Browse > Article
http://dx.doi.org/10.5713/ajas.2005.1326

The Effects of Dietary Lysine Deficiency on Muscle Protein Turnover in Postweanling Pigs  

Chang, Yi-Ming (Department of Animal Science, National Taiwan University)
Wei, Hen-Wei (Department of Animal Science, National Taiwan University)
Publication Information
Asian-Australasian Journal of Animal Sciences / v.18, no.9, 2005 , pp. 1326-1335 More about this Journal
Abstract
The main purpose of this study is to investigate the effects of dietary lysine deficiency on protein turnover of porcine muscles. There were 18 LYD three-breed-crossing postweanling barrows from six litters cannulated with gastric tubes through the esophagus at approximate 10 kg of body weight and allocated into three treatment groups. When their body weights reached over 12 kg, one group was sacrificed for determining the initial protein masses of m. masseter, m. longissimus dorsi, m. adductor and m. biceps femoris from the right body side. The others received a diet containing 100% or 61.4% (calculated values) of the lysine requirement (NRC, 1998) multiplied by 1.103 for a period of 17 days. Daily feed provision was computed for each pig according to body weight at the same day. All pigs were infused a flooding dose of $^2$H$_5$-phenylalanine to determine the fractional protein synthesis rates (FSR) of the aforementioned muscles in the end. Their four muscles from the right body side were also dissected for measuring the fractional rates of protein accretion (FAR). As for protein degradation, fractional rates (FDR) were calculated by differences between synthesis and accretion. Results showed that the lysine deficiency resulted in, significantly (p<0.05), lighter body weights, smaller muscles and a slower growth rate. The protein mass, accreted by the muscles, of the deficient group was only 54% averaged of the pigs fed adequately (p<0.05). The FAR of these muscles in the deficient group was significantly lower (p<0.05) and only achieved 61.1% averaged of the control; there was no significant difference (p>0.05), nevertheless, in the amino-acid composition of muscles between two groups. The lysine deficiency reduced significantly (p<0.05) the FSR of m. longissimus dorsi but did not influence its FDR. The m. biceps femoris also presented an inhibited FSR while its FDR reduced only exhibited a very high tendency (p = 0.055) compared to the adequately-fed pigs. As for the m. masseter and m. adductor, both of the FSR and FDR were depressed significantly (p<0.05) by the lysine deficiency, and changes in the FSR were severer than those in the FDR, so that their FAR were significantly slower (p<0.05) in comparison with the control group. The lysine deficiency also inhibited the RNA translation activity of the muscles while the effects on RNA capacity were not significant (p>0.05). In conclusion, the FAR of muscle protein was changed by the current lysine deficiency through the alterations in the FSR and/or FDR.
Keywords
Lysine Deficiency; Muscle Protein Turnover; Fractional Accretion Rate; Fractional Synthesis Rate; Fractional Degradation Rate; Postweanling Pig;
Citations & Related Records

Times Cited By Web Of Science : 6  (Related Records In Web of Science)
Times Cited By SCOPUS : 5
연도 인용수 순위
1 Allen, R. E., P. L. Raines and D. M. Regen. 1969. Regulatory significance of transfer RNA charging levels: I. Measurements of charging levels in livers of chow-fed rats, fasting rats, and rats fed balanced or imbalanced mixtures of amino acids. Biochim. Biophys. Acta. 190:323-336.
2 Batterham, E. S., L. M. Andersen, D. R. Baigent and E. White. 1990. Utilization of ileal digestible amino acids by growing pigs: effect of dietary lysine concentration on efficiency of lysine retention. Br. J. Nutr. 64:81-94.
3 Calder, A. G. and A. Smith. 1988. Stable isotope ratio analysis of leucine and ketoisocaproic acid in blood plasma by gas chromatography/ mass spectrometry. Use of tertiary butyldimethylsilyl derivatives. Rapid Commun. Mass Spectrom. 2:14-16.
4 Davies, A. S. 1974. A comparison of tissue development in Pietrain and Large White pigs from birth to 64 kg of live weight. Anim. Prod. 19:377-387.
5 Flaim, K. E., W. S. Liao, D. E. Peavy, J. M. Taylor and L. S. Jefferson. 1982. The role of amino acids in the regulation of protein synthesis in perfused rat liver: II. Effects of amino acid deficiency on peptide chain initiation, polysomal aggregation, and distribution of albumin mRNA. J. Biol. Chem. 257:2939-2946.
6 Hogberg, M. G. and D. R. Zimmerman. 1979. Effects of protein nutrition in young pigs on developmental changes in the body and skeletal muscles during growth. J. Anim. Sci. 49:472-481.
7 Hunter, K. A., P. E. Ballmer, S. E. Anderson, J. Broom, P. J. Garlick and M. A. McNurlan. 1995. Acute stimulation of albumin synthesis rate with oral meal feeding in healthy subjects measured with [ring-$^2H_5$] phenylalanine. Clin. Sci. (Lond). 88:235-242.
8 Kelly, F. J. and L. S. Jefferson. 1985. Control of peptide-chain initiation in rat skeletal muscle: Development of methods for preparation of native ribosomal subunits and analysis of the effect of insulin on formation of 40 S initiation complexes. J. Biol. Chem. 260:6677-6683.
9 McNurlan, M. A., P. Essen, A. Thorell and A. G. Calder. 1994. Response of protein synthesis in human skeletal muscle to insulin: an investigation with L-[$^2H_5$]phenylalanine. Am. J. Physiol. 267:E102-E108.
10 Mulvaney, D. R., R. A. Merkel and W. G. Bergen. 1985. Skeletal muscle protein turnover in young male pigs. J. Nutr. 115:1057-1064.
11 Ponter, A. A., N. O. Cortamira, B. Seve, D. N. Salter and L. M. Morgan. 1994. The effects of energy source and tryptophan on the rate of protein synthesis and on hormones of the enteroinsular axis in the piglet. Br. J. Nutr. 71:661-674.
12 Pronczuk, A. W., Q. R. Rogers and H. N. Munro. 1970. Liver polysome patterns of rats fed amino acid imbalanced diets. J. Nutr. 100:1249-1258.
13 Simon, O., R. Münchmeyer and H. Bergner. 1978. Estimation of rate of protein synthesis by constant infusion of labeled amino acids in pigs. Br. J. Nutr. 40:243-251.
14 Tawa, N. E., Jr., I. C. Kettelhut and A. L. Goldberg. 1992. Dietary protein deficiency reduces lysosomal and nonlysosomal ATPdependent proteolysis in muscle. Am. J. Physiol. 263:E326-E334.
15 Van den Hemel-Grootn, H. N. A., M. Koohmaraie, J. T. Yen, J. R. Arbona, J. A. Rathmacher, S. L. Nissen, M. L. Fiorotto, G. J. Garssen and M. W. A. Verstegen. 1995. Comparison between 3-methylhistidine production and proteinase activity as measures of skeletal muscle breakdown in protein-deficient growing barrows. J. Anim. Sci. 73:2272-2281.
16 Wing, S. S. and A. L. Goldberg. 1993. Glucocorticoids activate the ATP-ubiquitin-dependent proteolytic system in skeletal muscle during fasting. Am. J. Physiol. 264:E668-E676.
17 Willian, A. P. 1994. Recent developments in amino acid analysis. In: Amino acids in farm animal nutrition (Ed. J. P. F. D’Mello). CAB International, Oxon, UK. pp. 11-36.
18 Tesseraud, S., N. Maaa, R. Peresson and A. M. Chagneau. 1996a. Relative responses of protein turnover in three different skeletal muscles to dietary lysine deficiency in chicks. Br. Poult. Sci. 37:641-650.
19 Fuller, M. F., P. J. Reeds, A. Cadenhead, B. Seve and T. Preston. 1987. Effects of the amount and quality of dietary protein on nitrogen metabolism and protein turnover of pigs. Br. J. Nutr. 58:287-300.
20 Salter, D. N., A. I. Montgomery, A. Hudson, D. B. Quelch and R. J. Elliott. 1990. Lysine requirements and whole-body protein turnover in growing pigs. Br. J. Nutr. 63:503-513.
21 Campbell, I. M. 1974. Incorporation and dilution values their calculation in mass spectrally assayed stable isotope labeling experiments. Bioorg. Chem. 3:386-397.   DOI
22 Lobley, G. E. 1997. Nutritional and hormonal control of peripheral tissue metabolism in farm species. Livestock Prod. Sci. 56:91-114.   DOI   ScienceOn
23 Kimball, S. R., R. L. Horetsky and L. S. Jefferson. 1998. Implication of eIF2B rather than eIF4E in the regulation of global protein synthesis by amino acids in L6 myoblasts. J. Biol. Chem. 273:30945-30953.
24 Lee, D. N., Y. H. Cheng, Y. S. Chung, J. L. Shive, Y. M. Lian, H. W. Wei and C. F. Weng. 2004. Effects of dietary taurine supplementation on the growth performance, serum constituents and antibody production of broilers. Asian-Aust. J. Anim. Sci. 17:109-115.
25 Lowry, O. H., N. J. Rosebrough, A. L. Farr and R. J. Randall. 1951. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193:265-275.
26 McNurlan, M. A. and P. J. Garlick. 1981. Protein synthesis in liver and small intestine in protein deprivation and diabetes. Am. J. Physiol. 241:E238-E245.
27 Hara, K., K. Yonezawa, M. T. Kozlowski, T. Sugimoto, K. Andrabi, Q. P. Weng, M. Kasuga, I. Nishimoto and J. Avruch. 1997. Regulation of eIF-4E BP1 phosphorylation by mTOR. J. Biol. Chem. 272:26457-26463.
28 Millward, D. V., P. J. Garlick, R. J. C. Stewart, D. O. Nnanyelugo and J. C. Waterlow. 1975. Skeletal-muscle growth and protein turnover. Biochem. J. 150:235-243.
29 Rathmacher, J. A. 2000. Measurement and significance of protein turnover. In: Farm Animal Metabolism and Nutrition. (Ed. J. P. F. D’Mello). CAB International, Oxon, UK. pp. 25-47.
30 Sugden, P. H. and S. J. Fuller. 1991. Regulation of protein turnover in skeletal and cardiac muscle. Biochem. J. 273:21-37.
31 National Research Council. 1988. Nutrient Requirements of Swine, 9th Ed., National Academy Press, Washington, DC.
32 Garlick, P. J., D. J. Millward and W. P. James. 1973. The diurnal response of muscle and liver protein synthesis in vivo in mealfed rats. Biochem. J. 136:935-945.
33 Barrett, E. J. and R. A. Gelfand. 1989. The in vivo study of cardiac and skeletal muscle protein turnover. Diabetes Metab. Rev. 5:133-148.
34 Cortamira, N. O., B. Seve, Y. Lebreton and P. Ganier. 1991. Effect of dietary tryptophan on muscle, liver and whole-body protein synthesis in weaned piglets: relationship to plasma insulin. Br. J. Nutr. 66:423-435.
35 Calder, A. G., S. E. Anderson, I. Grant, M. A. McNurlan and P. J. Garlick. 1992. The Determination of low d5-phenylalanine enrichment (0.002-0.09 atom percent excess), after conversion to phenylethylamine, in relation to protein turnover studies by gas chromatography/electron ionization mass spectrometry. Rapid Commun. Mass Spectrom. 6:421-424.
36 Gietzen, D. W., L. F. Erecius and Q. R. Rogers. 1998. Neurochemical changes after imbalanced diets suggest a brain circuit mediating anorectic responses to amino acid deficiency in rats. J. Nutr. 128:771-781.
37 Shenoy, S. T. and Q. R. Rogers. 1977. Effect of starvation on the charging levels of transfer ribonucleic acid and total acceptor capacity in rat liver. Biochim. Biophys. Acta. 476:218-227.
38 SAS Institute Inc. 1990. SAS/STAT User’s Guide: Version 6. 4th edn. SAS Institute, Inc., Cary, North Carolina.
39 Garlick, P. J., J. Wernerman, M. A. McNurlan, P. Essen, G. E. Lobley, E. Milne, A. G. Calder and E. Vinnars. 1989. Measurement of the rate of protein synthesis in muscle of postabsorptive young men by injection of a 'flooding dose' of [1-$^{13}C$]leucine. Clin. Sci. (Lond). 77:329-336.
40 Preedy, V. R. and P. J. Garlick. 1986. The response of muscle protein synthesis to nutrient intake in postabsorptive rats: the role of insulin and amino acids. Biosci. Rep. 6:177-183.
41 De Lange, C. F. M., S. H. Birkett and P. C. H. Morel. 2001. Protein, fat and bone tissue growth in swine. In: Swine Nutrition. 2nd Ed. (Ed. A. J. Lewis and L. L. Southern). CRC Press, Florida, USA. pp. 65-81.
42 AOAC. 1984. Offical Methods of Analysis. 14th edn. Association of Official Analytical Chemists, Arlington, Virginia, USA.
43 Ip, C. C. and A. E. Harper. 1974. Liver polysome profiles and protein synthesis in rats fed a threonine-imbalanced diet. J. Nutr. 104:252-263.
44 National Research Council. 1998. Nutrient Requirements of Swine 10th Ed. National Academy Press, Washington, DC.
45 Remignon, H., L. Lefaucheur, J. C. Blum and F. H. Ricard. 1994. Effects of divergent selection for body weight on three skeletal muscles characteristics in the chicken. Br. Poult. Sci. 35:65-76.
46 Mahan, D. C., R. A. Eater, G. L. Cromwell, E. R. Miller and T. L. Veum. 1993. Effect of dietary lysine levels formulated by altering the ratio of corn:soybean meal with or without dried whey and L-lysine.HCl in diets for weanling pigs. NCR-42 Committee on Swine Nutrition. J. Anim. Sci. 71:1848-52.
47 Munro, H. N. and A. Fleck. 1969. Analysis of tissue and body fluids for nitrogenous constituents. In: Mammalian Protein Metabolism (Ed. H. N. Munro). Academic Press, New York, USA. pp. 424-525.
48 Smriga, M., H. Murakami, M. Mori and K. Torii. 2000. Effects of L-lysine deficient diet on the hypothalamic interstitial norepinephrine and diet-induced thermogenesis in rats in vivo. Biofactors 12:137-142.
49 Tesseraud, S., R. Peresson, J. Lopes and A. M. Chagneau. 1996b. Dietary lysine deficiency greatly affects muscle and liver protein turnover in growing chickens. Br. J. Nutr. 75:853-856.
50 Steel, R. D. G. and J. H. Torrie. 1980. Principles and Procedures of Statistics: A Biometrical Approach. 2nd edn. McGraw-Hill Book Company, New York, New York.
51 Wykes, L. J., M. Fiorotto, D. G. Burrin, M. D. Rosario, M. E. Frazer, W. G. Pond and F. Jahoor. 1996. Chronic low protein intake reduces tissue protein synthesis in a pig model of protein malnutrition. J. Nutr. 126:1481-1488.
52 Chung, T. K. and D. H. Baker. 1992. Efficiency of dietary methionine utilization by young pigs. J. Nutr. 122:1862-1869.
53 Hamilton, C. R. and T. L. Veum. 1986. Effect of biotin and (or) lysine additions to corn-soybean meal diets on the performance and nutrient balance of growing pigs. J. Anim. Sci. 62:155-162.
54 Laborde, D., A. Talmant and G. Monin. 1985. Activities enzymatiques metaboliques et contractiles de 30 muscles du porc: Relations avec le pH ultime atteint apres la mort (Enzyme metabolic and contractile activity in 30 pig muscles and their relationship to ultimate postmortem pH.). Reprod. Nutr. Develop. 25:619-628.
55 Lewis, S. E. M., F. J. Kelly and D. F. Goldspink. 1984. Pre- and post- natal growth and protein turnover in smooth muscle, heart and slow- and fast- twitch skeletal muscles of the rat. Biochem. J. 217:517-526.
56 Reeds, P. J., D. G. Burrin, T. A. Davis, M. A. Fiorotto, H. J. Mersmann and W. G. Pond. 1993. Growth regulation with particular reference to the pig. In: Growth of the Pig. (Ed. G. R. Hollos). CAB International, Oxon, UK. pp. 1-32.
57 McNurlan, M. A., A. M. Tomkins and P. J. Garlick. 1979. The effect of starvation on the rate of protein synthesis in rat liver and small intestine. Biochem. J. 178:373-379.
58 Wei, H. W. 1999. Effect of Long-term Amino-acid Deficiency on the Amino-acid Composition of the Body. Ph.D. Thesis, University of Aberdeen, Aberdeen, Scotland, UK.