抄録
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.
| 本文言語 | English |
|---|---|
| ページ（範囲） | 645-658.e5 |
| ジャーナル | Cell Reports |
| 巻 | 29 |
| 号 | 3 |
| DOI | |
| 出版ステータス | Published - 2019 10月 15 |
ASJC Scopus subject areas
- 生化学、遺伝学、分子生物学（全般）
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Evolutionary Gain of Dbx1 Expression Drives Subplate Identity in the Cerebral Cortex. / Arai, Yoko; Cwetsch, Andrzej W.; Coppola, Eva その他.
In: Cell Reports, Vol. 29, No. 3, 15.10.2019, p. 645-658.e5.研究成果: Article › 査読
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TY - JOUR
T1 - Evolutionary Gain of Dbx1 Expression Drives Subplate Identity in the Cerebral Cortex
AU - Arai, Yoko
AU - Cwetsch, Andrzej W.
AU - Coppola, Eva
AU - Cipriani, Sara
AU - Nishihara, Hidenori
AU - Kanki, Hiroaki
AU - Saillour, Yoann
AU - Freret-Hodara, Betty
AU - Dutriaux, Annie
AU - Okada, Norihiro
AU - Okano, Hideyuki
AU - Dehay, Colette
AU - Nardelli, Jeannette
AU - Gressens, Pierre
AU - Shimogori, Tomomi
AU - D'Onofrio, Giuseppe
AU - Pierani, Alessandra
N1 - Funding Information: We acknowledge the ImagoSeine facility, a member of the France BioImaging infrastructure supported by the Agence Nationale de la Recherche (ANR-10-INSB-04, “Investments for the future”), for help with confocal microscopy; Animalliance for technical assistance and animal care; N. Klaus, S. Goebbels, S.M. Barnat, and S. Humbert for providing the Nex-cre mouse line; S. Karaz, M. Courgeon, and F. Causeret for the pCAGGS-Dbx1-ires-EGFP plasmid and sequence; M. Moreau and F. Causeret for interrogating public databases; and J. Fei for providing pCAGGS-mCherry and pCAGGS-loxP-stop-loxP plasmids. We thank F. Matsuzaki, T. Suetsugu, and A. Shitamukai for training in exo utero electroporation; E. Taverna, J. Pulvers, M. Barber, T. Nomura, and J. Sap for critical reading of the manuscript; members of Pierani's laboratory for discussion; and L. Vigier for mouse maintenance. Y.A. was supported by the ARC (Association pour la Recherche sur le Cancer), FRM (Fondation pour la Recherche Médicale), and JSPS (Japan Society for the Promotion of Science); A.W.C. by the FRM. A.P. is a CNRS (Centre National de la Recherche Scientifique) Investigator and the Team member of the École des Neurosciences de Paris Ile-de-France (ENP). This work was supported by grants from the Agence Nationale de la Recherche (ANR-2011-BSV4-023-01 and ANR-15-CE16-0003-01), FRM (Equipe FRM DEQ20130326521), Fondation ARC pour la Recherche sur le Cancer (ARC, Project ARC SFI20111203674), Ville de Paris (2006 ASES 102), and Fédération pour la Recherche sur le Cerveau (FRC) to A.P.; and state funding from the Agence Nationale de la Recherche under “Investissements d'avenir” program (ANR-10-IAHU-01) to the Imagine Institute and Brain Mapping by Integrated Neurotechnologies for Disease Studies (Brain/MINDS) from the Ministry of Education, Culture, Sports, Science, and Technology of Japan (MEXT) to H.O. Y.A. and A.P. conceived the study, analyzed the data, and co-wrote the manuscript. Y.A. performed most of the experiments. A.W.C. performed electroporations and immunostaining in mouse and human, analyzed the data, and performed most of the revisions. E.C. participated in the analysis of transgenic lines and in the revisions. S.C. and Y.S. performed some human immunostaining. H.N. generated marmoset 10 kb transgenic mice. H.K. produced 5 kb and 10 kb marmoset DNA constructs. B.F.-H. performed mouse Dbx1 in situ hybridization and Nurr1/Ctip2 immunostaining. A.D. provided mouse colony maintenance. N.O. provided support for the generation of marmoset 10 kb transgenic mice. H.O. and T.S. provided marmoset material, T.S. also expertise in in utero electroporation at E11.5. P.G. and J.N. provided an access to donated human fetal tissue. C.D. provided macaque tissue. G.D. performed bioinformatics analyses. A.P. supervised the project. All authors discussed and edited the manuscript. H.O. is a paid member of the scientific advisory board of SanBio. The remaining authors declare no competing interests. Funding Information: We acknowledge the ImagoSeine facility, a member of the France BioImaging infrastructure supported by the Agence Nationale de la Recherche ( ANR-10-INSB-04 , “Investments for the future”), for help with confocal microscopy; Animalliance for technical assistance and animal care; N. Klaus, S. Goebbels, S.M. Barnat, and S. Humbert for providing the Nex-cre mouse line; S. Karaz, M. Courgeon, and F. Causeret for the pCAGGS-Dbx1-ires-EGFP plasmid and sequence; M. Moreau and F. Causeret for interrogating public databases; and J. Fei for providing pCAGGS-mCherry and pCAGGS-loxP-stop-loxP plasmids. We thank F. Matsuzaki, T. Suetsugu, and A. Shitamukai for training in exo utero electroporation; E. Taverna, J. Pulvers, M. Barber, T. Nomura, and J. Sap for critical reading of the manuscript; members of Pierani’s laboratory for discussion; and L. Vigier for mouse maintenance. Y.A. was supported by the ARC ( Association pour la Recherche sur le Cancer ), FRM ( Fondation pour la Recherche Médicale ), and JSPS ( Japan Society for the Promotion of Science ); A.W.C. by the FRM. A.P. is a CNRS ( Centre National de la Recherche Scientifique ) Investigator and the Team member of the École des Neurosciences de Paris Ile-de-France (ENP). This work was supported by grants from the Agence Nationale de la Recherche ( ANR-2011-BSV4-023-01 and ANR-15-CE16-0003-01 ), FRM (Equipe FRM DEQ20130326521 ), Fondation ARC pour la Recherche sur le Cancer ( ARC , Project ARC SFI20111203674 ), Ville de Paris (2006 ASES 102 ), and Fédération pour la Recherche sur le Cerveau (FRC) to A.P.; and state funding from the Agence Nationale de la Recherche under “Investissements d’avenir” program ( ANR-10-IAHU-01 ) to the Imagine Institute and Brain Mapping by Integrated Neurotechnologies for Disease Studies (Brain/MINDS) from the Ministry of Education, Culture, Sports, Science, and Technology of Japan (MEXT) to H.O. Publisher Copyright: © 2019 The Author(s)
PY - 2019/10/15
Y1 - 2019/10/15
N2 - 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.
AB - 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.
KW - Cajal-Retzius neurons
KW - Dbx1
KW - cortical evolution
KW - postmitotic
KW - primate-specific cis-regulatory elements
KW - subplate neurons
UR - http://www.scopus.com/inward/record.url?scp=85073101755&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=85073101755&partnerID=8YFLogxK
U2 - 10.1016/j.celrep.2019.09.007
DO - 10.1016/j.celrep.2019.09.007
M3 - Article
C2 - 31618633
AN - SCOPUS:85073101755
SN - 2211-1247
VL - 29
SP - 645-658.e5
JO - Cell Reports
JF - Cell Reports
IS - 3
ER -