Home LiteratureArticle Details
PMID: 16148239 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Combinatorial profiles of oligodendrocyte-selective classes of transcriptional regulators differentially modulate myelin basic protein gene expression.

Gokhan S, Marin-Husstege M, Yung SY, Fontanez D, Casaccia-Bonnefil P, Mehler MF

Abstract

Recent studies suggest that specific neural basic helix-loop-helix (HLH; i.e., Olig1 and Olig2, Mash1), associated inhibitory HLH (i.e., Id2 and Id4), high-mobility group domain (i.e., Sox10), and homeodomain (i.e., Nkx2.2) transcription factors are involved in oligodendrocyte (OL) lineage specification and progressive stages of maturation including myelination. However, the developmental interplay among these lineage-selective determinants, in a cell- and maturational stage-specific context, has not yet been defined. We show here in vivo and in vitro developmental expression profiles for these distinct classes of transcriptional regulators of OLs. We show that progressive stages of OL lineage maturation are characterized by dynamic changes in the subcellular distribution of these transcription factors and by different permutations of combinatorial transcriptional codes. Transient transfections of these precise combinatorial codes with a luciferase reporter gene driven by the myelin basic protein promoter define how changes in the molecular composition of these transcriptional complexes modulate myelin gene expression. Our overall findings suggest that the dynamic interplay between developmental stage-specific classes of transcriptional activators and associated inhibitory factors orchestrate myelin gene expression during terminal maturation of the mammalian CNS.

MeSH Terms
3T3 Cells Animals Animals, Newborn Culture Media Gene Expression Regulation/drug effects Genes, Reporter Homeobox Protein Nkx-2.2 Luciferases/genetics Mice Myelin Basic Protein/genetics Neuroglia/physiology Neurons/physiology Oligodendroglia/drug effects,physiology Platelet-Derived Growth Factor/pharmacology Prosencephalon/physiology Trans-Activators/metabolism Transcription, Genetic
Chemicals
Culture Media Homeobox Protein Nkx-2.2 Myelin Basic Protein Nkx2-2 protein, mouse Platelet-Derived Growth Factor Trans-Activators Luciferases
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Gokhan Solen
Institute for Brain Disorders and Neural Regeneration, Albert Einstein College of Medicine, Bronx, New York 10461, USA.
Marin-Husstege Mireya
Yung Shau Yu
Fontanez Darah
Casaccia-Bonnefil Patrizia
Mehler Mark F
References (45)
45 references, click to expand
  1. From head to toes: the multiple facets of Sox proteins.
    Nucleic Acids Res. 1999 Mar 15;27(6):1409-20 PMID: 10037800
  2. Sonic hedgehog and BMP2 exert opposing actions on proliferation and differentiation of embryonic neural progenitor cells.
    Dev Biol. 1999 Nov 1;215(1):118-29 PMID: 10525354
  3. A cell-intrinsic timer that operates during oligodendrocyte development.
    Bioessays. 2000 Jan;22(1):64-71 PMID: 10649292
  4. Developmental changes in progenitor cell responsiveness to bone morphogenetic proteins differentially modulate progressive CNS lineage fate.
    Dev Neurosci. 2000;22(1-2):74-85 PMID: 10657700
  5. Musashi1: an evolutionally conserved marker for CNS progenitor cells including neural stem cells.
    Dev Neurosci. 2000;22(1-2):139-53 PMID: 10657706
  6. The Id4 HLH protein and the timing of oligodendrocyte differentiation.
    EMBO J. 2000 May 2;19(9):1998-2007 PMID: 10790366
  7. Specific protein-protein interaction between basic helix-loop-helix transcription factors and homeoproteins of the Pitx family.
    Mol Cell Biol. 2000 Jul;20(13):4826-37 PMID: 10848608
  8. Basic helix-loop-helix proteins and the timing of oligodendrocyte differentiation.
    Development. 2000 Jul;127(14):2989-98 PMID: 10862737
  9. Sonic hedgehog signaling at gastrula stages specifies ventral telencephalic cells in the chick embryo.
    Development. 2000 Aug;127(15):3283-93 PMID: 10887084
  10. Oligodendrocyte precursor cells reprogrammed to become multipotential CNS stem cells.
    Science. 2000 Sep 8;289(5485):1754-7 PMID: 10976069
  11. ID helix-loop-helix proteins in cell growth, differentiation and tumorigenesis.
    J Cell Sci. 2000 Nov;113 ( Pt 22):3897-905 PMID: 11058077
  12. Notch1 and Notch3 instructively restrict bFGF-responsive multipotent neural progenitor cells to an astroglial fate.
    Neuron. 2001 Jan;29(1):45-55 PMID: 11182080
  13. A role for the helix-loop-helix protein Id2 in the control of oligodendrocyte development.
    Neuron. 2001 Mar;29(3):603-14 PMID: 11301021
  14. The neural RNA-binding protein Musashi1 translationally regulates mammalian numb gene expression by interacting with its mRNA.
    Mol Cell Biol. 2001 Jun;21(12):3888-900 PMID: 11359897
  15. Oligodendrocyte development in the spinal cord and telencephalon: common themes and new perspectives.
    Int J Dev Neurosci. 2001 Jul;19(4):379-85 PMID: 11378298
  16. Control of oligodendrocyte differentiation by the Nkx2.2 homeodomain transcription factor.
    Development. 2001 Jul;128(14):2723-33 PMID: 11526078
  17. Olig bHLH proteins interact with homeodomain proteins to regulate cell fate acquisition in progenitors of the ventral neural tube.
    Curr Biol. 2001 Sep 18;11(18):1413-20 PMID: 11566099
  18. Ventral neurogenesis and the neuron-glial switch.
    Neuron. 2001 Sep 13;31(5):677-80 PMID: 11567609
  19. Combinatorial roles of olig2 and neurogenin2 in the coordinated induction of pan-neuronal and subtype-specific properties of motoneurons.
    Neuron. 2001 Sep 13;31(5):757-71 PMID: 11567615
  20. Coordinate regulation of motor neuron subtype identity and pan-neuronal properties by the bHLH repressor Olig2.
    Neuron. 2001 Sep 13;31(5):773-89 PMID: 11567616
  21. Sonic hedgehog is required during an early phase of oligodendrocyte development in mammalian brain.
    Mol Cell Neurosci. 2001 Oct;18(4):434-41 PMID: 11640898
  22. Multipotent stem cells from the mouse basal forebrain contribute GABAergic neurons and oligodendrocytes to the cerebral cortex during embryogenesis.
    J Neurosci. 2001 Nov 15;21(22):8854-62 PMID: 11698597
  23. p27(Kip1) enhances myelin basic protein gene promoter activity.
    J Neurosci Res. 2002 Jan 1;67(1):100-5 PMID: 11754085
  24. Terminal differentiation of myelin-forming oligodendrocytes depends on the transcription factor Sox10.
    Genes Dev. 2002 Jan 15;16(2):165-70 PMID: 11799060
  25. The bHLH transcription factors OLIG2 and OLIG1 couple neuronal and glial subtype specification.
    Cell. 2002 Apr 5;109(1):61-73 PMID: 11955447
  26. Common developmental requirement for Olig function indicates a motor neuron/oligodendrocyte connection.
    Cell. 2002 Apr 5;109(1):75-86 PMID: 11955448
  27. Mechanisms regulating lineage diversity during mammalian cerebral cortical neurogenesis and gliogenesis.
    Results Probl Cell Differ. 2002;39:27-52 PMID: 12357985
  28. Histone deacetylase activity is necessary for oligodendrocyte lineage progression.
    J Neurosci. 2002 Dec 1;22(23):10333-45 PMID: 12451133
  29. Differential modulation of BMP signaling promotes the elaboration of cerebral cortical GABAergic neurons or oligodendrocytes from a common sonic hedgehog-responsive ventral forebrain progenitor species.
    Proc Natl Acad Sci U S A. 2002 Dec 10;99(25):16273-8 PMID: 12461181
  30. Basic helix-loop-helix factors in cortical development.
    Neuron. 2003 Jul 3;39(1):13-25 PMID: 12848929
  31. Evidence for a second wave of oligodendrogenesis in the postnatal cerebral cortex of the mouse.
    J Neurosci Res. 2003 Sep 1;73(5):581-92 PMID: 12929126
  32. Cross-repressive interaction of the Olig2 and Nkx2.2 transcription factors in developing neural tube associated with formation of a specific physical complex.
    J Neurosci. 2003 Oct 22;23(29):9547-56 PMID: 14573534
  33. Oligodendrocyte process outgrowth in vitro is modulated by epigenetic regulation of cytoskeletal severing proteins.
    Glia. 2003 Dec;44(3):264-74 PMID: 14603467
  34. Transcription factors Sox8 and Sox10 perform non-equivalent roles during oligodendrocyte development despite functional redundancy.
    Development. 2004 May;131(10):2349-58 PMID: 15102707
  35. Interactions between ID and OLIG proteins mediate the inhibitory effects of BMP4 on oligodendroglial differentiation.
    Development. 2004 Sep;131(17):4131-42 PMID: 15280210
  36. Expression of stathmin, a developmentally controlled cytoskeleton-regulating molecule, in demyelinating disorders.
    J Neurosci. 2005 Jan 19;25(3):737-47 PMID: 15659612
  37. Stage-specific expression of myelin basic protein in oligodendrocytes involves Nkx2.2-mediated repression that is relieved by the Sp1 transcription factor.
    J Biol Chem. 2005 Apr 22;280(16):16284-94 PMID: 15695521
  38. 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
  39. Lines of murine oligodendroglial precursor cells immortalized by an activated neu tyrosine kinase show distinct degrees of interaction with axons in vitro and in vivo.
    Eur J Neurosci. 1995 Jun 1;7(6):1245-65 PMID: 7582098
  40. Architectural transcription factors.
    Science. 1994 May 20;264(5162):1100-1 PMID: 8178167
  41. Sox-4, an Sry-like HMG box protein, is a transcriptional activator in lymphocytes.
    EMBO J. 1993 Oct;12(10):3847-54 PMID: 8404853
  42. Architectural transcription factors: proteins that remodel DNA.
    Cell. 1997 Mar 21;88(6):733-6 PMID: 9118214
  43. Pax6 controls progenitor cell identity and neuronal fate in response to graded Shh signaling.
    Cell. 1997 Jul 11;90(1):169-80 PMID: 9230312
  44. Differentiation of oligodendroglial progenitors derived from cortical multipotent cells requires extrinsic signals including activation of gp130/LIFbeta receptors.
    J Neurosci. 1998 Dec 1;18(23):9800-11 PMID: 9822739
  45. Isolation and developmental characterization of cerebral cortical multipotent progenitors.
    Dev Biol. 1998 Dec 15;204(2):577-91 PMID: 9882491
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
1529-2401
Published
2005-09-07
Pages
8311-21
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6725536
Subset
IM
Grants
NINDS NIH HHS · R01 NS042925 · United States
NIGMS NIH HHS · GM55145 · United States
NINDS NIH HHS · NS38902 · United States
NINDS NIH HHS · NS42925 · United States
NIGMS NIH HHS · R25 GM055145 · United States
NINDS NIH HHS · R37 NS042925 · United States
NIMH NIH HHS · MH66290 · United States
NIMH NIH HHS · R01 MH066290 · United States
NINDS NIH HHS · R01 NS038902 · 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