Elevated Th17 cells accompanied by decreased regulatory T cells and cytokine environment in infants with biliary atresia

Pediatric Surgery International

Volumn 29, Issue 12, 2013, Pages 1249-1260

  Yang, Ying ^a   Liu, Yong Jun ^a   Tang, Shao Tao ^a   Yang, Li ^a   Yang, Jun ^a   Cao, Guo Qing ^a   Zhang, Jing Hui ^a   Wang, Xin Xin ^a   Mao, Yong Zhong ^a  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

Biliary atresia; Treg cells; Th17 cells

Indexed keywords

CD4 ANTIGEN; CYTOKINE; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 23; INTERLEUKIN 6; MESSENGER RNA; ROR GAMMA T PROTEIN; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG;

ARTICLE; BILE DUCT; BILE DUCT ATRESIA; BILIRUBIN BLOOD LEVEL; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION; HUMAN; IMMUNOHISTOCHEMISTRY; INFANT; INTERLEUKIN 17A BLOOD LEVEL; INTERLEUKIN 23 BLOOD LEVEL; JAUNDICE; MAJOR CLINICAL STUDY; MALE; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY T LYMPHOCYTE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TH17 CELL; WESTERN BLOTTING;

BILIARY ATRESIA; BLOTTING, WESTERN; CYTOKINES; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; HUMANS; INFANT; INTERLEUKIN-17; INTERLEUKIN-1BETA; INTERLEUKIN-23; INTERLEUKIN-6; LEUKOCYTES, MONONUCLEAR; LIVER; MALE; PEPTIDE FRAGMENTS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; T-LYMPHOCYTES, REGULATORY; TH17 CELLS; TRANSFORMING GROWTH FACTOR BETA1;

EID: 84890510707     PISSN: 01790358     EISSN: 14379813     Source Type: Journal    
DOI: 10.1007/s00383-013-3421-6     Document Type: Article

References (40)

1. Hartley JL, Davenport M, Kelly DA (2009) Biliary atresia. Lancet 374(9702):1704-1713. doi: 10.1016/S0140-6736(09)60946-6
2. Ghoneim EM, Sira MM, Abd Elaziz AM, Khalil FO, Sultan MM, Mahmoud AB (2011) Diagnostic value of hepatic intercellular adhesion molecule-1 expression in Egyptian infants with biliary atresia and other forms of neonatal cholestasis. Hepatol Res 41(8):763-775. doi: 10.1111/j.1872-034X.2011.00832.x
3. Bezerra JA, Tiao G, Ryckman FC, Alonso M, Sabla GE, Shneider B, Sokol RJ, Aronow BJ (2002) Genetic induction of proinflammatory immunity in children with biliary atresia. Lancet 360(9346):1653-1659. doi: 10.1016/S0140-6736(02)11603-5
4. Mack CL, Falta MT, Sullivan AK, Karrer F, Sokol RJ, Freed BM, Fontenot AP (2007) Oligoclonal expansions of CD4+ and CD8+ T-cells in the target organ of patients with biliary atresia. Gastroenterology 133(1):278-287. doi: 10.1053/j.gastro.2007.04.032
5. Lu BR, Brindley SM, Tucker RM, Lambert CL, Mack CL (2010) alpha-enolase autoantibodies cross-reactive to viral proteins in a mouse model of biliary atresia. Gastroenterology 139(5):1753-1761. doi: 10.1053/j.gastro.2010.07.042
6. Petersen C, Biermanns D, Kuske M, Schakel K, Meyer-Junghanel L, Mildenberger H (1997) New aspects in a murine model for extrahepatic biliary atresia. J Pediatr Surg 32(8):1190-1195
7. Mack CL, Tucker RM, Sokol RJ, Karrer FM, Kotzin BL, Whitington PF, Miller SD (2004) Biliary atresia is associated with CD4+ Th1 cell-mediated portal tract inflammation. Pediatr Res 56(1):79-87. doi: 10.1203/01.PDR.0000130480. 51066.FB
8. Mack CL, Tucker RM, Sokol RJ, Kotzin BL (2005) Armed CD4+ Th1 effector cells and activated macrophages participate in bile duct injury in murine biliary atresia. Clin Immunol 115(2):200-209. doi: 10.1016/j.clim.2005.01.012
9. Miethke AG, Saxena V, Shivakumar P, Sabla GE, Simmons J, Chougnet CA (2010) Post-natal paucity of regulatory T cells and control of NK cell activation in experimental biliary atresia. J Hepatol 52(5):718-726. doi: 10.1016/j.jhep.2009.12.027
10. Harrington LE, Hatton RD, Mangan PR, Turner H, Murphy TL, Murphy KM, Weaver CT (2005) Interleukin 17-producing CD4+ effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat Immunol 6(11):1123-1132. doi: 10.1038/ni1254
11. Park H, Li Z, Yang XO, Chang SH, Nurieva R, Wang YH, Wang Y, Hood L, Zhu Z, Tian Q, Dong C (2005) A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat Immunol 6(11):1133-1141. doi: 10.1038/ni1261
12. Acosta-Rodriguez EV, Napolitani G, Lanzavecchia A, Sallusto F (2007) Interleukins 1beta and 6 but not transforming growth factor-beta are essential for the differentiation of interleukin 17-producing human T helper cells. Nat Immunol 8(9):942-949. doi: 10.1038/ni1496
13. Manel N, Unutmaz D, Littman DR (2008) The differentiation of human T(H)-17 cells requires transforming growth factor-beta and induction of the nuclear receptor RORgammat. Nat Immunol 9(6):641-649. doi: 10.1038/ni.1610
14. Iwakura Y, Ishigame H (2006) The IL-23/IL-17 axis in inflammation. J Clin Invest 116(5):1218-1222. doi: 10.1172/JCI28508
15. Bettelli E, Carrier Y, Gao W, Korn T, Strom TB, Oukka M, Weiner HL, Kuchroo VK (2006) Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 441(7090):235-238. doi: 10.1038/nature04753
16. Brindley SM, Lanham AM, Karrer FM, Tucker RM, Fontenot AP, Mack CL (2012) Cytomegalovirus-specific T-cell reactivity in biliary atresia at the time of diagnosis is associated with deficits in regulatory T cells. Hepatology 55(4):1130-1138. doi: 10.1002/hep.24807
17. Lages CS, Simmons J, Chougnet CA, Miethke AG (2012) Regulatory T cells control the CD8 adaptive immune response at the time of ductal obstruction in experimental biliary atresia. Hepatology 56(1):219-227. doi: 10.1002/hep.25662
18. Gaffen SL (2008) An overview of IL-17 function and signaling. Cytokine 43(3):402-407. doi: 10.1016/j.cyto.2008.07.017
19. Eastaff-Leung N, Mabarrack N, Barbour A, Cummins A, Barry S (2010) Foxp3+ regulatory T cells, Th17 effector cells, and cytokine environment in inflammatory bowel disease. J Clin Immunol 30(1):80-89
20. Allan SE, Crome SQ, Crellin NK, Passerini L, Steiner TS, Bacchetta R, Roncarolo MG, Levings MK (2007) Activation-induced FOXP3 in human T effector cells does not suppress proliferation or cytokine production. Int Immunol 19(4):345-354. doi: 10.1093/intimm/dxm014
21. Shen LS, Wang J, Shen DF, Yuan XL, Dong P, Li MX, Xue J, Zhang FM, Ge HL, Xu D (2009) CD4(+)CD25(+)CD127(low/-) regulatory T cells express Foxp3 and suppress effector T cell proliferation and contribute to gastric cancers progression. Clin Immunol 131(1):109-118. doi: 10.1016/j.clim.2008.11.010
22. Klein S, Kretz CC, Krammer PH, Kuhn A (2010) CD127(low/-) and FoxP3(+) expression levels characterize different regulatory T-cell populations in human peripheral blood. J Invest Dermatol 130(2):492-499. doi: 10.1038/jid.2009.313
23. Loong CC, Hsieh HG, Lui WY, Chen A, Lin CY (2002) Evidence for the early involvement of interleukin 17 in human and experimental renal allograft rejection. J Pathol 197(3):322-332. doi: 10.1002/path.1117
24. Van Kooten C, Boonstra JG, Paape ME, Fossiez F, Banchereau J, Lebecque S, Bruijn JA, De Fijter JW, Van Es LA, Daha MR (1998) Interleukin-17 activates human renal epithelial cells in vitro and is expressed during renal allograft rejection. J Am Soc Nephrol 9(8):1526-1534
25. Huang F, Kao CY, Wachi S, Thai P, Ryu J, Wu R (2007) Requirement for both JAK-mediated PI3K signaling and ACT1/TRAF6/TAK1-dependent NF-kappaB activation by IL-17A in enhancing cytokine expression in human airway epithelial cells. J Immunol 179(10):6504-6513 (pii 179/10/6504)
26. Schmidt-Weber CB, Akdis M, Akdis CA (2007) TH17 cells in the big picture of immunology. J Allergy Clin Immunol 120(2):247-254. doi: 10.1016/j.jaci.2007. 06.039
27. Qian Y, Liu C, Hartupee J, Altuntas CZ, Gulen MF, Jane-Wit D, Xiao J, Lu Y, Giltiay N, Liu J, Kordula T, Zhang QW, Vallance B, Swaidani S, Aronica M, Tuohy VK, Hamilton T, Li X (2007) The adaptor Act1 is required for interleukin 17-dependent signaling associated with autoimmune and inflammatory disease. Nat Immunol 8(3):247-256. doi: 10.1038/ni1439
28. Langrish CL, Chen Y, Blumenschein WM, Mattson J, Basham B, Sedgwick JD, McClanahan T, Kastelein RA, Cua DJ (2005) IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J Exp Med 201(2):233-240. doi: 10.1084/jem.20041257
29. Yen D, Cheung J, Scheerens H, Poulet F, McClanahan T, McKenzie B, Kleinschek MA, Owyang A, Mattson J, Blumenschein W, Murphy E, Sathe M, Cua DJ, Kastelein RA, Rennick D (2006) IL-23 is essential for T cell-mediated colitis and promotes inflammation via IL-17 and IL-6. J Clin Invest 116(5):1310-1316. doi: 10.1172/JCI21404
30. Shneider BL, Brown MB, Haber B, Whitington PF, Schwarz K, Squires R, Bezerra J, Shepherd R, Rosenthal P, Hoofnagle JH, Sokol RJ (2006) A multicenter study of the outcome of biliary atresia in the United States, 1997 to 2000. J Pediatr 148(4):467-474
31. Lien TH, Chang MH, Wu JF, Chen HL, Lee HC, Chen AC, Tiao MM, Wu TC, Yang YJ, Lin CC, Lai MW, Hsu HY, Ni YH (2010) Effects of the infant stool color card screening program on 5-year outcome of biliary atresia in Taiwan. Hepatology 53(1):202-208
32. Rong G, Zhou Y, Xiong Y, Zhou L, Geng H, Jiang T, Zhu Y, Lu H, Zhang S, Wang P, Zhang B, Zhong R (2009) 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 156(2):217-225. doi: 10.1111/j.1365-2249.2009.03898.x
33. Yasumi Y, Takikawa Y, Endo R, Suzuki K (2007) Interleukin-17 as a new marker of severity of acute hepatic injury. Hepatol Res 37(4):248-254. doi: 10.1111/j.1872-034X.2007.00040.x
34. Nistala K, Moncrieffe H, Newton KR, Varsani H, Hunter P, Wedderburn LR (2008) Interleukin-17-producing T cells are enriched in the joints of children with arthritis, but have a reciprocal relationship to regulatory T cell numbers. Arthr Rheum 58(3):875-887. doi: 10.1002/art.23291
35. Beriou G, Costantino CM, Ashley CW, Yang L, Kuchroo VK, Baecher-Allan C, Hafler DA (2009) IL-17-producing human peripheral regulatory T cells retain suppressive function. Blood 113(18):4240-4249. doi: 10.1182/blood-2008-10-183251
36. Koenen HJ, Smeets RL, Vink PM, van Rijssen E, Boots AM, Joosten I (2008) Human CD25highFoxp3pos regulatory T cells differentiate into IL-17-producing cells. Blood 112(6):2340-2352. doi: 10.1182/blood-2008-01-133967
37. Wilson NJ, Boniface K, Chan JR, McKenzie BS, Blumenschein WM, Mattson JD, Basham B, Smith K, Chen T, Morel F, Lecron JC, Kastelein RA, Cua DJ, McClanahan TK, Bowman EP, de Waal Malefyt R (2007) Development, cytokine profile and function of human interleukin 17-producing helper T cells. Nat Immunol 8(9):950-957. doi: 10.1038/ni1497
38. Yang L, Anderson DE, Baecher-Allan C, Hastings WD, Bettelli E, Oukka M, Kuchroo VK, Hafler DA (2008) IL-21 and TGF-beta are required for differentiation of human T(H)17 cells. Nature 454(7202):350-352. doi: 10.1038/nature07021
39. Ogura H, Murakami M, Okuyama Y, Tsuruoka M, Kitabayashi C, Kanamoto M, Nishihara M, Iwakura Y, Hirano T (2008) Interleukin-17 promotes autoimmunity by triggering a positive-feedback loop via interleukin-6 induction. Immunity 29(4):628-636. doi: 10.1016/j.immuni.2008.07.018
40. Zhou L, Lopes JE, Chong MM, Ivanov II, Min R, Victora GD, Shen Y, Du J, Rubtsov YP, Rudensky AY, Ziegler SF, Littman DR (2008) TGF-beta-induced Foxp3 inhibits T(H)17 cell differentiation by antagonizing RORgammat function. Nature 453(7192):236-240. doi: 10.1038/nature06878