Hyperglycemia Aggravates Hepatic Ischemia Reperfusion Injury by Inducing Chronic Oxidative Stress and Inflammation

Oxidative Medicine and Cellular Longevity

Volumn 2016, Issue , 2016, Pages

  Zhang, Yihan ^a   Yuan, Dongdong ^a   Yao, Weifeng ^a   Zhu, Qianqian ^a   Liu, Yue ^a   Huang, Fei ^a   Feng, Jiayu ^a   Chen, Xi ^a   Huang, Yong ^a   Chi, Xinjin ^a   Hei, Ziqing ^a  

^a THE THIRD AFFILIATED HOSPITAL OF SUN YAT SEN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCYSTEINE; AMINO ACIDS; GLUCOSE; OXIDATIVE STRESS; PATHOLOGY; RATS;

ANTIOXIDATIVE SYSTEM; CHRONIC OXIDATIVE STRESS; HEPATIC ISCHEMIA; INFLAMMATORY CYTOKINES; N-ACETYL-L-CYSTEINE; NUCLEAR FACTOR ERYTHROID 2-RELATED FACTOR 2; REACTIVE OXYGEN SPECIES; SPRAGUE-DAWLEY RATS;

BIOLOGICAL ORGANS;

3,4 METHYLENEDIOXYAMPHETAMINE; 8 ISOPROSTANE; ACETYLCYSTEINE; ADVANCED GLYCATION END PRODUCT; ALANINE AMINOTRANSFERASE; ALDEHYDE REDUCTASE; APOCYNIN; ASPARTATE AMINOTRANSFERASE; CYTOCHROME P450; GLUCOSE; GLUTATHIONE; HYDROGEN PEROXIDE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 6; MONOCYTE CHEMOTACTIC PROTEIN 1; POLYOL; PROTEIN KINASE C; REACTIVE OXYGEN METABOLITE; STREPTOZOCIN; TRANSCRIPTION FACTOR NRF2; TRANSFERASE; TUMOR NECROSIS FACTOR;

ALANINE AMINOTRANSFERASE BLOOD LEVEL; ALCOHOLIC FATTY LIVER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASPARTATE AMINOTRANSFERASE BLOOD LEVEL; CELL COMPONENT; CELL VIABILITY; CHRONIC STRESS; CONTROLLED STUDY; HEPATIC ISCHEMIA REPERFUSION INJURY; HISTOLOGY; HYPERGLYCEMIA; IMMUNE RESPONSE; INFLAMMATION; INSULIN DEPENDENT DIABETES MELLITUS; KUPFFER CELL; LIPID PEROXIDATION; LIVER CELL; LIVER HISTOLOGY; LIVER ISCHEMIA; LIVER NECROSIS; MITOCHONDRION; NEUTROPHIL; NITROSATIVE STRESS; NONALCOHOLIC FATTY LIVER; NONHUMAN; OXIDATIVE STRESS; RAT; REPERFUSION INJURY; SINUS CONGESTION; VIRUS HEPATITIS;

EID: 84987896964     PISSN: 19420900     EISSN: 19420994     Source Type: Journal    
DOI: 10.1155/2016/3919627     Document Type: Article

References (55)

1. S. Haga, S. J. Remington, N. Morita, K. Terui, and M. Ozaki, "Hepatic ischemia induced immediate oxidative stress after reperfusion and determined the severity of the reperfusioninduced damage," Antioxidants and Redox Signaling, vol. 11, no. 10, pp. 2563-2572, 2009.
2. B. F. Trump and I. K. Berezesky, "Calcium-mediated cell injury and cell death," The FASEB Journal, vol. 9, no. 2, pp. 219-228, 1995.
3. B. Vollmar, M. D. Menger, J. Glasz, R. Leiderer, and K. Messmer, "Impact of leukocyte-endothelial cell interaction in hepatic ischemia-reperfusion injury," American Journal of Physiology-Gastrointestinal and Liver Physiology, vol. 267, no. 5, pp. G786-G793, 1994.
4. N. G. Frangogiannis, "Chemokines in ischemia and reperfusion," Thrombosis and Haemostasis, vol. 97, no. 5, pp. 738-747, 2007.
5. N.-E. L. Saris and K. O. Eriksson, "Mitochondrial dysfunction in ischaemia-reperfusion," Acta Anaesthesiologica Scandinavica, Supplement, vol. 39, no. 107, pp. 171-176, 1995.
6. H. Jaeschke and B. L. Woolbright, "Current strategies to minimize hepatic ischemia-reperfusion injury by targeting reactive oxygen species," Transplantation Reviews, vol. 26, no. 2, pp. 103-114, 2012.
7. W. M. Ricci, P. N. Streubel, S. Morshed, C. A. Collinge, S. E. Nork, and M. J. Gardner, "Risk factors for failure of locked plate fixation of distal femur fractures: an analysis of 335 cases," Journal of Orthopaedic Trauma, vol. 28, no. 2, pp. 83-89, 2014.
8. B. A. Ponce, M. E. Menendez, L. O. Oladeji, and F. Soldado, "Diabetes as a risk factor for poorer early postoperative outcomes after shoulder arthroplasty," Journal of Shoulder and Elbow Surgery, vol. 23, no. 5, pp. 671-678, 2014.
9. M. Ardeshiri, Z. Faritus, Z. Ojaghi Haghighi, H. Bakhshandeh, F. Kargar, and R. Aghili, "Impact of metabolic syndrome on mortality and morbidity after coronary artery bypass grafting surgery," Research in Cardiovascular Medicine, vol. 3, no. 3, Article ID e20270, 2014.
10. M. Ding, J. Lei, H. Han et al., "SIRT1 protects againstmyocardial ischemia-reperfusion injury via activating eNOS in diabetic rats," Cardiovascular Diabetology, vol. 14, no. 1, article 143, 2015.
11. J. Parekh, G. R. Roll, S. Feng, C. U. Niemann, and R. Hirose, "Peri-operative hyperglycemia is associated with delayed graft function in deceased donor renal transplantation," Clinical Transplantation, vol. 27, no. 4, pp. E424-E430, 2013.
12. M. Abdelsaid, R. Prakash, W. Li et al., "Metformin treatment in the period after stroke prevents nitrative stress and restores angiogenic signaling in the brain in diabetes," Diabetes, vol. 64, no. 5, pp. 1804-1817, 2015.
13. J. L. Evans, I. D. Goldfine, B. A. Maddux, and G.M. Grodsky, "Oxidative stress and stress-activated signaling pathways: a unifying hypothesis of type 2 diabetes," Endocrine Reviews, vol. 23, no. 5, pp. 599-622, 2002.
14. R. Ni, D. Zheng, S. Xiong et al., "Mitochondrial calpain- 1 disrupts ATP synthase and induces superoxide generation in type-1 diabetic hearts: a novel mechanism contributing to diabetic cardiomyopathy," Diabetes, vol. 65, no. 1, pp. 255-268, 2016.
15. H. Ha, R. Y. Mi, J. C. Yoon, M. Kitamura, and B. L. Hi, "Role of high glucose-induced nuclear factor-κB activation in monocyte chemoattractant protein-1 expression by mesangial cells," Journal of the American Society of Nephrology, vol. 13, no. 4, pp. 894-902, 2002.
16. X. Cheng, R. C. M. Siow, and G. E. Mann, "Impaired redox signaling and antioxidant gene expression in endothelial cells in diabetes: a role for mitochondria and the nuclear factor-E2-related factor 2-Kelch-like ECH-associated protein 1 defense pathway," Antioxidants and Redox Signaling, vol. 14, no. 3, pp. 469-487, 2011.
17. R. Badalzadeh, B. Mokhtari, and R. Yavari, "Contribution of apoptosis in myocardial reperfusion injury and loss of cardioprotection in diabetes mellitus," Journal of Physiological Sciences, vol. 65, no. 3, pp. 201-215, 2015.
18. H. S. Kim, J. E. Cho, K. C. Hwang, Y. H. Shim, J. H. Lee, and Y. L. Kwak, "Diabetes mellitus mitigates cardioprotective effects of remifentanil preconditioning in ischemia-reperfused rat heart in association with anti-apoptotic pathways of survival," European Journal of Pharmacology, vol. 628, no. 1-3, pp. 132-139, 2010.
19. H. O. Altunkaynak and A. T. Ozcelikay, "Cardioprotective effect of postconditioning against ischemia-reperfusion injury is lost in heart of 8-week diabetic rat," General Physiology and Biophysics, vol. 35, no. 1, pp. 63-69, 2015.
20. S. Bonapace, F. Valbusa, L. Bertolini et al., "Nonalcoholic fatty liver disease is associated with aortic valve sclerosis in patients with type 2 diabetes mellitus," PLoS ONE, vol. 9, no. 2, Article ID e88371, 2014.
21. J.-Y. Chen, H.-C. Chou, Y.-H. Chen, and H.-L. Chan, "High glucose-induced proteome alterations in hepatocytes and its possible relevance to diabetic liver disease," Journal of Nutritional Biochemistry, vol. 24, no. 11, pp. 1889-1910, 2013.
22. G. Zoppini, U. Fedeli, N. Gennaro, M. Saugo, G. Targher, and E. Bonora, "Mortality from chronic liver diseases in diabetes," American Journal of Gastroenterology, vol. 109, no. 7, pp. 1020-1025, 2014.
23. R. S. Hoehn, A. Singhal, K. Wima et al., "Effect of pretransplant diabetes on short-term outcomes after liver transplantation: a National cohort study," Liver International, vol. 35, no. 7, pp. 1902-1909, 2015.
24. Z. M. Younossi, M. Stepanova, S. Saab et al., "The impact of type 2 diabetes and obesity on the long-term outcomes of more than 85 000 liver transplant recipients in the US," Alimentary Pharmacology and Therapeutics, vol. 40, no. 6, pp. 686-694, 2014.
25. K. W. Brudvik, Y. Mise, C. Conrad, G. Zimmitti, T. A. Aloia, and J.-N. Vauthey, "Definition of readmission in 3,041 patients undergoing hepatectomy," Journal of the American College of Surgeons, vol. 221, no. 1, pp. 38-46, 2015.
26. A. C. C. Bragança and M. R. Álvares-Da-Silva, "Prevalence of diabetes mellitus and impaired glucose tolerance in patients with decompensated cirrhosis being evaluated for liver transplantation: the utility of oral glucose tolerance test," Arquivos de Gastroenterologia, vol. 47, no. 1, pp. 22-27, 2010.
27. X. Chen and W. Yang, "Epidemic trend of diabetes in China: for the Xiaoren Pan Distinguished Research Award in AASD," Journal of Diabetes Investigation, vol. 5, no. 5, pp. 478-481, 2014.
28. K. Huang, J. Huang, X. Xie et al., "Sirt1 resists advanced glycation end products-induced expressions of fibronectin and TGF-β1 by activating the Nrf2/ARE pathway in glomerular mesangial cells," Free Radical Biology and Medicine, vol. 65, pp. 528-540, 2013.
29. C. Liu, X. Wang, Z. Chen, L. Zhang, Y. Wu, and Y. Zhang, "Hepatic ischemia-reperfusion induces insulin resistance via down-regulation during the early steps in insulin signaling in rats," Transplantation Proceedings, vol. 40, no. 10, pp. 3330-3334, 2008.
30. M. Ge, W. Yao, Y. Wang et al., "Propofol alleviates liver oxidative stress via activating Nrf2 pathway," Journal of Surgical Research, vol. 196, no. 2, pp. 373-381, 2015.
31. C. Fondevila, X.-D. Shen, S. Tsuchihashi et al., "The membrane attack complex (C5b-9) in liver cold ischemia and reperfusion injury," Liver Transplantation, vol. 14, no. 8, pp. 1133-1141, 2008.
32. M. Ge, X. Chi, A. Zhang et al., "Intestinal NF-E2-relatedfactor-2 expression and antioxidant activity changes in rats undergoing orthotopic liver autotransplantation," Oncology Letters, vol. 6, no. 5, pp. 1307-1312, 2013.
33. M. Behrends, G. Martinez-Palli, C. U. Niemann, S. Cohen, R. Ramachandran, and R. Hirose, "Acute hyperglycemia worsens hepatic ischemia/reperfusion injury in rats," Journal of Gastrointestinal Surgery, vol. 14, no. 3, pp. 528-535, 2010.
34. K. A. Lockman, J. P. Baren, C. J. Pemberton et al., "Oxidative stress rather than triglyceride accumulation is a determinant of mitochondrial dysfunction in in vitromodels of hepatic cellular steatosis," Liver International, vol. 32, no. 7, pp. 1079-1092, 2012.
35. G. Daniele, R. Guardado Mendoza, D. Winnier et al., "The inflammatory status score including IL-6, TNF-α, osteopontin, fractalkine, MCP-1 and adiponectin underlies whole-body insulin resistance and hyperglycemia in type 2 diabetes mellitus," Acta Diabetologica, vol. 51, no. 1, pp. 123-131, 2014.
36. T. Nishikawa, D. Edelstein, X. L. Du et al., "Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage," Nature, vol. 404, no. 6779, pp. 787-790, 2000.
37. E. Schleicher and U. Friess, "Oxidative stress, AGE, and atherosclerosis," Kidney International. Supplement, no. 106, pp. S17-S26, 2007.
38. N. Y. Spencer, W. Zhou, Q. Li et al., "Hepatocytes produce TNF-α following hypoxia-reoxygenation and liver ischemiareperfusion in a NADPH oxidase- and c-Src-dependent manner," American Journal of Physiology-Gastrointestinal and Liver Physiology, vol. 305, no. 1, pp. G84-G94, 2013.
39. M. J. Morgan and Z.-G. Liu, "Crosstalk of reactive oxygen species and NF-κB signaling," Cell Research, vol. 21, no. 1, pp. 103-115, 2011.
40. M. Niwa, A. Hara, Y. Kanamori et al., "Nuclear factor-κB activates dual inhibition sites in the regulation of tumor necrosis factor-α-induced neutrophil apoptosis," European Journal of Pharmacology, vol. 407, no. 3, pp. 211-219, 2000.
41. R. F. Saidi and S. K. H. Kenari, "Liver ischemia/reperfusion injury: an overview," Journal of Investigative Surgery, vol. 27, no. 6, pp. 366-379, 2014.
42. M.O. Leonard, N. E. Kieran, K. Howell et al., "Reoxygenationspecific activation of the antioxidant transcription factor Nrf2 mediates cytoprotective gene expression in ischemiareperfusion injury," The FASEB Journal, vol. 20, no. 14, pp. 2624-2626, 2006.
43. M. M. Lasram, I. B. Dhouib, A. Annabi, S. El Fazaa, and N. Gharbi, "A review on the possible molecular mechanism of action of N-acetylcysteine against insulin resistance and type-2 diabetes development," Clinical Biochemistry, vol. 48, no. 16-17, pp. 1200-1208, 2015.
44. A. Ceriello, "New insights on oxidative stress and diabetic complications may lead to a 'causal' antioxidant therapy," Diabetes Care, vol. 26, no. 5, pp. 1589-1596, 2003.
45. K. Aquilano, S. Baldelli, and M. R. Ciriolo, "Glutathione: new roles in redox signalling for an old antioxidant," Frontiers in Pharmacology, vol. 5, article 196, 2014.
46. D. L. Severson, "Diabetic cardiomyopathy: recent evidence from mouse models of type 1 and type 2 diabetes," Canadian Journal of Physiology and Pharmacology, vol. 82, no. 10, pp. 813-823, 2004.
47. P. Palsamy and S. Subramanian, "Resveratrol protects diabetic kidney by attenuating hyperglycemia-mediated oxidative stress and renal inflammatory cytokines via Nrf2-Keap1 signaling," Biochimica et Biophysica Acta-Molecular Basis of Disease, vol. 1812, no. 7, pp. 719-731, 2011.
48. L. Cominacini, C. Mozzini, U. Garbin et al., "Endoplasmic reticulum stress and Nrf2 signaling in cardiovascular diseases," Free Radical Biology and Medicine, vol. 88, pp. 233-242, 2015.
49. M. Buelna-Chontal and C. Zazueta, "Redox activation of Nrf2 & NF-κB: a double end sword?" Cellular Signalling, vol. 25, no. 12, pp. 2548-2557, 2013.
50. G.-H. Liu, J. Qu, and X. Shen, "NF-κB/p65 antagonizes Nrf2-ARE pathway by depriving CBP from Nrf2 and facilitating recruitment of HDAC3 to MafK," Biochimica et Biophysica Acta-Molecular Cell Research, vol. 1783, no. 5, pp. 713-727, 2008.
51. Y. Lavrovsky, M. L. Schwartzman, R. D. Levere, A. Kappas, and N. G. Abraham, "Identification of binding sites for transcription factors NF-κB and AP-2 in the promoter region of the human heme oxygenase 1 gene," Proceedings of the National Academy of Sciences of the United States of America, vol. 91, no. 13, pp. 5987-5991, 1994.
52. T. Wang, S. Qiao, S. Lei et al., "N-acetylcysteine and allopurinol synergistically enhance cardiac adiponectin content and reduce myocardial reperfusion injury in diabetic rats," PLoS ONE, vol. 6, no. 8, Article ID e23967, 2011.
53. A. J. F. King, "The use of animal models in diabetes research," British Journal of Pharmacology, vol. 166, no. 3, pp. 877-894, 2012.
54. T. Szkudelski, "Streptozotocin-nicotinamide-induced diabetes in the rat. Characteristics of the experimental model," Experimental Biology and Medicine, vol. 237, no. 5, pp. 481-490, 2012.
55. J. Rocha, M.-E. Figueira, A. Barateiro et al., "Inhibition of glycogen synthase kinase-3β attenuates organ injury and dysfunction associated with liver ischemia-reperfusion and thermal injury in the rat," Shock, vol. 43, no. 4, pp. 369-378, 2015.