Lower expression of tight junction protein 1 gene and increased FOXP3 expression in the small bowel mucosa in coeliac disease and associated type 1 diabetes mellitus

International Archives of Allergy and Immunology

Volumn 156, Issue 4, 2011, Pages 451-461

  Vorobjova, Tamara ^a   Uibo, Oivi ^a   Ojakivi, Ivi ^a   Teesalu, Kaupo ^a   Panarina, Marina ^a   Heilman, Kaire ^a   Uibo, Raivo ^a  

^a UNIVERSITY OF TARTU   (Estonia)

Author keywords

Coeliac disease; Food antigens; FOXP3; IgA antibodies; IgG antibodies; Regulatory T cells; Tight junction protein 1; Type 1 diabetes

Indexed keywords

ALPHA CASEIN; GLIADIN ANTIBODY; IMMUNOGLOBULIN A ANTIBODY; IMMUNOGLOBULIN G ANTIBODY; IMMUNOGLOBULIN M ANTIBODY; MESSENGER RNA; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE ANTIBODY; PROTEIN ZO1; TRANSCRIPTION FACTOR FOXP3;

ANTIBODY BLOOD LEVEL; ARTICLE; CELIAC DISEASE; CHILD; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE ASSOCIATION; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; GENE EXPRESSION; HUMAN; HUMAN TISSUE; INSULIN DEPENDENT DIABETES MELLITUS; INTESTINE BIOPSY; INTESTINE MUCOSA PERMEABILITY; MALE; PRESCHOOL CHILD; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; SCHOOL CHILD; SMALL INTESTINE MUCOSA;

ADOLESCENT; CELIAC DISEASE; CHILD; CHILD, PRESCHOOL; DIABETES MELLITUS, TYPE 1; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION; GLIADIN; HUMANS; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; INTESTINAL MUCOSA; INTESTINE, SMALL; MALE; MEMBRANE PROTEINS; PHOSPHOPROTEINS; RNA, MESSENGER;

EID: 81155158231     PISSN: 10182438     EISSN: 14230097     Source Type: Journal    
DOI: 10.1159/000324456     Document Type: Article

References (54)

1. Stevenson BR, Siliciano JD, Mooseker MS, Goodenough DA: Identification of ZO-1: a high molecular weight polypeptide associated with the tight junction (zonula occludens) in a variety of epithelia. J Cell Biol 1986; 103: 755-766. (Pubitemid 17177325)
2. Fasano A, Shea-Donohue T: Mechanisms of disease: the role of intestinal barrier function in the pathogenesis of gastrointestinal autoimmune diseases. Nat Clin Pract Gastroenterol Hepatol 2005; 9: 416-422. (Pubitemid 41486094)
3. Turner JR: Intestinal mucosal barrier function in health and disease. Nat Rev Immunol 2009; 9: 799-809.
4. Guttman JA, Finlay BB: Tight junctions as targets of infectious agents. Biochim Biophys Acta 2009; 1788: 832-841.
5. Green PH, Jabri B: Celiac disease. Lancet 2003; 362: 383-391.
6. Ciccocioppo R, Di Sabatino A, Corazza GR: The immune recognition of gluten in coeliac disease. Clin Exp Immunol 2005; 140: 408-416. (Pubitemid 40823041)
7. Hopper AD, Hadjivassiliou M, Butt S, Sanders DS: Adult coeliac disease. BMJ 2007; 335: 558-562. (Pubitemid 47477689)
8. Myléus A, Ivarsson A, Webb C, Danielsson L, Hernell O, Högberg L, Karlsson E, Lagerqvist C, Norström F, Rosèn A, Sandström O, Stenhammer L, Steinlund H, Wall S, Carlsson A: Celiac disease revealed in 3% of Swedish 12-year-olds born during an epidemic. J Pediatr Gastroenterol Nutr 2009; 49: 170-176.
9. Ress K, Harro M, Maaroos H-I, Harro J, Uibo R, Uibo O: High prevalence of celiac disease: need for increasing awareness among physicians. Dig Liver Dis 2007; 39: 136-139. (Pubitemid 46117924)
10. Schumann M, Richter JF, Wedell I, Moos V, Zimmermann-Kordman M, Schneider T, Daum S, Zeitz M, Fromm M, Schulzke JD: Mechanisms of epithelial translocation of the alpha (2)-gliadin-33mer in coeliac sprue. Gut 2008; 57: 747-754. (Pubitemid 351716965)
11. Kerblom HK, Knip M: Putative environmental factors in type 1 diabetes. Diabetes Metab Rev 1998; 14: 31-67. (Pubitemid 28207035)
12. Luopajärvi K, Savilahti E, Virtanen SM, Ilonen J, Knip M, Kerblom HK, Vaarala O: Enhanced levels of cow's milk antibodies in infancy in children who develop type 1 diabetes later in childhood. Pediatr Diabetes 2008; 9: 434-441.
13. Vaarala O, Atkinson M, Neu J: The 'perfect storm' for type 1 diabetes. The complex interplay between intestinal microbiota, gut permeability, and mucosal immunity. Diabetes 2008; 10: 2555-2562.
14. Holmes GKT: Screening for coeliac disease in type 1 diabetes. Arch Dis Child 2002; 87: 495-499. (Pubitemid 35440700)
15. 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. (Pubitemid 38438431)
16. Uibo O, Heilman K, Rägo T, Shor R, Paal M, Metsküla K, Tillmann V, Uibo R: Symptomless coeliac disease in type I diabetes: 12-year experience in Estonia. Pediatr Int 2010; 52: 230-233.
17. Visser J, Rozing J, Sapone A, Lammers K, Fasano A: Tight junctions, intestinal permeability, and autoimmunity. Celiac disease and type 1 diabetes paradigms. Ann NY Acad Sci 2009; 1165: 195-205.
18. Vaarala O: Leaking gut in type 1 diabetes. Curr Opin Gastroenterol 2008; 24: 701-706.
19. Groschwitz KR, Hogan SP: Intestinal barrier function: molecular and disease pathogenesis. J Allergy Clin Immunol 2009; 124: 3-20.
20. Vilela EG, de Abreu Ferrari Mde L, De Gama Torres HO, Martins FP, Goulart EM, Lima AS, da Cunha AS: Intestinal permeability and antigliadin antibody test for monitoring adult patients with celiac disease. Dig Dis Sci 2007; 52: 1304-1309. (Pubitemid 46626182)
21. Schulzke JD, Bentzel CJ, Schulzke I, Riecken EO, Fromm M: Epithelial tight junction in the jejunum of children with acute and treated celiac sprue. Pediatr Res 1998; 43: 435-441. (Pubitemid 28157949)
22. Fasano A, Not T, Wang W, Uzzau S, Berti I, Tommasini A, Goldblum SE: Zonulin, a newly discovered modulator of intestinal permeability, and its expression in coeliac disease. Lancet 2000; 355: 1518-1519. (Pubitemid 30237361)
23. van Elburg RM, Uil JJ, Mulder CJJ, Heymans HAS: Intestinal permeability in patients with coeliac disease and relatives of patients with coeliac disease. Gut 1993; 34: 354-357. (Pubitemid 23080261)
24. Ciccocioppo R, Finamore A, Ara C, Di Sabatino A, Mengheri E, Corazza GR: Altered expression, localization, and phosphorylation of epithelial junctional proteins in celiac disease. Am J Clin Pathol 2006; 125: 502-511.
25. Zanoni G, Navone R, Lunardi C, Tridente G, Bason C, Sivori S, Beri R, Dolcino M, Valletta E, Corrocher R, Pucetti A: In celiac disease, a subset of autoantibodies against transglutaminase binds toll-like receptor 4 and induces activation of monocytes. PLoS Med 2006; 9: 1637-1652.
26. Duerksen DR, Wilhelm-Boyles C, Veitch R, Kryszak D, Parry DM: A comparison of antibody testing, permeability testing, and zonulin levels with small-bowel biopsy in celiac disease patients on a gluten-free diet. Dig Dis Sci 2010; 55: 1026-1031.
27. Watts T, Berti I, Sapone A, Gerarduzzi T, Not T, Zielke R, Fasano A: Role of the intestinal tight junction modulator zonulin in the pathogenesis of type 1 diabetes in BB diabetic-prone rats. Proc Natl Acad Sci USA 2005; 102: 2916-2921. (Pubitemid 40299891)
28. Bosi E, Molteni L, Radaelli MG, Folini L, Fermo L, Bazzigaluppi E, Piemonti L, Pastore MR, Paroni R: Increased intestinal permeability precedes clinical onset of type 1 diabetes. Diabetologia 2006; 49: 2824-2827. (Pubitemid 44730283)
29. Neu J, Reverte M, Mackey AD, Liboni K, Tuhacek-Tenace LM, Hatch M, Li N, Caicedo RA, Schatz DA, Atkinson M: Changes in intestinal morphology and permeability in the biobreeding rat before the onset of type 1 diabetes. J Pediatr Gastroenterol Nutr 2005; 40: 589-595. (Pubitemid 40617187)
30. 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: 113-123.
31. 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. (Pubitemid 351661513)
32. Barnes MJ, Powrie F: Regulatory T cells reinforce intestinal homeostasis. Immunity 2009; 31: 401-411.
33. Maynard CL, Weaver CT: Intestinal effector T cells in health and diseases. Immunity 2009; 31: 389-400.
34. Su L, Shen L, Clayburgh DR, Nalle SC, Sullivan EA, Meddings JB, Abraham C, Turner JR: Targeted epithelial tight junction dysfunction causes immune activation and contributes to development of experimental colitis. Gastroenterology 2009; 136: 551-563.
35. Boirivant M, Amendola A, Butera A, Sanchez M, Xu L, Marinaro M, Kitani A, Di Giacinto C, Strober W, Fuss IJ: A transient breach in the epithelial barrier leads to regulatory T-cell generation and resistance to experimental colitis. Gastroenterology 2008; 5: 1612-1623.
36. Iliev ID, Mileti E, Matteoli G, Chieppa M, Rescigno M: Intestinal epithelial cells promote colitis-protective regulatory T-cell differentiation through dendritic cell conditioning. Mucosal Immunol 2009; 4: 340-350.
37. Vorobjova T, Uibo O, Heilman K, Rägo T, Honkanen J, Vaarala O, Tillmann V, Ojakivi I, Uibo R: Increased FOXP3 expression in small-bowel mucosa of children with coeliac disease and type I diabetes mellitus. Scand J Gastroenterol 2009; 44: 422-430.
38. Walker-Smith J, Guandalini S, Schmitz J, Shmerling DH, Visakorpi JK: Revised criteria for diagnosis of celiac disease. Report of working group of European Society of Pediatric Gastroenterology and Nutrition. Arch Dis Child 1990; 65: 909-911.
39. 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: 330-354.
40. Green PHR, Rostami K, Marsh MN: Diagnosis of coeliac disease. Best Pract Res Clin Gastroenterol 2005; 19: 389-400. (Pubitemid 40753760)
41. Anderson JM, Van Itallie CM, Peterson MD, Stevenson BR, Carew EA, Mooseker MS: ZO-1 mRNA and protein expression during tight junction assembly in Caco-2 cells. J Cell Biol 1989; 109: 1047-1056. (Pubitemid 19220091)
42. Pizzuti D, Bortolami M, Mazzon E, Buda A, Guariso G, D'Odorico A, Chiarelli S, D'Incà RD, De lazzari F, Martines D: Transcriptional downregulation of tight junction protein ZO-1 in active coeliac disease is reversed after a gluten-free diet. Dig Liver Dis 2004; 36: 337-341. (Pubitemid 41115464)
43. Teesalu K, Agardh D, Panarina M, Utt M, Uibo O, Uibo R: A modified ELISA for improved detection of IgA, IgG, and IgM antitissue transglutaminase antibodies in celiac disease. Clin Chim Acta 2009; 403: 37-41.
44. Sapone A, de Magistris L, Pietzak M, Clemente MG, Tripathi A, Cucca F, Lampis R, Kryszak D, Carten. M, Generoso M, Iafusco D, Prisco F, Laghi F, Riegler G, Carratu R, Counts D, Fasano A: Zonulin upregulation is associated with increased gut permeability in subjects with type 1 diabetes and their relatives. Diabetes 2006; 55: 1443-1449. (Pubitemid 44195385)
45. Drago S, El Asmar R, Di Pierro M, Clemente MG, Tripathi A, Sapone A, Thakar M, Iacono G, Carroccio A, D'Agate C, Not T, Zampini L, Catassi C, Fasano A: Gliadin, zonulin and gut permeability: effects on celiac and non-celiac intestinal mucosa and intestinal cell lines. Scand J Gastroenterol 2006; 41: 408-419. (Pubitemid 43675406)
46. Ravelli A, Villanacci V, Monfredini C, Martinazzi S, Grassi V, Manenti S: How patchy is villous atrophy?: distribution pattern of histological lesions in the duodenum of children with celiac disease. Am J Gastroenterol 2010; 105: 2103-2110.
47. Bonamico M, Ballati G, Mariani P, Latini M, Triglione P, Rana I, Porro E, Mesturino MA, Criscione S: Screening for coeliac disease: the meaning of low titers of anti-gliadin antibodies (AGA) in non-coeliac children. Eur J Epidemiol 1997; 13: 55-59. (Pubitemid 27105182)
48. Savilahti ES, Saukkonen TT, Virtala ET, Tuomilehto J, ?kerblom HK: Increased levels of cow's milk and-lactoglobulin antibodies in young children with newly diagnosed IDDM. The Childhood Diabetes in Finland Study Group. Diabetes Care 1993; 16: 984-989. (Pubitemid 23184528)
49. Rodriguez-Juan C, Sala-Silveira L, Pérez-Blas M, Valeri AP, Aguilera N, López-Santalla M, Fuertes A, Martin-Villa JM: Increased levels of bovine serum albumin antibodies in patients with type 1 diabetes and celiac disease-related antibodies. J Pediatr Gastroenterol Nutr 2003; 37: 132-135. (Pubitemid 39274537)
50. Monetini L, Cavallo MG, Manfrini S, Stefanini L, Picarelli A, Di Tola M, Petrone A, Bianchi M, La Presa M, Di Giulio C, Baroni MG, Thorpe R, Walker BK, Pozzilli P; IMDIAB Group: Antibodies to bovine beta-casein in diabetes and other autoimmune diseases. Horm Metab Res 2002; 34: 455-459. (Pubitemid 35013370)
51. Kivling A, Nilsson L, Fält-Magnusson K, Söllvander S, Johanson C, Faresjö M: Diverse FOXP3 expression in children with type 1 diabetes and celiac disease. Ann NY Acad Sci 2008; 1150: 273-277.
52. 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: 2287-2295. (Pubitemid 37059499)
53. Maglio M, Florian F, Vecchiet M, Auricchio R, Paparo F, Spadaro R, Zanzi D, Rapacciuolo L, Franzese A, Sblattero D, Marzari R, Troncone R: Majority of children with type 1 diabetes produce and deposit anti-tissue transglutaminase antibodies in the small intestine. Diabetes 2009; 58: 1578-1584.
54. Salminen KK, Vuorinen T, Oikarinen S, Helminen M, Simell S, Knip M, Ilonen J, Simell O, Hyöty H: Isolation of enterovirus strains from children with preclinical type 1 diabetes. Diabet Med 2004; 21: 156-164. (Pubitemid 38221815)