Electron transfer and ROS production in brain mitochondria of intertidal and subtidal triplefin fish (Tripterygiidae)
While oxygen is essential for oxidative phosphorylation, O 2 can form reactive species (ROS) when interacting with electrons of mitochondrial electron transport system. ROS is dependent on O 2 pressure (PO 2 ) and has traditionally been assessed in O 2 saturated media, PO 2 at which mitochondria do...
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Veröffentlicht in: | Journal of comparative physiology. B, Biochemical, systemic, and environmental physiology Biochemical, systemic, and environmental physiology, 2023-08, Vol.193 (4), p.413-424 |
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creator | Devaux, Jules B. L. Hedges, Chris P. Birch, Nigel Herbert, Neill Renshaw, Gillian M. C. Hickey, Anthony J. R. |
description | While oxygen is essential for oxidative phosphorylation, O
2
can form reactive species (ROS) when interacting with electrons of mitochondrial electron transport system. ROS is dependent on O
2
pressure (PO
2
) and has traditionally been assessed in O
2
saturated media, PO
2
at which mitochondria do not typically function in vivo. Mitochondrial ROS can be significantly elevated by the respiratory complex II substrate succinate, which can accumulate within hypoxic tissues, and this is exacerbated further with reoxygenation. Intertidal species are repetitively exposed to extreme O
2
fluctuations, and have likely evolved strategies to avoid excess ROS production. We evaluated mitochondrial electron leakage and ROS production in permeabilized brain of intertidal and subtidal triplefin fish species from hyperoxia to anoxia, and assessed the effect of anoxia reoxygenation and the influence of increasing succinate concentrations. At typical intracellular PO
2
, net ROS production was similar among all species; however at elevated PO
2
, brain tissues of the intertidal triplefin fish released less ROS than subtidal species. In addition, following in vitro anoxia reoxygenation, electron transfer mediated by succinate titration was better directed to respiration, and not to ROS production for intertidal species. Overall, these data indicate that intertidal triplefin fish species better manage electrons within the ETS, from hypoxic–hyperoxic transitions. |
doi_str_mv | 10.1007/s00360-023-01495-4 |
format | Article |
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2
can form reactive species (ROS) when interacting with electrons of mitochondrial electron transport system. ROS is dependent on O
2
pressure (PO
2
) and has traditionally been assessed in O
2
saturated media, PO
2
at which mitochondria do not typically function in vivo. Mitochondrial ROS can be significantly elevated by the respiratory complex II substrate succinate, which can accumulate within hypoxic tissues, and this is exacerbated further with reoxygenation. Intertidal species are repetitively exposed to extreme O
2
fluctuations, and have likely evolved strategies to avoid excess ROS production. We evaluated mitochondrial electron leakage and ROS production in permeabilized brain of intertidal and subtidal triplefin fish species from hyperoxia to anoxia, and assessed the effect of anoxia reoxygenation and the influence of increasing succinate concentrations. At typical intracellular PO
2
, net ROS production was similar among all species; however at elevated PO
2
, brain tissues of the intertidal triplefin fish released less ROS than subtidal species. In addition, following in vitro anoxia reoxygenation, electron transfer mediated by succinate titration was better directed to respiration, and not to ROS production for intertidal species. Overall, these data indicate that intertidal triplefin fish species better manage electrons within the ETS, from hypoxic–hyperoxic transitions.</description><identifier>ISSN: 0174-1578</identifier><identifier>EISSN: 1432-136X</identifier><identifier>DOI: 10.1007/s00360-023-01495-4</identifier><identifier>PMID: 37145369</identifier><language>eng</language><publisher>Berlin/Heidelberg: Springer Berlin Heidelberg</publisher><subject>Animal Physiology ; Anoxia ; Bioaccumulation ; Biochemistry ; Biomedical and Life Sciences ; Biomedicine ; Brain ; Electron transfer ; Electron transport ; Fish ; Human Physiology ; Hyperoxia ; Hypoxia ; Life Sciences ; Mitochondria ; Original Paper ; Oxidative phosphorylation ; Phosphorylation ; Pressure dependence ; Species ; Substrates ; Titration ; Transportation systems ; Zoology</subject><ispartof>Journal of comparative physiology. B, Biochemical, systemic, and environmental physiology, 2023-08, Vol.193 (4), p.413-424</ispartof><rights>The Author(s) 2023</rights><rights>2023. The Author(s).</rights><rights>The Author(s) 2023. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c475t-2fe919064043e76eb410afdc3b734556ed0e45689f63ab0a3b5e2bd3e4a3f2283</citedby><cites>FETCH-LOGICAL-c475t-2fe919064043e76eb410afdc3b734556ed0e45689f63ab0a3b5e2bd3e4a3f2283</cites><orcidid>0000-0002-5280-3871</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1007/s00360-023-01495-4$$EPDF$$P50$$Gspringer$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1007/s00360-023-01495-4$$EHTML$$P50$$Gspringer$$Hfree_for_read</linktohtml><link.rule.ids>230,314,776,780,881,27901,27902,41464,42533,51294</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/37145369$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Devaux, Jules B. L.</creatorcontrib><creatorcontrib>Hedges, Chris P.</creatorcontrib><creatorcontrib>Birch, Nigel</creatorcontrib><creatorcontrib>Herbert, Neill</creatorcontrib><creatorcontrib>Renshaw, Gillian M. C.</creatorcontrib><creatorcontrib>Hickey, Anthony J. R.</creatorcontrib><title>Electron transfer and ROS production in brain mitochondria of intertidal and subtidal triplefin fish (Tripterygiidae)</title><title>Journal of comparative physiology. B, Biochemical, systemic, and environmental physiology</title><addtitle>J Comp Physiol B</addtitle><addtitle>J Comp Physiol B</addtitle><description>While oxygen is essential for oxidative phosphorylation, O
2
can form reactive species (ROS) when interacting with electrons of mitochondrial electron transport system. ROS is dependent on O
2
pressure (PO
2
) and has traditionally been assessed in O
2
saturated media, PO
2
at which mitochondria do not typically function in vivo. Mitochondrial ROS can be significantly elevated by the respiratory complex II substrate succinate, which can accumulate within hypoxic tissues, and this is exacerbated further with reoxygenation. Intertidal species are repetitively exposed to extreme O
2
fluctuations, and have likely evolved strategies to avoid excess ROS production. We evaluated mitochondrial electron leakage and ROS production in permeabilized brain of intertidal and subtidal triplefin fish species from hyperoxia to anoxia, and assessed the effect of anoxia reoxygenation and the influence of increasing succinate concentrations. At typical intracellular PO
2
, net ROS production was similar among all species; however at elevated PO
2
, brain tissues of the intertidal triplefin fish released less ROS than subtidal species. In addition, following in vitro anoxia reoxygenation, electron transfer mediated by succinate titration was better directed to respiration, and not to ROS production for intertidal species. Overall, these data indicate that intertidal triplefin fish species better manage electrons within the ETS, from hypoxic–hyperoxic transitions.</description><subject>Animal Physiology</subject><subject>Anoxia</subject><subject>Bioaccumulation</subject><subject>Biochemistry</subject><subject>Biomedical and Life Sciences</subject><subject>Biomedicine</subject><subject>Brain</subject><subject>Electron transfer</subject><subject>Electron transport</subject><subject>Fish</subject><subject>Human Physiology</subject><subject>Hyperoxia</subject><subject>Hypoxia</subject><subject>Life Sciences</subject><subject>Mitochondria</subject><subject>Original Paper</subject><subject>Oxidative phosphorylation</subject><subject>Phosphorylation</subject><subject>Pressure dependence</subject><subject>Species</subject><subject>Substrates</subject><subject>Titration</subject><subject>Transportation systems</subject><subject>Zoology</subject><issn>0174-1578</issn><issn>1432-136X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>C6C</sourceid><sourceid>BENPR</sourceid><recordid>eNp9kc1rFTEUxYMo9ln9B1zIgJu6GL35nMlKpNQPKBS0gruQmbl5L2Ve8kwyQv97006tHws3CeH8zsm9HEKeU3hNAbo3GYAraIHxFqjQshUPyIYKzlrK1beHZAO0Ey2VXX9EnuR8BQCC9uIxOeIdFZIrvSHL2YxjSTE0JdmQHabGhqn5fPGlOaQ4LWPxVfOhGZKt596XOO5imJK3TXRVKJiKn-x8a8vLsD5K8ocZXXU4n3fNyWV9V_J666uMr56SR87OGZ_d3cfk6_uzy9OP7fnFh0-n787bUXSytMyhphqUAMGxUzgICtZNIx86LqRUOAEKqXrtFLcDWD5IZMPEUVjuGOv5MXm75h6WYY_TiKFuOZtD8nubrk203vytBL8z2_jDUGBaa8FrwsldQorfF8zF7H0ecZ5twLhkw3oKmjHd36Av_0Gv4pJC3a9SNU6qdSS2UmOKOSd099NQMDe1mrVWU2s1t7UaUU0v_tzj3vKrxwrwFchVCltMv__-T-xPx0-vvg</recordid><startdate>20230801</startdate><enddate>20230801</enddate><creator>Devaux, Jules B. L.</creator><creator>Hedges, Chris P.</creator><creator>Birch, Nigel</creator><creator>Herbert, Neill</creator><creator>Renshaw, Gillian M. C.</creator><creator>Hickey, Anthony J. R.</creator><general>Springer Berlin Heidelberg</general><general>Springer Nature B.V</general><scope>C6C</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>7QG</scope><scope>7QR</scope><scope>7SS</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7U7</scope><scope>7X7</scope><scope>7XB</scope><scope>88A</scope><scope>88E</scope><scope>8AO</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7P</scope><scope>P64</scope><scope>PATMY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PYCSY</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-5280-3871</orcidid></search><sort><creationdate>20230801</creationdate><title>Electron transfer and ROS production in brain mitochondria of intertidal and subtidal triplefin fish (Tripterygiidae)</title><author>Devaux, Jules B. L. ; Hedges, Chris P. ; Birch, Nigel ; Herbert, Neill ; Renshaw, Gillian M. C. ; Hickey, Anthony J. 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B, Biochemical, systemic, and environmental physiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Devaux, Jules B. L.</au><au>Hedges, Chris P.</au><au>Birch, Nigel</au><au>Herbert, Neill</au><au>Renshaw, Gillian M. C.</au><au>Hickey, Anthony J. R.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Electron transfer and ROS production in brain mitochondria of intertidal and subtidal triplefin fish (Tripterygiidae)</atitle><jtitle>Journal of comparative physiology. B, Biochemical, systemic, and environmental physiology</jtitle><stitle>J Comp Physiol B</stitle><addtitle>J Comp Physiol B</addtitle><date>2023-08-01</date><risdate>2023</risdate><volume>193</volume><issue>4</issue><spage>413</spage><epage>424</epage><pages>413-424</pages><issn>0174-1578</issn><eissn>1432-136X</eissn><abstract>While oxygen is essential for oxidative phosphorylation, O
2
can form reactive species (ROS) when interacting with electrons of mitochondrial electron transport system. ROS is dependent on O
2
pressure (PO
2
) and has traditionally been assessed in O
2
saturated media, PO
2
at which mitochondria do not typically function in vivo. Mitochondrial ROS can be significantly elevated by the respiratory complex II substrate succinate, which can accumulate within hypoxic tissues, and this is exacerbated further with reoxygenation. Intertidal species are repetitively exposed to extreme O
2
fluctuations, and have likely evolved strategies to avoid excess ROS production. We evaluated mitochondrial electron leakage and ROS production in permeabilized brain of intertidal and subtidal triplefin fish species from hyperoxia to anoxia, and assessed the effect of anoxia reoxygenation and the influence of increasing succinate concentrations. At typical intracellular PO
2
, net ROS production was similar among all species; however at elevated PO
2
, brain tissues of the intertidal triplefin fish released less ROS than subtidal species. In addition, following in vitro anoxia reoxygenation, electron transfer mediated by succinate titration was better directed to respiration, and not to ROS production for intertidal species. Overall, these data indicate that intertidal triplefin fish species better manage electrons within the ETS, from hypoxic–hyperoxic transitions.</abstract><cop>Berlin/Heidelberg</cop><pub>Springer Berlin Heidelberg</pub><pmid>37145369</pmid><doi>10.1007/s00360-023-01495-4</doi><tpages>12</tpages><orcidid>https://orcid.org/0000-0002-5280-3871</orcidid><oa>free_for_read</oa></addata></record> |
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source | Springer Nature - Complete Springer Journals |
subjects | Animal Physiology Anoxia Bioaccumulation Biochemistry Biomedical and Life Sciences Biomedicine Brain Electron transfer Electron transport Fish Human Physiology Hyperoxia Hypoxia Life Sciences Mitochondria Original Paper Oxidative phosphorylation Phosphorylation Pressure dependence Species Substrates Titration Transportation systems Zoology |
title | Electron transfer and ROS production in brain mitochondria of intertidal and subtidal triplefin fish (Tripterygiidae) |
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