A Common Embryonic Origin of Stem Cells Drives Developmental and Adult Neurogenesis

Daniel A. Berg; Yijing Su; Dennisse Jimenez-Cyrus; Aneek Patel; Nancy Huang; David Morizet; Stephanie Lee; Reeti Shah; Francisca Rojas Ringeling; Rajan Jain; Jonathan A. Epstein; Qing Feng Wu; Stefan Canzar; Guo Li Ming; Hongjun Song; Allison M. Bond

doi:10.1016/j.cell.2019.02.010

A Common Embryonic Origin of Stem Cells Drives Developmental and Adult Neurogenesis

Daniel A. Berg, Yijing Su, Dennisse Jimenez-Cyrus, Aneek Patel, Nancy Huang, David Morizet, Stephanie Lee, Reeti Shah, Francisca Rojas Ringeling, Rajan Jain, Jonathan A. Epstein, Qing Feng Wu, Stefan Canzar, Guo Li Ming^*, Hongjun Song, Allison M. Bond

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

142 Citations (Scopus)

Abstract

New neurons arise from quiescent adult neural progenitors throughout life in specific regions of the mammalian brain. Little is known about the embryonic origin and establishment of adult neural progenitors. Here, we show that Hopx+ precursors in the mouse dentate neuroepithelium at embryonic day 11.5 give rise to proliferative Hopx+ neural progenitors in the primitive dentate region, and they, in turn, generate granule neurons, but not other neurons, throughout development and then transition into Hopx+ quiescent radial glial-like neural progenitors during an early postnatal period. RNA-seq and ATAC-seq analyses of Hopx+ embryonic, early postnatal, and adult dentate neural progenitors further reveal common molecular and epigenetic signatures and developmental dynamics. Together, our findings support a “continuous” model wherein a common neural progenitor population exclusively contributes to dentate neurogenesis throughout development and adulthood. Adult dentate neurogenesis may therefore represent a lifelong extension of development that maintains heightened plasticity in the mammalian hippocampus.

Original language	English
Pages (from-to)	654-668.e15
Number of pages	31
Journal	Cell
Volume	177
Issue number	3
Early online date	28 Mar 2019
DOIs	https://doi.org/10.1016/j.cell.2019.02.010
Publication status	Published - 18 Apr 2019
Externally published	Yes

Bibliographical note

Data and Software Availability: The access number for the RNA-seq and ATAC-seq data reported in this study is NCBI GEO: GSE125315.

Acknowledgments: We thank K.M. Christian for comments, members of Ming and Song laboratories for discussion, D. Johnson and B. Temsamrit for technical support, J. Schnoll for lab coordination, and V. Yoon and Y. Huang for providing Apoe-GFP transgenic mouse tissue.
This work was supported by grants from the NIH (P01NS097206 and R37NS047344 to H.S., R35NS097370 and R01MH105128 to G.-L.M., R35HL140018 to J.A.E., and DP2HL147123 to R.J.) and by the Dr. Miriam and Sheldon G. Adelson Medical Research Foundation (to G.-L.M.). R.J. was supported by the Burroughs Wellcome Foundation. D.A.B. was supported by an EMBO postdoctoral fellowship and a grant from the Swedish Research Council.

Author Contributions: D.A.B and A.M.B co-led the project and contributed equally to this work. Y.S., D.J.-C., R.S., A.P., N.H., D.M., S.L., F.R.R., Q.-F.W., and S.C. contributed to additional data collection and analyses. R.J. and J.A.E. contributed reagents. D.A.B., A.M.B., G.-L.M., and H.S. wrote the paper.

Keywords

brain development
chromatin landscape profiling
dentate gyrus
gene expression profiling
hippocampus
Hopx
lineage tracing
neural stem cells
neurogenesis

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Cite this

@article{63c15d18d4854deab3ab022e39fb2d05,

title = "A Common Embryonic Origin of Stem Cells Drives Developmental and Adult Neurogenesis",

abstract = "New neurons arise from quiescent adult neural progenitors throughout life in specific regions of the mammalian brain. Little is known about the embryonic origin and establishment of adult neural progenitors. Here, we show that Hopx+ precursors in the mouse dentate neuroepithelium at embryonic day 11.5 give rise to proliferative Hopx+ neural progenitors in the primitive dentate region, and they, in turn, generate granule neurons, but not other neurons, throughout development and then transition into Hopx+ quiescent radial glial-like neural progenitors during an early postnatal period. RNA-seq and ATAC-seq analyses of Hopx+ embryonic, early postnatal, and adult dentate neural progenitors further reveal common molecular and epigenetic signatures and developmental dynamics. Together, our findings support a “continuous” model wherein a common neural progenitor population exclusively contributes to dentate neurogenesis throughout development and adulthood. Adult dentate neurogenesis may therefore represent a lifelong extension of development that maintains heightened plasticity in the mammalian hippocampus.",

keywords = "brain development, chromatin landscape profiling, dentate gyrus, gene expression profiling, hippocampus, Hopx, lineage tracing, neural stem cells, neurogenesis",

author = "Berg, {Daniel A.} and Yijing Su and Dennisse Jimenez-Cyrus and Aneek Patel and Nancy Huang and David Morizet and Stephanie Lee and Reeti Shah and Ringeling, {Francisca Rojas} and Rajan Jain and Epstein, {Jonathan A.} and Wu, {Qing Feng} and Stefan Canzar and Ming, {Guo Li} and Hongjun Song and Bond, {Allison M.}",

note = "Data and Software Availability: The access number for the RNA-seq and ATAC-seq data reported in this study is NCBI GEO: GSE125315. Acknowledgments: We thank K.M. Christian for comments, members of Ming and Song laboratories for discussion, D. Johnson and B. Temsamrit for technical support, J. Schnoll for lab coordination, and V. Yoon and Y. Huang for providing Apoe-GFP transgenic mouse tissue. This work was supported by grants from the NIH (P01NS097206 and R37NS047344 to H.S., R35NS097370 and R01MH105128 to G.-L.M., R35HL140018 to J.A.E., and DP2HL147123 to R.J.) and by the Dr. Miriam and Sheldon G. Adelson Medical Research Foundation (to G.-L.M.). R.J. was supported by the Burroughs Wellcome Foundation. D.A.B. was supported by an EMBO postdoctoral fellowship and a grant from the Swedish Research Council. Author Contributions: D.A.B and A.M.B co-led the project and contributed equally to this work. Y.S., D.J.-C., R.S., A.P., N.H., D.M., S.L., F.R.R., Q.-F.W., and S.C. contributed to additional data collection and analyses. R.J. and J.A.E. contributed reagents. D.A.B., A.M.B., G.-L.M., and H.S. wrote the paper.",

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AU - Berg, Daniel A.

AU - Su, Yijing

AU - Jimenez-Cyrus, Dennisse

AU - Patel, Aneek

AU - Huang, Nancy

AU - Morizet, David

AU - Lee, Stephanie

AU - Shah, Reeti

AU - Ringeling, Francisca Rojas

AU - Jain, Rajan

AU - Epstein, Jonathan A.

AU - Wu, Qing Feng

AU - Canzar, Stefan

AU - Ming, Guo Li

AU - Song, Hongjun

AU - Bond, Allison M.

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N2 - New neurons arise from quiescent adult neural progenitors throughout life in specific regions of the mammalian brain. Little is known about the embryonic origin and establishment of adult neural progenitors. Here, we show that Hopx+ precursors in the mouse dentate neuroepithelium at embryonic day 11.5 give rise to proliferative Hopx+ neural progenitors in the primitive dentate region, and they, in turn, generate granule neurons, but not other neurons, throughout development and then transition into Hopx+ quiescent radial glial-like neural progenitors during an early postnatal period. RNA-seq and ATAC-seq analyses of Hopx+ embryonic, early postnatal, and adult dentate neural progenitors further reveal common molecular and epigenetic signatures and developmental dynamics. Together, our findings support a “continuous” model wherein a common neural progenitor population exclusively contributes to dentate neurogenesis throughout development and adulthood. Adult dentate neurogenesis may therefore represent a lifelong extension of development that maintains heightened plasticity in the mammalian hippocampus.

AB - New neurons arise from quiescent adult neural progenitors throughout life in specific regions of the mammalian brain. Little is known about the embryonic origin and establishment of adult neural progenitors. Here, we show that Hopx+ precursors in the mouse dentate neuroepithelium at embryonic day 11.5 give rise to proliferative Hopx+ neural progenitors in the primitive dentate region, and they, in turn, generate granule neurons, but not other neurons, throughout development and then transition into Hopx+ quiescent radial glial-like neural progenitors during an early postnatal period. RNA-seq and ATAC-seq analyses of Hopx+ embryonic, early postnatal, and adult dentate neural progenitors further reveal common molecular and epigenetic signatures and developmental dynamics. Together, our findings support a “continuous” model wherein a common neural progenitor population exclusively contributes to dentate neurogenesis throughout development and adulthood. Adult dentate neurogenesis may therefore represent a lifelong extension of development that maintains heightened plasticity in the mammalian hippocampus.

KW - brain development

KW - chromatin landscape profiling

KW - dentate gyrus

KW - gene expression profiling

KW - hippocampus

KW - Hopx

KW - lineage tracing

KW - neural stem cells

KW - neurogenesis

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DO - 10.1016/j.cell.2019.02.010

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JF - Cell

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ER -

A Common Embryonic Origin of Stem Cells Drives Developmental and Adult Neurogenesis

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Daniel Berg

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A Common Embryonic Origin of Stem Cells Drives Developmental and Adult Neurogenesis

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Daniel Berg

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