Sulforaphane protects against ethanol-induced apoptosis in neural crest cells through restoring epithelial-mesenchymal transition by epigenetically modulating the expression of Snail1

Caputo C, Wood E, Jabbour L. Impact of fetal alcohol exposure on body systems: A systematic review. Birth Defects Res C Embryo Today. 2016 Jun;108(2):174–80. doi: https://doi.org/10.1002/bdrc.21129. PubMed PMID: 27297122; eng. Del Campo M, Jones KL. A review of the physical features of the fetal alcohol spectrum disorders. Eur J Med Genet. 2017 Jan;60(1):55–64. doi: S1769–7212(16)30382–2 [pii] https://doi.org/10.1016/j.ejmg.2016.10.004. PubMed PMID: 27729236; eng. Chen SY, Dehart DB, Sulik KK. Protection from ethanol-induced limb malformations by the superoxide dismutase/catalase mimetic, EUK-134. FASEB J. Off. Publ. Feder. Am. Soc. Exp. Biol. 2004 Aug;18(11):1234–6. doi: https://doi.org/10.1096/fj.03-0850fje. PubMed PMID: 15208273. Sulik KK. Fetal alcohol spectrum disorder: pathogenesis and mechanisms. Handb. Clin. Neurol. 2014;125:463–75. doi: https://doi.org/10.1016/B978-0-444-62619-6.00026-4. PubMed PMID: 25307590. Granato A, Dering B. Alcohol and the developing brain: why neurons die and how survivors change. Int J Mol Sci. 2018 Sep 30;19(10). doi: https://doi.org/10.3390/ijms19102992. PubMed PMID: 30274375; PubMed Central PMCID: PMCPMC6213645. Sulik KK, Johnston MC, Daft PA, et al. Fetal alcohol syndrome and DiGeorge anomaly: critical ethanol exposure periods for craniofacial malformations as illustrated in an animal model. Am J Med Genet Suppl. 1986;2:97–112. PubMed PMID: 3146306; eng. Chen X, Liu J, Feng WK, et al. MiR-125b protects against ethanol-induced apoptosis in neural crest cells and mouse embryos by targeting Bak 1 and PUMA. Exp Neurol. 2015 Sep;271:104–11. doi: https://doi.org/10.1016/j.expneurol.2015.04.026 S0014-4886(15)00166-1. Smith SM. Alcohol-induced cell death in the embryo. Alcohol Health Res World. 1997;21(4):287–97. PubMed PMID: 15706739; eng. Huang X, Saint-Jeannet JP. Induction of the neural crest and the opportunities of life on the edge. Dev. Biol. 2004 Nov 1;275(1):1–11. doi: https://doi.org/10.1016/j.ydbio.2004.07.033. PubMed PMID: 15464568. Theveneau E, Mayor R. Neural crest delamination and migration: from epithelium-to-mesenchyme transition to collective cell migration. Dev. Biol. 2012 Jun 1;366(1):34–54. doi: https://doi.org/10.1016/j.ydbio.2011.12.041. PubMed PMID: 22261150. Zhang D, Ighaniyan S, Stathopoulos L, et al. The neural crest: a versatile organ system. Birth defects research Part C, Embryo Today: Reviews. 2014 Sep;102(3):275–98. doi: https://doi.org/10.1002/bdrc.21081. PubMed PMID: 25227568; eng. Maurer J, Fuchs S, Jager R, et al. Establishment and controlled differentiation of neural crest stem cell lines using conditional transgenesis. Differentiation. 2007 Sep;75(7):580–91. doi: https://doi.org/10.1111/j.1432-0436.2007.00164.x. PubMed PMID: 17381545. Shakhova O, Sommer L. Neural Crest-derived Stem Cells. 2008. doi: NBK44752 [bookaccession] https://doi.org/10.3824/stembook.1.51.1. PubMed PMID: 20614636; eng. Kalluri R, Weinberg RA. The basics of epithelial-mesenchymal transition. J Clin Invest. 2009 Jun;119(6):1420–8. doi: https://doi.org/10.1172/JCI39104. PubMed PMID: 19487818; PubMed Central PMCID: PMCPMC2689101. Thiery JP, Acloque H, Huang RY, et al. Epithelial-mesenchymal transitions in development and disease. Cell. 2009 Nov 25;139(5):871–90. doi: https://doi.org/10.1016/j.cell.2009.11.007. PubMed PMID: 19945376. Nieto MA, Huang RY, Jackson RA, et al. Emt: 2016. Cell. 2016 Jun 30;166(1):21–45. doi: https://doi.org/10.1016/j.cell.2016.06.028. PubMed PMID: 27368099. Barriere G, Tartary M, Rigaud M. Epithelial mesenchymal transition: a new insight into the detection of circulating tumor cells. ISRN Oncol. 2012;2012:382010. doi: https://doi.org/10.5402/2012/382010. PubMed PMID: 22577580; PubMed Central PMCID: PMCPMC3345219. Powell DR, Blasky AJ, Britt SG, et al. Riding the crest of the wave: parallels between the neural crest and cancer in epithelial-to-mesenchymal transition and migration. Wiley Interdiscip Rev Syst Biol Med. 2013 Jul-Aug;5(4):511–22. doi: https://doi.org/10.1002/wsbm.1224. PubMed PMID: 23576382; PubMed Central PMCID: PMCPMC3739939. Heldin CH, Landstrom M, Moustakas A. Mechanism of TGF-beta signaling to growth arrest, apoptosis, and epithelial-mesenchymal transition. Curr. Opin. Cell Biol. 2009 Apr;21(2):166–76. doi: https://doi.org/10.1016/j.ceb.2009.01.021. PubMed PMID: 19237272. Liu Y, He K, Hu Y, et al. YAP modulates TGF-beta 1-induced simultaneous apoptosis and EMT through upregulation of the EGF receptor. Sci Rep-Uk. 2017 Apr 20;7. doi: ARTN 45523https://doi.org/10.1038/srep45523. PubMed PMID: WOS:000399694400001; (English). Robson EJ, Khaled WT, Abell K, et al. Epithelial-to-mesenchymal transition confers resistance to apoptosis in three murine mammary epithelial cell lines. Differentiation. 2006 Jun;74(5):254–64. doi: https://doi.org/10.1111/j.1432-0436.2006.00075.x. PubMed PMID: 16759291. Park SJ, Park BS, Yu SB, et al. Induction of apoptosis and inhibition of epithelial mesenchymal transition by alpha-mangostin in MG-63 cell lines. Evid Based Complement Alternat Med. 2018;2018:3985082. doi: https://doi.org/10.1155/2018/3985082. PubMed PMID: 29853951; PubMed Central PMCID: PMC5944198. eng. Cano A, Perez-Moreno MA, Rodrigo I, et al. The transcription factor snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nat. Cell Biol. 2000 Feb;2(2):76–83. doi: https://doi.org/10.1038/35000025. PubMed PMID: 10655586. Kaufhold S, Bonavida B. Central role of Snail1 in the regulation of EMT and resistance in cancer: a target for therapeutic intervention. J Exp Clin Cancer Res. 2014 Aug 2;33:62. doi: https://doi.org/10.1186/s13046-014-0062-0. PubMed PMID: 25084828; PubMed Central PMCID: PMCPMC4237825. Lin Y, Dong C, Zhou BP. Epigenetic regulation of EMT: the Snail story. Curr Pharm Des. 2014;20(11):1698–705. PubMed PMID: 23888971; PubMed Central PMCID: PMCPMC4005722. Peinado H, Olmeda D, Cano A. Snail, Zeb and bHLH factors in tumour progression: an alliance against the epithelial phenotype? Nat. Rev. Cancer 2007 Jun;7(6):415–28. doi: https://doi.org/10.1038/nrc2131. PubMed PMID: 17508028. Batlle E, Sancho E, Franci C, et al. The transcription factor snail is a repressor of E-cadherin gene expression in epithelial tumour cells. Nat. Cell Biol. 2000 Feb;2(2):84–9. doi: https://doi.org/10.1038/35000034. PubMed PMID: 10655587. Kouzarides T. Chromatin modifications and their function. Cell. 2007 Feb 23;128(4):693–705. doi: S0092–8674(07)00184–5 [pii] https://doi.org/10.1016/j.cell.2007.02.005. PubMed PMID: 17320507; eng. Zhang T, Cooper S, Brockdorff N. The interplay of histone modifications - writers that read. EMBO Rep. 2015 Nov;16(11):1467–81. doi: 10.15252/embr.201540945. PubMed PMID: 26474904; PubMed Central PMCID: PMCPMC4641500. Vallianatos CN, Iwase S. Disrupted intricacy of histone H3K4 methylation in neurodevelopmental disorders. Epigenomics. 2015;7(3):503–19. doi: https://doi.org/10.2217/epi.15.1. PubMed PMID: 26077434; PubMed Central PMCID: PMC4501478. eng. Wynder C, Stalker L, Doughty ML. Role of H3K4 demethylases in complex neurodevelopmental diseases. Epigenomics. 2010 Jun;2(3):407–18. doi: https://doi.org/10.2217/epi.10.12. PubMed PMID: 22121901; eng. Hojfeldt JW, Agger K, Helin K. Histone lysine demethylases as targets for anticancer therapy. Nat. Rev. Drug Discov. 2013 Dec;12(12):917–30. doi: https://doi.org/10.1038/nrd4154. PubMed PMID: 24232376. Li D, Sun H, Sun WJ, et al. Role of RbBP5 and H3K4me3 in the vicinity of Snail transcription start site during epithelial-mesenchymal transition in prostate cancer cell. Oncotarget. 2016 Oct 4;7(40):65553–65567. doi: 10.18632/oncotarget.11549 11549 [pii]. PubMed PMID: 27566588; PubMed Central PMCID: PMC5323174. eng. Chen X, Liu J, Chen SY. Sulforaphane protects against ethanol-induced oxidative stress and apoptosis in neural crest cells by the induction of Nrf2-mediated antioxidant response. Br J Pharmacol. 2013 May;169(2):437–48. doi: https://doi.org/10.1111/bph.12133. PubMed PMID: 23425096; PubMed Central PMCID: PMCPMC3651668. Ali Khan M, Kedhari Sundaram M, Hamza A, et al. Sulforaphane reverses the expression of various tumor suppressor genes by targeting DNMT3B and HDAC1 in human cervical cancer cells. Evid Based Complement Alternat Med. 2015;2015:412149. doi: https://doi.org/10.1155/2015/412149. PubMed PMID: 26161119; PubMed Central PMCID: PMCPMC4487331. Fan H, Zhang R, Tesfaye D, et al. Sulforaphane causes a major epigenetic repression of myostatin in porcine satellite cells. Epigenetics. 2012 Dec 1;7(12):1379–90. doi: https://doi.org/10.4161/epi.22609. PubMed PMID: 23092945; PubMed Central PMCID: PMCPMC3528693. Su X, Jiang X, Meng L, et al. Anticancer activity of sulforaphane: the epigenetic mechanisms and the Nrf2 signaling pathway. Oxid Med Cell Longev. 2018;2018:5438179. doi: https://doi.org/10.1155/2018/5438179. PubMed PMID: 29977456; PubMed Central PMCID: PMCPMC6011061. Yuan F, Chen X, Liu J, et al. Sulforaphane restores acetyl-histone H3 binding to Bcl-2 promoter and prevents apoptosis in ethanol-exposed neural crest cells and mouse embryos. Exp Neurol. 2018 Feb;300:60–66. doi: https://doi.org/10.1016/j.expneurol.2017.10.020. PubMed PMID: 29069573; PubMed Central PMCID: PMCPMC5745274. Yan D, Dong J, Sulik KK, et al. Induction of the Nrf2-driven antioxidant response by tert-butylhydroquinone prevents ethanol-induced apoptosis in cranial neural crest cells. Biochemical Pharmacology. 2010 Jul 1;80(1):144–149. doi: https://doi.org/10.1016/j.bcp.2010.03.004. PubMed PMID: WOS:000277497600017; (English). Walport LJ, Hopkinson RJ, Schofield CJ. Mechanisms of human histone and nucleic acid demethylases. Curr Opin Chem Biol. 2012 Dec;16(5–6):525–534. doi: https://doi.org/10.1016/j.cbpa.2012.09.015. PubMed PMID: WOS:000313609300009; (English). Serrano-Gomez SJ, Maziveyi M, Alahari SK. Regulation of epithelial-mesenchymal transition through epigenetic and post-translational modifications. Mol Cancer. 2016 Feb 24;15:18. doi: https://doi.org/10.1186/s12943-016-0502-x. PubMed PMID: 26905733; PubMed Central PMCID: PMCPMC4765192. Franco DL, Mainez J, Vega S, et al. Snail1 suppresses TGF-beta-induced apoptosis and is sufficient to trigger EMT in hepatocytes. J. Cell Sci. 2010 Oct 15;123(Pt 20):3467–77. doi: https://doi.org/10.1242/jcs.068692. PubMed PMID: 20930141. Han B, Zhang YY, Xu K, et al. NUDCD1 promotes metastasis through inducing EMT and inhibiting apoptosis in colorectal cancer. Am J Cancer Res. 2018;8(5):810–823. PubMed PMID: 29888104; PubMed Central PMCID: PMCPMC5992514. Sauka-Spengler T, Meulemans D, Jones M, et al. Ancient evolutionary origin of the neural crest gene regulatory network. Dev. Cell 2007 Sep;13(3):405–20. doi: https://doi.org/10.1016/j.devcel.2007.08.005. PubMed PMID: 17765683. Lamouille S, Xu J, Derynck R. Molecular mechanisms of epithelial-mesenchymal transition. Nat Rev Mol Cell Biol. 2014 Mar;15(3):178–96. doi: https://doi.org/10.1038/nrm3758. PubMed PMID: 24556840; PubMed Central PMCID: PMCPMC4240281. Jones PA, Issa JP, Baylin S. Targeting the cancer epigenome for therapy. Nat. Rev. Genet. 2016 Sep 15;17(10):630–41. doi: https://doi.org/10.1038/nrg.2016.93. PubMed PMID: 27629931. Davies PF, Manduchi E, Jimenez JM, et al. Biofluids, cell mechanics and epigenetics: Flow-induced epigenetic mechanisms of endothelial gene expression. J Biomech. 2017 Jan 4;50:3–10. doi: https://doi.org/10.1016/j.jbiomech.2016.11.017. PubMed PMID: WOS:000392789300002; (English). Kushiro K, Nunez NP. Ethanol inhibits B16-BL6 melanoma metastasis and cell phenotypes associated with metastasis. In Vivo. 2012 Jan-Feb;26(1):47–58. PubMed PMID: 22210715. Smith SM, Garic A, Berres ME, et al. Genomic factors that shape craniofacial outcome and neural crest vulnerability in FASD. Front Genet. 2014;5:224. doi: https://doi.org/10.3389/fgene.2014.00224. PubMed PMID: 25147554; PubMed Central PMCID: PMCPMC4124534. Feng J, Cen J, Li J, et al. Histone deacetylase inhibitor valproic acid (VPA) promotes the epithelial mesenchymal transition of colorectal cancer cells via up regulation of Snail. Cell Adh Migr. 2015;9(6):495–501. doi: https://doi.org/10.1080/19336918.2015.1112486. PubMed PMID: 26632346; PubMed Central PMCID: PMCPMC4955961. Kong D, Ahmad A, Bao B, et al. Histone deacetylase inhibitors induce epithelial-to-mesenchymal transition in prostate cancer cells. PLoS One. 2012;7(9):e45045. doi: https://doi.org/10.1371/journal.pone.0045045. PubMed PMID: 23024790; PubMed Central PMCID: PMCPMC3443231. Natsume-Kitatani Y, Mamitsuka H. Classification of promoters based on the combination of core promoter elements exhibits different histone modification patterns. PLoS One. 2016;11(3):e0151917. doi: https://doi.org/10.1371/journal.pone.0151917. PubMed PMID: 27003446; PubMed Central PMCID: PMCPMC4803293. Liang G, Lin JC, Wei V, et al. Distinct localization of histone H3 acetylation and H3-K4 methylation to the transcription start sites in the human genome. Proc Natl Acad Sci U S A. 2004 May 11;101(19):7357–62. doi: https://doi.org/10.1073/pnas.0401866101. PubMed PMID: 15123803; PubMed Central PMCID: PMCPMC409923. Bradbury CA, Khanim FL, Hayden R, et al. Histone deacetylases in acute myeloid leukaemia show a distinctive pattern of expression that changes selectively in response to deacetylase inhibitors. Leukemia. 2005 Oct;19(10):1751–9. doi: https://doi.org/10.1038/sj.leu.2403910. PubMed PMID: 16121216. Lillico R, Sobral MG, Stesco N, et al. HDAC inhibitors induce global changes in histone lysine and arginine methylation and alter expression of lysine demethylases. J. Proteome 2016 Feb 5;133:125–133. doi: https://doi.org/10.1016/j.jprot.2015.12.018. PubMed PMID: 26721445. Marinova Z, Leng Y, Leeds P, et al. Histone deacetylase inhibition alters histone methylation associated with heat shock protein 70 promoter modifications in astrocytes and neurons. Neuropharmacology. 2011 Jun;60(7–8):1109–15. doi: https://doi.org/10.1016/j.neuropharm.2010.09.022. PubMed PMID: 20888352; PubMed Central PMCID: PMCPMC3036778. Abbas A, Hall JA, Patterson WL, 3rd, et al. Sulforaphane modulates telomerase activity via epigenetic regulation in prostate cancer cell lines. Biochem. Cell Biol. 2016 Feb;94(1):71–81. doi: https://doi.org/10.1139/bcb-2015-0038. PubMed PMID: 26458818. Milne TA, Briggs SD, Brock HW, et al. MLL targets SET domain methyltransferase activity to Hox gene promoters. Mol. Cell 2002 Nov;10(5):1107–17. PubMed PMID: 12453418. Nightingale KP, Gendreizig S, White DA, et al. Cross-talk between histone modifications in response to histone deacetylase inhibitors: MLL4 links histone H3 acetylation and histone H3K4 methylation. J. Biol. Chem. 2007 Feb 16;282(7):4408–16. doi: https://doi.org/10.1074/jbc.M606773200. PubMed PMID: 17166833. Lee MG, Wynder C, Bochar DA, et al. Functional interplay between histone demethylase and deacetylase enzymes. Mol Cell Biol. 2006 Sep;26(17):6395–402. doi: https://doi.org/10.1128/MCB.00723-06. PubMed PMID: 16914725; PubMed Central PMCID: PMCPMC1592851. Huang PH, Chen CH, Chou CC, et al. Histone deacetylase inhibitors stimulate histone H3 lysine 4 methylation in part via transcriptional repression of histone H3 lysine 4 demethylases. Mol Pharmacol. 2011 Jan;79(1):197–206. doi: https://doi.org/10.1124/mol.110.067702. PubMed PMID: 20959362; PubMed Central PMCID: PMCPMC3014276. Gottlicher M, Minucci S, Zhu P, et al. Valproic acid defines a novel class of HDAC inhibitors inducing differentiation of transformed cells. EMBO J. 2001 Dec 17;20(24):6969–78. doi: https://doi.org/10.1093/emboj/20.24.6969. PubMed PMID: 11742974; PubMed Central PMCID: PMCPMC125788.