Temporal and sequential transcriptional dynamics define lineage shifts in corticogenesis.


Journal

The EMBO journal
ISSN: 1460-2075
Titre abrégé: EMBO J
Pays: England
ID NLM: 8208664

Informations de publication

Date de publication:
15 12 2022
Historique:
revised: 09 09 2022
received: 10 03 2022
accepted: 26 09 2022
pubmed: 9 11 2022
medline: 17 12 2022
entrez: 8 11 2022
Statut: ppublish

Résumé

The cerebral cortex contains billions of neurons, and their disorganization or misspecification leads to neurodevelopmental disorders. Understanding how the plethora of projection neuron subtypes are generated by cortical neural stem cells (NSCs) is a major challenge. Here, we focused on elucidating the transcriptional landscape of murine embryonic NSCs, basal progenitors (BPs), and newborn neurons (NBNs) throughout cortical development. We uncover dynamic shifts in transcriptional space over time and heterogeneity within each progenitor population. We identified signature hallmarks of NSC, BP, and NBN clusters and predict active transcriptional nodes and networks that contribute to neural fate specification. We find that the expression of receptors, ligands, and downstream pathway components is highly dynamic over time and throughout the lineage implying differential responsiveness to signals. Thus, we provide an expansive compendium of gene expression during cortical development that will be an invaluable resource for studying neural developmental processes and neurodevelopmental disorders.

Identifiants

pubmed: 36345783
doi: 10.15252/embj.2022111132
pmc: PMC9753470
doi:

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e111132

Subventions

Organisme : NINDS NIH HHS
ID : R01 NS102228
Pays : United States

Informations de copyright

© 2022 The Authors. Published under the terms of the CC BY NC ND 4.0 license.

Références

J Neurosci Res. 1998 Jan 15;51(2):139-46
pubmed: 9469567
Brain. 2013 Apr;136(Pt 4):1155-60
pubmed: 23518707
Cereb Cortex. 2015 Oct;25(10):3758-78
pubmed: 25331604
Nat Rev Neurosci. 2007 Jun;8(6):427-37
pubmed: 17514196
Nat Biotechnol. 2016 Aug 9;34(8):888
pubmed: 27504780
Proc Natl Acad Sci U S A. 2004 Mar 2;101(9):3196-201
pubmed: 14963232
Trends Genet. 2004 Nov;20(11):563-9
pubmed: 15475116
J Mol Neurosci. 2016 May;59(1):1-17
pubmed: 26809286
Sci Adv. 2019 Apr 03;5(4):eaav7959
pubmed: 30949582
Science. 2003 Jul 18;301(5631):328-30
pubmed: 12869750
Mol Cell Neurosci. 1996;8(4):221-41
pubmed: 9000438
Stem Cells Dev. 2015 Sep 15;24(18):2114-26
pubmed: 26083238
Neuron. 2013 Dec 4;80(5):1103-5
pubmed: 24314721
Nat Commun. 2012 Feb 14;3:670
pubmed: 22334073
Nucleic Acids Res. 2017 Jan 4;45(D1):D183-D189
pubmed: 27899595
Methods Mol Biol. 2009;482:143-58
pubmed: 19089354
Nat Rev Mol Cell Biol. 2005 Oct;6(10):777-88
pubmed: 16314867
Cell. 2018 Aug 9;174(4):999-1014.e22
pubmed: 30096314
Front Neurosci. 2011 Jun 14;5:78
pubmed: 21716644
Annu Rev Cell Dev Biol. 2015;31:699-720
pubmed: 26359774
Genome Biol. 2016 Apr 14;17:67
pubmed: 27081004
F1000Res. 2016 Dec 15;5:
pubmed: 28232860
J Neurosci. 2012 Apr 18;32(16):5654-66
pubmed: 22514327
Eur J Neurosci. 2007 Feb;25(4):1006-22
pubmed: 17331197
Nat Neurosci. 2012 Jun 17;15(7):962-9
pubmed: 22706270
Cell. 2012 Nov 9;151(4):918-918.e1
pubmed: 23141546
Nat Biotechnol. 2016 May;34(5):525-7
pubmed: 27043002
Clin Neuropathol. 2013 Sep-Oct;32(5):340-69
pubmed: 23883617
Science. 2018 Apr 13;360(6385):176-182
pubmed: 29545511
Neuron. 2017 Nov 1;96(3):542-557
pubmed: 29096072
Sci Rep. 2020 Mar 13;10(1):4625
pubmed: 32170161
J Exp Neurosci. 2018 Mar 1;12:1179069518759332
pubmed: 29551911
Glia. 2015 Aug;63(8):1350-6
pubmed: 26013243
Adv Neurobiol. 2014;8:165-94
pubmed: 25300137
Genes Dev. 2000 Jan 1;14(1):67-80
pubmed: 10640277
Cell. 2015 Aug 27;162(5):1170-1170.e1
pubmed: 26317476
Neuron. 2005 Jan 20;45(2):207-21
pubmed: 15664173
Curr Opin Cell Biol. 2009 Dec;21(6):733-40
pubmed: 19783418
Dev Neurosci. 2006;28(1-2):58-69
pubmed: 16508304
Science. 2019 May 10;364(6440):
pubmed: 31073041
Neuron. 2013 Dec 4;80(5):1167-74
pubmed: 24314728
Development. 2017 Sep 1;144(17):3156-3167
pubmed: 28851724
Neuron. 2009 Jul 16;63(1):48-62
pubmed: 19607792
Genome Res. 2014 May;24(5):869-84
pubmed: 24515121
Nature. 2021 Aug;596(7870):92-96
pubmed: 34321664
Nature. 2021 Jul;595(7868):554-559
pubmed: 34163074
J Neurosci. 2010 Mar 3;30(9):3489-98
pubmed: 20203209
Nat Rev Neurosci. 2013 Nov;14(11):755-69
pubmed: 24105342
Nucleic Acids Res. 2021 Jan 8;49(D1):D325-D334
pubmed: 33290552
J Neurosci. 2011 Oct 26;31(43):15604-17
pubmed: 22031906
EMBO Rep. 2014 Apr;15(4):351-64
pubmed: 24639559
Dev Growth Differ. 2009 Apr;51(3):299-323
pubmed: 19379279
World J Stem Cells. 2015 Mar 26;7(2):437-47
pubmed: 25815127
Science. 2017 Dec 8;358(6368):1318-1323
pubmed: 29217575
Neuron. 2008 Apr 10;58(1):52-64
pubmed: 18400163
Development. 2002 Nov;129(22):5103-15
pubmed: 12399303
Genes Dev. 2012 May 1;26(9):891-907
pubmed: 22549954
J Neurosci. 1998 Nov 15;18(22):9312-25
pubmed: 9801370
Neuron. 2003 Jul 3;39(1):13-25
pubmed: 12848929
Dev Neurosci. 2003 Mar-Aug;25(2-4):139-51
pubmed: 12966212
Nat Rev Neurosci. 2006 Feb;7(2):93-102
pubmed: 16429119
Cell Stem Cell. 2010 May 7;6(5):445-56
pubmed: 20452319
Int J Dev Neurosci. 2005 Aug;23(5):413-24
pubmed: 15936920
CNS Neurol Disord Drug Targets. 2012 Nov 1;11(7):844-55
pubmed: 23131163
J Neurosci. 2011 Apr 27;31(17):6440-8
pubmed: 21525285
Genes Dev. 2008 Sep 15;22(18):2479-84
pubmed: 18794345
Cell. 2011 Jul 8;146(1):18-36
pubmed: 21729779
Curr Opin Neurobiol. 2010 Oct;20(5):588-94
pubmed: 20655735
Dev Neurosci. 2006;28(1-2):49-57
pubmed: 16508303
J Cheminform. 2014 Sep 17;6(1):44
pubmed: 25264459
Curr Opin Neurobiol. 2017 Feb;42:9-16
pubmed: 27888678
Cell. 2015 Sep 24;163(1):55-67
pubmed: 26406371
Cell. 2017 Nov 2;171(4):877-889.e17
pubmed: 28965759
Cereb Cortex. 2014 Mar;24(3):754-72
pubmed: 23180754
Dev Biol. 2008 Aug 15;320(2):456-68
pubmed: 18582453
Cancer Res. 2001 Mar 1;61(5):2162-8
pubmed: 11280781
Science. 2016 Mar 25;351(6280):1443-6
pubmed: 26940868
Neuron. 2008 Jan 24;57(2):232-47
pubmed: 18215621
Science. 2012 Aug 10;337(6095):746-9
pubmed: 22879516
Genesis. 2009 Nov;47(11):775-81
pubmed: 19830823
Stem Cells. 2011 Nov;29(11):1817-28
pubmed: 21898698
Curr Biol. 1998 May 7;8(10):R334-7
pubmed: 9601631
J Biol Chem. 1992 Oct 15;267(29):21065-71
pubmed: 1328219
Development. 2015 Apr 1;142(7):1375-86
pubmed: 25804741
J Neurosci. 2010 May 19;30(20):7028-36
pubmed: 20484645
Annu Rev Neurosci. 2002;25:471-90
pubmed: 12052917
Science. 2001 Nov 2;294(5544):1071-4
pubmed: 11567107
Cereb Cortex. 2017 Jun 1;27(6):3378-3396
pubmed: 27600842
Nat Rev Neurosci. 2008 Sep;9(9):678-85
pubmed: 19143049
Development. 2000 Jul;127(13):2863-72
pubmed: 10851131
Nat Rev Mol Cell Biol. 2006 Sep;7(9):678-89
pubmed: 16921404
Oncotarget. 2016 May 17;7(20):29306-20
pubmed: 27083054
Front Mol Neurosci. 2021 Jun 09;14:662774
pubmed: 34177462

Auteurs

Tanzila Mukhtar (T)

Department of Biomedicine, University of Basel, Basel, Switzerland.

Jeremie Breda (J)

Biozentrum, University of Basel, Basel, Switzerland.
Swiss Institute of Bioinformatics (SIB), Basel, Switzerland.

Manal A Adam (MA)

Eli and Edythe Broad Center of Regeneration Medicine and Stem cell Research, University of California, San Francisco, San Francisco, CA, USA.
Weill Institute for Neuroscience, San Francisco, CA, USA.
Department of Neurology, University of California, San Francisco, San Francisco, CA, USA.

Marcelo Boareto (M)

Swiss Institute of Bioinformatics (SIB), Basel, Switzerland.
Computational Biology Group, D-BSSE, ETH Zürich, Basel, Switzerland.

Pascal Grobecker (P)

Biozentrum, University of Basel, Basel, Switzerland.
Swiss Institute of Bioinformatics (SIB), Basel, Switzerland.

Zahra Karimaddini (Z)

Swiss Institute of Bioinformatics (SIB), Basel, Switzerland.
Computational Biology Group, D-BSSE, ETH Zürich, Basel, Switzerland.

Alice Grison (A)

Department of Biomedicine, University of Basel, Basel, Switzerland.

Katja Eschbach (K)

Department of Biosystems Science and Engineering, ETH Zürich, Basel, Switzerland.

Ramakrishnan Chandrasekhar (R)

Swiss Data Science Center, Zürich, Switzerland.

Swen Vermeul (S)

Scientific IT Services, ETH Zürich, Zürich, Switzerland.

Michal Okoniewski (M)

Scientific IT Services, ETH Zürich, Zürich, Switzerland.

Mikhail Pachkov (M)

Biozentrum, University of Basel, Basel, Switzerland.
Swiss Institute of Bioinformatics (SIB), Basel, Switzerland.

Corey C Harwell (CC)

Eli and Edythe Broad Center of Regeneration Medicine and Stem cell Research, University of California, San Francisco, San Francisco, CA, USA.
Weill Institute for Neuroscience, San Francisco, CA, USA.
Department of Neurology, University of California, San Francisco, San Francisco, CA, USA.

Suzana Atanasoski (S)

Department of Biomedicine, University of Basel, Basel, Switzerland.
Faculty of Medicine, University of Zürich, Zürich, Switzerland.

Christian Beisel (C)

Department of Biosystems Science and Engineering, ETH Zürich, Basel, Switzerland.

Dagmar Iber (D)

Swiss Institute of Bioinformatics (SIB), Basel, Switzerland.
Weill Institute for Neuroscience, San Francisco, CA, USA.

Erik van Nimwegen (E)

Biozentrum, University of Basel, Basel, Switzerland.
Swiss Institute of Bioinformatics (SIB), Basel, Switzerland.

Verdon Taylor (V)

Department of Biomedicine, University of Basel, Basel, Switzerland.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH