Preview

Diabetes mellitus

Advanced search

The role of gut microbiota in metabolic regulation

https://doi.org/10.14341/DM7704

Abstract

Obesity and metabolic syndrome are among the major problems of modern society. The increase in obesity is associated with a corresponding increase in type 2 diabetes, cardiovascular disease and cancer. A huge amount of scientific research has been devoted to the development of methods to reduce obesity and its complications. In recent years, attention has shifted towards studying the intestinal microbiota not only as a possible component of the pathological process but also as a target of therapeutic intervention. Recent evidence, primarily from investigations in animal models, suggests that the intestinal microbiota affects nutrient acquisition and energy regulation. This review will discuss the role of the intestinal microbiota in metabolic processes as well as the latest developments on the improvement of disturbances specific to obesity and metabolic syndrome.

About the Authors

Ekaterina N. Kravchuk
Almazov North-West Medical Research Centre
Russian Federation
MD, PhD
Competing Interests: No conflict of interest


Alexander E. Neimark
Almazov North-West Medical Research Centre
Russian Federation
MD, PhD
Competing Interests: No conflict of interest


Elena N. Grineva
Almazov North-West Medical Research Centre
Russian Federation
MD, PhD
Competing Interests: No conflict of interest


Mikhail M. Galagudza
Almazov North-West Medical Research Centre
Russian Federation
MD, PhD
Competing Interests: No conflict of interest


References

1. Всемирная организация здравоохранения, Центр СМИ, Ожирение и избыточный вес, Информационный бюллетень N 311, пересмотр январь 2015 г. Available from: http://www.who.int/mediacentre/factsheets/fs311/ru/ [Worldhealthorganization, Obesityandoverweight, FactsheetN 311, Updated January 2015. Available from: http://www.who.int/mediacentre/factsheets/fs311/ru/ (in Russ)]

2. Zhang PY. Cardiovascular disease in diabetes. Eur Rev Med Pharmacol Sci. 2014;18(15):2205-2214.

3. Badrick E, Renehan AG. Diabetes and cancer: 5 years into the recent controversy. Eur J Cancer. 2014;50(12):2119-2125. doi: 10.1016/j.ejca.2014.04.032

4. Sjostrom L. Review of the key results from the Swedish Obese Subjects (SOS) trial – a prospective controlled intervention study of bariatric surgery. J Intern Med. 2013;273(3):219-234. doi: 10.1111/joim.12012

5. Cunningham JW, Wiviott SD. Modern obesity pharmacotherapy: weighing cardiovascular risk and benefit. Clin Cardiol. 2014;37(11):693-699. doi: 10.1002/clc.22304

6. Backhed F, Ding H, Wang T, et al. The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci U S A. 2004;101(44):15718-15723. doi: 10.1073/pnas.0407076101

7. von Engelhardt W, Bartels J, Kirschberger S, et al. Role of short-chain fatty acids in the hind gut. Vet Q. 1998;20(sup3):52-59. doi: 10.1080/01652176.1998.9694970

8. Le Poul E, Loison C, Struyf S, et al. Functional characterization of human receptors for short chain fatty acids and their role in polymorphonuclear cell activation. J Biol Chem. 2003;278(28):25481-25489. doi: 10.1074/jbc.M301403200

9. Vangaveti V, Shashidhar V, Jarrod G, et al. Free fatty acid receptors: emerging targets for treatment of diabetes and its complications. Ther Adv Endocrinol Metab. 2010;1(4):165-175. doi: 10.1177/2042018810381066

10. Chambers ES, Viardot A, Psichas A, et al. Effects of targeted delivery of propionate to the human colon on appetite regulation, body weight maintenance and adiposity in overweight adults. Gut.2015;64(11):1744-1754. doi: 10.1136/gutjnl-2014-307913

11. Sina C, Gavrilova O, Forster M, et al. G protein-coupled receptor 43 is essential for neutrophil recruitment during intestinal inflammation. J Immunol. 2009;183(11):7514-7522. doi: 10.4049/jimmunol.0900063

12. Maslowski KM, Vieira AT, Ng A, et al. Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43. Nature. 2009;461(7268):1282-1286. doi: 10.1038/nature08530

13. Tazoe H, Otomo Y, Karaki S-i, et al. Expression of short-chain fatty acid receptor GPR41 in the human colon. Biomed Res. 2009;30(3):149-156. doi: 10.2220/biomedres.30.149

14. Xiong Y, Miyamoto N, Shibata K, et al. Short-chain fatty acids stimulate leptin production in adipocytes through the G protein-coupled receptor GPR41. Proc Natl Acad Sci U S A. 2004;101(4):1045-1050. doi: 10.1073/pnas.2637002100

15. Kimura I, Inoue D, Maeda T, et al. Short-chain fatty acids and ketones directly regulate sympathetic nervous system via G protein-coupled receptor 41 (GPR41). Proc Natl Acad Sci U S A.2011;108(19):8030-8035. doi: 10.1073/pnas.1016088108

16. Høverstad T, Midtvedt T. Short-chain fatty acids in germfree mice and rats. J Nutr. 1986;116(9):1772-1776.

17. Gao Z, Yin J, Zhang J, et al. Butyrate improves insulin sensitivity and increases energy expenditure in mice. Diabetes. 2009;58(7):1509-1517. doi: 10.2337/db08-1637

18. Duncan SH, Belenguer A, Holtrop G, et al. Reduced dietary intake of carbohydrates by obese subjects results in decreased concentrations of butyrate and butyrate-producing bacteria in feces. Appl Environ Microbiol. 2007;73(4):1073-1078. doi: 10.1128/AEM.02340-06

19. Ichimura A, Hasegawa S, Kasubuchi M, Kimura I. Free fatty acid receptors as therapeutic targets for the treatment of diabetes. Front Pharmacol. 2014;5:236. doi: 10.3389/fphar.2014.00236

20. Zhang Y, Lee FY, Barrera G, et al. Activation of the nuclear receptor FXR improves hyperglycemia and hyperlipidemia in diabetic mice. Proc Natl Acad Sci U S A. 2006;103(4):1006-1011. doi: 10.1073/pnas.0506982103

21. Wei J, Qiu DK, Ma X. Bile acids and insulin resistance: implications for treating nonalcoholic fatty liver disease. J Dig Dis. 2009;10(2):85-90. doi: 10.1111/j.1751-2980.2009.00369.x

22. Kawamata Y, Fujii R, Hosoya M, et al. A G protein-coupled receptor responsive to bile acids. J Biol Chem. 2003;278(11):9435-9440. doi: 10.1074/jbc.M209706200

23. Vassileva G, Golovko A, Markowitz L, et al. Targeted deletion of Gpbar1 protects mice from cholesterol gallstone formation. Biochem J. 2006;398(3):423-430. doi: 10.1042/BJ20060537

24. Watanabe M, Houten SM, Mataki C, et al. Bile acids induce energy expenditure by promoting intracellular thyroid hormone activation. Nature. 2006;439(7075):484-489. doi: 10.1038/nature04330

25. Thomas C, Gioiello A, Noriega L, et al. TGR5-mediated bile acid sensing controls glucose homeostasis. Cell Metab. 2009;10(3):167-177. doi: 10.1016/j.cmet.2009.08.001

26. Keitel V. Endocrine and paracrine role of bile acids. World J Gastroenterol. 2008;14(37):5620. doi: 10.3748/wjg.14.5620

27. Madsen D, Beaver M, Chang L, et al. Analysis of bile acids in conventional and germfree rats. J Lipid Res. 1976;17:107–111.

28. Wostmann BS. Intestinal bile acids and cholesterol absorption in the germfree rat. J Nutr. 1973;103(7):982-990.

29. Sayin SI, Wahlstrom A, Felin J, et al. Gut microbiota regulates bile acid metabolism by reducing the levels of tauro-beta-muricholic acid, a naturally occurring FXR antagonist. Cell Metab.2013;17(2):225-235. doi: 10.1016/j.cmet.2013.01.003

30. Turnbaugh PJ, Backhed F, Fulton L, Gordon JI. Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host Microbe. 2008;3(4):213-223. doi: 10.1016/j.chom.2008.02.015

31. Ley RE, Turnbaugh PJ, Klein S, Gordon JI. Microbial ecology: human gut microbes associated with obesity. Nature. 2006;444(7122):1022-1023. doi: 10.1038/4441022a

32. Turnbaugh PJ, Hamady M, Yatsunenko T, et al. A core gut microbiome in obese and lean twins. Nature. 2009;457(7228):480-484. doi: 10.1038/nature07540

33. Duncan SH, Lobley GE, Holtrop G, et al. Human colonic microbiota associated with diet, obesity and weight loss. Int J Obes (Lond). 2008;32(11):1720-1724. doi: 10.1038/ijo.2008.155

34. Schwiertz A, Taras D, Schafer K, et al. Microbiota and SCFA in lean and overweight healthy subjects. Obesity (Silver Spring). 2010;18(1):190-195. doi: 10.1038/oby.2009.167

35. Backhed F, Manchester JK, Semenkovich CF, Gordon JI. Mechanisms underlying the resistance to diet-induced obesity in germ-free mice. Proc Natl Acad Sci U S A. 2007;104(3):979-984. doi: 10.1073/pnas.0605374104

36. Rabot S, Membrez M, Bruneau A, et al. Germ-free C57BL/6J mice are resistant to high-fat-diet-induced insulin resistance and have altered cholesterol metabolism. FASEB J. 2010;24(12):4948-4959. doi: 10.1096/fj.10-164921

37. Santacruz A, Marcos A, Warnberg J, et al. Interplay between weight loss and gut microbiota composition in overweight adolescents. Obesity (Silver Spring). 2009;17(10):1906-1915. doi: 10.1038/oby.2009.112

38. David LA, Maurice CF, Carmody RN, et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature. 2014;505(7484):559-563. doi: 10.1038/nature12820

39. Damms-Machado A, Mitra S, Schollenberger AE, et al. Effects of surgical and dietary weight loss therapy for obesity on gut microbiota composition and nutrient absorption. Biomed Res Int.2015;2015:806248. doi: 10.1155/2015/806248

40. 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. 2012;143(4):913-916 e917. doi: 10.1053/j.gastro.2012.06.031

41. Sweeney TE, Morton JM. Metabolic surgery: action via hormonal milieu changes, changes in bile acids or gut microbiota? A summary of the literature. Best Pract Res Clin Gastroenterol. 2014;28(4):727-740. doi: 10.1016/j.bpg.2014.07.016

42. Kong LC, Tap J, Aron-Wisnewsky J, et al. Gut microbiota after gastric bypass in human obesity: increased richness and associations of bacterial genera with adipose tissue genes. Am J Clin Nutr.2013;98(1):16-24. doi: 10.3945/ajcn.113.058743

43. Liou AP, Paziuk M, Luevano JM, Jr., et al. Conserved shifts in the gut microbiota due to gastric bypass reduce host weight and adiposity. Sci Transl Med. 2013;5(178):178ra141. doi: 10.1126/scitranslmed.3005687

44. Damms-Machado A, Mitra S, Schollenberger AE, et al. Effects of surgical and dietary weight loss therapy for obesity on gut microbiota composition and nutrient absorption. Biomed Res Int.2015;2015:806248. doi: 10.1155/2015/806248

45. De Sa Del Fiol F, Tardelli Ferreira AC, Marciano JJ, et al. Obesity and the use of antibiotics and probiotics in rats. Chemotherapy. 2014;60(3):162-167. doi: 10.1159/000371737

46. Hwang I, Park YJ, Kim YR, et al. Alteration of gut microbiota by vancomycin and bacitracin improves insulin resistance via glucagon-like peptide 1 in diet-induced obesity. FASEB J. 2015;29(6):2397-2411. doi: 10.1096/fj.14-265983

47. Dalpe-Scott M, Heick HM, Begin-Heick N. Oxytetracycline treatment improves the response to insulin in the spontaneously diabetic (BB) rat. Diabetes. 1982;31(1):53-59. doi: 10.2337/diabetes.31.1.53

48. Thuny F, Richet H, Casalta JP, et al. Vancomycin treatment of infective endocarditis is linked with recently acquired obesity. PLoS One. 2010;5(2):e9074. doi: 10.1371/journal.pone.0009074

49. Vrieze A, Out C, Fuentes S, et al. Impact of oral vancomycin on gut microbiota, bile acid metabolism, and insulin sensitivity. J Hepatol. 2014;60(4):824-831. doi: 10.1016/j.jhep.2013.11.034

50. Попова П.В., Рязанцева Е.М., Зазерская И.Е. и др. Восстановление менструальной функции в результате терапии метформином у женщин с синдромом поликистозных яичников // Проблемы женского здоровья. – 2010. – Т. 5. – № 3. – С. 11–17. [Popova PV, Ryazantseva EM, Zazerskaya IУ, et al. Restoration of menstrual function as a result of treatment with metformin in women with polycystic ovary syndrome. Problemi genskogo zdorozia. 2010;3(5):11-17. (in Russ).]


Supplementary files

Review

For citations:


Kravchuk E.N., Neimark A.E., Grineva E.N., Galagudza M.M. The role of gut microbiota in metabolic regulation. Diabetes mellitus. 2016;19(4):280-285. (In Russ.) https://doi.org/10.14341/DM7704

Views: 2225


ISSN 2072-0351 (Print)
ISSN 2072-0378 (Online)