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Mini-Reviews in Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 1389-5575
ISSN (Online): 1875-5607

Review Article

The Role of Epigenetic Mechanisms in Autoimmune, Neurodegenerative, Cardiovascular, and Imprinting Disorders

Author(s): Ram Sharma, Sachin Sharma, Amandeep Thakur, Arshdeep Singh, Jagjeet Singh, Kunal Nepali* and Jing Ping Liou*

Volume 22, Issue 15, 2022

Published on: 19 April, 2022

Page: [1977 - 2011] Pages: 35

DOI: 10.2174/1389557522666220217103441

Price: $65

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Abstract

Epigenetic mutations like aberrant DNA methylation, histone modifications, or RNA silencing are found in a number of human diseases. This review article discusses the epigenetic mechanisms involved in neurodegenerative disorders, cardiovascular disorders, auto-immune disorders and genomic imprinting disorders. In addition, emerging epigenetic therapeutic strategies for the treatment of such disorders are presented. Medicinal chemistry campaigns highlighting the efforts of the chemists invested towards the rational design of small molecule inhibitors have also been included. Pleasingly, several classes of epigenetic inhibitors, DNMT, HDAC, BET, HAT, and HMT inhibitors, along with RNA based therapies, have exhibited the potential to emerge as therapeutics in the longer run. It is quite hopeful that epigenetic modulator-based therapies will advance to clinical stage investigations by leaps and bounds.

Keywords: Epigenetics, neurodegenerative disorders, cardiovascular disorders, auto-immune disorder, genomic imprinting disorders, DNA methylation.

Graphical Abstract
[1]
Feinberg, A.P.; Vogelstein, B. Hypomethylation distinguishes genes of some human cancers from their normal counterparts. Nature, 1983, 301(5895), 89-92.
[http://dx.doi.org/10.1038/301089a0] [PMID: 6185846]
[2]
Nakao, M. Epigenetics: Interaction of DNA methylation and chromatin. Gene, 2001, 278(1-2), 25-31.
[http://dx.doi.org/10.1016/S0378-1119(01)00721-1] [PMID: 11707319]
[3]
Zoghbi, H.Y.; Beaudet, A.L. Epigenetics and human disease. Cold Spring Harb. Perspect. Biol., 2016, 8(2), a019497.
[http://dx.doi.org/10.1101/cshperspect.a019497] [PMID: 26834142]
[4]
Biswas, S.; Rao, C.M. Epigenetic tools (The Writers, The Readers and The Erasers) and their implications in cancer therapy. Eur. J. Pharmacol., 2018, 837, 8-24.
[http://dx.doi.org/10.1016/j.ejphar.2018.08.021] [PMID: 30125562]
[5]
Baylin, S.B.; Jones, P.A. A decade of exploring the cancer epigenome - biological and translational implications. Nat. Rev. Cancer, 2011, 11(10), 726-734.
[http://dx.doi.org/10.1038/nrc3130] [PMID: 21941284]
[6]
Dawson, M.A.; Kouzarides, T.; Huntly, B.J. Targeting epigenetic readers in cancer. N. Engl. J. Med., 2012, 367(7), 647-657.
[http://dx.doi.org/10.1056/NEJMra1112635] [PMID: 22894577]
[7]
Xu, Y.; Zhang, S.; Lin, S.; Guo, Y.; Deng, W.; Zhang, Y.; Xue, Y. WERAM: A database of writers, erasers and readers of histone acetylation and methylation in eukaryotes. Nucleic Acids Res., 2016, gkw1011.
[PMID: 27789692]
[8]
Treviño, L.S.; Wang, Q.; Walker, C.L. Phosphorylation of epigenetic “readers, writers and erasers”: Implications for developmental reprogramming and the epigenetic basis for health and disease. Prog. Biophys. Mol. Biol., 2015, 118(1-2), 8-13.
[http://dx.doi.org/10.1016/j.pbiomolbio.2015.02.013] [PMID: 25841987]
[9]
Smeenk, G.; Mailand, N. Writers, readers, and erasers of histone ubiquitylation in DNA double-strand break repair. Front. Genet., 2016, 7, 122.
[http://dx.doi.org/10.3389/fgene.2016.00122] [PMID: 27446204]
[10]
Jacob, R.; Zander, S.; Gutschner, T. The dark side of the epitranscriptome: Chemical modifications in long non-coding RNAs. Int. J. Mol. Sci., 2017, 18(11), 2387.
[http://dx.doi.org/10.3390/ijms18112387] [PMID: 29125541]
[11]
Swank, M.W.; Sweatt, J.D. Increased histone acetyltransferase and lysine acetyltransferase activity and biphasic activation of the ERK/RSK cascade in insular cortex during novel taste learning. J. Neurosci., 2001, 21(10), 3383-3391.
[http://dx.doi.org/10.1523/JNEUROSCI.21-10-03383.2001] [PMID: 11331368]
[12]
Miller, C.A.; Sweatt, J.D. Covalent modification of DNA regulates memory formation. Neuron, 2007, 53(6), 857-869.
[http://dx.doi.org/10.1016/j.neuron.2007.02.022] [PMID: 17359920]
[13]
Kemme, C.A.; Marquez, R.; Luu, R.H.; Iwahara, J. Potential role of DNA methylation as a facilitator of target search processes for transcription factors through interplay with methyl-CpG-binding proteins. Nucleic Acids Res., 2017, 45(13), 7751-7759.
[http://dx.doi.org/10.1093/nar/gkx387] [PMID: 28486614]
[14]
Zhong, J.; Agha, G.; Baccarelli, A.A. The role of DNA methylation in cardiovascular risk and disease: Methodological aspects, study design, and data analysis for epidemiological studies. Circ. Res., 2016, 118(1), 119-131.
[http://dx.doi.org/10.1161/CIRCRESAHA.115.305206] [PMID: 26837743]
[15]
Kamnasaran, D.; Cox, D.W. Current status of human chromosome 14. J. Med. Genet., 2002, 39(2), 81-90.
[http://dx.doi.org/10.1136/jmg.39.2.81] [PMID: 11836355]
[16]
Nile, C.J.; Read, R.C.; Akil, M.; Duff, G.W.; Wilson, A.G. Methylation status of a single CpG site in the IL6 promoter is related to IL6 messenger RNA levels and rheumatoid arthritis. Arthritis Rheum., 2008, 58(9), 2686-2693.
[http://dx.doi.org/10.1002/art.23758] [PMID: 18759290]
[17]
Broide, R.S.; Redwine, J.M.; Aftahi, N.; Young, W.; Bloom, F.E.; Winrow, C.J. Distribution of histone deacetylases 1-11 in the rat brain. J. Mol. Neurosci., 2007, 31(1), 47-58.
[http://dx.doi.org/10.1007/BF02686117] [PMID: 17416969]
[18]
Guan, J-S.; Haggarty, S.J.; Giacometti, E.; Dannenberg, J-H.; Joseph, N.; Gao, J.; Nieland, T.J.; Zhou, Y.; Wang, X.; Mazitschek, R.; Bradner, J.E.; DePinho, R.A.; Jaenisch, R.; Tsai, L.H. HDAC2 negatively regulates memory formation and synaptic plasticity. Nature, 2009, 459(7243), 55-60.
[http://dx.doi.org/10.1038/nature07925] [PMID: 19424149]
[19]
Papait, R.; Cattaneo, P.; Kunderfranco, P.; Greco, C.; Carullo, P.; Guffanti, A.; Viganò, V.; Stirparo, G.G.; Latronico, M.V.; Hasenfuss, G.; Chen, J.; Condorelli, G. Genome-wide analysis of histone marks identifying an epigenetic signature of promoters and enhancers underlying cardiac hypertrophy. Proc. Natl. Acad. Sci. USA, 2013, 110(50), 20164-20169.
[http://dx.doi.org/10.1073/pnas.1315155110] [PMID: 24284169]
[20]
Montgomery, R.L.; Davis, C.A.; Potthoff, M.J.; Haberland, M.; Fielitz, J.; Qi, X.; Hill, J.A.; Richardson, J.A.; Olson, E.N. Histone deacetylases 1 and 2 redundantly regulate cardiac morphogenesis, growth, and contractility. Genes Dev., 2007, 21(14), 1790-1802.
[http://dx.doi.org/10.1101/gad.1563807] [PMID: 17639084]
[21]
Montgomery, R.L.; Potthoff, M.J.; Haberland, M.; Qi, X.; Matsuzaki, S.; Humphries, K.M.; Richardson, J.A.; Bassel-Duby, R.; Olson, E.N. Maintenance of cardiac energy metabolism by histone deacetylase 3 in mice. J. Clin. Invest., 2008, 118(11), 3588-3597.
[http://dx.doi.org/10.1172/JCI35847] [PMID: 18830415]
[22]
Pan, G.; Tian, S.; Nie, J.; Yang, C.; Ruotti, V.; Wei, H.; Jonsdottir, G.A.; Stewart, R.; Thomson, J.A. Whole-genome analysis of histone H3 lysine 4 and lysine 27 methylation in human embryonic stem cells. Cell Stem Cell, 2007, 1(3), 299-312.
[http://dx.doi.org/10.1016/j.stem.2007.08.003] [PMID: 18371364]
[23]
Zhang, Z.; Zhang, R. Epigenetics in autoimmune diseases: Pathogenesis and prospects for therapy. Autoimmun. Rev., 2015, 14(10), 854-863.
[http://dx.doi.org/10.1016/j.autrev.2015.05.008] [PMID: 26026695]
[24]
Packer, A.N.; Xing, Y.; Harper, S.Q.; Jones, L.; Davidson, B.L. The bifunctional microRNA miR-9/miR-9* regulates REST and CoREST and is downregulated in Huntington’s disease. J. Neurosci., 2008, 28(53), 14341-14346.
[http://dx.doi.org/10.1523/JNEUROSCI.2390-08.2008] [PMID: 19118166]
[25]
Lusardi, T.A.; Farr, C.D.; Faulkner, C.L.; Pignataro, G.; Yang, T.; Lan, J.; Simon, R.P.; Saugstad, J.A. Ischemic preconditioning regulates expression of microRNAs and a predicted target, MeCP2, in mouse cortex. J. Cereb. Blood Flow Metab., 2010, 30(4), 744-756.
[http://dx.doi.org/10.1038/jcbfm.2009.253] [PMID: 20010955]
[26]
Hwang, J-Y.; Kaneko, N.; Noh, K-M.; Pontarelli, F.; Zukin, R.S. The gene silencing transcription factor REST represses miR-132 expression in hippocampal neurons destined to die. J. Mol. Biol., 2014, 426(20), 3454-3466.
[http://dx.doi.org/10.1016/j.jmb.2014.07.032] [PMID: 25108103]
[27]
Lai, Y.; He, S.; Ma, L.; Lin, H.; Ren, B.; Ma, J.; Zhu, X.; Zhuang, S. HOTAIR functions as a competing endogenous RNA to regulate PTEN expression by inhibiting miR-19 in cardiac hypertrophy. Mol. Cell. Biochem., 2017, 432(1-2), 179-187.
[http://dx.doi.org/10.1007/s11010-017-3008-y] [PMID: 28316060]
[28]
Wang, J-X.; Zhang, X-J.; Li, Q.; Wang, K.; Wang, Y.; Jiao, J-Q.; Feng, C.; Teng, S.; Zhou, L-Y.; Gong, Y.; Zhou, Z.X.; Liu, J.; Wang, J.L.; Li, P.F. MicroRNA-103/107 regulate programmed necrosis and myocardial ischemia/reperfusion injury through targeting FADD. Circ. Res., 2015, 117(4), 352-363.
[http://dx.doi.org/10.1161/CIRCRESAHA.117.305781] [PMID: 26038570]
[29]
Yu, F.; Chen, B.; Dong, P.; Zheng, J. HOTAIR epigenetically modulates PTEN expression via MicroRNA-29b: A novel mechanism in regulation of liver fibrosis. Mol. Ther., 2017, 25(1), 205-217.
[http://dx.doi.org/10.1016/j.ymthe.2016.10.015] [PMID: 28129115]
[30]
Wawrzik, M.; Spiess, A-N.; Herrmann, R.; Buiting, K.; Horsthemke, B. Expression of SNURF-SNRPN upstream transcripts and epigenetic regulatory genes during human spermatogenesis. Eur. J. Hum. Genet., 2009, 17(11), 1463-1470.
[http://dx.doi.org/10.1038/ejhg.2009.83] [PMID: 19471314]
[31]
Xu, F.; Jin, L.; Jin, Y.; Nie, Z.; Zheng, H. Long noncoding RNAs in autoimmune diseases. J. Biomed. Mater. Res. A, 2019, 107(2), 468-475.
[http://dx.doi.org/10.1002/jbm.a.36562] [PMID: 30478988]
[32]
Hwang, J-Y.; Aromolaran, K.A.; Zukin, R.S. The emerging field of epigenetics in neurodegeneration and neuroprotection. Nat. Rev. Neurosci., 2017, 18(6), 347-361.
[http://dx.doi.org/10.1038/nrn.2017.46] [PMID: 28515491]
[33]
Day, J.J.; Kennedy, A.J.; Sweatt, J.D. DNA methylation and its implications and accessibility for neuropsychiatric therapeutics. Annu. Rev. Pharmacol. Toxicol., 2015, 55, 591-611.
[http://dx.doi.org/10.1146/annurev-pharmtox-010814-124527] [PMID: 25340930]
[34]
Gräff, J.; Kim, D.; Dobbin, M.M.; Tsai, L-H. Epigenetic regulation of gene expression in physiological and pathological brain processes. Physiol. Rev., 2011, 91(2), 603-649.
[http://dx.doi.org/10.1152/physrev.00012.2010] [PMID: 21527733]
[35]
Feng, J.; Zhou, Y.; Campbell, S.L.; Le, T.; Li, E.; Sweatt, J.D.; Silva, A.J.; Fan, G. Dnmt1 and Dnmt3a maintain DNA methylation and regulate synaptic function in adult forebrain neurons. Nat. Neurosci., 2010, 13(4), 423-430.
[http://dx.doi.org/10.1038/nn.2514] [PMID: 20228804]
[36]
Levenson, J.M.; O’Riordan, K.J.; Brown, K.D.; Trinh, M.A.; Molfese, D.L.; Sweatt, J.D. Regulation of histone acetylation during memory formation in the hippocampus. J. Biol. Chem., 2004, 279(39), 40545-40559.
[http://dx.doi.org/10.1074/jbc.M402229200] [PMID: 15273246]
[37]
Calderone, A.; Jover, T.; Noh, K.M.; Tanaka, H.; Yokota, H.; Lin, Y.; Grooms, S.Y.; Regis, R.; Bennett, M.V.; Zukin, R.S. Ischemic insults derepress the gene silencer REST in neurons destined to die. J. Neurosci., 2003, 23(6), 2112-2121.
[http://dx.doi.org/10.1523/JNEUROSCI.23-06-02112.2003] [PMID: 12657670]
[38]
Noh, K-M.; Hwang, J-Y.; Follenzi, A.; Athanasiadou, R.; Miyawaki, T.; Greally, J.M.; Bennett, M.V.; Zukin, R.S. Repressor element-1 silencing transcription factor (REST)-dependent epigenetic remodeling is critical to ischemia-induced neuronal death. Proc. Natl. Acad. Sci. USA, 2012, 109(16), E962-E971.
[http://dx.doi.org/10.1073/pnas.1121568109] [PMID: 22371606]
[39]
Schratt, G. MicroRNAs at the synapse. Nat. Rev. Neurosci., 2009, 10(12), 842-849.
[http://dx.doi.org/10.1038/nrn2763] [PMID: 19888283]
[40]
Aksoy-Aksel, A.; Zampa, F.; Schratt, G. MicroRNAs and synaptic plasticity-a mutual relationship. Philos. Trans. R. Soc. Lond. B Biol. Sci., 2014, 369(1652), 20130515.
[http://dx.doi.org/10.1098/rstb.2013.0515] [PMID: 25135976]
[41]
Woldemichael, B.T.; Mansuy, I.M. Micro-RNAs in cognition and cognitive disorders: Potential for novel biomarkers and therapeutics. Biochem. Pharmacol., 2016, 104, 1-7.
[http://dx.doi.org/10.1016/j.bcp.2015.11.021] [PMID: 26626188]
[42]
Liu, X.; Jiao, B.; Shen, L. The epigenetics of Alzheimer’s disease: Factors and therapeutic implications. Front. Genet., 2018, 9, 579.
[http://dx.doi.org/10.3389/fgene.2018.00579] [PMID: 30555513]
[43]
Ding, H.; Dolan, P.J.; Johnson, G.V. Histone deacetylase 6 interacts with the microtubule-associated protein tau. J. Neurochem., 2008, 106(5), 2119-2130.
[http://dx.doi.org/10.1111/j.1471-4159.2008.05564.x] [PMID: 18636984]
[44]
Gray, S.G.; Ekström, T.J. The human histone deacetylase family. Exp. Cell Res., 2001, 262(2), 75-83.
[http://dx.doi.org/10.1006/excr.2000.5080] [PMID: 11139331]
[45]
Johnson, A.A.; Sarthi, J.; Pirooznia, S.K.; Reube, W.; Elefant, F. Increasing Tip60 HAT levels rescues axonal transport defects and associated behavioral phenotypes in a Drosophila Alzheimer’s disease model. J. Neurosci., 2013, 33(17), 7535-7547.
[http://dx.doi.org/10.1523/JNEUROSCI.3739-12.2013] [PMID: 23616558]
[46]
Richardson, J.C.; Cogswell, J.P.; Ward, J.; Taylor, I.A.; Waters, M.; Shi, Y.; Cannon, B.; Kelnar, K.; Kemppainen, J.; Brown, D. O3‐02–07: Identification of miRNA changes in Alzheimer’s disease brain and CSF yields putative biomarkers and insights into disease pathways. Alzheimers Dement., 2008, 4, T162-T162.
[http://dx.doi.org/10.1016/j.jalz.2008.05.420]
[47]
Lee, J.; Hwang, Y.J.; Kim, K.Y.; Kowall, N.W.; Ryu, H. Epigenetic mechanisms of neurodegeneration in Huntington’s disease. Neurotherapeutics, 2013, 10(4), 664-676.
[http://dx.doi.org/10.1007/s13311-013-0206-5] [PMID: 24006238]
[48]
Ng, C.W.; Yildirim, F.; Yap, Y.S.; Dalin, S.; Matthews, B.J.; Velez, P.J.; Labadorf, A.; Housman, D.E.; Fraenkel, E. Extensive changes in DNA methylation are associated with expression of mutant huntingtin. Proc. Natl. Acad. Sci. USA, 2013, 110(6), 2354-2359.
[http://dx.doi.org/10.1073/pnas.1221292110] [PMID: 23341638]
[49]
Thomas, B.; Matson, S.; Chopra, V.; Sun, L.; Sharma, S.; Hersch, S.; Rosas, H.D.; Scherzer, C.; Ferrante, R.; Matson, W. A novel method for detecting 7-methyl guanine reveals aberrant methylation levels in Huntington disease. Anal. Biochem., 2013, 436(2), 112-120.
[http://dx.doi.org/10.1016/j.ab.2013.01.035] [PMID: 23416183]
[50]
Wood, H. Neurodegenerative disease: Altered DNA methylation and RNA splicing could be key mechanisms in Huntington disease. Nat. Rev. Neurol., 2013, 9(3), 119-119.
[http://dx.doi.org/10.1038/nrneurol.2013.23] [PMID: 23399643]
[51]
Suzuki, M.M.; Bird, A. DNA methylation landscapes: Provocative insights from epigenomics. Nat. Rev. Genet., 2008, 9(6), 465-476.
[http://dx.doi.org/10.1038/nrg2341] [PMID: 18463664]
[52]
Bannister, A.J.; Kouzarides, T. The CBP co-activator is a histone acetyltransferase. Nature, 1996, 384(6610), 641-643.
[http://dx.doi.org/10.1038/384641a0] [PMID: 8967953]
[53]
Ryu, H.; Lee, J.; Hagerty, S.W.; Soh, B.Y.; McAlpin, S.E.; Cormier, K.A.; Smith, K.M.; Ferrante, R.J. ESET/SETDB1 gene expression and histone H3 (K9) trimethylation in Huntington’s disease. Proc. Natl. Acad. Sci. USA, 2006, 103(50), 19176-19181.
[http://dx.doi.org/10.1073/pnas.0606373103] [PMID: 17142323]
[54]
Savas, J.N.; Makusky, A.; Ottosen, S.; Baillat, D.; Then, F.; Krainc, D.; Shiekhattar, R.; Markey, S.P.; Tanese, N. Huntington’s disease protein contributes to RNA-mediated gene silencing through association with Argonaute and P bodies. Proc. Natl. Acad. Sci. USA, 2008, 105(31), 10820-10825.
[http://dx.doi.org/10.1073/pnas.0800658105] [PMID: 18669659]
[55]
Chestnut, B.A.; Chang, Q.; Price, A.; Lesuisse, C.; Wong, M.; Martin, L.J. Epigenetic regulation of motor neuron cell death through DNA methylation. J. Neurosci., 2011, 31(46), 16619-16636.
[http://dx.doi.org/10.1523/JNEUROSCI.1639-11.2011] [PMID: 22090490]
[56]
Tétreault, N.; De Guire, V. miRNAs: their discovery, biogenesis and mechanism of action. Clin. Biochem., 2013, 46(10-11), 842-845.
[http://dx.doi.org/10.1016/j.clinbiochem.2013.02.009] [PMID: 23454500]
[57]
Tolia, N.H.; Joshua-Tor, L. Slicer and the argonautes. Nat. Chem. Biol., 2007, 3(1), 36-43.
[http://dx.doi.org/10.1038/nchembio848] [PMID: 17173028]
[58]
Gal, J.; Chen, J.; Barnett, K.R.; Yang, L.; Brumley, E.; Zhu, H. HDAC6 regulates mutant SOD1 aggregation through two SMIR motifs and tubulin acetylation. J. Biol. Chem., 2013, 288(21), 15035-15045.
[http://dx.doi.org/10.1074/jbc.M112.431957] [PMID: 23580651]
[59]
Du, Z-W.; Chen, H.; Liu, H.; Lu, J.; Qian, K.; Huang, C-L.; Zhong, X.; Fan, F.; Zhang, S-C. Generation and expansion of highly pure motor neuron progenitors from human pluripotent stem cells. Nat. Commun., 2015, 6(1), 6626.
[http://dx.doi.org/10.1038/ncomms7626] [PMID: 25806427]
[60]
Veldic, M.; Caruncho, H.J.; Liu, W.S.; Davis, J.; Satta, R.; Grayson, D.R.; Guidotti, A.; Costa, E. DNA-methyltransferase 1 mRNA is selectively overexpressed in telencephalic GABAergic interneurons of schizophrenia brains. Proc. Natl. Acad. Sci. USA, 2004, 101(1), 348-353.
[http://dx.doi.org/10.1073/pnas.2637013100] [PMID: 14684836]
[61]
Klein, C.J.; Botuyan, M-V.; Wu, Y.; Ward, C.J.; Nicholson, G.A.; Hammans, S.; Hojo, K.; Yamanishi, H.; Karpf, A.R.; Wallace, D.C.; Simon, M.; Lander, C.; Boardman, L.A.; Cunningham, J.M.; Smith, G.E.; Litchy, W.J.; Boes, B.; Atkinson, E.J.; Middha, S.; Dyck, B. P.J.; Parisi, J.E.; Mer, G.; Smith, D.I.; Dyck, P.J. Mutations in DNMT1 cause hereditary sensory neuropathy with dementia and hearing loss. Nat. Genet., 2011, 43(6), 595-600.
[http://dx.doi.org/10.1038/ng.830] [PMID: 21532572]
[62]
Xu, G-L.; Bestor, T.H.; Bourc’his, D.; Hsieh, C-L.; Tommerup, N.; Bugge, M.; Hulten, M.; Qu, X.; Russo, J.J.; Viegas-Péquignot, E. Chromosome instability and immunodeficiency syndrome caused by mutations in a DNA methyltransferase gene. Nature, 1999, 402(6758), 187-191.
[http://dx.doi.org/10.1038/46052] [PMID: 10647011]
[63]
Bollati, V.; Galimberti, D.; Pergoli, L.; Dalla Valle, E.; Barretta, F.; Cortini, F.; Scarpini, E.; Bertazzi, P.A.; Baccarelli, A. DNA methylation in repetitive elements and Alzheimer disease. Brain Behav. Immun., 2011, 25(6), 1078-1083.
[http://dx.doi.org/10.1016/j.bbi.2011.01.017] [PMID: 21296655]
[64]
Burdge, G.C.; Lillycrop, K.A.; Phillips, E.S.; Slater-Jefferies, J.L.; Jackson, A.A.; Hanson, M.A. Folic acid supplementation during the juvenile-pubertal period in rats modifies the phenotype and epigenotype induced by prenatal nutrition. J. Nutr., 2009, 139(6), 1054-1060.
[http://dx.doi.org/10.3945/jn.109.104653] [PMID: 19339705]
[65]
Jessberger, S.; Nakashima, K.; Clemenson, G.D., Jr; Mejia, E.; Mathews, E.; Ure, K.; Ogawa, S.; Sinton, C.M.; Gage, F.H.; Hsieh, J. Epigenetic modulation of seizure-induced neurogenesis and cognitive decline. J. Neurosci., 2007, 27(22), 5967-5975.
[http://dx.doi.org/10.1523/JNEUROSCI.0110-07.2007] [PMID: 17537967]
[66]
Takayanagi, Y.; Yoshida, M.; Bielsky, I.F.; Ross, H.E.; Kawamata, M.; Onaka, T.; Yanagisawa, T.; Kimura, T.; Matzuk, M.M.; Young, L.J.; Nishimori, K. Pervasive social deficits, but normal parturition, in oxytocin receptor-deficient mice. Proc. Natl. Acad. Sci. USA, 2005, 102(44), 16096-16101.
[http://dx.doi.org/10.1073/pnas.0505312102] [PMID: 16249339]
[67]
Gregory, S.G.; Connelly, J.J.; Towers, A.J.; Johnson, J.; Biscocho, D.; Markunas, C.A.; Lintas, C.; Abramson, R.K.; Wright, H.H.; Ellis, P.; Langford, C.F.; Worley, G.; Delong, G.R.; Murphy, S.K.; Cuccaro, M.L.; Persico, A.; Pericak-Vance, M.A. Genomic and epigenetic evidence for oxytocin receptor deficiency in autism. BMC Med., 2009, 7(1), 62.
[http://dx.doi.org/10.1186/1741-7015-7-62] [PMID: 19845972]
[68]
Ma, D.K.; Jang, M-H.; Guo, J.U.; Kitabatake, Y.; Chang, M.L.; Pow-Anpongkul, N.; Flavell, R.A.; Lu, B.; Ming, G.L.; Song, H. Neuronal activity-induced Gadd45b promotes epigenetic DNA demethylation and adult neurogenesis. Science, 2009, 323(5917), 1074-1077.
[http://dx.doi.org/10.1126/science.1166859] [PMID: 19119186]
[69]
Fraga, M.F.; Ballestar, E.; Paz, M.F.; Ropero, S.; Setien, F.; Ballestar, M.L.; Heine-Suñer, D.; Cigudosa, J.C.; Urioste, M.; Benitez, J.; Boix-Chornet, M.; Sanchez-Aguilera, A.; Ling, C.; Carlsson, E.; Poulsen, P.; Vaag, A.; Stephan, Z.; Spector, T.D.; Wu, Y.Z.; Plass, C.; Esteller, M. Epigenetic differences arise during the lifetime of monozygotic twins. Proc. Natl. Acad. Sci. USA, 2005, 102(30), 10604-10609.
[http://dx.doi.org/10.1073/pnas.0500398102] [PMID: 16009939]
[70]
Bayer, C.; Pitschelatow, G.; Hannemann, N.; Linde, J.; Reichard, J.; Pensold, D.; Zimmer-Bensch, G. DNA Methyltransferase 1 (DNMT1) acts on neurodegeneration by modulating proteostasis-relevant intracellular processes. Int. J. Mol. Sci., 2020, 21(15), 5420.
[http://dx.doi.org/10.3390/ijms21155420] [PMID: 32751461]
[71]
Sezgin, Z.; Dincer, Y. Alzheimer’s disease and epigenetic diet. Neurochem. Int., 2014, 78, 105-116.
[http://dx.doi.org/10.1016/j.neuint.2014.09.012] [PMID: 25290336]
[72]
(a)Singh, B.N.; Shankar, S.; Srivastava, R.K. Green tea catechin, epigallocatechin-3-gallate (EGCG): mechanisms, perspectives and clinical applications. Biochem. Pharmacol., 2011, 82(12), 1807-1821.
(b)NCT00951834. Sunphenon EGCg (Epigallocatechin-Gallate) in the Early Stage of Alzheimer´s Disease (SUN-AK),. 2009.
[73]
Teijido, O.; Cacabelos, R. Pharmacoepigenomic interventions as novel potential treatments for Alzheimer’s and Parkinson’s diseases. Int. J. Mol. Sci., 2018, 19(10), 3199.
[http://dx.doi.org/10.3390/ijms19103199] [PMID: 30332838]
[74]
Shukla, S.; Tekwani, B.L. Histone deacetylases inhibitors in neurodegenerative diseases, neuroprotection and neuronal differentiation. Front. Pharmacol., 2020, 11, 537.
[http://dx.doi.org/10.3389/fphar.2020.00537] [PMID: 32390854]
[75]
Ricobaraza, A.; Cuadrado-Tejedor, M.; Pérez-Mediavilla, A.; Frechilla, D.; Del Río, J.; García-Osta, A. Phenylbutyrate ameliorates cognitive deficit and reduces tau pathology in an Alzheimer’s disease mouse model. Neuropsychopharmacology, 2009, 34(7), 1721-1732.
[http://dx.doi.org/10.1038/npp.2008.229] [PMID: 19145227]
[76]
(a)Vila, M.; Vukosavic, S.; Jackson-Lewis, V.; Neystat, M.; Jakowec, M.; Przedborski, S. α-synuclein up-regulation in substantia nigra dopaminergic neurons following administration of the parkinsonian toxin MPTP. J. Neurochem., 2000, 74(2), 721-729.
[http://dx.doi.org/10.1046/j.1471-4159.2000.740721.x] [PMID: 10646524]
(b)NCT03533257. Study to assess the safety and biological activity of AMX0035 for the treatment of Alzheimer's Disease (PEGASUS),. , 2018.
(c)NCT02046434. Phenylbutyrate response as a biomarker for Alpha-synuclein clearance from the brain,. 2014.
[77]
Baharvand, Z.; Nabiuni, M.; Tahmaseb, M.; Amini, E.; Pandamooz, S. Investigating the synergic effects of valproic acid and crocin on BDNF and GDNF expression in epidermal neural crest stem cells. Acta Neurobiol. Exp. (Warsz.), 2020, 80(1), 38-46.
[http://dx.doi.org/10.21307/ane-2020-004] [PMID: 32214273]
[78]
Qing, H.; He, G.; Ly, P.T.; Fox, C.J.; Staufenbiel, M.; Cai, F.; Zhang, Z.; Wei, S.; Sun, X.; Chen, C-H.; Zhou, W.; Wang, K.; Song, W. Valproic acid inhibits Abeta production, neuritic plaque formation, and behavioral deficits in Alzheimer’s disease mouse models. J. Exp. Med., 2008, 205(12), 2781-2789.
[http://dx.doi.org/10.1084/jem.20081588] [PMID: 18955571]
[79]
Ganai, S.A.; Ramadoss, M.; Mahadevan, V. Histone Deacetylase (HDAC) Inhibitors - emerging roles in neuronal memory, learning, synaptic plasticity and neural regeneration. Curr. Neuropharmacol., 2016, 14(1), 55-71.
[http://dx.doi.org/10.2174/1570159X13666151021111609] [PMID: 26487502]
[80]
Su, Q.; Li, T.; He, P-F.; Lu, X-C.; Yu, Q.; Gao, Q-C.; Wang, Z-J.; Wu, M-N.; Yang, D.; Qi, J-S. Trichostatin A ameliorates Alzheimer’s disease-related pathology and cognitive deficits by increasing albumin expression and Aβ clearance in APP/PS1 mice. Alzheimers Res. Ther., 2021, 13(1), 7.
[http://dx.doi.org/10.1186/s13195-020-00746-8] [PMID: 33397436]
[81]
Hanson, J.E.; La, H.; Plise, E.; Chen, Y-H.; Ding, X.; Hanania, T.; Sabath, E.V.; Alexandrov, V.; Brunner, D.; Leahy, E.; Steiner, P.; Liu, L.; Scearce-Levie, K.; Zhou, Q. SAHA enhances synaptic function and plasticity in vitro but has limited brain availability in vivo and does not impact cognition. PLoS One, 2013, 8(7), e69964.
[http://dx.doi.org/10.1371/journal.pone.0069964] [PMID: 23922875]
[82]
Zhang, Z-Y.; Schluesener, H.J. Oral administration of histone deacetylase inhibitor MS-275 ameliorates neuroinflammation and cerebral amyloidosis and improves behavior in a mouse model. J. Neuropathol. Exp. Neurol., 2013, 72(3), 178-185.
[http://dx.doi.org/10.1097/NEN.0b013e318283114a] [PMID: 23399896]
[83]
(a)Panza, F.; Lozupone, M.; Seripa, D.; Daniele, A.; Watling, M.; Giannelli, G.; Imbimbo, B.P. Development of disease-modifying drugs for frontotemporal dementia spectrum disorders. Nat. Rev. Neurol., 2020, 16(4), 213-228.
(b)NCT02149160. Study to Assess the Safety, Tolerability, and Pharmacodynamic (PD) Effects of FRM-0334 in Subjects With Prodromal to Moderate Frontotemporal Dementia With Granulin Mutation, 2014.
[84]
Simões-Pires, C.; Zwick, V.; Nurisso, A.; Schenker, E.; Carrupt, P-A.; Cuendet, M. HDAC6 as a target for neurodegenerative diseases: What makes it different from the other HDACs? Mol. Neurodegener., 2013, 8(1), 7.
[http://dx.doi.org/10.1186/1750-1326-8-7] [PMID: 23356410]
[85]
Butler, K.V.; Kalin, J.; Brochier, C.; Vistoli, G.; Langley, B.; Kozikowski, A.P. Rational design and simple chemistry yield a superior, neuroprotective HDAC6 inhibitor, tubastatin A. J. Am. Chem. Soc., 2010, 132(31), 10842-10846.
[http://dx.doi.org/10.1021/ja102758v] [PMID: 20614936]
[86]
Majid, T.; Griffin, D.; Criss, Z.I.I.; Jarpe, M.; Pautler, R.G. Pharmocologic treatment with histone deacetylase 6 inhibitor (ACY-738) recovers Alzheimer’s disease phenotype in amyloid precursor protein/presenilin 1 (APP/PS1) mice. Alzheimers Dement. (N. Y.), 2015, 1(3), 170-181.
[http://dx.doi.org/10.1016/j.trci.2015.08.001] [PMID: 29854936]
[87]
Yalcin, G. Sirtuins and neurodegeneration. J. Neurol. Neuromedicine, 2018, 3(1), 13-20.
[http://dx.doi.org/10.29245/2572.942X/2017/1.1168]
[88]
Green, K.N.; Steffan, J.S.; Martinez-Coria, H.; Sun, X.; Schreiber, S.S.; Thompson, L.M.; LaFerla, F.M. Nicotinamide restores cognition in Alzheimer’s disease transgenic mice via a mechanism involving sirtuin inhibition and selective reduction of Thr231-phosphotau. J. Neurosci., 2008, 28(45), 11500-11510.
[http://dx.doi.org/10.1523/JNEUROSCI.3203-08.2008] [PMID: 18987186]
[89]
NTC03061474. 2008.
[90]
Chen, X.; Wales, P.; Quinti, L.; Zuo, F.; Moniot, S.; Herisson, F.; Rauf, N.A.; Wang, H.; Silverman, R.B.; Ayata, C.; Maxwell, M.M.; Steegborn, C.; Schwarzschild, M.A.; Outeiro, T.F.; Kazantsev, A.G. The sirtuin-2 inhibitor AK7 is neuroprotective in models of Parkinson’s disease but not amyotrophic lateral sclerosis and cerebral ischemia. PLoS One, 2015, 10(1), e0116919.
[http://dx.doi.org/10.1371/journal.pone.0116919] [PMID: 25608039]
[91]
Harrison, C. Rescuing from toxicity. Nat. Rev. Drug Discov., 2007, 6(9), 699.
[http://dx.doi.org/10.1038/nrd2407]
[92]
Jia, Y.; Wang, N.; Liu, X. Resveratrol and amyloid-beta: mechanistic insights. Nutrients, 2017, 9(10), 1122.
[http://dx.doi.org/10.3390/nu9101122] [PMID: 29036903]
[93]
(a)NCT00580931. Safety Study of Nicotinamide to Treat Alzheimer's Disease, 2007.
(b)NCT00678431. Randomized Trial of a Nutritional Supplement in Alzheimer's Disease, 2008.
(c)NCT02502253. BDPP Treatment for Mild Cognitive Impairment (MCI) and Prediabetes or Type 2 Diabetes Mellitus (T2DM) (BDPP) , 2015.
[94]
Selvi, B.R.; Cassel, J-C.; Kundu, T.K.; Boutillier, A-L. Tuning acetylation levels with HAT activators: Therapeutic strategy in neurodegenerative diseases. Biochim. Biophys. Acta, 2010, 1799(10-12), 840-853.
[http://dx.doi.org/10.1016/j.bbagrm.2010.08.012] [PMID: 20833281]
[95]
Ittner, L.M.; Götz, J. Amyloid-β and tau--a toxic pas de deux in Alzheimer’s disease. Nat. Rev. Neurosci., 2011, 12(2), 65-72.
[http://dx.doi.org/10.1038/nrn2967] [PMID: 21193853]
[96]
Sethi, P.; Jyoti, A.; Hussain, E.; Sharma, D. Curcumin attenuates aluminium-induced functional neurotoxicity in rats. Pharmacol. Biochem. Behav., 2009, 93(1), 31-39.
[http://dx.doi.org/10.1016/j.pbb.2009.04.005] [PMID: 19376155]
[97]
(a)NCT00164749. A pilot study of curcumin and Ginkgo for Treating Alzheimer's Disease,. 2005.
(b)NCT00099710. Curcumin in patients with mild to moderate Alzheimer's Disease,. 2004.
(c)NCT01716637. Short term efficacy and safety of perispinal administration of etanercept in mild to moderate Alzheimer's Disease,. 2012.
(d)NCT01811381. Curcumin and Yoga Therapy for Those at Risk for Alzheimer's Disease, 2013.
(e)NCT02114372. Cognitive Health in Ageing Register: Investigational, Observational and Trial Studies in Dementia Research: Prospective Readiness Cohort Study (CHARIOT:PRO), 2014.
[98]
Riederer, P.; Laux, G. MAO-inhibitors in Parkinson’s disease. Exp. Neurobiol., 2011, 20(1), 1-17.
[http://dx.doi.org/10.5607/en.2011.20.1.1] [PMID: 22110357]
[99]
Tsutsumi, T.; Iwao, K.; Hayashi, H.; Kirihara, T.; Kawaji, T.; Inoue, T.; Hino, S.; Nakao, M.; Tanihara, H. Potential neuroprotective effects of an LSD1 inhibitor in retinal ganglion cells via p38 MAPK activity. Invest. Ophthalmol. Vis. Sci., 2016, 57(14), 6461-6473.
[http://dx.doi.org/10.1167/iovs.16-19494] [PMID: 27893888]
[100]
Lemes, L.F.N.; de Andrade Ramos, G.; de Oliveira, A.S.; da Silva, F.M.R.; de Castro Couto, G.; da Silva Boni, M.; Guimarães, M.J.R.; Souza, I.N.O.; Bartolini, M.; Andrisano, V.; do Nascimento Nogueira, P.C.; Silveira, E.R.; Brand, G.D.; Soukup, O.; Korábečný, J.; Romeiro, N.C.; Castro, N.G.; Bolognesi, M.L.; Romeiro, L.A.S. Cardanol-derived AChE inhibitors: Towards the development of dual binding derivatives for Alzheimer’s disease. Eur. J. Med. Chem., 2016, 108, 687-700.
[http://dx.doi.org/10.1016/j.ejmech.2015.12.024] [PMID: 26735910]
[101]
Lee, H-Y.; Fan, S-J.; Huang, F-I.; Chao, H-Y.; Hsu, K-C.; Lin, T.E.; Yeh, T-K.; Lai, M-J.; Li, Y-H.; Huang, H-L.; Yang, C.R.; Liou, J.P. 5-Aroylindoles act as selective histone deacetylase 6 inhibitors ameliorating Alzheimer’s disease phenotypes. J. Med. Chem., 2018, 61(16), 7087-7102.
[http://dx.doi.org/10.1021/acs.jmedchem.8b00151] [PMID: 30028616]
[102]
De Simone, A.; La Pietra, V.; Betari, N.; Petragnani, N.; Conte, M.; Daniele, S.; Pietrobono, D.; Martini, C.; Petralla, S.; Casadei, R.; Davani, L.; Frabetti, F.; Russomanno, P.; Novellino, E.; Montanari, S.; Tumiatti, V.; Ballerini, P.; Sarno, F.; Nebbioso, A.; Altucci, L.; Monti, B.; Andrisano, V.; Milelli, A. Discovery of the first-in-class GSK-3β/HDAC dual inhibitor as disease-modifying agent to combat Alzheimer’s disease. ACS Med. Chem. Lett., 2019, 10(4), 469-474.
[http://dx.doi.org/10.1021/acsmedchemlett.8b00507] [PMID: 30996781]
[103]
He, F.; Ran, Y.; Li, X.; Wang, D.; Zhang, Q.; Lv, J.; Yu, C.; Qu, Y.; Zhang, X.; Xu, A.; Wei, C.; Chou, C.J.; Wu, J. Design, synthesis and biological evaluation of dual-function inhibitors targeting NMDAR and HDAC for Alzheimer’s disease. Bioorg. Chem., 2020, 103, 104109.
[http://dx.doi.org/10.1016/j.bioorg.2020.104109] [PMID: 32768741]
[104]
Soares Romeiro, L.A.; da Costa Nunes, J.L.; de Oliveira Miranda, C.; Simões Heyn Roth Cardoso, G.; de Oliveira, A.S.; Gandini, A.; Kobrlova, T.; Soukup, O.; Rossi, M.; Senger, J.; Jung, M.; Gervasoni, S.; Vistoli, G.; Petralla, S.; Massenzio, F.; Monti, B.; Bolognesi, M.L. Novel sustainable-by-design HDAC inhibitors for the treatment of Alzheimer’s disease. ACS Med. Chem. Lett., 2019, 10(4), 671-676.
[http://dx.doi.org/10.1021/acsmedchemlett.9b00071] [PMID: 30996816]
[105]
Yu, C-W.; Chang, P-T.; Hsin, L-W.; Chern, J-W. Quinazolin-4-one derivatives as selective histone deacetylase-6 inhibitors for the treatment of Alzheimer’s disease. J. Med. Chem., 2013, 56(17), 6775-6791.
[http://dx.doi.org/10.1021/jm400564j] [PMID: 23905680]
[106]
Tseng, H-J.; Lin, M-H.; Shiao, Y-J.; Yang, Y-C.; Chu, J-C.; Chen, C-Y.; Chen, Y-Y.; Lin, T.E.; Su, C-J.; Pan, S-L.; Chen, L.C.; Wang, C.Y.; Hsu, K.C.; Huang, W.J. Synthesis and biological evaluation of acridine-based histone deacetylase inhibitors as multitarget agents against Alzheimer’s disease. Eur. J. Med. Chem., 2020, 192, 112193.
[http://dx.doi.org/10.1016/j.ejmech.2020.112193] [PMID: 32151835]
[107]
Reneerkens, O.A.; Rutten, K.; Akkerman, S.; Blokland, A.; Shaffer, C.L.; Menniti, F.S.; Steinbusch, H.W.; Prickaerts, J. Phosphodiesterase type 5 (PDE5) inhibition improves object recognition memory: Indications for central and peripheral mechanisms. Neurobiol. Learn. Mem., 2012, 97(4), 370-379.
[http://dx.doi.org/10.1016/j.nlm.2012.02.008] [PMID: 22426465]
[108]
Rabal, O.; Sánchez-Arias, J.A.; Cuadrado-Tejedor, M.; de Miguel, I.; Pérez-González, M.; García-Barroso, C.; Ugarte, A.; Estella-Hermoso de Mendoza, A.; Sáez, E.; Espelosin, M.; Ursua, S.; Haizhong, T.; Wei, W.; Musheng, X.; Garcia-Osta, A.; Oyarzabal, J. Discovery of in vivo chemical probes for treating Alzheimer’s disease: Dual phosphodiesterase 5 (PDE5) and class I histone deacetylase selective inhibitors. ACS Chem. Neurosci., 2019, 10(3), 1765-1782.
[http://dx.doi.org/10.1021/acschemneuro.8b00648] [PMID: 30525452]
[109]
Rabal, O.; Sánchez-Arias, J.A.; Cuadrado-Tejedor, M.; de Miguel, I.; Pérez-González, M.; García-Barroso, C.; Ugarte, A.; Estella-Hermoso de Mendoza, A.; Sáez, E.; Espelosin, M.; Ursua, S.; Tan, H.; Wu, W.; Xu, M.; Pineda-Lucena, A.; Garcia-Osta, A.; Oyarzabal, J. Multitarget approach for the treatment of Alzheimer’s disease: Inhibition of Phosphodiesterase 9 (PDE9) and Histone Deacetylases (HDACs) covering diverse selectivity profiles. ACS Chem. Neurosci., 2019, 10(9), 4076-4101.
[http://dx.doi.org/10.1021/acschemneuro.9b00303] [PMID: 31441641]
[110]
Bürli, R.W.; Luckhurst, C.A.; Aziz, O.; Matthews, K.L.; Yates, D.; Lyons, K.A.; Beconi, M.; McAllister, G.; Breccia, P.; Stott, A.J.; Penrose, S.D.; Wall, M.; Lamers, M.; Leonard, P.; Müller, I.; Richardson, C.M.; Jarvis, R.; Stones, L.; Hughes, S.; Wishart, G.; Haughan, A.F.; O’Connell, C.; Mead, T.; McNeil, H.; Vann, J.; Mangette, J.; Maillard, M.; Beaumont, V.; Munoz-Sanjuan, I.; Dominguez, C. Design, synthesis, and biological evaluation of potent and selective class IIa histone deacetylase (HDAC) inhibitors as a potential therapy for Huntington’s disease. J. Med. Chem., 2013, 56(24), 9934-9954.
[http://dx.doi.org/10.1021/jm4011884] [PMID: 24261862]
[111]
Kozikowski, A.P.; Shen, S.; Pardo, M.; Tavares, M.T.; Szarics, D.; Benoy, V.; Zimprich, C.A.; Kutil, Z.; Zhang, G.; Bařinka, C.; Robers, M.B.; Van Den Bosch, L.; Eubanks, J.H.; Jope, R.S. Brain penetrable histone deacetylase 6 inhibitor SW-100 ameliorates memory and learning impairments in a mouse model of fragile X syndrome. ACS Chem. Neurosci., 2019, 10(3), 1679-1695.
[http://dx.doi.org/10.1021/acschemneuro.8b00600] [PMID: 30511829]
[112]
Zhao, W-N.; Ghosh, B.; Tyler, M.; Lalonde, J.; Joseph, N.F.; Kosaric, N.; Fass, D.M.; Tsai, L-H.; Mazitschek, R.; Haggarty, S.J. Class I histone deacetylase inhibition by tianeptinaline modulates neuroplasticity and enhances memory. ACS Chem. Neurosci., 2018, 9(9), 2262-2273.
[http://dx.doi.org/10.1021/acschemneuro.8b00116] [PMID: 29932631]
[113]
Lv, W.; Zhang, G.; Barinka, C.; Eubanks, J.H.; Kozikowski, A.P. Design and synthesis of mercaptoacetamides as potent, selective, and brain permeable histone deacetylase 6 inhibitors. ACS Med. Chem. Lett., 2017, 8(5), 510-515.
[http://dx.doi.org/10.1021/acsmedchemlett.7b00012] [PMID: 28523102]
[114]
Hiranaka, S.; Tega, Y.; Higuchi, K.; Kurosawa, T.; Deguchi, Y.; Arata, M.; Ito, A.; Yoshida, M.; Nagaoka, Y.; Sumiyoshi, T. Design, synthesis, and blood-brain barrier transport study of pyrilamine derivatives as histone deacetylase inhibitors. ACS Med. Chem. Lett., 2018, 9(9), 884-888.
[http://dx.doi.org/10.1021/acsmedchemlett.8b00099] [PMID: 30258535]
[115]
Seo, Y.J.; Kang, Y.; Muench, L.; Reid, A.; Caesar, S.; Jean, L.; Wagner, F.; Holson, E.; Haggarty, S.J.; Weiss, P.; King, P.; Carter, P.; Volkow, N.D.; Fowler, J.S.; Hooker, J.M.; Kim, S.W. Image-guided synthesis reveals potent blood-brain barrier permeable histone deacetylase inhibitors. ACS Chem. Neurosci., 2014, 5(7), 588-596.
[http://dx.doi.org/10.1021/cn500021p] [PMID: 24780082]
[116]
Reddy, R.G.; Surineni, G.; Bhattacharya, D.; Marvadi, S.K.; Sagar, A.; Kalle, A.M.; Kumar, A.; Kantevari, S.; Chakravarty, S. Crafting carbazole-based vorinostat and tubastatin-a-like histone deacetylase (HDAC) inhibitors with potent in vitro and in vivo neuroactive functions. ACS Omega, 2019, 4(17), 17279-17294.
[http://dx.doi.org/10.1021/acsomega.9b01950] [PMID: 31656902]
[117]
Castro, R.; Rivera, I.; Struys, E.A.; Jansen, E.E.; Ravasco, P.; Camilo, M.E.; Blom, H.J.; Jakobs, C.; Tavares de Almeida, I. Increased homocysteine and S-adenosylhomocysteine concentrations and DNA hypomethylation in vascular disease. Clin. Chem., 2003, 49(8), 1292-1296.
[http://dx.doi.org/10.1373/49.8.1292] [PMID: 12881445]
[118]
Stenvinkel, P.; Karimi, M.; Johansson, S.; Axelsson, J.; Suliman, M.; Lindholm, B.; Heimbürger, O.; Barany, P.; Alvestrand, A.; Nordfors, L.; Qureshi, A.R.; Ekström, T.J.; Schalling, M. Impact of inflammation on epigenetic DNA methylation - a novel risk factor for cardiovascular disease? J. Intern. Med., 2007, 261(5), 488-499.
[http://dx.doi.org/10.1111/j.1365-2796.2007.01777.x] [PMID: 17444888]
[119]
Breitling, L.P.; Salzmann, K.; Rothenbacher, D.; Burwinkel, B.; Brenner, H. Smoking, F2RL3 methylation, and prognosis in stable coronary heart disease. Eur. Heart J., 2012, 33(22), 2841-2848.
[http://dx.doi.org/10.1093/eurheartj/ehs091] [PMID: 22511653]
[120]
Breitling, L.P.; Yang, R.; Korn, B.; Burwinkel, B.; Brenner, H. Tobacco-smoking-related differential DNA methylation: 27K discovery and replication. Am. J. Hum. Genet., 2011, 88(4), 450-457.
[http://dx.doi.org/10.1016/j.ajhg.2011.03.003] [PMID: 21457905]
[121]
Buro-Auriemma, L.J.; Salit, J.; Hackett, N.R.; Walters, M.S.; Strulovici-Barel, Y.; Staudt, M.R.; Fuller, J.; Mahmoud, M.; Stevenson, C.S.; Hilton, H.; Ho, M.W.; Crystal, R.G. Cigarette smoking induces small airway epithelial epigenetic changes with corresponding modulation of gene expression. Hum. Mol. Genet., 2013, 22(23), 4726-4738.
[http://dx.doi.org/10.1093/hmg/ddt326] [PMID: 23842454]
[122]
El-Osta, A. Glycemic memory. Curr. Opin. Lipidol., 2012, 23(1), 24-29.
[http://dx.doi.org/10.1097/MOL.0b013e32834f319d] [PMID: 22186662]
[123]
Rivière, G.; Lienhard, D.; Andrieu, T.; Vieau, D.; Frey, B.M.; Frey, F.J. Epigenetic regulation of somatic angiotensin-converting enzyme by DNA methylation and histone acetylation. Epigenetics, 2011, 6(4), 478-489.
[http://dx.doi.org/10.4161/epi.6.4.14961] [PMID: 21364323]
[124]
Smolarek, I.; Wyszko, E.; Barciszewska, A.M.; Nowak, S.; Gawronska, I.; Jablecka, A.; Barciszewska, M.Z. Global DNA methylation changes in blood of patients with essential hypertension. Med. Sci. Monit., 2010, 16(3), CR149-CR155.
[PMID: 20190686]
[125]
Fuke, C.; Shimabukuro, M.; Petronis, A.; Sugimoto, J.; Oda, T.; Miura, K.; Miyazaki, T.; Ogura, C.; Okazaki, Y.; Jinno, Y. Age related changes in 5-methylcytosine content in human peripheral leukocytes and placentas: An HPLC-based study. Ann. Hum. Genet., 2004, 68(Pt 3), 196-204.
[http://dx.doi.org/10.1046/j.1529-8817.2004.00081.x] [PMID: 15180700]
[126]
Kumar, A.; Kumar, S.; Vikram, A.; Hoffman, T.A.; Naqvi, A.; Lewarchik, C.M.; Kim, Y-R.; Irani, K. Histone and DNA methylation– mediated epigenetic downregulation of endothelial Kruppel-like factor 2 by low-density lipoprotein cholesterol. Arterioscler. Thromb. Vasc. Biol., 2013, 33(8), 1936-1942.
[127]
Zhou, J.; Li, Y-S.; Wang, K-C.; Chien, S. Epigenetic mechanism in regulation of endothelial function by disturbed flow: Induction of DNA hypermethylation by DNMT1. Cell. Mol. Bioeng., 2014, 7(2), 218-224.
[http://dx.doi.org/10.1007/s12195-014-0325-z] [PMID: 24883126]
[128]
Jiang, Y-Z.; Jiménez, J.M.; Ou, K.; McCormick, M.E.; Zhang, L-D.; Davies, P.F. Hemodynamic disturbed flow induces differential DNA methylation of endothelial Kruppel-Like Factor 4 promoter in vitro and in vivo . Circ. Res., 2014, 115(1), 32-43.
[http://dx.doi.org/10.1161/CIRCRESAHA.115.303883] [PMID: 24755985]
[129]
Xie, S-A.; Zhang, T.; Wang, J.; Zhao, F.; Zhang, Y-P.; Yao, W-J.; Hur, S.S.; Yeh, Y-T.; Pang, W.; Zheng, L-S.; Fan, Y.B.; Kong, W.; Wang, X.; Chiu, J.J.; Zhou, J. Matrix stiffness determines the phenotype of vascular smooth muscle cell in vitro and in vivo : Role of DNA methyltransferase 1. Biomaterials, 2018, 155, 203-216.
[http://dx.doi.org/10.1016/j.biomaterials.2017.11.033] [PMID: 29182961]
[130]
Delgado-Olguín, P.; Huang, Y.; Li, X.; Christodoulou, D.; Seidman, C.E.; Seidman, J.G.; Tarakhovsky, A.; Bruneau, B.G. Epigenetic repression of cardiac progenitor gene expression by Ezh2 is required for postnatal cardiac homeostasis. Nat. Genet., 2012, 44(3), 343-347.
[http://dx.doi.org/10.1038/ng.1068] [PMID: 22267199]
[131]
Nguyen, A.T.; Xiao, B.; Neppl, R.L.; Kallin, E.M.; Li, J.; Chen, T.; Wang, D-Z.; Xiao, X.; Zhang, Y. DOT1L regulates dystrophin expression and is critical for cardiac function. Genes Dev., 2011, 25(3), 263-274.
[http://dx.doi.org/10.1101/gad.2018511] [PMID: 21289070]
[132]
Ito, E.; Miyagawa, S.; Fukushima, S.; Yoshikawa, Y.; Saito, S.; Saito, T.; Harada, A.; Takeda, M.; Kashiyama, N.; Nakamura, Y.; Shiozaki, M.; Toda, K.; Sawa, Y. Histone modification is correlated with reverse left ventricular remodeling in nonischemic dilated cardiomyopathy. Ann. Thorac. Surg., 2017, 104(5), 1531-1539.
[http://dx.doi.org/10.1016/j.athoracsur.2017.04.046] [PMID: 28760462]
[133]
Jiang, D-S.; Yi, X.; Li, R.; Su, Y-S.; Wang, J.; Chen, M-L.; Liu, L-G.; Hu, M.; Cheng, C.; Zheng, P.; Zhu, X.H.; Wei, X. The histone methyltransferase mixed lineage leukemia (MLL) 3 may play a potential role in clinical dilated cardiomyopathy. Mol. Med., 2017, 23(1), 196-203.
[http://dx.doi.org/10.2119/molmed.2017.00012] [PMID: 28805231]
[134]
Greißel, A.; Culmes, M.; Burgkart, R.; Zimmermann, A.; Eckstein, H-H.; Zernecke, A.; Pelisek, J. Histone acetylation and methylation significantly change with severity of atherosclerosis in human carotid plaques. Cardiovasc. Pathol., 2016, 25(2), 79-86.
[http://dx.doi.org/10.1016/j.carpath.2015.11.001] [PMID: 26764138]
[135]
Winnik, S.; Auwerx, J.; Sinclair, D.A.; Matter, C.M. Protective effects of sirtuins in cardiovascular diseases: From bench to bedside. Eur. Heart J., 2015, 36(48), 3404-3412.
[http://dx.doi.org/10.1093/eurheartj/ehv290] [PMID: 26112889]
[136]
Favero, G.; Franceschetti, L.; Rodella, L.F.; Rezzani, R. Sirtuins, aging, and cardiovascular risks. Age (Dordr.), 2015, 37(4), 9804.
[http://dx.doi.org/10.1007/s11357-015-9804-y] [PMID: 26099749]
[137]
Haigis, M.C.; Sinclair, D.A. Sirtuins in aging and age-related diseases. Handbook of the Biology of Aging; Masoro, E.J; Austad, S.N., Ed.; Elsevier, Academic Press: Cambridge, Massachusetts, 2011, pp. 243-274.
[http://dx.doi.org/10.1016/B978-0-12-378638-8.00011-7]
[138]
Wątroba, M.; Dudek, I.; Skoda, M.; Stangret, A.; Rzodkiewicz, P.; Szukiewicz, D. Sirtuins, epigenetics and longevity. Ageing Res. Rev., 2017, 40, 11-19.
[http://dx.doi.org/10.1016/j.arr.2017.08.001] [PMID: 28789901]
[139]
Cencioni, C.; Spallotta, F.; Mai, A.; Martelli, F.; Farsetti, A.; Zeiher, A.M.; Gaetano, C. Sirtuin function in aging heart and vessels. J. Mol. Cell. Cardiol., 2015, 83, 55-61.
[http://dx.doi.org/10.1016/j.yjmcc.2014.12.023] [PMID: 25579854]
[140]
Bindu, S.; Pillai, V.B.; Gupta, M.P. Role of sirtuins in regulating pathophysiology of the heart. Trends Endocrinol. Metab., 2016, 27(8), 563-573.
[http://dx.doi.org/10.1016/j.tem.2016.04.015] [PMID: 27210897]
[141]
Hershberger, K.A.; Martin, A.S.; Hirschey, M.D. Role of NAD+ and mitochondrial sirtuins in cardiac and renal diseases. Nat. Rev. Nephrol., 2017, 13(4), 213-225.
[http://dx.doi.org/10.1038/nrneph.2017.5] [PMID: 28163307]
[142]
van de Ven, R.A.H.; Santos, D.; Haigis, M.C. Mitochondrial sirtuins and molecular mechanisms of aging. Trends Mol. Med., 2017, 23(4), 320-331.
[http://dx.doi.org/10.1016/j.molmed.2017.02.005] [PMID: 28285806]
[143]
Liu, F.; Levin, M.D.; Petrenko, N.B.; Lu, M.M.; Wang, T.; Yuan, L.J.; Stout, A.L.; Epstein, J.A.; Patel, V.V. Histone-deacetylase inhibition reverses atrial arrhythmia inducibility and fibrosis in cardiac hypertrophy independent of angiotensin. J. Mol. Cell. Cardiol., 2008, 45(6), 715-723.
[http://dx.doi.org/10.1016/j.yjmcc.2008.08.015] [PMID: 18926829]
[144]
Oliveira-Carvalho, V.; Carvalho, V.O.; Bocchi, E.A. The emerging role of miR-208a in the heart. DNA Cell Biol., 2013, 32(1), 8-12.
[http://dx.doi.org/10.1089/dna.2012.1787] [PMID: 23121236]
[145]
Zhao, Y.; Ransom, J.F.; Li, A.; Vedantham, V.; von Drehle, M.; Muth, A.N.; Tsuchihashi, T.; McManus, M.T.; Schwartz, R.J.; Srivastava, D. Dysregulation of cardiogenesis, cardiac conduction, and cell cycle in mice lacking miRNA-1-2. Cell, 2007, 129(2), 303-317.
[http://dx.doi.org/10.1016/j.cell.2007.03.030] [PMID: 17397913]
[146]
Kim, G.H. MicroRNA regulation of cardiac conduction and arrhythmias. Transl. Res., 2013, 161(5), 381-392.
[http://dx.doi.org/10.1016/j.trsl.2012.12.004] [PMID: 23274306]
[147]
Gusterson, R.J.; Jazrawi, E.; Adcock, I.M.; Latchman, D.S. The transcriptional co-activators CREB-Binding Protein (CBP) and p300 play a critical role in cardiac hypertrophy that is dependent on their histone acetyltransferase activity. J. Biol. Chem., 2003, 278(9), 6838-6847.
[http://dx.doi.org/10.1074/jbc.M211762200] [PMID: 12477714]
[148]
Antos, C.L.; McKinsey, T.A.; Dreitz, M.; Hollingsworth, L.M.; Zhang, C-L.; Schreiber, K.; Rindt, H.; Gorczynski, R.J.; Olson, E.N. Dose-dependent blockade to cardiomyocyte hypertrophy by histone deacetylase inhibitors. J. Biol. Chem., 2003, 278(31), 28930-28937.
[http://dx.doi.org/10.1074/jbc.M303113200] [PMID: 12761226]
[149]
Kee, H.J.; Sohn, I.S.; Nam, K.I.; Park, J.E.; Qian, Y.R.; Yin, Z.; Ahn, Y.; Jeong, M.H.; Bang, Y-J.; Kim, N. Clinical perspective. Circulation, 2006, 113(1), 51-59.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.105.559724] [PMID: 16380549]
[150]
Kook, H.; Lepore, J.J.; Gitler, A.D.; Lu, M.M.; Wing-Man Yung, W.; Mackay, J.; Zhou, R.; Ferrari, V.; Gruber, P.; Epstein, J.A. Cardiac hypertrophy and histone deacetylase-dependent transcriptional repression mediated by the atypical homeodomain protein Hop. J. Clin. Invest., 2003, 112(6), 863-871.
[http://dx.doi.org/10.1172/JCI19137] [PMID: 12975471]
[151]
Haddad, F.; Bodell, P.W.; Qin, A.X.; Giger, J.M.; Baldwin, K.M. Role of antisense RNA in coordinating cardiac myosin heavy chain gene switching. J. Biol. Chem., 2003, 278(39), 37132-37138.
[http://dx.doi.org/10.1074/jbc.M305911200] [PMID: 12851393]
[152]
Barrick, C.J.; Roberts, R.B.; Rojas, M.; Rajamannan, N.M.; Suitt, C.B.; O’Brien, K.D.; Smyth, S.S.; Threadgill, D.W. Reduced EGFR causes abnormal valvular differentiation leading to calcific aortic stenosis and left ventricular hypertrophy in C57BL/6J but not 129S1/SvImJ mice. Am. J. Physiol. Heart Circ. Physiol., 2009, 297(1), H65-H75.
[http://dx.doi.org/10.1152/ajpheart.00866.2008] [PMID: 19448146]
[153]
Lund, G.; Andersson, L.; Lauria, M.; Lindholm, M.; Fraga, M.F.; Villar-Garea, A.; Ballestar, E.; Esteller, M.; Zaina, S. DNA methylation polymorphisms precede any histological sign of atherosclerosis in mice lacking apolipoprotein E. J. Biol. Chem., 2004, 279(28), 29147-29154.
[http://dx.doi.org/10.1074/jbc.M403618200] [PMID: 15131116]
[154]
Zhu, S.; Goldschmidt-Clermont, P.J.; Dong, C. Inactivation of monocarboxylate transporter MCT3 by DNA methylation in atherosclerosis. Circulation, 2005, 112(9), 1353-1361.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.104.519025] [PMID: 16116050]
[155]
Movassagh, M.; Choy, M-K.; Goddard, M.; Bennett, M.R.; Down, T.A.; Foo, R.S-Y. Differential DNA methylation correlates with differential expression of angiogenic factors in human heart failure. PLoS One, 2010, 5(1), e8564.
[http://dx.doi.org/10.1371/journal.pone.0008564] [PMID: 20084101]
[156]
Movassagh, M.; Choy, M-K.; Knowles, D.A.; Cordeddu, L.; Haider, S.; Down, T.; Siggens, L.; Vujic, A.; Simeoni, I.; Penkett, C.; Goddard, M.; Lio, P.; Bennett, M.R.; Foo, R.S. Distinct epigenomic features in end-stage failing human hearts. Circulation, 2011, 124(22), 2411-2422.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.111.040071] [PMID: 22025602]
[157]
Kaneda, R.; Takada, S.; Yamashita, Y.; Choi, Y.L.; Nonaka-Sarukawa, M.; Soda, M.; Misawa, Y.; Isomura, T.; Shimada, K.; Mano, H. Genome-wide histone methylation profile for heart failure. Genes Cells, 2009, 14(1), 69-77.
[http://dx.doi.org/10.1111/j.1365-2443.2008.01252.x] [PMID: 19077033]
[158]
Jin, J.; Wang, X.; Zhi, X.; Meng, D. Epigenetic regulation in diabetic vascular complications. J. Mol. Endocrinol., 2019, 63(4), R103-R115.
[http://dx.doi.org/10.1530/JME-19-0170] [PMID: 31600719]
[159]
Gilham, D.; Wasiak, S.; Tsujikawa, L.M.; Halliday, C.; Norek, K.; Patel, R.G.; Kulikowski, E.; Johansson, J.; Sweeney, M.; Wong, N.C.; Gordon, A.; McLure, K.; Young, P. RVX-208, a BET-inhibitor for treating atherosclerotic cardiovascular disease, raises ApoA-I/HDL and represses pathways that contribute to cardiovascular disease. Atherosclerosis, 2016, 247, 48-57.
[http://dx.doi.org/10.1016/j.atherosclerosis.2016.01.036] [PMID: 26868508]
[160]
Piquereau, J.; Perros, F. BET bromodomain inhibitors and pulmonary arterial hypertension: Take care of the heart. Am. J. Respir. Crit. Care Med., 2019, 200(9), 1187-1188.
[http://dx.doi.org/10.1164/rccm.201905-0993LE] [PMID: 31419391]
[161]
Cully, M. Cardiovascular disease: BET inhibitor attenuates heart failure. Nat. Rev. Drug Discov., 2017, 16(7), 453-453.
[http://dx.doi.org/10.1038/nrd.2017.125] [PMID: 28660902]
[162]
NCT02586155, Effect of selective BET protein inhibitor apabetalone on cardiovascular outcomes in patients with acute coronary syndrome and diabetes: Rationale, design, and baseline characteristics of the BETonMACE trial.
[163]
Paul, S.K.; Klein, K.; Thorsted, B.L.; Wolden, M.L.; Khunti, K. Delay in treatment intensification increases the risks of cardiovascular events in patients with type 2 diabetes. Cardiovasc. Diabetol., 2015, 14(1), 100.
[http://dx.doi.org/10.1186/s12933-015-0260-x] [PMID: 26249018]
[164]
Lee, H-A.; Lee, D-Y.; Cho, H-M.; Kim, S-Y.; Iwasaki, Y.; Kim, I.K. Histone deacetylase inhibition attenuates transcriptional activity of mineralocorticoid receptor through its acetylation and prevents development of hypertension. Circ. Res., 2013, 112(7), 1004-1012.
[http://dx.doi.org/10.1161/CIRCRESAHA.113.301071] [PMID: 23421989]
[165]
Zhang, L.X.; Du, J.; Zhao, Y.T.; Wang, J.; Zhang, S.; Dubielecka, P.M.; Wei, L.; Zhuang, S.; Qin, G.; Chin, Y.E.; Zhao, T.C. Transgenic overexpression of active HDAC4 in the heart attenuates cardiac function and exacerbates remodeling in infarcted myocardium. J. Appl. Physiol., 2018, 125(6), 1968-1978.
[http://dx.doi.org/10.1152/japplphysiol.00006.2018] [PMID: 30284520]
[166]
Xie, M.; Hill, J.A. HDAC-dependent ventricular remodeling. Trends Cardiovasc. Med., 2013, 23(6), 229-235.
[http://dx.doi.org/10.1016/j.tcm.2012.12.006] [PMID: 23499301]
[167]
Xie, M.; Kong, Y.; Tan, W.; May, H.; Battiprolu, P.K.; Pedrozo, Z.; Wang, Z.V.; Morales, C.; Luo, X.; Cho, G.; Jiang, N.; Jessen, M.E.; Warner, J.J.; Lavandero, S.; Gillette, T.G.; Turer, A.T.; Hill, J.A. Histone deacetylase inhibition blunts ischemia/reperfusion injury by inducing cardiomyocyte autophagy. Circulation, 2014, 129(10), 1139-1151.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.113.002416] [PMID: 24396039]
[168]
Bagchi, R.A.; Weeks, K.L. Histone deacetylases in cardiovascular and metabolic diseases. J. Mol. Cell. Cardiol., 2019, 130, 151-159.
[http://dx.doi.org/10.1016/j.yjmcc.2019.04.003] [PMID: 30978343]
[169]
Shultz, M.D.; Cao, X.; Chen, C.H.; Cho, Y.S.; Davis, N.R.; Eckman, J.; Fan, J.; Fekete, A.; Firestone, B.; Flynn, J.; Green, J.; Growney, J.D.; Holmqvist, M.; Hsu, M.; Jansson, D.; Jiang, L.; Kwon, P.; Liu, G.; Lombardo, F.; Lu, Q.; Majumdar, D.; Meta, C.; Perez, L.; Pu, M.; Ramsey, T.; Remiszewski, S.; Skolnik, S.; Traebert, M.; Urban, L.; Uttamsingh, V.; Wang, P.; Whitebread, S.; Whitehead, L.; Yan-Neale, Y.; Yao, Y.M.; Zhou, L.; Atadja, P. Optimization of the in vitro cardiac safety of hydroxamate-based histone deacetylase inhibitors. J. Med. Chem., 2011, 54(13), 4752-4772.
[http://dx.doi.org/10.1021/jm200388e] [PMID: 21650221]
[170]
Morimoto, T.; Sunagawa, Y.; Kawamura, T.; Takaya, T.; Wada, H.; Nagasawa, A.; Komeda, M.; Fujita, M.; Shimatsu, A.; Kita, T.; Hasegawa, K. The dietary compound curcumin inhibits p300 histone acetyltransferase activity and prevents heart failure in rats. J. Clin. Invest., 2008, 118(3), 868-878.
[http://dx.doi.org/10.1172/JCI33160] [PMID: 18292809]
[171]
Luo, T.; Chen, B.; Wang, X. 4-PBA prevents pressure overload-induced myocardial hypertrophy and interstitial fibrosis by attenuating endoplasmic reticulum stress. Chem. Biol. Interact., 2015, 242, 99-106.
[http://dx.doi.org/10.1016/j.cbi.2015.09.025] [PMID: 26428355]
[172]
Chen, M.; Zhang, Y.; Jiang, H.; Lin, P.; Chen, X. Effect of 5-AZA- 2′-dC on angiotensin II-induced cardiomyocyte hypertrophy. Zhonghua Jizhen Yixue Zazhi, 2018, 27(3), 301-306.
[173]
Fang, X.; Robinson, J.; Wang-Hu, J.; Jiang, L.; Freeman, D.A.; Rivkees, S.A.; Wendler, C.C. cAMP induces hypertrophy and alters DNA methylation in HL-1 cardiomyocytes. Am. J. Physiol. Cell Physiol., 2015, 309(6), C425-C436.
[http://dx.doi.org/10.1152/ajpcell.00058.2015] [PMID: 26224577]
[174]
Watson, C.J.; Horgan, S.; Neary, R.; Glezeva, N.; Tea, I.; Corrigan, N.; McDonald, K.; Ledwidge, M.; Baugh, J. Epigenetic therapy for the treatment of hypertension-induced cardiac hypertrophy and fibrosis. J. Cardiovasc. Pharmacol. Ther., 2016, 21(1), 127-137.
[http://dx.doi.org/10.1177/1074248415591698] [PMID: 26130616]
[175]
Kim, Y.S.; Kang, W.S.; Kwon, J.S.; Hong, M.H.; Jeong, H.Y.; Jeong, H.C.; Jeong, M.H.; Ahn, Y. Protective role of 5-azacytidine on myocardial infarction is associated with modulation of macrophage phenotype and inhibition of fibrosis. J. Cell. Mol. Med., 2014, 18(6), 1018-1027.
[http://dx.doi.org/10.1111/jcmm.12248] [PMID: 24571348]
[176]
Liu, H.; Li, G.; Zhao, W.; Hu, Y. Inhibition of MiR-92a may protect endothelial cells after acute myocardial infarction in rats: Role of KLF2/4. Med. Sci. Monit., 2016, 22, 2451-2462.
[http://dx.doi.org/10.12659/MSM.897266] [PMID: 27411964]
[177]
Liu, X.; Meng, H.; Jiang, C.; Yang, S.; Cui, F.; Yang, P. Differential microRNA expression and regulation in the rat model of post-infarction heart failure. PLoS One, 2016, 11(8), e0160920.
[http://dx.doi.org/10.1371/journal.pone.0160920] [PMID: 27504893]
[178]
Viereck, J.; Kumarswamy, R.; Foinquinos, A.; Xiao, K.; Avramopoulos, P.; Kunz, M.; Dittrich, M.; Maetzig, T.; Zimmer, K.; Remke, J. Long noncoding RNA Chast promotes cardiac remodeling. Sci. Transl. Med., 2016, 8(326), 326ra22.
[http://dx.doi.org/10.1126/scitranslmed.aaf1475]
[179]
Shapiro, M.D.; Tavori, H.; Fazio, S. PCSK9: From basic science discoveries to clinical trials. Circ. Res., 2018, 122(10), 1420-1438.
[http://dx.doi.org/10.1161/CIRCRESAHA.118.311227] [PMID: 29748367]
[180]
Nicholls, R.D.; Knepper, J.L. Genome organization, function, and imprinting in Prader-Willi and Angelman syndromes. Annu. Rev. Genomics Hum. Genet., 2001, 2(1), 153-175.
[http://dx.doi.org/10.1146/annurev.genom.2.1.153] [PMID: 11701647]
[181]
Weksberg, R.; Smith, A.C.; Squire, J.; Sadowski, P. Beckwith-Wiedemann syndrome demonstrates a role for epigenetic control of normal development. Hum. Mol. Genet., 2003, 12(Spec No 1)(Suppl. 1), R61-R68.
[http://dx.doi.org/10.1093/hmg/ddg067] [PMID: 12668598]
[182]
Hitchins, M.P.; Stanier, P.; Preece, M.A.; Moore, G.E. Silver-Russell syndrome: A dissection of the genetic aetiology and candidate chromosomal regions. J. Med. Genet., 2001, 38(12), 810-819.
[http://dx.doi.org/10.1136/jmg.38.12.810] [PMID: 11748303]
[183]
Verona, R.I.; Mann, M.R.; Bartolomei, M.S. Genomic imprinting: Intricacies of epigenetic regulation in clusters. Annu. Rev. Cell Dev. Biol., 2003, 19(1), 237-259.
[http://dx.doi.org/10.1146/annurev.cellbio.19.111401.092717] [PMID: 14570570]
[184]
Ulaner, G.A.; Yang, Y.; Hu, J-F.; Li, T.; Vu, T.H.; Hoffman, A.R. CTCF binding at the insulin-like growth factor-II (IGF2)/H19 imprinting control region is insufficient to regulate IGF2/H19 expression in human tissues. Endocrinology, 2003, 144(10), 4420-4426.
[http://dx.doi.org/10.1210/en.2003-0681] [PMID: 12960026]
[185]
Beygo, J.; Citro, V.; Sparago, A.; De Crescenzo, A.; Cerrato, F.; Heitmann, M.; Rademacher, K.; Guala, A.; Enklaar, T.; Anichini, C.; Cirillo Silengo, M.; Graf, N.; Prawitt, D.; Cubellis, M.V.; Horsthemke, B.; Buiting, K.; Riccio, A. The molecular function and clinical phenotype of partial deletions of the IGF2/H19 imprinting control region depends on the spatial arrangement of the remaining CTCF-binding sites. Hum. Mol. Genet., 2013, 22(3), 544-557.
[http://dx.doi.org/10.1093/hmg/dds465] [PMID: 23118352]
[186]
Jacob, K.J.; Robinson, W.P.; Lefebvre, L. Beckwith-Wiedemann and Silver-Russell syndromes: Opposite developmental imbalances in imprinted regulators of placental function and embryonic growth. Clin. Genet., 2013, 84(4), 326-334.
[http://dx.doi.org/10.1111/cge.12143] [PMID: 23495910]
[187]
Guenther, M.G.; Levine, S.S.; Boyer, L.A.; Jaenisch, R.; Young, R.A. A chromatin landmark and transcription initiation at most promoters in human cells. Cell, 2007, 130(1), 77-88.
[http://dx.doi.org/10.1016/j.cell.2007.05.042] [PMID: 17632057]
[188]
Mikkelsen, T.S.; Ku, M.; Jaffe, D.B.; Issac, B.; Lieberman, E.; Giannoukos, G.; Alvarez, P.; Brockman, W.; Kim, T-K.; Koche, R.P.; Lee, W.; Mendenhall, E.; O’Donovan, A.; Presser, A.; Russ, C.; Xie, X.; Meissner, A.; Wernig, M.; Jaenisch, R.; Nusbaum, C.; Lander, E.S.; Bernstein, B.E. Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature, 2007, 448(7153), 553-560.
[http://dx.doi.org/10.1038/nature06008] [PMID: 17603471]
[189]
Azuara, V.; Perry, P.; Sauer, S.; Spivakov, M.; Jørgensen, H.F.; John, R.M.; Gouti, M.; Casanova, M.; Warnes, G.; Merkenschlager, M.; Fisher, A.G. Chromatin signatures of pluripotent cell lines. Nat. Cell Biol., 2006, 8(5), 532-538.
[http://dx.doi.org/10.1038/ncb1403] [PMID: 16570078]
[190]
Angelman, H. ‘Puppet’ children a report on three cases. Dev. Med. Child Neurol., 1965, 7(6), 681-688.
[http://dx.doi.org/10.1111/j.1469-8749.1965.tb07844.x]
[191]
Henry, I.; Bonaïti-Pellié, C.; Chehensse, V. Uniparental paternal disomy in sporadic Beckwith-Wiedemann syndrome with Wilms’ tumor suggests genomic imprinting. Nature, 1991, 351, 665-667.
[http://dx.doi.org/10.1038/351665a0] [PMID: 1675767]
[192]
Buiting, K.; Barnicoat, A.; Lich, C.; Pembrey, M.; Malcolm, S.; Horsthemke, B. Disruption of the bipartite imprinting center in a family with Angelman syndrome. Am. J. Hum. Genet., 2001, 68(5), 1290-1294.
[http://dx.doi.org/10.1086/320120] [PMID: 11283796]
[193]
Demars, J.; Gicquel, C. Epigenetic and genetic disturbance of the imprinted 11p15 region in Beckwith-Wiedemann and Silver-Russell syndromes. Clin. Genet., 2012, 81(4), 350-361.
[http://dx.doi.org/10.1111/j.1399-0004.2011.01822.x] [PMID: 22150955]
[194]
Viljoen, D.; Ramesar, R. Evidence for paternal imprinting in familial Beckwith-Wiedemann syndrome. J. Med. Genet., 1992, 29(4), 221-225.
[http://dx.doi.org/10.1136/jmg.29.4.221] [PMID: 1583639]
[195]
Preece, M.A.; Price, S.M.; Davies, V.; Clough, L.; Stanier, P.; Trembath, R.C.; Moore, G.E. Maternal uniparental disomy 7 in Silver-Russell syndrome. J. Med. Genet., 1997, 34(1), 6-9.
[http://dx.doi.org/10.1136/jmg.34.1.6] [PMID: 9032641]
[196]
Eggermann, T.; Wollmann, H.A.; Kuner, R.; Eggermann, K.; Enders, H.; Kaiser, P.; Ranke, M.B. Molecular studies in 37 Silver-Russell syndrome patients: Frequency and etiology of uniparental disomy. Hum. Genet., 1997, 100(3-4), 415-419.
[http://dx.doi.org/10.1007/s004390050526] [PMID: 9272165]
[197]
Kotzot, D.; Balmer, D.; Baumer, A.; Chrzanowska, K.; Hamel, B.C.; Ilyina, H.; Krajewska-Walasek, M.; Lurie, I.W.; Otten, B.J.; Schoenle, E.; Tariverdian, G.; Schinzel, A. Maternal uniparental disomy 7-review and further delineation of the phenotype. Eur. J. Pediatr., 2000, 159(4), 247-256.
[http://dx.doi.org/10.1007/s004310050064] [PMID: 10789928]
[198]
Riesewijk, A.M.; Blagitko, N.; Schinzel, A.A.; Hu, L.; Schulz, U.; Hamel, B.C.; Ropers, H-H.; Kalscheuer, V.M. Evidence against a major role of PEG1/MEST in Silver-Russell syndrome. Eur. J. Hum. Genet., 1998, 6(2), 114-120.
[http://dx.doi.org/10.1038/sj.ejhg.5200164] [PMID: 9781054]
[199]
Fisher, A.M.; Thomas, N.S.; Cockwell, A.; Stecko, O.; Kerr, B.; Temple, I.K.; Clayton, P. Duplications of chromosome 11p15 of maternal origin result in a phenotype that includes growth retardation. Hum. Genet., 2002, 111(3), 290-296.
[http://dx.doi.org/10.1007/s00439-002-0787-2] [PMID: 12215843]
[200]
Eggermann, T.; Meyer, E.; Obermann, C.; Heil, I.; Schüler, H.; Ranke, M.B.; Eggermann, K.; Wollmann, H.A. Is maternal duplication of 11p15 associated with Silver-Russell syndrome? J. Med. Genet., 2005, 42(5), e26-e26.
[http://dx.doi.org/10.1136/jmg.2004.028936] [PMID: 15863658]
[201]
Arnold, F. Pseudohypoparathyroidism-an example of” Seabright- Bantam” syndrome. Endocrinology, 1942, 3, 922-932.
[202]
Chase, L.R.; Melson, G.L.; Aurbach, G.D. Pseudohypoparathyroidism: Defective excretion of 3′,5′-AMP in response to parathyroid hormone. J. Clin. Invest., 1969, 48(10), 1832-1844.
[http://dx.doi.org/10.1172/JCI106149] [PMID: 4309802]
[203]
Kozasa, T.; Itoh, H.; Tsukamoto, T.; Kaziro, Y. Isolation and characterization of the human Gs alpha gene. Proc. Natl. Acad. Sci. USA, 1988, 85(7), 2081-2085.
[http://dx.doi.org/10.1073/pnas.85.7.2081] [PMID: 3127824]
[204]
Weinstein, L.S.; Yu, S.; Warner, D.R.; Liu, J. Endocrine manifestations of stimulatory G protein α-subunit mutations and the role of genomic imprinting. Endocr. Rev., 2001, 22(5), 675-705.
[PMID: 11588148]
[205]
Davies, S.J.; Hughes, H.E. Imprinting in Albright’s hereditary osteodystrophy. J. Med. Genet., 1993, 30(2), 101-103.
[http://dx.doi.org/10.1136/jmg.30.2.101] [PMID: 8383205]
[206]
Linglart, A.; Carel, J.C.; Garabédian, M.; Lé, T.; Mallet, E.; Kottler, M.L. GNAS1 lesions in pseudohypoparathyroidism Ia and Ic: Genotype phenotype relationship and evidence of the maternal transmission of the hormonal resistance. J. Clin. Endocrinol. Metab., 2002, 87(1), 189-197.
[http://dx.doi.org/10.1210/jcem.87.1.8133] [PMID: 11788646]
[207]
Hayward, B.E.; Moran, V.; Strain, L.; Bonthron, D.T. Bidirectional imprinting of a single gene: GNAS1 encodes maternally, paternally, and biallelically derived proteins. Proc. Natl. Acad. Sci. USA, 1998, 95(26), 15475-15480.
[http://dx.doi.org/10.1073/pnas.95.26.15475] [PMID: 9860993]
[208]
Peters, J.; Wroe, S.F.; Wells, C.A.; Miller, H.J.; Bodle, D.; Beechey, C.V.; Williamson, C.M.; Kelsey, G. A cluster of oppositely imprinted transcripts at the Gnas locus in the distal imprinting region of mouse chromosome 2. Proc. Natl. Acad. Sci. USA, 1999, 96(7), 3830-3835.
[http://dx.doi.org/10.1073/pnas.96.7.3830] [PMID: 10097123]
[209]
Robinson, W.P. Mechanisms leading to uniparental disomy and their clinical consequences. BioEssays, 2000, 22(5), 452-459.
[http://dx.doi.org/10.1002/(SICI)1521-1878(200005)22:5<452:AID-BIES7>3.0.CO;2-K] [PMID: 10797485]
[210]
Horsthemke, B.; Zechner, U. Novel strategies to cure imprinting disorders. Med. Genetik, 2020, 32(4), 335-340.
[211]
Bird, A. Perceptions of epigenetics. Nature, 2007, 447(7143), 396-398.
[http://dx.doi.org/10.1038/nature05913] [PMID: 17522671]
[212]
Moosavi, A.; Motevalizadeh Ardekani, A. Role of epigenetics in biology and human diseases. Iran. Biomed. J., 2016, 20(5), 246-258.
[PMID: 27377127]
[213]
Mazzone, R.; Zwergel, C.; Mai, A.; Valente, S. Epi-drugs in combination with immunotherapy: A new avenue to improve anticancer efficacy. Clin. Epigenetics, 2017, 9(1), 59.
[http://dx.doi.org/10.1186/s13148-017-0358-y] [PMID: 28572863]
[214]
Hom, G.; Graham, R.R.; Modrek, B.; Taylor, K.E.; Ortmann, W.; Garnier, S.; Lee, A.T.; Chung, S.A.; Ferreira, R.C.; Pant, P.V.; Ballinger, D.G.; Kosoy, R.; Demirci, F.Y.; Kamboh, M.I.; Kao, A.H.; Tian, C.; Gunnarsson, I.; Bengtsson, A.A.; Rantapää-Dahlqvist, S.; Petri, M.; Manzi, S.; Seldin, M.F.; Rönnblom, L.; Syvänen, A.C.; Criswell, L.A.; Gregersen, P.K.; Behrens, T.W. Association of systemic lupus erythematosus with C8orf13-BLK and ITGAM-ITGAX. N. Engl. J. Med., 2008, 358(9), 900-909.
[http://dx.doi.org/10.1056/NEJMoa0707865] [PMID: 18204098]
[215]
D’Cruz, D.P.; Khamashta, M.A.; Hughes, G.R.V. Systemic lupus erythematosus. Lancet, 2007, 369(9561), 587-596.
[216]
Lei, W.; Luo, Y.; Lei, W.; Luo, Y.; Yan, K.; Zhao, S.; Li, Y.; Qiu, X.; Zhou, Y.; Long, H.; Zhao, M.; Liang, Y.; Su, Y.; Lu, Q. Abnormal DNA methylation in CD4+ T cells from patients with systemic lupus erythematosus, systemic sclerosis, and dermatomyositis. Scand. J. Rheumatol., 2009, 38(5), 369-374.
[http://dx.doi.org/10.1080/03009740902758875] [PMID: 19444718]
[217]
Richardson, B.; Scheinbart, L.; Strahler, J.; Gross, L.; Hanash, S.; Johnson, M. Evidence for impaired T cell DNA methylation in systemic lupus erythematosus and rheumatoid arthritis. Arthritis Rheum., 1990, 33(11), 1665-1673.
[http://dx.doi.org/10.1002/art.1780331109] [PMID: 2242063]
[218]
Du, J.; Johnson, L.M.; Jacobsen, S.E.; Patel, D.J. DNA methylation pathways and their crosstalk with histone methylation. Nat. Rev. Mol. Cell Biol., 2015, 16(9), 519-532.
[http://dx.doi.org/10.1038/nrm4043] [PMID: 26296162]
[219]
Torres, I.O.; Fujimori, D.G. Functional coupling between writers, erasers and readers of histone and DNA methylation. Curr. Opin. Struct. Biol., 2015, 35, 68-75.
[http://dx.doi.org/10.1016/j.sbi.2015.09.007] [PMID: 26496625]
[220]
Schübeler, D. Function and information content of DNA methylation. Nature, 2015, 517(7534), 321-326.
[http://dx.doi.org/10.1038/nature14192] [PMID: 25592537]
[221]
Bjornsson, H.T.; Fallin, M.D.; Feinberg, A.P. An integrated epigenetic and genetic approach to common human disease. Trends Genet., 2004, 20(8), 350-358.
[http://dx.doi.org/10.1016/j.tig.2004.06.009] [PMID: 15262407]
[222]
Kaiser, S.; Jurkowski, T.P.; Kellner, S.; Schneider, D.; Jeltsch, A.; Helm, M. The RNA methyltransferase Dnmt2 methylates DNA in the structural context of a tRNA. RNA Biol., 2017, 14(9), 1241-1251.
[http://dx.doi.org/10.1080/15476286.2016.1236170] [PMID: 27819523]
[223]
Rountree, M.R.; Bachman, K.E.; Baylin, S.B. DNMT1 binds HDAC2 and a new co-repressor, DMAP1, to form a complex at replication foci. Nat. Genet., 2000, 25(3), 269-277.
[http://dx.doi.org/10.1038/77023] [PMID: 10888872]
[224]
Wadhwa, E.; Nicolaides, T. Bromodomain inhibitor review: Bromodomain and extra-terminal family protein inhibitors as a potential new therapy in central nervous system tumors. Cureus, 2016, 8(5), e620.
[http://dx.doi.org/10.7759/cureus.620] [PMID: 27382528]
[225]
Chen, Z.; Miao, F.; Paterson, A.D.; Lachin, J.M.; Zhang, L.; Schones, D.E.; Wu, X.; Wang, J.; Tompkins, J.D.; Genuth, S.; Braffett, B.H.; Riggs, A.D.; Natarajan, R. Epigenomic profiling reveals an association between persistence of DNA methylation and metabolic memory in the DCCT/EDIC type 1 diabetes cohort. Proc. Natl. Acad. Sci. USA, 2016, 113(21), E3002-E3011.
[http://dx.doi.org/10.1073/pnas.1603712113] [PMID: 27162351]
[226]
Paul, D.S.; Teschendorff, A.E.; Dang, M.A.; Lowe, R.; Hawa, M.I.; Ecker, S.; Beyan, H.; Cunningham, S.; Fouts, A.R.; Ramelius, A.; Burden, F.; Farrow, S.; Rowlston, S.; Rehnstrom, K.; Frontini, M.; Downes, K.; Busche, S.; Cheung, W.A.; Ge, B.; Simon, M.M.; Bujold, D.; Kwan, T.; Bourque, G.; Datta, A.; Lowy, E.; Clarke, L.; Flicek, P.; Libertini, E.; Heath, S.; Gut, M.; Gut, I.G.; Ouwehand, W.H.; Pastinen, T.; Soranzo, N.; Hofer, S.E.; Karges, B.; Meissner, T.; Boehm, B.O.; Cilio, C.; Elding Larsson, H.; Lernmark, Å.; Steck, A.K.; Rakyan, V.K.; Beck, S.; Leslie, R.D. Increased DNA methylation variability in type 1 diabetes across three immune effector cell types. Nat. Commun., 2016, 7(1), 13555.
[http://dx.doi.org/10.1038/ncomms13555] [PMID: 27898055]
[227]
Tahara, T.; Hirata, I.; Nakano, N.; Nagasaka, M.; Nakagawa, Y.; Shibata, T.; Ohmiya, N. Comprehensive DNA methylation profiling of inflammatory mucosa in ulcerative colitis. Inflamm. Bowel Dis., 2017, 23(1), 165-173.
[http://dx.doi.org/10.1097/MIB.0000000000000990] [PMID: 27930411]
[228]
Lawrence, M.; Daujat, S.; Schneider, R. Lateral thinking: How histone modifications regulate gene expression. Trends Genet., 2016, 32(1), 42-56.
[http://dx.doi.org/10.1016/j.tig.2015.10.007] [PMID: 26704082]
[229]
Venkatesh, S.; Workman, J.L. Histone exchange, chromatin structure and the regulation of transcription. Nat. Rev. Mol. Cell Biol., 2015, 16(3), 178-189.
[http://dx.doi.org/10.1038/nrm3941] [PMID: 25650798]
[230]
Khalil, A.M.; Guttman, M.; Huarte, M.; Garber, M.; Raj, A.; Rivea Morales, D.; Thomas, K.; Presser, A.; Bernstein, B.E.; van Oudenaarden, A.; Regev, A.; Lander, E.S.; Rinn, J.L. Many human large intergenic noncoding RNAs associate with chromatin-modifying complexes and affect gene expression. Proc. Natl. Acad. Sci. USA, 2009, 106(28), 11667-11672.
[http://dx.doi.org/10.1073/pnas.0904715106] [PMID: 19571010]
[231]
Trenkmann, M.; Brock, M.; Gay, R.E.; Kolling, C.; Speich, R.; Michel, B.A.; Gay, S.; Huber, L.C. Expression and function of EZH2 in synovial fibroblasts: Epigenetic repression of the Wnt inhibitor SFRP1 in rheumatoid arthritis. Ann. Rheum. Dis., 2011, 70(8), 1482-1488.
[http://dx.doi.org/10.1136/ard.2010.143040] [PMID: 21515604]
[232]
Hügle, T.; O’Reilly, S.; Simpson, R.; Kraaij, M.D.; Bigley, V.; Collin, M.; Krippner-Heidenreich, A.; van Laar, J.M. Tumor necrosis factor-costimulated T lymphocytes from patients with systemic sclerosis trigger collagen production in fibroblasts. Arthritis Rheum., 2013, 65(2), 481-491.
[http://dx.doi.org/10.1002/art.37738] [PMID: 23045159]
[233]
Thabet, Y.; Le Dantec, C.; Ghedira, I.; Devauchelle, V.; Cornec, D.; Pers, J-O.; Renaudineau, Y. Epigenetic dysregulation in salivary glands from patients with primary Sjögren’s syndrome may be ascribed to infiltrating B cells. J. Autoimmun., 2013, 41, 175-181.
[http://dx.doi.org/10.1016/j.jaut.2013.02.002] [PMID: 23478041]
[234]
Lee, H.J.; Li, C.W.; Hammerstad, S.S.; Stefan, M.; Tomer, Y. Immunogenetics of autoimmune thyroid diseases: A comprehensive review. J. Autoimmun., 2015, 64, 82-90.
[http://dx.doi.org/10.1016/j.jaut.2015.07.009] [PMID: 26235382]
[235]
McLachlan, S.M.; Rapoport, B. Breaking tolerance to thyroid antigens: Changing concepts in thyroid autoimmunity. Endocr. Rev., 2014, 35(1), 59-105.
[http://dx.doi.org/10.1210/er.2013-1055] [PMID: 24091783]
[236]
Wang, B.; Shao, X.; Song, R.; Xu, D.; Zhang, J.A. The emerging role of epigenetics in autoimmune thyroid diseases. Front. Immunol., 2017, 8(396), 396.
[http://dx.doi.org/10.3389/fimmu.2017.00396] [PMID: 28439272]
[237]
Mazzone, R.; Zwergel, C.; Artico, M.; Taurone, S.; Ralli, M.; Greco, A.; Mai, A. The emerging role of epigenetics in human autoimmune disorders. Clin. Epigenetics, 2019, 11(1), 34.
[http://dx.doi.org/10.1186/s13148-019-0632-2] [PMID: 30808407]
[238]
Huang, W.; Connor, E.; Rosa, T.D.; Muir, A.; Schatz, D.; Silverstein, J.; Crockett, S.; She, J.X.; Maclaren, N.K. Although DR3-DQB1*0201 may be associated with multiple component diseases of the autoimmune polyglandular syndromes, the human leukocyte antigen DR4-DQB1*0302 haplotype is implicated only in beta-cell autoimmunity. J. Clin. Endocrinol. Metab., 1996, 81(7), 2559-2563.
[PMID: 8675578]
[239]
Sellmer, A.; Stangl, H.; Beyer, M.; Grünstein, E.; Leonhardt, M.; Pongratz, H.; Eichhorn, E.; Elz, S.; Striegl, B.; Jenei-Lanzl, Z.; Dove, S.; Straub, R.H.; Krämer, O.H.; Mahboobi, S. Marbostat-100 defines a new class of potent and selective antiinflammatory and antirheumatic histone deacetylase 6 inhibitors. J. Med. Chem., 2018, 61(8), 3454-3477.
[http://dx.doi.org/10.1021/acs.jmedchem.7b01593] [PMID: 29589441]
[240]
Liu, J.; Kelly, J.; Yu, W.; Clausen, D.; Yu, Y.; Kim, H.; Duffy, J.L.; Chung, C.C.; Myers, R.W.; Carroll, S.; Klein, D.J.; Fells, J.; Holloway, M.K.; Wu, J.; Wu, G.; Howell, B.J.; Barnard, R.J.O.; Kozlowski, J.A. Selective class I HDAC inhibitors based on aryl ketone zinc binding induce HIV-1 protein for clearance. ACS Med. Chem. Lett., 2020, 11(7), 1476-1483.
[http://dx.doi.org/10.1021/acsmedchemlett.0c00302] [PMID: 32676157]

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