Bile acids acutely stimulate insulin secretion of mouse β-cells via farnesoid X receptor activation and K ATP channel inhibition

Diabetes

Volumn 61, Issue 6, 2012, Pages 1479-1489

  Düfer, Martina ^a   Hörth, Katrin ^a   Wagner, Rebecca ^a   Schittenhelm, Björn ^a   Prowald, Susanne ^a   Wagner, Thomas F J ^b   Oberwinkler, Johannes ^c   Lukowski, Robert ^a   Gonzalez, Frank J ^d   Krippeit Drews, Peter ^a   Drews, Gisela ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c PHILIPPS UNIVERSITY MARBURG   (Germany)

^d NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3 [2 [2 CHLORO 4 [3 (2,6 DICHLOROPHENYL) 5 ISOPROPYL 4 ISOXAZOLYLMETHOXY]PHENYL]VINYL]BENZOIC ACID; ADENOSINE TRIPHOSPHATE SENSITIVE POTASSIUM CHANNEL; BILE ACID; CALCIUM; FARNESOID X RECEPTOR; GLUCOSE; GUGGULSTERONE; SULFONYLUREA RECEPTOR 1; TAUROCHENODEOXYCHOLIC ACID; TOLBUTAMIDE; TRANSIENT RECEPTOR POTENTIAL CHANNEL M3; URSODEOXYCHOLIC ACID;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; ELECTRIC ACTIVITY; GLUCOSE HOMEOSTASIS; INSULIN RELEASE; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL;

ANIMALS; GLUCOSE; INSULIN; INSULIN-SECRETING CELLS; MICE; MICE, KNOCKOUT; POTASSIUM CHANNELS, INWARDLY RECTIFYING; PREGNENEDIONES; RECEPTORS, CYTOPLASMIC AND NUCLEAR; TAURODEOXYCHOLIC ACID;

EID: 84861880073     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db11-0815     Document Type: Article

References (48)

1. Fiorucci S, Mencarelli A, Palladino G, Cipriani S. Bile-acid-activated receptors: targeting TGR5 and farnesoid-X-receptor in lipid and glucose disorders. Trends Pharmacol Sci 2009;30:570-580
2. Zhao X, Peter A, Fritsche J, et al. Changes of the plasma metabolome during an oral glucose tolerance test: is there more than glucose to look at? Am J Physiol Endocrinol Metab 2009;296:E384-E393
3. Shaham O, Wei R, Wang TJ, et al. Metabolic profiling of the human response to a glucose challenge reveals distinct axes of insulin sensitivity. Mol Syst Biol 2008;4:214
4. Lefebvre P, Cariou B, Lien F, Kuipers F, Staels B. Role of bile acids and bile acid receptors in metabolic regulation. Physiol Rev 2009;89:147-191
5. Glicksman C, Pournaras DJ, Wright M, et al. Postprandial plasma bile acid responses in normal weight and obese subjects. Ann Clin Biochem 2010; 47:482-484
6. Güliter S, Yilmaz S, Karakan T. Evaluation of gallbladder volume and motility in non-insulin-dependent diabetes mellitus patients using real-time ultrasonography. J Clin Gastroenterol 2003;37:288-291 (Pubitemid 37158990)
7. Andersén E, Karlaganis G, Sjövall J. Altered bile acid profiles in duodenal bile and urine in diabetic subjects. Eur J Clin Invest 1988;18:166-172
8. Bennion LJ, Grundy SM. Effects of diabetes mellitus on cholesterol metabolism in man. N Engl J Med 1977;296:1365-1371 (Pubitemid 8127337)
9. Nguyen A, Bouscarel B. Bile acids and signal transduction: role in glucose homeostasis. Cell Signal 2008;20:2180-2197
10. Staels B, Handelsman Y, Fonseca V. Bile acid sequestrants for lipid and glucose control. Curr Diab Rep 2010;10:70-77
11. Brinton EA. Novel pathways for glycaemic control in type 2 diabetes: focus on bile acid modulation. Diabetes Obes Metab 2008;10:1004-1011
12. Ozcan U, Yilmaz E, Ozcan L, et al. Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes. Science 2006;313:1137-1140 (Pubitemid 44300242)
13. Li LO, Hu YF,Wang L, Mitchell M, Berger A, Coleman RA. Early hepatic insulin resistance in mice: a metabolomics analysis. Mol Endocrinol 2010;24:657-666
14. Cariou B, van Harmelen K, Duran-Sandoval D, et al. The farnesoid X receptor modulates adiposity and peripheral insulin sensitivity in mice. J Biol Chem 2006;281:11039-11049 (Pubitemid 43855527)
15. Ma K, Saha PK, Chan L, Moore DD. Farnesoid X receptor is essential for normal glucose homeostasis. J Clin Invest 2006;116:1102-1109
16. 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 USA 2006;103:1006-1011 (Pubitemid 43212212)
17. Cipriani S, Mencarelli A, Palladino G, Fiorucci S. FXR activation reverses insulin resistance and lipid abnormalities and protects against liver steatosis in Zucker (fa/fa) obese rats. J Lipid Res 2010;51:771-784
18. Duran-Sandoval D, Cariou B, Percevault F, et al. The farnesoid X receptor modulates hepatic carbohydrate metabolism during the fasting-refeeding transition. J Biol Chem 2005;280:29971-29979 (Pubitemid 41177076)
19. Zhang Y, Castellani LW, Sinal CJ, Gonzalez FJ, Edwards PA. Peroxisome proliferator-activated receptor-gamma coactivator 1alpha (PGC-1alpha) regulates triglyceride metabolism by activation of the nuclear receptor FXR. Genes Dev 2004;18:157-169 (Pubitemid 38141784)
20. Claudel T, Staels B, Kuipers F. The Farnesoid X receptor: a molecular link between bile acid and lipid and glucose metabolism. Arterioscler Thromb Vasc Biol 2005;25:2020-2030
21. Duran-Sandoval D, Mautino G, Martin G, et al. Glucose regulates the expression of the farnesoid X receptor in liver. Diabetes 2004;53:890-898 (Pubitemid 38436600)
22. Renga B, Mencarelli A, Vavassori P, Brancaleone V, Fiorucci S. The bile acid sensor FXR regulates insulin transcription and secretion. Biochim Biophys Acta 2010;1802:363-372
23. Popescu IR, Helleboid-Chapman A, Lucas A, et al. The nuclear receptor FXR is expressed in pancreatic beta-cells and protects human islets from lipotoxicity. FEBS Lett 2010;584:2845-2851
24. Perez MJ, Briz O. Bile-acid-induced cell injury and protection. World J Gastroenterol 2009;15:1677-1689
25. Monte MJ, Marin JJ, Antelo A, Vazquez-Tato J. Bile acids: chemistry, physiology, and pathophysiology. World J Gastroenterol 2009;15:804-816
26. Xu HB, Li L, Liu GQ. Protection against hydrogen peroxide-induced cytotoxicity in PC12 cells by guggulsterone. Yao Xue Xue Bao 2008;43: 1190-1197
27. Lv N, Song MY, Kim EK, Park JW, Kwon KB, Park BH. Guggulsterone, a plant sterol, inhibits NF-kappaB activation and protects pancreatic beta cells from cytokine toxicity. Mol Cell Endocrinol 2008;289:49-59
28. Gier B, Krippeit-Drews P, Sheiko T, et al. Suppression of KATP channel activity protects murine pancreatic beta cells against oxidative stress. J Clin Invest 2009;119:3246-3256
29. Sinal CJ, Tohkin M, Miyata M, Ward JM, Lambert G, Gonzalez FJ. Targeted disruption of the nuclear receptor FXR/BAR impairs bile acid and lipid homeostasis. Cell 2000;102:731-744
30. Garrino MG, Plant TD, Henquin JC. Effects of putative activators of K+ channels in mouse pancreatic beta-cells. Br J Pharmacol 1989;98:957-965 (Pubitemid 19269821)
31. Düfer M, Gier B, Wolpers D, Krippeit-Drews P, Ruth P, Drews G. Enhanced glucose tolerance by SK4 channel inhibition in pancreatic beta-cells. Diabetes 2009;58:1835-1843
32. Wagner TF, Loch S, Lambert S, et al. Transient receptor potential M3 channels are ionotropic steroid receptors in pancreatic beta cells. Nat Cell Biol 2008;10:1421-1430
33. Urizar NL, Liverman AB, Dodds DT, et al. A natural product that lowers cholesterol as an antagonist ligand for FXR. Science 2002;296:1703-1706 (Pubitemid 34579172)
34. Willson TM, Jones SA, Moore JT, Kliewer SA. Chemical genomics: functional analysis of orphan nuclear receptors in the regulation of bile acid metabolism. Med Res Rev 2001;21:513-522 (Pubitemid 32959240)
35. Lew JL, Zhao A, Yu J, et al. The farnesoid X receptor controls gene expression in a ligand- and promoter-selective fashion. J Biol Chem 2004;279: 8856-8861 (Pubitemid 38295944)
36. Houten SM, Watanabe M, Auwerx J. Endocrine functions of bile acids. EMBO J 2006;25:1419-1425
37. Cai SY, Xiong L, Wray CG, Ballatori N, Boyer JL. The farnesoid X receptor FXRalpha/NR1H4 acquired ligand specificity for bile salts late in vertebrate evolution. Am J Physiol Regul Integr Comp Physiol 2007;293:R1400-R1409 (Pubitemid 47358967)
38. Cornil CA, Charlier TD. Rapid behavioural effects of oestrogens and fast regulation of their local synthesis by brain aromatase. J Neuroendocrinol 2010;22:664-673
39. Fatehi M, Kombian SB, Saleh TM. 17beta-estradiol inhibits outward potassium currents recorded in rat parabrachial nucleus cells in vitro. Neuroscience 2005;135:1075-1086 (Pubitemid 41416671)
40. Johnson JH, Newgard CB, Milburn JL, Lodish HF, Thorens B. The high Km glucose transporter of islets of Langerhans is functionally similar to the low affinity transporter of liver and has an identical primary sequence. J Biol Chem 1990;265:6548-6551
41. Heimberg H, De Vos A, Vandercammen A, Van Schaftingen E, Pipeleers D, Schuit F. Heterogeneity in glucose sensitivity among pancreatic beta-cells is correlated to differences in glucose phosphorylation rather than glucose transport. EMBO J 1993;12:2873-2879 (Pubitemid 23218337)
42. Tal M, Liang Y, Najafi H, Lodish HF, Matschinsky FM. Expression and function of GLUT-1 and GLUT-2 glucose transporter isoforms in cells of cultured rat pancreatic islets. J Biol Chem 1992;267:17241-17247
43. Kars M, Yang L, Gregor MF, et al. Tauroursodeoxycholic acid may improve liver and muscle but not adipose tissue insulin sensitivity in obese men and women. Diabetes 2010;59:1899-1905
44. Patti ME, Houten SM, Bianco AC, et al. Serum bile acids are higher in humans with prior gastric bypass: potential contribution to improved glucose and lipid metabolism. Obesity (Silver Spring) 2009;17:1671-1677
45. Prawitt J, Abdelkarim M, Stroeve JH, et al. Farnesoid X receptor deficiency improves glucose homeostasis in mouse models of obesity. Diabetes 2011; 60:1861-1871
46. Watanabe M, Horai Y, Houten SM, et al. Lowering bile acid pool size with a synthetic FXR agonist induces obesity and diabetes through reduced energy expenditure. J Biol Chem 2011;286:26913-26920
47. Schroder K, Zhou R, Tschopp J. The NLRP3 inflammasome: a sensor for metabolic danger? Science 2010;327:296-300
48. Zhang Y, Edwards PA. FXR signaling in metabolic disease. FEBS Lett 2008; 582:10-18 (Pubitemid 350297240)