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Articles

Regular Exercise Modulates Muscle Membrane Phospholipid Profile in Rats¹

Jørn W. Helge^2*, Kerry J. Ayre, Anthony J. Hulbert, Bente Kiens^* and Leonard H. Storlien

Metabolic Research Centre, University of Wollongong, NSW, Australia, ^* Copenhagen Muscle Research Centre, August Krogh Institute, University of Copenhagen, Denmark, and Department of Biological Sciences, University of Wollongong, NSW, Australia

²To whom correspondence should be addressed at Copenhagen Muscle Research Centre, Dept. Human Physiology, Universitetsparken 13, DK-2100 Copenhagen Ø, Denmark. E-mail: Jhelge{at}aki.ku.dk

	ABSTRACT

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We investigated the effect of regular exercise and changes in dietary fatty acid profile on skeletal muscle phospholipid fatty acid profile in rats. Rats were randomly divided into three groups and for 4 wk fed either a carbohydrate-rich diet (CHO, 10 percent of total energy (E%) fat, 20 E% protein, 70 E% CHO) or one of two fat-rich diets (65 E% fat, 20 E% protein, 15 E% CHO) containing predominantly either saturated or monounsaturated fatty acids. Each dietary group was randomly assigned to a trained (6 d/wk, progressive to 60 min, 28 m/min at a 10° incline) or a sedentary group. The effect of training was apparent in the three hindlimb muscles analyzed: red quadriceps, white quadriceps and soleus. The unsaturation index was significantly lower in the trained than in the sedentary groups (206 ± 2 vs. 215 ± 2, P < 0.01), which largely reflected a lower content of arachidonic acid [20:4(n-6): 14.5 ± 0.5 vs. 16.6 ± 0.4% of total fatty acids, P < 0.01] and docosahexaenoic acid [22:6(n-3): 11.1 ± 0.2 vs. 11.7 ± 0.3% of total fatty acids, P < 0.03] and a concomitant higher content of linoleic acid [18:2(n-6): 20.0 ± 0.4 vs. 17.8 ± 0.4% of total fatty acids, P < 0.01]. Training affected skeletal muscle membrane structural composition, and this occurred independently of dietary fatty acid changes. This change likely reflects an increased utilization of highly unsaturated fatty acids for energy, an effect which may have deleterious effects on insulin action.

KEY WORDS: • training • fatty acid • rat • diet • phospholipid • fiber types • insulin action

	INTRODUCTION

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The phospholipid fatty acids are an integral component of the membrane constituents which influence the physical properties of membrane function such as fluidity, permeability and anchoring of membrane-related proteins. Muscle membrane fatty acid composition is also linked to the prevalence of two of the major lifestyle diseases, obesity and insulin resistance, with a higher proportion of more saturated fatty acids linked to adverse outcomes (Storlien et al. 1996 ).

The control and regulation of membrane phospholipid composition are not clearly understood; however, dietary fatty acid profile significantly influences the incorporation of fatty acids into the membrane in both rats (Ayre and Hulbert 1996 , Pan and Storlien 1993 ) and humans (McMurchie et al. 1996 ). In rats these changes in muscle membrane fatty acid composition occur within days, and remodeling approaches a plateau within 3 to 4 wk (Pan and Storlien, unpublished observations). The membrane fatty acid composition is a dynamic system, which constantly adapts to changes in its precursor, the endogenous and exogenous fatty acid supply. Therefore factors which affect the drainage of the precursor pool could influence membrane phospholipid fatty acid composition. Evidence suggests that fatty acids are selectively recruited from fat depots (Raclot and Groscolas 1993 , Raclot et al. 1997 ) and oxidized preferentially in both rats (Leyton et al. 1987 ) and humans (Jones et al. 1985 ). Consistent with this, the lipolytic stimulus of vigorous exercise also appears to selectively mobilize unsaturated fatty acids (Mougios et al. 1995 ).

During low to moderate intensity, exercise induced fat oxidation contributes significantly to energy turnover, and it is possible that a recurring preferential recruitment and oxidation of fatty acids could modify the fatty acid composition of adipose tissue and fat stored within the muscle, and subsequently affect muscle membrane phospholipid fatty acid composition. In humans, Thomas and colleagues (1977) found a small but significant decrease in the content of palmitate and a borderline significant increase in the sum of C18–20 fatty acids in vastus lateralis muscle, when endurance-trained and sedentary males were compared. More recent work by Andersson and colleagues (1998) demonstrated that 6 wk of low-intensity exercise training resulted in significant changes in muscle phospholipid fatty acid composition with a significant increase in oleic acid and a decrease in arachidonic acid. Presently only limited information is available showing how changes in dietary fatty acid supply interact with regular exercise and whether this affects muscle phospholipid fatty acid composition.

The aim of this study was to investigate the effects of, and interactions between, exercise training and dietary fatty acid profile on skeletal muscle phospholipid fatty acid composition in rats.

	MATERIALS AND METHODS

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Experimental design.

The University of Wollongong Animal Experimentation Ethics Committee approved the experiment. Rats (n = 62) were randomly allocated to one of three dietary groups and consumed either a saturated high-fat diet (n = 22, SAT)³ , a monounsaturated high-fat diet (n = 20, MONO) or a high carbohydrate diet (n = 20, CHO). Each dietary group was randomly divided into two subgroups, of which one was trained and the other remained sedentary. After 4 wk, rats were anesthetized and muscle tissue excised.

Animal care.

Male Wistar rats (initial wt. 240–270 g) were acquired from the Animal Resource Center (Perth, Australia) and housed three per cage at 21 ± 2°C (12:12-h light/dark cycle, 1800–0600 h) for 1 wk before random allocation to three dietary groups. Each group was fed one of three diets for 4 wk. The diets were a high-fat diet rich in saturated fatty acids [65% of total energy (E%) fat, 20 E% protein, 15 E% carbohydrate], a high-fat diet rich in MONO fatty acids (65 E% fat, 20 E% protein, 15 E% CHO) and a high CHO (10 E% fat, 20 E% protein, 70 E% CHO) (Table 1 ).The fatty acid compositions of each of the three diets are listed in Table 2. Rats were given free access to food and water. During the experimental period, body weight was recorded weekly.

Each dietary group was randomly divided into two subgroups, one of which was trained for 4 wk; the other group remained sedentary. Rats were trained in the hours before the dark cycle 6 d/wk on a custom-built nine-lane motorized treadmill equipped with a rear electrical shock grid. Training was initiated at 15 min, 20 m/min, 0 degrees incline and in the course of 2 wk speed, incline and duration were progressively increased such that the rats were running for 60 min at 28 m/min on a 5° incline at the end of the second week. Over the third week the incline was gradually increased to 10° and the final load, 60 min at 28 m/min on a 10° incline, was maintained until the experiment was terminated. To avoid possible effects of routine handling, sedentary rats were habituated to the treadmill 3 d/wk for 10 min at 0° incline and at the same speed as the trained rats. After the completion of the training program, a total of seven animals had to be discarded from the trained groups (four SAT, two MONO, one CHO), since more than 5% of total running time was lost due to injured feet or toe nails.

Tissue sampling procedures.

At the conclusion of the experiment, all rats were food-deprived for 5 h during the morning and were then anesthetized by intraperitoneal injection of pentobarbitol (60 mg/100 g body wt of Nembutal, Abbott, Sydney, Australia) during the early afternoon to avoid diurnal effects. Red quadriceps, white quadriceps and soleus muscles were removed, freeze clamped and quickly stored in liquid nitrogen and subsequently the heart was stopped. All tissue was stored at -80°C until analyzed.

Biochemical analysis.

All red quadriceps muscle was analyzed, and this analysis was complemented by a random selection of four white quadriceps and four soleus from each of the six groups. Extraction and derivatization of the fatty acid components of muscle phospholipids were described in full detail elsewhere (Pan and Storlien 1993 ). In brief, muscle tissue was homogenized in 2:1 (vol/vol) chloroform/methanol and total lipid extracts prepared according to Folch et al. (1957) . Phospholipids were isolated from less polar lipids by solid-phase extraction on Sepp-Pak silica cartridges (Waters, Milford, MA). The phospholipids were then transmethylated and the methyl fatty acids separated, identified and quantified by gas chromatography. The content of individual fatty acids in the phospholipids extracted from the muscles was expressed as a percentage of the total fatty acids that were identified. Individual fatty acids that made up less than 1% of the total in all groups are not shown in the tables but are included in the statistical analyses. Two fatty acid indices were derived from these results; the average degree of unsaturation, the Unsaturation Index (UI, was calculated as the average number of double bonds per fatty acid residue multiplied by 100) and the total percentage of long-chain polyunsaturated fatty acids (PUFA) with 20 carbon units (C20–22 PUFA). Furthermore, the activity of one of the enzymes involved in the fatty acid biosynthesis, 5-desaturase, was estimated according to the product-precursor ratio between arachidonic acid [20:4(n-6)] and eicosatrienoic acid [20:3(n-6)].

Statistics.

Results are expressed as means ± SEM. Statistical analyses were performed using the SAS system release 6.10 (SAS Institute Inc. Cary, NC). Three-way analysis of variance (ANOVA) with diet (CHO, MONO, SAT), exercise (training-sedentary) and muscle (red quadriceps, white quadriceps and soleus) as factors was applied to the data set. Due to the number of samples analyzed, this is an unbalanced design and is thus susceptible to interpretational problems. To circumvent this problem, two-way ANOVA using diet and exercise as factors was applied to the data set for each muscle. In this way the data were evaluated in a balanced design. Wherever two-way ANOVA revealed significant effects, a Student-Newman-Keuls test was used to discern differences between groups. Statistical significance of differences was set at P < 0.05.

	RESULTS

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Before the study, body weight averaged 264 ± 3 g for all rats. Over the experimental period, body weight steadily increased in the sedentary rats to 386 ± 6, 362 ± 6 and 369 ± 7 g in SAT, MONO and CHO, respectively, significantly more so than in the trained rats 338 ± 7, 339 ± 6 and 339 ± 4 g that consumed the SAT, MONO and CHO diets, respectively. There was no significant effect of diet group on body weight accumulation over the experimental period. The final number of rats per group was 8 to 10.

The rats were not kept in metabolic cages, and thus diet intake was not measured. There may have been somewhat more energy consumed in rats fed fat- compared to carbohydrate-rich diet. But since body weight increased similarly in the groups, this would indicate that energy intake and thus nutrient intake was approximately similar. A difference in diet intake would also lead to a difference in vitamin and mineral intake; however, since the rats should be more than safely above minimum requirements, this should not be an issue. Furthermore, the key issue of the study is the activity effect, which is within the dietary groups.

There was a significant effect of regular exercise on all muscles analyzed for linoleic acid [18:2(n-6)], arachidonic acid [20:4(n-6)], docosahexaenoic acid [22:6(n-3)], the sum of long-chain polyunsaturates (20–22 PUFA), the unsaturation index and the 5-desaturase activity (Table 3 ).The relative difference in two representative fatty acids and two composite measures of fatty acid composition by regular exercise training are shown in Figure 1. Since different numbers of samples were analyzed between muscle groups, two-way ANOVA was also performed on each of the three muscles to complement the statistical analysis. The individual membrane phospholipid fatty acid composition of the three muscles analyzed, red quadriceps, white quadriceps and soleus, are tabulated in Tables 4 , 5 and 6, respectively. In each of the three muscles analyzed, regular exercise induced a significantly higher relative content of linoleic [18:2(n-6)], a lower content of arachidonic [20:4(n-6)] (in white quadriceps it tended to be lower P = 0.07) and a lower amount of polyunsaturated long-chain fatty acids (Tables 4 , 5 and 6) . The UI was significantly lower in the trained animals for red and white quadriceps, but not for soleus (Tables 4 and 5) . In red quadriceps muscle regular exercise also induced a significantly lower relative content of palmitic acid (16:0), a higher content of stearic acid (18:0) and a lower activity of the 5-desaturase (Table 4) . These changes were not present in white quadriceps or soleus, possibly due to the smaller number of muscles analyzed in each group (n = 4), as opposed to the red quadriceps (n = 8–10).

View larger version (30K): [in this window] [in a new window]   Figure 1. The relative difference to the overall mean for the fatty acids linoleic acid [18:2(n-6)] (panel A), arachidonic acid [20:4(n-6)] (panel B), the sum of long-chain polyunsaturated fatty acids (C20–22, PUFA) (panel C) and the unsaturation index (UI) (panel D) in red quadriceps rat muscle after 4 wk adaptation to training and diet. The rats consumed one of three diets, SAT: a high-fat diet containing predominantly saturated fatty acids, MONO: high-fat diet containing predominantly monounsaturated fatty acids, CHO: carbohydrate-rich diet. The values are means ± SEM (n = 8–10). * (P < 0.01) trained vs. sedentary; (P < 0.01) dietary groups different; (P < 0.01) CHO vs. SAT; $ (P < 0.01) SAT vs. (CHO and MONO).

The dietary fatty acid composition significantly affected the phospholipid fatty acid composition in the muscles (Tables 4 , 5 and 6) . The sum of saturated fatty acids was significantly higher in rats fed the SAT compared to the MONO and CHO diet for each of the three muscles (Tables 4 , 5 and 6) . As expected from the fatty acid profile of the MONO diet (Table 2) , the individual contents of oleic acid [18:1(n-9)] and vaccenic acid [18:1(n-7)] were significantly higher in rats fed the MONO than the SAT diet in each of the three muscles (Tables 4 , 5 and 6) . The CHO and MONO diets both contained canola oil as the only fat source, and thus by design the dietary fatty acid profiles were similar, if not identical (Table 2) . However since the absolute fat intake was dramatically different (42 vs 400 g/kg diet in rats fed the CHO and fat diets, respectively), the role of the endogenous fatty acid synthesis complicates the interpretation of a pure diet effect. It is noteworthy that the content of palmitic acid (16:0), one of the major endogenously synthesized fatty acids, was significantly higher in rats fed the CHO than in those fed the fat-rich diets in all three muscles (Tables 4 , 5 and 6) .

	DISCUSSION

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This study demonstrates that regular exercise training affects skeletal muscle phospholipid fatty acid composition in rats as evidenced by a decrease in the relative percentage of 20 and 22 carbon PUFA and the overall UI. The effect of training was evident in each of the three diet groups, indicating that the effect mediated by exercise training on the phospholipid fatty acid composition occurred independent of the dietary fatty acid intake.

In skeletal muscle, regular exercise induces a multitude of adaptations that enhances the oxidative capacity of the muscle cell and its ability to maintain homeostasis during sustained stress (Saltin and Gollnick 1983 ). Homeostasis is linked to the transport and maintenance of ion and metabolite concentrations within the cell, both of which are influenced by membrane function, which subsequently is influenced by membrane phospholipid fatty acid composition. In this study, regular exercise-induced changes in the muscle membrane phospholipid fatty acid profile and should thus be considered as a modulator of muscle phospholipid fatty acid composition.

Two studies in humans addressed a similar issue to this present study. A recent report by Andersson and colleagues (1998) demonstrated that 6 wk of low-intensity exercise training resulted in a larger decrease in arachidonic acid [20:4(n-6)] and a larger increase in oleic acid [18:1(n-9)] when compared to the changes in a sedentary group consuming the same diet. This change matched the training-induced decrease in the membrane content of arachidonic acid observed in the present study; however, training increased oleic acid membrane content in the human training study compared to an increase in linoleic acid [18:2(n-6)] in the present study.

The results of Andersson et al. (1998) and the present study can be contrasted to data from Thomas and colleagues (1977) . In a cross-sectional design of trained vs. untrained individuals with no dietary control, a small but significant decrease in the content of palmitate and a borderline significant increase in the sum of C18–20 in vastus lateralis muscle were apparent in trained compared to sedentary males. Dietary fatty acid composition is a potent moderator of membrane fatty acid composition (Pan and Storlien 1993 ). Possibly in the Thomas study the trained individuals were eating a lower saturated/higher unsaturated fat diet (Thomas et al. 1977 ). This suggests the interesting possibility that individuals who exercise regularly may compensate for the increased utilization of unsaturated fatty acids by modulating dietary fatty acid profile. They may do this merely as an associated lifestyle change or it may reflect a homeostatic regulatory mechanism. This latter possibility could be tested in experimental animals by allowing access to diets with differing fatty acid unsaturation concomitant with a training program.

One other study in experimental animals has looked at voluntary "wheel running" exercise and muscle membrane lipid composition. Kriketos and co-workers (1995) found no changes in phospholipid fatty acid composition in extensor digitorum longus muscle and only a significant decline in docosahexaenoic acid [22:6(n-3)] in soleus muscle in trained vs. untrained female rats. The differences between that study and the current one may reflect differences in the mode of exercise, with wheel exercise being done in short, high-intensity bursts which may utilize glucose almost entirely for fuel.

This study does not provide direct evidence to clarify the mechanism explaining an independent effect of exercise on muscle phospholipid fatty acid profile. However, as noted previously, numerous studies have now shown that lipolytic stimuli, including exercise, preferentially mobilize unsaturated fatty acids from fat depots (Raclot and Groscolas 1993 ); in addition, these unsaturated fatty acids are more likely to be oxidized for energy in both rats (Leyton et al. 1987 ) and humans (Jones et al. 1985 ).

Arguably, some correlate of physical activity rather than the activity itself could be responsible for the changes in phospholipid fatty acid composition. Gudbjarnason (1989) showed that catecholamine stress can alter the fatty acid composition of cardiac phospholipids. However in that study catecholamine stress caused an increase in arachidonic acid [20:4(n-6)] and docosahexaenoic acid [22:6(n-3)] content, and a decrease in linoleic acid [18:2(n-6)] content of cardiac phospholipids. This is exactly the opposite of the changes we observed in skeletal muscle following regular exercise training in the current study, and thus it appears unlikely that the changes we observed are due to catecholamine stress during the training regime.

Another possible mechanism underlying the changes in fatty acid composition after training is an increased lipid peroxidation caused by the increased exposure to reactive oxygen species produced during regular exercise (Dillard et al. 1978 ). Evidence from red blood cells indicates that phospholipids containing PUFA are more susceptible to lipid peroxidation (Chiu et al. 1989 ), and one study found that exercise affected the fatty acid profile in rat muscle mitochondria (Dohm et al. 1975 ). However more studies are needed to determine to what extent exposure to different modes, duration and intensities of exercise will lead to significant lipid peroxidation.

An interesting aspect of this study is the observed difference between muscle types in phospholipid fatty acid composition. The white quadriceps (mainly fast twitch glycolytic fibers) had a significantly higher degree of unsaturation, indicated by a higher UI, a higher content of C20–22 PUFA, and a higher 5-desaturase activity than either soleus (mainly slow oxidative fibers) or red quadriceps (a mixture of slow oxidative and oxidative glycolytic fibers) muscle. From the discussion above, it is tempting to speculate that the higher degree of unsaturation in the white quadriceps relates to the lower turnover of fat, and thus oxidation of unsaturated fatty acids, that is inherent with the fast twitch glycolytic fibers. However, we could also speculate that the increased unsaturation seen in the muscle with predominantly fast twitch fibers may relate to the necessity for rapid ion flux. It has been shown that the intrinsic activity of the sodium-potassium pump is increased in a more unsaturated lipid environment (Dr. Paul Else, personal communication).

In the literature it is well-documented that insulin sensitivity is related to muscle phospholipid fatty acid composition (Borkman et al. 1993 ), and it was demonstrated that a reduction in C20–22 PUFA (C20–22, PUFA) in muscle membranes is linked to an impaired insulin action (Pan et al. 1995 ). In the present study the decreased unsaturation and content of C20–22 fatty acids in the membrane indicate that training might attenuate the exercise-induced improvement in insulin action through an effect on the skeletal muscle membrane lipid profile. Further studies must investigate the role of exercise intensity in this effect on membrane fatty acid composition and possibly insulin sensitivity. In any case, attention to the dietary lipid profile, emphasizing intake of PUFA during a training program, may be important to achieve the full potential for individuals with predisposition to, or already existing, obesity and diabetes.

	ACKNOWLEDGMENTS

 
The skilled technical assistance of April Potts and Dinitra White is acknowledged. Adamandia Kriketos is thanked for excellent assistance during the final experiments and David Pan for excellent assistance during the analysis and identification of the fatty acids.

	FOOTNOTES

 
¹ The gelatin was kindly donated by Davis Gelatine (Australia Co). The study was supported by grants from the NHMRC Australia, the Danish Research Academy (V940098) and the Danish National Research Foundation (#504-14).

³ Abbreviations used: CHO, carbohydrate rich diet; E%, percent of total energy; MONO, fat-rich diet containing predominantly monounsaturated fatty acids; PUFA, polyunsaturated long-chain fatty acids; SAT, high-fat diet containing predominantly saturated fatty acids; UI, Unsaturation Index.

Manuscript received January 22, 1999. Initial review completed March 11, 1999. Revision accepted June 16, 1999.

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