Generic placeholder image

Current Molecular Pharmacology

Editor-in-Chief

ISSN (Print): 1874-4672
ISSN (Online): 1874-4702

Research Article

Sodium Valproate Modulates the Methylation Status of Lysine Residues 4, 9 and 27 in Histone H3 of HeLa Cells

Author(s): Marina Amorim Rocha, Benedicto de Campos Vidal and Maria Luiza Silveira Mello*

Volume 16, Issue 2, 2023

Published on: 31 May, 2022

Article ID: e160322202281 Pages: 14

DOI: 10.2174/1874467215666220316110405

Price: $65

Open Access Journals Promotions 2
Abstract

Background: Valproic acid/sodium valproate (VPA), a well-known anti-epileptic agent, inhibits histone deacetylases, induces histone hyperacetylation, promotes DNA demethylation, and affects the histone methylation status in some cell models. Histone methylation profiles have been described as potential markers for cervical cancer prognosis. However, histone methylation markers that can be studied in a cervical cancer cell line, like HeLa cells, have not been investigated following treatment with VPA.

Methods: In this study, the effect of 0.5 mM and 2.0 mM VPA for 24 h on H3K4me2/me3, H3K9me/me2 and H3K27me/me3 signals as well as on KMT2D, EZH2, and KDM3A gene expression was investigated using confocal microscopy, Western blotting, and RT-PCR. Histone methylation changes were also investigated by Fourier-transform infrared spectroscopy (FTIR).

Results: We found that VPA induces increased levels of H3K4me2/me3 and H3K9me, which are indicative of chromatin activation. Particularly, H3K4me2 markers appeared intensified close to the nuclear periphery, which may suggest their implication in increased transcriptional memory. The abundance of H3K4me2/me3 in the presence of VPA was associated with increased methyltransferase KMT2D gene expression. VPA induced hypomethylation of H3K9me2, which is associated with gene silencing, and concomitant with the demethylase KDM3A, it increased gene expression. Although VPA induces increased H3K27me/me3 levels, it is suggested that the role of the methyltransferase EZH2 in this context could be affected by interactions with this drug.

Conclusion: Histone FTIR spectra were not affected by VPA under present experimental conditions. Whether our epigenetic results are consistent with VPA affecting the aggressive tumorous state of HeLa cells, further investigation is required.

Keywords: Epigenetics, HeLa cells, histone methylation, histone demethylase, EZH2, VPA.

Graphical Abstract
[1]
Perucca, E. Overtreatment in epilepsy: Adverse consequences and mechanisms. Epilepsy Res., 2002, 52(1), 25-33.
[http://dx.doi.org/10.1016/S0920-1211(02)00182-1] [PMID: 12445957]
[2]
Chateauvieux, S.; Morceau, F.; Dicato, M.; Diederich, M. Molecular and therapeutic potential and toxicity of valproic acid. J. Biomed. Biotechnol., 2010, 2010, 479364.
[http://dx.doi.org/10.1155/2010/479364] [PMID: 20798865]
[3]
Göttlicher, M.; Minucci, S.; Zhu, P.; Krämer, O.H.; Schimpf, A.; Giavara, S.; Sleeman, J.P.; Lo Coco, F.; Nervi, C.; Pelicci, P.G.; Heinzel, T. Valproic acid defines a novel class of HDAC inhibitors inducing differentiation of transformed cells. EMBO J., 2001, 20(24), 6969-6978.
[http://dx.doi.org/10.1093/emboj/20.24.6969] [PMID: 11742974]
[4]
Phiel, C.J.; Zhang, F.; Huang, E.Y.; Guenther, M.G.; Lazar, M.A.; Klein, P.S. Histone deacetylase is a direct target of valproic acid, a potent anticonvulsant, mood stabilizer, and teratogen. J. Biol. Chem., 2001, 276(39), 36734-36741.
[http://dx.doi.org/10.1074/jbc.M101287200] [PMID: 11473107]
[5]
Lagace, D.C.; O’Brien, W.T.; Gurvich, N.; Nachtigal, M.W.; Klein, P.S. Valproic acid: How it works. Or not. Clin. Neurosci. Res., 2004, 4(3-4), 215-225.
[http://dx.doi.org/10.1016/j.cnr.2004.09.013]
[6]
Eyal, S.; Yagen, B.; Shimshoni, J.; Bialer, M. Histone deacetylases inhibition and tumor cells cytotoxicity by CNS-active VPA constitutional isomers and derivatives. Biochem. Pharmacol., 2005, 69(10), 1501-1508.
[http://dx.doi.org/10.1016/j.bcp.2005.02.012] [PMID: 15857614]
[7]
Sun, L.; Coy, D.H. Anti-convulsant drug valproic acid in cancers and in combination anti-cancer therapeutics. Mod. Chem. Appl., 2014, 02, 1000118.
[8]
Aztopal, N.; Erkisa, M.; Erturk, E.; Ulukaya, E.; Tokullugil, A.H.; Ari, F. Valproic acid, a histone deacetylase inhibitor, induces apoptosis in breast cancer stem cells. Chem. Biol. Interact., 2018, 280, 51-58.
[http://dx.doi.org/10.1016/j.cbi.2017.12.003] [PMID: 29225137]
[9]
Ibrahim, T.S.; Sheha, T.A.; Abo-Dya, N.E.; AlAwadh, M.A.; Alhakamy, N.A.; Abdel-Samii, Z.K.; Panda, S.S.; Abuo-Rahma, G.E.A.; Mohamed, M.F.A. Design, synthesis and anticancer activity of novel valproic acid conjugates with improved histone deacetylase (HDAC) inhibitory activity. Bioorg. Chem., 2020, 99, 103797.
[http://dx.doi.org/10.1016/j.bioorg.2020.103797] [PMID: 32247939]
[10]
Mcllo, M.L. Sodium valproate-induced chromatin remodeling. Front. Cell Dev. Biol., 2021, 9, 645518.
[http://dx.doi.org/10.3389/fcell.2021.645518] [PMID: 33959607]
[11]
Blaheta, R.A.; Cinatl, J., Jr Anti-tumor mechanisms of valproate: A novel role for an old drug. Med. Res. Rev., 2002, 22(5), 492-511.
[http://dx.doi.org/10.1002/med.10017] [PMID: 12210556]
[12]
Das, C.M.; Aguilera, D.; Vasquez, H.; Prasad, P.; Zhang, M.; Wolff, J.E.; Gopalakrishnan, V. Valproic acid induces p21 and topoisomerase-II (α/β) expression and synergistically enhances etoposide cytotoxicity in human glioblastoma cell lines. J. Neurooncol., 2007, 85(2), 159-170.
[http://dx.doi.org/10.1007/s11060-007-9402-7] [PMID: 17534580]
[13]
Sami, S.; Höti, N.; Xu, H.M.; Shen, Z.; Huang, X. Valproic acid inhibits the growth of cervical cancer both in vitro and in vivo. J. Biochem., 2008, 144(3), 357-362.
[http://dx.doi.org/10.1093/jb/mvn074] [PMID: 18515856]
[14]
Fang, E.; Wang, J.; Hong, M.; Zheng, L.; Tong, Q. Valproic acid suppresses Warburg effect and tumor progression in neuroblastoma. Biochem. Biophys. Res. Commun., 2019, 508(1), 9-16.
[http://dx.doi.org/10.1016/j.bbrc.2018.11.103] [PMID: 30466785]
[15]
Yang, Q.; Tian, Y.; Liu, S.; Zeine, R.; Chlenski, A.; Salwen, H.R.; Henkin, J.; Cohn, S.L. Thrombospondin-1 peptide ABT-510 combined with valproic acid is an effective antiangiogenesis strategy in neuroblastoma. Cancer Res., 2007, 67(4), 1716-1724.
[http://dx.doi.org/10.1158/0008-5472.CAN-06-2595] [PMID: 17308113]
[16]
Duenas-Gonzalez, A.; Candelaria, M.; Perez-Plascencia, C.; Perez-Cardenas, E.; de la Cruz-Hernandez, E.; Herrera, L.A. Valproic acid as epigenetic cancer drug: Preclinical, clinical and transcriptional effects on solid tumors. Cancer Treat. Rev., 2008, 34(3), 206-222.
[http://dx.doi.org/10.1016/j.ctrv.2007.11.003] [PMID: 18226465]
[17]
Batty, N.; Malouf, G.G.; Issa, J.P.J. Histone deacetylase inhibitors as anti-neoplastic agents. Cancer Lett., 2009, 280(2), 192-200.
[http://dx.doi.org/10.1016/j.canlet.2009.03.013] [PMID: 19345475]
[18]
Venkataramani, V.; Rossner, C.; Iffland, L.; Schweyer, S.; Tamboli, I.Y.; Walter, J.; Wirths, O.; Bayer, T.A. Histone deacetylase inhibitor valproic acid inhibits cancer cell proliferation via down-regulation of the alzheimer amyloid precursor protein. J. Biol. Chem., 2010, 285(14), 10678-10689.
[http://dx.doi.org/10.1074/jbc.M109.057836] [PMID: 20145244]
[19]
Heers, H.; Stanislaw, J.; Harrelson, J.; Lee, M.W. Valproic acid as an adjunctive therapeutic agent for the treatment of breast cancer. Eur. J. Pharmacol., 2018, 835, 61-74.
[http://dx.doi.org/10.1016/j.ejphar.2018.07.057] [PMID: 30075223]
[20]
Li, H.; Zhang, Z.; Gao, C.; Wu, S.; Duan, Q.; Wu, H.; Wang, C.; Shen, Q.; Yin, T. Combination chemotherapy of valproic acid (VPA) and gemcitabine regulates STAT3/Bmi1 pathway to differentially potentiate the motility of pancreatic cancer cells. Cell Biosci., 2019, 9(1), 50.
[http://dx.doi.org/10.1186/s13578-019-0312-0] [PMID: 31244991]
[21]
Tran, L.N.; Kichenadasse, G.; Morel, K.L.; Lavranos, T.C.; Klebe, S.; Lower, K.M.; Ormsby, R.J.; Elliot, D.J.; Sykes, P.J. The combination of metformin and valproic acid has a greater anti-tumoral effect on prostate cancer growth in vivo than either drug alone. IN VIVO (Brooklyn), 2019, 33(1), 99-108.
[http://dx.doi.org/10.21873/invivo.11445] [PMID: 30587609]
[22]
Milutinovic, S.; D’Alessio, A.C.; Detich, N.; Szyf, M. Valproate induces widespread epigenetic reprogramming which involves demethylation of specific genes. Carcinogenesis, 2007, 28(3), 560-571.
[http://dx.doi.org/10.1093/carcin/bgl167] [PMID: 17012225]
[23]
Lee, J.H.; Choy, M.L.; Ngo, L.; Foster, S.S.; Marks, P.A. Histone deacetylase inhibitor induces DNA damage, which normal but not transformed cells can repair. Proc. Natl. Acad. Sci. USA, 2010, 107(33), 14639-14644.
[http://dx.doi.org/10.1073/pnas.1008522107] [PMID: 20679231]
[24]
Perisic, T.; Zimmermann, N.; Kirmeier, T.; Asmus, M.; Tuorto, F.; Uhr, M.; Holsboer, F.; Rein, T.; Zschocke, J. Valproate and amitriptyline exert common and divergent influences on global and gene promoter-specific chromatin modifications in rat primary astrocytes. Neuropsychopharmacology, 2010, 35(3), 792-805.
[http://dx.doi.org/10.1038/npp.2009.188] [PMID: 19924110]
[25]
Jiang, J.; Lu, J.; Lu, D.; Liang, Z.; Li, L.; Ouyang, S.; Kong, X.; Jiang, H.; Shen, B.; Luo, C. Investigation of the acetylation mechanism by GCN5 histone acetyltransferase. PLoS One, 2012, 7(5), e36660.
[http://dx.doi.org/10.1371/journal.pone.0036660] [PMID: 22574209]
[26]
Veronezi, G.M.; Felisbino, M.B.; Gatti, M.S.; Mello, M.L.; Vidal, B.C. DNA methylation changes in valproic acid-treated HeLa cells as assessed by image analysis, immunofluorescence and vibrational microspectroscopy. PLoS One, 2017, 12(1), e0170740.
[http://dx.doi.org/10.1371/journal.pone.0170740] [PMID: 28114349]
[27]
Rocha, M.A.; Veronezi, G.M.; Felisbino, M.B.; Gatti, M.S.; Tamashiro, W.; Mello, M.L. Sodium valproate and 5-aza-2'-deoxycytidine differentially modulate DNA demethylation in G1 phase-arrested and proliferative HeLa cells. Sci. Rep., 2019, 9(1), 18236.
[http://dx.doi.org/10.1038/s41598-019-54848-x] [PMID: 31796828]
[28]
Marchion, D.C.; Bicaku, E.; Daud, A.I.; Sullivan, D.M.; Munster, P.N. Valproic acid alters chromatin structure by regulation of chromatin modulation proteins. Cancer Res., 2005, 65(9), 3815-3822.
[http://dx.doi.org/10.1158/0008-5472.CAN-04-2478] [PMID: 15867379]
[29]
Schuermann, D.; Weber, A.R.; Schär, P. Active DNA demethylation by DNA repair: Facts and uncertainties. DNA Repair, 2016, 44, 92-102.
[http://dx.doi.org/10.1016/j.dnarep.2016.05.013] [PMID: 27247237]
[30]
Ito, S.; D’Alessio, A.C.; Taranova, O.V.; Hong, K.; Sowers, L.C.; Zhang, Y. Role of Tet proteins in 5mC to 5hmC conversion, ES-cell self-renewal and inner cell mass specification. Nature, 2010, 466(7310), 1129-1133.
[http://dx.doi.org/10.1038/nature09303] [PMID: 20639862]
[31]
Blaschke, K.; Ebata, K.T.; Karimi, M.M.; Zepeda-Martínez, J.A.; Goyal, P.; Mahapatra, S.; Tam, A.; Laird, D.J.; Hirst, M.; Rao, A.; Lorincz, M.C.; Ramalho-Santos, M. Vitamin C induces Tet-dependent DNA demethylation and a blastocyst-like state in ES cells. Nature, 2013, 500(7461), 222-226.
[http://dx.doi.org/10.1038/nature12362] [PMID: 23812591]
[32]
Pastor, W.A.; Aravind, L.; Rao, A. TETonic shift: biological roles of TET proteins in DNA demethylation and transcription. Nat. Rev. Mol. Cell Biol., 2013, 14(6), 341-356.
[http://dx.doi.org/10.1038/nrm3589] [PMID: 23698584]
[33]
Palsamy, P.; Bidasee, K.R.; Shinohara, T. Valproic acid suppresses Nrf2/Keap1 dependent antioxidant protection through induction of endoplasmic reticulum stress and Keap1 promoter DNA demethylation in human lens epithelial cells. Exp. Eye Res., 2014, 121, 26-34.
[http://dx.doi.org/10.1016/j.exer.2014.01.021] [PMID: 24525405]
[34]
Lanouette, S.; Mongeon, V.; Figeys, D.; Couture, J.F. The functional diversity of protein lysine methylation. Mol. Syst. Biol., 2014, 10(4), 724.
[http://dx.doi.org/10.1002/msb.134974] [PMID: 24714364]
[35]
Greer, E.L.; Shi, Y. Histone methylation: A dynamic mark in health, disease and inheritance. Nat. Rev. Genet., 2012, 13(5), 343-357.
[http://dx.doi.org/10.1038/nrg3173] [PMID: 22473383]
[36]
Heintzman, N.D.; Stuart, R.K.; Hon, G.; Fu, Y.; Ching, C.W.; Hawkins, R.D.; Barrera, L.O.; Van Calcar, S.; Qu, C.; Ching, K.A.; Wang, W.; Weng, Z.; Green, R.D.; Crawford, G.E.; Ren, B. Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome. Nat. Genet., 2007, 39(3), 311-318.
[http://dx.doi.org/10.1038/ng1966] [PMID: 17277777]
[37]
Roh, T.Y.; Wei, G.; Farrell, C.M.; Zhao, K. Genome-wide prediction of conserved and nonconserved enhancers by histone acetylation patterns. Genome Res., 2007, 17(1), 74-81.
[http://dx.doi.org/10.1101/gr.5767907] [PMID: 17135569]
[38]
Völkel, P.; Angrand, P.O. The control of histone lysine methylation in epigenetic regulation. Biochimie, 2007, 89(1), 1-20.
[http://dx.doi.org/10.1016/j.biochi.2006.07.009] [PMID: 16919862]
[39]
Shinsky, S.A.; Monteith, K.E.; Viggiano, S.; Cosgrove, M.S. Biochemical reconstitution and phylogenetic comparison of human SET1 family core complexes involved in histone methylation. J. Biol. Chem., 2015, 290(10), 6361-6375.
[http://dx.doi.org/10.1074/jbc.M114.627646] [PMID: 25561738]
[40]
Bernstein, B.E.; Humphrey, E.L.; Erlich, R.L.; Schneider, R.; Bouman, P.; Liu, J.S.; Kouzarides, T.; Schreiber, S.L. Methylation of histone H3 Lys 4 in coding regions of active genes. Proc. Natl. Acad. Sci., 2002, 99(13), 8695-8700.
[http://dx.doi.org/10.1073/pnas.082249499] [PMID: 12060701]
[41]
Bernstein, B.E.; Kamal, M.; Lindblad-Toh, K.; Bekiranov, S.; Bailey, D.K.; Huebert, D.J.; McMahon, S.; Karlsson, E.K.; Kulbokas, E.J., III; Gingeras, T.R.; Schreiber, S.L.; Lander, E.S. Genomic maps and comparative analysis of histone modifications in human and mouse. Cell, 2005, 120(2), 169-181.
[http://dx.doi.org/10.1016/j.cell.2005.01.001] [PMID: 15680324]
[42]
Santos-Rosa, H.; Schneider, R.; Bannister, A.J.; Sherriff, J.; Bernstein, B.E.; Emre, N.C.T.; Schreiber, S.L.; Mellor, J.; Kouzarides, T. Active genes are tri-methylated at K4 of histone H3. Nature, 2002, 419(6905), 407-411.
[http://dx.doi.org/10.1038/nature01080] [PMID: 12353038]
[43]
Barski, A.; Cuddapah, S.; Cui, K.; Roh, T.Y.; Schones, D.E.; Wang, Z.; Wei, G.; Chepelev, I.; Zhao, K. High-resolution profiling of histone methylations in the human genome. Cell, 2007, 129(4), 823-837.
[http://dx.doi.org/10.1016/j.cell.2007.05.009] [PMID: 17512414]
[44]
Hyun, K.; Jeon, J.; Park, K.; Kim, J. Writing, erasing and reading histone lysine methylations. Exp. Mol. Med., 2017, 49(4), e324.
[http://dx.doi.org/10.1038/emm.2017.11] [PMID: 28450737]
[45]
Pan, M.R.; Hsu, M.C.; Chen, L.T.; Hung, W.C. Orchestration of H3K27 methylation: Mechanisms and therapeutic implication. Cell. Mol. Life Sci., 2018, 75(2), 209-223.
[http://dx.doi.org/10.1007/s00018-017-2596-8] [PMID: 28717873]
[46]
Herz, H.M.; Garruss, A.; Shilatifard, A. SET for life: Biochemical activities and biological functions of SET domain-containing proteins. Trends Biochem. Sci., 2013, 38(12), 621-639.
[http://dx.doi.org/10.1016/j.tibs.2013.09.004] [PMID: 24148750]
[47]
Young, M.D.; Willson, T.A.; Wakefield, M.J.; Trounson, E.; Hilton, D.J.; Blewitt, M.E.; Oshlack, A.; Majewski, I.J. ChIP-seq analysis reveals distinct H3K27me3 profiles that correlate with transcriptional activity. Nucleic Acids Res., 2011, 39(17), 7415-7427.
[http://dx.doi.org/10.1093/nar/gkr416] [PMID: 21652639]
[48]
Nightingale, K.P.; Gendreizig, S.; White, D.A.; Bradbury, C.; Hollfelder, F.; Turner, B.M. Cross-talk between histone modifications in response to histone deacetylase inhibitors: MLL4 links histone H3 acetylation and histone H3K4 methylation. J. Biol. Chem., 2007, 282(7), 4408-4416.
[http://dx.doi.org/10.1074/jbc.M606773200] [PMID: 17166833]
[49]
Tung, E.W.; Winn, L.M. Epigenetic modifications in valproic acid-induced teratogenesis. Toxicol. Appl. Pharmacol., 2010, 248(3), 201-209.
[http://dx.doi.org/10.1016/j.taap.2010.08.001] [PMID: 20705080]
[50]
Marinova, Z.; Leng, Y.; Leeds, P.; Chuang, D.M. Histone deacetylase inhibition alters histone methylation associated with heat shock protein 70 promoter modifications in astrocytes and neurons. Neuropharmacology, 2011, 60(7-8), 1109-1115.
[http://dx.doi.org/10.1016/j.neuropharm.2010.09.022] [PMID: 20888352]
[51]
Boudadi, E.; Stower, H.; Halsall, J.A.; Rutledge, C.E.; Leeb, M.; Wutz, A.; O’Neill, L.P.; Nightingale, K.P.; Turner, B.M. The histone deacetylase inhibitor sodium valproate causes limited transcriptional change in mouse embryonic stem cells but selectively overrides Polycomb-mediated Hoxb silencing. Epigenetics Chromatin, 2013, 6(1), 11.
[http://dx.doi.org/10.1186/1756-8935-6-11] [PMID: 23634885]
[52]
Ganai, S.A.; Kalladi, S.M.; Mahadevan, V. HDAC inhibition through valproic acid modulates the methylation profiles in human embryonic kidney cells. J. Biomol. Struct. Dyn., 2015, 33(6), 1185-1197.
[http://dx.doi.org/10.1080/07391102.2014.938247] [PMID: 25012937]
[53]
McLaughlin-Drubin, M.E.; Crum, C.P.; Münger, K. Human papillomavirus E7 oncoprotein induces KDM6A and KDM6B histone demethylase expression and causes epigenetic reprogramming. Proc. Natl. Acad. Sci., 2011, 108(5), 2130-2135.
[http://dx.doi.org/10.1073/pnas.1009933108] [PMID: 21245294]
[54]
Beyer, S.; Zhu, J.; Mayr, D.; Kuhn, C.; Schulze, S.; Hofmann, S.; Dannecker, C.; Jeschke, U.; Kost, B.P. Histone H3 acetyl K9 and histone H3 tri methyl K4 as prognostic markers for patients with cervical cancer. Int. J. Mol. Sci., 2017, 18(3), 477.
[http://dx.doi.org/10.3390/ijms18030477] [PMID: 28241481]
[55]
Han, B.R.; You, B.R.; Park, W.H. Valproic acid inhibits the growth of HeLa cervical cancer cells via caspase-dependent apoptosis. Oncol. Rep., 2013, 30(6), 2999-3005.
[http://dx.doi.org/10.3892/or.2013.2747] [PMID: 24064712]
[56]
Li, X.M.; Luo, X.G.; He, J.F.; Wang, N.; Zhou, H.; Yang, P.L.; Zhang, T.C. Induction of apoptosis in human cervical carcinoma HeLa cells by active compounds from Hypericum ascyron L. Oncol. Lett., 2018, 15(3), 3944-3950.
[PMID: 29556280]
[57]
Dejligbjerg, M.; Grauslund, M.; Litman, T.; Collins, L.; Qian, X.; Jeffers, M.; Lichenstein, H.; Jensen, P.B.; Sehested, M. Differential effects of class I isoform histone deacetylase depletion and enzymatic inhibition by belinostat or valproic acid in HeLa cells. Mol. Cancer, 2008, 7(1), 70.
[http://dx.doi.org/10.1186/1476-4598-7-70] [PMID: 18789133]
[58]
Felisbino, M.B.; Tamashiro, W.; Mello, M.L. Chromatin remodeling, cell proliferation and cell death in valproic acid-treated HeLa cells. PLoS One, 2011, 6(12), e29144.
[http://dx.doi.org/10.1371/journal.pone.0029144] [PMID: 22206001]
[59]
Sargolzaei, J.; Rabbani-Chadegani, A.; Mollaei, H.; Deezagi, A. Spectroscopic analysis of the interaction of valproic acid with histone H1 in solution and in chromatin structure. Int. J. Biol. Macromol., 2017, 99, 427-432.
[http://dx.doi.org/10.1016/j.ijbiomac.2017.02.098] [PMID: 28263810]
[60]
de Campos Vidal, B.; Mello, M.L. Sodium valproate (VPA) interactions with DNA and histones. Int. J. Biol. Macromol., 2020, 163, 219-231.
[http://dx.doi.org/10.1016/j.ijbiomac.2020.06.265] [PMID: 32619665]
[61]
Rocha, M.A.; Oliveira, C.B.; Mello, M.L. Sodium valproate cytotoxicity effects as assessed by the MTT assay. Reposit. Rese. Data Unicamp, 201535(1), 62-65.
[http://dx.doi.org/10.25824/redu/XPTX4F]
[62]
Shechter, D.; Dormann, H.L.; Allis, C.D.; Hake, S.B. Extraction, purification and analysis of histones. Nat. Protoc., 2007, 2(6), 1445-1457.
[http://dx.doi.org/10.1038/nprot.2007.202] [PMID: 17545981]
[63]
Fabian, H.; Mäntele, W. Infrared spectroscopy of proteins.Handbook of Vibrational Spectroscop0++yWiley: Chichester; , 2002, pp. 3399-3425.
[64]
Vidal, B.C. Fluorescence, aggregation properties and FT-IR microspectroscopy of elastin and collagen fibers. Acta Histochem., 2014, 116(8), 1359-1366.
[http://dx.doi.org/10.1016/j.acthis.2014.08.007] [PMID: 25213809]
[65]
Pavia, D.L.; Lampman, G.M.; Kriz, G.S.; Vyvyan, J.R. Introduction to Spectroscopy, 4th ed; Brooks/Cole: Belmont, 2009.
[66]
Polyanichko, A.M.; Romanov, N.M.; Starkova, T.Y.; Kostyleva, E.I.; Chikhirzhina, E.V. Analysis of the secondary structure of linker histone H1 based on IR absorption spectra. Cell Tissue Biol., 2014, 8(4), 352-358.
[http://dx.doi.org/10.1134/S1990519X14040087]
[67]
Vidal, B.C.; Mello, M.L. Collagen type I amide I band infrared spectroscopy. Micron, 2011, 42(3), 283-289.
[http://dx.doi.org/10.1016/j.micron.2010.09.010] [PMID: 21134761]
[68]
Singh, B.; Gautam, R.; Kumar, S.; Kumar Bn, V.; Nongthomba, U.; Nandi, D.; Mukherjee, G.; Santosh, V.; Somasundaram, K.; Umapathy, S. Application of vibrational microspectroscopy to biology and medicine. Curr. Sci., 2012, 102, 232-244.
[69]
Zelig, U.; Mordechai, S.; Shubinsky, G.; Sahu, R.K.; Huleihel, M.; Leibovitz, E.; Nathan, I.; Kapelushnik, J. Pre-screening and follow-up of childhood acute leukemia using biochemical infrared analysis of peripheral blood mononuclear cells. Biochim. Biophys. Acta, 2011, 1810(9), 827-835.
[http://dx.doi.org/10.1016/j.bbagen.2011.06.010] [PMID: 21722709]
[70]
Petruševski, G.; Naumov, P.; Jovanovski, G.; Bogoeva-Gaceva, G.; Ng, S.W. Solid-state forms of sodium valproate, active component of the anticonvulsant drug epilim. ChemMedChem, 2008, 3(9), 1377-1386.
[http://dx.doi.org/10.1002/cmdc.200800112] [PMID: 18613204]
[71]
Bradbury, C.A.; Khanim, F.L.; Hayden, R.; Bunce, C.M.; White, D.A.; Drayson, M.T.; Craddock, C.; Turner, B.M. Histone deacetylases in acute myeloid leukaemia show a distinctive pattern of expression that changes selectively in response to deacetylase inhibitors. Leukemia, 2005, 19(10), 1751-1759.
[http://dx.doi.org/10.1038/sj.leu.2403910] [PMID: 16121216]
[72]
Huang, Y.; Vasilatos, S.N.; Boric, L.; Shaw, P.G.; Davidson, N.E. Inhibitors of histone demethylation and histone deacetylation cooperate in regulating gene expression and inhibiting growth in human breast cancer cells. Breast Cancer Res. Treat., 2012, 131(3), 777-789.
[http://dx.doi.org/10.1007/s10549-011-1480-8] [PMID: 21452019]
[73]
Huang, Y.; Yuan, L.; Li, T.; Wang, A.; Li, Z.; Pang, D.; Wang, B.; Ouyang, H. Valproic acid improves porcine parthenogenetic embryo development through transient remodeling of histone modifiers. Cell. Physiol. Biochem., 2015, 37(4), 1463-1473.
[http://dx.doi.org/10.1159/000438515] [PMID: 26510156]
[74]
Downing, T.L.; Soto, J.; Morez, C.; Houssin, T.; Fritz, A.; Yuan, F.; Chu, J.; Patel, S.; Schaffer, D.V.; Li, S. Biophysical regulation of epigenetic state and cell reprogramming. Nat. Mater., 2013, 12(12), 1154-1162.
[http://dx.doi.org/10.1038/nmat3777] [PMID: 24141451]
[75]
Lee, R.S.; Pirooznia, M.; Guintivano, J.; Ly, M.; Ewald, E.R.; Tamashiro, K.L.; Gould, T.D.; Moran, T.H.; Potash, J.B. Search for common targets of lithium and valproic acid identifies novel epigenetic effects of lithium on the rat leptin receptor gene. Transl. Psychiatry, 2015, 5(7), e600.
[http://dx.doi.org/10.1038/tp.2015.90] [PMID: 26171981]
[76]
Russ, B.E.; Olshanksy, M.; Smallwood, H.S.; Li, J.; Alice, E.; Prier, J.E.; Stock, A.T.; Croom, H.A.; Cullen, J.G.; Nguyen, M.L.; Rowe, S.; Olson, M.R.; Finkelstein, D.B.; Kelso, A.; Thomas, P.G.; Speed, T.P.; Rao, S.; Turner, S.J. Mapping histone methylation dynamics during virus-specific CD8+ T cell differentiation in response to infection. Immunity, 2014, 41, 853-865.
[http://dx.doi.org/10.1016/j.immuni.2014.11.001] [PMID: 25517617]
[77]
Taddei, A.; Maison, C.; Roche, D.; Almouzni, G. Reversible disruption of pericentric heterochromatin and centromere function by inhibiting deacetylases. Nat. Cell Biol., 2001, 3(2), 114-120.
[http://dx.doi.org/10.1038/35055010] [PMID: 11175742]
[78]
Bártová, E.; Pacherník, J.; Harnicarová, A.; Kovarík, A.; Kovaríková, M.; Hofmanová, J.; Skalníková, M.; Kozubek, M.; Kozubek, S. Nuclear levels and patterns of histone H3 modification and HP1 proteins after inhibition of histone deacetylases. J. Cell Sci., 2005, 118(Pt 21), 5035-5046.
[http://dx.doi.org/10.1242/jcs.02621] [PMID: 16254244]
[79]
Rada-Iglesias, A.; Enroth, S.; Ameur, A.; Koch, C.M.; Clelland, G.K.; Respuela-Alonso, P.; Wilcox, S.; Dovey, O.M.; Ellis, P.D.; Langford, C.F.; Dunham, I.; Komorowski, J.; Wadelius, C. Butyrate mediates decrease of histone acetylation centered on transcription start sites and down-regulation of associated genes. Genome Res., 2007, 17(6), 708-719.
[http://dx.doi.org/10.1101/gr.5540007] [PMID: 17567991]
[80]
Light, W.H.; Brickner, J.H. Nuclear pore proteins regulate chromatin structure and transcriptional memory by a conserved mechanism. Nucleus, 2013, 4(5), 357-360.
[http://dx.doi.org/10.4161/nucl.26209] [PMID: 23962805]
[81]
Fišerová, J.; Efenberková, M.; Sieger, T.; Maninová, M. Uhlířová, J.; Hozák, P. Chromatin organization at the nuclear periphery as revealed by image analysis of structured illumination microscopy data. J. Cell Sci., 2017, 130(12), 2066-2077.
[PMID: 28476938]
[82]
Rice, J.C.; Briggs, S.D.; Ueberheide, B.; Barber, C.M.; Shabanowitz, J.; Hunt, D.F.; Shinkai, Y.; Allis, C.D. Histone methyltransferases direct different degrees of methylation to define distinct chromatin domains. Mol. Cell, 2003, 12(6), 1591-1598.
[http://dx.doi.org/10.1016/S1097-2765(03)00479-9] [PMID: 14690610]
[83]
Wu, R.; Terry, A.V.; Singh, P.B.; Gilbert, D.M. Differential subnuclear localization and replication timing of histone H3 lysine 9 methylation states. Mol. Biol. Cell, 2005, 16(6), 2872-2881.
[http://dx.doi.org/10.1091/mbc.e04-11-0997] [PMID: 15788566]
[84]
Mehedint, M.G.; Niculescu, M.D.; Craciunescu, C.N.; Zeisel, S.H. Choline deficiency alters global histone methylation and epigenetic marking at the Re1 site of the calbindin 1 gene. FASEB J., 2010, 24(1), 184-195.
[http://dx.doi.org/10.1096/fj.09-140145] [PMID: 19752176]
[85]
Felisbino, M.B.; Alves da Costa, T.; Gatti, M.S.V.; Mello, M.L.S. Differential response of human hepatocyte chromatin to HDAC inhibitors as a function of microenvironmental glucose level. J. Cell. Physiol., 2016, 231(10), 2257-2265.
[http://dx.doi.org/10.1002/jcp.25343] [PMID: 26888775]
[86]
Zhang, X.; He, X.; Li, Q.; Kong, X.; Ou, Z.; Zhang, L.; Gong, Z.; Long, D.; Li, J.; Zhang, M.; Ji, W.; Zhang, W.; Xu, L.; Xuan, A. PI3K/AKT/mTOR signaling mediates valproic acid-induced neuronal differentiation of neural stem cells through epigenetic modifications. Stem Cell Reports, 2017, 8(5), 1256-1269.
[http://dx.doi.org/10.1016/j.stemcr.2017.04.006] [PMID: 28494938]
[87]
Margueron, R.; Reinberg, D. The polycomb complex PRC2 and its mark in life. Nature, 2011, 469(7330), 343-349.
[http://dx.doi.org/10.1038/nature09784] [PMID: 21248841]
[88]
Barth, T.K.; Imhof, A. Fast signals and slow marks: The dynamics of histone modifications. Trends Biochem. Sci., 2010, 35(11), 618-626.
[http://dx.doi.org/10.1016/j.tibs.2010.05.006] [PMID: 20685123]
[89]
Cui, K.; Zang, C.; Roh, T.Y.; Schones, D.E.; Childs, R.W.; Peng, W.; Zhao, K. Chromatin signatures in multipotent human hematopoietic stem cells indicate the fate of bivalent genes during differentiation. Cell Stem Cell, 2009, 4(1), 80-93.
[http://dx.doi.org/10.1016/j.stem.2008.11.011] [PMID: 19128795]
[90]
Halsall, J.A.; Turan, N.; Wiersma, M.; Turner, B.M. Cells adapt to the epigenomic disruption caused by histone deacetylase inhibitors through a coordinated, chromatin-mediated transcriptional response. Epigenetics Chromatin, 2015, 8(1), 29.
[http://dx.doi.org/10.1186/s13072-015-0021-9] [PMID: 26380582]
[91]
Scialdone, A.; Hasni, M.S.; Damm, J.K.; Lennartsson, A.; Gullberg, U.; Drott, K. The HDAC inhibitor valproate induces a bivalent status of the CD20 promoter in CLL patients suggesting distinct epigenetic regulation of CD20 expression in CLL in vivo. Oncotarget, 2017, 8(23), 37409-37422.
[http://dx.doi.org/10.18632/oncotarget.16964] [PMID: 28445158]
[92]
Mello, M.L.; Vidal, B.C. Infrared data of sodium valproate (VPA), histones and VPA-histone mixtures; Repost Rese. Data Unicamp, 2021.
[http://dx.doi.org/10.25824/redu/OSK2UP]
[93]
Fang, J.; Zhang, H.; Jin, S. Epigenetics and cervical cancer: From pathogenesis to therapy. Tumour Biol., 2014, 35(6), 5083-5093.
[http://dx.doi.org/10.1007/s13277-014-1737-z] [PMID: 24554414]
[94]
Baumann, C.; Zhang, X.; Zhu, L.; Fan, Y.; De La Fuente, R. Changes in chromatin accessibility landscape and histone H3 core acetylation during valproic acid-induced differentiation of embryonic stem cells. Epigenetics & Chromatin, 2021, 14, 58.
[http://dx.doi.org/10.1186/s13072-021-00432-5]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy