Hippocampal neurons' cytosolic and membrane-bound ribosomal transcript profiles are differentially regulated by learning and subsequent sleep.
Animals
Cytosol
/ metabolism
Fear
/ physiology
Female
Gene Expression
/ genetics
Gene Expression Regulation
/ genetics
Hippocampus
/ metabolism
Learning
/ physiology
Male
Membrane Proteins
/ genetics
Memory
/ physiology
Memory Consolidation
/ physiology
Mice
Mice, Inbred C57BL
Neuronal Plasticity
/ physiology
Neurons
/ metabolism
Protein Biosynthesis
/ genetics
Ribosomes
/ metabolism
Sleep
/ genetics
Sleep Deprivation
/ physiopathology
Transcriptome
/ genetics
bioinformatics
memory consolidation
ribosomes
synaptic plasticity
translation
Journal
Proceedings of the National Academy of Sciences of the United States of America
ISSN: 1091-6490
Titre abrégé: Proc Natl Acad Sci U S A
Pays: United States
ID NLM: 7505876
Informations de publication
Date de publication:
30 11 2021
30 11 2021
Historique:
accepted:
08
10
2021
entrez:
25
11
2021
pubmed:
26
11
2021
medline:
15
1
2022
Statut:
ppublish
Résumé
The hippocampus is essential for consolidating transient experiences into long-lasting memories. Memory consolidation is facilitated by postlearning sleep, although the underlying cellular mechanisms are largely unknown. We took an unbiased approach to this question by using a mouse model of hippocampally mediated, sleep-dependent memory consolidation (contextual fear memory). Because synaptic plasticity is associated with changes to both neuronal cell membranes (e.g., receptors) and cytosol (e.g., cytoskeletal elements), we characterized how these cell compartments are affected by learning and subsequent sleep or sleep deprivation (SD). Translating ribosome affinity purification was used to profile ribosome-associated RNAs in different subcellular compartments (cytosol and membrane) and in different cell populations (whole hippocampus, Camk2a+ neurons, or highly active neurons with phosphorylated ribosomal subunit S6 [pS6+]). We examined how transcript profiles change as a function of sleep versus SD and prior learning (contextual fear conditioning; CFC). While sleep loss altered many cytosolic ribosomal transcripts, CFC altered almost none, and CFC-driven changes were occluded by subsequent SD. In striking contrast, SD altered few transcripts on membrane-bound (MB) ribosomes, while learning altered many more (including long non-coding RNAs [lncRNAs]). The cellular pathways most affected by CFC were involved in structural remodeling. Comparisons of post-CFC MB transcript profiles between sleeping and SD mice implicated changes in cellular metabolism in Camk2a+ neurons and protein synthesis in highly active pS6+ (putative "engram") neurons as biological processes disrupted by SD. These findings provide insights into how learning affects hippocampal neurons and suggest that the effects of SD on memory consolidation are cell type and subcellular compartment specific.
Identifiants
pubmed: 34819370
pii: 2108534118
doi: 10.1073/pnas.2108534118
pmc: PMC8640746
pii:
doi:
Substances chimiques
Membrane Proteins
0
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : NIMH NIH HHS
ID : DP2 MH104119
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS118440
Pays : United States
Organisme : NINDS NIH HHS
ID : RF1 NS118440
Pays : United States
Informations de copyright
Copyright © 2021 the Author(s). Published by PNAS.
Déclaration de conflit d'intérêts
The authors declare no competing interest.
Références
Learn Mem. 2003 May-Jun;10(3):168-76
pubmed: 12773581
Elife. 2016 Aug 23;5:
pubmed: 27549340
Mol Brain. 2021 Aug 12;14(1):125
pubmed: 34384474
Eur Cytokine Netw. 2014 Jul-Sep;25(3):52-7
pubmed: 25373853
Methods Mol Biol. 2018;1649:85-94
pubmed: 29130191
Arch Ital Biol. 2009 Sep;147(3):59-68
pubmed: 20014652
Front Mol Neurosci. 2015 Dec 16;8:75
pubmed: 26733799
Nat Commun. 2019 May 20;10(1):2232
pubmed: 31110186
Proc Natl Acad Sci U S A. 2021 Aug 10;118(32):
pubmed: 34344824
Front Behav Neurosci. 2017 Nov 29;11:239
pubmed: 29238297
Science. 2019 Oct 11;366(6462):
pubmed: 31601740
Bioinformatics. 2014 Apr 1;30(7):923-30
pubmed: 24227677
Science. 2006 Aug 25;313(5790):1093-7
pubmed: 16931756
Learn Mem. 1998 Sep-Oct;5(4-5):365-74
pubmed: 10454361
Learn Mem. 2005 Jul-Aug;12(4):375-82
pubmed: 16027176
Physiol Genomics. 2010 Aug;42(3):427-36
pubmed: 20501693
Curr Opin Neurobiol. 2017 Jun;44:13-19
pubmed: 28242433
Front Neural Circuits. 2021 Sep 13;15:750541
pubmed: 34588960
Physiol Rev. 2013 Apr;93(2):681-766
pubmed: 23589831
Curr Protoc Neurosci. 2019 Jun;88(1):e77
pubmed: 31216392
Nat Commun. 2017 Apr 06;8:15039
pubmed: 28382952
J Neurochem. 2005 Mar;92(5):1150-7
pubmed: 15715665
Cell. 2014 Mar 27;157(1):163-86
pubmed: 24679534
Nature. 1997 Mar 20;386(6622):284-8
pubmed: 9069287
Genome Biol. 2014;15(12):550
pubmed: 25516281
Physiol Genomics. 2012 Oct 17;44(20):981-91
pubmed: 22930738
Elife. 2019 Dec 11;8:
pubmed: 31825308
Neuron. 2007 Jan 18;53(2):261-77
pubmed: 17224407
Brain Res Bull. 2003 Dec 15;62(2):143-50
pubmed: 14638388
Learn Mem. 2018 Apr 16;25(5):214-229
pubmed: 29661834
Mol Brain. 2020 Dec 3;13(1):165
pubmed: 33272296
Cereb Cortex. 2018 Oct 1;28(10):3711-3723
pubmed: 30060138
Sleep. 2019 Jul 8;42(7):
pubmed: 31100149
Bioinformatics. 2014 Feb 15;30(4):523-30
pubmed: 24336805
Proc Natl Acad Sci U S A. 2017 Sep 26;114(39):10485-10490
pubmed: 28893999
Neuron. 2014 Jan 8;81(1):12-34
pubmed: 24411729
Genome Biol. 2003;4(5):P3
pubmed: 12734009
Elife. 2017 Sep 29;6:
pubmed: 28960176
Nature. 2009 Oct 22;461(7267):1122-5
pubmed: 19847264
J Neurosci. 2021 Jun 23;41(25):5386-5398
pubmed: 34001629
Biochem J. 1971 Oct;124(5):883-9
pubmed: 5131012
Trends Neurosci. 2013 Nov;36(11):641-51
pubmed: 24035135
Mol Brain. 2012 May 14;5:14
pubmed: 22583753
Neurobiol Learn Mem. 2016 Oct;134 Pt B:221-35
pubmed: 27451143
Science. 2019 Oct 11;366(6462):
pubmed: 31601739
Nat Neurosci. 2015 Oct;18(10):1446-54
pubmed: 26322927
Neuroscience. 2011 May 19;182:98-104
pubmed: 21439355
RNA Dis. 2016;3(2):
pubmed: 27713923
Neuron. 2004 Sep 30;44(1):59-73
pubmed: 15450160
Physiol Genomics. 2008 Mar 14;33(1):91-9
pubmed: 18171722
Nat Rev Mol Cell Biol. 2015 Apr;16(4):221-31
pubmed: 25735911
Front Syst Neurosci. 2014 Apr 17;8:61
pubmed: 24860440
J Neurosci. 2007 Jun 6;27(23):6128-40
pubmed: 17553985
Science. 2015 Oct 2;350(6256):82-7
pubmed: 26430118
Genome Biol. 2018 Apr 12;19(1):53
pubmed: 29650040
Genome Res. 2014 Aug;24(8):1396-410
pubmed: 24904046
Brain Res Mol Brain Res. 2004 Dec 20;132(2):146-54
pubmed: 15582154
Mol Neurobiol. 2019 Aug;56(8):5507-5519
pubmed: 30623374
Learn Mem. 2016 May 18;23(6):255-69
pubmed: 27194793
Science. 2016 May 13;352(6287):812-6
pubmed: 27174984
Nat Rev Neurosci. 2017 Jul;18(7):404-418
pubmed: 28515433
Neuron. 2004 Jan 8;41(1):35-43
pubmed: 14715133
Neurobiol Learn Mem. 2019 Apr;160:83-90
pubmed: 29588221
Proc Natl Acad Sci U S A. 2010 Jan 5;107(1):349-54
pubmed: 20018662
Front Neural Circuits. 2017 Sep 06;11:61
pubmed: 28932187
Cell Rep. 2017 Jul 11;20(2):344-355
pubmed: 28700937
Nat Commun. 2021 Feb 22;12(1):1200
pubmed: 33619256
Trends Neurosci. 2020 Jun;43(6):385-393
pubmed: 32459991
Sci Signal. 2016 Apr 26;9(425):ra41
pubmed: 27117251
Mol Neuropsychiatry. 2019 Jun;5(3):147-161
pubmed: 31312636
Neurobiol Learn Mem. 2019 Apr;160:73-82
pubmed: 29635031
Proc Natl Acad Sci U S A. 2007 Dec 11;104(50):20090-5
pubmed: 18077435
Proc Natl Acad Sci U S A. 2009 Aug 18;106(33):13939-44
pubmed: 19666516
Proteome Sci. 2008 May 22;6:14
pubmed: 18498662
J Neurosci. 2019 Aug 21;39(34):6613-6625
pubmed: 31263066
PLoS One. 2016 Sep 29;11(9):e0163500
pubmed: 27684481
J Biol Chem. 2011 Mar 11;286(10):8688-8696
pubmed: 21233202
Cell. 2012 Nov 21;151(5):1126-37
pubmed: 23178128
Science. 2009 May 15;324(5929):904-9
pubmed: 19443779
J Neurosci. 2015 Oct 7;35(40):13773-83
pubmed: 26446228
Brief Bioinform. 2019 Nov 27;20(6):2044-2054
pubmed: 30099484
Proc Natl Acad Sci U S A. 2018 Mar 27;115(13):E3017-E3025
pubmed: 29545273
Neuropharmacology. 2009 Sep;57(4):369-74
pubmed: 19615388
Cell. 1997 Mar 7;88(5):615-26
pubmed: 9054501
J Neurosci. 2002 Aug 1;22(15):6781-9
pubmed: 12151558
Physiol Genomics. 2007 Nov 14;31(3):441-57
pubmed: 17698924
J Neurosci. 2013 Apr 10;33(15):6460-8
pubmed: 23575844