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Sonic hedgehog functions through dynamic changes in temporal competence in the developing forebrain
Open accessAbstract
Morphogens act during development to provide graded spatial information that controls patterning and cell lineage specification in the nervous system. The role of morphogen signaling in instructing the expression of downstream effector transcription factors has been well established. However, a key requirement for morphogen signaling is the existence of functional intracellular machinery able to mediate the appropriate response in target cells. Here we suggest that dynamic changes in the temporal responses to Shh in the developing ventral telencephalon occur through alterations in progenitor competence. We suggest these developmental changes in competence are mediated by a transcriptional mechanism that intrinsically integrates information from the distinct signaling pathways that act to pattern the telencephalic neuroepithelium.
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“consistent with a role in MGE fate repression41 and LGE neuron state regulation (Extended Data Fig. 9h,i).”
From Inferring and perturbing cell fate regulomes in human brain organoids (2023) · cites this paper as [41]
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“Efficiency of GABAergic interneuron production in vitro We generated ESNPs for transplantation using nutrient-poor medium in a feeder-free monolayer culture system (Ying and Smith, 2003) and applied a hedgehog agonist in vitro to promote survival and differentiation of GABAergic progenitors (Barberi et al., 2003; Li e…”
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“In vivo, Shh is expressed in the ventral telencephalon and hypothalamus and is essential to the regionalization of the subpallium [10, 11] while along the dorsal midline, secreted molecules of the bone morphogenetic proteins (BMP) and WNT families control patterning of the medial and dorsal pallium.”
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Kaye, J., & Finkbeiner, S. M. (2013) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2013.02.005 · Cited by 68
“During subdivision of the MGE and LGE, inhibiting Wnt signaling in dorsal structures is key to promoting LGE patterning.”
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“On the contrary, Shh, a molecule involved in the organization of subpallial neural precursors (Shimamura et al., 1995; Crossley et al., 2001; Sousa and Fishell, 2010), together with Noggin and Chordin (two Bmps antagonists expressed in the ANR) (Piccolo et al.”
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Wnt3 and Wnt3a are required for induction of the mid-diencephalic organizer in the caudal forebrain
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“…line between emerging thalamic nuclei in the caudal diencephalon that extends dorsally from the FP in the midbrain, and later still in distinct foci in the preoptic area, presumptive amygdala, and the medial ganglionic eminence (MGE), the anlage to the basal ganglia (Sousa and Fishell, 2010).”
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“The role of Shh signaling has also been investigated throughout the developing brain (Fuccillo and others 2006; Sousa and Fishell 2010).”
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Mechanisms of Cortical Differentiation
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“…development, the sonic hedgehog (shh) signaling pathway regulates the early induction and expansion of progenitors in the ventral forebrain, midbrain, and midbrain/ hindbrain boundary (MHB) (Blaess et al., 2006; Fuccillo et al., 2004; Hynes et al., 1995; Sousa and Fishell, 2010).”
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Decoding the transcriptional basis for GABAergic interneuron diversity in the mouse neocortex
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“…of the ventral telencephalon (Fuccillo et al., 2004; Xu et al., 2005), although the actions of this morphogen, and Fgf8 from the anterior neural ridge, are complex and remain dynamic from the days immediately following neural tube closure (for a detailed review, see Sousa & Fishell, 2010).”
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“Thecentralmechanism that determines neural progenitor competence to Hh signaling is the activity of the Gli family of transcriptional regulators–Gli1, Gli2, and Gli3 [68,69].”
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“…to understand cyclic HES gene expression regulation in various processes that are also under joint FGF and SHH regulation, such as somitogenesis (Resende et al., 2010) neurogenesis (Shimojo et al., 2008; Sousa and Fishell, 2010) and stem cell pluripotency (Shi et al., 2008; Kobayashi et al., 2009).”
BackgroundSonic Hedgehog Signaling and Potential Therapeutic Indications
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Phylogenetic Origins of Brain Organisers
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“Once ventral identity has been established, Shh is expressed in the diencephalic basal plate, throughout most of the hypothalamus and in a ventroanterior area known as the lamina terminalis that is located just ventral to the ANR and gives rise to the medial ganglionic eminence (MGE, Figure 1(a)) [158].”
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“In line with previous studies in the telencephalon and the spinal cord [30-33], these results suggest that coordination of neural tube patterning and morphogenesis relies on stage-dependent regulation of morphogen signalling.”
BackgroundResultSpecification of GABAergic Neocortical Interneurons
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“During development lateral, medial and caudal ganglionic eminences produce cells that contribute to a number of brain structures, in particular, cells of the lateral ganglionic eminence contribute to the striatum, however, nearby structures, such as the medial ganglionic eminence and subcortical plate, also share comp…”
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“The fibroblast growth factor (Fgf2) gene is an SHH-responding proneural gene able to restore hippocampal functions in a model of Alzheimer’s disease, partly as a result of enhanced neurogenesis [59,60].”
BackgroundNogoR1 and PirB Signaling Stimulates Neural Stem Cell Survival and Proliferation
Ramasamy, S., Yu, F., Yu, Y. H., Hariharan, S., Dawe, G. S., & Ahmed, S. (2014) · Stem Cells · doi:10.1002/stem.1645 · Cited by 14
PRISM: A Progenitor-Restricted Intersectional Fate Mapping Approach Redefines Forebrain Lineages
Poulin, J.-F., Luppi, M. P., Hofer, C., Caronia, G., Hsu, P.-K., Chan, C. S., & Awatramani, R. B. (2020) · Developmental Cell · doi:10.1016/j.devcel.2020.05.019 · Cited by 11
Marczenke, M., Sunaga, D. Y., Popp, O., Althaus, I. W., Sauer, S., Mertins, P., Christ, A., Allen, B. L., & Willnow, T. E. (2021) · Development · doi:10.1242/dev.200080 · Cited by 10
“1), specify ventral midline identity and counteract dorsalizing signals by bone morphogenetic protein 4 (BMP4) (Hoch et al., 2009; Sousa and Fishell, 2010).”
BackgroundChen, Z., Pan, T., Zhang, Y., Wang, B., Sun, X., Gao, M., Sun, Y., Xu, M., Han, S., Shi, X., et al. (2025) · Developmental Cell · doi:10.1016/j.devcel.2025.03.009 · Cited by 11
Strell, P., Johnson, S. T., Carchi, C., & Low, W. C. (2023) · Cell Transplantation · doi:10.1177/09636897231164712 · Cited by 10
Gupta, R., Mehan, S., Chhabra, S., Giri, A., & Sherawat, K. (2022) · Neurotoxicity Research · doi:10.1007/s12640-022-00586-4 · Cited by 10
“1995; Sousa and Fishell 2010).”
Capetian, P., Pauly, M. G., Azmitia, L. M., & Klein, C. (2014) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2014.00205 · Cited by 9
“…of morphogens mediating the expression of downstream effectors, the most important in this respect being SHH, fibroblast growth factors (FGFs), bone morphogenetic proteins (BMPs), and agonists of the wingless/Int-1 pathway (WNT; Hébert and Fishell, 2008; Sousa and Fishell, 2010; Cho et al., 2013).”
The Crossroads of Neural Stem Cell Development and Tumorigenesis
Yabut, O., & Pleasure, S. J. (2016) · PubMed · doi:10.20388/omp2016.003.0040 · Cited by 8
“…the roles of molecules that have been specifically implicated in the proliferation of NSCs and BTSCs. Shh signaling is widely known for its mitogenic effect on proliferative cells throughout development (Sousa and Fishell, 2010), a role that is maintained in the postnatal V-SVZ (Choe et al., 2016).”
BackgroundLoss of Suppressor of Fused in Mid-Corticogenesis Leads to the Expansion of Intermediate Progenitors
Yabut, O., Ng, H., Fernández, G., Yoon, K., Kuhn, J., & Pleasure, S. J. (2016) · Journal of Developmental Biology · doi:10.3390/jdb4040029 · Cited by 8
“Sonic Hedgehog (Shh) signaling is centrally involved in this process and is required during distinct developmental windows to direct patterning, specification, and proliferation of progenitors [5].”
Backgroundten Donkelaar, H. J. (2014) · Springer eBooks · doi:10.1007/978-3-642-54687-7_2 · Cited by 8
Rudy, M. J., Salois, G., Cubello, J., Newell, R., & Mayer‐Pröschel, M. (2023) · Development · doi:10.1242/dev.201068 · Cited by 7
Chang, C.-C., Kuo, H., Chen, S., Lu, K.-M., Fong, W. L., Wu, H.-L., Saito, T., & Liu, F.-C. (2020) · The Journal of Comparative Neurology · doi:10.1002/cne.24900 · Cited by 7
Kiecker, C. M., Graham, A., & Logan, M. P. O. (2016) · Journal of Developmental Biology · doi:10.3390/jdb4040036 · Cited by 7
“It is possible that this mechanism has developed to prevent a ‘domino effect’ in places where SHH can induce its own expression such as the ventral neural tube [98].”
BackgroundMicroRNAs in Brain Development
Coolen, M., & Bally‐Cuif, L. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-405544-5.00018-6 · Cited by 6
Nasu, M., Esumi, S., Hatakeyama, J., Tamamaki, N., & Shimamura, K. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.632381 · Cited by 7
PAR3 restricts the expansion of neural precursor cells by regulating hedgehog signaling
Hirose, T., Sugitani, Y., Kurihara, H., Kazama, H., Kusaka, C., Noda, T., Takahashi, H., & Ohno, S. (2022) · Development · doi:10.1242/dev.199931 · Cited by 4
Kadoshima, T., Sakaguchi, H., & Eiraku, M. (2017) · Methods in molecular biology · doi:10.1007/978-1-4939-6949-4_1 · Cited by 4
Only scratching the cell surface: extracellular signals in cerebrum development
Hébert, J. M. (2013) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2013.04.004 · Cited by 4
Wada, Y., Yamauchi, K., Murakami, F., & Tanabe, Y. (2012) · Developmental Neurobiology · doi:10.1002/dneu.20861 · Cited by 5
“…of the forebrain (Echelard et al., 1993; Ericson et al., 1995; Marti et al., 1995; Chiang et al., 1996; Gunhaga et al., 2000; Gunhaga et al., 2003; Marklund et al., 2004; Shimogori and Grove, 2005; Fuccillo et al., 2006; Hebert and Fishell, 2008; Shimogori et al., 2010; Sousa and Fishell, 2010).”
BackgroundTran, L. N., Shinde, A., Schuster, K. H., Sabaawy, A., Dale, E., Welch, M. J., Isner, T. J., Nunez, S. A., García‐Moreno, F., Sagerström, C. G., et al. (2025) · Genes & Development · doi:10.1101/gad.352555.124 · Cited by 4
Sonic hedgehog elevates N-myc gene expression in neural stem cells.
Liu, D., Wang, S., Cui, Y. R., Shen, L., Du, Y., Li, G., Zhang, B., & Wang, R. (2012) · PubMed Central · doi:10.3969/j.issn.1673-5374.2012.22.004 · Cited by 3
“Neural stem cells are self-renewing, multipotent progenitor cells that reside in the subventricular zone of the lateral ventricle and the subgranular zone of the dentate gyrus within the nervous system, and are capable of differentiating into all major neural cell types, namely, neurons, astrocytes and oligodendrocyte…”
BackgroundDevelopment of the Basal Ganglia and the Basal Forebrain
ten Donkelaar, H. J. (2015) · Elsevier eBooks · doi:10.1016/b978-0-12-397025-1.00236-0 · Cited by 3
Pedraza, M., Grampa, V., Scotto‐Lomassese, S., Puech, J., Muzerelle, A., Mohammad, A., Lebon, S., Renier, N., Métin, C., & Masson, J. (2024) · eLife · doi:10.7554/elife.100328 · Cited by 4
The evolutionary and organizational bases of active affordance
Luu, P., Tucker, D. M., & Friston, K. J. (2026) · Cerebral Cortex · doi:10.1093/cercor/bhag057 · Cited by 2
Temporal establishment of neural cell identityin vivoandin vitro
Yuen, S. M., & Kwok, H. F. (2016) · Journal of Tissue Engineering and Regenerative Medicine · doi:10.1002/term.2158 · Cited by 2
“to morphogens is essential for regulating the specification of different organs and tissues in vivo (Sousa and Fishell, 2010), the observed change in the patterning response exhibited by neural progenitor cells over time implies that as progenitor cells differentiate they irreversibly become more restricted in terms o…”
BackgroundNeural Cell Fate Determination
Moore, S., & Livesey, F. J. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-405945-0.00016-8 · Cited by 3
Carlson, B. M. (2014) · Elsevier eBooks · doi:10.1016/b978-1-4557-2794-0.00011-5 · Cited by 2
Early Patterning and Development of the Central Nervous System
Carlson, B. M. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-801238-3.05440-4 · Cited by 1
Development and Developmental Disorders of the Forebrain
ten Donkelaar, H. J., Lammens, M. M. Y., Cruysberg, J. R. M., Ulzen, K. K.-V., Hori, A., Shiota, K., Itoh, K., & Willemsen, M. A. A. P. (2023) · Springer eBooks · doi:10.1007/978-3-031-26098-8_9 · Cited by 2
Pedraza, M., Grampa, V., Scotto‐Lomassese, S., Puech, J., Muzerelle, A., Mohammad, A., Renier, N., Métin, C., & Masson, J. (2024) · eLife · doi:10.7554/elife.100328.1 · Cited by 1
Pedraza, M., Grampa, V., Scotto‐Lomassese, S., Puech, J., Muzerelle, A., Mohammad, A., Lebon, S., Renier, N., Métin, C., & Masson, J. (2025) · eLife · doi:10.7554/elife.100328.3 · Cited by 1
The Role of Dysfunctional Subcortical Circuitry in Mouse Models of Developmental Disability
Wells, M. F. (2015) · DukeSpace (Duke University)
The role of LRP2 in forebrain development of the mouse
Christ, A. (2011) · Universitätsbibliothek der FU Berlin Hochschulschriftenstelle u. Dokumentenserver · doi:10.17169/refubium-9830
Developmental programming of cortical interneurons
Welagen, J. (2011)
Telencephalic Tissue Formation in 3D Stem Cell Culture
Kadoshima, T., Sakaguchi, H., & Eiraku, M. (2017) · Springer eBooks · doi:10.1007/978-981-10-3768-9_1
The construction of 3D cognitive networks from iPSCs through precise spatiotemporal specification
Miu, K.-K., Cao, D., Wang, Z., Hao, S., & Chan, W. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-823809-7.00012-8
Bovolenta, P. (2011) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.13277019.14635134
Metadata
- Authors
- Sousa, V. H., & Fishell, G.
- Affiliations
- NYU Langone Health (US)
- Corresponding author
- Fishell, Gord
- Venue
- Current Opinion in Genetics & Development
- Publisher
- Elsevier BV
- Published
- 2010-08
- Volume
- 20
- Issue
- 4
- Pages
- 391-399
- ISSN
- 0959-437X (ISSN-L)
- PMC
- PMC2991106
- OpenAlex
- W2022089796
- Cited by
- 106
- References
- 73
- Citations by year
- 2026: 1 · 2025: 5 · 2024: 3 · 2023: 5 · 2022: 3 · 2021: 9 · 2020: 5 · 2019: 2 · 2018: 3 · 2017: 6 · 2016: 9 · 2015: 5 · 2014: 14 · 2013: 10 · 2012: 14
- FWCI
- 1.01
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Current Opinion in Genetics & Development (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of Mental Health (R01MH068469, R01MH071679, R37MH071679)
- National Institute of Neurological Disorders and Stroke (R01NS032993, R01NS039007)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Hedgehog Signaling Pathway Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- Sonic hedgehog, morphogen signaling, temporal competence, ventral telencephalon, forebrain development, transcriptional regulation, signaling pathway integration, cell lineage specification
- MeSH terms
- Zinc Finger Protein GLI1, Thyroid Nuclear Factor 1, Animals, Cell Differentiation, Fibroblast Growth Factors, Nuclear Proteins, Telencephalon, Transcription Factors, Signal Transduction, Oncogene Proteins, Trans-Activators, Gene Expression Regulation, Developmental, Body Patterning, Mice, Hedgehog Proteins
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