Regulation of cerebral cortical neurogenesis by the Pax6 transcription factor

Manuel, Martine N.; Mi, Da; Mason, John O.; Price, David J.

doi:10.3389/fncel.2015.00070

Cited by 153Neurogenesis and neuroplasticity mechanismsDevelopmental Biology and Gene RegulationGenetics and Neurodevelopmental Disorders

Regulation of cerebral cortical neurogenesis by the Pax6 transcription factor

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Manuel, Martine N., Mi, Da, Mason, John O., Price, David J.·2015·Frontiers in Cellular Neuroscience

DOI 10.3389/fncel.2015.00070PMC PMC4354436

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Abstract

Understanding brain development remains a major challenge at the heart of understanding what makes us human. The neocortex, in evolutionary terms the newest part of the cerebral cortex, is the seat of higher cognitive functions. Its normal development requires the production, positioning, and appropriate interconnection of very large numbers of both excitatory and inhibitory neurons. Pax6 is one of a relatively small group of transcription factors that exert high-level control of cortical development, and whose mutation or deletion from developing embryos causes major brain defects and a wide range of neurodevelopmental disorders. Pax6 is very highly conserved between primate and non-primate species, is expressed in a gradient throughout the developing cortex and is essential for normal corticogenesis. Our understanding of Pax6's functions and the cellular processes that it regulates during mammalian cortical development has significantly advanced in the last decade, owing to the combined application of genetic and biochemical analyses. Here, we review the functional importance of Pax6 in regulating cortical progenitor proliferation, neurogenesis, and formation of cortical layers and highlight important differences between rodents and primates. We also review the pathological effects of PAX6 mutations in human neurodevelopmental disorders. We discuss some aspects of Pax6's molecular actions including its own complex transcriptional regulation, the distinct molecular functions of its splice variants and some of Pax6's known direct targets which mediate its actions during cortical development.

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Pax6 is one of the few master regulator neural transcription factors with a well-known role in cortical development.
“Pax6 is one of the few “master regulator” neural TFs with a well-known role in cortical development (Manuel et al., 2015).”
From Multiscale 3D Genome Rewiring during Mouse Neural Development (2017) · cites this paper as Manuel et al., 2015

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Multiscale 3D Genome Rewiring during Mouse Neural Development
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PAX6 maintains β cell identity by repressing genes of alternative islet cell types
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Pax6 is essential for the generation of late-born retinal neurons and for inhibition of photoreceptor-fate during late stages of retinogenesis
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Lhx2 regulates the timing of β-catenin-dependent cortical neurogenesis
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The Long Noncoding RNA Paupar Modulates PAX6 Regulatory Activities to Promote Alpha Cell Development and Function
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Regulation of Chromatin Structure During Neural Development
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The intracellular domain of CX3CL1 regulates adult neurogenesis and Alzheimer’s amyloid pathology
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Chlorpyrifos inhibits neural induction via Mfn1-mediated mitochondrial dysfunction in human induced pluripotent stem cells
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Spatially resolved gene regulatory and disease-related vulnerability map of the adult Macaque cortex
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3D promoter architecture re-organization during iPSC-derived neuronal cell differentiation implicates target genes for neurodevelopmental disorders
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PAX6, brain structure and function in human adults: advanced MRI in aniridia
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Development and Characteristics of Pancreatic Epsilon Cells
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Functional Characterization of Three-Dimensional Cortical Cultures for In Vitro Modeling of Brain Networks
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Evolution of genetic mechanisms regulating cortical neurogenesis
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High-resolution transcriptomics informs glial pathology in human temporal lobe epilepsy
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Generation of a PAX6 knockout glioblastoma cell line with changes in cell cycle distribution and sensitivity to oxidative stress
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Vascular endothelial growth factor promotes transdifferentiation of astrocytes into neurons via activation of the MAPK / Erk‐Pax6 signal pathway
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Early Developmental Marginal Zinc Deficiency Affects Neurogenesis Decreasing Neuronal Number and Altering Neuronal Specification in the Adult Rat Brain
Adamo, A. M., Liu, X., Mathieu, P., Nuttall, J. R., Supasai, S., & Oteiza, P. I. (2019) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2019.00062 · Cited by 35 · see citing works
The transcription factor Pax6 contributes to the induction of GLT‐1 expression in astrocytes through an interaction with a distal enhancer element
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FGF-MAPK signaling regulates human deep-layer corticogenesis
Gantner, C. W., Hunt, C. J., Niclis, J. C., Penna, V., McDougall, S. J., Thompson, L. H., & Parish, C. L. (2021) · Stem Cell Reports · doi:10.1016/j.stemcr.2021.03.014 · Cited by 33 · see citing works
Design and validation of an ontology-driven animal-free testing strategy for developmental neurotoxicity testing
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Silver nanoparticles inhibit neural induction in human induced pluripotent stem cells
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The Cytokine CX3CL1 and ADAMs/MMPs in Concerted Cross-Talk Influencing Neurodegenerative Diseases
Iemmolo, M., Ghersi, G., & Bivona, G. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24098026 · Cited by 33 · see citing works
GSK3β Inhibition Restores Impaired Neurogenesis in Preterm Neonates With Intraventricular Hemorrhage
Dohare, P., Kidwai, A., Kaur, J., Singla, P., Krishna, S., Klebe, D. W., Zhang, X., Hevner, R. F., & Ballabh, P. (2018) · Cerebral Cortex · doi:10.1093/cercor/bhy217 · Cited by 31 · see citing works
Dynamics of cortical progenitors and production of subcerebral neurons are altered in embryos of a maternal inflammation model for autism
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Chromatin features, RNA polymerase II and the comparative expression of lens genes encoding crystallins, transcription factors, and autophagy mediators.
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BDNF and JNK Signaling Modulate Cortical Interneuron and Perineuronal Net Development: Implications for Schizophrenia-Linked 16p11.2 Duplication Syndrome
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Network Reconstruction Reveals that Valproic Acid Activates Neurogenic Transcriptional Programs in Adult Brain Following Traumatic Injury
Higgins, G. A., Georgoff, P. E., Nikolian, V. C., Allyn-Feuer, A., Pauls, B., Higgins, R., Athey, B. D., & Alam, H. E. (2017) · Pharmaceutical Research · doi:10.1007/s11095-017-2130-6 · Cited by 28 · see citing works
The relationship between growth and pattern formation
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The impact of maternal immune activation on embryonic brain development
McEwan, F., Glazier, J. D., & Hager, R. (2023) · Frontiers in Neuroscience · doi:10.3389/fnins.2023.1146710 · Cited by 27 · see citing works
Extracellular Pax6 Regulates Tangential Cajal–Retzius Cell Migration in the Developing Mouse Neocortex
Kaddour, H., Coppola, E., Nardo, A. A. D., Poupon, C. L., Mailly, P., Wizenmann, A., Volovitch, M., Prochiantz, A., & Pierani, A. (2019) · Cerebral Cortex · doi:10.1093/cercor/bhz098 · Cited by 25 · see citing works
Rapid and robust directed differentiation of mouse epiblast stem cells into definitive endoderm and forebrain organoids
Medina-Cano, D., Corrigan, E. K., Glenn, R. A., Islam, M. T., Lin, Y., Kim, J., Cho, H., & Vierbuchen, T. (2022) · Development · doi:10.1242/dev.200561 · Cited by 26 · see citing works
OCT parameters of the optic nerve head and the retina as surrogate markers of brain volume in a normal population, a pilot study
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Arx Expression Suppresses Ventralization of the Developing Dorsal Forebrain
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Effects of spike protein and toxin-like peptides found in COVID-19 patients on human 3D neuronal/glial model undergoing differentiation: Possible implications for SARS-CoV-2 impact on brain development
Pistollato, F., Petrillo, M., Clerbaux, L., Leoni, G., Ponti, J., Bogni, A., Brogna, C., Cristoni, S., Sanges, R., Gyves, E. M., et al. (2022) · Reproductive Toxicology · doi:10.1016/j.reprotox.2022.04.011 · Cited by 24 · see citing works
Developmental disruption and restoration of brain synaptome architecture in the murine Pax6 neurodevelopmental disease model
Tomás‐Roca, L., Qiu, Z., Fransén, E. A., Gokhale, R., Bulovaite, E., Price, D. J., Komiyama, N. H., & Grant, S. G. N. (2022) · Nature Communications · doi:10.1038/s41467-022-34131-w · Cited by 22 · see citing works
5-Fluorouracil inhibits neural differentiation via Mfn1/2 reduction in human induced pluripotent stem cells
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GSK126 an inhibitor of epigenetic regulator EZH2 suppresses cardiac fibrosis by regulating the EZH2-PAX6-CXCL10 pathway
Aziz, S., Li, Y., Raza, M. A., Jiao, L., Bilal, A. H. M., & Zhao, W. (2022) · Biochemistry and Cell Biology · doi:10.1139/bcb-2022-0224 · Cited by 22 · see citing works
MeCP2 dysfunction prevents proper BMP signaling and neural progenitor expansion in brain organoid
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Kappa opioid receptor controls neural stem cell differentiation via a miR-7a/Pax6 dependent pathway
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Paired box 6 inhibits cardiac fibroblast differentiation
Feng, Y., Li, M., Wang, S., Cong, W., Hu, G., Song, Y., Xiao, H., Dong, E., & Zhang, Y. (2020) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2020.05.146 · Cited by 19 · see citing works
Enhanced Abventricular Proliferation Compensates Cell Death in the Embryonic Cerebral Cortex
Freret-Hodara, B., Cui, Y., Griveau, A., Vigier, L., Arai, Y., Touboul, J. D., & Pierani, A. (2016) · Cerebral Cortex · doi:10.1093/cercor/bhw264 · Cited by 18 · see citing works
Conserved and divergent functions of Pax6 underlie species-specific neurogenic patterns in the developing amniote brain
Yamashita, W., Takahashi, M., Kikkawa, T., Gotoh, H., Osumi, N., Ono, K., & Nomura, T. (2018) · Development · doi:10.1242/dev.159764 · Cited by 18 · see citing works
Tissue-Specific Actions of Pax6 on Proliferation and Differentiation Balance in Developing Forebrain Are Foxg1 Dependent
Urzainqui, I. Q., Kozić, Z., Mitra, S., Tian, T., Manuel, M. N., Mason, J. O., & Price, D. J. (2018) · iScience · doi:10.1016/j.isci.2018.11.031 · Cited by 18 · see citing works
Dissecting gene regulatory networks governing human cortical cell fate
Ding, J. W., Kim, C. N., Ostrowski, M. S., Abeykoon, Y., Pavlovic, B. J., Wallace, J. L., Schaefer, N. K., Nowakowski, T. J., & Pollen, A. A. (2026) · Nature · doi:10.1038/s41586-025-09997-7 · Cited by 20 · see citing works
Deep mutational scanning quantifies DNA binding and predicts clinical outcomes of PAX6 variants
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Authors: Manuel, M. N., Mi, D., Mason, J. O., & Price, D. J.
Affiliations: University of Edinburgh (GB)
Corresponding author: Price, David J.
ORCID: Manuel, Martine N.
Mi, Da
Mason, John O.
Price, David J.
Venue: Frontiers in Cellular Neuroscience
Publisher: Frontiers Media SA
Published: 2015-03-10
Volume: 9
Pages: 70-70
ISSN: 1662-5102 (ISSN-L)
DOI: 10.3389/fncel.2015.00070
PMC: PMC4354436
OpenAlex: W2054346966
Cited by: 153
References: 249
Citations by year: 2026: 6 · 2025: 11 · 2024: 8 · 2023: 15 · 2022: 25 · 2021: 11 · 2020: 22 · 2019: 16 · 2018: 18 · 2017: 6 · 2016: 8 · 2015: 7
FWCI: 5.26
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
Locations: Frontiers in Cellular Neuroscience (publishedVersion, cc-by)
Europe PMC (PubMed Central) (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
Edinburgh Research Explorer (University of Edinburgh) (submittedVersion, cc-by)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders: Wellcome Trust (099175/Z/12/Z, 099175)
Medical Research Council (MC_PC_15004, J003662/1, MR/J003662/1, J003662, 099175/Z/12/Z)
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 › Genetics › Genetics and Neurodevelopmental Disorders
Keywords: Pax6, cortical development, neocortex, cortical neurogenesis, cortical lamination, transcriptional regulation, PAX6 mutations, neurodevelopmental disorders, excitatory and inhibitory neurons

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Regulation of cerebral cortical neurogenesis by the Pax6 transcription factor

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