Assembly of neuron- and radial glial-cell-derived extracellular matrix molecules promotes radial migration of developing cortical neurons.
biochemistry
chemical biology
cortical development
extracellular matrix
hyaluronic acid
mouse
neuroscience
proteoglycans
radial migration
tenascin
Journal
eLife
ISSN: 2050-084X
Titre abrégé: Elife
Pays: England
ID NLM: 101579614
Informations de publication
Date de publication:
21 Mar 2024
21 Mar 2024
Historique:
medline:
21
3
2024
pubmed:
21
3
2024
entrez:
21
3
2024
Statut:
epublish
Résumé
Radial neuronal migration is a key neurodevelopmental event for proper cortical laminar organization. The multipolar-to-bipolar transition, a critical step in establishing neuronal polarity during radial migration, occurs in the subplate/intermediate zone (SP/IZ), a distinct region of the embryonic cerebral cortex. It has been known that the extracellular matrix (ECM) molecules are enriched in the SP/IZ. However, the molecular constitution and functions of the ECM formed in this region remain poorly understood. Here, we identified neurocan (NCAN) as a major chondroitin sulfate proteoglycan in the mouse SP/IZ. NCAN binds to both radial glial-cell-derived tenascin-C (TNC) and hyaluronan (HA), a large linear polysaccharide, forming a ternary complex of NCAN, TNC, and HA in the SP/IZ. Developing cortical neurons make contact with the ternary complex during migration. The enzymatic or genetic disruption of the ternary complex impairs radial migration by suppressing the multipolar-to-bipolar transition. Furthermore, both TNC and NCAN promoted the morphological maturation of cortical neurons in vitro. The present results provide evidence for the cooperative role of neuron- and radial glial-cell-derived ECM molecules in cortical development.
Identifiants
pubmed: 38512724
doi: 10.7554/eLife.92342
pii: 92342
doi:
pii:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Ministry of Education, Culture, Sports, Science and Technology
ID : 15K21067
Organisme : Ministry of Education, Culture, Sports, Science and Technology
ID : 18K06130
Organisme : Ministry of Education, Culture, Sports, Science and Technology
ID : 21H05681
Organisme : Lotte Foundation
ID : Lotte Shigemitsu Prize
Informations de copyright
© 2023, Mubuchi et al.
Déclaration de conflit d'intérêts
AM, MT, SN, TM, YI, CS, KK, HK, SM No competing interests declared
Références
Proc Natl Acad Sci U S A. 1997 Sep 16;94(19):10116-21
pubmed: 9294172
J Cell Biol. 1992 Mar;116(6):1475-86
pubmed: 1371773
Neuron. 2014 Feb 19;81(4):814-29
pubmed: 24559674
Biochim Biophys Acta Gen Subj. 2021 Feb;1865(2):129804
pubmed: 33253804
Cold Spring Harb Perspect Biol. 2011 Jan 01;3(1):a005108
pubmed: 21123393
Annu Rev Neurosci. 2009;32:149-84
pubmed: 19555289
Curr Opin Neurobiol. 2021 Feb;66:77-84
pubmed: 33099181
Cell. 2015 Sep 24;163(1):55-67
pubmed: 26406371
J Neurosci. 2003 Nov 5;23(31):9996-10001
pubmed: 14602813
Nucleic Acids Res. 2014 Jul;42(Web Server issue):W320-4
pubmed: 24753421
Neuron. 2018 Aug 22;99(4):702-719.e6
pubmed: 30078576
Biochim Biophys Acta Gen Subj. 2017 Oct;1861(10):2420-2434
pubmed: 28625420
Neuroscience. 1997 Dec;81(3):829-46
pubmed: 9316032
iScience. 2021 Mar 06;24(4):102277
pubmed: 33851097
Cell Mol Life Sci. 2001 Nov;58(12-13):1842-56
pubmed: 11766883
J Neurosci. 2006 Apr 12;26(15):4082-94
pubmed: 16611825
Int J Exp Pathol. 2012 Feb;93(1):1-10
pubmed: 22264297
Mol Biol Evol. 2013 Apr;30(4):772-80
pubmed: 23329690
Nat Protoc. 2018 Oct;13(10):2297-2311
pubmed: 30258174
J Neurosci. 2009 Apr 29;29(17):5546-57
pubmed: 19403822
Nat Methods. 2022 Jun;19(6):679-682
pubmed: 35637307
Development. 2007 Aug;134(15):2727-38
pubmed: 17596283
J Cell Biol. 1994 May;125(3):669-80
pubmed: 7513709
Biochem Biophys Res Commun. 2022 Jul 5;612:50-56
pubmed: 35504089
J Comp Neurol. 1997 Jun 2;382(2):141-52
pubmed: 9183685
Nat Protoc. 2019 Aug;14(8):2452-2482
pubmed: 31341289
Annu Rev Neurosci. 2009;32:347-81
pubmed: 19400726
J Neurosci. 2002 Aug 1;22(15):6596-609
pubmed: 12151539
Biochim Biophys Acta. 1970 Mar 18;198(3):607-9
pubmed: 5436162
Development. 2004 Jul;131(14):3423-32
pubmed: 15226258
Histochem Cell Biol. 2008 Oct;130(4):635-53
pubmed: 18696101
J Biochem. 2018 Aug 1;164(2):113-125
pubmed: 29490044
Mol Cell Biol. 2001 Sep;21(17):5970-8
pubmed: 11486035
J Biol Chem. 1992 Sep 25;267(27):19536-47
pubmed: 1326557
Mol Psychiatry. 2022 Aug;27(8):3192-3203
pubmed: 35760878
Cell. 2010 Jul 9;142(1):144-57
pubmed: 20603020
J Biol Chem. 2002 Feb 15;277(7):4585-8
pubmed: 11717315
EMBO J. 2016 May 17;35(10):1021-44
pubmed: 27056680
PLoS One. 2020 Jul 16;15(7):e0234529
pubmed: 32673338
Cell Mol Life Sci. 2000 Feb;57(2):276-89
pubmed: 10766023
J Biol Chem. 1997 Oct 24;272(43):26905-12
pubmed: 9341124
Genome Biol. 2018 Feb 26;19(1):25
pubmed: 29482575
Bone Marrow Transplant. 2013 Mar;48(3):452-8
pubmed: 23208313
Science. 2018 Apr 20;360(6386):313-317
pubmed: 29674592
J Comp Neurol. 1995 May 15;355(4):615-28
pubmed: 7636035
Int J Biochem Cell Biol. 2015 Aug;65:165-8
pubmed: 26055518
Neurochem Res. 2011 Jul;36(7):1228-40
pubmed: 21110089
Glycobiology. 2023 Oct 6;33(8):615-625
pubmed: 36924076
J Neurosci. 1999 Nov 15;19(22):9953-63
pubmed: 10559403
Nat Neurosci. 2011 Jun;14(6):697-703
pubmed: 21516100
Structure. 2004 Aug;12(8):1495-506
pubmed: 15296743
Biochim Biophys Acta Gen Subj. 2020 Oct;1864(10):129679
pubmed: 32623025
Int J Biochem Cell Biol. 2016 Dec;81(Pt A):174-183
pubmed: 27157088
Nat Neurosci. 2004 Feb;7(2):136-44
pubmed: 14703572
Cereb Cortex. 2013 Jan;23(1):105-13
pubmed: 22267309
Dev Neurobiol. 2011 Nov;71(11):889-900
pubmed: 21739613
Nat Neurosci. 2012 Jan 15;15(3):414-22, S1-2
pubmed: 22246436
Cytometry A. 2004 Apr;58(2):167-76
pubmed: 15057970
Annu Rev Cell Dev Biol. 2014;30:465-502
pubmed: 25000993
Nature. 1995 Apr 20;374(6524):719-23
pubmed: 7715726
Eur J Neurosci. 1997 Mar;9(3):496-506
pubmed: 9104592
Nature. 2000 Apr 6;404(6778):567-73
pubmed: 10766232
Science. 2016 Mar 25;351(6280):1443-6
pubmed: 26940868
Nat Neurosci. 2008 Jan;11(1):36-44
pubmed: 18059265
Nucleic Acids Res. 2007 Jul;35(Web Server issue):W473-6
pubmed: 17584791
Protein Sci. 2018 Jan;27(1):129-134
pubmed: 28875543
J Cell Biol. 1991 Jun;113(5):1159-71
pubmed: 1710226
Proc Natl Acad Sci U S A. 2012 Jul 17;109(29):11836-41
pubmed: 22753484
Physiol Rev. 2015 Jul;95(3):995-1024
pubmed: 26133936
Nat Biotechnol. 2001 Jul;19(7):661-7
pubmed: 11433279
Glia. 2015 Aug;63(8):1330-49
pubmed: 25913849
Nat Methods. 2012 Jul;9(7):671-5
pubmed: 22930834
Mol Cell Neurosci. 2017 Jun;81:22-31
pubmed: 27836730
J Biol Chem. 2008 Nov 21;283(47):32610-20
pubmed: 18819920
J Cell Sci. 2014 Dec 1;127(Pt 23):5038-51
pubmed: 25300795
Nat Rev Neurosci. 2015 Mar;16(3):133-46
pubmed: 25697157
Am J Pathol. 1998 May;152(5):1237-45
pubmed: 9588892
Mol Cell Neurosci. 2020 Jul;106:103503
pubmed: 32485296