Cited by 1,059Neurogenesis and neuroplasticity mechanismsDevelopmental Biology and Gene RegulationCongenital heart defects research

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The bHLH Transcription Factors OLIG2 and OLIG1 Couple Neuronal and Glial Subtype Specification

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Zhou, Qiao, Anderson, David J.·2002·Cell

DOI 10.1016/s0092-8674(02)00677-3

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Abstract

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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Background
The bHLH transcription factor Olig3 marks the dorsal neuroepithelium of the hindbrain and is essential for the development of brainstem nuclei
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“In contrast, Olig2 is a neural-lineage-specific transcription factor that is expressed in oligodendrocyte precursors and astrocytes of the developing brain and spinal cord and is important for their differentiation (Lu et al., 2000; Zhou and Anderson, 2002; Liu and Rao, 2004).”
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Genetically engineered human neural stem cells for brain repair in neurological diseases.
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“…factor Olig2 plays an essential role in the differentiation of oligodendrocytes and motor neurons in the embryonic spinal cord (Takebayashi et al., 2002; Zhou and Anderson, 2002), and in oligodendrocyte maturation in the developing ventral forebrain (Parras et al., 2007; Petryniak et al., 2007).”
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Ectopic Expression of Neurogenin 2 Alone is Sufficient to Induce Differentiation of Embryonic Stem Cells into Mature Neurons
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“For instance, in the developing spinal cord, NG2-positive OPCs appear for the first time at embryonic day 12.5 (Lu et al., 2002; Takebayashi et al., 2002; Zhou and Anderson, 2002).”
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“Since OLIG2 is essential for oligodendrocyte specification throughout the entire neuraxis, except for the hindbrain (Lu et al., 2000; Zhou and Anderson, 2002; Zhou et al., 2000), OLIG2 expression is a useful earlymarker of successful respecification of hESC-NPCs toward OPC-generating domains of the…”
Platelet-derived growth factor-AA mediates oligodendrocyte lineage differentiation through activation of extracellular signal-regulated kinase signaling pathway
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Neural progenitors adopt specific identities by directly repressing all alternative progenitor transcriptional programs
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“2 (Table S4), Irx3 expression expands ventrally in theOlig1/Olig2mutant but does not cross the dorsal boundary of the p3 domain (Zhou and Anderson, 2002).”
Background
Adult Neurogenesis Restores Dopaminergic Neuronal Loss in the Olfactory Bulb
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“, 2010), the number of cells positive for the transcription factor Olig2, a marker of oligodendrogenesis and of neuronal precursors (Zhou and Anderson, 2002), was assessed at 7 d after lesion.”
Background
Evidence that nucleocytoplasmic Olig2 translocation mediates brain‐injury‐induced differentiation of glial precursors to astrocytes
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Glial Progenitors in the CNS and Possible Lineage Relationships Among Them
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Immunological Markers for Central Nervous System Glia
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“Consistent with the regional difference in OLIG2 expression, deletion of the Olig2 gene affects the development of cortical astrocytes [45, 49], but not that of spinal astrocytes [50, 51].”
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Expression of the Oligodendroglial Lineage‐Associated Markers Olig1 and Olig2 in Different Types of Human Gliomas
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Using the lineage determinants Olig2 and Sox10 to explore transcriptional regulation of oligodendrocyte development
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Astrocyte heterogeneity across the brain and spinal cord occurs developmentally, in adulthood and in response to demyelination
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“…these, Olig2, which encodes a bHLH transcription factor known to be critical for oligodendrocyte specification and differentiation (Lu et al., 2002; Zhou and Anderson, 2002; Yue et al., 2006), was among the genes with the most significantly different H3K27Ac recruitment in LPC-treated and…”
Background
Temporal identity transition from Purkinje cell progenitors to GABAergic interneuron progenitors in the cerebellum
Seto, Y., Nakatani, T., Masuyama, N., Taya, S., Kumai, M., Minaki, Y., Hamaguchi, A., Inoue, Y., Inoue, T., Miyashita, S., et al. (2014) · Nature Communications · doi:10.1038/ncomms4337 · Cited by 85
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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
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“Key to the neuron glia switch is the expression of the basic helix-loop-helix transcription factors oligodendrocyte transcription factor (Olig)1 and Olig2 (Zhou & Anderson, 2002).”
BackgroundInfluential
Initiation of Oligodendrocyte Progenitor Cell Migration by a PDGF-A Activated Extracellular Regulated Kinase (ERK) Signaling Pathway
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From CNS stem cells to neurons and glia: Sox for everyone
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“Olig2 is expressed already in NEP cells of the pMN domain and induces the expression of Sox10.”
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Motor neurons and oligodendrocytes arise from distinct cell lineages by progenitor recruitmentPreprint
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“In the CNS, Sirt2 is expressed throughout the oligodendrocyte lineage, and is associated with myelin [108] [109] , although its function in myelination is unknown.”
BackgroundInfluential
Cyclin D1 promotes neurogenesis in the developing spinal cord in a cell cycle-independent manner
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Self-citation
Transient upregulation of Nkx2.2 expression in oligodendrocyte lineage cells during remyelination
Watanabe, M., Hadžić, T., & Nishiyama, A. (2004) · Glia · doi:10.1002/glia.20006 · Cited by 86
Two Opposing Roles of RBP-J in Notch Signaling
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ZFP191 is required by oligodendrocytes for CNS myelinationPreprint
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Nucleoporin Seh1 Interacts with Olig2/Brd7 to Promote Oligodendrocyte Differentiation and Myelination
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PDGF α-Receptor Signal Strength Controls an RTK Rheostat That Integrates Phosphoinositol 3′-Kinase and Phospholipase Cγ Pathways during Oligodendrocyte Maturation
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“Their codependence on the bHLH (basic helixloop-helix) protein Olig2 further suggests coupled mechanisms for specification (Zhou and Anderson, 2002) and a common motor neuron-oligodendrocyte ancestry (Lu et al.”
Background
Getting a GR(i)P on oligodendrocyte development
Noble, M., Pröschel, C., & Mayer-Pröschel, M. (2003) · Developmental Biology · doi:10.1016/j.ydbio.2003.06.002 · Cited by 85
“Similarly, in Olig1 / Olig2 / mice in which GFP was expressed in the Olig2 locus, half of the GFP-expressing cells differentiated into astrocytes in vivo (Zhou and Anderson, 2002).”
BackgroundResultInfluential
A Critical Period in Cortical Interneuron Neurogenesis in Down Syndrome Revealed by Human Neural Progenitor Cells
Bhattacharyya, A., McMillan, E., Chen, S. I., Wallace, K., & Svendsen, C. N. (2009) · Developmental Neuroscience · doi:10.1159/000236899 · Cited by 79
“While OLIG gene function is necessary for the development of oligodendrocytes [Lu et al., 2002; Zhou and Anderson, 2002], additional functions of the OLIG genes have been revealed in both neural development and in disease [for a review, see Ligon et al., 2006].”
Background
Wnt signaling determines ventral spinal cord cell fates in a time-dependent manner
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“…involved in specifying different ventral neuronal cell fates in specific groups of ventral progenitors, we used Olig1-Cre to induce recombination in discrete progenitor groups (pMN and pV3) in the ventral spinal cord starting from late E8 (Lu et al., 2002; Wu et al., 2006; Zhou and Anderson, 2002).”
Method
BMP signaling mutant mice exhibit glial cell maturation defects.
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Nkx6.1 controls migration and axon pathfinding of cranial branchio-motoneurons
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Evidence for a second wave of oligodendrogenesis in the postnatal cerebral cortex of the mouse
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Oligodendrocyte Precursor Cells in Spinal Cord Injury: A Review and Update
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“Double-mutant OLIG1 and OLIG2 would eliminate the formation of OPCs and the genesis of motor-neurons and oligodendrocytes [129], while transient expression of OLIG1 would induce the formation of OPCs from neural stem cells [130].”
Background
MicroRNAs Are Essential for the Developmental Switch from Neurogenesis to Gliogenesis in the Developing Spinal Cord
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“By contrast, astrocyte precursor cells originate from other domains of neuroepithelial cells and reach their final destinations through radial migration (Lu et al., 2002; Zhou and Anderson, 2002; Hochstim et al., 2008).”
Background
Converse control of oligodendrocyte and astrocyte lineage development by Sonic hedgehog in the chick spinal cord.
Agius, E., Soukkarieh, C., Danesin, C., Kan, P., Takebayashi, H., Soula, C., & Cochard, P. (2004) · Developmental Biology · doi:10.1016/j.ydbio.2004.02.015 · Cited by 78
“Finally, loss of function of olig genes severely affects motoneuron development and totally abolishes that of OLs (Lu et al., 2002; Park et al., 2002; Takebayashi et al., 2002; Zhou and Anderson, 2002).”
BackgroundInfluential
Emerging roles for bone morphogenetic proteins in central nervous system glial biology
Hall, A. K., & Miller, R. H. (2004) · Journal of Neuroscience Research · doi:10.1002/jnr.20019 · Cited by 68
A regulatory toolbox of MiniPromoters to drive selective expression in the brain
Portales-Casamar, E., Swanson, D. J., Liu, L., Leeuw, C. N. D., Banks, K. G., Ho Sui, S. J., Fulton, D. L., Ali, J., Amirabbasi, M., Arenillas, D. J., et al. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1009158107 · Cited by 77

Authors: Zhou, Q., & Anderson, D. J.
Affiliations: California Institute of Technology (US)
Corresponding author: Anderson, David J.
ORCID: Zhou, Qiao
Anderson, David J.
Venue: Cell
Publisher: Elsevier BV
Published: 2002-04
Volume: 109
Issue: 1
Pages: 61-73
ISSN: 0092-8674 (ISSN-L)
DOI: 10.1016/s0092-8674(02)00677-3
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: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 4125 d)
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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The bHLH Transcription Factors OLIG2 and OLIG1 Couple Neuronal and Glial Subtype Specification

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