Roles of nitric oxide, nitrite and myoglobin on myocardial efficiency in trout (Oncorhynchus mykiss) and goldfish (Carassius auratus): implications for hypoxia tolerance.
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 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 low-affinity 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.
Pedersen
Claus Lunde
CL
Department of Biological Sciences, Universitetsparken, Aarhus University, DK-8000, Aarhus C, Denmark.
Faggiano
Serena
S
Helbo
Signe
S
Gesser
Hans
H
Fago
Angela
A
D000818:Animals; D006054:Goldfish / Q000378:metabolism*; D000860:Hypoxia / Q000378:metabolism*; D009200:Myocardial Contraction / Q000502:physiology; D009206:Myocardium / Q000378:metabolism*; D009211:Myoglobin / Q000378:metabolism*; D009569:Nitric Oxide / Q000378:metabolism*; D019001:Nitric Oxide Synthase / Q000378:metabolism; D009573:Nitrites / Q000378:metabolism*; D017686:Oncorhynchus mykiss / Q000378:metabolism*; D010101:Oxygen Consumption / Q000502:physiology
D009211:Myoglobin; D009573:Nitrites; D009569:Nitric Oxide; D019001:Nitric Oxide Synthase