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Research Paper

Gut microbiota regulates postprandial GLP-1 response via ileal bile acid-TGR5 signaling

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Article: 2274124 | Received 27 Apr 2023, Accepted 18 Oct 2023, Published online: 09 Nov 2023

References

  • Drucker DJ. The biology of incretin hormones. Cell Metab. 2006;3(3):153–16. doi:10.1016/j.cmet.2006.01.004.
  • Finan B, Ma T, Ottaway N, Muller TD, Habegger KM, Heppner KM, Kirchner H, Holland J, Hembree J, Raver C, et al. Unimolecular dual incretins maximize metabolic benefits in rodents, monkeys, and humans. Sci Transl Med. 2013;5(209):209ra151. doi:10.1126/scitranslmed.3007218.
  • Finan B, Yang B, Ottaway N, Smiley DL, Ma T, Clemmensen C, Chabenne J, Zhang L, Habegger KM, Fischer K, et al. A rationally designed monomeric peptide triagonist corrects obesity and diabetes in rodents. Nat Med. 2015;21(1):27–36. doi:10.1038/nm.3761.
  • Herrmann C, Goke R, Richter G, Fehmann HC, Arnold R, Goke B. Glucagon-like peptide-1 and glucose-dependent insulin-releasing polypeptide plasma levels in response to nutrients. Digestion. 1995;56(2):117–126. doi:10.1159/000201231.
  • Chia CW, Egan JM. Incretins in obesity and diabetes. Ann N Y Acad Sci. 2020;1461(1):104–126. doi:10.1111/nyas.14211.
  • Bryant MG, Bloom SR, Polak JM, Hobbs S, Domschke W, Domschke S, Mitznegg P, Ruppin H, Demling L. Measurement of gut hormonal peptides in biopsies from human stomach and proximal small intestine. Gut. 1983;24(2):114–119. doi:10.1136/gut.24.2.114.
  • Muller TD, Finan B, Bloom SR, D’Alessio D, Drucker DJ, Flatt PR, Fritsche A, Gribble F, Grill HJ, Habener JF, et al. Glucagon-like peptide 1 (GLP-1). Mol Metab. 2019;30:72–130. doi:10.1016/j.molmet.2019.09.010.
  • Eissele R, Goke R, Willemer S, Harthus HP, Vermeer H, Arnold R, Göke B. Glucagon-like peptide-1 cells in the gastrointestinal tract and pancreas of rat, pig and man. Eur J Clin Invest. 1992;22(4):283–291. doi:10.1111/j.1365-2362.1992.tb01464.x.
  • Toft-Nielson M, Madsbad S, Holst JJ. The effect of glucagon-like peptide I (GLP-I) on glucose elimination in healthy subjects depends on the pancreatic glucoregulatory hormones. Diabetes. 1996;45(5):552–556. doi:10.2337/diab.45.5.552.
  • Vilsboll T, Krarup T, Sonne J, Madsbad S, Volund A, Juul AG, Holst JJ. Incretin secretion in relation to meal size and body weight in healthy subjects and people with type 1 and type 2 diabetes mellitus. J Clin Endocrinol Metab. 2003;88(6):2706–2713. doi:10.1210/jc.2002-021873.
  • Nakajima S, Hira T, Hara H. Postprandial glucagon-like peptide-1 secretion is increased during the progression of glucose intolerance and obesity in high-fat/high-sucrose diet-fed rats. Br J Nutr. 2015;113(9):1477–1488. doi:10.1017/S0007114515000550.
  • Gribble FM, Williams L, Simpson AK, Reimann F. A novel glucose-sensing mechanism contributing to glucagon-like peptide-1 secretion from the GLUTag cell line. Diabetes. 2003;52(5):1147–1154. doi:10.2337/diabetes.52.5.1147.
  • Hirasawa A, Tsumaya K, Awaji T, Katsuma S, Adachi T, Yamada M, Sugimoto Y, Miyazaki S, Tsujimoto G. Free fatty acids regulate gut incretin glucagon-like peptide-1 secretion through GPR120. Nat Med. 2005;11(1):90–94. doi:10.1038/nm1168.
  • Mochida T, Hira T, Hara H. The corn protein, zein hydrolysate, administered into the ileum attenuates hyperglycemia via its dual action on glucagon-like peptide-1 secretion and dipeptidyl peptidase-IV activity in rats. Endocrinology. 2010;151(7):3095–3104. doi:10.1210/en.2009-1510.
  • Reimann F, Williams L, da Silva Xavier G, Rutter GA, Gribble FM. Glutamine potently stimulates glucagon-like peptide-1 secretion from GLUTag cells. Diabetologia. 2004;47(9):1592–1601. doi:10.1007/s00125-004-1498-0.
  • Panaro BL, Yusta B, Matthews D, Koehler JA, Song Y, Sandoval DA, Drucker DJ. Intestine-selective reduction of gcg expression reveals the importance of the distal gut for GLP-1 secretion. Mol Metab. 2020;37:100990. doi:10.1016/j.molmet.2020.100990.
  • Canfora EE, Meex RCR, Venema K, Blaak EE. Gut microbial metabolites in obesity, NAFLD and T2DM. Nat Rev Endocrinol. 2019;15(5):261–273. doi:10.1038/s41574-019-0156-z.
  • Liu R, Hong J, Xu X, Feng Q, Zhang D, Gu Y, Shi J, Zhao S, Liu W, Wang X, et al. Gut microbiome and serum metabolome alterations in obesity and after weight-loss intervention. Nat Med. 2017;23(7):859–868. doi:10.1038/nm.4358.
  • Greiner TU, Backhed F. Microbial regulation of GLP-1 and L-cell biology. Mol Metab. 2016;5(9):753–758. doi:10.1016/j.molmet.2016.05.012.
  • Di Ciaula A, Garruti G, Lunardi Baccetto R, Molina-Molina E, Bonfrate L, Wang DQ, Portincasa P. Bile acid physiology. Ann Hepatol. 2017;16:s4–s14. doi:10.5604/01.3001.0010.5493.
  • Funabashi M, Grove TL, Wang M, Varma Y, McFadden ME, Brown LC, Guo C, Higginbottom S, Almo SC, Fischbach MA, et al. A metabolic pathway for bile acid dehydroxylation by the gut microbiome. Nature. 2020;582(7813):566–570. doi:10.1038/s41586-020-2396-4.
  • Thomas C, Gioiello A, Noriega L, Strehle A, Oury J, Rizzo G, Macchiarulo A, Yamamoto H, Mataki C, Pruzanski M, 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.
  • Kuhre RE, Wewer Albrechtsen NJ, Larsen O, Jepsen SL, Balk-Moller E, Andersen DB, Deacon CF, Schoonjans K, Reimann F, Gribble FM, et al. Bile acids are important direct and indirect regulators of the secretion of appetite- and metabolism-regulating hormones from the gut and pancreas. Mol Metab. 2018;11:84–95. doi:10.1016/j.molmet.2018.03.007.
  • Trabelsi MS, Daoudi M, Prawitt J, Ducastel S, Touche V, Sayin SI, Perino A, Brighton CA, Sebti Y, Kluza J, et al. Farnesoid X receptor inhibits glucagon-like peptide-1 production by enteroendocrine L cells. Nat Commun. 2015;6(1):7629. doi:10.1038/ncomms8629.
  • Li K, Zou J, Li S, Guo J, Shi W, Wang B, Han X, Zhang H, Zhang P, Miao Z, et al. Farnesoid X receptor contributes to body weight-independent improvements in glycemic control after roux-en-Y gastric bypass surgery in diet-induced obese mice. Mol Metab. 2020;37:100980. doi:10.1016/j.molmet.2020.100980.
  • Wichmann A, Allahyar A, Greiner TU, Plovier H, Lunden GO, Larsson T, Drucker D, Delzenne N, Cani P, Bäckhed F, et al. Microbial modulation of energy availability in the colon regulates intestinal transit. Cell Host & Microbe. 2013;14(5):582–590. doi:10.1016/j.chom.2013.09.012.
  • Zarrinpar A, Chaix A, Xu ZZ, Chang MW, Marotz CA, Saghatelian A, Knight R, Panda S. Antibiotic-induced microbiome depletion alters metabolic homeostasis by affecting gut signaling and colonic metabolism. Nat Commun. 2018;9(1):2872. doi:10.1038/s41467-018-05336-9.
  • Gorboulev V, Schurmann A, Vallon V, Kipp H, Jaschke A, Klessen D, Friedrich A, Scherneck S, Rieg T, Cunard R, et al. Na+- d -glucose cotransporter SGLT1 is pivotal for intestinal glucose absorption and glucose-dependent incretin secretion. Diabetes. 2012;61(1):187–196. doi:10.2337/db11-1029.
  • Arora T, Akrami R, Pais R, Bergqvist L, Johansson BR, Schwartz TW, Reimann F, Gribble FM, Bäckhed F. Microbial regulation of the L cell transcriptome. Sci Rep. 2018;8(1):1207. doi:10.1038/s41598-017-18079-2.
  • Zhao M, Ren K, Xiong X, Cheng M, Zhang Z, Huang Z, Han X, Yang X, Alejandro EU, Ruan H-B, et al. Protein O-GlcNAc modification links dietary and gut microbial cues to the differentiation of enteroendocrine L cells. Cell Rep. 2020;32(6):108013. doi:10.1016/j.celrep.2020.108013.
  • Alamshah A, McGavigan AK, Spreckley E, Kinsey-Jones JS, Amin A, Tough IR, O’Hara HC, Moolla A, Banks K, France R, et al. L-arginine promotes gut hormone release and reduces food intake in rodents. Diabetes Obes Metab. 2016;18(5):508–518. doi:10.1111/dom.12644.
  • Reijnders D, Goossens GH, Hermes GD, Neis EP, van der Beek CM, Most J, Holst J, Lenaerts K, Kootte R, Nieuwdorp M, et al. Effects of gut microbiota manipulation by antibiotics on host metabolism in obese humans: a randomized Double-blind placebo-controlled trial. Cell Metab. 2016;24(1):63–74. doi:10.1016/j.cmet.2016.06.016.
  • Cornejo-Pareja I, Martin-Nunez GM, Roca-Rodriguez MM, Cardona F, Coin-Araguez L, Sanchez-Alcoholado L, Gutiérrez-Repiso C, Muñoz-Garach A, Fernández-García J, Moreno-Indias I, et al. H. pylori eradication treatment alters gut microbiota and GLP-1 secretion in humans. J Clin Med. 2019;8(4):451. doi:10.3390/jcm8040451.
  • Goodman BE. Insights into digestion and absorption of major nutrients in humans. Adv Physiol Educ. 2010;34(2):44–53. doi:10.1152/advan.00094.2009.
  • Grasset E, Puel A, Charpentier J, Collet X, Christensen JE, Terce F, Burcelin R. A specific gut microbiota dysbiosis of type 2 diabetic mice Induces GLP-1 resistance through an enteric NO-Dependent and gut-brain axis mechanism. Cell Metab. 2017;25(5):1075–90 e5. doi:10.1016/j.cmet.2017.04.013.
  • Grasset E, Puel A, Charpentier J, Klopp P, Christensen JE, Lelouvier B, Servant F, Blasco-Baque V, Tercé F, Burcelin R, et al. Gut microbiota dysbiosis of type 2 diabetic mice impairs the intestinal daily rhythms of GLP-1 sensitivity. Acta Diabetol. 2022;59(2):243–258. doi:10.1007/s00592-021-01790-y.
  • Xie C, Huang W, Young RL, Jones KL, Horowitz M, Rayner CK, Wu T. Role of bile acids in the regulation of food intake, and their Dysregulation in metabolic disease. Nutrients. 2021;13(4):1104. doi:10.3390/nu13041104.
  • Agus A, Clement K, Sokol H. Gut microbiota-derived metabolites as central regulators in metabolic disorders. Gut. 2021;70(6):1174–1182. doi:10.1136/gutjnl-2020-323071.
  • Perino A, Schoonjans K. Metabolic messengers: bile acids. Nat Metab. 2022;4(4):416–423. doi:10.1038/s42255-022-00559-z.
  • Cai J, Sun L, Gonzalez FJ. Gut microbiota-derived bile acids in intestinal immunity, inflammation, and tumorigenesis. Cell Host Microbe. 2022;30(3):289–300. doi:10.1016/j.chom.2022.02.004.
  • Han H, Yi B, Zhong R, Wang M, Zhang S, Ma J, Yin Y, Yin J, Chen L, Zhang H, et al. From gut microbiota to host appetite: gut microbiota-derived metabolites as key regulators. Microbiome. 2021;9(1):162. doi:10.1186/s40168-021-01093-y.
  • Molinaro A, Wahlstrom A, Marschall HU. Role of bile acids in metabolic control. Trends Endocrinol Metab. 2018;29(1):31–41. doi:10.1016/j.tem.2017.11.002.
  • Sayin SI, Wahlstrom A, Felin J, Jantti S, Marschall HU, Bamberg K, Angelin B, Hyötyläinen T, Orešič M, Bäckhed F, 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.
  • Katsuma S, Hirasawa A, Tsujimoto G. Bile acids promote glucagon-like peptide-1 secretion through TGR5 in a murine enteroendocrine cell line STC-1. Biochem Biophys Res Commun. 2005;329(1):386–390. doi:10.1016/j.bbrc.2005.01.139.
  • Parker HE, Wallis K, le Roux CW, Wong KY, Reimann F, Gribble FM. Molecular mechanisms underlying bile acid-stimulated glucagon-like peptide-1 secretion. Br J Pharmacol. 2012;165(2):414–423. doi:10.1111/j.1476-5381.2011.01561.x.
  • Brighton CA, Rievaj J, Kuhre RE, Glass LL, Schoonjans K, Holst JJ, Gribble FM, Reimann F. Bile acids trigger GLP-1 release predominantly by accessing basolaterally located G protein–coupled bile acid receptors. Endocrinology. 2015;156(11):3961–3970. doi:10.1210/en.2015-1321.
  • Lund ML, Sorrentino G, Egerod KL, Kroone C, Mortensen B, Knop FK, Reimann F, Gribble FM, Drucker DJ, de Koning EJP, et al. L-Cell differentiation is induced by bile acids through GPBAR1 and Paracrine GLP-1 and serotonin signaling. Diabetes. 2020;69(4):614–623. doi:10.2337/db19-0764.
  • Zheng X, Chen T, Jiang R, Zhao A, Wu Q, Kuang J, Sun D, Ren Z, Li M, Zhao M, et al. Hyocholic acid species improve glucose homeostasis through a distinct TGR5 and FXR signaling mechanism. Cell Metab. 2021;33(4):791–803 e7. doi:10.1016/j.cmet.2020.11.017.
  • Pathak P, Xie C, Nichols RG, Ferrell JM, Boehme S, Krausz KW, Patterson AD, Gonzalez FJ, Chiang JYL. Intestine farnesoid X receptor agonist and the gut microbiota activate G-protein bile acid receptor-1 signaling to improve metabolism. Hepatology. 2018;68(4):1574–1588. doi:10.1002/hep.29857.
  • Liszt KI, Wang Q, Farhadipour M, Segers A, Thijs T, Nys L, Deleus E, Van der Schueren B, Gerner C, Neuditschko B, et al. Human intestinal bitter taste receptors regulate innate immune responses and metabolic regulators in obesity. J Clin Invest. 2022;132(3):132. doi:10.1172/JCI144828.
  • Wang Q, Liszt KI, Deloose E, Canovai E, Thijs T, Farre R, Ceulemans LJ, Lannoo M, Tack J, Depoortere I, et al. Obesity alters adrenergic and chemosensory signaling pathways that regulate ghrelin secretion in the human gut. FASEB J. 2019;33(4):4907–4920. doi:10.1096/fj.201801661RR.