Nitric oxide increases myocardial efficiency in the hypoxia-tolerant turtle <i>Trachemys scripta</i>

Misfeldt, Mikkel; Fago, Angela; Gesser, H.

doi:10.1242/jeb.025171

Cited by 18 publications

(20 citation statements)

References 41 publications

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“…In a previous study we found that generation of NO from NOS (by adding L-arginine) significantly decreased O 2 consumption in the Trachemys myocardium, thereby increasing myocardial efficiency (i.e. ratio of developed force to O 2 consumption), particularly at low oxygenation (Misfeldt et al, 2009). Such effects of NO would be of importance not only in maintaining cardiac function during anoxia but also in favouring metabolic depression in other tissues as well.…”

Section: Cardiovascular Changes and Role Of Circulating No Metabolitementioning

confidence: 90%

Circulating nitric oxide metabolites and cardiovascular changes in the turtleTrachemys scriptaduring normoxia, anoxia and reoxygenation

Jacobsen

Hansen

Frank

et al. 2012

Journal of Experimental Biology

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SUMMARYTurtles of the genus Trachemys show a remarkable ability to survive prolonged anoxia. This is achieved by a strong metabolic depression, redistribution of blood flow and high levels of antioxidant defence. To understand whether nitric oxide (NO), a major regulator of vasodilatation and oxygen consumption, may be involved in the adaptive response of Trachemys to anoxia, we measured NO metabolites (nitrite, S-nitroso, Fe-nitrosyl and N-nitroso compounds) in the plasma and red blood cells of venous and arterial blood of Trachemys scripta turtles during normoxia and after anoxia (3h) and reoxygenation (30min) at 21°C, while monitoring blood oxygen content and circulatory parameters. Anoxia caused complete blood oxygen depletion, decrease in heart rate and arterial pressure, and increase in venous pressure, which may enhance heart filling and improve cardiac contractility. Nitrite was present at high, micromolar levels in normoxic blood, as in some other anoxia-tolerant species, without significant arterial-venous differences. Normoxic levels of erythrocyte S-nitroso compounds were within the range found for other vertebrates, despite very high measured thiol content. Fe-nitrosyl and N-nitroso compounds were present at high micromolar levels under normoxia and increased further after anoxia and reoxygenation, suggesting NO generation from nitrite catalysed by deoxygenated haemoglobin, which in turtle had a higher nitrite reductase activity than in hypoxia-intolerant species. Taken together, these data indicate constitutively high circulating levels of NO metabolites and significant increases in blood NO after anoxia and reoxygenation that may contribute to the complex physiological response in the extreme anoxia tolerance of Trachemys turtles.

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Section: Cardiovascular Changes and Role Of Circulating No Metabolitementioning

confidence: 90%

Circulating nitric oxide metabolites and cardiovascular changes in the turtleTrachemys scriptaduring normoxia, anoxia and reoxygenation

Jacobsen

Hansen

Frank

et al. 2012

Journal of Experimental Biology

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“…The experimental setup has been described in detail previously (Kalinin and Gesser, 2002;Overgaard and Gesser, 2004;Misfeldt et al, 2009). Briefly, a single ring-shaped ventricle preparation was mounted on two hooks, of which one was connected to a force transducer (Fort 10; World Precision Instruments, Sarasota, FL, USA).…”

Section: Measurements Of Twitch Force and O 2 Consumptionmentioning

confidence: 99%

“…The rate of O 2 consumption was obtained by linear regression and the twitch force by the difference between the minimal (resting tension) and the maximal force developed. Calibration of the O 2 electrode was performed as described (Misfeldt et al, 2009).…”

Section: Measurements Of Twitch Force and O 2 Consumptionmentioning

confidence: 99%

“…NO is a signaling molecule with a widespread mode of action, playing an important physiological role in limiting mitochondrial O 2 consumption in tissues (Erusalimsky and Moncada, 2007). In heart muscle this effect has been shown to be associated with an increased O 2 utilization capacity, in terms of the mechanical activity per O 2 consumed (Shen et al, 2001;Misfeldt et al, 2009). Furthermore, the effects of NO on myocardial O 2 consumption appear to be prominent under hypoxia (Misfeldt et al, 2009) and may relate to the fact that NO binds competitively with O 2 to cytochrome c oxidase (Cleeter et al, 1994;Brown and Cooper, 1994;Erusalimsky and Moncada, 2007).…”

Section: Introductionmentioning

confidence: 99%

“…In heart muscle this effect has been shown to be associated with an increased O 2 utilization capacity, in terms of the mechanical activity per O 2 consumed (Shen et al, 2001;Misfeldt et al, 2009). Furthermore, the effects of NO on myocardial O 2 consumption appear to be prominent under hypoxia (Misfeldt et al, 2009) and may relate to the fact that NO binds competitively with O 2 to cytochrome c oxidase (Cleeter et al, 1994;Brown and Cooper, 1994;Erusalimsky and Moncada, 2007). As NO limits O 2 consumption, it is of interest to examine how it acts in combination with factors involved in the upregulation of the cellular energy demand.…”

Section: Introductionmentioning

confidence: 99%

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

Pedersen

Faggiano

Helbo

et al. 2010

Journal of Experimental Biology

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SUMMARYThe 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 O 2 consumption rate and isometric twitch force development in electrically paced ventricular preparations during hypoxia, and measured O 2 affinity and nitrite reductase activity of the purified heart Mbs of both species. Upon hypoxia (9% O 2 ), O 2 consumption and developed force decreased in both trout and goldfish myocardium, with trout showing a significant increase in the O 2 utilization efficiency, i.e. the ratio of twitch force to O 2 consumption, suggesting an increased anaerobic metabolism. NOS inhibition enhanced myocardial O 2 consumption and decreased efficiency, indicating that mitochondrial respiration is under a tone of NOS-produced NO. When trout myocardial twitch force and O 2 consumption are enhanced by adrenaline, this NO tone disappears. Consistent with its conversion to NO, nitrite reduced O 2 consumption and increased myocardial efficiency in trout but not in goldfish. Such a difference correlates with the lower O 2 affinity measured for trout Mb that would increase the fraction of deoxygenated heme available to catalyze the reduction of nitrite to NO. Whereas lowaffinity trout Mb would favor O 2 diffusion within cardiomyocytes at high in vivo O 2 tensions, goldfish Mb having higher O 2 affinity and higher nitrite reductase activity appears better suited to facilitate O 2 diffusion and nitrite reduction in the heart during severe hypoxia, a condition particularly well tolerated by this species.

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Seasonal acclimation and latitudinal adaptation are of the same magnitude in Mytilus edulis and Mytilus trossulus mitochondrial respiration

2017

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Nitric oxide increases myocardial efficiency in the hypoxia-tolerant turtle Trachemys scripta

Abstract: SUMMARY

Cited by 18 publications

References 41 publications

Circulating nitric oxide metabolites and cardiovascular changes in the turtleTrachemys scriptaduring normoxia, anoxia and reoxygenation

Circulating nitric oxide metabolites and cardiovascular changes in the turtleTrachemys scriptaduring normoxia, anoxia and reoxygenation

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

Seasonal acclimation and latitudinal adaptation are of the same magnitude in Mytilus edulis and Mytilus trossulus mitochondrial respiration

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