Amanda Bundgaard
Low production of mitochondrial reactive oxygen species after anoxia and reoxygenation in turtle hearts
Bundgaard, Amanda; Gruszczyk, Anja V.; Prag, Hiran A.; Williams, Catherine; McIntyre, Angela; Ruhr, Ilan M.; James, Andrew M.; Galli, Gina L.J.; Murphy, Michael P.; Fago, Angela
Authors
Anja V. Gruszczyk
Hiran A. Prag
Catherine Williams
Angela McIntyre
Dr Ilan Ruhr I.M.Ruhr@salford.ac.uk
University Fellow
Andrew M. James
Gina L.J. Galli
Michael P. Murphy
Angela Fago
Abstract
Extremely anoxia-tolerant animals, such as freshwater turtles, survive anoxia and reoxygenation without sustaining tissue damage to their hearts. In contrast, for mammals, the ischemia–reperfusion (IR) injury that leads to tissue damage during a heart attack is initiated by a burst of superoxide (O2·−) production from the mitochondrial respiratory chain upon reperfusion of ischemic tissue. Whether turtles avoid oxidative tissue damage because of an absence of mitochondrial superoxide production upon reoxygenation, or because the turtle heart is particularly protected against this damage, is unclear. Here, we investigated whether there was an increase in mitochondrial O2·− production upon the reoxygenation of anoxic red-eared slider turtle hearts in vivo and in vitro. This was done by measuring the production of H2O2, the dismutation product of O2·−, using the mitochondria-targeted mass-spectrometric probe in vivo MitoB, while in parallel assessing changes in the metabolites driving mitochondrial O2·− production, succinate, ATP and ADP levels during anoxia, and H2O2 consumption and production rates of isolated heart mitochondria. We found that there was no excess production of in vivo H2O2 during 1 h of reoxygenation in turtles after 3 h anoxia at room temperature, suggesting that turtle hearts most likely do not suffer oxidative injury after anoxia because their mitochondria produce no excess O2·− upon reoxygenation. Instead, our data support the conclusion that both the low levels of succinate accumulation and the maintenance of ADP levels in the anoxic turtle heart are key factors in preventing the surge of O2·− production upon reoxygenation.
Journal Article Type | Article |
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Acceptance Date | Apr 3, 2023 |
Publication Date | May 10, 2023 |
Deposit Date | Jun 11, 2025 |
Journal | Journal of Experimental Biology |
Print ISSN | 0022-0949 |
Electronic ISSN | 1477-9145 |
Publisher | Company of Biologists |
Peer Reviewed | Peer Reviewed |
Volume | 226 |
Issue | 9 |
DOI | https://doi.org/10.1242/jeb.245516 |
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