Control of glycogenosis in rainbow trout muscle during exercise

1988 ◽  
Vol 66 (2) ◽  
pp. 345-351 ◽  
Author(s):  
W. S. Parkhouse ◽  
G. P. Dobson ◽  
P. W. Hochachka

The purpose of this study was to measure and compare the in vivo levels of glycolytic pathway intermediates during high-intensity, progressive exercise in rainbow trout red and white muscle. The mass action ratios of those reactions catalyzed by the enzymes hexokinase, phosphofructokinase, and pyruvate kinase appear to be displaced far from thermodynamic equilibrium (greater than log 2) under all experimental conditions in both tissue types. Furthermore, the near-equilibrium glyceral-dehyde 3-phosphate dehydrogenase – phosphoglycerate kinase complex deviated from thermodynamic equilibrium during the exhaustive swim for white muscle and for all exercise intensities in red muscle. The mass action ratio of the combined glyceraldehyde 3-phosphate dehydrogenase – phosphoglycerate kinase/lactate dehydrogenase demonstrated displacements from thermodynamic equilibrium similar to those of the glyceraldehyde 3-phosphate dehydrogenase complex. Potential control sites were identified as phosphorylase for white muscle and hexokinase and glyceraldehyde 3-phosphate dehydrogenase – phosphoglycerate kinase for red muscle. No alterations in potential control sites were found in white muscle with changing flux rates (sustained and burst swims) provided sufficient glycogen was available as precursor. Phosphofructokinase and glyceraldehyde 3-phosphate dehydrogenase only demonstrated potential control in this tissue when glycogen content and flux rates were low (exhaustive swim). These changes coincided with substrate depletion to low levels and large declines in the ATP/ADPf ratio. Therefore, it would appear that glycogen content is the primary factor regulating glycolytic flux and control sites via alterations in adenylate levels.

1988 ◽  
Vol 254 (2) ◽  
pp. R302-R309 ◽  
Author(s):  
W. S. Parkhouse ◽  
G. P. Dobson ◽  
P. W. Hochachka

The purpose of this investigation was to examine the fuels supporting high-intensity progressive exercise and their regulation within rainbow trout. During the sustained swim, red muscle (RM) used 97% (17.5 mumol/g) of its glycogen, whereas white muscle (WM) glycogen only declined 31% (7.3 mumol/g). During the burst swim, WM glycogen content decreased 10.4 mumol/g at a rate that exceeded the sustained swim rate by 6.2-fold. Lactate content increased 11-fold at a rate 25 times its sustained swim rate. The exhaustive swim resulted in a decrease of 36.6 mumol/g in liver glycogen, whereas WM glycogen content declined to very low values and lactate reached 43 mumol/g. RM glycogen levels remained low during these exercise bouts. Phosphocreatine (PCr)-buffered ATP declines (WM 7.3-2.7 mumol/g, RM 3.4-1.6 mumol/g) with the time course of the large ATP decreases being related to near depletion of PCr. Decreases in the total adenylate pool were compensated for by the accumulation of inosine 5'-monophosphate in both tissue types. Free ADP (ADPf) contents increased in both tissues by three- to fivefold. ATP/ADPf and cytosolic phosphorylation potentials decreased from 7- to 20-fold. Cytosolic redox potential remained relatively constant at approximately 145 within both fiber types. The changes in adenine nucleotide parameters are associated with the respective activation of the different fiber types and glycolytic flux.


1981 ◽  
Vol 59 (10) ◽  
pp. 1909-1915 ◽  
Author(s):  
V. Krishna Murthy ◽  
P. Reddanna ◽  
M. Bhaskar ◽  
S. Govindappa

Freshwater fish, Tilapia mossambica (Peters), were subjected to acute exposure and acclimation to sublethal acid water (pH 4.0), and the muscle metabolism was investigated. Differential patterns of carbohydrate metabolism were witnessed in the red and white muscles in response to both acute exposure and acclimation. The glycogen content of red muscle was elevated whereas that of white muscle was depleted on acute exposure. But on acclimation, both the muscles had elevated glycogen content. The red muscle seems to mobilize carbohydrates into both hexose mono- and di-phosphate pathways, but white muscle does so only into the hexose monophosphate pathway on acclimation. In general, both the muscles exhibited suppressed glycolysis and elevated oxidative phase leading to elevated glycogen level. The muscle metabolism was oriented towards conservation of carbohydrates and lesser production of organic acids on acclimation, as a possible metabolic adaptive mechanism of the fish, enabling them to counteract the imposed acid stress.


2002 ◽  
Vol 205 (14) ◽  
pp. 2067-2077 ◽  
Author(s):  
Jeff G. Richards ◽  
Ashley J. Mercado ◽  
Cheryl A. Clayton ◽  
George J. F. Heigenhauser ◽  
Chris M. Wood

SUMMARY A biochemical approach was employed to examine the oxidative utilization of carbohydrate and lipid in red muscle of rainbow trout (Oncorhynchus mykiss) during sustained swimming at 30 and 60% of their critical swimming speed (Ucrit; for 2, 15 and 240 min) and during non-sustainable swimming at 90% Ucrit (for 2, 15 and 45 min). Measurements included pyruvate dehydrogenase (PDH) activity, creatine phosphate, ATP, glycogen, glycolytic intermediates, acetyl-CoA, acetyl-,total-, free-, short-chain fatty acyl- and long-chain fatty acyl- carnitine,intramuscular triacylglycerol and malonyl-CoA concentrations, and whole body oxygen consumption(ṀO2). During the first 2 min at 30 and 60% Ucrit, oxidation of endogenous glycogen by PDH activation increased 4- and 8-fold, respectively, yielding 1.5- to 2.5-fold increases in acetyl-CoA and 2- to 6-fold increases in acetyl-carnitine concentrations. Within 15 min, PDH activity returned to control values (153.9±30.1 nmol g-1 wet tissue min-1); after 240 min there were small 1.7- to 2.6-fold increases in long-chain fatty acyl-carnitine and approx. 50% decreases in malonyl-CoA concentrations, indicating an overall enhancement of lipid oxidation. Sustainable swimming at 30 and 60% Ucrit was further characterized by 1.5- and 2.2-fold increases in ṀO2,respectively. Non-sustainable swimming at 90% Ucrit was characterized by a sustained tenfold (approx.) elevation of red muscle PDH activity (approx. 1600 nmol g-1 wet tissue min-1). Significant 67% decreases in white muscle creatine phosphate and 73% decreases in glycogen levels, without matching increases in lactate levels, point to significant recruitment of white muscle during high-speed swimming for power production, and the potential export of white muscle lactate to red muscle for oxidation. Overall, sustainable exercise at 30 and 60%Ucrit is supported by approximately equal contributions of carbohydrate (approx. 45%) and lipid (approx. 35%) oxidation, whereas non-sustainable swimming is supported primarily by carbohydrate oxidation with only moderate contributions from lipid oxidation.


1963 ◽  
Vol 20 (1) ◽  
pp. 45-58 ◽  
Author(s):  
Hans Buttkus

The superficial red muscle of lingcod (Ophiodon elongatus) was shown to exhibit unique properties of post-mortem contraction and tension development. In comparison with white muscle, rigor contraction and isometric rigor tension in red muscle were about three times as great. The rate of contraction of the red muscle was dependent on temperature and also on the oxygen concentration in the surrounding atmosphere. The elastic modulus of the red muscle of trout and lingcod increased with increasing post-mortem time. Following the onset of rigor mortis a gradual increase in elasticity was observed. The maximum effects of contraction, tension and elasticity coincided with the onset of rigor mortis and each could therefore be used as a measure of this phenomenon. It was concluded from these experiments that stiffening of a fish with the onset of rigor mortis is not due to contraction or tension development of the muscles, but rather to their changing mechanical properties. A convenient measure of the changing mechanical properties in the muscle was the elastic modulus.Morphological differences between the very active, myoglobin rich, red muscle and the white muscle of lingcod were demonstrated by means of electron micrographs. The high glycogen content in the area of sarcoplasm of the red muscle, as indicated in electron micrographs, was confirmed by chemical analysis. Red muscle in rested fish was shown to contain from 1 to 3 times more glycogen than white muscle.


2013 ◽  
Vol 304 (11) ◽  
pp. R1036-R1043 ◽  
Author(s):  
Teye Omlin ◽  
Jean-Michel Weber

Transmembrane lactate movements are mediated by monocarboxylate transporters (MCTs), but these proteins have never been characterized in rainbow trout. Our goals were to clone potential trout MCTs, determine tissue distribution, and quantify the effects of exhausting exercise on MCT expression. Such information could prove important to understand the mechanisms underlying the classic “lactate retention ” seen in trout white muscle after intense exercise. Four isoforms were identified and partially characterized in rainbow trout: MCT1a, MCT1b, MCT2, and MCT4. MCT1b was the most abundant in heart and red muscle but poorly expressed in the gill and brain where MCT1a and MCT2 were prevalent. MCT expression was strongly stimulated by exhausting exercise in brain (MCT2: +260%) and heart (MCT1a: +90% and MCT1b: +50%), possibly to increase capacity for lactate uptake in these highly oxidative tissues. By contrast, the MCTs of gill, liver, and muscle remained unaffected by exercise. This study provides a possible functional explanation for postexercise “lactate retention” in trout white muscle. Rainbow trout may be unable to release large lactate loads rapidly during recovery because: 1) they only poorly express MCT4, the main lactate exporter found in mammalian glycolytic muscles; 2) the combined expression of all trout MCTs is much lower in white muscle than in any other tissue; and 3) exhausting exercise fails to upregulate white muscle MCT expression. In this tissue, carbohydrates act as an “energy spring” that alternates between explosive power release during intense swimming (glycogen to lactate) and recoil during protracted recovery (slow glycogen resynthesis from local lactate).


1970 ◽  
Vol 18 (8) ◽  
pp. 552-558 ◽  
Author(s):  
C. A. GILLESPIE ◽  
D. R. SIMPSON ◽  
V. R. EDGERTON

Histochemical examination of rabbit, rat, guinea pig and mouse limb skeletal muscles in our laboratory has revealed that most red muscle fibers in any given muscle stain more intensely for glycogen (periodic acid-Schiff's reaction) than white or intermediate fibers. Since most studies have concluded that white muscle has more glycogen than red muscle, this discrepancy was investigated. Eleven vastus lateralis muscles were resected from six adult male guinea pigs and cropped to yield "red," "moderate" and "white" regions. Cross-sections of each region were employed for histochemical fiber typing and the remaining pieces for biochemical glycogen analysis. These analyses have shown the red region to have significantly more glycogen (9.7 mg per g) and more red fibers (77%) than the white region (7.4 mg/g, 29%). Having essentially eliminated intermediate fibers by cropping, these findings reflect glycogen concentration in red and white muscle fibers. The existence of significant numbers of intermediate fibers usually found in red muscles may be responsible for the frequently exhibited higher glycogen content in white muscles.


1988 ◽  
Vol 255 (2) ◽  
pp. R289-R294
Author(s):  
S. P. Brooks ◽  
K. B. Storey

The effect of exercise on the binding of glycolytic enzymes to subcellular structures was examined in rainbow trout (Salmo gardneri). Both “burst” and “endurance” type exercise produced an increase of approximately 50% in the percentage of phosphofructokinase (PFK), glyceraldehyde 3-phosphate dehydrogenase (GAPDH), aldolase, and 3-phosphoglycerate kinase associated with particulate matter in white skeletal muscle. In contrast, cardiac muscle showed no change in enzyme binding when trout were exercised, suggesting that the effects seen in white muscle are related to an increased anaerobic glycolytic flux in this tissue. Modulation of binding by altered pH or calcium ion concentration was tested: a decrease in pH increased PFK binding to subcellular particles, whereas 2 mM CaCl2 decreased GAPDH binding. These results are discussed with respect to the formation of a glycolytic complex during exercise in trout white muscle.


2004 ◽  
Vol 287 (6) ◽  
pp. R1344-R1353 ◽  
Author(s):  
Jason Frolow ◽  
C. Louise Milligan

To test the hypothesis that cortisol and epinephrine have direct regulatory roles in muscle glycogen metabolism and to determine what those roles might be, we developed an in vitro white muscle slice preparation from rainbow trout ( Oncorhynchus mykiss Walbaum). In the absence of hormones, glycogen-depleted muscle slices obtained from exercised trout were capable of significant glycogen synthesis, and the amount of glycogen synthesized was inversely correlated with the initial postexercise glycogen content. When postexercise glycogen levels were <5 μmol/g, about 4.3 μmol/g of glycogen were synthesized, but when postexercise glycogen levels were >5 μmol/g, only about 1.7 μmol/g of glycogen was synthesized. This difference in the amount of glycogen synthesized was reflected in the degree of activation of glycogen synthase. Postexercise glycogen content also influenced the response of the muscle to 10−8 M epinephrine and 10−8 M dexamethasone (a glucocorticoid analog). At high glycogen levels (>5 μmol/g), epinephrine and dexamethasone stimulated glycogen phosphorylase activity and net glycogenolysis, whereas at low (<5 μmol/g) glycogen levels, glycogenesis and activation of glycogen synthase activity prevailed. These data clearly indicate not only is trout muscle capable of in situ glycogenesis, but the amount of glycogen synthesized is a function of initial glycogen content. Furthermore, whereas dexamethasone and epinephrine directly stimulate muscle glycogen metabolism, the net effect is dependent on initial glycogen content.


1989 ◽  
Vol 147 (1) ◽  
pp. 493-505 ◽  
Author(s):  
EDWARD M. GOOLISH

The scaling of anaerobic metabolism and red muscle mass was examined in rainbow trout (Salmo gairdneri) ranging in size from 2 to 1200 g. The initial rate of white muscle lactate production during maximal burst activity was significantly higher in large (28.1 cm) than in small (8.0 cm) fish. ‘Resting’ lactate concentrations in anesthetized trout (approximately 30 s of stress) increased with fish size, also reflecting higher glycolytic potential for larger fish. Maximum muscle lactate concentrations following 6min of exhaustive exercise increased from approximately 25 to 45μmolg−1 with increased fish size (= L0.36, where L is fish length). Total white muscle lactate production, including changes in muscle mass, scaled as L3.52. A scaling comparison of total anaerobic capacity with theoretically predicted power requirements indicated decreased burst swimming performance with increased size. Red muscle mass increased from approximately 1 to 3 % of body mass with increased fish size. The positive allometry in red muscle mass (= L3.62) is greater than the scaling of power requirements during aerobic swimming predicted from hydrodynamic theory, and may provide compensation for decreased mass-specific power output with increased size.


Author(s):  
I. A. Johnston ◽  
G. Goldspink

The locomotor roles of the myotomal muscles of fish are dependent on swimming speed. The mean maximum sustained swimming speed for coalfish (Gadus virens L.) during a 6-h period in an experimental exercise chamber was determined using a fixedvelocity technique and found to be 4 bodylengths/s. Biochemical measurements were made on the concentration of glycogen and lactate in the red muscle and white muscle at a series of known swimming speeds. Evidence is provided that red muscle alone is used at speeds below 2 bodylengths/s. The fall in concentration of red muscle glycogen was directly proportional to increased swimming speed. At speeds in excess of 2 bodylengths/s a statistically significant increase in lactate concentration occurred in the white muscle fibres. A reduction in glycogen content of the white muscle was also noted at speeds at and above the estimated mean sustained swimming speed. These results are discussed in the light of the current ideas pertaining to the division of labour between myotomal muscles in fish.


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