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Original Research Communication |
1 From the School of Health Sciences, Deakin University, Burwood, Australia (DC-S, RJT, and MH); Sports Science and Sports Medicine, Australian Institute of Sport, Belconnen, Australia (LMB, DJA, and GRC); the Department of Kinesiology, University of Waterloo, Waterloo, Canada (AB); and the Exercise Metabolism Group, School of Medical Sciences, RMIT University, Bundoora, Australia (JAH).
2 Supported by grants from Kellogg (Australia) Pty Ltd, the Australian Institute of Sport, Deakin University, and the Canadian Institutes of Health Research.
3 Reprints not available. Address correspondence to D Cameron-Smith, School of Health Sciences, Deakin University, 221 Burwood Highway, Burwood, Victoria 3125, Australia. E-mail: davidcs{at}deakin.edu.au.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Objective: The objective was to determine the effect of altered dietary fat intake on the expression of genes encoding proteins necessary for fatty acid transport and ß-oxidation in skeletal muscle.
Design: Fourteen well-trained male cyclists and triathletes with a mean (± SE) age of 26.9 ± 1.7 y, weight of 73.7 ± 1.7 kg, and peak oxygen uptake of 67.0 ± 1.3 mL · kg-1 · min-1 consumed either a high-fat diet (HFat: > 65% of energy as lipids) or an isoenergetic high-carbohydrate diet (HCho: 70–75% of energy as carbohydrate) for 5 d in a crossover design. On day 1 (baseline) and again after 5 d of dietary intervention, resting muscle and blood samples were taken. Muscle samples were analyzed for gene expression [fatty acid translocase (FAT/CD36), plasma membrane fatty acid binding protein (FABPpm), carnitine palmitoyltransferase I (CPT I), ß-hydroxyacyl-CoA dehydrogenase (ß-HAD), and uncoupling protein 3 (UCP3)] and concentrations of the proteins FAT/CD36 and FABPpm.
Results: The gene expression of FAT/CD36 and ß -HAD and the gene abundance of FAT/CD36 were greater after the HFat than after the HCho diet (P < 0.05). Messenger RNA expression of FABPpm, CPT I, and UCP-3 did not change significantly with either diet.
Conclusions: A rapid and marked capacity for changes in dietary fatty acid availability to modulate the expression of mRNA-encoding proteins is necessary for fatty acid transport and oxidative metabolism. This finding is evidence of nutrient-gene interactions in human skeletal muscle.
Key Words: Diet-gene interaction • messenger RNA • high-fat diet • skeletal muscle • metabolism • dietary intervention • fat oxidation • carbohydrate oxidation • gene expression
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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In addition to their role as important oxidative substrates, fatty acids regulate the expression of many genes (9, 10). Several rodent studies indicate that dietary lipids modulate the expression of genes in skeletal muscle, with an increase in the messenger RNA (mRNA)expression of genes involved in fatty acid metabolism after isoenergetic high-fat diets compared with low fat, high-carbohydrate diets (11, 12). More recently, the actions of dietary fatty acids have been extended to human skeletal muscle; it was shown that dietary fatty acids have a significant effect on the expression of the gene encoding for uncoupling protein 3 (UCP3) (13). However, that study did not examine the response of those genes central to the regulation of fatty acid transport and mitochondrial ß-oxidation, whose actions are likely to be pivotal in the increased capacity to oxidize fatty acids.
Therefore, the aim of the current study was to determine the effect of marked changes in the proportion of dietary fat and carbohydrate intakes of persons undergoing extensive daily endurance training on the abundance of fatty acid–sensitive genes encoding proteins necessary for fatty acid transport and ß-oxidation in skeletal muscle. The genes chosen for investigation included the putative fatty acid transporters fatty acid translocase (FAT/CD36) and the plasma membrane fatty acid binding protein (FABPpm) (14), the mitochondrial fatty acid transporter carnitine palmitoyltransferase I (CPT I; EC2.3.1.21) (15), the ß-oxidation pathway enzyme ß-hydroxyacyl-CoA dehydrogenase (ß-HAD; EC 1.1.1.211) (16), and UCP3 (13). We also determined the protein abundance of the fatty acid–transport proteins FAT/CD36 and FABPpm.
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SUBJECTS AND METHODS |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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O2peak) for each subject according to the methods previously described in detail (7, 8). The subjects had a mean (± SE) age of 26.9 ± 1.7 y, weight of 73.7 ± 1.7 kg, and O2peak of 67.0 ± 1.3 mL · kg-1 · min-1.
Dietary intervention
Each subject underwent 2 trials in a randomized crossover design with a 2-wk washout period separating each trial as described in detail previously (7, 8). Briefly, subjects received either a high-carbohydrate diet (HCho) or an isoenergetic high-fat diet (HFat) for 5 d. The HCho diet provided 70–75% of energy as carbohydrate and < 15% of energy as lipids, whereas the HFat diet provided > 65% of energy as lipids and < 20% of energy as carbohydrate. To ensure compliance, all meals and snacks were supplied to the subjects, and the diets were individualized on the basis of food preferences and body mass. At least one meal each day was eaten under supervision in the laboratory; the remaining food for each 24-h period was provided in preprepared packages. The subjects were required to keep a food diary, in which they reported the daily intake of all food and drink to maximize compliance with the designed diets. Food intake data (7) and sample menus (8) were reported previously.
Experimental intervention and muscle collection
An identical protocol was followed for each diet. For both trials, the subjects reported to the laboratory on day 1, after they had fasted overnight. After voiding, the subjects were weighed, and a resting blood sample (10–12 mL) was drawn from an antecubital vein. A muscle sample (baseline) was then obtained from the vastus lateralis by using the percutaneous needle biopsy technique with suction applied (17). The excised muscle was immediately frozen in liquid nitrogen. After 10–15 min of rest, the subjects then completed 20 min of cycling at 70% of O2peak. For the last 10 min of cycling, the subjects breathed through the previously described gas analysis system so that whole-body rates of carbohydrate and fat oxidation (g/min) could be estimated (7). Over the 5 d of the dietary intervention, the subjects maintained the same intensive training program, which was described previously (7). On the morning of day 6, the subjects reported to the laboratory after fasting overnight for 12–14 h, and a resting muscle biopsy was taken. After a 10–15-min rest, the subjects underwent 20 min of cycling at 70% O2peak, as described for day 1. Because the muscle samples (30–40 mg) were of insufficient size to enable analysis of both gene expression and protein abundance, they were randomized for either gene analysis (n = 6) or protein analysis (n = 8).
Gene quantitation with real-time reverse transcriptase–polymerase chain reaction
Total RNA was extracted from 30 mg frozen muscle by using RNAzol (Bresatec, Adelaide, Australia). First-strand complementary DNA (cDNA) was generated from 1 µg RNA by using avian myeloblastosis virus reverse transcriptase (RT) (Promega, Madison, WI). cDNA was stored at -20 °C for subsequent analysis.
Primer and probes for each gene were designed by using PRIMER EXPRESS software package version 1.0 (Applied Biosystems, CA) from gene sequences obtained from GenBank (National Library of Medicine, Bethesda, MD; Internet: www.ncbi.nlm.nih.gov/blast/): FAT/CD36—L06850, FABPpm/mASPAT—M22632, CPT I—Y08683, ß-HAD—NM_000182, and UCP3 – XM_055241. A BLAST search for each primer and probe confirmed homologous binding to the desired mRNA of skeletal muscle (18).
Real-time RT–polymerase chain reaction (RT-PCR) was performed with the use of the ABI PRISM 5700 sequence detection system (Applied Biosystems, Foster City, CA). All samples for each gene were run simultaneously, in duplicate, to control for amplification efficiency. Fluorescent emission data were captured, and mRNA concentrations were quantified by using the critical threshold value (19). For mRNA quantification, a real-time PCR mix of 0.5 x TaqMan Universal PCR master mix (Applied Biosystems), TaqMan oligonucleotide probe (1 µmol/L; Applied Biosystems), forward and reverse primers (3 µmol/L), and cDNA (12 ng) were run for 40 cycles of RT-PCR in a total volume of 25 µL. To compensate for variations in the amount of input RNA and the efficiency of reverse transcription, ß-actin (GenBank-X00351) mRNA was quantified, and the results were normalized to these values.
Immunoblot analysis
For the detection of FAT/CD36 and FABPpm, we used a monoclonal antibody against human CD36 (provided by NN Tandon) and a rabbit polyclonal anti-FABPpm antiserum (provided by J Calles-Escandon), respectively, as previously described (20). Briefly, muscle samples were solubilized and electrophoresed on 10% sodium dodecyl sulfate–polyacrylamide gels and then transferred onto immobilon polyvinylidene difluoride membranes. The membranes were incubated for 2 h with either the monoclonal CD-36 antibody (1:500) or the polyclonal FABPpm antibody) (1:200). Secondary complexes were generated by using an anti-mouse immunoglobulin G horseradish peroxidase secondary antibody (1:10 000; Santa Cruz Biotechnology, Santa Cruz, CA) for FAT/CD36 and donkey anti-rabbit immunoglobulin G horseradish peroxidase–conjugated secondary antibody (1:3000; Amersham Biosciences Corp, Piscataway, NJ) for FABPpm. Enhanced chemiluminescence detection (Hyperfilm-ECL; Amersham, Oakville, Canada) was performed according to the instructions of the manufacturer; band densities were obtained by scanning the blots on a densitometer connected to a Macintosh LC computer (Apple Computer, Inc, Cupertino, CA) with appropriate software.
Blood analyses
Blood was portioned into tubes containing fluoride-heparin, lithium-heparin, or a preservative solution containing EGTA and reducing glutathione in isotonic sodium chloride solution. All tubes were spun, and the plasma aliquots were stored at -80 °C. The plasma prepared with fluoride-heparin was used for the analysis of plasma glucose and lactate (EML-105; Radiometer, Copenhagen). The plasma prepared with lithium-heparin was used for the analysis of plasma insulin by radioimmunoassay (Incstar, Stillwater, MN). The plasma preserved with EGTA and glutathione was analyzed for plasma fatty acids (Wako, Toyko).
Statistical analysis
All data are presented as means ± SEs. The baseline data (muscle, blood, and rates of substrate oxidation), collected before each dietary intervention (HCho and HFat), did not differ significantly; therefore for the purpose of data analysis, these values were pooled. One-way analysis of variance was used to compare data across dietary groups (baseline, HCho, and HFat). Post hoc analysis was performed to determine differences between groups with the use of Tukey’s test, where appropriate. Significance was accepted at P < 0.05. SPSS version 11.0.0 (SPSS Inc, Chicago) was used for the analyses.
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RESULTS |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Plasma glucose, lactate, fatty acid, and insulin concentrations
The fasting plasma glucose, lactate, and insulin concentrations did not change significantly after the dietary interventions (Table 1
). Fatty acid concentrations increased after both diets and were significantly greater after 5 d of the HFat diet than after the baseline or HCho diet.
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). Furthermore, the expression of ß-HAD mRNA was significantly greater after the HFat diet than after both the baseline and HCho diets. The expression of FABPpm tended to be highest after the HCho diet, although there was considerable interindividual variation in the measurement of this gene, possibly because of the low abundance relative to the housekeeping gene, ß-actin. CPT I and UCP-3 did not change significantly after the dietary treatments.
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). The abundance of FABPpm did not change significantly by either of the dietary treatments.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The importance of nutrient-gene interactions is well recognized as a key feature of single cellular organisms, in which adaptation to differing nutrient supplies is necessary for survival (21). The capacity of fatty acids to regulate gene expression in complex cellular systems in which fatty acid availability is a major determinant of cellular function is now well described (9, 10). The current data, together with data from earlier studies in rodents and humans (13, 22), provide strong evidence for a functional role of dietary fatty acid in the regulation of gene expression as one step in skeletal muscle cellular adaptation. Although mRNA abundance is a significant determinant of protein synthesis, this relation is neither simple nor linear (23). The half-lives of many mRNAs are short compared with their transcribed proteins, with transient gene activation occurring before sustained increases in protein (24). Furthermore, many intermediary steps between gene and functional protein might also be subject to fatty acid regulation (25). Thus, further studies aimed at elucidating the relation between the increased mRNA abundance after high-fat feeding reported in the current study and downstream protein synthesis rates and enzyme activities are required.
The current study was performed in highly trained athletes who maintained a matched exercise program while consuming either the HFat or HCho diet. Their high aerobic fitness and intense training schedule might have influenced the extent and degree of gene expression adaptation observed. Indeed, our group and others reported on the capacity of exercise to activate muscle gene expression (26–29). However, the sustained nature of the exercise training undertaken by these subjects, ie, competing for an average of 8 y (range: 2–20 y), together with the precise matching of the exercise workload during both trials would act to limit this potential confounding factor.
FAT/CD36 is present in tissues with high fatty acid demands, including heart, adipose tissue, intestine, and skeletal muscle (14). Currently, the contribution of FAT/CD36 to skeletal muscle fatty acid uptake is not well described. Of the available data, compelling evidence has emerged of a significant role of FAT/CD36 in fatty acid transport when the actions of FAT/CD36 are analyzed by using either selective chemical inhibition or muscle-specific gene overexpression (30, 31). A further notable feature of FAT/CD36 is the recruitment of this protein to the plasma membrane from intracellular sites by muscle contraction, highlighting a role as an adaptable regulator of intracellular fatty acid uptake during periods of increased demand (32). In support of the adaptable nature of FAT/CD36, the current study showed 215% and 17% increases in gene and protein abundance, respectively, when the HFat diet was compared with the HCho diet. These data are consistent with rapid increases in the expression of FAT/CD36 after lipid infusion in the adipocytes of human subjects (33) and in the skeletal muscle of rats (34). Similarly, increases in FAT/CD36 protein have been shown after high-fat feeding and in disorders in which lipid metabolism is dysregulated, including obesity and diabetes (20, 35). These data indicate that an increase in dietary fatty acids results in the up-regulation of FAT/CD36 and FAT/CD36 protein, suggesting a role in facilitating greater skeletal muscle fatty acid uptake.
Along with FAT/CD36 protein, FABPpm protein is also an important mediator of fatty acid plasma membrane transport, present in tissues with high fatty acid flux (14). In addition to facilitating fatty acid transport, FABPpm is identical to mitochondrial aspartate aminotransferase (EC 2.6.1.1) and thus can perform multiple cellular functions (36). An increased abundance of skeletal muscle FABPpm protein is observed in conditions of increased fatty acid utilization, including fasting (37) and endurance training (38), which supports its role as an adaptable regulator of fatty acid transport. In contrast, the current study did not show increased expression of mRNA FABPpm or abundance of FABPpm protein after 5 d adaptation to a high-fat diet. Therefore, FABPpm is differentially regulated from FAT/CD36, with no evidence of an effect of diet on FABPpm.
Currently, there is little known about the regulation of ß-HAD in skeletal muscle. The 2.6-fold greater abundance of ß-HAD after the HFat diet than after the HCho diet indicates the marked transcriptional activation of this gene. However, the significance of the induced expression of ß-HAD relative to the abundance and enzyme activity of the ß-HAD protein remains unclear. In a previous study, the increase in ß-HAD enzyme activity was 120% greater after 7-wk of a high-fat diet (62% of energy as fat) than after an isoenergetic high-carbohydrate diet (37% of energy as fat) (16). However, the consumption of a high-fat diet for 6 d by untrained subjects had little effect on ß-HAD enzyme activity relative to the effect of a low-fat control diet (33% of energy as fat) (39). Furthermore, a diet moderately high in fat (53% of total energy), relative to a lower-fat diet (43% of energy as fat), fed for 4 wk also did not alter ß-HAD enzyme activity (40). Taken collectively, these data suggest that with the short duration of the current study, it is unlikely that an increase in ß-HAD would have been translated into significantly increased functional protein concentrations. However, with prolonged high-fat feeding, the increased gene transcript may support the maintenance of increased steady state enzyme abundance.
A surprising feature of the current study was the absence of a diet-mediated action on the expression of CPT I and UCP3, particularly because these genes are responsive to fatty acid exposure in vitro with the use of a variety of cell types, including myocytes (15, 41, 42). The absence of dietary-induced changes in gene expression in human skeletal muscle suggests that significant regulation of CPT I function is exerted via posttranslational control mechanisms (2).
An unresolved issue is the possible molecular mechanism selectively activating gene expression after a high-fat diet. Signaling to the nucleus by many fatty acids has been shown to occur via the multiple isoforms of the peroxisome proliferators–activated receptor (PPAR) family of transcription factors (9, 10, 43). PPAR-
and PPAR-
isoform selective agonists activate the expression of the gene FAT/CD36 (44, 45), suggesting a role for increased activity of these transcription factors after a high-fat diet. However, PPAR activation alone cannot fully account for the observed regulation of the genes ß-HAD, CPT I, and UCP3. Interestingly, there is no evidence for a PPAR response element, upstream from ß-HAD in humans (46), yet this gene was markedly activated by the HFat diet in the current study. In contrast, despite functional PPAR response elements, which can regulate the expression of CPT I (47) and UCP3 (42), the expression of these genes did not change significantly with the HFat diet. Thus, the mechanisms linking the increased availability of dietary fatty acid to the regulation of FAT/CD36 and ß-HAD in human skeletal muscle are far from being understood; thus, more detailed molecular biological investigations are needed.
In summary, the results of the current study indicate that short-term consumption of a high-fat diet selectively increases the gene expression of FAT/CD36 and ß-HAD in human skeletal muscle. These actions failed to extend to the expression of FABPpm, CPT I, and UCP3. Consistent with the gene data, the abundance of FAT/CD36 protein increased significantly, but that of FABPpm did not change significantly. In addition to the significant regulation of enzyme activity by high-fat diets, these data show that one additional component in the adaptation to high-fat diets may be regulated by changes in the expression of genes in skeletal muscle.
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ACKNOWLEDGMENTS |
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