Human colonic myofibroblasts promote expansion of CD4+ CD25 high Foxp3+ regulatory T cells

Gastroenterology

Volumn 140, Issue 7, 2011, Pages 2019-2030

  Pinchuk, Irina V ^a   Beswick, Ellen J ^b   Saada, Jamal I ^a   Boya, Gushyalatha ^a   Schmitt, David ^a   Raju, Gottumukkala S ^a   Brenmoehl, Julia ^c   Rogler, Gerhard ^d   Reyes, Victor E ^a   Powell, Don W ^a  

^a UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

^b UNIVERSITY OF NEW MEXICO SCHOOL OF MEDICINE   (United States)

^c LEIBNIZ INSTITUTE FOR FARM ANIMAL BIOLOGY FBN   (Germany)

^d UNIVERSITY HOSPITAL ZURICH   (Switzerland)

Author keywords

Immune Regulation; Immune Response; Inflammation; Inflammatory Bowel Disease; Stromal Cells

Indexed keywords

CD4 ANTIGEN; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; INTERLEUKIN 10; INTERLEUKIN 2 RECEPTOR ALPHA; INTERLEUKIN 7 RECEPTOR; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; PROSTAGLANDIN E2; RECOMBINANT INTERLEUKIN 2; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA;

ANTIGEN PRESENTING CELL; ARTICLE; CD4+ CD25+ T LYMPHOCYTE; CELL ACTIVATION; CELL EXPANSION; CELL LINE; CELL MATURATION; CELL PROLIFERATION; COCULTURE; COLON CANCER; COLON CROHN DISEASE; COLON MUCOSA; COLON RESECTION; COLONIC CD90+ MESENCHYMAL MYOFIBROBLAST AND FIBROBLAST; CONTROLLED STUDY; DENDRITIC CELL; EFFECTOR CELL; ENTERITIS; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNE RESPONSE; IMMUNOPHENOTYPING; IMMUNOREGULATION; MAJOR HISTOCOMPATIBILITY COMPLEX; MYOFIBROBLAST; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; ULCERATIVE COLITIS;

EID: 79958169148     PISSN: 00165085     EISSN: 15280012     Source Type: Journal    
DOI: 10.1053/j.gastro.2011.02.059     Document Type: Article

References (41)

1. O. Annacker, and F. Powrie Homeostasis of intestinal immune regulation Microbes Infect 4 2002 567 574 (Pubitemid 34312055)
2. S. Makita, T. Kanai, and Y. Nemoto Intestinal lamina propria retaining CD4+CD25+ regulatory T cells is a suppressive site of intestinal inflammation J Immunol 178 2007 4937 4946 (Pubitemid 46595276)
3. M. Allez, and L. Mayer Regulatory T cells: peace keepers in the gut Inflamm Bowel Dis 10 2004 666 676 (Pubitemid 39276480)
4. Q. Tang, and J.A. Bluestone The Foxp3+ regulatory T cell: a jack of all trades, master of regulation Nat Immunol 9 2008 239 244 (Pubitemid 351267321)
5. H. von Boehmer Mechanisms of suppression by suppressor T cells Nat Immunol 6 2005 338 344 (Pubitemid 41716770)
6. M. Gad Regulatory T cells in experimental colitis Curr Top Microbiol Immunol 293 2005 179 208 (Pubitemid 40791230)
7. F. Powrie, M.W. Leach, and S. Mauze Phenotypically distinct subsets of CD4+ T cells induce or protect from chronic intestinal inflammation in C. B-17 scid mice Int Immunol 5 1993 1461 1471 (Pubitemid 23325202)
8. C. Mottet, H.H. Uhlig, and F. Powrie Cutting edge: cure of colitis by CD4+CD25+ regulatory T cells J Immunol 170 2003 3939 3943 (Pubitemid 36428153)
9. J. Maul, C. Loddenkemper, and P. Mundt Peripheral and intestinal regulatory CD4+ CD25(high) T cells in inflammatory bowel disease Gastroenterology 128 2005 1868 1878 (Pubitemid 40824698)
10. + regulatory T cells Mucosal Immunol 1 Suppl 1 2008 S34 S38
11. A.M. Westendorf, D. Fleissner, and L. Groebe CD4+Foxp3+ regulatory T cell expansion induced by antigen-driven interaction with intestinal epithelial cells independent of local dendritic cells Gut 58 2009 211 219
12. J.I. Saada, I.V. Pinchuk, and C.A. Barrera Subepithelial myofibroblasts are novel nonprofessional APCs in the human colonic mucosa J Immunol 177 2006 5968 5979 (Pubitemid 44628810)
13. A. Andoh, S. Bamba, and M. Brittan Role of intestinal subepithelial myofibroblasts in inflammation and regenerative response in the gut Pharmacol Ther 114 2007 94 106 (Pubitemid 46498158)
14. I.V. Pinchuk, E.J. Beswick, and J.I. Saada Monocyte chemoattractant protein-1 production by intestinal myofibroblasts in response to staphylococcal enterotoxin a: relevance to staphylococcal enterotoxigenic disease J Immunol 178 2007 8097 8106 (Pubitemid 46898082)
15. I.V. Pinchuk, J.I. Saada, and E.J. Beswick PD-1 ligand expression by human colonic myofibroblasts/fibroblasts regulates CD4+ T-cell activity Gastroenterology 135 2008 1228 1237
16. I.V. Pinchuk, R.C. Mifflin, and J.I. Saada Intestinal mesenchymal cells Curr Gastroenterol Rep 12 2010 310 318
17. Y.R. Mahida, J. Beltinger, and S. Makh Adult human colonic subepithelial myofibroblasts express extracellular matrix proteins and cyclooxygenase-1 and -2 Am J Physiol 273 1997 G1341 G1348
18. S.E. Allan, S.Q. Crome, and N.K. Crellin Activation-induced FOXP3 in human T effector cells does not suppress proliferation or cytokine production Int Immunol 19 2007 345 354 (Pubitemid 46523383)
19. T.Y. Wuest, J. Willette-Brown, and S.K. Durum The influence of IL-2 family cytokines on activation and function of naturally occurring regulatory T cells J Leukoc Biol 84 2008 973 980
20. R. Setoguchi, S. Hori, and T. Takahashi Homeostatic maintenance of natural Foxp3(+) CD25(+) CD4(+) regulatory T cells by interleukin (IL)-2 and induction of autoimmune disease by IL-2 neutralization J Exp Med 201 2005 723 735 (Pubitemid 40395118)
21. W. Liu, A.L. Putnam, and Z. Xu-Yu CD127 expression inversely correlates with FoxP3 and suppressive function of human CD4+ T reg cells J Exp Med 203 2006 1701 1711 (Pubitemid 44036276)
22. L. Michel, L. Berthelot, and S. Pettr Patients with relapsing-remitting multiple sclerosis have normal Treg function when cells expressing IL-7 receptor alpha-chain are excluded from the analysis J Clin Invest 118 2008 3411 3419
23. T. Totsuka, T. Kanai, and Y. Nemoto IL-7 Is essential for the development and the persistence of chronic colitis J Immunol 178 2007 4737 4748 (Pubitemid 46595254)
24. K. English, J.M. Ryan, and L. Tobin Cell contact, prostaglandin E(2) and transforming growth factor beta 1 play non-redundant roles in human mesenchymal stem cell induction of CD4+CD25(High) forkhead box P3+ regulatory T cells Clin Exp Immunol 156 2009 149 160
25. P. Brandtzaeg Nature and function of gastrointestinal antigen-presenting cells Allergy 56 Suppl 67 2001 16 20 (Pubitemid 32545228)
26. S.N. Mueller, and R.N. Germain Stromal cell contributions to the homeostasis and functionality of the immune system Nat Rev Immunol 9 2009 618 629
27. M.A. Haniffa, X.N. Wang, and U. Holtick Adult human fibroblasts are potent immunoregulatory cells and functionally equivalent to mesenchymal stem cells J Immunol 179 2007 1595 1604
28. M. Di Ianni, B. Del Papa, and M. De Ioanni Mesenchymal cells recruit and regulate T regulatory cells Exp Hematol 36 2008 309 318 (Pubitemid 351221170)
29. M. Benito-Miguel, Y. Garca-Carmona, and A. Balsa A dual action of rheumatoid arthritis synovial fibroblast IL-15 expression on the equilibrium between CD4+CD25+ regulatory T cells and CD4+CD25- responder T cells J Immunol 183 2009 8268 8279
30. P. Hoffmann, R. Eder, and L.A. Kunz-Schughart Large-scale in vitro expansion of polyclonal human CD4(+)CD25high regulatory T cells Blood 104 2004 895 903 (Pubitemid 38970590)
31. A. Yu, and T.R. Malek Selective availability of IL-2 is a major determinant controlling the production of CD4+CD25+Foxp3+ T regulatory cells J Immunol 177 2006 5115 5121 (Pubitemid 44527582)
32. R.A. Clark, and T.S. Kupper IL-15 and dermal fibroblasts induce proliferation of natural regulatory T cells isolated from human skin Blood 109 2007 194 202 (Pubitemid 46053061)
33. G. Jiang, H.R. Yang, and L. Wang Hepatic stellate cells preferentially expand allogeneic CD4+ CD25+ FoxP3+ regulatory T cells in an IL-2-dependent manner Transplantation 86 2008 1492 1502
34. A. Merlo, E. Tagliabue, and S. Menard Matured human monocyte-derived dendritic cells (MoDCs) induce expansion of CD4(+)CD25(+)FOXP3(+) T cells lacking regulatory properties Immunol Lett 117 2008 106 113
35. D.Q. Tran, H. Ramsey, and E.M. Shevach Induction of FOXP3 expression in naive humanCD4+FOXP3 T cells by T-cell receptor stimulation is transforming growth factor-beta dependent but does not confer a regulatory phenotype Blood 110 2007 2983 2990 (Pubitemid 350006952)
36. E.J. Beswick, I.V. Pinchuk, and S. Das Expression of the programmed death ligand 1, B7-H1, on gastric epithelial cells after Helicobacter pylori exposure promotes development of CD4+ CD25+ FoxP3+ regulatory T cells Infect Immun 75 2007 4334 4341 (Pubitemid 47378090)
37. J. Wang, T.W. Huizinga, and R.E. Toes De novo generation and enhanced suppression of human CD4+CD25+ regulatory T cells by retinoic acid J Immunol 183 2009 4119 4126
38. S.J. Flavell, T.Z. Hou, and S. Lax Fibroblasts as novel therapeutic targets in chronic inflammation Br J Pharmacol 153 Suppl 1 2008 S241 S246
39. B.C. McKaig, K. Hughes, and P.J. Tighe Differential expression of TGF-beta isoforms by normal and inflammatory bowel disease intestinal myofibroblasts Am J Physiol Cell Physiol 282 2002 C172 C182
40. A. Di Sabatino, S.L. Pender, and C.L. Jackson Functional modulation of Crohn's disease myofibroblasts by anti-tumor necrosis factor antibodies Gastroenterology 133 2007 137 149 (Pubitemid 47031137)
41. A. Di Sabatino, C.L. Jackson, and K.M. Pickard Transforming growth factor beta signalling and matrix metalloproteinases in the mucosa overlying Crohn's disease strictures Gut 58 2009 777 789