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Article

Various Macronutrient Intakes Additively Stimulate Protein Synthesis in Liver and Muscle of Food-Deprived Chicks¹

Laboratory of Animal Nutrition, Graduate School of Bioagricultural Sciences, Nagoya University, Nagoya 464-8601, Japan

²To whom correspondence should be addressed. The present address is Laboratory of Grassland Science, University Farm, School of Agricultural Sciences, Nagoya University, Togo, Aichi 470-0151, Japan.

	ABSTRACT

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We investigated the influence of refeeding food-deprived chicks with either protein, carbohydrate, fat or combinations thereof on the rates of liver and muscle protein synthesis. After 2 d of food-deprivation, chicks were given individual or mixed protein, carbohydrate and fat. At 30 min after refeeding, the protein fractional synthesis rate (K_s) was measured by a large dose injection of L-[2,6-³H]phenylalanine. When chicks were food-deprived for 2 d, liver K_s was 67% lower and muscle fractional synthesis rate was half that of well-fed controls. Upon refeeding starved chicks a complete diet, K_s in the liver and muscle returned to the level of fed controls within 30 min. When food-deprived chicks were refed protein alone or two of the three macronutrients, liver and muscle K_s were significantly higher than those in the starved group. There was no effect of refeeding with carbohydrate or fat alone. Plasma glucose concentration was significantly greater than in fed or starved groups in chicks refed the complete diet, carbohydrate or carbohydrate mixed with either protein or fat. Refeeding chicks with the various macronutrients did not affect the plasma insulin or insulin-like growth factor-I concentrations. These results suggest that intakes of individual macronutrients additively increase liver and muscle protein synthesis and that the acute increase in muscle protein synthesis after refeeding chicks diets containing the three macronutrients was mainly regulated by the change in ribosomal efficiency.

KEY WORDS: • protein synthesis • nutrient • chickens • liver • muscle

	INTRODUCTION

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The rates of liver and muscle protein synthesis in avian species are very sensitive to changes in nutritional status. When growing chickens are deprived of dietary protein, liver protein synthesis is reduced, largely by a decrease in ribosomal capacity for protein synthesis (C_s, RNA-to-protein ratio)³ and/or by a reduction in ribosomal efficiency for protein synthesis (K_RNA, total protein synthesized per total RNA) (Kita et al. 1996a , Muramatsu et al. 1983 ). A dietary protein concentration twice that of the required amount recommended by NRC (1984) and Scott et al. (1982) also decreases liver protein synthesis in chickens due to a fall in C_s (Kita and Okumura 1993 ). Furthermore, muscle protein synthesis in chicks given a protein-free diet is almost halved as a result of a fall in K_RNA (MacDonald and Swick 1981 ), which was confirmed by Muramatsu et al. (1987) .

Many studies have reported that protein synthesis in skeletal muscle and the liver rises immediately after the beginning of feeding. In starved mice, an acute rise of protein synthesis in skeletal muscle and the liver was observed after 1 h of refeeding a complete diet (Yoshizawa et al. 1995 ). However, there is little information concerning the roles and interactions of individual dietary components in stimulating tissue protein synthesis of chicks. Therefore, the aim of this study was to refeed food-deprived chicks protein, carbohydrate and fat, alone or in combination, to examine their influence on the rate of protein synthesis in the liver and muscle. Since it was found that insulin (Bark et al. 1988, Garlick and Grant 1988 ) and insulin-like growth factor-I (IGF-I) (Douglas et al. 1991 ) play an important role in the regulation of protein synthesis, we also measured these.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Animals and diets.

Two experiments were conducted to investigate the effect of macronutrients on protein synthesis and plasma components of food-deprived chicks. In expt. 1, 200 single-comb White Leghorn male chicks from a local hatchery (Hattori Yokei Ltd., Nagoya, Japan) were fed a commercial chick mash diet (crude protein 21.5%, metabolizable energy 12.1 kJ/g; Marubeni Siryou Ltd., Tokyo, Japan) from hatching until 7 d of age. Chicks were housed in electrically heated brooders. According to Scott et al. (1982) and NRC (1984) , the dietary protein requirements for male Leghorn-type chicks are 21.5 and 18.0%, respectively. In the present study, 20% dietary protein was fed. At this age, the birds were allowed free access to a complete diet for 8 d (Table 1 ). At 15 d of age, 72 birds of uniform body weight (average initial body weight ± SD was 129.6 ± 1.1 g) were selected and divided evenly into nine experimental groups of eight birds each. The birds were placed in individual stainless steel metabolism cages in a temperature-controlled (29 ± 1°C) room. Continuous illumination was provided. At this age, 64 chicks in eight experimental groups were deprived of food. The eight chicks in the remaining group were allowed free access to the complete diet and served as reference controls. Experiments were performed after 2 d of food-deprivation. Eight chicks in one of the food-deprived groups were force-fed 4.80 g of the complete diet mixed with 9.6 mL of water. This amount was the maximum amount of the complete diet which could be force-fed into the crop of chicks at once. Forty-eight starved birds in the six other treatment groups were force-fed one of the experimental diets containing only protein, carbohydrate or fat, or combinations thereof. The amounts of each experimental diet force-fed with water were 1.19, 2.41, 0.14, 3.60, 1.33 and 2.55 g of the protein, carbohydrate, fat, protein plus carbohydrate, protein plus fat and carbohydrate plus fat diets, respectively (Table 1) . These amounts corresponded to the equivalent level of each nutrient in 4.80 g of the complete diet. The remaining group of food-deprived chicks were used as food-deprived controls. After 30 min of refeeding, liver and muscle protein synthesis was determined. In expt. 2, to measure the concentration of plasma components, expt. 1 was repeated but blood was collected and plasma glucose, triglyceride, albumin, total protein, nonesterified fatty acid (NEFA), cholesterol, insulin and IGF-I were measured. Animal care was in compliance with the applicable guidelines of the Nagoya University Policy on Animal Care and Use.

Fractional synthesis rates (K_s) of liver and muscle protein were measured using a large dose injection of L-[2,6-³H]phenylalanine (12.3 MBq/mol; Amersham Japan, Tokyo, Japan) (Garlick et al. 1980 ). Measurement of the rate of protein synthesis of chickens was previously described by Muramatsu and Okumura (1985) . To determine the free and bound phenylalanine specific activity, ~1 g of tissue was added to 5 mL of perchloric acid (0.14 mol/L PCA) homogenized and then centrifuged. The supernatant was neutralized with 0.3–0.5 mL of saturated potassium citrate solution. The specific radioactivity of free phenylalanine was measured in the supernatant. Protein-bound phenylalanine was obtained after protein reprecipitation with PCA and subsequent hydrolysis with 6 mol/L of HCl overnight at 110°C. Hydrochloric acid was then removed from hydrolysate by evaporation. The samples containing free amino acids or hydrolysate were incubated with L-tyrosine decarboxylase and pyridoxal phosphate (PLP) overnight at 37°C. ß-Phenylethylamine was extracted by addition of sodium hydrochloride and heptane. Sulfuric acid (0.01 mol/L) was then added to the supernatant. Radioactivity was measured by liquid scintillation counting, and the assay of ß-phenylethylamine was performed by fluorospectrophotometry using ninhydrin and L-leucylalanine. The K_s of protein was calculated using formula described by McNurlan et al. (1979) as follows: K_s = Sb x 100/Sa x t, where Sb, Sa and t represent the specific radioactivity of protein-bound phenylalanine at 10 min, the mean specific radioactivity of free phenylalanine over the time interval of 0–10 min, and the time expressed in days, respectively.

Insulin, IGF-1 and other plasma components.

Blood samples were obtained and centrifuged. The plasma was frozen at -80°C until analyzed. Plasma metabolites were measured using commercial kits (Wako Pure Chemicals Industries, Ltd., Osaka, Japan; glucose CII-test Wako kits for plasma glucose, triglyceride G-test Wako kits for triglyceride, A/G B-test Wako kits for albumin and total protein, NEFA C-test Wako kits for nonesterified fatty acid and cholesterol E-test Wako kits for cholesterol concentrations. Plasma insulin concentration was determined by radioimmunoassay (RIA) which was developed by McMurtry et al. (1983) . Polyclonal antiserum from guinea pigs raised against chicken insulin was generously donated by J. P. McMurtry (Growth Biology Laboratory USDA, Beltsville, MD). Plasma IGF-I concentration was determined by radioimmunoassay according to the method described by Ballard et al. (1990) . Rabbit polyclonal antiserum against human IGF-I was a gift from Dr. P. C. Owens (Cooperative Research Center for Tissue Growth and Repair, Adelaide, SA, Australia). In our previous report (Kita et al. 1996c ), the cross reactivities of chicken IGF-I, human IGF-I and human insulin were compared in the chicken IGF-I RIA. In this assay, 50% of competition for binding occurred with 285 pg of chicken IGF-I/tube. Human IGF-I had equal potency to chicken IGF-I. The coefficients of variation within and between assays for chicken insulin were 11.6 and 5.3%, for chicken IGF were 5.4 and 4.1%, respectively.

Statistics.

Statistical analyses of data were performed by one-way ANOVA followed by Duncan’s multiple range test. Three-way ANOVA was also performed to test main and interactive effects of the three nutrients. All statistical analyses were performed using the General Linear Model Procedures (GLM; SAS/STAT Version 6; SAS Institute, Cary, NC). Differences between means were considered to be significant at P < 0.05. Regression analysis was also performed using GLM.

	RESULTS

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Body, liver and muscle weight.

After food-deprivation for 2 d, the weights of body, liver and muscle of chicks were lower than those of fed chicks. Refeeding did not alter body, liver and muscle weights within 30 min (Table 2 ).

Hepatic protein and RNA contents of food-deprived chicks were lower than those of fed controls. These variables did not respond to refeeding. Muscle protein and RNA contents showed similar trends to those observed in the liver.

Tissue protein synthesis.

The K_s in the liver was significantly lower than in fed controls after 2 d of food-deprivation and was not different from that of fed chicks in those refed a complete diet (Table 3 ). The additive response of liver and muscle K_s on refeeding various macronutrients was also presented in Figure 1 . When chicks were refed protein alone, K_s increased significantly but was not fully restored to the value in fed chicks. The hepatic K_s was not increased by refeeding chicks with either carbohydrate or fat alone. In chicks refed protein mixed with either carbohydrate or fat, the K_s values were not significantly different from those of fed controls. Refeeding with carbohydrate plus fat increased the K_s compared with that in food-deprived chicks but did normalize the value. Protein synthesized in the liver showed similar trends to those of K_s in response to food-deprivation and refeeding although values in all experimental groups were significantly lower than in fed controls.

View larger version (37K): [in this window] [in a new window]   Figure 1. Relationship between the fractional synthesis rate of protein (Ks) stimulated by refeeding starved chicks the complete diet and the sum of increase in Ks stimulated by refeeding individual macronutrients in the liver and muscle. The increase was derived from the difference between Ks stimulated by refeeding and that in the food-deprived group. Values are means ± SD; n = 5.

Hepatic C_s, as indicated by the RNA-to-protein ratio, was unaffected by starvation or refeeding (Table 4 ). In the liver, K_RNA was not affected by dietary treatments. Although protein synthesized in the muscle changed in a manner similar to K_s in response to food-deprivation and refeeding, the influence of refeeding on protein synthesized was less than that on K_s (Table 3) . In the muscle, food-deprivation and refeeding did not alter C_s but after refeeding a complete diet which contained three macronutrients, K_RNA returned to the control level (Table 4) .

Two-day of food-deprivation reduced plasma IGF-I concentration, but no change was observed in glucose or insulin concentrations (Table 5 ). The concentration of glucose was greater than in fed or starved groups when chicks were refed for 30 min with the complete diet, carbohydrate only or carbohydrate mixed with either protein or fat. However, the positive effect of refeeding was not observed on insulin and IGF-I concentrations.

Plasma triglyceride, albumin and total protein concentrations were significantly lower after 2 d of food-deprivation but no change was observed in free fatty acid or cholesterol concentrations (data were not shown). In all treatments, refeeding did not alter the concentration of these plasma metabolites.

	DISCUSSION

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On the basis of nutritional and experimental studies, it has been assumed that nutrient intakes are regulatory factors for stimulation of liver and muscle protein synthesis. The present study was done to investigate systematically the effects of refeeding various macronutrients, namely protein, carbohydrate and fat, on liver and muscle protein synthesis in chicks which had been food-deprived. The amounts of protein, carbohydrate and fat which were refed were equivalent to the levels of each nutrient in 4.8 g of the complete diet, which was the maximum amount force-fed to chicks at once after 2 d of food-deprivation (Table 1) . Our previous study indicated that the average food intake of a complete diet by growing Leghorn-type chicks between 7 to 17 d of age was 16.2 g/d (Muramatsu et al. 1987 ). The amount of diet force-fed to chicks, 4.8 g/chick (Table 1) , corresponded to about 30% of the daily food consumption of 17-d-old chicks. This amount was considered sufficient for the purpose of the present study because tissue protein synthesis was measured after only 30 min of refeeding.

As shown in Table 3 , when chicks were food-deprived for 2 d, liver and muscle K_s were decreased to 67% and about half of well-fed controls, respectively. Chicks refed with the complete diet had normal K_s in both tissues. These results are inconsistent with those obtained in different species. In rats, the rate of liver protein synthesis was reduced by food-deprivation and recovered by refeeding (McNurlan et al. 1979 , Mosoni et al. 1996 , Preedy et al. 1988 ). Similar trends for liver protein synthesis were reported in growing chickens (Nieto et al. 1994 ). The response of muscle protein synthesis to food-deprivation and refeeding appears to be similar in humans (Rennie et al. 1982 ), rats (Davis et al. 1993 , Garlick et al. 1975 , Garlick et al. 1983 , Garlick et al. 1987 , Millward and Waterlow 1978 , Mosoni et al. 1996 , Preedy et al. 1988 ), pigs (Davis et al. 1996 ) and chickens (Nieto et al. 1994 ). In general, these results suggest that during food-deprivation muscle protein synthesis is decreased to about half that of fed controls and that refeeding returns the level to that before food-deprivation. There was no significant difference among the K_s of chicks given each nutrient alone (Nieto et al. 1994 ) and K_s in the carbohydrate- and fat-fed groups tended to be higher than that of starved chicks (Kita et al. 1996b ). We conclude that the acute increase in muscle and liver K_s was stimulated by refeeding of protein only or a combination of two macronutrients.

We previously reported that the rate of whole-body protein synthesis was dependent on nonprotein energy intake in growing chicks given a fixed level of dietary protein, and vice versa (Kita et al. 1989 and 1993 , Muramatsu et al. 1987 ). In these reports, the effect of dietary protein intake was much greater than that of dietary nonprotein energy intake, carbohydrate and fat. Furthermore, in growing pigs, additional protein in a conventional diet increased whole-body protein synthesis to a much greater extent than added carbohydrate or fat (Reeds et al. 1981 ). Garlick and Grant (1988) also reported that muscle protein synthesis in postabsorptive rats was increased by the intravenous infusion of amino acids in combination with low doses of insulin had a greater effect than that of insulin alone. These findings support the results of present study in which refeeding protein alone resulted in a much greater influence on the recovery of both liver and muscle protein synthesis following food-deprivation than carbohydrate or fat alone (Table 3) .

When food-deprived chicks were refed a mixture of protein, carbohydrate and fat, a higher stimulation of the K_s in both liver and muscle was seen compared to chicks given each nutrient alone. To investigate whether the stimulatory effects of protein, carbohydrate or fat intakes on liver and muscle K_s were interactive, a three-way ANOVA was performed (Table 6 ). Analysis showed that the main effects of refeeding with either protein or carbohydrate on liver and muscle K_s were significant. Moreover, in liver, the provision of fat also significantly increased the K_s of food-deprived chicks. This result is in agreement with the findings of Estornell et al. (1994) in which the addition of supplementary fat to a well-balanced diet improved liver protein synthesis in rats. Altogether, these results suggest that the addition of fat to protein or carbohydrate is also able to stimulate liver protein synthesis which was reduced by food-deprivation, and its effect was much higher than that in chicks refed fat alone.

Since Millward et al. (1973) found a positive correlation between muscle K_s and C_s, changes in K_s have been assessed by the use of two different parameters: C_s and K_RNA. In the present study, we measured the amount of tissue RNA and assessed the relationship of either C_s or K_RNA to K_s. As we had expected, in both liver and muscle, K_s was only closely related to K_RNA. The derived correlation equations were as follows: Liver; K_s (%/d) = 67.8 + 0.85 K_RNA (mg protein.mg RNA^-1 · d^-1) (r = 0.42, P = 0.004): Muscle; K_s (%/d) = 6.1 + K_RNA (mg protein.mg RNA^-1 · d^-1) (r = 0.55, P < 0.001). However, the changes in K_s were not related to changes in C_s when chicks were refed any of the experimental diets after food-deprivation. These results also indicated that compared to liver protein synthesis, the change in K_RNA largely regulated the acute increase of muscle protein synthesis during the first 30 min following cessation of food-deprivation. Waterlow et al. (1978) reviewed short-term changes in the K_s are due to changes in K_RNA and chronic change in K_s is associated with changes in C_s. Recently, Yoshizawa et al. (1995) have reported that when food-deprived mice were given a complete diet, liver and muscle protein synthesis increased within 1 h after refeeding and were accompanied by a rise in translation initiation activity. It was also reported that the mechanisms responsible for the stimulation of acute protein synthesis by refeeding could operate to affect the rate of elongation and the polysome size and involve the change of activity in both initiation and elongation. Therefore, the acute increase in K_s by refeeding chicks with individual macronutrients in the present study may also be associated with changes in translation initiation and/or elongation activities, and this issue should be studied in the future.

In the present study, we investigated whether the response of protein synthesis to refeeding various macronutrients was associated with changes in circulating concentrations of insulin, IGF-I or other plasma components. Plasma insulin (Dupont et al. 1998 ) and IGF-I concentrations of chickens (Ketelslegers et al. 1995 , Morishita et al. 1993 ) are very sensitive to chronic change in nutritional status, but no significant effects on these variables were found. We (Kita et al. 1998 ) have shown that plasma IGF-I concentration was decreased by food-deprivation and no response was observed within 1 h after refeeding. Therefore, plasma IGF-I concentration is not responsive acute to changes in nutritional status. In the present study, no significant effect on plasma insulin due to food-deprivation and refeeding was observed. Although Dupont et al. (1998) reported that plasma insulin concentration in chickens was decreased by food-deprivation and increased by refeeding, Langslow et al. (1970) showed no change in plasma insulin due to food-deprivation. Therefore, the change in plasma insulin level of avian species may be less responsive to changes in nutritional conditions than in mammalian species. When chicks were refed with carbohydrate only, or carbohydrate mixed with either protein or fat, plasma glucose concentration was higher than that in fed chicks. In the present study, no significant change in plasma glucose concentration due to food-deprivation was observed. This result was consistent with the report by Langslow at al (1970), which suggests that the blood glucose of chicks is much more resistant to starvation-induced hypoglycemia than in rats (Belo et al. 1976 , Brady et al. 1978 ).

We conclude that refeeding starved chicks protein and carbohydrate can increase liver and muscle protein synthesis in chicks which had been food-deprived. These results also indicate that the stimulation muscle protein synthesis after refeeding with diets containing three macronutrients was mainly regulated by the change in K_RNA compared to liver protein synthesis. The effects of each of these macronutrients on protein synthesis appear to be additive rather than interactive. Stimulation of liver and muscle protein synthesis by refeeding various nutrients was not due to the changes in plasma glucose, insulin or IGF-I concentrations.

	FOOTNOTES

 
¹ Financial support was provided by a grant-in-aid (Number 08456140) for Scientific Research (B) from The Ministry of Education, Science Sports and Culture, Japan.

³ Abbreviations used: C, carbohydrate; Cs, ribosomal capacity; F, fat; FSR, fractional synthesis rate; GLM, General Linear Model; IGF-I, insulin-like growth factor-I; K_s, the fractional rate of protein synthesis; K_RNA, ribosomal efficiency; NEFA, nonesterified fatty acid; P, protein; PCA, perchloric acid; RIA, radioimmunoassay; Sa, specific radioactivity of free phenylalanine; Sb, specific radioactivity of protein-bound phenylalanine.

Manuscript received May 10, 1999. Initial review completed June 18, 1999. Revision accepted October 7, 1999.

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