Antioxidant and hepatoprotective effects of procyanidins from wild grape (Vitis amurensis) seeds in ethanol-induced cells and rats

International Journal of Molecular Sciences

Volumn 17, Issue 5, 2016, Pages

  Bak, Min Ji ^a   Truong, Van Long ^a   Ko, Se Yeon ^a   Nguyen, Xuan Ngan Giang ^a   Ingkasupart, Pajaree ^a   Jun, Mira ^b   Shin, Jin Young ^c   Jeong, Woo Sik ^a  

^a Inje University   (South Korea)

^b Dong A University   (South Korea)

^c CITY UNIVERSITY OF NEW YORK   (United States)

Author keywords

Alcohol; CYP2E1; Hepatoprotection; MAPKs; Oxidative stress; Procyanidins

Indexed keywords

ALANINE AMINOTRANSFERASE; ALCOHOL DEHYDROGENASE; ALDEHYDE DEHYDROGENASE; ASPARTATE AMINOTRANSFERASE; CATALASE; CYTOCHROME P450 2E1; GLUTATHIONE PEROXIDASE; MITOGEN ACTIVATED PROTEIN KINASE; PROCYANIDIN; SILYMARIN; SUPEROXIDE DISMUTASE; ALCOHOL; ANTIOXIDANT; PLANT EXTRACT; PROANTHOCYANIDIN;

ALCOHOL METABOLISM; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIOXIDANT ACTIVITY; ARTICLE; BODY WEIGHT; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; DRUG DOSE COMPARISON; GRAPE; HUMAN; HUMAN CELL; LIVER PROTECTION; LIVER WEIGHT; MTT ASSAY; NONHUMAN; OXIDATIVE STRESS; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; UPREGULATION; ANIMAL; CELL SURVIVAL; CHEMISTRY; DRUG EFFECTS; GENE EXPRESSION REGULATION; HEP-G2 CELL LINE; LIVER DISEASES, ALCOHOLIC; METABOLISM; RAT; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT; VITIS;

ALANINE TRANSAMINASE; ANIMALS; ANTIOXIDANTS; ASPARTATE AMINOTRANSFERASES; CELL SURVIVAL; ETHANOL; GENE EXPRESSION REGULATION; HEP G2 CELLS; HUMANS; LIVER DISEASES, ALCOHOLIC; MAP KINASE SIGNALING SYSTEM; PLANT EXTRACTS; PROANTHOCYANIDINS; RATS; RATS, SPRAGUE-DAWLEY; VITIS;

EID: 84969131762     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms17050758     Document Type: Article

References (54)

1. Lieber, C.S. Alcohol and the liver:1994 update. Gastroenterology 1994, 106, 1085-1105. [PubMed]
2. Surrenti, C.; Galli, M. Molecular mechanisms of alcohol-induced liver injury. An update. Minerva Gastroenterol. Dietol. 2003, 49, 95-105. [PubMed]
3. Seitz, H.K.; Stickel, F. Molecular mechanisms of alcohol-mediated carcinogenesis. Nat. Rev. Cancer 2007, 7, 599-612. [CrossRef] [PubMed]
4. Louvet, A.; Mathurin, P. Alcoholic liver disease: Mechanisms of injury and targeted treatment. Nat. Rev. Gastroenterol. Hepatol. 2015, 12, 231-242. [CrossRef] [PubMed]
5. Swift, R. Direct measurement of alcohol and its metabolites. Addiction 2003, 98, 73-80. [CrossRef] [PubMed]
6. Song, Z.; Deaciuc, I.; Song, M.; Lee, D.Y.; Liu, Y.; Ji, X.; McClain, C. Silymarin protects against acute ethanol-induced hepatotoxicity in mice. Alcohol. Clin. Exp. Res. 2006, 30, 407-413. [CrossRef] [PubMed]
7. Cederbaum, A.I.; Lu, Y.;Wu, D. Role of oxidative stress in alcohol-induced liver injury. Arch. Toxicol. 2009, 83, 519-548. [CrossRef] [PubMed]
8. Lieber, C.S. Cytochrome P-4502E1: Its physiological and pathological role. Physiol. Rev. 1997, 77, 517-544. [PubMed]
9. Dey, A. Cytochrome P450 2E1: Its clinical aspects and a brief perpective on the current research scenario. Subcell. Biochem. 2013, 67, 1-104. [PubMed]
10. Teschke, R.; Gellert, J. Hepatic microsomal ethanol-oxidizing system (MEOS): Metabolic aspects and clinical implications. Alcohol. Clin. Exp. Res. 1986, 10, 20S-32S. [CrossRef] [PubMed]
11. Teschke, R.; Hasumura, Y.; Joly, J.G.; Lieber, C.S. Microsomal ethanol-oxidizing system (MEOS): Purification and properties of a rat liver system free of catalase and alcohol dehydrogenase. Biochem. Biophys. Res. Commun. 1972, 49, 1187-1193. [CrossRef]
12. Gonzalez, F.J. Role of cytochromes P450 in chemical toxicity and oxidative stress: Studies with CYP2E1. Mutat. Res. 2005, 569, 101-110. [CrossRef] [PubMed]
13. Correa, M.; Viaggi, C.; Escrig, M.A.; Pascual, M.; Guerri, C.; Vaglini, F.; Aragon, C.M.; Corsini, G.U. Ethanol intake and ethanol-induced locomotion and locomotor sensitization in CYP2E1 knockout mice. Pharmacogenet. Genom. 2009, 19, 217-225. [CrossRef] [PubMed]
14. Das, S.K.; Vasudevan, D.M. Protective effects of silymarin, a milk thistle (Silybium marianum) derivative on ethanol-induced oxidative stress in liver. Indian J. Biochem. Biophys. 2006, 43, 306-311. [PubMed]
15. Kim, Y.D.; Eom, S.Y.; Ogawa, M.; Oyama, T.; Isse, T.; Kang, J.W.; Zhang, Y.W.; Kawamoto, T.; Kim, H. Ethanol-induced oxidative DNA damage and CYP2E1 expression in liver tissue of ALDH2 knockout mice. J. Occup. Health 2007, 49, 363-369. [CrossRef] [PubMed]
16. Wu, D.; Wang, X.; Zhou, R.; Cederbaum, A. CYP2E1 enhances ethanol-induced lipid accumulation but impairs autophagy in HepG2 E47 cells. Biochem. Biophys. Res. Commun. 2010, 402, 116-122. [CrossRef] [PubMed]
17. Alirezaei, M.; Dezfoulian, O.; Neamati, S.; Rashidipour, M.; Tanideh, N.; Kheradmand, A. Oleuropein prevents ethanol-induced gastric ulcers via elevation of antioxidant enzyme activities in rats. J. Physiol. Biochem. 2012, 68, 583-592. [CrossRef] [PubMed]
18. Farbiszewski, R.; Radecka, A.; Chwiecko, M.; Holownia, A. The effect of heparegen on antioxidant enzyme activities in ethanol-induced liver injury in rats. Alcohol 1992, 9, 403-407. [CrossRef]
19. Cho, M.H.; Shim, S.M.; Lee, S.R.; Mar,W.; Kim, G.H. Effect of Evodiae fructus extracts on gene expressions related with alcohol metabolism and antioxidation in ethanol-loaded mice. Food. Chem. Toxicol. 2005, 43, 1365-1371. [CrossRef] [PubMed]
20. McDonough, K.H. Antioxidant nutrients and alcohol. Toxicology 2003, 189, 89-97. [CrossRef]
21. Yang, L.; Wu, D.; Cederbaum, A. CYP2E1, oxidative stress and mapk signaling pathways in alcohol-induced hepatotoxicity. J. Biochem. Pharmacol. Res. 2014, 2, 74-90.
22. Li, Y.; Gao, C.; Shi, Y.; Tang, Y.; Liu, L.; Xiong, T.; Du, M.; Xing, M.; Yao, P. Carbon monoxide alleviates ethanol-induced oxidative damage and inflammatory stress through activating p38 MAPK pathway. Toxicol. Appl. Pharmacol. 2013, 273, 53-58. [CrossRef] [PubMed]
23. Park, H.M.; Kim, S.J.; Mun, A.R.; Go, H.K.; Kim, G.B.; Kim, S.Z.; Jang, S.I.; Lee, S.J.; Kim, J.S.; Kang, H.S. Korean red ginseng and its primary ginsenosides inhibit ethanol-induced oxidative injury by suppression of the MAPK pathway in TIB-73 cells. J. Ethnopharmacol. 2012, 141, 1071-1076. [CrossRef] [PubMed]
24. Yao, P.; Nussler, A.; Liu, L.; Hao, L.; Song, F.; Schirmeier, A.; Nussler, N. Quercetin protects human hepatocytes from ethanol-derived oxidative stress by inducing heme oxygenase-1 via the MAPK/Nrf2 pathways. J. Hepatol. 2007, 47, 253-261. [CrossRef] [PubMed]
25. Noh, J.R.; Kim, Y.H.; Gang, G.T.; Hwang, J.H.; Lee, H.S.; Ly, S.Y.; Oh, W.K.; Song, K.S.; Lee, C.H. Hepatoprotective effects of chestnut (Castanea crenata) inner shell extract against chronic ethanol-induced oxidative stress in C57BL/6 mice. Food Chem. Toxicol. 2011, 49, 1537-1543. [CrossRef] [PubMed]
26. Szuster-Ciesielska, A.; Plewka, K.; Daniluk, J.; Kandefer-Szerszen, M. Betulin and betulinic acid attenuate ethanol-induced liver stellate cell activation by inhibiting reactive oxygen species (ROS), cytokine (TNF-α, TGF-β) production and by influencing intracellular signaling. Toxicology 2011, 280, 152-163. [CrossRef] [PubMed]
27. Yang, X.; Dong, C.; Ren, G. Effect of soyasaponins-rich extract from soybean on acute alcohol-induced hepatotoxicity in mice. J. Agric. Food Chem. 2011, 59, 1138-1144. [CrossRef] [PubMed]
28. Bak, M.J.; Jun, M.; Jeong,W.S. Procyanidins from wild grape (Vitis amurensis) seeds regulate are-mediated enzyme expression via Nrf2 coupled with p38 and PI3K/Akt pathway in HepG2 cells. Int. J. Mol. Sci. 2012, 13, 801-818. [CrossRef] [PubMed]
29. Bak, M.J.; Truong, V.L.; Kang, H.S.; Jun, M.; Jeong, W.S. Anti-inflammatory effect of procyanidins from wild grape (Vitis amurensis) seeds in LPS-induced RAW 264.7 cells. Oxid. Med. Cell. Longev. 2013, 2013, 409321-409331. [CrossRef] [PubMed]
30. Mukherjee, S.; Das, S.K.; Vasudevan, D.M. Dietary grapes (Vitis vinifera) feeding attenuates ethanol-induced oxidative stress in blood and modulates immune functions in mice. Indian J. Biochem. Biophys. 2012, 49, 379-385. [PubMed]
31. Jimenez-Lopez, J.M.; Cederbaum, A.I. Green tea polyphenol epigallocatechin-3-gallate protects hepg2 cells against CYP2E1-dependent toxicity. Free Radic. Biol. Med. 2004, 36, 359-370. [CrossRef] [PubMed]
32. Kasdallah-Grissa, A.; Mornagui, B.; Aouani, E.; Hammami, M.; El May, M.; Gharbi, N.; Kamoun, A.; El-Fazaa, S. Resveratrol, a red wine polyphenol, attenuates ethanol-induced oxidative stress in rat liver. Life Sci. 2007, 80, 1033-1039. [CrossRef] [PubMed]
33. Truong, V.L.; Bak, M.J.; Jun, M.; Kong, A.N.; Ho, C.T.; Jeong, W.S. Antioxidant defense and hepatoprotection by procyanidins from almond (Prunus amygdalus) skins. J. Agric. Food Chem. 2014, 62, 8668-8678. [CrossRef] [PubMed]
34. Guo, L.;Wang, L.H.; Sun, B.; Yang, J.Y.; Zhao, Y.Q.; Dong, Y.X.; Spranger, M.I.;Wu, C.F. Direct in vivo evidence of protective effects of grape seed procyanidin fractions and other antioxidants against ethanol-induced oxidative DNA damage in mouse brain cells. J. Agric. Food Chem. 2007, 55, 5881-5891. [CrossRef] [PubMed]
35. Shoji, T.; Masumoto, S.; Moriichi, N.; Akiyama, H.; Kanda, T.; Ohtake, Y.; Goda, Y. Apple procyanidin oligomers absorption in rats after oral administration: Analysis of procyanidins in plasma using the porter method and high-performance liquid chromatography/tandem mass spectrometry. J. Agric. Food Chem. 2006, 54, 884-892. [CrossRef] [PubMed]
36. Déprez, S.; Brezillon, C.; Rabot, S.; Philippe, C.; Mila, I.; Lapierre, C.; Scalbert, A. Polymeric proanthocyanidins are catabolized by human colonic microflora into low-molecular-weight phenolic acids. J. Nutr. 2000, 130, 2733-2738. [PubMed]
37. Zhang, C.; Tian, X.; Luo, Y.; Meng, X. Ginkgolide B attenuates ethanol-induced neurotoxicity through regulating nadph oxidases. Toxicology 2011, 287, 124-130. [CrossRef] [PubMed]
38. Lee, K.M.; Kang, H.S.; Yun, C.H.; Kwak, H.S. Potential in vitro protective effect of quercetin, catechin, caffeic acid and phytic acid against ethanol-induced oxidative stress in SK-Hep-1 cells. Biomol. Ther. 2012, 20, 492-498. [CrossRef] [PubMed]
39. Abhilash, P.A.; Harikrishnan, R.; Indira, M. Ascorbic acid is superior to silymarin in the recovery of ethanol-induced inflammatory reactions in hepatocytes of guinea pigs. J. Physiol. Biochem. 2013, 69, 785-798. [CrossRef] [PubMed]
40. Monzoni, A.; Masutti, F.; Saccoccio, G.; Bellentani, S.; Tiribelli, C.; Giacca, M. Genetic determinants of ethanol-induced liver damage. Mol. Med. 2001, 7, 255-262. [PubMed]
41. Valko, M.; Rhodes, C.J.; Moncol, J.; Izakovic, M.; Mazur, M. Free radicals, metals and antioxidants in oxidative stress-induced cancer. Chem. Biol. Interact. 2006, 160, 1-40. [CrossRef] [PubMed]
42. Panda, V.; Ashar, H.; Srinath, S. Antioxidant and hepatoprotective effect of Garcinia indica fruit rind in ethanol-induced hepatic damage in rodents. Interdiscip. Toxicol. 2012, 5, 207-213. [CrossRef] [PubMed]
43. Bak, M.J.; Jun, M.; Jeong,W.S. Antioxidant and hepatoprotective effects of the red ginseng essential oil in H2O2-treated HepG2 cells and CCl4-treated mice. Int. J. Mol. Sci. 2012, 13, 2314-2330. [CrossRef] [PubMed]
44. Drever, N.; Yin, H.; Kechichian, T.; Costantine, M.; Longo, M.; Saade, G.R.; Bytautiene, E. The expression of antioxidant enzymes in a mouse model of fetal alcohol syndrome. Am. J. Obstet. Gynecol. 2012, 206, 19-22. [CrossRef] [PubMed]
45. Jin, M.; Ande, A.; Kumar, A.; Kumar, S. Regulation of cytochrome P450 2E1 expression by ethanol: Role of oxidative stress-mediated PKC/JNK/SP1 pathway. Cell Death Dis. 2013, 4, e554. [CrossRef] [PubMed]
46. Oliva, J.; Bardag-Gorce, F.; Tillman, B.; French, S.W. Protective effect of quercetin, EGCG, catechin and betaine against oxidative stress induced by ethanol in vitro. Exp. Mol. Pathol. 2011, 90, 295-299. [CrossRef] [PubMed]
47. Liu, S.; Hou, W.; Yao, P.; Zhang, B.; Sun, S.; Nussler, A.K.; Liu, L. Quercetin protects against ethanol-induced oxidative damage in rat primary hepatocytes. Toxicol. in Vitro 2010, 24, 516-522. [CrossRef] [PubMed]
48. Wang, X.; Martindale, J.L.; Liu, Y.; Holbrook, N.J. The cellular response to oxidative stress: Influences of mitogen-activated protein kinase signalling pathways on cell survival. Biochem. J. 1998, 333, 291-300. [CrossRef] [PubMed]
49. Xiao, J.; Wang, J.; Xing, F.; Han, T.; Jiao, R.; Liong, E.C.; Fung, M.L.; So, K.F.; Tipoe, G.L. Zeaxanthin dipalmitate therapeutically improves hepatic functions in an alcoholic fatty liver disease model through modulating mapk pathway. PLoS ONE 2014, 9, e95214. [CrossRef] [PubMed]
50. Zeng, T.; Zhang, C.L.; Song, F.Y.; Zhao, X.L.; Yu, L.H.; Zhu, Z.P.; Xie, K.Q. PI3k/Akt pathway activation was involved in acute ethanol-induced fatty liver in mice. Toxicology 2012, 296, 56-66. [CrossRef] [PubMed]
51. Dikalov, S.; Griendling, K.K.; Harrison, D.G. Measurement of reactive oxygen species in cardiovascular studies. Hypertension 2007, 49, 717-727. [CrossRef] [PubMed]
52. Oyanagui, Y. Reevaluation of assay methods and establishment of kit for superoxide dismutase activity. Anal. Biochem. 1984, 142, 290-296. [CrossRef]
53. Carrillo, M.C.; Kanai, S.; Nokubo, M.; Kitani, K. (-) deprenyl induces activities of both superoxide dismutase and catalase but not of glutathione peroxidase in the striatum of young male rats. Life Sci. 1991, 48, 517-521. [CrossRef]
54. Bogdanska, J.J.; Korneti, P.; Todorova, B. Erythrocyte superoxide dismutase, glutathione peroxidase and catalase activities in healthy male subjects in republic of macedonia. Bratisl. Lek. Listy 2003, 104, 108-114. [PubMed]