Akkermansia muciniphila induces gut microbiota remodelling and controls islet autoimmunity in NOD mice

Gut

Volumn 67, Issue 8, 2018, Pages 1445-1453

  Hänninen, Arno ^a,b   Toivonen, Raine ^a   Pöysti, Sakari ^a   Belzer, Clara ^c   Plovier, Hubert ^d   Ouwerkerk, Janneke P ^c   Emani, Rohini ^a   Cani, Patrice D ^d   De Vos, Willem M ^c,e  

^a UNIVERSITY OF TURKU   (Finland)

^b TURKU UNIVERSITY HOSPITAL   (Finland)

^c WAGENINGEN UNIVERSITY   (Netherlands)

^d UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^e UNIVERSITY OF HELSINKI   (Finland)

Author keywords

autoimmunity; bacterial interactions; diabetes mellitus; gut immunology; probiotics

Indexed keywords

ANTIMICROBIAL PEPTIDE REG3GAMMA; AUTOANTIBODY; BACTERIAL DNA; ENDOTOXIN; POLYPEPTIDE ANTIBIOTIC AGENT; RNA 16S; UNCLASSIFIED DRUG; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, MOUSE; INTERLEUKIN 10; TOLL LIKE RECEPTOR;

AKKERMANSIA MUCINIPHILA; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOIMMUNITY; BACTERIAL COUNT; BACTERIUM; BACTERIUM COLONY; BACTERIUM DETECTION; BIFIDOBACTERIACEAE; CORIOBACTERIACEAE; ENDOPLASMIC RETICULUM STRESS; EPITHELIUM CELL; FEMALE; GENE AMPLIFICATION; GENE SEQUENCE; IMMUNE RESPONSE; IMMUNOLOGICAL TOLERANCE; IMMUNOREGULATION; INCIDENCE; INSULIN DEPENDENT DIABETES MELLITUS; INTESTINE FLORA; MOUSE; NONHUMAN; NONOBESE DIABETIC MOUSE; POPULATION ABUNDANCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA SEQUENCE; SPECIES DIVERSITY; SPECIES RICHNESS; SYMBIONT; ANIMAL; DISEASE MODEL; METABOLISM; MICROBIOLOGY; PANCREAS ISLET; PATHOLOGY; PHYSIOLOGY; REGULATORY T LYMPHOCYTE; VERRUCOMICROBIA;

ANIMALS; DIABETES MELLITUS, TYPE 1; DISEASE MODELS, ANIMAL; FORKHEAD TRANSCRIPTION FACTORS; GASTROINTESTINAL MICROBIOME; INTERLEUKIN-10; ISLETS OF LANGERHANS; MICE; MICE, INBRED NOD; T-LYMPHOCYTES, REGULATORY; TOLL-LIKE RECEPTORS; VERRUCOMICROBIA;

EID: 85049963474     PISSN: 00175749     EISSN: 14683288     Source Type: Journal    
DOI: 10.1136/gutjnl-2017-314508     Document Type: Article

References (53)

1. Yurkovetskiy LA, Pickard JM, Chervonsky AV. Microbiota and autoimmunity: Exploring new avenues. Cell Host Microbe 2015;17:548-52.
2. Davis-Richardson AG, Ardissone AN, Dias R, et al. Bacteroides dorei dominates gut microbiome prior to autoimmunity in Finnish children at high risk for type 1 diabetes. Front Microbiol 2014;5:678.
3. Kostic AD, Gevers D, Siljander H, et al. The dynamics of the human infant gut microbiome in development and in progression toward type 1 diabetes. Cell Host Microbe 2015;17:260-73.
4. Davis-Richardson AG, Triplett EW. A model for the role of gut bacteria in the development of autoimmunity for type 1 diabetes. Diabetologia 2015;58:1386-93.
5. Hänninen AL, Toivonen RK. On the role of gut bacteria and infant diet in the development of autoimmunity for type 1 diabetes. Diabetologia 2015;58:2195-6.
6. Chervonsky AV. Microbiota and autoimmunity. Cold Spring Harb Perspect Biol 2013;5:a007294.
7. Vatanen T, Kostic AD, d'Hennezel E, et al. Variation in microbiome LPS immunogenicity contributes to autoimmunity in humans. Cell 2016;165:842-53.
8. Gülden E, Ihira M, Ohashi A, et al. Toll-like receptor 4 deficiency accelerates the development of insulin-deficient diabetes in non-obese diabetic mice. PLoS One 2013;8:e75385.
9. Brown K, Godovannyi A, Ma C, et al. Prolonged antibiotic treatment induces a diabetogenic intestinal microbiome that accelerates diabetes in NOD mice. Isme J 2016;10:321-32.
10. Chow J, Mazmanian SK. Getting the bugs out of the immune system: Do bacterial microbiota "fix" intestinal T cell responses? Cell Host Microbe 2009;5:8-12.
11. Cox LM, Yamanishi S, Sohn J, et al. Altering the intestinal microbiota during a critical developmental window has lasting metabolic consequences. Cell 2014;158:705-21.
12. Hooper LV, Littman DR, Macpherson AJ. Interactions between the microbiota and the immune system. Science 2012;336:1268-73.
13. Atarashi K, Tanoue T, Oshima K, et al. Treg induction by a rationally selected mixture of Clostridia strains from the human microbiota. Nature 2013;500:232-6.
14. Atarashi K, Tanoue T, Shima T, et al. Induction of colonic regulatory T cells by indigenous Clostridium species. Science 2011;331:337-41.
15. Atarashi K, Tanoue T, Ando M, et al. Th17 cell induction by adhesion of microbes to intestinal epithelial cells. Cell 2015;163:367-80.
16. Ivanov II, Frutos RL, Manel N, et al. Specific microbiota direct the differentiation of IL-17-producing T-helper cells in the mucosa of the small intestine. Cell Host Microbe 2008;4:337-49.
17. Mazmanian SK, Round JL, Kasper DL. A microbial symbiosis factor prevents intestinal inflammatory disease. Nature 2008;453:620-5.
18. Round JL, Mazmanian SK. Inducible Foxp3+ regulatory T-cell development by a commensal bacterium of the intestinal microbiota. Proc Natl Acad Sci U S A 2010;107:12204-9.
19. Derrien M, Vaughan EE, Plugge CM, et al. Akkermansia muciniphila gen. nov., sp. nov., a human intestinal mucin-degrading bacterium. Int J Syst Evol Microbiol 2004;54(Pt 5):1469-76.
20. Shin NR, Lee JC, Lee HY, et al. An increase in the Akkermansia spp. population induced by metformin treatment improves glucose homeostasis in diet-induced obese mice. Gut 2014;63:727-35.
21. Brown CT, Davis-Richardson AG, Giongo A, et al. Gut microbiome metagenomics analysis suggests a functional model for the development of autoimmunity for type 1 diabetes. PLoS One 2011;6:e25792.
22. de Goffau MC, Fuentes S, van den Bogert B, et al. Aberrant gut microbiota composition at the onset of type 1 diabetes in young children. Diabetologia 2014;57:1569-77.
23. Endesfelder D, Engel M, Davis-Richardson AG, et al. Towards a functional hypothesis relating anti-islet cell autoimmunity to the dietary impact on microbial communities and butyrate production. Microbiome 2016;4:17.
24. Derrien M, Van Baarlen P, Hooiveld G, et al. Modulation of mucosal immune response, tolerance, and proliferation in mice colonized by the mucin-degrader akkermansia muciniphila. Front Microbiol 2011;2:166.
25. Everard A, Belzer C, Geurts L, et al. Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proc Natl Acad Sci U S A 2013;110:9066-71.
26. Plovier H, Everard A, Druart C, et al. A purified membrane protein from Akkermansia muciniphila or the pasteurized bacterium improves metabolism in obese and diabetic mice. Nat Med 2017;23:107-13.
27. Vaishnava S, Yamamoto M, Severson KM, et al. The antibacterial lectin RegIIIgamma promotes the spatial segregation of microbiota and host in the intestine. Science 2011;334:255-8.
28. Niederreiter L, Fritz TM, Adolph TE, et al. ER stress transcription factor Xbp1 suppresses intestinal tumorigenesis and directs intestinal stem cells. J Exp Med 2013;210:2041-56.
29. Toivonen R, Kong L, Rasool O, et al. Activation of plasmacytoid dendritic cells in colon-draining lymph nodes during citrobacter rodentium infection involves pathogensensing and inflammatory pathways distinct from conventional dendritic cells. J Immunol 2016;196:4750-9.
30. Turley SJ, Lee JW, Dutton-Swain N, et al. Endocrine self and gut non-self intersect in the pancreatic lymph nodes. Proc Natl Acad Sci U S A 2005;102:17729-33.
31. Pozzilli P, Signore A, Williams AJ, et al. NOD mouse colonies around the world-recent facts and figures. Immunol Today 1993;14:193-6.
32. Murri M, Leiva I, Gomez-Zumaquero JM, et al. Gut microbiota in children with type 1 diabetes differs from that in healthy children: A case-control study. BMC Med 2013;11:46.
33. Krych Ł, Nielsen DS, Hansen AK, et al. Gut microbial markers are associated with diabetes onset, regulatory imbalance, and IFN-γ level in NOD mice. Gut Microbes 2015;6:101-9.
34. Luo C, Knight R, Siljander H, et al. ConStrains identifies microbial strains in metagenomic datasets. Nat Biotechnol 2015;33:1045-52.
35. Hansen CH, Krych L, Nielsen DS, et al. Early life treatment with vancomycin propagates Akkermansia muciniphila and reduces diabetes incidence in the NOD mouse. Diabetologia 2012;55:2285-94.
36. Belzer C, de Vos WM. Microbes inside-from diversity to function: The case of Akkermansia. Isme J 2012;6:1449-58.
37. van Passel MW, Kant R, Zoetendal EG, et al. The genome of Akkermansia muciniphila, a dedicated intestinal mucin degrader, and its use in exploring intestinal metagenomes. PLoS One 2011;6:e16876.
38. Png CW, Lindén SK, Gilshenan KS, et al. Mucolytic bacteria with increased prevalence in IBD mucosa augment in vitro utilization of mucin by other bacteria. Am J Gastroenterol 2010;105:2420-8.
39. Santacruz A, Collado MC, García-Valdés L, et al. Gut microbiota composition is associated with body weight, weight gain and biochemical parameters in pregnant women. Br J Nutr 2010;104:83-92.
40. Zhang H, DiBaise JK, Zuccolo A, et al. Human gut microbiota in obesity and after gastric bypass. Proc Natl Acad Sci U S A 2009;106:2365-70.
41. Swidsinski A, Dörffel Y, Loening-Baucke V, et al. Acute appendicitis is characterised by local invasion with Fusobacterium nucleatum/necrophorum. Gut 2011;60:34-40.
42. Derrien M, van Passel MW, van de Bovenkamp JH, et al. Mucin-bacterial interactions in the human oral cavity and digestive tract. Gut Microbes 2010;1:254-68.
43. Routy B, Le Chatelier E, Derosa L, et al. Gut microbiome influences efficacy of PD-1-based immunotherapy against epithelial tumors. Science 2017:eaan3706.
44. Schultz M. Clinical use of E. coli Nissle 1917 in inflammatory bowel disease. Inflamm Bowel Dis 2008;14:1012-8.
45. Lau K, Benitez P, Ardissone A, et al. Inhibition of type 1 diabetes correlated to a Lactobacillus johnsonii N6.2-mediated Th17 bias. J Immunol 2011;186:3538-46.
46. Matsuzaki T, Nagata Y, Kado S, et al. Prevention of onset in an insulin-dependent diabetes mellitus model, NOD mice, by oral feeding of Lactobacillus casei. APMIS 1997;105:643-9.
47. Alam C, Valkonen S, Palagani V, et al. Inflammatory tendencies and overproduction of IL-17 in the colon of young NOD mice are counteracted with diet change. Diabetes 2010;59:2237-46.
48. Lee AS, Gibson DL, Zhang Y, et al. Gut barrier disruption by an enteric bacterial pathogen accelerates insulitis in NOD mice. Diabetologia 2010;53:741-8.
49. Toivonen RK, Emani R, Munukka E, et al. Fermentable fibres condition colon microbiota and promote diabetogenesis in NOD mice. Diabetologia 2014;57:2183-92.
50. Wen L, Peng J, Li Z, et al. The effect of innate immunity on autoimmune diabetes and the expression of Toll-like receptors on pancreatic islets. J Immunol 2004;172:3173-80.
51. Halmos EP, Christophersen CT, Bird AR, et al. Consistent prebiotic effect on gut microbiota with altered FODMAP intake in patients with Crohn's disease: A randomised, controlled cross-over trial of well-defined diets. Clin Transl Gastroenterol 2016;7:e164.
52. Kuczynski J, Stombaugh J, Walters WA, et al. Using QIIME to analyze 16S rRNA gene sequences from microbial communities. Curr Protoc Bioinformatics 2011;Chapter 10:Unit 10.7.
53. Chassaing B, Koren O, Goodrich JK, et al. Dietary emulsifiers impact the mouse gut microbiota promoting colitis and metabolic syndrome. Nature 2015;519:92-6.