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Published in: Obesity Surgery 11/2017

01-11-2017 | Original Contributions

Effects of Sleeve Gastrectomy on Serum 12α-Hydroxylated Bile Acids in a Diabetic Rat Model

Authors: Minggang Wang, Qunzheng Wu, Haibin Xie, Yi Shao, Mingwei Zhong, Xiang Zhang, Shaozhuang Liu, Xiao He, Sanyuan Hu, Guangyong Zhang

Published in: Obesity Surgery | Issue 11/2017

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Abstract

Background

Diabetes mellitus is a prevalent disease that endangers human health. Bariatric surgery can effectively relieve insulin resistance with elevated serum bile acids (BAs). 12α-Hydroxylated BAs were previously reported to be associated with insulin resistance. The aim of this study was to analyze changes in 12α-hydroxylated BA composition and possible associated mechanisms in diabetic rats following sleeve gastrectomy (SG).

Methods

SG and sham operations were performed in diabetic rats induced by high-fat diet feeding and streptozotocin. Body weight, food intake, oral glucose tolerance test (OGTT), insulin tolerance test (ITT), and serum BAs were analyzed at corresponding time points. Cholesterol 12α-hydroxylase (CYP8B1) and transcription factor V-Maf Avian Musculoaponeurotic Fibrosarcoma Oncogene Homolog G (MAFG) expression levels were assessed by RT-PCR and western blotting.

Results

Compared with the SHAM group, the SG group displayed significant weight loss from 6 weeks postoperatively, accompanied by decreased food intake from 4 weeks after the operation. At 2 and 12 weeks postoperatively, the areas under the curve of OGTT and ITT were significantly decreased in the SG group. At 12 weeks post-operation, the SG group displayed elevated serum BAs, but the percentage of 12α-hydroxylated BAs was reduced. Furthermore, SG rats exhibited higher MAFG and lower CYP8B1 protein and mRNA levels in the liver (P < 0.05).

Conclusion

The percentage of 12α-hydroxylated bile acids was reduced after SG, which was relevant with the inhibition of CYP8B1 and overexpression of MAFG. These outcomes may play an important role in the improvement of insulin sensitivity following SG.
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 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.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.PubMedPubMedCentral
3.
go back to reference Standards of medical care in diabetes-2016: summary of revisions. Diabetes Care. 2016;39 Suppl 1:S4-5. Standards of medical care in diabetes-2016: summary of revisions. Diabetes Care. 2016;39 Suppl 1:S4-5.
4.
go back to reference Rubino F, Nathan DM, Eckel RH, et al. Metabolic surgery in the treatment algorithm for type 2 diabetes: a joint statement by international diabetes organizations. Diabetes Care. 2016;39(6):861–77.CrossRefPubMed Rubino F, Nathan DM, Eckel RH, et al. Metabolic surgery in the treatment algorithm for type 2 diabetes: a joint statement by international diabetes organizations. Diabetes Care. 2016;39(6):861–77.CrossRefPubMed
5.
go back to reference Angrisani L, Santonicola A, Iovino P, et al. Bariatric surgery worldwide 2013. Obes Surg. 2015;25(10):1822–32.CrossRefPubMed Angrisani L, Santonicola A, Iovino P, et al. Bariatric surgery worldwide 2013. Obes Surg. 2015;25(10):1822–32.CrossRefPubMed
6.
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
7.
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
8.
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
9.
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
11.
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
12.
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
14.
go back to reference Haeusler RA, Astiarraga B, Camastra S, et al. Human insulin resistance is associated with increased plasma levels of 12alpha-hydroxylated bile acids. Diabetes. 2013;62(12):4184–91.CrossRefPubMedPubMedCentral Haeusler RA, Astiarraga B, Camastra S, et al. Human insulin resistance is associated with increased plasma levels of 12alpha-hydroxylated bile acids. Diabetes. 2013;62(12):4184–91.CrossRefPubMedPubMedCentral
15.
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
16.
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
17.
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
18.
go back to reference 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. 2016;26(10):2384–92.CrossRefPubMed 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. 2016;26(10):2384–92.CrossRefPubMed
19.
go back to reference De Aguiar Vallim TQ, Tarling EJ, Ahn H, et al. MAFG is a transcriptional repressor of bile acid synthesis and metabolism. Cell Metab. 2015;21(2):298–310.CrossRefPubMedPubMedCentral De Aguiar Vallim TQ, Tarling EJ, Ahn H, et al. MAFG is a transcriptional repressor of bile acid synthesis and metabolism. Cell Metab. 2015;21(2):298–310.CrossRefPubMedPubMedCentral
20.
go back to reference Burkard I, von Eckardstein A, Rentsch KM. Differentiated quantification of human bile acids in serum by high-performance liquid chromatography-tandem mass spectrometry. J Chromatogr B. 2005;826(1–2):147–59.CrossRef Burkard I, von Eckardstein A, Rentsch KM. Differentiated quantification of human bile acids in serum by high-performance liquid chromatography-tandem mass spectrometry. J Chromatogr B. 2005;826(1–2):147–59.CrossRef
21.
go back to reference Trung VN, Yamamoto H, Yamaguchi T, et al. Effect of sleeve gastrectomy on body weight, food intake, glucose tolerance, and metabolic hormone level in two different rat models: Goto-Kakizaki and diet-induced obese rat. J Surg Res. 2013;185(1):159–65.CrossRefPubMed Trung VN, Yamamoto H, Yamaguchi T, et al. Effect of sleeve gastrectomy on body weight, food intake, glucose tolerance, and metabolic hormone level in two different rat models: Goto-Kakizaki and diet-induced obese rat. J Surg Res. 2013;185(1):159–65.CrossRefPubMed
22.
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
23.
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
24.
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
25.
go back to reference Nagana Gowda GA, Shanaiah N, Cooper A, et al. Bile acids conjugation in human bile is not random: new insights from (1)H-NMR spectroscopy at 800 MHz. Lipids. 2009;44(6):527–35.CrossRefPubMedPubMedCentral Nagana Gowda GA, Shanaiah N, Cooper A, et al. Bile acids conjugation in human bile is not random: new insights from (1)H-NMR spectroscopy at 800 MHz. Lipids. 2009;44(6):527–35.CrossRefPubMedPubMedCentral
26.
go back to reference Denk GU, Kleiss CP, Wimmer R, et al. Tauro-beta-muricholic acid restricts bile acid-induced hepatocellular apoptosis by preserving the mitochondrial membrane potential. Biochem Biophys Res Commun. 2012;424(4):758–64.CrossRefPubMed Denk GU, Kleiss CP, Wimmer R, et al. Tauro-beta-muricholic acid restricts bile acid-induced hepatocellular apoptosis by preserving the mitochondrial membrane potential. Biochem Biophys Res Commun. 2012;424(4):758–64.CrossRefPubMed
27.
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
28.
29.
go back to reference Kaur A, Patankar JV, de Haan W, et al. Loss of Cyp8b1 improves glucose homeostasis by increasing GLP-1. Diabetes. 2015;64(4):1168–79.CrossRefPubMed Kaur A, Patankar JV, de Haan W, et al. Loss of Cyp8b1 improves glucose homeostasis by increasing GLP-1. Diabetes. 2015;64(4):1168–79.CrossRefPubMed
30.
go back to reference Dutia R, Embrey M, O'Brien S, et al. Temporal changes in bile acid levels and 12alpha-hydroxylation after Roux-en-Y gastric bypass surgery in type 2 diabetes. Int J Obes. 2016;40(3):554.CrossRef Dutia R, Embrey M, O'Brien S, et al. Temporal changes in bile acid levels and 12alpha-hydroxylation after Roux-en-Y gastric bypass surgery in type 2 diabetes. Int J Obes. 2016;40(3):554.CrossRef
31.
go back to reference Sachdev S, Wang Q, Billington C, et al. FGF 19 and bile acids increase following Roux-en-Y gastric bypass but not after medical management in patients with type 2 diabetes. Obes Surg. 2016;26(5):957–65.CrossRefPubMedPubMedCentral Sachdev S, Wang Q, Billington C, et al. FGF 19 and bile acids increase following Roux-en-Y gastric bypass but not after medical management in patients with type 2 diabetes. Obes Surg. 2016;26(5):957–65.CrossRefPubMedPubMedCentral
32.
go back to reference Zhang X, Wang Y, Zhong M, et al. Duodenal-jejunal bypass preferentially elevates serum taurine-conjugated bile acids and alters gut microbiota in a diabetic rat model. Obes Surg. 2016;26(8):1890–9.CrossRefPubMed Zhang X, Wang Y, Zhong M, et al. Duodenal-jejunal bypass preferentially elevates serum taurine-conjugated bile acids and alters gut microbiota in a diabetic rat model. Obes Surg. 2016;26(8):1890–9.CrossRefPubMed
Metadata
Title
Effects of Sleeve Gastrectomy on Serum 12α-Hydroxylated Bile Acids in a Diabetic Rat Model
Authors
Minggang Wang
Qunzheng Wu
Haibin Xie
Yi Shao
Mingwei Zhong
Xiang Zhang
Shaozhuang Liu
Xiao He
Sanyuan Hu
Guangyong Zhang
Publication date
01-11-2017
Publisher
Springer US
Published in
Obesity Surgery / Issue 11/2017
Print ISSN: 0960-8923
Electronic ISSN: 1708-0428
DOI
https://doi.org/10.1007/s11695-017-2714-6

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