Heterogeneity of glial progenitor cells during the neurogenesis-to-gliogenesis switch in the developing human cerebral cortex

Fu, Yuanyuan; Yang, Ming; Yu, Hong-Min; Wang, Yicheng; Wu, Xinglong; Yong, Jun; Mao, Yunuo; Cui, Yueli; Fan, Xiaoying; Wen, Lu; Qiao, Jie; Tang, Fuchou

doi:10.1016/j.celrep.2021.108788

Cited by 69 publications

(75 citation statements)

References 65 publications

(93 reference statements)

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“…We re-analyzed published single-cell RNA-Seq datasets, including 3,355 EGFR ? cells from human frontal cortex at GW21-GW26 [35] and 33,976 cells from human cortex at GW17-GW18 [36], in the context of our immunohistochemistry results, and provide evidence that human cortical EGFR ? tRGs generate bMIPCs that coexpress EGFR, ASCL1, OLIG2 and OLIG1.…”

Section: Introductionsupporting

confidence: 58%

“…1F-H); these genes are typical markers for OPCs. This might be the reason why previous studies termed bMIPC as ''Pre-OPCs'' or ''Pri-OPCs'' (IPC types preceding committed OPC) [35,[46][47][48][49]. Slingshot analysis [50], predicting a developmental trajectory and pseudo-timeline progression of IPCs, suggest that bMIPCs give rise to OPCs (ASCL1 ?…”

Section: Scrna-seq Analysis Reveals Human Cortical Trg Lineage At Gw21-gw26mentioning

confidence: 99%

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Developmental Origins of Human Cortical Oligodendrocytes and Astrocytes

Yang

Liu

et al. 2021

Neurosci. Bull.

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Human cortical radial glial cells are primary neural stem cells that give rise to cortical glutaminergic projection pyramidal neurons, glial cells (oligodendrocytes and astrocytes) and olfactory bulb GABAergic interneurons. One of prominent features of the human cortex is enriched with glial cells, but there are major gaps in understanding how these glial cells are generated. Herein, by integrating analysis of published human cortical single-cell RNA-Seq datasets with our immunohistochemistical analyses, we show that around gestational week 18, EGFR-expressing human cortical truncated radial glial cells (tRGs) give rise to basal multipotent intermediate progenitors (bMIPCs) that express EGFR, ASCL1, OLIG2 and OLIG1. These bMIPCs undergo several rounds of mitosis and generate cortical oligodendrocytes, astrocytes and olfactory bulb interneurons. We also characterized molecular features of the cortical tRG. Integration of our findings suggests a general picture of the lineage progression of cortical radial glial cells, a fundamental process of the developing human cerebral cortex.

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Section: Introductionsupporting

confidence: 58%

Section: Scrna-seq Analysis Reveals Human Cortical Trg Lineage At Gw21-gw26mentioning

confidence: 99%

Developmental Origins of Human Cortical Oligodendrocytes and Astrocytes

Yang

Liu

et al. 2021

Neurosci. Bull.

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“…We have reported that astrocyte progenitors assemble in the ventral half of the spinal cord at E15.5 ( Karus et al, 2011 ). Significant heterogeneity of astrocytes has been concluded from transcriptome studies and bioinformatic analysis ( John Lin et al, 2017 ; Fu et al, 2021 ). However, tools to enrich and separately study these asserted subpopulations in the spinal cord still remain to be developed.…”

Section: Discussionmentioning

confidence: 99%

Sulfation of Glycosaminoglycans Modulates the Cell Cycle of Embryonic Mouse Spinal Cord Neural Stem Cells

Schaberg

Theocharidis

May

et al. 2021

Front. Cell Dev. Biol.

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In the developing spinal cord neural stem and progenitor cells (NSPCs) secrete and are surrounded by extracellular matrix (ECM) molecules that influence their lineage decisions. The chondroitin sulfate proteoglycan (CSPG) DSD-1-PG is an isoform of receptor protein tyrosine phosphatase-beta/zeta (RPTPβ/ζ), a trans-membrane receptor expressed by NSPCs. The chondroitin sulfate glycosaminoglycan chains are sulfated at distinct positions by sulfotransferases, thereby generating the distinct DSD-1-epitope that is recognized by the monoclonal antibody (mAb) 473HD. We detected the epitope, the critical enzymes and RPTPβ/ζ in the developing spinal cord. To obtain insight into potential biological functions, we exposed spinal cord NSPCs to sodium chlorate. The reagent suppresses the sulfation of glycosaminoglycans, thereby erasing any sulfation code expressed by the glycosaminoglycan polymers. When NSPCs were treated with chlorate and cultivated in the presence of FGF2, their proliferation rate was clearly reduced, while NSPCs exposed to EGF were less affected. Time-lapse video microscopy and subsequent single-cell tracking revealed that pedigrees of NSPCs cultivated with FGF2 were strongly disrupted when sulfation was suppressed. Furthermore, the NSPCs displayed a protracted cell cycle length. We conclude that the inhibition of sulfation with sodium chlorate interferes with the FGF2-dependent cell cycle progression in spinal cord NSPCs.

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“…Activated EGFR recruits adapter proteins which in turn activates complex downstream signaling cascades [35]. Emerging evidence indicates that EGFR signaling plays an important role in oligodendrogenesis [27,[36][37][38][39][40][41]. While EGFR knock-out appeared to reduce the density of OPCs and mature oligodendrocytes in corpus callosum [36], enhancing EGFR signaling by intraventricular infusion of EGF induced type B cells to differentiate into oligodendrocytes [38].…”

Section: Discussionmentioning

confidence: 99%

EGF signaling promotes the lineage conversion of astrocytes into oligodendroglias

Liu

Xie

et al. 2021

Preprint

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Background The conversion of astrocytes activated by nerve injuries to oligodendrocytes is not only beneficial to axonal remyelination, but also helpful for reversal of glial scar. Recent studies have shown that Sox10 transcription factor can achieve this transdifferentiation process in collaboration with some unknown factors in the pathological microenvironment. The extracellular factors underlying the cell fate switching are not known. Methods Astrocytes were obtained from mouse cortical dissociation culture and purified by differential adherent properties. The lineage conversion of astrocytes into oligodendrocyte lineage cells was carried out by Sox10-expressing virus infection both in vitro and in vivo, meanwhile, epidermal growth factor (EGF) and epidermal growth factor receptor (EGFR) inhibitor Gefitinib were adopted to investigate the function of EGF signaling in this fate transition process. Pharmacological inhibition analyses were performed to examine the pathway connecting the EGF with the expression of oligodendrogenic genes and cell fate transdifferentiation. Results EGF treatment facilitated the Sox10-induced transformation of astrocytes to O4+ induced oligodendrocyte precursor cells (iOPCs) in vitro. The transdifferentiation of astrocytes to iOPCs went through two distinct but interconnected processes: (1) dedifferentiation of astrocytes to astrocyte precursor cells (APCs); (2) transformation of APCs to iOPCs, EGF signaling was involved in both processes. And EGF triggered astrocytes to express oligodendrogenic genes Olig1 and Olig2 by activating extracellular signal-regulated kinase 1 and 2 (Erk1/2) pathway. In addition, we discovered that EGF can enhance astrocyte transdifferentiation in injured spinal cord tissues. Conclusions These findings provide strong evidence that EGF facilitates the transdifferentiation of astrocytes to oligodendroglias, and suggest that targeting the EGF-EGFR-Erk1/2 signaling axis may represent a novel therapeutic strategy for myelin repair in injured central nervous system (CNS) tissues.

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Heterogeneity of glial progenitor cells during the neurogenesis-to-gliogenesis switch in the developing human cerebral cortex

Cited by 69 publications

References 65 publications

Developmental Origins of Human Cortical Oligodendrocytes and Astrocytes

Developmental Origins of Human Cortical Oligodendrocytes and Astrocytes

Sulfation of Glycosaminoglycans Modulates the Cell Cycle of Embryonic Mouse Spinal Cord Neural Stem Cells

EGF signaling promotes the lineage conversion of astrocytes into oligodendroglias

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