Type 1 diabetes and gut microbiota: Friend or foe?

Pharmacological Research

Volumn 98, Issue , 2015, Pages 9-15

  Hu, Changyun ^a   Wong, F Susan ^b   Wen, Li ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b CARDIFF UNIVERSITY SCHOOL OF MEDICINE   (United Kingdom)

Author keywords

Autoimmunity; Gut microbiota; NOD mice; Type 1 diabetes

Indexed keywords

G PROTEIN COUPLED RECEPTOR;

AUTOIMMUNE DISEASE; BACTEROIDES; BACTEROIDES FRAGILIS; BIFIDOBACTERIUM ADOLESCENTIS; CELLULAR IMMUNITY; CLOSTRIDIUM; DEVELOPED COUNTRY; DISEASE COURSE; ENVIRONMENTAL FACTOR; GENETIC PREDISPOSITION; HUMAN; INCIDENCE; INFECTION CONTROL; INSULIN DEPENDENT DIABETES MELLITUS; INTESTINE FLORA; INTESTINE MUCOSA PERMEABILITY; MOUSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; RAT; REVIEW; ANIMAL; DIABETES MELLITUS, TYPE 1; GASTROINTESTINAL TRACT; IMMUNOLOGY; MICROBIOLOGY; NONOBESE DIABETIC MOUSE; PHYSIOLOGY;

ANIMALS; DIABETES MELLITUS, TYPE 1; GASTROINTESTINAL MICROBIOME; GASTROINTESTINAL TRACT; HUMANS; MICE, INBRED NOD;

EID: 84930757929     PISSN: 10436618     EISSN: 10961186     Source Type: Journal    
DOI: 10.1016/j.phrs.2015.02.006     Document Type: Review

References (112)

1. A. Lehuen, J. Diana, P. Zaccone, and A. Cooke Immune cell crosstalk in type 1 diabetes Nat Rev Immunol 10 2010 501 513
2. M.J. Ansari, P. Fiorina, S. Dada, I. Guleria, T. Ueno, and X. Yuan Role of ICOS pathway in autoimmune and alloimmune responses in NOD mice Clin Immunol 126 2008 140 147
3. I. Guleria, M. Gubbels Bupp, S. Dada, B. Fife, Q. Tang, and M.J. Ansari Mechanisms of PDL1-mediated regulation of autoimmune diabetes Clin Immunol 125 2007 16 25
4. M. Ben Nasr, F. D'Addio, V. Usuelli, S. Tezza, R. Abdi, and P. Fiorina The rise, fall, and resurgence of immunotherapy in type 1 diabetes Pharmacol Res 2014
5. K.C. Herold, J.A. Bluestone, A.G. Montag, A. Parihar, A. Wiegner, and R.E. Gress Prevention of autoimmune diabetes with nonactivating anti-CD3 monoclonal antibody Diabetes 41 1992 385 391
6. K.C. Herold, W. Hagopian, J.A. Auger, E. Poumian-Ruiz, L. Taylor, and D. Donaldson Anti-CD3 monoclonal antibody in new-onset type 1 diabetes mellitus N Engl J Med 346 2002 1692 1698
7. C.Y. Hu, D. Rodriguez-Pinto, W. Du, A. Ahuja, O. Henegariu, and F.S. Wong Treatment with CD20-specific antibody prevents and reverses autoimmune diabetes in mice J Clin Invest 117 2007 3857 3867
8. J. Tuomilehto The emerging global epidemic of type 1 diabetes Curr Diab Rep 13 2013 795 804
9. J.A. Todd, N.M. Walker, J.D. Cooper, D.J. Smyth, K. Downes, and V. Plagnol Robust associations of four new chromosome regions from genome-wide analyses of type 1 diabetes Nat Genet 39 2007 857 864
10. J.C. Barrett, D.G. Clayton, P. Concannon, B. Akolkar, J.D. Cooper, and H.A. Erlich Genome-wide association study and meta-analysis find that over 40 loci affect risk of type 1 diabetes Nat Genet 41 2009 703 707
11. M.J. Redondo, L. Yu, M. Hawa, T. Mackenzie, D.A. Pyke, and G.S. Eisenbarth Heterogeneity of type I diabetes: analysis of monozygotic twins in Great Britain and the United States Diabetologia 44 2001 354 362
12. K.M. Gillespie, S.C. Bain, A.H. Barnett, P.J. Bingley, M.R. Christie, and G.V. Gill The rising incidence of childhood type 1 diabetes and reduced contribution of high-risk HLA haplotypes Lancet 364 2004 1699 1700
13. S. Fourlanos, M.D. Varney, B.D. Tait, G. Morahan, M.C. Honeyman, and P.G. Colman The rising incidence of type 1 diabetes is accounted for by cases with lower-risk human leukocyte antigen genotypes Diabetes Care 31 2008 1546 1549
14. J.F. Bach The effect of infections on susceptibility to autoimmune and allergic diseases N Engl J Med 347 2002 911 920
15. M. Trucco Gene-environment interaction in type 1 diabetes mellitus Endocrinol Nutr 56 Suppl. 4 2009 56 59
16. J.A. Todd Etiology of type 1 diabetes Immunity 32 2010 457 467
17. L. Krogvold, B. Edwin, T. Buanes, G. Frisk, O. Skog, and M. Anagandula Detection of a low-grade enteroviral infection in the islets of Langerhans of living patients newly diagnosed with type 1 diabetes Diabetes 2014
18. M. Heinig, E. Petretto, C. Wallace, L. Bottolo, M. Rotival, and H. Lu A trans-acting locus regulates an anti-viral expression network and type 1 diabetes risk Nature 467 2010 460 464
19. G.R. Gallagher, M.A. Brehm, R.W. Finberg, B.A. Barton, L.D. Shultz, and D.L. Greiner Viral infection of engrafted human islets leads to diabetes Diabetes 2014
20. E.V. Marietta, A.M. Gomez, C. Yeoman, A.Y. Tilahun, C.R. Clark, and D.H. Luckey Low incidence of spontaneous type 1 diabetes in non-obese diabetic mice raised on gluten-free diets is associated with changes in the intestinal microbiome PLOS ONE 8 2013 e78687
21. C.H. Hansen, L. Krych, K. Buschard, S.B. Metzdorff, C. Nellemann, and L.H. Hansen A maternal gluten-free diet reduces inflammation and diabetes incidence in the offspring of NOD mice Diabetes 63 2014 2821 2832
22. O. Vaarala Is type 1 diabetes a disease of the gut immune system triggered by cow's milk insulin? Adv Exp Med Biol 569 2005 151 156
23. H. Kolb, and P. Pozzilli Cow's milk and type I diabetes: the gut immune system deserves attention Immunol Today 20 1999 108 110
24. J.L. Sonnenburg, J. Xu, D.D. Leip, C.H. Chen, B.P. Westover, and J. Weatherford Glycan foraging in vivo by an intestine-adapted bacterial symbiont Science 307 2005 1955 1959
25. T. Yatsunenko, F.E. Rey, M.J. Manary, I. Trehan, M.G. Dominguez-Bello, and M. Contreras Human gut microbiome viewed across age and geography Nature 486 2012 222 227
26. A.L. Kau, P.P. Ahern, N.W. Griffin, A.L. Goodman, and J.I. Gordon Human nutrition, the gut microbiome and the immune system Nature 474 2011 327 336
27. S. Fukuda, H. Toh, K. Hase, K. Oshima, Y. Nakanishi, and K. Yoshimura Bifidobacteria can protect from enteropathogenic infection through production of acetate Nature 469 2011 543 547
28. T. Olszak, D. An, S. Zeissig, M.P. Vera, J. Richter, and A. Franke Microbial exposure during early life has persistent effects on natural killer T cell function Science 336 2012 489 493
29. P.P. Ahern, J.J. Faith, and J.I. Gordon Mining the human gut microbiota for effector strains that shape the immune system Immunity 40 2014 815 823
30. P.J. Turnbaugh, R.E. Ley, M. Hamady, C.M. Fraser-Liggett, R. Knight, and J.I. Gordon The human microbiome project Nature 449 2007 804 810
31. P.J. Turnbaugh, F. Backhed, L. Fulton, and J.I. Gordon Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome Cell Host Microbe 3 2008 213 223
32. C.P. Moran, and F. Shanahan Gut microbiota and obesity: role in aetiology and potential therapeutic target Best Pract Res Clin Gastroenterol 28 2014 585 597
33. R.E. Ley, P.J. Turnbaugh, S. Klein, and J.I. Gordon Microbial ecology: human gut microbes associated with obesity Nature 444 2006 1022 1023
34. P. Bekkering, I. Jafri, F.J. van Overveld, and G.T. Rijkers The intricate association between gut microbiota and development of type 1, type 2 and type 3 diabetes Expert Rev Clin Immunol 9 2013 1031 1041
35. L. Yurkovetskiy, M. Burrows, A.A. Khan, L. Graham, P. Volchkov, and L. Becker Gender bias in autoimmunity is influenced by microbiota Immunity 39 2013 400 412
36. H.J. Wu, and E. Wu The role of gut microbiota in immune homeostasis and autoimmunity Gut Microbes 3 2012 4 14
37. C. Sorini, and M. Falcone Shaping the (auto)immune response in the gut: the role of intestinal immune regulation in the prevention of type 1 diabetes Am J Clin Exp Immunol 2 2013 156 171
38. J.G. Markle, D.N. Frank, S. Mortin-Toth, C.E. Robertson, L.M. Feazel, and U. Rolle-Kampczyk Sex differences in the gut microbiome drive hormone-dependent regulation of autoimmunity Science 339 2013 1084 1088
39. R.S. Longman, Y. Yang, G.E. Diehl, S.V. Kim, and D.R. Littman Microbiota: host interactions in mucosal homeostasis and systemic autoimmunity Cold Spring Harb Symp Quant Biol 78 2013 193 201
40. A.V. Chervonsky Microbiota and autoimmunity Cold Spring Harb Perspect Biol 5 2013 a007294
41. M.P. Sherman, H. Zaghouani, and V. Niklas Gut microbiota, the immune system, and diet influence the neonatal gut-brain axis Pediatr Res 2014
42. A. Gonzalez, J. Stombaugh, C. Lozupone, P.J. Turnbaugh, J.I. Gordon, and R. Knight The mind-body-microbial continuum Dialogues Clin Neurosci 13 2011 55 62
43. F. Backhed, C.M. Fraser, Y. Ringel, M.E. Sanders, R.B. Sartor, and P.M. Sherman Defining a healthy human gut microbiome: current concepts, future directions, and clinical applications Cell Host Microbe 12 2012 611 622
44. B.L. Cantarel, V. Lombard, and B. Henrissat Complex carbohydrate utilization by the healthy human microbiome PLoS ONE 7 2012 e28742
45. D. Gevers, R. Knight, J.F. Petrosino, K. Huang, A.L. McGuire, and B.W. Birren The Human Microbiome Project: a community resource for the healthy human microbiome PLoS Biol 10 2012 e1001377
46. C. Human Microbiome Project Structure, function and diversity of the healthy human microbiome Nature 486 2012 207 214
47. J. Qin, R. Li, J. Raes, M. Arumugam, K.S. Burgdorf, and C. Manichanh A human gut microbial gene catalogue established by metagenomic sequencing Nature 464 2010 59 65
48. P.B. Eckburg, E.M. Bik, C.N. Bernstein, E. Purdom, L. Dethlefsen, and M. Sargent Diversity of the human intestinal microbial flora Science 308 2005 1635 1638
49. G.D. Wu, J.D. Lewis, C. Hoffmann, Y.Y. Chen, R. Knight, and K. Bittinger Sampling and pyrosequencing methods for characterizing bacterial communities in the human gut using 16S sequence tags BMC Microbiol 10 2010 206
50. W.R. Wikoff, A.T. Anfora, J. Liu, P.G. Schultz, S.A. Lesley, and E.C. Peters Metabolomics analysis reveals large effects of gut microflora on mammalian blood metabolites Proc Natl Acad Sci U S A 106 2009 3698 3703
51. K. Atarashi, and K. Honda Microbiota in autoimmunity and tolerance Curr Opin Immunol 23 2011 761 768
52. T. Suzuki, Y.T. Takao, T. Fujimura, T. Kawamura, E. Shimizu, and Z.M. Tamashita Diabetogenic effects of lymphocyte transfusion on the NOD or NOD nude mice M.B.J. Rygaard, N. Graem, M. Sprang-Thomsen, Immune-deficient animals in biomedical research 1987 Karger Basel 112 116
53. C. Alam, E. Bittoun, D. Bhagwat, S. Valkonen, A. Saari, and U. Jaakkola Effects of a germ-free environment on gut immune regulation and diabetes progression in non-obese diabetic (NOD) mice Diabetologia 54 2011 1398 1406
54. L. Wen, R.E. Ley, P.Y. Volchkov, P.B. Stranges, L. Avanesyan, and A.C. Stonebraker Innate immunity and intestinal microbiota in the development of Type 1 diabetes Nature 455 2008 1109 1113
55. A. Giongo, K.A. Gano, D.B. Crabb, N. Mukherjee, L.L. Novelo, and G. Casella Toward defining the autoimmune microbiome for type 1 diabetes ISME J 5 2011 82 91
56. C.T. Brown, A.G. Davis-Richardson, A. Giongo, K.A. Gano, D.B. Crabb, and N. Mukherjee Gut microbiome metagenomics analysis suggests a functional model for the development of autoimmunity for type 1 diabetes PLoS ONE 6 2011 e25792
57. M.C. de Goffau, K. Luopajarvi, M. Knip, J. Ilonen, T. Ruohtula, and T. Harkonen Fecal microbiota composition differs between children with beta-cell autoimmunity and those without Diabetes 62 2013 1238 1244
58. M.C. de Goffau, S. Fuentes, B. van den Bogert, H. Honkanen, W.M. de Vos, and G.W. Welling Aberrant gut microbiota composition at the onset of type 1 diabetes in young children Diabetologia 57 2014 1569 1577
59. J. Neu, C.M. Reverte, A.D. Mackey, K. Liboni, L.M. Tuhacek-Tenace, and M. Hatch Changes in intestinal morphology and permeability in the biobreeding rat before the onset of type 1 diabetes J Pediatr Gastroenterol Nutr 40 2005 589 595
60. E. Bosi, L. Molteni, M.G. Radaelli, L. Folini, I. Fermo, and E. Bazzigaluppi Increased intestinal permeability precedes clinical onset of type 1 diabetes Diabetologia 49 2006 2824 2827
61. A. Sapone, L. de Magistris, M. Pietzak, M.G. Clemente, A. Tripathi, and F. Cucca Zonulin upregulation is associated with increased gut permeability in subjects with type 1 diabetes and their relatives Diabetes 55 2006 1443 1449
62. S. Graham, P. Courtois, W.J. Malaisse, J. Rozing, F.W. Scott, and A.M. Mowat Enteropathy precedes type 1 diabetes in the BB rat Gut 53 2004 1437 1444
63. O. Vaarala Leaking gut in type 1 diabetes Curr Opin Gastroenterol 24 2008 701 706
64. R.F. Schwartz, J. Neu, D. Schatz, M.A. Atkinson, and C. Wasserfall Comment on: Brugman S, et al.;1; (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 2007 2105 2108 Diabetologia, 50, 220-221
65. S. Brugman, F.A. Klatter, J.T. Visser, A.C. Wildeboer-Veloo, H.J. Harmsen, and J. Rozing 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 2006 2105 2108
66. L.F. Roesch, G.L. Lorca, G. Casella, A. Giongo, A. Naranjo, and A.M. Pionzio Culture-independent identification of gut bacteria correlated with the onset of diabetes in a rat model ISME J 3 2009 536 548
67. T. Watts, I. Berti, A. Sapone, T. Gerarduzzi, T. Not, and R. Zielke Role of the intestinal tight junction modulator zonulin in the pathogenesis of type I diabetes in BB diabetic-prone rats Proc Natl Acad Sci U S A 102 2005 2916 2921
68. O. Vaarala, M.A. Atkinson, and J. Neu The perfect storm for type 1 diabetes: the complex interplay between intestinal microbiota, gut permeability, and mucosal immunity Diabetes 57 2008 2555 2562
69. A. Hague, A.J. Butt, and C. Paraskeva The role of butyrate in human colonic epithelial cells: an energy source or inducer of differentiation and apoptosis? Proc Nutr Soc 55 1996 937 943
70. J.R. Brestoff, and D. Artis Commensal bacteria at the interface of host metabolism and the immune system Nat Immunol 14 2013 676 684
71. D. Bouskra, C. Brezillon, M. Berard, C. Werts, R. Varona, and I.G. Boneca Lymphoid tissue genesis induced by commensals through NOD1 regulates intestinal homeostasis Nature 456 2008 507 510
72. K. Atarashi, T. Tanoue, T. Shima, A. Imaoka, T. Kuwahara, and Y. Momose Induction of colonic regulatory T cells by indigenous Clostridium species Science 331 2011 337 341
73. M.C. Moreau, R. Ducluzeau, D. Guy-Grand, and M.C. Muller Increase in the population of duodenal immunoglobulin A plasmocytes in axenic mice associated with different living or dead bacterial strains of intestinal origin Infect Immun 21 1978 532 539
74. S.K. Mazmanian, C.H. Liu, A.O. Tzianabos, and D.L. Kasper An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system Cell 122 2005 107 118
75. J. Cahenzli, Y. Koller, M. Wyss, M.B. Geuking, and K.D. McCoy Intestinal microbial diversity during early-life colonization shapes long-term IgE levels Cell Host Microbe 14 2013 559 570
76. S.D. Kingma, N. Li, F. Sun, R.B. Valladares, J. Neu, and G.L. Lorca Lactobacillus johnsonii N6.2 stimulates the innate immune response through Toll-like receptor 9 in Caco-2 cells and increases intestinal crypt Paneth cell number in biobreeding diabetes-prone rats J Nutr 141 2011 1023 1028
77. J.A. Hall, N. Bouladoux, C.M. Sun, E.A. Wohlfert, R.B. Blank, and Q. Zhu Commensal DNA limits regulatory T cell conversion and is a natural adjuvant of intestinal immune responses Immunity 29 2008 637 649
78. J.Z. Oh, R. Ravindran, B. Chassaing, F.A. Carvalho, M.S. Maddur, and M. Bower TLR5-mediated sensing of gut microbiota is necessary for antibody responses to seasonal influenza vaccination Immunity 41 2014 478 492
79. J.L. Round, S.M. Lee, J. Li, G. Tran, B. Jabri, and T.A. Chatila The Toll-like receptor 2 pathway establishes colonization by a commensal of the human microbiota Science 332 2011 974 977
80. K.M. Maslowski, A.T. Vieira, A. Ng, J. Kranich, F. Sierro, and D. Yu Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43 Nature 461 2009 1282 1286
81. M. Thangaraju, G.A. Cresci, K. Liu, S. Ananth, J.P. Gnanaprakasam, and D.D. Browning GPR109A is a G-protein-coupled receptor for the bacterial fermentation product butyrate and functions as a tumor suppressor in colon Cancer Res 69 2009 2826 2832
82. M. Vijay-Kumar, J.D. Aitken, F.A. Carvalho, T.C. Cullender, S. Mwangi, and S. Srinivasan Metabolic syndrome and altered gut microbiota in mice lacking Toll-like receptor 5 Science 328 2010 228 231
83. R.L. Greer, A. Morgun, and N. Shulzhenko Bridging immunity and lipid metabolism by gut microbiota J Allergy Clin Immunol 132 2013 253 262 quiz 263
84. P.M. Smith, M.R. Howitt, N. Panikov, M. Michaud, C.A. Gallini, and Y.M. Bohlooly The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis Science 341 2013 569 573
85. M.S. Inan, R.J. Rasoulpour, L. Yin, A.K. Hubbard, D.W. Rosenberg, and C. Giardina The luminal short-chain fatty acid butyrate modulates NF-kappaB activity in a human colonic epithelial cell line Gastroenterology 118 2000 724 734
86. N. Arpaia, C. Campbell, X. Fan, S. Dikiy, J. van der Veeken, and P. deRoos Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation Nature 504 2013 451 455
87. Y. Furusawa, Y. Obata, S. Fukuda, T.A. Endo, G. Nakato, and D. Takahashi Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells Nature 504 2013 446 450
88. M. Rossi, A. Amaretti, and S. Raimondi Folate production by probiotic bacteria Nutrients 3 2011 118 134
89. L. Kjer-Nielsen, O. Patel, A.J. Corbett, J. Le Nours, B. Meehan, and L. Liu MR1 presents microbial vitamin B metabolites to MAIT cells Nature 491 2012 717 723
90. C. Mathieu, and K. Badenhoop Vitamin D and type 1 diabetes mellitus: state of the art Trends Endocrinol Metab 16 2005 261 266
91. J.T. Visser, K. Lammers, A. Hoogendijk, M.W. Boer, S. Brugman, and S. Beijer-Liefers Restoration of impaired intestinal barrier function by the hydrolysed casein diet contributes to the prevention of type 1 diabetes in the diabetes-prone BioBreeding rat Diabetologia 53 2010 2621 2628
92. J. Peng, S. Narasimhan, J.R. Marchesi, A. Benson, F.S. Wong, and L. Wen Long term effect of gut microbiota transfer on diabetes development J Autoimmun 53 2014 85 94
93. A. Hanninen, R. Nurmela, M. Maksimow, J. Heino, S. Jalkanen, and C. Kurts Islet beta-cell-specific T cells can use different homing mechanisms to infiltrate and destroy pancreatic islets Am J Pathol 170 2007 240 250
94. R. Valladares, D. Sankar, N. Li, E. Williams, K.K. Lai, and A.S. Abdelgeliel Lactobacillus johnsonii N6.2 mitigates the development of type 1 diabetes in BB-DP rats PLoS ONE 5 2010 e10507
95. K. Lau, P. Benitez, A. Ardissone, T.D. Wilson, E.L. Collins, and G. Lorca Inhibition of type 1 diabetes correlated to a Lactobacillus johnsonii N6.2-mediated Th17 bias J Immunol 186 2011 3538 3546
96. M.A. Kriegel, E. Sefik, J.A. Hill, H.J. Wu, C. Benoist, and D. Mathis Naturally transmitted segmented filamentous bacteria segregate with diabetes protection in nonobese diabetic mice Proc Natl Acad Sci U S A 108 2011 11548 11553
97. A.K. Marwaha, S.Q. Crome, C. Panagiotopoulos, K.B. Berg, H. Qin, and Q. Ouyang Cutting edge: Increased IL-17-secreting T cells in children with new-onset type 1 diabetes J Immunol 185 2010 3814 3818
98. J. Honkanen, J.K. Nieminen, R. Gao, K. Luopajarvi, H.M. Salo, and J. Ilonen IL-17 immunity in human type 1 diabetes J Immunol 185 2010 1959 1967
99. S. Li, C. Joseph, C. Becourt, J. Klibi, S. Luce, and D. Dubois-Laforgue Potential role of IL-17-producing iNKT cells in type 1 diabetes PLOS ONE 9 2014 e96151
100. B.O. Boehm, S. Rosinger, G. Sauer, B.J. Manfras, D. Palesch, and S. Schiekofer Protease-resistant human GAD-derived altered peptide ligands decrease TNF-alpha and IL-17 production in peripheral blood cells from patients with type 1 diabetes mellitus Mol Immunol 46 2009 2576 2584
101. J.A. Silva, D.L. Ferrucci, L.A. Peroni, P.G. Abrahao, A.F. Salamene, and C. Rossa-Junior Sequential IL-23 and IL-17 and increased Mmp8 and Mmp14 expression characterize the progression of an experimental model of periodontal disease in type 1 diabetes J Cell Physiol 227 2012 2441 2450
102. A.K. Marwaha, S. Tan, and J.P. Dutz Targeting the IL-17/IFN-gamma axis as a potential new clinical therapy for type 1 diabetes Clin Immunol 154 2014 84 89
103. C. Palmer, E.M. Bik, D.B. DiGiulio, D.A. Relman, and P.O. Brown Development of the human infant intestinal microbiota PLoS Biol 5 2007 e177
104. N. Sudo, X.N. Yu, Y. Aiba, N. Oyama, J. Sonoda, and Y. Koga An oral introduction of intestinal bacteria prevents the development of a long-term Th2-skewed immunological memory induced by neonatal antibiotic treatment in mice Clin Exp Allergy 32 2002 1112 1116
105. S. Brugman, F.A. Klatter, J. Visser, N.A. Bos, D. Elias, and J. Rozing Neonatal oral administration of DiaPep277, combined with hydrolysed casein diet, protects against Type 1 diabetes in BB-DP rats. An experimental study Diabetologia 47 2004 1331 1333
106. F.W. Scott, P. Rowsell, G.S. Wang, K. Burghardt, H. Kolb, and S. Flohe Oral exposure to diabetes-promoting food or immunomodulators in neonates alters gut cytokines and diabetes Diabetes 51 2002 73 78
107. C.H. Hansen, L. Krych, D.S. Nielsen, F.K. Vogensen, L.H. Hansen, and S.J. Sorensen Early life treatment with vancomycin propagates Akkermansia muciniphila and reduces diabetes incidence in the NOD mouse Diabetologia 55 2012 2285 2294
108. F. Calcinaro, S. Dionisi, M. Marinaro, P. Candeloro, V. Bonato, and S. Marzotti Oral probiotic administration induces interleukin-10 production and prevents spontaneous autoimmune diabetes in the non-obese diabetic mouse Diabetologia 48 2005 1565 1575
109. S. Robert, C. Gysemans, T. Takiishi, H. Korf, I. Spagnuolo, and G. Sebastiani Oral delivery of glutamic acid decarboxylase (GAD)-65 and IL10 by Lactococcus lactis reverses diabetes in recent-onset NOD mice Diabetes 63 2014 2876 2887
110. T. Takiishi, H. Korf, T.L. Van Belle, S. Robert, F.A. Grieco, and S. Caluwaerts Reversal of autoimmune diabetes by restoration of antigen-specific tolerance using genetically modified Lactococcus lactis in mice J Clin Invest 122 2012 1717 1725
111. E. Allen-Vercoe, G. Reid, N. Viner, G.B. Gloor, S. Hota, and P. Kim A Canadian Working Group report on fecal microbial therapy: microbial ecosystems therapeutics Can J Gastroenterol 26 2012 457 462
112. E.O. Petrof, E.C. Claud, G.B. Gloor, and E. Allen-Vercoe Microbial ecosystems therapeutics: a new paradigm in medicine? Benef Microbes 4 2013 53 65