Cargando…

The Effect of Sleep Deprivation and Subsequent Recovery Period on the Synaptic Proteome of Rat Cerebral Cortex

Sleep deprivation (SD) is commonplace in the modern way of life and has a substantial social, medical, and human cost. Sleep deprivation induces cognitive impairment such as loss of executive attention, working memory decline, poor emotion regulation, increased reaction times, and higher cognitive f...

Descripción completa

Detalles Bibliográficos
Autores principales: Gulyássy, Péter, Todorov-Völgyi, Katalin, Tóth, Vilmos, Györffy, Balázs A., Puska, Gina, Simor, Attila, Juhász, Gábor, Drahos, László, Kékesi, Katalin Adrienna
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Springer US 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8857111/
https://www.ncbi.nlm.nih.gov/pubmed/34988919
http://dx.doi.org/10.1007/s12035-021-02699-x
_version_ 1784653974016622592
author Gulyássy, Péter
Todorov-Völgyi, Katalin
Tóth, Vilmos
Györffy, Balázs A.
Puska, Gina
Simor, Attila
Juhász, Gábor
Drahos, László
Kékesi, Katalin Adrienna
author_facet Gulyássy, Péter
Todorov-Völgyi, Katalin
Tóth, Vilmos
Györffy, Balázs A.
Puska, Gina
Simor, Attila
Juhász, Gábor
Drahos, László
Kékesi, Katalin Adrienna
author_sort Gulyássy, Péter
collection PubMed
description Sleep deprivation (SD) is commonplace in the modern way of life and has a substantial social, medical, and human cost. Sleep deprivation induces cognitive impairment such as loss of executive attention, working memory decline, poor emotion regulation, increased reaction times, and higher cognitive functions are particularly vulnerable to sleep loss. Furthermore, SD is associated with obesity, diabetes, cardiovascular diseases, cancer, and a vast majority of psychiatric and neurodegenerative disorders are accompanied by sleep disturbances. Despite the widespread scientific interest in the effect of sleep loss on synaptic function, there is a lack of investigation focusing on synaptic transmission on the proteome level. In the present study, we report the effects of SD and recovery period (RP) on the cortical synaptic proteome in rats. Synaptosomes were isolated after 8 h of SD performed by gentle handling and after 16 h of RP. The purity of synaptosome fraction was validated with western blot and electron microscopy, and the protein abundance alterations were analyzed by mass spectrometry. We observed that SD and RP have a wide impact on neurotransmitter-related proteins at both the presynaptic and postsynaptic membranes. The abundance of synaptic proteins has changed to a greater extent in consequence of SD than during RP: we identified 78 proteins with altered abundance after SD and 39 proteins after the course of RP. Levels of most of the altered proteins were upregulated during SD, while RP showed the opposite tendency, and three proteins (Gabbr1, Anks1b, and Decr1) showed abundance changes with opposite direction after SD and RP. The functional cluster analysis revealed that a majority of the altered proteins is related to signal transduction and regulation, synaptic transmission and synaptic assembly, protein and ion transport, and lipid and fatty acid metabolism, while the interaction network analysis revealed several connections between the significantly altered proteins and the molecular processes of synaptic plasticity or sleep. Our proteomic data implies suppression of SNARE-mediated synaptic vesicle exocytosis and impaired endocytic processes after sleep deprivation. Both SD and RP altered GABA neurotransmission and affected protein synthesis, several regulatory processes and signaling pathways, energy homeostatic processes, and metabolic pathways. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s12035-021-02699-x.
format Online
Article
Text
id pubmed-8857111
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher Springer US
record_format MEDLINE/PubMed
spelling pubmed-88571112022-02-23 The Effect of Sleep Deprivation and Subsequent Recovery Period on the Synaptic Proteome of Rat Cerebral Cortex Gulyássy, Péter Todorov-Völgyi, Katalin Tóth, Vilmos Györffy, Balázs A. Puska, Gina Simor, Attila Juhász, Gábor Drahos, László Kékesi, Katalin Adrienna Mol Neurobiol Article Sleep deprivation (SD) is commonplace in the modern way of life and has a substantial social, medical, and human cost. Sleep deprivation induces cognitive impairment such as loss of executive attention, working memory decline, poor emotion regulation, increased reaction times, and higher cognitive functions are particularly vulnerable to sleep loss. Furthermore, SD is associated with obesity, diabetes, cardiovascular diseases, cancer, and a vast majority of psychiatric and neurodegenerative disorders are accompanied by sleep disturbances. Despite the widespread scientific interest in the effect of sleep loss on synaptic function, there is a lack of investigation focusing on synaptic transmission on the proteome level. In the present study, we report the effects of SD and recovery period (RP) on the cortical synaptic proteome in rats. Synaptosomes were isolated after 8 h of SD performed by gentle handling and after 16 h of RP. The purity of synaptosome fraction was validated with western blot and electron microscopy, and the protein abundance alterations were analyzed by mass spectrometry. We observed that SD and RP have a wide impact on neurotransmitter-related proteins at both the presynaptic and postsynaptic membranes. The abundance of synaptic proteins has changed to a greater extent in consequence of SD than during RP: we identified 78 proteins with altered abundance after SD and 39 proteins after the course of RP. Levels of most of the altered proteins were upregulated during SD, while RP showed the opposite tendency, and three proteins (Gabbr1, Anks1b, and Decr1) showed abundance changes with opposite direction after SD and RP. The functional cluster analysis revealed that a majority of the altered proteins is related to signal transduction and regulation, synaptic transmission and synaptic assembly, protein and ion transport, and lipid and fatty acid metabolism, while the interaction network analysis revealed several connections between the significantly altered proteins and the molecular processes of synaptic plasticity or sleep. Our proteomic data implies suppression of SNARE-mediated synaptic vesicle exocytosis and impaired endocytic processes after sleep deprivation. Both SD and RP altered GABA neurotransmission and affected protein synthesis, several regulatory processes and signaling pathways, energy homeostatic processes, and metabolic pathways. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s12035-021-02699-x. Springer US 2022-01-05 2022 /pmc/articles/PMC8857111/ /pubmed/34988919 http://dx.doi.org/10.1007/s12035-021-02699-x Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Gulyássy, Péter
Todorov-Völgyi, Katalin
Tóth, Vilmos
Györffy, Balázs A.
Puska, Gina
Simor, Attila
Juhász, Gábor
Drahos, László
Kékesi, Katalin Adrienna
The Effect of Sleep Deprivation and Subsequent Recovery Period on the Synaptic Proteome of Rat Cerebral Cortex
title The Effect of Sleep Deprivation and Subsequent Recovery Period on the Synaptic Proteome of Rat Cerebral Cortex
title_full The Effect of Sleep Deprivation and Subsequent Recovery Period on the Synaptic Proteome of Rat Cerebral Cortex
title_fullStr The Effect of Sleep Deprivation and Subsequent Recovery Period on the Synaptic Proteome of Rat Cerebral Cortex
title_full_unstemmed The Effect of Sleep Deprivation and Subsequent Recovery Period on the Synaptic Proteome of Rat Cerebral Cortex
title_short The Effect of Sleep Deprivation and Subsequent Recovery Period on the Synaptic Proteome of Rat Cerebral Cortex
title_sort effect of sleep deprivation and subsequent recovery period on the synaptic proteome of rat cerebral cortex
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8857111/
https://www.ncbi.nlm.nih.gov/pubmed/34988919
http://dx.doi.org/10.1007/s12035-021-02699-x
work_keys_str_mv AT gulyassypeter theeffectofsleepdeprivationandsubsequentrecoveryperiodonthesynapticproteomeofratcerebralcortex
AT todorovvolgyikatalin theeffectofsleepdeprivationandsubsequentrecoveryperiodonthesynapticproteomeofratcerebralcortex
AT tothvilmos theeffectofsleepdeprivationandsubsequentrecoveryperiodonthesynapticproteomeofratcerebralcortex
AT gyorffybalazsa theeffectofsleepdeprivationandsubsequentrecoveryperiodonthesynapticproteomeofratcerebralcortex
AT puskagina theeffectofsleepdeprivationandsubsequentrecoveryperiodonthesynapticproteomeofratcerebralcortex
AT simorattila theeffectofsleepdeprivationandsubsequentrecoveryperiodonthesynapticproteomeofratcerebralcortex
AT juhaszgabor theeffectofsleepdeprivationandsubsequentrecoveryperiodonthesynapticproteomeofratcerebralcortex
AT drahoslaszlo theeffectofsleepdeprivationandsubsequentrecoveryperiodonthesynapticproteomeofratcerebralcortex
AT kekesikatalinadrienna theeffectofsleepdeprivationandsubsequentrecoveryperiodonthesynapticproteomeofratcerebralcortex
AT gulyassypeter effectofsleepdeprivationandsubsequentrecoveryperiodonthesynapticproteomeofratcerebralcortex
AT todorovvolgyikatalin effectofsleepdeprivationandsubsequentrecoveryperiodonthesynapticproteomeofratcerebralcortex
AT tothvilmos effectofsleepdeprivationandsubsequentrecoveryperiodonthesynapticproteomeofratcerebralcortex
AT gyorffybalazsa effectofsleepdeprivationandsubsequentrecoveryperiodonthesynapticproteomeofratcerebralcortex
AT puskagina effectofsleepdeprivationandsubsequentrecoveryperiodonthesynapticproteomeofratcerebralcortex
AT simorattila effectofsleepdeprivationandsubsequentrecoveryperiodonthesynapticproteomeofratcerebralcortex
AT juhaszgabor effectofsleepdeprivationandsubsequentrecoveryperiodonthesynapticproteomeofratcerebralcortex
AT drahoslaszlo effectofsleepdeprivationandsubsequentrecoveryperiodonthesynapticproteomeofratcerebralcortex
AT kekesikatalinadrienna effectofsleepdeprivationandsubsequentrecoveryperiodonthesynapticproteomeofratcerebralcortex