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

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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.

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References

  1. 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.

    Article  PubMed  Google Scholar 

  2. 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.

    Article  PubMed  Google Scholar 

  3. 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.

    Article  CAS  PubMed  Google Scholar 

  4. 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.

    PubMed  PubMed Central  Google Scholar 

  5. 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.

    Article  PubMed  Google Scholar 

  6. 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.

    Article  PubMed  Google Scholar 

  7. 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.

    Article  PubMed  Google Scholar 

  8. Angrisani L, Santonicola A, Iovino P, et al. Bariatric surgery worldwide 2013. Obes Surg. 2015

  9. Himpens J, Dobbeleir J, Peeters G. Long-term results of laparoscopic sleeve gastrectomy for obesity. Ann Surg. 2010;252(2):319–24.

    Article  PubMed  Google Scholar 

  10. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. 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.

    Article  CAS  PubMed  Google Scholar 

  12. 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.

    Article  CAS  Google Scholar 

  13. 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.

    Article  PubMed  Google Scholar 

  14. de Aguiar Vallim TQ, Tarling EJ, Edwards PA. Pleiotropic roles of bile acids in metabolism. Cell Metab. 2013;17(5):657–69.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Li T, Chiang JYL. Bile acids as metabolic regulators. Curr Opin Gastroenterol. 2015;31(2):159–65.

    Article  PubMed  PubMed Central  Google Scholar 

  16. 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.

    Article  CAS  PubMed  Google Scholar 

  17. 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.

    Article  CAS  PubMed  Google Scholar 

  18. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  19. 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.

    Article  CAS  PubMed  Google Scholar 

  20. 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.

    Article  PubMed  Google Scholar 

  21. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. 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.

    Article  CAS  PubMed  Google Scholar 

  23. Zwicker BL, Agellon LB. Transport and biological activities of bile acids. Int J Biochem Cell Biol. 2013;45(7):1389–98.

    Article  CAS  PubMed  Google Scholar 

  24. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Trauner M, Boyer JL. Bile salt transporters: molecular characterization, function, and regulation. Physiol Rev. 2003;83(2):633–71.

    Article  CAS  PubMed  Google Scholar 

  26. Dawson PA, Lan T, Rao A. Bile acid transporters. J Lipid Res. 2009;50(12):2340–57.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Ferrannini E, Camastra S, Astiarraga B, et al. Increased bile acid synthesis and deconjugation after biliopancreatic diversion. Diabetes. 2015;64(10):3377–85.

    Article  CAS  PubMed  Google Scholar 

  28. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. 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.

    Article  PubMed  Google Scholar 

  30. 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.

    Article  CAS  PubMed  Google Scholar 

  31. 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.

    Article  CAS  PubMed  Google Scholar 

  32. Hayes KC, Sturman JA. Taurine in metabolism. Annu Rev Nutr. 1981;1:401–25.

    Article  CAS  PubMed  Google Scholar 

  33. Jeevanandam M, Ramias L, Schiller WR. Altered plasma free amino acid levels in obese traumatized man. Metabolism. 1991;40(4):385–90.

    Article  CAS  PubMed  Google Scholar 

  34. 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.

    Article  CAS  PubMed  Google Scholar 

  35. 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.

    Article  CAS  PubMed  Google Scholar 

  36. Carneiro EA, Latorraca MQ, Araujo E, et al. Taurine supplementation modulates glucose homeostasis and islet fanction. J Nutr Biochem. 2009;20(7):503–11.

    Article  CAS  PubMed  Google Scholar 

  37. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. 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.

    Article  PubMed  Google Scholar 

  39. 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.

    Article  CAS  PubMed  Google Scholar 

  40. Rembacz KP, Woudenberg J, Hoekstra M, et al. Unconjugated bile salts shuttle through hepatocyte peroxisomes for taurine conjugation. Hepatology. 2010;52(6):2167–76.

    Article  CAS  PubMed  Google Scholar 

  41. 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.

    Article  CAS  PubMed  Google Scholar 

  42. 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.

    CAS  PubMed  Google Scholar 

  43. Alrefai W, Gill R. Bile acid transporters: structure, function, regulation and pathophysiological implications. Pharm Res. 2007;24(10):1803–23.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Natural Science Foundation of China (no.81270888/H0713, no.81370496/H0308), the Fundamental Research Funds of Shandong University (no. 2014QLKY22), and the Taishan Scholar Foundation.

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Authors and Affiliations

  1. Department of General Surgery, Qilu Hospital of Shandong University, 107# Wenhua Xi Road, Jinan, 250012, Shandong, People’s Republic of China

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

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  1. Qunzheng Wu
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Correspondence to Guangyong Zhang.

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All study protocols were approved by the Animal Care and Utilization Committee of Shandong University.

Conflict of Interest

The authors declare that they have no competing interests.

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All applicable institutional and national guidelines for the care and use of animals were followed.

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Wu, Q., Zhang, X., Zhong, M. et al. Effects of Bariatric Surgery on Serum Bile Acid Composition and Conjugation in a Diabetic Rat Model. OBES SURG 26, 2384–2392 (2016). https://doi.org/10.1007/s11695-016-2087-2

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