REVIEW

Oxidative Damage Induced by Aflatoxin B1 and Antioxidant Defense Mechanism of Different Bioactive Substances in Animals

  • WAN Xiaoli ,
  • YANG Haiming ,
  • WANG Zhiyue
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  • 1. College of Animal Science and Technology, Yangzhou University, Yangzhou 225009, China;
    2. Institutes of Agricultural Science and Technology Development, Yangzhou University, Yangzhou 225009, China

Received date: 2021-07-31

  Online published: 2022-02-15

Abstract

Mycotoxins are found in a wide range of agricultural products and pose a threat to human and animal health. Aflatoxin is the most harmful, among which aflatoxin B1 (AFB1) is the most toxic. Oxidative stress can be induced during AFB1 poisoning in animals. In this paper, the mechanism of AFB1 induced oxidative stress, and the antioxidant defense effect of different bioactive substances and the potential mechanism in animals were summarized. This paper will provide reference for the prevention and control of AFB1 pollution in animal production.

Cite this article

WAN Xiaoli , YANG Haiming , WANG Zhiyue . Oxidative Damage Induced by Aflatoxin B1 and Antioxidant Defense Mechanism of Different Bioactive Substances in Animals[J]. Chinese Journal of Animal Nutrition, 2022 , 34(2) : 710 -719 . DOI: 10.3969/j.issn.1006-267x.2022.02.004

References

[1] 范楷, 祭芳, 徐剑宏, 等.长三角地区市场常见农产品中40种真菌毒素的污染状况和特征分析[J].中国农业科学, 2021, 54(13):2870-2884. FAN K, JI F, XU J H, et al.Natural occurrence and characteristic analysis of 40 mycotoxins in agro-products from Yangtze delta region[J].Scientia Agricultura Sinica, 2021, 54(13):2870-2884.(in Chinese)
[2] SAINI S S, KAUR A.Aflatoxin B1:toxicity, characteristics and analysis:mini review[J].Global Advanced Research Journal of Chemistry and Material Science, 2012, 1(4):63-70.
[3] 周建川, 郑文革, 赵丽红, 等.2016年中国饲料和原料中霉菌毒素污染调查报告[J].中国猪业, 2017, 12(6):22-26, 32. ZHOU J C, ZHENG W G, ZHAO L H, et al.Investigation report on mycotoxin contamination in feed and raw materials in China in 2016[J].China Swine Industry, 2017, 12(6):22-26, 32.(in Chinese)
[4] 夏超笃, 艾琴, 湛穗璋, 等.霉菌毒素吸附剂在动物饲料中应用的研究进展[J].畜牧与饲料科学, 2017, 38(4):27-31. XIA C D, AI Q, ZHAN S Z, et al.Research progress on application of mycotoxin adsorbent in animal feed[J].Animal Husbandry and Feed Science, 2017, 38(4):27-31.(in Chinese)
[5] LEE S E, CAMPBELL B C, MOLYNEUX R J, et al.Inhibitory effects of naturally occurring compounds on aflatoxin B1 biotransformation[J].Journal of Agricultural and Food Chemistry, 2001, 49(11):5171-5177.  
[6] MUGHAL M J, PENG X, KAMBOH A A, et al.Aflatoxin B1 induced systemic toxicity in poultry and rescue effects of selenium and zinc[J].Biological Trace Element Research, 2017, 178(2):292-300.  
[7] MARIN D E, TARANU I.Overview on aflatoxins and oxidative stress[J].Toxin Reviews, 2012, 31(3/4):32-43.
[8] DIAZ G J, MURCIA H W, CEPEDA S M.Cytochrome P450 enzymes involved in the metabolism of aflatoxin B1 in chickens and quail[J].Poultry Science, 2010, 89(11):2461-2469.  
[9] SHIMAMOTO N.A pathophysiological role of cytochrome p450 involved in production of reactive oxygen species[J].Yakugaku Zasshi, 2013, 133(4):435-450.  
[10] RAWAL S, KIM J E, COULOMBE R, Jr.Aflatoxin B1 in poultry:toxicology, metabolism and prevention[J].Research in Veterinary Science, 2010, 89(3):325-331.  
[11] YILMAZ S, KAYA E, KARACA A, et al.Aflatoxin B1 induced renal and cardiac damage in rats:protective effect of lycopene[J].Research in Veterinary Science, 2018, 119:268-275.
[12] VAKIFAHMETOGLU-NORBERG H, OUCHIDA A T, NORBERG E.The role of mitochondria in metabolism and cell death[J].Biochemical and Biophysical Research Communications, 2017, 482(3):426-431.  
[13] CHEN J, CHEN K J, YUAN S B, et al.Effects of aflatoxin B1 on oxidative stress markers and apoptosis of spleens in broilers[J].Toxicology and Industrial Health, 2016, 32(2):278-284.  
[14] 余程, 刘妍, 王胜军, 等.黄曲霉毒素B1致肉仔鸡肝损伤的氧化应激机制研究[J].中国畜牧杂志, 2017, 53(6):92-97. YU C, LIU Y, WANG S J, et al.Oxidative stress mechanism of aflatoxin B1 induced liver injury in broilers[J].Chinese Journal of Animal Science, 2017, 53(6):92-97.(in Chinese)
[15] 石达友, 李燕华, 黄墁玲, 等.黄曲霉毒素B1对肉鸡肝线粒体自由基代谢的影响[J].中国兽医杂志, 2011, 47(3):9-12. SHI D Y, LI Y H, HUANG M L, et al.Influences of aflatoxin B1 on hepatic mitochondrial free radical metabolism in broiler[J].Chinese Journal of Veterinary Medicine, 2011, 47(3):9-12.(in Chinese)
[16] SHI D Y, LIAO S Q, GUO S N, et al.Protective effects of selenium on aflatoxin B1-induced mitochondrial permeability transition, DNA damage, and histological alterations in duckling liver[J].Biological Trace Element Research, 2015, 163(1/2):162-168.
[17] HUANG W Y, CAO Z, YAO Q C, et al.Mitochondrial damage are involved in aflatoxin B1-induced testicular damage and spermatogenesis disorder in mice[J].The Science of the Total Environment, 2020, 701:135077.
[18] NITURE S K, KASPAR J W, SHEN J, et al.Nrf2 signaling and cell survival[J].Toxicology and Applied Pharmacology, 2010, 244(1):37-42.  
[19] PALL M L, LEVINE S.Nrf2, a master regulator of detoxification and also antioxidant, anti-inflammatory and other cytoprotective mechanisms, is raised by health promoting factors[J].Acta Physiologica Sinica, 2015, 67(1):1-18.
[20] DINKOVA-KOSTOVA A T, ABRAMOV A Y.The emerging role of Nrf2 in mitochondrial function[J].Free Radical Biology & Medicine, 2015, 88(Pt B):179-188.  
[21] HOLMSTRÖM K M, KOSTOV R V, DINKOVA-KOSTOVA A T.The multifaceted role of Nrf2 in mitochondrial function[J].Current Opinion in Toxicology, 2016, 1:80-91.
[22] KOVAC S, ANGELOVA P R, HOLMSTRÖM K M, et al.Nrf2 regulates ROS production by mitochondria and NADPH oxidase[J].Biochimica et Biophysica Acta, 2015, 1850(4):794-801.  
[23] LUDTMANN M H R, ANGELOVA P R, ZHANG Y, et al.Nrf2 affects the efficiency of mitochondrial fatty acid oxidation[J].Biochemical Journal, 2014, 457(3):415-424.  
[24] THIMMULAPPA R K, MAI K H, SRISUMA S, et al.Identification of Nrf2-regulated genes induced by the chemopreventive agent sulforaphane by oligonucleotide microarray[J].Cancer Research, 2002, 62(18):5196-5203.
[25] TAGUCHI K, TAKAKU M, EGNER P A, et al.Generation of a new model rat:Nrf2 knockout rats are sensitive to aflatoxin B1 toxicity[J].Toxicological Sciences, 2016, 152(1):40-52.  
[26] ILIC Z, CRAWFORD D, VAKHARIA D, et al.Glutathione-S-transferase A3 knockout mice are sensitive to acute cytotoxic and genotoxic effects of aflatoxin B1[J].Toxicology and Applied Pharmacology, 2010, 242(3):241-246.  
[27] GOWDA N K S, LEDOUX D R, ROTTINGHAUS G E, et al.Efficacy of turmeric (Curcuma longa), containing a known level of curcumin, and a hydrated sodium calcium aluminosilicate to ameliorate the adverse effects of aflatoxin in broiler chicks[J].Poultry Science, 2008, 87(6):1125-1130.  
[28] GOWDA N K S, LEDOUX D R, ROTTINGHAUS G E, et al.Antioxidant efficacy of curcuminoids from turmeric (Curcuma longa L.) powder in broiler chickens fed diets containing aflatoxin B1[J].The British Journal of Nutrition, 2009, 102(11):1629-1634.  
[29] ZHANG N Y, QI M, ZHAO L, et al.Curcumin prevents aflatoxin B1 hepatoxicity by inhibition of cytochrome P450 isozymes in chick liver[J].Toxins, 2016, 8(11):327.
[30] EL-AGAMY D S.Comparative effects of curcumin and resveratrol on aflatoxin B1-induced liver injury in rats[J].Archives of Toxicology, 2010, 84(5):389-396.  
[31] SRIDHAR M, SUGANTHI R U, THAMMIAHA V.Effect of dietary resveratrol in ameliorating aflatoxin B1-induced changes in broiler birds[J].Journal of Animal Physiology and Animal Nutrition, 2015, 99(6):1094-1104.  
[32] ZHOU Y F, JIN Y C, YU H, et al.Resveratrol inhibits aflatoxin B1-induced oxidative stress and apoptosis in bovine mammary epithelial cells and is involved the Nrf2 signaling pathway[J].Toxicon, 2019, 164:10-15.
[33] YILMAZ S, KAYA E, KISACAM M A, et al.The effect on oxidative stress of aflatoxin and protective effect of lycopene on aflatoxin damage[M]//ABDULRA'UF L B.Aflatoxin-control, analysis, detection and health risks.London:IntechOpen, 2017.
[34] TANG L L, GUAN H X, DING X L, et al.Modulation of aflatoxin toxicity and biomarkers by lycopene in F344 rats[J].Toxicology and Applied Pharmacology, 2007, 219(1):10-17.  
[35] XU F B, YU K Y, YU H Y, et al.Lycopene relieves AFB1-induced liver injury through enhancing hepatic antioxidation and detoxification potential with Nrf2 activation[J].Journal of Functional Foods, 2017, 39:215-224.
[36] REDDY L, ODHAV B, BHOOLA K.Aflatoxin B1-induced toxicity in HepG2 cells inhibited by carotenoids:morphology, apoptosis and DNA damage[J].Biological Chemistry, 2006, 387(1):87-93.  
[37] CHOI K C, CHUNG W T, KWON J K, et al.Inhibitory effects of quercetin on aflatoxin B1-induced hepatic damage in mice[J].Food and Chemical Toxicology, 2010, 48(10):2747-2753.  
[38] 李丽, 张根义.槲皮素对黄曲霉毒素B1致大鼠肝细胞毒性的保护作用[J].食品工业科技, 2018, 39(13):117-121, 127. LI L, ZHANG G Y.Protective effect of quercetin against the toxicity of aflatoxin B1 toward buffalo rat liver cells[J].Science and Technology of Food Industry, 2018, 39(13):117-121, 127.(in Chinese)
[39] GHADIRI S, SPALENZA V, DELLAFIORA L, et al.Modulation of aflatoxin B1 cytotoxicity and aflatoxin M1 synthesis by natural antioxidants in a bovine mammary epithelial cell line[J].Toxicology in Vitro, 2019, 57:174-183.
[40] GAO S S, CHEN X Y, ZHU R Z, et al.Dual effects of phloretin on aflatoxin B1 metabolism:activation and detoxification of aflatoxin B1[J].BioFactors, 2012, 38(1):34-43.  
[41] 赵静芳, 邓志杰, 肖德强, 等.表没食子儿茶素没食子酸酯对黄曲霉毒素B1诱导大鼠急性肝损伤的抗氧化作用[J].实用医学杂志, 2018, 34(11):1753-1756, 1761. ZHAO J F, DENG Z J, XIAO D Q, et al.Antioxidant effect of EGCG on AFB1 induced acute liver injury in rats[J].The Journal of Practical Medicine, 2018, 34(11):1753-1756, 1761.(in Chinese)
[42] RAJPUT S A, SUN L H, ZHANG N Y, et al.Ameliorative effects of grape seed proanthocyanidin extract on growth performance, immune function, antioxidant capacity, biochemical constituents, liver histopathology and aflatoxin residues in broilers exposed to aflatoxin B1[J].Toxins, 2017, 9(11):371.
[43] RAJPUT S A, SUN L H, ZHANG N Y, et al.Grape seed proanthocyanidin extract alleviates aflatoxin B1-induced immunotoxicity and oxidative stress via modulation of NF-κB and Nrf2 signaling pathways in broilers[J].Toxins, 2019, 11(1):23.
[44] RAJPUT S A, ZHANG C, FENG Y, et al.Proanthocyanidins alleviates aflatoxin B1-induced oxidative stress and apoptosis through mitochondrial pathway in the bursa of fabricius of broilers[J].Toxins, 2019, 11(3):157.
[45] SINGH C, PRAKASH C, MISHRA P, et al.Hepatoprotective efficacy of Premna integrifolia L. leaves against aflatoxin B1-induced toxicity in mice[J].Toxicon, 2019, 166:88-100.
[46] LIAO S Q, SHI D Y, CLEMONS-CHEVIS C L, et al.Protective role of selenium on aflatoxin B1-induced hepatic dysfunction and apoptosis of liver in ducklings[J].Biological Trace Element Research, 2014, 162(1/2/3):296-301.
[47] SHI D Y, GUO S, LIAO S Q, et al.Protection of selenium on hepatic mitochondrial respiratory control ratio and respiratory chain complex activities in ducklings intoxicated with aflatoxin B1[J].Biological Trace Element Research, 2012, 145(3):312-317.  
[48] WANG F Y, SHU G, PENG X, et al.Protective effects of sodium selenite against aflatoxin B1-induced oxidative stress and apoptosis in broiler spleen[J].International Journal of Environmental Research and Public Health, 2013, 10(7):2834-2844.  
[49] SUN L H, ZHANG N Y, ZHU M K, et al.Prevention of aflatoxin B1 hepatoxicity by dietary selenium is associated with inhibition of cytochrome P450 isozymes and up-regulation of 6 selenoprotein genes in chick liver[J].The Journal of Nutrition, 2015, 146(4):655-661.  
[50] 芮小丽, 陈思潭, 李春梅.硒对黄曲霉毒素 B1暴露肉鸡肝脏氧化损伤的保护作用[J].动物营养学报, 2014, 26(8):2281-2288. RUI X L, CHEN S T, LI C M.Protective effects of selenium on aflatoxin B1 induced hepatic oxidative stress in broilers[J].Chinese Journal of Animal Nutrition, 2014, 26(8):2281-2288.(in Chinese)
[51] LIU L N, CHEN F, QIN S Y, et al.Effects of selenium-enriched yeast improved aflatoxin B1-induced changes in growth performance, antioxidation capacity, IL-2 and IFN-γ contents, and gene expression in mice[J].Biological Trace Element Research, 2019, 191(1):183-188.  
[52] ZHU L Y, HUANG C C, YANG X, et al.Proteomics reveals the alleviation of zinc towards aflatoxin B1-induced cytotoxicity in human hepatocyes (HepG2 cells)[J].Ecotoxicology and Environmental Safety, 2020, 198:110596.
[53] MA Q G, GAO X, ZHOU T, et al.Protective effect of Bacillus subtilis ANSB060 on egg quality, biochemical and histopathological changes in layers exposed to aflatoxin B1[J].Poultry Science, 2012, 91(11):2852-2857.  
[54] FAN Y, ZHAO L H, MA Q G, et al.Effects of Bacillus subtilis ANSB060 on growth performance, meat quality and aflatoxin residues in broilers fed moldy peanut meal naturally contaminated with aflatoxins[J].Food and Chemical Toxicology, 2013, 59:748-753.
[55] FAN Y, ZHAO L H, JI C, et al.Protective effects of Bacillus subtilis ANSB060 on serum biochemistry, histopathological changes and antioxidant enzyme activities of broilers fed moldy peanut meal naturally contaminated with aflatoxins[J].Toxins, 2015, 7(8):3330-3343.  
[56] ZHANG L Y, MA Q G, MA S S, et al.Ameliorating effects of Bacillus subtilis ANSB060 on growth performance, antioxidant functions, and aflatoxin residues in ducks fed diets contaminated with aflatoxins[J].Toxins, 2016, 9(1):1.
[57] LI X T, LV Z M, CHEN J, et al.Bacillus amyloliquefaciens B10 can alleviate liver apoptosis and oxidative stress induced by aflatoxin B1[J].Food and Chemical Toxicology, 2021, 151:112124.
[58] ZHAO Y Q, WANG T C, LI P, et al.Bacillus amyloliquefaciens B10 can alleviate aflatoxin B1-induced kidney oxidative stress and apoptosis in mice[J].Ecotoxicology and Environmental Safety, 2021, 218:112286.
[59] KHANIAN M, KARIMI-TORSHIZI M A, ALLAMEH A.Alleviation of aflatoxin-related oxidative damage to liver and improvement of growth performance in broiler chickens consumed Lactobacillus plantarum 299v for entire growth period[J].Toxicon, 2019, 158:57-62.
[60] 蒲俊宁, 原清会, 陈代文, 等.营养性复合添加剂对饲喂含黄曲霉毒素B1饲粮生长育肥猪生长性能、抗氧化能力、肝脏功能和毒素残留的影响[J].动物营养学报, 2019, 31(10):4691-4700. PU J N, YUAN Q H, CHEN D W, et al.Effects of nutritional compound additives on growth performance, antioxidant capacity, liver function and toxin residues of growing-finishing pigs fed diets contaminated with aflatoxin B1[J].Chinese Journal of Animal Nutrition, 2019, 31(10):4691-4700.(in Chinese)
[61] LI Y, MA Q G, ZHAO L H, et al.Protective efficacy of alpha-lipoic acid against aflatoxin B1-induced oxidative damage in the liver[J].Asian-Australasian Journal of Animal Sciences, 2014, 27(6):907-915.  
[62] ELWAN H, XIE C, MIAO L P, et al.Methionine alleviates aflatoxin B1-induced broiler chicks embryotoxicity through inhibition of caspase-dependent apoptosis and enhancement of cellular antioxidant status[J].Poultry Science, 2021, 100(8):101103.
[63] YATES M S, KWAK M K, EGNER P A, et al.Potent protection against aflatoxin-induced tumorigenesis through induction of Nrf2-regulated pathways by the triterpenoid 1-[2-cyano-3-, 12-dioxooleana-1, 9(11)-dien-28-oyl]imidazole[J].Cancer Research, 2006, 66(4):2488-2494.  
[64] 扈红蕾, 高健, 郭文君, 等.富氢水在黄曲霉毒素B1致大鼠肝损伤模型中的抗损伤作用[J].生理学报, 2019, 71(5):725-731. HU H L, GAO J, GUO W J, et al.Anti-injury effect of hydrogen-enriched water in a rat model of liver injury induced by aflatoxin B1[J].Acta Physiologica Sinica, 2019, 71(5):725-731.(in Chinese)
[65] 谢佳雨, 张雯, 杨靖亚, 等.壳寡糖对黄曲霉毒素B1诱导大鼠肝细胞毒性损伤的干预作用[J/OL].上海海洋大学学报:1-14.(2021-02-05).http://kns.cnki.net/kcms/detail/31.2024.S.20210205.1346.006.html. XIE J Y, ZAHNG W, YANG J Y, et al.Intervention effect of chitooligosaccharides on aflatoxin B1 induced toxic damage of rat liver cells[J/OL].Journal of Shanghai Ocean University:1-14.(2021-02-05)].http://kns.cnki.net/kcms/detail/31.2024.S.20210205.1346.006.html.(in Chinese)
[66] 唐日益.牛磺酸对大鼠黄曲霉毒素B1中毒的干预作用及机制研究[D].博士学位论文.沈阳:沈阳农业大学, 2019. TANG R Y.Protective effect and mechanism of taurine on AFB1 induced injury in rats[D].Ph.D.Thesis.Shenyang:Shenyang Agricultural University, 2019.(in Chinese)
[67] 师文文, 吕攀, 徐庆强, 等.油酸在黄曲霉毒素诱导肝细胞损伤中的保护作用[J].中国油料作物学报, 2019, 41(2):267-274. SHI W W, LYU P, XU Q Q, et al.Protective effect of oleic acid on aflatoxin-induced hepatocyte injury[J].Chinese Journal of Oil Crop Sciences, 2019, 41(2):267-274.(in Chinese)
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