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Temporally-Divergent Regulatory Mechanisms Govern Neuronal Development and Diversification in the Neocortex

View ORCID ProfileWen Yuan, Sai Ma, View ORCID ProfileJuliana R. Brown, Kwanho Kim, Vanessa Murek, Lucia Trastulla, Alexander Meissner, Simona Lodato, Ashwin Shetty, View ORCID ProfileJoshua Z. Levin, Jason D. Buenrostro, Michael J. Ziller, View ORCID ProfilePaola Arlotta
doi: https://doi.org/10.1101/2020.08.23.263434
Wen Yuan
1Department of Stem Cell and Regenerative Biology, Harvard University, Cambridge, MA 02138, USA
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  • ORCID record for Wen Yuan
Sai Ma
1Department of Stem Cell and Regenerative Biology, Harvard University, Cambridge, MA 02138, USA
2Klarman Cell Observatory, Broad Institute of MIT and Harvard, Cambridge, MA, 02142, USA
3Department of Biology and Koch Institute, Massachusetts Institute of Technology, Cambridge, MA, 02142 USA
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Juliana R. Brown
1Department of Stem Cell and Regenerative Biology, Harvard University, Cambridge, MA 02138, USA
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  • ORCID record for Juliana R. Brown
Kwanho Kim
1Department of Stem Cell and Regenerative Biology, Harvard University, Cambridge, MA 02138, USA
2Klarman Cell Observatory, Broad Institute of MIT and Harvard, Cambridge, MA, 02142, USA
4Stanley Center for Psychiatric Research, Broad Institute of Harvard and MIT, Cambridge, MA 02142, USA
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Vanessa Murek
5Max Planck Institute of Psychiatry, 80804 Munich, Germany
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Lucia Trastulla
5Max Planck Institute of Psychiatry, 80804 Munich, Germany
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Alexander Meissner
1Department of Stem Cell and Regenerative Biology, Harvard University, Cambridge, MA 02138, USA
6Department of Genome Regulation, Max Planck Institute for Molecular Genetics, 14195 Berlin, Germany
7Broad Institute of MIT and Harvard, Cambridge, MA 02142, USA
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Simona Lodato
8Department of Biomedical Sciences and Humanitas Clinical and Research Center – IRCCS, Humanitas University, Milan, Italy
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Ashwin Shetty
1Department of Stem Cell and Regenerative Biology, Harvard University, Cambridge, MA 02138, USA
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Joshua Z. Levin
2Klarman Cell Observatory, Broad Institute of MIT and Harvard, Cambridge, MA, 02142, USA
4Stanley Center for Psychiatric Research, Broad Institute of Harvard and MIT, Cambridge, MA 02142, USA
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  • ORCID record for Joshua Z. Levin
Jason D. Buenrostro
1Department of Stem Cell and Regenerative Biology, Harvard University, Cambridge, MA 02138, USA
7Broad Institute of MIT and Harvard, Cambridge, MA 02142, USA
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Michael J. Ziller
5Max Planck Institute of Psychiatry, 80804 Munich, Germany
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  • For correspondence: paola_arlotta@harvard.edu michael_ziller@psych.mpg.de
Paola Arlotta
1Department of Stem Cell and Regenerative Biology, Harvard University, Cambridge, MA 02138, USA
4Stanley Center for Psychiatric Research, Broad Institute of Harvard and MIT, Cambridge, MA 02142, USA
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  • ORCID record for Paola Arlotta
  • For correspondence: paola_arlotta@harvard.edu michael_ziller@psych.mpg.de
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Abstract

Mammalian neocortical neurons span one of the most diverse cell type spectra of any tissue. The regulatory strategies that neurons use during progressive development and maturation remain unclear. We present an integrated single-cell epigenomic and transcriptional analysis of individual classes of neurons from both mouse and marmoset neocortex, sampled during both early postmitotic stages of identity acquisition and later stages of neuronal plasticity and circuit integration. We find that in both species, the regulatory strategies controlling these early and late stages diverge: early postmitotic neurons use molecular regulatory programs with broader tissue distribution and greater evolutionary conservation, while programs active during later neuronal maturation implement more brain- and neuron-specific mechanisms showing greater evolutionary divergence. The data uncovers a temporally-regulated shift in regulatory choices, likely reflecting unique evolutionary constraints on distinct events of neuronal development in the neocortex.

Competing Interest Statement

The authors have declared no competing interest.

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Posted August 24, 2020.
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Temporally-Divergent Regulatory Mechanisms Govern Neuronal Development and Diversification in the Neocortex
Wen Yuan, Sai Ma, Juliana R. Brown, Kwanho Kim, Vanessa Murek, Lucia Trastulla, Alexander Meissner, Simona Lodato, Ashwin Shetty, Joshua Z. Levin, Jason D. Buenrostro, Michael J. Ziller, Paola Arlotta
bioRxiv 2020.08.23.263434; doi: https://doi.org/10.1101/2020.08.23.263434
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Temporally-Divergent Regulatory Mechanisms Govern Neuronal Development and Diversification in the Neocortex
Wen Yuan, Sai Ma, Juliana R. Brown, Kwanho Kim, Vanessa Murek, Lucia Trastulla, Alexander Meissner, Simona Lodato, Ashwin Shetty, Joshua Z. Levin, Jason D. Buenrostro, Michael J. Ziller, Paola Arlotta
bioRxiv 2020.08.23.263434; doi: https://doi.org/10.1101/2020.08.23.263434

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