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Seasonal and Regional Differences in Gene Expression in the Brain of a Hibernating Mammal

Mammalian hibernation presents a unique opportunity to study naturally occurring neuroprotection. Hibernating ground squirrels undergo rapid and extreme physiological changes in body temperature, oxygen consumption, and heart rate without suffering neurological damage from ischemia and reperfusion i...

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Autores principales: Schwartz, Christine, Hampton, Marshall, Andrews, Matthew T.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2013
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3603966/
https://www.ncbi.nlm.nih.gov/pubmed/23526982
http://dx.doi.org/10.1371/journal.pone.0058427
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author Schwartz, Christine
Hampton, Marshall
Andrews, Matthew T.
author_facet Schwartz, Christine
Hampton, Marshall
Andrews, Matthew T.
author_sort Schwartz, Christine
collection PubMed
description Mammalian hibernation presents a unique opportunity to study naturally occurring neuroprotection. Hibernating ground squirrels undergo rapid and extreme physiological changes in body temperature, oxygen consumption, and heart rate without suffering neurological damage from ischemia and reperfusion injury. Different brain regions show markedly different activity during the torpor/arousal cycle: the cerebral cortex shows activity only during the periodic returns to normothermia, while the hypothalamus is active over the entire temperature range. Therefore, region-specific neuroprotective strategies must exist to permit this compartmentalized spectrum of activity. In this study, we use the Illumina HiSeq platform to compare the transcriptomes of these two brain regions at four collection points across the hibernation season: April Active, October Active, Torpor, and IBA. In the cerebral cortex, 1,085 genes were found to be differentially expressed across collection points, while 1,063 genes were differentially expressed in the hypothalamus. Comparison of these transcripts indicates that the cerebral cortex and hypothalamus implement very different strategies during hibernation, showing less than 20% of these differentially expressed genes in common. The cerebral cortex transcriptome shows evidence of remodeling and plasticity during hibernation, including transcripts for the presynaptic cytomatrix proteins bassoon and piccolo, and extracellular matrix components, including laminins and collagens. Conversely, the hypothalamic transcriptome displays upregulation of transcripts involved in damage response signaling and protein turnover during hibernation, including the DNA damage repair gene RAD50 and ubiquitin E3 ligases UBR1 and UBR5. Additionally, the hypothalamus transcriptome also provides evidence of potential mechanisms underlying the hibernation phenotype, including feeding and satiety signaling, seasonal timing mechanisms, and fuel utilization. This study provides insight into potential neuroprotective strategies and hibernation control mechanisms, and also specifically shows that the hibernator brain exhibits both seasonal and regional differences in mRNA expression.
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spelling pubmed-36039662013-03-22 Seasonal and Regional Differences in Gene Expression in the Brain of a Hibernating Mammal Schwartz, Christine Hampton, Marshall Andrews, Matthew T. PLoS One Research Article Mammalian hibernation presents a unique opportunity to study naturally occurring neuroprotection. Hibernating ground squirrels undergo rapid and extreme physiological changes in body temperature, oxygen consumption, and heart rate without suffering neurological damage from ischemia and reperfusion injury. Different brain regions show markedly different activity during the torpor/arousal cycle: the cerebral cortex shows activity only during the periodic returns to normothermia, while the hypothalamus is active over the entire temperature range. Therefore, region-specific neuroprotective strategies must exist to permit this compartmentalized spectrum of activity. In this study, we use the Illumina HiSeq platform to compare the transcriptomes of these two brain regions at four collection points across the hibernation season: April Active, October Active, Torpor, and IBA. In the cerebral cortex, 1,085 genes were found to be differentially expressed across collection points, while 1,063 genes were differentially expressed in the hypothalamus. Comparison of these transcripts indicates that the cerebral cortex and hypothalamus implement very different strategies during hibernation, showing less than 20% of these differentially expressed genes in common. The cerebral cortex transcriptome shows evidence of remodeling and plasticity during hibernation, including transcripts for the presynaptic cytomatrix proteins bassoon and piccolo, and extracellular matrix components, including laminins and collagens. Conversely, the hypothalamic transcriptome displays upregulation of transcripts involved in damage response signaling and protein turnover during hibernation, including the DNA damage repair gene RAD50 and ubiquitin E3 ligases UBR1 and UBR5. Additionally, the hypothalamus transcriptome also provides evidence of potential mechanisms underlying the hibernation phenotype, including feeding and satiety signaling, seasonal timing mechanisms, and fuel utilization. This study provides insight into potential neuroprotective strategies and hibernation control mechanisms, and also specifically shows that the hibernator brain exhibits both seasonal and regional differences in mRNA expression. Public Library of Science 2013-03-20 /pmc/articles/PMC3603966/ /pubmed/23526982 http://dx.doi.org/10.1371/journal.pone.0058427 Text en © 2013 Schwartz et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Schwartz, Christine
Hampton, Marshall
Andrews, Matthew T.
Seasonal and Regional Differences in Gene Expression in the Brain of a Hibernating Mammal
title Seasonal and Regional Differences in Gene Expression in the Brain of a Hibernating Mammal
title_full Seasonal and Regional Differences in Gene Expression in the Brain of a Hibernating Mammal
title_fullStr Seasonal and Regional Differences in Gene Expression in the Brain of a Hibernating Mammal
title_full_unstemmed Seasonal and Regional Differences in Gene Expression in the Brain of a Hibernating Mammal
title_short Seasonal and Regional Differences in Gene Expression in the Brain of a Hibernating Mammal
title_sort seasonal and regional differences in gene expression in the brain of a hibernating mammal
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3603966/
https://www.ncbi.nlm.nih.gov/pubmed/23526982
http://dx.doi.org/10.1371/journal.pone.0058427
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