Skip to main content
Top
Published in: Obesity Surgery 10/2016

01-10-2016 | Original Contributions

Effects of Bariatric Surgery on Serum Bile Acid Composition and Conjugation in a Diabetic Rat Model

Authors: Qunzheng Wu, Xiang Zhang, Mingwei Zhong, Haifeng Han, Shaozhuang Liu, Teng Liu, Meng Wei, Wei Guo, Haibin Xie, Sanyuan Hu, Guangyong Zhang

Published in: Obesity Surgery | Issue 10/2016

Login to get access

Abstract

Background

Serum bile acids (BAs) are elevated following bariatric surgery and have emerged as a potential glucose-lowering beneficial factor. The change of BA components and its underlying mechanisms may be of great significance during bariatric surgery. The aim of this study is to investigate the effects of different bariatric procedures on serum BA composition and explore the potential mechanisms using a diabetic rat model.

Methods

Duodenal-jejunal bypass (DJB), sleeve gastrectomy (SG), and sham operation were performed in diabetic rats induced by high-fat diet (HFD) and streptozotocin (STZ). Body weight, food intake, oral glucose tolerance test (OGTT), and insulin tolerance test (ITT) were measured at indicated time points. Serum BAs composition and the expression of cholesterol 7α hydroxylase (CYP7A1), bile acid: CoA synthase (BACS) and bile acid-CoA: amino acid N-acyltransferase (BAAT) at both transcriptional and protein levels in the liver were evaluated at 12 weeks postoperatively.

Results

Compared with sham group, DJB and SG both achieved rapid and sustained improvements in glucose tolerance and insulin sensitivity. They also resulted in increased serum BAs, especially the taurine-conjugated BAs by elevated conjugation. No obvious difference was detected between DJB and SG except that SG achieved decreased weight gain and food intake.

Conclusions

The preferentially elevated serum taurine-conjugated BAs were similar after different bariatric surgeries, and the enhanced conjugation of BAs in the liver might account for the changed serum BAs profiles.
Literature
1.
go back to reference Whiting DR, Guariguata L, Weil C, et al. IDF diabetes atlas: global estimates of the prevalence of diabetes for 2011 and 2030. Diabetes Res Clin Pract. 2011;94(3):311–21.CrossRefPubMed Whiting DR, Guariguata L, Weil C, et al. IDF diabetes atlas: global estimates of the prevalence of diabetes for 2011 and 2030. Diabetes Res Clin Pract. 2011;94(3):311–21.CrossRefPubMed
2.
go back to reference Buchwald H, Estok R, Fahrbach K, et al. Weight and type 2 diabetes after bariatric surgery: systematic review and meta-analysis. Am J Med. 2009;122(3):248–56. e5.CrossRefPubMed Buchwald H, Estok R, Fahrbach K, et al. Weight and type 2 diabetes after bariatric surgery: systematic review and meta-analysis. Am J Med. 2009;122(3):248–56. e5.CrossRefPubMed
3.
go back to reference Sjostrom L. Review of the key results from the Swedish Obese Subjects (SOS) trial—a prospective controlled intervention study of bariatric surgery. J Intern Med. 2013;273(3):219–34.CrossRefPubMed Sjostrom L. Review of the key results from the Swedish Obese Subjects (SOS) trial—a prospective controlled intervention study of bariatric surgery. J Intern Med. 2013;273(3):219–34.CrossRefPubMed
4.
go back to reference Schauer PR, Burguera B, Ikramuddin S, et al. Effect of laparoscopic Roux-en Y gastric bypass on type 2 diabetes mellitus. Ann Surg. 2003;238(4):467–84. discussion 84–5.PubMedPubMedCentral Schauer PR, Burguera B, Ikramuddin S, et al. Effect of laparoscopic Roux-en Y gastric bypass on type 2 diabetes mellitus. Ann Surg. 2003;238(4):467–84. discussion 84–5.PubMedPubMedCentral
5.
go back to reference Wang TT, Hu SY, Gao HD, et al. Ileal transposition controls diabetes as well as modified duodenal jejunal bypass with better lipid lowering in a nonobese rat model of type II diabetes by increasing GLP-1. Ann Surg. 2008;247(6):968–75.CrossRefPubMed Wang TT, Hu SY, Gao HD, et al. Ileal transposition controls diabetes as well as modified duodenal jejunal bypass with better lipid lowering in a nonobese rat model of type II diabetes by increasing GLP-1. Ann Surg. 2008;247(6):968–75.CrossRefPubMed
6.
go back to reference Liu S, Zhang G, Wang L, et al. The entire small intestine mediates the changes in glucose homeostasis after intestinal surgery in Goto-Kakizaki rats. Ann Surg. 2012;256(6):1049–58.CrossRefPubMed Liu S, Zhang G, Wang L, et al. The entire small intestine mediates the changes in glucose homeostasis after intestinal surgery in Goto-Kakizaki rats. Ann Surg. 2012;256(6):1049–58.CrossRefPubMed
7.
go back to reference Sun D, Liu S, Zhang G, et al. Sub-sleeve gastrectomy achieves good diabetes control without weight loss in a non-obese diabetic rat model. Surg Endosc. 2014;28(3):1010–8.CrossRefPubMed Sun D, Liu S, Zhang G, et al. Sub-sleeve gastrectomy achieves good diabetes control without weight loss in a non-obese diabetic rat model. Surg Endosc. 2014;28(3):1010–8.CrossRefPubMed
8.
go back to reference Angrisani L, Santonicola A, Iovino P, et al. Bariatric surgery worldwide 2013. Obes Surg. 2015 Angrisani L, Santonicola A, Iovino P, et al. Bariatric surgery worldwide 2013. Obes Surg. 2015
9.
go back to reference Himpens J, Dobbeleir J, Peeters G. Long-term results of laparoscopic sleeve gastrectomy for obesity. Ann Surg. 2010;252(2):319–24.CrossRefPubMed Himpens J, Dobbeleir J, Peeters G. Long-term results of laparoscopic sleeve gastrectomy for obesity. Ann Surg. 2010;252(2):319–24.CrossRefPubMed
10.
go back to reference Kohli R, Bradley D, Setchell KD, et al. Weight loss induced by Roux-en-Y gastric bypass but not laparoscopic adjustable gastric banding increases circulating bile acids. J Clin Endocrinol Metab. 2013;98(4):E708–12.CrossRefPubMedPubMedCentral Kohli R, Bradley D, Setchell KD, et al. Weight loss induced by Roux-en-Y gastric bypass but not laparoscopic adjustable gastric banding increases circulating bile acids. J Clin Endocrinol Metab. 2013;98(4):E708–12.CrossRefPubMedPubMedCentral
11.
go back to reference Cummings BP, Bettaieb A, Graham JL, et al. Bile-acid-mediated decrease in endoplasmic reticulum stress: a potential contributor to the metabolic benefits of ileal interposition surgery in UCD-T2DM rats. Dis Model Mech. 2013;6(2):443–56.CrossRefPubMed Cummings BP, Bettaieb A, Graham JL, et al. Bile-acid-mediated decrease in endoplasmic reticulum stress: a potential contributor to the metabolic benefits of ileal interposition surgery in UCD-T2DM rats. Dis Model Mech. 2013;6(2):443–56.CrossRefPubMed
12.
go back to reference Myronovych A, Kirby M, Ryan KK, et al. Vertical sleeve gastrectomy reduces hepatic steatosis while increasing serum bile acids in a weight-loss-independent manner. Obesity (Silver Spring). 2014;22(2):390–400.CrossRef Myronovych A, Kirby M, Ryan KK, et al. Vertical sleeve gastrectomy reduces hepatic steatosis while increasing serum bile acids in a weight-loss-independent manner. Obesity (Silver Spring). 2014;22(2):390–400.CrossRef
13.
go back to reference Han H, Hu C, Wang L, et al. Duodenal-jejunal bypass surgery suppresses hepatic de novo lipogenesis and alleviates liver fat accumulation in a diabetic rat model. Obes Surg. 2014;24(12):2152–60.CrossRefPubMed Han H, Hu C, Wang L, et al. Duodenal-jejunal bypass surgery suppresses hepatic de novo lipogenesis and alleviates liver fat accumulation in a diabetic rat model. Obes Surg. 2014;24(12):2152–60.CrossRefPubMed
16.
go back to reference Fiorucci S, Mencarelli A, Palladino G, et al. Bile-acid-activated receptors: targeting TGR5 and farnesoid-X-receptor in lipid and glucose disorders. Trends Pharmacol Sci. 2009;30(11):570–80.CrossRefPubMed Fiorucci S, Mencarelli A, Palladino G, et al. Bile-acid-activated receptors: targeting TGR5 and farnesoid-X-receptor in lipid and glucose disorders. Trends Pharmacol Sci. 2009;30(11):570–80.CrossRefPubMed
17.
go back to reference Watanabe M, Houten SM, Mataki C, et al. Bile acids induce energy expenditure by promoting intracellular thyroid hormone activation. Nature. 2006;439(7075):484–9.CrossRefPubMed Watanabe M, Houten SM, Mataki C, et al. Bile acids induce energy expenditure by promoting intracellular thyroid hormone activation. Nature. 2006;439(7075):484–9.CrossRefPubMed
18.
go back to reference Patriti A, Facchiano E, Donini A. Effect of duodenal-jejunal exclusion in a non-obese animal model of type 2 diabetes: a new perspective for an old disease. Ann Surg. 2004;240(2):388–9. author reply 9–91.CrossRefPubMedPubMedCentral Patriti A, Facchiano E, Donini A. Effect of duodenal-jejunal exclusion in a non-obese animal model of type 2 diabetes: a new perspective for an old disease. Ann Surg. 2004;240(2):388–9. author reply 9–91.CrossRefPubMedPubMedCentral
19.
go back to reference Srinivasan K, Viswanad B, Asrat L, et al. Combination of high-fat diet-fed and low-dose streptozotocin-treated rat: a model for type 2 diabetes and pharmacological screening. Pharmacol Res. 2005;52(4):313–20.CrossRefPubMed Srinivasan K, Viswanad B, Asrat L, et al. Combination of high-fat diet-fed and low-dose streptozotocin-treated rat: a model for type 2 diabetes and pharmacological screening. Pharmacol Res. 2005;52(4):313–20.CrossRefPubMed
20.
go back to reference Pereferrer FS, Gonzalez MH, Rovira AF, et al. Influence of sleeve gastrectomy on several experimental models of obesity: metabolic and hormonal implications. Obes Surg. 2008;18(1):97–108.CrossRefPubMed Pereferrer FS, Gonzalez MH, Rovira AF, et al. Influence of sleeve gastrectomy on several experimental models of obesity: metabolic and hormonal implications. Obes Surg. 2008;18(1):97–108.CrossRefPubMed
21.
go back to reference Bruinsma BG, Uygun K, Yarmush ML, et al. Surgical models of Roux-en-Y gastric bypass surgery and sleeve gastrectomy in rats and mice. Nat Protoc. 2015;10(3):495–507.CrossRefPubMedPubMedCentral Bruinsma BG, Uygun K, Yarmush ML, et al. Surgical models of Roux-en-Y gastric bypass surgery and sleeve gastrectomy in rats and mice. Nat Protoc. 2015;10(3):495–507.CrossRefPubMedPubMedCentral
22.
go back to reference Kawasaki T, Ohta M, Kawano Y, et al. Effects of sleeve gastrectomy and gastric banding on the hypothalamic feeding center in an obese rat model. Surg Today. 2015;45(12):1560–6.CrossRefPubMed Kawasaki T, Ohta M, Kawano Y, et al. Effects of sleeve gastrectomy and gastric banding on the hypothalamic feeding center in an obese rat model. Surg Today. 2015;45(12):1560–6.CrossRefPubMed
23.
go back to reference Zwicker BL, Agellon LB. Transport and biological activities of bile acids. Int J Biochem Cell Biol. 2013;45(7):1389–98.CrossRefPubMed Zwicker BL, Agellon LB. Transport and biological activities of bile acids. Int J Biochem Cell Biol. 2013;45(7):1389–98.CrossRefPubMed
24.
go back to reference Li T, Owsley E, Matozel M, et al. Transgenic expression of cholesterol 7 alpha-hydroxylase in the liver prevents high-fat diet induced obesity and insulin resistance in mice. Hepatology. 2010;52(2):678–90.CrossRefPubMedPubMedCentral Li T, Owsley E, Matozel M, et al. Transgenic expression of cholesterol 7 alpha-hydroxylase in the liver prevents high-fat diet induced obesity and insulin resistance in mice. Hepatology. 2010;52(2):678–90.CrossRefPubMedPubMedCentral
25.
go back to reference Trauner M, Boyer JL. Bile salt transporters: molecular characterization, function, and regulation. Physiol Rev. 2003;83(2):633–71.CrossRefPubMed Trauner M, Boyer JL. Bile salt transporters: molecular characterization, function, and regulation. Physiol Rev. 2003;83(2):633–71.CrossRefPubMed
27.
go back to reference Ferrannini E, Camastra S, Astiarraga B, et al. Increased bile acid synthesis and deconjugation after biliopancreatic diversion. Diabetes. 2015;64(10):3377–85.CrossRefPubMed Ferrannini E, Camastra S, Astiarraga B, et al. Increased bile acid synthesis and deconjugation after biliopancreatic diversion. Diabetes. 2015;64(10):3377–85.CrossRefPubMed
28.
go back to reference Kohli R, Kirby M, Setchell KD, et al. Intestinal adaptation after ileal interposition surgery increases bile acid recycling and protects against obesity-related comorbidities. Am J Physiol Gastrointest Liver Physiol. 2010;299(3):G652–60.CrossRefPubMedPubMedCentral Kohli R, Kirby M, Setchell KD, et al. Intestinal adaptation after ileal interposition surgery increases bile acid recycling and protects against obesity-related comorbidities. Am J Physiol Gastrointest Liver Physiol. 2010;299(3):G652–60.CrossRefPubMedPubMedCentral
29.
go back to reference Braghetto I, Davanzo C, Korn O, et al. Scintigraphic evaluation of gastric emptying in obese patients submitted to sleeve gastrectomy compared to normal subjects. Obes Surg. 2009;19(11):1515–21.CrossRefPubMed Braghetto I, Davanzo C, Korn O, et al. Scintigraphic evaluation of gastric emptying in obese patients submitted to sleeve gastrectomy compared to normal subjects. Obes Surg. 2009;19(11):1515–21.CrossRefPubMed
30.
go back to reference Sjovall J. Dietary glycine and taurine on bile acid conjugation in man; bile acids and steroids 75. Proc Soc Exp Biol Med. 1959;100(4):676–8.CrossRefPubMed Sjovall J. Dietary glycine and taurine on bile acid conjugation in man; bile acids and steroids 75. Proc Soc Exp Biol Med. 1959;100(4):676–8.CrossRefPubMed
31.
go back to reference Shonsey EM, Wheeler J, Johnson M, et al. Synthesis of bile acid coenzyme a thioesters in the amino acid conjugation of bile acids. Methods Enzymol. 2005;400:360–73.CrossRefPubMed Shonsey EM, Wheeler J, Johnson M, et al. Synthesis of bile acid coenzyme a thioesters in the amino acid conjugation of bile acids. Methods Enzymol. 2005;400:360–73.CrossRefPubMed
33.
go back to reference Jeevanandam M, Ramias L, Schiller WR. Altered plasma free amino acid levels in obese traumatized man. Metabolism. 1991;40(4):385–90.CrossRefPubMed Jeevanandam M, Ramias L, Schiller WR. Altered plasma free amino acid levels in obese traumatized man. Metabolism. 1991;40(4):385–90.CrossRefPubMed
34.
go back to reference Tsuboyama-Kasaoka N, Shozawa C, Sano K, et al. Taurine (2-aminoethanesulfonic acid) deficiency creates a vicious circle promoting obesity. Endocrinology. 2006;147(7):3276–84.CrossRefPubMed Tsuboyama-Kasaoka N, Shozawa C, Sano K, et al. Taurine (2-aminoethanesulfonic acid) deficiency creates a vicious circle promoting obesity. Endocrinology. 2006;147(7):3276–84.CrossRefPubMed
35.
go back to reference Rosa FT, Freitas EC, Deminice R, et al. Oxidative stress and inflammation in obesity after taurine supplementation: a double-blind, placebo-controlled study. Eur J Nutr. 2014;53(3):823–30.CrossRefPubMed Rosa FT, Freitas EC, Deminice R, et al. Oxidative stress and inflammation in obesity after taurine supplementation: a double-blind, placebo-controlled study. Eur J Nutr. 2014;53(3):823–30.CrossRefPubMed
36.
go back to reference Carneiro EA, Latorraca MQ, Araujo E, et al. Taurine supplementation modulates glucose homeostasis and islet fanction. J Nutr Biochem. 2009;20(7):503–11.CrossRefPubMed Carneiro EA, Latorraca MQ, Araujo E, et al. Taurine supplementation modulates glucose homeostasis and islet fanction. J Nutr Biochem. 2009;20(7):503–11.CrossRefPubMed
37.
go back to reference Cummings BP, Bettaieb A, Graham JL, et al. Vertical sleeve gastrectomy improves glucose and lipid metabolism and delays diabetes onset in UCD-T2DM rats. Endocrinology. 2012;153(8):3620–32.CrossRefPubMedPubMedCentral Cummings BP, Bettaieb A, Graham JL, et al. Vertical sleeve gastrectomy improves glucose and lipid metabolism and delays diabetes onset in UCD-T2DM rats. Endocrinology. 2012;153(8):3620–32.CrossRefPubMedPubMedCentral
38.
go back to reference Chong CPK, Mills PB, McClean P, et al. Bile acid-CoA ligase deficiency—a new inborn error of bile acid metabolism. J Inherit Metab Dis. 2012;35(3):521–30.CrossRefPubMed Chong CPK, Mills PB, McClean P, et al. Bile acid-CoA ligase deficiency—a new inborn error of bile acid metabolism. J Inherit Metab Dis. 2012;35(3):521–30.CrossRefPubMed
39.
go back to reference Sayin SI, Wahlstrom A, Felin J, 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):225–35.CrossRefPubMed Sayin SI, Wahlstrom A, Felin J, 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):225–35.CrossRefPubMed
40.
go back to reference Rembacz KP, Woudenberg J, Hoekstra M, et al. Unconjugated bile salts shuttle through hepatocyte peroxisomes for taurine conjugation. Hepatology. 2010;52(6):2167–76.CrossRefPubMed Rembacz KP, Woudenberg J, Hoekstra M, et al. Unconjugated bile salts shuttle through hepatocyte peroxisomes for taurine conjugation. Hepatology. 2010;52(6):2167–76.CrossRefPubMed
41.
go back to reference Fisher E, Nitz I, Lindner I, et al. Candidate gene association study of type 2 diabetes in a nested case–control study of the EPIC-Potsdam cohort—role of fat assimilation. Mol Nutr Food Res. 2007;51(2):185–91.CrossRefPubMed Fisher E, Nitz I, Lindner I, et al. Candidate gene association study of type 2 diabetes in a nested case–control study of the EPIC-Potsdam cohort—role of fat assimilation. Mol Nutr Food Res. 2007;51(2):185–91.CrossRefPubMed
42.
go back to reference Garbutt JT, Wilkins RM, Lack L, et al. Bacterial modification of taurocholate during enterohepatic recirculation in normal man and patients with small intestinal disease. Gastroenterology. 1970;59(4):553–66.PubMed Garbutt JT, Wilkins RM, Lack L, et al. Bacterial modification of taurocholate during enterohepatic recirculation in normal man and patients with small intestinal disease. Gastroenterology. 1970;59(4):553–66.PubMed
43.
go back to reference Alrefai W, Gill R. Bile acid transporters: structure, function, regulation and pathophysiological implications. Pharm Res. 2007;24(10):1803–23.CrossRefPubMed Alrefai W, Gill R. Bile acid transporters: structure, function, regulation and pathophysiological implications. Pharm Res. 2007;24(10):1803–23.CrossRefPubMed
Metadata
Title
Effects of Bariatric Surgery on Serum Bile Acid Composition and Conjugation in a Diabetic Rat Model
Authors
Qunzheng Wu
Xiang Zhang
Mingwei Zhong
Haifeng Han
Shaozhuang Liu
Teng Liu
Meng Wei
Wei Guo
Haibin Xie
Sanyuan Hu
Guangyong Zhang
Publication date
01-10-2016
Publisher
Springer US
Published in
Obesity Surgery / Issue 10/2016
Print ISSN: 0960-8923
Electronic ISSN: 1708-0428
DOI
https://doi.org/10.1007/s11695-016-2087-2

Other articles of this Issue 10/2016

Obesity Surgery 10/2016 Go to the issue