Gut microbial metabolites limit the frequency of autoimmune T cells and protect against type 1 diabetes

Nature Immunology

Volumn 18, Issue 5, 2017, Pages 552-562

  Mariño, Eliana ^a   Richards, James L ^a   McLeod, Keiran H ^a   Stanley, Dragana ^b   Yap, Yu Anne ^a   Knight, Jacinta ^a   McKenzie, Craig ^a   Kranich, Jan ^c   Oliveira, Ana Carolina ^d   Rossello, Fernando J ^a   Krishnamurthy, Balasubramanian ^e   Nefzger, Christian M ^a   Macia, Laurence ^a,f   Thorburn, Alison ^a   Baxter, Alan G ^g   Morahan, Grant ^h   Wong, Lee H ^a   Polo, Jose M ^a   Moore, Robert J ^a,i   Lockett, Trevor J ^j   Clarke, Julie M ^j   Topping, David L ^j   Harrison, Leonard C ^k   Mackay, Charles R ^a   more..

^a MONASH UNIVERSITY   (Australia)

^b CENTRAL QUEENSLAND UNIVERSITY   (Australia)

^c UNIVERSITY OF MUNICH   (Germany)

^d FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^e ST VINCENT'S INSTITUTE OF MEDICAL RESEARCH   (Australia)

^f UNIVERSITY OF SYDNEY   (Australia)

^g JAMES COOK UNIVERSITY   (Australia)

^h UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

ⁱ RMIT UNIVERSITY   (Australia)

^j CSIRO   (Australia)

^k WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ACETIC ACID DERIVATIVE; ACETYLATED HIGH AMYLOSE MAIZE STARCH; BUTYRIC ACID DERIVATIVE; BUTYRYLATED HIGH AMYLOSE MAIZE STARCH; INTERLEUKIN 21; INTERLEUKIN 22; SHORT CHAIN FATTY ACID; STARCH; UNCLASSIFIED DRUG; INTERLEUKIN DERIVATIVE;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOIMMUNITY; B LYMPHOCYTE; CELL DIFFERENTIATION; COLON; COMPARATIVE STUDY; CONTROLLED STUDY; DIABETIC DIET; FEMALE; FERMENTATION; IMMUNOLOGICAL TOLERANCE; IMMUNOREACTIVITY; INSULIN DEPENDENT DIABETES MELLITUS; INTESTINE FLORA; LYMPHOCYTE COUNT; LYMPHOCYTE FUNCTION; LYMPHOID TISSUE; MALE; METABOLITE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; REGULATORY T LYMPHOCYTE; SEX DIFFERENCE; T LYMPHOCYTE; ANIMAL; BLOOD; CELL CULTURE; DIET THERAPY; DYSBIOSIS; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; NONOBESE DIABETIC MOUSE; PATHOLOGY;

ACETATES; ANIMALS; AUTOIMMUNITY; B-LYMPHOCYTES; BUTYRATES; CELLS, CULTURED; COLON; DIABETES MELLITUS, TYPE 1; DIET THERAPY; DYSBIOSIS; GASTROINTESTINAL MICROBIOME; INTERLEUKINS; MICE; MICE, INBRED NOD; T-LYMPHOCYTES, REGULATORY;

EID: 85016122461     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni.3713     Document Type: Article

References (57)

1. Atkinson, M.A., Eisenbarth, G.S. &Michels, A.W. Type 1 diabetes. Lancet 383, 69-82 (2014).
2. Vatanen, T. et al. Variation in microbiome LPS immunogenicity contributes to autoimmunity in humans. Cell 165, 842-853 (2016).
3. Livanos, A.E. et al. Antibiotic-mediated gut microbiome perturbation accelerates development of type 1 diabetes in mice. Nat. Microbiol. 1, 16140 (2016).
4. Thorburn, A.N., Macia, L. &Mackay, C.R. Diet, metabolites, and "western-lifestyle" inflammatory diseases. Immunity 40, 833-842 (2014).
5. Maslowski, K.M. &Mackay, C.R. Diet, gut microbiota and immune responses. Nat. Immunol. 12, 5-9 (2011).
6. Wen, L. et al. Innate immunity and intestinal microbiota in the development of type 1 diabetes. Nature 455, 1109-1113 (2008).
7. Markle, J.G. et al. Sex differences in the gut microbiome drive hormone-dependent regulation of autoimmunity. Science 339, 1084-1088 (2013).
8. Smith, P.M. et al. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science 341, 569-573 (2013).
9. Furusawa, Y. et al. Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature 504, 446-450 (2013).
10. Arpaia, N. et al. Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature 504, 451-455 (2013).
11. Fukuda, S. et al. Bifidobacteria can protect from enteropathogenic infection through production of acetate. Nature 469, 543-547 (2011).
12. Maslowski, K.M. et al. Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43. Nature 461, 1282-1286 (2009).
13. Zhang, Y. et al. Genome-wide DNA methylation analysis identifies hypomethylated genes regulated by FOXP3 in human regulatory T cells. Blood 122, 2823-2836 (2013).
14. Sakaguchi, S. Naturally arising Foxp3-expressing CD25+CD4+ regulatory T cells in immunological tolerance to self and non-self. Nat. Immunol. 6, 345-352 (2005).
15. Turley, S.J., Lee, J.W., Dutton-Swain, N., Mathis, D. &Benoist, C. Endocrine self and gut non-self intersect in the pancreatic lymph nodes. Proc. Natl. Acad. Sci. USA 102, 17729-17733 (2005).
16. Vaarala, O., Atkinson, M.A. &Neu, J. The "perfect storm" for type 1 diabetes: the complex interplay between intestinal microbiota, gut permeability, and mucosal immunity. Diabetes 57, 2555-2562 (2008).
17. de Goffau, M.C. et al. Fecal microbiota composition differs between children with beta-cell autoimmunity and those without. Diabetes 62, 1238-1244 (2013).
18. Endesfelder, D. et al. Compromised gut microbiota networks in children with anti-islet cell autoimmunity. Diabetes 63, 2006-2014 (2014).
19. Tan, J. et al. Dietary fiber and bacterial SCFA enhance oral tolerance and protect against food allergy through diverse cellular pathways. Cell Rep. 15, 2809-2824 (2016).
20. Topping, D.L. &Clifton, P.M. Short-chain fatty acids and human colonic function: roles of resistant starch and nonstarch polysaccharides. Physiol. Rev. 81, 1031-1064 (2001).
21. Clarke, J.M., Topping, D.L., Bird, A.R., Young, G.P. &Cobiac, L. Effects of high-amylose maize starch and butyrylated high-amylose maize starch on azoxymethane-induced intestinal cancer in rats. Carcinogenesis 29, 2190-2194 (2008).
22. Perry, R.J. et al. Acetate mediates a microbiome-brain-beta-cell axis to promote metabolic syndrome. Nature 534, 213-217 (2016).
23. Amrani, A. et al. Progression of autoimmune diabetes driven by avidity maturation of a T-cell population. Nature 406, 739-742 (2000).
24. Marino, E., Tan, B., Binge, L., Mackay, C.R. &Grey, S.T. B-cell cross-presentation of autologous antigen precipitates diabetes. Diabetes 61, 2893-2905 (2012).
25. Brummel, R., Roberts, T.L., Stacey, K.J. &Lenert, P. Higher-order CpG-DNA stimulation reveals distinct activation requirements for marginal zone and follicular B cells in lupus mice. Eur. J. Immunol. 36, 1951-1962 (2006).
26. van den Elsen, P.J., Holling, T.M., Kuipers, H.F. &van der Stoep, N. Transcriptional regulation of antigen presentation. Curr. Opin. Immunol. 16, 67-75 (2004).
27. Martins, G. &Calame, K. Regulation and functions of Blimp-1 in T and B lymphocytes. Annu. Rev. Immunol. 26, 133-169 (2008).
28. Saemann, M.D. et al. Bacterial metabolite interference with maturation of human monocyte-derived dendritic cells. J. Leukoc. Biol. 71, 238-246 (2002).
29. Thorburn, A.N. et al. Evidence that asthma is a developmental origin disease influenced by maternal diet and bacterial metabolites. Nat. Commun. 6, 7320 (2015).
30. Vignali, D.A., Collison, L.W. &Workman, C.J. How regulatory T cells work. Nat. Rev. Immunol. 8, 523-532 (2008).
31. Shi, G. et al. Free fatty acid receptor 2, a candidate target for type 1 diabetes, induces cell apoptosis through ERK signaling. J. Mol. Endocrinol. 53, 367-380 (2014).
32. Macia, L. et al. Metabolite-sensing receptors GPR43 and GPR109A facilitate dietary fibre-induced gut homeostasis through regulation of the inflammasome. Nat. Commun. 6, 6734 (2015).
33. Sutherland, A.P. et al. Interleukin-21 is required for the development of type 1 diabetes in NOD mice. Diabetes 58, 1144-1155 (2009).
34. Spolski, R., Kashyap, M., Robinson, C., Yu, Z. &Leonard, W.J. IL-21 signaling is critical for the development of type I diabetes in the NOD mouse. Proc. Natl. Acad. Sci. USA 105, 14028-14033 (2008).
35. Feehily, C. &Karatzas, K.A. Role of glutamate metabolism in bacterial responses towards acid and other stresses. J. Appl. Microbiol. 114, 11-24 (2013).
36. Marino, E. et al. CD4+CD25+ T-cells control autoimmunity in the absence of B-cells. Diabetes 58, 1568-1577 (2009).
37. Buhlmann, J.E. et al. In the absence of a CD40 signal, B cells are tolerogenic. Immunity 2, 645-653 (1995).
38. Kostic, A.D. et al. The dynamics of the human infant gut microbiome in development and in progression toward type 1 diabetes. Cell Host Microbe 17, 260-273 (2015).
39. Macfarlane, S. &Macfarlane, G.T. Regulation of short-chain fatty acid production. Proc. Nutr. Soc. 62, 67-72 (2003).
40. Atarashi, K. et al. Treg induction by a rationally selected mixture of Clostridia strains from the human microbiota. Nature 500, 232-236 (2013).
41. Chen, X. et al. Requirement for the histone deacetylase Hdac3 for the inflammatory gene expression program in macrophages. Proc. Natl. Acad. Sci. USA 109, E2865-E2874 (2012).
42. White, C.A. et al. Histone deacetylase inhibitors upregulate B cell microRNAs that silence AID and Blimp-1 expression for epigenetic modulation of antibody and autoantibody responses. J. Immunol. 193, 5933-5950 (2014).
43. Reddy, P. et al. Histone deacetylase inhibition modulates indoleamine 2,3-dioxygenase-dependent DC functions and regulates experimental graft-versus-host disease in mice. J. Clin. Invest. 118, 2562-2573 (2008).
44. Le Leu, R.K. et al. Butyrylated starch intake can prevent red meat-induced O6-methyl-2-deoxyguanosine adducts in human rectal tissue: a randomised clinical trial. Br. J. Nutr. 114, 220-230 (2015).
45. Bajka, B.H., Topping, D.L., Cobiac, L. &Clarke, J.M. Butyrylated starch is less susceptible to enzymic hydrolysis and increases large-bowel butyrate more than high-amylose maize starch in the rat. Br. J. Nutr. 96, 276-282 (2006).
46. Round, J.L. &Mazmanian, S.K. Inducible Foxp3+ regulatory T-cell development by a commensal bacterium of the intestinal microbiota. Proc. Natl. Acad. Sci. USA 107, 12204-12209 (2010).
47. Marino, E. et al. BAFF regulates activation of self-reactive T cells through B-cell dependent mechanisms and mediates protection in NOD mice. Eur. J. Immunol. 44, 983-993 (2014).
48. Yi, W. et al. Targeted regulation of self-peptide presentation prevents type I diabetes in mice without disrupting general immunocompetence. J. Clin. Invest. 120, 1324-1336 (2010).
49. Ashelford, K.E., Chuzhanova, N.A., Fry, J.C., Jones, A.J. &Weightman, A.J. At least 1 in 20 16S rRNA sequence records currently held in public repositories is estimated to contain substantial anomalies. Appl. Environ. Microbiol. 71, 7724-7736 (2005).
50. Bragg, L., Stone, G., Imelfort, M., Hugenholtz, P. &Tyson, G.W. Fast, accurate error-correction of amplicon pyrosequences using Acacia. Nat. Methods 9, 425-426 (2012).
51. DeSantis, T.Z. et al. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl. Environ. Microbiol. 72, 5069-5072 (2006).
52. Fadrosh, D.W. et al. An improved dual-indexing approach for multiplexed 16S rRNA gene sequencing on the Illumina MiSeq platform. Microbiome 2, 6 (2014).
53. Mariño, E. et al. Marginal-zone B-cells of nonobese diabetic mice expand with diabetes onset, invade the pancreatic lymph nodes, and present autoantigen to diabetogenic T-cells. Diabetes 57, 395-404 (2008).
54. Dobin, A. et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29, 15-21 (2013).
55. Liao, Y., Smyth, G.K. &Shi, W. The Subread aligner: fast, accurate and scalable read mapping by seed-and-vote. Nucleic Acids Res. 41, e108 (2013).
56. Robinson, M.D., McCarthy, D.J. &Smyth, G.K. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139-140 (2010).
57. Polo, J.M. et al. A molecular roadmap of reprogramming somatic cells into iPS cells. Cell 151, 1617-1632 (2012).