrophils Eur J Immunol 41 2011 306 312
47. S. Clement, S. Pascarella, S. Conzelmann, C. Gonelle-Gispert, K. Guilloux, and F. Negro The hepatitis C virus core protein indirectly induces alpha-smooth muscle actin expression in hepatic stellate cells via interleukin-8 J Hepatol 52 2010 635 643
48. Y. Jia, L. Wei, D. Jiang, J. Wang, X. Cong, and R. Fei Antiviral action of interferon-alpha against hepatitis C virus replicon and its modulation by interferon-gamma and interleukin-8 J Gastroenterol Hepatol 22 2007 1278 1285
49. S. Girard, P. Shalhoub, P. Lescure, A. Sabile, D.E. Misek, and S. Hanash An altered cellular response to interferon and up-regulation of interleukin-8 induced by the hepatitis C viral protein NS5A uncovered by microarray analysis Virology 295 2002 272 283