Proinflammatory cytokines in the pathogenesis of inflammatory bowel diseases

Gastroenterology

Volumn 140, Issue 6, 2011, Pages 1756-1767.e1

  Strober, Warren ^a   Fuss, Ivan J ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

Crohn's Disease; Cytokines; IFN ; IL 12; IL 17; IL 22; IL 23; TL1A; Ulcerative Colitis

Indexed keywords

CYTOKINE; GAMMA INTERFERON; INTERLEUKIN 13; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 22; INTERLEUKIN 6; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR LIKE LIGAND 1A; UNCLASSIFIED DRUG;

ARTICLE; CD4+ T LYMPHOCYTE; CELL DIFFERENTIATION; CROHN DISEASE; EFFECTOR CELL; ENTERITIS; HUMAN; IMMUNE RESPONSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; TH1 CELL; TH17 CELL; TH2 CELL; ULCERATIVE COLITIS;

EID: 79955563439     PISSN: 00165085     EISSN: None     Source Type: Journal    
DOI: 10.1053/j.gastro.2011.02.016     Document Type: Article

References (88)

1. T.R. Mosmann, H. Cherwinski, and M.W. Bond Two types of murine helper T cell clone I. Definition according to profiles of lymphokine activities and secreted proteins J Immunol 136 1986 2348 2357 (Pubitemid 16136806)
2. E. Braese, C.P. Braegger, and C.J. Corrigan Interleukin-2- and interferon-gamma-secreting T cells in normal and diseased human intestinal mucosa Immunology 78 1993 127 131 (Pubitemid 23035859)
3. I.J. Fuss, M. Neurath, and M. Boirivant Disparate CD4+ lamina propria (LP) lymphokine secretion profiles in inflammatory bowel disease Crohn's disease LP cells manifest increased secretion of IFN-gamma, whereas ulcerative colitis LP cells manifest increased secretion of IL-5 J Immunol 157 1996 1261 1270 (Pubitemid 126449643)
4. M.F. Neurath, I. Fuss, and B.L. Kelsall Antibodies to interleukin 12 abrogate established experimental colitis in mice J Exp Med 182 1995 12911290
5. Z. Liu, K. Beboes, and H. Heremans Role of interleukin-12 in the induction of mucosal inflammation and abrogation of regulatory T cell function in chronic experimental colitis Eur J Immunol 31 2001 1550 1560 (Pubitemid 32454704)
6. I.J. Fuss, C. Becker, and Z. Yang Both IL-12p70 and IL-23 are synthesized during active Crohn's disease and are down-regulated by treatment with anti-IL-12 p40 monoclonal antibody Inflamm Bowel Dis 12 2006 9 15 (Pubitemid 43032445)
7. A.L. Hart, H.O. Al-Hassi, and R.J. Rigby Characteristics of intestinal dendritic cells in inflammatory bowel diseases Gastroenterology 129 2005 50 65 (Pubitemid 41002042)
8. K. Matsuaka, N. Inoue, and T. Sato T-bet upregulation and subsequent interleukin 12 stimulation are essential for induction of Th1 mediated Immunopathology in Crohn's disease Gut 53 2004 1303 1308 (Pubitemid 39120117)
9. P.J. Mannon, I.J. Fuss, and C.O. Elson Anti-interleukin-12 antibody for active Crohn's disease N Engl J Med 351 2004 2069 2079 (Pubitemid 39482500)
10. W.J. Sandborn, B.G. Feagan, and R.N. Fedorak A randomized trial of Ustekinumab, a human interleukin-12/23 monoclonal antibody, in patients with moderate-to-severe Crohn's disease Gastroenterology 135 2008 1130 1141
11. I.J. Fuss, F. Heller, and M. Boirivant Nonclassical CD1d-restricted NK T cells that produce IL-13 characterize an atypical Th2 response in ulcerative colitis J Clin Invest 113 2004 1490 1497 (Pubitemid 39071705)
12. B. Oppman, R. Lesley, and B. Blom Novel p19 protein engages IL-12p40 to form a cytokine, IL-23, with biological activities similar as well as distinct from IL-12 Immunity 13 2000 715 725
13. S. Aggarwal, N. Ghilardi, and M.H. Xie Interleukin-23 promotes a distinct CD4 T cell activation state characterized by the production of interleukin-17 J Biol Chem 278 2003 1910 1914 (Pubitemid 36801431)
14. D. Yen, J. Cheung, and H. Scheerens IL-23 is essential for T cell-mediated colitis and promotes inflammation via IL-17 and IL-6 J Clin Invest 116 2006 1310 1316
15. Y. Chen, C.L. Langrish, and B. McKenzie Anti-IL-23 therapy inhibits multiple inflammatory pathways and ameliorates autoimmune encephalomyelitis J Clin Invest 116 2006 1317 1326
16. S. Hue, P. Ahern, and S. Buonocore Interleukin-23 drives innate and T cell-mediated intestinal inflammation J Exp Med 203 2006 2473 2483 (Pubitemid 44664617)
17. M.C. Kullberg, D. Jankovic, and C.G. Feng IL-23 plays a key role in Helicobacter hepaticus-induced T cell-dependent colitis J Exp Med 203 2006 2485 2494 (Pubitemid 44664618)
18. G. Trinchieri Interleukin-12: a proinflammatory cytokine with immunoregulatory functions that bridge innate resistance and antigen-specific adaptive immunity Ann Rev Immunol 13 1995 251 276
19. M. Veldhoen, R.J. Hocking, and C.J. Atkins TGFbeta in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells Immunity 24 2006 179 189 (Pubitemid 43214587)
20. M.J. McGeachy, Y. Chen, and C.M. Tato The interleukin 23 receptor is essential for the terminal differentiation of interleukin 17-producing effector T helper cells in vivo Nat Immunol 10 2009 314 324
21. I.I. Ivanov, L. Zhou, and D.R. Littman Transcriptional regulation of Th17 cell differentiation Semin Immunol 19 2007 409 417 (Pubitemid 351274050)
22. E. Bettelli, M. Oukka, and V.K. Kuchroo T(H)-17 cells in the circle of immunity and autoimmunity Nat Immunol 8 2007 345 350 (Pubitemid 46745409)
23. M.J. McGeachey, K.S. Bak-Jensen, and Y. Chen TGF-beta and IL-6 drive the production of IL-17 and IL-10 by T cells and restrain T(H)-17 cell-mediated pathology Nat Immunol 8 2007 1390 1397 (Pubitemid 350138974)
24. K. Ghoreschi, A. Laurence, and X.P. Yang Generation of pathogenic T(H)17 cells in the absence of TGF-β signaling Nature 467 2010 967 971
25. L. Zhou, and D.R. Littman Transcriptional regulatory networks in Th17 cell differentiation Curr Opin Immunol 21 2009 146 152
26. X.O. Yang, B.P. Pappu, and R. Nurieva T helper 17 lineage differentiation is programmed by orphan nuclear receptors ROR alpha and ROR gamma Immunity 28 2008 29 39
27. L. Xu, A. Kitani, and I. Fuss Cutting edge: regulatory T cells induce CD4+CD25-Foxp3- T cells or are self-induced to become Th17 cells in the absence of exogenous TGF-beta J Immunol 178 2007 6725 6729 (Pubitemid 46847395)
28. L. Zhou, J.E. Lopes, and M.M. Chong TGF-beta-induced Foxp3 inhibits T(H)17 cell differentiation by antagonizing RORgammat function Nature 453 2008 236 240 (Pubitemid 351667978)
29. J.H. Koenen, R.L. Smeets, and P.M. Vink Human CD25highFoxp3pos regulatory T cells differentiate into IL-17-producing cells Blood 112 2008 2340 2352
30. X.O. Yang, R. Nrurieva, and G.J. Martinez Molecular antagonism and plasticity of regulatory and inflammatory T cell programs Immunity 29 2008 44 56
31. L.E. Harrington, R.D. Hatton, and P.R. Mangan Interleukin 17-producing CD4+ effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages Nat Immunol 6 2005 1123 1132 (Pubitemid 41541790)
32. P.R. Mangan, L.E. Harrington, and D.B. O'Quinn Transforming growth factor-beta induces development of the T(H)17 lineage Nature 441 2006 231 234
33. Y.K. Lee, H. Turner, and C.L. Maynard Late developmental plasticity in the T helper 17 lineage Immunity 30 2009 92 107
34. F. Powrie, R. Correa-Oliveira, and S. Mauze Regulatory interactions between CD45RBhigh and CD45RBlow CD4+ T cells are important for the balance between protective and pathogenic cell-mediated immunity J Exp Med 179 1994 589 600
35. F. Powrie, and D. Mason OX-22 high CD4+ T cells induce wasting disease with multiple organ pathology: prevention by the OX-22 low subset J Exp Med 172 1990 1701 1708
36. F. Powrie, M.W. Leach, and S. Mauze Inhibition of Th1 responses prevents inflammatory bowel disease in scid mice reconstituted with CD45RBhi CD4+ T cells Immunity 1 1994 553 562
37. M.F. Neurath, B. Weigmann, and S. Finotto The transcription factor T-bet regulates mucosal T cell activation in experimental colitis and Crohn's disease J Exp Med 195 2002 1129 1143 (Pubitemid 34517139)
38. T. Griseri, M. Asquith, and C. Thompson OX40 is required for regulatory T cell-mediated control of colitis JEM 207 2010 699 709
39. Y. Mikami, T. Kanai, and T. Sujino Competition between colitogenic Th1 and Th17 cells contributes to the amelioration of colitis Eur J Immunol 40 2010 2409 2422
40. H.H. Uhlig, B.S. McKenzie, and S. Huie Differential activity of IL-12 and IL-23 in mucosal and systemic innate immune pathology Immunity 25 2006 309 318
41. L.W. Collison, C.J. Workman, and T.T. Kuo The inhibitory cytokine IL-35 contributes to regulatory T-cell function Nature 450 2007 566 569 (Pubitemid 350190247)
42. P.P. Ahern, C. Schiering, and S. Buonocore Interleukin-23 drives intestinal inflammation through direct activity on T cells Immunity 33 2010 279 288
43. C.O. Elson, Y. Cong, and C.T. Weaver Monoclonal anti-interleukin 23 reverses active colitis in a T cell-mediated model in mice Gastroenterology 132 2007 2359 2370 (Pubitemid 46890867)
44. M. Leppkes, C. Becker, and I.I. Ivanov RORgamma-expressing Th17 cells induce murine chronic intestinal inflammation via redundant effects of IL-17A and IL-17F Gastroenterology 136 2009 256 267
45. A. Izcue, S. Hue, and S. Buonocore Interleukin-23 restrains regulatory T cell activity to drive T cell-dependent colitis Immunity 28 2008 559 570 (Pubitemid 351467043)
46. O. O'Connor Jr, M. Kamanaka, and C. Booth A protective function for interleukin 17A in T cell-mediated intestinal inflammation Nat Immunol 10 2009 603 609
47. X.O. Yang, S.H. Chang, and H. Park Regulation of inflammatory responses by IL-17F J Exp Med 205 2008 1063 1075 (Pubitemid 351679682)
48. C. Becker, H. Domhoff, and C. Neufert Cutting edge: IL-23 cross-regulates IL-12 production in T cell-dependent experimental colitis J Immunol 177 2006 2760 2764 (Pubitemid 44277789)
49. K. Sugimoto, A. Ogawa, and E. Mizoguchi IL-22 ameliorates intestinal inflammation in a mouse model of ulcerative colitis J Clin Invest 118 2008 534 544 (Pubitemid 351206544)
50. L.A. Zenewicz, G.D. Yancopoulos, and D.M. Valenzuela Innate and adaptive interleukin-22 protects mice from inflammatory bowel disease Immunity 29 2008 947 957
51. G. Pickert, C. Neufert, and M. Leppkes STAT3 links IL-22 signaling in intestinal epithelial cells to mucosal wound healing JEM 206 2009 1465 1472
52. N.R. Klatt, L.D. Harris, and C.L. Vinton Compromised gastrointestinal integrity in pigtail macaques is associated with increased microbial translocation, immune activation, and IL-17 production in the absence of SIV infection Mucosal Immunol 3 2010 387 398
53. W. Strober, I.J. Fuss, and P. Mannon The fundamental basis of inflammatory bowel disease J Clin Invest 117 2007 514 521 (Pubitemid 46348505)
54. G. Bouma, A. Kaushiva, and W. Strober Experimental murine colitis is regulated by two genetic loci, including one on chromosome 11 that regulates IL-12 responses Gastroenterology 123 2002 554 565 (Pubitemid 34827199)
55. S. Fichtner-Feigl, I.J. Fuss, and J.C. Preiss Treatment of murine Th1- and Th2-mediated inflammatory bowel disease with NF-kappa B decoy oligonucleotides J Clin Invest 115 2005 3057 3071 (Pubitemid 41567571)
56. T. Parello, G. Monteleone, and S. Cucchiara Up-regulation of the IL-12 receptor beta 2 chain in Crohn's disease J Immunol 165 2000 7234 7239 (Pubitemid 32001201)
57. S. Fujino, A. Ando, and S. Bamba Increased expression of interleukin 17 in inflammatory bowel disease Gut 52 2003 65 70 (Pubitemid 36020767)
58. O.H. Nielsen, I. Kiman, and N. Rdiger Upregulation of interleukin-12 and -17 in active inflammatory bowel disease Scand J Gastroenterol 38 2003 180 185 (Pubitemid 36349930)
59. T. Kobayashi, S. Okoamoto, and T. Hisamatsu IL23 differentially regulates the Th1/Th17 balance in ulcerative colitis and Crohn's disease Gut 57 2008 1682 1689
60. R.H. Duerr, K.D. Taylor, and S.R. Brant A genome-wide association study identifies IL23R as an inflammatory bowel disease gene Science 314 2006 1461 1463 (Pubitemid 44871953)
61. A. Sakuraba, T. Sato, and N. Kamada Th1/Th17 immune response is induced by mesenteric lymph node dendritic cells in Crohn's disease Gasttroenterology 137 2009 1736 1745
62. M.A. Kleinschek, K. Boniface, and S. Sadekova Circulating and gut-resident human Th17 cells express CD161 and promote intestinal inflammation J Exp Med 206 2009 525 534
63. A. Jarry, C. Bossard, and C. Bou-Hanna Mucosal IL-10 and TGF-beta play crucial roles in preventing LPS-driven, IFN-gamma-mediated epithelial damage in human colon explants J Clin Invest 118 2008 1132 1142 (Pubitemid 351364620)
64. W. Strober, I.J. Fuss, and R.S. Blumberg The immunology of mucosal models of inflammation Ann Rev Immunol 20 2002 495 549 (Pubitemid 34293433)
65. M. Boirivant, I.J. Fuss, and A. Chu Oxazalone colitis: a murine model of T helper cell type 2 colitis treatable with antibodies to interleukin 4 J Exp Med 188 1998 1929 1939 (Pubitemid 28536780)
66. F. Heller, I.J. Fuss, and E.E. Nieuwenhuis Oxazalone colitis, a Th2 colitis model resembling ulcerative colitis, is mediated by IL-13-producing NK-T cells Immunity 17 2002 629 638 (Pubitemid 35351508)
67. F. Heller, P. Florian, and C. Bojarski Interleukin-13 is the key effector Th2 cytokine in ulcerative colitis that affects epithelial tight junctions, apoptosis, and cell restitution Gastroenterology 129 2005 550 564 (Pubitemid 41096643)
68. A.V. Rachitskaya, A.M. Hansen, and R. Horai Cutting edge: NK T cells constitutively express IL-23 receptor and RORgammat and rapidly produce IL-17 upon receptor ligation in an IL-6 dependent fashion J Immunol 180 2008 5167 5171
69. P.J. Mannon, R.L. Hornung, and Z. Yang Suppression of inflammation in ulcerative colitis by interferon-beta-1a is accompanied by inhibition of IL-13 production Gut 60 2011 449 455
70. G. Meng, F. Zhang, and I.J. Fuss A mutation in the Nirp3 gene causing inflammasome hyperactivation potentiates Th17 cell-dominant immune responses Immunity 30 2009 860 874
71. J.L. Prehn, L.S. Thomas, and C.J. Landers The T cell costimulator TL1A is induced by FcgammaR signaling in human monocytes and dendritic cells J Immunol 178 2007 4033 4038 (Pubitemid 46492351)
72. N. Kamada, T. Hisamatsu, and H. Honda TL1A produced by lamina propria macrophages induces Th1 and Th17 immune responses in cooperation with IL-23 in patients with Crohn's disease Inflamm Bowel Dis 16 2010 568 575
73. H17 activation Gastroenterology 135 2008 552 567
74. F. Meylan, Y.-J. Song, and I.J. Fuss The TNF-family cytokine TL1A drives IL-13-dependent small intestinal inflammation Mucosal Immunol 4 2011 172 185
75. F. Meylan, T.S. Davidson, and E. Kahle The TNF-family receptor DR3 is essential for diverse T cell-mediated inflammatory diseases Immunity 29 2008 79 89
76. T.H. Schreiber, D. Wolf, and M.S. Tsai Therapeutic Treg expansion in mice by TNFRSF25 prevents allergic lung inflammation J Clin Invest 120 2010 3629 3640
77. J.L. Prehn, S. Mehldizadeh, and C.J. Landers Potential role for TL1A, the new TNF-family member and potent costimulator of IFN-gamma, in mucosal inflammation Clin Immunol 112 2004 66 77 (Pubitemid 38781059)
78. rd, and M. Marini Expression, localization, and functional activity of TL1A, a novel Th1-polarizing cytokine in inflammatory bowel disease J Immunol 171 2003 4868 4874 (Pubitemid 37310609)
79. K.S. Michelson, L.S. Thomas, and K.D. Taylor IBD-associated TL1A gene (TNFSF15) haplotypes determine increased expression of TL1A proteins PLoS One 4; 2009 e4719
80. L. Peyrin-Biroulet, P. Deltenre, and N. de Suray Efficacy and safety of tumor necrosis factor antagonists in Crohn's disease: meta-analysis of placebo-controlled trials Clin Gastroenterol Hepatol 6 2008 644 653 (Pubitemid 351783447)
81. H. Tilig, A. Moschen, and A. Kaser Mode of function of biological anti-TNF agents in the treatment of inflammatory bowel diseases Expert Opin Biol Ther 7 2007 1051 1059 (Pubitemid 47204358)
82. H. Mitoma, T. Horiuchi, and N. Hatta Infliximab induces potent anti-inflammatory responses by outside-to-inside signals through transmembrane TNF-alpha Gastroenterology 128 2005 376 392 (Pubitemid 40431090)
83. R. Panaccione, W. Sandborn, and G. Gordon Briakinumab (anti-interleukin 12/23 P40, ABT874) for treatment of Crohn's disease Highlights from ACG 2010 Gastroenterol Hepatol 12 Suppl 17 2010 17
84. W. Reinisch, W. de Villiers, and L. Bene Fontolizumab in moderate to servere Crohn's disease: a phase 2, randomized, double-blind, placebo-controlled, multiple-dose study Inflamm Bowel Dis 16 2010 233 242
85. I.J. Fuss, T. Marth, and M.F. Neurath Anti-interleukin 12 treatment regulates apoptosis of Th1 T cells in experimental colitis in mice Gastroenterology 117 1999 1078 1088 (Pubitemid 29512666)
86. N. Nishimoto, and T. Kishimoto Humanized antihuman IL-6 receptor antibody, tocilizumab Handb Exp Pharmacol 181 2008 151 160
87. N. Nishimoto, and T. Kishimoto inhibition of IL-6 for the treatment of inflammatory diseases Curr Opin Pharmacol 4 2004 386 391 (Pubitemid 38987066)
88. R. Atreya, J. Mudter, and S. Finotto Blockade of interleukin 6 trans signaling suppresses T-cell resistance against apoptosis in chronic intestinal inflammation: evidence in Crohn disease and experimental colitis in vivo Nat Med 6 2000 583 588 (Pubitemid 30305911)