Lipid oxidation fuels recovery from exhaustive exercise in white muscle of rainbow trout

Abstract

. Lipid oxidation fuels recovery from exhaustive exercise in white muscle of rainbow trout. Am J Physiol Regulatory Integrative Comp Physiol 282: R89-R99, 2002; 10.1152/ajpregu.00238.2001.-The oxidative utilization of lipid and carbohydrate was examined in white muscle of rainbow trout (Oncorhynchus mykiss) at rest, immediately after exhaustive exercise, and for 32-h recovery. In addition to creatine phosphate and glycolysis fueling exhaustive exercise, near maximal activation of pyruvate dehydrogenase (PDH) at the end of exercise points to oxidative phosphorylation of carbohydrate as an additional source of ATP during exercise. Within 15 min postexercise, PDH activation returned to resting values, thus sparing accumulated lactate from oxidation. Glycogen synthase activity matched the rate of glycogen resynthesis and represented near maximal activation. Decreases in white muscle free carnitine, increases in long-chain fatty acyl carnitine, and sustained elevations of acetyl-CoA and acetyl carnitine indicate a rapid utilization of lipid to supply ATP for recovery. Increases in malonyl-CoA during recovery suggest that malonyl-CoA may not regulate carnitine palmitoyltransferase-1 in trout muscle during recovery, but instead it may act to elongate short-chain fatty acids for mitochondrial oxidation. In addition, decreases in intramuscular triacylglycerol and in plasma nonesterified fatty acids indicate that both endogenous and exogenous lipid fuels may be oxidized during recovery. pyruvate dehydrogenase; glycogen synthase; carbohydrate; lactate; metabolism; malonyl-coenzyme A; nonesterified fatty acids OVER THE PAST several decades many studies have examined the metabolic responses of fish white muscle to high-intensity, exhaustive exercise together with the pattern of metabolite recovery (16). These studies have led to the development of a model of fuel selection during exhaustive exercise based on hydrolysis of highenergy phosphates [i.e., creatine phosphate (CrP) and ATP] and "anaerobic" glycolysis leading to lactate accumulation. Furthermore, it has been demonstrated that there is a temporal shift in fuel selection during exhaustive exercise from an initial hydrolysis of CrP (7,8) to an activation of glycogenolysis and glycolysis (25). As a result, exhaustion in rainbow trout is characterized by a 40 to 60% decrease in white muscle ATP and CrP concentrations and up to a 90% decrease in muscle glycogen concentrations with reciprocal and stoichiometric increases in inosine monophosphate (IMP), free creatine (Cr), and lactate, respectively (e.g., Ref. 39).During recovery, pathways must be activated to resynthesize ATP, CrP, and glycogen in preparation for another possible bout of exercise. To this end, trout experience an excess postexercise O 2 consumption (EPOC) (34), in part, representing a stimulation of oxidative phosphorylation for ATP production during recovery. The tricarboxcylic acid (TCA) cycle supplies reducing equivalents for mitochondrial oxidative phosphorylation through the utilization of acetyl-Co...

Metabolic fuel kinetics in fish: swimming, hypoxia and muscle membranes

“…Therefore, fish muscle is particularly dependent on fat stores to support endurance swimming. Lipid oxidation also plays an important role after swimming to exhaustion, when it provides most of the ATP for white muscle recovery (Richards et al, 2002). Early work on the lipid kinetics of rainbow trout shows that the mobilization of fat reserves [or lipolysis measured as the rate of appearance of glycerol (R a glycerol)] and fatty acid fluxes are not stimulated by submaximal exercise like they are in mammals, even when swimming lasts for several days (Fig.…”

Ontogenesis of expression of metabolic genes and microRNAs in rainbow trout alevins during the transition from the endogenous to the exogenous feeding period

“…Alevins that develop towards an exogenous nutritional may THE JOURNAL OF EXPERIMENTAL BIOLOGY 1606 thus, through this molecular pathway, favour deposition of lipids, which has been observed in trout alevins following first feeding (F.M., unpublished data) and in the muscle of juvenile trout (Fauconneau et al, 1997). In adult trout, these stores will later fulfill metabolic demands during fasting (Jezierska et al, 1982) and exercise (Richards et al, 2002), and also play a role in cold acclimatization (Egginton et al, 2000). In order to substantiate the potential role of omy-miRNA-143 as a potential marker for the process of lipid deposition during ontogenesis, we equally investigated the expression of cd36, a fatty acid transporter with a rate-limiting function on triglyceride synthesis in adipocytes and muscle (Coburn et al, 2001; Christiaens et al, 2012), which in rainbow trout has been identified as a marker for muscular lipid deposition (Kolditz et al, 2010).…”

Fuel use during glycogenesis in rainbow trout (Oncorhynchus mykissWalbaum) white muscle studiedin vitro

“…Milligan, 1996;Richards et al, 2002a;Richards et al, 2002b). At exhaustion, glycogen, adenosine 5Ј-triphosphate (ATP) and phosphocreatine (PCr) stores in working muscle are reduced and lactate and H + levels are elevated (Richards et al, 2002a).…”

“…The current model for the restoration of muscle energy reserves in fish after exhaustive exercise suggests that in adult fish glycogen is resynthesized in situ with lactate as the main substrate (Milligan and Girard, 1993;Wang et al, 1997;Richards et al, 2002a). Glucose, the main glycogenic substrate in mammalian muscle, is probably not an important glycogenic or oxidative substrate for trout white muscle since muscle has low hexokinase activity (Knox et al, 1980;Storey, 1991) and the expression of glucose transporters in the muscle membrane is extremely low and their physiological role is unclear (Legate et al, 2001;Teerijoki et al, 2001;Capilla et al, 2002).…”