Fumonisin B1 induces autophagic cell death via activation of ERN1-MAPK8/9/10 pathway in monkey kidney MARC-145 cells
详细信息    查看全文
  • 作者:Shutao Yin ; Xiao Guo ; Jinghua Li ; Linghong Fan ; Hongbo Hu
  • 关键词:Fumonisin B1 ; Autophagy ; Autophagic cell death ; ERN1 ; MAPK8/9/10 ; Nephrotoxicity ; Curcumin
  • 刊名:Archives of Toxicology
  • 出版年:2016
  • 出版时间:April 2016
  • 年:2016
  • 卷:90
  • 期:4
  • 页码:985-996
  • 全文大小:2,644 KB
  • 参考文献:Aoki H, Takada Y, Kondo S, Sawaya R, Aggarwal BB, Kondo Y (2007) Evidence that curcumin suppresses the growth of malignant gliomas in vitro and in vivo through induction of autophagy: role of Akt and extracellular signal-regulated kinase signaling pathways. Mol Pharmacol 72:29–39CrossRef PubMed
    Bennett JW, Klich M (2003) Mycotoxins. Clin Microbiol Rev 16:497–516CrossRef PubMed PubMedCentral
    Bronte E, Coppola G, Di Miceli R, Sucato V, Russo A, Novo S (2013) Role of curcumin in idiopathic pulmonary arterial hypertension treatment: a new therapeutic possibility. Med Hypotheses 81:923–926CrossRef PubMed
    Chen YR, Tan TH (1998) Inhibition of the c-Jun N-terminal kinase (JNK) signaling pathway by curcumin. Oncogene 17:173–178CrossRef PubMed
    Corcelle E, Djerbi N, Mari M, Nebout M, Fiorini C, Fénichel P, Hofman P, Poujeol P, Mograbi B (2007) Control of the autophagy maturation step by the MAPK ERK and p38: lessons from environmental carcinogens. Autophagy 3:57–59CrossRef PubMed
    Costa S, Utan A, Cervellati R, Speroni E, Guerra MC (2007a) Catechins: natural free-radical scavengers against ochratoxin A-induced cell damage in a pig kidney cell line (LLC-PK1). Food Chem Toxicol 45:1910–1917CrossRef PubMed
    Costa S, Utan A, Speroni E, Cervellati R, Piva G, Prandini A, Guerra MC (2007b) Carnosic acid from rosemary extracts: a potential chemoprotective agent against aflatoxin B1. An in vitro study. J Appl Toxicol 27:152–159CrossRef PubMed
    Degterev A, Hitomi J, Germscheid M, Ch’en IL, Korkina O, Teng X, Abbott D, Cuny GD, Yuan C, Wagner G, Hedrick SM, Gerber SA, Lugovskoy A, Yuan J (2008) Identification of RIP1 kinase as a specific cellular target of necrostatins. Nat Chem Biol 4:313–321CrossRef PubMed
    Desai K, Sullards MC, Allegood J, Wang E, Schmelz EM, Hartl M, Humpf HU, Liotta DC, Peng Q, Merrill AH Jr (2002) Fumonisins and fumonisin analogs as inhibitors of ceramide synthase and inducers of apoptosis. Biochim Biophys Acta 1585:188–192CrossRef PubMed
    Domijan AM, Peraica M, Vrdoljak AL, Radić B, Zlender V, Fuchs R (2007) The involvement of oxidative stress in ochratoxin A and fumonisin B1 toxicity in rats. Mol Nutr Food Res 51:1147–1151CrossRef PubMed
    Gao Q, Liu H, Yao Y, Geng L, Zhang X, Jiang L, Shi B, Yang F (2014) Carnosic acid induces autophagic cell death through inhibition of the Akt/mTOR pathway in human hepatoma cells. J Appl Toxicol. doi:10.​1002/​jat.​3049 PubMedCentral
    Ghosh SS, Krieg R, Massey HD, Sica DA, Fakhry I, Ghosh S, Gehr TW (2009) Curcumin and enalapril ameliorate renal failure by antagonizing inflammation in 5/6 nephrectomized rats: role of phospholipase and cyclooxygenase. Am J Physiol Renal Physiol 302:F439–F454CrossRef
    Green DR, Levine B (2014) To be or not to be? How selective autophagy and cell death govern cell fate. Cell 157:65–75CrossRef PubMed PubMedCentral
    Guo X, Dong Y, Yin S, Zhao C, Huo Y, Fan L, Hu H (2013) Patulin induces pro-survival functions via autophagy inhibition and p62 accumulation. Cell Death Dis 4:e822. doi:10.​1038/​cddis.​2013.​349 CrossRef PubMed PubMedCentral
    Han J, Pan XY, Xu Y, Xiao Y, An Y, Tie L, Pan Y, Li XJ (2012) Curcumin induces autophagy to protect vascular endothelial cell survival from oxidative stress damage. Autophagy 8:812–825CrossRef PubMed
    Hassan AM, Mohamed SR, El-Nekeety AA, Hassan NS, Abdel-Wahhab MA (2010) Aquilegia vulgaris L. extract counteracts oxidative stress and cytotoxicity of fumonisin in rats. Toxicon 56:8–18CrossRef PubMed
    He C, Klionsky DJ (2009) Regulation mechanisms and signaling pathways of autophagy. Annu Rev Genet 43:67–93CrossRef PubMed PubMedCentral
    He J, Zhou T (2010) Patented techniques for detoxification of mycotoxins in feeds and food matrices. Recent Pat Food Nutr Agric 2:96–104CrossRef PubMed
    He Q, Riley RT, Sharma RP (2001) Fumonisin-induced tumor necrosis factor-alpha expression in a porcine kidney cell line is independent of sphingoid base accumulation induced by ceramide synthase inhibition. Toxicol Appl Pharmacol 174:69–77CrossRef PubMed
    He Q, Suzuki H, Sharma N, Sharma RP (2006) Ceramide synthase inhibition by fumonisin B1 treatment activates sphingolipid-metabolizing systems in mouse liver. Toxicol Sci 94:388–397CrossRef PubMed
    He W, Wang Q, Xu J, Xu X, Padilla MT, Ren G, Gou X, Lin Y (2012) Attenuation of TNFSF10/TRAIL-induced apoptosis by an autophagic survival pathway involving TRAF2- and RIPK1/RIP1-mediated MAPK8/JNK activation. Autophagy 8:1811–1821CrossRef PubMed PubMedCentral
    Hojjati MR, Li Z, Zhou H, Tang S, Huan C, Ooi E, Lu S, Jiang XC (2005) Effect of ISP-1 on plasma sphingolipid metabolism and atherosclerosis in apoE-deficient mice. J Biol Chem 280:10284–10289CrossRef PubMed
    Huang Z, Ye B, Dai Z, Wu X, Lu Z, Shan P, Huang W (2015) Curcumin inhibits autophagy and apoptosis in hypoxia/reoxygenation-induced myocytes. Mol Med Rep 11:4678–4684PubMed
    Kim JY, Cho TJ, Woo BH, Choi KU, Lee CH, Ryu MH, Park HR (2012) Curcumin-induced autophagy contributes to the decreased survival of oral cancer cells. Arch Oral Biol 57:1018–1025CrossRef PubMed
    Klionsky DJ, Schulman BA (2014) Dynamic regulation of macroautophagy by distinctive ubiquitin-like proteins. Nat Struct Mol Biol 21:336–345CrossRef PubMed PubMedCentral
    Kroemer G, Levine B (2008) Autophagic cell death: the story of a misnomer. Nat Rev Mol Cell Biol 9:1004–1010CrossRef PubMed PubMedCentral
    McCormick SP (2013) Microbial detoxification of mycotoxins. J Chem Ecol 39:907–918CrossRef PubMed
    Park EJ, Jeon CH, Ko G, Kim J, Sohn DH (2000) Protective effect of curcumin in rat liver injury induced by carbon tetrachloride. J Pharm Pharmacol 52:437–440CrossRef PubMed
    Prasad S, Gupta SC, Tyagi AK, Aggarwal BB (2014) Curcumin, a component of golden spice: from bedside to bench and back. Biotechnol Adv 32:1053–1064CrossRef PubMed
    Rumora L, Kovacić S, Rozgaj R, Cepelak I, Pepeljnjak S, Zanić Grubisić T (2002) Cytotoxic and genotoxic effects of fumonisin B1 on rabbit kidney RK13 cell line. Arch Toxicol 76:55–61CrossRef PubMed
    Ryter SW, Mizumura K, Choi AM (2014) The impact of autophagy on cell death modalities. Int J Cell Biol 2014:502676. doi:10.​1155/​2014/​502676 CrossRef PubMed PubMedCentral
    Schneider JL, Cuervo AM (2014) Autophagy and human disease: emerging themes. Curr Opin Genet Dev 26C:16–23CrossRef
    Seefelder W, Humpf HU, Schwerdt G, Freudinger R, Gekle M (2003) Induction of apoptosis in cultured human proximal tubule cells by fumonisins and fumonisin metabolites. Toxicol Appl Pharmacol 192:146–153CrossRef PubMed
    Stockmann-Juvala H, Savolainen K (2008) A review of the toxic effects and mechanisms of action of fumonisin B1. Hum Exp Toxicol 27:799–809CrossRef PubMed
    Thayyullathil F, Rahman A, Pallichankandy S, Patel M, Galadari S (2014) ROS-dependent prostate apoptosis response-4 (Par-4) up-regulation and ceramide generation are the prime signaling events associated with curcumin-induced autophagic cell death in human malignant glioma. FEBS Open Bio 4:763–776CrossRef PubMed PubMedCentral
    Tiwari V, Chopra K (2013) Protective effect of curcumin against chronic alcohol-induced cognitive deficits and neuroinflammation in the adult rat brain. Neuroscience 244:147–158CrossRef PubMed
    Varga J, Kocsubé S, Péteri Z, Vágvölgyi C, Tóth B (2010) Chemical, physical and biological approaches to prevent ochratoxin induced toxicoses in humans and animals. Toxins (Basel) 2:1718–1750CrossRef
    Voss KA, Riley RT, Norred WP, Bacon CW, Meredith FI, Howard PC, Plattner RD, Collins TF, Hansen DK, Porter JK (2001) An overview of rodent toxicities: liver and kidney effects of fumonisins and Fusarium moniliforme. Environ Health Perspect 109(Suppl 2):259–266CrossRef PubMed PubMedCentral
    Wang H, Lu Q, Cheng S, Wang X, Zhang H (2013) Autophagy activity contributes to programmed cell death in Caenorhabditis elegans. Autophagy 9:1975–1982CrossRef PubMed
    Wang Y, Zheng W, Bian X, Yuan Y, Gu J, Liu X, Liu Z, Bian J (2014) Zearalenone induces apoptosis and cytoprotective autophagy in primary Leydig cells. Toxicol Lett 226(1):82–191
    Yamauchi Y, Izumi Y, Asakura K, Hayashi Y, Nomori H (2012) Curcumin induces autophagy in ACC-MESO-1 cells. Phytother Res 26:1779–1783CrossRef PubMed
  • 作者单位:Shutao Yin (1)
    Xiao Guo (1)
    Jinghua Li (1)
    Linghong Fan (2)
    Hongbo Hu (1)

    1. Department of Nutrition and Health, College of Food Science and Nutritional Engineering, China Agricultural University, No 17 Qinghua East Road, Haidian District, Beijing, 100083, China
    2. College of Veterinary Medicine, China Agricultural University, No 2 Yunmingyuan West Road, Hiadian District, Beijing, 1000193, China
  • 刊物主题:Pharmacology/Toxicology; Occupational Medicine/Industrial Medicine; Environmental Health; Biomedicine general;
  • 出版者:Springer Berlin Heidelberg
  • ISSN:1432-0738
文摘
Mycotoxins are secondary fungal metabolites that are capable of inducing a variety of toxic effects in animals and humans resulting from the consumption of the contaminated food. Understanding the mechanisms of the toxicities behind these mycotoxins is required to develop mechanism-based approach to counteract their toxic potential. Fumonisin B1 (FB1) is the most prevalent member of fumonisins that are a group of mycotoxins produced primarily by Fusarium verticillioides and Fusarium proliferatum. Kidney is one of the primary target organs for FB1 action. Using monkey kidney MARC-145 cells as an intro model, we found that FB1 induced caspase-independent programmed cell death accompanied with autophagy induction. Inhibition of autophagy by either chemical inhibitors or RNAi approach led to a significant reduction in cell death by FB1 exposure, indicating possible involvement of autophagy-mediated cell death in nephrotoxicity of FB1. Further mechanistic investigation revealed that activation of ERN1-MAPK8/9/10 axis played a critical role in autophagy induction and autophagy-mediated cell death by FB1 exposure. In addition, we demonstrated that disruption of sphingolipid metabolism was an apical event in FB1-induced ERN1-MAPK8/9/10-mediated autophagic cell death in MARC-145 cells. Lastly, we identified curcumin, a naturally occurring plant phenolic compound, as a possible anti-FB1 agent that can be used to protect kidney cells from FB1-induced cell death through inhibition of MAPK8/9/10 activation.

© 2004-2018 中国地质图书馆版权所有 京ICP备05064691号 京公网安备11010802017129号

地址:北京市海淀区学院路29号 邮编:100083

电话:办公室:(+86 10)66554848;文献借阅、咨询服务、科技查新:66554700