Multifaceted Regulation of Neural Stem Cell Fate in the Developing Brain
Article Sidebar
Published
Mar 26, 2024
Downloads
Download data is not yet available.
Submit your own article
Register as an author to reserve your spot in the next issue of the Medical Research Archives.
Author RegistrationJoin the Society
The European Society of Medicine is more than a professional association. We are a community. Our members work in countries across the globe, yet are united by a common goal: to promote health and health equity, around the world.
Join Europe’s leading medical society and discover the many advantages of membership, including free article publication.
MembershipMain Article Content
Abstract
Stem cells are the source of diverse cell types, and therefore their fate decisions are tightly regulated by multiple layers of controls in each tissue. Without a doubt, the brain is one of the most complex and highly functional tissues, as we now know more than 70 million neurons and even more non-neuronal cells are distributed across dozens of cortical areas in the mouse cerebral cortex, and a single region of cortex contains more than 40 cell types. These diverse neuronal cells emerge from initially homogeneous neural stem cells during embryonic development. In the course of differentiation, neural stem cells undergo cellular division to produce daughter cells with new cellular identities, during which epigenetic and transcriptional regulations determine their fate. Recent advances in the field of neural stem cell biology have revealed that not only epigenetic regulators and transcription factors but also specialized intracellular organelles regulate many aspects of stem cell functions and fate choices, and therefore it is timely to review the mechanisms of sophisticated changes of the properties of neural stem cells during development and how they impact the function of the daughter cells.
Keywords:
Neural stem cells, fate specification, epigenetics, transcription factors, organelles
Article Details
How to Cite
UOTSU, Takanobu et al.
Multifaceted Regulation of Neural Stem Cell Fate in the Developing Brain.
Medical Research Archives, [S.l.], v. 12, n. 3, mar. 2024.
ISSN 2375-1924.
Available at: <https://esmed.org/MRA/mra/article/view/5084>. Date accessed: 30 apr. 2024.
doi: https://doi.org/10.18103/mra.v12i3.5084.
Section
Research Articles
The Medical Research Archives grants authors the right to publish and reproduce the unrevised contribution in whole or in part at any time and in any form for any scholarly non-commercial purpose with the condition that all publications of the contribution include a full citation to the journal as published by the Medical Research Archives.
References
1. Paridaen JTML, Huttner WB. Neurogenesis during development of the vertebrate central nervous system. EMBO Rep. 2014;15(4):351-364. doi:10.1002/embr.201438447
2. Stepien BK, Vaid S, Huttner WB. Length of the neurogenic period-A key determinant for the generation of upper-layer neurons during neocortex development and evolution. Front Cell Dev Biol. 2021;9:676911. doi:10.3389/fcell.2021.676911
3. Hemberger M, Dean W, Reik W. Epigenetic dynamics of stem cells and cell lineage commitment: digging Waddington’s canal. Nat Rev Mol Cell Biol. 2009;10(8):526-537. doi:10.1038/nrm2727
4. Bowles J, Schepers G, Koopman P. Phylogeny of the SOX family of developmental transcription factors based on sequence and structural indicators. Dev Biol. 2000;227(2):239-255. doi:10.1006/dbio.2000.9883
5. Skinner MK, Rawls A, Wilson-Rawls J, Roalson EH. Basic helix-loop-helix transcription factor gene family phylogenetics and nomenclature. Differentiation. 2010;80(1):1-8. doi:10.1016/j.diff.2010.02.003
6. Temple S. The development of neural stem cells. Nature. 2001;414(6859):112-117. doi:10.1038/35102174
7. Lefebvre V, Dumitriu B, Penzo-Méndez A, Han Y, Pallavi B. Control of cell fate and differentiation by Sry-related high-mobility-group box (Sox) transcription factors. Int J Biochem Cell Biol. 2007;39(12):2195-2214. doi:10.1016/j.biocel.2007.05.019
8. Pevny L, Placzek M. SOX genes and neural progenitor identity. Curr Opin Neurobiol. 2005;15(1):7-13. doi:10.1016/j.conb.2005.01.016
9. Wegner M, Stolt CC. From stem cells to neurons and glia: a Soxist’s view of neural development. Trends Neurosci. 2005;28(11):583-588. doi:10.1016/j.tins.2005.08.008
10. Shimojo H, Ohtsuka T, Kageyama R. Oscillations in notch signaling regulate maintenance of neural progenitors. Neuron. 2008;58(1):52-64. doi:10.1016/j.neuron.2008.02.014
11. Ishibashi M, Ang SL, Shiota K, Nakanishi S, Kageyama R, Guillemot F. Targeted disruption of mammalian hairy and Enhancer of split homolog-1 (HES-1) leads to up-regulation of neural helix-loop-helix factors, premature neurogenesis, and severe neural tube defects. Genes Dev. 1995;9(24):3136-3148. doi:10.1101/gad.9.24.3136
12. Takebayashi K, Sasai Y, Sakai Y, Watanabe T, Nakanishi S, Kageyama R. Structure, chromosomal locus, and promoter analysis of the gene encoding the mouse helix-loop-helix factor HES-1. Negative autoregulation through the multiple N box elements. J Biol Chem. 1994;269(7):5150-5156. doi:10.1016/S0021-9258(17)37668-8
13. Sommer L, Ma Q, Anderson DJ. neurogenins, a novel family of atonal-related bHLH transcription factors, are putative mammalian neuronal determination genes that reveal progenitor cell heterogeneity in the developing CNS and PNS. Mol Cell Neurosci. 1996;8(4):221-241. doi:10.1006/mcne.1996.0060
14. Bertrand N, Castro DS, Guillemot F. Proneural genes and the specification of neural cell types. Nat Rev Neurosci. 2002;3(7):517-530. doi:10.1038/nrn874
15. Ma Q, Kintner C, Anderson DJ. Identification of neurogenin, a vertebrate neuronal determination gene. Cell. 1996;87(1):43-52. doi:10.1016/s0092-8674(00)81321-5
16. Sun Y, Nadal-Vicens M, Misono S, et al. Neurogenin promotes neurogenesis and inhibits glial differentiation by independent mechanisms. Cell. 2001;104(3):365-376. doi:10.1016/s0092-8674(01)00224-0
17. Farah MH, Olson JM, Sucic HB, Hume RI, Tapscott SJ, Turner DL. Generation of neurons by transient expression of neural bHLH proteins in mammalian cells. Development. 2000;127(4):693-702. doi:10.1242/dev.127.4.693
18. Fode C, Ma Q, Casarosa S, Ang SL, Anderson DJ, Guillemot F. A role for neural determination genes in specifying the dorsoventral identity of telencephalic neurons. Genes Dev. 2000;14(1):67-80. doi:10.1101/gad.14.1.67
19. Ma Q, Sommer L, Cserjesi P, Anderson DJ. Mash1 and neurogenin1 expression patterns define complementary domains of neuroepithelium in the developing CNS and are correlated with regions expressing notch ligands. J Neurosci. 1997;17(10):3644-3652. doi:10.1523/jneurosci.17-10-03644.1997
20. Tutukova S, Tarabykin V, Hernandez-Miranda LR. The role of Neurod genes in brain development, function, and disease. Front Mol Neurosci. 2021;14:662774. doi:10.3389/fnmol.2021.662774
21. Uchikawa M, Kamachi Y, Kondoh H. Two distinct subgroups of Group B Sox genes for transcriptional activators and repressors: their expression during embryonic organogenesis of the chicken. Mech Dev. 1999;84(1-2):103-120. doi:10.1016/s0925-4773(99)00083-0
22. Bergsland M, Ramsköld D, Zaouter C, Klum S, Sandberg R, Muhr J. Sequentially acting Sox transcription factors in neural lineage development. Genes Dev. 2011;25(23):2453-2464. doi:10.1101/gad.176008.111
23. Bergsland M, Werme M, Malewicz M, Perlmann T, Muhr J. The establishment of neuronal properties is controlled by Sox4 and Sox11. Genes Dev. 2006;20(24):3475-3486. doi:10.1101/gad.403406
24. Klum S, Zaouter C, Alekseenko Z, et al. Sequentially acting SOX proteins orchestrate astrocyte- and oligodendrocyte-specific gene expression. EMBO Rep. 2018;19(11):e46635. doi:10.15252/embr.201846635
25. Maka M, Stolt CC, Wegner M. Identification of Sox8 as a modifier gene in a mouse model of Hirschsprung disease reveals underlying molecular defect. Dev Biol. 2005;277(1):155-169. doi:10.1016/j.ydbio.2004.09.014
26. Sock E, Schmidt K, Hermanns-Borgmeyer I, Bösl MR, Wegner M. Idiopathic weight reduction in mice deficient in the high-mobility-group transcription factor Sox8. Mol Cell Biol. 2001;21(20):6951-6959. doi:10.1128/MCB.21.20.6951-6959.2001
27. International Multiple Sclerosis Genetics Consortium, Lill CM, Schjeide BMM, et al. MANBA, CXCR5, SOX8, RPS6KB1 and ZBTB46 are genetic risk loci for multiple sclerosis. Brain. 2013;136(Pt 6):1778-1782. doi:10.1093/brain/awt101
28. Iwamoto K, Bundo M, Yamada K, et al. DNA methylation status of SOX10 correlates with its downregulation and oligodendrocyte dysfunction in schizophrenia. J Neurosci. 2005;25(22):5376-5381. doi:10.1523/JNEUROSCI.0766-05.2005
29. Meijer DH, Kane MF, Mehta S, et al. Separated at birth? The functional and molecular divergence of OLIG1 and OLIG2. Nat Rev Neurosci. 2012;13(12):819-831. doi:10.1038/nrn3386
30. Takebayashi H, Yoshida S, Sugimori M, et al. Dynamic expression of basic helix-loop-helix Olig family members: implication of Olig2 in neuron and oligodendrocyte differentiation and identification of a new member, Olig3. Mech Dev. 2000;99(1-2):143-148. doi:10.1016/s0925-4773(00)00466-4
31. Othman A, Frim DM, Polak P, Vujicic S, Arnason BGW, Boullerne AI. Olig1 is expressed in human oligodendrocytes during maturation and regeneration. Glia. 2011;59(6):914-926. doi:10.1002/glia.21163
32. Li H, Lu Y, Smith HK, Richardson WD. Olig1 and Sox10 interact synergistically to drive myelin basic protein transcription in oligodendrocytes. J Neurosci. 2007;27(52):14375-14382. doi:10.1523/JNEUROSCI.4456-07.2007
33. Ono K, Takebayashi H, Ikeda K, et al. Regional- and temporal-dependent changes in the differentiation of Olig2 progenitors in the forebrain, and the impact on astrocyte development in the dorsal pallium. Dev Biol. 2008;320(2):456-468. doi:10.1016/j.ydbio.2008.06.001
34. Vierbuchen T, Ostermeier A, Pang ZP, Kokubu Y, Südhof TC, Wernig M. Direct conversion of fibroblasts to functional neurons by defined factors. Nature. 2010;463(7284):1035-1041. doi:10.1038/nature08797
35. Pang ZP, Yang N, Vierbuchen T, et al. Induction of human neuronal cells by defined transcription factors. Nature. 2011;476(7359):220-223. doi:10.1038/nature10202
36. Heinrich C, Blum R, Gascón S, et al. Directing astroglia from the cerebral cortex into subtype specific functional neurons. PLoS Biol. 2010;8(5):e1000373. doi:10.1371/journal.pbio.1000373
37. Guo Z, Zhang L, Wu Z, Chen Y, Wang F, Chen G. In vivo direct reprogramming of reactive glial cells into functional neurons after brain injury and in an Alzheimer’s disease model. Cell Stem Cell. 2014;14(2):188-202. doi:10.1016/j.stem.2013.12.001
38. Brulet R, Matsuda T, Zhang L, et al. NEUROD1 instructs neuronal conversion in non-reactive astrocytes. Stem Cell Reports. 2017;8(6):1506-1515. doi:10.1016/j.stemcr.2017.04.013
39. Liu Y, Miao Q, Yuan J, et al. Ascl1 converts dorsal midbrain astrocytes into functional neurons in vivo. J Neurosci. 2015;35(25):9336-9355. doi:10.1523/JNEUROSCI.3975-14.2015
40. Matsuda T, Irie T, Katsurabayashi S, et al. Pioneer factor NeuroD1 rearranges transcriptional and epigenetic profiles to execute microglia-neuron conversion. Neuron. 2019;101(3):472-485.e7. doi:10.1016/j.neuron.2018.12.010
41. Takouda J, Katada S, Imamura T, Sanosaka T, Nakashima K. SoxE group transcription factor Sox8 promotes astrocytic differentiation of neural stem/precursor cells downstream of Nfia. Pharmacol Res Perspect. 2021;9(6):e00749. doi:10.1002/prp2.749
42. Katada S, Takouda J, Nakagawa T, et al. Neural stem/precursor cells dynamically change their epigenetic landscape to differentially respond to BMP signaling for fate switching during brain development. Genes Dev. 2021;35(21-22):1431-1444. doi:10.1101/gad.348797.121
43. Monk D, Mackay DJG, Eggermann T, Maher ER, Riccio A. Genomic imprinting disorders: lessons on how genome, epigenome and environment interact. Nat Rev Genet. 2019;20(4):235-248. doi:10.1038/s41576-018-0092-0
44. Ohgane J, Wakayama T, Kogo Y, et al. DNA methylation variation in cloned mice. Genesis. 2001;30(2):45-50. doi:10.1002/gene.1031
45. Song X, Li F, Jiang Z, et al. Imprinting disorder in donor cells is detrimental to the development of cloned embryos in pigs. Oncotarget. 2017;8(42):72363-72374. doi:10.18632/oncotarget.20390
46. Imamura T, Ohgane J, Ito S, et al. CpG island of rat sphingosine kinase-1 gene: tissue-dependent DNA methylation status and multiple alternative first exons. Genomics. 2001;76(1-3):117-125. doi:10.1006/geno.2001.6607
47. Sanosaka T, Imamura T, Hamazaki N, et al. DNA Methylome Analysis Identifies Transcription Factor-Based Epigenomic Signatures of Multilineage Competence in Neural Stem/Progenitor Cells. Cell Rep. 2017;20(12):2992-3003. doi:10.1016/j.celrep.2017.08.086
48. Takizawa T, Nakashima K, Namihira M, et al. DNA methylation is a critical cell-intrinsic determinant of astrocyte differentiation in the fetal brain. Dev Cell. 2001;1(6):749-758. doi:10.1016/s1534-5807(01)00101-0
49. Namihira M, Kohyama J, Semi K, et al. Committed neuronal precursors confer astrocytic potential on residual neural precursor cells. Dev Cell. 2009;16(2):245-255. doi:10.1016/j.devcel.2008.12.014
50. Peterson CL, Laniel MA. Histones and histone modifications. Curr Biol. 2004;14(14):R546-51. doi:10.1016/j.cub.2004.07.007
51. Torres IO, Fujimori DG. Functional coupling between writers, erasers and readers of histone and DNA methylation. Curr Opin Struct Biol. 2015;35:68-75. doi:10.1016/j.sbi.2015.09.007
52. Li F, Wan M, Zhang B, et al. Bivalent histone modifications and development. Curr Stem Cell Res Ther. 2018;13(2):83-90. doi:10.2174/1574888X12666170123144743
53. Sarmento OF, Digilio LC, Wang Y, et al. Dynamic alterations of specific histone modifications during early murine development. J Cell Sci. 2004;117(Pt 19):4449-4459. doi:10.1242/jcs.01328
54. Zhang B, Zheng H, Huang B, et al. Allelic reprogramming of the histone modification H3K4me3 in early mammalian development. Nature. 2016;537(7621):553-557. doi:10.1038/nature19361
55. Eissenberg JC, Shilatifard A. Histone H3 lysine 4 (H3K4) methylation in development and differentiation. Dev Biol. 2010;339(2):240-249. doi:10.1016/j.ydbio.2009.08.017
56. Flanagan JF, Mi LZ, Chruszcz M, et al. Double chromodomains cooperate to recognize the methylated histone H3 tail. Nature. 2005;438(7071):1181-1185. doi:10.1038/nature04290
57. Sun G, Alzayady K, Stewart R, et al. Histone demethylase LSD1 regulates neural stem cell proliferation. Mol Cell Biol. 2010;30(8):1997-2005. doi:10.1128/MCB.01116-09
58. Kong SY, Kim W, Lee HR, Kim HJ. The histone demethylase KDM5A is required for the repression of astrocytogenesis and regulated by the translational machinery in neural progenitor cells. FASEB J. 2018;32(2):1108-1119. doi:10.1096/fj.201700780r
59. Golebiewska A, Atkinson SP, Lako M, Armstrong L. Epigenetic landscaping during hESC differentiation to neural cells. Stem Cells. 2009;27(6):1298-1308. doi:10.1002/stem.59
60. Lin H, Zhu X, Chen G, et al. KDM3A-mediated demethylation of histone H3 lysine 9 facilitates the chromatin binding of Neurog2 during neurogenesis. Development. 2017;144(20):3674-3685. doi:10.1242/dev.144113
61. Cao R, Wang L, Wang H, et al. Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science. 2002;298(5595):1039-1043. doi:10.1126/science.1076997
62. Lavarone E, Barbieri CM, Pasini D. Dissecting the role of H3K27 acetylation and methylation in PRC2 mediated control of cellular identity. Nat Commun. 2019;10(1):1679. doi:10.1038/s41467-019-09624-w
63. Min IM, Waterfall JJ, Core LJ, Munroe RJ, Schimenti J, Lis JT. Regulating RNA polymerase pausing and transcription elongation in embryonic stem cells. Genes Dev. 2011;25(7):742-754. doi:10.1101/gad.2005511
64. Laible G, Wolf A, Dorn R, et al. Mammalian homologues of the Polycomb-group gene Enhancer of zeste mediate gene silencing in Drosophila heterochromatin and at S. cerevisiae telomeres. EMBO J. 1997;16(11):3219-3232. doi:10.1093/emboj/16.11.3219
65. Hirabayashi Y, Suzki N, Tsuboi M, et al. Polycomb limits the neurogenic competence of neural precursor cells to promote astrogenic fate transition. Neuron. 2009;63(5):600-613. doi:10.1016/j.neuron.2009.08.021
66. He S, Wu Z, Tian Y, et al. Structure of nucleosome-bound human BAF complex. Science. 2020;367(6480):875-881. doi:10.1126/science.aaz9761
67. Sokpor G, Xie Y, Rosenbusch J, Tuoc T. Chromatin remodeling BAF (SWI/SNF) complexes in neural development and disorders. Front Mol Neurosci. 2017;10:243. doi:10.3389/fnmol.2017.00243
68. Tuoc TC, Boretius S, Sansom SN, et al. Chromatin regulation by BAF170 controls cerebral cortical size and thickness. Dev Cell. 2013;25(3):256-269. doi:10.1016/j.devcel.2013.04.005
69. Torchy MP, Hamiche A, Klaholz BP. Structure and function insights into the NuRD chromatin remodeling complex. Cell Mol Life Sci. 2015;72(13):2491-2507. doi:10.1007/s00018-015-1880-8
70. Nitarska J, Smith JG, Sherlock WT, et al. A Functional Switch of NuRD Chromatin Remodeling Complex Subunits Regulates Mouse Cortical Development. Cell Rep. 2016;17(6):1683-1698. doi:10.1016/j.celrep.2016.10.022
71. Sansom SN, Griffiths DS, Faedo A, et al. The level of the transcription factor Pax6 is essential for controlling the balance between neural stem cell self-renewal and neurogenesis. PLoS Genet. 2009;5(6):e1000511. doi:10.1371/journal.pgen.1000511
72. Graham V, Khudyakov J, Ellis P, Pevny L. SOX2 Functions to Maintain Neural Progenitor Identity. Neuron. 2003;39(5):749-765. doi:10.1016/S0896-6273(03)00497-5
73. Nakashima K, Takizawa T, Ochiai W, et al. BMP2-mediated alteration in the developmental pathway of fetal mouse brain cells from neurogenesis to astrocytogenesis. Proc Natl Acad Sci U S A. 2001;98(10):5868-5873. doi:10.1073/pnas.101109698
74. Nakashima K, Yanagisawa M, Arakawa H, et al. Synergistic signaling in fetal brain by STAT3-Smad1 complex bridged by p300. Science. 1999;284(5413):479-482. doi:10.1126/science.284.5413.479
75. Wang X, Tsai JW, Imai JH, Lian WN, Vallee RB, Shi SH. Asymmetric centrosome inheritance maintains neural progenitors in the neocortex. Nature. 2009;461(7266):947-955. doi:10.1038/nature08435
76. Wilsch-Bräuninger M, Huttner WB. Primary cilia and centrosomes in neocortex development. Front Neurosci. 2021;15:755867. doi:10.3389/fnins.2021.755867
77. Shao W, Yang J, He M, et al. Centrosome anchoring regulates progenitor properties and cortical formation. Nature. 2020;580(7801):106-112. doi:10.1038/s41586-020-2139-6
78. Failler M, Gee HY, Krug P, et al. Mutations of CEP83 cause infantile nephronophthisis and intellectual disability. Am J Hum Genet. 2014;94(6):905-914. doi:10.1016/j.ajhg.2014.05.002
79. O’Neill AC, Uzbas F, Antognolli G, et al. Spatial centrosome proteome of human neural cells uncovers disease-relevant heterogeneity. Science. 2022;376(6599):eabf9088. doi:10.1126/science.abf9088
80. Iaconis D, Monti M, Renda M, et al. The centrosomal OFD1 protein interacts with the translation machinery and regulates the synthesis of specific targets. Sci Rep. 2017;7(1). doi:10.1038/s41598-017-01156-x
81. Taverna E, Mora-Bermúdez F, Strzyz PJ, et al. Non-canonical features of the Golgi apparatus in bipolar epithelial neural stem cells. Sci Rep. 2016;6(1):21206. doi:10.1038/srep21206
82. Xie Z, Hur SK, Zhao L, Abrams CS, Bankaitis VA. A Golgi lipid signaling pathway controls apical Golgi distribution and cell polarity during neurogenesis. Dev Cell. 2018;44(6):725-740.e4. doi:10.1016/j.devcel.2018.02.025
83. Ge X, Gong H, Dumas K, et al. Missense-depleted regions in population exomes implicate ras superfamily nucleotide-binding protein alteration in patients with brain malformation. NPJ Genom Med. 2016;1(1). doi:10.1038/npjgenmed.2016.36
84. Settembre C, Fraldi A, Medina DL, Ballabio A. Signals from the lysosome: a control centre for cellular clearance and energy metabolism. Nat Rev Mol Cell Biol. 2013;14(5):283-296. doi:10.1038/nrm3565
85. Yuizumi N, Harada Y, Kuniya T, et al. Maintenance of neural stem-progenitor cells by the lysosomal biosynthesis regulators TFEB and TFE3 in the embryonic mouse telencephalon. Stem Cells. 2021;39(7):929-944. doi:10.1002/stem.3359
86. Leeman DS, Hebestreit K, Ruetz T, et al. Lysosome activation clears aggregates and enhances quiescent neural stem cell activation during aging. Science. 2018;359(6381):1277-1283. doi:10.1126/science.aag3048
87. Kobayashi T, Piao W, Takamura T, et al. Enhanced lysosomal degradation maintains the quiescent state of neural stem cells. Nat Commun. 2019;10(1):5446. doi:10.1038/s41467-019-13203-4
88. Cochard LM, Levros LC Jr, Joppé SE, Pratesi F, Aumont A, Fernandes KJL. Manipulation of EGFR-induced signaling for the recruitment of quiescent neural stem cells in the adult mouse forebrain. Front Neurosci. 2021;15:621076. doi:10.3389/fnins.2021.621076
89. Kann O, Kovács R. Mitochondria and neuronal activity. Am J Physiol Cell Physiol. 2007;292(2):C641-57. doi:10.1152/ajpcell.00222.2006
90. Youle RJ, van der Bliek AM. Mitochondrial fission, fusion, and stress. Science. 2012;337(6098):1062-1065. doi:10.1126/science.1219855
91. Iwata R, Casimir P, Vanderhaeghen P. Mitochondrial dynamics in postmitotic cells regulate neurogenesis. Science. 2020;369(6505):858-862. doi:10.1126/science.aba9760
92. Iwata R, Casimir P, Erkol E, et al. Mitochondria metabolism sets the species-specific tempo of neuronal development. Science. 2023;379(6632):eabn4705. doi:10.1126/science.abn4705
93. Namba T, Dóczi J, Pinson A, et al. Human-Specific ARHGAP11B Acts in Mitochondria to Expand Neocortical Progenitors by Glutaminolysis. Neuron. 2020;105(5):867-881.e9. doi:10.1016/j.neuron.2019.11.027
94. Journiac N, Gilabert-Juan J, Cipriani S, et al. Cell Metabolic Alterations due to Mcph1 Mutation in Microcephaly. Cell Rep. 2020;31(2):107506. doi:10.1016/j.celrep.2020.03.070
95. Zeisel A, Muñoz-Manchado AB, Codeluppi S, et al. Brain structure. Cell types in the mouse cortex and hippocampus revealed by single-cell RNA-seq. Science. 2015;347(6226):1138-1142. doi:10.1126/science.aaa1934
96. John Lin CC, Yu K, Hatcher A, et al. Identification of diverse astrocyte populations and their malignant analogs. Nat Neurosci. 2017;20(3):396-405. doi:10.1038/nn.4493
97. Lanjakornsiripan D, Pior BJ, Kawaguchi D, et al. Layer-specific morphological and molecular differences in neocortical astrocytes and their dependence on neuronal layers. Nat Commun. 2018;9(1). doi:10.1038/s41467-018-03940-3
2. Stepien BK, Vaid S, Huttner WB. Length of the neurogenic period-A key determinant for the generation of upper-layer neurons during neocortex development and evolution. Front Cell Dev Biol. 2021;9:676911. doi:10.3389/fcell.2021.676911
3. Hemberger M, Dean W, Reik W. Epigenetic dynamics of stem cells and cell lineage commitment: digging Waddington’s canal. Nat Rev Mol Cell Biol. 2009;10(8):526-537. doi:10.1038/nrm2727
4. Bowles J, Schepers G, Koopman P. Phylogeny of the SOX family of developmental transcription factors based on sequence and structural indicators. Dev Biol. 2000;227(2):239-255. doi:10.1006/dbio.2000.9883
5. Skinner MK, Rawls A, Wilson-Rawls J, Roalson EH. Basic helix-loop-helix transcription factor gene family phylogenetics and nomenclature. Differentiation. 2010;80(1):1-8. doi:10.1016/j.diff.2010.02.003
6. Temple S. The development of neural stem cells. Nature. 2001;414(6859):112-117. doi:10.1038/35102174
7. Lefebvre V, Dumitriu B, Penzo-Méndez A, Han Y, Pallavi B. Control of cell fate and differentiation by Sry-related high-mobility-group box (Sox) transcription factors. Int J Biochem Cell Biol. 2007;39(12):2195-2214. doi:10.1016/j.biocel.2007.05.019
8. Pevny L, Placzek M. SOX genes and neural progenitor identity. Curr Opin Neurobiol. 2005;15(1):7-13. doi:10.1016/j.conb.2005.01.016
9. Wegner M, Stolt CC. From stem cells to neurons and glia: a Soxist’s view of neural development. Trends Neurosci. 2005;28(11):583-588. doi:10.1016/j.tins.2005.08.008
10. Shimojo H, Ohtsuka T, Kageyama R. Oscillations in notch signaling regulate maintenance of neural progenitors. Neuron. 2008;58(1):52-64. doi:10.1016/j.neuron.2008.02.014
11. Ishibashi M, Ang SL, Shiota K, Nakanishi S, Kageyama R, Guillemot F. Targeted disruption of mammalian hairy and Enhancer of split homolog-1 (HES-1) leads to up-regulation of neural helix-loop-helix factors, premature neurogenesis, and severe neural tube defects. Genes Dev. 1995;9(24):3136-3148. doi:10.1101/gad.9.24.3136
12. Takebayashi K, Sasai Y, Sakai Y, Watanabe T, Nakanishi S, Kageyama R. Structure, chromosomal locus, and promoter analysis of the gene encoding the mouse helix-loop-helix factor HES-1. Negative autoregulation through the multiple N box elements. J Biol Chem. 1994;269(7):5150-5156. doi:10.1016/S0021-9258(17)37668-8
13. Sommer L, Ma Q, Anderson DJ. neurogenins, a novel family of atonal-related bHLH transcription factors, are putative mammalian neuronal determination genes that reveal progenitor cell heterogeneity in the developing CNS and PNS. Mol Cell Neurosci. 1996;8(4):221-241. doi:10.1006/mcne.1996.0060
14. Bertrand N, Castro DS, Guillemot F. Proneural genes and the specification of neural cell types. Nat Rev Neurosci. 2002;3(7):517-530. doi:10.1038/nrn874
15. Ma Q, Kintner C, Anderson DJ. Identification of neurogenin, a vertebrate neuronal determination gene. Cell. 1996;87(1):43-52. doi:10.1016/s0092-8674(00)81321-5
16. Sun Y, Nadal-Vicens M, Misono S, et al. Neurogenin promotes neurogenesis and inhibits glial differentiation by independent mechanisms. Cell. 2001;104(3):365-376. doi:10.1016/s0092-8674(01)00224-0
17. Farah MH, Olson JM, Sucic HB, Hume RI, Tapscott SJ, Turner DL. Generation of neurons by transient expression of neural bHLH proteins in mammalian cells. Development. 2000;127(4):693-702. doi:10.1242/dev.127.4.693
18. Fode C, Ma Q, Casarosa S, Ang SL, Anderson DJ, Guillemot F. A role for neural determination genes in specifying the dorsoventral identity of telencephalic neurons. Genes Dev. 2000;14(1):67-80. doi:10.1101/gad.14.1.67
19. Ma Q, Sommer L, Cserjesi P, Anderson DJ. Mash1 and neurogenin1 expression patterns define complementary domains of neuroepithelium in the developing CNS and are correlated with regions expressing notch ligands. J Neurosci. 1997;17(10):3644-3652. doi:10.1523/jneurosci.17-10-03644.1997
20. Tutukova S, Tarabykin V, Hernandez-Miranda LR. The role of Neurod genes in brain development, function, and disease. Front Mol Neurosci. 2021;14:662774. doi:10.3389/fnmol.2021.662774
21. Uchikawa M, Kamachi Y, Kondoh H. Two distinct subgroups of Group B Sox genes for transcriptional activators and repressors: their expression during embryonic organogenesis of the chicken. Mech Dev. 1999;84(1-2):103-120. doi:10.1016/s0925-4773(99)00083-0
22. Bergsland M, Ramsköld D, Zaouter C, Klum S, Sandberg R, Muhr J. Sequentially acting Sox transcription factors in neural lineage development. Genes Dev. 2011;25(23):2453-2464. doi:10.1101/gad.176008.111
23. Bergsland M, Werme M, Malewicz M, Perlmann T, Muhr J. The establishment of neuronal properties is controlled by Sox4 and Sox11. Genes Dev. 2006;20(24):3475-3486. doi:10.1101/gad.403406
24. Klum S, Zaouter C, Alekseenko Z, et al. Sequentially acting SOX proteins orchestrate astrocyte- and oligodendrocyte-specific gene expression. EMBO Rep. 2018;19(11):e46635. doi:10.15252/embr.201846635
25. Maka M, Stolt CC, Wegner M. Identification of Sox8 as a modifier gene in a mouse model of Hirschsprung disease reveals underlying molecular defect. Dev Biol. 2005;277(1):155-169. doi:10.1016/j.ydbio.2004.09.014
26. Sock E, Schmidt K, Hermanns-Borgmeyer I, Bösl MR, Wegner M. Idiopathic weight reduction in mice deficient in the high-mobility-group transcription factor Sox8. Mol Cell Biol. 2001;21(20):6951-6959. doi:10.1128/MCB.21.20.6951-6959.2001
27. International Multiple Sclerosis Genetics Consortium, Lill CM, Schjeide BMM, et al. MANBA, CXCR5, SOX8, RPS6KB1 and ZBTB46 are genetic risk loci for multiple sclerosis. Brain. 2013;136(Pt 6):1778-1782. doi:10.1093/brain/awt101
28. Iwamoto K, Bundo M, Yamada K, et al. DNA methylation status of SOX10 correlates with its downregulation and oligodendrocyte dysfunction in schizophrenia. J Neurosci. 2005;25(22):5376-5381. doi:10.1523/JNEUROSCI.0766-05.2005
29. Meijer DH, Kane MF, Mehta S, et al. Separated at birth? The functional and molecular divergence of OLIG1 and OLIG2. Nat Rev Neurosci. 2012;13(12):819-831. doi:10.1038/nrn3386
30. Takebayashi H, Yoshida S, Sugimori M, et al. Dynamic expression of basic helix-loop-helix Olig family members: implication of Olig2 in neuron and oligodendrocyte differentiation and identification of a new member, Olig3. Mech Dev. 2000;99(1-2):143-148. doi:10.1016/s0925-4773(00)00466-4
31. Othman A, Frim DM, Polak P, Vujicic S, Arnason BGW, Boullerne AI. Olig1 is expressed in human oligodendrocytes during maturation and regeneration. Glia. 2011;59(6):914-926. doi:10.1002/glia.21163
32. Li H, Lu Y, Smith HK, Richardson WD. Olig1 and Sox10 interact synergistically to drive myelin basic protein transcription in oligodendrocytes. J Neurosci. 2007;27(52):14375-14382. doi:10.1523/JNEUROSCI.4456-07.2007
33. Ono K, Takebayashi H, Ikeda K, et al. Regional- and temporal-dependent changes in the differentiation of Olig2 progenitors in the forebrain, and the impact on astrocyte development in the dorsal pallium. Dev Biol. 2008;320(2):456-468. doi:10.1016/j.ydbio.2008.06.001
34. Vierbuchen T, Ostermeier A, Pang ZP, Kokubu Y, Südhof TC, Wernig M. Direct conversion of fibroblasts to functional neurons by defined factors. Nature. 2010;463(7284):1035-1041. doi:10.1038/nature08797
35. Pang ZP, Yang N, Vierbuchen T, et al. Induction of human neuronal cells by defined transcription factors. Nature. 2011;476(7359):220-223. doi:10.1038/nature10202
36. Heinrich C, Blum R, Gascón S, et al. Directing astroglia from the cerebral cortex into subtype specific functional neurons. PLoS Biol. 2010;8(5):e1000373. doi:10.1371/journal.pbio.1000373
37. Guo Z, Zhang L, Wu Z, Chen Y, Wang F, Chen G. In vivo direct reprogramming of reactive glial cells into functional neurons after brain injury and in an Alzheimer’s disease model. Cell Stem Cell. 2014;14(2):188-202. doi:10.1016/j.stem.2013.12.001
38. Brulet R, Matsuda T, Zhang L, et al. NEUROD1 instructs neuronal conversion in non-reactive astrocytes. Stem Cell Reports. 2017;8(6):1506-1515. doi:10.1016/j.stemcr.2017.04.013
39. Liu Y, Miao Q, Yuan J, et al. Ascl1 converts dorsal midbrain astrocytes into functional neurons in vivo. J Neurosci. 2015;35(25):9336-9355. doi:10.1523/JNEUROSCI.3975-14.2015
40. Matsuda T, Irie T, Katsurabayashi S, et al. Pioneer factor NeuroD1 rearranges transcriptional and epigenetic profiles to execute microglia-neuron conversion. Neuron. 2019;101(3):472-485.e7. doi:10.1016/j.neuron.2018.12.010
41. Takouda J, Katada S, Imamura T, Sanosaka T, Nakashima K. SoxE group transcription factor Sox8 promotes astrocytic differentiation of neural stem/precursor cells downstream of Nfia. Pharmacol Res Perspect. 2021;9(6):e00749. doi:10.1002/prp2.749
42. Katada S, Takouda J, Nakagawa T, et al. Neural stem/precursor cells dynamically change their epigenetic landscape to differentially respond to BMP signaling for fate switching during brain development. Genes Dev. 2021;35(21-22):1431-1444. doi:10.1101/gad.348797.121
43. Monk D, Mackay DJG, Eggermann T, Maher ER, Riccio A. Genomic imprinting disorders: lessons on how genome, epigenome and environment interact. Nat Rev Genet. 2019;20(4):235-248. doi:10.1038/s41576-018-0092-0
44. Ohgane J, Wakayama T, Kogo Y, et al. DNA methylation variation in cloned mice. Genesis. 2001;30(2):45-50. doi:10.1002/gene.1031
45. Song X, Li F, Jiang Z, et al. Imprinting disorder in donor cells is detrimental to the development of cloned embryos in pigs. Oncotarget. 2017;8(42):72363-72374. doi:10.18632/oncotarget.20390
46. Imamura T, Ohgane J, Ito S, et al. CpG island of rat sphingosine kinase-1 gene: tissue-dependent DNA methylation status and multiple alternative first exons. Genomics. 2001;76(1-3):117-125. doi:10.1006/geno.2001.6607
47. Sanosaka T, Imamura T, Hamazaki N, et al. DNA Methylome Analysis Identifies Transcription Factor-Based Epigenomic Signatures of Multilineage Competence in Neural Stem/Progenitor Cells. Cell Rep. 2017;20(12):2992-3003. doi:10.1016/j.celrep.2017.08.086
48. Takizawa T, Nakashima K, Namihira M, et al. DNA methylation is a critical cell-intrinsic determinant of astrocyte differentiation in the fetal brain. Dev Cell. 2001;1(6):749-758. doi:10.1016/s1534-5807(01)00101-0
49. Namihira M, Kohyama J, Semi K, et al. Committed neuronal precursors confer astrocytic potential on residual neural precursor cells. Dev Cell. 2009;16(2):245-255. doi:10.1016/j.devcel.2008.12.014
50. Peterson CL, Laniel MA. Histones and histone modifications. Curr Biol. 2004;14(14):R546-51. doi:10.1016/j.cub.2004.07.007
51. Torres IO, Fujimori DG. Functional coupling between writers, erasers and readers of histone and DNA methylation. Curr Opin Struct Biol. 2015;35:68-75. doi:10.1016/j.sbi.2015.09.007
52. Li F, Wan M, Zhang B, et al. Bivalent histone modifications and development. Curr Stem Cell Res Ther. 2018;13(2):83-90. doi:10.2174/1574888X12666170123144743
53. Sarmento OF, Digilio LC, Wang Y, et al. Dynamic alterations of specific histone modifications during early murine development. J Cell Sci. 2004;117(Pt 19):4449-4459. doi:10.1242/jcs.01328
54. Zhang B, Zheng H, Huang B, et al. Allelic reprogramming of the histone modification H3K4me3 in early mammalian development. Nature. 2016;537(7621):553-557. doi:10.1038/nature19361
55. Eissenberg JC, Shilatifard A. Histone H3 lysine 4 (H3K4) methylation in development and differentiation. Dev Biol. 2010;339(2):240-249. doi:10.1016/j.ydbio.2009.08.017
56. Flanagan JF, Mi LZ, Chruszcz M, et al. Double chromodomains cooperate to recognize the methylated histone H3 tail. Nature. 2005;438(7071):1181-1185. doi:10.1038/nature04290
57. Sun G, Alzayady K, Stewart R, et al. Histone demethylase LSD1 regulates neural stem cell proliferation. Mol Cell Biol. 2010;30(8):1997-2005. doi:10.1128/MCB.01116-09
58. Kong SY, Kim W, Lee HR, Kim HJ. The histone demethylase KDM5A is required for the repression of astrocytogenesis and regulated by the translational machinery in neural progenitor cells. FASEB J. 2018;32(2):1108-1119. doi:10.1096/fj.201700780r
59. Golebiewska A, Atkinson SP, Lako M, Armstrong L. Epigenetic landscaping during hESC differentiation to neural cells. Stem Cells. 2009;27(6):1298-1308. doi:10.1002/stem.59
60. Lin H, Zhu X, Chen G, et al. KDM3A-mediated demethylation of histone H3 lysine 9 facilitates the chromatin binding of Neurog2 during neurogenesis. Development. 2017;144(20):3674-3685. doi:10.1242/dev.144113
61. Cao R, Wang L, Wang H, et al. Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science. 2002;298(5595):1039-1043. doi:10.1126/science.1076997
62. Lavarone E, Barbieri CM, Pasini D. Dissecting the role of H3K27 acetylation and methylation in PRC2 mediated control of cellular identity. Nat Commun. 2019;10(1):1679. doi:10.1038/s41467-019-09624-w
63. Min IM, Waterfall JJ, Core LJ, Munroe RJ, Schimenti J, Lis JT. Regulating RNA polymerase pausing and transcription elongation in embryonic stem cells. Genes Dev. 2011;25(7):742-754. doi:10.1101/gad.2005511
64. Laible G, Wolf A, Dorn R, et al. Mammalian homologues of the Polycomb-group gene Enhancer of zeste mediate gene silencing in Drosophila heterochromatin and at S. cerevisiae telomeres. EMBO J. 1997;16(11):3219-3232. doi:10.1093/emboj/16.11.3219
65. Hirabayashi Y, Suzki N, Tsuboi M, et al. Polycomb limits the neurogenic competence of neural precursor cells to promote astrogenic fate transition. Neuron. 2009;63(5):600-613. doi:10.1016/j.neuron.2009.08.021
66. He S, Wu Z, Tian Y, et al. Structure of nucleosome-bound human BAF complex. Science. 2020;367(6480):875-881. doi:10.1126/science.aaz9761
67. Sokpor G, Xie Y, Rosenbusch J, Tuoc T. Chromatin remodeling BAF (SWI/SNF) complexes in neural development and disorders. Front Mol Neurosci. 2017;10:243. doi:10.3389/fnmol.2017.00243
68. Tuoc TC, Boretius S, Sansom SN, et al. Chromatin regulation by BAF170 controls cerebral cortical size and thickness. Dev Cell. 2013;25(3):256-269. doi:10.1016/j.devcel.2013.04.005
69. Torchy MP, Hamiche A, Klaholz BP. Structure and function insights into the NuRD chromatin remodeling complex. Cell Mol Life Sci. 2015;72(13):2491-2507. doi:10.1007/s00018-015-1880-8
70. Nitarska J, Smith JG, Sherlock WT, et al. A Functional Switch of NuRD Chromatin Remodeling Complex Subunits Regulates Mouse Cortical Development. Cell Rep. 2016;17(6):1683-1698. doi:10.1016/j.celrep.2016.10.022
71. Sansom SN, Griffiths DS, Faedo A, et al. The level of the transcription factor Pax6 is essential for controlling the balance between neural stem cell self-renewal and neurogenesis. PLoS Genet. 2009;5(6):e1000511. doi:10.1371/journal.pgen.1000511
72. Graham V, Khudyakov J, Ellis P, Pevny L. SOX2 Functions to Maintain Neural Progenitor Identity. Neuron. 2003;39(5):749-765. doi:10.1016/S0896-6273(03)00497-5
73. Nakashima K, Takizawa T, Ochiai W, et al. BMP2-mediated alteration in the developmental pathway of fetal mouse brain cells from neurogenesis to astrocytogenesis. Proc Natl Acad Sci U S A. 2001;98(10):5868-5873. doi:10.1073/pnas.101109698
74. Nakashima K, Yanagisawa M, Arakawa H, et al. Synergistic signaling in fetal brain by STAT3-Smad1 complex bridged by p300. Science. 1999;284(5413):479-482. doi:10.1126/science.284.5413.479
75. Wang X, Tsai JW, Imai JH, Lian WN, Vallee RB, Shi SH. Asymmetric centrosome inheritance maintains neural progenitors in the neocortex. Nature. 2009;461(7266):947-955. doi:10.1038/nature08435
76. Wilsch-Bräuninger M, Huttner WB. Primary cilia and centrosomes in neocortex development. Front Neurosci. 2021;15:755867. doi:10.3389/fnins.2021.755867
77. Shao W, Yang J, He M, et al. Centrosome anchoring regulates progenitor properties and cortical formation. Nature. 2020;580(7801):106-112. doi:10.1038/s41586-020-2139-6
78. Failler M, Gee HY, Krug P, et al. Mutations of CEP83 cause infantile nephronophthisis and intellectual disability. Am J Hum Genet. 2014;94(6):905-914. doi:10.1016/j.ajhg.2014.05.002
79. O’Neill AC, Uzbas F, Antognolli G, et al. Spatial centrosome proteome of human neural cells uncovers disease-relevant heterogeneity. Science. 2022;376(6599):eabf9088. doi:10.1126/science.abf9088
80. Iaconis D, Monti M, Renda M, et al. The centrosomal OFD1 protein interacts with the translation machinery and regulates the synthesis of specific targets. Sci Rep. 2017;7(1). doi:10.1038/s41598-017-01156-x
81. Taverna E, Mora-Bermúdez F, Strzyz PJ, et al. Non-canonical features of the Golgi apparatus in bipolar epithelial neural stem cells. Sci Rep. 2016;6(1):21206. doi:10.1038/srep21206
82. Xie Z, Hur SK, Zhao L, Abrams CS, Bankaitis VA. A Golgi lipid signaling pathway controls apical Golgi distribution and cell polarity during neurogenesis. Dev Cell. 2018;44(6):725-740.e4. doi:10.1016/j.devcel.2018.02.025
83. Ge X, Gong H, Dumas K, et al. Missense-depleted regions in population exomes implicate ras superfamily nucleotide-binding protein alteration in patients with brain malformation. NPJ Genom Med. 2016;1(1). doi:10.1038/npjgenmed.2016.36
84. Settembre C, Fraldi A, Medina DL, Ballabio A. Signals from the lysosome: a control centre for cellular clearance and energy metabolism. Nat Rev Mol Cell Biol. 2013;14(5):283-296. doi:10.1038/nrm3565
85. Yuizumi N, Harada Y, Kuniya T, et al. Maintenance of neural stem-progenitor cells by the lysosomal biosynthesis regulators TFEB and TFE3 in the embryonic mouse telencephalon. Stem Cells. 2021;39(7):929-944. doi:10.1002/stem.3359
86. Leeman DS, Hebestreit K, Ruetz T, et al. Lysosome activation clears aggregates and enhances quiescent neural stem cell activation during aging. Science. 2018;359(6381):1277-1283. doi:10.1126/science.aag3048
87. Kobayashi T, Piao W, Takamura T, et al. Enhanced lysosomal degradation maintains the quiescent state of neural stem cells. Nat Commun. 2019;10(1):5446. doi:10.1038/s41467-019-13203-4
88. Cochard LM, Levros LC Jr, Joppé SE, Pratesi F, Aumont A, Fernandes KJL. Manipulation of EGFR-induced signaling for the recruitment of quiescent neural stem cells in the adult mouse forebrain. Front Neurosci. 2021;15:621076. doi:10.3389/fnins.2021.621076
89. Kann O, Kovács R. Mitochondria and neuronal activity. Am J Physiol Cell Physiol. 2007;292(2):C641-57. doi:10.1152/ajpcell.00222.2006
90. Youle RJ, van der Bliek AM. Mitochondrial fission, fusion, and stress. Science. 2012;337(6098):1062-1065. doi:10.1126/science.1219855
91. Iwata R, Casimir P, Vanderhaeghen P. Mitochondrial dynamics in postmitotic cells regulate neurogenesis. Science. 2020;369(6505):858-862. doi:10.1126/science.aba9760
92. Iwata R, Casimir P, Erkol E, et al. Mitochondria metabolism sets the species-specific tempo of neuronal development. Science. 2023;379(6632):eabn4705. doi:10.1126/science.abn4705
93. Namba T, Dóczi J, Pinson A, et al. Human-Specific ARHGAP11B Acts in Mitochondria to Expand Neocortical Progenitors by Glutaminolysis. Neuron. 2020;105(5):867-881.e9. doi:10.1016/j.neuron.2019.11.027
94. Journiac N, Gilabert-Juan J, Cipriani S, et al. Cell Metabolic Alterations due to Mcph1 Mutation in Microcephaly. Cell Rep. 2020;31(2):107506. doi:10.1016/j.celrep.2020.03.070
95. Zeisel A, Muñoz-Manchado AB, Codeluppi S, et al. Brain structure. Cell types in the mouse cortex and hippocampus revealed by single-cell RNA-seq. Science. 2015;347(6226):1138-1142. doi:10.1126/science.aaa1934
96. John Lin CC, Yu K, Hatcher A, et al. Identification of diverse astrocyte populations and their malignant analogs. Nat Neurosci. 2017;20(3):396-405. doi:10.1038/nn.4493
97. Lanjakornsiripan D, Pior BJ, Kawaguchi D, et al. Layer-specific morphological and molecular differences in neocortical astrocytes and their dependence on neuronal layers. Nat Commun. 2018;9(1). doi:10.1038/s41467-018-03940-3