920
Views
58
CrossRef citations to date
0
Altmetric
Perspectives

The intricate association between gut microbiota and development of Type 1, Type 2 and Type 3 diabetes

, , &
Pages 1031-1041 | Published online: 10 Jan 2014

References

  • Qin J, Li R, Raes J et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464, 59–65 (2010).
  • Ackerman J. The ultimate social network. Sci. Am. 306, 36–43 (2012).
  • Cho I, Blaser MJ. The human microbiome: at the interface of health and disease. Nat. Rev. Genet. 13, 260–270 (2012).
  • Pugliese A. The multiple origins of Type 1 diabetes. Diabet. Med. 30, 135–146 (2013).
  • Shen J, Obin MS, Zhao L. The gut microbiota, obesity and insulin resistance. Mol. Aspects Med. 34, 39–58 (2013).
  • Bäckhed F. Programming of host metabolism by the gut microbiota. Ann. Nutr. Metab. 58, 44–52 (2011).
  • Buccigrossi V, Nicastro E, Guarino A. Intestinal microbiota composition in children. In: World Review of Nutrition and Dietetics (Volume 107), Probiotic Bacteria and Their Effect on Human Health and Well-Being. Guarino A, Quigley EMM, Walker WA ( Eds). Karger, Basel, 9–16 (2013).
  • Robles Alonso V and Guarner F. Intestinal microbiota composition in adults. In: World Review of Nutrition and Dietetics (Volume 107), Probiotic Bacteria and Their Effect on Human Health and Well-Being. Guarino A, Quigley EMM, Walker WA ( Eds). Karger, Basel, 17–24 (2013).
  • Arumugam M, Raes J, Pelletier E et al. Enterotypes of the human gut microbiome. Nature 473, 174–180 (2011).
  • Barrett E, Dinan TG, Cryan JF et al. Effects of the intestinal microbiota on behavior and brain biochemistry. In: World Review of Nutrition and Dietetics (Volume 107), Probiotic Bacteria and Their Effect on Human Health and Well-Being. Guarino A, Quigley EMM, Walker WA ( Eds). Karger, Basel, 56–63 (2013).
  • de Goffau MC, Luopajarvi K, Knip M et al. Fecal microbiota composition differs between children with beta-cell autoimmunity and those without. Diabetes 62, 1238–1244 (2013).
  • 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. 11, 46 (2013).
  • Beyan H, Wen L, Leslie RD. Guts, germs, and meals: the origin of type 1 diabetes. Curr. Diab. Rep. 12, 456–462 (2012).
  • Vaarala O. Is the origin of type 1 diabetes in the gut? Immunol. Cell Biol. 90, 271–276 (2012).
  • Hara N, Alkanani AK, Ir D et al. The role of the intestinal microbiota in type 1 diabetes. Clin. Immunol. 146, 112–119 (2013).
  • Fowler MJ. Microvascular and macrovascular complications of diabetes. Clin. Diabetes 29, 116–122 (2011).
  • Muller LM, Gorter KJ, Hak E et al. Increased risk of common infections in patients with type 1 and type 2 diabetes mellitus. Clin. Infect. Dis. 41, 281–288 (2005).
  • Green A, Patterson CC. Trends in the incidence of childhood-onset diabetes in Europe 1989-1998. Diabetologia 44, B3–B8 (2001).
  • Patterson CC, Dahlquist GG, Gyurus E, Green A, Soltesz G. Incidence trends for childhood type 1 diabetes in Europe during 1989-2003 and predicted new cases 2005-20: a multicentre prospective registration study. Lancet 373, 2027–2033 (2009).
  • Borchers AT, Uibo R, Gershwin ME. The geoepidemiology of type 1 diabetes. Autoimmun. Rev. 9, A355–A365 (2010).
  • Yeung WC, Rawlinson WD, Craig ME. Enterovirus infection and type 1 diabetes mellitus: systematic review and meta-analysis of observational molecular studies. BMJ 342, d35 (2011).
  • Filippi C, von Herrath M. How viral infections affect the autoimmune process leading to type 1 diabetes. Cell Immunol. 233, 125–132 (2005).
  • Svoren BM, Volkening LK, Wood JR, Laffel LM. Significant vitamin D deficiency in youth with type 1 diabetes mellitus. J. Pediatr. 154, 132–134 (2009).
  • Cooper JD, Smyth DJ, Walker NM et al. Inherited variation in vitamin D genes is associated with predisposition to autoimmune disease type 1 diabetes. Diabetes 60, 1624–1631 (2011).
  • Knip M, Virtanen SM, Becker D, Dupre J, Krischer JP, Akerblom HK. Early feeding and risk of type 1 diabetes: experiences from the Trial to Reduce Insulin-dependent diabetes mellitus in the Genetically at Risk (TRIGR). Am. J. Clin. Nutr. 94, 1814S–1820S (2011).
  • Patelarou E, Girvalaki C, Brokalaki H, Patelarou A, Androulaki Z, Vardavas C. Current evidence on the associations of breastfeeding, infant formula, and cow’s milk introduction with type 1 diabetes mellitus: a systematic review. Nutr. Rev. 70, 509–519 (2012).
  • Kukreja A, Maclaren NK. Current cases in which epitope mimicry is considered as a component cause of autoimmune disease: immune-mediated (type 1) diabetes. Cell Mol. Life Sci. 57, 534–541 (2000).
  • Patrick C, Wang GS, Lefebvre DE et al. Promotion of autoimmune diabetes by cereal diet in the presence or absence of microbes associated with gut immune activation, regulatory imbalance, and altered cathelicidin antimicrobial Peptide. Diabetes 62, 2036–2047 (2013).
  • Stene LC, Gale EA. The prenatal environment and type 1 diabetes. Diabetologia 56(9), 1888–1897 (2013).
  • Todd JA. Etiology of type 1 diabetes. Immunity 32, 457–467 (2010).
  • Biason-Lauber A, Boni-Schnetzler M, Hubbard BP et al. Identification of a SIRT1 mutation in a family with type 1 diabetes. Cell Metab. 17, 448–455 (2013).
  • Giongo A, Gano KA, Crabb DB et al. Toward defining the autoimmune microbiome for type 1 diabetes. ISME J. 5, 82–91 (2011).
  • Cebula A, Seweryn M, Rempala GA et al. Thymus-derived regulatory T cells contribute to tolerance to commensal microbiota. Nature 497, 258–262 (2013).
  • Romano-Keeler J, Weitkamp JH, Moore DJ. Regulatory properties of the intestinal microbiome effecting the development and treatment of diabetes. Curr. Opin. Endocrinol. Diabetes Obes. 19, 73–80 (2012).
  • Sonier B, Patrick C, Ajjikuttira P, Scott FW. Intestinal immune regulation as a potential diet modifiable feature of gut inflammation and autoimmunity. Int. Rev. Immunol. 28, 414–445 (2009).
  • Johansson ME, Ambort D, Pelaseyed T et al. Composition and functional role of the mucus layers in the intestine. Cell Mol. Life Sci. 68, 3635–3641 (2011).
  • Suzuki T. Regulation of intestinal epithelial permeability by tight junctions. Cell Mol. Life Sci. 70, 631–659 (2013).
  • Camilleri M, Madsen K, Spiller R, Greenwood-Van MB, Verne GN. Intestinal barrier function in health and gastrointestinal disease. J. Neurogastroenterol. Motil. 24, 503–512 (2012).
  • Su LF, Kidd BA, Han A, Kotzin JJ, Davis MM. Virus-specific CD4(+) memory-phenotype T cells are abundant in unexposed adults. Immunity 38, 373–383 (2013).
  • Wen L, Ley RE, Volchkov PY et al. Innate immunity and intestinal microbiota in the development of Type 1 diabetes. Nature 455, 1109–1113 (2008).
  • Hemmi H, Akira S. TLR signalling and the function of dendritic cells. Chem. Immunol. Allergy 86, 120–135 (2005).
  • Alam C, Bittoun E, Bhagwat D et al. Effects of a germ-free environment on gut immune regulation and diabetes progression in non-obese diabetic (NOD) mice. Diabetologia 54, 1398–1406 (2011).
  • King C, Sarvetnick N. The incidence of type-1 diabetes in NOD mice is modulated by restricted flora not germ-free conditions. PLoS ONE 6, e17049 (2011).
  • Markle JG, Frank DN, Mortin-Toth S et al. Sex differences in the gut microbiome drive hormone-dependent regulation of autoimmunity. Science 339, 1084–1088 (2013).
  • 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 48, 1565–1575 (2005).
  • Valladares R, Sankar D, Li N et al. Lactobacillus johnsonii N6.2 mitigates the development of type 1 diabetes in BB-DP rats. PLoS ONE 5, e10507 (2010).
  • Petrovsky N. Immunomodulation with microbial vaccines to prevent type 1 diabetes mellitus. Nat. Rev. Endocrinol. 6, 131–138 (2010).
  • Harrison LC. Vaccination against self to prevent autoimmune disease: the type 1 diabetes model. Immunol. Cell Biol. 86, 139–145 (2008).
  • Rijkers GT, Mulder L, Rombouts FM, Akkermans LMA. What is the future for therapies derived from the microbiome (pharmabiotics)? In: World Review of Nutrition and Dietetics (Volume 107), Probiotic Bacteria and Their Effect on Human Health and Well-Being. Guarino A, Quigley EMM, Walker WA ( Eds). Karger, Basel, 186–196 (2013).
  • Ley RE, Bäckhed F, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI. Obesity alters gut microbial ecology. Proc. Natl Acad. Sci. USA 102, 11070–11075 (2005).
  • Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI. An obesity associated gut microbiome with increased capacity for energy harvest. Nature 444, 1027–1031 (2006).
  • Ley RE, Turnbaugh PJ, Klein S, Gordon JI. Microbial ecology: human gut microbes associated with obesity. Nature 444, 1022–1023 (2006).
  • Schwiertz A, Taras D, Schafer K et al. Microbiota and SCFA in lean and overweight healthy subjects. Obesity (Silver. Spring) 18, 190–195 (2010).
  • Karlsson FH, Tremaroli V, Nookaew I et al. Gut metagenome in European women with normal, impaired and diabetic glucose control. Nature 498, 99–103 (2013).
  • Qin J, Li Y, Cai Z et al. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature 490, 55–60 (2012).
  • Kobayashi KS. Shaping intestinal bacterial community by TLR and NLR signaling. In: World Review of Nutrition and Dietetics (Volume 107), Probiotic Bacteria and Their Effect on Human Health and Well-Being. Guarino A, Quigley EMM, Walker WA ( Eds). Karger, Basel, 32–42 (2013).
  • Bäckhed F, Manchester JK, Semenkovich CF, Gordon JI. Mechanisms underlying the resistance to diet-induced obesity in germ-free mice. Proc. Natl Acad. Sci. USA 104, 979–984 (2007).
  • Jumpertz R, Le DS, Turnbaugh PJ et al. Energy-balance studies reveal associations between gut microbes, caloric load, and nutrient absorption in humans. Am. J. Clin. Nutr. 94, 58–65 (2011).
  • Tremaroli V, Bäckhed F. Functional interactions between the gut microbiota and host metabolism. Nature 489, 242–249 (2012).
  • Power SE, Fitzgerald GF, O’Toole PW et al. Metabolic syndrome and obesity in adults. In: World Review of Nutrition and Dietetics (Volume 107), Probiotic Bacteria and Their Effect on Human Health and Well-Being. Guarino A, Quigley EMM, Walker WA ( Eds). Karger, Basel, 103–121 (2013).
  • Bjursell M, Admyre T, Goransson M et al. Improved glucose control and reduced body fat mass in free fatty acid receptor 2-deficient mice fed a high-fat diet. Am. J. Physiol. Endocrinol. Metab. 300, E211–E220 (2011).
  • Cani PD, Osto M, Geurts L, Everard A. Involvement of gut microbiota in the development of low-grade inflammation and type 2 diabetes associated with obesity. Gut Microbes 3, 279–288 (2012).
  • Guo S, Al-Sadi R, Said HM, Ma TY. Lipopolysaccharide causes an increase in intestinal tight junction permeability in vitro and in vivo by inducing enterocyte membrane expression and localization of TLR-4 and CD14. Am. J. Pathol. 182, 375–387 (2013).
  • Teixeira TF, Collado MC, Ferreira CL, Bressan J, Peluzio MC. Potential mechanisms for the emerging link between obesity and increased intestinal permeability. Nutr. Res. 32, 637–647 (2012).
  • Moreno-Navarrete JM, Sabater M, Ortega F, Ricart W, Fernandez-Real JM. Circulating zonulin, a marker of intestinal permeability, is increased in association with obesity-associated insulin resistance. PLoS ONE 7, e37160 (2012).
  • Caesar R, Reigstad CS, Backhed HK et al. Gut-derived lipopolysaccharide augments adipose macrophage accumulation but is not essential for impaired glucose or insulin tolerance in mice. Gut 61, 1701–1707 (2012).
  • Liang H, Hussey SE, Sanchez-Avila A, Tantiwong P, Musi N. Effect of lipopolysaccharide on inflammation and insulin action in human muscle. PLoS ONE 8, e63983 (2013).
  • Schertzer JD, Tamrakar AK, Magalhaes JG et al. NOD1 activators link innate immunity to insulin resistance. Diabetes 60, 2206–2215 (2011).
  • Al-Daghri NM, Clerici M, Al-Attas O et al. A nonsense polymorphism (R392X) in TLR5 protects from obesity but predisposes to diabetes. J. Immunol. 190, 3716–3720 (2013).
  • Vijay-Kumar M, Aitken JD, Carvalho FA et al. Metabolic syndrome and altered gut microbiota in mice lacking Toll-like receptor 5. Science 328, 228–231 (2010).
  • Blohmke CJ, Park J, Hirschfeld AF et al. TLR5 as an anti-inflammatory target and modifier gene in cystic fibrosis. J. Immunol. 185, 7731–7738 (2010).
  • Franco BE, Altagracia MM, Sanchez Rodriguez MA, Wertheimer AI. The determinants of the antibiotic resistance process. Infect. Drug Resist. 2, 1–11 (2009).
  • Manichanh C, Reeder J, Gibert P et al. Reshaping the gut microbiome with bacterial transplantation and antibiotic intake. Genome Res. 20, 1411–1419 (2010).
  • Blaser M. Antibiotic overuse: stop the killing of beneficial bacteria. Nature 476, 393–394 (2011).
  • Ajslev TA, Andersen CS, Gamborg M, Sorensen TI, Jess T. Childhood overweight after establishment of the gut microbiota: the role of delivery mode, pre-pregnancy weight and early administration of antibiotics. Int. J. Obes. (Lond.) 35, 522–529 (2011).
  • Luoto R, Kalliomaki M, Laitinen K, Isolauri E. The impact of perinatal probiotic intervention on the development of overweight and obesity: follow-up study from birth to 10 years. Int. J. Obes. (Lond) 34, 1531–1537 (2010).
  • van Nood E, Vrieze A, Nieuwdorp M et al. Duodenal infusion of donor feces for recurrent Clostridium difficile. N. Engl. J. Med. 368, 407–415 (2013).
  • Vrieze A, van Nood E, Holleman F et al. Transfer of intestinal microbiota from lean donors increases insulin sensitivity in individuals with metabolic syndrome. Gastroenterology 143, 913–916 (2012).
  • Nicholson JK, Holmes E, Kinross J et al. Host-gut microbiota metabolic interactions. Science 336, 1262–1267 (2012).
  • Morelli L. Probiotics: definition and taxonomy 10 years after the FAO/WHO guidelines. In: World Review of Nutrition and Dietetics (Volume 107), Probiotic Bacteria and Their Effect on Human Health and Well-Being. Guarino A, Quigley EMM, Walker WA ( Eds). Karger, Basel, 1–8 (2013).
  • Patton TJ, Guandalini S. Are probiotic effects dose-related? In: World Review of Nutrition and Dietetics (Volume 107), Probiotic Bacteria and Their Effect on Human Health and Well-Being. Guarino A, Quigley EMM, Walker WA ( Eds). Karger, Basel, 151–160 (2013).
  • Million M, Angelakis E, Paul M, Armougom F, Leibovici L, Raoult D. Comparative meta-analysis of the effect of Lactobacillus species on weight gain in humans and animals. Microb. Pathog. 53, 100–108 (2012).
  • de Punder K, Pruimboom L. The dietary intake of wheat and other cereal grains and their role in inflammation. Nutrients 5, 771–787 (2013).
  • Roberfroid M. Prebiotics: the concept revisited. J. Nutr. 137, 830S–837S (2007).
  • Hvistendahl M. My microbiome and me. Science 336, 1248–1250 (2012).
  • Janson J, Laedtke T, Parisi JE, O’Brien P, Petersen RC, Butler PC. Increased risk of type 2 diabetes in Alzheimer disease. Diabetes 53, 474–481 (2004).
  • Talbot K, Wang HY, Kazi H et al. Demonstrated brain insulin resistance in Alzheimer’s disease patients is associated with IGF-1 resistance, IRS-1 dysregulation, and cognitive decline. J. Clin. Invest. 122, 1316–1338 (2012).
  • Bomfim TR, Forny-Germano L, Sathler LB et al. An anti-diabetes agent protects the mouse brain from defective insulin signaling caused by Alzheimer’s disease-associated Abeta oligomers. J. Clin. Invest. 122, 1339–1353 (2012).
  • Kaisaki PJ, Delepine M, Woon PY et al. Polymorphisms in type II SH2 domain-containing inositol 5-phosphatase (INPPL1, SHIP2) are associated with physiological abnormalities of the metabolic syndrome. Diabetes 53, 1900–1904 (2004).
  • Accardi G, Caruso C, Colonna-Romano G, Camarda C, Monastero R, Candore G. Can Alzheimer disease be a form of type 3 diabetes? Rejuvenation Res. 15, 217–221 (2012).
  • Lue LF, Andrade C, Sabbagh M, Walker D. Is there inflammatory synergy in Type II diabetes mellitus and Alzheimer's disease? Int. J. Alzheimers. Dis. 2012, 918680 (2012).
  • Arab L, Sadeghi R, Walker DG, Lue LF, Sabbagh MN. Consequences of aberrant insulin regulation in the brain: can treating diabetes be effective for Alzheimer’s Disease. Curr. Neuropharmacol. 9, 693–705 (2011).
  • Brenner SR. Blue-green algae or cyanobacteria in the intestinal micro-flora may produce neurotoxins such as beta-N-methylamino-l-alanine (BMAA) which may be related to development of amyotrophic lateral sclerosis, Alzheimer’s disease and Parkinson-Dementia-Complex in humans and Equine Motor Neuron Disease in horses. Med. Hypotheses 80, 103–103 (2013).
  • Forsythe P, Kunze WA, Bienenstock J. On communication between gut microbes and the brain. Curr. Opin. Gastroenterol. 28, 557–562 (2012).
  • Asemi Z, Khorrami-Rad A, Alizadeh SA, Shakeri H, Esmaillzadeh A. Effects of symbiotic food consumption on metabolic status of diabetic patients: a double-blind randomized crossover controlled clinical trial. Clin. Nutr. doi:10.1016/j.clnu.2013.05.015 (2013) ( Epub ahead of print).
  • Tillisch K, Labus J, Kilpatrick L et al. Consumption of fermented milk product with probiotic modulates brain activity. Gastroenterology 144, 1394–1401 (2013).

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.