Transcriptomes Suggest That Pinniped and Cetacean Brains Have a High Capacity for Aerobic Metabolism While Reducing Energy-Intensive Processes Such as Synaptic Transmission
The mammalian brain is characterized by high energy expenditure and small energy reserves, making it dependent on continuous vascular oxygen and nutritional supply. The brain is therefore extremely vulnerable to hypoxia. While neurons of most terrestrial mammals suffer from irreversible damage after...
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ftdoajarticles:oai:doaj.org/article:0082546eb6644cf6bd9cb70454830b88 2023-05-15T15:36:00+02:00 Transcriptomes Suggest That Pinniped and Cetacean Brains Have a High Capacity for Aerobic Metabolism While Reducing Energy-Intensive Processes Such as Synaptic Transmission Cornelia Geßner Alena Krüger Lars P. Folkow Wilfrid Fehrle Bjarni Mikkelsen Thorsten Burmester 2022-05-01T00:00:00Z https://doi.org/10.3389/fnmol.2022.877349 https://doaj.org/article/0082546eb6644cf6bd9cb70454830b88 EN eng Frontiers Media S.A. https://www.frontiersin.org/articles/10.3389/fnmol.2022.877349/full https://doaj.org/toc/1662-5099 1662-5099 doi:10.3389/fnmol.2022.877349 https://doaj.org/article/0082546eb6644cf6bd9cb70454830b88 Frontiers in Molecular Neuroscience, Vol 15 (2022) hooded seal neurons hypoxia transcriptome marine mammals brain Neurosciences. Biological psychiatry. Neuropsychiatry RC321-571 article 2022 ftdoajarticles https://doi.org/10.3389/fnmol.2022.877349 2022-12-30T22:38:13Z The mammalian brain is characterized by high energy expenditure and small energy reserves, making it dependent on continuous vascular oxygen and nutritional supply. The brain is therefore extremely vulnerable to hypoxia. While neurons of most terrestrial mammals suffer from irreversible damage after only short periods of hypoxia, neurons of the deep-diving hooded seal (Cystophora cristata) show a remarkable hypoxia-tolerance. To identify the molecular mechanisms underlying the intrinsic hypoxia-tolerance, we excised neurons from the visual cortices of hooded seals and mice (Mus musculus) by laser capture microdissection. A comparison of the neuronal transcriptomes suggests that, compared to mice, hooded seal neurons are endowed with an enhanced aerobic metabolic capacity, a reduced synaptic transmission and an elevated antioxidant defense. Publicly available whole-tissue brain transcriptomes of the bowhead whale (Balaena mysticetus), long-finned pilot whale (Globicephala melas), minke whale (Balaenoptera acutorostrata) and killer whale (Orcinus orca), supplemented with 2 newly sequenced long-finned pilot whales, suggest that, compared to cattle (Bos taurus), the cetacean brain also displays elevated aerobic capacity and reduced synaptic transmission. We conclude that the brain energy balance of diving mammals is preserved during diving, due to reduced synaptic transmission that limits energy expenditure, while the elevated aerobic capacity allows efficient use of oxygen to restore energy balance during surfacing between dives. Article in Journal/Newspaper Balaena mysticetus Balaenoptera acutorostrata bowhead whale Cystophora cristata hooded seal Killer Whale minke whale Orca Orcinus orca Killer whale Directory of Open Access Journals: DOAJ Articles Frontiers in Molecular Neuroscience 15 |
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Directory of Open Access Journals: DOAJ Articles |
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English |
topic |
hooded seal neurons hypoxia transcriptome marine mammals brain Neurosciences. Biological psychiatry. Neuropsychiatry RC321-571 |
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hooded seal neurons hypoxia transcriptome marine mammals brain Neurosciences. Biological psychiatry. Neuropsychiatry RC321-571 Cornelia Geßner Alena Krüger Lars P. Folkow Wilfrid Fehrle Bjarni Mikkelsen Thorsten Burmester Transcriptomes Suggest That Pinniped and Cetacean Brains Have a High Capacity for Aerobic Metabolism While Reducing Energy-Intensive Processes Such as Synaptic Transmission |
topic_facet |
hooded seal neurons hypoxia transcriptome marine mammals brain Neurosciences. Biological psychiatry. Neuropsychiatry RC321-571 |
description |
The mammalian brain is characterized by high energy expenditure and small energy reserves, making it dependent on continuous vascular oxygen and nutritional supply. The brain is therefore extremely vulnerable to hypoxia. While neurons of most terrestrial mammals suffer from irreversible damage after only short periods of hypoxia, neurons of the deep-diving hooded seal (Cystophora cristata) show a remarkable hypoxia-tolerance. To identify the molecular mechanisms underlying the intrinsic hypoxia-tolerance, we excised neurons from the visual cortices of hooded seals and mice (Mus musculus) by laser capture microdissection. A comparison of the neuronal transcriptomes suggests that, compared to mice, hooded seal neurons are endowed with an enhanced aerobic metabolic capacity, a reduced synaptic transmission and an elevated antioxidant defense. Publicly available whole-tissue brain transcriptomes of the bowhead whale (Balaena mysticetus), long-finned pilot whale (Globicephala melas), minke whale (Balaenoptera acutorostrata) and killer whale (Orcinus orca), supplemented with 2 newly sequenced long-finned pilot whales, suggest that, compared to cattle (Bos taurus), the cetacean brain also displays elevated aerobic capacity and reduced synaptic transmission. We conclude that the brain energy balance of diving mammals is preserved during diving, due to reduced synaptic transmission that limits energy expenditure, while the elevated aerobic capacity allows efficient use of oxygen to restore energy balance during surfacing between dives. |
format |
Article in Journal/Newspaper |
author |
Cornelia Geßner Alena Krüger Lars P. Folkow Wilfrid Fehrle Bjarni Mikkelsen Thorsten Burmester |
author_facet |
Cornelia Geßner Alena Krüger Lars P. Folkow Wilfrid Fehrle Bjarni Mikkelsen Thorsten Burmester |
author_sort |
Cornelia Geßner |
title |
Transcriptomes Suggest That Pinniped and Cetacean Brains Have a High Capacity for Aerobic Metabolism While Reducing Energy-Intensive Processes Such as Synaptic Transmission |
title_short |
Transcriptomes Suggest That Pinniped and Cetacean Brains Have a High Capacity for Aerobic Metabolism While Reducing Energy-Intensive Processes Such as Synaptic Transmission |
title_full |
Transcriptomes Suggest That Pinniped and Cetacean Brains Have a High Capacity for Aerobic Metabolism While Reducing Energy-Intensive Processes Such as Synaptic Transmission |
title_fullStr |
Transcriptomes Suggest That Pinniped and Cetacean Brains Have a High Capacity for Aerobic Metabolism While Reducing Energy-Intensive Processes Such as Synaptic Transmission |
title_full_unstemmed |
Transcriptomes Suggest That Pinniped and Cetacean Brains Have a High Capacity for Aerobic Metabolism While Reducing Energy-Intensive Processes Such as Synaptic Transmission |
title_sort |
transcriptomes suggest that pinniped and cetacean brains have a high capacity for aerobic metabolism while reducing energy-intensive processes such as synaptic transmission |
publisher |
Frontiers Media S.A. |
publishDate |
2022 |
url |
https://doi.org/10.3389/fnmol.2022.877349 https://doaj.org/article/0082546eb6644cf6bd9cb70454830b88 |
genre |
Balaena mysticetus Balaenoptera acutorostrata bowhead whale Cystophora cristata hooded seal Killer Whale minke whale Orca Orcinus orca Killer whale |
genre_facet |
Balaena mysticetus Balaenoptera acutorostrata bowhead whale Cystophora cristata hooded seal Killer Whale minke whale Orca Orcinus orca Killer whale |
op_source |
Frontiers in Molecular Neuroscience, Vol 15 (2022) |
op_relation |
https://www.frontiersin.org/articles/10.3389/fnmol.2022.877349/full https://doaj.org/toc/1662-5099 1662-5099 doi:10.3389/fnmol.2022.877349 https://doaj.org/article/0082546eb6644cf6bd9cb70454830b88 |
op_doi |
https://doi.org/10.3389/fnmol.2022.877349 |
container_title |
Frontiers in Molecular Neuroscience |
container_volume |
15 |
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1766366338788360192 |