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Research Paper

Epigenetic repression of LEDGF during UVB exposure by recruitment of SUV39H1 and HDAC1 to the Sp1-responsive elements within LEDGF promoter CpG island

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Pages 268-280 | Received 15 Dec 2012, Accepted 01 Feb 2013, Published online: 05 Feb 2013

References

  • Poeschla EM. Integrase, LEDGF and HIV replication. Cell Mol Life Sci 2008; 65:1403 - 24; http://dx.doi.org/10.1007/s00018-008-7540-5; PMID: 18264802
  • Shinohara T, Singh DP, Fatma N. LEDGF, a survival factor, activates stress-related genes. Prog Retin Eye Res 2002; 21:341 - 58; http://dx.doi.org/10.1016/S1350-9462(02)00007-1; PMID: 12052388
  • Singh DP, Ohguro N, Chylack LT Jr., Shinohara T. Lens epithelium-derived growth factor: increased resistance to thermal and oxidative stresses. Invest Ophthalmol Vis Sci 1999; 40:1444 - 51; PMID: 10359326
  • Nakamura M, Singh DP, Kubo E, Chylack LT Jr., Shinohara T. LEDGF: survival of embryonic chick retinal photoreceptor cells. Invest Ophthalmol Vis Sci 2000; 41:1168 - 75; PMID: 10752956
  • Singh DP, Kubo E, Takamura Y, Shinohara T, Kumar A, Chylack LT Jr., et al. DNA binding domains and nuclear localization signal of LEDGF: contribution of two helix-turn-helix (HTH)-like domains and a stretch of 58 amino acids of the N-terminal to the trans-activation potential of LEDGF. J Mol Biol 2006; 355:379 - 94; http://dx.doi.org/10.1016/j.jmb.2005.10.054; PMID: 16318853
  • Bhargavan B, Fatma N, Chhunchha B, Singh V, Kubo E, Singh DP. LEDGF gene silencing impairs the tumorigenicity of prostate cancer DU145 cells by abating the expression of Hsp27 and activation of the Akt/ERK signaling pathway. Cell Death Dis 2012; 3:e316; http://dx.doi.org/10.1038/cddis.2012.57; PMID: 22647853
  • Matsui H, Lin L-R, Singh DP, Shinohara T, Reddy VN. Lens epithelium-derived growth factor: increased survival and decreased DNA breakage of human RPE cells induced by oxidative stress. Invest Ophthalmol Vis Sci 2001; 42:2935 - 41; PMID: 11687539
  • Sharma P, Shingh D, Fatma N, Chattopadhyay N, Chylack L, Shinohara T. Attenuation of LEDGF-DNA Binding Affinity and Down Regulation of LEDGF Promoter Activity in Human Lens Epithelial Cells Treated with TGFb1. Invest Ophthalmol Vis Sci 2002; 43:E2344
  • Singh DP, Bhargavan B, Chhunchha B, Kubo E, Kumar A, Fatma N. Transcriptional protein Sp1 regulates LEDGF transcription by directly interacting with its cis-elements in GC-rich region of TATA-less gene promoter. PLoS One 2012; 7:e37012; http://dx.doi.org/10.1371/journal.pone.0037012; PMID: 22615874
  • Singh DP, Fatma N, Kimura A, Chylack LT Jr., Shinohara T. LEDGF binds to heat shock and stress-related element to activate the expression of stress-related genes. Biochem Biophys Res Commun 2001; 283:943 - 55; http://dx.doi.org/10.1006/bbrc.2001.4887; PMID: 11350077
  • Ge H, Si Y, Roeder RG. Isolation of cDNAs encoding novel transcription coactivators p52 and p75 reveals an alternate regulatory mechanism of transcriptional activation. EMBO J 1998; 17:6723 - 9; http://dx.doi.org/10.1093/emboj/17.22.6723; PMID: 9822615
  • Singh DP, Kimura A, Chylack LT Jr., Shinohara T. Lens epithelium-derived growth factor (LEDGF) and p52 are derived from a single gene by alternative splicing. Gene 2000; 242:265 - 73; http://dx.doi.org/10.1016/S0378-1119(99)00506-5; PMID: 10721720
  • Sutherland HG, Newton K, Brownstein DG, Holmes MC, Kress C, Semple CA, et al. Disruption of Ledgf/Psip1 results in perinatal mortality and homeotic skeletal transformations. Mol Cell Biol 2006; 26:7201 - 10; http://dx.doi.org/10.1128/MCB.00459-06; PMID: 16980622
  • Maurer-Stroh S, Dickens NJ, Hughes-Davies L, Kouzarides T, Eisenhaber F, Ponting CP. The Tudor domain ‘Royal Family’: Tudor, plant Agenet, Chromo, PWWP and MBT domains. Trends Biochem Sci 2003; 28:69 - 74; http://dx.doi.org/10.1016/S0968-0004(03)00004-5; PMID: 12575993
  • Stec I, Nagl SB, van Ommen GJ, den Dunnen JT. The PWWP domain: a potential protein-protein interaction domain in nuclear proteins influencing differentiation?. FEBS Lett 2000; 473:1 - 5; http://dx.doi.org/10.1016/S0014-5793(00)01449-6; PMID: 10802047
  • Engelman A, Cherepanov P. The lentiviral integrase binding protein LEDGF and HIV-1 replication. PLoS Pathog 2008; 4:e1000046; http://dx.doi.org/10.1371/journal.ppat.1000046; PMID: 18369482
  • Fatma N, Singh DP, Shinohara T, Chylack LT Jr.. Transcriptional regulation of the antioxidant protein 2 gene, a thiol-specific antioxidant, by lens epithelium-derived growth factor to protect cells from oxidative stress. J Biol Chem 2001; 276:48899 - 907; http://dx.doi.org/10.1074/jbc.M100733200; PMID: 11677226
  • Sharma P, Fatma N, Kubo E, Shinohara T, Chylack LT Jr., Singh DP. Lens epithelium-derived growth factor relieves transforming growth factor-beta1-induced transcription repression of heat shock proteins in human lens epithelial cells. J Biol Chem 2003; 278:20037 - 46; http://dx.doi.org/10.1074/jbc.M212016200; PMID: 12649267
  • Machida S, Chaudhry P, Shinohara T, Singh DP, Reddy VN, Chylack LT Jr., et al. Lens epithelium-derived growth factor promotes photoreceptor survival in light-damaged and RCS rats. Invest Ophthalmol Vis Sci 2001; 42:1087 - 95; PMID: 11274090
  • De Rijck J, Bartholomeeusen K, Ceulemans H, Debyser Z, Gijsbers R. High-resolution profiling of the LEDGF chromatin interaction in the ENCODE region. Nucleic Acids Res 2010; 38:6135 - 47; http://dx.doi.org/10.1093/nar/gkq410; PMID: 20484370
  • Tsutsui KM, Sano K, Hosoya O, Miyamoto T, Tsutsui K. Nuclear protein LEDGF recognizes supercoiled DNA by a novel DNA-binding domain. Nucleic Acids Res 2011; 39:5067 - 81; http://dx.doi.org/10.1093/nar/gkr088; PMID: 21345933
  • Maertens GN, Cherepanov P, Engelman A. Transcriptional co-activator p75 binds and tethers the Myc-interacting protein JPO2 to chromatin. J Cell Sci 2006; 119:2563 - 71; http://dx.doi.org/10.1242/jcs.02995; PMID: 16735438
  • Yokoyama A, Cleary ML. Menin critically links MLL proteins with LEDGF on cancer-associated target genes. Cancer Cell 2008; 14:36 - 46; http://dx.doi.org/10.1016/j.ccr.2008.05.003; PMID: 18598942
  • Bartholomeeusen K, Christ F, Hendrix J, Rain JC, Emiliani S, Benarous R, et al. Lens epithelium-derived growth factor/p75 interacts with the transposase-derived DDE domain of PogZ. J Biol Chem 2009; 284:11467 - 77; http://dx.doi.org/10.1074/jbc.M807781200; PMID: 19244240
  • Hughes S, Jenkins V, Dar MJ, Engelman A, Cherepanov P. Transcriptional co-activator LEDGF interacts with Cdc7-activator of S-phase kinase (ASK) and stimulates its enzymatic activity. J Biol Chem 2010; 285:541 - 54; http://dx.doi.org/10.1074/jbc.M109.036491; PMID: 19864417
  • Leoh LS, van Heertum B, De Rijck J, Filippova M, Rios-Colon L, Basu A, et al. The stress oncoprotein LEDGF interacts with the methyl CpG binding protein MeCP2 and influences its transcriptional activity. Mol Cancer Res 2012; 10:378 - 91; http://dx.doi.org/10.1158/1541-7786.MCR-11-0314; PMID: 22275515
  • Bueno MTD, Garcia-Rivera JA, Kugelman JR, Morales E, Rosas-Acosta G, Llano M. SUMOylation of the lens epithelium-derived growth factor/p75 attenuates its transcriptional activity on the heat shock protein 27 promoter. J Mol Biol 2010; 399:221 - 39; http://dx.doi.org/10.1016/j.jmb.2010.03.063; PMID: 20382164
  • Ishihara K, Fatma N, Bhargavan B, Chhunchha B, Kubo E, Dey S, et al. Lens epithelium-derived growth factor deSumoylation by Sumo-specific protease-1 regulates its transcriptional activation of small heat shock protein and the cellular response. FEBS J 2012; 279:3048 - 70; http://dx.doi.org/10.1111/j.1742-4658.2012.08686.x; PMID: 22748127
  • Ames BN, Shigenaga MK, Hagen TM. Oxidants, antioxidants, and the degenerative diseases of aging. Proc Natl Acad Sci U S A 1993; 90:7915 - 22; http://dx.doi.org/10.1073/pnas.90.17.7915; PMID: 8367443
  • Kubo ERI, Miyoshi N, Fukuda M, Akagi Y. Cataract formation through the polyol pathway is associated with free radical production. Exp Eye Res 1999; 68:457 - 64; http://dx.doi.org/10.1006/exer.1998.0624; PMID: 10192803
  • Marsili S, Salganik RI, Albright CD, Freel CD, Johnsen S, Peiffer RL, et al. Cataract formation in a strain of rats selected for high oxidative stress. Exp Eye Res 2004; 79:595 - 612; http://dx.doi.org/10.1016/j.exer.2004.06.008; PMID: 15500819
  • Salganik RI. The benefits and hazards of antioxidants: controlling apoptosis and other protective mechanisms in cancer patients and the human population. J Am Coll Nutr 2001; 20:Suppl 464S - 72S, discussion 473S-5S; PMID: 11603657
  • Salganik RI, Solovyova NA, Dikalov SI, Grishaeva ON, Semenova LA, Popovsky AV. Inherited enhancement of hydroxyl radical generation and lipid peroxidation in the S strain rats results in DNA rearrangements, degenerative diseases, and premature aging. Biochem Biophys Res Commun 1994; 199:726 - 33; http://dx.doi.org/10.1006/bbrc.1994.1289; PMID: 8135816
  • Spector A. Oxidative stress-induced cataract: mechanism of action. FASEB J 1995; 9:1173 - 82; PMID: 7672510
  • Spector A. Review: Oxidative stress and disease. J Ocul Pharmacol Ther 2000; 16:193 - 201; http://dx.doi.org/10.1089/jop.2000.16.193; PMID: 10803430
  • Spector A, Kuszak JR, Ma W, Wang R-R, Ho Ys, Yang Y. The effect of photochemical stress upon the lenses of normal and glutathione peroxidase-1 knockout mice. Exp Eye Res 1998; 67:457 - 71; http://dx.doi.org/10.1006/exer.1998.0548; PMID: 9820794
  • Fartasch M, Diepgen TL, Schmitt J, Drexler H. The relationship between occupational sun exposure and non-melanoma skin cancer: clinical basics, epidemiology, occupational disease evaluation, and prevention. Dtsch Arztebl Int 2012; 109:715 - 20; PMID: 23181135
  • Zawia NH, Lahiri DK, Cardozo-Pelaez F. Epigenetics, oxidative stress, and Alzheimer disease. Free Radic Biol Med 2009; 46:1241 - 9; http://dx.doi.org/10.1016/j.freeradbiomed.2009.02.006; PMID: 19245828
  • Holliday R. Epigenetics: a historical overview. Epigenetics 2006; 1:76 - 80; http://dx.doi.org/10.4161/epi.1.2.2762; PMID: 17998809
  • Desfarges S, Abderrahmani A, Hernàndez-Novoa B, Munoz M, Ciuffi A. LEDGF TATA-less promoter is driven by the transcription factor Sp1. J Mol Biol 2011; 414:177 - 93; http://dx.doi.org/10.1016/j.jmb.2011.10.010; PMID: 22019592
  • Yuen RK, Neumann SM, Fok AK, Peñaherrera MS, McFadden DE, Robinson WP, et al. Extensive epigenetic reprogramming in human somatic tissues between fetus and adult. Epigenetics Chromatin 2011; 4:7; http://dx.doi.org/10.1186/1756-8935-4-7; PMID: 21545704
  • Peters AHFM, Kubicek S, Mechtler K, O’Sullivan RJ, Derijck AA, Perez-Burgos L, et al. Partitioning and plasticity of repressive histone methylation states in mammalian chromatin. Mol Cell 2003; 12:1577 - 89; http://dx.doi.org/10.1016/S1097-2765(03)00477-5; PMID: 14690609
  • Zhang Y, Reinberg D. Transcription regulation by histone methylation: interplay between different covalent modifications of the core histone tails. Genes Dev 2001; 15:2343 - 60; http://dx.doi.org/10.1101/gad.927301; PMID: 11562345
  • Fischle W, Wang Y, Allis CD. Histone and chromatin cross-talk. Curr Opin Cell Biol 2003; 15:172 - 83; http://dx.doi.org/10.1016/S0955-0674(03)00013-9; PMID: 12648673
  • Bannister AJ, Zegerman P, Partridge JF, Miska EA, Thomas JO, Allshire RC, et al. Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature 2001; 410:120 - 4; http://dx.doi.org/10.1038/35065138; PMID: 11242054
  • Czermin B, Melfi R, McCabe D, Seitz V, Imhof A, Pirrotta V. Drosophila enhancer of Zeste/ESC complexes have a histone H3 methyltransferase activity that marks chromosomal Polycomb sites. Cell 2002; 111:185 - 96; http://dx.doi.org/10.1016/S0092-8674(02)00975-3; PMID: 12408863
  • Schotta G, Lachner M, Sarma K, Ebert A, Sengupta R, Reuter G, et al. A silencing pathway to induce H3-K9 and H4-K20 trimethylation at constitutive heterochromatin. Genes Dev 2004; 18:1251 - 62; http://dx.doi.org/10.1101/gad.300704; PMID: 15145825
  • Jørgensen S, Schotta G, Sørensen CS. Histone H4 Lysine 20 methylation: key player in epigenetic regulation of genomic integrity. Nucleic Acids Res 2013; In press http://dx.doi.org/10.1093/nar/gkt012; PMID: 23345616
  • Martin C, Zhang Y. The diverse functions of histone lysine methylation. Nat Rev Mol Cell Biol 2005; 6:838 - 49; http://dx.doi.org/10.1038/nrm1761; PMID: 16261189
  • Garcia SN, Pereira-Smith O. MRGing chromatin dynamics and cellular senescence. Cell Biochem Biophys 2008; 50:133 - 41; http://dx.doi.org/10.1007/s12013-008-9006-7; PMID: 18231726
  • Lang-Mladek C, Popova O, Kiok K, Berlinger M, Rakic B, Aufsatz W, et al. Transgenerational inheritance and resetting of stress-induced loss of epigenetic gene silencing in Arabidopsis. Mol Plant 2010; 3:594 - 602; http://dx.doi.org/10.1093/mp/ssq014; PMID: 20410255
  • Low M, Read EL, Borek E. Methylation of DNA in HeLa cells after ultraviolet irradiation. Int J Radiat Oncol Biol Phys 1976; 1:289 - 94; http://dx.doi.org/10.1016/0360-3016(76)90053-5; PMID: 972089
  • Jones PA, Baylin SB. The epigenomics of cancer. Cell 2007; 128:683 - 92; http://dx.doi.org/10.1016/j.cell.2007.01.029; PMID: 17320506
  • Fahrner JA, Eguchi S, Herman JG, Baylin SB. Dependence of histone modifications and gene expression on DNA hypermethylation in cancer. Cancer Res 2002; 62:7213 - 8; PMID: 12499261
  • Katiyar SK, Singh T, Prasad R, Sun Q, Vaid M. Epigenetic alterations in ultraviolet radiation-induced skin carcinogenesis: interaction of bioactive dietary components on epigenetic targets. Photochem Photobiol 2012; 88:1066 - 74; http://dx.doi.org/10.1111/j.1751-1097.2011.01020.x; PMID: 22017262
  • Donkena KV, Young CY, Tindall DJ. Oxidative stress and DNA methylation in prostate cancer. Obstet Gynecol Int 2010; 2010:302051; http://dx.doi.org/10.1155/2010/302051; PMID: 20671914
  • Okano M, Xie S, Li E. Cloning and characterization of a family of novel mammalian DNA (cytosine-5) methyltransferases. Nat Genet 1998; 19:219 - 20; http://dx.doi.org/10.1038/890; PMID: 9662389
  • Moresi V, Carrer M, Grueter CE, Rifki OF, Shelton JM, Richardson JA, et al. Histone deacetylases 1 and 2 regulate autophagy flux and skeletal muscle homeostasis in mice. Proc Natl Acad Sci U S A 2012; 109:1649 - 54; http://dx.doi.org/10.1073/pnas.1121159109; PMID: 22307625
  • Mihaylova MM, Vasquez DS, Ravnskjaer K, Denechaud PD, Yu RT, Alvarez JG, et al. Class IIa histone deacetylases are hormone-activated regulators of FOXO and mammalian glucose homeostasis. Cell 2011; 145:607 - 21; http://dx.doi.org/10.1016/j.cell.2011.03.043; PMID: 21565617
  • Zhong L, D’Urso A, Toiber D, Sebastian C, Henry RE, Vadysirisack DD, et al. The histone deacetylase Sirt6 regulates glucose homeostasis via Hif1alpha. Cell 2010; 140:280 - 93; http://dx.doi.org/10.1016/j.cell.2009.12.041; PMID: 20141841
  • Deaton AM, Bird A. CpG islands and the regulation of transcription. Genes Dev 2011; 25:1010 - 22; http://dx.doi.org/10.1101/gad.2037511; PMID: 21576262
  • Stewart MD, Li J, Wong J. Relationship between histone H3 lysine 9 methylation, transcription repression, and heterochromatin protein 1 recruitment. Mol Cell Biol 2005; 25:2525 - 38; http://dx.doi.org/10.1128/MCB.25.7.2525-2538.2005; PMID: 15767660
  • Li B, Jackson J, Simon MD, Fleharty B, Gogol M, Seidel C, et al. Histone H3 lysine 36 dimethylation (H3K36me2) is sufficient to recruit the Rpd3s histone deacetylase complex and to repress spurious transcription. J Biol Chem 2009; 284:7970 - 6; http://dx.doi.org/10.1074/jbc.M808220200; PMID: 19155214
  • Papp B, Müller J. Histone trimethylation and the maintenance of transcriptional ON and OFF states by trxG and PcG proteins. Genes Dev 2006; 20:2041 - 54; http://dx.doi.org/10.1101/gad.388706; PMID: 16882982
  • Ganapathy V, Daniels T, Casiano CA. LEDGF: a novel nuclear autoantigen at the crossroads of cell survival and apoptosis. Autoimmun Rev 2003; 2:290 - 7; http://dx.doi.org/10.1016/S1568-9972(03)00063-6; PMID: 12965181
  • Mediavilla-Varela M, Pacheco FJ, Almaguel F, Perez J, Sahakian E, Daniels TR, et al. Docetaxel-induced prostate cancer cell death involves concomitant activation of caspase and lysosomal pathways and is attenuated by LEDGF. Mol Cancer 2009; 8:68; http://dx.doi.org/10.1186/1476-4598-8-68; PMID: 19715609
  • Blackledge NP, Zhou JC, Tolstorukov MY, Farcas AM, Park PJ, Klose RJ. CpG islands recruit a histone H3 lysine 36 demethylase. Mol Cell 2010; 38:179 - 90; http://dx.doi.org/10.1016/j.molcel.2010.04.009; PMID: 20417597
  • Bernstein BE, Mikkelsen TS, Xie X, Kamal M, Huebert DJ, Cuff J, et al. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 2006; 125:315 - 26; http://dx.doi.org/10.1016/j.cell.2006.02.041; PMID: 16630819
  • Guenther MG, Levine SS, Boyer LA, Jaenisch R, Young RA. A chromatin landmark and transcription initiation at most promoters in human cells. Cell 2007; 130:77 - 88; http://dx.doi.org/10.1016/j.cell.2007.05.042; PMID: 17632057
  • Tyson F, Heindel J. Environmental Influences on Epigenetic Regulation. Environ Health Perspect 2005; 113:A839
  • Jenuwein T, Allis CD. Translating the histone code. Science 2001; 293:1074 - 80; http://dx.doi.org/10.1126/science.1063127; PMID: 11498575
  • Margueron R, Trojer P, Reinberg D. The key to development: interpreting the histone code?. Curr Opin Genet Dev 2005; 15:163 - 76; http://dx.doi.org/10.1016/j.gde.2005.01.005; PMID: 15797199
  • Okano M, Bell DW, Haber DA, Li E. DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 1999; 99:247 - 57; http://dx.doi.org/10.1016/S0092-8674(00)81656-6; PMID: 10555141
  • Murray K. The Occurrence of Epsilon-N-Methyl Lysine in Histones. Biochemistry 1964; 3:10 - 5; http://dx.doi.org/10.1021/bi00889a003; PMID: 14114491
  • Gary JD, Clarke S. RNA and protein interactions modulated by protein arginine methylation. Prog Nucleic Acid Res Mol Biol 1998; 61:65 - 131; http://dx.doi.org/10.1016/S0079-6603(08)60825-9; PMID: 9752719
  • Kubo E, Fatma N, Akagi Y, Beier DR, Singh SP, Singh DP. TAT-mediated PRDX6 protein transduction protects against eye lens epithelial cell death and delays lens opacity. Am J Physiol Cell Physiol 2008; 294:C842 - 55; http://dx.doi.org/10.1152/ajpcell.00540.2007; PMID: 18184874
  • Fatma N, Kubo E, Sharma P, Beier DR, Singh DP. Impaired homeostasis and phenotypic abnormalities in Prdx6-/-mice lens epithelial cells by reactive oxygen species: increased expression and activation of TGFbeta. [beta] Cell Death Differ 2005; 12:734 - 50; http://dx.doi.org/10.1038/sj.cdd.4401597; PMID: 15818411
  • Takamura Y, Fatma N, Kubo E, Singh DP. Regulation of heavy subunit chain of gamma-glutamylcysteine synthetase by tumor necrosis factor-alpha in lens epithelial cells: role of LEDGF. Am J Physiol Cell Physiol 2006; 290:C554 - 66; http://dx.doi.org/10.1152/ajpcell.00398.2005; PMID: 16403949
  • Fatma N, Singh DP, Shinohara T, Chylack LT Jr.. Transcriptional regulation of the antioxidant protein 2 gene, a thiol-specific antioxidant, by lens epithelium-derived growth factor to protect cells from oxidative stress. J Biol Chem 2001; 276:48899 - 907; http://dx.doi.org/10.1074/jbc.M100733200; PMID: 11677226
  • Zhu WG, Srinivasan K, Dai Z, Duan W, Druhan LJ, Ding H, et al. Methylation of adjacent CpG sites affects Sp1/Sp3 binding and activity in the p21(Cip1) promoter. Mol Cell Biol 2003; 23:4056 - 65; http://dx.doi.org/10.1128/MCB.23.12.4056-4065.2003; PMID: 12773551

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