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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

Published online by Cambridge University Press:  18 August 2016

M. Katsumata ,
S. Kawakami ,
Y. Kaji  and
R. Takada§
M. Katsumata*
Affiliation:
Department of Animal and Grassland Research, National Agricultural Research Centre for Kyushu Okinawa Region, Kumamoto, 861-1192, Japan
S. Kawakami
Affiliation:
Department of Animal and Grassland Research, National Agricultural Research Centre for Kyushu Okinawa Region, Kumamoto, 861-1192, Japan
Y. Kaji
Affiliation:
Department of Animal and Grassland Research, National Agricultural Research Centre for Kyushu Okinawa Region, Kumamoto, 861-1192, Japan
R. Takada§
Affiliation:
Department of Animal and Grassland Research, National Agricultural Research Centre for Kyushu Okinawa Region, Kumamoto, 861-1192, Japan
*
†E-mail:masaya@affrc.go.jp
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Abstract

The aim was to determine whether dietary threonine levels affected hepatic insulin-like growth factor-1 (IGF-1) mRNA expression as well as plasma IGF-1 concentration and IGF binding protein (IGFBP) profile in growing pigs. Two male 6-week-old pigs from each of seven litters were used. Each littermate was assigned to one of two diets, control or low threonine (LT), providing per kg 14·3 MJ digestible energy in both diets, 170 g protein in the control diet and 167 g protein in the LT diet. The control diet contained all essential amino acids in the recommended amounts, including 8·2 g threonine per kg. The LT diet was similar but contained only 5·1 g threonine per kg. Pigs were pair-fed these diets for 3 weeks. Growth rate and food efficiency of pigs given the LT diet were significantly lower than those of pigs given the control diet (P 0·001). Plasma IGF-1 concentration of pigs given the LT diet was proportionately 0·44 lower than that of pigs given the control diet (P 0·01). Plasma free threonine concentration of pigs given the LT diet was lower than that of the pigs given the control diet (P 0·001). Plasma IGFBP2 level of pigs given the LT diet was significantly higher than that of pigs given the control diet (P 0·05). Pigs given the LT diet had a significantly lower plasma IGFBP3 level compared with their littermates given the control diet (P 0·05) suggesting that clearance rate of circulating IGF-1 was higher in the LT group. Dietary threonine level did not affect IGF-1 mRNA abundance in the liver. It is concluded that lower plasma IGF-1 level caused by reduced dietary threonine level may have been partly due to increased clearance rate of circulating IGF-1 but not due to IGF-1 gene expression in the liver.

Keywords

insulin-like growth factorpigsthreonine
Type
Growth, development and meat science
Information
Animal Science , Volume 79 , Issue 1 , August 2004 , pp. 85 - 92
Copyright
Copyright © British Society of Animal Science 2004

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References

Brameld, J. M., Gilmour, R. S. and Buttery, P. J. 1999. Glucose and amino acids interact with hormones to control expression of insulin-like growth factor-I and growth hormone receptor mRNA in cultured pig hepatocytes. Journal of Nutrition 129: 1298–1306.Google Scholar
Carew, L. B., McMurty, J. P. and Alster, F. A. 2003. Effects of methionine deficiency on plasma levels of thyroid hormones, insulin-like growth factor-I and –II, liver and body weights, and feed intake in growing chickens. Poultry Science 82: 1932–1938.CrossRefGoogle ScholarPubMed
Cheng, C. M., Reinhardt, R. R., Lee, W. -H., Joncas, G., Patel, S. C. and Bondy, C. A. 2000. Insulin-like growth factor 1 regulates developing brain glucose metabolism. Proceedings of the National Academy of Sciences of the United States of America 97: 10236–10241.CrossRefGoogle ScholarPubMed
Chomczynski, P. and Sacchi, N. 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Analytical Biochemistry 162: 156–159.Google Scholar
Dauncey, M. J., Rudd, B. T., White, D. A. and Shakespear, R. A. 1993. Regulation of insulin-like growth factor binding proteins in young growing animals by alteration of energy status. Growth Regulation 3: 198–207.Google Scholar
Donovan, S. M., Atilano, L. C., Hintz, R. L., Wilson, D. M. and Rosenfeld, R. G. 1991. Differential regulation of the insulin-like growth factors (IGF-1 and –II) and IGF binding proteins during malnutrition in the neonatal rat. Endocrinology 129: 149–157.Google Scholar
Guler, H. -P., Zapf, J., Schmid, C. and Froesch, E. R. 1989. Insulin-like growth factors I and II in healthy man. Estimations of half-lives and production rates. Acta Endocrinologica 121: 753–758.Google Scholar
Hoeflich, A., Wu, M., Mohan, S., Föll, J., Wanke, R., Froehlich, T., Arnold, G. J., Lahm, H., Kolb, H. J. and Wolf, E. 1999. Overexpression of insulin-like growth factorbinding protein-2 in transgenic mice reduces postnatal body weight gain. Endocrinology 140: 5488–5496.Google Scholar
Katsumata, M., Burton, K. A., Li, J. and Dauncey, M. J. 1999. Suboptimal energy balance selectively up-regulates muscle GLUT4 gene expression but reduces insulin-dependent glucose uptake during postnatal development. FASEB Journal 13: 1405–1413.Google Scholar
Katsumata, M., Cattaneo, D., White, P., Burton, K. A. and Dauncey, M. J. 2000. Growth hormone receptor gene expression in porcine skeletal muscle and cardiac muscle is selectively regulated by postnatal undernutrition. Journal of Nutrition 130: 2482–2488.Google Scholar
Katsumata, M., Kawakami, S., Kaji, Y. and Takada, R. 2003a. A low-threonine diet down-regulates circulating level of IGF-1 by altering plasma IGFBP profile without affecting hepatic IGF-1 mRNA expression. Archives of Animal Breeding 46: 170 (abstr. ).Google Scholar
Katsumata, M., Kawakami, S., Kaji, Y., Takada, R. and Dauncey, M. J. 2001. Low lysine diet selectively up-regulates muscle GLUT4 gene and protein expression during postnatal development. In Energy metabolism in animals (ed. Chwalibog, A. and Jakobsen, K.) European Association for Animal Production publication no. 103, pp. 237–240. Wageningen Pers, Wageningen.Google Scholar
Katsumata, M., Kawakami, S., Kaji, Y., Takada, R. and Dauncey, M. J. 2002. Differential regulation of porcine hepatic IGF-1 mRNA expression and plasma IGF-1 concentration by a low lysine diet. Journal of Nutrition 132: 688–692.Google Scholar
Katsumata, M., Matsumoto, M. and Kaji, Y. 2003b. Effects of a low lysine diet on glucose metabolism in skeletal muscle of growing pigs. In Progress in research on energy and protein metabolism (ed. Souffrant, W. B. and Metges, C. C.) European Association for Animal Production publication no. 109, pp. 187–190. Wageningen Academic Publishers, Wageningen.Google Scholar
Kita, K., Nagao, K., Taneda, N., Inagaki, Y., Hirano, K., Shibata, T., Yaman, M. A., Conlon, M. A. and Okumura, J. 2002. Insulin-like growth factor binding protein-2 gene expression can be regulated by diet manipulation in several tissues of young chickens. Journal of Nutrition 132: 145–151.Google Scholar
Kong, X., Manchester, J., Salmons, S. and Lawrence Jr, J. C. 1994. Glucose transporters in single skeletal muscle fibers. Relationship to hexokinase and regulation by contractile activity. Journal of Biological Chemistry 269: 12963–12967.Google Scholar
Louveau, I. and Le Dividich, J. 2002. GH and IGF-1 binding in adipose tissue, liver, and skeletal muscle in response to milk intake level in piglets. General and Comparative Endocrinology 126: 310–317.Google Scholar
Louveau, I., Quesnel, H. and Prunier, A. 2000. GH and IGF-1 binding sites in adipose tissue, liver skeletal muscle and ovaries of feed-restricted gilts. Reproduction, Nutrition, Development 40: 571–578.CrossRefGoogle ScholarPubMed
Maor, G. and Karnieli, E. 1999. The insulin-sensitive glucose transporter (GLUT4) is involved in early bone growth in control and diabetic mice, but is regulated through the insulin-like growth factor I receptor. Endocrinology 140: 1841–1851.Google Scholar
Matsumura, Y., Domeki, M., Sugahara, K., Kubo, T., Roberts Jr, C. T., Le Roith, D. and Kato, H. 1996. Nutritional regulation of insulin-like growth factor-I receptor mRNA levels in growing chickens. Bioscience, Biotechnology, and Biochemistry 60: 979–982.Google Scholar
Murphy, L. J., Bell, G. I. and Friesen, H. G. 1987. Tissue distribution of insulin-like growth factor I and II messenger ribonucleic acid in the adult rat. Endocrinology 120: 1279–1282.Google Scholar
National Research Council. 1998. Nutrient requirements of swine, 10th revised edition. National Academy Press, Washington, DC.Google Scholar
Pell, J. M. and Glassford, J. 1996. Insulin-like growth factor-I and its binding proteins: role in post-natal growth. In Molecular physiology of growth (ed. Loughna, P. T. and Pell, J. M.), pp. 13–33. Cambridge University Press, Cambridge.Google Scholar
Rawn, J. D. 1989. Biochemistry. Neil Patterson Publishers, Burlington.Google Scholar
Sohlström, A., Katsman, A., Kind, K. L., Grant, P. A., Owens, P. C., Robinson, J. S. and Owens, J. A. 1998. Effects of acute and chronic food restriction on the insulin-like growth factor axis in the guinea pig. Journal of Endocrinology 157: 107–114.Google Scholar
Statistical Analysis Systems Institute. 1988. SAS/STAT user’s guide, release 6·03 edition. SAS Institute, Cary, NC.Google Scholar
Stubbs, A. K., Wheelhouse, N. M., Lomax, M. A. and Hazlerigg, D. G. 2002. Nutrient-hormone interaction in ovine liver: methionine supply selectively modulates growth hormone-induced IGF-1 gene expression. Journal of Endocrinology 174: 335–341.Google Scholar
Takenaka, A., Oki, N., Takahashi, S. and Noguchi, T. 2000. Dietary restriction of single essential amino acids reduced plasma insulin-like growth factor-I (IGF-1) but does not affect plasma IGF-binding protein-1 in rats. Journal of Nutrition 130: 2910–2914.Google Scholar
Takenaka, A., Takahashi, S. and Noguchi, T. 1996. Effect of protein nutrition on insulin-like growth factor-I (IGF-1) receptor in various tissues of rats. Journal of Nutritional Science and Vitaminology 42: 347–357.CrossRefGoogle ScholarPubMed
Urban, R. J., Bodenburg, Y. H., Nagamani, M. and Peirce, J. 1994. Dexamethasone potentiates IGF-1 actions in porcine granulosa cells. American Journal of Physiology 267: E115–E123.Google Scholar
Valverde, A. M., Navarro, P., Teruel, T., Conejo, R., Benito, M. and Lorenzo, M. 1999. Insulin and insulin-like growth factor I up-regulate GLUT4 gene expression in fetal brown adipocytes, in a phosphoinositide 3-kinase-dependent manner. Biochemical Journal 337: 397–405.CrossRefGoogle Scholar
Weller, P. A., Dauncey, M. J., Bates, P. C., Brameld, J. M., Buttery, P. J. and Gilmour, R. S. 1994. Regulation of porcine insulin-like growth factor I and growth hormone receptor mRNA expression by energy status. American Journal of Physiology 266: E776–E785.Google Scholar
Weller, P. A., Dickson, M. C., Huskisson, N. S., Dauncey, M. J., Buttery, P. J. and Gilmour, R. S. 1993. The porcine insulin-like growth factor-I gene: characterization and expression of alternate transcription sites. Journal of Molecular Endocrinology 11: 201–211.Google Scholar