Table of Contents Author Guidelines Submit a Manuscript
Oxidative Medicine and Cellular Longevity
Volume 2016, Article ID 3919627, 16 pages
http://dx.doi.org/10.1155/2016/3919627
Research Article

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

1Department of Anesthesiology, The Third Affiliated Hospital of Sun Yat-sen University, Guangzhou 510630, China
2Department of Thyroid and Breast Surgery, The Third Affiliated Hospital of Sun Yat-sen University, Guangzhou 510630, China

Received 16 April 2016; Revised 28 June 2016; Accepted 12 July 2016

Academic Editor: Ruchi Shah

Copyright © 2016 Yihan Zhang et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  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 reperfusion-induced damage,” Antioxidants and Redox Signaling, vol. 11, no. 10, pp. 2563–2572, 2009. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  4. N. G. Frangogiannis, “Chemokines in ischemia and reperfusion,” Thrombosis and Haemostasis, vol. 97, no. 5, pp. 738–747, 2007. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar
  10. M. Ding, J. Lei, H. Han et al., “SIRT1 protects against myocardial ischemia-reperfusion injury via activating eNOS in diabetic rats,” Cardiovascular Diabetology, vol. 14, no. 1, article 143, 2015. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar
  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. View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  32. M. Ge, X. Chi, A. Zhang et al., “Intestinal NF-E2-related factor-2 expression and antioxidant activity changes in rats undergoing orthotopic liver autotransplantation,” Oncology Letters, vol. 6, no. 5, pp. 1307–1312, 2013. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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 vitro models of hepatic cellular steatosis,” Liver International, vol. 32, no. 7, pp. 1079–1092, 2012. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  37. E. Schleicher and U. Friess, “Oxidative stress, AGE, and atherosclerosis,” Kidney International. Supplement, no. 106, pp. S17–S26, 2007. View at Google Scholar · View at Scopus
  38. N. Y. Spencer, W. Zhou, Q. Li et al., “Hepatocytes produce TNF-α following hypoxia-reoxygenation and liver ischemia-reperfusion 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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  42. M. O. Leonard, N. E. Kieran, K. Howell et al., “Reoxygenation-specific activation of the antioxidant transcription factor Nrf2 mediates cytoprotective gene expression in ischemia-reperfusion injury,” The FASEB Journal, vol. 20, no. 14, pp. 2624–2626, 2006. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus