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Dietary Nitrogen Intake Regulates Hepatic Malic Enzyme Messenger Ribonucleic Acid Expression¹

Department of Poultry Science, University of Georgia, Athens 30602

² Corresponding author: ajdavis{at}uga.edu

	ABSTRACT

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Increased dietary protein intake rapidly (3 h) decreases malic enzyme and increases hepatic histidase mRNA expression. Experiments were conducted to determine the role that individual dispensable amino acids and nonprotein N sources might have in regulating the activity of these enzymes and to determine if the addition of a N supplement to a practical broiler diet during the entire rearing period would reduce abdominal fat accumulation in broilers. Broiler chicks were fed a basal diet containing 22% protein or this diet supplemented with 9.5% L-Glu, 5% Gly, 6% L-Ala, 5.08% ammonium bicarbonate, or 4.25% dibasic ammonium phosphate for 24 h. Each of the dietary supplements added 0.90% total N to the diet. Hepatic malic enzyme mRNA expression was significantly (P < 0.05) depressed in chicks fed any of the supplemented diets compared with chicks fed the basal diet. Histidase mRNA expression, however, was only significantly increased in the chicks fed the basal diet supplemented with Gly. Broilers fed practical corn-soybean meal starter and developer diets supplemented with 2.3, 4.7, or 9.5% Glu from 0 to 40 d of age had significantly smaller abdominal fat pads relative to BW than broilers fed the unsupplemented corn-soybean meal diets. Feeding the Glu supplements, however, reduced the overall BW gain of broilers by 100 to 150 g compared with broilers fed the unsupplemented diets. The results suggest that hepatic mRNA expression of malic enzyme may be regulated by total dietary N intake, whereas hepatic mRNA expression of histidase may be regulated by specific amino acids.

Key Words: broiler chick • fat synthesis • nonprotein nitrogen

	INTRODUCTION

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Malic enzyme (EC 1.1.1.40 [EC] ) is a cytoplasmic protein that catalyzes the oxidative decarboxylation of malate to pyruvate and CO₂ while simultaneously generating NADPH from NADP⁺. The generated NADPH can be utilized in the de novo synthesis of palmitate, which is the precursor molecule for the formation of other long-chain fatty acids. The activity of hepatic malic enzyme is positively correlated with the rate of fatty acid synthesis, the percentage of body fat, and the percentage of abdominal fat in chicks (Yeh and Leveille, 1969; Pfaff, 1977; Tanaka et al., 1983; Grisoni et al., 1991; Adams and Davis, 2001; Chendrimada et al., 2006).

Histidase (EC 4.3.1.3 [EC] ) deaminates L-His to trans-urocanic acid. In the liver, urocanase converts trans-urocanic acid to imidazolonepropionic acid, which is subsequently converted to Glu. Hepatic histidase mRNA expression and activity increase when chicks are fed increasing levels of dietary protein (Scott and Austic, 1982; Keene and Austic, 2001; Chendrimada and Davis, 2005; Chendrimada et al., 2006).

Adams and Davis (2001) reported that switching chicks from a basal protein diet (22 g/100 g of diet) to a low-(13 g/100 g of diet) or high- (40 g/100 g of diet) protein diet resulted in a rapid (3 h) change in the expression of the mRNA for malic enzyme. A switch to a low-protein diet increased the level of malic enzyme mRNA, whereas feeding a high-protein diet decreased its level. In contrast, the activity of hepatic histidase was significantly increased 3 h after the chicks were fed the diets containing higher levels of dietary protein (Chendrimada and Davis, 2005). Subsequent research to determine if malic enzyme and histidase mRNA expression were regulated by a mixture of indispensable or dispensable amino acids indicated that although supplementing the basal (22%) protein diet with indispensable or dispensable amino acids significantly altered the mRNA expression of malic enzyme and histidase, both supplements failed to elicit a response equivalent to the high (40%) protein diet (Chendrimada et al., 2006). When the indispensable or dispensable amino acid supplements were added to the basal diet, the concentration of the individual indispensable or dispensable amino acids of the supplemented diet equaled the concentrations of these amino acids in the high-protein diet. Thus, the total N content of the indispensable and dispensable amino acid-supplemented diets was intermediate to the levels contained in the basal and high-protein diets. Therefore, the intermediate mRNA expression of malic enzyme and histidase in the chicks fed either the indispensable or dispensable amino acid supplement suggested that the regulation of the hepatic mRNA expression of these 2 enzymes is based on the intake of a specific mixture of indispensable and dispensable amino acids or simply on total dietary N intake.

The present research was conducted to determine if supplementing the basal protein diet with individual amino acids or nonprotein N compounds would elicit a change in both histidase and malic enzyme mRNA expression. In addition, the present research will determine if the addition of a dietary supplement, known to rapidly depress malic enzyme mRNA expression, to practical corn-soybean meal starter and grower-finisher diets will reduce the abdominal fat pad weight of broilers raised on these diets from 0 to 40 d of age.

	MATERIALS AND METHODS

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Experiments 1 and 2
These experiments were conducted to determine the role of increased dietary N intake from individual amino acid or nonprotein N supplements on the regulation of malic enzyme and histidase mRNA expression. One-day-old mixed-sex broiler chicks were raised in thermostatically controlled, electrically heated battery brooder cages with wire floors. The cages were lighted for 24 h/d, and the chicks had free access to a practical chick starter diet and water. Seven days after hatching, the chicks were sorted by weight, and those with extreme weights were discarded. The remaining chicks were randomly assigned to experimental groups so as to achieve a similar weight distribution among all pens. The chicks were then fed a glucose monohydrate and isolated soybean protein-based basal diet containing 22% protein for an acclimation period of 4 or 5 d, after which they were given access to the experimental diets. The semipurified basal diet used in the present experiments was the adjusted basal diet reported previously (Adams and Davis, 2001). For the sake of convenience, the adjusted basal diet will be designated as the basal diet in this manuscript. At the end of each experiment, feed consumption and BW gain were determined for each pen. The chicks were killed by cervical dislocation to obtain liver samples for RNA extraction. The Institutional Animal Care and Use Committee of the University of Georgia approved all animal procedures.

After the acclimation period in experiment 1, the chicks were divided into 5 groups of 6 replicate pens of 2 birds each. The chicks in 1 group were maintained on the basal diet, and the chicks in another group were fed the high-(40%) protein diet. The ingredient composition of the high-protein diet has been reported previously (Adams and Davis, 2001). The chicks in the remaining 3 groups were fed the basal diet supplemented with 9.5% L-Glu, 6% L-Ala, or 5% Gly. The addition of L-Glu, L-Ala, and Gly was at the expense of sand in the original adjusted basal diet (Adams and Davis, 2001), and to keep the diet isocaloric to the basal and high-protein diets, the corn oil of the basal diet was reduced from 11.50 to 8.10, 9.40, and 10.60% for the L-Glu-, L-Ala-, and Gly-supplemented diets, respectively. Each supplement contributed an additional 0.90% total N to the diet, which made the total amount of dietary N present in the basal-supplemented diets equivalent to the total amount of N present in the dispensable amino acid-supplemented basal diet utilized in our previous research (Chendrimada et al., 2006). The chicks were given free access to these diets for 24 h. At the end of the experiment, total feed consumption was determined for each pen, and liver samples were collected from each bird and combined by pen for RNA extraction.

Experiment 2 had an equivalent protocol as experiment 1 except for the dietary treatments. There were 4 dietary treatments consisting of 6 replicate pens of 2 birds each. One group of birds was maintained on the basal protein diet, whereas the other groups were fed either the high-protein diet or the basal diet supplemented with either 4.25% dibasic ammonium phosphate or 5.08% ammonium bicarbonate. The addition of the ammonium phosphate and ammonium bicarbonate supplements was at the expense of sand in the original adjusted basal diet (Adams and Davis, 2001). The amount of total N present in the supplemented basal diets was equivalent to that provided by the amino acid-supplemented diets in experiment 1.

Experiment 3
A broiler grow-out experiment was conducted to determine if supplementing a standard corn-soy diet with L-Glu would reduce the amount of abdominal fat present in broilers at processing age. A total of 500 straight-run 1-d-old broiler chicks (Ross x Ross, ConAgra, Athens, GA) were obtained and distributed to 24 floor pens containing pine shaving litter. The pens were maintained in an environmentally controlled room under a 24-h light cycle. Twenty pens with 20 chicks each (0.17 m²/bird) were randomly assigned to 4 diets (5 replicate pens per treatment). From 0 to 21 d, the chicks in these pens were fed either a practical corn-soybean meal diet or the corn-soybean meal diet supplemented with 2.3, 4.7, or 9.5% L-Glu (Table 1). The remaining 4 pens each contained 20 chicks, and these chicks were fed a diet that was similar to the 9.5% L-Glu-supplemented diet, except that the L-Glu was replaced by glucose monohydrate and sand. This final diet was included as a control diet to ensure that any differences between the practical corn-soybean meal diet and the diet supplemented with 9.5% L-Glu were related to the Glu supplementation and not due to the increase in the fat content of this diet to keep it isocaloric to the practical corn-soybean meal diet. After 21 d, the chicks were fed grower-finisher diets supplemented with L-Glu at levels equivalent to those used in the starter diets (Table 2).

RNA Extraction and Northern Blot Analysis
Total RNA was extracted from liver samples pooled by pen using a guanidinium thiocyanate-phenol-chloroform method (Chomczynski and Sacchi, 1987). Total RNA (40 µg/sample) was electrophoresed on an agarose-formaldehyde gel and then transferred to a nylon membrane as previously described (Davis and Johnson, 1998). Duck malic enzyme (Glynias et al., 1984), chicken histidase (Chendrimada and Davis, 2005), and chicken glyceraldehyde-3-phosphate dehydrogenase (GAPDH; Davis and Johnson, 1998) cDNA clones were prepared and labeled with ³²P for Northern blot analysis as previously described (Davis and Johnson, 1998). The hybridization and densitometry procedures followed those described previously (Davis and Johnson, 1998). There were 2 blots for each experimental period, and the replicate samples for each dietary treatment were divided equally between the 2 blots. The 2 blots were hybridized at the same time and exposed together on the same film. The blots were stripped (Davis and Johnson, 1998) of the previously hybridized probe before being hybridized with a subsequent probe. The order of the hybridizations was malic enzyme, histidase, and GAPDH. The relative mRNA expression of malic enzyme or histidase was determined for the samples of each blot by calculating the signal intensity of each sample relative to the strongest signal, which was assigned a value of 1. Before calculation of relative malic enzyme or histidase mRNA levels, GAPDH mRNA expression was used to correct the malic enzyme and histidase values for equality of RNA loading and transfer for each blot.

Statistical Analyses
Data from each experiment were subjected to ANOVA according to the GLM procedure, and Tukey’s multiple-comparison procedure was used to detect significant differences among the dietary treatments (Neter et al., 1990). All statistical procedures were done with the Minitab Statistical Software package (Release 13, State College, PA). Differences were considered significant when P < 0.05.

	RESULTS

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Experiments 1 and 2
Food consumption for the 24-h experimental period was significantly depressed in chicks fed either the Gly-supplemented diet (experiment 1) or the dibasic ammonium phosphate-supplemented diet (experiment 2) when compared with chicks fed any of the other experimental diets (Table 3).

View larger version (17K): [in this window] [in a new window]   Figure 1. The relative density of hepatic malic enzyme (A) and histidase (B) mRNA of chicks fed the basal diet, high-protein diet, or the basal diet supplemented with 9.5% L-Glu, 5% Gly, or 6% L-Ala (experiment 1) for 24 h. Values are means ± SEM, n = 6 replicate pens. a–cMeans with different letters differ (P < 0.05). Note that the relative densities of malic enzyme and histidase mRNA to one another are specific for each dietary group and that all statistical comparisons are within a given dietary group.

View larger version (16K): [in this window] [in a new window]   Figure 2. The relative density of hepatic malic enzyme (A) and histidase (B) mRNA of chicks fed the basal diet, high-protein diet, or the basal diet supplemented with either of the following nonprotein N (NPN) sources: 5.08% ammonium bicarbonate or 4.25% ammonium phosphate (experiment 2) for 24 h. Values are means ± SEM, n = 6 replicate pens. a–cMeans with different letters differ (P < 0.05). Note that the relative densities of malic enzyme and histidase mRNA to one another are specific for each dietary group and that all statistical comparisons are within a given dietary group.

For the entire experimental period (0 to 40 d), birds fed the basal corn-soybean meal diet gained more weight than the birds fed any of the diets supplemented with Glu (Table 4). Birds fed the control diet and the diet supplemented with 9.5% Glu had the lowest feed:gain values (Table 4). There were no significant differences in the prechilled percentage carcass yields among the birds fed the different dietary treatments (Table 5). Birds fed the 2.3, 4.7, and 9.5% Glu-supplemented diets had significantly lower relative abdominal fat pad weights than birds fed the practical corn-soybean meal diet or the control diet (Table 5).

	DISCUSSION

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The decision to use individual dispensable amino acids in the current research was made because dietary excesses of dispensable amino acids tend to have less effect on food consumption when compared with feeding a diet containing excess levels of an individual indispensable amino acid. Furthermore, dietary supplements of a mixture of dispensable or indispensable amino acids had each altered the mRNA expression of malic enzyme and histidase in a similar fashion (Chendrimada et al., 2006). Of the 3 amino acids chosen to supplement the basal diet, only the Gly supplement depressed food intake by broiler chicks. Davis and Austic (1997) reported a decrease in total food consumption over a 9-d period in Leghorn chicks that were fed a protein-adequate diet supplemented with 4% Gly. The current research indicates that the aversion of chicks to a protein-adequate diet supplemented with 5% Gly develops very quickly.

Goldman et al. (1985) found that when well-fed ducklings were starved, the level of malic enzyme mRNA rapidly decreased. The maximum inhibition of the transcription of malic enzyme mRNA by starvation occurs within 3 to 6 h of food removal (Goldman et al., 1985). Even though the situation for the birds fed the basal diet supplemented with Gly or ammonium phosphate is not equivalent to fasting, the reduced food consumption could have contributed to the reduced levels of malic enzyme mRNA expression in chicks fed these diets. In fact, the reduced food consumption with these 2 diets probably explains why the expression of malic enzyme in birds fed these 2 dietary treatments was equivalent or lower than the chicks fed the high-protein diet, even though the total dietary N content of the 2 basal-supplemented diets was intermediate to the basal and high-protein diets.

The severe reduction in food consumption in birds fed the dibasic ammonium phosphate-supplemented diet may have been due to a Ca-P imbalance. Holcombe et al. (1976) reported that laying hens exhibited an aversion to a 2.43% P diet compared with a 1.00% P diet when both diets contained 3% Ca. However, when the Ca level of the 2.43% P diet was elevated to 6%, the hens increased the consumption of this diet (Holcombe et al., 1976). In the current research, the amount of dietary P was increased by 1% when the ammonium phosphate supplement was added to the basal diet and the Ca content of the diet was not adjusted. The decision not to adjust the Ca content of the diet was based on the assumption that because the experimental duration was only 24 h, the poor Ca:P ratio would not affect food consumption. However, the broilers appeared to detect and respond to the imbalance in the Ca:P ratio very quickly. Feed intake of the broilers fed the dibasic ammonium phosphate-supplemented diet was significantly lower at 6 h (6 ± 1.5 vs. 16 ± 1.8, mean ± SEM, g/chick) than in broilers fed the basal diet.

In contrast to the results for malic enzyme, not all of the dietary supplements to the basal diet altered histidase mRNA expression. Only Gly supplementation significantly increased the mRNA expression of histidase. Although the increase in histidase mRNA expression by feeding the dietary Gly supplement is confounded by the decrease in food intake by birds fed this supplement, it appears that Gly may be a potent stimulator of the expression of hepatic histidase mRNA, because the decrease in food intake associated with feeding the dibasic ammonium phosphate supplement did not alter histidase mRNA expression. Previously, Chendrimada and Davis (2005) reported that supplementing the basal diet with His had no effect on histidase mRNA expression. Determining the specific amino acids that mediate the effect of dietary protein on histidase mRNA expression could help elucidate the hormonal and transcriptional factors involved in this response.

The problem of excess body fat continues to be a financial liability for the poultry industry, in particular, the accumulation of excessive body fat in the abdominal area. As an ever-increasing proportion of poultry products are sold as cut up and deboned products, it is no longer possible to include abdominal fat pads with the whole carcass. Thus, they may enter the rendering chain at a drastic decrease in value. Increasing the dietary protein content of broiler diets reduces abdominal fat pad weight (Cabel et al., 1988; Cabel and Waldroup, 1991; Summers et al., 1992; Deschepper and De Groote, 1995; Smith et al., 1998; Sklan and Plavnik, 2002). Previous research in our laboratory established that feeding broilers increasing dietary levels of protein reduces hepatic mRNA expression and subsequently the activity of malic enzyme, a key regulatory enzyme in the production of de novo fatty acids (Adams and Davis, 2001). However, the previous research in our laboratory and experiments 1 and 2 of the current research utilized semipurified diets and involved feeding the diets to broilers for 24 h or less. Experiment 3 of the current research was completed to determine if feeding a practical corn-soybean meal diet containing a supplement known to reduce malic enzyme mRNA expression to broilers from 0 to 40 d of age would reduce abdominal fat pad weight at processing age. L-Glutamic acid supplementation of a practical corn-soy broiler diet significantly reduced abdominal fat pad weights at slaughter. The difference in abdominal fat pad weight between a bird fed the practical diet supplemented with 2.3% L-Glu and one fed the practical diet was 7 g, and this difference increased to over 12 g for a bird fed the diet supplemented with 9.5% L-Glu. These results clearly demonstrate the potential utility of limiting the expression of malic enzyme activity in reducing abdominal fat pad size. Further research is needed to determine if an inexpensive dietary N supplement can be identified, which when added to practical broiler diets, reduces abdominal fat pad weights without causing a decrease in total weight gain and performance efficiency. In addition, further research is needed to determine the least amount of dietary supplementary N needed to significantly reduce fat pad weight and to determine if the additional dietary N could be fed for a shorter duration, possibly just during the finisher period, and still significantly reduce abdominal fat pad weights.

In summary, supplementing a protein-adequate diet with the dispensable amino acids L-Glu, L-Ala, or Gly as well as with the nonprotein N sources dibasic ammonium phosphate or ammonium bicarbonate significantly lowered the hepatic mRNA expression of malic enzyme. In contrast, histidase mRNA expression was only altered by the Gly supplement. Supplementing a practical, nutrient-adequate corn-soybean meal diet with 2.3, 4.7, or 9.5% Glu during an entire 40-d broiler production cycle reduced the abdominal fat content of these birds. The results suggest that hepatic malic enzyme mRNA expression may be regulated by dietary N content, whereas hepatic histidase mRNA expression is regulated by specific amino acids.

	FOOTNOTES

 
¹ This research was supported in part by grant number 280 from the US Poultry and Egg Association, Tucker, Georgia.

Received for publication February 3, 2007. Accepted for publication May 24, 2007.

	REFERENCES

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Adams, K. A., and A. J. Davis. 2001. Dietary protein concentration regulates the mRNA expression of chicken hepatic malic enzyme. J. Nutr. 131:2269–2274.[Abstract/Free Full Text]

Cabel, M. C., T. L. Goodwin, and P. W. Waldroup. 1988. Feather meal as a nonspecific nitrogen source for abdominal fat reduction in broilers during the finishing period. Poult. Sci. 67:300–306.[Web of Science][Medline]

Cabel, M. C., and P. W. Waldroup. 1991. Effect of dietary protein level and length of feeding on performance and abdominal fat content of broiler chickens. Poult. Sci. 70:1550–1558.[Web of Science][Medline]

Chendrimada, T. P., K. A. Adams, M. E. Freeman, and A. J. Davis. 2006. The role of glucagons in regulating chicken hepatic malic enzyme and histidase messenger ribonucleic acid expression in response to an increase in dietary protein. Poult. Sci. 85:753–760.[Abstract/Free Full Text]

Chendrimada, T, P., and A. J. Davis. 2005. Molecular cloning of chicken hepatic histidase and the regulation of histidase mRNA expression by dietary protein. J. Nutr. Biochem. 16:114–120.[Web of Science][Medline]

Chomczynski, P., and N. Sacchi. 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162:156–159.[Web of Science][Medline]

Dale, N. M. 2001. Feedstuffs ingredient analysis table. Feedstuffs 73:28–37.

Davis, A. J., and R. E. Austic. 1997. Dietary protein and amino acid levels alter threonine dehydrogenase activity in hepatic mitochondria of Gallus domesticus. J. Nutr. 127:738–744.[Abstract/Free Full Text]

Davis, A. J., and P. A. Johnson. 1998. Expression pattern of messenger ribonucleic acid for follistatin and the inhibin/ activin subunits during follicular and testicular development in Gallus domesticus. Biol. Reprod. 59:271–277.[Abstract/Free Full Text]

Deschepper, K., and G. De Groote. 1995. Effect of dietary protein, essential and non-essential amino acids on the performance and carcass composition of male broiler chickens. Br. Poult. Sci. 36:229–245.[Web of Science][Medline]

Glynias, M. J., S. M. Morris Jr., D. A. Fantozzi, L. K. Winberry, D. W. Back, J. E. Fisch, and A. G. Goodridge. 1984. A cloned cDNA for duck malic enzyme detects abnormally large malic enzyme mRNAs in a strain of mice (Mod-1ⁿ) that does not express malic enzyme protein. Biochemistry 23:3454–3459.[Medline]

Goldman, M. J., D. W. Back, and A. G. Goodridge. 1985. Nutritional regulation of the synthesis and degradation of malic enzyme messenger RNA in duck liver. J. Biol. Chem. 260:4404–4408.[Abstract/Free Full Text]

Grisoni, M. L., G. Uzu, M. Labier, and P. A. Geraert. 1991. Effect of dietary lysine level on lipogenesis in broilers. Reprod. Nutr. Dev. 31:683–690.[Web of Science][Medline]

Holcombe, D. J., D. A. Roland, and R. H. Harms. 1976. The ability of hens to regulate phosphorus intake when offered diets containing different levels of phosphorus. Poult. Sci. 55:308–317.[Web of Science][Medline]

Keene, J. C., and R. E. Austic. 2001. Dietary supplements of mixtures of indispensable amino acids lacking threonine, phenylalanine or histidine increase the activity of hepatic threonine dehydrogenase, phenylalanine hydroxylase or histidase, respectively, and prevent growth depressions in chicks caused by dietary excesses of threonine, phenylalanine, or histidine. J. Nutr. Biochem. 12:274–284.[Web of Science][Medline]

Neter, J., W. Wasserman, and M. H. Kutner. 1990. Page 580 in Applied Linear Statistical Models. 3rd ed. Richard D. Irwin Inc., Boston, MA.

Pfaff, F. E. 1977. Effects of dietary protein and amino acids on carcass composition and lipogenesis in the growing chick. PhD Thesis. Cornell Univ., Ithaca, NY.

Rosebrough, R. W., J. P. McMurtry, A. D. Mitchell, and N. C. Steele. 1988. Chicken hepatic metabolism in vitro. Protein and energy relations in the broiler chicken. VI. Effect of dietary protein and energy restrictions on in vitro carbohydrate and lipid metabolism and metabolic hormone profiles. Comp. Biochem. Physiol. 90B:311–316.[Medline]

Rosebrough, R. W., J. P. McMurtry, and R. Vasilatos-Younken. 1999. Dietary fat and protein interactions in the broiler. Poult. Sci. 78:992–998.[Abstract/Free Full Text]

Rosebrough, R. W., A. D. Mitchel, and J. P. McMurtry. 1996. Dietary crude protein changes rapidly alter metabolism and plasma insulin-like growth factor I concentration in broiler chickens. J. Nutr. 126:2888–2898.[Abstract/Free Full Text]

Rosebrough, R. W., S. M. Poch, B. A. Russell, and M. P. Richards. 2002. Dietary protein regulates in vitro lipogenesis and lipogenic gene expression in broilers. Comp. Biochem. Physiol. 132A:423–431.[Medline]

Rosebrough, R. W., and N. C. Steele. 1985. Energy and protein relations in the broiler chicken. 2. Effect of varied protein and constant carbohydrate levels on body composition and lipid metabolism. Growth 49:479–489.[Web of Science][Medline]

Rosebrough, R. W., and N. C. Steele. 1990. Dietary crude protein levels and the effect of isoproterenol on in vitro lipogenesis in the chicken. J. Nutr. 120:1684–1691.[Abstract/Free Full Text]

Scott, R. L., and R. E. Austic. 1982. Effect of dietary histidine on histidine degrading enzymes in the chicken (Gallus domesticus). Nutr. Res. 2:185–192.[Web of Science]

Sklan, D., and I. Plavnik. 2002. Interactions between dietary crude protein and essential amino acid intake on performance in broilers. Br. Poult. Sci. 43:442–449.[Web of Science][Medline]

Smith, E. R., G. M. Pesti, R. I. Bakalli, G. O. Ware, and J. F. M. Menten. 1998. Further studies on the influence of genotype and dietary protein on the performance of broilers. Poult. Sci. 77:1678–1687.[Abstract/Free Full Text]

Summers, J. D., D. Spratt, and J. L. Atkinson. 1992. Broiler weight gain and carcass composition when fed diets varying in amino acid balance, dietary energy, and protein level. Poult. Sci. 71:263–273.[Web of Science][Medline]

Tanaka, K., S. Ohtani, and K. Shigeno. 1983. Effect of increasing dietary energy on hepatic lipogenesis in growing chicks. II. Increasing energy by fat protein supplementation. Poult. Sci. 62:452–458.[Web of Science][Medline]

Yeh, Y.-Y., and G. Leveille. 1969. Effect of dietary protein on hepatic lipogenesis in the growing chick. J. Nutr. 98:356–366.[Abstract/Free Full Text]

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