Separated at birth? the functional and molecular divergence of OLIG1 and OLIG2

Nature Reviews Neuroscience

Volumn 13, Issue 12, 2012, Pages 819-831

  Meijer, Dimphna H ^a   Kane, Michael F ^a   Mehta, Shwetal ^a   Liu, Hongye ^b   Harrington, Emily ^c   Taylor, Christopher M ^a,d   Stiles, Charles D ^a   Rowitch, David H ^c  

^a DANA FARBER CANCER INSTITUTE   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^d EMD Serono Research Institute   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NUCLEIC ACID BINDING PROTEIN; OLIGODENDROCYTE TRANSCRIPTION FACTOR 1 PROTEIN; OLIGODENDROCYTE TRANSCRIPTION FACTOR 2; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

CEREBRAL PALSY; GLIOBLASTOMA; HUMAN; MOLECULAR BIOLOGY; MULTIPLE SCLEROSIS; NEUROLOGIC DISEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN MODIFICATION; PROTEIN PROCESSING; PROTEIN STRUCTURE; REVIEW;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BRAIN; HUMANS; NERVE TISSUE PROTEINS; NERVOUS SYSTEM DISEASES; NEURONS; OLIGODENDROGLIA; PROTEIN PROCESSING, POST-TRANSLATIONAL;

EID: 84872020822     PISSN: 1471003X     EISSN: 14710048     Source Type: Journal    
DOI: 10.1038/nrn3386     Document Type: Review

References (128)

1. Charcot, J. M. Histologie de la sclose en plaques. Gazette des hopitaux 41, 554-555 (1868) (in French).
2. Marburg, O. Die sogenannte akute multiple Sklerose. Jahrb. Psychiatrie 27, 211-312 (1906) (in German).
3. Prineas, J. W. & Connell, F. Remyelination in multiple sclerosis. Ann. Neurol. 5, 22-31 (1979).
4. Lucchinetti, C. et al. A quantitative analysis of oligodendrocytes in multiple sclerosis lesions. A study of 113 cases. Brain 122, 2279-2295 (1999).
5. Warf, B. C., Fok-Seang, J. & Miller, R. H. Evidence for the ventral origin of oligodendrocyte precursors in the rat spinal cord. J. Neurosci. 11, 2477-2488 (1991).
6. Pringle, N. P. & Richardson, W. D. A singularity of PDGF alpha-receptor expression in the dorsoventral axis of the neural tube may define the origin of the oligodendrocyte lineage. Development 117, 525-533 (1993).
7. Yu, W. P., Collarini, E. J., Pringle, N. P. & Richardson, W. D. Embryonic expression of myelin genes: evidence for a focal source of oligodendrocyte precursors in the ventricular zone of the neural tube. Neuron 12, 1353-1362 (1994).
8. Timsit, S. et al. Oligodendrocytes originate in a restricted zone of the embryonic ventral neural tube defined by DM20 mRNA expression. J. Neurosci. 15, 1012-1024 (1995).
9. Cameron-Curry, P. & Le Douarin, N. M. Oligodendrocyte precursors originate from both the dorsal and the ventral parts of the spinal cord. Neuron 15, 1299-1310 (1995).
10. Raff, M. C., Miller, R. H. & Noble, M. A glial progenitor cell that develops in vitro into an astrocyte or an oligodendrocyte depending on culture medium. Nature 303, 390-396 (1983).
11. Rao, M. S., Noble, M. & Mayer-Proschel, M. A tripotential glial precursor cell is present in the developing spinal cord. Proc. Natl Acad. Sci. USA 95, 3996-4001 (1998).
12. Lee, J. C., Mayer-Proschel, M. & Rao, M. S. Gliogenesis in the central nervous system. Glia 30, 105-121 (2000).
13. Jessell, T. M. Neuronal specification in the spinal cord: inductive signals and transcriptional codes. Nature Rev. Genet. 1, 20-29 (2000).
14. Lu, Q. R. et al. Sonic hedgehog-regulated oligodendrocyte lineage genes encoding bHLH proteins in the mammalian central nervous system. Neuron 25, 317-329 (2000).
15. Zhou, Q., Wang, S. & Anderson, D. J. Identification of a novel family of oligodendrocyte lineage-specific basic helix-loop-helix transcription factors. Neuron 25, 331-343 (2000).
16. Takebayashi, H. et al. 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. 99, 143-148 (2000).
17. Lu, Q. R. et al. Common developmental requirement for Olig function indicates a motor neuron/oligodendrocyte connection. Cell 109, 75-86 (2002).
18. Zhou, Q. & Anderson, D. J. The bHLH transcription factors OLIG2 and OLIG1 couple neuronal and glial subtype specification. Cell 109, 61-73 (2002).
19. Cai, J. et al. Generation of oligodendrocyte precursor cells from mouse dorsal spinal cord independent of Nkx6 regulation and Shh signaling. Neuron 45, 41-53 (2005).
20. Vallstedt, A., Klos, J. M. & Ericson, J. Multiple dorsoventral origins of oligodendrocyte generation in the spinal cord and hindbrain. Neuron 45, 55-67 (2005).
21. Fogarty, M., Richardson, W. D. & Kessaris, N. A subset of oligodendrocytes generated from radial glia in the dorsal spinal cord. Development 132, 1951-1959 (2005).
22. Menn, B. et al. Origin of oligodendrocytes in the subventricular zone of the adult brain. J. Neurosci. 26, 7907-7918 (2006).
23. Fancy, S. P., Zhao, C. & Franklin, R. J. Increased expression of Nkx2.2 and Olig2 identifies reactive oligodendrocyte progenitor cells responding to demyelination in the adult CNS. Mol. Cell Neurosci. 27, 247-254 (2004).
24. Buffo, A. et al. Expression pattern of the transcription factor Olig2 in response to brain injuries: implications for neuronal repair. Proc. Natl Acad. Sci. USA 102, 18183-18188 (2005).
25. Arnett, H. A. et al. bHLH transcription factor Olig1 is required to repair demyelinated lesions in the CNS. Science 306, 2111-2115 (2004).
26. Georgieva, L. et al. Convergent evidence that oligodendrocyte lineage transcription factor 2 (OLIG2) and interacting genes influence susceptibility to schizophrenia. Proc. Natl Acad. Sci. USA 103, 12469-12474 (2006).
27. Sims, R. et al. Evidence that variation in the oligodendrocyte lineage transcription factor 2 (OLIG2) gene is associated with psychosis in Alzheimer's disease. Neurosci. Lett. 461, 54-59 (2009).
28. Huang, K. et al. Positive association between OLIG2 and schizophrenia in the Chinese Han population. Hum. Genet. 122, 659-660 (2008).
29. Chakrabarti, L. et al. Olig1 and Olig2 triplication causes developmental brain defects in Down syndrome. Nature Neurosci. 13, 927-934 (2010).
30. Bouvier, C. et al. Shared oligodendrocyte lineage gene expression in gliomas and oligodendrocyte progenitor cells. J. Neurosurg. 99, 344-350 (2003).
31. Ligon, K. L. et al. The oligodendroglial lineage marker OLIG2 is universally expressed in diffuse gliomas. J. Neuropathol. Exp. Neurol. 63, 499-509 (2004).
32. Lu, Q. R. et al. Oligodendrocyte lineage genes (OLIG) as molecular markers for human glial brain tumors. Proc. Natl Acad. Sci. USA 98, 10851-10856 (2001).
33. Marie, Y. et al. OLIG2 as a specific marker of oligodendroglial tumour cells. Lancet 358, 298-300 (2001).
34. Ohnishi, A. et al. Expression of the oligodendroglial lineage-associated markers Olig1 and Olig2 in different types of human gliomas. J. Neuropathol. Exp. Neurol. 62, 1052-1059 (2003).
35. Ledent, V., Paquet, O. & Vervoort, M. Phylogenetic analysis of the human basic helix-loop-helix proteins. Genome Biol. 3, research0030- research0030.18 (2002).
36. Gray, P. A. et al. Mouse brain organization revealed through direct genome-scale TF expression analysis. Science 306, 2255-2257 (2004).
37. Malatesta, P. et al. Neuronal or glial progeny: regional differences in radial glia fate. Neuron 37, 751-764 (2003).
38. Tsai, H. H. et al. Regional astrocyte allocation regulates CNS synaptogenesis and repair. Science 337, 358-362 (2012).
39. Ligon, K. L. et al. Oligregulated lineage-restricted pathway controls replication competence in neural stem cells and malignant glioma. Neuron 53, 503-517 (2007).
40. Chen, J. A. et al. Mir173p controls spinal neural progenitor patterning by regulating Olig2/Irx3 cross-repressive loop. Neuron 69, 721-735 (2011).
41. Takebayashi, H. et al. Non-overlapping expression of Olig3 and Olig2 in the embryonic neural tube. Mech. Dev. 113, 169-174 (2002).
42. Liu, Z. et al. Control of precerebellar neuron development by Olig3 bHLH transcription factor. J. Neurosci. 28, 10124-10133 (2008).
43. Lee, S. K., Lee, B., Ruiz, E. C. & Pfaff, S. L. Olig2 and Ngn2 function in opposition to modulate gene expression in motor neuron progenitor cells. Genes Dev. 19, 282-294 (2005).
44. Li, H., de Faria, J. P., Andrew, P., Nitarska, J. & Richardson, W. D. Phosphorylation regulates OLIG2 cofactor choice and the motor neuron-oligodendrocyte fate switch. Neuron 69, 918-929 (2011).
45. Furusho, M. et al. Involvement of the Olig2 transcription factor in cholinergic neuron development of the basal forebrain. Dev. Biol. 293, 348-357 (2006).
46. Xin, M. et al. Myelinogenesis and axonal recognition by oligodendrocytes in brain are uncoupled in Olig1null mice. J. Neurosci. 25, 1354-1365 (2005).
47. Marshall, C. A., Novitch, B. G. & Goldman, J. E. Olig2 directs astrocyte and oligodendrocyte formation in postnatal subventricular zone cells. J. Neurosci. 25, 7289-7298 (2005).
48. Cahoy, J. D. et al. A transcriptome database for astrocytes, neurons, and oligodendrocytes: a new resource for understanding brain development and function. J. Neurosci. 28, 264-278 (2008).
49. Chen, Y. et al. The basic helix-loop-helix transcription factor Olig2 is critical for reactive astrocyte proliferation after cortical injury. J. Neurosci. 28, 10983-10989 (2008).
50. Kageyama, R. & Nakanishi, S. Helix-loop-helix factors in growth and differentiation of the vertebrate nervous system. Curr. Opin. Genet. Dev. 7, 659-665 (1997).
51. Lee, J. E. Basic helix-loop-helix genes in neural development. Curr. Opin. Neurobiol. 7, 13-20 (1997).
52. Parras, C. M. et al. Mash1 specifies neurons and oligodendrocytes in the postnatal brain. EMBO J. 23, 4495-4505 (2004).
53. Singh, S. K. et al. Identification of human brain tumour initiating cells. Nature 432, 396-401 (2004).
54. Bao, S. et al. Targeting cancer stem cells through L1CAM suppresses glioma growth. Cancer Res. 68, 6043-6048 (2008).
55. Barrett, L. E. et al. Self-renewal does not predict tumor growth potential in mouse models of high-grade glioma. Cancer Cell 21, 11-24 (2012).
56. Appolloni, I. et al. Antagonistic modulation of gliomagenesis by Pax6 and Olig2 in PDGF-induced oligodendroglioma. Int. J. Cancer 131, e1078-e1087 (2012).
57. Mehta, S. et al. The central nervous system-restricted transcription factor Olig2 opposes p53 responses to genotoxic damage in neural progenitors and malignant glioma. Cancer Cell 19, 359-371 (2011).
58. Kitada, M. & Rowitch, D. H. Transcription factor coexpression patterns indicate heterogeneity of oligodendroglial subpopulations in adult spinal cord. Glia 54, 35-46 (2006).
59. Chang, A., Tourtellotte, W. W., Rudick, R. & Trapp, B. D. Premyelinating oligodendrocytes in chronic lesions of multiple sclerosis. N. Engl. J. Med. 346, 165-173 (2002).
60. Kuhlmann, T. et al. Differentiation block of oligodendroglial progenitor cells as a cause for remyelination failure in chronic multiple sclerosis. Brain 131, 1749-1758 (2008).
61. Billiards, S. S. et al. Myelin abnormalities without oligodendrocyte loss in periventricular leukomalacia. Brain Pathol. 18, 153-163 (2008).
62. Verney, C. et al. Microglial reaction in axonal crossroads is a hallmark of noncystic periventricular white matter injury in very preterm infants. J. Neuropathol. Exp. Neurol. 71, 251-264 (2012).
63. Fancy, S. P. et al. Axin2 as regulatory and therapeutic target in newborn brain injury and remyelination. Nature Neurosci. 14,1009-1016 (2011).
64. Pekny, M. & Nilsson, M. Astrocyte activation and reactive gliosis. Glia 50, 427-434 (2005).
65. Gabay, L., Lowell, S., Rubin, L. L. & Anderson, D. J. Deregulation of dorsoventral patterning by FGF confers trilineage differentiation capacity on CNS stem cells in vitro. Neuron 40, 485-499 (2003).
66. Setoguchi, T. & Kondo, T. Nuclear export of OLIG2 in neural stem cells is essential for ciliary neurotrophic factor-induced astrocyte differentiation. J. Cell Biol. 166, 963-968 (2004).
67. Muroyama, Y., Fujiwara, Y., Orkin, S. H. & Rowitch, D. H. Specification of astrocytes by bHLH protein SCL in a restricted region of the neural tube. Nature 438, 360-363 (2005).
68. Dimou, L., Simon, C., Kirchhoff, F., Takebayashi, H. & Gotz, M. Progeny of Oligexpressing progenitors in the gray and white matter of the adult mouse cerebral cortex. J. Neurosci. 28, 10434-10442 (2008).
69. Komitova, M., Serwanski, D. R., Lu, Q. R. & Nishiyama, A. NG2 cells are not a major source of reactive astrocytes after neocortical stab wound injury. Glia 59, 800-809 (2011).
70. Zawadzka, M. et al. CNS-resident glial progenitor/stem cells produce Schwann cells as well as oligodendrocytes during repair of CNS demyelination. Cell Stem Cell 6, 578-590 (2010).
71. Tripathi, R. B., Rivers, L. E., Young, K. M., Jamen, F. & Richardson, W. D. NG2 glia generate new oligodendrocytes but few astrocytes in a murine experimental autoimmune encephalomyelitis model of demyelinating disease. J. Neurosci. 30, 16383-16390 (2010).
72. Buffo, A. et al. Origin and progeny of reactive gliosis: a source of multipotent cells in the injured brain. Proc. Natl Acad. Sci. USA 105, 3581-3586 (2008).
73. Magnus, T. et al. Evidence that nucleocytoplasmic Olig2 translocation mediates brain-injury-induced differentiation of glial precursors to astrocytes. J. Neurosci. Res. 85, 2126-2137 (2007).
74. Zhao, J. W., Raha-Chowdhury, R., Fawcett, J. W. & Watts, C. Astrocytes and oligodendrocytes can be generated from NG2+ progenitors after acute brain injury: intracellular localization of oligodendrocyte transcription factor 2 is associated with their fate choice. Eur. J. Neurosci. 29, 1853-1869 (2009).
75. Cassiani-Ingoni, R. et al. Cytoplasmic translocation of Olig2 in adult glial progenitors marks the generation of reactive astrocytes following autoimmune inflammation. Exp. Neurol. 201, 349-358 (2006).
76. Fernandez, F. & Garner, C. C. Over-inhibition: a model for developmental intellectual disability. Trends Neurosci. 30, 497-503 (2007).
77. Belichenko, P. V. et al. Synaptic structural abnormalities in the Ts65Dn mouse model of Down syndrome. J. Comp. Neurol. 480, 281-298 (2004).
78. Haydar, T. F. & Reeves, R. H. Trisomy 21 and early brain development. Trends Neurosciences 35, 81-91 (2012).
79. Lu, J. et al. OLIG2 over-expression impairs proliferation of human Down syndrome neural progenitors. Hum. Mol. Genet. 21, 2330-2340 (2012).
80. Wang, S. Z. et al. An oligodendrocyte-specific zinc-finger transcription regulator cooperates with Olig2 to promote oligodendrocyte differentiation. Development 133, 3389-3398 (2006).
81. Massari, M. E. & Murre, C. Helix-loop-helix proteins: regulators of transcription in eucaryotic organisms. Mol. Cell. Biol. 20, 429-440 (2000).
82. Zhou, Q., Choi, G. & Anderson, D. J. The bHLH transcription factor Olig2 promotes oligodendrocyte differentiation in collaboration with Nkx2.2. Neuron 31, 791-807 (2001).
83. Novitch, B. G., Chen, A. I. & Jessell, T. M. Coordinate regulation of motor neuron subtype identity and pan-neuronal properties by the bHLH repressor Olig2. Neuron 31, 773-789 (2001).
84. Mizuguchi, R. et al. Combinatorial roles of olig2 and neurogenin2 in the coordinated induction of pan-neuronal and subtype-specific properties of motoneurons. Neuron 31, 757-771 (2001).
85. Kuspert, M., Hammer, A., Bosl, M. R. & Wegner, M. Olig2 regulates Sox10 expression in oligodendrocyte precursors through an evolutionary conserved distal enhancer. Nucleic Acids Res. 39, 1280-1293 (2011).
86. Mazzoni, E. O. et al. Embryonic stem cell-based mapping of developmental transcriptional programs. Nature Methods 8, 1056-1058 (2011).
87. Weng, Q. et al. Dual-mode modulation of smad signaling by smad-interacting protein sip1 is required for myelination in the central nervous system. Neuron 73, 713-728 (2012).
88. Guo, X. et al. Delayed onset of experimental autoimmune encephalomyelitis in Olig1 deficient mice. PLoS ONE 5, e13083 (2010).
89. Chen, Y. et al. The oligodendrocyte-specific G protein-coupled receptor GPR17 is a cell-intrinsic timer of myelination. Nature Neurosci. 12, 1398-1406 (2009).
90. Li, H., Lu, Y., Smith, H. K. & Richardson, W. D. Olig1 and Sox10 interact synergistically to drive myelin basic protein transcription in oligodendrocytes. J. Neurosci. 27, 14375-14382 (2007).
91. Beckett, D. Regulated assembly of transcription factors and control of transcription initiation. J. Mol. Biol. 314, 335-352 (2001).
92. Featherstone, M. Coactivators in transcription initiation: here are your orders. Curr. Opin. Genet. Dev. 12, 149-155 (2002).
93. Torchia, J., Glass, C. & Rosenfeld, M. G. Coactivators and corepressors in the integration of transcriptional responses. Curr. Opin. Cell Biol. 10, 373-383 (1998).
94. Ravasi, T. et al. An atlas of combinatorial transcriptional regulation in mouse and man. Cell 140, 744-752 (2010).
95. Samanta, J. & Kessler, J. A. Interactions between ID and OLIG proteins mediate the inhibitory effects of BMP4 on oligodendroglial differentiation. Development 131, 4131-4142 (2004).
96. Benezra, R., Davis, R. L., Lockshon, D., Turner, D. L. & Weintraub, H. The protein Id: a negative regulator of helix-loop-helix DNA binding proteins. Cell 61, 49-59 (1990).
97. Poulin, G., Lebel, M., Chamberland, M., Paradis, F. W. & Drouin, J. Specific protein-protein interaction between basic helix-loop-helix transcription factors and homeoproteins of the Pitx family. Mol. Cell. Biol. 20, 4826-4837 (2000).
98. Babu, D. A., Chakrabarti, S. K., Garmey, J. C. & Mirmira, R. G. Pdx1 and BETA2/NeuroD1 participate in a transcriptional complex that mediates short-range DNA looping at the insulin gene. J. Biol. Chem. 283, 8164-8172 (2008).
99. Makarenkova, H. P., Gonzalez, K. N., Kiosses, W. B. & Meech, R. Barx2 controls myoblast fusion and promotes MyoD-mediated activation of the smooth muscle α-actin gene. J. Biol. Chem. 284, 14866-14874 (2009).
100. Sun, T. et al. Olig bHLH proteins interact with homeodomain proteins to regulate cell fate acquisition in progenitors of the ventral neural tube. Curr. Biol. 11, 1413-1420 (2001).
101. Fukuda, S., Kondo, T., Takebayashi, H. & Taga, T. Negative regulatory effect of an oligodendrocytic bHLH factor OLIG2 on the astrocytic differentiation pathway. Cell Death Differ. 11, 196-202 (2004).
102. Ogryzko, V. V., Schiltz, R. L., Russanova, V., Howard, B. H. & Nakatani, Y. The transcriptional coactivators p300 and CBP are histone acetyltransferases. Cell 87, 953-959 (1996).
103. Ikushima, H. et al. An Idlike molecule, HHM, is a synexpression group-restricted regulator of TGF-β signalling. EMBO J. 27, 2955-2965 (2008).
104. Huillard, E. et al. Disruption of CK2β in embryonic neural stem cells compromises proliferation and oligodendrogenesis in the mouse telencephalon. Mol. Cell. Biol. 30, 2737-2749 (2010).
105. Sun, Y. et al. Phosphorylation state of Olig2 regulates proliferation of neural progenitors. Neuron 69, 906-917 (2011).
106. Sun, T. et al. 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. 23, 9547-9556 (2003).
107. Niu, J. et al. Phosphorylated olig1 localizes to the cytosol of oligodendrocytes and promotes membrane expansion and maturation. Glia 60, 1427-1436 (2012).
108. Gill, G. SUMO and ubiquitin in the nucleus: different functions, similar mechanisms? Genes Dev. 18, 2046-2059 (2004).
109. Hay, R. T. SUMO: a history of modification. Mol. Cell 18, 1-12 (2005).
110. Johnson, E. S. Protein modification by SUMO. Annu. Rev. Biochem. 73, 355-382 (2004).
111. Verger, A., Perdomo, J. & Crossley, M. Modification with SUMO. A role in transcriptional regulation. EMBO Rep. 4, 137-142 (2003).
112. Huang, T. T., Wuerzberger-Davis, S. M., Wu, Z. H. & Miyamoto, S. Sequential modification of NEMO/IKKγ by SUMO1 and ubiquitin mediates NFκB activation by genotoxic stress. Cell 115, 565-576 (2003).
113. Hay, R. T. Modifying NEMO. Nature Cell Biol. 6, 89-91 (2004).
114. Imoto, S. et al. Sumoylation of Smad3 stimulates its nuclear export during PIASy-mediated suppression of TGF-β signaling. Biochem. Biophys. Res. Commun. 370, 359-365 (2008).
115. Martin, S., Wilkinson, K. A., Nishimune, A. & Henley, J. M. Emerging extranuclear roles of protein SUMOylation in neuronal function and dysfunction. Nature Rev. Neurosci. 8, 948-959 (2007).
116. Zhou, F., Xue, Y., Lu, H., Chen, G. & Yao, X. A genome-wide analysis of sumoylation-related biological processes and functions in human nucleus. FEBS Lett. 579, 3369-3375 (2005).
117. Frazer, K. A. et al. Evolutionarily conserved sequences on human chromosome 21. Genome Res. 11, 1651-1659 (2001).
118. Muskal, S. M., Holbrook, S. R. & Kim, S. H. Prediction of the disulfide-bonding state of cysteine in proteins. Protein Eng. 3, 667-672 (1990).
119. Smith, E. & Shilatifard, A. The chromatin signaling pathway: diverse mechanisms of recruitment of histone-modifying enzymes and varied biological outcomes. Mol. Cell 40, 689-701 (2010).
120. elHusseini Ael, D. & Bredt, D. S. Protein palmitoylation: a regulator of neuronal development and function. Nature Rev. Neurosci. 3, 791-802 (2002).
121. Rowitch, D. H., Lu, Q. R., Kessaris, N. & Richardson, W. D. An. 'oligarchy' rules neural development. Trends Neurosci. 25, 417-422 (2002).
122. Muller, T. et al. The bHLH factor Olig3 coordinates the specification of dorsal neurons in the spinal cord. Genes Dev. 19, 733-743 (2005).
123. Ligon, K. L. et al. Development of NG2 neural progenitor cells requires Olig gene function. Proc. Natl Acad. Sci. USA 103, 7853-7858 (2006).
124. Miyoshi, G., Butt, S. J., Takebayashi, H. & Fishell, G. Physiologically distinct temporal cohorts of cortical interneurons arise from telencephalic Oligexpressing precursors. J. Neurosci. 27, 7786-7798 (2007).
125. Plenge, R. M. et al. Two independent alleles at 6q23 associated with risk of rheumatoid arthritis. Nature Genet. 39, 1477-1482 (2007).
126. Thomson, W. et al. Rheumatoid arthritis association at 6q23. Nature Genet. 39, 1431-1433 (2007).
127. Buser, J. R. et al. Arrested preoligodendrocyte maturation contributes to myelination failure in premature infants. Ann. Neurol. 71, 93-109 (2012).
128. Hack, M. A. et al. Neuronal fate determinants of adult olfactory bulb neurogenesis. Nature Neurosci. 8, 865-872 (2005).