Dietary gluten and the development of type 1 diabetes

Diabetologia

Volumn 57, Issue 9, 2014, Pages 1770-1780

  Antvorskov, Julie C ^a   Josefsen, Knud ^a   Engkilde, Kåre ^a   Funda, David P ^a,b   Buschard, Karsten ^a  

^a Rigshospitalet   (Denmark)

^b INSTITUTE OF MICROBIOLOGY   (Czech Republic)

Author keywords

Coeliac disease; Diet; Gluten; Gluten free; Type 1 diabetes

Indexed keywords

CHEMOKINE; CYTOKINE; GLUTEN; HOMING RECEPTOR;

CELIAC DISEASE; CELL FUNCTION; DIETARY INTAKE; DISEASE COURSE; GLUTEN FREE DIET; HUMAN; IMMUNE SYSTEM; IMMUNOCOMPETENT CELL; INFLAMMATION; INSULIN DEPENDENT DIABETES MELLITUS; INTESTINE; INTESTINE FLORA; NONHUMAN; PANCREAS ISLET BETA CELL; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; SEVERE COMBINED IMMUNODEFICIENCY; SUSCEPTIBLE POPULATION; T LYMPHOCYTE; ANIMAL; IMMUNOLOGY; METABOLISM; PATHOLOGY;

ANIMALS; DIABETES MELLITUS, TYPE 1; GLUTENS; HUMANS; INTESTINES;

EID: 84905564138     PISSN: 0012186X     EISSN: 14320428     Source Type: Journal    
DOI: 10.1007/s00125-014-3265-1     Document Type: Review

References (99)

1. Eurodiab, ACE Study Group (2000) Variation and trends in incidence of childhood diabetes in Europe. Lancet 355:873-876
2. Akerblom HK, Vaarala O, Hyoty H, Ilonen J, Knip M (2002) Environmental factors in the etiology of type 1 diabetes. Am J Med Genet 115:18-29
3. Strachan DP (1989) Hay fever, hygiene, and household size. BMJ 299:1259-1260
4. Jabri B, Sollid LM (2009) Tissue-mediated control of immunopathology in coeliac disease. Nat Rev Immunol 9:858-870
5. Fasano A, Berti I, Gerarduzzi T, et al. (2003) Prevalence of celiac disease in at-risk and not-at-risk groups in the United States: a large multicenter study. Arch Intern Med 163:286-292
6. Shan L, Molberg O, Parrot I, et al. (2002) Structural basis for gluten intolerance in celiac sprue. Science 297:2275-2279
7. Nikulina M, Habich C, Flohe SB, Scott FW, Kolb H (2004) Wheat gluten causes dendritic cell maturation and chemokine secretion. J Immunol 173:1925-1933
8. Palova-Jelinkova L, Rozkova D, Pecharova B, et al. (2005) Gliadin fragments induce phenotypic and functional maturation of human dendritic cells. J Immunol 175:7038-7045
9. Sollid LM (2000) Molecular basis of celiac disease. Annu Rev Immunol 18:53-81
10. Maiuri L, Ciacci C, Ricciardelli I, et al. (2003) Association between innate response to gliadin and activation of pathogenic T cells in coeliac disease. Lancet 362:30-37
11. Smyth DJ, Plagnol V, Walker NM, et al. (2008) Shared and distinct genetic variants in type 1 diabetes and celiac disease. N Engl J Med 359:2767-2777
12. Collin P, Kaukinen K, Valimaki M, Salmi J (2002) Endocrinological disorders and celiac disease. Endocr Rev 23:464-483
13. Hansen D, Brock-Jacobsen B, Lund E, et al. (2006) Clinical benefit of a gluten-free diet in type 1 diabetic children with screening-detected celiac disease: a population-based screening study with 2 years' follow-up. Diabetes Care 29:2452-2456
14. Cosnes J, Cellier C, Viola S, et al. (2008) Incidence of autoimmune diseases in celiac disease: protective effect of the gluten-free diet. Clin Gastroenterol Hepatol 6:753-758
15. Shewry PR, Halford NG, Belton PS, Tatham AS (2002) The structure and properties of gluten: an elastic protein from wheat grain. Philos Trans R Soc Lond B Biol Sci 357:133-142
16. Shewry PR, Halford NG (2002) Cereal seed storage proteins: structures, properties and role in grain utilization. J Exp Bot 53:947-958
17. Piper JL, Gray GM, Khosla C (2004) Effect of prolyl endopeptidase on digestive-resistant gliadin peptides in vivo. J Pharmacol Exp Ther 311:213-219
18. Helmerhorst EJ, Zamakhchari M, Schuppan D, Oppenheim FG (2010) Discovery of a novel and rich source of gluten-degrading microbial enzymes in the oral cavity. PLoS One 5:e13264
19. Bernardo D, Garrote JA, Nadal I, et al. (2009) Is it true that coeliacs do not digest gliadin? Degradation pattern of gliadin in coeliac disease small intestinal mucosa. Gut 58:886-887
20. Nadal I, Donat E, Ribes-Koninckx C, Calabuig M, Sanz Y (2007) Imbalance in the composition of the duodenal microbiota of children with coeliac disease. J Med Microbiol 56:1669-1674
21. Tlaskalova-Hogenova H, Stepankova R, Farre M, et al. (1997) Autoimmune reactions induced by gliadin feeding in germ-free AVN rats and athymic nude mice. Animal models for celiac disease. Ann N Y Acad Sci 815:503-505
22. Stepankova R, Tlaskalova-Hogenova H, Sinkora J, Jodl J, Fric P (1996) Changes in jejunal mucosa after long-term feeding of germfree rats with gluten. Scand J Gastroenterol 31:551-557
23. Pozzilli P, Signore A, Williams AJ, Beales PE (1993) NOD mouse colonies around the world - recent facts and figures. Immunol Today 14:193-196
24. Buschard K, Pedersen C, Hansen SV, Hageman I, Aaen K, Bendtzen K (1992) Anti-diabetogenic effect of fusidic acid in diabetes prone BB rats. Autoimmunity 14:101-104
25. Hansen CH, Krych L, Nielsen DS, et al. (2012) Early life treatment with vancomycin propagates Akkermansia muciniphila and reduces diabetes incidence in the NOD mouse. Diabetologia 55:2285-2294
26. Matsuzaki T, Nagata Y, Kado S, et al. (1997) Prevention of onset in an insulin-dependent diabetes mellitus model, NOD mice, by oral feeding of Lactobacillus casei. APMIS 105:643-649
27. Wen L, Ley RE, Volchkov PY, et al. (2008) Innate immunity and intestinal microbiota in the development of type 1 diabetes. Nature 455:1109-1113
28. Hansen AK, Ling F, Kaas A, Funda DP, Farlov H, Buschard K (2006) Diabetes preventive gluten-free diet decreases the number of caecal bacteria in non-obese diabetic mice. Diabetes Metab Res Rev 22:220-225
29. Marietta EV, Gomez AM, Yeoman C, et al. (2013) Low incidence of spontaneous type 1 diabetes in non-obese diabetic mice raised on gluten-free diets is associated with changes in the intestinal microbiome. PLoS One 8:e78687
30. Patrick C, Wang GS, Lefebvre DE, et al. (2013) Promotion of autoimmune diabetes by cereal diet in the presence or absence of microbes associated with gut immune activation, regulatory imbalance, and altered cathelicidin antimicrobial peptide. Diabetes 62:2036-2047
31. Funda DP, Kaas A, Bock T, Tlaskalova-Hogenova H, Buschard K (1999) Gluten-free diet prevents diabetes in NOD mice. Diabetes Metab Res Rev 15:323-327
32. Funda DP, Kaas A, Tlaskalova-Hogenova H, Buschard K (2008) Gluten-free but also gluten-enriched (gluten+) diet prevent diabetes in NOD mice; the gluten enigma in type 1 diabetes. Diabetes Metab Res Rev 24:59-63
33. Hoorfar J, Scott FW, Cloutier HE (1991) Dietary plant materials and development of diabetes in the BB rat. J Nutr 121:908-916
34. Coleman DL, Kuzava JE, Leiter EH (1990) Effect of diet on incidence of diabetes in nonobese diabetic mice. Diabetes 39:432-436
35. Scott FW (1996) Food-induced type 1 diabetes in the BB rat. Diabetes Metab Rev 12:341-359
36. Pastore MR, Bazzigaluppi E, Belloni C, Arcovio C, Bonifacio E, Bosi E (2003) Six months of gluten-free diet do not influence autoantibody titers, but improve insulin secretion in subjects at high risk for type 1 diabetes. J Clin Endocrinol Metab 88:162-165
37. Fuchtenbusch M, Ziegler AG, Hummel M (2004) Elimination of dietary gluten and development of type 1 diabetes in high risk subjects. Rev Diabet Stud 1:39-41
38. Sildorf SM, Fredheim S, Svensson J, Buschard K (2012) Remission without insulin therapy on gluten-free diet in a 6-year old boy with type 1 diabetes mellitus. BMJ Case Rep. doi: 10.1136/bcr.02.2012.5878
39. Saadah OI, Zacharin M, O'Callaghan A, Oliver MR, Catto-Smith AG (2004) Effect of gluten-free diet and adherence on growth and diabetic control in diabetics with coeliac disease. Arch Dis Child 89:871-876
40. Rami B, Sumnik Z, Schober E, et al. (2005) Screening detected celiac disease in children with type 1 diabetes mellitus: effect on the clinical course (a case control study). J Pediatr Gastroenterol Nutr 41:317-321
41. Westman E, Ambler GR, Royle M, Peat J, Chan A (1999) Children with coeliac disease and insulin dependent diabetes mellitus - growth, diabetes control and dietary intake. J Pediatr Endocrinol Metab 12:433-442
42. Troncone R, Franzese A, Mazzarella G, et al. (2003) Gluten sensitivity in a subset of children with insulin dependent diabetes mellitus. Am J Gastroenterol 98:590-595
43. Mojibian M, Chakir H, Lefebvre DE, et al. (2009) Diabetes-specific HLA-DR-restricted proinflammatory T cell response to wheat polypeptides in tissue transglutaminase antibody-negative patients with type 1 diabetes. Diabetes 58:1789-1796
44. Klemetti P, Savilahti E, Ilonen J, Akerblom HK, Vaarala O (1998) T cell reactivity to wheat gluten in patients with insulin-dependent diabetes mellitus. Scand J Immunol 47:48-53
45. MacFarlane AJ, Burghardt KM, Kelly J, et al. (2003) 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 278:54-63
46. Simpson M, Mojibian M, Barriga K, et al. (2009) An exploration of Glo-3A antibody levels in children at increased risk for type 1 diabetes mellitus. Pediatr Diabetes 10:563-572
47. Mueller DB, Koczwara K, Mueller AS, Pallauf J, Ziegler AG, Bonifacio E (2009) Influence of early nutritional components on the development of murine autoimmune diabetes. Ann Nutr Metab 54:208-217
48. Ziegler AG, Schmid S, Huber D, Hummel M, Bonifacio E (2003) Early infant feeding and risk of developing type 1 diabetes-associated autoantibodies. JAMA 290:1721-1728
49. Norris JM, Barriga K, Klingensmith G, et al. (2003) Timing of initial cereal exposure in infancy and risk of islet autoimmunity. JAMA 290:1713-1720
50. Atkinson M, Gale EA (2003) Infant diets and type 1 diabetes: too early, too late, or just too complicated? JAMA 290:1771-1772
51. Strobel S, Mowat AM (1998) Immune responses to dietary antigens: oral tolerance. Immunol Today 19:173-181
52. Hummel S, Pfluger M, Hummel M, Bonifacio E, Ziegler AG (2011) Primary dietary intervention study to reduce the risk of islet autoimmunity in children at increased risk for type 1 diabetes: the BABYDIET study. Diabetes Care 34:1301-1305
53. Ludvigsson J (2003) Cow-milk-free diet during last trimester of pregnancy does not influence diabetes-related autoantibodies in nondiabetic children. Ann N Y Acad Sci 1005:275-278
54. Virtanen SM, Takkinen HM, Nevalainen J, et al. (2011) Early introduction of root vegetables in infancy associated with advanced β-cell autoimmunity in young children with human leukocyte antigen-conferred susceptibility to type 1 diabetes. Diabet Med 28:965-971
55. Scott FW, Rowsell P, Wang GS, Burghardt K, Kolb H, Flohe S (2002) Oral exposure to diabetes-promoting food or immunomodulators in neonates alters gut cytokines and diabetes. Diabetes 51:73-78
56. Schmid S, Koczwara K, Schwinghammer S, Lampasona V, Ziegler AG, Bonifacio E (2004) Delayed exposure to wheat and barley proteins reduces diabetes incidence in non-obese diabetic mice. Clin Immunol 111:108-118
57. Ivarsson A, Persson LA, Nystrom L, et al. (2000) Epidemic of coeliac disease in Swedish children. Acta Paediatr 89:165-171
58. Ivarsson A, Hernell O, Stenlund H, Persson LA (2002) Breast-feeding protects against celiac disease. Am J Clin Nutr 75:914-921
59. Kimpimaki T, Erkkola M, Korhonen S, et al. (2001) Short-term exclusive breastfeeding predisposes young children with increased genetic risk of type I diabetes to progressive beta-cell autoimmunity. Diabetologia 44:63-69
60. Savilahti E, Ormala T, Saukkonen T, et al. (1999) Jejuna of patients with insulin-dependent diabetes mellitus (IDDM) show signs of immune activation. Clin Exp Immunol 116:70-77
61. Westerholm-Ormio M, Vaarala O, Pihkala P, Ilonen J, Savilahti E (2003) Immunologic activity in the small intestinal mucosa of pediatric patients with type 1 diabetes. Diabetes 52:2287-2295
62. Hanninen A, Salmi M, Simell O, Jalkanen S (1996) Mucosa-associated (beta 7-integrin high) lymphocytes accumulate early in the pancreas of NOD mice and show aberrant recirculation behavior. Diabetes 45:1173-1180
63. Yang XD, Sytwu HK, McDevitt HO, Michie SA (1997) Involvement of beta 7 integrin and mucosal addressin cell adhesion molecule-1 (MAdCAM-1) in the development of diabetes in obese diabetic mice. Diabetes 46:1542-1547
64. Hanninen A, Jaakkola I, Jalkanen S (1998) Mucosal addressin is required for the development of diabetes in nonobese diabetic mice. J Immunol 160:6018-6025
65. Jaakkola I, Jalkanen S, Hanninen A (2003) Diabetogenic T cells are primed both in pancreatic and gut-associated lymph nodes in NOD mice. Eur J Immunol 33:3255-3264
66. Hanninen A, Salmi M, Simell O, Jalkanen S (1993) Endothelial cell-binding properties of lymphocytes infiltrated into human diabetic pancreas. Implications for pathogenesis of IDDM. Diabetes 42:1656-1662
67. Paronen J, Klemetti P, Kantele JM, et al. (1997) Glutamate decarboxylase-reactive peripheral blood lymphocytes from patients with IDDM express gut-specific homing receptor α4β7-integrin. Diabetes 46:583-588
68. Neu J, Reverte CM, Mackey AD, et al. (2005) Changes in intestinal morphology and permeability in the biobreeding rat before the onset of type 1 diabetes. J Pediatr Gastroenterol Nutr 40:589-595
69. Graham S, Courtois P, Malaisse WJ, Rozing J, Scott FW, Mowat AM (2004) Enteropathy precedes type 1 diabetes in the BB rat. Gut 53:1437-1444
70. Bosi E, Molteni L, Radaelli MG, et al. (2006) Increased intestinal permeability precedes clinical onset of type 1 diabetes. Diabetologia 49:2824-2827
71. Secondulfo M, Iafusco D, Carratu R, et al. (2004) Ultrastructural mucosal alterations and increased intestinal permeability in non-celiac, type I diabetic patients. Dig Liver Dis 36:35-45
72. Kuitunen M, Saukkonen T, Ilonen J, Akerblom HK, Savilahti E (2002) Intestinal permeability to mannitol and lactulose in children with type 1 diabetes with the HLA-DQB102 allele. Autoimmunity 35:365-368
73. Fasano A, Not T, Wang W, et al. (2000) Zonulin, a newly discovered modulator of intestinal permeability, and its expression in coeliac disease. Lancet 355:1518-1519
74. Watts T, Berti I, Sapone A, et al. (2005) Role of the intestinal tight junction modulator zonulin in the pathogenesis of type I diabetes in BB diabetic-prone rats. Proc Natl Acad Sci U S A 102:2916-2921
75. Sapone A, de Magistris L, Pietzak M, et al. (2006) Zonulin upregulation is associated with increased gut permeability in subjects with type 1 diabetes and their relatives. Diabetes 55:1443-1449
76. Visser JT, Lammers K, Hoogendijk A, et al. (2010) Restoration of impaired intestinal barrier function by the hydrolysed casein diet contributes to the prevention of type 1 diabetes in the diabetes-prone BioBreeding rat. Diabetologia 53:2621-2628
77. Lammers KM, Lu R, Brownley J, et al. (2008) Gliadin induces an increase in intestinal permeability and zonulin release by binding to the chemokine receptor CXCR3. Gastroenterology 135:194-204
78. Flohe SB, Wasmuth HE, Kerad JB, et al. (2003) A wheat-based, diabetes-promoting diet induces a Th1-type cytokine bias in the gut of NOD mice. Cytokine 21:149-154
79. Chakir H, Lefebvre DE, Wang H, Caraher E, Scott FW (2005) Wheat protein-induced proinflammatory T helper 1 bias in mesenteric lymph nodes of young diabetes-prone rats. Diabetologia 48:1576-1584
80. Nilsen EM, Jahnsen FL, Lundin KE, et al. (1998) Gluten induces an intestinal cytokine response strongly dominated by interferon gamma in patients with celiac disease. Gastroenterology 115:551-563
81. Antvorskov JC, Fundova P, Buschard K, Funda DP (2012) Impact of dietary gluten on regulatory T cells and Th17 cells in BALB/c mice. PLoS One 7:e33315
82. Antvorskov JC, Fundova P, Buschard K, Funda DP (2013) Dietary gluten alters the balance of pro-inflammatory and anti-inflammatory cytokines in T cells of BALB/c mice. Immunology 138:23-33
83. Scott FW, Cloutier HE, Kleemann R, et al. (1997) Potential mechanisms by which certain foods promote or inhibit the development of spontaneous diabetes in BB rats: dose, timing, early effect on islet area, and switch in infiltrate from Th1 to Th2 cells. Diabetes 46:589-598
84. Ciccocioppo R, Rossi M, Pesce I, et al. (2008) Effects of gliadin stimulation on bone marrow-derived dendritic cells from HLA-DQ8 transgenic MICE. Dig Liver Dis 40:927-935
85. Thomas KE, Sapone A, Fasano A, Vogel SN (2006) Gliadin stimulation of murine macrophage inflammatory gene expression and intestinal permeability are MyD88-dependent: role of the innate immune response in celiac disease. J Immunol 176:2512-2521
86. Tuckova L, Flegelova Z, Tlaskalova-Hogenova H, Zidek Z (2000) Activation of macrophages by food antigens: enhancing effect of gluten on nitric oxide and cytokine production. J Leukoc Biol 67:312-318
87. Gianfrani C, Auricchio S, Troncone R (2005) Adaptive and innate immune responses in celiac disease. Immunol Lett 99:141-145
88. Di SA, Pickard KM, Gordon JN, et al. (2007) Evidence for the role of interferon-alfa production by dendritic cells in the Th1 response in celiac disease. Gastroenterology 133:1175-1187
89. Hue S, Mention JJ, Monteiro RC, et al. (2004) A direct role for NKG2D/MICA interaction in villous atrophy during celiac disease. Immunity 21:367-377
90. Terrazzano G, Sica M, Gianfrani C, et al. (2007) Gliadin regulates the NK-dendritic cell cross-talk by HLA-E surface stabilization. J Immunol 179:372-381
91. Meresse B, Chen Z, Ciszewski C, et al. (2004) Coordinated induction by IL15 of a TCR-independent NKG2D signaling pathway converts CTL into lymphokine-activated killer cells in celiac disease. Immunity 21:357-366
92. Junker Y, Zeissig S, Kim SJ, et al. (2012) Wheat amylase trypsin inhibitors drive intestinal inflammation via activation of toll-like receptor 4. J Exp Med 209:2395-2408
93. Dall M, Calloe K, Haupt-Jorgensen M, et al. (2013) Gliadin fragments and a specific gliadin 33-mer peptide close KATP channels and induce insulin secretion in INS-1E cells and rat islets of Langerhans. PLoS One 8:e66474
94. Gotfredsen CF, Buschard K, Frandsen EK (1985) Reduction of diabetes incidence of BB Wistar rats by early prophylactic insulin treatment of diabetes-prone animals. Diabetologia 28:933-935
95. Hardin JA, Donegan L, Woodman RC, Trevenen C, Gall DG (2002) Mucosal inflammation in a genetic model of spontaneous type I diabetes mellitus. Can J Physiol Pharmacol 80:1064-1070
96. Meddings JB, Jarand J, Urbanski SJ, Hardin J, Gall DG (1999) Increased gastrointestinal permeability is an early lesion in the spontaneously diabetic BB rat. Am J Physiol 276:G951-G957
97. Tuckova L, Novotna J, Novak P, et al. (2002) Activation of macrophages by gliadin fragments: isolation and characterization of active peptide. J Leukoc Biol 71:625-631
98. Alam C, Valkonen S, Palagani V, Jalava J, Eerola E, Hanninen A (2010) Inflammatory tendencies and overproduction of IL-17 in the colon of young NOD mice are counteracted with diet change. Diabetes 59:2237-2246
99. Bernardo D, Garrote JA, Fernandez-Salazar L, Riestra S, Arranz E (2007) Is gliadin really safe for non-coeliac individuals? Production of interleukin 15 in biopsy culture from non-coeliac individuals challenged with gliadin peptides. Gut 56:889-890