Metabolic effects of cholecystectomy: Gallbladder ablation increases basal metabolic rate through G-protein Coupled Bile acid Receptor Gpbar1-dependent mechanisms in mice

PLoS ONE

Volumn 10, Issue 3, 2015, Pages

  Cortés, Víctor ^a   Amigo, Ludwig ^a   Zanlungo, Silvana ^a   Galgani, José ^a   Robledo, Fermín ^a   Arrese, Marco ^a   Bozinovic, Francisco ^b   Nervi, Flavio ^a  

^a PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^b PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

Author keywords

[No Author keywords available]

Indexed keywords

BILE ACID; CHOLESTEROL; CYCLIC AMP; G PROTEIN COUPLED BILE ACID RECEPTOR 1; G PROTEIN COUPLED RECEPTOR; MESSENGER RNA; UNCLASSIFIED DRUG; UNCOUPLING PROTEIN 1; UNCOUPLING PROTEIN 2; UNCOUPLING PROTEIN 3; GPBAR1 PROTEIN, MOUSE; MITOCHONDRIAL PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BASAL METABOLIC RATE; BILIARY TRACT SURGERY; BLOOD SAMPLING; BROWN ADIPOSE TISSUE; CALORIMETRY; CHOLECYSTECTOMY; CHOLESTEROL BILE LEVEL; CIRCADIAN RHYTHM; CONTROLLED STUDY; ENERGY EXPENDITURE; FATTY ACID OXIDATION; GENE EXPRESSION; LIQUID CHROMATOGRAPHY; LIVER; METABOLIC REGULATION; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; SKELETAL MUSCLE; TANDEM MASS SPECTROMETRY; ABLATION THERAPY; ANIMAL; BLOOD; C57BL MOUSE; DEFICIENCY; GALLBLADDER; GENETICS; MALE; METABOLISM; OXIDATION REDUCTION REACTION; SECRETION (PROCESS); SURGERY;

ANIMALIA; MUS;

ABLATION TECHNIQUES; ADIPOSE TISSUE, BROWN; ANIMALS; BASAL METABOLISM; BILE ACIDS AND SALTS; CHOLECYSTECTOMY; CHOLESTEROL; CIRCADIAN RHYTHM; GALLBLADDER; MALE; MICE; MICE, INBRED C57BL; MITOCHONDRIAL PROTEINS; MUSCLE, SKELETAL; OXIDATION-REDUCTION; RECEPTORS, G-PROTEIN-COUPLED; RNA, MESSENGER;

EID: 84928902808     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0118478     Document Type: Article

References (46)

1. Shen C, Wu X, Xu C, Yu C, Chen P, Li Y. Association of cholecystectomy with metabolic syndrome in a Chinese population. PLoS ONE 2014 Feb. 5; 9(2):e88189. doi: 10.1371/journal.pone.0088189 PMID: 24505425
2. Ruhl CE, Everhart JE. Relationship of non-alcoholic fatty liver disease with cholecystectomy in the US population. Am J Gastroenterol 2013;108:952-958. doi: 10.1038/ajg.2013.70 PMID: 23545713
3. Nervi F, Arrese M. Cholecystectomy and NAFLD: does gallbladder removal have metabolic consequences? Am J Gastroenterol 2013;108:959-961. doi: 10.1038/ajg.2013.84 PMID: 23735917
4. Chávez-Tapia NC, Kinney-Novelo IM, Sifuentes-Rentería SE, Torres-Zavala M, Castro-Gastelum G, Sánchez-Lara K, et al. Association between cholecystectomy for gallstone disease and risk factors for cardiovascular disease. Ann Hepatol 2012;11:85-89. PMID: 22166565
5. Ruhl CE, Everhart JE. Gallstone disease is associated with increased mortality in the United States. Gastroenterology 2011;140:508-516. doi: 10.1053/j.gastro.2010.10.060 PMID: 21075109
6. Ioannou GN. Cholelithiasis, cholecystectomy, and liver disease. Am J Gastroenterol 2010;105:1364-1373. doi: 10.1038/ajg.2009.737 PMID: 20068558
7. Amigo L, Husche C, Zanlungo S, Lütjohann D, Arrese M, Miquel JF, et al. Cholecystectomy increases hepatic triglyceride content and very-low-density lipoproteins production in mice. Liver Int 2011;31:52-64. doi: 10.1111/j.1478-3231.2010.02361.x PMID: 21040411
8. Shaffer EA, Small DM. Biliary lipid secretion in cholesterol gallstone disease. The effect of cholecystectomy and obesity. J Clin Invest 1977;59:828-840. PMID: 856870
9. Roda E, Aldini R, Mazzella G, Roda A, Sama C, Festi D, et al. Enterohepatic circulation of bile acids after cholecystectomy. Gut 1978;19:640-649. PMID: 567165
10. Kullak-Ublick G-A, Paumgartner G, Berr F. Long-term effects of cholecystectomy on bile acid metabolism. Hepatology 1995;21:41-45. PMID: 7806167
11. Hylemon PB, Zhou H, Pandak WM, Ren S, Gil G, Dent P. Bile acids as regulatory molecules. J Lipid Res 2009;50:1509-1520. doi: 10.1194/jlr. R900007-JLR200 PMID: 19346331
12. 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. doi: 10.1152/physrev. 00010.2008 PMID: 19126757
13. Trauner M, Claudel T, Fickert P, Moustafa T, Wagner M. Bile acids as regulators of hepatic lipid and glucose metabolism. Dig Dis 2010;28:220-224. doi: 10.1159/000282091 PMID: 20460915
14. Pols T. W. L. G., Nomura M., Auwerx J., Schoonjans K. The bile acid membrane teceptor TGR5 as an emerging target in metabolism and inflammation. J Hepatol 2011;54:1263-1272. doi: 10.1016/j.jhep. 2010.12.004 PMID: 21145931
15. De Aguiar Vallim TQ, Tarling EJ, Edwards PA. Pleiotropic roles of bile acids in metabolism. Cell Metab 2013;17:657-669. doi: 10.1016/j.cmet.2013.03.013 PMID: 23602448
16. Kuipers F, Bloks VW, Groen AK. Beyond intestinal soap-bile acids in metabolic control. Nat Rev Endocrinol 2014;10:488-498. doi: 10.1038/nrendo.2014.60 PMID: 24821328
17. Bjursell M, Wedin M, Admyre T, Hermansson M, Böttcher G, Göransson M, et al. Ageing Fxr deficient mice develop increased energy expenditure, improved glucose control and liver damage resembling NASH. PLoS One 2013 May 20; 8(5):e64721. doi: 10.1371/journal.pone.0064721 PMID: 23700488
18. Maruyama T, Tanaka K, Suzuki J, Miyoshi H, Harada N, Nakamura T, et al. Targeted disruption of G protein-coupled bile acid receptor 1 (Gpbar1/M-Bar) in mice. J Endocrinol 2006;19:197-205.
19. Poole DP, Godfrey C, Cattaruzza F, Cottrell GS, Kirkland JG, Pelayo JC, et al. Expression and function of the bile acid receptor GpBAR1 (TGR5) in the murine enteric nervous system. Neurogastroenterology and Motility 2010;22:814-825. doi: 10.1111/j.1365-2982.2010.01487.x PMID: 20236244
20. Bunnett NW. Neuro-humoral signalling by bile acids and the TGR5 receptor in the gastrointestinal tract. J Physiol 2014;592:2943-2950. doi: 10.1113/jphysiol.2014.271155 PMID: 24614746
21. Watanabe M, Houten SM, Mataki C, Christoffolete MA, Kim BW, Sato H, et al. Bile acid induce energy expenditure by promoting intracellular thyroid hormone activation. Nature 2006;439:484-489. PMID: 16400329
22. Thomas C, Gioiello A, Noriega L, Strehle A, Oury J, Rizzo G, et al. TGR5-mediated bile acid sensing controls glucose homeostasis. Cell Metab 2009;10:167-177. doi: 10.1016/j.cmet.2009.08.001 PMID: 19723493
23. Hulbert AJ, Else PL. Basal metabolic rate: history, composition, regulation, and usefulness. Physiol Biochem Zool 2004;7:869-876.
24. McNab BK. (1997) On the utility of uniformity in the definition of basal rate of metabolism. Physiol Zool 70:718-720. PMID: 9361146
25. Rolfe DF, Brown GC. Cellular energy utilization and molecular origin of standard metabolic rate in mammals. Physiol Rev 1997;77:731-758. PMID: 9234964
26. Palou A., Remesar X, Arola L, Herrera E, Alemany M. Metabolic effects of short-term food deprivation in the rat. Horm Metab Res 1981;13:326-30. PMID: 7262833
27. Le Boeuf RC, Caldwell M, Kirk E. Regulation by nutritional status of lipids and apolipoproteins A-I, A-II, and A-IV in inbred mice. J Lipid Res 1994;35:121-133. PMID: 8138713
28. Alnouti Y, Csanaky IL, Klaassen CD. Quantitative-profiling of bile acids and their conjugates in mouse liver, bile, plasma, and urine using LC MS/MS. J Chromatogr B Analyt Technol Biomed Life Sci 2008;873:209-217. doi: 10.1016/j.jchromb.2008.08.018 PMID: 18801708
29. Nespolo R. F., Bacigalupe L. D., Bozinovic F. The influence of heat increment of feeding on basal metabolic rate in Phyllotis darwini (Muridae). Comp Biochem Physiol 2003;134:139-145.
30. Veloso C., Bozinovic F. Dietary and digestive constraints on basal energy metabolism in a small herbivorous rodent. Ecology 1993;74:2003-2010.
31. Veerkamp JH, Van Moerkerk TB, Glatz JF, Zuurveld JG, Jacobs AE, Wagenmakers AJ. 14CO2 production is no adequate measure of [14C] fatty acid oxidation. Biochem Med Metab Biol 1986;35:248-259. PMID: 3087394
32. Nervi F., Marinovic I., Rigotti A., Ulloa N. Regulation of biliary cholesterol secretion. Functional relationship between the canalicular and sinusoidal cholesterol secretory pathways in the rat. J Clin Invest 1988;82:1818-1825. PMID: 3198756
33. Keitel V, Häussinger D. TGR5 in the biliary tree. Dig Dis. 2011;29:45-47. doi: 10.1159/000324127 PMID: 21691103
34. Li T, Holmstrom SR, Kir S, Umetani M, Schmidt DR, Kliewer SA, et al. The G protein-coupled bile acid receptor, TGR5, stimulates gallbladder filling. Mol Endocrinol 2011;25:1066-1071. doi: 10.1210/me. 2010-0460 PMID: 21454404
35. Dawson PA, Karpen SJ. (2014). Intestinal Transport and Metabolism of Bile Acids. J Lipid Res. 2014 10. pii: jlr. R054114
36. Chiang JY. Bile acid metabolism and signaling. Compr Physiol 2013;3:1191-1212. doi: 10.1002/cphy. c120023 PMID: 23897684
37. Erlinger S. Does Na+-K+-atpase have any role in bile secretion? Am J Physiol 1982;243:G243-247. PMID: 6289678
38. Yu XH, Qian K, Jiang N, Zheng XL, Cayabyab FS, Tang CK, et al. ABCG5/ABCG8 in cholesterol excretion and atherosclerosis. Clin Chim Acta. 2014;428:82-88. doi: 10.1016/j.cca.2013.11.010 PMID: 24252657
39. Dikkers A, Tietge UJ. (2010) Biliary cholesterol secretion: more than a simple ABC. World J Gastroenterol 16:5936-5945. PMID: 21157969
40. Zanlungo S, Rigotti A, Nervi F. Hepatic cholesterol transport from plasma into bile: implications for gallstone disease. Curr Opin Lipidol 2004;15:279-286. PMID: 15166783
41. Rao A, Haywood J, Craddock AL, Belinsky MG, Kruh GD, Dawson PA. The organic solute transporter alpha-beta, Ostalpha-Ostbeta, is essential for intestinal bile acid transport and homeostasis. Proc Natl Acad Sci USA 2008;105:3891-3896. doi: 10.1073/pnas.0712328105 PMID: 18292224
42. Soroka CJ, Ballatori N, Boyer JL. Organic solute transporter, OSTalpha-OSTbeta: its role in bile acid transport and cholestasis. Semin Liver Dis 2010:30:178-185. doi: 10.1055/s-0030-1253226 PMID: 20422499
43. Watanabe M, Morimoto K, Houten SM, Kaneko-Iwasaki N, Sugizaki T, et al. (2012) Bile acid binding resin improves metabolic control through the induction of energy expenditure. Plos One 7(8):e38286. doi: 10.1371/journal.pone.0038286 PMID: 22952571
44. Watanabe M, Horai Y, Houten SM, Morimoto K, Sugizaki T, Arita E, et al. Lowering bile acid pool size with a synthetic farnesoid X receptor (FXR) agonist induces obesity and diabetes through reduced energy expenditure. J Biol Chem 2011;286:26913-26920. doi: 10.1074/jbc. M111.248203 PMID: 21632533
45. Brufau G, Stellaard F, Prado K, Bloks VW, Jonkers E, Boverhof R, et al. Improved glycemic control with colesevelam treatment in patients with type 2 diabetes is not directly associated with changes in bile acid metabolism. Hepatology 2010;52:1455-1464. doi: 10.1002/hep. 23831 PMID: 20725912
46. Brufau G, Bahr MJ, Staels B, Claudel T, Ockenga J, Böker KH, et al. (2010) Plasma bile acids are not associated with energy metabolism in humans. Nutr Metab (Lond). 2010 Sep. 3; 7:73. doi: 10.1186/1743-7075-7-73