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

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 credited. This article is also available via DOI: 10.1186/s12864-016-2892...

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Published in:BMC Genomics
Main Authors: Fabrizius, Andrej, Hoff, Mariana Leivas Müller, Engler, Gerhard, Folkow, Lars, Burmester, Thorsten
Format: Article in Journal/Newspaper
Language:English
Published: BioMed Central 2016
Subjects:
Online Access:https://hdl.handle.net/10037/10261
https://doi.org/10.1186/s12864-016-2892-y
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record_format openpolar
spelling ftunivtroemsoe:oai:munin.uit.no:10037/10261 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 Leivas Müller Engler, Gerhard Folkow, Lars Burmester, Thorsten 2016-08-09 https://hdl.handle.net/10037/10261 https://doi.org/10.1186/s12864-016-2892-y eng eng BioMed Central BMC Genomics Fabrizius A, Hoff ML, Engler, Folkow P., Burmester T. When the brain goes diving: transcriptome analysis reveals a reduced aerobic energy metabolism and increased stress proteins in the seal brain. BMC Genomics. 2016;17(1) FRIDAID 1382834 doi:10.1186/s12864-016-2892-y 1471-2164 https://hdl.handle.net/10037/10261 openAccess Brain Calcium Diving Glucose Hypoxia Hooded seal Marine mammals Stress VDP::Matematikk og Naturvitenskap: 400::Zoologiske og botaniske fag: 480::Marinbiologi: 497 VDP::Mathematics and natural science: 400::Zoology and botany: 480::Marine biology: 497 Journal article Tidsskriftartikkel Peer reviewed 2016 ftunivtroemsoe https://doi.org/10.1186/s12864-016-2892-y 2021-06-25T17:55:01Z 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 credited. This article is also available via DOI: 10.1186/s12864-016-2892-y 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 University of Tromsø: Munin Open Research Archive BMC Genomics 17 1
institution Open Polar
collection University of Tromsø: Munin Open Research Archive
op_collection_id ftunivtroemsoe
language English
topic Brain
Calcium
Diving
Glucose
Hypoxia
Hooded seal
Marine mammals
Stress
VDP::Matematikk og Naturvitenskap: 400::Zoologiske og botaniske fag: 480::Marinbiologi: 497
VDP::Mathematics and natural science: 400::Zoology and botany: 480::Marine biology: 497
spellingShingle Brain
Calcium
Diving
Glucose
Hypoxia
Hooded seal
Marine mammals
Stress
VDP::Matematikk og Naturvitenskap: 400::Zoologiske og botaniske fag: 480::Marinbiologi: 497
VDP::Mathematics and natural science: 400::Zoology and botany: 480::Marine biology: 497
Fabrizius, Andrej
Hoff, Mariana Leivas Müller
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 Brain
Calcium
Diving
Glucose
Hypoxia
Hooded seal
Marine mammals
Stress
VDP::Matematikk og Naturvitenskap: 400::Zoologiske og botaniske fag: 480::Marinbiologi: 497
VDP::Mathematics and natural science: 400::Zoology and botany: 480::Marine biology: 497
description 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 credited. This article is also available via DOI: 10.1186/s12864-016-2892-y 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 Leivas Müller
Engler, Gerhard
Folkow, Lars
Burmester, Thorsten
author_facet Fabrizius, Andrej
Hoff, Mariana Leivas Müller
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 BioMed Central
publishDate 2016
url https://hdl.handle.net/10037/10261
https://doi.org/10.1186/s12864-016-2892-y
genre Cystophora cristata
hooded seal
genre_facet Cystophora cristata
hooded seal
op_relation BMC Genomics
Fabrizius A, Hoff ML, Engler, Folkow P., Burmester T. When the brain goes diving: transcriptome analysis reveals a reduced aerobic energy metabolism and increased stress proteins in the seal brain. BMC Genomics. 2016;17(1)
FRIDAID 1382834
doi:10.1186/s12864-016-2892-y
1471-2164
https://hdl.handle.net/10037/10261
op_rights openAccess
op_doi https://doi.org/10.1186/s12864-016-2892-y
container_title BMC Genomics
container_volume 17
container_issue 1
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