When the brain goes diving: transcriptome analysis reveals a reduced aerobic energy metabolism and increased stress proteins in the seal brain

Abstract Background During long dives, the brain of whales and seals experiences a reduced supply of oxygen (hypoxia). The brain neurons of the hooded seal (Cystophora cristata) are more tolerant towards low-oxygen conditions than those of mice, and also better survive other hypoxia-related stress c...

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Main Authors: Fabrizius, Andrej, Hoff, Mariana, Engler, Gerhard, Folkow, Lars, Burmester, Thorsten
Format: Article in Journal/Newspaper
Language:unknown
Published: Figshare 2016
Subjects:
Online Access:https://dx.doi.org/10.6084/m9.figshare.c.3636611
https://figshare.com/collections/When_the_brain_goes_diving_transcriptome_analysis_reveals_a_reduced_aerobic_energy_metabolism_and_increased_stress_proteins_in_the_seal_brain/3636611
id ftdatacite:10.6084/m9.figshare.c.3636611
record_format openpolar
spelling ftdatacite:10.6084/m9.figshare.c.3636611 2023-05-15T15:59:54+02:00 When the brain goes diving: transcriptome analysis reveals a reduced aerobic energy metabolism and increased stress proteins in the seal brain Fabrizius, Andrej Hoff, Mariana Engler, Gerhard Folkow, Lars Burmester, Thorsten 2016 https://dx.doi.org/10.6084/m9.figshare.c.3636611 https://figshare.com/collections/When_the_brain_goes_diving_transcriptome_analysis_reveals_a_reduced_aerobic_energy_metabolism_and_increased_stress_proteins_in_the_seal_brain/3636611 unknown Figshare https://dx.doi.org/10.1186/s12864-016-2892-y CC BY 4.0 https://creativecommons.org/licenses/by/4.0 CC-BY Cell Biology Molecular Biology Neuroscience Physiology FOS Biological sciences Evolutionary Biology 59999 Environmental Sciences not elsewhere classified FOS Earth and related environmental sciences Ecology 69999 Biological Sciences not elsewhere classified 111714 Mental Health FOS Health sciences Collection article 2016 ftdatacite https://doi.org/10.6084/m9.figshare.c.3636611 https://doi.org/10.1186/s12864-016-2892-y 2021-11-05T12:55:41Z Abstract Background During long dives, the brain of whales and seals experiences a reduced supply of oxygen (hypoxia). The brain neurons of the hooded seal (Cystophora cristata) are more tolerant towards low-oxygen conditions than those of mice, and also better survive other hypoxia-related stress conditions like a reduction in glucose supply and high concentrations of lactate. Little is known about the molecular mechanisms that support the hypoxia tolerance of the diving brain. Results Here we employed RNA-seq to approach the molecular basis of the unusual stress tolerance of the seal brain. An Illumina-generated transcriptome of the visual cortex of the hooded seal was compared with that of the ferret (Mustela putorius furo), which served as a terrestrial relative. Gene ontology analyses showed a significant enrichment of transcripts related to translation and aerobic energy production in the ferret but not in the seal brain. Clusterin, an extracellular chaperone, is the most highly expressed gene in the seal brain and fourfold higher than in the ferret or any other mammalian brain transcriptome. The largest difference was found for S100B, a calcium-binding stress protein with pleiotropic function, which was 38-fold enriched in the seal brain. Notably, significant enrichment of S100B mRNA was also found in the transcriptomes of whale brains, but not in the brains of terrestrial mammals. Conclusion Comparative transcriptomics indicates a lower aerobic capacity of the seal brain, which may be interpreted as a general energy saving strategy. Elevated expression of stress-related genes, such as clusterin and S100B, possibly contributes to the remarkable hypoxia tolerance of the brain of the hooded seal. Moreover, high levels of S100B that possibly protect the brain appear to be the result of the convergent adaptation of diving mammals. Article in Journal/Newspaper Cystophora cristata hooded seal DataCite Metadata Store (German National Library of Science and Technology)
institution Open Polar
collection DataCite Metadata Store (German National Library of Science and Technology)
op_collection_id ftdatacite
language unknown
topic Cell Biology
Molecular Biology
Neuroscience
Physiology
FOS Biological sciences
Evolutionary Biology
59999 Environmental Sciences not elsewhere classified
FOS Earth and related environmental sciences
Ecology
69999 Biological Sciences not elsewhere classified
111714 Mental Health
FOS Health sciences
spellingShingle Cell Biology
Molecular Biology
Neuroscience
Physiology
FOS Biological sciences
Evolutionary Biology
59999 Environmental Sciences not elsewhere classified
FOS Earth and related environmental sciences
Ecology
69999 Biological Sciences not elsewhere classified
111714 Mental Health
FOS Health sciences
Fabrizius, Andrej
Hoff, Mariana
Engler, Gerhard
Folkow, Lars
Burmester, Thorsten
When the brain goes diving: transcriptome analysis reveals a reduced aerobic energy metabolism and increased stress proteins in the seal brain
topic_facet Cell Biology
Molecular Biology
Neuroscience
Physiology
FOS Biological sciences
Evolutionary Biology
59999 Environmental Sciences not elsewhere classified
FOS Earth and related environmental sciences
Ecology
69999 Biological Sciences not elsewhere classified
111714 Mental Health
FOS Health sciences
description Abstract Background During long dives, the brain of whales and seals experiences a reduced supply of oxygen (hypoxia). The brain neurons of the hooded seal (Cystophora cristata) are more tolerant towards low-oxygen conditions than those of mice, and also better survive other hypoxia-related stress conditions like a reduction in glucose supply and high concentrations of lactate. Little is known about the molecular mechanisms that support the hypoxia tolerance of the diving brain. Results Here we employed RNA-seq to approach the molecular basis of the unusual stress tolerance of the seal brain. An Illumina-generated transcriptome of the visual cortex of the hooded seal was compared with that of the ferret (Mustela putorius furo), which served as a terrestrial relative. Gene ontology analyses showed a significant enrichment of transcripts related to translation and aerobic energy production in the ferret but not in the seal brain. Clusterin, an extracellular chaperone, is the most highly expressed gene in the seal brain and fourfold higher than in the ferret or any other mammalian brain transcriptome. The largest difference was found for S100B, a calcium-binding stress protein with pleiotropic function, which was 38-fold enriched in the seal brain. Notably, significant enrichment of S100B mRNA was also found in the transcriptomes of whale brains, but not in the brains of terrestrial mammals. Conclusion Comparative transcriptomics indicates a lower aerobic capacity of the seal brain, which may be interpreted as a general energy saving strategy. Elevated expression of stress-related genes, such as clusterin and S100B, possibly contributes to the remarkable hypoxia tolerance of the brain of the hooded seal. Moreover, high levels of S100B that possibly protect the brain appear to be the result of the convergent adaptation of diving mammals.
format Article in Journal/Newspaper
author Fabrizius, Andrej
Hoff, Mariana
Engler, Gerhard
Folkow, Lars
Burmester, Thorsten
author_facet Fabrizius, Andrej
Hoff, Mariana
Engler, Gerhard
Folkow, Lars
Burmester, Thorsten
author_sort Fabrizius, Andrej
title When the brain goes diving: transcriptome analysis reveals a reduced aerobic energy metabolism and increased stress proteins in the seal brain
title_short When the brain goes diving: transcriptome analysis reveals a reduced aerobic energy metabolism and increased stress proteins in the seal brain
title_full When the brain goes diving: transcriptome analysis reveals a reduced aerobic energy metabolism and increased stress proteins in the seal brain
title_fullStr When the brain goes diving: transcriptome analysis reveals a reduced aerobic energy metabolism and increased stress proteins in the seal brain
title_full_unstemmed When the brain goes diving: transcriptome analysis reveals a reduced aerobic energy metabolism and increased stress proteins in the seal brain
title_sort when the brain goes diving: transcriptome analysis reveals a reduced aerobic energy metabolism and increased stress proteins in the seal brain
publisher Figshare
publishDate 2016
url https://dx.doi.org/10.6084/m9.figshare.c.3636611
https://figshare.com/collections/When_the_brain_goes_diving_transcriptome_analysis_reveals_a_reduced_aerobic_energy_metabolism_and_increased_stress_proteins_in_the_seal_brain/3636611
genre Cystophora cristata
hooded seal
genre_facet Cystophora cristata
hooded seal
op_relation https://dx.doi.org/10.1186/s12864-016-2892-y
op_rights CC BY 4.0
https://creativecommons.org/licenses/by/4.0
op_rightsnorm CC-BY
op_doi https://doi.org/10.6084/m9.figshare.c.3636611
https://doi.org/10.1186/s12864-016-2892-y
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