Roles of nitric oxide, nitrite and myoglobin on myocardial efficiency in trout (Oncorhynchus mykiss) and goldfish (Carassius auratus): implications for hypoxia tolerance

Claus Lunde Pedersen, Serena Faggiano, Signe Helbo, Hans Gesser, Angela Fago

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    Abstract

    The roles of nitric oxide synthase activity (NOS), nitrite and myoglobin (Mb) in the regulation of myocardial function during hypoxia were examined in trout and goldfish, a hypoxia-intolerant and hypoxia-tolerant species, respectively. We measured the effect of NOS inhibition, adrenaline and nitrite on the O2 consumption rate and isometric twitch force development in electrically paced ventricular preparations during hypoxia, and measured O2 affinity and nitrite reductase activity of the purified heart Mbs of both species. Upon hypoxia (9% O2), O2 consumption and developed force decreased in both trout and goldfish myocardium, with trout showing a significant increase in the O2 utilization efficiency, i.e. the ratio of twitch force to O2 consumption, suggesting an increased anaerobic metabolism. NOS inhibition enhanced myocardial O2 consumption and decreased efficiency, indicating that mitochondrial respiration is under a tone of NOS-produced NO. When trout myocardial twitch force and O2 consumption are enhanced by adrenaline, this NO tone disappears. Consistent with its conversion to NO, nitrite reduced O2 consumption and increased myocardial efficiency in trout but not in goldfish. Such a difference correlates with the lower O2 affinity measured for trout Mb that would increase the fraction of deoxygenated heme available to catalyze the reduction of nitrite to NO. Whereas low-affinity trout Mb would favor O2 diffusion within cardiomyocytes at high in vivo O2 tensions, goldfish Mb having higher O2 affinity and higher nitrite reductase activity appears better suited to facilitate O2 diffusion and nitrite reduction in the heart during severe hypoxia, a condition particularly well tolerated by this species.
    Original languageEnglish
    JournalJournal of Experimental Biology
    Volume213
    Pages (from-to)2755-2762
    ISSN0022-0949
    DOIs
    Publication statusPublished - 2010

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