Subcellular mRNA localization and local translation of Arhgap11a in radial glial progenitors regulates cortical development.

Humans Mice Animals Ependymoglial Cells / metabolism RNA, Messenger / metabolism Neuroglia / metabolism Neurogenesis Cerebral Cortex GTPase-Activating Proteins / genetics
Arhgap11a RhoGAP cortical development interneuron positioning neuronal migration local translation mRNA localization mRNA transport mouse radial glial endfeet

Journal

Neuron
ISSN: 1097-4199
Titre abrégé: Neuron
Pays: United States
ID NLM: 8809320

Informations de publication

Date de publication:
15 03 2023
Historique:
received: 08 09 2020
revised: 26 11 2022
accepted: 10 02 2023
pmc-release: 15 03 2024
entrez: 16 3 2023
pubmed: 17 3 2023
medline: 21 3 2023
Statut: ppublish

Résumé

mRNA localization and local translation enable exquisite spatial and temporal control of gene expression, particularly in polarized, elongated cells. These features are especially prominent in radial glial cells (RGCs), which are neural and glial precursors of the developing cerebral cortex and scaffolds for migrating neurons. Yet the mechanisms by which subcellular RGC compartments accomplish their diverse functions are poorly understood. Here, we demonstrate that mRNA localization and local translation of the RhoGAP ARHGAP11A in the basal endfeet of RGCs control their morphology and mediate neuronal positioning. Arhgap11a transcript and protein exhibit conserved localization to RGC basal structures in mice and humans, conferred by the 5' UTR. Proper RGC morphology relies upon active Arhgap11a mRNA transport and localization to the basal endfeet, where ARHGAP11A is locally synthesized. This translation is essential for positioning interneurons at the basement membrane. Thus, local translation spatially and acutely activates Rho signaling in RGCs to compartmentalize neural progenitor functions.

Identifiants

DOI: 10.1016/j.neuron.2023.02.023 PMID: 36924763 PMC: PMC10132781
pubmed: 36924763
pii: S0896-6273(23)00127-7
doi: 10.1016/j.neuron.2023.02.023
pmc: PMC10132781
mid: NIHMS1881420
pii:
doi:

Substances chimiques

RNA, Messenger 0
ARHGAP11A protein, human 0
GTPase-Activating Proteins 0

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

839-856.e5

Subventions

Organisme : NINDS NIH HHS
ID : R01 NS083897
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS110388
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS120667
Pays : United States

Informations de copyright

Copyright © 2023 Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests The authors declare no competing interests.

Références

Nature. 2001 Feb 8;409(6821):714-20
pubmed: 11217860
J Cell Biol. 2008 Nov 3;183(3):401-8
pubmed: 18955552
J Neurosci. 2006 Jan 18;26(3):1045-56
pubmed: 16421324
Elife. 2020 Jun 08;9:
pubmed: 32510328
Dev Biol. 2001 Dec 1;240(1):237-46
pubmed: 11784059
Cell Rep. 2018 Dec 4;25(10):2729-2741.e6
pubmed: 30517861
Nature. 2007 Aug 23;448(7156):901-7
pubmed: 17713529
Nature. 2005 Nov 24;438(7067):512-5
pubmed: 16306994
Nat Neurosci. 2018 Jul;21(7):920-931
pubmed: 29915195
Traffic. 2020 Dec;21(12):737-748
pubmed: 33058331
Dev Cell. 2015 Feb 23;32(4):435-46
pubmed: 25710530
Glia. 2003 Jul;43(1):19-32
pubmed: 12761862
PLoS One. 2007 Aug 29;2(8):e794
pubmed: 17726524
Neuron. 2016 Jan 20;89(2):248-68
pubmed: 26796689
Cereb Cortex. 2011 Apr;21(4):845-52
pubmed: 20732898
Annu Rev Cell Dev Biol. 2015;31:699-720
pubmed: 26359774
Neuron. 2022 Apr 6;110(7):1100-1115
pubmed: 35216663
PLoS One. 2013 Dec 30;8(12):e83629
pubmed: 24386239
J Neurosci. 2007 Dec 12;27(50):13854-65
pubmed: 18077697
Neuron. 2017 Aug 16;95(4):852-868.e8
pubmed: 28781168
Cell. 2018 May 31;173(6):1370-1384.e16
pubmed: 29856955
Cell. 2018 May 31;173(6):1356-1369.e22
pubmed: 29856954
J Neurosci. 2009 Jun 17;29(24):7694-705
pubmed: 19535581
J Neuropathol Exp Neurol. 2012 Dec;71(12):1047-63
pubmed: 23147502
Nat Neurosci. 2010 Jun;13(6):690-9
pubmed: 20436478
Curr Opin Neurobiol. 2019 Jun;56:117-124
pubmed: 30677551
Nat Struct Mol Biol. 2019 Jul;26(7):557-566
pubmed: 31270476
Nature. 2010 Mar 25;464(7288):554-561
pubmed: 20154730
Brain Res. 2015 Mar 2;1599:57-66
pubmed: 25553615
Dev Growth Differ. 2014 Jun;56(5):349-57
pubmed: 24835888
Mech Dev. 2001 Jul;105(1-2):47-56
pubmed: 11429281
EMBO J. 2012 Apr 18;31(8):1879-92
pubmed: 22395070
J Comp Neurol. 1972 May;145(1):61-83
pubmed: 4624784
Science. 2019 May 10;364(6440):
pubmed: 31073041
Brain Res Dev Brain Res. 1990 Mar 1;52(1-2):39-56
pubmed: 2331800
Nat Methods. 2011 Feb;8(2):165-70
pubmed: 21240280
Cell Commun Signal. 2018 Dec 13;16(1):99
pubmed: 30545369
FEBS Lett. 2017 Jun;591(11):1526-1539
pubmed: 28304078
Development. 2000 Dec;127(24):5253-63
pubmed: 11076748
Nat Rev Neurosci. 2013 Nov;14(11):755-69
pubmed: 24105342
Cell. 2012 May 11;149(4):923-35
pubmed: 22559944
Nature. 2019 Jan;565(7739):356-360
pubmed: 30626971
Science. 2017 Dec 8;358(6368):1318-1323
pubmed: 29217575
J Neurosci. 1999 Sep 15;19(18):7881-8
pubmed: 10479690
Science. 2020 Jul 31;369(6503):546-550
pubmed: 32554627
Neuron. 2012 May 10;74(3):453-66
pubmed: 22578497
Nature. 2007 Sep 20;449(7160):351-5
pubmed: 17721509
Nat Rev Mol Cell Biol. 2015 Feb;16(2):95-109
pubmed: 25549890
Nat Rev Neurosci. 2019 Jun;20(6):318-329
pubmed: 30874623
Dev Cell. 2020 Jul 6;54(1):43-59.e4
pubmed: 32634398
Cell Rep. 2017 Jan 31;18(5):1157-1170
pubmed: 28147272
J Neurosci. 2008 May 28;28(22):5817-26
pubmed: 18509043
Neuron. 2019 Sep 4;103(5):836-852.e5
pubmed: 31277925
Neuron. 2013 Oct 16;80(2):442-57
pubmed: 24139044
Neuron. 2012 Mar 8;73(5):911-24
pubmed: 22405202
J Vis Exp. 2014 Jun 04;(88):
pubmed: 24961595
Nat Commun. 2019 Jan 11;10(1):134
pubmed: 30635555
Curr Biol. 2016 Dec 19;26(24):3383-3392
pubmed: 27916527
J Neurosci. 2009 Feb 4;29(5):1300-11
pubmed: 19193877
Brain Res Dev Brain Res. 1995 Jan 14;84(1):109-29
pubmed: 7720210
Cell. 2016 Mar 10;164(6):1302-1302.e1
pubmed: 26967295
Development. 2010 Dec;137(23):4101-10
pubmed: 21062867
Dev Cell. 2013 Sep 16;26(5):496-510
pubmed: 24012485
Cell Stem Cell. 2019 Apr 4;24(4):535-550.e9
pubmed: 30905618
Science. 2021 Jan 22;371(6527):
pubmed: 33479124
Neuron. 2016 Jan 6;89(1):83-99
pubmed: 26748089
Development. 2002 Mar;129(6):1327-38
pubmed: 11880342
Semin Cell Dev Biol. 2021 Oct;118:35-49
pubmed: 34034988
Nat Rev Neurosci. 2001 Nov;2(11):780-90
pubmed: 11715055
Science. 2015 Mar 27;347(6229):1465-70
pubmed: 25721503
Elife. 2018 Mar 21;7:
pubmed: 29561261
J Neurosci Res. 2007 Dec;85(16):3567-73
pubmed: 17671991
Curr Opin Neurobiol. 2020 Aug;63:15-22
pubmed: 32087477
Curr Opin Neurobiol. 2021 Feb;66:125-134
pubmed: 33186879
Cell Rep. 2013 May 30;3(5):1526-38
pubmed: 23684608
Development. 2006 Aug;133(16):3245-54
pubmed: 16873583
Elife. 2018 Nov 28;7:
pubmed: 30484771

Auteurs

Louis-Jan Pilaz (LJ)

Department of Molecular Genetics and Microbiology, Duke University School of Medicine, Durham, NC 27710, USA; Pediatrics and Rare Diseases Group, Sanford Research, Sioux Falls, SD 57104, USA; Department of Pediatrics, Sanford School of Medicine, University of South Dakota, Sioux Falls, SD 57105, USA.

Jing Liu (J)

Department of Molecular Genetics and Microbiology, Duke University School of Medicine, Durham, NC 27710, USA.

Kaumudi Joshi (K)

Department of Neuroscience, Columbia University Medical Center, New York, NY 10032, USA.

Yuji Tsunekawa (Y)

Laboratory for Cell Asymmetry, RIKEN Center for Biosystems Dynamics Research, Kobe, Japan.

Camila M Musso (CM)

Department of Molecular Genetics and Microbiology, Duke University School of Medicine, Durham, NC 27710, USA.

Brooke R D'Arcy (BR)

Department of Molecular Genetics and Microbiology, Duke University School of Medicine, Durham, NC 27710, USA.

Ikuo K Suzuki (IK)

Department of Biological Sciences, Graduate School of Science, The University of Tokyo, Tokyo, Japan.

Fernando C Alsina (FC)

Department of Molecular Genetics and Microbiology, Duke University School of Medicine, Durham, NC 27710, USA.

Pratiksha Kc (P)

Pediatrics and Rare Diseases Group, Sanford Research, Sioux Falls, SD 57104, USA; Department of Pediatrics, Sanford School of Medicine, University of South Dakota, Sioux Falls, SD 57105, USA.

Sahil Sethi (S)

Department of Molecular Genetics and Microbiology, Duke University School of Medicine, Durham, NC 27710, USA.

Pierre Vanderhaeghen (P)

VIB-KU Leuven Center for Brain & Disease Research, 3000 Leuven, Belgium; KU Leuven, Department of Neurosciences & Leuven Brain Institute, 3000 Leuven, Belgium; Université Libre de Bruxelles (U.L.B.), Institut de Recherches en Biologie Humaine et Moléculaire (IRIBHM), and ULB Neuroscience Institute (UNI), 1070 Brussels, Belgium.

Franck Polleux (F)

Department of Neuroscience, Columbia University Medical Center, New York, NY 10032, USA; Mortimer B. Zuckerman Mind Brain Behavior Institute, New York, NY 10027, USA; Kavli Institute for Brain Sciences, Columbia University Medical Center, New York, NY 10027, USA.

Debra L Silver (DL)

Department of Molecular Genetics and Microbiology, Duke University School of Medicine, Durham, NC 27710, USA; Departments of Cell Biology and Neurobiology, Duke University School of Medicine, Durham, NC 27710, USA; Duke Institute for Brain Sciences and Duke Regeneration Center, Duke University School of Medicine, Durham, NC 27710, USA. Electronic address: debra.silver@duke.edu.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female

Evaluation of Low-Value Services Across Major Medicare Advantage Insurers and Traditional Medicare.

Ciara Duggan, Adam L Beckman, Ishani Ganguli et al.
1.00
Humans United States Aged Cross-Sectional Studies Medicare Part C

Effectiveness of Virtual Yoga for Chronic Low Back Pain: A Randomized Clinical Trial.

Hallie Tankha, Devyn Gaskins, Amanda Shallcross et al.
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH

questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Primates › Haplorhini › Catarrhini › Hominidae › Humains › Subcellular mRNA localization and local...
questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Rodentia › Muridae › Murinae › Souris › Subcellular mRNA localization and local...
questionsmedicales.fr › Eucaryotes › Animaux › Subcellular mRNA localization and local...
questionsmedicales.fr › Cellules › Névroglie › Cellules épendymogliales › Subcellular mRNA localization and local...
questionsmedicales.fr › Acides nucléiques, nucléotides et nucléosides › Acides nucléiques › ARN › ARN messager › Subcellular mRNA localization and local...
questionsmedicales.fr › Cellules › Névroglie › Subcellular mRNA localization and local...
questionsmedicales.fr › Phénomènes physiologiques de l'appareil locomoteur et du système nerveux › Phénomènes physiologiques du système nerveux › Neurogenèse › Subcellular mRNA localization and local...
questionsmedicales.fr › Système nerveux › Système nerveux central › Encéphale › Prosencéphale › Télencéphale › Cerveau › Cortex cérébral › Subcellular mRNA localization and local...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines et peptides de signalisation intracellulaire › Régulateurs des protéines G › Protéines d'activation de la GTPase › Subcellular mRNA localization and local...