Regulation of Downstream Neuronal Genes by Proneural Transcription Factors During Initial Neurogenesis in the Vertebrate Brain

Overview

Journal Neural Dev

Publisher Biomed Central

Specialty Neurology

Date 2016 Dec 8

PMID 27923395

Citations 10

Authors

Michelle Ware

Houda Hamdi-Roze

Julien Le Friec

Veronique David

Valerie Dupe

Affiliations

Soon will be listed here.

Abstract

Background: Neurons arise in very specific regions of the neural tube, controlled by components of the Notch signalling pathway, proneural genes, and other bHLH transcription factors. How these specific neuronal areas in the brain are generated during development is just beginning to be elucidated. Notably, the critical role of proneural genes during differentiation of the neuronal populations that give rise to the early axon scaffold in the developing brain is not understood. The regulation of their downstream effectors remains poorly defined.

Results: This study provides the first overview of the spatiotemporal expression of proneural genes in the neuronal populations of the early axon scaffold in both chick and mouse. Overexpression studies and mutant mice have identified a number of specific neuronal genes that are targets of proneural transcription factors in these neuronal populations.

Conclusion: Together, these results improve our understanding of the molecular mechanisms involved in differentiation of the first neuronal populations in the brain.

Citing Articles

A neuroepithelial wave of BMP signalling drives anteroposterior specification of the tuberal hypothalamus.

Chinnaiya K, Burbridge S, Jones A, Kim D, Place E, Manning E Elife. 2023; 12.

PMID: 36718990 PMC: 9917434. DOI: 10.7554/eLife.83133.

Identity, lineage and fates of a temporally distinct progenitor population in the embryonic olfactory epithelium.

Paronett E, Bryan C, Maynard T, LaMantia A Dev Biol. 2023; 495:76-91.

PMID: 36627077 PMC: 9926479. DOI: 10.1016/j.ydbio.2023.01.001.

Genetic Effects of ITPK1 Polymorphisms on the Risk of Neural Tube Defects: a Population-Based Study.

Guan Z, Liang Y, Zhu Z, Yang A, Li S, Wang X Reprod Sci. 2022; 30(5):1585-1593.

PMID: 36323916 DOI: 10.1007/s43032-022-01116-5.

EmAtlas: a comprehensive atlas for exploring spatiotemporal activation in mammalian embryogenesis.

Zheng L, Liang P, Long C, Li H, Li H, Liang Y Nucleic Acids Res. 2022; 51(D1):D924-D932.

PMID: 36189903 PMC: 9825456. DOI: 10.1093/nar/gkac848.

SHH and Notch regulate SOX9+ progenitors to govern arcuate POMC neurogenesis.

Place E, Manning E, Kim D, Kinjo A, Nakamura G, Ohyama K Front Neurosci. 2022; 16:855288.

PMID: 36033614 PMC: 9404380. DOI: 10.3389/fnins.2022.855288.

References

Gohlke J, Armant O, Parham F, Smith M, Zimmer C, Castro D . Characterization of the proneural gene regulatory network during mouse telencephalon development. BMC Biol. 2008; 6:15. PMC: 2330019. DOI: 10.1186/1741-7007-6-15. View

Ware M, Schubert F . Development of the early axon scaffold in the rostral brain of the chick embryo. J Anat. 2011; 219(2):203-16. PMC: 3162240. DOI: 10.1111/j.1469-7580.2011.01389.x. View

Hamburger V, HAMILTON H . A series of normal stages in the development of the chick embryo. J Morphol. 2014; 88(1):49-92. View

Shi M, Hu Z, Zheng M, Song N, Huang Y, Zhao G . Notch-Rbpj signaling is required for the development of noradrenergic neurons in the mouse locus coeruleus. J Cell Sci. 2012; 125(Pt 18):4320-32. DOI: 10.1242/jcs.102152. View

Wapinski O, Vierbuchen T, Qu K, Lee Q, Chanda S, Fuentes D . Hierarchical mechanisms for direct reprogramming of fibroblasts to neurons. Cell. 2013; 155(3):621-35. PMC: 3871197. DOI: 10.1016/j.cell.2013.09.028. View

Lumsden A, Keynes R . Segmental patterns of neuronal development in the chick hindbrain. Nature. 1989; 337(6206):424-8. DOI: 10.1038/337424a0. View

Huang H, Redmond T, Kubish G, Gupta S, Thompson R, Turner D . Transcriptional regulatory events initiated by Ascl1 and Neurog2 during neuronal differentiation of P19 embryonic carcinoma cells. J Mol Neurosci. 2014; 55(3):684-705. DOI: 10.1007/s12031-014-0408-2. View

Castro D, Martynoga B, Parras C, Ramesh V, Pacary E, Johnston C . A novel function of the proneural factor Ascl1 in progenitor proliferation identified by genome-wide characterization of its targets. Genes Dev. 2011; 25(9):930-45. PMC: 3084027. DOI: 10.1101/gad.627811. View

Powell L, Deaton A, Wear M, Jarman A . Specificity of Atonal and Scute bHLH factors: analysis of cognate E box binding sites and the influence of Senseless. Genes Cells. 2008; 13(9):915-29. PMC: 3287287. DOI: 10.1111/j.1365-2443.2008.01217.x. View

10.

Kroger S, Schwarz U . The avian tectobulbar tract: development, explant culture, and effects of antibodies on the pattern of neurite outgrowth. J Neurosci. 1990; 10(9):3118-34. PMC: 6570245. View

11.

Wilson S, Rubenstein J . Induction and dorsoventral patterning of the telencephalon. Neuron. 2001; 28(3):641-51. DOI: 10.1016/s0896-6273(00)00171-9. View

12.

Casarosa S, Fode C, Guillemot F . Mash1 regulates neurogenesis in the ventral telencephalon. Development. 1999; 126(3):525-34. DOI: 10.1242/dev.126.3.525. View

13.

Geoffroy C, Critchley J, Castro D, Ramelli S, Barraclough C, Descombes P . Engineering of dominant active basic helix-loop-helix proteins that are resistant to negative regulation by postnatal central nervous system antineurogenic cues. Stem Cells. 2009; 27(4):847-56. DOI: 10.1002/stem.17. View

14.

Pelling M, Anthwal N, McNay D, Gradwohl G, Leiter A, Guillemot F . Differential requirements for neurogenin 3 in the development of POMC and NPY neurons in the hypothalamus. Dev Biol. 2010; 349(2):406-16. DOI: 10.1016/j.ydbio.2010.11.007. View

15.

Pattyn A, Guillemot F, Brunet J . Delays in neuronal differentiation in Mash1/Ascl1 mutants. Dev Biol. 2006; 295(1):67-75. DOI: 10.1016/j.ydbio.2006.03.008. View

16.

Mastick G, Easter Jr S . Initial organization of neurons and tracts in the embryonic mouse fore- and midbrain. Dev Biol. 1996; 173(1):79-94. DOI: 10.1006/dbio.1996.0008. View

17.

Ratie L, Ware M, Barloy-Hubler F, Rome H, Gicquel I, Dubourg C . Novel genes upregulated when NOTCH signalling is disrupted during hypothalamic development. Neural Dev. 2013; 8:25. PMC: 3880542. DOI: 10.1186/1749-8104-8-25. View

18.

Murdoch J, Eddleston J, Leblond-Bourget N, Stanier P, Copp A . Sequence and expression analysis of Nhlh1: a basic helix-loop-helix gene implicated in neurogenesis. Dev Genet. 1999; 24(1-2):165-77. DOI: 10.1002/(SICI)1520-6408(1999)24:1/2<165::AID-DVG15>3.0.CO;2-V. View

19.

Wolman M, Sittaramane V, Essner J, Yost H, Chandrasekhar A, Halloran M . Transient axonal glycoprotein-1 (TAG-1) and laminin-alpha1 regulate dynamic growth cone behaviors and initial axon direction in vivo. Neural Dev. 2008; 3:6. PMC: 2278142. DOI: 10.1186/1749-8104-3-6. View

20.

Schubert F, Lumsden A . Transcriptional control of early tract formation in the embryonic chick midbrain. Development. 2005; 132(8):1785-93. DOI: 10.1242/dev.01731. View