Foxp3+ regulatory T cells, Th17 effector cells, and cytokine environment in inflammatory bowel disease

Journal of Clinical Immunology

Volumn 30, Issue 1, 2010, Pages 80-89

  Eastaff Leung, Nicola ^a,b   Mabarrack, Nicholas ^b   Barbour, Angela ^b   Cummins, Adrian ^a,c   Barry, Simon ^b  

^a QUEEN ELIZABETH HOSPITAL   (Australia)

^b UNIVERSITY OF ADELAIDE   (Australia)

^c UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

Crohn's disease; Inflammatory bowel disease; Regulatory T cells; Th17 effector cells; Ulcerative colitis

Indexed keywords

AZATHIOPRINE; CORTICOSTEROID; CYTOKINE; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 21; INTERLEUKIN 23; INTERLEUKIN 6; MERCAPTOPURINE; MESALAZINE; MESSENGER RNA; METHOTREXATE; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA;

ARTICLE; BLOOD SAMPLING; CLINICAL ARTICLE; CONTROLLED STUDY; CROHN DISEASE; DISEASE ACTIVITY; EFFECTOR CELL; ENTERITIS; FLOW CYTOMETRY; HUMAN; HUMAN TISSUE; INTESTINE BIOPSY; INTESTINE MUCOSA; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY T LYMPHOCYTE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TH17 CELL; ULCERATIVE COLITIS;

ADULT; AGED; CELL COUNT; CELLS, CULTURED; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; INFLAMMATORY BOWEL DISEASES; INTERLEUKIN-17; INTERLEUKIN-1BETA; INTERLEUKIN-6; INTESTINAL MUCOSA; MALE; MIDDLE AGED; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES, REGULATORY; TRANSFORMING GROWTH FACTOR BETA; YOUNG ADULT;

EID: 77249137663     PISSN: 02719142     EISSN: 15732592     Source Type: Journal    
DOI: 10.1007/s10875-009-9345-1     Document Type: Article

References (56)

1. CD Packey RB Sartor 2008 Interplay of commensal and pathogenic bacteria, genetic mutations, and immunoregulatory defects in the pathogenesis of inflammatory bowel diseases J Intern Med 263 597 606 10.1111/j.1365-2796.2008. 01962.x 18479259 (Pubitemid 351678591)
2. R Duchmann I Kaiser E Hermann W Mayet K Ewe KH Meyer zum Buschenfelde 1995 Tolerance exists towards resident intestinal flora but is broken in active inflammatory bowel disease (IBD) Clin Exp Immunol 102 448 455 8536356
3. S Sakaguchi N Sakaguchi M Asano M Itoh M Toda 1995 Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor alpha-chains (CD25). Breakdown of a single mechanism of self-tolerance causes various autoimmune diseases J Immunol 155 1151 1164 7636184
4. SE Allan SQ Crome NK Crellin L Passerini TS Steiner R Bacchetta, et al. 2007 Activation-induced FOXP3 in human T effector cells does not suppress proliferation or cytokine production Int Immunol 19 345 354 10.1093/intimm/ dxm014 17329235 (Pubitemid 46523383)
5. S Hori T Nomura S Sakaguchi 2003 Control of regulatory T cell development by the transcription factor Foxp3 Science 299 1057 1061 10.1126/science.1079490 12522256 (Pubitemid 36222930)
6. M Miyara S Sakaguchi 2007 Natural regulatory T cells: mechanisms of suppression Trends Mol Med 13 108 116 10.1016/j.molmed.2007.01.003 17257897 (Pubitemid 46341958)
7. C Mottet HH Uhlig F Powrie 2003 Cutting edge: cure of colitis by CD4+CD25+ regulatory T cells J Immunol 170 3939 3943 12682220
8. CL Bennett J Christie F Ramsdell ME Brunkow PJ Ferguson L Whitesell, et al. 2001 The immune dysregulation, polyendocrinopathy, enteropathy, X-linked syndrome (IPEX) is caused by mutations of FOXP3 Nat Genet 27 20 21 10.1038/83713 11137993 (Pubitemid 32044513)
9. RS Wildin F Ramsdell J Peake F Faravelli JL Casanova N Buist, et al. 2001 X-linked neonatal diabetes mellitus, enteropathy and endocrinopathy syndrome is the human equivalent of mouse scurfy Nat Genet 27 18 20 10.1038/83707 11137992 (Pubitemid 32044512)
10. E Bettelli Y Carrier W Gao T Korn TB Strom M Oukka, et al. 2006 Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells Nature 441 235 238 10.1038/nature04753 16648838
11. M Veldhoen RJ Hocking CJ Atkins RM Locksley B Stockinger 2006 TGFbeta in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells Immunity 24 179 189 10.1016/j.immuni.2006.01.001 16473830 (Pubitemid 43214587)
12. NJ Wilson K Boniface JR Chan BS McKenzie WM Blumenschein JD Mattson, et al. 2007 Development, cytokine profile and function of human interleukin 17-producing helper T cells Nat Immunol 8 950 957 10.1038/ni1497 17676044 (Pubitemid 47300009)
13. EV Acosta-Rodriguez G Napolitani A Lanzavecchia F Sallusto 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 8 942 949 10.1038/ni1496 17676045 (Pubitemid 47300008)
14. N Manel D Unutmaz DR Littman 2008 The differentiation of human T(H)-17 cells requires transforming growth factor-beta and induction of the nuclear receptor RORgammat Nat Immunol 9 641 649 10.1038/ni.1610 18454151 (Pubitemid 351714729)
15. E Volpe N Servant R Zollinger SI Bogiatzi P Hupe E Barillot, et al. 2008 A critical function for transforming growth factor-beta, interleukin 23 and proinflammatory cytokines in driving and modulating human T(H)-17 responses Nat Immunol 9 650 657 10.1038/ni.1613 18454150 (Pubitemid 351712635)
16. L Yang DE Anderson C Baecher-Allan WD Hastings E Bettelli M Oukka, et al. 2008 IL-21 and TGF-beta are required for differentiation of human T(H)17 cells Nature 454 350 352 10.1038/nature07021 18469800
17. S LeibundGut-Landmann O Gross MJ Robinson F Osorio EC Slack SV Tsoni, et al. 2007 Syk- and CARD9-dependent coupling of innate immunity to the induction of T helper cells that produce interleukin 17 Nat Immunol 8 630 638 10.1038/ni1460 17450144 (Pubitemid 46785127)
18. P Ye FH Rodriguez S Kanaly KL Stocking J Schurr P Schwarzenberger, et al. 2001 Requirement of interleukin 17 receptor signaling for lung CXC chemokine and granulocyte colony-stimulating factor expression, neutrophil recruitment, and host defense J Exp Med 194 519 527 10.1084/jem.194.4.519 11514607 (Pubitemid 32835046)
19. SL Gaffen 2008 An overview of IL-17 function and signaling Cytokine 43 402 407 10.1016/j.cyto.2008.07.017 18701318
20. OH Nielsen I Kirman N Rudiger J Hendel B Vainer 2003 Upregulation of interleukin-12 and -17 in active inflammatory bowel disease Scand J Gastroenterol 38 180 185 10.1080/00365520310000672 12678335
21. S Fujino A Andoh S Bamba A Ogawa K Hata Y Araki, et al. 2003 Increased expression of interleukin 17 in inflammatory bowel disease Gut 52 65 70 10.1136/gut.52.1.65 12477762 (Pubitemid 36020767)
22. A Andoh Y Yagi M Shioya A Nishida T Tsujikawa Y Fujiyama 2008 Mucosal cytokine network in inflammatory bowel disease World J Gastroenterol 14 5154 5161 10.3748/wjg.14.5154 18777592
23. X Cheng X Yu YJ Ding QQ Fu JJ Xie TT Tang, et al. 2008 The Th17/Treg imbalance in patients with acute coronary syndrome Clin Immunol 127 89 97 18294918
24. K Nistala H Moncrieffe KR Newton H Varsani P Hunter LR Wedderburn 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 Arthritis Rheum 58 875 887 10.1002/art.23291 18311821
25. G Rong Y Zhou Y Xiong L Zhou H Geng T Jiang, et al. 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 156 217 225 10.1111/j.1365-2249.2009.03898.x 19302244
26. I Ricciardelli KJ Lindley M Londei S Quaratino 2008 Anti tumour necrosis-alpha therapy increases the number of FOXP3 regulatory T cells in children affected by Crohn's disease Immunology 125 178 183 10.1111/j.1365-2567. 2008.02839.x 18422560
27. A Fattorossi A Battaglia A Buzzonetti F Ciaraffa G Scambia A Evoli 2005 Circulating and thymic CD4 CD25 T regulatory cells in myasthenia gravis: effect of immunosuppressive treatment Immunology 116 134 141 10.1111/j.1365-2567.2005. 02220.x 16108825 (Pubitemid 41208360)
28. M Braitch S Harikrishnan RA Robins C Nichols AJ Fahey L Showe, et al. 2009 Glucocorticoids increase CD4CD25 cell percentage and Foxp3 expression in patients with multiple sclerosis Acta Neurol Scand 119 239 245 10.1111/j.1600-0404.2008.01090.x 18771523
29. H Kopf GM de la Rosa OM Howard X Chen 2007 Rapamycin inhibits differentiation of Th17 cells and promotes generation of FoxP3+ T regulatory cells Int Immunopharmacol 7 1819 1824 10.1016/j.intimp.2007.08.027 17996694 (Pubitemid 350046435)
30. S Makita T Kanai S Oshima K Uraushihara T Totsuka T Sawada, et al. 2004 CD4+CD25bright T cells in human intestinal lamina propria as regulatory cells J Immunol 173 3119 3130 15322172
31. B Sitohy S Hammarstrom A Danielsson ML Hammarstrom 2008 Basal lymphoid aggregates in ulcerative colitis colon: a site for regulatory T cell action Clin Exp Immunol 151 326 333 18190460
32. QT Yu M Saruta A Avanesyan PR Fleshner AH Banham KA Papadakis 2007 Expression and functional characterization of FOXP3+ CD4+ regulatory T cells in ulcerative colitis Inflamm Bowel Dis 13 191 199 10.1002/ibd.20053 17206665 (Pubitemid 46806228)
33. J Maul C Loddenkemper P Mundt E Berg T Giese A Stallmach, et al. 2005 Peripheral and intestinal regulatory CD4+ CD25(high) T cells in inflammatory bowel disease Gastroenterology 128 1868 1878 10.1053/j.gastro.2005.03.043 15940622 (Pubitemid 40824698)
34. G Beriou CM Costantino CW Ashley L Yang VK Kuchroo C Baecher-Allan, et al. 2009 IL-17-producing human peripheral regulatory T cells retain suppressive function Blood 113 4240 4249 10.1182/blood-2008-10-183251 19171879
35. HJ Koenen RL Smeets PM Vink E van Rijssen AM Boots I Joosten 2008 Human CD25highFoxp3pos regulatory T cells differentiate into IL-17-producing cells Blood 112 2340 2352 10.1182/blood-2008-01-133967 18617638
36. KA Brown SJ Back ED Ruchelli J Markowitz M Mascarenhas R Verma, et al. 2002 Lamina propria and circulating interleukin-6 in newly diagnosed pediatric inflammatory bowel disease patients Am J Gastroenterol 97 2603 2608 10.1111/j.1572-0241.2002.06030.x 12385446
37. K Mitsuyama A Toyonaga E Sasaki O Ishida H Ikeda O Tsuruta, et al. 1995 Soluble interleukin-6 receptors in inflammatory bowel disease: relation to circulating interleukin-6 Gut 36 45 49 10.1136/gut.36.1.45 7890234
38. JM Reimund C Wittersheim S Dumont CD Muller JS Kenney R Baumann, et al. 1996 Increased production of tumour necrosis factor-alpha interleukin-1 beta, and interleukin-6 by morphologically normal intestinal biopsies from patients with Crohn's disease Gut 39 684 689 10.1136/gut.39.5.684 9026483
39. A Woywodt P Neustock A Kruse K Schwarting D Ludwig EF Stange, et al. 1994 Cytokine expression in intestinal mucosal biopsies. In situ hybridisation of the mRNA for interleukin-1 beta, interleukin-6 and tumour necrosis factor-alpha in inflammatory bowel disease Eur Cytokine Netw 5 387 395 7841354
40. SY Hwang HY Kim 2005 Expression of IL-17 homologs and their receptors in the synovial cells of rheumatoid arthritis patients Mol Cells 19 180 184 15879699
41. D Matusevicius P Kivisakk B He N Kostulas V Ozenci S Fredrikson, et al. 1999 Interleukin-17 mRNA expression in blood and CSF mononuclear cells is augmented in multiple sclerosis Mult Scler 5 101 104 10335518
42. C Lock G Hermans R Pedotti A Brendolan E Schadt H Garren, et al. 2002 Gene-microarray analysis of multiple sclerosis lesions yields new targets validated in autoimmune encephalomyelitis Nat Med 8 500 508 10.1038/nm0502-500 11984595 (Pubitemid 34546753)
43. DM Bullens E Truyen L Coteur E Dilissen PW Hellings LJ Dupont, et al. 2006 IL-17 mRNA in sputum of asthmatic patients: linking T cell driven inflammation and granulocytic influx? Respir Res 7 135 10.1186/1465-9921-7-135 17083726 (Pubitemid 44774212)
44. CK Wong CY Ho EK Li CW Lam 2000 Elevation of proinflammatory cytokine (IL-18, IL-17, IL-12) and Th2 cytokine (IL-4) concentrations in patients with systemic lupus erythematosus Lupus 9 589 593 10.1191/096120300678828703 11035433
45. S Dominitzki MC Fantini C Neufert A Nikolaev PR Galle J Scheller, et al. 2007 Cutting edge: trans-signaling via the soluble IL-6R abrogates the induction of FoxP3 in naive CD4+CD25 T cells J Immunol 179 2041 2045 17675459
46. C Pasare R Medzhitov 2003 Toll pathway-dependent blockade of CD4+CD25+ T cell-mediated suppression by dendritic cells Science 299 1033 1036 10.1126/science.1078231 12532024 (Pubitemid 36222922)
47. Z Liu L Yang Y Cui X Wang C Guo Z Huang, et al. 2009 Il-21 enhances NK cell activation and cytolytic activity and induces Th17 cell differentiation in inflammatory bowel disease Inflamm Bowel Dis 15 1133 1144 10.1002/ibd.20923 19322899
48. S Aggarwal N Ghilardi MH Xie FJ de Sauvage AL Gurney 2003 Interleukin-23 promotes a distinct CD4 T cell activation state characterized by the production of interleukin-17 J Biol Chem 278 1910 1914 10.1074/jbc.M207577200 12417590 (Pubitemid 36801431)
49. CL Langrish Y Chen WM Blumenschein J Mattson B Basham JD Sedgwick, et al. 2005 IL-23 drives a pathogenic T cell population that induces autoimmune inflammation J Exp Med 201 233 240 10.1084/jem.20041257 15657292 (Pubitemid 40189432)
50. D Yen J Cheung H Scheerens F Poulet T McClanahan B McKenzie, et al. 2006 IL-23 is essential for T cell-mediated colitis and promotes inflammation via IL-17 and IL-6 J Clin Invest 116 1310 1316 10.1172/JCI21404 16670770
51. T Kobayashi S Okamoto T Hisamatsu N Kamada H Chinen R Saito, et al. 2008 IL23 differentially regulates the Th1/Th17 balance in ulcerative colitis and Crohn's disease Gut 57 1682 1689 10.1136/gut.2007.135053 18653729
52. C Schmidt T Giese B Ludwig I Mueller-Molaian T Marth S Zeuzem, et al. 2005 Expression of interleukin-12-related cytokine transcripts in inflammatory bowel disease: elevated interleukin-23p19 and interleukin-27p28 in Crohn's disease but not in ulcerative colitis Inflamm Bowel Dis 11 16 23 10.1097/00054725-200501000-00003 15674109 (Pubitemid 40340252)
53. G Monteleone I Monteleone D Fina P Vavassori G Del Vecchio Blanco R Caruso, et al. 2005 Interleukin-21 enhances T-helper cell type I signaling and interferon-gamma production in Crohn's disease Gastroenterology 128 687 694 10.1053/j.gastro.2004.12.042 15765404 (Pubitemid 40585371)
54. KB Hahm YH Im TW Parks SH Park S Markowitz HY Jung, et al. 2001 Loss of transforming growth factor beta signalling in the intestine contributes to tissue injury in inflammatory bowel disease Gut 49 190 198 10.1136/gut.49.2.190 11454793 (Pubitemid 32675110)
55. B Del Zotto G Mumolo AM Pronio C Montesani R Tersigni M Boirivant 2003 TGF-beta1 production in inflammatory bowel disease: differing production patterns in Crohn's disease and ulcerative colitis Clin Exp Immunol 134 120 126 10.1046/j.1365-2249.2003.02250.x 12974764 (Pubitemid 37186597)
56. L Zhou JE Lopes MM Chong II Ivanov R Min GD Victora, et al. 2008 TGF-beta-induced Foxp3 inhibits T(H)17 cell differentiation by antagonizing RORgammat function Nature 453 236 240 10.1038/nature06878 18368049 (Pubitemid 351667978)