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Journal of Diabetes Research
Volume 2017 (2017), Article ID 9631435, 9 pages
https://doi.org/10.1155/2017/9631435
Review Article

Role of the Gastrointestinal Tract Microbiome in the Pathophysiology of Diabetes Mellitus

1Biomedical Research Center, Qatar University, P.O. Box 2713, Doha, Qatar
2Government College University, Faisalabad 38000, Pakistan
3College of Health Sciences, Qatar University, P.O. Box 2713, Doha, Qatar
4Institute of Cell Biology and Neurobiology (IBCN), Italian National Council of Research (CNR), Rome, Italy

Correspondence should be addressed to Muhammad U. Sohail; moc.liamg@liahosramurd

Received 24 May 2017; Accepted 24 August 2017; Published 26 September 2017

Academic Editor: Ponnusamy Saravanan

Copyright © 2017 Muhammad U. Sohail et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. A. J. McDermott and G. B. Huffnagle, “The microbiome and regulation of mucosal immunity,” Immunology, vol. 142, no. 1, pp. 24–31, 2014. View at Publisher · View at Google Scholar · View at Scopus
  2. L. Galland, “The gut microbiome and the brain,” Journal of Medicinal Food, vol. 17, no. 12, pp. 1261–1272, 2014. View at Publisher · View at Google Scholar · View at Scopus
  3. M. Carabotti, A. Scirocco, M. A. Maselli, and C. Severi, “The gut-brain axis: interactions between enteric microbiota, central and enteric nervous systems,” Annals of Gastroenterology: Quarterly Publication of the Hellenic Society of Gastroenterology, vol. 28, no. 2, pp. 203–209, 2015. View at Google Scholar
  4. J. M. Brown and S. L. Hazen, “The gut microbial endocrine organ: bacterially derived signals driving cardiometabolic diseases,” Annual Review of Medicine, vol. 66, pp. 343–359, 2015. View at Publisher · View at Google Scholar · View at Scopus
  5. C. L. Boulangé, A. L. Neves, J. Chilloux, J. K. Nicholson, and M. E. Dumas, “Impact of the gut microbiota on inflammation, obesity, and metabolic disease,” Genome Medicine, vol. 8, no. 1, p. 42, 2016. View at Publisher · View at Google Scholar · View at Scopus
  6. T. N. Kelly, L. A. Bazzano, N. J. Ajami et al., “Gut microbiome associates with lifetime cardiovascular disease risk profile among bogalusa heart study participants,” Circulation Research, vol. 119, 2016. View at Publisher · View at Google Scholar · View at Scopus
  7. T. M. Paras, F. Percival, and E. McQuade, “The gut microbiome influences arthritis development in IIJ mice,” The Journal of Immunology, vol. 196, 2016. View at Google Scholar
  8. S. P. Rosshart, B. G. Vassallo, D. Angeletti et al., “Wild mouse gut microbiome protects laboratory mice against lethal influenza virus infection and colorectal cancer,” The Journal of Immunology, vol. 198, 2017. View at Google Scholar
  9. C. D. Mathers and D. Loncar, “Projections of global mortality and burden of disease from 2002 to 2030,” PLoS Medicine, vol. 3, no. 11, article e442, 2006. View at Publisher · View at Google Scholar · View at Scopus
  10. L. P. Aiello and DCCT/EDIC Research Group, “Diabetic retinopathy and other ocular findings in the diabetes control and complications trial/epidemiology of diabetes interventions and complications study,” Diabetes Care, vol. 37, no. 1, pp. 17–23, 2014. View at Publisher · View at Google Scholar · View at Scopus
  11. C. L. Martin, J. W. Albers, R. Pop-Busui, and for the DCCT/EDIC Research Group, “Neuropathy and related findings in the diabetes control and complications trial/epidemiology of diabetes interventions and complications study,” Diabetes Care, vol. 37, no. 1, pp. 31–38, 2014. View at Publisher · View at Google Scholar · View at Scopus
  12. S. Brugman, F. A. Klatter, J. T. Visser 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, vol. 49, no. 9, pp. 2105–2108, 2006. View at Publisher · View at Google Scholar · View at Scopus
  13. J. F. Bach, “The effect of infections on susceptibility to autoimmune and allergic diseases,” New England Journal of Medicine, vol. 347, no. 12, pp. 911–920, 2002. View at Publisher · View at Google Scholar · View at Scopus
  14. B. Xie, M. J. Waters, and H. J. Schirra, “Investigating potential mechanisms of obesity by metabolomics,” BioMed Research International, vol. 2012, Article ID 805683, 10 pages, 2012. View at Publisher · View at Google Scholar · View at Scopus
  15. A. Wang, Z. Gu, B. Heid, R. M. Akers, and H. Jiang, “Identification and characterization of the bovine G protein-coupled receptor GPR41 and GPR43 genes,” Journal of Dairy Science, vol. 92, no. 6, pp. 2696–2705, 2009. View at Publisher · View at Google Scholar · View at Scopus
  16. E. Le Poul, C. Loison, S. Struyf et al., “Functional characterization of human receptors for short chain fatty acids and their role in polymorphonuclear cell activation,” Journal of Biological Chemistry, vol. 278, no. 28, pp. 25481–25489, 2003. View at Publisher · View at Google Scholar · View at Scopus
  17. G. Tolhurst, H. Heffron, Y. S. Lam et al., “Short-chain fatty acids stimulate glucagon-like peptide-1 secretion via the G-protein-coupled receptor FFAR2,” Diabetes, vol. 61, no. 2, pp. 364–371, 2012. View at Publisher · View at Google Scholar · View at Scopus
  18. L. V. Hooper, M. H. Wong, A. Thelin, L. Hansson, P. G. Falk, and J. I. Gordon, “Molecular analysis of commensal host-microbial relationships in the intestine,” Science, vol. 291, no. 5505, pp. 881–884, 2001. View at Publisher · View at Google Scholar · View at Scopus
  19. T. S. Stappenbeck, L. V. Hooper, and J. I. Gordon, “Developmental regulation of intestinal angiogenesis by indigenous microbes via Paneth cells,” Proceedings of the National Academy of Sciences, vol. 99, no. 24, pp. 15451–15455, 2002. View at Publisher · View at Google Scholar · View at Scopus
  20. A. Ibrahim, K. Mbodji, A. Hassan et al., “Anti-inflammatory and anti-angiogenic effect of long chain n-3 polyunsaturated fatty acids in intestinal microvascular endothelium,” Clinical Nutrition, vol. 30, no. 5, pp. 678–687, 2011. View at Publisher · View at Google Scholar · View at Scopus
  21. F. Bäckhed, J. K. Manchester, C. F. Semenkovich, and J. I. Gordon, “Mechanisms underlying the resistance to diet-induced obesity in germ-free mice,” Proceedings of the National Academy of Sciences, vol. 104, no. 3, pp. 979–984, 2007. View at Publisher · View at Google Scholar · View at Scopus
  22. D. R. Donohoe, N. Garge, X. Zhang et al., “The microbiome and butyrate regulate energy metabolism and autophagy in the mammalian colon,” Cell Metabolism, vol. 13, no. 5, pp. 517–526, 2011. View at Publisher · View at Google Scholar · View at Scopus
  23. V. A. Matheus, L. Monteiro, R. B. Oliveira, D. A. Maschio, and C. B. Collares-Buzato, “Butyrate reduces high-fat diet-induced metabolic alterations, hepatic steatosis and pancreatic beta cell and intestinal barrier dysfunctions in prediabetic mice,” Experimental Biology and Medicine, vol. 242, no. 12, pp. 1214–1226, 2017. View at Publisher · View at Google Scholar
  24. A. Everard, V. Lazarevic, M. Derrien et al., “Responses of gut microbiota and glucose and lipid metabolism to prebiotics in genetic obese and diet-induced leptin-resistant mice,” Diabetes, vol. 60, no. 11, pp. 2775–2786, 2011. View at Publisher · View at Google Scholar · View at Scopus
  25. P. D. Cani, E. Joly, Y. Horsmans, and N. M. Delzenne, “Oligofructose promotes satiety in healthy human: a pilot study,” European Journal of Clinical Nutrition, vol. 60, no. 5, pp. 567–572, 2006. View at Publisher · View at Google Scholar · View at Scopus
  26. X. Li, E. Wang, B. Yin et al., “Effects of Lactobacillus casei CCFM419 on insulin resistance and gut microbiota in type 2 diabetic mice,” Beneficial Microbes, vol. 8, pp. 421–432, 2017. View at Publisher · View at Google Scholar
  27. E. F. Murphy, P. D. Cotter, S. Healy et al., “Composition and energy harvesting capacity of the gut microbiota: relationship to diet, obesity and time in mouse models,” Gut, vol. 59, no. 12, pp. 1635–1642, 2010. View at Publisher · View at Google Scholar · View at Scopus
  28. P. J. Turnbaugh, F. Bäckhed, 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, vol. 3, no. 4, pp. 213–223, 2008. View at Publisher · View at Google Scholar · View at Scopus
  29. P. J. Turnbaugh, R. E. Ley, M. A. Mahowald, V. Magrini, E. R. Mardis, and J. I. Gordon, “An obesity-associated gut microbiome with increased capacity for energy harvest,” Nature, vol. 444, no. 7122, pp. 1027–1131, 2006. View at Publisher · View at Google Scholar · View at Scopus
  30. J. P. Després, I. Lemieux, J. Bergeron et al., “Abdominal obesity and the metabolic syndrome: contribution to global cardiometabolic risk,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 28, no. 6, pp. 1039–1049, 2008. View at Publisher · View at Google Scholar · View at Scopus
  31. J. R. Marchesi, D. H. Adams, F. Fava et al., “The gut microbiota and host health: a new clinical frontier,” Gut, vol. 65, no. 2, pp. 330–339, 2016. View at Publisher · View at Google Scholar · View at Scopus
  32. J. Ochoa-Repáraz, D. W. Mielcarz, Y. Wang et al., “A polysaccharide from the human commensal Bacteroides fragilis protects against CNS demyelinating disease,” Mucosal Immunology, vol. 3, no. 5, pp. 487–495, 2010. View at Publisher · View at Google Scholar · View at Scopus
  33. 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, vol. 122, no. 1, pp. 107–118, 2005. View at Publisher · View at Google Scholar · View at Scopus
  34. K. M. Maslowski, A. T. Vieira, A. Ng et al., “Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43,” Nature, vol. 461, no. 7268, pp. 1282–1286, 2009. View at Publisher · View at Google Scholar · View at Scopus
  35. P. D. Cani, R. Bibiloni, C. Knauf et al., “Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet-induced obesity and diabetes in mice,” Diabetes, vol. 57, no. 6, pp. 1470–1481, 2008. View at Publisher · View at Google Scholar · View at Scopus
  36. P. D. Cani, J. Amar, M. A. Iglesias et al., “Metabolic endotoxemia initiates obesity and insulin resistance,” Diabetes, vol. 56, no. 7, pp. 1761–1772, 2007. View at Publisher · View at Google Scholar · View at Scopus
  37. J. F. Tanti, F. Ceppo, J. Jager, and F. Berthou, “Implication of inflammatory signaling pathways in obesity-induced insulin resistance,” Obesity-Induced Inflammation and Insulin Resistance, vol. 3, no. 181, p. 6, 2015. View at Google Scholar
  38. D. M. Arrick and W. G. Mayhan, “Cerebrovascular disease in type 1 diabetes: role of oxidative stress,” in Studies in Diabetes, pp. 13–36, Springer, 2014. View at Publisher · View at Google Scholar
  39. L. Wen, R. E. Ley, P. Y. Volchkov et al., “Innate immunity and intestinal microbiota in the development of type 1 diabetes,” Nature, vol. 455, no. 7216, pp. 1109–1113, 2008. View at Publisher · View at Google Scholar · View at Scopus
  40. P. Bourlioux, B. Koletzko, F. Guarner, and V. Braesco, “The intestine and its microflora are partners for the protection of the host: report on the Danone Symposium “The Intelligent Intestine,” held in Paris, June 14, 2002,” The American Journal of Clinical Nutrition, vol. 78, no. 4, pp. 675–683, 2003. View at Google Scholar
  41. G. Musso, R. Gambino, and M. Cassader, “Interactions between gut microbiota and host metabolism predisposing to obesity and diabetes,” Annual Review of Medicine, vol. 62, pp. 361–380, 2011. View at Publisher · View at Google Scholar · View at Scopus
  42. C. T. Brown, A. G. Davis-Richardson, A. Giongo et al., “Gut microbiome metagenomics analysis suggests a functional model for the development of autoimmunity for type 1 diabetes,” PLoS One, vol. 6, no. 10, article e25792, 2011. View at Publisher · View at Google Scholar · View at Scopus
  43. A. Giongo, K. A. Gano, D. B. Crabb et al., “Toward defining the autoimmune microbiome for type 1 diabetes,” The ISME Journal, vol. 5, no. 1, pp. 82–91, 2011. View at Publisher · View at Google Scholar · View at Scopus
  44. N. Larsen, F. K. Vogensen, F. W. van den Berg et al., “Gut microbiota in human adults with type 2 diabetes differs from non-diabetic adults,” PLoS One, vol. 5, no. 2, article e9085, 2010. View at Publisher · View at Google Scholar · View at Scopus
  45. M. Murri, I. Leiva, J. M. Gomez-Zumaquero et al., “Gut microbiota in children with type 1 diabetes differs from that in healthy children: a case-control study,” BMC Medicine, vol. 11, no. 1, p. 46, 2013. View at Publisher · View at Google Scholar · View at Scopus
  46. J. Qin, Y. Li, Z. Cai et al., “A metagenome-wide association study of gut microbiota in type 2 diabetes,” Nature, vol. 490, no. 7418, pp. 55–60, 2012. View at Publisher · View at Google Scholar · View at Scopus
  47. Y. K. Lee, J. S. Menezes, Y. Umesaki, and S. K. Mazmanian, “Proinflammatory T-cell responses to gut microbiota promote experimental autoimmune encephalomyelitis,” Proceedings of the National Academy of Sciences, vol. 108, Supplement 1, pp. 4615–4622, 2011. View at Publisher · View at Google Scholar · View at Scopus
  48. S. Devaraj, P. Hemarajata, and J. Versalovic, “The human gut microbiome and body metabolism: implications for obesity and diabetes,” Clinical Chemistry, vol. 59, no. 4, pp. 617–628, 2013. View at Publisher · View at Google Scholar · View at Scopus
  49. X. C. Morgan, T. L. Tickle, H. Sokol et al., “Dysfunction of the intestinal microbiome in inflammatory bowel disease and treatment,” Genome Biology, vol. 13, no. 9, article R79, 2012. View at Publisher · View at Google Scholar · View at Scopus
  50. H. Yadav, S. Jain, and P. R. Sinha, “Oral administration of dahi containing probiotic Lactobacillus acidophilus and Lactobacillus casei delayed the progression of streptozotocin-induced diabetes in rats,” Journal of Dairy Research, vol. 75, no. 02, pp. 189–195, 2008. View at Publisher · View at Google Scholar · View at Scopus
  51. H. Wu, E. Esteve, V. Tremaroli et al., “Metformin alters the gut microbiome of individuals with treatment-naive type 2 diabetes, contributing to the therapeutic effects of the drug,” Nature Medicine, vol. 23, 2017. View at Publisher · View at Google Scholar
  52. S. Ussar, S. Fujisaka, and C. R. Kahn, “Interactions between host genetics and gut microbiome in diabetes and metabolic syndrome,” Molecular Metabolism, vol. 5, no. 9, pp. 795–803, 2016. View at Publisher · View at Google Scholar · View at Scopus
  53. J. Xu and J. I. Gordon, “Honor thy symbionts,” Proceedings of the National Academy of Sciences, vol. 100, no. 18, pp. 10452–10459, 2003. View at Publisher · View at Google Scholar · View at Scopus
  54. A. Everard and P. D. Cani, “Diabetes, obesity and gut microbiota,” Best Practice & Research Clinical Gastroenterology, vol. 27, no. 1, pp. 73–83, 2013. View at Publisher · View at Google Scholar · View at Scopus
  55. J. F. Tanti, F. Ceppo, J. Jager, and F. Berthou, “Implication of inflammatory signaling pathways in obesity-induced insulin resistance,” Frontiers in Endocrinology, vol. 3, 2012. View at Publisher · View at Google Scholar · View at Scopus
  56. N. M. Delzenne and P. D. Cani, “Gut microbiota and the pathogenesis of insulin resistance,” Current Diabetes Reports, vol. 11, no. 3, pp. 154–159, 2011. View at Publisher · View at Google Scholar · View at Scopus
  57. X. Wu, C. Ma, L. Han et al., “Molecular characterisation of the faecal microbiota in patients with type II diabetes,” Current Microbiology, vol. 61, no. 1, pp. 69–78, 2010. View at Publisher · View at Google Scholar · View at Scopus
  58. F. H. Karlsson, V. Tremaroli, I. Nookaew et al., “Gut metagenome in European women with normal, impaired and diabetic glucose control,” Nature, vol. 498, no. 7452, pp. 99–103, 2013. View at Publisher · View at Google Scholar · View at Scopus
  59. K. H. Allin, T. Nielsen, and O. Pedersen, “Mechanisms in endocrinology: gut microbiota in patients with type 2 diabetes mellitus,” European Journal of Endocrinology, vol. 172, no. 4, pp. R167–R177, 2015. View at Publisher · View at Google Scholar · View at Scopus
  60. 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,” Journal of Autoimmunity, vol. 53, pp. 85–94, 2014. View at Publisher · View at Google Scholar · View at Scopus