Inhibition of Matrix Metalloproteinase 9 Activity Promotes Synaptogenesis in the Hippocampus.
Animals
CA1 Region, Hippocampal
/ cytology
Carbachol
/ pharmacology
Cholinergic Agonists
/ pharmacology
Excitatory Postsynaptic Potentials
/ drug effects
Hippocampus
/ drug effects
Matrix Metalloproteinase 9
/ drug effects
Matrix Metalloproteinase Inhibitors
/ pharmacology
Neurogenesis
/ drug effects
Neuronal Plasticity
/ drug effects
Patch-Clamp Techniques
Rats
MMP-9
carbachol
excitatory
inhibitory
synaptogenesis
Journal
Cerebral cortex (New York, N.Y. : 1991)
ISSN: 1460-2199
Titre abrégé: Cereb Cortex
Pays: United States
ID NLM: 9110718
Informations de publication
Date de publication:
05 07 2021
05 07 2021
Historique:
received:
22
07
2020
revised:
21
01
2021
accepted:
12
02
2021
pubmed:
20
3
2021
medline:
8
3
2022
entrez:
19
3
2021
Statut:
ppublish
Résumé
Information coding in the hippocampus relies on the interplay between various neuronal ensembles. We discovered that the application of a cholinergic agonist, carbachol (Cch), which triggers oscillatory activity in the gamma range, induces the activity of matrix metalloproteinase 9 (MMP-9)-an enzyme necessary for the maintenance of synaptic plasticity. Using electrophysiological recordings in hippocampal organotypic slices, we show that Cch potentiates the frequency of miniature inhibitory and excitatory postsynaptic currents (mIPSCs and mEPSCs, respectively) in CA1 neurons and this effect is MMP-9 dependent. Interestingly, though MMP-9 inhibition prevents the potentiation of inhibitory events, it further boosts the frequency of excitatory mEPSCs. Such enhancement of the frequency of excitatory events is a result of increased synaptogenesis onto CA1 neurons. Thus, the function of MMP-9 in cholinergically induced plasticity in the hippocampus is to maintain the fine-tuned balance between the excitatory and the inhibitory synaptic transmission.
Identifiants
pubmed: 33739386
pii: 6178422
doi: 10.1093/cercor/bhab050
pmc: PMC8258443
doi:
Substances chimiques
Cholinergic Agonists
0
Matrix Metalloproteinase Inhibitors
0
Carbachol
8Y164V895Y
Matrix Metalloproteinase 9
EC 3.4.24.35
Mmp9 protein, rat
EC 3.4.24.35
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
3804-3819Subventions
Organisme : National Science Centre
ID : 2017/26/A/NZ3/00379
Organisme : Foundation for Polish Science
ID : MAB/2018/10
Organisme : International Research Agendas programme
Organisme : European Regional Development Fund
Commentaires et corrections
Type : ErratumIn
Informations de copyright
© The Author(s) 2021. Published by Oxford University Press.
Références
J Neurosci Res. 2015 Jul;93(7):1067-78
pubmed: 25808046
Proc Natl Acad Sci U S A. 2008 Dec 9;105(49):19520-5
pubmed: 19047646
Brain Res. 1981 Feb 23;207(1):109-27
pubmed: 6258725
Methods Mol Biol. 2017;1626:79-102
pubmed: 28608202
PLoS Biol. 2008 Sep 9;6(9):e219
pubmed: 18788894
Mol Cell Neurosci. 2004 Mar;25(3):515-23
pubmed: 15033179
J Neurochem. 2016 Oct;139 Suppl 2:91-114
pubmed: 26525923
J Neurosci. 2002 Feb 1;22(3):920-30
pubmed: 11826121
Neurosci Biobehav Rev. 2010 Jun;34(7):1023-35
pubmed: 20060015
Nat Rev Neurosci. 2003 Jun;4(6):456-68
pubmed: 12778118
Behav Brain Res. 2011 Aug 10;221(2):505-14
pubmed: 21130117
Neuron. 1997 Jun;18(6):995-1008
pubmed: 9208866
Methods Mol Biol. 2012;814:221-33
pubmed: 22144310
Hippocampus. 2013 Jun;23(6):529-43
pubmed: 23418057
J Neurosci. 2010 Nov 17;30(46):15337-57
pubmed: 21084591
Biomaterials. 2014 Feb;35(5):1402-10
pubmed: 24290700
Nat Rev Neurosci. 2012 Nov;13(11):743-57
pubmed: 23047773
Sleep. 2009 Sep;32(9):1135-47
pubmed: 19750918
Prog Neuropsychopharmacol Biol Psychiatry. 2001 May;25(4):835-53
pubmed: 11383980
J Neurophysiol. 1993 Feb;69(2):626-9
pubmed: 8459290
Science. 2008 Apr 11;320(5873):201-5
pubmed: 18403705
PLoS One. 2015 Jun 15;10(6):e0129934
pubmed: 26076353
Sci Rep. 2016 Jun 10;6:27757
pubmed: 27282248
Neuron. 2015 Feb 18;85(4):787-803
pubmed: 25661182
PLoS One. 2014 May 22;9(5):e98274
pubmed: 24853857
J Neurosci. 2005 Nov 30;25(48):11194-200
pubmed: 16319319
Nature. 1995 Nov 2;378(6552):75-8
pubmed: 7477292
Prog Neurobiol. 1993 Aug;41(2):157-208
pubmed: 8332751
Cell. 1998 May 1;93(3):411-22
pubmed: 9590175
Nat Protoc. 2006;1(5):2452-6
pubmed: 17406491
Hippocampus. 1993 Jul;3(3):317-30
pubmed: 8353611
Hippocampus. 2009 Dec;19(12):1232-46
pubmed: 19280660
Learn Mem. 2007 Mar 09;14(3):214-23
pubmed: 17353546
Brain Res Bull. 2018 Jan;136:101-108
pubmed: 28284900
Curr Protoc Neurosci. 2004 May;Chapter 1:Unit 1.12
pubmed: 18428594
Neuroscience. 2009 May 5;160(2):484-91
pubmed: 19272425
Neural Plast. 2007;2007:73813
pubmed: 17502908
PLoS One. 2013 May 16;8(5):e63314
pubmed: 23696812
Science. 1993 Oct 29;262(5134):754-7
pubmed: 7901909
J Physiol. 2012 Aug 15;590(16):3953-64
pubmed: 22674722
J Cell Biol. 2008 Mar 10;180(5):1021-35
pubmed: 18332222
J Biol Chem. 2007 Jun 1;282(22):16036-41
pubmed: 17426029
Methods Enzymol. 1995;248:510-28
pubmed: 7674942
Front Integr Neurosci. 2017 Aug 02;11:16
pubmed: 28824389
Nature. 1993 Aug 19;364(6439):723-5
pubmed: 8355787
J Neurochem. 2006 Mar;96(5):1227-41
pubmed: 16464240
Nature. 1993 Dec 9;366(6455):569-72
pubmed: 7902955
J Neurochem. 2019 Mar;148(6):810-821
pubmed: 30697747
J Neurosci. 2012 May 2;32(18):6081-91
pubmed: 22553015
J Neurosci. 2006 Feb 15;26(7):1923-34
pubmed: 16481424
Neuron. 2012 Oct 4;76(1):116-29
pubmed: 23040810
Nat Protoc. 2006;1(3):1165-71
pubmed: 17406399
Learn Mem. 2005 Nov-Dec;12(6):587-93
pubmed: 16287724
J Neurophysiol. 2010 Apr;103(4):1748-57
pubmed: 20107127
Science. 1983 Sep 23;221(4617):1299-301
pubmed: 6612345