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. 基于我們的研究工作簡述活性氧生物學效應研究進展. 中國活性氧生物學效應學術會議, 中國陜西西安, 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.	陳瑾歆, 唐聰明. 氧自由基的研究進展. 海南醫學院學報, 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. 活性氧對細胞凋亡和增殖的調控作用. 基礎醫學與臨床, 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.	張麗華, 王切, 劉釗, 等. 過氧化物還原酶I-硫氧還蛋白、超氧化物歧化酶及過氧化氫酶在大鼠肝臟缺血再灌注損傷中的表達變化. 解剖學報, 2013, 44(4):550-553.
28.	孫凱, 劉志蘇, 孫權. 缺血后處理對肝臟缺血再灌注損傷的保護效應. 南方醫科大學學報, 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.	趙文波, 任智, 李正中. 維生素E在大鼠肝臟缺血再灌注損傷中的作用. 中國藥物與臨床, 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, 張斯文. 維生素C和維生素E聯合應用對大鼠腎缺血再灌注損傷的保護作用. 中國民族民間醫藥, 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.	顧全凱, 楊標, 袁慶鑫, 等. 芹菜素對大鼠肝臟局部缺血再灌注損傷的保護作用. 中藥藥理與臨床, 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. 基于我們的研究工作簡述活性氧生物學效應研究進展. 中國活性氧生物學效應學術會議, 中國陜西西安, 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. 陳瑾歆, 唐聰明. 氧自由基的研究進展. 海南醫學院學報, 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. 活性氧對細胞凋亡和增殖的調控作用. 基礎醫學與臨床, 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. 張麗華, 王切, 劉釗, 等. 過氧化物還原酶I-硫氧還蛋白、超氧化物歧化酶及過氧化氫酶在大鼠肝臟缺血再灌注損傷中的表達變化. 解剖學報, 2013, 44(4):550-553.
28. 孫凱, 劉志蘇, 孫權. 缺血后處理對肝臟缺血再灌注損傷的保護效應. 南方醫科大學學報, 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. 趙文波, 任智, 李正中. 維生素E在大鼠肝臟缺血再灌注損傷中的作用. 中國藥物與臨床, 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, 張斯文. 維生素C和維生素E聯合應用對大鼠腎缺血再灌注損傷的保護作用. 中國民族民間醫藥, 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. 顧全凱, 楊標, 袁慶鑫, 等. 芹菜素對大鼠肝臟局部缺血再灌注損傷的保護作用. 中藥藥理與臨床, 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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