Inter-relationship between mitochondrial function and susceptibility to oxidative stress in red- and white-blooded Antarctic notothenioid fishes

It is unknown whether Antarctic fishes can defend themselves against oxidative stress induced by elevations in temperature. We hypothesized that Antarctic icefishes, lacking the oxygen-binding protein hemoglobin, might be more vulnerable to temperature-induced oxidative stress compared with red-bloo...

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Published in:Journal of Experimental Biology
Main Authors: Mueller, Irina A., Grim, Jeffrey M., Beers, Jody M., Crockett, Elizabeth L., O'Brien, Kristin M.
Format: Text
Language:English
Published: Company of Biologists 2011
Subjects:
Online Access:http://jeb.biologists.org/cgi/content/short/214/22/3732
https://doi.org/10.1242/jeb.062042
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spelling fthighwire:oai:open-archive.highwire.org:jexbio:214/22/3732 2023-05-15T13:47:32+02:00 Inter-relationship between mitochondrial function and susceptibility to oxidative stress in red- and white-blooded Antarctic notothenioid fishes Mueller, Irina A. Grim, Jeffrey M. Beers, Jody M. Crockett, Elizabeth L. O'Brien, Kristin M. 2011-11-15 00:00:00.0 text/html http://jeb.biologists.org/cgi/content/short/214/22/3732 https://doi.org/10.1242/jeb.062042 en eng Company of Biologists http://jeb.biologists.org/cgi/content/short/214/22/3732 http://dx.doi.org/10.1242/jeb.062042 Copyright (C) 2011, Company of Biologists Research Articles TEXT 2011 fthighwire https://doi.org/10.1242/jeb.062042 2013-05-27T12:25:48Z It is unknown whether Antarctic fishes can defend themselves against oxidative stress induced by elevations in temperature. We hypothesized that Antarctic icefishes, lacking the oxygen-binding protein hemoglobin, might be more vulnerable to temperature-induced oxidative stress compared with red-blooded notothenioids because of differences in their mitochondrial properties. Mitochondria from icefishes have higher densities of phospholipids per mg of mitochondrial protein compared with red-blooded species, and these phospholipids are rich in polyunsaturated fatty acids (PUFA), which can promote the formation of reactive oxygen species (ROS). Additionally, previous studies have shown that multiple tissues in icefishes have lower levels of antioxidants compared with red-blooded species. We quantified several properties of mitochondria, including proton leak, rates of ROS production, membrane composition and susceptibility to lipid peroxidation (LPO), the activity of superoxide dismutase (SOD) and total antioxidant power (TAOP) in mitochondria isolated from hearts of icefishes and red-blooded notothenioids. Mitochondria from icefishes were more tightly coupled than those of red-blooded fishes at both 2°C and 10°C, which increased the production of ROS when the electron transport chain was disrupted. The activity of SOD and TAOP per mg of mitochondrial protein was equivalent between icefishes and red-blooded species, but TAOP normalized to mitochondrial phospholipid content was significantly lower in icefishes compared with red-blooded fishes. Additionally, membrane susceptibility to peroxidation was only detectable in icefishes at 1°C and not in red-blooded species. Together, our results suggest that the high density of mitochondrial phospholipids in hearts of icefishes may make them particularly vulnerable to oxidative stress as temperatures rise. Text Antarc* Antarctic HighWire Press (Stanford University) Antarctic Journal of Experimental Biology 214 22 3732 3741
institution Open Polar
collection HighWire Press (Stanford University)
op_collection_id fthighwire
language English
topic Research Articles
spellingShingle Research Articles
Mueller, Irina A.
Grim, Jeffrey M.
Beers, Jody M.
Crockett, Elizabeth L.
O'Brien, Kristin M.
Inter-relationship between mitochondrial function and susceptibility to oxidative stress in red- and white-blooded Antarctic notothenioid fishes
topic_facet Research Articles
description It is unknown whether Antarctic fishes can defend themselves against oxidative stress induced by elevations in temperature. We hypothesized that Antarctic icefishes, lacking the oxygen-binding protein hemoglobin, might be more vulnerable to temperature-induced oxidative stress compared with red-blooded notothenioids because of differences in their mitochondrial properties. Mitochondria from icefishes have higher densities of phospholipids per mg of mitochondrial protein compared with red-blooded species, and these phospholipids are rich in polyunsaturated fatty acids (PUFA), which can promote the formation of reactive oxygen species (ROS). Additionally, previous studies have shown that multiple tissues in icefishes have lower levels of antioxidants compared with red-blooded species. We quantified several properties of mitochondria, including proton leak, rates of ROS production, membrane composition and susceptibility to lipid peroxidation (LPO), the activity of superoxide dismutase (SOD) and total antioxidant power (TAOP) in mitochondria isolated from hearts of icefishes and red-blooded notothenioids. Mitochondria from icefishes were more tightly coupled than those of red-blooded fishes at both 2°C and 10°C, which increased the production of ROS when the electron transport chain was disrupted. The activity of SOD and TAOP per mg of mitochondrial protein was equivalent between icefishes and red-blooded species, but TAOP normalized to mitochondrial phospholipid content was significantly lower in icefishes compared with red-blooded fishes. Additionally, membrane susceptibility to peroxidation was only detectable in icefishes at 1°C and not in red-blooded species. Together, our results suggest that the high density of mitochondrial phospholipids in hearts of icefishes may make them particularly vulnerable to oxidative stress as temperatures rise.
format Text
author Mueller, Irina A.
Grim, Jeffrey M.
Beers, Jody M.
Crockett, Elizabeth L.
O'Brien, Kristin M.
author_facet Mueller, Irina A.
Grim, Jeffrey M.
Beers, Jody M.
Crockett, Elizabeth L.
O'Brien, Kristin M.
author_sort Mueller, Irina A.
title Inter-relationship between mitochondrial function and susceptibility to oxidative stress in red- and white-blooded Antarctic notothenioid fishes
title_short Inter-relationship between mitochondrial function and susceptibility to oxidative stress in red- and white-blooded Antarctic notothenioid fishes
title_full Inter-relationship between mitochondrial function and susceptibility to oxidative stress in red- and white-blooded Antarctic notothenioid fishes
title_fullStr Inter-relationship between mitochondrial function and susceptibility to oxidative stress in red- and white-blooded Antarctic notothenioid fishes
title_full_unstemmed Inter-relationship between mitochondrial function and susceptibility to oxidative stress in red- and white-blooded Antarctic notothenioid fishes
title_sort inter-relationship between mitochondrial function and susceptibility to oxidative stress in red- and white-blooded antarctic notothenioid fishes
publisher Company of Biologists
publishDate 2011
url http://jeb.biologists.org/cgi/content/short/214/22/3732
https://doi.org/10.1242/jeb.062042
geographic Antarctic
geographic_facet Antarctic
genre Antarc*
Antarctic
genre_facet Antarc*
Antarctic
op_relation http://jeb.biologists.org/cgi/content/short/214/22/3732
http://dx.doi.org/10.1242/jeb.062042
op_rights Copyright (C) 2011, Company of Biologists
op_doi https://doi.org/10.1242/jeb.062042
container_title Journal of Experimental Biology
container_volume 214
container_issue 22
container_start_page 3732
op_container_end_page 3741
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