Concerted roles of LRRTM1 and SynCAM 1 in organizing prefrontal cortex synapses and cognitive functions.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
28 01 2023
28 01 2023
Historique:
received:
29
09
2020
accepted:
13
01
2023
pubmed:
29
1
2023
medline:
1
2
2023
entrez:
28
1
2023
Statut:
epublish
Résumé
Multiple trans-synaptic complexes organize synapse development, yet their roles in the mature brain and cooperation remain unclear. We analyzed the postsynaptic adhesion protein LRRTM1 in the prefrontal cortex (PFC), a region relevant to cognition and disorders. LRRTM1 knockout (KO) mice had fewer synapses, and we asked whether other synapse organizers counteract further loss. This determined that the immunoglobulin family member SynCAM 1 controls synapse number in PFC and was upregulated upon LRRTM1 loss. Combined LRRTM1 and SynCAM 1 deletion substantially lowered dendritic spine number in PFC, but not hippocampus, more than the sum of single KO impairments. Their cooperation extended presynaptically, and puncta of Neurexins, LRRTM1 partners, were less abundant in double KO (DKO) PFC. Electrophysiology and fMRI demonstrated aberrant neuronal activity in DKO mice. Further, DKO mice were impaired in social interactions and cognitive tasks. Our results reveal concerted roles of LRRTM1 and SynCAM 1 across synaptic, network, and behavioral domains.
Identifiants
pubmed: 36709330
doi: 10.1038/s41467-023-36042-w
pii: 10.1038/s41467-023-36042-w
pmc: PMC9884278
doi:
Substances chimiques
LRRTM1 protein, mouse
0
Membrane Proteins
0
Nerve Tissue Proteins
0
Cadm1 protein, mouse
0
Cell Adhesion Molecule-1
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
459Subventions
Organisme : NEI NIH HHS
ID : P30 EY026878
Pays : United States
Organisme : NIA NIH HHS
ID : R01 AG066165
Pays : United States
Organisme : NIDA NIH HHS
ID : R01 DA018928
Pays : United States
Organisme : NCATS NIH HHS
ID : UL1 TR001863
Pays : United States
Organisme : NINDS NIH HHS
ID : P30 NS052519
Pays : United States
Organisme : NIA NIH HHS
ID : P30 AG066508
Pays : United States
Organisme : NIA NIH HHS
ID : RF1 AG070926
Pays : United States
Organisme : NINDS NIH HHS
ID : R35 NS097283
Pays : United States
Informations de copyright
© 2023. The Author(s).
Références
Cell. 2020 Jul 23;182(2):329-344.e19
pubmed: 32589946
Structure. 2019 Jun 4;27(6):893-906.e9
pubmed: 30956130
Mol Psychiatry. 2009 Aug;14(8):743-5
pubmed: 19626025
Cell. 1995 May 5;81(3):435-43
pubmed: 7736595
Neuron. 2009 Mar 12;61(5):734-49
pubmed: 19285470
Behav Brain Res. 2013 Feb 1;238:69-78
pubmed: 23089646
J Neurosci. 2007 Nov 14;27(46):12516-30
pubmed: 18003830
Proc Natl Acad Sci U S A. 2010 Jun 15;107(24):11116-21
pubmed: 20534458
Proc Natl Acad Sci U S A. 2014 May 20;111(20):7438-43
pubmed: 24799682
Science. 2002 Aug 30;297(5586):1525-31
pubmed: 12202822
Psychopharmacology (Berl). 1987;92(2):180-5
pubmed: 3110839
Science. 2004 Jul 2;305(5680):96-9
pubmed: 15232109
Neuron. 2007 Oct 4;56(1):43-57
pubmed: 17920014
Cereb Cortex. 2020 Jan 10;30(1):226-240
pubmed: 31034037
J Cell Biol. 2019 Aug 5;218(8):2677-2698
pubmed: 31262725
Cell. 2016 Aug 25;166(5):1295-1307.e21
pubmed: 27565350
Am J Med Genet B Neuropsychiatr Genet. 2014 Oct;165B(7):555-63
pubmed: 25111784
J Neurophysiol. 1985 Oct;54(4):782-806
pubmed: 2999347
Nature. 2014 Feb 13;506(7487):179-84
pubmed: 24463507
Cell. 2017 Nov 2;171(4):745-769
pubmed: 29100073
Front Mol Neurosci. 2018 Apr 30;11:142
pubmed: 29760652
J Comp Neurol. 1985 Nov 15;241(3):253-67
pubmed: 2418068
Neuroimage. 2009 Feb 1;44(3):893-905
pubmed: 18976716
Neuron. 2012 Dec 20;76(6):1057-70
pubmed: 23259943
Elife. 2022 Jun 06;11:
pubmed: 35662394
Neuron. 2009 Dec 24;64(6):799-806
pubmed: 20064388
Neuron. 2009 Dec 24;64(6):791-8
pubmed: 20064387
J Neurosci. 2010 Jun 2;30(22):7495-506
pubmed: 20519524
Neuron. 2020 Apr 8;106(1):108-125.e12
pubmed: 31995730
J Hum Genet. 2014 Jun;59(6):332-6
pubmed: 24785688
Cell. 2013 Jul 3;154(1):75-88
pubmed: 23827676
Proteomes. 2018 Nov 28;6(4):
pubmed: 30487426
Neuron. 2012 Sep 20;75(6):963-80
pubmed: 22998866
Psychiatry Res. 2007 Mar 30;150(2):111-21
pubmed: 17292970
NMR Biomed. 2008 May;21(4):410-6
pubmed: 18435491
Proc Natl Acad Sci U S A. 2011 Oct 4;108(40):16502-9
pubmed: 21953696
Front Psychol. 2015 Nov 26;6:1805
pubmed: 26635701
Nature. 2022 Apr;604(7906):502-508
pubmed: 35396580
Curr Top Dev Biol. 2021;142:319-370
pubmed: 33706921
Arch Gen Psychiatry. 2000 Jan;57(1):65-73
pubmed: 10632234
Cell Rep. 2022 Apr 5;39(1):110624
pubmed: 35385735
Proc Natl Acad Sci U S A. 2010 Apr 20;107(16):7568-73
pubmed: 20368431
Annu Rev Cell Dev Biol. 2014;30:417-37
pubmed: 25150010
Nat Neurosci. 2011 Mar;14(3):285-93
pubmed: 21346746
NMR Biomed. 2014 Aug;27(8):897-906
pubmed: 24839167
Mol Psychiatry. 2007 Dec;12(12):1129-39, 1057
pubmed: 17667961
J Neurosci. 2016 Jun 29;36(26):6926-36
pubmed: 27358451
Nature. 2014 Jul 24;511(7510):421-7
pubmed: 25056061
Neurotox Res. 2008 Oct;14(2-3):249-62
pubmed: 19073430
J Neurosci. 2016 Jul 13;36(28):7464-75
pubmed: 27413156
Genes Brain Behav. 2021 Mar;20(3):e12696
pubmed: 32808443
Schizophr Bull. 2021 Jan 23;47(1):31-43
pubmed: 32621612
Dialogues Clin Neurosci. 2006;8(1):9-16
pubmed: 16640109
J Cell Biol. 2011 Jul 25;194(2):323-34
pubmed: 21788371
Neuroimage. 2014 Nov 15;102 Pt 2:838-47
pubmed: 25175535
Nat Rev Neurosci. 2016 Jan;17(1):22-35
pubmed: 26656254
Curr Protoc Neurosci. 2001 May;Chapter 8:Unit 8.7
pubmed: 18428548
Neuron. 2018 Jul 25;99(2):329-344.e7
pubmed: 29983322
eNeuro. 2017 Dec 06;4(6):
pubmed: 29218324
Psychopharmacology (Berl). 2001 Jul;156(2-3):194-215
pubmed: 11549223
J Neurosci. 2005 Feb 23;25(8):2138-45
pubmed: 15728854
Genes Brain Behav. 2004 Oct;3(5):303-14
pubmed: 15344923
Nat Commun. 2016 Mar 16;7:10773
pubmed: 26979420
Mol Cell Biol. 2006 Jan;26(2):718-26
pubmed: 16382161
Brain Res. 1967 Dec;6(4):716-27
pubmed: 4169903
Proc Natl Acad Sci U S A. 2011 Apr 5;108(14):5475-6
pubmed: 21441108
J Neurol Neurosurg Psychiatry. 1998 Oct;65(4):446-53
pubmed: 9771764
Brain Connect. 2016 Jul;6(6):435-47
pubmed: 27029438
Stress. 2018 Sep;21(5):443-452
pubmed: 29451062
Trends Neurosci. 2008 Dec;31(12):599-608
pubmed: 18835649
Neuron. 2017 Nov 15;96(4):808-826.e8
pubmed: 29107521
Neuron. 2010 Dec 9;68(5):894-906
pubmed: 21145003
Neuron. 2012 Oct 4;76(1):223-39
pubmed: 23040817
Cell Rep. 2019 Jan 8;26(2):381-393.e6
pubmed: 30625321
Nature. 2008 Oct 16;455(7215):903-11
pubmed: 18923512
Genes Brain Behav. 2004 Oct;3(5):287-302
pubmed: 15344922
Neuron. 2010 Feb 25;65(4):472-9
pubmed: 20188652
Neuropsychopharmacology. 2013 Mar;38(4):628-38
pubmed: 23169347
J Neurosci. 1992 Jul;12(7):2685-705
pubmed: 1613552
Neuron. 2015 Dec 16;88(6):1165-1172
pubmed: 26687224
Neuron. 2017 May 3;94(3):611-625.e4
pubmed: 28472659
Brain Res Brain Res Rev. 2002 Jun;39(1):29-54
pubmed: 12086707
Cell Rep. 2021 Jun 15;35(11):109266
pubmed: 34133920
Neuron. 2022 Oct 5;110(19):3168-3185.e8
pubmed: 36007521
Mol Psychiatry. 2005 Jan;10(1):40-68; image 5
pubmed: 15263907
Schizophr Res. 2013 May;146(1-3):201-8
pubmed: 23490758
Biol Psychiatry. 2017 May 15;81(10):862-873
pubmed: 27455897
J Neurosci. 2008 Nov 26;28(48):12969-81
pubmed: 19036990
J Neurophysiol. 2009 Jun;101(6):3270-83
pubmed: 19339462
Neuroimage. 2012 Feb 1;59(3):2142-54
pubmed: 22019881
PLoS One. 2011;6(7):e22716
pubmed: 21818371
Proc Natl Acad Sci U S A. 2010 Jun 1;107(22):10238-43
pubmed: 20439733
J Comp Neurol. 1996 Sep 23;373(3):340-54
pubmed: 8889932
Magn Reson Imaging. 1995;13(1):97-103
pubmed: 7898286
Biochim Biophys Acta. 1974 Aug 9;356(3):276-87
pubmed: 4367725
Curr Opin Neurobiol. 2019 Aug;57:126-133
pubmed: 30826628
Neuron. 2015 Aug 19;87(4):764-80
pubmed: 26291160
J Neurophysiol. 2004 Jul;92(1):600-8
pubmed: 15056678
Mol Psychiatry. 2021 Nov;26(11):6912-6925
pubmed: 33981006
Nature. 2013 Dec 12;504(7479):272-6
pubmed: 24336286
eNeuro. 2018 Oct 25;5(5):
pubmed: 30406193
Neuron. 2018 Oct 24;100(2):276-293
pubmed: 30359597
J Neurosci. 2015 Oct 07;35(40):13629-47
pubmed: 26446217