Infiltration of forkhead box P3-expressing cells in small intestinal mucosa in coeliac disease but not in type 1 diabetes

Clinical and Experimental Immunology

Volumn 152, Issue 3, 2008, Pages 498-507

  Tiittanen, M ^a   Westerholm Ormio, M ^b   Verkasalo, M ^b   Savilahti, E ^b   Vaarala, O ^a,c  

^a NATIONAL PUBLIC HEALTH INSTITUTE   (Finland)

^b UNIVERSITY OF HELSINKI   (Finland)

^c LINKÖPING UNIVERSITY   (Sweden)

Author keywords

Coeliac disease; FoxP3; Gut; Regulatory T cells; Type 1 diabetes

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 18; MESSENGER RNA; TRANSCRIPTION FACTOR FOXP3;

ARTICLE; CELIAC DISEASE; CELL INFILTRATION; CHILD; CONTROLLED STUDY; HUMAN; IMMUNOHISTOCHEMISTRY; INSULIN DEPENDENT DIABETES MELLITUS; MAJOR CLINICAL STUDY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SMALL INTESTINE MUCOSA; T LYMPHOCYTE; UPREGULATION;

ADOLESCENT; CELIAC DISEASE; CHILD; CHILD, PRESCHOOL; CYTOKINES; DIABETES MELLITUS, TYPE 1; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; IMMUNITY, MUCOSAL; IMMUNOENZYME TECHNIQUES; INFANT; INTERFERON TYPE II; INTERLEUKIN-2 RECEPTOR ALPHA SUBUNIT; INTESTINAL MUCOSA; INTESTINE, SMALL; MALE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; T-LYMPHOCYTES, REGULATORY;

EID: 43349106670     PISSN: 00099104     EISSN: 13652249     Source Type: Journal    
DOI: 10.1111/j.1365-2249.2008.03662.x     Document Type: Article

References (42)

1. Holm K, Mäki M, Savilahti E, Lipsanen V, Laippala P, Koskimies S. Intraepithelial gamma delta T-cell-receptor lymphocytes and genetic susceptibility to coeliac disease. Lancet 1992 339 : 1500 3.
2. Maiuri L, Ciacci C, Ricciardelli I et al. Association between innate response to gliadin and activation of pathogenic T cells in coeliac disease. Lancet 2003 362 : 30 7.
3. Meresse B, Chen Z, Ciszewski C et al. Coordinated induction by IL15 of a TCR-independent NKG2D signaling pathway converts CTL into lymphokine-activated killer cells in celiac disease. Immunity 2004 21 : 357 66.
4. Koning F, Schuppan D, Cerf-Bensussan N, Sollid LM. Pathomechanisms in celiac disease. Best Pract Res Clin Gastroenterol 2005 19 : 373 87.
5. Kontakou M, Sturgess RP, Przemioslo RT, Limb GA, Nelufer JM, Ciclitira PJ. Detection of interferon gamma mRNA in the mucosa of patients with coeliac disease by in situ hybridisation. Gut 1994 35 : 1037 41.
6. Przemioslo RT, Kontakou M, Nobili V, Ciclitira PJ. Raised pro-inflammatory cytokines interleukin 6 and tumour necrosis factor alpha in coeliac disease mucosa detected by immunohistochemistry. Gut 1994 5 : 1398 403.
7. Holm K, Savilahti E, Koskimies S, Lipsanen V, Mäki M. Immunohistochemical changes in the jejunum in first degree relatives of patients with coeliac disease and the coeliac disease marker DQ genes. HLA class II antigen expression, interleukin-2 receptor positive cells and dividing crypt cells. Gut 1994 35 : 55 60.
8. Green PH, Rostami K, Marsh M. Diagnosis of coeliac disease. Best Pract Res Clin Gastroenterol 2005 19 : 389 400.
9. Holmes GK. Screening for coeliac disease in type 1 diabetes. Arch Dis Child 2002 87 : 495 8.
10. Klemetti P, Savilahti E, Ilonen J, Åkerblom HK, Vaarala O. T-cell reactivity to wheat gluten in patients with insulin-dependent diabetes mellitus. Scand J Immunol 1998 47 : 48 53.
11. MacFarlane AJ, Burghardt KM, Kelly J et al. A type 1 diabetes-related protein from wheat (Triticum aestivum). cDNA clone of a wheat storage globulin, Glb1, linked to islet damage. J Biol Chem 2003 278 : 54 63.
12. Auricchio R, Paparo F, Maglio M et al. In vitro-deranged intestinal immune response to gliadin in type 1 diabetes. Diabetes 2004 53 : 1680 3.
13. Westerholm-Ormio M, Vaarala O, Pihkala P, Ilonen J, Savilahti E. Immunologic activity in the small intestinal mucosa of pediatric patients with type 1 diabetes. Diabetes 2003 52 : 2287 95.
14. Fontenot JD, Rudensky AY. A well adapted regulatory contrivance: regulatory T cell development and the forkhead family transcription factor Foxp3. Nat Immunol 2005 6 : 331 7.
15. Sakaguchi S. Naturally arising Foxp3-expressing CD25+CD4+ regulatory T cells in immunological tolerance to self and non-self. Nat Immunol 2005 6 : 345 52.
16. Revised Criteria for Diagnosis of Coeliac Disease. Report of the Working Group of European Society of Paediatric Gastroenterology and Nutrition. Arch Dis Child 1990 65 : 909 11.
17. Savilahti E, Arato A, Verkasalo M. Intestinal gamma/delta receptor-bearing T lymphocytes in celiac disease and inflammatory bowel diseases in children. Constant increase in celiac disease. Pediatr Res 1990 28 : 579 81.
18. Westerholm-Ormio M, Garioch J, Ketola I, Savilahti E. Inflammatory cytokines in small intestinal mucosa of patients with potential coeliac disease. Clin Exp Immunol 2002 128 : 94 101.
19. Fontenot JD, Gavin MA, Rudensky AY. Foxp3 programs the development and function of CD4+CD25+ regulatory T cells. Nat Immunol 2003 4 : 330 6.
20. Khattri R, Cox T, Yasayko S-A, Ramsdell F. An essential role for Scurfin in CD4+CD25+ T regulatory cells. Nat Immunol 2003 4 : 337 42.
21. Walker MR, Kasprowicz DJ, Gersuk VH et al. Induction of FoxP3 and acquisition of T regulatory activity by stimulated human CD4+CD25- T cells. J Clin Invest 2003 112 : 1437 43.
22. Morgan ME, van Bilsen JH, Bakker AM et al. Expression of FOXP3 mRNA is not confined to CD4+CD25+ T regulatory cells in humans. Hum Immunol 2005 66 : 13 20.
23. 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 64.
24. Wang J, Ioan-Facsinay A, van der Voort EI, Huizinga TW, Toes RE. Transient expression of FOXP3 in human activated nonregulatory CD4+ T cells. Eur J Immunol 2007 37 : 129 38.
25. Halstensen TS, Brandtzaeg P. Activated T lymphocytes in the celiac lesion: non-proliferative activation (CD25) of CD4+ alpha/beta cells in the lamina propria but proliferation (Ki-67) of alpha/beta and gamma/delta cells in the epithelium. Eur J Immunol 1993 23 : 505 10.
26. Nilsen EM, Jahnsen FL, Lundin KE et al. Gluten induces an intestinal cytokine response strongly dominated by interferon gamma in patients with celiac disease. Gastroenterology 1998 115 : 551 63.
27. Halstensen TS, Scott H, Fausa O, Brandtzaeg P. Gluten stimulation of coeliac mucosa in vitro induces activation (CD25) of lamina propria CD4+ T cells and macrophages but no crypt-cell hyperplasia. Scand J Immunol 1993 38 : 581 90.
28. Gregg RK, Jain R, Schoenleber SJ et al. A sudden decline in active membrane-bound TGF-β impairs both T regulatory cell function and protection against autoimmune diabetes. J Immunol 2004 173 : 7308 16.
29. + T cells with regulatory properties can be cultured from colonic mucosa of patients with Crohn's disease. Clin Exp Immunol 2005 141 : 549 57.
30. Hue S, Mention JJ, Monteiro RC et al. A direct role for NKG2D/MICA interaction in villous atrophy during celiac disease. Immunity 2004 21 : 367 77.
31. Stock P, Akbari O, Berry G, Freeman GJ, Dekruyff RH, Umetsu DT. Induction of T helper type 1-like regulatory cells that express Foxp3 and protect against airway hyper-reactivity. Nat Immunol 2004 5 : 1149 56.
32. Forsberg G, Hernell O, Melgar S, Israelsson A, Hammarström S, Hammarström ML. Paradoxical coexpression of proinflammatory and down-regulatory cytokines in intestinal T cells in childhood celiac disease. Gastroenterology 2002 123 : 667 78.
33. Salvati VM, Mazzarella G, Gianfrani C et al. Recombinant human interleukin 10 suppresses gliadin dependent T cell activation in ex vivo cultured coeliac intestinal mucosa. Gut 2005 54 : 46 53.
34. Gianfrani C, Levings MK, Sartirana C et al. Gliadin-specific type 1 regulatory T cells from the intestinal mucosa of treated celiac patients inhibit pathogenic T cells. J Immunol 2006 177 : 4178 86.
35. Maiuri L, Ciacci C, Auricchio S, Brown V, Quaratino S, Londei M. Interleukin 15 mediates epithelial changes in celiac disease. Gastroenterology 2000 119 : 996 1006.
36. Salvati VM, MacDonald TT, Bajaj-Elliott M et al. Interleukin 18 and associated markers of T helper cell type 1 activity in coeliac disease. Gut 2002 50 : 186 90.
37. Mention JJ, Ben Ahmed M, Bègue B et al. Interleukin 15: a key to disrupted intraepithelial lymphocyte homeostasis and lymphomagenesis in celiac disease. Gastroenterology 2003 125 : 730 45.
38. León AJ, Garrote JA, Blanco-Quirós A et al. Interleukin 18 maintains a long-standing inflammation in coeliac disease patients. Clin Exp Immunol 2006 146 : 479 85.
39. Pirhonen J, Sareneva T, Julkunen I, Matikainen S. Virus infection induces proteolytic processing of IL-18 in human macrophages via caspase-1 and caspase-3 activation. Eur J Immunol 2001 31 : 726 33.
40. Hong TP, Andersen NA, Nielsen K et al. Interleukin-18 mRNA, but not interleukin-18 receptor mRNA, is constitutively expressed in islet beta-cells and up-regulated by interferon-gamma. Eur Cytokine Netw 2000 11 : 193 205.
41. Nicoletti F, Conget I, Di Marco R et al. Serum levels of the interferon-gamma-inducing cytokine interleukin-18 are increased in individuals at high risk of developing type I diabetes. Diabetologia 2001 44 : 309 11.
42. Kretowski A, Mironczuk K, Karpinska A et al. Interleukin-18 promoter polymorphisms in type 1 diabetes. Diabetes 2002 51 : 3347 9.