Influence on expression of MG53 protein in skeletal muscle tissue of non-obese type 2 diabetic mellitus rats after gastric bypass operation_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

GONG Shuai ¹ , ZHANG Pengbo ¹ , ZHANG Chong ¹ , WU Nai ¹ , ZHANG Yi ¹ , ZHANG Xiuzhong ¹ , MENG Fanchao ² , QI Yanwei ² ,  REN Zeqiang ¹

1. Department of General Surgery, Affiliated Hospital of Xuzhou Medical University, Xuzhou, Jiangsu 221000, P. R. China;
2. Graduate School of Xuzhou Medical University, Xuzhou, Jiangsu 221002, P. R. China;

Corresponding author：

REN Zeqiang, Email: rzq0805@163.com

Keywords：

type 2 diabetes mellitus; gastric bypass operation; mitsugumin53; insulin receptor substrate 1; E3 ubiquitin ligase; insulin resistance

DOI：

10.7507/1007-9424.201908050

Video：

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Objective To observe expressions of E3 ubiquitin ligase—mitsugmin53 (MG53) protein, MG53 mRNA, and insulin receptor substrate 1 (IRS-1) mRNA in skeletal muscle of non-obese type 2 diabetic mellitus (T2DM) rats after gastric bypass operation (GBP), and to investigate possible mechanism of GBP in improving insulin resistance.Methods Twenty-four healthy male GK rats were randomly divided into diabetic operation group, diabetic sham operation group, and diabetic control group, 8 rats in each group; besides, 8 male Wistar rats were served as normal control group. The expressions of MG53 protein in skeletal muscle tissue were detected by using Western blot method on week8 after operation. The mRNA levels of IRS-1 and MG53 in skeletal muscles tissue were measured by RT-PCR methods on week 8 after operation.Results ① The expressions of MG53 protein and MG53 mRNA in the diabetic sham operation group and diabetic control group were significantly higher than those in the diabetic operation group and the normal control group on week 8 after operation (P<0.05), respectively, which had no significant differences between the diabetic operation group and the normal control group (P>0.05), and between the diabetic sham operation group and the diabetic control group (P>0.05) on week 8 after surgery. ② Compared with the normal control group, the expression of IRS-1 mRNA was significantly decreased in the diabetic operation group, the diabetic sham operation group, and the diabetic control group (P<0.05), while there were no significant differences between the diabetic operation group, diabetic sham operation group, and the diabetic control group on week 8 after operation (P>0.05).Conclusion Expression of E3 ubiquitin ligase—MG53 protein in skeletal muscle tissue in T2DM rats following GBP is decreased, thus reduces the IRS-1 ubiquitin-degradation, increase the expression of IRS-1 protein in insulin signaling pathway of skeletal muscle tissue, and improve insulin resistance of skeletal muscle.

Citation： GONG Shuai, ZHANG Pengbo, ZHANG Chong, WU Nai, ZHANG Yi, ZHANG Xiuzhong, MENG Fanchao, QI Yanwei, REN Zeqiang. Influence on expression of MG53 protein in skeletal muscle tissue of non-obese type 2 diabetic mellitus rats after gastric bypass operation. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2020, 27(4): 448-453. doi: 10.7507/1007-9424.201908050 Copy

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2.	Mingrone G, Panunzi S, De Gaetano A, et al. Bariatric surgery versus conventional medical therapy for type 2 diabetes. N Engl J Med, 2012, 366(17): 1577-1585.
3.	温雨晴, 谭迎春, 张蓬波, 等. 胃转流术对2型糖尿病大鼠脂肪组织胰岛素抵抗的影响. 中华实验外科杂志, 2013, 30(11): 2324-2326.
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5.	张秀忠, 任泽强, 张蓬波. 胃转流术对2型糖尿病大鼠的降糖作用及对糖耐量和胰岛素抵抗的影响. 中华实验外科杂志, 2010, 27(12): 1892-1894.
6.	何劲松, 张井潇, 李利发, 等. 空回肠旁路术对2型糖尿病大鼠骨骼肌蛋白酪氨酸磷酸酶1B表达的影响. 中国普外基础与临床杂志, 2016, 23(8): 910-914.
7.	Song R, Peng W, Zhang Y, et al. Central role of E3 ubiquitin ligase MG53 in insulin resistance and metabolic disorders. Nature, 2013, 494(7437): 375-379.
8.	Blaak EE. Metabolic fluxes in skeletal muscle in relation to obesity and insulin resistance. Best Pract Res Clin Endocrinol Metab, 2005, 19(3): 391-403.
9.	龚帅, 任泽强, 张蓬波, 等. 胃转流术对非肥胖型2型糖尿病大鼠骨骼肌胰岛素受体底物-1及泛素化蛋白表达的影响. 中国普外基础与临床杂志, 2016, 23(8): 915-921.
10.	Lima MM, Pareja JC, Alegre SM, et al. Acute effect of roux-en-y gastric bypass on whole-body insulin sensitivity: a study with the euglycemic-hyperinsulinemic clamp. J Clin Endocrinol Metab, 2010, 95(8): 3871-3875.
11.	Rubino F, Forgione A, Cummings DE, et al. The mechanism of diabetes control after gastrointestinal bypass surgery reveals a role of the proximal small intestine in the pathophysiology of type 2 diabetes. Ann Surg, 2006, 244(5): 741-749.
12.	Ramos AC, Galvão Neto MP, de Souza YM, et al. Laparoscopic duodenal-jejunal exclusion in the treatment of type 2 diabetes mellitus in patients with BMI <30 kg/m² (LBMI). Obes Surg, 2009, 19(3): 307-312.
13.	Rubino F, Marescaux J. 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, 239(1): 1-11.
14.	张新国, 杨学军, 徐红, 等. 胃旁路手术治疗Ⅱ型糖尿病的体会. 中华普通外科杂志, 2005, 20(9): 599.
15.	王瑜, 王燕婷, 王烈. 胃转流术对非肥胖型2型糖尿病的治疗作用. 中国普通外科杂志, 2008, 17(10): 1003-1006.
16.	Han H, Wang L, Du H, et al. Expedited biliopancreatic juice flow to the distal gut benefits the diabetes control after duodenal-jejunal bypass. Obes Surg, 2015, 25(10): 1802-1809.
17.	李正才, 石志平, 莫涛, 等. 空回肠旁路术治疗2型糖尿病24例疗效观察. 临床外科杂志, 2018, 26(1): 45-46.
18.	万鹏, 王瑜. 十二指肠空肠旁路术及迷走神经肝支对非肥胖2型糖尿病大鼠糖代谢的影响. 中国普外基础与临床杂志, 2015, 22(5): 565-570.
19.	洪智, 黄鹤, 张起维, 等. 不同Roux肠袢长度的十二指肠空肠旁路术对2型糖尿病模型大鼠糖代谢的影响. 沈阳医学院学报, 2019, 21(4): 299-304.
20.	Gagliani N, Jofra T, Posgai AL, et al. Immune depletion in combination with allogeneic islets permanently restores tolerance to self-antigens in diabetic NOD mice. PLoS One, 2015, 10(11): e0142318.
21.	Bonfleur ML, Ribeiro RA, Pavanello A, et al. Duodenal-jejunal bypass restores insulin action and beta-cell function in hypothalamic-obese rats. Obes Surg, 2015, 25(4): 656-665.
22.	Dong X, Park S, Lin X, et al. Irs1 and Irs2 signaling is essential for hepatic glucose homeostasis and systemic growth. J Clin Invest, 2006, 116(1): 101-114.
23.	Grundy SM. Metabolic syndrome: connecting and reconciling cardiovascular and diabetes worlds. J Am Coll Cardiol, 2006, 47(6): 1093-1100.
24.	DeFronzo RA, Tripathy D. Skeletal muscle insulin resistance is the primary defect in type 2 diabetes. Diabetes Care, 2009, 32(Suppl 2): S157-S163.
25.	Goodyear LJ, Giorgino F, Sherman LA, et al. Insulin receptor phosphorylation, insulin receptor substrate-1 phosphorylation, and phosphatidylinositol 3-kinase activity are decreased in intact skeletal muscle strips from obese subjects. J Clin Invest, 1995, 95(5): 2195-2204.
26.	Caro JF, Ittoop O, Pories WJ, et al. Studies on the mechanism of insulin resistance in the liver from humans with noninsulin-dependent diabetes. Insulin action and binding in isolated hepatocytes, insulin receptor structure, and kinase activity. J Clin Invest, 1986, 78(1): 249-258.
27.	Rome S, Meugnier E, Vidal H. The ubiquitin-proteasome pathway is a new partner for the control of insulin signaling. Curr Opin Clin Nutr Metab Care, 2004, 7(3): 249-254.
28.	Laustsen PG, Russell SJ, Cui L, et al. Essential role of insulin and insulin-like growth factor 1 receptor signaling in cardiac development and function. Mol Cell Biol, 2007, 27(5): 1649-1664.

1. Schauer PR, Kashyap SR, Wolski K, et al. Bariatric surgery versus intensive medical therapy in obese patients with diabetes. N Engl J Med, 2012, 366(17): 1567-1576.
2. Mingrone G, Panunzi S, De Gaetano A, et al. Bariatric surgery versus conventional medical therapy for type 2 diabetes. N Engl J Med, 2012, 366(17): 1577-1585.
3. 温雨晴, 谭迎春, 张蓬波, 等. 胃转流术对2型糖尿病大鼠脂肪组织胰岛素抵抗的影响. 中华实验外科杂志, 2013, 30(11): 2324-2326.
4. 张蓬波, 陈守坤, 张秀忠, 等. 胃转流术对2型糖尿病大鼠肝组织胰岛素受体底物-2、葡萄糖转运体-2表达的影响. 中华实验外科杂志, 2013, 30(12): 2587-2589.
5. 张秀忠, 任泽强, 张蓬波. 胃转流术对2型糖尿病大鼠的降糖作用及对糖耐量和胰岛素抵抗的影响. 中华实验外科杂志, 2010, 27(12): 1892-1894.
6. 何劲松, 张井潇, 李利发, 等. 空回肠旁路术对2型糖尿病大鼠骨骼肌蛋白酪氨酸磷酸酶1B表达的影响. 中国普外基础与临床杂志, 2016, 23(8): 910-914.
7. Song R, Peng W, Zhang Y, et al. Central role of E3 ubiquitin ligase MG53 in insulin resistance and metabolic disorders. Nature, 2013, 494(7437): 375-379.
8. Blaak EE. Metabolic fluxes in skeletal muscle in relation to obesity and insulin resistance. Best Pract Res Clin Endocrinol Metab, 2005, 19(3): 391-403.
9. 龚帅, 任泽强, 张蓬波, 等. 胃转流术对非肥胖型2型糖尿病大鼠骨骼肌胰岛素受体底物-1及泛素化蛋白表达的影响. 中国普外基础与临床杂志, 2016, 23(8): 915-921.
10. Lima MM, Pareja JC, Alegre SM, et al. Acute effect of roux-en-y gastric bypass on whole-body insulin sensitivity: a study with the euglycemic-hyperinsulinemic clamp. J Clin Endocrinol Metab, 2010, 95(8): 3871-3875.
11. Rubino F, Forgione A, Cummings DE, et al. The mechanism of diabetes control after gastrointestinal bypass surgery reveals a role of the proximal small intestine in the pathophysiology of type 2 diabetes. Ann Surg, 2006, 244(5): 741-749.
12. Ramos AC, Galvão Neto MP, de Souza YM, et al. Laparoscopic duodenal-jejunal exclusion in the treatment of type 2 diabetes mellitus in patients with BMI <30 kg/m² (LBMI). Obes Surg, 2009, 19(3): 307-312.
13. Rubino F, Marescaux J. 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, 239(1): 1-11.
14. 张新国, 杨学军, 徐红, 等. 胃旁路手术治疗Ⅱ型糖尿病的体会. 中华普通外科杂志, 2005, 20(9): 599.
15. 王瑜, 王燕婷, 王烈. 胃转流术对非肥胖型2型糖尿病的治疗作用. 中国普通外科杂志, 2008, 17(10): 1003-1006.
16. Han H, Wang L, Du H, et al. Expedited biliopancreatic juice flow to the distal gut benefits the diabetes control after duodenal-jejunal bypass. Obes Surg, 2015, 25(10): 1802-1809.
17. 李正才, 石志平, 莫涛, 等. 空回肠旁路术治疗2型糖尿病24例疗效观察. 临床外科杂志, 2018, 26(1): 45-46.
18. 万鹏, 王瑜. 十二指肠空肠旁路术及迷走神经肝支对非肥胖2型糖尿病大鼠糖代谢的影响. 中国普外基础与临床杂志, 2015, 22(5): 565-570.
19. 洪智, 黄鹤, 张起维, 等. 不同Roux肠袢长度的十二指肠空肠旁路术对2型糖尿病模型大鼠糖代谢的影响. 沈阳医学院学报, 2019, 21(4): 299-304.
20. Gagliani N, Jofra T, Posgai AL, et al. Immune depletion in combination with allogeneic islets permanently restores tolerance to self-antigens in diabetic NOD mice. PLoS One, 2015, 10(11): e0142318.
21. Bonfleur ML, Ribeiro RA, Pavanello A, et al. Duodenal-jejunal bypass restores insulin action and beta-cell function in hypothalamic-obese rats. Obes Surg, 2015, 25(4): 656-665.
22. Dong X, Park S, Lin X, et al. Irs1 and Irs2 signaling is essential for hepatic glucose homeostasis and systemic growth. J Clin Invest, 2006, 116(1): 101-114.
23. Grundy SM. Metabolic syndrome: connecting and reconciling cardiovascular and diabetes worlds. J Am Coll Cardiol, 2006, 47(6): 1093-1100.
24. DeFronzo RA, Tripathy D. Skeletal muscle insulin resistance is the primary defect in type 2 diabetes. Diabetes Care, 2009, 32(Suppl 2): S157-S163.
25. Goodyear LJ, Giorgino F, Sherman LA, et al. Insulin receptor phosphorylation, insulin receptor substrate-1 phosphorylation, and phosphatidylinositol 3-kinase activity are decreased in intact skeletal muscle strips from obese subjects. J Clin Invest, 1995, 95(5): 2195-2204.
26. Caro JF, Ittoop O, Pories WJ, et al. Studies on the mechanism of insulin resistance in the liver from humans with noninsulin-dependent diabetes. Insulin action and binding in isolated hepatocytes, insulin receptor structure, and kinase activity. J Clin Invest, 1986, 78(1): 249-258.
27. Rome S, Meugnier E, Vidal H. The ubiquitin-proteasome pathway is a new partner for the control of insulin signaling. Curr Opin Clin Nutr Metab Care, 2004, 7(3): 249-254.
28. Laustsen PG, Russell SJ, Cui L, et al. Essential role of insulin and insulin-like growth factor 1 receptor signaling in cardiac development and function. Mol Cell Biol, 2007, 27(5): 1649-1664.

CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Influence on expression of MG53 protein in skeletal muscle tissue of non-obese type 2 diabetic mellitus rats after gastric bypass operation

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