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Coordinated control of oligodendrocyte development by extrinsic and intrinsic signaling cues

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Abstract

Oligodendrocytes, the myelin-forming cells for axon ensheathment in the central nervous system, are critical for maximizing and maintaining the conduction velocity of nerve impulses and proper brain function. Demyelination caused by injury or disease together with failure of myelin regeneration disrupts the rapid propagation of action potentials along nerve fibers, and is associated with acquired and inherited disorders, including devastating multiple sclerosis and leukodystrophies. The molecular mechanisms of oligodendrocyte myelination and remyelination remain poorly understood. Recently, a series of signaling pathways including Shh, Notch, BMP and Wnt signaling and their intracellular effectors such as Olig1/2, Hes1/5, Smads and TCFs, have been shown to play important roles in regulating oligodendrocyte development and myelination. In this review, we summarize our recent understanding of how these signaling pathways modulate the progression of oligodendrocyte specification and differentiation in a spatiotemporally-specific manner. A better understanding of the complex but coordinated function of extracellular signals and intracellular determinants during oligodendrocyte development will help to devise effective strategies to promote myelin repair for patients with demyelinating diseases.

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References

  1. Trapp BD, Peterson J, Ransohoff RM, Rudick R, Mork S, Bo L. Axonal transection in the lesions of multiple sclerosis. N Engl J Med 1998, 338: 278–285.

    Article  PubMed  CAS  Google Scholar 

  2. Reindl M, Knipping G, Wicher I, Dilitz E, Egg R, Deisenhammer F, et al. Increased intrathecal production of apolipoprotein D in multiple sclerosis. J Neuroimmunol 2001, 119: 327–332.

    Article  PubMed  CAS  Google Scholar 

  3. Pfeiffer SE, Warrington AE, Bansal R. The oligodendrocyte and its many cellular processes. Trends Cell Biol 1993, 3: 191–197.

    Article  PubMed  CAS  Google Scholar 

  4. Marti E, Bumcrot DA, Takada R, McMahon AP. Requirement of 19K form of Sonic hedgehog for induction of distinct ventral cell types in CNS explants. Nature 1995, 375: 322–325.

    Article  PubMed  CAS  Google Scholar 

  5. Poncet C, Soula C, Trousse F, Kan P, Hirsinger E, Pourquie O, et al. Induction of oligodendrocyte progenitors in the trunk neural tube by ventralizing signals: effects of notochord and floor plate grafts, and of sonic hedgehog. Mech Dev 1996, 60: 13–32.

    Article  PubMed  CAS  Google Scholar 

  6. Pringle NP, Yu WP, Guthrie S, Roelink H, Lumsden A, Peterson AC, et al. Determination of neuroepithelial cell fate: induction of the oligodendrocyte lineage by ventral midline cells and sonic hedgehog. Dev Biol 1996, 177: 30–42.

    Article  PubMed  CAS  Google Scholar 

  7. Orentas DM, Hayes JE, Dyer KL, Miller RH. Sonic hedgehog signaling is required during the appearance of spinal cord oligodendrocyte precursors. Development 1999, 126: 2419–2429.

    PubMed  CAS  Google Scholar 

  8. Lu QR, Yuk D, Alberta JA, Zhu Z, Pawlitzky I, Chan J, et al. Sonic hedgehog—regulated oligodendrocyte lineage genes encoding bHLH proteins in the mammalian central nervous system. Neuron 2000, 25: 317–329.

    Article  PubMed  CAS  Google Scholar 

  9. Zhou Q, Wang S, Anderson DJ. Identification of a novel family of oligodendrocyte lineage-specific basic helix-loop-helix transcription factors. Neuron 2000, 25: 331–343.

    Article  PubMed  CAS  Google Scholar 

  10. Takebayashi H, Yoshida S, Sugimori M, Kosako H, Kominami R, Nakafuku M, et al. Dynamic expression of basic helixloop-helix Olig family members: implication of Olig2 in neuron and oligodendrocyte differentiation and identification of a new member, Olig3. Mech Dev 2000, 99: 143–148.

    Article  PubMed  CAS  Google Scholar 

  11. Nery S, Wichterle H, Fishell G. Sonic hedgehog contributes to oligodendrocyte specification in the mammalian forebrain. Development 2001, 128: 527–540.

    PubMed  CAS  Google Scholar 

  12. Tekki-Kessaris N, Woodruff R, Hall AC, Gaffield W, Kimura S, Stiles CD, et al. Hedgehog-dependent oligodendrocyte lineage specification in the telencephalon. Development 2001, 128: 2545–2554.

    PubMed  CAS  Google Scholar 

  13. Soula C, Danesin C, Kan P, Grob M, Poncet C, Cochard P. Distinct sites of origin of oligodendrocytes and somatic motoneurons in the chick spinal cord: oligodendrocytes arise from Nkx2.2-expressing progenitors by a Shh-dependent mechanism. Development 2001, 128: 1369–1379.

    PubMed  CAS  Google Scholar 

  14. Qi Y, Tan M, Hui CC, Qiu M. Gli2 is required for normal Shh signaling and oligodendrocyte development in the spinal cord. Mol Cell Neurosci 2003, 23: 440–450.

    Article  PubMed  CAS  Google Scholar 

  15. Wang Y, Imitola J, Rasmussen S, O’Connor KC, Khoury SJ. Paradoxical dysregulation of the neural stem cell pathway sonic hedgehog-Gli1 in autoimmune encephalomyelitis and multiple sclerosis. Ann Neurol 2008, 64: 417–427.

    Article  PubMed  CAS  Google Scholar 

  16. Lelievre V, Ghiani CA, Seksenyan A, Gressens P, de Vellis J, Waschek JA. Growth factor-dependent actions of PACAP on oligodendrocyte progenitor proliferation. Regul Pept 2006, 137: 58–66.

    Article  PubMed  CAS  Google Scholar 

  17. Kessaris N, Jamen F, Rubin LL, Richardson WD. Cooperation between sonic hedgehog and fibroblast growth factor/ MAPK signalling pathways in neocortical precursors. Development 2004, 131: 1289–1298.

    Article  PubMed  CAS  Google Scholar 

  18. Gabay L, Lowell S, Rubin LL, Anderson DJ. Deregulation of dorsoventral patterning by FGF confers trilineage differentia tion capacity on CNS stem cells in vitro. Neuron 2003, 40: 485–499.

    Article  PubMed  CAS  Google Scholar 

  19. Naruse M, Nakahira E, Miyata T, Hitoshi S, Ikenaka K, Bansal R. Induction of oligodendrocyte progenitors in dorsal forebrain by intraventricular microinjection of FGF-2. Dev Biol 2006, 297: 262–273.

    Article  PubMed  CAS  Google Scholar 

  20. Bansal R, Pfeiffer SE. FGF-2 converts mature oligodendrocytes to a novel phenotype. J Neurosci Res 1997, 50: 215–228.

    Article  PubMed  CAS  Google Scholar 

  21. Fortin D, Rom E, Sun H, Yayon A, Bansal R. Distinct fibroblast growth factor (FGF)/FGF receptor signaling pairs initiate diverse cellular responses in the oligodendrocyte lineage. J Neurosci 2005, 25: 7470–7479.

    Article  PubMed  CAS  Google Scholar 

  22. Chandran S, Kato H, Gerreli D, Compston A, Svendsen CN, Allen ND. FGF-dependent generation of oligodendrocytes by a hedgehog-independent pathway. Development 2003, 130: 6599–6609.

    Article  PubMed  CAS  Google Scholar 

  23. Calver AR, Hall AC, Yu WP, Walsh FS, Heath JK, Betsholtz C, et al. Oligodendrocyte population dynamics and the role of PDGF in vivo. Neuron 1998, 20: 869–882.

    Article  PubMed  CAS  Google Scholar 

  24. Fruttiger M, Karlsson L, Hall AC, Abramsson A, Calver AR, Bostrom H, et al. Defective oligodendrocyte development and severe hypomyelination in PDGF-A knockout mice. Development 1999, 126: 457–467.

    PubMed  CAS  Google Scholar 

  25. Pringle NP, Richardson WD. A singularity of PDGF alphareceptor expression in the dorsoventral axis of the neural tube may define the origin of the oligodendrocyte lineage. Development 1993, 117: 525–533.

    PubMed  CAS  Google Scholar 

  26. Hardy RJ. Dorsoventral patterning and oligodendroglial specification in the developing central nervous system. J Neurosci Res 1997, 50: 139–145.

    Article  PubMed  CAS  Google Scholar 

  27. McKinnon RD, Waldron S, Kiel ME. PDGF alpha-receptor signal strength controls an RTK rheostat that integrates phosphoinositol 3′-kinase and phospholipase Cgamma pathways during oligodendrocyte maturation. J Neurosci 2005, 25: 3499–3508.

    Article  PubMed  CAS  Google Scholar 

  28. Baron W, Shattil SJ, ffrench-Constant C. The oligodendrocyte precursor mitogen PDGF stimulates proliferation by activation of alpha(v)beta3 integrins. EMBO J 2002, 21: 1957–1966.

    Article  PubMed  CAS  Google Scholar 

  29. McKinnon RD, Matsui T, Dubois-Dalcq M, Aaronson SA. FGF modulates the PDGF-driven pathway of oligodendrocyte development. Neuron 1990, 5: 603–614.

    Article  PubMed  CAS  Google Scholar 

  30. Wolswijk G, Noble M. Cooperation between PDGF and FGF converts slowly dividing O-2Aadult progenitor cells to rapidly dividing cells with characteristics of O-2Aperinatal progenitor cells. J Cell Biol 1992, 118: 889–900.

    Article  PubMed  CAS  Google Scholar 

  31. Baron W, Metz B, Bansal R, Hoekstra D, de Vries H. PDGF and FGF-2 signaling in oligodendrocyte progenitor cells: regulation of proliferation and differentiation by multiple intracellular signaling pathways. Mol Cell Neurosci 2000, 15: 314–329.

    Article  PubMed  CAS  Google Scholar 

  32. Murtie JC, Zhou YX, Le TQ, Vana AC, Armstrong RC. PDGF and FGF2 pathways regulate distinct oligodendrocyte lineage responses in experimental demyelination with spontaneous remyelination. Neurobiol Dis 2005, 19: 171–182.

    Article  PubMed  CAS  Google Scholar 

  33. Furusho M, Dupree JL, Nave KA, Bansal R. Fibroblast growth factor receptor signaling in oligodendrocytes regulates myelin sheath thickness. J Neurosci 2012, 32: 6631–6641.

    Article  PubMed  CAS  Google Scholar 

  34. van der Pal RH, Koper JW, van Golde LM, Lopes-Cardozo M. Effects of insulin and insulin-like growth factor (IGF-I) on oligodendrocyte-enriched glial cultures. J Neurosci Res 1988, 19: 483–490.

    Article  PubMed  Google Scholar 

  35. Zeger M, Popken G, Zhang J, Xuan S, Lu QR, Schwab MH, et al. Insulin-like growth factor type 1 receptor signaling in the cells of oligodendrocyte lineage is required for normal in vivo oligodendrocyte development and myelination. Glia 2007, 55: 400–411.

    Article  PubMed  Google Scholar 

  36. Ye P, Carson J, D’Ercole AJ. In vivo actions of insulin-like growth factor-I (IGF-I) on brain myelination: studies of IGF-I and IGF binding protein-1 (IGFBP-1) transgenic mice. J Neurosci 1995, 15: 7344–7356.

    PubMed  CAS  Google Scholar 

  37. Mathews LS, Hammer RE, Behringer RR, D’Ercole AJ, Bell GI, Brinster RL, et al. Growth enhancement of transgenic mice expressing human insulin-like growth factor I. Endocrinology 1988, 123: 2827–2833.

    Article  PubMed  CAS  Google Scholar 

  38. Jiang F, Frederick TJ, Wood TL. IGF-I synergizes with FGF-2 to stimulate oligodendrocyte progenitor entry into the cell cycle. Dev Biol 2001, 232: 414–423.

    Article  PubMed  CAS  Google Scholar 

  39. Frederick TJ, Wood TL. IGF-I and FGF-2 coordinately enhance cyclin D1 and cyclin E-cdk2 association and activity to promote G1 progression in oligodendrocyte progenitor cells. Mol Cell Neurosci 2004, 25: 480–492.

    Article  PubMed  CAS  Google Scholar 

  40. Frederick TJ, Min J, Altieri SC, Mitchell NE, Wood TL. Synergistic induction of cyclin D1 in oligodendrocyte progenitor cells by IGF-I and FGF-2 requires differential stimulation of multiple signaling pathways. Glia 2007, 55: 1011–1022.

    Article  PubMed  Google Scholar 

  41. Hsieh J, Aimone JB, Kaspar BK, Kuwabara T, Nakashima K, Gage FH. IGF-I instructs multipotent adult neural progenitor cells to become oligodendrocytes. J Cell Biol 2004, 164: 111–122.

    Article  PubMed  CAS  Google Scholar 

  42. Buttery PC, ffrench-Constant C. Laminin-2/integrin interactions enhance myelin membrane formation by oligodendrocytes. Mol Cell Neurosci 1999, 14: 199–212.

    Article  PubMed  CAS  Google Scholar 

  43. Colognato H, Baron W, Avellana-Adalid V, Relvas JB, Baron-Van Evercooren A, Georges-Labouesse E, et al. CNS integrins switch growth factor signalling to promote targetdependent survival. Nat Cell Biol 2002, 4: 833–841.

    Article  PubMed  CAS  Google Scholar 

  44. Milner R, Edwards G, Streuli C, Ffrench-Constant C. A role in migration for the alpha V beta 1 integrin expressed on oligodendrocyte precursors. J Neurosci 1996, 16: 7240–7252.

    PubMed  CAS  Google Scholar 

  45. Frost EE, Buttery PC, Milner R, ffrench-Constant C. Integrins mediate a neuronal survival signal for oligodendrocytes. Curr Biol 1999, 9: 1251–1254.

    Article  PubMed  CAS  Google Scholar 

  46. Decker L, ffrench-Constant C. Lipid rafts and integrin activation regulate oligodendrocyte survival. J Neurosci 2004, 24: 3816–3825.

    Article  PubMed  CAS  Google Scholar 

  47. Gudz TI, Komuro H, Macklin WB. Glutamate stimulates oligodendrocyte progenitor migration mediated via an alphav integrin/myelin proteolipid protein complex. J Neurosci 2006, 26: 2458–2466.

    Article  PubMed  CAS  Google Scholar 

  48. Shimizu T, Kagawa T, Wada T, Muroyama Y, Takada S, Ikenaka K. Wnt signaling controls the timing of oligodendrocyte development in the spinal cord. Dev Biol 2005, 282: 397–410.

    Article  PubMed  CAS  Google Scholar 

  49. Ye F, Chen Y, Hoang T, Montgomery RL, Zhao XH, Bu H, et al. HDAC1 and HDAC2 regulate oligodendrocyte differentiation by disrupting the beta-catenin-TCF interaction. Nat Neurosci 2009, 12: 829–838.

    Article  PubMed  CAS  Google Scholar 

  50. Fancy SP, Baranzini SE, Zhao C, Yuk DI, Irvine KA, Kaing S, et al. Dysregulation of the Wnt pathway inhibits timely myelination and remyelination in the mammalian CNS. Genes Dev 2009, 23: 1571–1585.

    Article  PubMed  CAS  Google Scholar 

  51. Fu H, Cai J, Clevers H, Fast E, Gray S, Greenberg R, et al. A genome-wide screen for spatially restricted expression patterns identifies transcription factors that regulate glial development. J Neurosci 2009, 29: 11399–11408.

    Article  PubMed  CAS  Google Scholar 

  52. Fancy SP, Harrington EP, Yuen TJ, Silbereis JC, Zhao C, Baranzini SE, et al. Axin2 as regulatory and therapeutic target in newborn brain injury and remyelination. Nat Neurosci 2011, 14: 1009–1016.

    Article  PubMed  CAS  Google Scholar 

  53. Wang S, Sdrulla A, Johnson JE, Yokota Y, Barres BA. A role for the helix-loop-helix protein Id2 in the control of oligodendrocyte development. Neuron 2001, 29: 603–614.

    Article  PubMed  CAS  Google Scholar 

  54. Memezawa A, Takada I, Takeyama K, Igarashi M, Ito S, Aiba S, et al. Id2 gene-targeted crosstalk between Wnt and retinoid signaling regulates proliferation in human keratinocytes. Oncogene 2007, 26: 5038–5045.

    Article  PubMed  CAS  Google Scholar 

  55. Park HC, Boyce J, Shin J, Appel B. Oligodendrocyte specification in zebrafish requires notch-regulated cyclin-dependent kinase inhibitor function. J Neurosci 2005, 25: 6836–6844.

    Article  PubMed  CAS  Google Scholar 

  56. Kim H, Shin J, Kim S, Poling J, Park HC, Appel B. Notchregulated oligodendrocyte specification from radial glia in the spinal cord of zebrafish embryos. Dev Dyn 2008, 237: 2081–2089.

    Article  PubMed  Google Scholar 

  57. Stidworthy MF, Genoud S, Li WW, Leone DP, Mantei N, Suter U, et al. Notch1 and Jagged1 are expressed after CNS demyelination, but are not a major rate-determining factor during remyelination. Brain 2004, 127: 1928–1941.

    Article  PubMed  Google Scholar 

  58. Wang S, Sdrulla AD, diSibio G, Bush G, Nofziger D, Hicks C, et al. Notch receptor activation inhibits oligodendrocyte differentiation. Neuron 1998, 21: 63–75.

    Article  PubMed  Google Scholar 

  59. Genoud S, Lappe-Siefke C, Goebbels S, Radtke F, Aguet M, Scherer SS, et al. Notch1 control of oligodendrocyte differentiation in the spinal cord. J Cell Biol 2002, 158: 709–718.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  61. Hu QD, Ang BT, Karsak M, Hu WP, Cui XY, Duka T, et al. F3/ contactin acts as a functional ligand for Notch during oligodendrocyte maturation. Cell 2003, 115: 163–175.

    Article  PubMed  CAS  Google Scholar 

  62. Zhang Y, Argaw AT, Gurfein BT, Zameer A, Snyder BJ, Ge C, et al. Notch1 signaling plays a role in regulating precursor differentiation during CNS remyelination. Proc Natl Acad Sci U S A 2009, 106: 19162–19167.

    Article  PubMed  CAS  Google Scholar 

  63. Li H, de Faria JP, Andrew P, Nitarska J, Richardson WD. Phosphorylation regulates OLIG2 cofactor choice and the motor neuron-oligodendrocyte fate switch. Neuron 2011, 69: 918–929.

    Article  PubMed  CAS  Google Scholar 

  64. Shah NM, Groves AK, Anderson DJ. Alternative neural crest cell fates are instructively promoted by TGFbeta superfamily members. Cell 1996, 85: 331–343.

    Article  PubMed  CAS  Google Scholar 

  65. Liem KF, Jr., Jessell TM, Briscoe J. Regulation of the neural patterning activity of sonic hedgehog by secreted BMP inhibitors expressed by notochord and somites. Development 2000, 127: 4855–4866.

    PubMed  CAS  Google Scholar 

  66. See J, Zhang X, Eraydin N, Mun SB, Mamontov P, Golden JA, et al. Oligodendrocyte maturation is inhibited by bone morphogenetic protein. Mol Cell Neurosci 2004, 26: 481–492.

    Article  PubMed  CAS  Google Scholar 

  67. Gomes WA, Mehler MF, Kessler JA. Transgenic overexpression of BMP4 increases astroglial and decreases oligodendroglial lineage commitment. Dev Biol 2003, 255: 164–177.

    Article  PubMed  CAS  Google Scholar 

  68. Samanta J, Kessler JA. Interactions between ID and OLIG proteins mediate the inhibitory effects of BMP4 on oligodendroglial differentiation. Development 2004, 131: 4131–4142.

    Article  PubMed  CAS  Google Scholar 

  69. Korchynskyi O, ten Dijke P. Identification and functional characterization of distinct critically important bone morphogenetic protein-specific response elements in the Id1 promoter. J Biol Chem 2002, 277: 4883–4891.

    Article  PubMed  CAS  Google Scholar 

  70. Lopez-Rovira T, Chalaux E, Massague J, Rosa JL, Ventura F. Direct binding of Smad1 and Smad4 to two distinct motifs mediates bone morphogenetic protein-specific transcriptional activation of Id1 gene. J Biol Chem 2002, 277: 3176–3185.

    Article  PubMed  CAS  Google Scholar 

  71. Miyazono K, Miyazawa K. Id: a target of BMP signaling. Sci STKE 2002, 2002: pe40.

    Article  PubMed  Google Scholar 

  72. Massague J, Seoane J, Wotton D. Smad transcription factors. Genes Dev 2005, 19: 2783–2810.

    Article  PubMed  CAS  Google Scholar 

  73. Cheng X, Wang Y, He Q, Qiu M, Whittemore SR, Cao Q. Bone morphogenetic protein signaling and olig1/2 interact to regulate the differentiation and maturation of adult oligodendrocyte precursor cells. Stem Cells 2007, 25: 3204–3214.

    Article  PubMed  CAS  Google Scholar 

  74. Weng Q, Chen Y, Wang H, Xu X, Yang B, He Q, et al. Dualmode modulation of Smad signaling by Smad-interacting protein Sip1 is required for myelination in the central nervous system. Neuron 2012, 73: 713–728.

    Article  PubMed  CAS  Google Scholar 

  75. Jablonska B, Aguirre A, Raymond M, Szabo G, Kitabatake Y, Sailor KA, et al. Chordin-induced lineage plasticity of adult SVZ neuroblasts after demyelination. Nat Neurosci 2010, 13: 541–550.

    Article  PubMed  CAS  Google Scholar 

  76. Carim-Todd L, Escarceller M, Estivill X, Sumoy L. LRRN6A/ LERN1 (leucine-rich repeat neuronal protein 1), a novel gene with enriched expression in limbic system and neocortex. Eur J Neurosci 2003, 18: 3167–3182.

    Article  PubMed  Google Scholar 

  77. Mi S, Lee X, Shao Z, Thill G, Ji B, Relton J, et al. LINGO-1 is a component of the Nogo-66 receptor/p75 signaling complex. Nat Neurosci 2004, 7: 221–228.

    Article  PubMed  CAS  Google Scholar 

  78. Mi S, Miller RH, Lee X, Scott ML, Shulag-Morskaya S, Shao Z, et al. LINGO-1 negatively regulates myelination by oligodendrocytes. Nat Neurosci 2005, 8: 745–751.

    Article  PubMed  CAS  Google Scholar 

  79. Ji B, Li M, Wu WT, Yick LW, Lee X, Shao Z, et al. LINGO-1 antagonist promotes functional recovery and axonal sprouting after spinal cord injury. Mol Cell Neurosci 2006, 33: 311–320.

    Article  PubMed  CAS  Google Scholar 

  80. Mi S, Hu B, Hahm K, Luo Y, Kam Hui ES, Yuan Q, et al. LINGO-1 antagonist promotes spinal cord remyelination and axonal integrity in MOG-induced experimental autoimmune encephalomyelitis. Nat Med 2007, 13: 1228–1233.

    Article  PubMed  CAS  Google Scholar 

  81. Rudick RA, Mi S, Sandrock AW Jr. LINGO-1 antagonists as therapy for multiple sclerosis: in vitro and in vivo evidence. Expert Opin Biol Ther 2008, 8: 1561–1570.

    Article  PubMed  CAS  Google Scholar 

  82. Cahoy JD, Emery B, Kaushal A, Foo LC, Zamanian JL, Christopherson KS, et al. A transcriptome database for astrocytes, neurons, and oligodendrocytes: a new resource for understanding brain development and function. J Neurosci 2008, 28: 264–278.

    Article  PubMed  CAS  Google Scholar 

  83. Chen Y, Wu H, Wang S, Koito H, Li J, Ye F, et al. The oligodendrocyte-specific G protein-coupled receptor GPR17 is a cell-intrinsic timer of myelination. Nat Neurosci 2009, 12: 1398–1406.

    Article  PubMed  CAS  Google Scholar 

  84. Fumagalli M, Daniele S, Lecca D, Lee PR, Parravicini C, Fields RD, et al. Phenotypic changes, signaling pathway, and functional correlates of GPR17-expressing neural precursor cells during oligodendrocyte differentiation. J Biol Chem 2011, 286: 10593–10604.

    Article  PubMed  CAS  Google Scholar 

  85. Lu QR, Sun T, Zhu Z, Ma N, Garcia M, Stiles CD, et al. Common developmental requirement for Olig function indicates a motor neuron/oligodendrocyte connection. Cell 2002, 109: 75–86.

    Article  PubMed  CAS  Google Scholar 

  86. Zhou Q, Anderson DJ. The bHLH transcription factors OLIG2 and OLIG1 couple neuronal and glial subtype specification. Cell 2002, 109: 61–73.

    Article  PubMed  CAS  Google Scholar 

  87. Yue T, Xian K, Hurlock E, Xin M, Kernie SG, Parada LF, et al. A critical role for dorsal progenitors in cortical myelination. J Neurosci 2006, 26: 1275–1280.

    Article  PubMed  CAS  Google Scholar 

  88. Zhu X, Zuo H, Maher BJ, Serwanski DR, LoTurco JJ, Lu QR, et al. Olig2-dependent developmental fate switch of NG2 cells. Development 2012, 139: 2299–2307.

    Article  PubMed  CAS  Google Scholar 

  89. Xin M, Yue T, Ma Z, Wu FF, Gow A, Lu QR. Myelinogenesis and axonal recognition by oligodendrocytes in brain are uncoupled in Olig1-null mice. J Neurosci 2005, 25: 1354–1365.

    Article  PubMed  CAS  Google Scholar 

  90. Li H, Lu Y, Smith HK, Richardson WD. Olig1 and Sox10 interact synergistically to drive myelin basic protein transcription in oligodendrocytes. J Neurosci 2007, 27: 14375–14382.

    Article  PubMed  CAS  Google Scholar 

  91. Arnett HA, Fancy SP, Alberta JA, Zhao C, Plant SR, Kaing S, et al. bHLH transcription factor Olig1 is required to repair demyelinated lesions in the CNS. Science 2004, 306: 2111–2115.

    Article  PubMed  CAS  Google Scholar 

  92. Burton A. Olig1 needed for remyelination. Lancet Neurol 2005, 4: 80.

    Article  PubMed  Google Scholar 

  93. Yu Y, Chen Y, Kim B, Wang H, Zhao C, He X, et al. Olig2 targets chromatin remodelers to enhancers to initiate oligodendrocyte differentiation. Cell 2013, 152: 248–261.

    Article  PubMed  CAS  Google Scholar 

  94. Mizuguchi R, Sugimori M, Takebayashi H, Kosako H, Nagao M, Yoshida S, et al. Combinatorial roles of olig2 and neurogenin2 in the coordinated induction of pan-neuronal and subtype-specific properties of motoneurons. Neuron 2001, 31: 757–771.

    Article  PubMed  CAS  Google Scholar 

  95. Novitch BG, Chen AI, Jessell TM. Coordinate regulation of motor neuron subtype identity and pan-neuronal properties by the bHLH repressor Olig2. Neuron 2001, 31: 773–789.

    Article  PubMed  CAS  Google Scholar 

  96. Cai J, Chen Y, Cai WH, Hurlock EC, Wu H, Kernie SG, et al. A crucial role for Olig2 in white matter astrocyte development. Development 2007, 134: 1887–1899.

    Article  PubMed  CAS  Google Scholar 

  97. Sun Y, Meijer DH, Alberta JA, Mehta S, Kane MF, Tien AC, et al. Phosphorylation state of Olig2 regulates proliferation of neural progenitors. Neuron 2011, 69: 906–917.

    Article  PubMed  CAS  Google Scholar 

  98. Emery B, Agalliu D, Cahoy JD, Watkins TA, Dugas JC, Mulinyawe SB, et al. Myelin gene regulatory factor is a critical transcriptional regulator required for CNS myelination. Cell 2009, 138: 172–185.

    Article  PubMed  CAS  Google Scholar 

  99. Koenning M, Jackson S, Hay CM, Faux C, Kilpatrick TJ, Willingham M, et al. Myelin gene regulatory factor is required for maintenance of myelin and mature oligodendrocyte identity in the adult CNS. J Neurosci 2012, 32: 12528–12542.

    Article  PubMed  CAS  Google Scholar 

  100. Wang SZ, Dulin J, Wu H, Hurlock E, Lee SE, Jansson K, et al. An oligodendrocyte-specific zinc-finger transcription regulator cooperates with Olig2 to promote oligodendrocyte differentiation. Development 2006, 133: 3389–3398.

    Article  PubMed  CAS  Google Scholar 

  101. Soundarapandian MM, Selvaraj V, Lo UG, Golub MS, Feldman DH, Pleasure DE, et al. Zfp488 promotes oligodendrocyte differentiation of neural progenitor cells in adult mice after demyelination. Sci Rep 2011, 1: 2.

    Article  PubMed  CAS  Google Scholar 

  102. Verstappen G, van Grunsven LA, Michiels C, Van de Putte T, Souopgui J, Van Damme J, et al. Atypical Mowat-Wilson patient confirms the importance of the novel association between ZFHX1B/SIP1 and NuRD corepressor complex. Hum Mol Genet 2008, 17: 1175–1183.

    Article  PubMed  CAS  Google Scholar 

  103. Marin-Husstege M, Muggironi M, Liu A, Casaccia-Bonnefil P. Histone deacetylase activity is necessary for oligodendrocyte lineage progression. J Neurosci 2002, 22: 10333–10345.

    PubMed  CAS  Google Scholar 

  104. Shen S, Li J, Casaccia-Bonnefil P. Histone modifications affect timing of oligodendrocyte progenitor differentiation in the developing rat brain. J Cell Biol 2005, 169: 577–589.

    Article  PubMed  CAS  Google Scholar 

  105. Shen S, Sandoval J, Swiss VA, Li J, Dupree J, Franklin RJ, et al. Age-dependent epigenetic control of differentiation inhibitors is critical for remyelination efficiency. Nat Neurosci 2008, 11: 1024–1034.

    Article  PubMed  CAS  Google Scholar 

  106. Liu H, Hu Q, D’Ercole A J, Ye P. Histone deacetylase 11 regulates oligodendrocyte-specific gene expression and cell development in OL-1 oligodendroglia cells. Glia 2009, 57: 1–12.

    Article  PubMed  Google Scholar 

  107. Beirowski B, Gustin J, Armour SM, Yamamoto H, Viader A, North BJ, et al. Sir-two-homolog 2 (Sirt2) modulates peripheral myelination through polarity protein Par-3/atypical protein kinase C (aPKC) signaling. Proc Natl Acad Sci U S A 2011, 108: E952–961.

    Article  PubMed  CAS  Google Scholar 

  108. Li W, Zhang B, Tang J, Cao Q, Wu Y, Wu C, et al. 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. J Neurosci 2007, 27: 2606–2616.

    Article  PubMed  CAS  Google Scholar 

  109. Werner HB, Kuhlmann K, Shen S, Uecker M, Schardt A, Dimova K, et al. Proteolipid protein is required for transport of sirtuin 2 into CNS myelin. J Neurosci 2007, 27: 7717–7730.

    Article  PubMed  CAS  Google Scholar 

  110. Zhu H, Zhao L, Wang E, Dimova N, Liu G, Feng Y, et al. The QKI-PLP pathway controls SIRT2 abundance in CNS myelin. Glia 2012, 60: 69–82.

    Article  PubMed  CAS  Google Scholar 

  111. Lin ST, Fu YH. miR-23 regulation of lamin B1 is crucial for oligodendrocyte development and myelination. Dis Model Mech 2009, 2: 178–188.

    Article  PubMed  CAS  Google Scholar 

  112. Zhao X, He X, Han X, Yu Y, Ye F, Chen Y, et al. MicroRNA-mediated control of oligodendrocyte differentiation. Neuron 2010, 65: 612–626.

    Article  PubMed  CAS  Google Scholar 

  113. Dugas JC, Cuellar TL, Scholze A, Ason B, Ibrahim A, Emery B, et al. Dicer1 and miR-219 Are required for normal oligodendrocyte differentiation and myelination. Neuron 2010, 65: 597–611.

    Article  PubMed  CAS  Google Scholar 

  114. Zheng K, Li H, Zhu Y, Zhu Q, Qiu M. MicroRNAs are essential for the developmental switch from neurogenesis to gliogenesis in the developing spinal cord. J Neurosci 2010, 30: 8245–8250.

    Article  PubMed  CAS  Google Scholar 

  115. Zhao X, Wu J, Zheng M, Gao F, Ju G. Specification and maintenance of oligodendrocyte precursor cells from neural progenitor cells: involvement of microRNA-7a. Mol Biol Cell 2012, 23: 2867–2878.

    Article  PubMed  CAS  Google Scholar 

  116. Bauer NM, Moos C, van Horssen J, Witte M, van der Valk P, Altenhein B, et al. Myelin basic protein synthesis is regulated by small non-coding RNA 715. EMBO Rep 2012, 13: 827–834.

    Article  PubMed  CAS  Google Scholar 

  117. Weider M, Kuspert M, Bischof M, Vogl MR, Hornig J, Loy K, et al. Chromatin-remodeling factor Brg1 is required for Schwann cell differentiation and myelination. Dev Cell 2012, 23: 193–201.

    Article  PubMed  CAS  Google Scholar 

  118. Limpert AS, Bai S, Narayan M, Wu J, Yoon SO, Carter BD, et al. NF-kB forms a complex with the chromatin remodeler BRG1 to regulate Schwann cell differentiation. J Neurosci 2012, 33(6): 2388–2397.

    Article  Google Scholar 

  119. Hung H, Kohnken R, Svaren J. The nucleosome remodeling and deacetylase chromatin remodeling (NuRD) complex is required for peripheral nerve myelination. J Neurosci 2012, 32: 1517–1527.

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Pediatrics and Obstetrics/Gynaecology, Institute of Stem Cell and Developmental Biology, West China Second Hospital, Sichuan University, Chengdu, 610041, China

    Li He

  2. Department of Developmental Biology and Kent Waldrep Foundation Center for Basic Neuroscience Research on Nerve Growth and Regeneration, University of Texas Southwestern Medical Center, Dallas, TX, 75390, USA

    Q. Richard Lu

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  1. Li He
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Correspondence to Q. Richard Lu.

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He, L., Lu, Q.R. Coordinated control of oligodendrocyte development by extrinsic and intrinsic signaling cues. Neurosci. Bull. 29, 129–143 (2013). https://doi.org/10.1007/s12264-013-1318-y

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  • DOI: https://doi.org/10.1007/s12264-013-1318-y

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