Tcf7l2 plays crucial roles in forebrain development through regulation of thalamic and habenular neuron identity and connectivity
Open accessAbstract
The thalamus acts as a central integrator for processing and relaying sensory and motor information to and from the cerebral cortex, and the habenula plays pivotal roles in emotive decision making by modulating dopaminergic and serotonergic circuits. These neural compartments are derived from a common developmental progenitor domain, called prosomere 2, in the caudal forebrain. Thalamic and habenular neurons exhibit distinct molecular profile, neurochemical identity, and axonal circuitry. However, the mechanisms of how their progenitors in prosomere 2 give rise to these two populations of neurons and contribute to the forebrain circuitry remains unclear. In this study, we discovered a previously unrecognized role for Tcf7l2, a transcription factor known as the canonical Wnt nuclear effector and diabetes risk-conferring gene, in establishing neuronal identity and circuits of the caudal forebrain. Using genetic and chemical axon tracers, we showed that efferent axons of the thalamus, known as the thalamocortical axons (TCAs), failed to elongate normally and strayed from their normal course to inappropriate locations in the absence of Tcf7l2. Further experiments with thalamic explants revealed that the pathfinding defects of Tcf7l2-deficient TCAs were associated at least in part with downregulation of guidance receptors Robo1 and Robo2 expression. Moreover, the fasciculus retroflexus, the main habenular output tract, was missing in embryos lacking Tcf7l2. These axonal defects may result from dysregulation of Nrp2 guidance receptor. Strikingly, loss of Tcf7l2 caused a post-mitotic identity switch between thalamic and habenular neurons. Despite normal acquisition of progenitor identity in prosomere 2, Tcf7l2-deficient thalamic neurons adopted a molecular profile of a neighboring forebrain derivative, the habenula. Conversely, habenular neurons failed to maintain their normal post-mitotic neuronal identity and acquired a subset of thalamic neuronal features in the absence of Tcf7l2. Our findings suggest a unique role for Tcf7l2 in generating distinct neuronal phenotypes from homogeneous progenitor population, and provide a better understanding of the mechanism underlying neuronal specification, differentiation, and connectivity of the developing caudal forebrain.
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Gbx2, Shox2 and Tcf7l2 are highly expressed in thalamus glutamatergic neurons, whereas Shox2 and Tcf7l2 are also expressed in midbrain.
“Gbx2, Shox2 and Tcf7l2 are highly expressed in thalamus glutamatergic neurons91,92, whereas Shox2 and Tcf7l2 are also expressed in midbrain.”
From A high-resolution transcriptomic and spatial atlas of cell types in the whole mouse brain (2023) · cites this paper as [91]
Section 2.1 reports high Tcf7l2 expression in thalamic neurons and substantial overlap with Gbx2 in the caudal thalamic mantle zone. Our copy does not establish that these cells are glutamatergic or report Shox2 expression. The midbrain clause follows the citations and is not clearly attributed to this source. (LLM, conf=0.86)
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A high-resolution transcriptomic and spatial atlas of cell types in the whole mouse brain
Yao, Z., van Velthoven, C. T. J., Kunst, M., Zhang, M., McMillen, D., Lee, C., Jung, W., Goldy, J., Abdelhak, A., Aitken, M., et al. (2023) · Nature · doi:10.1038/s41586-023-06812-z · Cited by 1,194 · see citing works
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- Authors
- Lee, M., Yoon, J., Song, H., Lee, B., Lam, D. T., Yoon, J., Baek, K., Clevers, H., & Jeong, Y.
- Affiliations
- Kyung Hee University (KR)
- Royal Netherlands Academy of Arts and Sciences (NL)
- Corresponding author
- Jeong, Yongsu
- Venue
- Developmental Biology
- Publisher
- Elsevier BV
- Published
- 2017-04
- Volume
- 424
- Issue
- 1
- Pages
- 62-76
- ISSN
- 0012-1606 (ISSN-L)
- OpenAlex
- W2590045466
- Cited by
- 48
- References
- 74
- Citations by year
- 2026: 3 · 2025: 5 · 2024: 6 · 2023: 8 · 2022: 8 · 2021: 5 · 2020: 4 · 2019: 6 · 2018: 2
- FWCI
- 1.61
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Developmental Biology (publishedVersion)
- PubMed (publishedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- Utrecht University Repository (Utrecht University) (submittedVersion, other-oa)
- KNAW Research Portal (The Royal Netherlands Academy of Arts and Sciences) (submittedVersion)
- Utrecht University Repository (Utrecht University) (submittedVersion)
- Funders
- National Research Foundation (2015R1A2A2A01002373)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Axon Guidance and Neuronal Signaling
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Keywords
- TCF7L2, thalamus, habenula, neuronal identity specification, axon guidance, thalamocortical connections, fasciculus retroflexus, ROBO1, Robo2, neuropilin-2, Wnt signaling, neuronal specification
- MeSH terms
- Axon Guidance, Animals, Axons, Diencephalon, Mitosis, Mutation, Nerve Net, Neurons, Protein Binding, Stem Cells, Thalamus, Transcription, Genetic, Biomarkers, Homeodomain Proteins, Habenula, Body Patterning, Mice, Transcription Factor 7-Like 2 Protein
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