CD4+ T-cell proliferation responses to wheat polypeptide stimulation in children at different stages of type 1 diabetes autoimmunity

Pediatric Diabetes

Volumn 16, Issue 3, 2015, Pages 177-188

  Hamari, Susanna ^a   Kirveskoski, Tiina ^a   Glumoff, Virpi ^a   Kulmala, Petri ^a   Simell, Olli ^b   Knip, Mikael ^c,d,e,f   Ilonen, Jorma ^g,h   Veijola, Riitta ^a  

^a OULU UNIVERSITY HOSPITAL   (Finland)

^b TURKU UNIVERSITY HOSPITAL   (Finland)

^c UNIVERSITY OF HELSINKI AND HELSINKI UNIVERSITY HOSPITAL   (Finland)

^d UNIVERSITY OF HELSINKI   (Finland)

^e FOLKHÄLSAN RESEARCH CENTER   (Finland)

^f TAMPERE UNIVERSITY HOSPITAL   (Finland)

^g UNIVERSITY OF TURKU   (Finland)

^h UNIVERSITY OF EASTERN FINLAND   (Finland)

Author keywords

Autoimmunity; Environmental trigger; Gluten; Proliferation response; T cell; Type 1 diabetes

Indexed keywords

CARBOXYFLUORESCEIN DIACETATE SUCCINIMIDYL ESTER; FOOD ANTIGEN; GLIADIN; GLUTEN; HLA DQ ANTIGEN; HLA DR ANTIGEN; PANCREAS ISLET CELL ANTIBODY; POLYPEPTIDE; TETANUS TOXOID; UNCLASSIFIED DRUG; WHEAT POLYPEPTIDE; AUTOANTIBODY; HLA ANTIGEN;

ADOLESCENT; ARTICLE; AUTOIMMUNITY; CD4+ T LYMPHOCYTE; CELLULAR IMMUNITY; CHILD; CLINICAL ARTICLE; CONTROLLED STUDY; DIABETOGENESIS; DISEASE COURSE; FEMALE; FLUORESCENCE ACTIVATED CELL SORTING; GENOTYPE; HUMAN; HUMAN CELL; IMMUNOPATHOGENESIS; IMMUNOSTIMULATION; IMPAIRED GLUCOSE TOLERANCE; IN VITRO STUDY; INSULIN DEPENDENT DIABETES MELLITUS; LYMPHOCYTE PROLIFERATION; MALE; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; WHEAT; BLOOD; CASE CONTROL STUDY; CELL PROLIFERATION; GENETICS; IMMUNOLOGY; INFANT; PHYSIOLOGY; PRESCHOOL CHILD; TIME;

ADOLESCENT; AUTOANTIBODIES; CASE-CONTROL STUDIES; CD4-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; CHILD; CHILD, PRESCHOOL; DIABETES MELLITUS, TYPE 1; FEMALE; GENOTYPE; GLIADIN; GLUTENS; HLA ANTIGENS; HUMANS; INFANT; MALE; TETANUS TOXOID; TIME FACTORS;

EID: 84926205866     PISSN: 1399543X     EISSN: 13995448     Source Type: Journal    
DOI: 10.1111/pedi.12256     Document Type: Article

References (42)

1. Knip M, Veijola R, Virtanen SM, Hyöty H, Vaarala O, Åkerblom HK. Environmental triggers and determinants of type 1 diabetes. Diabetes 2005: 54 (Suppl. 2): S125-S136.
2. Kelly MA, Rayner ML, Mijovic CH, Barnett AH. Molecular aspects of type 1 diabetes. Mol Pathol 2003: 56: 1-10.
3. Parikka V, Näntö-Salonen K, Saarinen M et al. Early seroconversion and rapidly increasing autoantibody concentrations predict prepubertal manifestation of type 1 diabetes in children at genetic risk. Diabetologia 2012: 55: 1926-1936.
4. Plenge RM. Shared genetic risk factors for type 1 diabetes and celiac disease. N Engl J Med 2008: 359: 2837-2838.
5. Ventura A, Neri E, Ughi C, Leopaldi A, Citta A, Not T. Gluten-dependent diabetes-related and thyroid-related autoantibodies in patients with celiac disease. J Pediatr 2000: 137: 263-265.
6. Visser J, Rozing J, Sapone A, Lammers K, Fasano A. Tight junctions, intestinal permeability, and autoimmunity: celiac disease and type 1 diabetes paradigms. Ann N Y Acad Sci 2009: 1165: 195-205.
7. Smyth DJ, Plagnol V, Walker NM et al. Shared and distinct genetic variants in type 1 diabetes and celiac disease. N Engl J Med 2008: 359: 2767-2777.
8. Barbeau WE. What is the key environmental trigger in type 1 diabetes - is it viruses, or wheat gluten, or both? Autoimmun Rev 2012: 12: 295-299.
9. Antvorskov JC, Josefsen K, Engkilde K, Funda DP, Buschard K. Dietary gluten and the development of type 1 diabetes. Diabetologia 2014: 57: 1770-1780.
10. Frisk G, Hansson T, Dahlbom I, Tuvemo T. A unifying hypothesis on the development of type 1 diabetes and celiac disease: Gluten consumption may be a shared causative factor. Med Hypotheses 2008: 70: 1207-1209.
11. Vaarala O, Atkinson MA, Neu J. The "perfect storm" for type 1 diabetes: the complex interplay between intestinal microbiota, gut permeability, and mucosal immunity. Diabetes 2008: 57: 2555-2562.
12. Bosi E, Molteni L, Radaelli MG et al. Increased intestinal permeability precedes clinical onset of type 1 diabetes. Diabetologia 2006: 49: 2824-2827.
13. Drago S, El Asmar R, Di Pierro M et al. Gliadin, zonulin and gut permeability: effects on celiac and non-celiac intestinal mucosa and intestinal cell lines. Scand J Gastroenterol 2006: 41: 408-419.
14. Sapone A, de Magistris L, Pietzak M et al. Zonulin upregulation is associated with increased gut permeability in subjects with type 1 diabetes and their relatives. Diabetes 2006: 55: 1443-1449.
15. 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.
16. Auricchio R, Paparo F, Maglio M et al. In vitro-deranged intestinal immune response to gliadin in type 1 diabetes. Diabetes 2004: 53: 1680-1683.
17. Galipeau HJ, Rulli NE, Jury J et al. Sensitization to gliadin induces moderate enteropathy and insulitis in nonobese diabetic-DQ8 mice. J Immunol 2011: 187: 4338-4346.
18. Norris JM, Barriga K, Klingensmith G et al. Timing of initial cereal exposure in infancy and risk of islet autoimmunity. JAMA 2003: 290: 1713-1720.
19. Ziegler AG, Schmid S, Huber D, Hummel M, Bonifacio E. Early infant feeding and risk of developing type 1 diabetes-associated autoantibodies. JAMA 2003: 290: 1721-1728.
20. Funda DP, Kaas A, Bock T, Tlaskalova-Hogenova H, Buschard K. Gluten-free diet prevents diabetes in NOD mice. Diabetes Metab Res Rev 1999: 15: 323-327.
21. Funda DP, Kaas A, Tlaskalova-Hogenova H, Buschard K. Gluten-free but also gluten-enriched (gluten+) diet prevent diabetes in NOD mice: the gluten enigma in type 1 diabetes. Diabetes Metab Res Rev 2008: 24: 59-63.
22. Schmid S, Koczwara K, Schwinghammer S, Lampasona V, Ziegler AG, Bonifacio E. Delayed exposure to wheat and barley proteins reduces diabetes incidence in non-obese diabetic mice. Clin Immunol 2004: 111: 108-118.
23. Cosnes J, Cellier C, Viola S et al. Incidence of autoimmune diseases in celiac disease: protective effect of the gluten-free diet. Clin Gastroenterol Hepatol 2008: 6: 753-758.
24. Pastore MR, Bazzigaluppi E, Belloni C, Arcovio C, Bonifacio E, Bosi E. 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 2003: 88: 162-165.
25. Fuchtenbusch M, Ziegler AG, Hummel M. Elimination of dietary gluten and development of type 1 diabetes in high risk subjects. Rev Diabet Stud 2004: 1: 39-41.
26. Hummel S, Pfluger M, Hummel M, Bonifacio E, Ziegler AG. 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 2011: 34: 1301-1305.
27. Mueller DB, Koczwara K, Mueller AS, Pallauf J, Ziegler AG, Bonifacio E. Influence of early nutritional components on the development of murine autoimmune diabetes. Ann Nutr Metab 2009: 54: 208-1721.
28. 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.
29. Mojibian M, Chakir H, Lefebvre DE et al. Diabetes-specific HLA-DR-restricted proinflammatory T-cell response to wheat polypeptides in tissue transglutaminase antibody-negative patients with type 1 diabetes. Diabetes 2009: 58: 1789-1796.
30. Mannering SI, Morris JS, Stone NL, Jensen KP, VAN Endert PM, Harrison LC. CD4+ T cell proliferation in response to GAD and proinsulin in healthy, pre-diabetic, and diabetic donors. Ann N Y Acad Sci 2004: 1037: 16-21.
31. Hermann R, Turpeinen H, Laine AP et al. HLA DR-DQ-encoded genetic determinants of childhood-onset type 1 diabetes in Finland: an analysis of 622 nuclear families. Tissue Antigens 2003: 62: 162-169.
32. Mikk M-L, Kiviniemi M, Laine A-P et al. the Finnish Paediatric Diabetes Register. The HLA-B*39 allele increases type 1 diabetes risk conferred by HLA-DRB1*04:04-DQB1*03:02 and HLA-DRB1*08.DQB1*04 class II haplotypes. Hum Immunol 2014: 75: 65-70.
33. Siljander HT, Simell S, Hekkala A et al. Predictive characteristics of diabetes-associated autoantibodies among children with HLA-conferred disease susceptibility in the general population. Diabetes 2009: 58: 2835-2842.
34. Kukreja A, Cost G, Marker J et al. Multiple immuno-regulatory defects in type-1 diabetes. J Clin Invest 2002: 109: 131-140.
35. Skarsvik S, Ludvigsson J, Vaarala O. Aberrant regulation of interleukin-12 receptor beta2 chain on type 1 cytokine-stimulated T lymphocytes in type 1 diabetes. Immunology 2005: 114: 287-293.
36. Hedman M, Faresjö M, Axelsson S, Ludvigsson J, Casas R. Impaired CD4 and CD8 T cell phenotype and reduced chemokine secretion in recent-onset type 1 diabetic children. Clin Exp Immunol 2008: 153: 360-368.
37. Lohmann T, Laue S, Nietzschmann U et al. Reduced expression of Th1-associated chemokine receptors on peripheral blood lymphocytes at diagnosis of type 1 diabetes. Diabetes 2002: 51: 2474-2480.
38. Aarnisalo J, Treszl A, Svec P et al. Reduced CD4+ T cell activation in children with type 1 diabetes carrying the PTPN22/lyp 620Trp variant. J Autoimmun 2008: 31: 13-21.
39. Eibl N, Spatz M, Fischer GF et al. Impaired primary immune response in type-1 diabetes: results from a controlled vaccination study. Clin Immunol 2002: 103 (3 Pt 1): 249-259.
40. Spatz M, Eibl N, Hink S et al. Impaired primary immune response in type-1 diabetes. Functional impairment at the level of APCs and T-cells. Cell Immunol 2003: 221: 15-26.
41. Orban T, Kis J, Szereday L et al. Reduced CD4+ T-cell-specific gene expression in human type 1 diabetes mellitus. J Autoimmun 2007: 28: 177-187.
42. Elo LL, Mykkänen J, Nikula T et al. Early suppression of immune response pathways characterizes children with prediabetes in genome-wide gene expression profiling. J Autoimmun 2010: 35: 70-76.