Hepatitis C virus promotes t-helper (Th)17 responses through thymic stromal lymphopoietin production by infected hepatocytes

Hepatology

Volumn 57, Issue 4, 2013, Pages 1314-1324

  Lee, Hai Chon ^a   Sung, Sung Sang J ^a   Krueger, Peter D ^a   Jo, Yoon Ah ^a   Rosen, Hugo R ^b   Ziegler, Steven F ^c   Hahn, Young S ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

^b UNIVERSITY OF COLORADO   (United States)

^c BENAROYA RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD40 ANTIGEN; CD86 ANTIGEN; INTERLEUKIN 21; INTERLEUKIN 6; MACROPHAGE DERIVED CHEMOKINE; MACROPHAGE INFLAMMATORY PROTEIN 3ALPHA; NEUTRALIZING ANTIBODY; THYMIC STROMAL LYMPHOPOIETIN; THYMUS AND ACTIVATION REGULATED CHEMOKINE; TRANSFORMING GROWTH FACTOR BETA;

ARTICLE; CD4+ T LYMPHOCYTE; CELL ACTIVATION; CELL MATURATION; COCULTURE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; GENE OVEREXPRESSION; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; HUMAN CELL; LIVER CELL; LYMPHOCYTE DIFFERENTIATION; MONOCYTE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN SECRETION; TH17 CELL; UPREGULATION;

ANTIBODIES, NEUTRALIZING; CARCINOMA, HEPATOCELLULAR; CD4-POSITIVE T-LYMPHOCYTES; CELL COMMUNICATION; CELL DIFFERENTIATION; CELL LINE, TUMOR; CELLS, CULTURED; COCULTURE TECHNIQUES; CYTOKINES; DENDRITIC CELLS; HEPACIVIRUS; HEPATITIS C; HEPATOCYTES; HUMANS; LIVER NEOPLASMS; MONOCYTES; NF-KAPPA B; TH17 CELLS;

EID: 84876143271     PISSN: 02709139     EISSN: 15273350     Source Type: Journal    
DOI: 10.1002/hep.26128     Document Type: Article

References (29)

1. Dustin LB, Rice CM. Flying under the radar: the immunobiology of hepatitis C. Annu Rev Immunol 2007; 25: 71-99.
2. Gerlach JT, Diepolder HM, Jung MC, Gruener NH, Schraut WW, Zachoval R, et al. Recurrence of hepatitis C virus after loss of virus-specific CD4(+) T-cell response in acute hepatitis C. Gastroenterology 1999; 117: 933-941.
3. Kaplan DE, Sugimoto K, Newton K, Valiga ME, Ikeda F, Aytaman A, et al. Discordant role of CD4 T-cell response relative to neutralizing antibody and CD8 T-cell responses in acute hepatitis C. Gastroenterology 2007; 132: 654-666.
4. Smyk-Pearson S, Tester IA, Klarquist J, Palmer BE, Pawlotsky JM, Golden-Mason L, et al. Spontaneous recovery in acute human hepatitis C virus infection: functional T-cell thresholds and relative importance of CD4 help. J Virol 2008; 82: 1827-1837.
5. LeibundGut-Landmann S, Gross O, Robinson MJ, Osorio F, Slack EC, Tsoni SV, et al. Syk- and CARD9-dependent coupling of innate immunity to the induction of T helper cells that produce interleukin 17. Nat Immunol 2007; 8: 630-638.
6. Lemmers A, Moreno C, Gustot T, Marechal R, Degre D, Demetter P, et al. The interleukin-17 pathway is involved in human alcoholic liver disease. HEPATOLOGY 2009; 49: 646-657.
7. Rong G, Zhou Y, Xiong Y, Zhou L, Geng H, Jiang T, et al. Imbalance between T helper type 17 and T regulatory cells in patients with primary biliary cirrhosis: the serum cytokine profile and peripheral cell population. Clin Exp Immunol 2009; 156: 217-225.
8. Tanaka J, Watanabe N, Kido M, Saga K, Akamatsu T, Nishio A, et al. Human TSLP and TLR3 ligands promote differentiation of Th17 cells with a central memory phenotype under Th2-polarizing conditions. Clin Exp Allergy 2009; 39: 89-100.
9. Su AI, Pezacki JP, Wodicka L, Brideau AD, Supekova L, Thimme R, et al. Genomic analysis of the host response to hepatitis C virus infection. Proc Natl Acad Sci U S A 2002; 99: 15669-15674.
10. Bigger CB, Guerra B, Brasky KM, Hubbard G, Beard MR, Luxon BA, et al. Intrahepatic gene expression during chronic hepatitis C virus infection in chimpanzees. J Virol 2004; 78: 13779-13792.
11. Foster RG, Golden-Mason L, Rutebemberwa A, Rosen HR. Interleukin (IL)-17/IL-22-producing T cells enriched within the liver of patients with chronic hepatitis C viral (HCV) infection. Dig Dis Sci; 57: 381-389.
12. Ziegler SF, Liu YJ. Thymic stromal lymphopoietin in normal and pathogenic T cell development and function. Nat Immunol 2006; 7: 709-714.
13. Kato A, Favoreto SJr., Avila PC, Schleimer RP. TLR3- and Th2 cytokine-dependent production of thymic stromal lymphopoietin in human airway epithelial cells. J Immunol 2007; 179: 1080-1087.
14. Tacke RS, Lee HC, Goh C, Courtney J, Polyak SJ, Rosen HR, et al. Myeloid suppressor cells induced by hepatitis C virus suppress T-cell responses through the production of reactive oxygen species. HEPATOLOGY 2012; 55: 343-353.
15. McMahan RH, Golden-Mason L, Nishimura MI, McMahon BJ, Kemper M, Allen TM, et al. Tim-3 expression on PD-1+ HCV-specific human CTLs is associated with viral persistence, and its blockade restores hepatocyte-directed in vitro cytotoxicity. J Clin Invest 2011; 120: 4546-4557.
16. Bellecave P, Cazenave C, Rumi J, Staedel C, Cosnefroy O, Andreola ML, et al. Inhibition of hepatitis C virus (HCV) RNA polymerase by DNA aptamers: mechanism of inhibition of in vitro RNA synthesis and effect on HCV-infected cells. Antimicrob Agents Chemother 2008; 52: 2097-2110.
17. Lee HC, Headley MB, Iseki M, Ikuta K, Ziegler SF. Cutting edge: inhibition of NF-kappaB-mediated TSLP expression by retinoid X receptor. J Immunol 2008; 181: 5189-5193.
18. Lee HC, Ziegler SF. Inducible expression of the proallergic cytokine thymic stromal lymphopoietin in airway epithelial cells is controlled by NFkappaB. Proc Natl Acad Sci U S A 2007; 104: 914-919.
19. Hall CH, Kassel R, Tacke RS, Hahn YS. HCV+ hepatocytes induce human regulatory CD4+ T cells through the production of TGF-beta. PLoS One 2011; 5: e12154.
20. Soumelis V, Reche PA, Kanzler H, Yuan W, Edward G, Homey B, et al. Human epithelial cells trigger dendritic cell mediated allergic inflammation by producing TSLP. Nat Immunol 2002; 3: 673-680.
21. Hirota K, Yoshitomi H, Hashimoto M, Maeda S, Teradaira S, Sugimoto N, et al. Preferential recruitment of CCR6-expressing Th17 cells to inflamed joints via CCL20 in rheumatoid arthritis and its animal model. J Exp Med 2007; 204: 2803-2812.
22. Chang Q, Wang YK, Zhao Q, Wang CZ, Hu YZ, Wu BY. Th17 cells are increased with severity of liver inflammation in patients with chronic hepatitis C. J Gastroenterol Hepatol 2012; 27: 273-278.
23. Rowan AG, Fletcher JM, Ryan EJ, Moran B, Hegarty JE, O'Farrelly C, et al. Hepatitis C virus-specific Th17 cells are suppressed by virus-induced TGF-beta. J Immunol 2008; 181: 4485-4494.
24. Grafmueller S, Billerbeck E, Blum HE, Neumann-Haefelin C, Thimme R. Differential antigen specificity of hepatitis C virus-specific interleukin 17- and interferon gamma-producing CD8(+) T cells during chronic infection. J Infect Dis 2011; 205: 1142-1146.
25. Zhang JY, Zhang Z, Lin F, Zou ZS, Xu RN, Jin L, et al. Interleukin-17-producing CD4(+) T cells increase with severity of liver damage in patients with chronic hepatitis B. HEPATOLOGY 2010; 51: 81-91.
26. Tacke RS, Tosello-Trampont A, Nguyen V, Mullins DW, Hahn YS. Extracellular hepatitis C virus core protein activates STAT3 in human monocytes/macrophages/dendritic cells via an IL-6 autocrine pathway. J Biol Chem 2011; 286: 10847-10855.
27. Isaksen DE, Baumann H, Zhou B, Nivollet S, Farr AG, Levin SD, et al. Uncoupling of proliferation and Stat5 activation in thymic stromal lymphopoietin-mediated signal transduction. J Immunol 2002; 168: 3288-3294.
28. Takahashi K, Asabe S, Wieland S, Garaigorta U, Gastaminza P, Isogawa M, et al. Plasmacytoid dendritic cells sense hepatitis C virus-infected cells, produce interferon, and inhibit infection. Proc Natl Acad Sci U S A 2010; 107: 7431-7436.
29. Fontenot D, He H, Hanabuchi S, Nehete PN, Zhang M, Chang M, et al. TSLP production by epithelial cells exposed to immunodeficiency virus triggers DC-mediated mucosal infection of CD4+ T cells. Proc Natl Acad Sci U S A 2009; 106: 16776-16781.