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First published online June 15, 2007
Journal of Experimental Biology 210, 2346-2351 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.002857
Physiological regulation of glucose transporter (GLUT4) protein content in brown trout (Salmo trutta) skeletal muscle
Departament de Fisiologia, Facultat de Biologia, Universitat de Barcelona, 08028 Barcelona, Spain
Author for correspondence (e-mail:
jplanas{at}ub.edu)
Accepted 18 April 2007
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Summary |
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 TOP Summary IntroductionMaterials and methodsResultsDiscussionReferences |
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Key words: GLUT4, insulin, muscle, protein, trout
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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; Moon, 2001)
in view of the fact that in various fish species a glucose load results in
persistent hyperglycemia (Blasco et al.,
1996; Legate et al.,
2001; Palmer and Ryman,
1972; Wright et al.,
1998). Since teleost fish have been shown to have functional
insulin receptors and insulin involved in the postprandial regulation of
circulating glucose levels (Mommsen and
Plisetskaya, 1991; Planas et
al., 2000c), some authors pointed to a possible lack of an
insulin-regulated glucose transporter as an explanation for the glucose
intolerance of teleost fish (Wright et
al., 1998). However, our group has identified GLUT4-homologs in
brown trout (btGLUT4) (Planas et al.,
2000a) and coho salmon (okGLUT4)
(Capilla et al., 2004) that are
expressed in skeletal muscle and adipose tissue, among other tissues.
In mammals, GLUT4 appears to be essential for the maintenance of glucose
homeostasis because it mediates the action of insulin by enhancing the uptake
of glucose by peripheral tissues in postprandial conditions
(Watson and Pessin, 2006). By
expressing okGLUT4 in Xenopus oocytes, we have recently shown that
okGLUT4 is a functional glucose transporter with similar biochemical
properties to mammalian GLUT4 but with a lower affinity for glucose
(Capilla et al., 2004).
Furthermore, both btGLUT4 and okGLUT4 have been shown to be regulated by
insulin, providing the first evidence for the existence of an
insulin-regulated glucose transporter in fish. Our group recently reported
that insulin regulates the subcellular localization of okGLUT4 when expressed
in 3T3-L1 adipocytes by stimulating its translocation to the plasma membrane
(Capilla et al., 2004). In
addition, we have studied the physiological regulation of btGLUT4 gene
expression in vivo in trout skeletal muscle
(Capilla et al., 2002), because
skeletal muscle is the most important tissue for regulated glucose uptake in
fish (Blasco et al., 1996). The
results from our previous studies indicate that btGLUT4 mRNA levels in the
slow aerobic red muscle, but not in the fast anaerobic white muscle, correlate
with the levels of insulin in the blood in brown trout. We hypothesized that
insulin might regulate GLUT4 mRNA expression in vivo specifically in
red muscle and that this may be in relation to the particular metabolic
characteristics of this type of muscle in fish. However, since the
physiological regulation of fish GLUT4 protein levels is not known to date in
either type of muscle, it is not possible to conclude that changes in mRNA
levels will result in changes in the amount of btGLUT4 protein in skeletal
muscle. Therefore, the purpose of the present study was to analyze the changes
in btGLUT4 protein content in brown trout red and white skeletal muscle in
different experimental situations known to alter the circulating levels of
insulin and to determine whether btGLUT4 mRNA and protein levels are
correlated in vivo.
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Materials and methods |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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In vivo experiments
Fasting
Brown trout were fed daily with a commercial diet (control; N=6)
or deprived of food for 45 days (fasted; N=6). This period of fasting
has been shown not to be life threatening
(Navarro and Gutiérrez,
1995) and effective in decreasing insulin plasma levels
(Baños et al., 1999;
Capilla et al., 2002;
Planas et al., 2000b) and
btGLUT4 mRNA expression in skeletal muscle in this species
(Capilla et al., 2002). After
the 45-day period, animals were anesthetized in 3-aminobenzoic acid ethyl
ester (0.1 g l-1; Sigma, Tres Cantos, Spain) dissolved in fresh
water and subsequently sacrificed by a blow to the head. Tissue samples of red
and white muscle were excised, collected, rapidly frozen in liquid nitrogen
and stored at -80°C until processed. Red muscle samples were taken from
the midsection of the lateral line and white muscle samples were taken from
the anterior dorsal musculature, and care was taken to avoid
cross-contaminating the two different muscle types.
Insulin treatment
One group of brown trout (N=6) received an intraperitoneal
injection of porcine insulin (1.7 µg/100 g fish; Sigma) after an overnight
fast, and another group (control; N=6) received an injection with the
vehicle (saline) under the same conditions as the insulin-injected group.
Although a heterologous insulin was used for this experiment, previous studies
have shown that mammalian insulin can be used to study the effects of insulin
in fish because it binds fish insulin receptors equally well as fish insulin
(Gutiérrez et al.,
1995; Gutiérrez and
Plisetskaya, 1991) and because it has a similar hypoglycemic
activity in fish (Plisetskaya et al.,
1985). Twenty-four hours after the injection, samples of red and
white muscle were obtained as described in the fasting experiment.
Arginine treatment
One group of brown trout (N=10) received an intraperitoneal
injection of L-arginine (6.6 µmol g-1 fish; Sigma) after an
overnight fast. Another group of brown trout (N=10) received one
injection of the vehicle (saline) under the same conditions as the
arginine-injected group. Arginine is a potent secretagogue of insulin in
salmonid fish (Baños et al.,
1999; Capilla et al.,
2002; Mommsen and Plisetskaya,
1991; Planas et al.,
2000b). Twenty-four hours after the injection, samples of red and
white muscle were obtained as described in the fasting experiment.
In all the experiments, blood samples were obtained from the caudal vein of the anesthetized fish and were immediately centrifuged at 700 g for 10 min. Plasma fractions were collected and stored at -80°C until analyzed. In the insulin treatment experiment, blood samples were obtained at 6 h and 24 h after the injection.
Preparation of total membrane fractions from skeletal muscle
Total membrane fractions from brown trout skeletal muscle were obtained as
described by Muñoz et al.
(Muñoz et al., 1996).
One gram of skeletal muscle was homogenized with a Polytron in 10 volumes of
homogenization buffer (25 mmol l-1 Hepes, 4 mmol l-1
EDTA, 250 mmol l-1 sucrose, 25 mmol l-1 benzamidine, 0.2
mmol l-1 phenylmethylsulphonyl fluoride, 1 µmol l-1
leupeptin, 1 µmol l-1 pepstatin, 1 unit ml-1
aprotinin, pH 7.4), and the homogenate was centrifuged at 15 000
g for 20 min at 4°C. The supernatant was recovered and KCl
was added to a final concentration of 0.8 mol l-1. The supernatant
was incubated for 30 min at 4°C with agitation and subsequently
centrifuged at 200 000 g for 90 min at 4°C. The membrane
pellet was resuspended in homogenization buffer and stored at -80°C.
Protein concentration was determined by the Bradford method
(Bradford, 1976).
Electrophoresis and immunoblotting
Total membrane samples (25 µg) were diluted in Laemmli sample buffer and
heated for 5 min at 95°C. Proteins were separated on 12% SDS-PAGE gels and
then transferred to a polyvinylidene difluoride (PVDF) membrane (Millipore,
Madrid, Spain). After blocking in Tris-buffered saline containing 0.1% Tween
20 and 5% non-fat dry milk for 2 h, membranes were incubated with a polyclonal
antibody raised against the last 15 amino acids of the carboxyl terminus of
okGLUT4 (Capilla et al., 2004),
diluted 1:500 in blocking buffer, for 2 h at room temperature. The secondary
antibody against rabbit IgG conjugated with horseradish peroxidase (BD
Biosciences, Madrid, Spain) was used at a 1:5000 dilution in blocking buffer.
Immune complexes were detected using an enhanced chemiluminiscence kit
(Amersham, Barcelona, Spain). The membranes were stripped and immunoblotted
with a monoclonal antibody against chicken actin (Developmental Studies
Hybridoma Bank, University of Iowa, USA) as a loading control. In this case
the secondary antibody was anti-mouse IgM conjugated with horseradish
peroxidase (Santa Cruz Biotechnology, Santa Cruz, CA, USA). Immunoreactive
bands were quantified using TotalLab v1.11. The densitometric values of
btGLUT4 protein expression were corrected to the densitometric values of the
loading control (actin) for each sample and the results were expressed as the
ratio between btGLUT4 and actin.
Plasma glucose measurements
Plasma glucose concentrations were determined by the glucose oxidase
colorimetric method with a commercial assay kit (Menarini Diagnostics,
Florence, Italy).
Statistical analysis
Results are expressed as means ± s.e.m. Data were analyzed using
StatView 5.0 (Cary, NC, USA). Differences between two groups were evaluated by
the unpaired Student's t-test.
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Results |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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; Capilla et al.,
2002; Navarro and
Gutiérrez, 1995; Planas
et al., 2000b).
Western blot analysis performed with total membrane preparations from brown
trout red and white muscle to detect btGLUT4 protein levels showed a single
band of a molecular mass of approximately 50 kDa in both red and white muscle
(Fig. 1A). Under normal,
non-stimulated conditions, the levels of btGLUT4 protein in red muscle are
approximately threefold higher than in white muscle in brown trout
(Fig. 1). Therefore, btGLUT4
protein levels correlate well with the higher basal expression of btGLUT4 mRNA
in red versus white muscle in trout reported previously by our group
(Capilla et al., 2002;
Planas et al., 2000a).
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Effects of fasting
Brown trout fasted for 45 days showed a 50% reduction in the amount of
btGLUT4 protein in both red and white muscle
(Fig. 2). As shown previously
(Capilla et al., 2002;
Navarro and Gutiérrez,
1995; Navarro et al.,
1992), glucose plasma levels of fasted animals were also
significantly lower than in non-fasted animals
(Table 1).
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Effects of insulin treatment
In order to evaluate the in vivo effects of insulin on btGLUT4
protein levels in trout skeletal muscle, porcine insulin was administered to
brown trout by intraperitoneal injection. Twenty-four hours after the
injection the amount of btGLUT4 protein increased significantly in red muscle
of insulin-injected trout. Conversely, btGLUT4 protein levels in white muscle
were not affected by the injection of insulin
(Fig. 3). The plasma levels of
glucose at 6 h after the injection were significantly lower in insulin-treated
fish when compared with the control fish, but no differences in plasma glucose
levels were detected after 24 h (Table
1).
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;
Capilla et al., 2002;
Planas et al., 2000b;
Plisetskaya et al., 1991).
Thus, we administered arginine by intraperitoneal injection to one group of
brown trout in order to determine the effects of an increase in the
circulating levels of endogenous insulin on btGLUT4 protein levels in trout
skeletal muscle. Arginine treatment did not significantly change the levels of
btGLUT4 protein in red muscle, despite a trend towards slightly higher btGLUT4
protein levels in samples from arginine-injected fish
(Fig. 4). Similarly, btGLUT4
protein levels in white muscle were not modified in arginine-injected trout.
The plasma levels of glucose at 24 h after the injection were significantly
higher in arginine-injected trout than in saline-injected trout
(Table 1), as previously
reported (Capilla et al.,
2002).
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Discussion |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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). In
comparison, GLUT4 protein levels in the mammalian red muscle also diminish
after fasting (Camps et al.,
1992), but either decrease or do not change in response to
hyperinsulinemic conditions (Cusin et al.,
1990; Postic et al.,
1993).
Although plasma insulin levels were not measured in this study, it has been
previously shown in brown trout, under experimental conditions similar to
those used in the present study, that insulin plasma levels decrease after
fasting, in parallel to glucose levels
(Baños et al., 1999;
Capilla et al., 2002;
Navarro and Gutiérrez,
1995; Planas et al.,
2000b), and increase after insulin and arginine treatments,
contrary to glucose levels (Baños et
al., 1997; Capilla et al.,
2002; Parrizas et al.,
1994; Planas et al.,
2000b). Therefore, the observed changes in glucose plasma levels
in the present study suggest that insulin levels probably decreased after
fasting and increased after insulin treatment. Our results evidence parallel
changes in btGLUT4 mRNA and protein levels in brown trout red muscle which, in
turn, appear to be related to changes in insulin plasma levels. By contrast,
btGLUT4 mRNA and protein levels appear to change independently of glucose
plasma levels. This is evidenced by the lack of a direct relationship between
glucose plasma levels and the levels of btGLUT4 mRNA or protein in brown trout
red muscle after insulin- and arginine-induced hypoglycemia and also after
adaptation to a high-carbohydrate diet and the resulting hyperglycemia
(Capilla et al., 2002).
Interestingly, fasted brown trout given a glucose load show marked
hyperglycemia, decreased insulin levels as well as a decreased glucose uptake
rate in white and red muscle (Blasco et
al., 1996), suggesting that the lowering of insulin levels by
fasting may be the driving force behind the change in glucose uptake in
muscle. Furthermore, post-exercise glucose utilization rates in white muscle
were reported to be independent of plasma glucose levels in rainbow trout,
although in red muscle this appeared to be true only at high glucose plasma
levels (West et al.,
1994).
Overall, these data suggest that glucose plasma levels may not be involved
in the regulation of btGLUT4 expression in red muscle. Therefore, given the
presence of specific insulin receptors in brown trout red muscle
(Baños et al., 1997;
Planas et al., 2000c) and that
GLUT4 is one of the main metabolic targets of insulin in the skeletal muscle
of mammals (Klip and Paquet,
1990), we believe that the observed changes in mRNA expression of
btGLUT4 and in the total amount of btGLUT4 protein in brown trout red muscle
could have been caused by changes in the circulating levels of insulin. In
support of the hypothesis that plasma insulin could influence GLUT4 expression
in brown trout red muscle, we have evidence indicating that insulin increases
the level of expression of GLUT4 mRNA in primary trout muscle cells
(Díaz, 2006). Further
studies should be performed to determine whether insulin can directly increase
the amount of btGLUT4 protein in primary trout muscle cells.
In contrast to the known stimulation of btGLUT4 mRNA expression by arginine
administration in red muscle (Capilla et
al., 2002), arginine did not affect the amount of btGLUT4 protein
content in the present study. However, it is worth noting that arginine not
only stimulates insulin secretion but also promotes glucagon release by
endocrine pancreatic cells in fish
(Mommsen and Plisetskaya,
1991; Navarro et al.,
2002), which could explain the hyperglycemia observed 24 h after
arginine administration in this and other studies
(Capilla et al., 2002).
Therefore, the different effects of arginine treatment on btGLUT4 protein and
mRNA levels in red muscle could be due to the fact that other factors, in
addition to insulin, might be involved in the regulation of btGLUT4 protein
levels by affecting the rate of btGLUT4 protein degradation or the
translational efficiency of btGLUT4 transcripts. Further studies should be
performed to determine whether hormones such as glucagon can affect the amount
of btGLUT4 protein in trout red muscle.
In this study we also examined the regulation of the content of btGLUT4
protein in vivo in white muscle of brown trout. In contrast to that
observed in red muscle, btGLUT4 protein content in white muscle, like btGLUT4
mRNA expression (Capilla et al.,
2002), was not affected by arginine or insulin treatments.
However, btGLUT4 protein levels in white muscle were significantly lower in
fasted trout whereas btGLUT4 mRNA content in white muscle did not change after
an identical fasting period (Capilla et
al., 2002), suggesting a differential regulation of btGLUT4 at the
protein level in white muscle, most likely at the post-transcriptional level.
In mammals, fasting also differentially affects GLUT4 mRNA and protein levels
in white muscle, increasing GLUT4 mRNA levels and causing no change in GLUT4
protein levels (Camps et al.,
1992), contrary to that observed in brown trout. Interestingly,
the expression of cod GLUT4 has recently been shown to increase in white
muscle with fasting, suggesting species-specific differences in the regulation
of GLUT4 in this tissue (Hall et al.,
2006).
The different in vivo regulation of btGLUT4 protein levels in red
and white muscle of brown trout suggests that btGLUT4 is regulated in a
fiber-type-dependent manner in agreement with the distinct metabolic
properties of the different muscle fibers
(Bone, 1978). Red muscle fibers
are enriched in mitochondria and have greater oxidative capacity compared with
white muscle fibers. In mammals, this correlates with a higher expression of
GLUT4 protein and mRNA in red skeletal muscle, providing a greater capacity
for glucose transport and insulin sensitivity
(Camps et al., 1992;
Kern et al., 1990;
Marette et al., 1992). In the
same way, brown trout red muscle also shows a higher amount of both btGLUT4
mRNA (Capilla et al., 2002) and
protein (this study) compared with white muscle, along with a higher number of
insulin receptors (Baños et al.,
1997) and a higher glucose transport rate
(Blasco et al., 1996). The
results from the present study suggest the possibility that insulin levels in
the blood could modulate the amount of btGLUT4 protein in red muscle and,
therefore, regulate the ability of this tissue to take up glucose. Supporting
this hypothesis, trout red muscle has been shown to significantly increase its
glucose uptake rate after a glucose load-induced increase in circulating
insulin (Blasco et al., 1996).
However, white muscle also increases its glucose uptake rate after a glucose
load and contributes approximately five times more than red muscle to the
total glucose uptake when expressed as percent of the total body mass
(Blasco et al., 1996), thus
probably playing a predominant role in normoglycemia. In this context, it is
interesting that in white muscle btGLUT4 protein and mRNA levels as well as
GLUT1 mRNA levels do not change after insulin or arginine administration (this
study) (Capilla et al., 2002).
Therefore, it will be important in future studies to elucidate which
regulatory factors and transport mechanisms may underlie glucose uptake in
white muscle.
In summary, this study shows that the physiological changes in the amount
of btGLUT4 protein in red muscle are similar to those previously described at
the mRNA level (Capilla et al.,
2002) and that they may be related to blood insulin levels.
Similar to what was detected at the mRNA level
(Capilla et al., 2002;
Planas et al., 2000a), the
present study shows that the content of btGLUT4 protein is higher in red than
in white muscle and that the physiological regulation of btGLUT4 takes place
predominantly in red muscle.
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Acknowledgments |
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Footnotes |
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References |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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Baños, N., Moon, T. W., Castejón, C., Gutiérrez, J. and Navarro, I. (1997). Insulin and insulin-like growth factor-I (IGF-I) binding in fish red muscle: regulation by high insulin levels. Regul. Pept. 68,181 -187.[CrossRef][Medline]
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Blasco, J., Fernàndez-Borràs, J., Marimon, I. and Requena, A. (1996). Plasma glucose kinetics and tissue uptake in brown trout in vivo: effect of an intravascular glucose load. J. Comp. Physiol. B 165,534 -541.[CrossRef]
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