Fermentable fibres condition colon microbiota and promote diabetogenesis in NOD mice

Diabetologia

Volumn 57, Issue 10, 2014, Pages 2183-2192

  Toivonen, Raine K ^a   Emani, Rohini ^a   Munukka, Eveliina ^a   Rintala, Anniina ^a   Laiho, Asta ^b   Pietilä, Sami ^b   Pursiheimo, Juha Pekka ^b   Soidinsalo, Pasi ^b   Linhala, Mari ^a   Eerola, Erkki ^a   Huovinen, Pentti ^a   Hänninen, Arno ^a  

^a UNIVERSITY OF TURKU   (Finland)

^b TURKU CENTRE FOR BIOTECHNOLOGY   (Finland)

Author keywords

Dietary intervention; Gut immune system; Microbiota; Type 1 diabetes

Indexed keywords

INTERLEUKIN 18; INTERLEUKIN 22; INTERLEUKIN 4; MUCIN; RNA 16S; SHORT CHAIN FATTY ACID; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA; FOXA3 PROTEIN, MOUSE; HEPATOCYTE NUCLEAR FACTOR 3GAMMA; INTERLEUKIN DERIVATIVE; INTERLEUKIN-22; PECTIN; XYLAN;

ACTINOBACTERIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIUM; BACTEROIDETES; CLOSTRIDIACEAE; CLOSTRIDIALES; COLON; COLON FLORA; DIABETES MELLITUS; DIABETOGENESIS; DIET SUPPLEMENTATION; DIETARY FIBER; ENTEROCOCCACEAE; ERYSIPELOTRICHACEAE; FATTY ACID METABOLISM; FEMALE; FERMENTABLE FIBER; FIRMICUTES; GENE EXPRESSION; INSULITIS; LACHNOSPIRACEAE; LACTOBACILLACEAE; MOLLICUTES; MOUSE; NEXT GENERATION SEQUENCING; NONHUMAN; NONOBESE DIABETIC MOUSE; PANCREATIC LYMPH NODE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RNA SEQUENCE; RUMINOCOCCACEAE; ANIMAL; CHEMICALLY INDUCED; DRUG EFFECTS; GASTROINTESTINAL TRACT; INSULIN DEPENDENT DIABETES MELLITUS; LYMPH NODE; METABOLISM; MICROBIOLOGY; MICROFLORA;

ANIMALS; COLON; DIABETES MELLITUS, TYPE 1; FEMALE; GASTROINTESTINAL TRACT; HEPATOCYTE NUCLEAR FACTOR 3-GAMMA; INTERLEUKIN-18; INTERLEUKIN-4; INTERLEUKINS; LYMPH NODES; MICE; MICE, INBRED NOD; MICROBIOTA; PECTINS; TRANSFORMING GROWTH FACTOR BETA; XYLANS;

EID: 84937210412     PISSN: 0012186X     EISSN: 14320428     Source Type: Journal    
DOI: 10.1007/s00125-014-3325-6     Document Type: Article

References (37)

1. Gallegos AM, Bevan MJ (2004) Driven to autoimmunity: the nod mouse. Cell 117:149–151
2. Anderson MS, Bluestone JA (2005) The NOD mouse: a model of immune dysregulation. Annu Rev Immunol 23:447–485
3. 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
4. Auricchio R, Paparo F, Maglio M et al (2004) In vitro-deranged intestinal immune response to gliadin in type 1 diabetes. Diabetes 53:1680–1683
5. Tiittanen M, Westerholm-Ormio M, Verkasalo M, Savilahti E, Vaarala O (2008) Infiltration of forkhead box P3-expressing cells in small intestinal mucosa in coeliac disease but not in type 1 diabetes. Clin Exp Immunol 152:498–507
6. Hanninen A, Salmi M, Simell O, Jalkanen S (1996) Mucosa-associated (beta 7-integrinhigh) lymphocytes accumulate early in the pancreas of NOD mice and show aberrant recirculation behavior. Diabetes 45:1173–1180
7. 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
8. Bosi E, Molteni L, Radaelli MG et al (2006) Increased intestinal permeability precedes clinical onset of type 1 diabetes. Diabetologia 49:2824–2827
9. Maurano F, Mazzarella G, Luongo D et al (2005) Small intestinal enteropathy in non-obese diabetic mice fed a diet containing wheat. Diabetologia 48:931–937
10. Atkinson MA, Winter WE, Skordis N, Beppu H, Riley WM, Maclaren NK (1988) Dietary protein restriction reduces the frequency and delays the onset of insulin dependent diabetes in BB rats. Autoimmunity 2:11–19
11. Beales PE, Elliott RB, Flohe S et al (2002) A multi-centre, blinded international trial of the effect of A(1) and A(2) beta-casein variants on diabetes incidence in two rodent models of spontaneous type I diabetes. Diabetologia 45:1240–1246
12. Emani R, Asghar MN, Toivonen R et al (2013) Casein hydrolysate diet controls intestinal T cell activation, free radical production and microbial colonisation in NOD mice. Diabetologia 56:1781–1791
13. Brugman S, Klatter FA, Visser JT et al (2006) Antibiotic treatment partially protects against type 1 diabetes in the Bio-Breeding diabetes-prone rat. Is the gut flora involved in the development of type 1 diabetes? Diabetologia 49:2105–2108
14. Turley SJ, Lee JW, Dutton-Swain N, Mathis D, Benoist C (2005) Endocrine self and gut non-self intersect in the pancreatic lymph nodes. Proc Natl Acad Sci U S A 102:17729–17733
15. Lee AS, Gibson DL, Zhang Y, Sham HP, Vallance BA, Dutz JP (2010) Gut barrier disruption by an enteric bacterial pathogen accelerates insulitis in NOD mice. Diabetologia 53:741–748
16. 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
17. Vanhoutvin SA, Troost FJ, Kilkens TO et al (2009) The effects of butyrate enemas on visceral perception in healthy volunteers. Neurogastroenterol Motil 21:952–e76
18. Hamer HM, de Preter V, Windey K, Verbeke K (2012) Functional analysis of colonic bacterial metabolism: relevant to health? Am J Physiol Gastrointest Liver Physiol 302:G1–G9
19. Borthakur A, Bhattacharyya S, Dudeja PK, Tobacman JK (2007) Carrageenan induces interleukin-8 production through distinct Bcl10 pathway in normal human colonic epithelial cells. Am J Physiol Gastrointest Liver Physiol 292:G829–G838
20. Bhattacharyya S, Borthakur A, Dudeja PK, Tobacman JK (2008) Carrageenan induces cell cycle arrest in human intestinal epithelial cells in vitro. J Nutr 138:469–475
21. Caporaso JG, Kuczynski J, Stombaugh J et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336
22. Bokulich NA, Subramanian S, Faith JJ et al (2013) Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nat Methods 10:57–59
23. Russell JB, Rychlik JL (2001) Factors that alter rumen microbial ecology. Science 292:1119–1122
24. de Goffau MC, Luopajarvi K, Knip M et al (2013) Fecal microbiota composition differs between children with beta-cell autoimmunity and those without. Diabetes 62:1238–1244
25. 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
26. Knip M, Virtanen SM, Seppa K et al (2010) Dietary intervention in infancy and later signs of beta-cell autoimmunity. N Engl J Med 363:1900–1908
27. Elliott RB, Reddy SN, Bibby NJ, Kida K (1988) Dietary prevention of diabetes in the non-obese diabetic mouse. Diabetologia 31:62–64
28. Brown CT, Davis-Richardson AG, Giongo A et al (2011) Gut microbiome metagenomics analysis suggests a functional model for the development of autoimmunity for type 1 diabetes. PLoS One 6:e25792
29. Flint HJ, Bayer EA, Rincon MT, Lamed R, White BA (2008) Polysaccharide utilization by gut bacteria: potential for new insights from genomic analysis. Nat Rev Microbiol 6:121–131
30. Chassard C, Delmas E, Lawson PA, Bernalier-Donadille A (2008) Bacteroides xylanisolvens sp. nov., a xylan-degrading bacterium isolated from human faeces. Int J Syst Evol Microbiol 58:1008–1013
31. Salyers AA, West SE, Vercellotti JR, Wilkins TD (1977) Fermentation of mucins and plant polysaccharides by anaerobic bacteria from the human colon. Appl Environ Microbiol 34:529–533
32. Roesch LF, Lorca GL, Casella G et al (2009) Culture-independent identification of gut bacteria correlated with the onset of diabetes in a rat model. ISME J 3:536–548
33. Giongo A, Gano KA, Crabb DB et al (2011) Toward defining the autoimmune microbiome for type 1 diabetes. ISME J 5:82–91
34. Alenghat T, Osborne LC, Saenz SA et al (2013) Histone deacetylase 3 coordinates commensal-bacteria-dependent intestinal homeostasis. Nature 504:153–157
35. Smith PM, Howitt MR, Panikov N et al (2013) The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science 341:569–573
36. Atarashi K, Tanoue T, Shima T et al (2011) Induction of colonic regulatory T cells by indigenous Clostridium species. Science 331:337–341
37. Ouwerkerk JP, de Vos WM, Belzer C (2013) Glycobiome: bacteria and mucus at the epithelial interface. Best Pract Res Clin Gastroenterol 27:25–38