Home LiteratureArticle Details
PMID: 15574597 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Chromatin remodeling and histone modification in the conversion of oligodendrocyte precursors to neural stem cells.

Genes & development ·Vol. 18 ·No. 23 ·2004-12-01 ·Pages 2963-72

Kondo T, Raff M

Abstract

We showed previously that purified rat oligodendrocyte precursor cells (OPCs) can be induced by extracellular signals to convert to multipotent neural stem-like cells (NSLCs), which can then generate both neurons and glial cells. Because the conversion of precursor cells to stem-like cells is of both intellectual and practical interest, it is important to understand its molecular basis. We show here that the conversion of OPCs to NSLCs depends on the reactivation of the sox2 gene, which in turn depends on the recruitment of the tumor suppressor protein Brca1 and the chromatin-remodeling protein Brahma (Brm) to an enhancer in the sox2 promoter. Moreover, we show that the conversion is associated with the modification of Lys 4 and Lys 9 of histone H3 at the same enhancer. Our findings suggest that the conversion of OPCs to NSLCs depends on progressive chromatin remodeling, mediated in part by Brca1 and Brm.

MeSH Terms
Animals Base Sequence Cell Differentiation Cell Proliferation Chromatin/metabolism DNA Primers Histones/metabolism Immunohistochemistry Immunoprecipitation Oligodendroglia/cytology RNA, Messenger/genetics Rats Reverse Transcriptase Polymerase Chain Reaction Stem Cells/cytology
Chemicals
Chromatin DNA Primers Histones RNA, Messenger
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Kondo Toru
Medical Research Council Laboratory for Molecular Cell Biology, Cell Biology Unit, University College London, London WC1E 6BT, United Kingdom. tk294@cam.ac.uk
Raff Martin
References (62)
62 references, click to expand
  1. A multidrug resistance transporter from human MCF-7 breast cancer cells.
    Proc Natl Acad Sci U S A. 1998 Dec 22;95(26):15665-70 PMID: 9861027
  2. The developmental pattern of Brca1 expression implies a role in differentiation of the breast and other tissues.
    Nat Genet. 1995 Sep;11(1):17-26 PMID: 7550308
  3. The activity of mammalian brm/SNF2alpha is dependent on a high-mobility-group protein I/Y-like DNA binding domain.
    Mol Cell Biol. 1999 Jun;19(6):3931-9 PMID: 10330133
  4. Neurofilament functions in health and disease.
    Curr Opin Neurobiol. 1999 Oct;9(5):554-60 PMID: 10508735
  5. Sonic hedgehog--regulated oligodendrocyte lineage genes encoding bHLH proteins in the mammalian central nervous system.
    Neuron. 2000 Feb;25(2):317-29 PMID: 10719888
  6. Identification of a novel family of oligodendrocyte lineage-specific basic helix-loop-helix transcription factors.
    Neuron. 2000 Feb;25(2):331-43 PMID: 10719889
  7. A method to identify cDNAs based on localization of green fluorescent protein fusion products.
    Proc Natl Acad Sci U S A. 2000 Mar 28;97(7):3062-6 PMID: 10716735
  8. Isolation, characterization, and differential expression of the murine Sox-2 promoter.
    Gene. 2000 Apr 4;246(1-2):383-93 PMID: 10767561
  9. The Id4 HLH protein and the timing of oligodendrocyte differentiation.
    EMBO J. 2000 May 2;19(9):1998-2007 PMID: 10790366
  10. Sox2 regulatory sequences direct expression of a (beta)-geo transgene to telencephalic neural stem cells and precursors of the mouse embryo, revealing regionalization of gene expression in CNS stem cells.
    Development. 2000 Jun;127(11):2367-82 PMID: 10804179
  11. Basic helix-loop-helix proteins and the timing of oligodendrocyte differentiation.
    Development. 2000 Jul;127(14):2989-98 PMID: 10862737
  12. BRCA1 is associated with a human SWI/SNF-related complex: linking chromatin remodeling to breast cancer.
    Cell. 2000 Jul 21;102(2):257-65 PMID: 10943845
  13. Oligodendrocyte precursor cells reprogrammed to become multipotential CNS stem cells.
    Science. 2000 Sep 8;289(5485):1754-7 PMID: 10976069
  14. The tumor suppressor gene Brca1 is required for embryonic cellular proliferation in the mouse.
    Cell. 1996 Jun 28;85(7):1009-23 PMID: 8674108
  15. Inactivation of the mouse Brca1 gene leads to failure in the morphogenesis of the egg cylinder in early postimplantation development.
    Genes Dev. 1996 Jul 15;10(14):1835-43 PMID: 8698242
  16. Bone morphogenetic proteins induce astroglial differentiation of oligodendroglial-astroglial progenitor cells.
    J Neurosci. 1997 Jun 1;17(11):4112-20 PMID: 9151728
  17. ras transformation is associated with decreased expression of the brm/SNF2alpha ATPase from the mammalian SWI-SNF complex.
    EMBO J. 1998 Jan 2;17(1):223-31 PMID: 9427756
  18. Generation of purified neural precursors from embryonic stem cells by lineage selection.
    Curr Biol. 1998 Aug 27;8(17):971-4 PMID: 9742400
  19. Active remodeling of somatic nuclei in egg cytoplasm by the nucleosomal ATPase ISWI.
    Science. 2000 Sep 29;289(5488):2360-2 PMID: 11009424
  20. Dynamic expression of basic helix-loop-helix Olig family members: implication of Olig2 in neuron and oligodendrocyte differentiation and identification of a new member, Olig3.
    Mech Dev. 2000 Dec;99(1-2):143-8 PMID: 11091082
  21. Cofactor dynamics and sufficiency in estrogen receptor-regulated transcription.
    Cell. 2000 Dec 8;103(6):843-52 PMID: 11136970
  22. Correlation between histone lysine methylation and developmental changes at the chicken beta-globin locus.
    Science. 2001 Sep 28;293(5539):2453-5 PMID: 11498546
  23. 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
  24. LeX/ssea-1 is expressed by adult mouse CNS stem cells, identifying them as nonependymal.
    Neuron. 2002 Aug 29;35(5):865-75 PMID: 12372282
  25. Corepressor-dependent silencing of chromosomal regions encoding neuronal genes.
    Science. 2002 Nov 29;298(5599):1747-52 PMID: 12399542
  26. EGF converts transit-amplifying neurogenic precursors in the adult brain into multipotent stem cells.
    Neuron. 2002 Dec 19;36(6):1021-34 PMID: 12495619
  27. Multipotent cell lineages in early mouse development depend on SOX2 function.
    Genes Dev. 2003 Jan 1;17(1):126-40 PMID: 12514105
  28. Tumor suppressor gene BRCA-1 is expressed by embryonic and adult neural stem cells and involved in cell proliferation.
    J Neurosci Res. 2003 Mar 15;71(6):769-76 PMID: 12605402
  29. Transcriptional specificity of human SWI/SNF BRG1 and BRM chromatin remodeling complexes.
    Mol Cell. 2003 Feb;11(2):377-89 PMID: 12620226
  30. Identification and isolation of multipotential neural progenitor cells from the subcortical white matter of the adult human brain.
    Nat Med. 2003 Apr;9(4):439-47 PMID: 12627226
  31. Functional analysis of chicken Sox2 enhancers highlights an array of diverse regulatory elements that are conserved in mammals.
    Dev Cell. 2003 Apr;4(4):509-19 PMID: 12689590
  32. Postnatal NG2 proteoglycan-expressing progenitor cells are intrinsically multipotent and generate functional neurons.
    J Cell Biol. 2003 Apr 14;161(1):169-86 PMID: 12682089
  33. SOX2 functions to maintain neural progenitor identity.
    Neuron. 2003 Aug 28;39(5):749-65 PMID: 12948443
  34. NG2-expressing glial progenitor cells: an abundant and widespread population of cycling cells in the adult rat CNS.
    Mol Cell Neurosci. 2003 Oct;24(2):476-88 PMID: 14572468
  35. Vertebrate neurogenesis is counteracted by Sox1-3 activity.
    Nat Neurosci. 2003 Nov;6(11):1162-8 PMID: 14517545
  36. Negative regulatory effect of an oligodendrocytic bHLH factor OLIG2 on the astrocytic differentiation pathway.
    Cell Death Differ. 2004 Feb;11(2):196-202 PMID: 14576772
  37. Persistence of a small subpopulation of cancer stem-like cells in the C6 glioma cell line.
    Proc Natl Acad Sci U S A. 2004 Jan 20;101(3):781-6 PMID: 14711994
  38. A role for Noggin in the development of oligodendrocyte precursor cells.
    Dev Biol. 2004 Mar 1;267(1):242-51 PMID: 14975730
  39. FGF2-induced chromatin remodeling regulates CNTF-mediated gene expression and astrocyte differentiation.
    Nat Neurosci. 2004 Mar;7(3):229-35 PMID: 14770186
  40. Localization of the glial fibrillary acidic protein in astrocytes by immunofluorescence.
    Brain Res. 1972 Aug 25;43(2):429-35 PMID: 4559710
  41. Galactocerebroside is a specific cell-surface antigenic marker for oligodendrocytes in culture.
    Nature. 1978 Aug 24;274(5673):813-6 PMID: 355894
  42. Monoclonal antibody to a plasma membrane antigen of neurons.
    Proc Natl Acad Sci U S A. 1979 Oct;76(10):4913-7 PMID: 388422
  43. A glial progenitor cell that develops in vitro into an astrocyte or an oligodendrocyte depending on culture medium.
    Nature. 1983 Jun 2-8;303(5916):390-6 PMID: 6304520
  44. Detection of human white cell proliferative responses by immunoenzymatic measurement of bromodeoxyuridine uptake.
    J Immunol Methods. 1988 Jan 21;106(1):95-100 PMID: 3276790
  45. CNS stem cells express a new class of intermediate filament protein.
    Cell. 1990 Feb 23;60(4):585-95 PMID: 1689217
  46. The protein Id: a negative regulator of helix-loop-helix DNA binding proteins.
    Cell. 1990 Apr 6;61(1):49-59 PMID: 2156629
  47. A gene mapping to the sex-determining region of the mouse Y chromosome is a member of a novel family of embryonically expressed genes.
    Nature. 1990 Jul 19;346(6281):245-50 PMID: 2374589
  48. An Id-related helix-loop-helix protein encoded by a growth factor-inducible gene.
    Proc Natl Acad Sci U S A. 1991 Mar 1;88(5):1815-9 PMID: 2000388
  49. Identification of cooperating oncogenes in E mu-myc transgenic mice by provirus tagging.
    Cell. 1991 May 31;65(5):737-52 PMID: 1904008
  50. Id proteins Id1 and Id2 selectively inhibit DNA binding by one class of helix-loop-helix proteins.
    Mol Cell Biol. 1991 Nov;11(11):5603-11 PMID: 1922066
  51. A human Id-like helix-loop-helix protein expressed during early development.
    Proc Natl Acad Sci U S A. 1992 Feb 15;89(4):1512-6 PMID: 1741406
  52. The persistent expression of a highly polysialylated NCAM in the dentate gyrus of the adult rat.
    Neurosci Res. 1991 Dec;12(4):503-13 PMID: 1665554
  53. Cell death and control of cell survival in the oligodendrocyte lineage.
    Cell. 1992 Jul 10;70(1):31-46 PMID: 1623522
  54. Molecular characterization of a rat negative regulator with a basic helix-loop-helix structure predominantly expressed in the developing nervous system.
    J Biol Chem. 1992 Oct 25;267(30):21879-85 PMID: 1400497
  55. A human homologue of Saccharomyces cerevisiae SNF2/SWI2 and Drosophila brm genes potentiates transcriptional activation by the glucocorticoid receptor.
    EMBO J. 1993 Nov;12(11):4279-90 PMID: 8223438
  56. Two mammalian helix-loop-helix factors structurally related to Drosophila hairy and Enhancer of split.
    Genes Dev. 1992 Dec;6(12B):2620-34 PMID: 1340473
  57. The expression pattern of Id4, a novel dominant negative helix-loop-helix protein, is distinct from Id1, Id2 and Id3.
    Nucleic Acids Res. 1994 Mar 11;22(5):749-55 PMID: 8139914
  58. Control of oligodendrocyte number in the developing rat optic nerve.
    Neuron. 1994 May;12(5):935-42 PMID: 8185952
  59. A novel role for thyroid hormone, glucocorticoids and retinoic acid in timing oligodendrocyte development.
    Development. 1994 May;120(5):1097-108 PMID: 8026323
  60. Musashi, a neural RNA-binding protein required for Drosophila adult external sensory organ development.
    Neuron. 1994 Jul;13(1):67-81 PMID: 8043282
  61. A strong candidate for the breast and ovarian cancer susceptibility gene BRCA1.
    Science. 1994 Oct 7;266(5182):66-71 PMID: 7545954
  62. Synergistic signaling in fetal brain by STAT3-Smad1 complex bridged by p300.
    Science. 1999 Apr 16;284(5413):479-82 PMID: 10205054
Article Info
Journal
Genes & development
Abbr.
Genes Dev
ISSN
0890-9369
Published
2004-12-01
Pages
2963-72
Language
English
Region
United States
NLM ID
8711660
PMCID
PMC534656
Subset
IM
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