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First published online December 14, 2007
Journal of Experimental Biology 211, 114-120 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.012674
Antioxidative defence alterations in skeletal muscle during prolonged acclimation to cold: role of L-arginine/NO-producing pathway
1
i1211unovi21,*
1 Department of Physiology, Institute for Biological Research `Sini
a
Stankovi', University of Belgrade, Bulevar Despota Stefana 142, 11060
Belgrade, Serbia
2 Institute of Zoology, Faculty of Biology, University of Belgrade, Studentski
trg 16, 11000 Belgrade, Serbia
* Author for correspondence (e-mail: koracb{at}ibiss.bg.ac.yu)
Accepted 18 October 2007
 |
Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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-nitro-L-arginine methyl ester
(L-NAME) treated. The AD parameters were determined in the
gastrocnemius muscle on day 1, 3, 7, 12, 21 and 45 of cold acclimation. The
results showed an improvement of skeletal muscle AD in both early and late
cold acclimation. Clear phase-dependent changes were seen only in copper, zinc
superoxide dismutase activity, which was increased in early cold acclimation
but returned to the control level in late acclimation. In contrast, there were
no phase-dependent changes in manganese superoxide dismutase, catalase,
glutathione peroxidase, glutathione reductase and glutathione S-transferase,
the activities of which were increased during the whole cold exposure,
indicating their engagement in both thermogenic phases. L-Arginine
in early cold acclimation accelerated the cold-induced AD response, while in
the late phase it sustained increases achieved in the early period.
L-NAME affected both early and late acclimation through attenuation
and a decrease in the AD response. These data strongly suggest the involvement
of the L-arginine/NO pathway in the modulation of skeletal muscle
AD.
Key words: skeletal muscle, antioxidative defence, nitric oxide, cold
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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). Shivering thermogenesis, achieved by increased skeletal
muscle activity, occurs early in response to cold exposure
(Jansky and Hart, 1968). A
later decrease in shivering thermogenesis has been found to be accompanied by
an increase in NST (Griggio,
1982). NST is achieved by the uncoupling of oxidative metabolism
from ATP production, primarily in brown adipose tissue
(Jansky, 1966;
Foster and Frydman, 1979). In
contrast to the clear role of skeletal muscle in shivering thermogenesis, the
extent of NST in this tissue remains controversial, with some reports
demonstrating NST in the skeletal muscle of pigeons
(Skulachev and Maslov, 1960),
ducklings (Barre et al., 1987)
and rats (Mollica et al.,
2005), whilst others found no NST in this tissue
(Golozoubova et al., 2001).
However, skeletal muscle, which represents a large percentage of body mass,
significantly contributes to the intensification of metabolic activity of the
whole organism during thermogenesis (Rolfe
and Brand, 1996) due to its huge capacity for β-oxidation and
the oxidative capacity of mitochondria
(Hoppeler and Fluck,
2003).
Heat production increases metabolic rate and oxygen consumption in
metabolically active tissues (Shiota and
Masumi, 1988) that is implacably associated with the elevation of
reactive oxygen species generation. Cellular homeostasis under conditions of
increased reactive oxygen species production is achieved by a proportional
increase in tissue antioxidative defence (AD)
(Halliwell and Gutteridge,
1990; Buzadi et
al., 1997;
Buzadi et al.,
1999; Kora and
Buzadi, 2001;
Petrovi et al., 2006).
AD consists of enzymes – copper, zinc and manganese superoxide dismutase
(CuZnSOD and MnSOD, EC 1.15.1.1), catalase (CAT, EC 1.11.1.6), glutathione
peroxidase (GSH-Px, EC 1.11.1.9), glutathione S-transferase (GST, EC
2.5.1.18), thioredoxin reductase (TR, EC 1.6.4.5), glutathione reductase (GR,
EC 1.6.4.2) and low molecular mass antioxidants such as vitamins E and C,
glutathione (GSH), etc. (Chance et al.,
1979; Cadenas et al.,
1989; Aruoma,
1996). In recent years, considerable progress has been achieved in
the field of redox regulation and the concept of the protective effect of AD
was extended to its regulatory role, since AD activity determines reactive
species availability (Mugge et al.,
1991; Kora and
Buzadi, 2000;
Buzadi et al.,
2006).
Reactive species in moderate concentrations, especially superoxide anion
radical (O2·–) and nitric oxide (NO), play
an important role as regulatory mediators in biological processes
(Dröge, 2002). In
skeletal muscle, NO is produced by the activity of constitutively expressed
endothelial and neuronal NO synthase (NOS), localized on the surface of the
sarcolemmal membrane and the endothelial plasmalemmal caveolae, as well as by
inducible NOS, the localization of which varies depending on the state of the
cell (Kobzik et al., 1995;
Bates et al., 1996). NO
regulates many physiological functions of skeletal muscle including glucose
uptake and oxidation (Young et al.,
1997), mitochondriogenesis
(Puigserver et al., 1998),
contractile functions (Joneschild et al.,
1999; Maréchal and
Gailly, 1999), blood flow
(Brevetti et al., 2003) and
fatty acid oxidation (Jobgen et al.,
2006), as well as muscle repair through satellite cell activation
and the release of myotrophic factors
(Anderson, 2000;
Brunelli et al., 2007).
On the other hand, it is known that both endurance training and acclimation
to cold increase skeletal muscle oxygen uptake and, consequently, production
of reactive oxygen species. So far, most studies have focused on the changes
of skeletal muscle AD during exercise
(Tiidus et al., 1996;
Tonkonogi et al., 2000;
Pansarasa et al., 2002).
However, knowledge of the changes in AD in skeletal muscle during acclimation
to cold is very limited and there are no data concerning the possible role of
NO in the modulation of skeletal muscle AD.
Hence, the aim of the present study was to assess changes in AD in skeletal
muscle during early and late cold acclimation with a special focus on the
possible role of NO in the modulation of AD in this tissue. For this purpose,
adult male rats were kept at room temperature, or were exposed to cold for 45
days and received the NO-manipulating agents L-arginine or
N-nitro-L-arginine methyl ester
(L-NAME) as drinking liquid, and the effects on AD over time were
assessed.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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) and by us
(Vasilijevi et al.,
2007) in a dose (2.25% L-arginine HCl and 0.01%
L-NAME HCl in tap water) that caused no toxic effects
(Petrovi et al.,
2005). The animals were killed at the same time of the day after
1, 3, 7, 12, 21 or 45 days of cold acclimation. The rats were housed in
individual plastic cages with drinking liquid and food ad libitum.
Each experimental group consisted of six individuals. Body mass, food and
fluid intake were recorded daily for each animal. The experimental protocol
was approved by the Ethical Committee for the Treatment of Experimental
Animals of the Institute for Biological Research, Belgrade.
The rats were killed by decapitation, and the gastrocnemius dissected and
rinsed with physiological saline to wash out traces of blood. The tissue was
homogenized (Ultra/Turrax homogenizer, Janke und Kunkel Ka/Werke, Staufen,
Germany; 0–4°C) in 0.25 mol l–1 sucrose, 0.1 mmol
l–1 EDTA and 50 mmol l–1 Tris-HCl buffer, pH
7.4, and the homogenates sonicated (Takada
et al., 1982).
Activity of antioxidative enzymes
Total SOD activity was examined by a modified method of Misra and Fridovich
(Misra and Fridovich, 1972).
MnSOD activity was determined after preincubation with 4 mmol
l–1 KCN. CuZnSOD activity was calculated as the difference
between total SOD and MnSOD activities. Enzymatic activity was expressed in U
mg–1 protein. SOD units were defined as the amount of the
enzyme inhibiting epinephrine (adrenaline) auto-oxidation under appropriate
reaction conditions. CAT was assayed as suggested by the supplier
(Sigma-Aldrich, St Louis, MO, USA) and the activity expressed in µmol
H2O2 min–1 mg–1
protein. GSH-Px was determined with t-butylhydroperoxide as a
substrate (Paglia and Valentine,
1967) and the activity expressed in nmol of reduced NADPH
min–1 mg–1 protein. GST was measured by the
method of Habig et al. (Habig et al.,
1974) and the activity expressed in nmol GSH used
min–1 mg–1 protein. GR activity was assayed
according to Glatzle et al. (Glatzle et
al., 1974) and expressed as nmol GSH min–1
mg–1 protein.
Determination of GSH
The content of GSH was examined in the tissue after deproteinization with
sulphosalicylic acid. Total GSH was measured by enzyme recycling assay
according to Griffith (Griffith,
1980) and expressed in nmol GSH g–1 tissue.
Other assays and statistics
Protein content was estimated by the method of Lowry et al.
(Lowry et al., 1951) using
bovine serum albumin as a reference. Analysis of variance (ANOVA) was used for
within-group comparison of the data. If the F test showed an overall
difference, Tukey's test was applied to identify significant differences.
Statistical significance was accepted at P<0.05.
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RESULTS |
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During the whole experiment no changes in fluid intake were observed. In contrast, as acclimation to cold started, animals in all examined groups increased food intake by 100% and this increase remained constant to the end of experiment (data not shown).
Generally, the results showed improvement of skeletal muscle AD in both early and late cold acclimation. Clear phase-dependent changes were seen only in CuZnSOD activity (Fig. 1), which was increased in early cold acclimation but returned to the control level in late acclimation. In contrast, there were no phase-dependent changes in MnSOD (Fig. 2) and peroxidative- and GSH-related parts of AD (CAT, GSH-Px, GR and GST; Figs 3, 4, 5, 6), the activities of which were increased during the whole period of cold exposure.
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Changes in MnSOD activity during cold acclimation are depicted in Fig. 2. As shown, in the untreated group, MnSOD activity increased from day 3 (P<0.01), while in L-arginine-treated rats, MnSOD activity was increased on day 1 of early cold exposure compared with the control (P<0.01) and untreated group (P<0.05). During the late cold acclimation, increase in MnSOD activity achieved early was sustained in the untreated group and was unaffected by L-arginine, related to the untreated group. L-NAME treatment decreased MnSOD activity from day 3 to day 12 compared with the untreated group, and delayed the cold-induced increase in MnSOD activity on day 21 of late cold-acclimation (P<0.001).
CAT activity (Fig. 3) progressively increased in all three cold-acclimated groups with the highest increase on day 7 (P<0.001). A higher CAT activity was observed on day 3 of the early phase of acclimation in both untreated (P<0.05) and L-NAME-treated rats (P<0.001), while increased activity of this enzyme was recorded as early as day 1 of exposure to cold in L-arginine-treated animals (P<0.05) compared with the control (P<0.05) and untreated group (P<0.05). CAT activity remained elevated during the whole of the late cold acclimation in both untreated and L-arginine-treated rats, while in the L-NAME-treated group it returned to control values on day 21 and decreased compared with the untreated group at days 21 (P<0.01) and 45 (P<0.001) of late cold acclimation.
Time-dependent changes of GSH-Px activity are shown in Fig. 4. Similar time-course changes in the activity of this enzyme were observed in all three cold-acclimated groups, during both the early and late phases, with the highest increase seen on day 7 in untreated (P<0.001) and L-NAME-treated animals (P<0.01). However, in the L-arginine-treated group the maximal increase of GSH-Px activity was recorded on day 3 of early cold exposure and it was higher (P<0.05) compared with that observed at the same time in the untreated group. The increase in GSH-Px activity originated in the early cold acclimation remained during the whole late cold acclimation in untreated and L-arginine-treated groups, while it returned to the control level on day 21 in L-NAME-treated rats and stayed below values observed in the untreated group at days 21 (P<0.001) and 45 (P<0.01).
As shown, L-arginine in early cold acclimation accelerated the cold-induced increase in MnSOD, CuZnSOD and CAT activity, while in the late phase it sustained increases achieved in the early period. L-NAME affected both early and late acclimation through attenuation and decreases in the AD response. That is, L-NAME treatment postponed the cold-induced increase of MnSOD activity and reversed CAT and GSH-Px activities to the control level on day 21 of late cold acclimation, and decreased CuZnSOD activity during the whole acclimation period. In contrast, neither L-arginine nor L-NAME changed GR and GST activities, which increased from day 1 of cold acclimation and stayed unchanged until the end of the experiment.
From Fig. 5 it can be seen that GST activity was increased in the untreated group on day 1 of early cold exposure (P<0.001) and remained elevated for the whole duration of the experiment compared with the control, with the maximum reached on day 7 of cold exposure (P<0.001). Both L-arginine and L-NAME failed to affect changes in GST activity seen in the untreated group.
GR activity (Fig. 6) showed time-dependent changes similar to those of GST activity, i.e. it was increased on day 1 of the early phase in all examined groups and remained elevated during the whole period of both early and late cold acclimation, with the maximum increase on day 7 (P<0.001).
GSH content in the gastrocnemius (Fig. 7) was decreased from day 1 of early cold exposure in all examined groups, and remained decreased during the whole period of cold acclimation in L-NAME-treated rats in relation to the control. However, in the untreated group the GSH content was restored to the control level on day 45 of late cold acclimation, while in the L-arginine-treated group its restitution was observed on day 3 of early cold acclimation and remained unchanged until the end of the experiment.
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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In the course of the early period of cold exposure, shivering thermogenesis
is activated. During this time, to overcome cold, nerve stimulation induces
permanent skeletal muscle contractions and relaxation. This period may
therefore be seen as muscular training, which is known to increase the rate of
oxygen consumption (Wickler,
1981) and the proportion of the O2–
and H2O2 formed from oxygen utilized by mitochondria
(Vasilaki et al., 2006).
Accordingly, increases in MnSOD and CuZnSOD as well as CAT and GSH-Px
activities observed in the untreated group during early cold acclimation could
be explained as a response of these enzymes to an increased production of
their substrates and are in line with several reports related to
exercise-improved AD (Higuchi et al.,
1985; Pansarasa et al.,
2002). Supplementation with the physiological substrate for NOSs,
L-arginine, in the early phase resulted in an acceleration of the
increase in cold-induced AD enzymes (MnSOD, CuZnSOD, CAT and GSH-Px)
activities, and restoration of GSH level compared with the untreated group. In
contrast, L-NAME, the non-selective NOSs inhibitor, postponed the
cold-induced increase in MnSOD activity seen in the untreated group in the
early phase to day 21 of late cold exposure and decreased CuZnSOD activity
during the acclimation to cold. It was found that L-arginine
enhanced exercise-induced NOSs activation and NO production, which improves
aerobic capacity (Maxwell et al.,
2001), mechanical and metabolic muscle capability
(Maréchal and Gailly,
1999; Ohta et al.,
2007) and increases glucose oxidation
(Fu et al., 2005). In
contrast, L-NAME, through inhibition of NOSs and a decrease in NO
availability, diminished skeletal muscle contractions, as well as glucose
uptake and oxidation (Robberts et al.,
1997). Thus, the accelerated increase in MnSOD, CuZnSOD and CAT
activities observed here in L-arginine-treated rats during the
early acclimation to cold could be connected to improved skeletal muscle
contraction and oxidative capacity by NO and, consequently, to
O2·– and H2O2
production.
However, after a period of 7 (Cannon
and Nedergaard, 2004) or 10 days
(Peralta et al., 2003) on
cold, the impact of shivering decreases and cannot account for thermogenesis
(Griggio, 1982), while NST
markedly increases. During prolonged exposure to cold, despite decreased
shivering, skeletal muscle retains an enhanced capacity for aerobic support of
energy metabolism (although, less than in shivering), i.e. working as a
supportive tissue to supply brown adipose tissue with oxygen, contributing to
the overall acclimation to cold (Wickler,
1981; Wibom et al.,
1992). In our study, after 7 days, CuZnSOD activity in the
untreated group was restored to the control level, while MnSOD activity
remained increased during the whole acclimation period. The different
responses of SOD isoforms seen after early cold acclimation could be connected
to their different subcellular organization; MnSOD is compartmentalized in the
mitochondrial inner membrane, whereas CuZnSOD is found mainly in cytosol.
Thus, it might be proposed that in the period when shivering ceases,
production of O2·– is such that
mitochondrial MnSOD is sufficient to cope with it and to prevent an increase
of O2·– in the cytosol and a competent
response in CuZnSOD activity.
The observed changes in enzyme activities during cold acclimation could be
interpreted in terms of different tissue conditions characterized by different
fuel utilization. It is known that maximal utilization of glucose by skeletal
muscle is associated with acute cold exposure, while in long-term cold
acclimation a marked increase in the utilization of lipid substrates occurs
(Vallerand et al., 1990).
Accordingly, a conspicuous increase of CAT and GSH-Px activities recorded here
from day 7 of cold acclimation could be attributed to increased
β-oxidation of fatty acids and, connected to that, increased
H2O2 production. These data are in line with studies on
various tissues that reported increases in CAT and GSH-Px activity during cold
exposure, as a response to increased peroxidative pressure
(Alptekin et al., 1996;
Buzadi et al.,
1997; Selman et al.,
2000).
L-arginine treatment sustained the shown increases in AD
achieved in the early period until the end of cold acclimation. In contrast,
L-NAME treatment postponed the cold-induced increase of MnSOD
activity and reversed CAT and GSH-Px activities to the control level on day 21
of late cold exposure. These data showing attenuated and delayed cold-induced
responses in AD components by L-NAME treatment in late cold
acclimation strongly indicate the involvement of the L-arginine/NO
pathway in the modulation of skeletal muscle AD. At this stage, considering
our data, we cannot say how L-arginine/NO affects skeletal muscle
AD. Fu et al. (Fu et al.,
2005) showed that L-arginine, by increasing
NOSs-derived NO production, enhances expression of the genes responsible for
fatty acid oxidation and, thereby, H2O2 production. In
contrast, Nagase et al. (Nagase et al.,
1997) showed that incubation of L-arginine under
peroxidative conditions leads to the non-enzymatic production of NO-dependent
species, which are known to increase production of
O2·– and H2O2
(Navarro et al., 2005).
Peralta et al. (Peralta et al.,
2003) reported that L-arginine/NO, by mitochondrial NOS
(mtNOS) activation, in early cold acclimation increased O2 uptake
but significantly decreased it at day 24 of late cold exposure via
inhibition of cytochrome c oxidase and an increase in
O2·– production. Additionally, these
authors emphasized that in skeletal muscle the major NOS isoform that
participates in the response to cold acclimation is mtNOS, which in this
tissue was described varyingly as post-translationally modified nNOS
(Elfering et al., 2002) or as
eNOS (Punkt et al., 2006). In
the present study, restoration of GSH level was seen in the
L-arginine-treated group at day 3 and in the untreated group at day
45, while in the L-NAME-treated group it stayed below the control
level during the whole period of cold acclimation. Thus, it could be
hypothesized that L-arginine, i.e. NO, acted by restoring the GSH
amount to the control level. This hypothesis is based on the results of
Moellering et al. (Moellering et al.,
1998), who reported induction of GSH synthesis in skeletal muscle
as well as in endothelial cells
(Moellering et al., 1999) in
response to NO via the activation of 
-glutamyl cysteine
synthetase. Further studies along these lines are necessary for clarification
of the precise mechanisms involved. The data presented here demonstrating that
the cold-induced AD response is improved by L-arginine but
attenuated by L-NAME clearly showed opposing effects of
L-arginine and L-NAME on the modulation of AD in
skeletal muscle. However, there are several reports, with different model
systems, concerning the same effect of L-NAME treatment as that
seen after L-arginine treatment. Conflicting observations in
experiments with the NOSs inhibitor L-NAME are explained by
non-enzymatic production of NO during incubation with L-NAME in the
presence of NADPH, GSH and ascorbate
(Moroz et al., 1998).
Henningsson et al. (Henningsson et al.,
2000) showed that chronic L-NAME treatment in diabetic
rats blocked constitutive NOSs that evoked iNOS-derived NO production to
compensate for NO level, while Krippeit-Drews et al.
(Krippeit-Drews et al., 1996)
reported that L-NAME can also act directly, not via
intracellular messengers. We have recently reported that L-arginine
and L-NAME affect pancreatic AD in the same manner
(Vasilijevi et al.,
2007). Thus, tissue-specific effects of these two NO-manipulating
agents could be proposed.
The presented results clearly show improvement of skeletal muscle AD in both early and late cold acclimation, indicating intensive oxidative metabolism in this tissue during both shivering and NST. Moreover, L-arginine in early cold acclimation accelerated the cold-induced AD response, while in the late phase it simply sustained increases achieved in the early period. L-NAME exerted effects on both early and late acclimation through attenuation and a decrease in the AD response. These data strongly suggest the involvement of the L-arginine/NO pathway in the modulation, i.e. the improvement of skeletal muscle AD during cold acclimation. However, in order to understand the precise mechanisms, additional studies, primarily related to the determination of the relative contributions of the L-arginine-dependent and NOSs-dependent effects, are needed. Our efforts along these lines are in progress.
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Acknowledgments |
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