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Reviews in Endocrine and Metabolic Disorders

, Volume 15, Issue 3, pp 189–196 | Cite as

Gut microbiota and GLP-1

  • Amandine Everard
  • Patrice D. CaniEmail author
Article

Abstract

A large body of evidence suggests that the regulation of energy balance and glucose homeostasis by fermentable carbohydrates induces specific changes in the gut microbiota. Among the mechanisms, our research group and others have demonstrated that the gut microbiota fermentation (i.e., bacterial digestion of specific compounds) of specific prebiotics or other non-digestible carbohydrates is associated with the secretion of enteroendocrine peptides, such as the glucagon-like peptide-1 (GLP-1) and peptide YY (PYY), produced by L-cells. In this review, we highlight past and recent results describing how dietary manipulation of the gut microbiota, using nutrients or specific microbes, can stimulate GLP-1 secretion in rodents and humans. Furthermore, the purpose of this review is to discuss the putative mechanisms by which specific bacterial metabolites, such as short chain fatty acids, trigger GLP-1 secretion through GPR41/43-dependent mechanisms. Moreover, we conclude by discussing the molecular advance showing that the endocannabinoid system or related bioactive lipids modulated by the gut microbiota may contribute to the regulation of glucose, lipid and energy homeostasis.

Keywords

Gut microbiota GLP-1 L-cells Endocannabinoids Prebiotics 

Notes

Acknowledgments

P. D. Cani is a research associate from the FRS-FNRS (Fonds de la Recherche Scientifique) and a recipient of grants from the FNRS and PDR (projet de recherche, Belgium) and ARC (Concerted Research Activities–French Community of Belgium convention: 12/17-047). Moreover, P. D. Cani is a recipient of the ERC Starting Grant 2013 (European Research Council, Starting grant 336452-ENIGMO). A.E. is a research fellow from the FRS-FNRS.

Conflict of interest

None of the authors have conflict of interest to declare in relation with the content of this manuscript.

References

  1. 1.
    Eri R, Chieppa M. Messages from the Inside. The Dynamic Environment that Favors Intestinal Homeostasis. Frontiers in immunol. 2013;4:323. doi: 10.3389/fimmu.2013.00323.Google Scholar
  2. 2.
    Costello EK, Lauber CL, Hamady M, Fierer N, Gordon JI, Knight R. Bacterial community variation in human body habitats across space and time. Science. 2009;326(5960):1694–7. doi: 10.1126/science.1177486.PubMedCentralPubMedGoogle Scholar
  3. 3.
    Reinhardt C, Reigstad CS, Backhed F. Intestinal microbiota during infancy and its implications for obesity. J Pediatr Gastroenterol Nutr. 2009;48(3):249–56.PubMedGoogle Scholar
  4. 4.
    Savage DC. Microbial ecology of the gastrointestinal tract. Annu Rev Microbiol. 1977;31:107–33.PubMedGoogle Scholar
  5. 5.
    Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C, et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature. 2010;464(7285):59–65.PubMedCentralPubMedGoogle Scholar
  6. 6.
    Rajilic-Stojanovic M, Heilig HG, Molenaar D, Kajander K, Surakka A, Smidt H, et al. Development and application of the human intestinal tract chip, a phylogenetic microarray: Analysis of universally conserved phylotypes in the abundant microbiota of young and elderly adults. Environ Microbiol. 2009;11(7):1736–51.PubMedCentralPubMedGoogle Scholar
  7. 7.
    Cheng J, Palva AM, de Vos WM, Satokari R. Contribution of the intestinal microbiota to human health: From birth to 100 years of age. Curr Top Microbiol Immunol. 2013;358:323–46. doi: 10.1007/82_2011_189.PubMedGoogle Scholar
  8. 8.
    Claesson MJ, Jeffery IB, Conde S, Power SE, O’Connor EM, Cusack S, et al. Gut microbiota composition correlates with diet and health in the elderly. Nature. 2012;488(7410):178–84. doi: 10.1038/nature11319.PubMedGoogle Scholar
  9. 9.
    Turnbaugh PJ, Hamady M, Yatsunenko T, Cantarel BL, Duncan A, Ley RE, et al. A core gut microbiome in obese and lean twins. Nature. 2009;457(7228):480–4.PubMedCentralPubMedGoogle Scholar
  10. 10.
    Consortium THMP. Structure, function and diversity of the healthy human microbiome. Nature. 2012;486(7402):207–14. doi: 10.1038/nature11234.Google Scholar
  11. 11.
    Mondot S, de Wouters T, Dore J, Lepage P. The human gut microbiome and its dysfunctions. Dig Dis. 2013;31(3–4):278–85. doi: 10.1159/000354678.PubMedGoogle Scholar
  12. 12.
    Rajilic-Stojanovic M. Function of the microbiota. Best Pract Res Clin Gastroenterol. 2013;27(1):5–16. doi: 10.1016/j.bpg.2013.03.006.PubMedGoogle Scholar
  13. 13.
    Everard A, Cani PD. Diabetes, obesity and gut microbiota. Best Pract Res Clin Gastroenterol. 2013;27(1):73–83. doi: 10.1016/j.bpg.2013.03.007.PubMedGoogle Scholar
  14. 14.
    Cani PD, Delzenne NM. The role of the gut microbiota in energy metabolism and metabolic disease. Curr Pharm Des. 2009;15(13):1546–58.PubMedGoogle Scholar
  15. 15.
    Tremaroli V, Backhed F. Functional interactions between the gut microbiota and host metabolism. Nature. 2012;489(7415):242–9. doi: 10.1038/nature11552.PubMedGoogle Scholar
  16. 16.
    Round JL, Mazmanian SK. The gut microbiota shapes intestinal immune responses during health and disease. Nat Rev Immunol. 2009;9(5):313–23.PubMedCentralPubMedGoogle Scholar
  17. 17.
    LeBlanc JG, Milani C, de Giori GS, Sesma F, van Sinderen D, Ventura M. Bacteria as vitamin suppliers to their host: a gut microbiota perspective. Curr Opin Biotechnol. 2013;24(2):160–8. doi: 10.1016/j.copbio.2012.08.005.PubMedGoogle Scholar
  18. 18.
    Flint HJ, Scott KP, Louis P, Duncan SH. The role of the gut microbiota in nutrition and health. Nat Rev Gastroenterol Hepatol. 2012;9(10):577–89. doi: 10.1038/nrgastro.2012.156.PubMedGoogle Scholar
  19. 19.
    Cani PD, Amar J, Iglesias MA, Poggi M, Knauf C, Bastelica D, et al. Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes. 2007;56(7):1761–72.PubMedGoogle Scholar
  20. 20.
    Backhed F, Ding H, Wang T, Hooper LV, Koh GY, Nagy A, et al. The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci USA. 2004;101(44):15718–23.PubMedCentralPubMedGoogle Scholar
  21. 21.
    Holmes E, Li JV, Marchesi JR, Nicholson JK. Gut microbiota composition and activity in relation to host metabolic phenotype and disease risk. Cell Metab. 2012;16(5):559–64. doi: 10.1016/j.cmet.2012.10.007.PubMedGoogle Scholar
  22. 22.
    Cani PD, Everard A, Duparc T. Gut microbiota, enteroendocrine functions and metabolism. Curr Opin Pharmacol. 2013;13(6):935–40.PubMedGoogle Scholar
  23. 23.
    Cho SS, Qi L, Fahey Jr GC, Klurfeld DM. Consumption of cereal fiber, mixtures of whole grains and bran, and whole grains and risk reduction in type 2 diabetes, obesity, and cardiovascular disease. Am J Clin Nutr. 2013;98(2):594–619. doi: 10.3945/ajcn.113.067629.PubMedGoogle Scholar
  24. 24.
    Slavin J. Fiber and prebiotics: Mechanisms and health benefits. Nutr. 2013;5(4):1417–35. doi: 10.3390/nu5041417.Google Scholar
  25. 25.
    Delzenne NM, Neyrinck AM, Cani PD. Gut microbiota and metabolic disorders: How prebiotic can work? Br J Nutr. 2013;109 Suppl 2:S81–5. doi: 10.1017/S0007114512004047.PubMedGoogle Scholar
  26. 26.
    Petschow B, Dore J, Hibberd P, Dinan T, Reid G, Blaser M, et al. Probiotics, prebiotics, and the host microbiome: The science of translation. Ann N Y Acad Sci. 2013;22(10):12303.Google Scholar
  27. 27.
    Birt DF, Boylston T, Hendrich S, Jane JL, Hollis J, Li L, et al. Resistant starch: Promise for improving human health. Adv Nutr. 2013;4(6):587–601. doi: 10.3945/an.113.004325.PubMedGoogle Scholar
  28. 28.
    Slavin JL, Savarino V, Paredes-Diaz A, Fotopoulos G. A review of the role of soluble fiber in health with specific reference to wheat dextrin. J Int Med Res. 2009;37(1):1–17.PubMedGoogle Scholar
  29. 29.
    Neyrinck AM, Delzenne NM. Potential interest of gut microbial changes induced by non-digestible carbohydrates of wheat in the management of obesity and related disorders. CurrOpinClinNutrMetab Care. 2010Google Scholar
  30. 30.
    Geurts L, Neyrinck AM, Delzenne NM, Knauf C, Cani PD. Gut microbiota controls adipose tissue expansion, gut barrier and glucose metabolism: novel insights into molecular targets and interventions using prebiotics. Beneficial microbes. 2013:1–15. doi: 10.3920/BM2012.0065
  31. 31.
    Flint HJ. The impact of nutrition on the human microbiome. Nutr Rev. 2012;70 Suppl 1:S10–3. doi: 10.1111/j.1753-4887.2012.00499.x.PubMedGoogle Scholar
  32. 32.
    Goodlad RA, Lenton W, Ghatei MA, Adrian TE, Bloom SR, Wright NA. Effects of an elemental diet, inert bulk and different types of dietary fibre on the response of the intestinal epithelium to refeeding in the rat and relationship to plasma gastrin, enteroglucagon, and PYY concentrations. Gut. 1987;28(2):171–80.PubMedCentralPubMedGoogle Scholar
  33. 33.
    Sinclair EM, Drucker DJ. Proglucagon-derived peptides: Mechanisms of action and therapeutic potential. Physiology (Bethesda). 2005;20:357–65. doi: 10.1152/physiol.00030.2005.Google Scholar
  34. 34.
    Longo WE, Ballantyne GH, Savoca PE, Adrian TE, Bilchik AJ, Modlin IM. Short-chain fatty acid release of peptide YY in the isolated rabbit distal colon. Scand J Gastroenterol. 1991;26(4):442–8.PubMedGoogle Scholar
  35. 35.
    Gee JM, Lee-Finglas W, Wortley GW, Johnson IT. Fermentable carbohydrates elevate plasma enteroglucagon but high viscosity is also necessary to stimulate small bowel mucosal cell proliferation in rats. J Nutr. 1996;126(2):373–9.PubMedGoogle Scholar
  36. 36.
    Reimer RA, McBurney MI. Dietary fiber modulates intestinal proglucagon messenger ribonucleic acid and postprandial secretion of glucagon-like peptide-1 and insulin in rats. Endocrinology. 1996;137(9):3948–56.PubMedGoogle Scholar
  37. 37.
    Gibson GR, Roberfroid MB. Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J Nutr. 1995;125(6):1401–12.PubMedGoogle Scholar
  38. 38.
    Roberfroid M, Gibson GR, Hoyles L, McCartney AL, Rastall R, Rowland I, et al. Prebiotic effects: Metabolic and health benefits. Br J Nutr. 2010;104(S2):S1–S63.PubMedGoogle Scholar
  39. 39.
    Kok NN, Morgan LM, Williams CM, Roberfroid MB, Thissen JP, Delzenne NM. Insulin, glucagon-like peptide 1, glucose-dependent insulinotropic polypeptide and insulin-like growth factor I as putative mediators of the hypolipidemic effect of oligofructose in rats. J Nutr. 1998;128(7):1099–103.PubMedGoogle Scholar
  40. 40.
    Cani PD, Dewever C, Delzenne NM. Inulin-type fructans modulate gastrointestinal peptides involved in appetite regulation (glucagon-like peptide-1 and ghrelin) in rats. Br J Nutr. 2004;92(3):521–6.PubMedGoogle Scholar
  41. 41.
    Cani PD, Montoya ML, Neyrinck AM, Delzenne NM, Lambert DM. Potential modulation of plasma ghrelin and glucagon-like peptide-1 by anorexigenic cannabinoid compounds, SR141716A (rimonabant) and oleoylethanolamide. Br J Nutr. 2004;92(5):757–61.PubMedGoogle Scholar
  42. 42.
    Cani PD, Neyrinck AM, Maton N, Delzenne NM. Oligofructose promotes satiety in rats fed a high-fat diet: Involvement of glucagon-like Peptide-1. Obes Res. 2005;13(6):1000–7.PubMedGoogle Scholar
  43. 43.
    Delzenne NM, Cani PD, Daubioul C, Neyrinck AM. Impact of inulin and oligofructose on gastrointestinal peptides. Br J Nutr. 2005;93 Suppl 1:S157–S61.PubMedGoogle Scholar
  44. 44.
    Cani PD, Knauf C, Iglesias MA, Drucker DJ, Delzenne NM, Burcelin R. Improvement of glucose tolerance and hepatic insulin sensitivity by oligofructose requires a functional glucagon-like peptide 1 receptor. Diabetes. 2006;55(5):1484–90.PubMedGoogle Scholar
  45. 45.
    Cani PD, Possemiers S, Van de WT, Guiot Y, Everard A, Rottier O, et al. Changes in gut microbiota control inflammation in obese mice through a mechanism involving GLP-2-driven improvement of gut permeability. Gut. 2009;58:1091–103.PubMedCentralPubMedGoogle Scholar
  46. 46.
    Aziz AA, Kenney LS, Goulet B, Abdel-Aal E. Dietary starch type affects body weight and glycemic control in freely fed but not energy-restricted obese rats. J Nutr. 2009;139(10):1881–9.PubMedGoogle Scholar
  47. 47.
    Charrier JA, Martin RJ, McCutcheon KL, Raggio AM, Goldsmith F, Goita M, et al. High fat diet partially attenuates fermentation responses in rats fed resistant starch from high-amylose maize. Obesity (Silver Spring). 2013. doi: 10.1002/oby.20362.Google Scholar
  48. 48.
    Keenan MJ, Zhou J, McCutcheon KL, Raggio AM, Bateman HG, Todd E, et al. Effects of resistant starch, a non-digestible fermentable fiber, on reducing body fat. Obesity (SilverSpring). 2006;14(9):1523–34.Google Scholar
  49. 49.
    Shen L, Keenan MJ, Martin RJ, Tulley RT, Raggio AM, McCutcheon KL, et al. Dietary resistant starch increases hypothalamic POMC expression in rats. Obesity (SilverSpring). 2009;17(1):40–5.Google Scholar
  50. 50.
    Zhou J, Hegsted M, McCutcheon KL, Keenan MJ, Xi X, Raggio AM, et al. Peptide YY and proglucagon mRNA expression patterns and regulation in the gut. Obesity (SilverSpring). 2006;14(4):683–9.Google Scholar
  51. 51.
    Zhou J, Martin RJ, Tulley RT, Raggio AM, McCutcheon KL, Shen L, et al. Dietary resistant starch upregulates total GLP-1 and PYY in a sustained day-long manner through fermentation in rodents. Am J Physiol Endocrinol Metab. 2008;295(5):E1160–E6.PubMedCentralPubMedGoogle Scholar
  52. 52.
    Neyrinck AM, Van Hee VF, Piront N, De Backer F, Toussaint O, Cani PD, et al. Wheat-derived arabinoxylan oligosaccharides with prebiotic effect increase satietogenic gut peptides and reduce metabolic endotoxemia in diet-induced obese mice. Nutr & diabetes. 2012;2:e28. doi: 10.1038/nutd.2011.24.Google Scholar
  53. 53.
    Parnell JA, Reimer RA. Prebiotic fibres dose-dependently increase satiety hormones and alter Bacteroidetes and Firmicutes in lean and obese JCR:LA-cp rats. Br J Nutr. 2012;107(4):601–13. doi: 10.1017/S0007114511003163.PubMedGoogle Scholar
  54. 54.
    Maurer AD, Eller LK, Hallam MC, Taylor K, Reimer RA. Consumption of diets high in prebiotic fiber or protein during growth influences the response to a high fat and sucrose diet in adulthood in rats. NutrMetab (Lond). 2010;7:77.Google Scholar
  55. 55.
    Parnell JA, Reimer RA. Differential secretion of satiety hormones with progression of obesity in JCR:LA-corpulent rats. Obesity (SilverSpring). 2008;16(4):736–42.Google Scholar
  56. 56.
    Ropert A, Cherbut C, Roze C, Le Quellec A, Holst JJ, Fu-Cheng X, et al. Colonic fermentation and proximal gastric tone in humans. Gastroenterology. 1996;111(2):289–96.PubMedGoogle Scholar
  57. 57.
    Piche T, des Varannes SB, Sacher-Huvelin S, Holst JJ, Cuber JC, Galmiche JP. Colonic fermentation influences lower esophageal sphincter function in gastroesophageal reflux disease. Gastroenterology. 2003;124(4):894–902.PubMedGoogle Scholar
  58. 58.
    Archer BJ, Johnson SK, Devereux HM, Baxter AL. Effect of fat replacement by inulin or lupin-kernel fibre on sausage patty acceptability, post-meal perceptions of satiety and food intake in men. Br J Nutr. 2004;91(4):591–9.PubMedGoogle Scholar
  59. 59.
    Whelan K, Efthymiou L, Judd PA, Preedy VR, Taylor MA. Appetite during consumption of enteral formula as a sole source of nutrition: The effect of supplementing pea-fibre and fructo-oligosaccharides. Br J Nutr. 2006;96(2):350–6.PubMedGoogle Scholar
  60. 60.
    Cani PD, Joly E, Horsmans Y, Delzenne NM. Oligofructose promotes satiety in healthy human: A pilot study. Eur J Clin Nutr. 2006;60(5):567–72.PubMedGoogle Scholar
  61. 61.
    Cani PD, Lecourt E, Dewulf EM, Sohet FM, Pachikian BD, Naslain D, et al. Gut microbiota fermentation of prebiotics increases satietogenic and incretin gut peptide production with consequences for appetite sensation and glucose response after a meal. Am J Clin Nutr. 2009;90(5):1236–43.PubMedGoogle Scholar
  62. 62.
    Parnell JA, Reimer RA. Weight loss during oligofructose supplementation is associated with decreased ghrelin and increased peptide YY in overweight and obese adults. Am J Clin Nutr. 2009;89(6):1751–9.PubMedGoogle Scholar
  63. 63.
    Peters HP, Boers HM, Haddeman E, Melnikov SM, Qvyjt F. No effect of added beta-glucan or of fructooligosaccharide on appetite or energy intake. Am J Clin Nutr. 2009;89(1):58–63.PubMedGoogle Scholar
  64. 64.
    Tarini J, Wolever TM. The fermentable fibre inulin increases postprandial serum short-chain fatty acids and reduces free-fatty acids and ghrelin in healthy subjects. Appl Physiol Nutr Metab. 2010;35(1):9–16.PubMedGoogle Scholar
  65. 65.
    Klosterbuer AS, Thomas W, Slavin JL. Resistant starch and pullulan reduce postprandial glucose, insulin, and GLP-1, but have no effect on satiety in healthy humans. J Agric Food Chem. 2012;60(48):11928–34. doi: 10.1021/jf303083r.PubMedGoogle Scholar
  66. 66.
    Frost G, Brynes A, Leeds A. Effect of large bowel fermentation on insulin, glucose, free fatty acids, and glucagon-like peptide 1 (7–36) amide in patients with coronary heart disease. Nutrition. 1999;15(3):183–8.PubMedGoogle Scholar
  67. 67.
    Bird AR, Conlon MA, Christophersen CT, Topping DL. Resistant starch, large bowel fermentation and a broader perspective of prebiotics and probiotics. Benefic microbes. 2010;1(4):423–31. doi: 10.3920/BM2010.0041.Google Scholar
  68. 68.
    Robertson MD. Dietary-resistant starch and glucose metabolism. Curr Opin Clin Nutr Metab Care. 2012;15(4):362–7. doi: 10.1097/MCO.0b013e3283536931.PubMedGoogle Scholar
  69. 69.
    Nilsson A, Johansson E, Ekstrom L, Bjorck I. Effects of a brown beans evening meal on metabolic risk markers and appetite regulating hormones at a subsequent standardized breakfast: A randomized cross-over study. PLoS One. 2013;8(4):e59985. doi: 10.1371/journal.pone.0059985.PubMedCentralPubMedGoogle Scholar
  70. 70.
    Bergman EN. Energy contributions of volatile fatty acids from the gastrointestinal tract in various species. Physiol Rev. 1990;70(2):567–90.PubMedGoogle Scholar
  71. 71.
    Ley RE, Turnbaugh PJ, Klein S, Gordon JI. Microbial ecology: Human gut microbes associated with obesity. Nature. 2006;444(7122):1022–3.PubMedGoogle Scholar
  72. 72.
    Le Poul E, Loison C, Struyf S, Springael JY, Lannoy V, Decobecq ME, 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):25481–9. doi: 10.1074/jbc.M301403200.PubMedGoogle Scholar
  73. 73.
    Brown AJ, Goldsworthy SM, Barnes AA, Eilert MM, Tcheang L, Daniels D, et al. The orphan G protein-coupled receptors GPR41 and GPR43 are activated by propionate and other short chain carboxylic acids. J Biol Chem. 2003;278(13):11312–9.PubMedGoogle Scholar
  74. 74.
    Nohr MK, Pedersen MH, Gille A, Egerod KL, Engelstoft MS, Husted AS, et al. GPR41/FFAR3 and GPR43/FFAR2 as cosensors for short-chain fatty acids in enteroendocrine cells vs FFAR3 in enteric neurons and FFAR2 in enteric leukocytes. Endocrinology. 2013;154(10):3552–64. doi: 10.1210/en.2013-1142.PubMedGoogle Scholar
  75. 75.
    Gribble FM. RD Lawrence Lecture 2008: Targeting GLP-1 release as a potential strategy for the therapy of Type 2 diabetes. Diabet med : a j of the British Diabet Assoc. 2008;25(8):889–94. doi: 10.1111/j.1464-5491.2008.02514.x.Google Scholar
  76. 76.
    Samuel BS, Shaito A, Motoike T, Rey FE, Backhed F, Manchester JK, et al. Effects of the gut microbiota on host adiposity are modulated by the short-chain fatty-acid binding G protein-coupled receptor, Gpr41. Proc Natl Acad Sci USA. 2008;105(43):16767–72.PubMedCentralPubMedGoogle Scholar
  77. 77.
    Tolhurst G, Heffron H, Lam YS, Parker HE, Habib AM, Diakogiannaki E, et al. Short-chain fatty acids stimulate glucagon-like peptide-1 secretion via the g-protein-coupled receptor ffar2. Diabetes. 2012;61(2):364–71.PubMedCentralPubMedGoogle Scholar
  78. 78.
    Wichmann A, Allahyar A, Greiner TU, Plovier H, Lunden GO, Larsson T, et al. Microbial modulation of energy availability in the colon regulates intestinal transit. Cell Host Microbe. 2013;14(5):582–90. doi: 10.1016/j.chom.2013.09.012.PubMedGoogle Scholar
  79. 79.
    Freeland KR, Wilson C, Wolever TM. Adaptation of colonic fermentation and glucagon-like peptide-1 secretion with increased wheat fibre intake for 1 year in hyperinsulinaemic human subjects. Br J Nutr. 2010;103(1):82–90.PubMedGoogle Scholar
  80. 80.
    Freeland KR, Wolever TM. Acute effects of intravenous and rectal acetate on glucagon-like peptide-1, peptide YY, ghrelin, adiponectin and tumour necrosis factor-alpha. Br J Nutr. 2010;103(3):460–6.PubMedGoogle Scholar
  81. 81.
    Zaibi MS, Stocker CJ, O’Dowd J, Davies A, Bellahcene M, Cawthorne MA, et al. Roles of GPR41 and GPR43 in leptin secretory responses of murine adipocytes to short chain fatty acids. FEBS Lett. 2010;584(11):2381–6.PubMedGoogle Scholar
  82. 82.
    Xiong Y, Miyamoto N, Shibata K, Valasek MA, Motoike T, Kedzierski RM, et al. Short-chain fatty acids stimulate leptin production in adipocytes through the G protein-coupled receptor GPR41. Proc Natl Acad Sci USA. 2004;101(4):1045–50.PubMedCentralPubMedGoogle Scholar
  83. 83.
    Lin HV, Frassetto A, Kowalik Jr EJ, Nawrocki AR, Lu MM, Kosinski JR, et al. Butyrate and propionate protect against diet-induced obesity and regulate gut hormones via free fatty acid receptor 3-independent mechanisms. PLoS One. 2012;7(4):e35240. doi: 10.1371/journal.pone.0035240.PubMedCentralPubMedGoogle Scholar
  84. 84.
    Bellahcene M, O’Dowd JF, Wargent ET, Zaibi MS, Hislop DC, Ngala RA, et al. Male mice that lack the G-protein-coupled receptor GPR41 have low energy expenditure and increased body fat content. Br J Nutr. 2013;109(10):1755–64. doi: 10.1017/S0007114512003923.PubMedGoogle Scholar
  85. 85.
    Kimura I, Ozawa K, Inoue D, Imamura T, Kimura K, Maeda T, et al. The gut microbiota suppresses insulin-mediated fat accumulation via the short-chain fatty acid receptor GPR43. Nat Commun. 2013;4:1829. doi: 10.1038/ncomms2852.PubMedCentralPubMedGoogle Scholar
  86. 86.
    Bjursell M, Admyre T, Goransson M, Marley AE, Smith DM, Oscarsson J, et al. Improved glucose control and reduced body fat mass in free fatty acid receptor 2-deficient mice fed a high-fat diet. AmJ Physiol Endocrinol Metab. 2011;300(1):E211–E20.Google Scholar
  87. 87.
    Hamer HM, De Preter V, Windey K, Verbeke K. Functional analysis of colonic bacterial metabolism: Relevant to health? Am J Physiol Gastrointest Liver Physiol. 2012;302(1):G1–9. doi: 10.1152/ajpgi.00048.2011.PubMedCentralPubMedGoogle Scholar
  88. 88.
    Chu ZL, Carroll C, Alfonso J, Gutierrez V, He H, Lucman A, et al. A role for intestinal endocrine cell-expressed g protein-coupled receptor 119 in glycemic control by enhancing glucagon-like Peptide-1 and glucose-dependent insulinotropic Peptide release. Endocrinology. 2008;149(5):2038–47.PubMedGoogle Scholar
  89. 89.
    Lan H, Vassileva G, Corona A, Liu L, Baker H, Golovko A, et al. GPR119 is required for physiological regulation of glucagon-like peptide-1 secretion but not for metabolic homeostasis. J Endocrinol. 2009;201(2):219–30.PubMedGoogle Scholar
  90. 90.
    Overton HA, Babbs AJ, Doel SM, Fyfe MC, Gardner LS, Griffin G, et al. Deorphanization of a G protein-coupled receptor for oleoylethanolamide and its use in the discovery of small-molecule hypophagic agents. Cell Metab. 2006;3(3):167–75. doi: 10.1016/j.cmet.2006.02.004.PubMedGoogle Scholar
  91. 91.
    de Rodriguez FF, Navarro M, Gomez R, Escuredo L, Nava F, Fu J, et al. An anorexic lipid mediator regulated by feeding. Nature. 2001;414(6860):209–12.Google Scholar
  92. 92.
    Oveisi F, Gaetani S, Eng KT, Piomelli D. Oleoylethanolamide inhibits food intake in free-feeding rats after oral administration. Pharmacol res : the official j of the Italian Pharmacol Soc. 2004;49(5):461–6. doi: 10.1016/j.phrs.2003.12.006.Google Scholar
  93. 93.
    Bradshaw HB, Walker JM. The expanding field of cannabimimetic and related lipid mediators. Br J Pharmacol. 2005;144(4):459–65. doi: 10.1038/sj.bjp.0706093.PubMedCentralPubMedGoogle Scholar
  94. 94.
    Lauffer LM, Iakoubov R, Brubaker PL. GPR119 is essential for oleoylethanolamide-induced glucagon-like peptide-1 secretion from the intestinal enteroendocrine L-cell. Diabetes. 2009;58(5):1058–66.PubMedCentralPubMedGoogle Scholar
  95. 95.
    Hansen KB, Rosenkilde MM, Knop FK, Wellner N, Diep TA, Rehfeld JF, et al. 2-Oleoyl glycerol is a GPR119 agonist and signals GLP-1 release in humans. J Clin Endocrinol Metab. 2011;96(9):E1409–17. doi: 10.1210/jc.2011-0647.PubMedGoogle Scholar
  96. 96.
    Syed SK, Bui HH, Beavers LS, Farb TB, Ficorilli J, Chesterfield AK, et al. Regulation of GPR119 receptor activity with endocannabinoid-like lipids. Am J Physiol Endocrinol Metab. 2012;303(12):E1469–78. doi: 10.1152/ajpendo.00269.2012.PubMedGoogle Scholar
  97. 97.
    Muccioli GG, Naslain D, Backhed F, Reigstad CS, Lambert DM, Delzenne NM, et al. The endocannabinoid system links gut microbiota to adipogenesis. Mol Syst Biol. 2010;6:392.PubMedCentralPubMedGoogle Scholar
  98. 98.
    Everard A, Belzer C, Geurts L, Ouwerkerk JP, Druart C, Bindels LB, et al. Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proc Natl Acad Sci U S A. 2013;110(22):9066–71. doi: 10.1073/pnas.1219451110.PubMedCentralPubMedGoogle Scholar
  99. 99.
    Sternini C, Anselmi L, Rozengurt E. Enteroendocrine cells: A site of ‘taste’ in gastrointestinal chemosensing. Curr Opin Endocrinol Diabetes Obes. 2008;15(1):73–8. doi: 10.1097/MED.0b013e3282f43a73.PubMedCentralPubMedGoogle Scholar
  100. 100.
    Li Y, Kokrashvili Z, Mosinger B, Margolskee RF. Gustducin couples fatty acid receptors to GLP-1 release in colon. Am J Physiol Endocrinol Metab. 2013;304(6):E651–60. doi: 10.1152/ajpendo.00471.2012.PubMedCentralPubMedGoogle Scholar
  101. 101.
    Cani PD, Dewever C, Delzenne NM. Inulin-type fructans modulate gastrointestinal peptides involved in appetite regulation (glucagon-like peptide-1 and ghrelin) in rats. Br J Nutr. 2004;92(3):521–6.PubMedGoogle Scholar
  102. 102.
    Cani PD, Neyrinck AM, Fava F, Knauf C, Burcelin RG, Tuohy KM, et al. Selective increases of bifidobacteria in gut microflora improve high-fat-diet-induced diabetes in mice through a mechanism associated with endotoxaemia. Diabetologia. 2007;50(11):2374–83.PubMedGoogle Scholar
  103. 103.
    Cani PD, Hoste S, Guiot Y, Delzenne NM. Dietary non-digestible carbohydrates promote L-cell differentiation in the proximal colon of rats. Br J Nutr. 2007;98(1):32–7.PubMedGoogle Scholar
  104. 104.
    Everard A, Lazarevic V, Derrien M, Girard M, Muccioli GM, Neyrinck AM, et al. Responses of gut microbiota and glucose and lipid metabolism to prebiotics in genetic obese and diet-induced leptin-resistant mice. Diabetes. 2011;60(11):2775–86.PubMedCentralPubMedGoogle Scholar
  105. 105.
    Kaji I, Karaki S, Tanaka R, Kuwahara A. Density distribution of free fatty acid receptor 2 (FFA2)-expressing and GLP-1-producing enteroendocrine L cells in human and rat lower intestine, and increased cell numbers after ingestion of fructo-oligosaccharide. J Mol Histol. 2011;42(1):27–38.PubMedGoogle Scholar
  106. 106.
    Pedersen C, Lefevre S, Peters V, Patterson M, Ghatei MA, Morgan LM, et al. Gut hormone release and appetite regulation in healthy non-obese participants following oligofructose intake. A dose-escalation study Appetite. 2013;66:44–53. doi: 10.1016/j.appet.2013.02.017.Google Scholar
  107. 107.
    Verhoef SP, Meyer D, Westerterp KR. Effects of oligofructose on appetite profile, glucagon-like peptide 1 and peptide YY3-36 concentrations and energy intake. BrJNutr. 2011:1–6.Google Scholar
  108. 108.
    Rousseaux C, Thuru X, Gelot A, Barnich N, Neut C, Dubuquoy L, et al. Lactobacillus acidophilus modulates intestinal pain and induces opioid and cannabinoid receptors. Nat Med. 2007;13(1):35–7.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  1. 1.WELBIO (Walloon Excellence in Life sciences and BIOtechnology), Metabolism and Nutrition research groupUniversité catholique de Louvain, Louvain Drug Research InstituteBrusselsBelgium

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