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DOI10.1073/pnas.2108534118
Hippocampal neurons' cytosolic and membrane-bound ribosomal transcript profiles are differentially regulated by learning and subsequent sleep
Delorme J.; Wang L.; Kodoth V.; Wang Y.; Ma J.; Jiang S.; Aton S.J.
发表日期2021
ISSN0027-8424
卷号118期号:48
英文摘要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. © 2021 National Academy of Sciences. All rights reserved.
英文关键词Bioinformatics; Memory consolidation; Ribosomes; Synaptic plasticity; Translation
语种英语
scopus关键词long untranslated RNA; messenger RNA; membrane protein; transcriptome; animal cell; animal tissue; Article; binding affinity; brain nerve cell; cell membrane; cell metabolism; cell population; controlled study; cytoskeleton; cytosol; hippocampus; learning; memory consolidation; mouse; nerve cell plasticity; nonhuman; protein phosphorylation; protein synthesis; ribosome; signal transduction; sleep; transcription regulation; animal; C57BL mouse; cytosol; fear; female; gene expression; gene expression regulation; genetics; hippocampus; learning; male; memory; metabolism; nerve cell; pathophysiology; physiology; ribosome; sleep; sleep deprivation; Animals; Cytosol; Fear; Female; Gene Expression; Gene Expression Regulation; Hippocampus; Learning; Male; Membrane Proteins; Memory; Memory Consolidation; Mice; Mice, Inbred C57BL; Neuronal Plasticity; Neurons; Protein Biosynthesis; Ribosomes; Sleep; Sleep Deprivation; Transcriptome
来源期刊Proceedings of the National Academy of Sciences of the United States of America
文献类型期刊论文
条目标识符http://gcip.llas.ac.cn/handle/2XKMVOVA/250969
作者单位Department of Molecular, Cellular, and Developmental Biology, University of Michigan, Ann Arbor, MI 48019, United States; Department of Computational Medicine and Bioinformatics, University of Michigan, Ann Arbor, MI 48019, United States; Bioinformatics Core, Biomedical Research Core Facilities, University of Michigan, Ann Arbor, MI 48019, United States
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Delorme J.,Wang L.,Kodoth V.,et al. Hippocampal neurons' cytosolic and membrane-bound ribosomal transcript profiles are differentially regulated by learning and subsequent sleep[J],2021,118(48).
APA Delorme J..,Wang L..,Kodoth V..,Wang Y..,Ma J..,...&Aton S.J..(2021).Hippocampal neurons' cytosolic and membrane-bound ribosomal transcript profiles are differentially regulated by learning and subsequent sleep.Proceedings of the National Academy of Sciences of the United States of America,118(48).
MLA Delorme J.,et al."Hippocampal neurons' cytosolic and membrane-bound ribosomal transcript profiles are differentially regulated by learning and subsequent sleep".Proceedings of the National Academy of Sciences of the United States of America 118.48(2021).
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