Gut microbiome in type 1 diabetes: A comprehensive review

Diabetes/Metabolism Research and Reviews

Volumn 34, Issue 7, 2018, Pages

  Zheng, Peilin ^a,b   Li, Zhixia ^a,b   Zhou, Zhiguang ^a,b  

^a CENTRAL SOUTH UNIVERSITY   (China)

^b CENTRAL SOUTH UNIVERSITY   (China)

Author keywords

environmental factors; genetics; gut microbiome; immune system; type 1 diabetes

Indexed keywords

BIOLOGICAL MARKER; CHINESE DRUG; IMMUNOMODULATING AGENT; INSULIN;

ADAPTIVE IMMUNITY; CHINESE MEDICINE; ENVIRONMENTAL FACTOR; HUMAN; INNATE IMMUNITY; INSULIN DEPENDENT DIABETES MELLITUS; INTESTINE FLORA; INTESTINE MUCOSA PERMEABILITY; MOLECULAR MIMICRY; NONHUMAN; PRIORITY JOURNAL; REVIEW; TAXONOMY; ANIMAL; DISEASE PREDISPOSITION; IMMUNOLOGY; MICROBIOLOGY; PHYSIOLOGY;

ANIMALS; DIABETES MELLITUS, TYPE 1; DISEASE SUSCEPTIBILITY; GASTROINTESTINAL MICROBIOME; HUMANS;

EID: 85050619460     PISSN: 15207552     EISSN: 15207560     Source Type: Journal    
DOI: 10.1002/dmrr.3043     Document Type: Review

References (99)

1. Boldison J, Wong FS. Immune and pancreatic beta cell interactions in type 1 diabetes. Trends Endocrinol Metab. 2016;27(12):856-867
2. Yi B, Huang G, Zhou ZG. Current and future clinical applications of zinc transporter-8 in type 1 diabetes mellitus. Chin Med J (Engl). 2015;128(17):2387-2394
3. Yang L, Luo S, Huang G, et al. The diagnostic value of zinc transporter 8 autoantibody (ZnT8A) for type 1 diabetes in Chinese. Diabetes Metab Res Rev. 2010;26(7):579-584
4. Chao C, Huang G, Li X, et al. Change of glutamic acid decarboxylase antibody and protein tyrosine phosphatase antibody in Chinese patients with acute-onset type 1 diabetes mellitus. Chin Med J (Engl). 2013;126(21):4006-4012
5. Wang Z, Xie Z, Lu Q, et al. Beyond genetics: what causes type 1 diabetes. Clinic Rev Allerg Immunol. 2016;52(2):273-584
6. Amur S, Parekh A, Mummaneni P. Sex differences and genomics in autoimmune diseases. J Autoimmun. 2012;38:254-265
7. Beeson PB. Age and sex associations of 40 autoimmune diseases. Am J Med. 1994;96(5):457-462
8. Yurkovetskiy L, Burrows M, Khan AA, et al. Gender bias in autoimmunity is influenced by microbiota. Immunity. 2013;39(2):400-412
9. Gülden E, Wong FS, Wen L. The gut microbiota and type 1 diabetes. Clin Immunol. 2015;159(2):143-153
10. Pociot F, McDermott MF. Genetics of type 1 diabetes mellitus. Genes Immun. 2002;3(5):235-249
11. Ziegler AG, Nepom GT. Prediction and pathogenesis in type 1 diabetes. Immunity. 2010;32(4):468-478
12. van Belle TL, Coppieters KT, Coppieters MG. Type 1 diabetes: etiology, immunology, and therapeutic strategies. Physiol Rev. 2011;91(1):79-118
13. Zheng P, Kissler S. PTPN22 silencing in the NOD model indicates the type 1 diabetes-associated allele is not a loss-of-function variant. Diabetes. 2013;62(3):896-904
14. Xie Z, Chang C, Zhou Z. Molecular mechanisms in autoimmune type 1 diabetes: a critical review. Clin Rev Allergy Immunol. 2014;47(2):174-192
15. Knip M, Siljander H. The role of the intestinal microbiota in type 1 diabetes mellitus. Nat Rev Endocrinol. 2016;12(3):154-167
16. Knip M. Environmental triggers and determinants of beta-cell autoimmunity and type 1 diabetes. Rev Endocr Metab Disord. 2003;4(3):213-223
17. Kaufman DL, Erlander MG, Clare-Salzler M, Atkinson MA, Maclaren NK, Tobin AJ. Autoimmunity to two forms of glutamate decarboxylase in insulin-dependent diabetes mellitus. J Clin Invest. 1992;89(1):283-292
18. Yoon JW, Onodera T, Notkins AL. Virus-induced diabetes mellitus. XV. Beta cell damage and insulin-dependent hyperglycemia in mice infected with coxsackie virus B4. J Exp Med. 1978;148(4):1068-1080
19. Luopajarvi K, Savilahti E, Virtanen SM, et al. Enhanced levels of cow's milk antibodies in infancy in children who develop type 1 diabetes later in childhood. Pediatr Diabetes. 2008;9(5):434-441
20. Du T, Zhou Z, You S, et al. Regulation by 1, 25-dihydroxy-vitamin D3 on altered TLRs expression and response to ligands of monocyte from autoimmune diabetes. Clin Chim Acta. 2009;402(1-2):133-138
21. Ghazarian L, Diana J, Simoni Y, Beaudoin L, Lehuen A. Prevention or acceleration of type 1 diabetes by viruses. Cell Mol Life Sci. 2013;70(2):239-255
22. Candon S, Perez-Arroyo A, Marquet C, et al. Antibiotics in early life alter the gut microbiome and increase disease incidence in a spontaneous mouse model of autoimmune insulin-dependent diabetes. PLoS One. 2015;10:e125448
23. Brugman S, Klatter FA, Visser JT, et al. 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. 2006;49(9):2105-2108
24. 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(8):2285-2294
25. Mikkelsen KH, Knop FK, Vilsbøll T, Frost M, Hallas J, Pottegård A. Use of antibiotics in childhood and risk of type 1 diabetes: a population-based case-control study. Diabet Med. 2017;34(2):272-277
26. Hooper LV, Gordon JI. Commensal host-bacterial relationships in the gut. Science. 292(5519):1115-1118
27. Consortium HMP. Structure, function and diversity of the healthy human microbiome. Nature. 2012;486:207-214
28. Hu Y, Peng J, Tai N, et al. Maternal antibiotic treatment protects offspring from diabetes development in nonobese diabetic mice by generation of tolerogenic APCs. J Immunol. 2015;195(9):4176-4184
29. Bibbò S, Dore MP, Pes GM, Delitala G, Delitala AP. Is there a role for gut microbiota in type 1 diabetes pathogenesis? Ann Med. 2017;49(1):11-22
30. Hidalgo-Cantabrana C, Delgado S, Ruiz L, Ruas-Madiedo P, Sánchez B, Margolles A. Bifidobacteria and their health-promoting effects. Microbiol Spectr. 2017;5(3)
31. Samantha A, Whiteside HRSD. The microbiome of the urinary tract—a role beyond infection. Nat Rev Urol. 2015;12:81-90
32. Dominguez-Bello MG, Costello EK, Contreras M, et al. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc Natl Acad Sci U S A. 2010;107(26):11971-11975
33. Biasucci G, Benenati B, Morelli L, Bessi E, Boehm G̈. Cesarean delivery may affect the early biodiversity of intestinal bacteria. J Nutr. 2008;138(9):1796S-1800S
34. Brown K, DeCoffe D, Molcan E, Gibson DL. Diet-induced Dysbiosis of the intestinal microbiota and the effects on immunity and disease. Nutrients. 2012;4(8):1095-1119
35. Hu Y, Wong FS, Wen L. Antibiotics, gut microbiota, environment in early life and type 1 diabetes. Pharmacol Res. 2017;119:219-226
36. Geach T. Gut microbiota: Antibiotics do not affect metabolism in obesity. Nat Rev Endocrinol. 2016;12:558
37. Jackson MA, Goodrich JK, Maxan ME, et al. Proton pump inhibitors alter the composition of the gut microbiota. Gut. 2016;65(5):749-756
38. Sofi MH, Gudi R, Karumuthil-Melethil S, Perez N, Johnson BM, Vasu C. pH of drinking water influences the composition of gut microbiome and type 1 diabetes incidence. Diabetes. 2014;63(2):632-644
39. Wolf KJ, Daft JG, Tanner SM, Hartmann R, Khafipour E, Lorenz RG. Consumption of acidic water alters the gut microbiome and decreases the risk of diabetes in NOD mice. J Histochem Cytochem. 2014;62(4):237-250
40. Alkanani AK, Hara N, Gottlieb PA, et al. Alterations in intestinal microbiota correlate with susceptibility to type 1 diabetes. Diabetes. 2015;64:3510-3520
41. Wen L, Ley RE, Volchkov PY, et al. Innate immunity and intestinal microbiota in the development of type 1 diabetes. Nature. 2008;455(7216):1109-1113
42. King C, Sarvetnick N. The incidence of type-1 diabetes in NOD mice is modulated by restricted flora not germ-free conditions. PLoS One. 2011;6(2):e17049
43. Tai N, Peng J, Liu F, et al. Microbial antigen mimics activate diabetogenic CD8 T cells in NOD mice. J Exp Med. 2016;213(10):2129-2146
44. Knip M, Honkanen J. Modulation of type 1 diabetes risk by the intestinal microbiome. Curr Diab Rep. 2017;17(11):105
45. Giongo A, Gano KA, Crabb DB, et al. Toward defining the autoimmune microbiome for type 1 diabetes. ISME J. 2011;5(1):82-91
46. 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
47. 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(8):1569-1577
48. de Goffau MC, Luopajarvi K, Knip M, et al. Fecal microbiota composition differs between children with beta-cell autoimmunity and those without. Diabetes. 2013;62(4):1238-1244
49. Vaarala O. Human intestinal microbiota and type 1 diabetes. Curr Diab Rep. 2013;13(5):601-607
50. 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(10):e25792
51. Krych Ł, Nielsen DS, Hansen AK, Hansen CHF. Gut microbial markers are associated with diabetes onset, regulatory imbalance, and IFN-γlevel in NOD mice. Gut Microbes. 2015;6(2):101-109
52. Hara N, Alkanani AK, Ir D, et al. The role of the intestinal microbiota in type 1 diabetes. Clin Immunol. 2013;146(2):112-119
53. Mejía-León M, Barca A. Diet, microbiota and immune system in type 1 diabetes development and evolution. Nutrients. 2015;7(11):9171-9184
54. 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(2):260-273
55. Patterson E, Marques TM, O'Sullivan O, et al. Streptozotocin-induced type-1-diabetes disease onset in Sprague-Dawley rats is associated with an altered intestinal microbiota composition and decreased diversity. Microbiology. 2015;161(1):182-193
56. Li X, Atkinson MA. The role for gut permeability in the pathogenesis of type 1 diabetes—a solid or leaky concept? Pediatr Diabetes. 2015;16(7):485-492
57. Maffeis C, Martina A, Corradi M, et al. Association between intestinal permeability and faecal microbiota composition in Italian children with beta cell autoimmunity at risk for type 1 diabetes. Diabetes Metab Res Rev. 2016;32(7):700-709
58. Ohkusa T, Okayasu I, Ogihara T, Morita K, Ogawa M, Sato N. Induction of experimental ulcerative colitis by Fusobacterium varium isolated from colonic mucosa of patients with ulcerative colitis. Gut. 2003;52(1):79-83
59. Strauss J, Kaplan GG, Beck PL, et al. Invasive potential of gut mucosa-derived Fusobacterium nucleatum positively correlates with IBD status of the host. Inflamm Bowel Dis. 2011;17(9):1971-1978
60. Legaria MC, Lumelsky G, Rodriguez V, Rosetti S. Clindamycin-resistant Fusobacterium varium bacteremia and decubitus ulcer infection. J Clin Microbiol. 2005;43(8):4293-4295
61. Hevia A, Milani C, Lopez P, et al. Intestinal dysbiosis associated with systemic lupus erythematosus. MBio. 2014;5:e1514-e1548
62. Schickel JN, Glauzy S, Ng YS, et al. Self-reactive VH4-34-expressing IgG B cells recognize commensal bacteria. J Exp Med. 2017;214(7):2161
63. Hebbandi NR, Ronchi F, Wang J, et al. A gut microbial mimic that hijacks Diabetogenic autoreactivity to suppress colitis. Cell. 2017;171(3):655-667
64. Ferris ST, Zakharov PN, Wan X, et al. The islet-resident macrophage is in an inflammatory state and senses microbial products in blood. J Exp Med. 2017;214(8):2369-2385
65. Willcox A, Richardson SJ, Bone AJ, Foulis AK, Morgan NG. Analysis of islet inflammation in human type 1 diabetes. Clin Exp Immunol. 2009;155(2):173-181
66. Janeway CJ. Approaching the asymptote? Evolution and revolution in immunology. Cold Spring Harb Symp Quant Biol. 1989;54(0):1-13
67. Akira S, Uematsu S, Takeuchi O. Pathogen recognition and innate immunity. Cell. 2006;124(4):783-801
68. Kieser KJ, Kagan JC. Multi-receptor detection of individual bacterial products by the innate immune system. Nat Rev Immunol. 2017;77:376-390
69. Burrows MP, Volchkov P, Kobayashi KS, Chervonsky AV. Microbiota regulates type 1 diabetes through toll-like receptors. Proc Natl Acad Sci U S A. 2015;112(32):9973-9977
70. McCoy KD, Ronchi F, Geuking MB. Host-microbiota interactions and adaptive immunity. Immunol Rev. 2017;279(1):63-69
71. Ivanov II, Atarashi K, Manel N, et al. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell. 2009;139(3):485-498
72. Yu H, Gagliani N, Ishigame H, et al. Intestinal type 1 regulatory T cells migrate to periphery to suppress diabetogenic T cells and prevent diabetes development. Proc Natl Acad Sci U S A. 2017;114(39):10443-10448
73. Cummings JH, Pomare EW, Branch WJ, Naylor CP, Macfarlane GT. Short chain fatty acids in human large intestine, portal, hepatic and venous blood. Gut. 1987;28(10):1221-1227
74. Postler TS, Ghosh S. Understanding the holobiont: how microbial metabolites affect human health and shape the immune system. Cell Metab. 2017;26(1):110-130
75. Arpaia N, Campbell C, Fan X, et al. Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature. 2013;504(7480):451-455
76. Mariño E, Richards JL, McLeod KH, et al. Gut microbial metabolites limit the frequency of autoimmune T cells and protect against type 1 diabetes. Nat Immunol. 2017;18(5):552-562
77. 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(27):12204-12209
78. Furusawa Y, Obata Y, Fukuda S, et al. Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature. 2013;504(7480):446-450
79. Kudoh K, Shimizu J, Wada M, et al. Effect of indigestible saccharides on B lymphocyte response of intestinal mucosa and cecal fermentation in rats. J Nutr Sci Vitaminol (Tokyo). 1998;44(1):103-112
80. Kim CH. B cell-helping functions of gut microbial metabolites. Microb Cell. 2016;3(10):529-531
81. Kim M, Qie Y, Park J, Kim CH. Gut microbial metabolites fuel host antibody responses. Cell Host Microbe. 2016;20(2):202-214
82. Calcinaro F, Dionisi S, Marinaro M, et al. Oral probiotic administration induces interleukin-10 production and prevents spontaneous autoimmune diabetes in the non-obese diabetic mouse. Diabetologia. 2005;48(8):1565-1575
83. Zhu W, Winter MG, Byndloss MX, et al. Precision editing of the gut microbiota ameliorates colitis. Nature. 2018;553(7687):208-211
84. Lee H, Ko G. Effect of metformin on metabolic improvement and gut microbiota. Appl Environ Microbiol. 2014;80(19):5935-5943
85. Wang L, Li P, Tang Z, Yan X, Feng B. Structural modulation of the gut microbiota and the relationship with body weight: compared evaluation of liraglutide and saxagliptin treatment. Sci Rep. 2016;6(1):33251
86. Kihl P, Krych L, Buschard K, et al. Oral insulin does not alter gut microbiota composition of NOD mice. Diabetes Metab Res Rev. 2018;34(6):e3010
87. Raz I, Elias D, Avron A, Tamir M, Metzger M, Cohen IR. β-Cell function in new-onset type 1 diabetes and immunomodulation with a heat-shock protein peptide (DiaPep277): a randomised, double-blind, phase II trial. Lancet. 2001;358(9295):1749-1753
88. Fenalti G, Rowley M. GAD65 as a prototypic autoantigen. J Autoimmun. 2008;32:228-232
89. Chatenoud L, Thervet E, Primo J, Bach JF. Anti-CD3 antibody induces long-term remission of overt autoimmunity in nonobese diabetic mice. Proc Natl Acad Sci U S A. 1994;91(1):123-127
90. Alegre ML, Peterson LJ, Xu D, et al. A non-activating “humanized” anti-CD3 monoclonal antibody retains immunosuppressive properties in vivo. Transplantation. 1994;57(11):1537-1543
91. Kremer JM, Genant HK, Moreland LW, et al. Effects of abatacept in patients with methotrexate-resistant active rheumatoid arthritis: a randomized trial. Ann Intern Med. 2006;144(12):865-876
92. Hu CY, Rodriguezpinto D, Du W, et al. Treatment with CD20-specific antibody prevents and reverses autoimmune diabetes in mice. J Clin Invest. 2007;117(12):3857-3867
93. Waldron-Lynch F, Henegariu O, Deng S, et al. Teplizumab induces human gut-tropic regulatory cells in humanized mice and patients. Sci Transl Med. 2012;4:112r-118r
94. Chang CJ, Lin CS, Lu CC, et al. Ganoderma lucidum reduces obesity in mice by modulating the composition of the gut microbiota. Nat Commun. 2015;6(1):7489
95. Zheng S, Zhao M, Wu Y, et al. Suppression of pancreatic beta cell apoptosis by Danzhi Jiangtang capsule contributes to the attenuation of type 1 diabetes in rats. BMC Complement Altern Med. 2016;16:31
96. Li J, Casteels T, Frogne T, et al. Artemisinins target GABA A receptor signaling and impair α cell identity. Cell. 2017;168(1-2):86-100
97. Michael S, Lindsay K, Alessandro T, et al. Protective major histocompatibility complex allele prevents type 1 diabetes by shaping the intestinal microbiota early in ontogeny. Proc Natl Acad Sci U S A. 2017;114:9671-9676
98. Onengut-Gumuscu S, Chen W, Burren O, et al. Fine mapping of type 1 diabetes susceptibility loci and evidence for colocalization of causal variants with lymphoid gene enhancers. Nat Genet. 2015;47(4):381-386
99. Li AH, Morrison AC, Kovar C, et al. Analysis of loss-of-function variants and 20 risk factor phenotypes in 8,554 individuals identifies loci influencing chronic disease. Nat Genet. 2015;47(6):640-642