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Post-Translational Modifications of Nucleosomal Histones in Oligodendrocyte Lineage Cells in Development and Disease

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Abstract

The role of epigenetics in modulating gene expression in the development of organs and tissues and in disease states is becoming increasingly evident. Epigenetics refers to the several mechanisms modulating inheritable changes in gene expression that are independent of modifications of the primary DNA sequence and include post-translational modifications of nucleosomal histones, changes in DNA methylation, and the role of microRNA. This review focuses on the epigenetic regulation of gene expression in oligodendroglial lineage cells. The biological effects that post-translational modifications of critical residues in the N-terminal tails of nucleosomal histones have on oligodendroglial cells are reviewed, and the implications for disease and repair are critically discussed.

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References

  • Aguirre, A. A., Chittajallu, R., Belachew, S., & Gallo, V. (2004). NG2-expressing cells in the subventricular zone are type C-like cells and contribute to interneuron generation in the postnatal hippocampus. Journal of Cell Biology, 165, 575–589.

    PubMed  CAS  Google Scholar 

  • Anand, R., & Marmorstein, R. (2007). Structure and mechanism of lysine specific demethylase enzymes. Journal of Biological Chemistry (in press)

  • Andres, M. E., Burger, C., Peral-Rubio, M. J., Battaglioli, E., Anderson, M. E., & Grimes, J. (1999). CoREST: A functional corepressor required for regulation of neural-specific gene expression. Proceedings of the National Academy of Sciences of the United States of America, 96, 9873–9878.

    PubMed  CAS  Google Scholar 

  • Ashraf, S. I., & Ip, Y. T. (1998). Transcriptional control: Repression by local chromatin modification. Current Biology, 8, R683–686.

    PubMed  CAS  Google Scholar 

  • Asklund, T., Appelskog, I. B., Ammerpohl, O., Ekstrom, T. J., & Almqvist, P. M. (2004). Histone deacetylase inhibitor 4-phenylbutyrate modulates glial fibrillary acidic protein and connexin 43 expression, and enhances gap-junction communication, in human glioblastoma cells. European Journal of Cancer, 40, 1073–1081.

    PubMed  CAS  Google Scholar 

  • Ballas, N., Battaglioli, E., Atouf, F., Andres, M. E., Chenoweth, J., Anderson, M. E., et al. (2001). Regulation of neuronal traits by a novel transcriptional complex. Neuron, 31, 353–365.

    PubMed  CAS  Google Scholar 

  • Bannister, A. J., & Kouzarides, T. (2005). Reversing histone methylation. Nature, 436, 1103–1106.

    PubMed  CAS  Google Scholar 

  • Bannister, A. J., Schneider, R., & Kouzarides, T. (2002). Histone methylation: Dynamic or static? Cell, 109, 801–806.

    PubMed  CAS  Google Scholar 

  • Bansal, R., & Pfeiffer, S. E. (1997). FGF-2 converts mature oligodendrocytes to a novel phenotype. Journal of Neuroscience Research, 50, 215–228.

    PubMed  CAS  Google Scholar 

  • Bauer, U. M., Daujat, S., Nielsen, S. J., Nightingale, K., & Kouzarides, T. (2002). Methylation at arginine 17 of histone H3 is linked to gene activation. EMBO Reports, 3, 39–44.

    PubMed  CAS  Google Scholar 

  • Bedford, M. T., & Richard, S. (2005). Arginine methylation an emerging regulator of protein function. Molecular Cell, 18, 263–272.

    PubMed  CAS  Google Scholar 

  • Belachew, S., Chittajallu, R., Aguirre, A. A., Yuan, X., Kirby, M., Anderson, S., et al. (2003). Postnatal NG2 proteoglycan-expressing progenitor cells are intrinsically multipotent and generate functional neurons. Journal of Cell Biology, 161, 169–186.

    PubMed  CAS  Google Scholar 

  • Berger, S. L. (2002). Histone modifications in transcriptional regulation. Current Opinion in G0enetics & Development, 12, 142–148.

    CAS  Google Scholar 

  • Bird, A. (2007). Perceptions of epigenetics. Nature, 447, 396–398.

    PubMed  CAS  Google Scholar 

  • Bird, A. P., & Wolffe, A. P. (1999). Methylation-induced repression—belts, braces, and chromatin. Cell, 99, 451–454.

    PubMed  CAS  Google Scholar 

  • Boisvert, F. M., Chenard, C. A., & Richard, S. (2005). Protein interfaces in signaling regulated by arginine methylation. Sci STKE, 2005(271), re2.

    PubMed  Google Scholar 

  • Bonni, A., Sun, Y., Nadal-Vicens, M., Bhatt, A., Frank, D. A., Rozovsky, I., et al. (1997). Regulation of gliogenesis in the central nervous system by the JAK-STAT signaling pathway. Science, 278, 477–483.

    PubMed  CAS  Google Scholar 

  • Camelo, S., Iglesias, A. H., Hwang, D., Due, B., Ryu, H., Smith, K., et al. (2005). Transcriptional therapy with the histone deacetylase inhibitor trichostatin A ameliorates experimental autoimmune encephalomyelitis. Journal of Neuroimmunology, 164, 10–21.

    PubMed  CAS  Google Scholar 

  • Cao, X., Yeo, G., Muotri, A. R., Kuwabara, T., & Gage, F. H. (2006). Noncoding RNAs in the mammalian central nervous system. Annual Review of Neuroscience, 29, 77–103.

    PubMed  CAS  Google Scholar 

  • Casaccia-Bonnefil, P., Hardy, R. J., Teng, K. K., Levine, J. M., Koff, A., & Chao, M. V. (1999). Loss of p27Kip1 function results in increased proliferative capacity of oligodendrocyte progenitors but unaltered timing of differentiation. Development, 126, 4027–4037.

    PubMed  CAS  Google Scholar 

  • Casaccia-Bonnefil, P., Tikoo, R., Kiyokawa, H., Friedrich Jr., V., Chao, M. V., & Koff, A. (1997). Oligodendrocyte precursor differentiation is perturbed in the absence of the cyclin-dependent kinase inhibitor p27Kip1. Genes & Development, 11, 2335–2346.

    CAS  Google Scholar 

  • Chen, D., Ma, H., Hong, H., Koh, S. S., Huang, S. M., Schurter, B. T., et al. (1999). Regulation of transcription by a protein methyltransferase. Science, 284, 2174–2177.

    PubMed  CAS  Google Scholar 

  • Cheng, L. C., Tavazoie, M., & Doetsch, F. (2005). Stem cells: From epigenetics to microRNAs. Neuron, 46, 363–367.

    PubMed  CAS  Google Scholar 

  • Cheung, W. L., Briggs, S. D., & Allis, C. D. (2000). Acetylation and chromosomal functions. Current Opinion in Cell Biology, 12, 326–333.

    PubMed  CAS  Google Scholar 

  • Cunliffe, V. T., & Casaccia-Bonnefil, P. (2006). Histone deacetylase 1 is essential for oligodendrocyte specification in the zebrafish CNS. Mechanisms of Development, 123, 24–30.

    PubMed  CAS  Google Scholar 

  • Davie, J. K., & Dent, S. Y. (2002). Transcriptional control: an activating role for arginine methylation. Current Biology, 12, R59–R61.

    PubMed  CAS  Google Scholar 

  • de Ruijter, A. J., van Gennip, A. H., Caron, H. N., Kemp, S., & van Kuilenburg, A. B. (2003). Histone deacetylases (HDACs): characterization of the classical HDAC family. Biochemical Journal, 370, 737–749.

    PubMed  Google Scholar 

  • Denman, R. B. (2005). PAD: the smoking gun behind arginine methylation signaling? Bioessays, 27, 242–246.

    PubMed  CAS  Google Scholar 

  • Dugas, J. C., Ibrahim, A., & Barres, B. A. (2007). A crucial role for p57(Kip2) in the intracellular timer that controls oligodendrocyte differentiation. Journal of Neuroscience, 27, 6185–6196.

    PubMed  CAS  Google Scholar 

  • Durand, B., Fero, M. L., Roberts, J. M., & Raff, M. C. (1998). p27Kip1 alters the response of cells to mitogen and is part of a cell-intrinsic timer that arrests the cell cycle and initiates differentiation. Current Biology, 8, 431–440.

    PubMed  CAS  Google Scholar 

  • Durand, B., & Raff, M. (2000). A cell-intrinsic timer that operates during oligodendrocyte development. Bioessays, 22, 64–71.

    PubMed  CAS  Google Scholar 

  • Dutnall, R. N., & Ramakrishnan, V. (1997). Twists and turns of the nucleosome: tails without ends. Structure, 5, 1255–1259.

    PubMed  CAS  Google Scholar 

  • Fancy, S. P., Zhao, C., & Franklin, R. J. (2004). Increased expression of Nkx2.2 and Olig2 identifies reactive oligodendrocyte progenitor cells responding to demyelination in the adult CNS. Molecular and Cellular Neurosciences, 27, 247–254.

    PubMed  CAS  Google Scholar 

  • Feng, J., Chang, H., Li, E., & Fan, G. (2005). Dynamic expression of de novo DNA methyltransferases Dnmt3a and Dnmt3b in the central nervous system. Journal of neuroscience research, 79, 734–746.

    PubMed  CAS  Google Scholar 

  • Feng, J., Fouse, S., & Fan, G. (2007). Epigenetic regulation of neural gene expression and neuronal function. Pediatric Research, 61, 58R–63R.

    PubMed  CAS  Google Scholar 

  • Fukuda, S., & Taga, T. (2005). Cell fate determination regulated by a transcriptional signal network in the developing mouse brain. Anat Sci Int, 80, 12–18.

    PubMed  CAS  Google Scholar 

  • Gard, A. L., & Pfeiffer, S. E. (1993). Glial cell mitogens bFGF and PDGF differentially regulate development of O4  GalC-oligodendrocyte progenitors. Developments in Biologicals, 159, 618–630.

    CAS  Google Scholar 

  • Ghiani, C. A., Eisen, A. M., Yuan, X., DePinho, R. A., McBain, C. J., & Gallo, V. (1999). Neurotransmitter receptor activation triggers p27(Kip1)and p21(CIP1) accumulation and G1 cell cycle arrest in oligodendrocyte progenitors. Development, 126, 1077–1090.

    PubMed  CAS  Google Scholar 

  • Goll, M. G., & Bestor, T. H. (2002). Histone modification and replacement in chromatin activation. Genes & Development, 16, 1739–1742.

    CAS  Google Scholar 

  • Gottschling, D. E. (2006). DNA repair: corrections in the golden years. Current Biology, 16, R956–R958.

    PubMed  CAS  Google Scholar 

  • Graham, V., Khudyakov, J., Ellis, P., & Pevny, L. (2003). SOX2 functions to maintain neural progenitor identity. Neuron, 39, 749–765.

    PubMed  CAS  Google Scholar 

  • Grunstein, M. (1997). Histone acetylation in chromatin structure and transcription. Nature, 389, 349–352.

    PubMed  CAS  Google Scholar 

  • Guillemot, F. (1995). Analysis of the role of basic-helix-loop-helix transcription factors in the development of neural lineages in the mouse. Biology of the Cell, 84, 3–6.

    PubMed  CAS  Google Scholar 

  • Hao, Y., Creson, T., Zhang, L., Li, P., Du, F., Yuan, P., et al. (2004). Mood stabilizer valproate promotes ERK pathway-dependent cortical neuronal growth and neurogenesis. Journal of Neuroscience, 24, 6590–6599.

    PubMed  CAS  Google Scholar 

  • He, Y., Dupree, J., Wang, J., Sandoval, J., Li, J., Liu, H., et al. (2007). The transcription factor Yin Yang 1 is essential for oligodendrocyte progenitor differentiation. Neuron, 55, 217–230.

    PubMed  CAS  Google Scholar 

  • Horio, Y., Hisahara, S., & Sakamoto, J. (2003). Functional analysis of SIR2. Nippon Yakurigaku Zasshi, 122(Suppl), 30P–32P.

    PubMed  Google Scholar 

  • Hsieh, J., Nakashima, K., Kuwabara, T., Mejia, E., & Gage, F. H. (2004). Histone deacetylase inhibition-mediated neuronal differentiation of multipotent adult neural progenitor cells. Proceedings of the National Academy of Sciences of the United States of America, 101, 16659–16664.

    PubMed  CAS  Google Scholar 

  • Huang, Y., Myers, S. J., & Dingledine, R. (1999). Transcriptional repression by REST: Recruitment of Sin3A and histone deacetylase to neuronal genes. Nature Neuroscience, 2, 867–872.

    PubMed  CAS  Google Scholar 

  • Imai, S., Armstrong, C. M., Kaeberlein, M., & Guarente, L. (2000). Transcriptional silencing and longevity protein Sir2 is an NAD-dependent histone deacetylase. Nature, 403, 795–800.

    PubMed  CAS  Google Scholar 

  • John, G. R., Shankar, S. L., Shafit-Zagardo, B., Massimi, A., Lee, S. C., Raine, C. S., et al. (2002). Multiple sclerosis: Re-expression of a developmental pathway that restricts oligodendrocyte maturation. Natural Medicines, 8, 1115–1121.

    CAS  Google Scholar 

  • Kageyama, R., Ohtsuka, T., Hatakeyama, J., & Ohsawa, R. (2005). Roles of bHLH genes in neural stem cell differentiation. Exp Cell Res, 306, 343–348.

    PubMed  CAS  Google Scholar 

  • Klose, R. J., & Zhang, Y. (2007). Regulation of histone methylation by demethylimination and demethylation. Nature Reviews. Molecular Cell Biology, 8, 307–318.

    PubMed  CAS  Google Scholar 

  • Kondo, T., & Raff, M. (2000a). Basic helix-loop-helix proteins and the timing of oligodendrocyte differentiation. Development, 127, 2989–2998.

    PubMed  CAS  Google Scholar 

  • Kondo, T., & Raff, M. (2000b). The Id4 HLH protein and the timing of oligodendrocyte differentiation. EMBO Journal, 19, 1998–2007.

    PubMed  CAS  Google Scholar 

  • Kondo, T., & Raff, M. (2000c). Oligodendrocyte precursor cells reprogrammed to become multipotential CNS stem cells. Science, 289, 1754–1757.

    PubMed  CAS  Google Scholar 

  • Kondo, T., & Raff, M. (2004). Chromatin remodeling and histone modification in the conversion of oligodendrocyte precursors to neural stem cells. Genes & Development, 18, 2963–2972.

    CAS  Google Scholar 

  • Kouzarides, T. (2002). Histone methylation in transcriptional control. Current Opinion in Genetics & Development, 12, 198–209.

    CAS  Google Scholar 

  • Kozik, M. B. (1976). The electron-microscopic picture of postnatal development of oligodendroglia. Folia Histochemica et Cytochemica (Krakow), 14, 99–106.

    CAS  Google Scholar 

  • Kubicek, S., & Jenuwein, T. (2004). A crack in histone lysine methylation. Cell, 119, 903–906.

    PubMed  CAS  Google Scholar 

  • Kuhlbrodt, K., Herbarth, B., Sock, E., Enderich, J., Hermans-Borgmeyer, I., & Wegner, M. (1998). Cooperative function of POU proteins and SOX proteins in glial cells. Journal of Biological Chemistry, 273, 16050–16057.

    PubMed  CAS  Google Scholar 

  • Kuo, M. H., & Allis, C. D. (1998). Roles of histone acetyltransferases and deacetylases in gene regulation. Bioessays, 20, 615–626.

    PubMed  CAS  Google Scholar 

  • Lachner, M., & Jenuwein, T. (2002). The many faces of histone lysine methylation. Current Opinion in Cell Biology, 14, 286–298.

    PubMed  CAS  Google Scholar 

  • Larocque, D., Galarneau, A., Liu, H. N., Scott, M., Almazan, G., & Richard, S. (2005). Protection of p27(Kip1) mRNA by quaking RNA binding proteins promotes oligodendrocyte differentiation. Nature Neuroscience, 8, 27–33.

    PubMed  CAS  Google Scholar 

  • Li, W., Zhang, B., Tang, J., Cao, Q., Wu, Y., Wu, C., et al. (2007). Sirtuin 2, a mammalian homolog of yeast silent information regulator-2 longevity regulator, is an oligodendroglial protein that decelerates cell differentiation through deacetylating alpha-tubulin. Nature Neuroscience, 27, 2606–2616.

    Google Scholar 

  • Liu, A., Han, Y. R., Li, J., Sun, D., Ouyang, M., Plummer, M. R., et al. (2007). The glial or neuronal fate choice of oligodendrocyte progenitors is modulated by their ability to acquire an epigenetic memory. Journal of Neuroscience, 27, 7339–7343.

    PubMed  CAS  Google Scholar 

  • Liu, A., Li, J., Marin-Husstege, M., Kageyama, R., Fan, Y., Gelinas, C., et al. (2006). A molecular insight of Hes5-dependent inhibition of myelin gene expression: old partners and new players. EMBO Journal, 25, 4833–4842.

    PubMed  CAS  Google Scholar 

  • Liu, A., Muggironi, M., Marin-Husstege, M., & Casaccia-Bonnefil, P. (2003). Oligodendrocyte process outgrowth in vitro is modulated by epigenetic regulation of cytoskeletal severing proteins. Glia, 44, 264–274.

    PubMed  Google Scholar 

  • Liu, A., Stadelmann, C., Moscarello, M., Bruck, W., Sobel, A., Mastronardi, F. G., et al. (2005). Expression of stathmin, a developmentally controlled cytoskeleton-regulating molecule, in demyelinating disorders. Journal of Neuroscience, 25, 737–747.

    PubMed  CAS  Google Scholar 

  • Lyssiotis, C. A., Walker, J., Wu, C., Kondo, T., Schultz, P. G., & Wu, X. (2007). Inhibition of histone deacetylase activity induces developmental plasticity in oligodendrocyte precursor cells. Proceedings of the National Academy of Sciences of the United States of America, 104, 14982–14987.

    PubMed  CAS  Google Scholar 

  • Magnaghi-Jaulin, L., Ait-Si-Ali, S., & Harel-Bellan, A. (1999). Histone acetylation in signal transduction by growth regulatory signals. Seminars in Cell & Developmental Biology, 10, 197–203.

    CAS  Google Scholar 

  • Marin-Husstege, M., He, Y., Li, J., Kondo, T., Sablitzky, F., & Casaccia-Bonnefil, P. (2006). Multiple roles of Id4 in developmental myelination: Predicted outcomes and unexpected findings. Glia, 54, 285–296.

    PubMed  Google Scholar 

  • Marin-Husstege, M., Muggironi, M., Liu, A., & Casaccia-Bonnefil, P. (2002). Histone deacetylase activity is necessary for oligodendrocyte lineage progression. Journal of neuroscience, 22, 10333–10345.

    PubMed  CAS  Google Scholar 

  • Mastronardi, F. G., daCruz, L. A., Wang, H., Boggs, J., & Moscarello, M. A. (2003). The amount of sonic hedgehog in multiple sclerosis white matter is decreased and cleavage to the signaling peptide is deficient. Multiple Sclerosis, 9, 362–371.

    PubMed  CAS  Google Scholar 

  • Mastronardi, F. G., Wood, D. D., Mei, J., Raijmakers, R., Tseveleki, V., Dosch, H. M., et al. (2006). Increased citrullination of histone H3 in multiple sclerosis brain and animal models of demyelination: A role for tumor necrosis factor-induced peptidylarginine deiminase 4 translocation. Journal of Neuroscience, 26, 11387–11396.

    PubMed  CAS  Google Scholar 

  • Mehler, M. F., & Mattick, J. S. (2006). Non-coding RNAs in the nervous system. Journal of Physiology, 575, 333–341.

    PubMed  CAS  Google Scholar 

  • Mehler, M. F., & Mattick, J. S. (2007). Noncoding RNAs and RNA editing in brain development, functional diversification, and neurological disease. Physiological Reviews, 87, 799–823.

    PubMed  CAS  Google Scholar 

  • Miskimins, R., Srinivasan, R., Marin-Husstege, M., Miskimins, W. K., & Casaccia-Bonnefil, P. (2002). p27(Kip1) enhances myelin basic protein gene promoter activity. Journal of Neuroscience Research, 67, 100–105.

    PubMed  CAS  Google Scholar 

  • Nakashima, K., Yanagisawa, M., Arakawa, H., Kimura, N., Hisatsune, T., Kawabata, M., et al. (1999). Synergistic signaling in fetal brain by STAT3-Smad1 complex bridged by p300. Science, 284, 479–482.

    PubMed  CAS  Google Scholar 

  • Naruse, Y., Aoki, T., Kojima, T., & Mori, N. (1999). Neural restrictive silencer factor recruits mSin3 and histone deacetylase complex to repress neuron-specific target genes. Proceedings of the National Academy of Sciences of the United States of America, 96, 13691–13696.

    PubMed  CAS  Google Scholar 

  • Natarajan, C., & Bright, J. J. (2002). Curcumin inhibits experimental allergic encephalomyelitis by blocking IL-12 signaling through Janus kinase-STAT pathway in T lymphocytes. Journal of Immunology, 168, 6506–6513.

    CAS  Google Scholar 

  • Nishiyama, A. (2007). Polydendrocytes: NG2 cells with many roles in development and repair of the CNS. Neuroscientist, 13, 62–76.

    PubMed  CAS  Google Scholar 

  • Noble, M., & Murray, K. (1984). Purified astrocytes promote the in vitro division of a bipotential glial progenitor cell. EMBO Journal, 3, 2243–2247.

    PubMed  CAS  Google Scholar 

  • Pahlich, S., Zakaryan, R. P., & Gehring, H. (2006). Protein arginine methylation: Cellular functions and methods of analysis. Biochimica et Biophysica Bcta, 1764, 1890–1903.

    CAS  Google Scholar 

  • Pal, S., Vishwanath, S. N., Erdjument-Bromage, H., Tempst, P., & Sif, S. (2004). Human SWI/SNF-associated PRMT5 methylates histone H3 arginine 8 and negatively regulates expression of ST7 and NM23 tumor suppressor genes. Molecular and Cellular Biology, 24, 9630–9645.

    PubMed  CAS  Google Scholar 

  • Rice, J. C., & Allis, C. D. (2001). Histone methylation versus histone acetylation: New insights into epigenetic regulation. Current Opinion in Cell Biology, 13, 263–273.

    PubMed  CAS  Google Scholar 

  • Richards, E. J. (2002). Chromatin methylation: Who’s on first? Current Biology, 12, R694–695.

    PubMed  CAS  Google Scholar 

  • Romm, E., Nielsen, J. A., Kim, J. G., & Hudson, L. D. (2005). Myt1 family recruits histone deacetylase to regulate neural transcription. Journal of Neurochemistry, 93, 1444–1453.

    PubMed  CAS  Google Scholar 

  • Roopra, A., Sharling, L., Wood, I. C., Briggs, T., Bachfischer, U., Paquette, A. J., et al. (2000). Transcriptional repression by neuron-restrictive silencer factor is mediated via the Sin3-histone deacetylase complex. Molecular and Cellular Biology, 20, 2147–2157.

    PubMed  CAS  Google Scholar 

  • Sakamoto, M., Hirata, H., Ohtsuka, T., Bessho, Y., & Kageyama, R. (2003). The basic helix-loop-helix genes Hesr1/Hey1 and Hesr2/Hey2 regulate maintenance of neural precursor cells in the brain. Journal of Biological Chemistry, 278, 44808–44815.

    PubMed  CAS  Google Scholar 

  • Samanta, J., & Kessler, J. A. (2004). Interactions between ID and OLIG proteins mediate the inhibitory effects of BMP4 on oligodendroglial differentiation. Development, 131, 4131–4142.

    PubMed  CAS  Google Scholar 

  • Shen, S., Li, J., & Casaccia-Bonnefil, P. (2005). Histone modifications affect timing of oligodendrocyte progenitor differentiation in the developing rat brain. Journal of Cell Biology, 169, 577–589.

    PubMed  CAS  Google Scholar 

  • Shen, S., Liu, A., Li, J., Wolubah, C., & Casaccia-Bonnefil, P. (2007). Epigenetic memory loss in aging oligodendrocytes in the corpus callosum. Neurobiology of Aging (in press)

  • Sohn, J., Natale, J., Chew, L. J., Belachew, S., Cheng, Y., Aguirre, A., et al. (2006). Identification of Sox17 as a transcription factor that regulates oligodendrocyte development. Journal of Neuroscience, 26, 9722–9735.

    PubMed  CAS  Google Scholar 

  • Song, M. R., & Ghosh, A. (2004). FGF2-induced chromatin remodeling regulates CNTF-mediated gene expression and astrocyte differentiation. Nature Neuroscience, 7, 229–235.

    PubMed  Google Scholar 

  • Southwood, C. M., Peppi, M., Dryden, S., Tainsky, M. A., & Gow, A. (2007). Microtubule deacetylases, SirT2 and HDAC6, in the nervous system. Neurochemical Research, 32, 187–195.

    PubMed  CAS  Google Scholar 

  • Spencer, V. A., & Davie, J. R. (1999). Role of covalent modifications of histones in regulating gene expression. Gene, 240, 1–12.

    PubMed  CAS  Google Scholar 

  • Spencer, V. A., & Davie, J. R. (2000). Signal transduction pathways and chromatin structure in cancer cells. Journal of Cellular Biochemistry. Supplement, 35, 27–35.

    Article  PubMed  Google Scholar 

  • Stavropoulos, P., & Hoelz, A. (2007). Lysine-specific demethylase 1 as a potential therapeutic target. Expert Opinion on Therapeutic Targets, 11, 809–820.

    PubMed  CAS  Google Scholar 

  • Stidworthy, M. F., Genoud, S., Li, W. W., Leone, D. P., Mantei, N., Suter, U., et al. (2004). Notch1 and Jagged1 are expressed after CNS demyelination, but are not a major rate-determining factor during remyelination. Brain, 127, 1928–1941.

    PubMed  Google Scholar 

  • Strahl, B. D., Briggs, S. D., Brame, C. J., Caldwell, J. A., Koh, S. S., Ma, H., et al. (2001). Methylation of histone H4 at arginine 3 occurs in vivo and is mediated by the nuclear receptor coactivator PRMT1. Current Biology, 11, 996–1000.

    PubMed  CAS  Google Scholar 

  • Struhl, K. (1998). Histone acetylation and transcriptional regulatory mechanisms. Genes & Development, 12, 599–606.

    CAS  Google Scholar 

  • Takeuchi, T., Watanabe, Y., Takano-Shimizu, T., & Kondo, S. (2006). Roles of jumonji and jumonji family genes in chromatin regulation and development. Developmental Dynamics, 235, 2449–2459.

    PubMed  CAS  Google Scholar 

  • Takizawa, T., Nakashima, K., Namihira, M., Ochiai, W., Uemura, A., Yanagisawa, M., et al. (2001). DNA methylation is a critical cell-intrinsic determinant of astrocyte differentiation in the fetal brain. Developmental Cell, 1, 749–758.

    PubMed  CAS  Google Scholar 

  • Tang, X. M., Beesley, J. S., Grinspan, J. B., Seth, P., Kamholz, J., & Cambi, F. (1999). Cell cycle arrest induced by ectopic expression of p27 is not sufficient to promote oligodendrocyte differentiation. Journal of Cellular Biochemistry, 76, 270–279.

    PubMed  CAS  Google Scholar 

  • Tanny, J. C., Dowd, G. J., Huang, J., Hilz, H., & Moazed, D. (1999). An enzymatic activity in the yeast Sir2 protein that is essential for gene silencing. Cell, 99, 735–745.

    PubMed  CAS  Google Scholar 

  • Taylor, C. M., Marta, C. B., Claycomb, R. J., Han, D. K., Rasband, M. N., Coetzee, T., & Pfeiffer, S. E. (2004). Proteomic mapping provides powerful insights into functional myelin biology. Proceedings of the National Academy of Sciences of the United States of America, 101, 4643–4648.

    PubMed  CAS  Google Scholar 

  • Temple, S., & Raff, M. C. (1985). Differentiation of a bipotential glial progenitor cell in a single cell microculture. Nature, 313, 223–225.

    PubMed  CAS  Google Scholar 

  • Teter, B., Osterburg, H. H., Anderson, C. P., & Finch, C. E. (1994). Methylation of the rat glial fibrillary acidic protein gene shows tissue-specific domains. Journal of Neuroscience Research, 39, 680–693.

    PubMed  CAS  Google Scholar 

  • Thompson, P. R., & Fast, W. (2006). Histone citrullination by protein arginine deiminase: Is arginine methylation a green light or a roadblock? ACS Chem Biol, 1, 433–441.

    PubMed  CAS  Google Scholar 

  • Thomson, S., Clayton, A. L., Hazzalin, C. A., Rose, S., Barratt, M. J., & Mahadevan, L. C. (1999). The nucleosomal response associated with immediate-early gene induction is mediated via alternative MAP kinase cascades: MSK1 as a potential histone H3/HMG-14 kinase. EMBO Journal, 18, 4779–4793.

    PubMed  CAS  Google Scholar 

  • Tikoo, R., Osterhout, D. J., Casaccia-Bonnefil, P., Seth, P., Koff, A., & Chao, M. V. (1998). Ectopic expression of p27Kip1 in oligodendrocyte progenitor cells results in cell-cycle growth arrest. Journal of Neurobiology, 36, 431–440.

    PubMed  CAS  Google Scholar 

  • Tokumoto, Y. M., Apperly, J. A., Gao, F. B., & Raff, M. C. (2002). Posttranscriptional regulation of p18 and p27 Cdk inhibitor proteins and the timing of oligodendrocyte differentiation. Developments in Biologicals, 245, 224–234.

    Article  CAS  Google Scholar 

  • Turner, B. M. (2000). Histone acetylation and an epigenetic code. Bioessays, 22, 836–845.

    PubMed  CAS  Google Scholar 

  • Tyler, J. K., & Kadonaga, J. T. (1999). The “dark side” of chromatin remodeling: Repressive effects on transcription. Cell, 99, 443–446.

    PubMed  CAS  Google Scholar 

  • Vanrobaeys, F., Van Coster, R., Dhondt, G., Devreese, B., & Van Beeumen, J. (2005). Profiling of myelin proteins by 2D-gel electrophoresis and multidimensional liquid chromatography coupled to MALDI TOF-TOF mass spectrometry. J Proteome Res, 4, 2283–2293.

    PubMed  CAS  Google Scholar 

  • Vidali, G., Ferrari, N., & Pfeffer, U. (1988). Histone acetylation: A step in gene activation. Advances in Experimental Medicine and Biology, 231, 583–596.

    PubMed  CAS  Google Scholar 

  • Wang, H., Huang, Z. Q., Xia, L., Feng, Q., Erdjument-Bromage, H., Strahl, B. D., et al. (2001a). Methylation of histone H4 at arginine 3 facilitating transcriptional activation by nuclear hormone receptor. Science, 293, 853–857.

    PubMed  CAS  Google Scholar 

  • Wang, S., Sdrulla, A., Johnson, J. E., Yokota, Y., & Barres, B. A. (2001b). A role for the helix-loop-helix protein Id2 in the control of oligodendrocyte development. Neuron, 29, 603–614.

    PubMed  CAS  Google Scholar 

  • Wang, Y., Wysocka, J., Sayegh, J., Lee, Y. H., Perlin, J. R., Leonelli, L., et al. (2004). Human PAD4 regulates histone arginine methylation levels via demethylimination. Science, 306, 279–283.

    PubMed  CAS  Google Scholar 

  • Wei, Q., Miskimins, W. K., & Miskimins, R. (2005). Stage-specific expression of myelin basic protein in oligodendrocytes involves Nkx2.2-mediated repression that is relieved by the Sp1 transcription factor. Advances in Experimental Medicine and Biology, 280, 16284–16294.

    CAS  Google Scholar 

  • Werner, H. B., Kuhlmann, K., Shen, S., Uecker, M., Schardt, A., Dimova, K., et al. (2007). Proteolipid protein is required for transport of sirtuin 2 into CNS myelin. Journal of Neuroscience, 27, 7717–7730.

    PubMed  CAS  Google Scholar 

  • Wilson, J. R. (2007). Targeting the JMJD2A histone lysine demethylase. Nature Structural and Molecular Biology, 14, 682–684.

    PubMed  CAS  Google Scholar 

  • Wolffe, A. P. (1996). Histone deacetylase: a regulator of transcription. Science, 272, 371–372.

    PubMed  CAS  Google Scholar 

  • Wysocka, J., Allis, C. D., & Coonrod, S. (2006). Histone arginine methylation and its dynamic regulation. Frontiers in Bioscience, 11, 344–355.

    PubMed  CAS  Google Scholar 

  • Wysocka, J., Milne, T. A., & Allis, C. D. (2005). Taking LSD 1 to a new high. Cell, 122, 654–658.

    PubMed  CAS  Google Scholar 

  • Zhang, Y., & Reinberg, D. (2001). Transcription regulation by histone methylation: Interplay between different covalent modifications of the core histone tails. Genes & Development, 15, 2343–2360.

    CAS  Google Scholar 

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Acknowledgment

Partially supported by grants from NIH-NINDS (RO1NS042925 and RO1 052738) and from the National Multiple Sclerosis Society (NMSS3957) to P.C.B. We thank Dr. Juan Sandoval for the help with the graphic illustrations.

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Correspondence to Patrizia Casaccia-Bonnefil.

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Shen, S., Casaccia-Bonnefil, P. Post-Translational Modifications of Nucleosomal Histones in Oligodendrocyte Lineage Cells in Development and Disease. J Mol Neurosci 35, 13–22 (2008). https://doi.org/10.1007/s12031-007-9014-x

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  • DOI: https://doi.org/10.1007/s12031-007-9014-x

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