Protective effect of castanospermine on severe acute pancreatitis-induced renal injury in Sprague Dawley rats_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

Nodjimadji Tamlengar Martial ¹ , HONG Yupu ^1,2 , ZHAO Liang ^1,2 , XIANG Mingwei ^1,2 , LI Man ¹ , CHEN Chen ¹ ,  WANG Weixing ¹

1. Department of General Surgery, Renmin Hospital of Wuhan University, Wuhan 430060, P. R. China;
2. Key Laboratory of Hubei Province for Digestive System Disease, Wuhan 430060, P. R. China;

Corresponding author：

WANG Weixing, Email: sate.llite@163.com

Keywords：

acute pancreatitis; renal injury; castanospermine; cytokines; rat

DOI：

10.7507/1007-9424.201703079

Video：

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Objective To investigate the protective effect of castanospermine (CS) on renal injury induced by severe acute pancreatitis (SAP) in rats and its possible mechanism. Methods Twenty-four SPF adult male Sprague Dawley rats were randomly divided into three groups: shame operation group (SO group, n=8), SAP group (n=8), and CS group (n=8). SAP models were induced by retrograde injection of 5% sodium taurocholate (1 mL/kg) in biliopancreatic duct in the SAP group and the CS group. CS solution (200 mg/kg) was immediately administered via intraperitoneal injection after the induction of pancreatitis in the CS group. Rats in the SO group were subjected to a sham surgery that the pancreas and duodenum were flipped a number of times. All rats were sacrificed at 12 h after modeling. Blood samples were collected by inferior vena cava puncture, and serum activities of amylase (AMY), levels of blood urea nitrogen (BUN) and creatinine (Cr) were measured by using a fully automatic chemistry analyzer. The head of pancreas and renal tissues were harvested and pathological change was observed under the light microscope. Expressions of nuclear factor-κB (NF-κB), tumor necrosis factor-α (TNF-α), intercellular adhesion molecule-1 (ICAM-1), and Caspase-3 in renal tissues were evaluated by immunohistochemistry assay. Results ① Compared with the SO group, the damages of the pancreas and kidney tissues were significantly worse in the SAP group, and the above damages in the CS group were significantly decreased when comparing with the SAP group. ② Compared with the SO group, the serum activities of AMY, levels of BUN and Cr were significantly increased in the SAP group (P<0.05). The serum activities of AMY, levels of BUN and Cr in the CS group were significantly lower than those of the SAP group (P<0.05). ③ Compared with the SO group, the integrated optical density (IOD) of NF-κB, TNF-α, ICAM-1, and Caspase-3 in renal tissues were significantly increased in the SAP group (P<0.05), and the above indicators in kidney tissues of the CS group were significantly decreased when comparing with the SAP group (P<0.05). Conclusions CS can mitigate severe acute pancreatitis-induced renal injuries in rats, it ameliorates renal injury and improves renal function. The mechanism for the above improvements is that CS can widely inhibit the activation of NF-κB, and then downregulate the expressions of TNF-α, ICAM-1, and Caspase-3.

Citation： Nodjimadji Tamlengar Martial, HONG Yupu, ZHAO Liang, XIANG Mingwei, LI Man, CHEN Chen, WANG Weixing. Protective effect of castanospermine on severe acute pancreatitis-induced renal injury in Sprague Dawley rats. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2017, 24(10): 1200-1205. doi: 10.7507/1007-9424.201703079 Copy

1.	Pavlidis P, Crichton S, Lemmich Smith J, et al. Improved outcome of severe acute pancreatitis in the intensive care unit. Crit Care Res Pract, 2013, 2013: 897107.
2.	den Dulk M, Wang C, Li J, et al. Combined donor leucocyte administration and immunosuppressive drug treatment for survival of rat heart allografts. Transpl Immunol, 2004, 13(3): 177-184.
3.	Willenborg DO, Parish CR, Cowden WB. Inhibition of experimental allergic encephalomyelitis by the alpha-glucosidase inhibitor castanospermine. J Neurol Sci, 1989, 90(1): 77-85.
4.	Willenborg DO, Parish CR, Cowden WB. Inhibition of adjuvant arthritis in the rat by phosphosugars and the alpha-glucosidase inhibitor castanospermine. Immunol Cell Biol, 1992, 70 (Pt 6): 369-377.
5.	Whitby K, Pierson TC, Geiss B, et al. Castanospermine, a potent inhibitor of dengue virus infection in vitro and in vivo. J Virol, 2005, 79(14): 8698-8706.
6.	Hong YP, Guo WY, Wang WX, et al. 4-phenylbutyric acid attenuates pancreatic beta-cell injury in rats with experimental severe acute pancreatitis. Int J Endocrinol, 2016, 2016: 4592346.
7.	Sporek M, Gala-Błądzińska A, Dumnicka P, et al. Urine NGAL is useful in the clinical evaluation of renal function in the early course of acute pancreatitis. Folia Med Cracov, 2016, 56(1): 13-25.
8.	Zhou J, Li Y, Tang Y, et al. Effect of acute kidney injury on mortality and hospital stay in patient with severe acute pancreatitis. Nephrology (Carlton), 2015, 20(7): 485-491.
9.	Sporek M, Dumnicka P, Gala-Bladzinska A, et al. Angiopoietin-2 is an early indicator of acute pancreatic-renal syndrome in patients with acute pancreatitis. Mediators Inflamm, 2016, 2016: 5780903.
10.	Kim SY, Hwang JS, Han IO. Tunicamycin inhibits Toll-like receptor-activated inflammation in RAW264.7 cells by suppression of NF-κB and c-Jun activity via a mechanism that is independent of ER-stress and N-glycosylation. Eur J Pharmacol, 2013, 721(1-3): 294-300.
11.	Walter S, Fassbender K, Gulbins E, et al. Glycosylation processing inhibition by castanospermine prevents experimental autoimmune encephalomyelitis by interference with IL-2 receptor signal transduction. J Neuroimmunol, 2002, 132(1-2): 1-10.
12.	Durantel D. Celgosivir. An alpha-glucosidase Ⅰ inhibitor for the potential treatment of HCV infection. Curr Opin Investig Drugs, 2009, 10(8): 860-870.
13.	洪育蒲, 郭闻一, 赵亮, 等. 4-苯基丁酸对重症急性胰腺炎大鼠肝损伤的保护作用. 中国普外基础与临床杂志, 2017, 24(1): 18-23.0.
14.	Shi Q, Liao KS, Zhao KL, et al. Hydrogen-rich saline attenuates acute renal injury in sodium taurocholate-induced severe acute pancreatitis by inhibiting ROS and NF-κB pathway. Mediators Inflamm, 2015, 2015: 685043.
15.	惠远见, 王卫星, 余佳, 等. 急性胰腺炎大鼠肾脏中聚腺苷二磷酸核糖聚合酶-1 mRNA 的表达及意义. 中国普外基础与临床杂志, 2010, 17(3): 272-274.0.
16.	Liu Y, Chen XD, Yu J, et al. Deletion of XIAP reduces the severity of acute pancreatitis via regulation of cell death and nuclear factor-κB activity. Cell Death Dis, 2017, 8(3): e2685.
17.	Yang YZ, Xiang Y, Chen M, et al. Clinical significance of dynamic detection for serum levels of MCP-1, TNF-α and IL-8 in patients with acute pancreatitis. Asian Pac J Trop Med, 2016, 9(11): 1111-1114.
18.	Zhang XP, Wang L, Zhou YF. The pathogenic mechanism of severe acute pancreatitis complicated with renal injury: a review of current knowledge. Dig Dis Sci, 2008, 53(2): 297-306.
19.	Wang G, Han B, Zhou H, et al. Inhibition of hydrogen sulfide synthesis provides protection for severe acute pancreatitis rats via apoptosis pathway. Apoptosis, 2013, 18(1): 28-42.
20.	Dabrowski A, Osada J, Dabrowska MI, et al. Increased expression of the intercellular adhesion molecule-1 (ICAM-1) on peripheral blood neutrophils in acute pancreatitis. Adv Med Sci, 2014, 59(1): 102-107.
21.	Tamizhselvi R, Koh YH, Sun J, et al. Hydrogen sulfide induces ICAM-1 expression and neutrophil adhesion to caerulein-treated pancreatic acinar cells through NF-kappaB and Src-family kinases pathway. Exp Cell Res, 2010, 316(9): 1625-1636.
22.	Fan YT, Yin GJ, Xiao WQ, et al. Rosmarinic acid attenuates sodium taurocholate-induced acute pancreatitis in rats by inhibiting nuclear factor-κB activation. Am J Chin Med, 2015, 43(6): 1117-1135.
23.	Lv P, Li HY, Ji SS, et al. Thalidomide alleviates acute pancreatitis-associated lung injury via down-regulation of NFκB induced TNF-α. Pathol Res Pract, 2014, 210(9): 558-564.
24.	Huang H, Liu Y, Daniluk J, et al. Activation of nuclear factor-κB in acinar cells increases the severity of pancreatitis in mice. Gastroenterology, 2013, 144(1): 202-210.
25.	Larsen BD, Sørensen CS. The caspase-activated DNase: apoptosis and beyond. FEBS J, 2017, 284(8): 1160-1170.
26.	Yen JH, Ganea D. Interferon beta induces mature dendritic cell apoptosis through caspase-11/caspase-3 activation. Blood, 2009, 114(7): 1344-1354.

1. Pavlidis P, Crichton S, Lemmich Smith J, et al. Improved outcome of severe acute pancreatitis in the intensive care unit. Crit Care Res Pract, 2013, 2013: 897107.
2. den Dulk M, Wang C, Li J, et al. Combined donor leucocyte administration and immunosuppressive drug treatment for survival of rat heart allografts. Transpl Immunol, 2004, 13(3): 177-184.
3. Willenborg DO, Parish CR, Cowden WB. Inhibition of experimental allergic encephalomyelitis by the alpha-glucosidase inhibitor castanospermine. J Neurol Sci, 1989, 90(1): 77-85.
4. Willenborg DO, Parish CR, Cowden WB. Inhibition of adjuvant arthritis in the rat by phosphosugars and the alpha-glucosidase inhibitor castanospermine. Immunol Cell Biol, 1992, 70 (Pt 6): 369-377.
5. Whitby K, Pierson TC, Geiss B, et al. Castanospermine, a potent inhibitor of dengue virus infection in vitro and in vivo. J Virol, 2005, 79(14): 8698-8706.
6. Hong YP, Guo WY, Wang WX, et al. 4-phenylbutyric acid attenuates pancreatic beta-cell injury in rats with experimental severe acute pancreatitis. Int J Endocrinol, 2016, 2016: 4592346.
7. Sporek M, Gala-Błądzińska A, Dumnicka P, et al. Urine NGAL is useful in the clinical evaluation of renal function in the early course of acute pancreatitis. Folia Med Cracov, 2016, 56(1): 13-25.
8. Zhou J, Li Y, Tang Y, et al. Effect of acute kidney injury on mortality and hospital stay in patient with severe acute pancreatitis. Nephrology (Carlton), 2015, 20(7): 485-491.
9. Sporek M, Dumnicka P, Gala-Bladzinska A, et al. Angiopoietin-2 is an early indicator of acute pancreatic-renal syndrome in patients with acute pancreatitis. Mediators Inflamm, 2016, 2016: 5780903.
10. Kim SY, Hwang JS, Han IO. Tunicamycin inhibits Toll-like receptor-activated inflammation in RAW264.7 cells by suppression of NF-κB and c-Jun activity via a mechanism that is independent of ER-stress and N-glycosylation. Eur J Pharmacol, 2013, 721(1-3): 294-300.
11. Walter S, Fassbender K, Gulbins E, et al. Glycosylation processing inhibition by castanospermine prevents experimental autoimmune encephalomyelitis by interference with IL-2 receptor signal transduction. J Neuroimmunol, 2002, 132(1-2): 1-10.
12. Durantel D. Celgosivir. An alpha-glucosidase Ⅰ inhibitor for the potential treatment of HCV infection. Curr Opin Investig Drugs, 2009, 10(8): 860-870.
13. 洪育蒲, 郭闻一, 赵亮, 等. 4-苯基丁酸对重症急性胰腺炎大鼠肝损伤的保护作用. 中国普外基础与临床杂志, 2017, 24(1): 18-23.0.
14. Shi Q, Liao KS, Zhao KL, et al. Hydrogen-rich saline attenuates acute renal injury in sodium taurocholate-induced severe acute pancreatitis by inhibiting ROS and NF-κB pathway. Mediators Inflamm, 2015, 2015: 685043.
15. 惠远见, 王卫星, 余佳, 等. 急性胰腺炎大鼠肾脏中聚腺苷二磷酸核糖聚合酶-1 mRNA 的表达及意义. 中国普外基础与临床杂志, 2010, 17(3): 272-274.0.
16. Liu Y, Chen XD, Yu J, et al. Deletion of XIAP reduces the severity of acute pancreatitis via regulation of cell death and nuclear factor-κB activity. Cell Death Dis, 2017, 8(3): e2685.
17. Yang YZ, Xiang Y, Chen M, et al. Clinical significance of dynamic detection for serum levels of MCP-1, TNF-α and IL-8 in patients with acute pancreatitis. Asian Pac J Trop Med, 2016, 9(11): 1111-1114.
18. Zhang XP, Wang L, Zhou YF. The pathogenic mechanism of severe acute pancreatitis complicated with renal injury: a review of current knowledge. Dig Dis Sci, 2008, 53(2): 297-306.
19. Wang G, Han B, Zhou H, et al. Inhibition of hydrogen sulfide synthesis provides protection for severe acute pancreatitis rats via apoptosis pathway. Apoptosis, 2013, 18(1): 28-42.
20. Dabrowski A, Osada J, Dabrowska MI, et al. Increased expression of the intercellular adhesion molecule-1 (ICAM-1) on peripheral blood neutrophils in acute pancreatitis. Adv Med Sci, 2014, 59(1): 102-107.
21. Tamizhselvi R, Koh YH, Sun J, et al. Hydrogen sulfide induces ICAM-1 expression and neutrophil adhesion to caerulein-treated pancreatic acinar cells through NF-kappaB and Src-family kinases pathway. Exp Cell Res, 2010, 316(9): 1625-1636.
22. Fan YT, Yin GJ, Xiao WQ, et al. Rosmarinic acid attenuates sodium taurocholate-induced acute pancreatitis in rats by inhibiting nuclear factor-κB activation. Am J Chin Med, 2015, 43(6): 1117-1135.
23. Lv P, Li HY, Ji SS, et al. Thalidomide alleviates acute pancreatitis-associated lung injury via down-regulation of NFκB induced TNF-α. Pathol Res Pract, 2014, 210(9): 558-564.
24. Huang H, Liu Y, Daniluk J, et al. Activation of nuclear factor-κB in acinar cells increases the severity of pancreatitis in mice. Gastroenterology, 2013, 144(1): 202-210.
25. Larsen BD, Sørensen CS. The caspase-activated DNase: apoptosis and beyond. FEBS J, 2017, 284(8): 1160-1170.
26. Yen JH, Ganea D. Interferon beta induces mature dendritic cell apoptosis through caspase-11/caspase-3 activation. Blood, 2009, 114(7): 1344-1354.

CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Protective effect of castanospermine on severe acute pancreatitis-induced renal injury in Sprague Dawley rats

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