Brevican, Neurocan, Tenascin-C, and Tenascin-R Act as Important Regulators of the Interplay Between Perineuronal Nets, Synaptic Integrity, Inhibitory Interneurons, and Otx2.
Otx2
brevican
neurocan
parvalbumin
perineuronal nets
synapses
tenascin-C
tenascin-R
Journal
Frontiers in cell and developmental biology
ISSN: 2296-634X
Titre abrégé: Front Cell Dev Biol
Pays: Switzerland
ID NLM: 101630250
Informations de publication
Date de publication:
2022
2022
Historique:
received:
28
02
2022
accepted:
11
04
2022
entrez:
20
6
2022
pubmed:
21
6
2022
medline:
21
6
2022
Statut:
epublish
Résumé
Fast-spiking parvalbumin interneurons are critical for the function of mature cortical inhibitory circuits. Most of these neurons are enwrapped by a specialized extracellular matrix (ECM) structure called perineuronal net (PNN), which can regulate their synaptic input. In this study, we investigated the relationship between PNNs, parvalbumin interneurons, and synaptic distribution on these cells in the adult primary visual cortex (V1) of quadruple knockout mice deficient for the ECM molecules brevican, neurocan, tenascin-C, and tenascin-R. We used super-resolution structured illumination microscopy (SIM) to analyze PNN structure and associated synapses. In addition, we examined parvalbumin and calretinin interneuron populations. We observed a reduction in the number of PNN-enwrapped cells and clear disorganization of the PNN structure in the quadruple knockout V1. This was accompanied by an imbalance of inhibitory and excitatory synapses with a reduction of inhibitory and an increase of excitatory synaptic elements along the PNNs. Furthermore, the number of parvalbumin interneurons was reduced in the quadruple knockout, while calretinin interneurons, which do not wear PNNs, did not display differences in number. Interestingly, we found the transcription factor Otx2 homeoprotein positive cell population also reduced. Otx2 is crucial for parvalbumin interneuron and PNN maturation, and a positive feedback loop between these parameters has been described. Collectively, these data indicate an important role of brevican, neurocan, tenascin-C, and tenascin-R in regulating the interplay between PNNs, inhibitory interneurons, synaptic distribution, and Otx2 in the V1.
Identifiants
pubmed: 35721494
doi: 10.3389/fcell.2022.886527
pii: 886527
pmc: PMC9201762
doi:
Types de publication
Journal Article
Langues
eng
Pagination
886527Informations de copyright
Copyright © 2022 Mueller-Buehl, Reinhard, Roll, Bader, Winklhofer and Faissner.
Déclaration de conflit d'intérêts
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Références
Int J Mol Sci. 2019 Aug 22;20(17):
pubmed: 31443560
Nat Rev Neurosci. 2019 Aug;20(8):451-465
pubmed: 31263252
Oncotarget. 2016 Nov 29;7(48):78224-78225
pubmed: 27861161
Proc Natl Acad Sci U S A. 2014 Nov 25;111(47):16895-900
pubmed: 25385583
Eur J Neurosci. 2008 Mar;27(6):1373-90
pubmed: 18364019
Brain Res Rev. 2010 May;63(1-2):26-38
pubmed: 20096729
Mol Psychiatry. 2017 May;22(5):680-688
pubmed: 28194008
Development. 1991 Sep;113(1):151-64
pubmed: 1764992
Proc Natl Acad Sci U S A. 2006 May 30;103(22):8517-22
pubmed: 16709670
Nucleic Acids Res. 2002 May 1;30(9):e36
pubmed: 11972351
Brain Struct Funct. 2020 Jan;225(1):321-344
pubmed: 31858237
J Pineal Res. 2001 Nov;31(4):356-62
pubmed: 11703566
Adv Exp Med Biol. 2012;970:153-71
pubmed: 22351055
J Neurochem. 2014 Sep;130(6):797-804
pubmed: 24903590
Nat Genet. 1994 Jun;7(2):154-7
pubmed: 7920633
J Glaucoma. 2014 Oct-Nov;23(8 Suppl 1):S20-3
pubmed: 25275899
Hippocampus. 2017 Aug;27(8):920-933
pubmed: 28512860
Brain Res. 1985 Jul;353(1):73-81
pubmed: 4027684
J Comp Neurol. 2021 Aug 1;529(11):2827-2841
pubmed: 33576496
Proc Natl Acad Sci U S A. 2013 May 28;110(22):9130-5
pubmed: 23671099
Neuron. 2015 Aug 19;87(4):684-98
pubmed: 26291155
Mol Cell Biol. 2002 Nov;22(21):7417-27
pubmed: 12370289
Neural Plast. 2016;2016:7931693
pubmed: 26881132
Cells. 2021 May 29;10(6):
pubmed: 34072323
Neuroscience. 2006;138(2):365-75
pubmed: 16427210
Mol Psychiatry. 2019 Sep;24(9):1248-1257
pubmed: 31089192
Front Integr Neurosci. 2018 Feb 02;12:3
pubmed: 29456495
J Neurochem. 2015 Dec;135(5):849-58
pubmed: 26338675
Proc Natl Acad Sci U S A. 1996 Jun 25;93(13):6594-9
pubmed: 8692862
Nat Neurosci. 2000 Apr;3(4):366-71
pubmed: 10725926
Brain Struct Funct. 2017 Jan;222(1):393-415
pubmed: 27089885
Dev Biol. 1998 Oct 1;202(1):56-66
pubmed: 9758703
Front Neural Circuits. 2013 Oct 01;7:153
pubmed: 24101895
Neuroscience. 2010 Nov 10;170(4):1314-27
pubmed: 20732394
J Neurosci. 1999 Jun 1;19(11):4245-62
pubmed: 10341229
Front Integr Neurosci. 2017 Dec 01;11:33
pubmed: 29249944
Biol Psychiatry. 2017 May 15;81(10):838-847
pubmed: 27450033
Histochem Cell Biol. 2008 Oct;130(4):635-53
pubmed: 18696101
Neural Plast. 2018 Feb 4;2018:5735789
pubmed: 29531525
J Neurosci. 2005 Aug 3;25(31):7150-8
pubmed: 16079397
Mol Cell Biol. 2001 Sep;21(17):5970-8
pubmed: 11486035
Cell. 2008 Aug 8;134(3):508-20
pubmed: 18692473
Neuron. 1990 Nov;5(5):627-37
pubmed: 1699568
BMC Bioinformatics. 2021 Sep 10;22(1):433
pubmed: 34507520
Cell Rep. 2013 Jun 27;3(6):1815-23
pubmed: 23770240
J Neurosci. 2021 May 27;:
pubmed: 34045309
Cell Mol Life Sci. 2000 Feb;57(2):276-89
pubmed: 10766023
Am J Neurodegener Dis. 2012;1(2):122-9
pubmed: 23383386
J Cell Mol Med. 2016 Nov;20(11):2122-2137
pubmed: 27374750
Elife. 2018 Dec 18;7:
pubmed: 30561327
Science. 2002 Nov 8;298(5596):1248-51
pubmed: 12424383
Physiol Res. 2010;59(5):665-677
pubmed: 20406030
Cell Tissue Res. 2012 Jul;349(1):147-60
pubmed: 22437874
Mol Cell Neurosci. 2003 Sep;24(1):148-59
pubmed: 14550776
Trends Neurosci. 2019 Jul;42(7):458-470
pubmed: 31174916
Ann Biomed Eng. 2020 Mar;48(3):1071-1089
pubmed: 31485876
Front Mol Neurosci. 2013 Dec 30;6:55
pubmed: 24415998
Trends Neurosci. 1998 Dec;21(12):510-5
pubmed: 9881847
eNeuro. 2019 May 7;6(2):
pubmed: 31064838
Prog Brain Res. 2013;207:3-34
pubmed: 24309249
J Comp Neurol. 2012 Jun 1;520(8):1721-36
pubmed: 22121037
Neuroreport. 1992 Oct;3(10):869-72
pubmed: 1421090
Neural Plast. 2016;2016:5214961
pubmed: 26881114
Dev Neurobiol. 2007 Apr;67(5):570-88
pubmed: 17443809
J Neurosci. 1996 Feb 15;16(4):1380-8
pubmed: 8778289
J Cell Biochem. 1999 Jun 1;73(3):321-31
pubmed: 10321832
J Biol Chem. 2006 Jun 30;281(26):17789-800
pubmed: 16644727
Int J Mol Sci. 2021 Aug 19;22(16):
pubmed: 34445655
Structure. 2004 Aug;12(8):1495-506
pubmed: 15296743
Front Mol Neurosci. 2021 Apr 12;14:597812
pubmed: 33912009
eNeuro. 2017 Jun 7;4(3):
pubmed: 28593193
Science. 2009 Nov 27;326(5957):1216-9
pubmed: 19965464
J Neurosci. 2013 May 1;33(18):7742-55
pubmed: 23637166
Cell Mol Life Sci. 2021 Jul;78(14):5647-5663
pubmed: 34128077
Front Neurosci. 2015 Mar 23;9:98
pubmed: 25852466
J Chem Neuroanat. 2003 Aug;26(1):37-50
pubmed: 12954529
J Cell Sci. 2010 Dec 15;123(Pt 24):4195-200
pubmed: 21123617
Front Neurosci. 2017 May 31;11:307
pubmed: 28620275
J Neurosci Methods. 2012 Feb 15;204(1):144-149
pubmed: 22108140
J Comp Neurol. 2000 Dec 25;428(4):616-29
pubmed: 11077416
Annu Rev Neurosci. 2012;35:309-30
pubmed: 22462544
Cold Spring Harb Perspect Biol. 2012 Jan 01;4(1):a004903
pubmed: 21937732
Eur J Neurosci. 2011 Jun;33(12):2187-202
pubmed: 21615557
J Neurochem. 1985 Jan;44(1):99-109
pubmed: 2856886
Neuron. 2017 Aug 2;95(3):639-655.e10
pubmed: 28712654
Cereb Cortex. 2005 Jul;15(7):950-62
pubmed: 15537675
Proc Natl Acad Sci U S A. 2019 Apr 2;116(14):7071-7076
pubmed: 30890637
Philos Trans R Soc Lond B Biol Sci. 2014 Oct 19;369(1654):20140046
pubmed: 25225104
Biochem Biophys Res Commun. 2005 Mar 11;328(2):608-17
pubmed: 15694392
Neuroscience. 2001;104(2):359-69
pubmed: 11377840
Sci Rep. 2019 Sep 26;9(1):13939
pubmed: 31558805
J Neurosci. 2016 Jun 8;36(23):6312-20
pubmed: 27277807
Biomolecules. 2020 Oct 30;10(11):
pubmed: 33143303
J Neurosci. 2002 Sep 1;22(17):7536-47
pubmed: 12196577
BMC Neurosci. 2008 Jan 25;9:14
pubmed: 18221525
J Neurosci. 2018 Nov 21;38(47):10102-10113
pubmed: 30282728
Cereb Cortex. 2019 Jun 1;29(6):2384-2395
pubmed: 29771284
J Neurosci. 2012 Jul 4;32(27):9429-37
pubmed: 22764251