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Research Paper

Fusaric acid-induced promoter methylation of DNA methyltransferases triggers DNA hypomethylation in human hepatocellular carcinoma (HepG2) cells

ORCID Icon, ORCID Icon, ORCID Icon & ORCID Icon
Pages 804-817 | Received 01 Feb 2019, Accepted 26 Apr 2019, Published online: 16 May 2019

References

  • Bacon C, Porter J, Norred W, et al. Production of fusaric acid by Fusarium species. Appl Environ Microbiol. 1996 Nov;62:4039–4043. PubMed PMID: 8899996
  • Streit E, Schwab C, Sulyok M, et al. Multi-mycotoxin screening reveals the occurrence of 139 different secondary metabolites in feed and feed ingredients. Toxins (Basel). 2013 Mar;5:504–523. PubMed PMID: 23529186
  • Chen Z, Luo Q, Wang M, et al. A rapid method with UPLC for the determination of fusaric acid in fusarium strains and commercial food and feed products. Indian J Microbiol 2016 Aug;57:68–74. PubMed Central PMCID: PMC5243244.
  • Singh VK, Singh HB, Upadhyay RS. Role of fusaric acid in the development of Fusarium wilt symptoms in tomato: physiological, biochemical and proteomic perspectives. Plant Physiol Biochem. 2017 Sept;118:320–332. PubMed PMID: 28683401
  • D’Alton A, Etherton B. Effects of fusaric acid on tomato root hair membrane potentials and ATP levels. Plant Physiol. 1984 Jan;74:39–42. PubMed PMID: 16663382
  • Diniz S, Oliveira R Effects of fusaric acid on Zea mays L. seedlings. Phyton Int J Exp Bot. 2009 Jan;78:155–160.
  • Pavlovkin J, Mistrik I, Prokop M Some aspects of the phytotoxic action of fusaric acid on primary Ricinus roots. Plant Soil Environ. 2004 Sept;50:397–401.
  • Singh VK, Upadhyay RS. Fusaric acid induced cell death and changes in oxidative metabolism of Solanum lycopersicum L. Bot Stud. 2014 Dec;55:66–76. PubMed PMID: 28510945
  • Sapko O, Utarbaeva AS, Makulbek S Effect of fusaric acid on prooxidant and antioxidant properties of the potato cell suspension culture. Russian J Plant Physiol 2011 Sept;58:828–835.
  • Abdul NS, Nagiah S, Chuturgoon AA. Fusaric acid induces mitochondrial stress in human hepatocellular carcinoma (HepG2) cells. Toxicon. 2016 Sept;119:336–344. PubMed PMID: 27390038
  • Köhler K, Bentrup FW The effect of fusaric acid upon electrical membrane properties and ATP level in photoautotrophic cell suspension cultures of Chenopodium rubrum L. Z Pflanzenphysiol. 1983 Mar;109:355–361.
  • Ghazi T, Nagiah S, Tiloke C, et al. Fusaric acid induces DNA damage and post‐translational modifications of p53 in human hepatocellular carcinoma (HepG2) cells. J Cell Biochem. 2017 Nov;118:3866–3874. PubMed PMID: 28387973
  • Stack BC Jr, Hansen JP, Ruda JM, et al. Fusaric acid: a novel agent and mechanism to treat HNSCC. Otolaryngol Head Neck Surg. 2004 Jul;131:54–60. PubMed PMID: 15243558
  • Dhani S, Nagiah S, Naidoo DB, et al. Fusaric acid immunotoxicity and MAPK activation in normal peripheral blood mononuclear cells and Thp-1 cells. Sci Rep. 2017 Jun;7:3051–3060. PubMed PMID: 28596589
  • Ogata S, Inoue K, Iwata K, et al. Apoptosis induced by picolinic acid-related compounds in HL-60 cells. Biosci Biotechnol Biochem. 2001 Oct;65:2337–2339. PubMed PMID: 11758936
  • Fernandez-Pol J, Klos D, Hamilton P. Cytotoxic activity of fusaric acid on human adenocarcinoma cells in tissue culture. Anticancer Res. 1993;13(Jan):57–64. PubMed PMID: 8476229
  • Diringer MN, Kramarcy NR, Brown JW, et al. Effect of fusaric acid on aggression, motor activity, and brain monoamines in mice. Pharmacol Biochem Behav. 1982 Jan;16:73–79. PubMed PMID: 6173886
  • Li X, Zhang Z-L, Wang HF. Fusaric acid (FA) protects heart failure induced by isoproterenol (ISP) in mice through fibrosis prevention via TGF-β1/SMADs and PI3K/AKT signaling pathways. Biomed Pharmacother. 2017 Sept;93:130–145. PubMed PMID: 28624424
  • Reddy R, Larson C, Brimer G, et al. Developmental toxic effects of fusaric acid in CD1 mice. Bull Environ Contam Toxicol. 1996 Sept;57:354–360. PubMed PMID: 8672059
  • Devaraja S, Girish KS, Santhosh MS, et al. Fusaric acid, a mycotoxin, and its influence on blood coagulation and platelet function. Blood Coagul Fibrinolysis. 2013 Jun;24:419–423. PubMed PMID: 23343693
  • Hidaka H, Nagatsu T, Takeya K, et al. Fusaric acid, a hypotensive agent produced by fungi. J Antibiot. 1969 May;22:228–230. PubMed PMID: 5811396
  • Terasawa F, Kameyama M. The clinical trial of a new hypotensive agent, fusaric acid (5-butylpicolinic acid): the preliminary report. Circ J. 1971 Mar;35:339–357. PubMed PMID: 4932992
  • Yin ES, Rakhmankulova M, Kucera K, et al. Fusaric acid induces a notochord malformation in zebrafish via copper chelation. Biometals. 2015 Aug;28:783–789. PubMed PMID: 25913293
  • Bacon CW, Porter JK, Norred WP. Toxic interaction of fumonisin B1 and fusaric acid measured by injection into fertile chicken egg. Mycopathologia. 1995;129(Jan):29–35. PubMed PMID: 7617015
  • Smith T, MacDonald E. Effect of fusaric acid on brain regional neurochemistry and vomiting behavior in swine. J Anim Sci. 1991 May;69:2044–2049. PubMed PMID: 1712354
  • Fairchild AS, Grimes JL, Porter JK, et al. Effects of diacetoxyscirpenol and fusaric acid on poults: individual and combined effects of dietary diacetoxyscirpenol and fusaric acid on turkey poult performance. Int J Poult Sci. 2005;4(3):350–355.
  • Gopalakrishnan S, Van Emburgh BO, Robertson KD. DNA methylation in development and human disease. Mutat Res. 2008 Dec;647:30–38. PubMed PMID: 18778722
  • Iraola‐Guzmán S, Estivill X, Rabionet R. DNA methylation in neurodegenerative disorders: a missing link between genome and environment? Clin Genet. 2011 Jul;80:1–14. PubMed PMID: 21542837
  • R-K L, Y-C W. Dysregulated transcriptional and post-translational control of DNA methyltransferases in cancer. Cell Biosci. 2014 Aug;4:46–56. PubMed PMID: 25949795
  • Winter J, Jung S, Keller S, et al. Many roads to maturity: microRNA biogenesis pathways and their regulation. Nat Cell Biol. 2009 Mar;11:228–234. PubMed PMID: 19255566
  • Park SY, Lee JH, Ha M, et al. miR-29 miRNAs activate p53 by targeting p85 alpha and CDC42. Nat Struct Mol Biol. 2009 Jan;16:23–29. PubMed PMID: 19079265
  • Wei W, He HB, Zhang WY, et al. miR-29 targets Akt3 to reduce proliferation and facilitate differentiation of myoblasts in skeletal muscle development. Cell Death Dis. 2013 Jun;4:e668–e678. PubMed PMID: 23764849
  • Wang J, Esh C, H-Y C, et al. microRNA-29b prevents liver fibrosis by attenuating hepatic stellate cell activation and inducing apoptosis through targeting PI3K/AKT pathway. Oncotarget. 2015 Mar;6:7325–7338. PubMed PMID: 25356754
  • Teng Y, Zhang Y, Qu K, et al. MicroRNA-29B (mir-29b) regulates the Warburg effect in ovarian cancer by targeting AKT2 and AKT3. Oncotarget. 2015 Dec;6:40799–40814. PubMed PMID: 26512921
  • Garzon R, Liu S, Fabbri M, et al. MicroRNA-29b induces global DNA hypomethylation and tumor suppressor gene reexpression in acute myeloid leukemia by targeting directly DNMT3A and 3B and indirectly DNMT1. Blood. 2009 Jun;113:6411–6418. PubMed PMID: 19211935
  • Fabbri M, Garzon R, Cimmino A, et al. MicroRNA-29 family reverts aberrant methylation in lung cancer by targeting DNA methyltransferases 3A and 3B. Proc Natl Acad Sci USA. 2007 Oct;104:15805–15810. PubMed PMID: 17890317
  • Scott A, Song J, Ewing R, et al. Regulation of protein stability of DNA methyltransferase 1 by post-translational modifications. Acta Biochim Biophys Sin. 2014 Mar;46:199–203. PubMed PMID: 24389641.
  • Denis H, Ndlovu MN, Fuks F. Regulation of mammalian DNA methyltransferases: a route to new mechanisms. EMBO Rep. 2011 Jul;12:647–656. PubMed PMID: 21660058
  • Detich N, Theberge J, Szyf M. Promoter-specific activation and demethylation by MBD2/demethylase. J Biol Chem. 2002 Sept;277:35791–35794. PubMed PMID: 12177048
  • Qin H, Zhu X, Liang J, et al. MicroRNA-29b contributes to DNA hypomethylation of CD4+ T cells in systemic lupus erythematosus by indirectly targeting DNA methyltransferase 1. J Dermatol Sci. 2013 Jan;69:61–67. PubMed PMID: 23142053
  • Novakovic B, Wong NC, Sibson M, et al. DNA methylation-mediated down-regulation of DNA methylatransferase-1 (DNMT1), is coincident with, but not essential for, global hypomethylation in human placenta. J Biol Chem. 2010 Mar;285:9583–9593. PubMed PMID: 20071334
  • Naghitorabi M, Asl JM, Sadeghi HMM, et al. Quantitative evaluation of DNMT3B promoter methylation in breast cancer patients using differential high resolution melting analysis. Res Pharm Sci. 2013 Jul;8:167–175. PubMed PMID: 24019826
  • Peng L, Yuan Z, Ling H, et al. SIRT1 deacetylates the DNA methyltransferase 1 (DNMT1) protein and alters its activities. Mol Cell Biol. 2011 Dec;31:4720–4734. PubMed PMID: 21947282
  • Du Z, Song J, Wang Y, et al. DNMT1 stability is regulated by proteins coordinating deubiquitination and acetylation-driven ubiquitination. Sci Signal. 2010 Nov;3:ra80–ra101. PubMed PMID: 21045206
  • Cheng J, Yang H, Fang J, et al. Molecular mechanism for USP7-mediated DNMT1 stabilization by acetylation. Nat Commun. 2015 May;6:7023–7033. PubMed PMID: 25960197
  • Jia Y, Li P, Fang L, et al. Negative regulation of DNMT3A de novo DNA methylation by frequently overexpressed UHRF family proteins as a mechanism for widespread DNA hypomethylation in cancer. Cell Discov. 2016 Apr;2:16007–16026. PubMed PMID: 27462454
  • Bostick M, Kim JK, Estève PO, et al. UHRF1 plays a role in maintaining DNA methylation in mammalian cells. Science. 2007 Sept;317:1760–1764. PubMed PMID: 17673620
  • Yuan K, Xie K, Fox J, et al. Decreased levels of miR-224 and the passenger strand of miR-221 increase MBD2, suppressing maspin and promoting colorectal tumor growth and metastasis in mice. Gastroenterology. 2013 Oct;145:853–864. PubMed PMID: 23770133
  • Stirzaker C, Song JZ, Ng W, et al. Methyl-CpG-binding protein MBD2 plays a key role in maintenance and spread of DNA methylation at CpG islands and shores in cancer. Oncogene. 2017 Mar;36:1328–1338. PubMed PMID: 27593931
  • Fazio C, Covre A, Cutaia O, et al. Immunomodulatory properties of DNA hypomethylating agents: selecting the optimal epigenetic partner for cancer immunotherapy. Front Pharmacol. 2018 Dec;9:1443–1456. PubMed PMID: 30581389
  • Jackson M, Krassowska A, Gilbert N, et al. Severe global DNA hypomethylation blocks differentiation and induces histone hyperacetylation in embryonic stem cells. Mol Cell Biol. 2004 Oct;24:8862–8871. PubMed PMID: 15456861
  • Rodriguez J, Frigola J, Vendrell E, et al. Chromosomal instability correlates with genome-wide DNA demethylation in human primary colorectal cancers. Cancer Res. 2006 Sept;66:8462–9468. PubMed PMID: 16951157
  • Dodge JE, Okano M, Dick F, et al. Inactivation of Dnmt3b in mouse embryonic fibroblasts results in DNA hypomethylation, chromosomal instability, and spontaneous immortalization. J Biol Chem. 2005 May;280:17986–17991. PubMed PMID: 15757890
  • Jackson-Grusby L, Beard C, Possemato R, et al. Loss of genomic methylation causes p53-dependent apoptosis and epigenetic deregulation. Nat Genet. 2001 Jan;27:31–39. PubMed PMID: 11137995
  • Chuturgoon A, Phulukdaree A, Moodley D. Fumonisin B1 induces global DNA hypomethylation in HepG2 cells – an alternative mechanism of action. Toxicology. 2014 Jan;315:65–69. PubMed PMID: 24280379
  • Demirel G, Alpertunga B, Ozden S. Role of fumonisin B1 on DNA methylation changes in rat kidney and liver cells. Pharm Biol. 2015 Apr;53:1302–1310. PubMed PMID: 25858139
  • Sancak D, Ozden S. Global histone modifications in fumonisin B1 exposure in rat kidney epithelial cells. Toxicol In Vitro. 2015 Oct;29:1809–1815. PubMed PMID: 26208285
  • Chuturgoon AA, Phulukdaree A, Moodley D. Fumonisin B1 modulates expression of human cytochrome P450 1b1 in human hepatoma (Hepg2) cells by repressing Mir-27b. Toxicol Lett. 2014 May;227:50–55. PubMed PMID: 24614526
  • So MY, Tian Z, Phoon YS, et al. Gene expression profile and toxic effects in human bronchial epithelial cells exposed to zearalenone. PLoS One. 2014;9(May):e96404–e96422. PubMed PMID: 24788721
  • Lan M, Han J, Pan MH, et al. Melatonin protects against defects induced by deoxynivalenol during mouse oocyte maturation. J Pineal Res. 2018 Aug;65:e12477–e12487. PubMed PMID: 29453798
  • Zhu C-C, Zhang Y, Duan X, et al. Toxic effects of HT-2 toxin on mouse oocytes and its possible mechanisms. Arch Toxicol. 2016 Jun;90:1495–1505. PubMed PMID: 26138683
  • Mamur S, Ünal F, Yılmaz S, et al. Evaluation of the cytotoxic and genotoxic effects of mycotoxin fusaric acid. Drug Chem Toxicol. 2018 Sept;11:1–9. PubMed PMID: 30204001.
  • Ahn EY, Kim JS, Kim GJ, et al. RASSF1A-mediated regulation of AREG via the Hippo pathway in hepatocellular carcinoma. Mol Cancer Res. 2013 Jul;11:748–758. PubMed PMID: 23594797
  • Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. Methods. 2001 Dec;25:402–408. PubMed PMID: 11846609

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