Home LiteratureArticle Details
PMID: 17182153 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Epigenetic memory loss in aging oligodendrocytes in the corpus callosum.

Neurobiology of aging ·Vol. 29 ·No. 3 ·2008-03-00 ·Pages 452-63

Shen S, Liu A, Li J, Wolubah C, Casaccia-Bonnefil P

Abstract

In this study, we address the hypothesis that aging modifies the intrinsic properties of oligodendrocytes, the myelin-forming cells of the brain. According to our model, an "epigenetic memory" is stored in the chromatin of the oligodendrocyte lineage cells and is responsible for the maintenance of a mature phenotype, characterized by low levels of expression of transcriptional inhibitors. We report here an age-related decline of histone deacetylation and methylation, the molecular mechanisms responsible for the establishment and maintenance of this "epigenetic memory" of the differentiated state. We further show that lack of histone methylation and increased acetylation in mature oligodendrocytes are associated with global changes in gene expression, that include the re-expression of bHLH inhibitors (i.e. Hes5 and Id4) and precursor markers (i.e. Sox2). These changes characteristic of the "aging" oligodendrocytes can be recapitulated in vitro, by treating primary oligodendrocyte cultures with histone deacetylase inhibitors. Thus, we conclude that the "epigenetic memory loss" detected in white matter tracts of older mice induces global changes of gene expression that modify the intrinsic properties of aged oligodendrocytes and may functionally modulate the responsiveness of these cells to external stimuli.

MeSH Terms
Age Factors Aging/physiology Animals Animals, Newborn Autophagy-Related Proteins Cells, Cultured Cerebral Cortex/cytology Corpus Callosum/cytology DNA-Binding Proteins/metabolism Female Gene Expression Regulation/physiology Histone Deacetylases/metabolism Intracellular Signaling Peptides and Proteins/metabolism Male Mice Mice, Inbred C57BL Oligodendroglia/physiology Rats SOXB1 Transcription Factors Stem Cells/drug effects,physiology Trans-Activators/metabolism
Chemicals
Autophagy-Related Proteins DNA-Binding Proteins Intracellular Signaling Peptides and Proteins Rb1cc1 protein, mouse SOXB1 Transcription Factors Sox2 protein, mouse Sox2 protein, rat Trans-Activators Histone Deacetylases
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Shen Siming
Department Neuroscience and Cell Biology, Robert Wood Johnson Medical School, UMDNJ, Piscataway, NJ 08854, USA.
Liu Aixiao
Li Jiadong
Wolubah Candy
Casaccia-Bonnefil Patrizia
References (41)
41 references, click to expand
  1. Control of transcription through intragenic patterns of nucleosome composition.
    Cell. 2005 Dec 29;123(7):1187-90 PMID: 16377560
  2. Combinatorial profiles of oligodendrocyte-selective classes of transcriptional regulators differentially modulate myelin basic protein gene expression.
    J Neurosci. 2005 Sep 7;25(36):8311-21 PMID: 16148239
  3. Cellular memory and dynamic regulation of polycomb group proteins.
    Curr Opin Cell Biol. 2006 Jun;18(3):275-83 PMID: 16650749
  4. Multiple roles of Id4 in developmental myelination: predicted outcomes and unexpected findings.
    Glia. 2006 Sep;54(4):285-96 PMID: 16862533
  5. Identifying regulatory mechanisms using individual variation reveals key role for chromatin modification.
    Proc Natl Acad Sci U S A. 2006 Sep 19;103(38):14062-7 PMID: 16968785
  6. A molecular insight of Hes5-dependent inhibition of myelin gene expression: old partners and new players.
    EMBO J. 2006 Oct 18;25(20):4833-42 PMID: 17006542
  7. Microtubule deacetylases, SirT2 and HDAC6, in the nervous system.
    Neurochem Res. 2007 Feb;32(2):187-95 PMID: 16933150
  8. Remembering the cell fate during cellular differentiation.
    J Cell Biochem. 2005 Dec 1;96(5):962-70 PMID: 16187292
  9. Sir2 links chromatin silencing, metabolism, and aging.
    Genes Dev. 2000 May 1;14(9):1021-6 PMID: 10809662
  10. Delayed changes in growth factor gene expression during slow remyelination in the CNS of aged rats.
    Mol Cell Neurosci. 2000 Nov;16(5):542-56 PMID: 11083917
  11. Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins.
    Nature. 2001 Mar 1;410(6824):116-20 PMID: 11242053
  12. Role of histone H3 lysine 9 methylation in epigenetic control of heterochromatin assembly.
    Science. 2001 Apr 6;292(5514):110-3 PMID: 11283354
  13. CREB-binding protein and p300 in transcriptional regulation.
    J Biol Chem. 2001 Apr 27;276(17):13505-8 PMID: 11279224
  14. Linking global histone acetylation to the transcription enhancement of X-chromosomal genes in Drosophila males.
    J Biol Chem. 2001 Aug 24;276(34):31483-6 PMID: 11445559
  15. Methylation of histone H3 at Lys-9 is an early mark on the X chromosome during X inactivation.
    Cell. 2001 Dec 14;107(6):727-38 PMID: 11747809
  16. Increasing local levels of IGF-I mRNA expression using adenoviral vectors does not alter oligodendrocyte remyelination in the CNS of aged rats.
    Mol Cell Neurosci. 2002 Jan;19(1):32-42 PMID: 11817896
  17. The age-related decrease in CNS remyelination efficiency is attributable to an impairment of both oligodendrocyte progenitor recruitment and differentiation.
    J Neurosci. 2002 Apr 1;22(7):2451-9 PMID: 11923409
  18. The human silent information regulator (Sir)2 homologue hSIRT3 is a mitochondrial nicotinamide adenine dinucleotide-dependent deacetylase.
    J Cell Biol. 2002 Aug 19;158(4):647-57 PMID: 12186850
  19. Growth factor treatment promotes mobilization of young but not aged adult subventricular zone precursors in response to demyelination.
    J Neurosci Res. 2002 Sep 15;69(6):763-71 PMID: 12205670
  20. Transcriptional inhibition of genes with severe histone h3 hypoacetylation in the coding region.
    Mol Cell. 2002 Oct;10(4):925-33 PMID: 12419235
  21. Histone deacetylase activity is necessary for oligodendrocyte lineage progression.
    J Neurosci. 2002 Dec 1;22(23):10333-45 PMID: 12451133
  22. Histone deacetylases (HDACs): characterization of the classical HDAC family.
    Biochem J. 2003 Mar 15;370(Pt 3):737-49 PMID: 12429021
  23. Maintenance of chromatin states: an open-and-shut case.
    Curr Opin Cell Biol. 2003 Jun;15(3):266-74 PMID: 12787767
  24. Aging, progenitor cell exhaustion, and atherosclerosis.
    Circulation. 2003 Jul 29;108(4):457-63 PMID: 12860902
  25. Longevity regulation in Saccharomyces cerevisiae: linking metabolism, genome stability, and heterochromatin.
    Microbiol Mol Biol Rev. 2003 Sep;67(3):376-99, table of contents PMID: 12966141
  26. Decline in rate of colonization of oligodendrocyte progenitor cell (OPC)-depleted tissue by adult OPCs with age.
    J Neuropathol Exp Neurol. 2003 Sep;62(9):908-16 PMID: 14533780
  27. Increasing local levels of neuregulin (glial growth factor-2) by direct infusion into areas of demyelination does not alter remyelination in the rat CNS.
    Eur J Neurosci. 2003 Oct;18(8):2253-64 PMID: 14622186
  28. Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue.
    J Cell Biol. 1980 Jun;85(3):890-902 PMID: 6248568
  29. Chromatin as an essential part of the transcriptional mechanism.
    Nature. 1992 Jan 16;355(6357):219-24 PMID: 1731219
  30. Wound healing and aging.
    Dermatol Clin. 1993 Oct;11(4):749-57 PMID: 8222358
  31. Aging of the human eye lens--a morphological point of view.
    Comp Biochem Physiol A Physiol. 1995 Aug;111(4):519-32 PMID: 7671147
  32. The effects of ageing on cutaneous wound healing in mammals.
    J Anat. 1995 Aug;187 ( Pt 1):1-26 PMID: 7591970
  33. Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex.
    Nature. 1998 May 28;393(6683):386-9 PMID: 9620804
  34. Remyelination occurs as extensively but more slowly in old rats compared to young rats following gliotoxin-induced CNS demyelination.
    Glia. 1999 Oct;28(1):77-83 PMID: 10498825
  35. Chromatin remodeling and histone modification in the conversion of oligodendrocyte precursors to neural stem cells.
    Genes Dev. 2004 Dec 1;18(23):2963-72 PMID: 15574597
  36. Age-related loss of skeletal muscle function; impairment of gene expression.
    J Musculoskelet Neuronal Interact. 2004 Jun;4(2):143-7 PMID: 15615114
  37. Expression of stathmin, a developmentally controlled cytoskeleton-regulating molecule, in demyelinating disorders.
    J Neurosci. 2005 Jan 19;25(3):737-47 PMID: 15659612
  38. Impaired progenitor cell activity in age-related endothelial dysfunction.
    J Am Coll Cardiol. 2005 May 3;45(9):1441-8 PMID: 15862416
  39. Histone modifications affect timing of oligodendrocyte progenitor differentiation in the developing rat brain.
    J Cell Biol. 2005 May 23;169(4):577-89 PMID: 15897262
  40. Stroke-induced neurogenesis in aged brain.
    Stroke. 2005 Aug;36(8):1790-5 PMID: 16002766
  41. Histone deacetylase 1 is essential for oligodendrocyte specification in the zebrafish CNS.
    Mech Dev. 2006 Jan;123(1):24-30 PMID: 16324829
Article Info
Journal
Neurobiology of aging
Abbr.
Neurobiol Aging
ISSN
1558-1497
Published
2008-03-00
Epub
2006-00-19
Pages
452-63
Language
English
Region
United States
NLM ID
8100437
PMCID
PMC2323437
Subset
IM
Grants
NINDS NIH HHS · R01 NS042925 · United States
NINDS NIH HHS · R01 NS042925-05A1 · United States
NINDS NIH HHS · R01-NS42925 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com