Force development, energy state and ATP production of cardiac muscle from turtles and trout during normoxia and severe hypoxia

Abstract

SUMMARYThe effects of hypoxia on energy economy of cardiac muscle were compared between the hypoxia-tolerant freshwater turtle at 20°C and the hypoxia-sensitive rainbow trout at 15°C. Isolated ventricular preparations were left either at rest or stimulated at 30 min-1 to develop isometric twitch force. Under oxygenated conditions, twitch force and oxygen consumption were similar for the two species. Overall metabolism was reduced during severe hypoxia in both resting and stimulated preparations and under these conditions most of the ATP production was derived from anaerobic metabolism. During hypoxia, a metabolic depression of approximately 2/3 occurred for non-contractile processes in both turtle and trout preparations. During hypoxia, lactate production and residual oxygen consumption were similar in turtle and trout. Cellular energy state and phosphorylation potential decreased during severe hypoxia in both species and this reduction was more severe in preparations stimulated to contraction. However, in turtle ventricular preparations the energy state and phosphorylation potential stabilised at higher levels than in trout, and turtle preparations also maintained a higher twitch force throughout the hypoxic period. Moreover,twitch force relative to total ATP hydrolysis was markedly increased during hypoxia in turtle while this ratio was unchanged for trout. The main findings of this study are: (1) cellular energy liberation and the energy demand of non-contractile processes decreased to similar levels in hypoxic turtle and trout myocardium; (2) turtle myocardium maintained a substantially higher cellular energy state and twitch force development than trout myocardium during hypoxia and (3) the ratio of twitch force to ATP hydrolysis increased during hypoxia in turtle but was unchanged in trout. It is possible that this superior economy of the contracting turtle myocardium contributes to the remarkable hypoxia tolerance of freshwater turtles.

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

“…Shi et al, 1999;Jackson, 2002). Accordingly, heart muscle from turtles (Trachemys scripta and Chrysemys picta) shows an excellent maintenance of contractility and energy state when subjected to severe hypoxia (Overgaard and Gesser, 2004;Overgaard et al, 2007). The finding that hypoxia, compared with full oxygenation, increased twitch force development relative to the energy liberated, as assessed by O 2 consumption and lactate production (Overgaard and Gesser, 2004), is of particular interest in the present study as NO may contribute to this process.…”

“…Accordingly, heart muscle from turtles (Trachemys scripta and Chrysemys picta) shows an excellent maintenance of contractility and energy state when subjected to severe hypoxia (Overgaard and Gesser, 2004;Overgaard et al, 2007). The finding that hypoxia, compared with full oxygenation, increased twitch force development relative to the energy liberated, as assessed by O 2 consumption and lactate production (Overgaard and Gesser, 2004), is of particular interest in the present study as NO may contribute to this process. For these reasons, we examined the influence of NO on mechanical performance, recorded as twitch force and resting tension, and also on cellular energy liberation, in terms of O 2 consumption and lactate production, in turtle ventricular muscle under exposure to full oxygenation and hypoxia.…”

“…The experimental setup has been described previously (Kalinin and Gesser, 2002;Overgaard and Gesser, 2004). Briefly, a single ringshaped preparation was mounted on two hooks.…”

Functional and energetic characterization of P-gp-mediated doxorubicin transport in rainbow trout (Oncorhynchus mykiss) hepatocytes

“…A study in 2004 examined the effects of hypoxia on cellular energy state in cardiac muscle extracts in the hypoxia tolerant freshwater turtle and the hypoxia sensitive rainbow trout. These authors reported decreases in PP of 94% and 57% in the trout and turtle respectively during a period of severe hypoxia (Overgaard and Gesser, 2004).…”

“…However, adenlyate ratios such as adenylate energy charge (AEC), and phosphorylation potential (PP) have been shown to be better indicators of cellular energy status (LeBras, 1995;Li et aI., 2005;Overgaard and Gesser, 2004). AEC is an indicator of the degree of phosphorylation of the ATP-ADP-AMP system, and is calculated from the following ratio:…”