Progress in Research of The Reactive Oxygen Species in The Hepatic Ischemia-Reperfusion Injury_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

 ZHOUXian-feng ^1,2 , YAOYu-tong ² ,  HUANGXiao-lun ²

1. North Sichuan Medical College, Nanchong 637000, Sichuan Privince, China;
2. Center of Cell Transplantation, Affiliated Hospital of University of Electronic Science and Technology of China & Sichuan Provincal People's Hospital, Chengdu 610072, Sichuan Province, China;

Corresponding author：

HUANGXiao-lun, Email: garrymd@163.com

Keywords：

Reactive oxygen species; Ischemia-reperfusion injury; Liver

DOI：

10.7507/1007-9424.20150234

Video：

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Abstract Full text Figures/Tables Video References Cited by

Objective To review the recent research progress about the pathogenesis and prevention of reactive oxygen species (ROS) in the hepatic ischemia-reperfusion injury (HIRI). Methods Searched the related literatures in recent years from the databases such as CNKI, PubMed and so on, summarized the recent research progress about the generation mechanism of ROS, the damage mechanism of ROS, and the prevention method of ROS. Results A mass of ROS originated from polymorphonuclear leukocytes, Kupffer cells, mitochondria, and the enzymes in hepatic tissue in HIRI. It mainly destroyed sugar molecules of oligosaccharide chains on the cell membrane, unsaturated fatty acid, protein molecules, mitochondrial, and genetic material. This mechanism lead to cell injuried or even death. The main method of prevention and cure to HIRI is eliminating ROS by using enzymes, vitamins, Chinese herbal medicines etc. Conclusions The research about ROS in HIRI has advanced. Aiming at the damage resulted from ROS in the liver, Scholars have came up with a variety of control methods which is feasible. However, many issues need to be further investigated.

Citation： ZHOUXian-feng, YAOYu-tong, HUANGXiao-lun. Progress in Research of The Reactive Oxygen Species in The Hepatic Ischemia-Reperfusion Injury. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2015, 22(7): 898-F3. doi: 10.7507/1007-9424.20150234 Copy

1.	Kim YI. Ischemia-reperfusion injury of the human liver during hepatic resection. J Hepatobiliary Pancreat Surg, 2003, 10(3):195-199.
2.	Rushing GD, Britt LD. Reperfusion injury after hemorrhage:a collective review. Ann Surg, 2008, 247(6):929-937.
3.	Banga NR, Homer-Vanniasinkam S, Graham A, et al. Ischaemic preconditioning in transplantation and major resection of the liver. Br J Surg, 2005, 92(5):528-538.
4.	Weigand K, Brost S, Steinebrunner N, et al. Ischemia/Reperfusion injury in liver surgery and transplantation:pathophysiology. HPB Surg, 2012, 2012:176723.
5.	海春旭. 基于我们的研究工作简述活性氧生物学效应研究进展. 中国活性氧生物学效应学术会议, 中国陕西西安, 2011:2011(1):1-4.
6.	Halliwell B, Cross CE. Oxygen-derived species:their relation to human disease and environmental stress. Environ Health Perspect, 1994, 102 Suppl 10:5-12.
7.	Halliwell B. Free radicals and antioxidants:updating a personal view. Nutr Rev, 2012,70(5):257-265.
8.	Halliwell B. The antioxidant paradox:less paradoxical now? Br J Clin Pharmacol, 2013, 75(3):637-644.
9.	Ciz M, Denev P, Kratchanova M, et al. Flavonoids inhibit the respiratory burst of neutrophils in mammals. Oxid Med Cell Longev, 2012, 2012:181295.
10.	Jaeschke H, Woolbright BL. Current strategies to minimize hepatic ischemia-reperfusion injury by targeting reactive oxygen species. Transplant Rev (Orlando), 2012, 26(2):103-114.
11.	Murphy MP. How mitochondria produce reactive oxygen species. Biochem J, 2009, 417(1):1-13.
12.	Cantu-Medellin N, Kelley EE. Xanthine oxidoreductase-catalyzed reactive species generation:A process in critical need of reevaluation. Redox Biol, 2013, 1(1):353-358.
13.	陈瑾歆, 唐聪明. 氧自由基的研究进展. 海南医学院学报, 2004, 10(3):206-208.
14.	Jaeschke H. Reactive oxygen and ischemia/reperfusion injury of the liver. Chem Biol Interact, 1991, 79(2):115-136.
15.	Negre-Salvayre A, Auge N, Ayala V, et al. Pathological aspects of lipid peroxidation. Free Radic Res, 2010, 44(10):1125-1171.
16.	Jaeschke H. Reactive oxygen and mechanisms of inflammatory liver injury:Present concepts. J Gastroenterol Hepatol, 2011, 26 Suppl 1:173-179.
17.	Mittal M, Siddiqui MR, Tran K, et al. Reactive oxygen species in inflammation and tissue injury. Antioxid Redox Signal, 2014, 20(7):1126-1167.
18.	Fleury C, Mignotte B, Vayssiere JL. Mitochondrial reactive oxygen species in cell death signaling. Biochimie, 2002, 84(2-3):131-141.
19.	Wheeler MD, Katuna M, Smutney OM, et al. Comparison of the effect of adenoviral delivery of three superoxide dismutase genes against hepatic ischemia-reperfusion injury. Hum Gene Ther, 2001, 12(18):2167-2177.
20.	Lemasters JJ, Qian T, He L, et al. Role of mitochondrial inner membrane permeabilization in necrotic cell death, apoptosis, and autophagy. Antioxid Redox Signal, 2002, 4(5):769-781.
21.	Marubayashi S, Dohi K, Ochi K, et al. Role of free radicals in ischemic rat liver cell injury:prevention of damage by alpha-tocopherol administration. Surgery, 1986, 99(2):184-192.
22.	易健, 舒徐. 活性氧对细胞凋亡和增殖的调控作用. 基础医学与临床, 2013, 33(10):1341-1344.
23.	Padayatty SJ, Katz A, Wang Y, et al. Vitamin C as an antioxidant:evaluation of its role in disease prevention. J Am Coll Nutr, 2003, 22(1):18-35.
24.	Chow CK. Nutritional influence on cellular antioxidant defense systems. Am J Clin Nutr, 1979, 32(5):1066-1081.
25.	Hide D, Ortega-Ribera M, Fernandez-Iglesias A, et al. A novel form of the human manganese superoxide dismutase protects rat and human livers undergoing ischaemia and reperfusion injury. Clin Sci (Lond), 2014, 127(8):527-537.
26.	Kodydkova J, Vavrova L, Kocik M, et al. Human catalase, its polymorphisms, regulation and changes of its activity in different diseases. Folia Biol (Praha), 2014, 60(4):153-167.
27.	张丽华, 王切, 刘钊, 等. 过氧化物还原酶I-硫氧还蛋白、超氧化物歧化酶及过氧化氢酶在大鼠肝脏缺血再灌注损伤中的表达变化. 解剖学报, 2013, 44(4):550-553.
28.	孙凯, 刘志苏, 孙权. 缺血后处理对肝脏缺血再灌注损伤的保护效应. 南方医科大学学报, 2009, 29(12):2480-2484.
29.	Pan TL, Wu TH, Wang PW, et al. Functional proteomics reveals the protective effects of saffron ethanolic extract on hepatic ischemia-reperfusion injury. Proteomics, 2013, 13(15):2297-2311.
30.	Aquilano K, Baldelli S, Ciriolo MR. Glutathione:new roles in redox signaling for an old antioxidant. Front Pharmacol, 2014, 5:196.
31.	Jaeschke H, Farhood A. Neutrophil and Kupffer cell-induced oxidant stress and ischemia-reperfusion injury in rat liver. Am J Physiol, 1991, 260(3 Pt 1):G355-G362.
32.	Smyrniotis V, Arkadopoulos N, Kostopanagiotou G, et al. Attenuation of ischemic injury by N-acetylcysteine preconditioning of the liver. J Surg Res, 2005, 129(1):31-37.
33.	Fusai G, Glantzounis GK, Hafez T, et al. N-Acetylcysteine ameliorates the late phase of liver ischaemia/reperfusion injury in the rabbit with hepatic steatosis. Clin Sci (Lond), 2005, 109(5):465-473.
34.	Jegatheeswaran S, Siriwardena AK. Experimental and clinical evidence for modification of hepatic ischaemia-reperfusion injury by N-acetylcysteine during major liver surgery. HPB (Oxford), 2011, 13(2):71-78.
35.	Mahmoud MF, Gamal S, El-Fayoumi HM. Limonin attenuates hepatocellular injury following liver ischemia and reperfusion in rats via toll-like receptor dependent pathway. Eur J Pharmacol, 2014, 740:676-682.
36.	Sharanova NE, Kulakova SN, Baturina VA, et al. Effect of coenzyme Q10 on the proteomic profile of the cytosolic and microsomal fractions from rat hepatocytes upon dietary consumption of various lipid components during ontogeny. Bull Exp Biol Med, 2013, 154(3):320-325.
37.	Amano A, Sato Y, Kishimoto Y, et al. Effects of ascorbic acid deficiency on protein and lipid oxidation in livers from SMP30/GNL knockout mice. J Nutr Sci Vitaminol (Tokyo), 2013, 59(6):489-495.
38.	Tao X, Wan X, Xu Y, et al. Dioscin attenuates hepatic ischemia-reperfusion injury in rats through inhibition of oxidative-nitrative stress, inflammation and apoptosis. Transplantation, 2014, 98(6):604-611.
39.	Hsu CC, Wang JJ. L-ascorbic acid and alpha-tocopherol attenuates liver ischemia-reperfusion induced of cardiac function impairment. Transplant Proc, 2012, 44(4):933-936.
40.	赵文波, 任智, 李正中. 维生素E在大鼠肝脏缺血再灌注损伤中的作用. 中国药物与临床, 2007, 7(2):115-118.
41.	Suo L, Kang K, Wang X, et al. Carvacrol alleviates ischemia reperfusion injury by regulating the PI3K-Akt pathway in rats. PLoS One, 2014, 9(8):e104043.
42.	彭燕, 程也, 张斯文. 维生素C和维生素E联合应用对大鼠肾缺血再灌注损伤的保护作用. 中国民族民间医药, 2013, 10:23-25.
43.	Beatty S, Koh H, Phil M, et al. The role of oxidative stress in the pathogenesis of age-related macular degeneration. Surv Ophthalmol, 2000, 45(2):115-134.
44.	顾全凯, 杨标, 袁庆鑫, 等. 芹菜素对大鼠肝脏局部缺血再灌注损伤的保护作用. 中药药理与临床, 2014, 30(4):36-39.
45.	Singh AK, Mani H, Seth P, et al. Picroliv preconditioning protects the rat liver against ischemia-reperfusion injury. Eur J Pharmacol, 2000, 395(3):229-239.
46.	Tomatsuri N, Yoshida N, Takagi T, et al. Edaravone, a newly developed radical scavenger, protects against ischemia-reperfusion injury of the small intestine in rats. Int J Mol Med, 2004, 13(1):105-109.
47.	Boyko VV, Pisetska ME, Tyshchenko OM, et al. Role of ischemic preconditioning in hepatic ischemia-reperfusion injury. Hepatobiliary Surg Nutr, 2014, 3(4):179-184.
48.	De Rougemont O, Lehmann K, Clavien PA. Preconditioning, organ preservation, and postconditioning to prevent ischemia-reperfusion injury to the liver. Liver Transpl, 2009, 15(10):1172-1182.
49.	Lv X, Yang L, Tao K, et al. Isoflurane preconditioning at clinically relevant doses induce protective effects of heme oxygenase-1 on hepatic ischemia reperfusion in rats. BMC Gastroenterol, 2011, 11:31.
50.	Beck-Schimmer B, Breitenstein S, Urech S, et al. A randomized controlled trial on pharmacological preconditioning in liver surgery using a volatile anesthetic. Ann Surg, 2008, 248(6):909-918.
51.	Zhang L, Huang H, Cheng J, et al. Pre-treatment with isoflurane ameliorates renal ischemic-reperfusion injury in mice. Life Sci, 2011, 88(25-26):1102-1107.

1. Kim YI. Ischemia-reperfusion injury of the human liver during hepatic resection. J Hepatobiliary Pancreat Surg, 2003, 10(3):195-199.
2. Rushing GD, Britt LD. Reperfusion injury after hemorrhage:a collective review. Ann Surg, 2008, 247(6):929-937.
3. Banga NR, Homer-Vanniasinkam S, Graham A, et al. Ischaemic preconditioning in transplantation and major resection of the liver. Br J Surg, 2005, 92(5):528-538.
4. Weigand K, Brost S, Steinebrunner N, et al. Ischemia/Reperfusion injury in liver surgery and transplantation:pathophysiology. HPB Surg, 2012, 2012:176723.
5. 海春旭. 基于我们的研究工作简述活性氧生物学效应研究进展. 中国活性氧生物学效应学术会议, 中国陕西西安, 2011:2011(1):1-4.
6. Halliwell B, Cross CE. Oxygen-derived species:their relation to human disease and environmental stress. Environ Health Perspect, 1994, 102 Suppl 10:5-12.
7. Halliwell B. Free radicals and antioxidants:updating a personal view. Nutr Rev, 2012,70(5):257-265.
8. Halliwell B. The antioxidant paradox:less paradoxical now? Br J Clin Pharmacol, 2013, 75(3):637-644.
9. Ciz M, Denev P, Kratchanova M, et al. Flavonoids inhibit the respiratory burst of neutrophils in mammals. Oxid Med Cell Longev, 2012, 2012:181295.
10. Jaeschke H, Woolbright BL. Current strategies to minimize hepatic ischemia-reperfusion injury by targeting reactive oxygen species. Transplant Rev (Orlando), 2012, 26(2):103-114.
11. Murphy MP. How mitochondria produce reactive oxygen species. Biochem J, 2009, 417(1):1-13.
12. Cantu-Medellin N, Kelley EE. Xanthine oxidoreductase-catalyzed reactive species generation:A process in critical need of reevaluation. Redox Biol, 2013, 1(1):353-358.
13. 陈瑾歆, 唐聪明. 氧自由基的研究进展. 海南医学院学报, 2004, 10(3):206-208.
14. Jaeschke H. Reactive oxygen and ischemia/reperfusion injury of the liver. Chem Biol Interact, 1991, 79(2):115-136.
15. Negre-Salvayre A, Auge N, Ayala V, et al. Pathological aspects of lipid peroxidation. Free Radic Res, 2010, 44(10):1125-1171.
16. Jaeschke H. Reactive oxygen and mechanisms of inflammatory liver injury:Present concepts. J Gastroenterol Hepatol, 2011, 26 Suppl 1:173-179.
17. Mittal M, Siddiqui MR, Tran K, et al. Reactive oxygen species in inflammation and tissue injury. Antioxid Redox Signal, 2014, 20(7):1126-1167.
18. Fleury C, Mignotte B, Vayssiere JL. Mitochondrial reactive oxygen species in cell death signaling. Biochimie, 2002, 84(2-3):131-141.
19. Wheeler MD, Katuna M, Smutney OM, et al. Comparison of the effect of adenoviral delivery of three superoxide dismutase genes against hepatic ischemia-reperfusion injury. Hum Gene Ther, 2001, 12(18):2167-2177.
20. Lemasters JJ, Qian T, He L, et al. Role of mitochondrial inner membrane permeabilization in necrotic cell death, apoptosis, and autophagy. Antioxid Redox Signal, 2002, 4(5):769-781.
21. Marubayashi S, Dohi K, Ochi K, et al. Role of free radicals in ischemic rat liver cell injury:prevention of damage by alpha-tocopherol administration. Surgery, 1986, 99(2):184-192.
22. 易健, 舒徐. 活性氧对细胞凋亡和增殖的调控作用. 基础医学与临床, 2013, 33(10):1341-1344.
23. Padayatty SJ, Katz A, Wang Y, et al. Vitamin C as an antioxidant:evaluation of its role in disease prevention. J Am Coll Nutr, 2003, 22(1):18-35.
24. Chow CK. Nutritional influence on cellular antioxidant defense systems. Am J Clin Nutr, 1979, 32(5):1066-1081.
25. Hide D, Ortega-Ribera M, Fernandez-Iglesias A, et al. A novel form of the human manganese superoxide dismutase protects rat and human livers undergoing ischaemia and reperfusion injury. Clin Sci (Lond), 2014, 127(8):527-537.
26. Kodydkova J, Vavrova L, Kocik M, et al. Human catalase, its polymorphisms, regulation and changes of its activity in different diseases. Folia Biol (Praha), 2014, 60(4):153-167.
27. 张丽华, 王切, 刘钊, 等. 过氧化物还原酶I-硫氧还蛋白、超氧化物歧化酶及过氧化氢酶在大鼠肝脏缺血再灌注损伤中的表达变化. 解剖学报, 2013, 44(4):550-553.
28. 孙凯, 刘志苏, 孙权. 缺血后处理对肝脏缺血再灌注损伤的保护效应. 南方医科大学学报, 2009, 29(12):2480-2484.
29. Pan TL, Wu TH, Wang PW, et al. Functional proteomics reveals the protective effects of saffron ethanolic extract on hepatic ischemia-reperfusion injury. Proteomics, 2013, 13(15):2297-2311.
30. Aquilano K, Baldelli S, Ciriolo MR. Glutathione:new roles in redox signaling for an old antioxidant. Front Pharmacol, 2014, 5:196.
31. Jaeschke H, Farhood A. Neutrophil and Kupffer cell-induced oxidant stress and ischemia-reperfusion injury in rat liver. Am J Physiol, 1991, 260(3 Pt 1):G355-G362.
32. Smyrniotis V, Arkadopoulos N, Kostopanagiotou G, et al. Attenuation of ischemic injury by N-acetylcysteine preconditioning of the liver. J Surg Res, 2005, 129(1):31-37.
33. Fusai G, Glantzounis GK, Hafez T, et al. N-Acetylcysteine ameliorates the late phase of liver ischaemia/reperfusion injury in the rabbit with hepatic steatosis. Clin Sci (Lond), 2005, 109(5):465-473.
34. Jegatheeswaran S, Siriwardena AK. Experimental and clinical evidence for modification of hepatic ischaemia-reperfusion injury by N-acetylcysteine during major liver surgery. HPB (Oxford), 2011, 13(2):71-78.
35. Mahmoud MF, Gamal S, El-Fayoumi HM. Limonin attenuates hepatocellular injury following liver ischemia and reperfusion in rats via toll-like receptor dependent pathway. Eur J Pharmacol, 2014, 740:676-682.
36. Sharanova NE, Kulakova SN, Baturina VA, et al. Effect of coenzyme Q10 on the proteomic profile of the cytosolic and microsomal fractions from rat hepatocytes upon dietary consumption of various lipid components during ontogeny. Bull Exp Biol Med, 2013, 154(3):320-325.
37. Amano A, Sato Y, Kishimoto Y, et al. Effects of ascorbic acid deficiency on protein and lipid oxidation in livers from SMP30/GNL knockout mice. J Nutr Sci Vitaminol (Tokyo), 2013, 59(6):489-495.
38. Tao X, Wan X, Xu Y, et al. Dioscin attenuates hepatic ischemia-reperfusion injury in rats through inhibition of oxidative-nitrative stress, inflammation and apoptosis. Transplantation, 2014, 98(6):604-611.
39. Hsu CC, Wang JJ. L-ascorbic acid and alpha-tocopherol attenuates liver ischemia-reperfusion induced of cardiac function impairment. Transplant Proc, 2012, 44(4):933-936.
40. 赵文波, 任智, 李正中. 维生素E在大鼠肝脏缺血再灌注损伤中的作用. 中国药物与临床, 2007, 7(2):115-118.
41. Suo L, Kang K, Wang X, et al. Carvacrol alleviates ischemia reperfusion injury by regulating the PI3K-Akt pathway in rats. PLoS One, 2014, 9(8):e104043.
42. 彭燕, 程也, 张斯文. 维生素C和维生素E联合应用对大鼠肾缺血再灌注损伤的保护作用. 中国民族民间医药, 2013, 10:23-25.
43. Beatty S, Koh H, Phil M, et al. The role of oxidative stress in the pathogenesis of age-related macular degeneration. Surv Ophthalmol, 2000, 45(2):115-134.
44. 顾全凯, 杨标, 袁庆鑫, 等. 芹菜素对大鼠肝脏局部缺血再灌注损伤的保护作用. 中药药理与临床, 2014, 30(4):36-39.
45. Singh AK, Mani H, Seth P, et al. Picroliv preconditioning protects the rat liver against ischemia-reperfusion injury. Eur J Pharmacol, 2000, 395(3):229-239.
46. Tomatsuri N, Yoshida N, Takagi T, et al. Edaravone, a newly developed radical scavenger, protects against ischemia-reperfusion injury of the small intestine in rats. Int J Mol Med, 2004, 13(1):105-109.
47. Boyko VV, Pisetska ME, Tyshchenko OM, et al. Role of ischemic preconditioning in hepatic ischemia-reperfusion injury. Hepatobiliary Surg Nutr, 2014, 3(4):179-184.
48. De Rougemont O, Lehmann K, Clavien PA. Preconditioning, organ preservation, and postconditioning to prevent ischemia-reperfusion injury to the liver. Liver Transpl, 2009, 15(10):1172-1182.
49. Lv X, Yang L, Tao K, et al. Isoflurane preconditioning at clinically relevant doses induce protective effects of heme oxygenase-1 on hepatic ischemia reperfusion in rats. BMC Gastroenterol, 2011, 11:31.
50. Beck-Schimmer B, Breitenstein S, Urech S, et al. A randomized controlled trial on pharmacological preconditioning in liver surgery using a volatile anesthetic. Ann Surg, 2008, 248(6):909-918.
51. Zhang L, Huang H, Cheng J, et al. Pre-treatment with isoflurane ameliorates renal ischemic-reperfusion injury in mice. Life Sci, 2011, 88(25-26):1102-1107.

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Progress in Research of The Reactive Oxygen Species in The Hepatic Ischemia-Reperfusion Injury

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