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Nutritional Regulation of GLUT Expression, Glucose Metabolism, and Intramuscular Fat Content in Porcine Muscle

  • Katsumata, M. (National Institute of Livestock and Grassland Sciences) ;
  • Kaji, Y. (National Agricultural Research Center for Kyushu Okinawa Region) ;
  • Takada, R. (National Institute of Livestock and Grassland Sciences) ;
  • Dauncey, M.J. (Wolfson College, University of Cambridge)
  • Published : 2007.08.01

Abstract

We conducted a series of investigations in order to elucidate role of nutritional status in regulating GLUT expression and energy metabolism in porcine muscle. Firstly, the role of mild undernutrition in regulating muscle GLUT gene expression and function was studied in growing pigs (3 wk of age) on a high (H) or low (L) food intake (H = 2L) at $35^{\circ}C$ or $26^{\circ}C$. Low food intake selectively upregulates GLUT1 and GLUT4 gene expression; mRNA levels were elevated in longissimus dorsi (L. dorsi) and rhomboideus muscles but not in diaphragm or cardiac muscles. Our next step was to determine whether dietary lysine, a major primary limiting amino acid in diets for pigs, affects muscle GLUT4 expression. Pigs of 6 wk of age were pair-fed a control or low lysine (LL) diet. The control diet contained optimal amounts of all essential amino acids, including 1.15% lysine. The LL diet was similar but contained only 0.70% lysine. GLUT4 mRNA expression was upregulated by the LL diet in L. dorsi and rhomboideus muscles, whereas that in cardiac muscle was unaffected. GLUT4 protein abundance was also higher in rhomboideus muscle of animals on the LL diet. We conducted another investigation in order to elucidate effects of the LL diet on post-GLUT4 glucose metabolism. Activity of hexokinase was unaffected by dietary lysine levels while that of citrate synthase was higher both in L. dorsi and rhomboideus muscles of pigs fed on the LL diet. Glucose 6-phosphate content was higher in L. dorsi msucle in the LL group. Glycogen content was higher both in L. dorsi and rhomboideus muscles in the LL group. Further, we determined the effects of dietary lysine levels on accumulation of intramuscular fat (IMF) in L. dorsi muscle of finishing pigs. A low lysine diet (lysine content was 0.40%) meeting approximately 70% of the requirement of lysine was given to finishing pigs for two months. IMF contents in L. dorsi of the pigs given the low lysine diet were twice higher than those of the pigs fed on a control diet (lysine content was 0.65%). Finally, we proved that a well known effect of breadcrumbs feeding to enhance IMF of finishing pigs could be attributed to shortage of amino acids in diets including breadcrumbs.

Keywords

References

  1. Charon, M. J. and B. B. Kahn. 1990. Divergent molecular mechanisms for insulin-resistant glucose transport in muscle and adipose cells in vivo. J. Biol. Chem. 265:7994-8000.
  2. Crace, C. J., P. G. Kohn, A. J. Strain and I. Swenne. 1990. Protein-energy malnutrition induces changes in insulin sensitivity. Diabete Metab. 16:484-491.
  3. Ellis, M. and F. McKeith. 1999. Nutritional influences on pork quality. In: Pork Fact Sheets, pp. 1-8. Am. Meat Sci. Assoc. Savoy, IL.
  4. Goodband, R. D., J. L. Nelssen, R. H. Hines, D. H. Kropf, R. C. Thaler, B. R. Schricker, G. E. Fitzner and A. J. Lewis. 1990. The effects of porcine somatotropin and dietary lysine on growth performance and carcass characteristics of finishing swine. J. Anim. Sci. 68:3261-3276. https://doi.org/10.2527/1990.68103261x
  5. Henriksen, E. J., R. E. Bourey, K. J. Rodnick, L. Koranyi, M. A. Permutt and J. O. Holloszy. 1990. Glucose transporter protein content and glucose transport activity in rat skelet al., muscles. Am. J. Physiol. 259:E593-E598.
  6. Ieiri, S., T. Sakimura, M. Ishibashi, M. Katsumata and Y. Kaji. 2007. Enhancement of intramuscular fat content in Longissimus Dorsi muscle of finishing pigs fed a low lysine diet including bread crumbs. Jpn. J. Swine Sci. 44:8-16. https://doi.org/10.5938/youton.44.8
  7. Katsumata, M., K. A. Burton, J. Li and M. J. Dauncey. 1999. Suboptimal energy balance selectively up-regulates muscle GLUT gene expression but reduces insulin-dependent glucose uptake during postnatal development. FASEB J. 13:1405-1413. https://doi.org/10.1096/fasebj.13.11.1405
  8. Katsumata, M., S. Kawakami, Y. Kaji, R. Takada and M. J. Dauncey. 2001. Low lysine diet selectively up-regulates muscle GLUT4 gene and protein expression during postnatal development. Energy metabolism in animals. EAAP publication No. 103:237-239.
  9. Katsumata, M., S. Kawakami, Y. Kaji, R. Takada and M. J. Dauncey. 2002. Differential regulation of porcine hepatic IGFI mRNA expression and plasma IGF-I concentration by a low lysine diet. J. Nutr. 132:688-692. https://doi.org/10.1093/jn/132.4.688
  10. Katsumata, M., S. Kawakami, Y. Kaji and R. Takada. 2004. Circulating levels of insulin-like growth factor-1 and associated binding proteins in plasma and mRNA expression in tissues of growing pigs on a low threonine diet. Anim. Sci. 79:85-92.
  11. Katsumata, M., S. Kobayashi, M. Matsumoto, E. Tsuneishi and Y. Kaji. 2005. Reduced intake of dietary lysine promotes accumulation of intramuscular fat in the Longissimus dorsi muscles of finishing gilts. Anim. Sci. J. 76:237-244. https://doi.org/10.1111/j.1740-0929.2005.00261.x
  12. Kim, Y., T. Tamura, S. Iwashita, K. Tokuyama and M. Suzuki. 1994. Effect of high-fat diet on gene expression of GLUT4 and insulin receptor in soleus muscle. Biochem. Biophys. Res. Commun. 202:519-526. https://doi.org/10.1006/bbrc.1994.1959
  13. Lohrke, B., E. Saggau, R. Schadereit, J. Voigt, M. Beyer, O. Bellmann, S. Kuhla and H. Hagemeister. 2001. Up-regulation of the skelet al., muscle system A for neutral amino acid transport in soy protein-fed pigs in comparison with casein diet. Energy metabolism in animals. EAAP publication No.103:249-252.
  14. Neufer, P. D., J. O. Carey and G. L. Dohm. 1993. Transcriptional regulation of the gene for glucose transporter GLUT4 in skelet al., muscle. Effects of diabetes and fasting. J. Biol. Chem. 268:13824-13829.
  15. Nikami, H., Y. Shimizu, D. Endoh, H. Yano and M. Saito. 1992. Cold exposure increases glucose utilization and glucose transporter expression in brown adipose tissue. Biochem. Biophys. Res. Commun. 185:1078-1082. https://doi.org/10.1016/0006-291X(92)91736-A
  16. Ozanne, S. E., C. L. Wang, N. Coleman and G. D. Smith. 1996. Altered muscle insulin sensitivity in the male offspring of protein-malnourished rats. Am. J. Physiol. 271:E1128-E1134.
  17. Reis, M. A. B., E. M. Carneiro, M. A. R. Mello, A. C. Boschero, M. J. A. Saad and L. A. Velloso. 1997. Glucose-induced insulin secretion is impaired and insulin-dependent phosphorylation of the insulin receptor and insulin receptor substrate-1 are increased in protein-deficient rats. J. Nutr. 127:403-410. https://doi.org/10.1093/jn/127.3.403
  18. Weinstein, S. P., E. O'Boyle and R. S. Haber. 1994. Thyroid hormone increases basal and insulin-stimulated glucose transport in skelet al., muscle. The role of GLUT4 glucose transporter expression. Diabetes 43:1185-1189. https://doi.org/10.2337/diabetes.43.10.1185

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