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J. Nutr. First published December 3, 2008; doi:10.3945/jn.108.095752
 Journal of Nutrition, doi:10.3945/jn.108.095752
Vol. 139, No. 1, 38-43, January 2009
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© 2009 American Society for Nutrition

Nutrient Physiology, Metabolism, and Nutrient-Nutrient Interactions

Daily Variations in Dietary Lysine Content Alter the Expression of Genes Related to Proteolysis in Chicken Pectoralis major Muscle1–3,

Sophie Tesseraud4,*, Isabelle Bouvarel5, Anne Collin4, Estelle Audouin4, Sabine Crochet4, Iban Seiliez6 and Christine Leterrier7

4 INRA, UR83 Recherches Avicoles, F-37380 Nouzilly, France; 5 Institut Technique de l'Aviculture, F-37380 Nouzilly, France; 6 INRA, UMR1067 Nutrition Aquaculture et Génomique, F-64310 St Pée-sur-Nivelle, France; and 7 INRA, UMR6175 Physiologie de la Reproduction et des Comportements, F-37380 Nouzilly, France

* To whom correspondence should be addressed. E-mail: tesserau{at}tours.inra.fr.


   ABSTRACT
TOP
 ABSTRACT
Introduction
 Materials and Methods
 Results
 Discussion
 LITERATURE CITED
 
Amino acids are known to be anabolic factors that affect protein metabolism, but the response of animals to daily amino acid changes is little understood. We aimed to test the effects of feeding birds with alternations of diets varying in lysine content on the expression of genes related to proteolysis in chicken muscle. Cyclic feeding programs with 2 diets, each given for 24 h during 48-h cycles, were carried out from 10 d of age. Three programs were used: 1) control treatment with continuous distribution of a complete diet containing standard medium lysine level (ML; 11.9 g/kg); 2) alternation of diets with high (HL) and low (LL) lysine levels; 3) alternation of ML and LL diets, where LL = 70%, ML = 100%, HL = 130% of standard lysine level. The Pectoralis major muscles were sampled after 2 wk of cyclic feeding. Measurements included the expression patterns of 6 genes involved in proteolysis, and mammalian target of rapamycin and Forkhead box-O transcription factor (FoxO) signaling. Cathepsin B, m-calpain, and E3 ubiquitin ligases Muscle Ring Finger-1 and Muscle Atrophy F box were significantly overexpressed in chickens transiently fed the LL diet, whereas the mRNA levels of 20S proteasome C2 subunit and ubiquitin remained unchanged. Modifications of E3 ubiquitin ligase expression can be partly explained by significant changes in FoxO phosphorylation with cyclic dietary treatments. Our results suggest timing-sensitive regulation of proteolysis in chicken muscle according to dietary treatment and a high metabolism capacity to compensate for changes in amino acid supply, which might be used for nutritional purposes.


   Introduction
TOP
 ABSTRACT
 Introduction
Materials and Methods
 Results
 Discussion
 LITERATURE CITED
 
Amino acids are major regulators of growth and protein metabolism [see (1) for a recent review]. For instance, feeding chickens with diets deficient in a specific limiting amino acid (i.e. lysine) decreases growth performance and protein accretion, with a particularly drastic effect observed on breast muscle development (2,3). Lysine supplementation of a lysine-deficient diet otherwise balanced in terms of other amino acids has been shown to greatly modify the amounts of protein synthesized and degraded in chickens (2,4,5). Similar results have been demonstrated in the growing pig (6) and in humans (7). These findings indicate the importance of optimizing animal and human amino acid nutrition, whether quantitative (level of intake) or qualitative (balance between amino acids). The nutritional regulation of protein metabolism also involves another major factor, i.e. the timing of nutrient delivery (1,8). In particular, there is evidence that the timing of protein feeding regulates protein metabolism (9,10). Nevertheless, to our knowledge, little is known regarding the response to temporal or cyclical changes in dietary amino acid composition to date.

Studies performed using lysine-deficient diets have revealed the possibility of a major effect of dietary amino acid levels on protein degradation: the fractional rates of proteolysis (values expressed as %/d) measured in the breast muscle of growing chickens are always higher in lysine-deprived animals (2,4,5), suggesting that the effects of fluctuation in amino acid feeding have to be explored in particular on muscle proteolysis. Protein degradation is a highly controlled, selective, and regulated process. Three major proteolytic systems are involved in vertebrate muscle proteolysis, i.e. lysosomal, ubiquitin-proteasome–dependent, and Ca2+-dependent systems (11,12). Lysosomal and Ca2+-dependent proteolysis involve cathepsins and the calpain/calpastatin system, respectively. Ubiquitin-proteasome–dependent proteolysis is initiated by the covalent attachment of ubiquitin molecule chains through the successive actions of the ubiquitin-activating enzyme, ubiquitin-conjugating enzymes, and E3 ubiquitin-ligases. Ubiquitinated proteins are then targeted for degradation to the 26S proteasome, which is a large proteolytic complex that hydrolyses protein conjugates. New evidence has demonstrated that the ubiquitin-proteasome proteolytic pathway is controlled by the expression of 2 important E3 ubiquitin ligases, i.e. Muscle Atrophy F box (MAFbx or atrogin-1)8 and Muscle Ring Finger-1 (MurF1); see (13–15) for reviews. These 2 muscle-specific E3 ligases (also called atrogenes) have been shown to be overexpressed in atrophic conditions, including diabetes, cancer, and fasting, and also following disuse (16–21). The aim of this study was to explore the effects of daily variations in dietary lysine supply on lysosomal, Ca2+-dependent, and ubiquitin-proteasome–dependent proteolytic systems in chicken muscle. More precisely, we examined the effect of cyclical changes in dietary lysine in terms of expression of proteolytic genes and change of associated signaling pathways with a focus placed on atrogene regulation.


   Materials and Methods
TOP
 ABSTRACT
 Introduction
 Materials and Methods
Results
 Discussion
 LITERATURE CITED
 
    Animals and experimental design. Male chickens (broiler pedigree) were housed in a conventional environmentally controlled poultry shed. The lighting schedule was 24 h of light for the first 3 d of life and a 20-h-light/4-h-dark cycle thereafter (dark period from 0000 to 0400). Environmental temperature was progressively reduced from 32°C to 23°C. Water and food were freely available during the whole experiment period. All the chickens received the same starter feed (metabolizable energy, 12.12 MJ/kg; crude protein, 21%).

From 10 to 24 d of age, chickens were given either control or cyclic feeding programs with alternation of the 2 diets varying in lysine content, each given for 24 h during 48-h cycles as previously described (22). Three experimental diets were used during the sequential feeding period (Table 1). These diets were isoenergetic and isoproteic but contained different lysine contents: control medium-lysine diet (ML) = 100% of the standard lysine level, low-lysine diet (LL) = 70% of the standard lysine level, and high-lysine diet (HL) = 130% of the standard lysine level. To explore the effects of daily variations in dietary lysine supply, sequential feeding programs were carried out by alternating the LL diet with either the ML or HL diet to test possibilities of compensation. In similar conditions, it has been shown that the LL diet was significantly less consumed in the sequence LL/ML but not in the sequence LL/HL (22). These diets were each given for 24 h and presented in 2 different orders, beginning with either the LL diet during the first period of the 48-h cycle, followed by the HL or ML diet during the 2nd period, or vice versa. The exchange of diets took place at 1400 each day (i.e. the middle of the light period). Body weights were measured throughout the experimental period (on d 10, 17, and 24). At 24 d of age, i.e. after 2 wk of cyclic feeding, chickens were killed at the end of a cycle (between 1400 and 1530) to investigate the impact of sequential feeding on protein metabolism. Five dietary treatments were thus compared: control treatment with the complete standard diet (ML-Ctl); 2 treatments with alternation of LL and HL diets (sequence S1; i.e. HL-S1, chickens receiving the HL diet on d 24, and LL-S1, chickens receiving the LL diet on d 24); and 2 treatments with alternation of LL and ML diets (sequence S2; i.e. ML-S2, chickens receiving the ML diet on d 24, and LL-S2, chickens receiving the LL diet on d 24). In these treatments, the indicated diet corresponded to the last diet in a cycle before tissue sampling. To further support our work conclusively, we also used another model of sequential feeding recently studied by our group as an alternative nutritional strategy for poultry production [see (23) for details on design and diets]. Briefly, sequential feeding was conducted during 48-h cycles from 10 d of age with an alternation of diets varying in protein content (low- and high-protein diets) and compared with a control treatment with a complete standard medium-protein diet.


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  		TABLE 1 Composition and characteristics of experimental feeds1

 
For the 2 experiment paradigms, chickens were killed by decapitation after blood sampling. The Pectoralis major muscles were removed and quickly frozen. Frozen tissues were ground in liquid nitrogen and stored at –80°C until analysis. All experiments were carried out with due regard to legislation governing the ethical treatment of animals and investigators were certified by the French government to conduct animal experiments.

    Measurement of muscle protein, RNA, and ribosomal capacity. Frozen powdered muscle samples were homogenized in 2% HClO4 according to the method of Schmidt-Thannhauser as modified by Munro and Fleck (24). Protein content was measured using the bicinchoninic acid kit (Interchim). Total RNA was measured on the basis of the UV absorbance at 260 nm, with a correction for peptide material based on the UV absorbance at 232 nm. Ribosomal capacity (Cs), i.e. the capacity for protein synthesis, was calculated as the ratio of RNA:protein (25).

    RNA isolation and RT-PCR. Total RNA was extracted using RNA Now (Biogentec) from 100-mg muscle samples according to the manufacturer's recommendations. After RNase-Free DNase treatment, RNA was reverse transcribed using Super Script II RNase H Reverse Transcriptase (Invitrogen) in the presence of Random Primers (Promega). Quantitative PCR were performed in duplicate using the Abi Prism 7000 apparatus (Applied Biosystems) as previously described (26). The sequences of primers used, specifically designed or reproduced from the literature (27), are shown in Supplemental Table 1. Gene expression levels were estimated on the basis of PCR efficiency and threshold cycle deviation of an unknown sample compared with a control, as previously described (26). 18S ribosomal RNA was chosen as the reference gene.

    Preparation of muscle lysates and Western blotting. For analyzing the signaling pathways potentially involved in proteolysis regulation (14,15), muscle lysates were prepared as previously described (28). Muscle lysates (60 µg of protein) were subjected to SDS-PAGE gel electrophoresis and western blotting using appropriate antibodies: p-mTOR [S2448] (Cell Signaling); p-FoxO3A [T32] and FoxO3A (Upstate Biotechnology); mTOR/FRAP (Santa Cruz Biotechnology); and Vinculin (Sigma). After washing, membranes were incubated with an Alexa Fluor secondary antibody (Molecular Probes). Bands were visualized by infrared fluorescence using the Odyssey Imaging System (LI-COR) and quantified by Odyssey infrared imaging system software (Application software, version 1.2).

    Statistical analysis. Values are expressed as means ± SEM. Statistical analysis was performed using ANOVA (Statview Software program; SAS Institute) to detect significant intergroup differences. The means were compared by Fisher's least significant difference test in the case of a significant effect and P < 0.05 was considered significant. To test the potential relationships between atrogene mRNA levels and protein phosphorylation status, Pearson correlation coefficients were analyzed by a Fisher's r to z test.


   Results
TOP
 ABSTRACT
 Introduction
 Materials and Methods
 Results
Discussion
 LITERATURE CITED
 
    Growth performance and muscle characteristics. Sequential feeding significantly affected growth performance; within-program body weights from sequential chickens were significantly reduced compared with ML-Ctl chickens (–9 and –12% for sequences S1 and S2, respectively). Groups, i.e. HL-S1, LL-S1, ML-S2, and LL-S2, did not significantly differ (Table 2). Protein content was significantly lower in the Pectoralis major muscle of chickens fed the LL diet compared with the HL-S1 and ML-Ctl groups, but this result was probably not due to reduced muscle RNA content or Cs (i.e. capacity for muscle protein synthesis). Moreover, feeding an alternation of diets varying in lysine content did not drastically modify the expression of adult fast myosin heavy chain (MyHC), which is the major MyHC in the Pectoralis major muscle of chickens and represents the bulk of muscle proteins.


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  		TABLE 2 Effects of 48-h–cycle sequential feeding with diets varying in lysine content on growth performance and muscle characteristics in chickens at 24 d of age1

 
    Muscle expression of genes related to proteolysis. Lysine intake greatly affects muscle protein breakdown, particularly in Pectoralis major muscle (4,5). We therefore investigated muscle expression of genes related to proteolysis. Expression of m-calpain and cathepsin B was significantly affected by dietary treatments, with significantly higher mRNA levels in the muscle of chickens fed the LL diet than in the HL-S1 and ML-S2 groups (Fig. 1). The ML-Ctl group exhibited intermediate values, which did not significantly differ from those of the other groups, i.e. HL-S1, LL-S1, ML-S2, and LL-S2. Conversely, the mRNA levels of the 20S proteasome C2 subunit and ubiquitin were unchanged, irrespective of dietary treatment (data not shown). Because the ubiquitin-proteasome proteolytic pathway is controlled by the expression of E3 ubiquitin ligases, we then examined the potential changes in MurF1 and atrogin-1. MurF1 mRNA levels were twice as high in the muscle of chickens fed the LL diet (S1 and S2) than in the HL-S1, ML-S2, and ML-Ctl groups (Fig. 2A). Atrogin-1 expression was twice as high in the LL-S1 group compared with the HL-S1 and ML-Ctl groups, but S2 did not differ between the LL and ML groups (Fig. 2B). To extend these findings, we investigated the regulation of MurF1 and Atrogin-1 in another original model of cyclical changes in diet composition (23). Interestingly, MurF1 and Atrogin-1 were overexpressed in the muscle of chickens transiently fed a low-protein diet compared with an isoenergetic high-protein diet (Supplemental Fig. 1).


Figure 1
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  		FIGURE 1  Effects of 48-h–cycle sequential feeding with diets varying in lysine content on the expression of genes related to Ca2+-dependent (A) and lysosomal (B) proteolysis in breast muscle of 24-d-old chickens. Analysis was using real-time RT-PCR for m-calpain, cathepsin B, 20S proteasome C2 subunit, and ubiquitin. mRNA levels were normalized using 18S rRNA; 18S was not significantly affected by dietary treatments. Data are expressed as means ± SEM, n = 6. Means without a common letter differ, P < 0.05. Whatever the dietary treatment within a sequence, the indicated diet corresponds to the last diet in a cycle before tissue sampling.

 

Figure 2
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  		FIGURE 2  Effects of 48-h–cycle sequential feeding with diets varying in lysine content on the expression of MurF1 (A) and atrogin-1 (B), and the phosphorylation of FoxO3A (C) and TOR (D) in breast muscle of 24-d-old chickens. (A,B) Analysis by real-time RT-PCR. mRNA levels were normalized using 18S rRNA; 18S was not significantly affected by dietary treatments. (C,D) Representative western blots of FoxO3A and TOR phosphorylation. Blots were quantified and the phospho-FoxO3A:FoxO3A ratio and phospho-TOR:TOR ratio were determined. Data are expressed as means ± SEM, n = 6. Means without a common letter differ, P < 0.05. Whatever the dietary treatment within a sequence, the indicated diet corresponds to the last diet in a cycle before tissue sampling.

 
    FoxO3A and TOR phosphorylation. MurF1 and atrogin-1 are regulated via mechanisms involving the protein kinase B/Forkhead box-O transcription factors (FoxO) and protein kinase B/mammalian target of rapamycin pathways (29–31). We first focused on the potential changes in FoxO3A phosphorylation induced by daily variations in dietary lysine content. The levels of phosphorylated FoxO3A were ~2-fold lower in muscle of chickens fed the LL diet (S1 or S2) compared with the HL-S1, ML-S2, and ML-Ctl groups (Fig. 2C), suggesting that the overexpression of the E3 ubiquitin ligases (at least MurF1) in LL groups can be partly explained by significantly decreased FoxO3A phosphorylation. We then examined TOR phosphorylation. Despite lower phospho-TOR levels in the muscle of chickens fed the LL diet compared with the HL diet in sequence S1 (data not shown), we did not demonstrate a significant effect of daily lysine variation in that sequence when TOR phosphorylation on residue S2448 was normalized for total TOR content (Fig. 2D). Nevertheless, the correlation between FoxO3A phosphorylation and expression of the genes studied was significant for MurF1 (r = –0.362; P < 0.05) but not for atrogin-1, suggesting quite different regulatory mechanisms for the 2 E3 ubiquitin ligases.


   Discussion
TOP
 ABSTRACT
 Introduction
 Materials and Methods
 Results
 Discussion
LITERATURE CITED
 
Our study was designed to explore the short-term regulation of muscle proteolysis induced by daily variations in dietary lysine content. Both sequential feeding programs significantly reduced chicken growth rate. In particular, giving the HL rather than the ML diet (sequence S1 vs. sequence S2) did not alleviate impaired chicken growth due to sequential feeding. As expected, because birds received a LL diet for one-half of the 48-h cycles, the reduction in body weight in sequential groups was less than that observed with chronic dietary lysine deficiency, i.e. approximately –11% compared with ~–40% using diets containing 75% of the standard lysine content (2,4). Under our experimental conditions and as previously observed (22), the reduction in body weight due to sequential feeding was also less pronounced than that in another study alternating diets of different lysine composition (~–20%) (32). These differences may have been due to the duration of sequential feeding cycles (48 vs. 24 h) that can affect growth performance (33) and the timing of beginning sequential feeding programs (at 10 vs. 2 d of age), resulting in a less deleterious effect on growth. For breast muscle characteristics, a transient decrease in muscle protein content was observed following the distribution of the LL diet, but sequential feeding did not induce any alteration in the capacity for muscle protein synthesis and myosin expression. Recent experiments performed using similar 48-h cycle sequential feeding programs indicated that breast muscle proportion (relative to body weight) was not impaired after 2 wk of cyclic feeding with alternations of LL and HL diets (C. Leterrier, P. Perrot, S. Tesseraud., unpublished data). Taken together, these findings suggest that feeding birds with alternations of diets varying in lysine content does not specifically affect breast muscle development.

In this study, cathepsin B and m-calpain expression significantly differed between the 2 diets within a sequence, with higher mRNA levels in the Pectoralis major muscle of chickens transiently receiving the LL diet and thus lower values for HL and ML diets (sequences S1 and S2, respectively). Our findings therefore indicate that daily variations in dietary lysine content regulate genes related to lysosomal and Ca2+-dependent proteolysis in chicken skeletal muscles. It is noteworthy that these findings do not depend on the extent of daily lysine variations (alternation of LL and HL diets compared with alternation of LL and ML diets), because results were similar between sequences S1 and S2. Cathepsins B, H, L, and D are major proteases of lysosomal protolysis, a process regulated by starvation and amino acid deprivation and having important functions in the physiology and pathology of skeletal muscles (34). Calpains such as m-calpain and µ-calpain are cytosolic cysteine proteases of the Ca2+-dependent system that may initiate myofibrillar proteolysis and be involved in muscle wasting (35). These findings support the involvement of lysosomal and Ca2+-dependent systems in the control of muscle proteolysis and mass, despite the undeniable role of a 3rd and predominant proteolytic process in muscle, i.e. the ubiquitin-proteasome–dependent pathway (11,12). In our experimental conditions, the mRNA levels of the 20S proteasome C2 subunit and ubiquitin were similar in all dietary treatments. However, expression of the E3 ubiquitin ligases MurF1 (both sequences S1 and S2) and atrogin-1 (sequence S1) was upregulated in chickens fed the LL diet, suggesting that ubiquitin-proteasome–dependent proteolysis is also affected by alternating diets of varying lysine content. Thus, our findings suggest activation of the 3 major proteolytic pathways in the chicken muscle of the LL groups, in agreement with higher proteolysis rates found in the muscle of chickens receiving lower lysine intake (4,5). Considering that the LL diet used was in other respects adequate in energy and balanced in terms of other amino acids, such exacerbated proteolysis was without the drastic and atrophic conditions in catabolic diseases or fasting. However, the breakdown of skeletal muscle proteins probably provides the body with amino acids (particularly lysine, the most abundant amino acid in skeletal muscle proteins) that are used in the synthesis of new proteins. Such particularly pronounced response in the Pectoralis major muscle (entirely fast-twitch glycolytic fiber type) is probably dependent on muscle type, because a muscle-specific regulation of the E3 ubiquitin ligases MurF1 and atrogin-1 has been previously observed in mature rats (36). Similarly, highly fast-twitch glycolytic rat muscles have been reported to respond the most to nutritional factors in terms of variation in protein turnover compared with slow-twitch oxidative muscles (37,38). A component of the variability could be also muscle-specific and related to the function and solicitation of a particular muscle (38). This is consistent with the idea that the breast muscle of growing chickens, which has been submitted to intensive genetic selection and has little functional purpose, could represent a sizeable protein store in deficient states (2,3).

This study provides evidence that the 2 atrophy-related E3 ubiquitin ligases can be overexpressed following cyclical decreases in lysine supply. Whether or not such transient changes in atrogene expression are induced by nutrients, hormones, or both is still uncertain, but our current findings extend the understanding of mechanisms regulating muscle proteolysis in physiological conditions. We observed different patterns of gene expression between atrogin-1 and MurF1 due to dissimilar regulation within S2. These findings are in agreement with previous results indicating differences in in vivo regulation of atrogin-1 and MurF1 expression (36). Moreover, correlations between FoxO phosphorylation and MurF1 expression support the hypothesis that the FoxO signaling cascade is involved in the control of E3 ubiquitin ligases (29–31,39). The TOR signaling pathway has also been shown to contribute to the regulation of atrogin-1 in in vitro studies (31,40,41). However, using these experimental conditions, we did not find significant differences in TOR phosphorylation due to daily variations in lysine intake. Altogether, our data suggest the contribution of FoxO signaling in atrogene regulation and do not exclude the possibility of different mechanisms regulating atrogin-1 and MurF1 expression, as demonstrated in in vitro studies (40).

We report here feeding-related changes in proteolytic gene expression, particularly atrogin-1 and MurF1 expression, in an original model of sequential feeding that is very different from the comparison of feeding status (e.g. fasting and/or refeeding after food deprivation) usually studied in the literature (18–20,42). Because food is consumed throughout the light period, providing an almost continuous supply of nutrients in chickens (43), there are no repeated cycles of postabsorptive and feeding states due to meals. However, the use of sequential feeding programs demonstrates the time-sensitive regulation of genes related to the 3 major proteolytic pathways in chicken muscle according to lysine intake. Such temporal regulation of atrogin-1 and MurF1 in response to changes in amino acid intake has also been found using 48-h–cycle sequential feeding with diets varying in protein content (Supplemental Fig. 1). These findings suggest that chickens exhibit a high metabolism capacity to compensate for variations in amino acid supply, which might provide new opportunities for formulating diets or developing new feeding programs (23,33). Interestingly, 2 cycles were sufficient to initiate changes in atrogene expression (protein alternation, Supplemental Fig. 1) and 7 cycles were still efficient in inducing these changes (lysine alternation, Fig. 2). These 2 experimental paradigms therefore indicate some consistent mechanisms of atrogene regulation under cyclic feeding regime.

In conclusion, daily variations in dietary lysine content affect the expression of genes related to proteolysis in chicken muscle. Our results suggest activation of the lysosomal, Ca2+-dependent, and ubiquitin-proteasome–dependent proteolytic systems in chickens transiently receiving lower lysine intake in sequential feeding programs. We demonstrated that the E3 ubiquitin ligases MurF1 and atrogin-1 were regulated by the cyclical dietary treatments, thereby providing new enlightenments in the understanding of atrogene regulation in physiological conditions. These findings also indicate that sequential feeding represents an interesting model for exploring chrononutrition, with the aim of developing new nutritional strategies or modifying constraints for diet formulation. To further explore the regulatory mechanism under sequential feeding, time-course experiments are needed to better integrate the dynamic nature of these regulations and test a possible long-term adaptation of gene expression.


   ACKNOWLEDGMENTS
 
We thank Florence Favreau, Paul Constantin, and Michel Derouet (INRA, Nouzilly, France) for their technical assistance. We also thank Cécile Berri (INRA, Nouzilly, France) for valuable discussions.


   FOOTNOTES
 
1 Supported by research grants from Association de Coordination Technique Agricole/Ministère de l'Agriculture et de la Pêche/Ministère de l'Enseignement Supérieur et de la Recherche and Institut National de la Recherche Agronomique (INRA). Back

2 Supplemental Table 1 and Supplemental Figure 1 are available with the online posting of this paper at jn.nutrition.org. Back

3 Author disclosures: S. Tesseraud, I. Bouvarel, A. Collin, E. Audouin, S. Crochet, I. Seiliez, and C. Leterrier, no conflicts of interest. Back

8 Abbreviations used: atrogin-1 or MAFbx, Muscle Atrophy F box; Ctl, control treatment with the complete standard diet; Cs, ribosomal capacity; FoxO, forkhead box-O transcription factor; HL, high-lysine diet; LL, low-lysine diet; ML, medium-lysine diet; mTOR, mammalian target of rapamycin; MurF1, Muscle Ring Finger-1; MyHC, myosin heavy chain; S1, sequential feeding with alternation of LL and HL diets; S2, sequential feeding with alternation of LL and ML diets. Back

Manuscript received 7 July 2008. Initial review completed 29 July 2008. Revision accepted 7 October 2008.


   LITERATURE CITED
TOP
 ABSTRACT
 Introduction
 Materials and Methods
 Results
 Discussion
 LITERATURE CITED
 

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