Hormetic response triggers multifaceted anti-oxidant strategies in immature king penguins (Aptenodytes patagonicus)

International audience Repeated deep dives are highly pro-oxidative events for air-breathing aquatic foragers such as penguins. At ␣edging, the transition from a strictly terrestrial to a marine lifestyle may therefore trigger a complex set of anti-oxidant responses to prevent chronic oxidative stre...

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Published in:Free Radical Biology and Medicine
Main Authors: Rey, Benjamin, Dégletagne, Cyril, Bodennec, Jacques, Monternier, Pierre-Axel, Mortz, Mathieu, Roussel, Damien, Romestaing, Caroline, Rouanet, Jean-Louis, Tornos, Jérémy, Duchamp, Claude
Other Authors: University of the Witwatersrand Johannesburg (WITS), Laboratoire de Biométrie et Biologie Evolutive - UMR 5558 (LBBE), Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS), Alfred-Wegener-Institut, Helmholtz-Zentrum für Polar- und Meeresforschung = Alfred Wegener Institute for Polar and Marine Research = Institut Alfred-Wegener pour la recherche polaire et marine (AWI), Helmholtz-Gemeinschaft = Helmholtz Association, Laboratoire d'Ecologie des Hydrosystèmes Naturels et Anthropisés (LEHNA), Université de Lyon-Université de Lyon-École Nationale des Travaux Publics de l'État (ENTPE)-Centre National de la Recherche Scientifique (CNRS), Centre de recherche en neurosciences de Lyon - Lyon Neuroscience Research Center (CRNL), Université de Lyon-Université de Lyon-Université Jean Monnet - Saint-Étienne (UJM)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)
Format: Article in Journal/Newspaper
Language:English
Published: HAL CCSD 2016
Subjects:
Online Access:https://sde.hal.science/hal-01368870
https://doi.org/10.1016/j.freeradbiomed.2016.07.015
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record_format openpolar
institution Open Polar
collection Université de Lyon: HAL
op_collection_id ftunivlyon
language English
topic Redox homeostasis Oxidative stress Penguin Lipid composition Hormesis Mitochondria
[SDE.BE]Environmental Sciences/Biodiversity and Ecology
spellingShingle Redox homeostasis Oxidative stress Penguin Lipid composition Hormesis Mitochondria
[SDE.BE]Environmental Sciences/Biodiversity and Ecology
Rey, Benjamin
Dégletagne, Cyril
Bodennec, Jacques
Monternier, Pierre-Axel
Mortz, Mathieu
Roussel, Damien
Romestaing, Caroline
Rouanet, Jean-Louis
Tornos, Jérémy
Duchamp, Claude
Hormetic response triggers multifaceted anti-oxidant strategies in immature king penguins (Aptenodytes patagonicus)
topic_facet Redox homeostasis Oxidative stress Penguin Lipid composition Hormesis Mitochondria
[SDE.BE]Environmental Sciences/Biodiversity and Ecology
description International audience Repeated deep dives are highly pro-oxidative events for air-breathing aquatic foragers such as penguins. At ␣edging, the transition from a strictly terrestrial to a marine lifestyle may therefore trigger a complex set of anti-oxidant responses to prevent chronic oxidative stress in immature penguins but these pro- cesses are still unde␣ned. By combining in vivo and in vitro approaches with transcriptome analysis, we investigated the adaptive responses of sea-acclimatized (SA) immature king penguins (Aptenodytes pa- tagonicus) compared with pre-␣edging never-immersed (NI) birds. In vivo, experimental immersion into cold water stimulated a higher thermogenic response in SA penguins than in NI birds, but both groups exhibited hypothermia, a condition favouring oxidative stress. In vitro, the pectoralis muscles of SA birds displayed increased oxidative capacity and mitochondrial protein abundance but unchanged reactive oxygen species (ROS) generation per g tissue because ROS production per mitochondria was reduced. The genes encoding oxidant-generating proteins were down-regulated in SA birds while mRNA abundance and activity of the main antioxidant enzymes were up-regulated. Genes encoding proteins involved in repair mechanisms of oxidized DNA or proteins and in degradation processes were also up-regulated in SA birds. Sea life also increased the degree of fatty acid unsaturation in muscle mitochondrial membranes resulting in higher intrinsic susceptibility to ROS. Oxidative damages to protein or DNA were reduced in SA birds. Repeated experimental immersions of NI penguins in cold-water partially mimicked the effects of acclimatization to marine life, modi␣ed the expression of fewer genes related to oxidative stress but in a similar way as in SA birds and increased oxidative damages to DNA. It is concluded that the multi- faceted plasticity observed after marine life may be crucial to maintain redox homeostasis in active tissues subjected to high pro-oxidative pressure in diving birds. ...
author2 University of the Witwatersrand Johannesburg (WITS)
Laboratoire de Biométrie et Biologie Evolutive - UMR 5558 (LBBE)
Université Claude Bernard Lyon 1 (UCBL)
Université de Lyon-Université de Lyon-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS)
Alfred-Wegener-Institut, Helmholtz-Zentrum für Polar- und Meeresforschung = Alfred Wegener Institute for Polar and Marine Research = Institut Alfred-Wegener pour la recherche polaire et marine (AWI)
Helmholtz-Gemeinschaft = Helmholtz Association
Laboratoire d'Ecologie des Hydrosystèmes Naturels et Anthropisés (LEHNA)
Université de Lyon-Université de Lyon-École Nationale des Travaux Publics de l'État (ENTPE)-Centre National de la Recherche Scientifique (CNRS)
Centre de recherche en neurosciences de Lyon - Lyon Neuroscience Research Center (CRNL)
Université de Lyon-Université de Lyon-Université Jean Monnet - Saint-Étienne (UJM)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)
format Article in Journal/Newspaper
author Rey, Benjamin
Dégletagne, Cyril
Bodennec, Jacques
Monternier, Pierre-Axel
Mortz, Mathieu
Roussel, Damien
Romestaing, Caroline
Rouanet, Jean-Louis
Tornos, Jérémy
Duchamp, Claude
author_facet Rey, Benjamin
Dégletagne, Cyril
Bodennec, Jacques
Monternier, Pierre-Axel
Mortz, Mathieu
Roussel, Damien
Romestaing, Caroline
Rouanet, Jean-Louis
Tornos, Jérémy
Duchamp, Claude
author_sort Rey, Benjamin
title Hormetic response triggers multifaceted anti-oxidant strategies in immature king penguins (Aptenodytes patagonicus)
title_short Hormetic response triggers multifaceted anti-oxidant strategies in immature king penguins (Aptenodytes patagonicus)
title_full Hormetic response triggers multifaceted anti-oxidant strategies in immature king penguins (Aptenodytes patagonicus)
title_fullStr Hormetic response triggers multifaceted anti-oxidant strategies in immature king penguins (Aptenodytes patagonicus)
title_full_unstemmed Hormetic response triggers multifaceted anti-oxidant strategies in immature king penguins (Aptenodytes patagonicus)
title_sort hormetic response triggers multifaceted anti-oxidant strategies in immature king penguins (aptenodytes patagonicus)
publisher HAL CCSD
publishDate 2016
url https://sde.hal.science/hal-01368870
https://doi.org/10.1016/j.freeradbiomed.2016.07.015
genre King Penguins
genre_facet King Penguins
op_source ISSN: 0891-5849
Free Radical Biology and Medicine
https://sde.hal.science/hal-01368870
Free Radical Biology and Medicine, 2016, 97, pp.577-587. ⟨10.1016/j.freeradbiomed.2016.07.015⟩
op_relation info:eu-repo/semantics/altIdentifier/doi/10.1016/j.freeradbiomed.2016.07.015
hal-01368870
https://sde.hal.science/hal-01368870
doi:10.1016/j.freeradbiomed.2016.07.015
op_doi https://doi.org/10.1016/j.freeradbiomed.2016.07.015
container_title Free Radical Biology and Medicine
container_volume 97
container_start_page 577
op_container_end_page 587
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spelling ftunivlyon:oai:HAL:hal-01368870v1 2024-06-23T07:54:23+00:00 Hormetic response triggers multifaceted anti-oxidant strategies in immature king penguins (Aptenodytes patagonicus) Rey, Benjamin Dégletagne, Cyril Bodennec, Jacques Monternier, Pierre-Axel Mortz, Mathieu Roussel, Damien Romestaing, Caroline Rouanet, Jean-Louis Tornos, Jérémy Duchamp, Claude University of the Witwatersrand Johannesburg (WITS) Laboratoire de Biométrie et Biologie Evolutive - UMR 5558 (LBBE) Université Claude Bernard Lyon 1 (UCBL) Université de Lyon-Université de Lyon-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS) Alfred-Wegener-Institut, Helmholtz-Zentrum für Polar- und Meeresforschung = Alfred Wegener Institute for Polar and Marine Research = Institut Alfred-Wegener pour la recherche polaire et marine (AWI) Helmholtz-Gemeinschaft = Helmholtz Association Laboratoire d'Ecologie des Hydrosystèmes Naturels et Anthropisés (LEHNA) Université de Lyon-Université de Lyon-École Nationale des Travaux Publics de l'État (ENTPE)-Centre National de la Recherche Scientifique (CNRS) Centre de recherche en neurosciences de Lyon - Lyon Neuroscience Research Center (CRNL) Université de Lyon-Université de Lyon-Université Jean Monnet - Saint-Étienne (UJM)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS) 2016 https://sde.hal.science/hal-01368870 https://doi.org/10.1016/j.freeradbiomed.2016.07.015 en eng HAL CCSD Elsevier info:eu-repo/semantics/altIdentifier/doi/10.1016/j.freeradbiomed.2016.07.015 hal-01368870 https://sde.hal.science/hal-01368870 doi:10.1016/j.freeradbiomed.2016.07.015 ISSN: 0891-5849 Free Radical Biology and Medicine https://sde.hal.science/hal-01368870 Free Radical Biology and Medicine, 2016, 97, pp.577-587. ⟨10.1016/j.freeradbiomed.2016.07.015⟩ Redox homeostasis Oxidative stress Penguin Lipid composition Hormesis Mitochondria [SDE.BE]Environmental Sciences/Biodiversity and Ecology info:eu-repo/semantics/article Journal articles 2016 ftunivlyon https://doi.org/10.1016/j.freeradbiomed.2016.07.015 2024-05-27T14:52:07Z International audience Repeated deep dives are highly pro-oxidative events for air-breathing aquatic foragers such as penguins. At ␣edging, the transition from a strictly terrestrial to a marine lifestyle may therefore trigger a complex set of anti-oxidant responses to prevent chronic oxidative stress in immature penguins but these pro- cesses are still unde␣ned. By combining in vivo and in vitro approaches with transcriptome analysis, we investigated the adaptive responses of sea-acclimatized (SA) immature king penguins (Aptenodytes pa- tagonicus) compared with pre-␣edging never-immersed (NI) birds. In vivo, experimental immersion into cold water stimulated a higher thermogenic response in SA penguins than in NI birds, but both groups exhibited hypothermia, a condition favouring oxidative stress. In vitro, the pectoralis muscles of SA birds displayed increased oxidative capacity and mitochondrial protein abundance but unchanged reactive oxygen species (ROS) generation per g tissue because ROS production per mitochondria was reduced. The genes encoding oxidant-generating proteins were down-regulated in SA birds while mRNA abundance and activity of the main antioxidant enzymes were up-regulated. Genes encoding proteins involved in repair mechanisms of oxidized DNA or proteins and in degradation processes were also up-regulated in SA birds. Sea life also increased the degree of fatty acid unsaturation in muscle mitochondrial membranes resulting in higher intrinsic susceptibility to ROS. Oxidative damages to protein or DNA were reduced in SA birds. Repeated experimental immersions of NI penguins in cold-water partially mimicked the effects of acclimatization to marine life, modi␣ed the expression of fewer genes related to oxidative stress but in a similar way as in SA birds and increased oxidative damages to DNA. It is concluded that the multi- faceted plasticity observed after marine life may be crucial to maintain redox homeostasis in active tissues subjected to high pro-oxidative pressure in diving birds. ... Article in Journal/Newspaper King Penguins Université de Lyon: HAL Free Radical Biology and Medicine 97 577 587