Linking DNA methylation and histone modification: patterns and paradigms (2024)

  • Kafri, T. et al. Developmental pattern of gene-specific DNA methylation in the mouse embryo and germline. Genes Dev. 6, 705–714 (1992).

    CAS PubMed Google Scholar

  • Monk, M., Boubelik, M. & Lehnert, S. Temporal and regional changes in DNA methylation in the embryonic, extraembryonic and germ cell lineages during mouse embryo development. Development 99, 371–382 (1987).

    CAS PubMed Google Scholar

  • Okano, M., Bell, D. W., Haber, D. A. & Li, E. DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 99, 247–257 (1999).

    CAS PubMed Google Scholar

  • Brandeis, M. et al. Sp1 elements protect a CpG island from de novo methylation. Nature 371, 435–438 (1994).

    CAS PubMed Google Scholar

  • Siegfried, Z. et al. DNA methylation represses transcription in vivo. Nature Genet. 22, 203–206 (1999).

    CAS PubMed Google Scholar

  • Macleod, D., Charlton, J., Mullins, J. & Bird, A. P. Sp1 sites in the mouse aprt gene promoter are required to prevent methylation of the CpG island. Genes Dev. 8, 2282–2292 (1994).

    CAS PubMed Google Scholar

  • Frank, D. et al. Demethylation of CpG islands in embryonic cells. Nature 351, 239–241 (1991).

    CAS PubMed Google Scholar

  • Ooi, S. K. et al. DNMT3L connects unmethylated lysine 4 of histone H3 to de novo methylation of DNA. Nature 448, 714–717 (2007). References 8 and 10 show that DNMT3L interacts with unmethylated H3K4 through its N terminus and with DNMT3A through its C terminus, thus linking the DNA methylation machinery to the modification state of histone tails.

    CAS PubMed PubMed Central Google Scholar

  • 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 130, 77–88 (2007).

    CAS PubMed PubMed Central Google Scholar

  • Jia, D., Jurkowska, R. Z., Zhang, X., Jeltsch, A. & Cheng, X. Structure of Dnmt3a bound to Dnmt3L suggests a model for de novo DNA methylation. Nature 449, 248–251 (2007).

    CAS PubMed PubMed Central Google Scholar

  • Bourc'his, D., Xu, G. L., Lin, C. S., Bollman, B. & Bestor, T. H. Dnmt3L and the establishment of maternal genomic imprints. Science 294, 2536–2539 (2001).

    CAS PubMed Google Scholar

  • Weber, M. et al. Distribution, silencing potential and evolutionary impact of promoter DNA methylation in the human genome. Nature Genet. 39, 457–466 (2007).

    CAS PubMed Google Scholar

  • Mohn, F. et al. Lineage-specific polycomb targets and de novo DNA methylation define restriction and potential of neuronal progenitors. Mol. Cell 30, 755–766 (2008). References 13 and 14 present genome-wide DNA methylation maps of pluripotent and differentiated stem cells. They show a link between DNA methylation patterns and histone methylation patterns.

    CAS PubMed Google Scholar

  • Meissner, A. et al. Genome-scale DNA methylation maps of pluripotent and differentiated cells. Nature 454, 766–770 (2008).

    CAS PubMed PubMed Central Google Scholar

  • Okitsu, C. Y. & Hsieh, C. L. DNA methylation dictates histone H3K4 methylation. Mol. Cell. Biol. 27, 2746–2757 (2007).

    CAS PubMed PubMed Central Google Scholar

  • Weber, M. et al. Chromosome-wide and promoter-specific analyses identify sites of differential DNA methylation in normal and transformed human cells. Nature Genet. 37, 853–862 (2005).

    CAS PubMed Google Scholar

  • Gidekel, S. & Bergman, Y. A unique developmental pattern of Oct-3/4 DNA methylation is controlled by a cis-demodification element. J. Biol. Chem. 277, 34521–34530 (2002).

    CAS PubMed Google Scholar

  • Sylvester, I. & Scholer, H. R. Regulation of the Oct-4 gene by nuclear receptors. Nucleic Acids Res. 22, 901–911 (1994).

    CAS PubMed PubMed Central Google Scholar

  • Ben-Shushan, E., Sharir, H., Pikarsky, E. & Bergman, Y. A dynamic balance between ARP-1/COUP-TFII, EAR-3/COUP-TFI, and retinoic acid receptor:retinoid X receptor heterodimers regulates Oct-3/4 expression in embryonal carcinoma cells. Mol. Cell. Biol. 15, 1034–1048 (1995).

    CAS PubMed PubMed Central Google Scholar

  • Fuhrmann, G. et al. Mouse germline restriction of Oct4 expression by germ cell nuclear factor. Dev. Cell 1, 377–387 (2001).

    CAS PubMed Google Scholar

  • Feldman, N. et al. G9a-mediated irreversible epigenetic inactivation of Oct-3/4 during early embryogenesis. Nature Cell Biol. 8, 188–194 (2006). References 21 and 22 show that G9a inactivates early embryonic genes. Histone methylation is shown to block target gene reactivation in the absence of repressors, whereas DNA methylation prevents reprogramming.

    CAS PubMed Google Scholar

  • Epsztejn-Litman, S. et al. De novo DNA methylation promoted by G9a prevents reprogramming of embryonically silenced genes. Nature Struct. Mol. Biol. 15, 1176–1183 (2008).

    CAS Google Scholar

  • Lehnertz, B. et al. Suv39h-mediated histone H3 lysine 9 methylation directs DNA methylation to major satellite repeats at pericentric heterochromatin. Curr. Biol. 13, 1192–1200 (2003).

    CAS PubMed Google Scholar

  • f*cks, F., Hurd, P. J., Deplus, R. & Kouzarides, T. The DNA methyltransferases associate with HP1 and the SUV39H1 histone methyltransferase. Nucleic Acids Res. 31, 2305–2312 (2003).

    CAS PubMed PubMed Central Google Scholar

  • Sugiyama, T., Cam, H., Verdel, A., Moazed, D. & Grewal, S. I. RNA-dependent RNA polymerase is an essential component of a self-enforcing loop coupling heterochromatin assembly to siRNA production. Proc. Natl. Acad. Sci. USA 102, 152–157 (2005).

    CAS PubMed Google Scholar

  • Kanellopoulou, C. et al. Dicer-deficient mouse embryonic stem cells are defective in differentiation and centromeric silencing. Genes Dev. 19, 489–501 (2005).

    CAS PubMed PubMed Central Google Scholar

  • f*ckagawa, T. et al. Dicer is essential for formation of the heterochromatin structure in vertebrate cells. Nature Cell Biol. 6, 784–791 (2004).

    CAS PubMed Google Scholar

  • Malinina, L. Possible involvement of the RNAi pathway in trinucleotide repeat expansion diseases. J. Biomol. Struct. Dyn. 23, 233–235 (2005).

    CAS PubMed Google Scholar

  • Pandey, R. R. et al. Kcnq1ot1 antisense noncoding RNA mediates lineage-specific transcriptional silencing through chromatin-level regulation. Mol. Cell 32, 232–246 (2008).

    CAS PubMed Google Scholar

  • Zhao, J., Sun, B. K., Erwin, J. A., Song, J. J. & Lee, J. T. Polycomb proteins targeted by a short repeat RNA to the mouse X chromosome. Science 322, 750–756 (2008).

    CAS PubMed PubMed Central Google Scholar

  • Nagano, T. et al. The Air noncoding RNA epigenetically silences transcription by targeting G9a to chromatin. Science 322, 1717–1720 (2008).

    CAS PubMed Google Scholar

  • Tamaru, H. & Selker, E. U. A histone H3 methyltransferase controls DNA methylation in Neurospora crassa. Nature 414, 277–283 (2001).

    CAS PubMed Google Scholar

  • Jackson, J. P., Lindroth, A. M., Cao, X. & Jacobsen, S. E. Control of CpNpG DNA methylation by the KRYPTONITE histone H3 methyltransferase. Nature 416, 556–560 (2002). References 32 and 33 were the first studies to report crosstalk between histone methylation and DNA methylation in N. crassa and A. thaliana .

    CAS PubMed Google Scholar

  • Osipovich, O. et al. Targeted inhibition of V(D)J recombination by a histone methyltransferase. Nature Immunol. 5, 309–316 (2004).

    CAS Google Scholar

  • Carlson, L. L., Page, A. W. & Bestor, T. H. Properties and localization of DNA methyltransferase in preimplantation mouse embryos: implications for genomic imprinting. Genes Dev. 6, 2536–2541 (1992).

    CAS PubMed Google Scholar

  • Leonhardt, H., Page, A. W., Weier, H. U. & Bestor, T. H. A targeting sequence directs DNA methyltransferase to sites of DNA replication in mammalian nuclei. Cell 71, 865–873 (1992).

    CAS PubMed Google Scholar

  • Bostick, M. et al. UHRF1 plays a role in maintaining DNA methylation in mammalian cells. Science 317, 1760–1764 (2007). References 37–39 show that UHRF1 contains an SRA domain that binds to hemimethylated CG sites and forms a complex with DNMT1, thus mediating epigenetic inheritance of DNA methylation.

    CAS PubMed Google Scholar

  • Sharif, J. et al. The SRA protein Np95 mediates epigenetic inheritance by recruiting Dnmt1 to methylated DNA. Nature 450, 908–912 (2007).

    CAS PubMed Google Scholar

  • Achour, M. et al. The interaction of the SRA domain of ICBP90 with a novel domain of DNMT1 is involved in the regulation of VEGF gene expression. Oncogene 27, 2187–2197 (2008).

    CAS PubMed Google Scholar

  • Suzuki, M. M. & Bird, A. DNA methylation landscapes: provocative insights from epigenomics. Nature Rev. Genet. 9, 465–476 (2008).

    CAS PubMed Google Scholar

  • Weber, M. & Schubeler, D. Genomic patterns of DNA methylation: targets and function of an epigenetic mark. Curr. Opin. Cell Biol. 19, 273–280 (2007).

    CAS PubMed Google Scholar

  • Eden, S., Hashimshony, T., Keshet, I., Thorne, A. W. & Cedar, H. DNA methylation models histone acetylation. Nature 394, 842–843 (1998).

    CAS PubMed Google Scholar

  • Hashimshony, T., Zhang, J., Keshet, I., Bustin, M. & Cedar, H. The role of DNA methylation in setting up chromatin structure during development. Nature Genet. 34, 187–192 (2003).

    CAS PubMed Google Scholar

  • Nan, X. et al. Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature 393, 386–389 (1998).

    CAS PubMed Google Scholar

  • Jones, P. L. et al. Methylated DNA and MeCP2 recruit histone deacetylase to repress transcription. Nature Genet. 19, 187–191 (1998).

    CAS PubMed Google Scholar

  • Esteve, P. O. et al. Direct interaction between DNMT1 and G9a coordinates DNA and histone methylation during replication. Genes Dev. 20, 3089–3103 (2006).

    CAS PubMed PubMed Central Google Scholar

  • Lande-Diner, L. et al. Role of DNA methylation in stable gene repression. J. Biol. Chem. 282, 12194–12200 (2007).

    CAS PubMed Google Scholar

  • Zilberman, D., Coleman-Derr, D., Ballinger, T. & Henikoff, S. Histone H2A.Z and DNA methylation are mutually antagonistic chromatin marks. Nature 456, 125–129 (2008).

    CAS PubMed PubMed Central Google Scholar

  • Tachibana, M., Matsumura, Y., f*ckuda, M., Kimura, H. & Shinkai, Y. G9a/GLP complexes independently mediate H3K9 and DNA methylation to silence transcription. EMBO J. 27, 2681–2690 (2008). References 49 and 50 show that G9a promotes DNA methylation of retrotransposons and a number of genes in embryonic stem cells independently of its catalytic activity.

    CAS PubMed PubMed Central Google Scholar

  • Dong, K. B. et al. DNA methylation in ES cells requires the lysine methyltransferase G9a but not its catalytic activity. EMBO J. 27, 2691–2701 (2008).

    CAS PubMed PubMed Central Google Scholar

  • Vire, E. et al. The Polycomb group protein EZH2 directly controls DNA methylation. Nature 439, 871–874 (2006).

    CAS PubMed Google Scholar

  • Li, H. et al. The histone methyltransferase SETDB1 and the DNA methyltransferase DNMT3A interact directly and localize to promoters silenced in cancer cells. J. Biol. Chem. 281, 19489–19500 (2006).

    CAS PubMed Google Scholar

  • Smallwood, A., Esteve, P. O., Pradhan, S. & Carey, M. Functional cooperation between HP1 and DNMT1 mediates gene silencing. Genes Dev. 21, 1169–1178 (2007).

    CAS PubMed PubMed Central Google Scholar

  • Freitag, M., Hickey, P. C., Khlafallah, T. K., Read, N. D. & Selker, E. U. HP1 is essential for DNA methylation in Neurospora. Mol. Cell 13, 427–434 (2004).

    CAS PubMed Google Scholar

  • Lande-Diner, L. & Cedar, H. Silence of the genes — mechanisms of long-term repression. Nature Rev. Genet. 6, 648–654 (2005).

    CAS PubMed Google Scholar

  • Schoenherr, C. J. & Anderson, D. J. The neuron-restrictive silencer factor (NRSF): a coordinate repressor of multiple neuron-specific genes. Science 267, 1360–1363 (1995).

    CAS PubMed Google Scholar

  • Franke, A. et al. Polycomb and polyhomeotic are constituents of a multimeric protein complex in chromatin of Drosophila melanogaster. EMBO J. 11, 2941–2950 (1992).

    CAS PubMed PubMed Central Google Scholar

  • Boyer, L. A. et al. Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature 441, 349–353 (2006).

    CAS PubMed Google Scholar

  • Lee, T. I. et al. Control of developmental regulators by polycomb in human embryonic stem cells. Cell 125, 301–313 (2006).

    CAS PubMed PubMed Central Google Scholar

  • Hansen, K. H. et al. A model for transmission of the H3K27me3 epigenetic mark. Nature Cell Biol. 10, 1291–1300 (2008). The authors suggest a mechanism by which H3K27me3 is propagated during the cell division cycle. Once H3K27me3 is established it recruits the PRC2 complex, leading to methylation of histone H3 on the newly synthesized DNA.

    CAS PubMed Google Scholar

  • Hajkova, P. et al. Chromatin dynamics during epigenetic reprogramming in the mouse germ line. Nature 452, 877–881 (2008). This study examines the erasure of parental imprints in mouse primordial germ cells during embryogenesis. The data suggest that DNA demethylation occurs prior to histone replacement, thus supporting a repair model for demethylation.

    CAS PubMed Google Scholar

  • Schwartz, Y. B. & Pirrotta, V. Polycomb complexes and epigenetic states. Curr. Opin. Cell Biol. 20, 266–273 (2008).

    CAS PubMed Google Scholar

  • Pietersen, A. M. & van Lohuizen, M. Stem cell regulation by polycomb repressors: postponing commitment. Curr. Opin. Cell Biol. 20, 201–207 (2008).

    CAS PubMed Google Scholar

  • Bernstein, B. E. et al. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125, 315–326 (2006).

    CAS PubMed Google Scholar

  • Mikkelsen, T. S. et al. Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 448, 553–560 (2007).

    CAS PubMed PubMed Central Google Scholar

  • Pan, G. et al. Whole-genome analysis of histone H3 lysine 4 and lysine 27 methylation in human embryonic stem cells. Cell Stem Cell 1, 299–312 (2007).

    CAS PubMed Google Scholar

  • Zhao, X. D. et al. Whole-genome mapping of histone H3 Lys4 and 27 trimethylations reveals distinct genomic compartments in human embryonic stem cells. Cell Stem Cell 1, 286–298 (2007).

    CAS PubMed Google Scholar

  • Barski, A. et al. High-resolution profiling of histone methylations in the human genome. Cell 129, 823–837 (2007).

    CAS PubMed Google Scholar

  • Hershko, A. Y., Kafri, T., Fainsod, A. & Razin, A. Methylation of HoxA5 and HoxB5 and its relevance to expression during mouse development. Gene 302, 65–72 (2003).

    CAS PubMed Google Scholar

  • Payer, B. & Lee, J. T. X chromosome dosage compensation: how mammals keep the balance. Annu. Rev. Genet. 42, 733–772 (2008).

    CAS PubMed Google Scholar

  • Lock, L. F., Takagi, N. & Martin, G. R. Methylation of the Hprt gene on the inactive X occurs after chromosome inactivation. Cell 48, 39–46 (1987).

    CAS PubMed Google Scholar

  • Samollow, P. B., Robinson, E. S., Ford, A. L. & Vandeberg, J. L. Developmental progression of Gpd expression from the inactive X chromosome of the virginia opossum. Dev. Genet. 16, 367–378 (1995).

    CAS PubMed Google Scholar

  • Migeon, B. R., Jan de Beur, S. & Axelman, J. Frequent derepression of G6PD and HPRT on the marsupial inactive X chromosome associated with cell proliferation in vitro. Exp. Cell Res. 182, 597–609 (1989).

    CAS PubMed Google Scholar

  • Gautsch, J. W. & Wilson, M. C. Delayed de novo methylation in teratocarcinoma suggests additional tissue-specific mechanisms for controlling gene expression. Nature 301, 32–37 (1983).

    CAS PubMed Google Scholar

  • Takahashi, K. & Yamanaka, S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126, 663–676 (2006). This is the first report showing the generation of iPS cells by introduction of four transcription factor genes into somatic cells.

    CAS PubMed Google Scholar

  • Maherali, N. et al. Directly reprogrammed fibroblasts show global epigenetic remodeling and widespread tissue contribution. Cell Stem Cell 1, 55–70 (2007).

    CAS PubMed Google Scholar

  • Wernig, M. et al. In vitro reprogramming of fibroblasts into a pluripotent ES-cell-like state. Nature 448, 318–324 (2007).

    CAS PubMed Google Scholar

  • Welstead, G. G., Schorderet, P. & Boyer, L. A. The reprogramming language of pluripotency. Curr. Opin. Genet. Dev. 18, 123–129 (2008).

    CAS PubMed Google Scholar

  • Mikkelsen, T. S. et al. Dissecting direct reprogramming through integrative genomic analysis. Nature 454, 49–55 (2008). This paper shows that partially reprogrammed cell lines have DNA hypermethylation at pluripotency-related loci. This suggests that DNA demethylation is an inefficient step accomplished late in the transition to pluripotency.

    CAS PubMed PubMed Central Google Scholar

  • Shi, Y. et al. A combined chemical and genetic approach for the generation of induced pluripotent stem cells. Cell Stem Cell 2, 525–528 (2008).

    CAS PubMed Google Scholar

  • Shi, Y. et al. Induction of pluripotent stem cells from mouse embryonic fibroblasts by Oct4 and Klf4 with small-molecule compounds. Cell Stem Cell 3, 568–574 (2008).

    CAS PubMed Google Scholar

  • Ma, D. K., Chiang, C. H., Ponnusamy, K., Ming, G. L. & Song, H. G9a and Jhdm2a regulate embryonic stem cell fusion-induced reprogramming of adult neural stem cells. Stem Cells 26, 2131–2141 (2008).

    CAS PubMed PubMed Central Google Scholar

  • Jones, P. A. & Baylin, S. B. The epigenomics of cancer. Cell 128, 683–692 (2007).

    CAS PubMed PubMed Central Google Scholar

  • De Marzo, A. M. et al. Abnormal regulation of DNA methyltransferase expression during colorectal carcinogenesis. Cancer Res. 59, 3855–3860 (1999).

    CAS PubMed Google Scholar

  • Robertson, K. D. et al. The human DNA methyltransferases (DNMTs) 1, 3a and 3b: coordinate mRNA expression in normal tissues and overexpression in tumors. Nucleic Acids Res. 27, 2291–2298 (1999).

    CAS PubMed PubMed Central Google Scholar

  • Keshet, I. et al. Evidence for an instructive mechanism of de novo methylation in cancer cells. Nature Genet. 38, 149–153 (2006).

    CAS PubMed Google Scholar

  • Schlesinger, Y. et al. Polycomb mediated histone H3(K27) methylation pre-marks genes for de novo methylation in cancer. Nature Genet. 39, 232–236 (2007). References 87–89 show that in cancer cells a large number of CpG islands marked by H3K27me3 undergo de novo methylation, indicating that Polycomb-directed de novo methylation might play an important part in carcinogenesis.

    CAS PubMed Google Scholar

  • Ohm, J. E. et al. A stem cell-like chromatin pattern may predispose tumor suppressor genes to DNA hypermethylation and heritable silencing. Nature Genet. 39, 237–242 (2007).

    CAS PubMed Google Scholar

  • Widschwendter, M. et al. Epigenetic stem cell signature in cancer. Nature Genet. 39, 157–158 (2007).

    CAS PubMed Google Scholar

  • Varambally, S. et al. The polycomb group protein EZH2 is involved in progression of prostate cancer. Nature 419, 624–629 (2002).

    CAS PubMed Google Scholar

  • Varambally, S. et al. Genomic loss of microRNA-101 leads to overexpression of histone methyltransferase EZH2 in cancer. Science 322, 1695–1699 (2008).

    CAS PubMed PubMed Central Google Scholar

  • Benetti, R. et al. A mammalian microRNA cluster controls DNA methylation and telomere recombination via Rbl2-dependent regulation of DNA methyltransferases. Nature Struct. Mol. Biol. 15, 268–279 (2008).

    CAS Google Scholar

  • Sinkkonen, L. et al. MicroRNAs control de novo DNA methylation through regulation of transcriptional repressors in mouse embryonic stem cells. Nature Struct. Mol. Biol. 15, 259–267 (2008).

    CAS Google Scholar

  • Gal-Yam, E. N. et al. Frequent switching of Polycomb repressive marks and DNA hypermethylation in the PC3 prostate cancer cell line. Proc. Natl. Acad. Sci. USA 105, 12979–12984 (2008).

    PubMed PubMed Central Google Scholar

  • McGarvey, K. M., Greene, E., Fahrner, J. A., Jenuwein, T. & Baylin, S. B. DNA methylation and complete transcriptional silencing of cancer genes persist after depletion of EZH2. Cancer Res. 67, 5097–5102 (2007).

    CAS PubMed Google Scholar

  • Lindroth, A. M. et al. Antagonism between DNA and H3K27 methylation at the imprinted Rasgrf1 locus. PLoS Genet. 4, e1000145 (2008).

    PubMed PubMed Central Google Scholar

  • Zhao, Q. et al. PRMT5-mediated methylation of histone H4R3 recruits DNMT3A, coupling histone and DNA methylation in gene silencing. Nature Struct. Mol. Biol. 16, 304–311 (2009).

    CAS Google Scholar

  • Wang, J. et al. The lysine demethylase LSD1 (KDM1) is required for maintenance of global DNA methylation. Nature Genet. 41, 125–129 (2009).

    CAS PubMed Google Scholar

  • Goldmit, M. et al. Epigenetic ontogeny of the κ locus during B cell development. Nature Immunol. 6, 198–203 (2005).

    CAS Google Scholar

  • Loh, Y. H., Zhang, W., Chen, X., George, J. & Ng, H. H. Jmjd1a and Jmjd2c histone H3 Lys 9 demethylases regulate self-renewal in embryonic stem cells. Genes Dev. 21, 2545–2557 (2007).

    CAS PubMed PubMed Central Google Scholar

  • Lan, F., Nottke, A. C. & Shi, Y. Mechanisms involved in the regulation of histone lysine demethylases. Curr. Opin. Cell Biol. 20, 316–325 (2008).

    CAS PubMed PubMed Central Google Scholar

  • Agger, K., Christensen, J., Cloos, P. A. & Helin, K. The emerging functions of histone demethylases. Curr. Opin. Genet. Dev. 18, 159–168 (2008).

    CAS PubMed Google Scholar

  • Paroush, Z., Keshet, I., Yisraeli, J. & Cedar, H. Dynamics of demethylation and activation of the α actin gene in myoblasts. Cell 63, 1229–1237 (1990).

    CAS PubMed Google Scholar

  • Barreto, G. et al. Gadd45a promotes epigenetic gene activation by repair-mediated DNA demethylation. Nature 445, 671–675 (2007). References 104, 105, 107 and 108 show that active DNA demethylation might be accomplished through DNA repair promoted by GADD45.

    CAS PubMed Google Scholar

  • Rai, K. et al. DNA Demethylation in zebrafish involves the coupling of a deaminase, a glycosylase, and Gadd45. Cell 135, 1201–1212 (2008).

    CAS PubMed PubMed Central Google Scholar

  • Weiss, A., Keshet, I., Razin, A. & Cedar, H. DNA demethylation in vitro: involvement of RNA. Cell 86, 709–718 (1996).

    CAS PubMed Google Scholar

  • Schmmitz, K. M. et al. TAF12 recruits Gadd45a and the nucleotide excision repair complex to the promoter of rRNA genes leading to active DNA demethylation. Mol. Cell 33, 344–353 (2009).

    Google Scholar

  • Ma, D. K. et al. Neuronal sctivity-induced Gadd45b promotes epigenetic DNA demethylation and adult neurogenesis. Science 323, 1074–1077 (2009).

    CAS PubMed PubMed Central Google Scholar

  • Linking DNA methylation and histone modification: patterns and paradigms (2024)
    Top Articles
    All Eligible Waitlist Members Now Have a Crypto Wallet - Lightning Network is Coming to Robinhood — Under the Hood
    Promoted Chats, Now on Kik!
    Where To Go After Howling Pit Code Vein
    Maxtrack Live
    Average Jonas Wife
    Research Tome Neltharus
    Is pickleball Betts' next conquest? 'That's my jam'
    Gunshots, panic and then fury - BBC correspondent's account of Trump shooting
    Encore Atlanta Cheer Competition
    State Of Illinois Comptroller Salary Database
    Tiger Island Hunting Club
    Mawal Gameroom Download
    What Was D-Day Weegy
    What Is A Good Estimate For 380 Of 60
    Gino Jennings Live Stream Today
    Download Center | Habasit
    The Largest Banks - ​​How to Transfer Money With Only Card Number and CVV (2024)
    London Ups Store
    Idaho Harvest Statistics
    R Personalfinance
    91 East Freeway Accident Today 2022
    Is The Yankees Game Postponed Tonight
    Japanese Mushrooms: 10 Popular Varieties and Simple Recipes - Japan Travel Guide MATCHA
    Atlases, Cartography, Asia (Collection Dr. Dupuis), Arch…
    Labcorp.leavepro.com
    Yale College Confidential 2027
    Summoners War Update Notes
    Japanese Emoticons Stars
    lol Did he score on me ?
    24 Hour Drive Thru Car Wash Near Me
    Mawal Gameroom Download
    Dl.high Stakes Sweeps Download
    Redding Activity Partners
    Tmj4 Weather Milwaukee
    Newcardapply Com 21961
    Litter-Robot 3 Pinch Contact & DFI Kit
    Lake Dunson Robertson Funeral Home Lagrange Georgia Obituary
    Autozone Locations Near Me
    Craigslist Lakeside Az
    Merkantilismus – Staatslexikon
    Encompass.myisolved
    Dragon Ball Super Super Hero 123Movies
    Noh Buddy
    Rocket Lab hiring Integration & Test Engineer I/II in Long Beach, CA | LinkedIn
    9:00 A.m. Cdt
    Ohio Road Construction Map
    Stitch And Angel Tattoo Black And White
    New Zero Turn Mowers For Sale Near Me
    Motorcycle For Sale In Deep East Texas By Owner
    How To Connect To Rutgers Wifi
    Room For Easels And Canvas Crossword Clue
    Latest Posts
    Article information

    Author: Rob Wisoky

    Last Updated:

    Views: 5781

    Rating: 4.8 / 5 (48 voted)

    Reviews: 87% of readers found this page helpful

    Author information

    Name: Rob Wisoky

    Birthday: 1994-09-30

    Address: 5789 Michel Vista, West Domenic, OR 80464-9452

    Phone: +97313824072371

    Job: Education Orchestrator

    Hobby: Lockpicking, Crocheting, Baton twirling, Video gaming, Jogging, Whittling, Model building

    Introduction: My name is Rob Wisoky, I am a smiling, helpful, encouraging, zealous, energetic, faithful, fantastic person who loves writing and wants to share my knowledge and understanding with you.