A direct fate exclusion mechanism by Sonic hedgehog-regulated transcriptional repressors
Open accessAbstract
Sonic hedgehog (Shh) signaling patterns the vertebrate spinal cord by activating a group of transcriptional repressors in distinct neural progenitors of somatic motor neuron and interneuron subtypes. To identify the action of this network, we performed a genome-wide analysis of the regulatory actions of three key ventral determinants in mammalian neural tube patterning: Nkx2.2, Nkx6.1 and Olig2. Previous studies have demonstrated that each factor acts predominantly as a transcriptional repressor, at least in part, to inhibit alternative progenitor fate choices. Here, we reveal broad and direct repression of multiple alternative fates as a general mechanism of repressor action. Additionally, the repressor network targets multiple Shh signaling components providing negative feedback to ongoing Shh signaling. Analysis of chromatin organization around Nkx2.2-, Nkx6.1- and Olig2-bound regions, together with co-analysis of engagement of the transcriptional activator Sox2, indicate that repressors bind to, and probably modulate the action of, neural enhancers. Together, the data suggest a model for neural progenitor specification downstream of Shh signaling, in which Nkx2.2 and Olig2 direct repression of alternative neural progenitor fate determinants, an action augmented by the overlapping activity of Nkx6.1 in each cell type. Integration of repressor and activator inputs, notably activator inputs mediated by Sox2, is probably a key mechanism in achieving cell type-specific transcriptional outcomes in mammalian neural progenitor fate specification.
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These TFs form a gene regulatory network that establishes progenitor identities by repressing not only adjacent progenitor identities but also a wide range of alternative fates.
“These TFs form a gene regulatory network that establishes progenitor identities by repressing not only adjacent progenitor identities but also a wide range of alternative fates (Kutejova et al., 2016; Nishi et al., 2015).”
From Single cell transcriptomics reveals spatial and temporal dynamics of gene expression in the developing mouse spinal cord (2019) · cites this paper as Nishi et al., 2015
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- Authors
- Nishi, Y., Zhang, X., Jeong, J., Peterson, K. A., Vedenko, A., Bulyk, M. L., Hide, W. A., & McMahon, A. P.
- Affiliations
- University of Southern California (US)
- Harvard University (US)
- Brigham and Women's Hospital (US)
- Corresponding author
- McMahon, Andrew P.
- Venue
- Development
- Publisher
- The Company of Biologists
- Published
- 2015-01-01
- Volume
- 142
- Issue
- 19
- Pages
- 3286-93
- ISSN
- 0950-1991 (ISSN-L)
- 1477-9129
- PMC
- PMC4631756
- OpenAlex
- W2228067260
- Cited by
- 53
- References
- 38
- Citations by year
- 2026: 2 · 2025: 6 · 2024: 6 · 2023: 7 · 2022: 2 · 2021: 6 · 2020: 4 · 2019: 4 · 2018: 3 · 2017: 6 · 2016: 6 · 2015: 1
- FWCI
- 2.31
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Development (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- White Rose Research Online (University of Leeds, The University of Sheffield, University of York) (acceptedVersion)
- Digital Access to Scholarship at Harvard (DASH) (Harvard University) (submittedVersion, cc-by)
- Funders
- University of Minnesota
- National Institutes of Health (NS-033642)
- Medical Research Council
- National Heart, Lung, and Blood Institute (T32HL087735)
- National Human Genome Research Institute (R01HG003985)
- National Institute of Neurological Disorders and Stroke (R01NS033642, R37NS033642)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Hedgehog Signaling Pathway Studies
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- Sonic hedgehog signaling, transcriptional repression, Nkx2.2, NKX6.1, Olig2, SOX2, chromatin organization, negative feedback, motor neuron subtypes, interneuron subtypes, cell-type-specific transcription
- MeSH terms
- Oligodendrocyte Transcription Factor 2, Homeobox Protein Nkx-2.2, Chromatin, Humans, Interneurons, Models, Biological, Motor Neurons, Nerve Tissue Proteins, Nuclear Proteins, Protein Binding, Repressor Proteins, Transcription Factors, Signal Transduction, Open Reading Frames, Homeodomain Proteins, Gene Expression Regulation, Developmental, Zebrafish Proteins, Protein Array Analysis, Chromatin Immunoprecipitation, Basic Helix-Loop-Helix Proteins, Hedgehog Proteins, Neural Tube, SOXB1 Transcription Factors, Neural Stem Cells
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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