Th17 cells: The emerging reciprocal partner of regulatory T cells in the liver

Journal of Digestive Diseases

Volumn 11, Issue 3, 2010, Pages 126-133

  Zhao, Li ^a   Qiu, De Kai ^a   Ma, Xiong ^a  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

Cytokine; Homeostasis; Inflammation; Regulatory T cell; Th17 cell

Indexed keywords

CYCLOPHOSPHAMIDE; ECALECTIN; ERYTHROPOIETIN; HISTONE; HISTONE H[71-94]; INTERLEUKIN 2; INTERLEUKIN 27; INTERLEUKIN 6; RAPAMYCIN; RETINOIC ACID; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; INTERLEUKIN 17;

ACUTE GRAFT REJECTION; AUTOIMMUNE DISEASE; EFFECTOR CELL; GRAFT REJECTION; HEPATITIS; HUMAN; IMMUNITY; LIVER; LIVER CARCINOMA; LIVER FAILURE; LOW DRUG DOSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; REVIEW; TH17 CELL; VIRUS HEPATITIS; ANIMAL; CELL COMMUNICATION; CYTOLOGY; HELPER CELL; IMMUNOLOGY; METABOLISM;

ANIMALS; CELL COMMUNICATION; HUMANS; INTERLEUKIN-17; LIVER; T-LYMPHOCYTES, HELPER-INDUCER; T-LYMPHOCYTES, REGULATORY;

EID: 77954129292     PISSN: 17512972     EISSN: 17512980     Source Type: Journal    
DOI: 10.1111/j.1751-2980.2010.00428.x     Document Type: Review

References (76)

1. Walker MR, Kasprowicz DJ, Gersuk VH. Induction of FoxP3 and acquisition of T regulatory activity by stimulated human CD4+CD25- T cells. J Clin Invest 2003, 112:1437-43.
2. Shimizu J, Yamazaki S, Takahashi T, Ishida Y, Sakaguchi S. Stimulation of CD25(+)CD4(+) regulatory T cells through GITR breaks immunological self-tolerance. Nat Immunol 2002, 3:135-42.
3. McHugh RS, Whitters MJ, Piccirillo CA. CD4(+)CD25(+) immunoregulatory T cells: gene expression analysis reveals a functional role for the glucocorticoid-induced TNF receptor. Immunity 2002, 16:311-23.
4. Asseman C, von Herrath M. About CD4pos CD25pos regulatory cells. Autoimmun Rev 2002, 1:190-7.
5. Fu S, Yopp AC, Mao X. CD4+ CD25+ CD62+ T-regulatory cell subset has optimal suppressive and proliferative potential. Am J Transplant 2004, 4:65-78.
6. Sakaguchi S, Ono M, Setoguchi R. Foxp3+ CD25+ CD4+ natural regulatory T cells in dominant self-tolerance and autoimmune disease. Immunol Rev 2006, 212:8-27.
7. Bettelli E, Carrier Y, Gao W. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 2006, 441:235-8.
8. Mosmann TR, Sad S. The expanding universe of T-cell subsets: Th1, Th2 and more. Immunol Today 1996, 17:138-46.
9. Zhou L, Ivanov II, Spolski R. IL-6 programs T(H)-17 cell differentiation by promoting sequential engagement of the IL-21 and IL-23 pathways. Nat Immunol 2007, 8:967-74.
10. Korn T, Bettelli E, Gao W. IL-21 initiates an alternative pathway to induce proinflammatory T(H)17 cells. Nature 2007, 448:484-7.
11. Veldhoen M, Hocking RJ, Atkins CJ, Locksley RM, Stockinger B. TGFbeta in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells. Immunity 2006, 24:179-89.
12. Ivanov II, McKenzie BS, Zhou L. The orphan nuclear receptor RORgammat directs the differentiation program of proinflammatory IL-17+ T helper cells. Cell 2006, 126:1121-33.
13. Brustle A, Heink S, Huber M. The development of inflammatory T(H)-17 cells requires interferon-regulatory factor 4. Nat Immunol 2007, 8:958-66.
14. Laurence A, Tato CM, Davidson TS. Interleukin-2 signaling via STAT5 constrains T helper 17 cell generation. Immunity 2007, 26:371-81.
15. Moisan J, Grenningloh R, Bettelli E, Oukka M, Ho IC. Ets-1 is a negative regulator of Th17 differentiation. J Exp Med 2007, 204:2825-35.
16. Yoshida H, Miyazaki Y, Wang S, Hamano S. Regulation of defense responses against protozoan infection by interleukin-27 and related cytokines. J Biomed Biotechnol 2007, 2007:79401.
17. Kleinschek MA, Owyang AM, Joyce-Shaikh B. IL-25 regulates Th17 function in autoimmune inflammation. J Exp Med 2007, 204:161-70.
18. Chen Z, Laurence A, Kanno Y. Selective regulatory function of Socs3 in the formation of IL-17-secreting T cells. Proc Natl Acad Sci U S A 2006, 103:8137-42.
19. Kolls JK, Linden A. Interleukin-17 family members and inflammation. Immunity 2004, 21:467-76.
20. Ikeuchi H, Kuroiwa T, Hiramatsu N. Expression of interleukin-22 in rheumatoid arthritis: potential role as a proinflammatory cytokine. Arthritis Rheum 2005, 52:1037-46.
21. Wolk K, Kunz S, Witte E, Friedrich M, Asadullah K, Sabat R. IL-22 increases the innate immunity of tissues. Immunity 2004, 21:241-54.
22. Andoh A, Zhang Z, Inatomi O. Interleukin-22, a member of the IL-10 subfamily, induces inflammatory responses in colonic subepithelial myofibroblasts. Gastroenterology 2005, 129:969-84.
23. Liang SC, Tan XY, Luxenberg DP. Interleukin (IL)-22 and IL-17 are coexpressed by Th17 cells and cooperatively enhance expression of antimicrobial peptides. J Exp Med 2006, 203:2271-9.
24. Wolk K, Witte E, Hoffmann U. IL-22 induces lipopolysaccharide-binding protein in hepatocytes: a potential systemic role of IL-22 in Crohn's disease. J Immunol 2007, 178:5973-81.
25. Zenewicz LA, Yancopoulos GD, Valenzuela DM, Murphy AJ, Karow M, Flavell RA. Interleukin-22 but not interleukin-17 provides protection to hepatocytes during acute liver inflammation. Immunity 2007, 27:647-59.
26. Cheng X, Yu X, Ding YJ. The Th17/Treg imbalance in patients with acute coronary syndrome. Clin Immunol 2008, 127:89-97.
27. Degauque N, Mariat C, Kenny J. Immunostimulatory Tim-1-specific antibody deprograms Tregs and prevents transplant tolerance in mice. J Clin Invest 2008, 118:735-41.
28. Mucida D, Park Y, Kim G. Reciprocal TH17 and regulatory T cell differentiation mediated by retinoic acid. Science 2007, 317:256-60.
29. Ichiyama K, Yoshida H, Wakabayashi Y. Foxp3 inhibits RORgammat-mediated IL-17A mRNA transcription through direct interaction with RORgammat. J Biol Chem 2008, 283:17003-8.
30. Zhou L, Lopes JE, Chong MM. TGF-beta-induced Foxp3 inhibits T(H)17 cell differentiation by antagonizing RORgammat function. Nature 2008, 453:236-40.
31. Yuan R, Maeda Y, Li W, Lu W, Cook S, Dowling P. Erythropoietin: a potent inducer of peripheral immuno/inflammatory modulation in autoimmune EAE. PLoS ONE 2008, 3:e1924.
32. Seki M, Oomizu S, Sakata KM. Galectin-9 suppresses the generation of Th17, promotes the induction of regulatory T cells, and regulates experimental autoimmune arthritis. Clin Immunol 2008, 127:78-88.
33. Kang HK, Liu M, Datta SK. Low-dose peptide tolerance therapy of lupus generates plasmacytoid dendritic cells that cause expansion of autoantigen-specific regulatory T cells and contraction of inflammatory Th17 cells. J Immunol 2007, 178:7849-58.
34. Kopf H, Rosa GM, Howard OM, Chen X. Rapamycin inhibits differentiation of Th17 cells and promotes generation of FoxP3+ T regulatory cells. Int Immunopharmacol 2007, 7:1819-24.
35. Lan RY, Cheng C, Lian ZX. Liver-targeted and peripheral blood alterations of regulatory T cells in primary biliary cirrhosis. Hepatology 2006, 43:729-37.
36. Liu B, Shi XH, Zhang FC, Zhang W, Gao LX. Antimitochondrial antibody-negative primary biliary cirrhosis: a subset of primary biliary cirrhosis. Liver Int 2008, 28:233-9.
37. Aoki CA, Roifman CM, Lian ZX. IL-2 receptor alpha deficiency and features of primary biliary cirrhosis. J Autoimmun 2006, 27:50-3.
38. Wakabayashi K, Lian ZX, Moritoki Y. IL-2 receptor alpha(-/-) mice and the development of primary biliary cirrhosis. Hepatology 2006, 44:1240-9.
39. Longhi MS, Hussain MJ, Mitry RR. Functional study of CD4+CD25+ regulatory T cells in health and autoimmune hepatitis. J Immunol 2006, 176:4484-91.
40. Longhi MS, Ma Y, Bogdanos DP, Cheeseman P, Mieli-Vergani G, Vergani D. Impairment of CD4(+)CD25(+) regulatory T-cells in autoimmune liver disease. J Hepatol 2004, 41:31-7.
41. Longhi MS, Meda F, Wang P. Expansion and de novo generation of potentially therapeutic regulatory T cells in patients with autoimmune hepatitis. Hepatology 2008, 47:581-91.
42. Chabaud M, Durand JM, Buchs N. Human interleukin-17: a T cell-derived proinflammatory cytokine produced by the rheumatoid synovium. Arthritis Rheum 1999, 42:963-70.
43. Matusevicius D, Kivisakk P, He B. Interleukin-17 mRNA expression in blood and CSF mononuclear cells is augmented in multiple sclerosis. Mult Scler 1999, 5:101-4.
44. Fujino S, Andoh A, Bamba S. Increased expression of interleukin 17 in inflammatory bowel disease. Gut 2003, 52:65-70.
45. Wilson NJ, Boniface K, Chan JR. Development, cytokine profile and function of human interleukin 17-producing helper T cells. Nat Immunol 2007, 8:950-7.
46. Wong CK, Ho CY, Li EK, Lam CW. Elevation of proinflammatory cytokine (IL-18, IL-17, IL-12) and Th2 cytokine (IL-4) concentrations in patients with systemic lupus erythematosus. Lupus 2000, 9:589-93.
47. Rong G, Zhou Y, Xiong Y. 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, 156:217-25.
48. Lan RYZ, Salunga T, Tsuneyama K. Hepatic IL-17 responses in human and murine primary biliary cirrhosis. J Autoimmun 2009, 32:43-51.
49. Harada KSS, Sato Y, Isse K, Ikeda H, Nakanuma Y. Periductal interleukin-17 production in association with biliary innate immunity contributes to the pathogenesis of cholangiopathy in primary biliary cirrhosis. Clin Exp Immunol 2009, 157:261-70.
50. Lin CY, Tsai MC, Huang CT. Liver injury is associated with enhanced regulatory T-cell activity in patients with chronic hepatitis B. J Viral Hepat 2007, 14:503-11.
51. Xu D, Fu J, Jin L. Circulating and liver resident CD4+CD25+ regulatory T cells actively influence the antiviral immune response and disease progression in patients with hepatitis B. J Immunol 2006, 177:739-47.
52. Ward SM, Fox BC, Brown PJ. Quantification and localisation of FOXP3+ T lymphocytes and relation to hepatic inflammation during chronic HCV infection. J Hepatol 2007, 47:316-24.
53. Cabrera R, Tu Z, Xu Y. An immunomodulatory role for CD4(+)CD25(+) regulatory T lymphocytes in hepatitis C virus infection. Hepatology 2004, 40:1062-71.
54. Ge JWK, Meng QH, Qi ZX, Meng FL, Fan YC. Implication of Th17 and Th1 cells in patients with chronic active hepatitis B. J Clin Immunol 2009
55. Zhang JY, ZZ, Lin F, Zou ZS. Interleukin-17-producing CD4(+) T cells increase with severity of liver damage in patients with chronic hepatitis B. Hepatology 2009, 51:81-91.
56. Lemmers AMC, Gustot T, Maréchal R. The interleukin-17 pathway is involved in human alcoholic liver disease. Hepatology 2009, 49:646-57.
57. Ormandy LA, Hillemann T, Wedemeyer H, Manns MP, Greten TF, Korangy F. Increased populations of regulatory T cells in peripheral blood of patients with hepatocellular carcinoma. Cancer Res 2005, 65:2457-64.
58. Unitt E, Rushbrook SM, Marshall A. Compromised lymphocytes infiltrate hepatocellular carcinoma: the role of T-regulatory cells. Hepatology 2005, 41:722-30.
59. Cao M, Cabrera R, Xu Y. Hepatocellular carcinoma cell supernatants increase expansion and function of CD4(+)CD25(+) regulatory T cells. Lab Invest 2007, 87:582-90.
60. Shima J, Yoshioka T, Kosugi A. Differential ability of tumor-unique and cross-reactive antigen(s) on two murine hepatoma cell lines to induce Lyt-1+2- T cells responsible for in vivo protective immunity. Biken J 1987, 30:1-8.
61. Nagayama Y, Hase W, Motoyoshi Y, Saitoh O, Sogawa R, Nakao K. Distinct responses of two hepatocellular carcinoma cell lines of a similar origin to immunotherapies targeting regulatory or effector T cells. Oncol Rep 2007, 17:1269-73.
62. Zhang JPYJ, Xu J, Pang XH. Increased intratumoral IL-17-producing cells correlate with poor survival in hepatocellular carcinoma patients. J Hepatol 2009, 50:980-9.
63. Zhang B, Rong G, Wei H. The prevalence of Th17 cells in patients with gastric cancer. Biochem Biophys Res Commun 2008, 374:533-7.
64. Kato T, Furumoto H, Ogura T. Expression of IL-17 mRNA in ovarian cancer. Biochem Biophys Res Commun 2001, 282:735-8.
65. Kryczek I, Wei S, Zou L. Cutting edge: Th17 and regulatory T cell dynamics and the regulation by IL-2 in the tumor microenvironment. J Immunol 2007, 178(11):6730-3.
66. Li W, Carper K, Zheng XX. The role of Foxp3+ regulatory T cells in liver transplant tolerance. Transplant Proc 2006, 38:3205-6.
67. Li W, Carper K, Liang Y. Anti-CD25 mAb administration prevents spontaneous liver transplant tolerance. Transplant Proc 2006, 38:3207-8.
68. Pu LY, Wang XH, Zhang F. Adoptive transfusion of ex vivo donor alloantigen-stimulated CD4(+)CD25(+) regulatory T cells ameliorates rejection of DA-to-Lewis rat liver transplantation. Surgery 2007, 142:67-73.
69. Demirkiran A, Baan CC, Kok A, Metselaar HJ, Tilanus HW, Laan LJ van der. Intrahepatic detection of FOXP3 gene expression after liver transplantation using minimally invasive aspiration biopsy. Transplantation 2007, 83:819-23.
70. Fábrega E, Lopez-Hoyos M, San Segundo D, Casafont F, Pons-Romero F. Changes in the serum levels of interleukin-17/interleukin-23 during acute rejection in liver transplantation. Liver Transpl 2009, 15:629-33.
71. Loong CC, Hsieh HG, Lui WY, Chen A, Lin CY. Evidence for the early involvement of interleukin 17 in human and experimental renal allograft rejection. J Pathol 2002, 197:322-32.
72. Vanaudenaerde BM, Dupont LJ, Wuyts WA. The role of interleukin-17 during acute rejection after lung transplantation. Eur Respir J 2006, 27:779-87.
73. Tang JL, Subbotin VM, Antonysamy MA, Troutt AB, Rao AS, Thomson AW. Interleukin-17 antagonism inhibits acute but not chronic vascular rejection. Transplantation 2001, 72:348-50.
74. Lemmers A, Moreno C, Gustot T. The interleukin-17 pathway is involved in human alcoholic liver disease. Hepatology 2009, 49:646-57.
75. Ma X, Hua J, Mohamood AR, Hamad AR, Ravi R, Li Z. A high-fat diet and regulatory T cells influence susceptibility to endotoxin-induced liver injury. Hepatology 46:1519-29.
76. Albano E, Vidali M. Immune mechanisms in alcoholic liver disease. Genes Nutr 2009, Oct 7. [Epub ahead of print