Colesevelam suppresses hepatic glycogenolysis by TGR5-mediated induction of GLP-1 action in DIO mice

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 304, Issue 4, 2013, Pages

  Potthoff, Matthew J ^a,b   Potts, Austin ^b   He, Tianteng ^b   Duarte, João A G ^b   Taussig, Ronald ^a   Mangelsdorf, David J ^a,b   Kliewer, Steven A ^a,b   Burgess, Shawn C ^a,b  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

Bile acids; Diabetes induced obesity; FGF 15; FXR; Glucagon like peptide 1; TGR5

Indexed keywords

COLESEVELAM; CYCLIC AMP; FARNESOID X RECEPTOR; GLUCAGON LIKE PEPTIDE 1; GLUCOSE; GLYCOGEN; PROTEIN; TGR 5 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CELL ASSAY; CHOLESTEROL METABOLISM; CONTROLLED STUDY; GLUCONEOGENESIS; GLUCOSE BLOOD LEVEL; GLYCOGENOLYSIS; HYPERCHOLESTEROLEMIA; IN VITRO STUDY; MALE; MOUSE; NONHUMAN; OBESITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION;

ALLYLAMINE; ANIMALS; BILE ACIDS AND SALTS; BLOOD GLUCOSE; CHOLESTEROL; DIET, HIGH-FAT; GLUCAGON-LIKE PEPTIDE 1; GLYCOGENOLYSIS; LIVER; MALE; MICE; MICE, OBESE; RECEPTORS, CYTOPLASMIC AND NUCLEAR; RECEPTORS, G-PROTEIN-COUPLED; RECEPTORS, GLUCAGON;

EID: 84874031840     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00400.2012     Document Type: Article

References (57)

1. Ayala JE, Bracy DP, James FD, Julien BM, Wasserman DH, Drucker DJ. The glucagon-like peptide-1 receptor regulates endogenous glucose production and muscle glucose uptake independent of its incretin action. Endocrinology 150: 1155-1164, 2009.
2. Basu R, Chandramouli V, Dicke B, Landau B, Rizza R. Obesity and type 2 diabetes impair insulin-induced suppression of glycogenolysis as well as gluconeogenesis. Diabetes 54: 1942-1948, 2005.
3. Best JD, Judzewitsch RG, Pfeifer MA, Beard JC, Halter JB, Porte D Jr. The effect of chronic sulfonylurea therapy on hepatic glucose production in non-insulin-dependent diabetes. Diabetes 31: 333-338, 1982.
4. Beysen C, Murphy EJ, Deines K, Chan M, Tsang E, Glass A, Turner SM, Protasio J, Riiff T, Hellerstein MK. Effect of bile acid sequestrants on glucose metabolism, hepatic de novo lipogenesis, and cholesterol and bile acid kinetics in type 2 diabetes: a randomised controlled study. Diabetologia 55: 432-442, 2012.
5. Braunlin W, Zhorov E, Smisek D, Guo A, Appruzese W, Xu Q, Hook P, Holmes-Farley R, Mandeville H. In vitro comparison of bile acid binding to colesevelam hcl and other bile acid sequestrants. Polymer Preprints 41: 708-709, 2000.
6. Burcelin R, Da Costa A, Drucker D, Thorens B. Glucose competence of the hepatoportal vein sensor requires the presence of an activated glucagon-like peptide-1 receptor. Diabetes 50: 1720-1728, 2001.
7. Burgess SC, Jeffrey FMH, Storey C, Milde A, Hausler N, Merritt ME, Mulder H, Holm C, Sherry AD, Malloy CR. Effect of murine strain on metabolic pathways of glucose production after brief or prolonged fasting. Am J Physiol Endocrinol Metab 289: E53-E61, 2005.
8. Burgess SC, Nuss M, Chandramouli V, Hardin DS, Rice M, Landau BR, Malloy CR, Sherry AD. Analysis of gluconeogenic pathways in vivo by distribution of 2H in plasma glucose: comparison of nuclear magnetic resonance and mass spectrometry. Anal Biochem 318: 321-324, 2003.
9. Burmeister MA, Ferre T, Ayala JE, King EM, Holt RM, Ayala JE. Acute activation of central GLP-1 receptors enhances hepatic insulin action and insulin secretion in high-fat-fed, insulin resistant mice. Am J Physiol Endocrinol Metab 302: E334-E343, 2012.
10. Chen L, McNulty J, Anderson D, Liu Y, Nystrom C, Bullard S, Collins J, Handlon AL, Klein R, Grimes A, Murray D, Brown R, Krull D, Benson B, Kleymenova E, Remlinger K, Young A, Yao X. Cholestyramine reverses hyperglycemia and enhances glucose-stimulated glucagon-like peptide 1 release in Zucker diabetic fatty rats. J Pharmacol Exp Ther 334: 164-170, 2010.
11. D'Alessio D, Vahl T, Prigeon R. Effects of glucagon-like peptide 1 on the hepatic glucose metabolism. Horm Metab Res 36: 837-841, 2004.
12. Damholt AB, Kofod H, Buchan AM. Immunocytochemical evidence for a paracrine interaction between GIP and GLP-1-producing cells in canine small intestine. Cell Tissue Res 298: 287-293, 1999.
13. Ding J, Gao Y, Zhao J, Yan H, Guo SY, Zhang QX, Li LS, Gao X. Pax6 haploinsufficiency causes abnormal metabolic homeostasis by downregulating glucagon-like peptide 1 in mice. Endocrinology 150: 2136-2144, 2009.
14. Donovan JM, Von Bergmann K, Setchell KD, Isaacsohn J, Pappu AS, Illingworth DR, Olson T, Burke SK. Effects of colesevelam HC1 on sterol and bile acid excretion in patients with type IIa hypercholesterolemia. Dig Dis Sci 50: 1232-1238, 2005.
15. Drucker DJ, Nauck MA. The incretin system: glucagon-like peptide-1 receptor agonists and dipeptidyl peptidase-4 inhibitors in type 2 diabetes. Lancet 368: 1696-1705, 2006.
16. Eissele R, Goke R, Willemer S, Harthus HP, Vermeer H, Arnold R, Goke B. Glucagon-like peptide-1 cells in the gastrointestinal tract and pancreas of rat, pig and man. Eur J Clin Invest 22: 283-291, 1992.
17. Evans DF, Pye G, Bramley R, Clark AG, Dyson TJ, Hardcastle JD. Measurement of gastrointestinal pH profiles in normal ambulant human subjects. Gut 29: 1035-1041, 1988.
18. Garg A, Grundy SM. Cholestyramine therapy for dyslipidemia in noninsulin-dependent diabetes mellitus. A short-term, double-blind, crossover trial. Ann Intern Med 121: 416-422, 1994.
19. Hanus M, Zhorov E. Bile acid salt binding with colesevelam HCl is not affected by suspension in common beverages. J Pharm Sci 95: 2751-2759, 2006.
20. Harach T, Pols TW, Nomura M, Maida A, Watanabe M, Auwerx J, Schoonjans K. TGR5 potentiates GLP-1 secretion in response to anionic exchange resins. Sci Rep 2: 430, 2012.
21. Herrema H, Meissner M, van Dijk TH, Brufau G, Boverhof R, Oosterveer MH, Reijngoud DJ, Muller M, Stellaard F, Groen AK, Kuipers F. Bile salt sequestration induces hepatic de novo lipogenesis through farnesoid X receptor-and liver X receptoralpha-controlled metabolic pathways in mice. Hepatology 51: 906-815, 2010.
22. 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 11: 90-94, 2005.
23. Inagaki T, Choi M, Moschetta A, Peng L, Cummins CL, McDonald JG, Luo G, Jones SA, Goodwin B, Richardson JA, Gerard RD, Repa JJ, Mangelsdorf DJ, Kliewer SA. Fibroblast growth factor 15 functions as an enterohepatic signal to regulate bile acid homeostasis. Cell Metab 2: 217-225, 2005.
24. Insull W Jr. Clinical utility of bile acid sequestrants in the treatment of dyslipidemia: a scientific review. South Med J 99: 257-273, 2006.
25. Ionut V, Hucking K, Liberty IF, Bergman RN. Synergistic effect of portal glucose and glucagon-like peptide-1 to lower systemic glucose and stimulate counter-regulatory hormones. Diabetologia 48: 967-975, 2005.
26. Jiang LI, Collins J, Davis R, Fraser ID, Sternweis PC. Regulation of cAMP responses by the G12/13 pathway converges on adenylyl cyclase VII. J Biol Chem 283: 23429-23439, 2008.
27. Jiang LI, Collins J, Davis R, Lin KM, DeCamp D, Roach T, Hsueh R, Rebres RA, Ross EM, Taussig R, Fraser I, Sternweis PC. Use of a cAMP BRET sensor to characterize a novel regulation of cAMP by the sphingosine 1-phosphate/G13 pathway. J Biol Chem 282: 10576-10584, 2007.
28. Kalaany NY, Gauthier KC, Zavacki AM, Mammen PP, Kitazume T, Peterson JA, Horton JD, Garry DJ, Bianco AC, Mangelsdorf DJ. LXRs regulate the balance between fat storage and oxidation. Cell Metab 1: 231-244, 2005.
29. Kir S, Beddow SA, Samuel VT, Miller P, Previs SF, Suino-Powell K, Xu HE, Shulman GI, Kliewer SA, Mangelsdorf DJ. FGF19 as a postprandial, insulin-independent activator of hepatic protein and glycogen synthesis. Science 331: 1621-1624, 2011.
30. Knauf C, Cani PD, Perrin C, Iglesias MA, Maury JF, Bernard E, Benhamed F, Gremeaux T, Drucker DJ, Kahn CR, Girard J, Tanti JF, Delzenne NM, Postic C, Burcelin R. Brain glucagon-like peptide-1 increases insulin secretion and muscle insulin resistance to favor hepatic glycogen storage. J Clin Invest 115: 3554-3563, 2005.
31. Lamont BJ, Drucker DJ. Differential antidiabetic efficacy of incretin agonists versus DPP-4 inhibition in high fat fed mice. Diabetes 57: 190-198, 2008.
32. Lan H, Vassileva G, Corona A, Liu L, Baker H, Golovko A, Abbondanzo SJ, Hu W, Yang S, Ning Y, Del Vecchio RA, Poulet F, Laverty M, Gustafson EL, Hedrick JA, Kowalski TJ. GPR119 is required for physiological regulation of glucagon-like peptide-1 secretion but not for metabolic homeostasis. J Endocrinol 201: 219-230, 2009.
33. Landau BR, Wahren J, Chandramouli V, Schumann WC, Ekberg K, Kalhan SC. Use of 2H2O for estimating rates of gluconeogenesis. Application to the fasted state. J Clin Invest 95: 172-178, 1995.
34. Larsson LI, Holst J, Hakanson R, Sundler F. Distribution and properties of glucagon immunoreactivity in the digestive tract of various mammals: an immunohistochemical and immunochemical study. Histochemistry 44: 281-290, 1975.
35. Lovshin JA, Drucker DJ. Incretin-based therapies for type 2 diabetes mellitus. Nat Rev Endocrinol 5: 262-269, 2009.
36. Luner PE, Amidon GL. Description and simulation of a multiple mixing tank model to predict the effect of bile sequestrants on bile salt excretion. J Pharm Sci 82: 311-318, 1993.
37. Marina AL, Utzschneider KM, Wright LA, Montgomery BK, Marcovina SM, Kahn SE. Colesevelam improves oral but not intravenous glucose tolerance by a mechanism independent of insulin sensitivity and β-cell function. Diabetes Care 35: 1119-1125, 2012.
38. Meissner M, Herrema H, van Dijk TH, Gerding A, Havinga R, Boer T, Müller M, Reijngoud DJ, Groen AK, Kuipers F. Bile acid sequestration reduces plasma glucose levels in db/db mice by increasing its metabolic clearance rate. PLos One 6: e24564, 2011.
39. Miyawaki K, Yamada Y, Ban N, Ihara Y, Tsukiyama K, Zhou H, Fujimoto S, Oku A, Tsuda K, Toyokuni S, Hiai H, Mizunoya W, Fushiki T, Holst JJ, Makino M, Tashita A, Kobara Y, Tsubamoto Y, Jinnouchi T, Jomori T, Seino Y. Inhibition of gastric inhibitory polypeptide signaling prevents obesity. Nat Med 8: 738-742, 2002.
40. Nakabayashi H, Nishizawa M, Nakagawa A, Takeda R, Niijima A. Vagal hepatopancreatic reflex effect evoked by intraportal appearance of tGLP-1. Am J Physiol Endocrinol Metab 271: E808-E813, 1996.
41. Nishizawa M, Nakabayashi H, Uchida K, Nakagawa A, Niijima A. The hepatic vagal nerve is receptive to incretin hormone glucagon-like peptide-1, but not to glucose-dependent insulinotropic polypeptide, in the portal vein. J Auton Nerv Syst 61: 149-154, 1996.
42. Out C, Groen AK, Brufau G. Bile acid sequestrants: more than simple resins. Curr Opin Lipidol 23: 43-55, 2012.
43. 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 165: 414-423, 2012.
44. Pols TW, Noriega LG, Nomura M, Auwerx J, Schoonjans K. The bile acid membrane receptor TGR5: a valuable metabolic target. Dig Dis 29: 37-44, 2011.
45. Potthoff MJ, Boney-Montoya J, Choi M, He T, Sunny NE, Satapati S, Suino-Powell K, Xu HE, Gerard RD, Finck BN, Burgess SC, Mangelsdorf DJ, Kliewer SA. FGF15/19 Regulates Hepatic Glucose Metabolism by Inhibiting the CREB-PGC-1alpha Pathway. Cell Metab 13: 729-738, 2011.
46. Potthoff MJ, Inagaki T, Satapati S, Ding X, He T, Goetz R, Mohammadi M, Finck BN, Mangelsdorf DJ, Kliewer SA, Burgess SC. FGF21 induces PGC-1alpha and regulates carbohydrate and fatty acid metabolism during the adaptive starvation response. Proc Natl Acad Sci USA 106: 10853-10858, 2009.
47. Prawitt J, Abdelkarim M, Stroeve JHM, Popescu I, Duez H, Velagapudi VR, Dumont J, Bouchaert E, van Dijk TH, Lucas A, Dorchies E, Daoudi M, Lestavel S, Gonzalez FJ, Oresic M, Cariou B, Kuipers F, Caron S, Staels B. Farnesoid X receptor deficiency improves glucose homeostasis in mouse models of obesity. Diabetes 60: 1861-1871, 2011.
48. Rafferty EP, Wylie AR, Hand KH, Elliott CE, Grieve DJ, Green BD. Investigating the effects of physiological bile acids on GLP-1 secretion and glucose tolerance in normal and GLP-1R(-/-) mice. Biol Chem 392: 539-546, 2011.
49. Russell DW. The enzymes, regulation, and genetics of bile acid synthesis. Annu Rev Biochem 72: 137-174, 2003.
50. Sandoval DA, Bagnol D, Woods SC, D'Alessio DA, Seeley RJ. Arcuate glucagon-like peptide 1 receptors regulate glucose homeostasis but not food intake. Diabetes 57: 2046-2054, 2008.
51. Shang Q, Saumoy M, Holst JJ, Salen G, Xu G. Colesevelam improves insulin resistance in a diet-induced obesity (F-DIO) rat model by increasing the release of GLP-1. Am J Physiol Gastrointest Liver Physiol 298: G419-G424, 2010.
52. 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 102: 731-744, 2000.
53. Sunny NE, Bequette BJ. Gluconeogenesis differs in developing chick embryos derived from small compared with typical size broiler breeder eggs. J Anim Sci 88: 912-921, 2010.
54. Thomas C, Gioiello A, Noriega L, Strehle A, Oury J, Rizzo G, Macchiarulo A, Yamamoto H, Mataki C, Pruzanski M, Pellicciari R, Auwerx J, Schoonjans K. TGR5-mediated bile acid sensing controls glucose homeostasis. Cell Metab 10: 167-177, 2009.
55. Vassileva G, Golovko A, Markowitz L, Abbondanzo SJ, Zeng M, Yang S, Hoos L, Tetzloff G, Levitan D, Murgolo NJ, Keane K, Davis HR Jr, Hedrick J, Gustafson EL. Targeted deletion of Gpbar1 protects mice from cholesterol gallstone formation. Biochem J 398: 423-430, 2006.
56. Watanabe M, Morimoto K, Houten SM, Kaneko-Iwasaki N, Sugizaki T, Horai Y, Mataki C, Sato H, Murahashi K, Arita E, Schoonjans K, Suzuki T, Itoh H, Auwerx J. Bile acid binding resin improves metabolic control through the induction of energy expenditure. PLos One 7: e38286, 2012.
57. Yoder SM, Yang Q, Kindel TL, Tso P. Stimulation of incretin secretion by dietary lipid: is it dose dependent? Am J Physiol Gastrointest Liver Physiol 297: G299-G305, 2009.