Apoptosis of regulatory T lymphocytes is increased in chronic inflammatory bowel disease and reversed by anti-TNFα treatment

Gut

Volumn 60, Issue 10, 2011, Pages 1345-1353

  Veltkamp, Claudia ^a   Anstaett, Matthias ^b   Wahl, Kristin ^b   Möller, Sarah ^b   Gangl, Saskia ^b   Bachmann, Oliver ^b   Hardtke Wolenski, Matthias ^b   Länger, Florian ^b   Stremmel, Wolfgang ^a   Manns, Michael P ^b   Schulze Osthoff, Klaus ^c   Bantel, Heike ^b  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b HANNOVER MEDICAL SCHOOL   (Germany)

^c UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AZATHIOPRINE; CASPASE 3; CASPASE 7; INFLIXIMAB;

ADULT; AGED; APOPTOSIS; ARTICLE; COLON BIOPSY; CONTROLLED STUDY; CROHN DISEASE; ENZYME ACTIVATION; ENZYME ACTIVITY; FEMALE; FLOW CYTOMETRY; HUMAN; HUMAN CELL; HUMAN TISSUE; ILEUM; IMMUNOHISTOCHEMISTRY; MAJOR CLINICAL STUDY; MALE; NICK END LABELING; PATHOGENESIS; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; ULCERATIVE COLITIS;

ADULT; AGED; ANTI-INFLAMMATORY AGENTS; ANTIBODIES, MONOCLONAL; APOPTOSIS; BIOPSY; CHRONIC DISEASE; COLON; FEMALE; FLOW CYTOMETRY; FOLLOW-UP STUDIES; HUMANS; ILEUM; IMMUNOHISTOCHEMISTRY; IN SITU NICK-END LABELING; INFLAMMATORY BOWEL DISEASES; INJECTIONS, INTRAVENOUS; INTESTINAL MUCOSA; MALE; MIDDLE AGED; PROSPECTIVE STUDIES; T-LYMPHOCYTES, REGULATORY; TREATMENT OUTCOME; TUMOR NECROSIS FACTOR-ALPHA; YOUNG ADULT;

EID: 80052573212     PISSN: 00175749     EISSN: 14683288     Source Type: Journal    
DOI: 10.1136/gut.2010.217117     Document Type: Article

References (42)

1. Kaser A., Zeissig S., Blumberg R.S. Inflammatory bowel disease. Annu Rev Immunol 2010;28:573-612.
2. Izcue A., Coombes J.L., Powrie F. Regulatory lymphocytes and intestinal inflammation. Annu Rev Immunol 2009;27:313-338
3. Abraham C., Cho J.H. Inflammatory bowel disease. N Engl J Med 2009;361:2066-2078
4. Sturm A., Mohr S., Fiocchi C. Critical role of caspases in the regulation of apoptosis and proliferation of mucosal T cells. Gastroenterology 2002;122:1334-1345 (Pubitemid 34465176)
5. Suri-Payer E., Amar A.Z., Thornton A.M., et al. CD4+CD25+ T-cells inhibit both the induction and effector function of autoreactive T-cells and represent a unique lineage of immunoregulatory cells. J Immunol 1998;160:1212-1218 (Pubitemid 28093417)
6. Tang Q., Bluestone J.A. The Foxp3+ regulatory T cell: A jack of all trades, master of regulation. Nat Immunol 2008;9:239-244 (Pubitemid 351267321)
7. Sakaguchi S., Yamaguchi T., Nomura T., et al. Regulatory T cells and immune tolerance. Cell 2008;133:775-787 (Pubitemid 351707693)
8. Sakaguchi S., Sakaguchi N., Asano M., et al. 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 1995;155:1151-1164
9. Hori S., Nomura T., Sakaguchi S. Control of regulatory T cell development by the transcription factor Foxp3. Science 2003;299:1057-1061 (Pubitemid 36222930)
10. Vignali D.A., Collison L.W., Workman C.J. How regulatory T cells work. Nat Rev Immunol 2008;8:523-532
11. Longhi M.S., Ma Y., Bogdanos D.P., et al. Impairment of CD4(+)CD25(+) regulatory T-cells in autoimmune liver disease. J Hepatol 2004;41:31-37 (Pubitemid 39005149)
12. Haas J., Fritzsching B., Trübswetter P., et al. Prevalence of newly generated naive regulatory T cells (Treg) is critical for Treg suppressive function and determines Treg dysfunction in multiple sclerosis. J Immunol 2007;179:1322-1330
13. Mottet C., Uhlig H.H., Powrie F. Cutting edge: Cure of colitis by CD4+CD25+ regulatory T cells. J Immunol 2003;170:3939-3943 (Pubitemid 36428153)
14. Veltkamp C., Ruhwald R., Giesem T., et al. CD4+CD25+ cell depletion from the normal CD4+ T cell pool prevents tolerance toward the intestinal flora and leads to chronic colitis in immunodeficient mice. Inflamm Bowel Dis 2006;12:437-446
15. Yu Q.T., Saruta M., Avanesyan A., et al. Expression and functional characterization of FoxP3+CD4+ regulatory T cells in ulcerative colitis. Inflamm Bowel Dis 2007;13:191-199 (Pubitemid 46806228)
16. Barnes M.J., Powrie F. Regulatory T cells reinforce intestinal homeostasis. Immunity 2009;31:401-411
17. Maul J., Loddenkemper C., Mundt P., et al. Peripheral and intestinal regulatory CD4+CD25 (high) T cells in inflammatory bowel disease. Gastroenterology 2005;128:1868-1878 (Pubitemid 40824698)
18. Fischer U., Jänicke R.U., Schulze-Osthoff K. Many cuts to ruin: A comprehensive update of caspase substrates. Cell Death Differ 2003;10:76-100. (Pubitemid 36511834)
19. Boirivant M., Pica R., DeMaria R., et al. Stimulated human lamina propria T cells manifest enhanced Fas-mediated apoptosis. J Clin Invest 1996;98:2616-2622 (Pubitemid 26415084)
20. Sturm A., Leite A.Z., Danese S., et al. Divergent cell cycle kinetics underlie the distinct functional capacity of mucosal T cells in Crohn's disease and ulcerative colitis. Gut 2004;53:1624-1631 (Pubitemid 39434106)
21. Rutgeerts P., Vermeire S., Van Assche G. Biological therapies for inflammatory bowel diseases. Gastroenterology 2009;136:1182-1197
22. Nadkarni S., Mauri C., Ehrenstein M.R. Anti-TNF-alpha therapy induces a distinct regulatory T cell population in patients with rheumatoid arthritis via TGF-beta. J Exp Med 2007;204:33-39 (Pubitemid 46148753)
23. Valencia X., Yarboro C., Illei G., et al. Deficient CD4+CD25high T regulatory cell function in patients with active systemic lupus erythematosus. J Immunol 2007;178:2579-2588 (Pubitemid 46233461)
24. Best W.R., Becktel J.M., Singleton J.W., et al. Development of a Crohn's disease activity index. National Cooperative Crohn's Disease Study. Gastroenterology 1976;70:439-444
25. Lichtiger S., Present D.H., Kornbluth A., et al. Cyclosporine in severe ulcerative colitis refractory to steroid therapy. N Engl J Med 1994;330:1841-1845 (Pubitemid 24188135)
26. Seidel N., Volkmann X., Länger F., et al. The extent of liver steatosis in chronic hepatitis C virus infection is mirrored by caspase activity in serum. Hepatology 2005;42:113-120 (Pubitemid 40911318)
27. Bantel H., Lügering A., Poremba C., et al. Caspase activation correlates with the degree of inflammatory liver injury in chronic hepatitis C virus infection. Hepatology 2001;34:758-767 (Pubitemid 32928001)
28. Bantel H., Lügering A., Heidemann J., et al. Detection of apoptotic caspase activation in sera from patients with chronic HCV infection is associated with fibrotic liver injury. Hepatology 2004;40:1078-1087 (Pubitemid 39425563)
29. Zhivotovsky B., Samali A., Gahm A., et al. Caspases: Their intracellular localization and translocation during apoptosis. Cell Death Differ 1999;6:644-651 (Pubitemid 29366654)
30. Saruta M., Yu Q.T., Fleshner P.R., et al. Characterization of FoxP3+CD4+ regulatory T cells in Crohn's disease. Clin Immunol 2007;125:281-290 (Pubitemid 350123608)
31. Ehrenstein M.R., Evans J.G., Singh A., et al. Compromised function of regulatory T cells in rheumatoid arthritis and reversal by anti-TNFalpha therapy. J Exp Med 2004;200:277-285 (Pubitemid 39031247)
32. Takahashi M., Nakamura K., Honda K., et al. An inverse correlation of human peripheral blood regulatory T cell frequency with the disease activity of ulcerative colitis. Dig Dis Sci 2006;51:677-686
33. Toubi E., Kessel A., Mahmudov Z., et al. Increased spontaneous apoptosis of CD4 +CD25+ T cells in patients with active rheumatoid arthritis is reduced by infliximab. Ann N Y Acad Sci 2005;442:157-181
34. Makita S., Kanai T., Oshima S., et al. CD4+CD25bright T cells in human intestinal lamina propria as regulatory cells. J Immunol 2004;173:3119-3130 (Pubitemid 39142018)
35. Reardon C., Wang A., McKay D.M. Transient local depletion of Foxp3+ regulatory T cells during recovery from colitis via Fas/Fas ligand-induced death. J Immunol 2008;180:8316-8326
36. Faubion W.A., De Jong Y.P., Molina A.A., et al. Colitis is associated with thymic destruction attenuating CD4+25+ regulatory T cells in the periphery. Gastroenterology 2004;126:1759-1770 (Pubitemid 38736341)
37. Veltkamp C., Tonkonogy S.L., De Jong Y.P., et al. Continuous stimulation by normal luminal bacteria is essential for the development and perpetuation of colitis in Tg (epsilon26) mice. Gastroenterology 2001;120:900-913 (Pubitemid 32193187)
38. Veltkamp C., Sartor R.B., Giese T., et al. Regulatory CD4+CD25+ cells reverse imbalances in the T cell pool of bone marrow transplanted TGepsilon26 mice leading to the prevention of colitis. Gut 2005;54:207-214 (Pubitemid 40139235)
39. Valencia X., Stephens G., Goldbach-Mansky R., et al. TNF downmodulates the function of human CD4+CD25hi T-regulatory cells. Blood 2006;108:253-261 (Pubitemid 43990636)
40. Goldstein I., Ben-Horin S., Koltakov A., et al. Alpha1beta1 Integrin+ and regulatory Foxp3+ T cells constitute two functionally distinct human CD4+ T cell subsets oppositely modulated by TNFalpha blockade. J Immunol 2007;178:201-210 (Pubitemid 46033602)
41. Maloy K.J., Salaun L., Cahill R., et al. CD4+CD25+ T(R) cells suppress innate immune pathology through cytokine-dependent mechanisms. J Exp Med 2003;197:111-119 (Pubitemid 36110262)
42. Li Z., Arijs I., De Hertogh G., et al. Reciprocal changes of Foxp3 expression in blood and intestinal mucosa in IBD patients responding to infliximab. Inflamm Bowel Dis 2010;16:1299-1310