Disruption of inflammatory signals by cytokine-targeted therapies for inflammatory bowel diseases

British Journal of Pharmacology

Volumn 165, Issue 4, 2012, Pages 820-828

  Caprioli, Flavio ^a   Caruso, Roberta ^b   Sarra, Massimiliano ^b   Pallone, Francesco ^b   Monteleone, Giovanni ^b  

^a FONDAZIONE IRCCS CA GRANDA OSPEDALE MAGGIORE POLICLINICO   (Italy)

^b UNIVERSITY OF ROME TOR VERGATA   (Italy)

Author keywords

anti IL 12; anti IL 6R; anti TNF; Crohn's disease; cytokines; IBD; ulcerative colitis

Indexed keywords

6 MERCAPTOPURINE DERIVATIVE; ADALIMUMAB; ANTISENSE OLIGONUCLEOTIDE; APILIMOD; BRIAKINUMAB; CERTOLIZUMAB PEGOL; CYTOKINE; FONTOLIZUMAB; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INFLIXIMAB; INTERLEUKIN 10; INTERLEUKIN 12 ANTIBODY; INTERLEUKIN 22; INTERLEUKIN 25; INTERLEUKIN 6; INTERLEUKIN 6 ANTIBODY; J 695; METHOTREXATE; PLACEBO; PROBIOTIC AGENT; RECOMBINANT INTERLEUKIN 10; SMAD2 PROTEIN; SMAD3 PROTEIN; TOCILIZUMAB; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR ANTIBODY; TUMOR NECROSIS FACTOR INHIBITOR; TUMOR NECROSIS FACTOR RECEPTOR 1; TUMOR NECROSIS FACTOR RECEPTOR 2; UNCLASSIFIED DRUG; UNINDEXED DRUG; USTEKINUMAB;

ANTIINFLAMMATORY ACTIVITY; ANXIETY; AUTOIMMUNE DISEASE; BACTERIAL IMMUNITY; BLEEDING; BRONCHITIS; COLITIS; CONCENTRATION RESPONSE; CROHN DISEASE; CYTOKINE PRODUCTION; DEMYELINATING DISEASE; DRUG BLOOD LEVEL; DRUG DOSE INCREASE; DRUG EFFICACY; DRUG ERUPTION; DRUG FEVER; DRUG HYPERSENSITIVITY; DRUG INDUCED HEADACHE; DRUG RECEPTOR BINDING; DRUG TARGETING; DRY SKIN; ENTERITIS; FLUSHING; GASTROINTESTINAL HEMORRHAGE; HEART FAILURE; HISTOPLASMOSIS; HUMAN; INFECTION; INJECTION SITE REACTION; INTESTINE FLORA; LUPUS LIKE SYNDROME; MOLECULARLY TARGETED THERAPY; NONHUMAN; PATHOGENESIS; PERIANAL ABSCESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PRURITUS; PSORIASIS; REVIEW; SERUM SICKNESS; SIDE EFFECT; SIGNAL TRANSDUCTION; SINUSITIS; T CELL LYMPHOMA; TH1 CELL; TH17 CELL; TUBERCULOSIS; ULCERATIVE COLITIS; UNSPECIFIED SIDE EFFECT; URINARY TRACT INFECTION; VIRAL GASTROENTERITIS;

ANIMALS; ANTIBODIES, MONOCLONAL; CYTOKINES; HUMANS; INFLAMMATORY BOWEL DISEASES; T-LYMPHOCYTES, HELPER-INDUCER;

EID: 84856291552     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/j.1476-5381.2011.01614.x     Document Type: Review

References (77)

1. Anderson P, Louie J, Lau A, Broder M, (2005). Mechanisms of differential immunogenicity of tumor necrosis factor inhibitors. Curr Rheumatol Rep 7: 3-9.
2. Arora T, Padaki R, Liu L, Hamburger AE, Ellison AR, Stevens SR, et al,. (2009). Differences in binding and effector functions between classes of TNF antagonists. Cytokine 45: 124-131.
3. Atreya R, Mudter J, Finotto S, Mullberg J, Jostock T, Wirtz S, et al,. (2000). 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: 583-588. (Pubitemid 30305911)
4. Atreya R, Atreya I, Neurath MF, (2006). Novel signal transduction pathways: analysis of STAT-3 and Rac-1 signaling in inflammatory bowel disease. Ann N Y Acad Sci 1072: 98-113. (Pubitemid 44448446)
5. Babyatsky MW, Rossiter G, Podolsky DK, (1996). Expression of transforming growth factors alpha and beta in colonic mucosa in inflammatory bowel disease. Gastroenterology 110: 975-984. (Pubitemid 26113734)
6. Baert F, Noman M, Vermeire S, Van Assche G, D'Haens G, Carbonez A, et al,. (2003). Influence of immunogenicity on the long-term efficacy of infliximab in Crohn's disease. N Engl J Med 348: 601-608. (Pubitemid 36204954)
7. Bazzoni F, Beutler B, (1996). The tumor necrosis factor ligand and receptor families. N Engl J Med 334: 1717-1725. (Pubitemid 26193625)
8. Biancone L, Orlando A, Kohn A, Colombo E, Sostegni R, Angelucci E, et al,. (2006). Infliximab and newly diagnosed neoplasia in Crohn's disease: a multicentre matched pair study. Gut 55: 228-233. (Pubitemid 43117283)
9. Black RA, Rauch CT, Kozlosky CJ, Peschon JJ, Slack JL, Wolfson MF, et al,. (1997). A metalloproteinase disintegrin that releases tumour-necrosis factor-alpha from cells. Nature 385: 729-733. (Pubitemid 27098094)
10. Boirivant M, Pallone F, Di Giacinto C, Fina D, Monteleone I, Marinaro M, et al,. (2006). Inhibition of Smad7 with a specific antisense oligonucleotide facilitates TGF-beta1-mediated suppression of colitis. Gastroenterology 131: 1786-1798. (Pubitemid 44958514)
11. Bongartz T, Sutton AJ, Sweeting MJ, Buchan I, Matteson EL, Montori V, (2006). Anti-TNF antibody therapy in rheumatoid arthritis and the risk of serious infections and malignancies: systematic review and meta-analysis of rare harmful effects in randomized controlled trials. JAMA 295: 2275-2285. (Pubitemid 43736578)
12. Braat H, Rottiers P, Hommes DW, Huyghebaert N, Remaut E, Remon JP, et al,. (2006). A phase I trial with transgenic bacteria expressing interleukin-10 in Crohn's disease. Clin Gastroenterol Hepatol 4: 754-759. (Pubitemid 43841860)
13. Brand S, (2009). Crohn's disease: Th1, Th17 or both? The change of a paradigm: new immunological and genetic insights implicate Th17 cells in the pathogenesis of Crohn's disease. Gut 58: 1152-1167.
14. Caruso R, Fina D, Peluso I, Stolfi C, Fantini MC, Gioia V, et al,. (2007). A functional role for interleukin-21 in promoting the synthesis of the T-cell chemoattractant, MIP-3alpha, by gut epithelial cells. Gastroenterology 132: 166-175. (Pubitemid 46108732)
15. Caruso R, Sarra M, Stolfi C, Rizzo A, Fina D, Fantini MC, et al,. (2009). Interleukin-25 inhibits interleukin-12 production and Th1 cell-driven inflammation in the gut. Gastroenterology 136: 2270-2279.
16. Colombel JF, Sandborn WJ, Rutgeerts P, Enns R, Hanauer SB, Panaccione R, et al,. (2007). Adalimumab for maintenance of clinical response and remission in patients with Crohn's disease: the CHARM trial. Gastroenterology 132: 52-65. (Pubitemid 46108762)
17. D'Haens G, Van Deventer S, Van Hogezand R, Chalmers D, Kothe C, Baert F, et al,. (1999). Endoscopic and histological healing with infliximab anti-tumor necrosis factor antibodies in Crohn's disease: a European multicenter trial. Gastroenterology 116: 1029-1034. (Pubitemid 29203012)
18. D'Haens GR, Panaccione R, Higgins PD, Vermeire S, Gassull M, Chowers Y, et al,. (2011). The London Position Statement of the World Congress of Gastroenterology on Biological Therapy for IBD with the European Crohn's and Colitis Organization: when to start, when to stop, which drug to choose, and how to predict response? Am J Gastroenterol 106: 199-212.
19. Efimov GA, Kruglov AA, Tillib SV, Kuprash DV, Nedospasov SA, (2009). Tumor necrosis factor and the consequences of its ablation in vivo. Mol Immunol 47: 19-27.
20. Fina D, Sarra M, Fantini MC, Rizzo A, Caruso R, Caprioli F, et al,. (2008). Regulation of gut inflammation and th17 cell response by interleukin-21. Gastroenterology 134: 1038-1048.
21. Fossati G, Nesbitt AM, (2005). Effect of the anti-TNF agents, adalimumab, etanercept, infliximab, and certolizumab pegol (CDP870) on the induction of apoptosis in activated peripheral blood lymphocytes and monocytes. Am J Gastroenterol 100 (Suppl. S): S298-S299.
22. Fujino S, Andoh A, Bamba S, Ogawa A, Hata K, Araki Y, et al,. (2003). Increased expression of interleukin 17 in inflammatory bowel disease. Gut 52: 65-70. (Pubitemid 36020767)
23. Fuss IJ, Neurath M, Boirivant M, Klein JS, Motte C, Strong SA, et al,. (1996). 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: 1261-1270. (Pubitemid 126449643)
24. Fuss IJ, Heller F, Boirivant M, Leon F, Yoshida M, Fichtner-Feigl S, et al,. (2004). Nonclassical CD1d-restricted NK T cells that produce IL-13 characterize an atypical Th2 response in ulcerative colitis. J Clin Invest 113: 1490-1497. (Pubitemid 39071705)
25. Glocker EO, Kotlarz D, Boztug K, Gertz EM, Schaffer AA, Noyan F, et al,. (2009). Inflammatory bowel disease and mutations affecting the interleukin-10 receptor. N Engl J Med 361: 2033-2045.
26. Gorelik L, Flavell RA, (2002). Transforming growth factor-beta in T-cell biology. Nat Rev Immunol 2: 46-53. (Pubitemid 37328775)
27. Gustot T, Lemmers A, Louis E, Nicaise C, Quertinmont E, Belaiche J, et al,. (2005). Profile of soluble cytokine receptors in Crohn's disease. Gut 54: 488-495. (Pubitemid 40395500)
28. Hanauer SB, Feagan BG, Lichtenstein GR, Mayer LF, Schreiber S, Colombel JF, et al,. (2002). Maintenance infliximab for Crohn's disease: the ACCENT I randomised trial. Lancet 359: 1541-1549. (Pubitemid 34621118)
29. Hanauer SB, Sandborn WJ, Rutgeerts P, Fedorak RN, Lukas M, MacIntosh D, et al,. (2006). Human anti-tumor necrosis factor monoclonal antibody (adalimumab) in Crohn's disease: the CLASSIC-I trial. Gastroenterology 130: 323-333.
30. Heldin CH, Miyazono K, ten Dijke P, (1997). TGF-beta signalling from cell membrane to nucleus through SMAD proteins. Nature 390: 465-471. (Pubitemid 28013118)
31. Heller F, Fuss IJ, Nieuwenhuis EE, Blumberg RS, Strober W, (2002). Oxazolone colitis, a Th2 colitis model resembling ulcerative colitis, is mediated by IL-13-producing NK-T cells. Immunity 17: 629-638. (Pubitemid 35351508)
32. Hommes DW, Mikhajlova TL, Stoinov S, Stimac D, Vucelic B, Lonovics J, et al,. (2006). Fontolizumab, a humanised anti-interferon gamma antibody, demonstrates safety and clinical activity in patients with moderate to severe Crohn's disease. Gut 55: 1131-1137. (Pubitemid 44085681)
33. ten Hove T, van Montfrans C, Peppelenbosch MP, van Deventer SJ, (2002). Infliximab treatment induces apoptosis of lamina propria T lymphocytes in Crohn's disease. Gut 50: 206-211. (Pubitemid 34087933)
34. Hyams JS, Fitzgerald JE, Treem WR, Wyzga N, Kreutzer DL, (1993). Relationship of functional and antigenic interleukin 6 to disease activity in inflammatory bowel disease. Gastroenterology 104: 1285-1292. (Pubitemid 23235400)
35. Iliev ID, Spadoni I, Mileti E, Matteoli G, Sonzogni A, Sampietro GM, et al,. (2009). Human intestinal epithelial cells promote the differentiation of tolerogenic dendritic cells. Gut 58: 1481-1489.
36. Ito H, Takazoe M, Fukuda Y, Hibi T, Kusugami K, Andoh A, et al,. (2004). A pilot randomized trial of a human anti-interleukin-6 receptor monoclonal antibody in active Crohn's disease. Gastroenterology 126: 989-996. (Pubitemid 38451170)
37. Kaser A, Zeissig S, Blumberg RS, (2010). Inflammatory bowel disease. Annu Rev Immunol 28: 573-621.
38. Keane J, Gershon S, Wise RP, Mirabile-Levens E, Kasznica J, Schwieterman WD, et al,. (2001). Tuberculosis associated with infliximab, a tumor necrosis factor alpha-neutralizing agent. N Engl J Med 345: 1098-1104.
39. Kontoyiannis D, Pasparakis M, Pizarro TT, Cominelli F, Kollias G, (1999). Impaired on/off regulation of TNF biosynthesis in mice lacking TNF AU-rich elements: implications for joint and gut-associated immunopathologies. Immunity 10: 387-398. (Pubitemid 29165293)
40. Ma HL, Napierata L, Stedman N, Benoit S, Collins M, Nickerson-Nutter C, et al,. (2010). Tumor necrosis factor alpha blockade exacerbates murine psoriasis-like disease by enhancing Th17 function and decreasing expansion of Treg cells. Arthritis Rheum 62: 430-440.
41. MacDonald TT, Hutchings P, Choy MY, Murch S, Cooke A, (1990). Tumour necrosis factor-alpha and interferon-gamma production measured at the single cell level in normal and inflamed human intestine. Clin Exp Immunol 81: 301-305. (Pubitemid 20242538)
42. MacDonald TT, Bajaj-Elliott M, Pender SL, (1999). T cells orchestrate intestinal mucosal shape and integrity. Immunol Today 20: 505-510. (Pubitemid 29507094)
43. MacEwan DJ, (2002). TNF ligands and receptors-a matter of life and death. Br J Pharmacol 135: 855-875. (Pubitemid 34214444)
44. Mannon PJ, Fuss IJ, Mayer L, Elson CO, Sandborn WJ, Present D, et al,. (2004). Anti-interleukin-12 antibody for active Crohn's disease. N Engl J Med 351: 2069-2079. (Pubitemid 39482500)
45. Monteleone G, Biancone L, Marasco R, Morrone G, Marasco O, Luzza F, et al,. (1997). Interleukin 12 is expressed and actively released by Crohn's disease intestinal lamina propria mononuclear cells. Gastroenterology 112: 1169-1178. (Pubitemid 27157528)
46. Monteleone G, Kumberova A, Croft NM, McKenzie C, Steer HW, MacDonald TT, (2001). Blocking Smad7 restores TGF-beta1 signaling in chronic inflammatory bowel disease. J Clin Invest 108: 601-609. (Pubitemid 32777740)
47. Monteleone G, Monteleone I, Fina D, Vavassori P, Del Vecchio Blanco G, Caruso R, et al,. (2005). Interleukin-21 enhances T-helper cell type I signaling and interferon-gamma production in Crohn's disease. Gastroenterology 128: 687-694. (Pubitemid 40585371)
48. Monteleone G, Caruso R, Fina D, Peluso I, Gioia V, Stolfi C, et al,. (2006). Control of matrix metalloproteinase production in human intestinal fibroblasts by interleukin 21. Gut 55: 1774-1780. (Pubitemid 44893577)
49. Monteleone I, Rizzo A, Sarra M, Sica G, Sileri P, Biancone L, et al,. (2011). Aryl hydrocarbon receptor-induced signals upregulate IL-22 production and inhibit inflammation in the gastrointestinal tract. Gastroenterology 141: 237-248.e1.
50. Moore KW, Malefyt R, Coffman RL, O'Garra A, (2001). Interleukin-10 and the interleukin-10 receptor. Annu Rev Immunol 19: 683-765. (Pubitemid 32368050)
51. Neurath MF, Fuss I, Kelsall BL, Stuber E, Strober W, (1995). Antibodies to interleukin 12 abrogate established experimental colitis in mice. J Exp Med 182: 1281-1290.
52. Neurath MF, Fuss I, Pasparakis M, Alexopoulou L, Haralambous S, Meyer zum Buschenfelde KH, et al,. (1997). Predominant pathogenic role of tumor necrosis factor in experimental colitis in mice. Eur J Immunol 27: 1743-1750. (Pubitemid 27302858)
53. Neurath MF, Weigmann B, Finotto S, Glickman J, Nieuwenhuis E, Iijima H, et al,. (2002). The transcription factor T-bet regulates mucosal T cell activation in experimental colitis and Crohn's disease. J Exp Med 195: 1129-1143. (Pubitemid 34517139)
54. Nishimoto N, Kishimoto T, (2006). Interleukin 6: from bench to bedside. Nat Clin Pract Rheumatol 2: 619-626. (Pubitemid 44650950)
55. Ouyang W, (2010). Distinct roles of IL-22 in human psoriasis and inflammatory bowel disease. Cytokine Growth Factor Rev 21: 435-441.
56. Parrello T, Monteleone G, Cucchiara S, Monteleone I, Sebkova L, Doldo P, et al,. (2000). Up-regulation of the IL-12 receptor beta 2 chain in Crohn's disease. J Immunol 165: 7234-7239. (Pubitemid 32001201)
57. Peluso I, Fantini MC, Fina D, Caruso R, Boirivant M, MacDonald TT, et al,. (2007). IL-21 counteracts the regulatory T cell-mediated suppression of human CD4+ T lymphocytes. J Immunol 178: 732-739. (Pubitemid 46095145)
58. Pender SL, Breese EJ, Gunther U, Howie D, Wathen NC, Schuppan D, et al,. (1998). Suppression of T cell-mediated injury in human gut by interleukin 10: role of matrix metalloproteinases. Gastroenterology 115: 573-583. (Pubitemid 28397292)
59. Peyrin-Biroulet L, Deltenre P, de Suray N, Branche J, Sandborn WJ, Colombel JF, (2008). Efficacy and safety of tumor necrosis factor antagonists in Crohn's disease: meta-analysis of placebo-controlled trials. Clin Gastroenterol Hepatol 6: 644-653. (Pubitemid 351783447)
60. Powrie F, Leach MW, Mauze S, Menon S, Caddle LB, Coffman RL, (1994). Inhibition of Th1 responses prevents inflammatory bowel disease in scid mice reconstituted with CD45RBhi CD4+ T cells. Immunity 1: 553-562.
61. Present DH, Rutgeerts P, Targan S, Hanauer SB, Mayer L, van Hogezand RA, et al,. (1999). Infliximab for the treatment of fistulas in patients with Crohn's disease. N Engl J Med 340: 1398-1405. (Pubitemid 29205403)
62. Reinisch W, Hommes DW, Van Assche G, Colombel JF, Gendre JP, Oldenburg B, et al,. (2006). A dose escalating, placebo controlled, double blind, single dose and multidose, safety and tolerability study of fontolizumab, a humanised anti-interferon gamma antibody, in patients with moderate to severe Crohn's disease. Gut 55: 1138-1144. (Pubitemid 44085682)
63. Reinisch W, de Villiers W, Bene L, Simon L, Racz I, Katz S, et al,. (2010). Fontolizumab in moderate to severe Crohn's disease: a phase 2, randomized, double-blind, placebo-controlled, multiple-dose study. Inflamm Bowel Dis 16: 233-242.
64. Rose-John S, Scheller J, Elson G, Jones SA, (2006). Interleukin-6 biology is coordinated by membrane-bound and soluble receptors: role in inflammation and cancer. J Leukoc Biol 80: 227-236. (Pubitemid 44835496)
65. Rutgeerts P, Sandborn WJ, Feagan BG, Reinisch W, Olson A, Johanns J, et al,. (2005). Infliximab for induction and maintenance therapy for ulcerative colitis. N Engl J Med 353: 2462-2476. (Pubitemid 41770166)
66. Sandborn WJ, Feagan BG, Fedorak RN, Scherl E, Fleisher MR, Katz S, et al,. (2008). A randomized trial of Ustekinumab, a human interleukin-12/23 monoclonal antibody, in patients with moderate-to-severe Crohn's disease. Gastroenterology 135: 1130-1141.
67. Sands BE, Jacobson EW, Sylwestrowicz T, Younes Z, Dryden G, Fedorak R, et al,. (2010). Randomized, double-blind, placebo-controlled trial of the oral interleukin-12/23 inhibitor apilimod mesylate for treatment of active Crohn's disease. Inflamm Bowel Dis 16: 1209-1218.
68. Schoepfer AM, Vavricka SR, Binek J, Felley C, Geyer M, Manz M, et al,. (2010). Efficacy and safety of certolizumab pegol induction therapy in an unselected Crohn's disease population: results of the FACTS survey. Inflamm Bowel Dis 16: 933-938.
69. Schreiber S, Fedorak RN, Nielsen OH, Wild G, Williams CN, Nikolaus S, et al,. (2000). Safety and efficacy of recombinant human interleukin 10 in chronic active Crohn's disease. Crohn's Disease IL-10 Cooperative Study Group. Gastroenterology 119: 1461-1472. (Pubitemid 32198671)
70. Schreiber S, Rutgeerts P, Fedorak RN, Khaliq-Kareemi M, Kamm MA, Boivin M, et al,. (2005). A randomized, placebo-controlled trial of certolizumab pegol (CDP870) for treatment of Crohn's disease. Gastroenterology 129: 807-818. (Pubitemid 41242673)
71. Sellon RK, Tonkonogy S, Schultz M, Dieleman LA, Grenther W, Balish E, et al,. (1998). Resident enteric bacteria are necessary for development of spontaneous colitis and immune system activation in interleukin-10-deficient mice. Infect Immun 66: 5224-5231. (Pubitemid 29044613)
72. Targan SR, Hanauer SB, van Deventer SJ, Mayer L, Present DH, Braakman T, et al,. (1997). A short-term study of chimeric monoclonal antibody cA2 to tumor necrosis factor alpha for Crohn's disease. Crohn's Disease cA2 Study Group. N Engl J Med 337: 1029-1035.
73. Trinchieri G, (2003). Interleukin-12 and the regulation of innate resistance and adaptive immunity. Nat Rev Immunol 3: 133-146. (Pubitemid 37328691)
74. Vermeire S, Noman M, Van Assche G, Baert F, Van Steen K, Esters N, et al,. (2003). Autoimmunity associated with anti-tumor necrosis factor alpha treatment in Crohn's disease: a prospective cohort study. Gastroenterology 125: 32-39. (Pubitemid 36799104)
75. Watanabe T, Kitani A, Murray PJ, Strober W, (2004). NOD2 is a negative regulator of Toll-like receptor 2-mediated T helper type 1 responses. Nat Immunol 5: 800-808. (Pubitemid 39172973)
76. Weir N, Athwal D, Brown D, Foulkes R, Kollias GI, Nesbitt A, et al,. (2006). A new generation of high-affinity humanized PEGylated Fab' fragment anti-tumor necrosis factor-(alpha) monoclonal antibodies. Therapy 3: 535-545. (Pubitemid 44420582)
77. Wollina U, Hansel G, Koch A, Schonlebe J, Kostler E, Haroske G, (2008). Tumor necrosis factor-alpha inhibitor-induced psoriasis or psoriasiform exanthemata: first 120 cases from the literature including a series of six new patients. Am J Clin Dermatol 9: 1-14.