Glycogen 'seas,' glycogen bodies, and glycogen granules in heart and skeletal muscle of two air-breathing, burrowing fishes

1978 ◽  
Vol 56 (4) ◽  
pp. 774-786 ◽  
Author(s):  
P. W. Hochachka ◽  
W. C. Hulbert
Keyword(s):  
Energy Source ◽  
Skeletal Muscle ◽  
White Muscle ◽  
Large Diameter ◽  
The Other ◽  
Air Breathing ◽  
Fermentative Metabolism ◽  
Red Muscle ◽  
Carbon Reservoir ◽  
Α Particles

Studies of the ultrastructures of heart, white muscle, and red muscle of two air-breathing, burrowing Amazon fishes, Lepidosiren paradoxa and Synbranchus marmarotus, indicated an overwhelming dependence upon glycogen as a storage carbon and energy source. In lungfish white muscle, unusually high quantities of glycogen were packaged as large-diameter rosettes or α-particles, typical of organs such as the liver in other species. In lungfish red muscle, glycogen was stored as the usual smaller β-particles, either randomly dispersed or organized into membrane–glycogen complexes called glycogen bodies. The hearts of both species also displayed numerous glycogen bodies, the membrane–glycogen complexes apparently being formed from specialized regions of the interfibrillar sarcoplasmic reticulum. These immense glycogen depots could be mobilized to support either oxidative or fermentative metabolism. However, neither mitochondrial abundance nor the levels of enzymes in oxidative metabolism were abnormally high compared with other fishes. Heart lactate dehydrogenase, on the other hand, occurred at higher levels than thus far found in any vertebrate heart, suggesting that heart glycogen bodies in these species serve primarily as a carbon reservoir for emergency use under conditions of O2 lack.

Metabolic biochemistry of water- vs. air-breathing fishes: muscle enzymes and ultrastructure

1978 ◽  
Vol 56 (4) ◽  
pp. 736-750 ◽  
Author(s):  
P. W. Hochachka ◽  
M. Guppy ◽  
H. E. Guderley ◽  
K. B. Storey ◽  
W. C. Hulbert
Keyword(s):  
White Muscle ◽  
Large Diameter ◽  
Oxidative Capacity ◽  
The Body ◽  
Muscle Enzymes ◽  
Air Breathing ◽  
Red Muscle ◽  
Phosphofructokinase Activity ◽  
Metabolic Biochemistry ◽  
Myotomal Muscle

To delineate what modifications in muscle metabolic biochemistry correlate with transition to air breathing in fishes, the myotomal muscles of aruana, an obligate water breather, and Arapaima, a related obligate air breather, were compared using electron microscopy and enzyme methods. White muscle in both species maintained a rather similar ultrastructure, characterized by large-diameter fibers, very few mitochondria, and few capillaries. However, aruana white muscle displayed nearly fivefold higher levels of pyruvate kinase, threefold higher levels of muscle-type lactate dehydrogenase, and a fourfold higher ratio of fructose diphosphatase –phosphofructokinase activity; at the same time, enzymes in aerobic metabolism occurred at about one-half the levels in Arapaima. Red muscle was never found in the myotomal mass of aruana, but in Arapaima, red muscle was present and seemed fueled by glycogen, lipid droplets never being observed. From these and other data, it was concluded that in myotomal muscle two processes correlate with the transition to air breathing in Amazon osteoglossids: firstly, an emphasis in oxidative metabolism, and secondly, a retention of red muscle. However, compared with more active water-breathing species, Arapaima sustains an overall dampening of enzyme activities in its myotomal muscle, which because of the large myotome mass explains why its overall metabolic rate is relatively low. By keeping the oxidative capacity of its myotomal muscle low, Arapaima automatically conserves O2 either for a longer time or for other more O2-requiring organs in the body, a perfectly understandable strategy for an air-breathing, diving fish, comparable with that observed in other diving vertebrates. A similar comparison was also made of two erythrinid fishes, one that skimmed the O2-rich surface layers of water and one that obtained three quarters of its O2 from water, one quarter from air. Ultrastructural and enzyme data led to the unexpected conclusion that the surface skimmer sustained a higher oxidative capacity in its myotomal muscles than did the facultative air breather.

scholarly journals Low intrinsic running capacity is associated with reduced skeletal muscle substrate oxidation and lower mitochondrial content in white skeletal muscle

2011 ◽  
Vol 300 (4) ◽  
pp. R835-R843 ◽  
Author(s):  
Donato A. Rivas ◽  
Sarah J. Lessard ◽  
Misato Saito ◽  
Anna M. Friedhuber ◽  
Lauren G. Koch ◽  
...  
Keyword(s):  
Skeletal Muscle ◽  
Insulin Sensitivity ◽  
Aerobic Capacity ◽  
Artificial Selection ◽  
White Muscle ◽  
Metabolic Diseases ◽  
Metabolic Health ◽  
Mitochondrial Content ◽  
Red Muscle ◽  
Selection For

Chronic metabolic diseases develop from the complex interaction of environmental and genetic factors, although the extent to which each contributes to these disorders is unknown. Here, we test the hypothesis that artificial selection for low intrinsic aerobic running capacity is associated with reduced skeletal muscle metabolism and impaired metabolic health. Rat models for low- (LCR) and high- (HCR) intrinsic running capacity were derived from genetically heterogeneous N:NIH stock for 20 generations. Artificial selection produced a 530% difference in running capacity between LCR/HCR, which was associated with significant functional differences in glucose and lipid handling by skeletal muscle, as assessed by hindlimb perfusion. LCR had reduced rates of skeletal muscle glucose uptake (∼30%; P = 0.04), glucose oxidation (∼50%; P = 0.04), and lipid oxidation (∼40%; P = 0.02). Artificial selection for low aerobic capacity was also linked with reduced molecular signaling, decreased muscle glycogen, and triglyceride storage, and a lower mitochondrial content in skeletal muscle, with the most profound changes to these parameters evident in white rather than red muscle. We show that a low intrinsic aerobic running capacity confers reduced insulin sensitivity in skeletal muscle and is associated with impaired markers of metabolic health compared with high intrinsic running capacity. Furthermore, selection for high running capacity, in the absence of exercise training, endows increased skeletal muscle insulin sensitivity and oxidative capacity in specifically white muscle rather than red muscle. These data provide evidence that differences in white muscle may have a role in the divergent aerobic capacity observed in this generation of LCR/HCR.

EFFECTS OF FEEDING AND FOOD DEPRIVATION ON OXYGEN CONSUMPTION, MUSCLE PROTEIN CONCENTRATION AND ACTIVITIES OF ENERGY METABOLISM ENZYMES IN MUSCLE AND BRAIN OF SHALLOW-LIVING (SCORPAENA GUTTATA) AND DEEP-LIVING (SEBASTOLOBUS ALASCANUS) SCORPAENID FISHES

1993 ◽  
Vol 181 (1) ◽  
pp. 213-232 ◽  
Author(s):  
T. H. Yang ◽  
G. N. Somero
Keyword(s):  
Skeletal Muscle ◽  
Metabolic Rate ◽  
Food Deprivation ◽  
Enzyme Activities ◽  
Protein Concentration ◽  
White Muscle ◽  
Muscle Protein ◽  
Metabolism Enzymes ◽  
Red Muscle ◽  
Ad Libitum

The effects of feeding and fasting were examined on the deep-living short-spine thornyhead (Sebastolobus alascanus) and the confamilial shallow-living spotted scorpionfish (Scorpaena guttata) to determine whether the low metabolic rate of the deeper-living species was in part a consequence of food deprivation in its habitat. Laboratory acclimation for periods of 90–115 days under either ad libitum feeding or complete fasting did not lead to similar rates of respiration in individuals of the two species held under identical conditions. Respiration of fish fed ad libitum was 52 % (S. guttata) or 68 % (S. alascanus) higher than for fasted fish of the same species. Furthermore, the metabolic rates of freshly collected specimens of S. alascanus resembled those of laboratory-fasted fish. In white skeletal muscle, both total protein concentration and the activities of four enzymes of ATP metabolism, lactate dehydrogenase (LDH) and pyruvate kinase (PK) of glycolysis, malate dehydrogenase (MDH) and citrate synthase (CS, a citric acid cycle indicator), were lower in S. alascanus than in S. guttata. Within a species, protein concentration and activities of the four enzymes in white muscle, but not in brain, were higher in fed than in starved fish, although these differences were greater in S. alascanus than in S. guttata. During fasting, LDH and PK activity in white muscle of S. alascanus decreased much more than MDH and CS activity; decreases in enzyme activities in red muscle were smaller than those in white muscle. Activities of enzymes in white skeletal muscle of field-collected S. alascanus generally resembled those of the fasted specimens. In contrast, red muscle of field- collected S. alascanus, compared with that of either fed or starved laboratory-held specimens, had a highly glycolytic poise (high LDH and PK activities relative to MDH and CS activities), which may suggest that muscle enzyme activities in the field-collected fish reflect adaptation to the low oxygen level in its adult habitat, the oxygen minimum layer. The strong correlations found between tissue biochemical properties and respiration rate allow us to develop a predictive index for metabolic rate from simple biochemical analyses, e.g. white muscle protein content or CS activity. We conclude that the low metabolic rate of S. alascanus is due to at least four depth-related factors: reduced abundance of food, low temperature, low ambient oxygen concentration and darkness, which may select for reduced locomotory activity.

scholarly journals Role of insulin on exercise-induced GLUT-4 protein expression and glycogen supercompensation in rat skeletal muscle

2004 ◽  
Vol 96 (2) ◽  
pp. 621-627 ◽  
Author(s):  
Chia-Hua Kuo ◽  
Hyonson Hwang ◽  
Man-Cheong Lee ◽  
Arthur L. Castle ◽  
John L. Ivy
Keyword(s):  
Skeletal Muscle ◽  
Protein Expression ◽  
Muscle Glycogen ◽  
White Muscle ◽  
Insulin Response ◽  
Exercise Session ◽  
Carbohydrate Supplementation ◽  
Glut 4 ◽  
Red Muscle

The purpose of this study was to investigate the role of insulin on skeletal muscle GLUT-4 protein expression and glycogen storage after postexercise carbohydrate supplementation. Male Sprague-Dawley rats were randomly assigned to one of six treatment groups: sedentary control (Con), Con with streptozocin (Stz/C), immediately postexercise (Ex0), Ex0 with Stz (Stz/Ex0), 5-h postexercise (Ex5), and Ex5 with Stz (Stz/Ex5). Rats were exercised by swimming (2 bouts of 3 h) and carbohydrate supplemented immediately after each exercise session by glucose intubation (1 ml of a 50% wt/vol). Stz was administered 72-h before exercise, which resulted in hyperglycemia and elimination of the insulin response to the carbohydrate supplement. GLUT-4 protein of Ex0 rats was 30% above Con in fast-twitch (FT) red and 21% above Con in FT white muscle. In Ex5, GLUT-4 protein was 52% above Con in FT red and 47% above Con in FT white muscle. Muscle glycogen in FT red and white muscle was also increased above Con in Ex5 rats. Neither GLUT-4 protein nor muscle glycogen was increased above Con in Stz/Ex0 or Stz/Ex5 rats. GLUT-4 mRNA in FT red muscle of Ex0 rats was 61% above Con but only 33% above Con in Ex5 rats. GLUT-4 mRNA in FT red muscle of Stz/C and Stz/Ex0 rats was similar but significantly elevated in Ex5/Stz rats. These results suggest that insulin is essential for the increase in GLUT-4 protein expression following postexercise carbohydrate supplementation.

A METHODOLOGICAL STUDY IN MEASURING T3 AND T4 CONCENTRATION IN RED AND WHITE SKELETAL MUSCLE AND PLASMA OF EUTHYROID RATS

1979 ◽  
Vol 90 (1) ◽  
pp. 81-89 ◽  
Author(s):  
J. W. Janssen ◽  
C. van Hardeveld ◽  
A. A. H. Kassenaar
Keyword(s):  
Skeletal Muscle ◽  
White Muscle ◽  
Female Rats ◽  
Normal Female ◽  
Tissue Samples ◽  
Tissue Extracts ◽  
Red Muscle ◽  
The Mean ◽  
Ethanol Extracts ◽  
Altered Thyroid

ABSTRACT T3 and T4 concentrations were determined in plasma and red and white skeletal muscle of the rat. Because of the small tissue samples (± 300 mg), the ultra-sensitive Wick radioimmunoassay (RIA) for serum was adapted for determination in ethanol extracts. The dilution curves of the plasma and tissue extracts showed excellent parallelism with the standard curves for both T3 and T4. The mean T4 level found in female rats (n = 6) was 22.6 ± 5.2 ng/ml in plasma and did not differ significantly between red (1.85 ± 0.28 ng/g) and white (1.90 ± 0.25 ng/g) skeletal muscle. The mean T3 level in 11 normal female rats was 0.629 ± 0.098 ng/ml in the plasma and was significantly higher in the red muscle (2.07 ± 0.26 ng/g) than in the white muscle (1.65 ± 0.20 ng/g). The higher T3 levels found in the red muscle as compared with the white muscle may help to elucidate the different responsiveness of these muscle types observed in altered thyroid states.

Physiological regulation of the expression of a GLUT4 homolog in fish skeletal muscle

2002 ◽  
Vol 283 (1) ◽  
pp. E44-E49 ◽  
Author(s):  
Encarnación Capilla ◽  
Mònica Dı́az ◽  
Joaquim Gutiérrez ◽  
Josep V. Planas
Keyword(s):  
Skeletal Muscle ◽  
Plasma Levels ◽  
White Muscle ◽  
Glucose Transporter ◽  
Physiological Regulation ◽  
Low Protein ◽  
Red Muscle ◽  
High Sequence Homology ◽  
Trout Muscle

We have recently cloned a glucose transporter from brown trout muscle (btGLUT) with high sequence homology to mammalian GLUT4 that is predominantly expressed in red and white skeletal muscle, the two major sites of glucose uptake in trout. To study the physiological regulation of this putative fish GLUT4, we have investigated the expression of btGLUT in red and white skeletal muscle of trout in which blood insulin levels have been altered experimentally. The expression of btGLUT in red muscle increased significantly when insulin plasma levels were elevated by either insulin or arginine treatment and decreased significantly when insulin plasma levels were reduced either by fasting or by feeding a low-protein, high-carbohydrate diet. In contrast, the expression of btGLUT in white muscle was not affected by changes in the plasma levels of insulin. These results strongly suggest that insulin could be regulating the expression of btGLUT in trout red muscle in vivo and set the ground to test the hypothesis that btGLUT may be considered a GLUT4 homolog in fish.

scholarly journals Effect of diabetes and fasting on GLUT-4 (muscle/fat) glucose-transporter expression in insulin-sensitive tissues. Heterogeneous response in heart, red and white muscle

1992 ◽  
Vol 282 (3) ◽  
pp. 765-772 ◽  
Author(s):  
M Camps ◽  
A Castelló ◽  
P Muñoz ◽  
M Monfar ◽  
X Testar ◽  
...  
Keyword(s):  
Skeletal Muscle ◽  
Adipose Tissue ◽  
Brown Adipose Tissue ◽  
White Adipose Tissue ◽  
White Muscle ◽  
Glucose Transporter ◽  
Mrna Levels ◽  
Glut 4 ◽  
Brown Adipose ◽  
Red Muscle

1. GLUT-4 glucose-transporter protein and mRNA levels were assessed in heart, red muscle and white muscle, as well as in brown and white adipose tissue from 7-day streptozotocin-induced diabetic and 48 h-fasted rats. 2. In agreement with previous data, white adipose tissue showed a substantial decrease in GLUT-4 mRNA and protein levels in response to both diabetes and fasting. Similarly, GLUT-4 mRNA and protein markedly decreased in brown adipose tissue in both insulinopenic conditions. 3. Under control conditions, the level of expression of GLUT-4 protein content differed substantially in heart, red and white skeletal muscle. Thus GLUT-4 protein was maximal in heart, and red muscle had a greater GLUT-4 content compared with white muscle. In spite of the large differences in GLUT-4 protein content, GLUT-4 mRNA levels were equivalent in heart and red skeletal muscle. 4. In heart, GLUT-4 mRNA decreased to a greater extent than GLUT-4 protein in response to diabetes and fasting. In contrast, red muscle showed a greater decrease in GLUT-4 protein than in mRNA in response to diabetes or fasting, and in fact no decrease in GLUT-4 mRNA content was detectable in fasting. On the other hand, preparations of white skeletal muscle showed a substantial increase in GLUT-4 mRNA under both insulinopenic conditions, and that was concomitant to either a modest decrease in GLUT-4 protein in diabetes or to no change in fasting. 5. These results indicate that (a) the effects of diabetes and fasting are almost identical and lead to changes in GLUT-4 expression that are tissue-specific, (b) white adipose tissue, brown adipose tissue and heart respond similarly to insulin deficiency by decreasing GLUT-4 mRNA to a larger extent than GLUT-4 protein, and (c) red and white skeletal muscle respond to insulinopenic conditions in a heterogeneous manner which is characterized by enhanced GLUT-4 mRNA/protein ratios.

A higher mitochondrial content is associated with greater oxidative damage, oxidative defenses, protein synthesis and ATP turnover in resting skeletal muscle

2021 ◽  
Vol 224 (19) ◽  
Author(s):  
Julie M. Neurohr ◽  
Erik T. Paulson ◽  
Stephen T. Kinsey
Keyword(s):  
Skeletal Muscle ◽  
Oxidative Damage ◽  
Aerobic Capacity ◽  
Protein Turnover ◽  
White Muscle ◽  
Primary Source ◽  
Volume Density ◽  
Mitochondrial Density ◽  
Atp Turnover ◽  
Red Muscle

ABSTRACT An unavoidable consequence of aerobic metabolism is the production of reactive oxygen species (ROS). Mitochondria have historically been considered the primary source of ROS; however, recent literature has highlighted the uncertainty in primary ROS production sites and it is unclear how variation in mitochondrial density influences ROS-induced damage and protein turnover. Fish skeletal muscle is composed of distinct, highly aerobic red muscle and anaerobic white muscle, offering an excellent model system in which to evaluate the relationship of tissue aerobic capacity and ROS-induced damage under baseline conditions. The present study used a suite of indices to better understand potential consequences of aerobic tissue capacity in red and white muscle of the pinfish, Lagodon rhomboides. Red muscle had a 7-fold greater mitochondrial volume density than white muscle, and more oxidative damage despite also having higher activity of the antioxidant enzymes superoxide dismutase and catalase. The dominant protein degradation system appears to be tissue dependent. Lysosomal degradation markers and autophagosome volume density were greater in white muscle, while ubiquitin expression and 20S proteasome activity were significantly greater in red muscle. However, ubiquitin ligase expression was significantly higher in white muscle. Red muscle had a more than 2-fold greater rate of translation and total ATP turnover than white muscle, results that may be due in part to the higher mitochondrial density and the associated increase in oxidative damage. Together, these results support the concept that an elevated aerobic capacity is associated with greater oxidative damage and higher costs of protein turnover.

EVIDENCE FOR A DIFFERENT RESPONSE OF RED AND WHITE SKELETAL MUSCLE OF THE RAT IN DIFFERENT THYROID STATES

1978 ◽  
Vol 87 (4) ◽  
pp. 768-775 ◽  
Author(s):  
J. W. Janssen ◽  
C. van Hardeveld ◽  
A. A. H. Kassenaar
Keyword(s):  
Skeletal Muscle ◽  
Body Weight ◽  
Weight Gain ◽  
Protein Content ◽  
White Muscle ◽  
Mitochondrial Protein ◽  
The Body ◽  
Mitochondrial Enzymes ◽  
Muscle Weight ◽  
Red Muscle

ABSTRACT The influence of thyroid hormone depletion and experimental hyperthyroidism on red and white skeletal muscle of the rat during periods of 2, 4 and 8 weeks were studied. Body weight, muscle weight, mitochondrial protein content, and specific activities of the mitochondrial enzymes α-glycerophosphate dehydrogenase (EC 1.1.99.5) (α-GPD) and succinate dehydrogenase (EC 1.3.99.1) (SDH) were used as parameters. The largest differences in body weight gain and muscle weight gain (both red and white muscle) in the hypothyroid rats were seen after 8 weeks of T4 treatment. In the hyperthyroid rats the weight of the red muscle and the ratio of the red muscle weight to the body weight increased, whereas the white muscle weight and the ratio of the white muscle weight to the body weight decreased relative to the control animals. In hypothyroid rats the mitochondrial protein content was lowered in both red and white muscle, the specific α-GPD activity only in the latter. No changes in specific SDH activity were observed in either type of muscle. The hyperthyroid rats showed an increase in the mitochondrial protein content and the specific α-GPD and SDH activity in the red muscle, whereas no significant changes were observed in the white muscle. The changes in the parameters under study show that the effect of the thyroid state differs in red and white muscle. An explanation for a possibly greater sensitivity of red than of white muscle to thyroid hormones is discussed.

Plasma catecholamine and corticosterone and their in vitro effects on lizard skeletal muscle lactate metabolism

1993 ◽  
Vol 265 (3) ◽  
pp. R632-R639 ◽  
Author(s):  
T. T. Gleeson ◽  
P. M. Dalessio ◽  
J. A. Carr ◽  
S. J. Wickler ◽  
R. S. Mazzeo
Keyword(s):  
Skeletal Muscle ◽  
White Muscle ◽  
Plasma Catecholamines ◽  
Plasma Catecholamine ◽  
Lactate Metabolism ◽  
Lactate Oxidation ◽  
Muscle Lactate ◽  
Glucose Incorporation ◽  
Red Muscle

Lizard skeletal muscles utilize primarily lactate as a gluconeogenic substrate for glycogen replenishment following exercise. To understand the influence of selected hormones on this process, we measured changes in plasma catecholamines and corticosterone resulting from exercise in the lizard Dipsosaurus dorsalis and then investigated the physiological effects of those hormones on skeletal muscle lactate and glucose metabolism in vitro. Plasma epinephrine (Epi), norepinephrine, and corticosterone (Cort) increased 5.8, 10.2, and 2.2 times, respectively, after 5 min of exhaustive exercise. Epi and Cort levels remained elevated after 2 h of recovery. Skeletal muscle fiber bundles isolated from the red and white regions of the iliofibularis muscle were incubated 2 h at 40 degrees C in the presence of postexercise concentrations of [14C]lactate (15 mM) and glucose (8.5 mM) in the presence and absence of Epi or Cort. Red muscle oxidized both substrates at 2-3 times the rate of white muscle, and both red and white fibers oxidized lactate at 5-10 times the rate of glucose oxidation. Epi had a stimulatory effect on lactate oxidation by white muscle. Lactate incorporation into glycogen proceeded at 2-3 times the rate of glucose incorporation in both muscle types, with rates in red muscle again 2-3 times that for white muscle. Epi stimulated lactate carbon incorporation into glycogen by 50-140% in both red and white muscle but had no effect on glucose incorporation into glycogen in either tissue. We interpret these data as evidence that epinephrine stimulates lactate removal by skeletal muscle. Cort had no effect on lactate metabolism in either muscle type.(ABSTRACT TRUNCATED AT 250 WORDS)

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