TY - JOUR
T1 - Roles of nitric oxide, nitrite and myoglobin on myocardial efficiency in trout (Oncorhynchus mykiss) and goldfish (Carassius auratus): implications for hypoxia tolerance
AU - Pedersen, Claus Lunde
AU - Faggiano, Serena
AU - Helbo, Signe
AU - Gesser, Hans
AU - Fago, Angela
PY - 2010
Y1 - 2010
N2 - 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.
AB - 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.
U2 - 10.1242/jeb.041624
DO - 10.1242/jeb.041624
M3 - Journal article
C2 - 20675545
SN - 0022-0949
VL - 213
SP - 2755
EP - 2762
JO - Journal of Experimental Biology
JF - Journal of Experimental Biology
ER -