Human-specific ARHGAP11B ensures human-like basal progenitor levels in hominid cerebral organoids.


Journal

EMBO reports
ISSN: 1469-3178
Titre abrégé: EMBO Rep
Pays: England
ID NLM: 100963049

Informations de publication

Date de publication:
07 11 2022
Historique:
revised: 18 08 2022
received: 25 01 2022
accepted: 23 08 2022
pubmed: 14 9 2022
medline: 9 11 2022
entrez: 13 9 2022
Statut: ppublish

Résumé

The human-specific gene ARHGAP11B has been implicated in human neocortex expansion. However, the extent of ARHGAP11B's contribution to this expansion during hominid evolution is unknown. Here we address this issue by genetic manipulation of ARHGAP11B levels and function in chimpanzee and human cerebral organoids. ARHGAP11B expression in chimpanzee cerebral organoids doubles basal progenitor levels, the class of cortical progenitors with a key role in neocortex expansion. Conversely, interference with ARHGAP11B's function in human cerebral organoids decreases basal progenitors down to the chimpanzee level. Moreover, ARHGAP11A or ARHGAP11B rescue experiments in ARHGAP11A plus ARHGAP11B double-knockout human forebrain organoids indicate that lack of ARHGAP11B, but not of ARHGAP11A, decreases the abundance of basal radial glia-the basal progenitor type thought to be of particular relevance for neocortex expansion. Taken together, our findings demonstrate that ARHGAP11B is necessary and sufficient to ensure the elevated basal progenitor levels that characterize the fetal human neocortex, suggesting that this human-specific gene was a major contributor to neocortex expansion during human evolution.

Identifiants

pubmed: 36098218
doi: 10.15252/embr.202254728
pmc: PMC9646322
mid: EMS155265
doi:

Substances chimiques

ARHGAP11B protein, human 0
GTPase-Activating Proteins 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e54728

Subventions

Organisme : European Research Council
ID : 101039421
Pays : International

Informations de copyright

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

Références

Nat Methods. 2015 Jul;12(7):671-8
pubmed: 26005811
Cell Stem Cell. 2020 May 7;26(5):766-781.e9
pubmed: 32142682
Nat Protoc. 2014 Oct;9(10):2329-40
pubmed: 25188634
Elife. 2016 Sep 26;5:
pubmed: 27669147
Nat Neurosci. 2005 Mar;8(3):288-96
pubmed: 15696161
Nature. 2013 Sep 19;501(7467):373-9
pubmed: 23995685
Neuron. 2008 Oct 9;60(1):56-69
pubmed: 18940588
Elife. 2018 Nov 28;7:
pubmed: 30484771
Nat Phys. 2018 May;14(5):515-522
pubmed: 29760764
Nat Rev Neurosci. 2009 Oct;10(10):724-35
pubmed: 19763105
Proc Natl Acad Sci U S A. 2015 Dec 22;112(51):15672-7
pubmed: 26644564
Cell Stem Cell. 2016 Apr 7;18(4):467-80
pubmed: 27049876
Nature. 2019 Oct;574(7778):418-422
pubmed: 31619793
Proc Natl Acad Sci U S A. 2004 Mar 2;101(9):3196-201
pubmed: 14963232
Trends Neurosci. 2008 Mar;31(3):113-9
pubmed: 18255163
Protein Cell. 2017 Nov;8(11):823-833
pubmed: 29058117
Curr Opin Neurobiol. 2014 Aug;27:39-46
pubmed: 24632307
Nat Rev Neurosci. 2017 Oct;18(10):573-584
pubmed: 28878372
Eur J Neurosci. 2006 Feb;23(4):921-34
pubmed: 16519657
Cell. 2018 May 31;173(6):1370-1384.e16
pubmed: 29856955
Nature. 2020 Feb;578(7793):142-148
pubmed: 31996853
Cell. 2018 May 31;173(6):1356-1369.e22
pubmed: 29856954
Nat Neurosci. 2019 Apr;22(4):669-679
pubmed: 30886407
Nat Rev Neurosci. 2007 Jun;8(6):427-37
pubmed: 17514196
Nat Neurosci. 2010 Jun;13(6):690-9
pubmed: 20436478
FEBS Lett. 2017 Dec;591(24):3978-3992
pubmed: 29194577
Sci Adv. 2016 Dec 07;2(12):e1601941
pubmed: 27957544
Development. 2014 Jun;141(11):2182-94
pubmed: 24866113
EMBO J. 2021 Jul 1;40(13):e107093
pubmed: 33938018
Proc Natl Acad Sci U S A. 2013 Dec 10;110(50):20284-9
pubmed: 24277810
Nature. 2002 Jul 11;418(6894):145-51
pubmed: 12110880
Nature. 2010 Mar 25;464(7288):554-561
pubmed: 20154730
Neuron. 2005 Jan 20;45(2):207-21
pubmed: 15664173
Nat Ecol Evol. 2017;1(3):69
pubmed: 28580430
EMBO J. 2016 May 17;35(10):1021-44
pubmed: 27056680
Nat Rev Neurosci. 2014 Apr;15(4):217-32
pubmed: 24646670
Cereb Cortex. 2011 Jul;21(7):1674-94
pubmed: 21127018
Neuron. 2008 Feb 7;57(3):378-92
pubmed: 18255031
Cell Rep. 2017 Apr 4;19(1):50-59
pubmed: 28380362
Neuron. 2015 Feb 18;85(4):683-94
pubmed: 25695268
J Cell Sci. 2008 Sep 1;121(Pt 17):2783-93
pubmed: 18716282
Development. 2004 Jul;131(13):3133-45
pubmed: 15175243
Science. 2020 Jul 31;369(6503):546-550
pubmed: 32554627
Front Cell Neurosci. 2019 Dec 17;13:558
pubmed: 31920558
Nat Rev Neurosci. 2019 Mar;20(3):161-176
pubmed: 30610227
Cell. 2016 May 19;165(5):1238-1254
pubmed: 27118425
EMBO Rep. 2022 May 4;23(5):e54027
pubmed: 35289477
Nat Methods. 2018 Jan 3;15(1):27-29
pubmed: 29298289
Nature. 2017 May 4;545(7652):48-53
pubmed: 28445462
Neuron. 2013 Oct 16;80(2):442-57
pubmed: 24139044
J Neurosci. 2005 Jan 5;25(1):247-51
pubmed: 15634788
Nat Neurosci. 2004 Feb;7(2):136-44
pubmed: 14703572
Nature. 2019 Jun;570(7762):523-527
pubmed: 31168097
Development. 2018 Oct 18;145(20):
pubmed: 30266827
Cell. 2011 Jul 8;146(1):18-36
pubmed: 21729779
Curr Opin Cell Biol. 2018 Dec;55:8-16
pubmed: 30006054
Neuron. 2020 Mar 4;105(5):867-881.e9
pubmed: 31883789
Cells. 2021 May 15;10(5):
pubmed: 34063381
J Anat. 2019 Sep;235(3):432-451
pubmed: 31373394
Cell. 2015 Sep 24;163(1):55-67
pubmed: 26406371
Brain Res. 2005 Aug 2;1052(1):71-81
pubmed: 16018988
Nat Biotechnol. 2017 Jul;35(7):659-666
pubmed: 28562594
Cell Stem Cell. 2008 Nov 6;3(5):519-32
pubmed: 18983967
Trends Neurosci. 2011 Jan;34(1):41-50
pubmed: 21129791
Cell Stem Cell. 2016 Jun 2;18(6):736-748
pubmed: 27257762
Nature. 2005 Apr 7;434(7034):752-5
pubmed: 15815627
Science. 2010 Oct 29;330(6004):641-6
pubmed: 21030649
J Vis Exp. 2018 Jan 23;(131):
pubmed: 29443048
Neuron. 2008 Feb 7;57(3):364-77
pubmed: 18255030
Science. 2015 Mar 27;347(6229):1465-70
pubmed: 25721503
Elife. 2018 Mar 21;7:
pubmed: 29561261

Auteurs

Jan Fischer (J)

Max Planck Institute of Molecular Cell Biology and Genetics, Pfotenhauerstrasse 108, Dresden, Germany.

Eduardo Fernández Ortuño (E)

Max Planck Institute of Molecular Cell Biology and Genetics, Pfotenhauerstrasse 108, Dresden, Germany.

Fabio Marsoner (F)

Central Institute of Mental Health, University of Heidelberg/Medical Faculty Mannheim, Mannheim, Germany.
Hector Institute for Translational Brain Research (HITBR gGmbH), Mannheim, Germany.
German Cancer Research Center (DKFZ), Heidelberg, Germany.

Annasara Artioli (A)

Central Institute of Mental Health, University of Heidelberg/Medical Faculty Mannheim, Mannheim, Germany.
Hector Institute for Translational Brain Research (HITBR gGmbH), Mannheim, Germany.
German Cancer Research Center (DKFZ), Heidelberg, Germany.

Jula Peters (J)

Max Planck Institute of Molecular Cell Biology and Genetics, Pfotenhauerstrasse 108, Dresden, Germany.

Takashi Namba (T)

Max Planck Institute of Molecular Cell Biology and Genetics, Pfotenhauerstrasse 108, Dresden, Germany.

Christina Eugster Oegema (C)

Max Planck Institute of Molecular Cell Biology and Genetics, Pfotenhauerstrasse 108, Dresden, Germany.

Wieland B Huttner (WB)

Max Planck Institute of Molecular Cell Biology and Genetics, Pfotenhauerstrasse 108, Dresden, Germany.

Julia Ladewig (J)

Central Institute of Mental Health, University of Heidelberg/Medical Faculty Mannheim, Mannheim, Germany.
Hector Institute for Translational Brain Research (HITBR gGmbH), Mannheim, Germany.
German Cancer Research Center (DKFZ), Heidelberg, Germany.

Michael Heide (M)

Max Planck Institute of Molecular Cell Biology and Genetics, Pfotenhauerstrasse 108, Dresden, Germany.
German Primate Center, Leibniz Institute for Primate Research, Göttingen, Germany.

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