Ontogeny of Carbon Monoxide-Related Gene Expression in a Deep-Diving Marine Mammal
Marine mammals such as northern elephant seals (NES) routinely experience hypoxemia and ischemia-reperfusion events to many tissues during deep dives with no apparent adverse effects. Adaptations to diving include increased antioxidants and elevated oxygen storage capacity associated with high hemop...
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ftpubmed:oai:pubmedcentral.nih.gov:8567018 2023-05-15T16:05:45+02:00 Ontogeny of Carbon Monoxide-Related Gene Expression in a Deep-Diving Marine Mammal Piotrowski, Elizabeth R. Tift, Michael S. Crocker, Daniel E. Pearson, Anna B. Vázquez-Medina, José P. Keith, Anna D. Khudyakov, Jane I. 2021-10-21 http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8567018/ https://doi.org/10.3389/fphys.2021.762102 en eng Frontiers Media S.A. http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8567018/ http://dx.doi.org/10.3389/fphys.2021.762102 Copyright © 2021 Piotrowski, Tift, Crocker, Pearson, Vázquez-Medina, Keith and Khudyakov. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. CC-BY Front Physiol Physiology Text 2021 ftpubmed https://doi.org/10.3389/fphys.2021.762102 2021-11-07T02:01:30Z Marine mammals such as northern elephant seals (NES) routinely experience hypoxemia and ischemia-reperfusion events to many tissues during deep dives with no apparent adverse effects. Adaptations to diving include increased antioxidants and elevated oxygen storage capacity associated with high hemoprotein content in blood and muscle. The natural turnover of heme by heme oxygenase enzymes (encoded by HMOX1 and HMOX2) produces endogenous carbon monoxide (CO), which is present at high levels in NES blood and has been shown to have cytoprotective effects in laboratory systems exposed to hypoxia. To understand how pathways associated with endogenous CO production and signaling change across ontogeny in diving mammals, we measured muscle CO and baseline expression of 17 CO-related genes in skeletal muscle and whole blood of three age classes of NES. Muscle CO levels approached those of animals exposed to high exogenous CO, increased with age, and were significantly correlated with gene expression levels. Muscle expression of genes associated with CO production and antioxidant defenses (HMOX1, BVR, GPX3, PRDX1) increased with age and was highest in adult females, while that of genes associated with protection from lipid peroxidation (GPX4, PRDX6, PRDX1, SIRT1) was highest in adult males. In contrast, muscle expression of mitochondrial biogenesis regulators (PGC1A, ESRRA, ESRRG) was highest in pups, while genes associated with inflammation (HMOX2, NRF2, IL1B) did not vary with age or sex. Blood expression of genes involved in regulation of inflammation (IL1B, NRF2, BVR, IL10) was highest in pups, while HMOX1, HMOX2 and pro-inflammatory markers (TLR4, CCL4, PRDX1, TNFA) did not vary with age. We propose that ontogenetic upregulation of baseline HMOX1 expression in skeletal muscle of NES may, in part, underlie increases in CO levels and expression of genes encoding antioxidant enzymes. HMOX2, in turn, may play a role in regulating inflammation related to ischemia and reperfusion in muscle and circulating immune cells. Our ... Text Elephant Seals PubMed Central (PMC) Nes ENVELOPE(7.634,7.634,62.795,62.795) Nes’ ENVELOPE(44.681,44.681,66.600,66.600) Frontiers in Physiology 12 |
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English |
topic |
Physiology |
spellingShingle |
Physiology Piotrowski, Elizabeth R. Tift, Michael S. Crocker, Daniel E. Pearson, Anna B. Vázquez-Medina, José P. Keith, Anna D. Khudyakov, Jane I. Ontogeny of Carbon Monoxide-Related Gene Expression in a Deep-Diving Marine Mammal |
topic_facet |
Physiology |
description |
Marine mammals such as northern elephant seals (NES) routinely experience hypoxemia and ischemia-reperfusion events to many tissues during deep dives with no apparent adverse effects. Adaptations to diving include increased antioxidants and elevated oxygen storage capacity associated with high hemoprotein content in blood and muscle. The natural turnover of heme by heme oxygenase enzymes (encoded by HMOX1 and HMOX2) produces endogenous carbon monoxide (CO), which is present at high levels in NES blood and has been shown to have cytoprotective effects in laboratory systems exposed to hypoxia. To understand how pathways associated with endogenous CO production and signaling change across ontogeny in diving mammals, we measured muscle CO and baseline expression of 17 CO-related genes in skeletal muscle and whole blood of three age classes of NES. Muscle CO levels approached those of animals exposed to high exogenous CO, increased with age, and were significantly correlated with gene expression levels. Muscle expression of genes associated with CO production and antioxidant defenses (HMOX1, BVR, GPX3, PRDX1) increased with age and was highest in adult females, while that of genes associated with protection from lipid peroxidation (GPX4, PRDX6, PRDX1, SIRT1) was highest in adult males. In contrast, muscle expression of mitochondrial biogenesis regulators (PGC1A, ESRRA, ESRRG) was highest in pups, while genes associated with inflammation (HMOX2, NRF2, IL1B) did not vary with age or sex. Blood expression of genes involved in regulation of inflammation (IL1B, NRF2, BVR, IL10) was highest in pups, while HMOX1, HMOX2 and pro-inflammatory markers (TLR4, CCL4, PRDX1, TNFA) did not vary with age. We propose that ontogenetic upregulation of baseline HMOX1 expression in skeletal muscle of NES may, in part, underlie increases in CO levels and expression of genes encoding antioxidant enzymes. HMOX2, in turn, may play a role in regulating inflammation related to ischemia and reperfusion in muscle and circulating immune cells. Our ... |
format |
Text |
author |
Piotrowski, Elizabeth R. Tift, Michael S. Crocker, Daniel E. Pearson, Anna B. Vázquez-Medina, José P. Keith, Anna D. Khudyakov, Jane I. |
author_facet |
Piotrowski, Elizabeth R. Tift, Michael S. Crocker, Daniel E. Pearson, Anna B. Vázquez-Medina, José P. Keith, Anna D. Khudyakov, Jane I. |
author_sort |
Piotrowski, Elizabeth R. |
title |
Ontogeny of Carbon Monoxide-Related Gene Expression in a Deep-Diving Marine Mammal |
title_short |
Ontogeny of Carbon Monoxide-Related Gene Expression in a Deep-Diving Marine Mammal |
title_full |
Ontogeny of Carbon Monoxide-Related Gene Expression in a Deep-Diving Marine Mammal |
title_fullStr |
Ontogeny of Carbon Monoxide-Related Gene Expression in a Deep-Diving Marine Mammal |
title_full_unstemmed |
Ontogeny of Carbon Monoxide-Related Gene Expression in a Deep-Diving Marine Mammal |
title_sort |
ontogeny of carbon monoxide-related gene expression in a deep-diving marine mammal |
publisher |
Frontiers Media S.A. |
publishDate |
2021 |
url |
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8567018/ https://doi.org/10.3389/fphys.2021.762102 |
long_lat |
ENVELOPE(7.634,7.634,62.795,62.795) ENVELOPE(44.681,44.681,66.600,66.600) |
geographic |
Nes Nes’ |
geographic_facet |
Nes Nes’ |
genre |
Elephant Seals |
genre_facet |
Elephant Seals |
op_source |
Front Physiol |
op_relation |
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8567018/ http://dx.doi.org/10.3389/fphys.2021.762102 |
op_rights |
Copyright © 2021 Piotrowski, Tift, Crocker, Pearson, Vázquez-Medina, Keith and Khudyakov. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. |
op_rightsnorm |
CC-BY |
op_doi |
https://doi.org/10.3389/fphys.2021.762102 |
container_title |
Frontiers in Physiology |
container_volume |
12 |
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1766401645045874688 |