Restoration of Foxp3 + Regulatory T-cell Subsets and Foxp3-Type 1 Regulatory-like T Cells in Inflammatory Bowel Diseases during Anti-tumor Necrosis Factor Therapy

Inflammatory Bowel Diseases

Volumn 21, Issue 10, 2015, Pages 2418-2428

  Li, Zhe ^a   Vermeire, Séverine ^a   Bullens, Dominique ^a   Ferrante, Marc ^a   Van Steen, Kristel ^a,b   Noman, Maja ^a   Rutgeerts, Paul ^a   Ceuppens, Jan L ^a   Van Assche, Gert ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b UNIVERSITY OF LIÈGE   (Belgium)

Author keywords

anti TNF therapy; Foxp3 + Treg subsets; inflammatory bowel diseases; prognosis; type 1 regulatory like T cells

Indexed keywords

C REACTIVE PROTEIN; CD4 ANTIGEN; CD45RA ANTIGEN; INFLIXIMAB; INTERLEUKIN 2 RECEPTOR ALPHA; INTERLEUKIN 7 RECEPTOR; TRANSCRIPTION FACTOR FOXP3; CD45 ANTIGEN; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, HUMAN; GASTROINTESTINAL AGENT; TUMOR NECROSIS FACTOR ALPHA;

ACTIVATED REGULATORY T LYMPHOCYTE; ADULT; AGED; ARTICLE; BLOOD SAMPLING; CLINICAL EVALUATION; COMPARATIVE STUDY; CONTROLLED STUDY; CROHN DISEASE; DRUG BLOOD LEVEL; DRUG RESPONSE; EFFECTOR CELL; FEMALE; FLOW CYTOMETRY; HUMAN; IMMUNOFLUORESCENCE; INFLAMMATORY BOWEL DISEASE; LONGITUDINAL STUDY; MAJOR CLINICAL STUDY; MALE; MIDDLE AGED; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; RESTING REGULATORY T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; T LYMPHOCYTE SUBPOPULATION; TYPE 1 REGULATORY LIKE T LYMPHOCYTE; ULCERATIVE COLITIS; UPREGULATION; BLOOD; CASE CONTROL STUDY; CD4+ T LYMPHOCYTE; CYTOLOGY; IMMUNOLOGY; INFLAMMATORY BOWEL DISEASES; METABOLISM; NORMAL HUMAN;

ADULT; AGED; ANTIGENS, CD45; CASE-CONTROL STUDIES; CD4-POSITIVE T-LYMPHOCYTES; FEMALE; FLOW CYTOMETRY; FORKHEAD TRANSCRIPTION FACTORS; GASTROINTESTINAL AGENTS; HEALTHY VOLUNTEERS; HUMANS; INFLAMMATORY BOWEL DISEASES; INFLIXIMAB; MALE; MIDDLE AGED; T-LYMPHOCYTES, REGULATORY; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84942246546     PISSN: 10780998     EISSN: 15364844     Source Type: Journal    
DOI: 10.1097/MIB.0000000000000509     Document Type: Article

References (46)

1. Abraham C, Cho JH. Mechanisms of disease inflammatory bowel disease. N Engl J Med. 2009;361:2066-2078.
2. Mayne CG, Williams CB. Induced and natural regulatory t cells in the development of inflammatory bowel disease. Inflamm Bowel Dis. 2013; 19:1772-1788.
3. 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.
4. 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.
5. Kuhn R, Lohler J, Rennick D, et al. Interleukin-10-deficient mice develop chronic enterocolitis. Cell. 1993;75:263-274.
6. Powrie F, Leach MW, Mauze S, et al. Phenotypically distinct subsets of CD4+ T cells induce or protect from chronic intestinal inflammation in C. B-17 scid mice. Int Immunol. 1993;5:1461-1471.
7. Maloy KJ, Powrie F. Regulatory T cells in the control of immune pathology. Nat Immunol. 2001;2:816-822.
8. Sakaguchi S, Sakaguchi N, Shimizu J, et al. Immunologic tolerance maintained by CD25+ CD4+ regulatory T cells: their common role in controlling autoimmunity, tumor immunity, and transplantation tolerance. Immunol Rev. 2001;182:18-32.
9. Hori S, Nomura T, Sakaguchi S. Control of regulatory T cell development by the transcription factor Foxp3. Science. 2003;299:1057-1061.
10. Chavele KM, Ehrenstein MR. Regulatory T-cells in systemic lupus erythematosus and rheumatoid arthritis. FEBS Lett. 2011;585:3603-3610.
11. Shalev I, Schmelzle M, Robson SC, et al. Making sense of regulatory T cell suppressive function. Semin Immunol. 2011;23:282-292.
12. Haringer B, Lozza L, Steckel B, et al. Identification and characterization of IL-10/IFN-gamma-producing effector-like T cells with regulatory function in human blood. J Exp Med. 2009;206:1009-1017.
13. Trivedi C, Kao J, Saxena M, et al. Efficacy, safety and durability of anti-TNF therapy in the treatment of inflammatory bowel disease. Am J Gastroenterol. 2008;103:S448.
14. Rutgeerts P, Sandborn WJ, Feagan BG, et al. Infliximab for induction and maintenance therapy for ulcerative colitis. N Engl J Med. 2005;353: 2462-2476.
15. Lewis JD. Anti-TNF antibodies for Crohn's disease-in pursuit of the perfect clinical trial. N Engl J Med. 2007;357:296-298.
16. Nadkarni S, Mauri C, Ehrenstein MR. 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.
17. 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.
18. 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.
19. Boschetti G, Nancey S, Sardi F, et al. Therapy with anti-TNFalpha antibody enhances number and function of Foxp3(+) regulatory T cells in inflammatory bowel diseases. Inflamm Bowel Dis. 2011;17:160-170.
20. Allan SE, Crome SQ, Crellin NK, et al. Activation-induced FOXP3 in human T effector cells does not suppress proliferation or cytokine production. Int Immunol. 2007;19:345-354.
21. Gavin MA, Torgerson TR, Houston E, et al. Single-cell analysis of normal and FOXP3-mutant human T cells: FOXP3 expression without regulatory T cell development. Proc Natl Acad Sci USA. 2006;103:6659-6664.
22. Tran DQ, Ramsey H, Shevach EM. Induction of FOXP3 expression in naive human CD4+FOXP3 T cells by T-cell receptor stimulation is transforming growth factor-beta dependent but does not confer a regulatory phenotype. Blood. 2007;110:2983-2990.
23. Wang J, Ioan-Facsinay A, van der Voort EI, et al. Transient expression of FOXP3 in human activated nonregulatory CD4+ T cells. Eur J Immunol. 2007;37:129-138.
24. Sakaguchi S. Naturally arising CD4+ regulatory t cells for immunologic self-tolerance and negative control of immune responses. Annu Rev Immunol. 2004;22:531-562.
25. Miyara M, Yoshioka Y, Kitoh A, et al. Functional delineation and differentiation dynamics of human CD4+ T cells expressing the FoxP3 transcription factor. Immunity. 2009;30:899-911.
26. Vermeire S, Van Assche G, Rutgeerts P. C-reactive protein as a marker for inflammatory bowel disease. Inflamm Bowel Dis. 2004;10:661-665.
27. Vermeire S, Van Assche G, Rutgeerts P. Laboratory markers in IBD: useful, magic, or unnecessary toys? Gut. 2006;55:426-431.
28. Mendoza JL, Abreu MT. Biological markers in inflammatory bowel disease: practical consideration for clinicians. Gastroenterol Clin Biol. 2009; 33(suppl 3):S158-S173.
29. Ryba M, Marek N, Hak L, et al. Anti-TNF rescue CD4+Foxp3+ regulatory T cells in patients with type 1 diabetes from effects mediated by TNF. Cytokine. 2011;55:353-361.
30. Sugita S, Yamada Y, Kaneko S, et al. Induction of regulatory T cells by infliximab in Behcet's disease. Invest Ophthalmol Vis Sci. 2011;52: 476-484.
31. Chen W, Jin W, Hardegen N, et al. Conversion of peripheral CD4+CD25-naive T cells to CD4+CD25+ regulatory T cells by TGF-beta induction of transcription factor Foxp3. J Exp Med. 2003;198:1875-1886.
32. Yamagiwa S, Gray JD, Hashimoto S, et al. A role for TGF-beta in the generation and expansion of CD4+CD25+ regulatory T cells from human peripheral blood. J Immunol. 2001;166:7282-7289.
33. Notley CA, Inglis JJ, Alzabin S, et al. Blockade of tumor necrosis factor in collagen-induced arthritis reveals a novel immunoregulatory pathway for Th1 and Th17 cells. J Exp Med. 2008;205:2491-2497.
34. Taylor PC, Peters AM, Paleolog E, et al. Reduction of chemokine levels and leukocyte traffic to joints by tumor necrosis factor alpha blockade in patients with rheumatoid arthritis. Arthritis Rheum. 2000;43:38-47.
35. Tak PP, Taylor PC, Breedveld FC, et al. Decrease in cellularity and expression of adhesion molecules by anti-tumor necrosis factor alpha monoclonal antibody treatment in patients with rheumatoid arthritis. Arthritis Rheum. 1996;39:1077-1081.
36. Rahman MK, Offord CP, Khanna S, et al. Regulatory T cell kinetics in the peripheral blood of patients with Crohn's disease. Hum Immunol. 2013; 74:145-150.
37. Greiner K, Murphy CC, Willermain F, et al. Anti-TNFalpha therapy modulates the phenotype of peripheral blood CD4+ T cells in patients with posterior segment intraocular inflammation. Invest Ophthalmol Vis Sci. 2004;45:170-176.
38. Ohshima S, Saeki Y, Mima T, et al. Long-term follow-up of the changes in circulating cytokines, soluble cytokine receptors, and white blood cell subset counts in patients with rheumatoid arthritis (RA) after monoclonal anti-TNF alpha antibody therapy. J Clin Immunol. 1999;19:305-313.
39. Louis E, Vermeire S, Rutgeerts P, et al. A positive response to infliximab in Crohn disease: association with a higher systemic inflammation before treatment but not with-308 TNF gene polymorphism. Scand J Gastroenterol. 2002;37:818-824.
40. Ferrante M, Vermeire S, Katsanos KH, et al. Predictors of early response to infliximab in patients with ulcerative colitis. Inflamm Bowel Dis. 2007; 13:123-128.
41. Jurgens M, Mahachie John JM, Cleynen I, et al. Levels of C-reactive protein are associated with response to infliximab therapy in patients with Crohn's disease. Clin Gastroenterol Hepatol. 2011;9:421-427.e1.
42. Rutgeerts P, Vermeire S, Van Assche G. Predicting the response to infliximab from trough serum levels. Gut. 2010;59:7-8.
43. Levesque BG, Greenberg GR, Zou G, et al. A prospective cohort study to determine the relationship between serum infliximab concentration and efficacy in patients with luminal Crohn's disease. Aliment Pharmacol Ther. 2014;39:1126-1135.
44. Arijs I, Quintens R, Van Lommel L, et al. Predictive value of Epithelial gene expression Profiles for response to infliximab in Crohn's disease. Inflamm Bowel Dis. 2010;16:2090-2098.
45. Hlavaty T, Ferrante M, Henckaerts L, et al. Predictive model for the outcome of infliximab therapy in Crohn's disease based on apoptotic pharmacogenetic index and clinical predictors. Inflamm Bowel Dis. 2007;13:372-379.
46. Ferkolj I, Ihan A, Markovic S. CD19+ in intestinal mucosa predict the response to infliximab in Crohn's disease. Hepatogastroenterology. 2005; 52:1128-1133.