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The bHLH Transcription Factors OLIG2 and OLIG1 Couple Neuronal and Glial Subtype Specification
Open accessAbstract
OLIG1 and OLIG2 are basic-helix-loop-helix (bHLH) transcription factors expressed in the pMN domain of the spinal cord, which sequentially generates motoneurons and oligodendrocytes. In Olig1/2 double-mutant mice, motoneurons are largely eliminated, and oligodendrocyte differentiation is abolished. Lineage tracing data suggest that Olig1(-/-)2(-/-) pMN progenitors instead generate V2 interneurons and then astrocytes. This apparent conversion likely reflects independent roles for OLIG1/2 in specifying motoneuron and oligodendrocyte fates. Olig genes therefore couple neuronal and glial subtype specification, unlike proneural bHLH factors that control the neuron versus glia decision. Our results suggest that in the spinal cord, Olig and proneural genes comprise a combinatorial code for the specification of neurons, astrocytes, and oligodendrocytes, the three fundamental cell types of the central nervous system.
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“Cell type-specific transcription factor expression is important for cell fate determination and cell differentiation (e.g., Neu-roD for specification of neuron cell fate, Olig2 for specification of oligodendrocyte fate, and GM98/Myrf for oligodendrocyte differentiation; Lee et al., 1995;Zhou and Anderson, 2002;Emery et al., 2009).”
From An RNA-Sequencing Transcriptome and Splicing Database of Glia, Neurons, and Vascular Cells of the Cerebral Cortex (2014) · cites this paper as Zhou and Anderson, 2002
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“In heterozygotes, Olig2-hGFP -derived precursors gave is restricted to oligodendrocyte precursors (Lu et al., 2000; Zhou et al., 2000), nearly all OLIG2-positive cells rise to Islet1/2 (cid:2) motoneurons (Figure 3A, yellow cells) but not Chx10 (cid:2) V2 interneurons (Figure 3B).”
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“In heterozygotes, Olig2-hGFP -derived precursors gave is restricted to oligodendrocyte precursors (Lu et al., 2000; Zhou et al., 2000), nearly all OLIG2-positive cells rise to Islet1/2 (cid:2) motoneurons (Figure 3A, yellow cells) but not Chx10 (cid:2) V2 interneurons (Figure 3B).”
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“At this stage, they have continued expression of Olig1 and Olig2, which suggest essential roles in the maintenance of the OPC phenotype (Emery & Lu, 2015; Zhou & Anderson, 2002).”
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“Thus, mutual antagonism between dorsally expressed Irx3 and ventrally expressed Olig2 set the border between the domains where dorsal V2 and ventral motor neurons arise (Briscoe et al., 2000; Mizuguchi et al., 2001; Novitch et al., 2001; Zhou and Anderson, 2002).”
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“OLIG1/2 are basis-helix-loop-helix transcriptions factors and are expressed in oligodendrocyte precursors [46].”
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“ing to the HA-tagged mouse Olig2(1-177) coding region was amplified using 5”
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“…through direct binding to Olig1 and Olig2, class B HLH transcription factors that promote specification and differentiation of oligodendrocytes (Lu et al., 2002; MekkiDauriac et al., 2002; Rowitch et al., 2002; Takebayashi et al., 2002; Zhou and Anderson, 2002; Rowitch, 2004; Ligon et al., 2006).”
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“…cells 90 are also expressed by reactive astrocytes (Duggal et al., 1997, Geisert et al., 1990, 91 Oki et al., 2010) and Olig1 and Olig2 expressed by motor neurons with Olig2 are 92 also shown to be required for NSC proliferation and maintenance (Ligon et al., 2007, 93 Zhou and Anderson, 2002).”
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“The related transcription factorOlig1 is expressed in cells of the oligodendrocyte lineage at a slightly later stage of differentiation (Schebesta and Serluca, 2009; Zhou and Anderson, 2002) and acts, together with Sox10, to activate thembp promoter in both fish andmammals (Li et al.”
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“OLIG2 Oligodendrocyte differentiation in the spinal cord [174] Universally expressed in gliomas [176]”
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“Genes of the olig family (olig1, olig2, and olig3) have key roles in the specification of motor neurons, dorsal interneurons, and oligodendrocytes in the vertebrate CNS [18,23,24,28-30].”
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“, 2002; Zhou and Anderson, 2002), but mutation of Olig1 and Olig2 drives the cells toward an astrocytic lineage (Zhou and Anderson, 2002).”
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“The results of this study suggest that PRPs are a unique population of oligodendrocyte precursors, with both distinct and similar properties to other OLPs described and reviewed previously (Liu and Rao, 2003; Noble et al., 2004; Rowitch, 2004).”
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“This new interpretation is consistent with the recent genetic evidence that oligodendrocyte development in embryonic mouse spinal cord is coupled to motoneuron development (Lu et al., 2002; Zhou and Anderson, 2002).”
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“We observed enrichment of many HMG-domain TF-family members, namely Sox1, Sox2, Sox4, Sox5, Sox6, Sox8, Sox10, Sox11, Transcription factor 7 like 1 (Tcf7l1), Tcf7l2, WD repeat and HMG-box DNA binding protein 1 (Wdhd1) and Thymocyte selectionassociated HMG box (Tox1).”
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“In the absence of OLIG2, OPCs are converted to astrocytes suggesting that OLIG2 not only promotes the oligodendrocyte fate but also serves to inhibit astrocyte fate (Takebayashi et al., 2002; Zhou and Anderson, 2002; Zhu et al., 2012).”
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“With the exception of OLIG3 , OLIG genes are specifically expressed in the CNS and have critical roles in promoting motor neuron (MN) and oligodendrocyte (OL) development and in inhibiting astrocyte differentiation in mic”
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“Olig1 and Olig2 are necessary for development of both motor neurons and OPCs [4,5], therefore, regulatory mechanisms must exist to specify Olig1/2 pMN precursors for either motor neuron or OPC fate.”
BackgroundCanonical Wnt Signalling Requires the BMP Pathway to Inhibit Oligodendrocyte Maturation
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“The antibody pairs used to detect internal antibodies were GFAP (glial fibrillary acidic protein) and Olig2.”
BackgroundInfluentialHh and Wnt signaling regulate formation of olig2+ neurons in the zebrafish cerebellum.
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Selective Expression of a Subset of Neuronal Genes in Oligodendroglioma with Chromosome 1p Loss
Mukasa, A., Ueki, K., Ge, X.-J., Ishikawa, S., Ide, T., Fujimaki, T., Nishikawa, R., Asai, A., Kirino, T., & Aburatani, H. (2004) · Brain Pathology · doi:10.1111/j.1750-3639.2004.tb00495.x · Cited by 61
“In line with such a still hypothetical proposition, recent studies indicated that some oligodendrocytes might share the same progenitor cells with neurons (13, 28).”
ResultWedel, M., Fröb, F., Elsesser, O., Wittmann, M., Lie, D. C., Reis, A., & Wegner, M. (2020) · Nucleic Acids Research · doi:10.1093/nar/gkaa218 · Cited by 68
“Heterodimerization with class II bHLH factors was much more likely of relevance, as all three oligodendroglial class II proteins promote oligodendrocyte differentiation and myelination (6,8,9).”
BackgroundErnsberger, U., & Rohrer, H. (2018) · Neural Development · doi:10.1186/s13064-018-0117-6 · Cited by 60
Developmental Pattern Formation in Phases.
Kicheva, A., & Briscoe, J. (2015) · Trends in Cell Biology · doi:10.1016/j.tcb.2015.07.006 · Cited by 60
Oligodendrocyte development in the embryonic brain: the contribution of the plp lineage
Bras, B. L., Chatzopoulou, E., Heydon, K., Martı́nez, S., Ikenaka, K., Prestoz, L., Spassky, N., Zalc, B., & Thomas, J. (2005) · The International Journal of Developmental Biology · doi:10.1387/ijdb.041963bl · Cited by 63
Developmental mechanisms for the generation of telencephalic interneurons
Corbin, J. G., & Butt, S. J. B. (2011) · Developmental Neurobiology · doi:10.1002/dneu.20890 · Cited by 58
Dynamism of an Astrocyte In Vivo: Perspectives on Identity and Function
Poskanzer, K. E., & Molofsky, A. V. (2017) · Annual Review of Physiology · doi:10.1146/annurev-physiol-021317-121125 · Cited by 62
Zujovic, V., Thibaud, J., Bachelin, C., Vidal, M., Deboux, C., Coulpier, F., Stadler, N., Charnay, P., Topilko, P., & Evercooren, A. B. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1018687108 · Cited by 62
Kazakova, N., Li, H., Mora, A., Jessen, K., Mirsky, R., Richardson, W., & Smith, H. (2006) · Developmental Biology · doi:10.1016/j.ydbio.2006.03.020 · Cited by 58
“Olig2 null mice or zebrafish treated with olig2suppressing morpholino oligonucleotides show deficiencies of both motor neurons and OLPs, indicating that these two cell types share common precursors in the spinal cord and brainstem (Lu et al., 2002; Park et al., 2002; Takebayashi et al., 2002; Zhou and Anderson, 2002).”
Du, J., Yi, M., Zhou, F., He, W., Yang, A., Qiu, M., & Huang, H. (2021) · Molecular Brain · doi:10.1186/s13041-021-00865-9 · Cited by 57
Duncan, I. D., Bugiani, M., Radcliff, A. B., Moran, J. J. M., Lopez‐Anido, C., Duong, P., August, B. K., Wolf, N. I., van der Knaap, M. S., & Svaren, J. P. (2017) · Annals of Neurology · doi:10.1002/ana.24930 · Cited by 68
Niu, J.-Q., Mei, F., Wang, L.-Y., Liu, S., Tian, Y., Mo, W., Li, H.-L., Lu, Q. R., & Xiao, L. (2012) · Glia · doi:10.1002/glia.22364 · Cited by 57
“Olig1/2 knockout mice fail to develop cells of the oligodendroglial lineage (Lu et al., 2002; Zhou and Anderson, 2002), which is thought to be attributed specifically to Olig2 function, as the Olig2-null mouse displays a similar impairment in the generation of oligodendroglia (Lu et al., 2002;…”
Ortega, M. C., Cases, O., Merchán, P., Kozyraki, R., Clemente, D., & de Castro, F. (2012) · Glia · doi:10.1002/glia.22316 · Cited by 67
Hu, Q., Ma, Q., Gennarini, G., & Xiao, Z. (2006) · Developmental Neuroscience · doi:10.1159/000090750 · Cited by 57
“Cells that express Olig2 can differentiate into OLs while those expressing both Olig2 and Ngns only develop as motoneurons [Zhou and Anderson, 2002].”
BackgroundLozano, D. C., Choe, T. E., Cepurna, W. O., Morrison, J., & Johnson, E. (2019) · Investigative Ophthalmology and Visual Science · doi:10.1167/iovs.18-25700 · Cited by 56
Olig1 Acetylation and Nuclear Export Mediate Oligodendrocyte Development
Dai, J., Bercury, K. K., Jin, W., & Macklin, W. B. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.0882-15.2015 · Cited by 59
“Although Olig1 is clearly important for oligodendrocyte specification and OPC differentiation (Lu et al., 2002; Zhou and Anderson, 2002; Silbereis et al., 2014; Dai et al., 2015), tight temporal control of Olig1 ex- pression and localization as oligodendrocytes initiate myelination implies a…”
Astrocyte Form and Function in the Developing Central Nervous System
Chaboub, L. S., & Deneen, B. (2013) · Seminars in Pediatric Neurology · doi:10.1016/j.spen.2013.10.003 · Cited by 60
Concise Review: Human Pluripotent Stem Cells in the Treatment of Spinal Cord Injury
Lukovic, D., Moreno‐Manzano, V., Stojković, M., Bhattacharya, S. S., & Erceg, S. (2012) · Stem Cells · doi:10.1002/stem.1159 · Cited by 55
Connexin 36 Expression Regulates Neuronal Differentiation from Neural Progenitor Cells
Hartfield, E., Rinaldi, F., Glover, C., Wong, L.-F., Caldwell, M., & Uney, J. (2011) · PLoS ONE · doi:10.1371/journal.pone.0014746 · Cited by 56
Gene expression profiling of choline-deprived neural precursor cells isolated from mouse brain.
Niculescu, M., Craciunescu, C., & Zeisel, S. (2005) · Brain Research. Molecular Brain Research · doi:10.1016/j.molbrainres.2004.11.001 · Cited by 56
“Interestingly, Olig1 was also overexpressed, suggesting a possible parallel commitment to oligodendrocyte differentiation [85].”
Klocke, C., Allen, J. L., Sobolewski, M., Blum, J. L., Zelikoff, J. T., & Cory-Slechta, D. A. (2018) · NeuroToxicology · doi:10.1016/j.neuro.2017.10.004 · Cited by 56
“Indeed, Olig2 is known to be expressed throughout the oligodendrocyte lineage (Zhou and Anderson, 2002); however, its importance in OPC fate specification makes it an ideal candidate for determining if gestational exposure to air pollution impacts OPC specification in the CC. Adenomatous polyposis…”
BackgroundInfluentialRegulation of the timing of oligodendrocyte differentiation: mechanisms and perspectives
Huang, H., Zhao, X., Zheng, K., & Qiu, M.-S. (2013) · Neuroscience Bulletin · doi:10.1007/s12264-013-1314-2 · Cited by 55
“olig2 functions to specify the fate of the oligodendroglial lineage, while olig1 appears to play an important role in timing oligodendrocyte differentiation([31,32]).”
Tapping into the glial reservoir: cells committed to remaining uncommitted
Chong, S. Y. C., & Chan, J. R. (2010) · The Journal of Cell Biology · doi:10.1083/jcb.200905111 · Cited by 56
“Olig1/2 knockout mice fail to develop cells of the oligodendroglial lineage (Lu et al., 2002; Zhou and Anderson, 2002), and this is attributed specifically to Olig2 function, as the Olig2-null mouse displays a similar impairment in the generation of oligodendroglia and deficits in motor neuron specification (Lu et al.”
Combinatorial signalling controls Neurogenin2 expression at the onset of spinal neurogenesis.
Ribes, V., Stutzmann, F., Bianchetti, L., Guillemot, F., Dollé, P., & Roux, I. L. (2008) · Developmental Biology · doi:10.1016/j.ydbio.2008.06.003 · Cited by 55
Goncalves, M. B., Boyle, J., Webber, D. J., Hall, S., Minger, S., & Corcoran, J. (2005) · Developmental Biology · doi:10.1016/j.ydbio.2004.10.015 · Cited by 55
“In support of this is the fact that in the spinal cord astrocytes are derived from the dorsal region of the cord (Lu et al., 2002; Pringle et al., 1998; Zhou and Anderson, 2002), while oligodendrocytes and motoneurons are derived from the ventral region (Hall et al.”
BackgroundCell fate control in the developing central nervous system
Guérout, N., Li, X., & Barnabé‐Heider, F. (2013) · Experimental Cell Research · doi:10.1016/j.yexcr.2013.10.003 · Cited by 60
Characterization and regulation of the hb9/mnx1 beta-cell progenitor specific enhancer in zebrafish
Arkhipova, V., Wendik, B., Devos, N., Ek, O., Peers, B., & Meyer, D. (2012) · Developmental Biology · doi:10.1016/j.ydbio.2012.03.001 · Cited by 61
Jordan, P. M., Ojeda, L., Thonhoff, J. R., Gao, J.-L., Boehning, D., Yu, Y.-J., & Wu, P. (2009) · Journal of Neuroscience Research · doi:10.1002/jnr.21856 · Cited by 54
Liu, Y., & Rao, M. S. (2003) · Glia · doi:10.1002/glia.10303 · Cited by 60
A direct fate exclusion mechanism by Sonic hedgehog-regulated transcriptional repressors
Nishi, Y., Zhang, X., Jeong, J., Peterson, K. A., Vedenko, A., Bulyk, M. L., Hide, W. A., & McMahon, A. P. (2015) · Development · doi:10.1242/dev.124636 · Cited by 53
Evolution of the CNS myelin gene regulatory program
Li, H., & Richardson, W. (2015) · Brain Research · doi:10.1016/j.brainres.2015.10.013 · Cited by 53
“Another study found that when Olig2 is conditionally deleted in cortical OPs using an OP-specific NG2-Cre, they change fate and transform into GFAPþ astrocytes (Zhu et al., 2012). f the CNS myelin gene regulatory program.”
BackgroundCorpening, J. C., Cantrell, V. A., Deal, K. K., & Southard-Smith, E. M. (2008) · Developmental Dynamics · doi:10.1002/dvdy.21498 · Cited by 53
Glial cells: old cells with new twists.
Ndubaku, U., & de Bellard, M. D. (2008) · Acta Histochemica · doi:10.1016/j.acthis.2007.10.003 · Cited by 52
“This group of cells divides and migrates radially to cover the spinal cord later in development (Talbott et al., 2005; Zhou and Anderson, 2002).”
BackgroundThe cellular fate of cortical progenitors is not maintained in neurosphere cultures.
Machoň, O., Backman, M., Krauss, S., & Kozmik, Z. (2005) · Molecular and cellular neurosciences · doi:10.1016/j.mcn.2005.08.003 · Cited by 52
Transcriptional control of glial cell development in Drosophila
Jones, B. W. (2004) · Developmental Biology · doi:10.1016/j.ydbio.2004.11.022 · Cited by 46
“…(bHLH) transcription factors homologous to the Drosophila proneural genes (e.g., Nieto et al., 2001; Sun et al., 2001a,b; Tomita et al., 2000; Zhou and Anderson, 2002; reviewed in Ross et al., 2002; Rowitch et al., 2002; Vetter, 2001), members of the Sox family of high-mobility-group (HMG)…”
Gli2 is required for normal Shh signaling and oligodendrocyte development in the spinal cord.
Qi, Y., Tan, M., Hui, C.-C., & Qiu, M.-S. (2003) · Molecular and cellular neurosciences · doi:10.1016/s1044-7431(03)00067-8 · Cited by 52
Newborn cortical neurons: only for neonates?
Feliciano, D. M., & Bordey, A. (2013) · Trends in Neurosciences · doi:10.1016/j.tins.2012.09.004 · Cited by 51
Weider, M., Wegener, A., Schmitt, C., Küspert, M., Hillgärtner, S., Bösl, M., Hermans-Borgmeyer, I., Nait-Oumesmar, B., & Wegner, M. (2015) · PLoS Genetics · doi:10.1371/journal.pgen.1005008 · Cited by 51
Du, Z., Li, X.-J., Nguyen, G. D., & Zhang, S.-C. (2006) · Molecular and cellular neurosciences · doi:10.1016/j.mcn.2006.08.007 · Cited by 51
Metadata
- Authors
- Zhou, Q., & Anderson, D. J.
- Affiliations
- California Institute of Technology (US)
- Corresponding author
- Anderson, David J.
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2002-04
- Volume
- 109
- Issue
- 1
- Pages
- 61-73
- ISSN
- 0092-8674 (ISSN-L)
- OpenAlex
- W2125920059
- Cited by
- 1,059
- References
- 70
- Citations by year
- 2026: 16 · 2025: 27 · 2024: 29 · 2023: 27 · 2022: 45 · 2021: 46 · 2020: 26 · 2019: 36 · 2018: 36 · 2017: 36 · 2016: 33 · 2015: 41 · 2014: 52 · 2013: 48 · 2012: 52
- FWCI
- 14.68
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- CaltechAUTHORS (California Institute of Technology) (submittedVersion)
- Funders
- National Institute of Neurological Disorders and Stroke (R01-NS23476, R01NS023476)
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Congenital heart defects research
- Keywords
- Olig2, Olig1, bHLH transcription factors, motor neurons, oligodendrocytes, astrocytes, proneural genes, lineage tracing
- MeSH terms
- Oligodendrocyte Transcription Factor 2, Animals, Astrocytes, Cell Differentiation, DNA-Binding Proteins, Female, Interneurons, Male, Motor Neurons, Mutation, Nerve Tissue Proteins, Neuroglia, Neurons, Oligodendroglia, Rhombencephalon, Spinal Cord, Stem Cells, Transcription Factors, Helix-Loop-Helix Motifs, Mice, Knockout, Homeodomain Proteins, Cell Lineage, Mice, Basic Helix-Loop-Helix Proteins
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