Increased FOXP3 expression in small-bowel mucosa of children with coeliac disease and type i diabetes mellitus

Scandinavian Journal of Gastroenterology

Volumn 44, Issue 4, 2009, Pages 422-430

  Vorobjova, Tamara ^a   Uibo, Oivi ^a,b   Heilman, Kaire ^a,b   Rägo, Tiina ^b   Honkanen, Jarno ^c   Vaarala, Outi ^c   Tillmann, Vallo ^a,b   Ojakivi, Ivi ^a   Uibo, Raivo ^a  

^a UNIVERSITY OF TARTU   (Estonia)

^b TARTU UNIVERSITY HOSPITAL   (Estonia)

^c NATIONAL PUBLIC HEALTH INSTITUTE   (Finland)

Author keywords

CD25; CD4; Children; Coeliac disease; FOXP3; Immunohistochemistry; Real time PCR; Treg cells; Type I diabetes

Indexed keywords

BIOLOGICAL MARKER; MESSENGER RNA; MONOCLONAL ANTIBODY; TRANSCRIPTION FACTOR FOXP3; CD4 ANTIGEN; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, HUMAN; INTERLEUKIN 2 RECEPTOR ALPHA;

ADOLESCENT; ADULT; ARTICLE; CD25+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CELIAC DISEASE; CELL COUNT; CHILD; COMORBIDITY; CONTROLLED STUDY; DISEASE ASSOCIATION; FEMALE; GENE EXPRESSION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; INFANT; INSULIN DEPENDENT DIABETES MELLITUS; INTESTINE BIOPSY; INTESTINE VILLUS ATROPHY; MAJOR CLINICAL STUDY; MALE; MOUSE; MUCOSA CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SMALL INTESTINE MUCOSA; STAINING; CASE CONTROL STUDY; GENETICS; INTESTINE MUCOSA; METABOLISM; PATHOLOGY; PHYSIOLOGY; PRESCHOOL CHILD; REGULATORY T LYMPHOCYTE; SMALL INTESTINE;

ADOLESCENT; ANTIGENS, CD4; CASE-CONTROL STUDIES; CELIAC DISEASE; CHILD; CHILD, PRESCHOOL; DIABETES MELLITUS, TYPE 1; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; INFANT; INTERLEUKIN-2 RECEPTOR ALPHA SUBUNIT; INTESTINAL MUCOSA; INTESTINE, SMALL; MALE; RNA, MESSENGER; T-LYMPHOCYTES, REGULATORY; YOUNG ADULT;

EID: 67049173940     PISSN: 00365521     EISSN: 15027708     Source Type: Journal    
DOI: 10.1080/00365520802624177     Document Type: Article

References (55)

1. Catassi C, Ratsch I-M, Fabiani E, Rossini M, Bordicchia F, Candela F, et al. Coeliac disease in the year 2000: exploring the iceberg. Lancet 1994;343:200-3.
2. Kolho KL, Färkkilä MA, Savilahti E. Undiagnosed celiac disease is common in Finnish adults. Scand J Gastroenterol 1998;33:1280-3.
3. Marsh MN. Gluten, major histocompatibility complex, and the small intestine: a molecular and immunobiologic approach to the spectrum of gluten sensitivity ("celiac sprue"). Gastroenterology 1992;102:330-54.
4. Ress K, Harro M, Maroos H-I, Harro J, Uibo R, Uibo O. High prevalence of celiac disease: need for increasing awareness among physicians. Dig Liv Dis 2007;39:136-9.
5. Green PH, Jabri B. Celiac disease. Lancet 2003;362:383-91.
6. Sollid LM. Molecular basis of celiac disease. Annu Rev Immunol 2000;18:53-81.
7. Croitoru K, Zhou P. T-cell-induced mucosal damage in the intestine. Curr Opin Gastroenterol 2004;20:581-6.
8. Banham AH, Powrie FM, Suri-Payer E. FOXP3+ regulatory T cells: current controversies and future perspectives. Eur J Immunol 2006;36:2832-6.
9. Gianfrani C, Levings MK, Sartirana C, Mazzarella G, Barba G, Zanzi D, 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.
10. bright T cells in human intestinal lamina propria as regulatory cells. J Immunol 2004;173:3119-30.
11. Kagnoff MF. Celiac disease: pathogenesis of a model immunogenetic disease. J Clin Invest 2007;117:41-9.
12. Koning F, Schuppan D, Cerf-Bensussan N, Sollid LM. Pathomechanism in celiac disease. Best Pract Res Clin Gastroenterol 2005;19:373-87.
13. Powrie F, Read S, Mottet C, Uhlig H, Maloy K. Control of immune pathology by regulatory T cells. Novartis Found Symp 2003;252:92-8.
14. Uhlig HH, Coombes J, Mottet C, Izcue A, Thompson C, Fanger A, et al. Characterization of Foxp3+CD4+CD25+ and IL-10 secreting CD4+CD25+T cells during cure of colitis. J Immunol 2006;177:5852-60.
15. Campbell DJ, Ziegler SF. FOXP3 modifies the phenotypic and functional properties of regulatory T cells. Nat Rev Immunol 2007;7:305-10.
16. Sakaguchi S, Sakaguchi N, Asano M, Itoh M, Toda M. Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor a-chains (CD25). Breakdown of a single mechanism of self-tolerance causes various autoimmune diseases. J Immunol 1995;155:1151-64.
17. Sakaguchi S. Naturally arising Foxp3-expressing CD25 + CD4+ regulatory T cells in immunological tolerance to self and non-self. Nature Immunol 2005;6:345-52.
18. Shevach EM. Regulatory T cells in autoimmunity. Ann Rev Immunol 2000;18:423.
19. +regulatory T cells in the control of autoimmunity: in vivo veritas. Curr Opin Immunol 2008;20: 655-62.
20. von Herrath M, Harrison LC. Antigen-induced regulatory T cells in autoimmunity. Nat Rev Immunol 2003;3:223-32.
21. Zhang L, Zhao Y. The regulation of Foxp3 expression in regulatory CD4 + CD25 + T cells: multiple pathways on the road. J Cell Physiol 2007;211:590-7.
22. Brunkow ME, Jeffery EW, Hjerrild KA, Paeper B, Clark LB, Yasayko S-A, et al. Disruption of a new forkhead/winged-helix protein, scurfin, results in the fatal lymphoproliferative disorder of the scurfy mouse. Nat Genet 2001;27:68-73.
23. Ramsdell F, Ziegler S. Transcription factors in autoimmunity. Curr Opin Immunol 2003;15:718-24.
24. Dejaco C, Duftner C, Grubeck-Loebenstein B, Schirmer M. Imbalance of regulatory T cells in human autoimmune diseases. Immunology 2006;117:289-300.
25. Ziegler SF. FOXP3: Of mice and men. Annu Rev Immunol 2006;24:209-26.
26. Mottet C, Uhlig HH, Powrie F Cutting edge: cure of colitis by CD4 + CD25 + regulatory T cells. J Immunol 2003;170: 3939-43.
27. Coombes JL, Robinson NJ, Maloy KJ, Uhlig HH, Powrie F. Regulatory T cells and intestinal homeostasis. Immunol Rev 2005;204:184-94.
28. Pillai V, Karandikar NJ. Human regulatory T cells: a unique thymic subset or a reversible peripheral state of differentiation? Immunol Lett 2007;114:9-15.
29. Izcue A, Powrie F. Special regulatory T-cell review: regulatory T cells and the intestinal tract-patrolling the frontier. Immunology 2008;123:6-10.
30. Fontenot JD, Gavin MA, Rudensky AY. FOXP3 programmes the development and function of CD4 + CD25 + regulatory T cells. Nat Immunol 2003;4:330-6.
31. Hori S, Nomura T, Sakaguchi S. Control of regulatory T cell development by the transcription factor FOXP3. Science 2003;299:1057-61.
32. Saukkonen T, Ilonen J, Akerblom HK, Savilahti E. Prevalence of celiac disease in siblings of patients with Type 1 diabetes is related to the prevalence of DQB1*02 allele. Diabetologia 2001;44:1051-3.
33. Rewers M, Liu E, Simmons J, Redondo MJ, Hoffenberg EJ. Celiac disease associated with type 1 diabetes mellitus. Endocrinol Metab Clin North Am 2004;33:197-214.
34. Sumnik Z, Kolouskova S, Malcova H, Vavrinec J, Venhacova J, Lebi J, et al. High prevalence of celiac disease in siblings of children with type 1 diabetes. Eur J Pediatr 2005;164:9-12.
35. Holmes GKT. Screening for coeliac disease in type 1 diabetes. Arch Dis Child 2002;87:495-9.
36. Larsson K, Carlsson A, Cederwall E, Jönsson B, Neiderud J, Jonsson B, et al. The Skane Study Group. Pediatr Diabetes 2008;9:354-9.
37. Kukreja A, Cost G, Marker J, Zhang C, Sun Z, Lin-Su K et al. Multiple immuno-regulatory defects in type-1 diabetes. J Clin Invest 2002;109:131-40.
38. Tritt M, Sgouroudis E, d'Hennezel E, Albanese A, Piccirillo CA. Functional waning of naturally occurring CD4 + regulatory T-cells contributes to the onset of autoimmune diabetes. Diabetes 2008;57:113-23.
39. Walker-Smith J, Guandalini S, Schmitz J, Shmerling DH, Visakorpi JK. Revised criteria for diagnosis of celiac disease. Report of the working group of the European Society of Pediatric Gastroenterology and Nutrition. Arch Dis Child 1990;65:909-11.
40. Roncador G, Brown PJ, Maestre L, Hue S, Martinez-Torrecuadrada JL, Ling KL, et al. Analysis of FOXP3 protein expression in human CD4 + CD25+ regulatory T cells at the single-cell level. Eur J Immunol 2005;35: 1681-91.
41. Tiittanen M, Westerholm-Ormio M, Verkasalo M, Savilahti E, Vaarala O. Infiltration of forkhead box P3-expressing cells in small intestinal mucosa in coeliac disease but not in type 1 diabetes. Clin Exp immunol 2008;152:498-507.
42. Halstensen TS, Brandztaeg 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.
43. Belkaid Y, Rouse B. Natural regulatory T cells in infectious disease. Nat Immunol 2005;6:353-60.
44. Link M, Salur L, Kisand K, Rajasalu T, Tillmann V, Uibo R. Higher FOXP3 mRNA expression in peripheral blood mononuclear cells of GAD65 or IA-2 autoantibody-positive compared with autoantibody-negative persons. APMIS 2008; 116. In press.
45. Tree TI, Roep BO, Peakman M. A mini meta-analysis of studies on CD4 + CD25+ T cells in human type 1 diabetes. Ann NY Acad Sci 2006;1079:9-18.
46. Brusko T, Wasserfall C, McGrail K, Schatz R, Viener HL, Schatz D, et al. No alterations in the frequency of FOXP3 + regulatory T-cells in type 1 diabetes. Diabetes 2007;56: 604-12.
47. Putnam AL, Vendrame F, Dotta F, Gottlieb PA. CD4 + CD25high regulatory T cells in human autoimmune diabetes. J Autoimmun 2005;24:55-62.
48. Olaussen RW, Karlsson MR, Lundin KEA, Jahnsen J, Brandtzaeg P, Farstad IN. Reduced chemokine receptor 9 on intraepithelial lymphocytes in celiac disease suggests persistent epithelial activation. Gastroenterology 2007;132: 2371-82.
49. Brandtzaeg P. The changing immunological paradigm in coeliac disease. Immunol Lett 2006;105:127-39.
50. Sitohy B, Hammarstrom S, Danileson A, Hammarstrom ML. Basal lymphoid aggregates in ulcerative colitis colon: a site for regulatory T cell action. Clin Exp Immunol 2007; 151:326-33.
51. Okui T, Ito H, Honda T, Amanuma R, Yoshie H, Yamazaki K. Characterization of CD4+ FOXP3+ T-cell clones established from chronic inflammatory lesions. Oral Microbiol Immunol 2008;23:49-54.
52. Suri-Payer E, Fritzsching B. Regulatory T cells in experimental autoimmune disease. Springer Semin Immunol 2006;28:3-16.
53. Kolkowski EC, Fernandez MA. Pujol-Borrell R, Jaraque-mada D. Human intestinal ab IEL clones in celiac disease show reduced IL-10 synthesis and enhanced IL-2 production. Cell Immunol 2006;244:1-9.
54. Fina D, Sarra M, Caruso R, Del Vecchio Blanco G, Pallone F, MacDonald TT, et al. Interleukin 21 contributes to the mucosal T helper cell type 1 response in coeliac disease. Gut 2008;57:879-81.
55. Garrote JA, Gomez-Gonalez E, Bernardo D, Arranz E, Chirdo F. Celiac disease pathogenesis: the proinflammatory cytokine network. J Pediatr Gastroenterol Nutr 2008;47: Suppl 1:S27-32.