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Cell Rep. 2019 Oct 15;29(3):645-658.e5. doi: 10.1016/j.celrep.2019.09.007.

Evolutionary Gain of Dbx1 Expression Drives Subplate Identity in the Cerebral Cortex.

Author information

1
Institut Jacques Monod, CNRS UMR 7592, Université de Paris, 75205 Paris Cedex, France.
2
Imagine Institute of Genetic Diseases, Université de Paris, Paris 75015, France; Institute of Psychiatry and Neuroscience of Paris, INSERM U1266, Université de Paris, Paris 75014, France.
3
Imagine Institute of Genetic Diseases, Université de Paris, Paris 75015, France; Institute of Psychiatry and Neuroscience of Paris, INSERM U1266, Université de Paris, Paris 75014, France; Institut Jacques Monod, CNRS UMR 7592, Université de Paris, 75205 Paris Cedex, France.
4
Université de Paris, NeuroDiderot, INSERM, Paris 75019, France.
5
Department of Life Science and Technology, Tokyo Institute of Technology, Yokohama 226-8501, Japan.
6
Department of Physiology, Keio University School of Medicine, Tokyo 160-8582, Japan.
7
Foundation for Advancement of International Science, Tsukuba 305-0821, Japan.
8
Department of Physiology, Keio University School of Medicine, Tokyo 160-8582, Japan; Laboratory for Marmoset Neural Architecture, RIKEN Center for Brain Science, Wako, Saitama 351-0198, Japan.
9
Université Lyon, Université Claude Bernard Lyon 1, INSERM, Stem Cell and Brain Research Institute U1208, 69500 Bron, France.
10
Molecular Mechanisms of Brain Development, RIKEN Center for Brain Science, Wako, Saitama 351-0198, Japan.
11
Department BEOM, Stazione Zoologica A. Dohrn, Napoli 80121, Italy.
12
Imagine Institute of Genetic Diseases, Université de Paris, Paris 75015, France; Institute of Psychiatry and Neuroscience of Paris, INSERM U1266, Université de Paris, Paris 75014, France; Institut Jacques Monod, CNRS UMR 7592, Université de Paris, 75205 Paris Cedex, France. Electronic address: alessandra.pierani@inserm.fr.

Abstract

Changes in transcriptional regulation through cis-regulatory elements are thought to drive brain evolution. However, how this impacts the identity of primate cortical neurons is still unresolved. Here, we show that primate-specific cis-regulatory sequences upstream of the Dbx1 gene promote human-like expression in the mouse embryonic cerebral cortex, and this imparts cell identity. Indeed, while Dbx1 is expressed in highly restricted cortical progenitors in the mouse ventral pallium, it is maintained in neurons in primates. Phenocopy of the primate-like Dbx1 expression in mouse cortical progenitors induces ectopic Cajal-Retzius and subplate (SP) neurons, which are transient populations playing crucial roles in cortical development. A conditional expression solely in neurons uncouples mitotic and postmitotic activities of Dbx1 and exclusively promotes a SP-like fate. Our results highlight how transcriptional changes of a single fate determinant in postmitotic cells may contribute to the expansion of neuronal diversity during cortical evolution.

KEYWORDS:

Cajal-Retzius neurons; Dbx1; cortical evolution; postmitotic; primate-specific cis-regulatory elements; subplate neurons

PMID:
31618633
DOI:
10.1016/j.celrep.2019.09.007
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