How to make an oligodendrocyte

Development (Cambridge)

Volumn 142, Issue 23, 2015, Pages 3983-3995

  Goldman, Steven A ^a,b,c   Kuypers, Nicholas J ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c Rigshospitalet   (Denmark)

Author keywords

Astrocyte; Glial progenitor cell; Leukodystrophy; Multiple sclerosis; Myelin; Neural stem cell; Remyelination; Stem cell; White matter

Indexed keywords

GROWTH FACTOR; MEMBRANE ANTIGEN; MICRORNA; PROTEIN; TRANSCRIPTION FACTOR;

ARTICLE; ASTROCYTE; BLASTOCYST; BRAIN DEVELOPMENT; BRAIN MATURATION; CELL DIFFERENTIATION; CELL FATE; CEREBRAL PALSY; EMBRYONIC STEM CELL; ENGRAFTMENT; FOREBRAIN; GASTRULATION; GLOBOID CELL LEUKODYSTROPHY; LEUKODYSTROPHY; METACHROMATIC LEUKODYSTROPHY; MULTIPLE SCLEROSIS; MYELINATION; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NEURAL STEM CELL TRANSPLANTATION; OLIGODENDROCYTE STEM CELL; OLIGODENDROGLIA; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; REMYELINIZATION; SAFETY; SOMATIC CELL; TAY SACHS DISEASE; WHITE MATTER; ANIMAL; CELL CULTURE TECHNIQUE; CELL TRANSPLANTATION; CYTOLOGY; DEMYELINATING DISEASE; DEVELOPMENTAL BIOLOGY; HUMAN; INDUCED PLURIPOTENT STEM CELL; METABOLISM; MOUSE; MYELIN SHEATH; PHENOTYPE; PHYSIOLOGY; PROCEDURES; SPINAL CORD;

ANIMALS; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELL TRANSPLANTATION; DEMYELINATING DISEASES; DEVELOPMENTAL BIOLOGY; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MICE; MULTIPLE SCLEROSIS; MYELIN SHEATH; OLIGODENDROGLIA; PHENOTYPE; PLURIPOTENT STEM CELLS; PROSENCEPHALON; SPINAL CORD;

EID: 84949469445     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.126409     Document Type: Article

References (151)

1. Abiraman, K., Pol, S. U., O’Bara, M. A., Chen, G.-D., Khaku, Z. M., Wang, J., Thorn, D., Vedia, B. H., Ekwegbalu, E. C., Li, J.-X. et al. (2015). Anti-muscarinic adjunct therapy accelerates functional human oligodendrocyte repair. J. Neurosci. 35, 3676-3688
2. Ackerman, S. D., Garcia, C., Piao, X., Gutmann, D. H. and Monk, K. R. (2015). The adhesion GPCR Gpr56 regulates oligodendrocyte development via interactions with Galpha12/13 and RhoA. Nat. Commun. 6, 6122
3. Ahmed, S., Gan, H. T., Lam, C. S., Poonepalli, A., Ramasamy, S., Tay, Y., Tham, M. and Yu, Y. H. (2009). Transcription factors and neural stem cell self-renewal, growth and differentiation. Cell Adh. Migr. 3, 412-424
4. Armstrong, R. C., Dorn, H. H., Kufta, C. V., Friedman, E. and Dubois-Dalcq, M. E. (1992). Pre-oligodendrocytes from adult human CNS. J. Neurosci. 12, 1538-1547
5. Back, S. A. and Rivkees, S. A. (2004). Emerging concepts in periventricular white matter injury. Semin. Perinatol. 28, 405-414
6. Bansal, R., Warrington, A. E., Gard, A., Ranscht, B. and Pfeiffer, S. (1989). Multiple and novel specificities of monoclonal antibodies O1, O4, and R-mAb used in the analysis of oligodendrocyte development. J. Neurosci. Res. 24, 548-557
7. Barca-Mayo, O. and Lu, Q. R. (2012). Fine-tuning oligodendrocyte development by microRNAs. Front. Neurosci. 6, 13
8. Barres, B. A., Schmid, R., Sendnter, M. and Raff, M. C. (1993). Multiple extracellular signals are required for long-term oligodendrocyte survival. Development 118, 283-295
9. Barres, B. A., Lazar, M. A. and Raff, M. C. (1994). A novel role for thyroid hormone, glucocorticoids and retinoic acid in timing oligodendrocyte development. Development 120, 1097-1108
10. Belachew, S., Chittajallu, R., Aguirre, A. A., Yuan, X., Kirby, M., Anderson, S. and Gallo, V. (2003). Postnatal NG2 proteoglycan-expressing progenitor cells are intrinsically multipotent and generate functional neurons. J. Cell Biol. 161, 169-186
11. Cahoy, J. D., Emery, B., Kaushal, A., Foo, L. C., Zamanian, J. L., Christopherson, K. S., Xing, Y., Lubischer, J. L., Krieg, P. A., Krupenko, S. A. et al. (2008). A transcriptome database for astrocytes, neurons, and oligodendrocytes: a new resource for understanding brain development and function. J. Neurosci. 28, 264-278
12. Cai, J., Qi, Y., Hu, X., Tan, M., Liu, Z., Zhang, J., Li, Q., Sander, M. and Qiu, M. (2005). Generation of oligodendrocyte precursor cells from mouse dorsal spinal cord independent of Nkx6 regulation and Shh signaling. Neuron 45, 41-53
13. Casaccia-Bonnefil, P., Hardy, R. J., Teng, K. K., Levine, J. M., Koff, A. and 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
14. Chambers, S. M., Fasano, C. A., Papapetrou, E. P., Tomishima, M., Sadelain, M. and Studer, L. (2009). Highly efficient neural conversion of human ES and iPS cells by dual inhibition of SMAD signaling. Nat. Biotechnol. 27, 275-280
15. Chang, A., Nishiyama, A., Peterson, J., Prineas, J. and Trapp, B. D. (2000). NG2- positive oligodendrocyte progenitor cells in adult human brain and multiple sclerosis lesions. J. Neurosci. 20, 6404-6412
16. Chapman, H., Waclaw, R. R., Pei, Z., Nakafuku, M. and Campbell, K. (2013). The homeobox gene Gsx2 controls the timing of oligodendroglial fate specification in mouse lateral ganglionic eminence progenitors. Development 140, 2289-2298
17. Chen, Y., Wu, H., Wang, S., Koito, H., Li, J., Ye, F., Hoang, J., Escobar, S. S., Gow, A., Arnett, H. A. et al. (2009). The oligodendrocyte-specific G protein– coupled receptor GPR17 is a cell-intrinsic timer of myelination. Nat. Neurosci. 12, 1398-1406
18. Chew, L.-J., Shen, W., Ming, X., Senatorov, V. V., Jr., Chen, H.-L., Cheng, Y., Hong, E., Knoblach, S. and Gallo, V. (2011). SRY-box containing gene 17 regulates the Wnt/beta-catenin signaling pathway in oligodendrocyte progenitor cells. J. Neurosci. 31, 13921-13935
19. Czepiel, M., Balasubramaniyan, V., Schaafsma, W., Stancic, M., Mikkers, H., Huisman, C., Boddeke, E. and Copray, S. (2011). Differentiation of induced pluripotent stem cells into functional oligodendrocytes. Glia 59, 882-892
20. Dawson, M. R. L., Levine, J. M. and Reynolds, R. (2000). NG2-expressing cells in the central nervous system: are they oligodendroglial progenitors? J. Neurosci. Res. 61, 471-479
21. Deshmukh, V. A., Tardif, V., Lyssiotis, C. A., Green, C. C., Kerman, B., Kim, H. J., Padmanabhan, K., Swoboda, J. G., Ahmad, I., Kondo, T. et al. (2013). A regenerative approach to the treatment of multiple sclerosis. Nature 502, 327-332
22. Dietrich, J., Noble, M. and Mayer-Proschel, M. (2002). Characterization of A2B5+ glial precursor cells from cryopreserved human fetal brain progenitor cells. Glia 40, 65-77
23. Douvaras, P. and Fossati, V. (2015). Generation and isolation of oligodendrocyte progenitor cells from human pluripotent stem cells. Nat. Protoc. 10, 1143-1154
24. Douvaras, P., Wang, J., Zimmer, M., Hanchuk, S., O’Bara, M. A., Sadiq, S., Sim, F. J., Goldman, J. and Fossati, V. (2014). Efficient generation of myelinating oligodendrocytes from primary progressive multiple sclerosis patients by induced pluripotent stem cells. Stem Cell Rep. 3, 250-259
25. Dugas, J. C., Tai, Y. C., Speed, T. P., Ngai, J. and Barres, B. A. (2006). Functional genomic analysis of oligodendrocyte differentiation. J. Neurosci. 26, 10967-10983
26. Dugas, J. C., Cuellar, T. L., Scholze, A., Ason, B., Ibrahim, A., Emery, B., Zamanian, J. L., Foo, L. C., McManus, M. T. and Barres, B. A. (2010). Dicer1 and miR-219 Are required for normal oligodendrocyte differentiation and myelination. Neuron 65, 597-611
27. Emery, B. and Lu, Q. R. (2015). Transcriptional and epigenetic regulation of oligodendrocyte development and myelination in the CNS. Cold Spring Harb. Perspect. Biol. 7, a020461
28. Emery, B., Agalliu, D., Cahoy, J. D., Watkins, T. A., Dugas, J. C., Mulinyawe, S. B., Ibrahim, A., Ligon, K. L., Rowitch, D. H. and Barres, B. A. (2009). Myelin gene regulatory factor is a critical transcriptional regulator required for CNS myelination. Cell 138, 172-185
29. Fancy, S. P. J., Baranzini, S. E., Zhao, C., Yuk, D.-I., Irvine, K.-A., Kaing, S., Sanai, N., Franklin, R. J. M. and Rowitch, D. H. (2009). Dysregulation of the Wnt pathway inhibits timely myelination and remyelination in the mammalian CNS. Genes Dev. 23, 1571-1585
30. Fancy, S. P. J., Kotter, M. R., Harrington, E. P., Huang, J. K., Zhao, C., Rowitch, D. H. and Franklin, R. J. M. (2010). Overcoming remyelination failure in multiple sclerosis and other myelin disorders. Exp. Neurol. 225, 18-23
31. Fancy, S. P. J., Harrington, E. P., Yuen, T. J., Silbereis, J. C., Zhao, C., Baranzini, S. E., Bruce, C. C., Otero, J. J., Huang, E. J., Nusse, R. et al. (2011). Axin2 as regulatory and therapeutic target in newborn brain injury and remyelination. Nat. Neurosci. 14, 1009-1016.
32. ffrench-Constant, C. and Raff, M. C. (1986). Proliferating bipotential glial progenitor cells in adult rat optic nerve. Nature 319, 499-502
33. Fogarty, M., Richardson, W. D. and Kessaris, N. (2005). A subset of oligodendrocytes generated from radial glia in the dorsal spinal cord. Development 132, 1951-1959
34. Fox, I. J., Daley, G. Q., Goldman, S. A., Huard, J., Kamp, T. J. and Trucco, M. (2014). Use of differentiated pluripotent stem cells in replacement therapy for treating disease. Science 345, 1247391
35. Franklin, R. J. M. (2002). Why does remyelination fail in multiple sclerosis? Nat. Rev. Neurosci. 3, 705-714
36. Franklin, R. J. M. and ffrench-Constant, C. (2008). Remyelination in the CNS: from biology to therapy. Nat. Rev. Neurosci. 9, 839-855
37. Franklin, R. J. and Goldman, S. A. (2015). Remyelination. In Glia (ed. B.A. Barres and M.R. Freeman). Cold Spring Harbor: Cold Spring Harbor Laboratory Press.
38. Gallo, V. and Deneen, B. (2014). Glial development: the crossroads of regeneration and repair in the CNS. Neuron 83, 283-308
39. Giera, S., Deng, Y., Luo, R., Ackerman, S. D., Mogha, A., Monk, K. R., Ying, Y., Jeong, S.-J., Makinodan, M., Bialas, A. R. et al. (2015). The adhesion G proteincoupled receptor GPR56 is a cell-autonomous regulator of oligodendrocyte development. Nat. Commun. 6, 6121
40. Goldman, S. A. (1990). Neuronal development and migration in explant cultures of the adult canary forebrain. J. Neurosci. 10, 2931-2939
41. Goldman, S. A. (2011). Progenitor cell–based treatment of the pediatric myelin disorders. Arch. Neurol. 68, 848-856
42. Goldman, S. A. (2013). White matter from fibroblasts. Nat. Biotechnol. 31, 412-413
43. Goldman, S. A., Nedergaard, M. and Windrem, M. S. (2012). Glial progenitor cellbased treatment and modeling of neurological disease. Science 338, 491-495
44. Goldman, S. A., Nedergaard, M. and Windrem, M. S. (2015). Modeling cognition and disease using human glial chimeric mice. Glia 63, 1483-1493
45. Guo, F., Maeda, Y., Ma, J., Xu, J., Horiuchi, M., Miers, L., Vaccarino, F. and Pleasure, D. (2010). Pyramidal neurons are generated from oligodendroglial progenitor cells in adult piriform cortex. J. Neurosci. 30, 12036-12049
46. Hart, I. K., Richardson, W. D., Heldin, C. H., Westermark, B. and Raff, M. C. (1989). PDGF receptors on cells of the oligodendrocyte-type-2 astrocyte (O-2A) cell lineage. Development 105, 595-603
47. He, X., Yu, Y., Awatramani, R. and Lu, Q. R. (2012). Unwrapping myelination by microRNAs. Neuroscientist 18, 45-55
48. Helman, G., Van Haren, K., Bonkowsky, J. L., Bernard, G., Pizzino, A., Braverman, N., Suhr, D., Patterson, M. C., Ali Fatemi, S., Leonard, J. et al. (2015). Disease specific therapies in leukodystrophies and leukoencephalopathies. Mol. Genet. Metab. 114, 527-536
49. Hu, B.-Y., Du, Z.-W., Li, X.-J., Ayala, M. and Zhang, S.-C. (2009). Human oligodendrocytes from embryonic stem cells: conserved SHH signaling networks and divergent FGF effects. Development 136, 1443-1452
50. Huang, J. K., Jarjour, A. A., Oumesmar, B. N., Kerninon, C., Williams, A., Krezel, W., Kagechika, H., Bauer, J., Zhao, C., Evercooren, A. B.-V. et al. (2011). Retinoid X receptor gamma signaling accelerates CNS remyelination. Nat. Neurosci. 14, 45-53
51. Huang, N., Niu, J., Feng, Y. and Xiao, L. (2015). Oligodendroglial development: new roles for chromatin accessibility. Neuroscientist, pii: 1073858414565467
52. Hughes, E. G., Kang, S. H., Fukaya, M. and Bergles, D. E. (2013). Oligodendrocyte progenitors balance growth with self-repulsion to achieve homeostasis in the adult brain. Nat. Neurosci. 16, 668-676
53. Huttner, W. B. and Brand, M. (1997). Asymmetric division and polarity of neuroepithelial cells. Curr. Opin. Neurobiol. 7, 29-39
54. Ishibashi, T., Ding, L., Ikenaka, K., Inoue, Y., Miyado, K., Mekada, E. and Baba, H. (2004). Tetraspanin protein CD9 is a novel paranodal component regulating paranodal junctional formation. J. Neurosci. 24, 96-102
55. Izrael, M., Zhang, P., Kaufman, R., Shinder, V., Ella, R., Amit, M., Itskovitz-Eldor, J., Chebath, J. and Revel, M. (2007). Human oligodendrocytes derived from embryonic stem cells: Effect of noggin on phenotypic differentiation in vitro and on myelination in vivo. Mol. Cell. Neurosci. 34, 310-323
56. Jan, Y.-N. and Jan, L. Y. (2001). Development: asymmetric cell division in the Drosophila nervous system. Nat. Rev. Neurosci. 2, 772-779
57. Kang, S. H., Fukaya, M., Yang, J. K., Rothstein, J. D. and Bergles, D. E. (2010). NG2+ CNS glial progenitors remain committed to the oligodendrocyte lineage in postnatal life and following neurodegeneration. Neuron 68, 668-681
58. Kaplan, M. R., Meyer-Franke, A., Lambert, S., Bennett, V., Duncan, I. D., Levinson, S. R. and Barres, B. A. (1997). Induction of sodium channel clustering by oligodendrocytes. Nature 386, 724-728
59. Keilhauer, G., Meier, D. H., Kuhlmann-Krieg, S., Nieke, J. and Schachner, M. (1985). Astrocytes support incomplete differentiation of an oligodendrocyte precursor cell. EMBO J. 4, 2499-2504
60. Kessaris, N., Fogarty, M., Iannarelli, P., Grist, M., Wegner, M. and Richardson, W. D. (2006). Competing waves of oligodendrocytes in the forebrain and postnatal elimination of an embryonic lineage. Nat. Neurosci. 9, 173-179
61. Kirschenbaum, B., Nedergaard, M., Preuss, A., Barami, K., Fraser, R. A. R. and Goldman, S. A. (1994). In vitro neuronal production and differentiation by precursor cells derived from the adult human forebrain. Cereb. Cortex 4, 576-589
62. Klambt, C. (2009). Modes and regulation of glial migration in vertebrates and invertebrates. Nat. Rev. Neurosci. 10, 769-779
63. Kondo, Y., Windrem, M. S., Zou, L., Chandler-Militello, D., Schanz, S. J., Auvergne, R. M., Betstadt, S. J., Harrington, A. R., Johnson, M., Kazarov, A. et al. (2014). Human glial chimeric mice reveal astrocytic dependence of JC virus infection. J. Clin. Invest. 124, 5323-5336
64. Krencik, R., Weick, J. P., Liu, Y., Zhang, Z.-J. and Zhang, S.-C. (2011). Specification of transplantable astroglial subtypes from human pluripotent stem cells. Nat. Biotechnol. 29, 528-534
65. Kuhlbrodt, K., Herbarth, B., Sock, E., Hermans-Borgmeyer, I. and Wegner, M. (1998). Sox10, a novel transcriptional modulator in glial cells. J. Neurosci. 18, 237-250
66. Larocque, D., Galarneau, A., Liu, H.-N., Scott, M., Almazan, G. and Richard, S. (2005). Protection of p27(Kip1) mRNA by quaking RNA binding proteins promotes oligodendrocyte differentiation. Nat. Neurosci. 8, 27-33
67. Lau, P., Verrier, J. D., Nielsen, J. A., Johnson, K. R., Notterpek, L. and Hudson, L. D. (2008). Identification of dynamically regulated microRNA and mRNA networks in developing oligodendrocytes. J. Neurosci. 28, 11720-11730
68. Lee, S., Leach, M. K., Redmond, S. A., Chong, S. Y. C., Mellon, S. H., Tuck, S. J., Feng, Z.-Q., Corey, J. M. and Chan, J. R. (2012). A culture system to study oligodendrocyte myelination processes using engineered nanofibers. Nat. Methods 9, 917-922
69. Lee, X., Shao, Z., Sheng, G., Pepinsky, B. and Mi, S. (2014). LINGO-1 regulates oligodendrocyte differentiation by inhibiting ErbB2 translocation and activation in lipid rafts. Mol. Cell. Neurosci. 60, 36-42
70. Levine, J. M., Reynolds, R. and Fawcett, J. W. (2001). The oligodendrocyte precursor cell in health and disease. Trends Neurosci. 24, 39-47
71. Li, H., Lu, Y., Smith, H. K. and Richardson, W. D. (2007). Olig1 and Sox10 interact synergistically to drive myelin basic protein transcription in oligodendrocytes. J. Neurosci. 27, 14375-14382
72. Li, M., Suzuki, K., Kim, N. Y., Liu, G.-H. and Izpisua Belmonte, J. C. (2014). A cut above the rest: targeted genome editing technologies in human pluripotent stem cells. J. Biol. Chem. 289, 4594-4599
73. Lin, S.-L. and Ying, S.-Y. (2013). Mechanism and method for generating tumor-free iPS cells using intronic microRNA miR-302 induction. Methods Mol. Biol. 936, 295-312
74. Lin, T., Ambasudhan, R., Yuan, X., Li, W., Hilcove, S., Abujarour, R., Lin, X., Hahm, H. S., Hao, E., Hayek, A. et al. (2009). A chemical platform for improved induction of human iPSCs. Nat. Methods 6, 805-808
75. Liu, A., Han, Y. R., Li, J., Sun, D., Ouyang, M., Plummer, M. R. and Casaccia- Bonnefil, P. (2007). The glial or neuronal fate choice of oligodendrocyte progenitors is modulated by their ability to acquire an epigenetic memory. J. Neurosci. 27, 7339-7343
76. Liu, Y., Jiang, P. and Deng, W. (2011). OLIG gene targeting in human pluripotent stem cells for motor neuron and oligodendrocyte differentiation. Nat. Protoc. 6, 640-655
77. Lu, Q. R., Yuk, D.-i., Alberta, J. A., Zhu, Z., Pawlitzky, I., Chan, J., McMahon, A. P., Stiles, C. D. and Rowitch, D. H. (2000). Sonic hedgehog–regulated oligodendrocyte lineage genes encoding bHLH proteins in the mammalian central nervous system. Neuron 25, 317-329
78. Mabie, P. C., Mehler, M. F., Marmur, R., Papavasiliou, A., Song, Q. and Kessler, J. A. (1997). Bone morphogenetic proteins induce astroglial differentiation of oligodendroglial-astroglial progenitor cells. J. Neurosci. 17, 4112-4120
79. Magri, L., Gacias, M., Wu, M., Swiss, V. A., Janssen, W. G. and Casaccia, P. (2014). c-Myc-dependent transcriptional regulation of cell cycle and nucleosomal histones during oligodendrocyte differentiation. Neuroscience 276, 72-86
80. Maherali, N. and Hochedlinger, K. (2008). Guidelines and techniques for the generation of induced pluripotent stem cells. Cell Stem Cell 3, 595-605
81. Mallanna, S. K. and Rizzino, A. (2010). Emerging roles of microRNAs in the control of embryonic stem cells and the generation of induced pluripotent stem cells. Dev. Biol. 344, 16-25
82. McClain, C. R., Sim, F. J. and Goldman, S. A. (2012). Pleiotrophin suppression of receptor protein tyrosine phosphatase-beta/zeta maintains the self-renewal competence of fetal human oligodendrocyte progenitor cells. J. Neurosci. 32, 15066-15075
83. Mei, F., Fancy, S. P. J., Shen, Y.-A. A., Niu, J., Zhao, C., Presley, B., Miao, E., Lee, S., Mayoral, S. R., Redmond, S. A. et al. (2014). Micropillar arrays as a highthroughput screening platform for therapeutics in multiple sclerosis. Nat. Med. 20, 954-960
84. Mi, S., Blake Pepinsky, R. and Cadavid, D. (2013). Blocking LINGO-1 as a therapy to promote CNS repair: from concept to the clinic. CNS Drugs 27, 493-503
85. Najm, F. J., Lager, A. M., Zaremba, A., Wyatt, K., Caprariello, A., Factor, D. C., Karl, R. T., Maeda, T., Miller, R. H. and Tesar, P. J. (2013). Transcription factor– mediated reprogramming of fibroblasts to expandable, myelinogenic oligodendrocyte progenitor cells. Nat. Biotechnol. 31, 426-433
86. Najm, F. J., Madhavan, M., Zaremba, A., Shick, E., Karl, R. T., Factor, D. C., Miller, T. E., Nevin, Z. S., Kantor, C., Sargent, A. et al. (2015). Drug-based modulation of endogenous stem cells promotes functional remyelination in vivo. Nature 522, 216-220
87. Namihira, M. and Nakashima, K. (2013). Mechanisms of astrocytogenesis in the mammalian brain. Curr. Opin. Neurobiol. 23, 921-927
88. Nave, K.-A. (2010a). Myelination and support of axonal integrity by glia. Nature 468, 244-252
89. Nave, K.-A. (2010b). Myelination and the trophic support of long axons. Nat. Rev. Neurosci. 11, 275-283
90. Nery, S., Wichterle, H. and Fishell, G. (2001). Sonic hedgehog contributes to oligodendrocyte specification in the mammalian forebrain. Development 128, 527-540
91. Nishiyama, A., Komitova, M., Suzuki, R. and Zhu, X. (2009). Polydendrocytes (NG2 cells): multifunctional cells with lineage plasticity. Nat. Rev. Neurosci. 10, 9-22
92. Nistor, G., Totoiu, M., Haque, N. S., Carpenter, M. and Keirstead, H. (2005). Human embryonic stem cells differentiate into oligodendrocytes in high purity and myelinate after spinal cord transplantation. Glia 49, 385-396
93. Noble, M., Murray, K., Stroobant, P., Waterfield, M. D. and Riddle, P. (1988). Platelet-derived growth factor promotes division and motility and inhibits premature differentiation of the oligodendrocyte/type-2 astrocyte progenitor cell. Nature 333, 560-562
94. Nunes, M. C., Roy, N. S., Keyoung, H. M., Goodman, R. R., McKhann, G., Jiang, L., Kang, J., Nedergaard, M. and Goldman, S. A. (2003). Identification and isolation of multipotential neural progenitor cells from the subcortical white matter of the adult human brain. Nat. Med. 9, 439-447
95. Orentas, D. M., Hayes, J. E., Dyer, K. L. and Miller, R. H. (1999). Sonic hedgehog signaling is required during the appearance of spinal cord oligodendrocyte precursors. Development 126, 2419-2429
96. Piao, J., Major, T., Auyeung, G., Policarpio, E., Menon, J., Droms, L., Gutin, P., Uryu, K., Tchieu, J., Soulet, D. et al. (2015). Human embryonic stem cell-derived oligodendrocyte progenitors remyelinate the brain and rescue behavioral deficits following radiation. Cell Stem Cell 16, 198-210
97. Powers, J. (2004). The leukodystrophies: overview and classification. In Myelin Biology and Disorders (ed. R. A. Lazzarini), pp. 663-690 San Diego: Elsevier Academic Press.
98. Qin, Z., Ren, F., Xu, X., Ren, Y., Li, H., Wang, Y., Zhai, Y. and Chang, Z. (2009). ZNF536, a novel zinc finger protein specifically expressed in the brain, negatively regulates neuron differentiation by repressing retinoic acid-induced gene transcription. Mol. Cell. Biol. 29, 3633-3643
99. Raff, M. C., Abney, E. R., Cohen, J., Lindsay, R. and Noble, M. (1983a). Two types of astrocytes in cultures of developing rat white matter: differences in morphology, surface gangliosides, and growth characteristics. J. Neurosci. 3, 1289-1300
100. Raff, M. C., Miller, R. H. and Noble, M. (1983b). A glial progenitor cell that develops in vitro into an astrocyte or an oligodendrocyte depending on culture medium. Nature 303, 390-396
101. Richardson, W. D., Pringle, N., Mosley, M. J., Westermark, B. and Dubois- Dalcg, M. (1988). A role for platelet-derived growth factor in normal gliogenesis in the central nervous system. Cell 53, 309-319
102. Rivers, L. E., Young, K. M., Rizzi, M., Jamen, F., Psachoulia, K., Wade, A., Kessaris, N. and Richardson, W. D. (2008). PDGFRA/NG2 glia generate myelinating oligodendrocytes and piriform projection neurons in adult mice. Nat. Neurosci. 11, 1392-1401
103. Rosati, G. (2001). The prevalence of multiple sclerosis in the world: an update. Neurol. Sci. 22, 117-139
104. Rowitch, D. H. (2004). Glial specification in the vertebrate neural tube. Nat. Rev. Neurosci. 5, 409-419
105. Rowitch, D. H. and Kriegstein, A. R. (2010). Developmental genetics of vertebrate glial–cell specification. Nature 468, 214-222
106. Roy, N. S., Wang, S., Harrison-Restelli, C., Benraiss, A., Fraser, R. A., Gravel, M., Braun, P. E. and Goldman, S. A. (1999). Identification, isolation, and promoter-defined separation of mitotic oligodendrocyte progenitor cells from the adult human subcortical white matter. J. Neurosci. 19, 9986-9995
107. Roy, N. S., Cleren, C., Singh, S. K., Yang, L., Beal, M. F. and Goldman, S. A. (2006). Functional engraftment of human ES cell–derived dopaminergic neurons enriched by coculture with telomerase-immortalized midbrain astrocytes. Nat. Med. 12, 1259-1268
108. Schoenwolf, G. C. and Alvarez, I. S. (1989). Roles of neuroepithelial cell rearrangement and division in shaping of the avian neural plate. Development 106, 427-439
109. Scolding, N. (1998). Glial precursor cells in the adult human brain. Neuroscientist 4, 264-272
110. Scolding, N. J., Rayner, P. J. and Compston, D. A. S. (1999). Identification of A2B5-positive putative oligodendrocyte progenitor cells and A2B5-positive astrocytes in adult human white matter. Neuroscience 89, 1-4
111. Shenoy, A. and Blelloch, R. H. (2014). Regulation of microRNA function in somatic stem cell proliferation and differentiation. Nat. Rev. Mol. Cell Biol. 15, 565-576
112. Sherman, D. L. and Brophy, P. J. (2005). Mechanisms of axon ensheathment and myelin growth. Nat. Rev. Neurosci. 6, 683-690
113. Shi, Y., Zhao, X., Hsieh, J., Wichterle, H., Impey, S., Banerjee, S., Neveu, P. and Kosik, K. S. (2010). MicroRNA regulation of neural stem cells and neurogenesis. J. Neurosci. 30, 14931-14936
114. Sim, F. J., Lang, J. K., Waldau, B., Roy, N. S., Schwartz, T. E., Pilcher, W. H., Chandross, K. J., Natesan, S., Merrill, J. E. and Goldmanm, S. A. (2006). Complementary patterns of gene expression by human oligodendrocyte progenitors and their environment predict determinants of progenitor maintenance and differentiation. Ann. Neurol. 59, 763-779
115. Sim, F. J., McClain, C. R., Schanz, S. J., Protack, T. L., Windrem, M. S. and Goldman, S. A. (2011). CD140a identifies a population of highly myelinogenic, migration-competent and efficiently engrafting human oligodendrocyte progenitor cells. Nat. Biotechnol. 29, 934-941
116. Sommer, I. and Schachner, M. (1981). Monoclonal antibodies (O1 to O4) to oligodendrocyte cell surfaces: an immunocytological study in the central nervous system. Dev. Biol. 83, 311-327
117. Stacpoole, S. R. L., Spitzer, S., Bilican, B., Compston, A., Karadottir, R., Chandran, S. and Franklin, R. J. (2013). High yields of oligodendrocyte lineage cells from human embryonic stem cells at physiological oxygen tensions for evaluation of translational biology. Stem Cell Rep. 1, 437-450
118. Stadtfeld, M. and Hochedlinger, K. (2010). Induced pluripotency: history, mechanisms, and applications. Genes Dev. 24, 2239-2263
119. Sugimori, M., Nagao, M., Parras, C. M., Nakatani, H., Lebel, M., Guillemot, F. and Nakafuku, M. (2008). Ascl1 is required for oligodendrocyte development in the spinal cord. Development 135, 1271-1281
120. Susuki, K. and Rasband, M. N. (2008). Molecular mechanisms of node of Ranvier formation. Curr. Opin. Cell Biol. 20, 616-623
121. Syed, Y. A., Baer, A., Hofer, M. P., González, G. A., Rundle, J., Myrta, S., Huang, J. K., Zhao, C., Rossner, M. J., Trotter, M. W. B. et al. (2013). Inhibition of phosphodiesterase-4 promotes oligodendrocyte precursor cell differentiation and enhances CNS remyelination. EMBO Mol. Med. 5, 1918-1934
122. Tekki-Kessaris, N., Woodruff, R., Hall, A. C., Gaffield, W., Kimura, S., Stiles, C. D., Rowitch, D. H. and Richardson, W. D. (2001). Hedgehog-dependent oligodendrocyte lineage specification in the telencephalon. Development 128, 2545-2554
123. Thomson, J. A., Itskovitz-Eldor, J., Shapiro, S. S., Waknitz, M. A., Swiergiel, J. J., Marshall, V. S. and Jones, J. M. (1998). Embryonic stem cell lines derived from human blastocysts. Science 282, 1145-1147
124. Tripathi, R. B., Rivers, L. E., Young, K. M., Jamen, F. and Richardson, W. D. (2010). NG2 glia generate new oligodendrocytes but few astrocytes in a murine experimental autoimmune encephalomyelitis model of demyelinating disease. J. Neurosci. 30, 16383-16390
125. Vallstedt, A., Klos, J. M. and Ericson, J. (2005). Multiple dorsoventral origins of oligodendrocyte generation in the spinal cord and hindbrain. Neuron 45, 55-67
126. Wang, S.-Z., Dulin, J., Wu, H., Hurlock, E., Lee, S.-E., Jansson, K. and Lu, Q. R. (2006). An oligodendrocyte-specific zinc-finger transcription regulator cooperates with Olig2 to promote oligodendrocyte differentiation. Development 133, 3389-3398
127. Wang, J., O’Bara, M. A., Pol, S. U. and Sim, F. J. (2013a). CD133/CD140a-based isolation of distinct human multipotent neural progenitor cells and oligodendrocyte progenitor cells. Stem Cells Dev. 22, 2121-2131
128. Wang, S., Bates, J., Li, X., Schanz, S., Chandler-Militello, D., Levine, C., Maherali, N., Studer, L., Hochedlinger, K., Windrem, M. et al. (2013b). Human iPSC-derived oligodendrocyte progenitor cells can myelinate and rescue a mouse model of congenital hypomyelination. Cell Stem Cell 12, 252-264
129. Wang, J., Pol, S. U., Haberman, A. K., Wang, C., O’Bara, M. A. and Sim, F. J. (2014). Transcription factor induction of human oligodendrocyte progenitor fate and differentiation. Proc. Natl. Acad. Sci. USA 111, E2885-E2894
130. Wegner, M. and Stolt, C. S. (2005). From stem cells to neurons and glia: a Soxist’s view of neural development. Trends Neurosci. 28, 583-588
131. Weider, M., Reiprich, S. and Wegner, M. (2013). Sox appeal – Sox10 attracts epigenetic and transcriptional regulators in myelinating glia. Biol. Chem. 394, 1583-1593
132. Windrem, M. S., Nunes, M. C., Rashbaum, W. K., Schwartz, T. H., Goodman, R. A., McKhann, G., Roy, N. S. and Goldman, S. A. (2004). Fetal and adult human oligodendrocyte progenitor cell isolates myelinate the congenitally dysmyelinated brain. Nat. Med. 10, 93-97
133. Windrem, M. S., Schanz, S. J., Guo, M., Tian, G.-F., Washco, V., Stanwood, N., Rasband, M., Roy, N. S., Nedergaard, M., Havton, L. A. et al. (2008). Neonatal chimerization with human glial progenitor cells can both remyelinate and rescue the otherwise lethally hypomyelinated shiverer mouse. Cell Stem Cell 2, 553-565
134. Windrem, M. S., Schanz, S. J., Morrow, C., Munir, J., Chandler-Militello, D., Wang, S. and Goldman, S. A. (2014). A competitive advantage by neonatally engrafted human glial progenitors yields mice whose brains are chimeric for human glia. J. Neurosci. 34, 16153-16161
135. Wolswijk, G. and Noble, M. (1989). Identification of an adult-specific glial progenitor cell. Development 105, 387-400
136. Woodruff, R. H., Tekki-Kessaris, N., Stiles, C. D., Rowitch, D. H. and Richardson, W. D. (2001). Oligodendrocyte development in the spinal cord and telencephalon: common themes and new perspectives. Int. J. Dev. Neurosci. 19, 379-385
137. Xin, M., Yue, T., Ma, Z., Wu, F.-F., Gow, A. and Lu, Q. R. (2005). Myelinogenesis and axonal recognition by oligodendrocytes in brain are uncoupled in Olig1-null mice. J. Neurosci. 25, 1354-1365
138. Yamanaka, S. (2007). Strategies and new developments in the generation of patient-specific pluripotent stem cells. Cell Stem Cell 1, 39-49
139. Yamanaka, S. (2008). Pluripotency and nuclear reprogramming. Philos. Trans. R. Soc. B Biol. Sci. 363, 2079-2087
140. Yang, N., Zuchero, J. B., Ahlenius, H., Marro, S., Ng, Y. H., Vierbuchen, T., Hawkins, J. S., Geissler, R., Barres, B. A. and Wernig, M. (2013). Generation of oligodendroglial cells by direct lineage conversion. Nat. Biotechnol. 31, 434-439
141. Young, R. A. (2011). Control of the embryonic stem cell state. Cell 144, 940-954
142. Yu, Y., Casaccia, P. and Lu, Q. R. (2010). Shaping the oligodendrocyte identity by epigenetic control. Epigenetics 5, 124-128
143. Yu, Y., Chen, Y., Kim, B., Wang, H., Zhao, C., He, X., Liu, L., Liu, W., Wu, L. M. N., Mao, M. et al. (2013). Olig2 targets chromatin remodelers to enhancers to initiate oligodendrocyte differentiation. Cell 152, 248-261
144. Yuan, S. H., Martin, J., Elia, J., Flippin, J., Paramban, R. I., Hefferan, M. P., Vidal, J. G., Mu, Y., Killian, R. L., Israel, M. A. et al. (2011). Cell-surface marker signatures for the isolation of neural stem cells, glia and neurons derived from human pluripotent stem cells. PLoS ONE 6, e17540
145. Zhang, S.-C. (2001). Defining glial cells during CNS development. Nat. Rev. Neurosci. 2, 840-843
146. Zhang, H. and Miller, R. H. (1996). Density-dependent feedback inhibition of oligodendrocyte precursor expansion. J. Neurosci. 16, 6886-6895
147. Zhang, Y., Chen, K., Sloan, S. A., Bennett, M. L., Scholze, A. R., O’Keeffe, S., Phatnani, H. P., Guarnieri, P., Caneda, C., Ruderisch, N. et al. (2014). An RNAsequencing transcriptome and splicing database of glia, neurons, and vascular cells of the cerebral cortex. J. Neurosci. 34, 11929-11947
148. Zhao, X., He, X., Han, X., Yu, Y., Ye, F., Chen, Y., Hoang, T., Xu, X., Mi, Q.-S., Xin, M. et al. (2010). MicroRNA-mediated control of oligodendrocyte differentiation. Neuron 65, 612-626
149. Zhao, W., Ji, X., Zhang, F., Li, L. and Ma, L. (2012). Embryonic stem cell markers. Molecules 17, 6196-6236
150. Zhu, Q., Whittemore, S. R., Devries, W. H., Zhao, X., Kuypers, N. J., and Qiu, M. (2011). Dorsally-derived oligodendrocytes in the spinal cord contribute to axonal myelination during development and remyelination following focal demyelination. Glia 59, 1612-1621
151. Zuchero, J. B. and Barres, B. A. (2013). Intrinsic and extrinsic control of oligodendrocyte development. Curr. Opin. Neurobiol. 23, 914-920.