Hostname: page-component-586b7cd67f-2brh9 Total loading time: 0 Render date: 2024-11-26T02:12:06.577Z Has data issue: false hasContentIssue false
  • English
  • Français

Whole body insulin responsiveness is higher in beef steers selected for increased muscling

Published online by Cambridge University Press:  06 April 2011

P. McGilchrist ,
D. W. Pethick ,
S. P. F. Bonny ,
P. L. Greenwood  and
G. E. Gardner
P. McGilchrist*
Affiliation:
Australian Cooperative Research Centre for Beef Genetic Technologies, Armidale, NSW, Australia Department of Health Sciences, School of Veterinary & Biomedical Science, Murdoch University, Murdoch, WA 6150, Australia
D. W. Pethick
Affiliation:
Australian Cooperative Research Centre for Beef Genetic Technologies, Armidale, NSW, Australia Department of Health Sciences, School of Veterinary & Biomedical Science, Murdoch University, Murdoch, WA 6150, Australia
S. P. F. Bonny
Affiliation:
Department of Health Sciences, School of Veterinary & Biomedical Science, Murdoch University, Murdoch, WA 6150, Australia
P. L. Greenwood
Affiliation:
Australian Cooperative Research Centre for Beef Genetic Technologies, Armidale, NSW, Australia Industry & Investment NSW, Beef Industry Centre of Excellence, Armidale, NSW 2351, Australia
G. E. Gardner
Affiliation:
Australian Cooperative Research Centre for Beef Genetic Technologies, Armidale, NSW, Australia Department of Health Sciences, School of Veterinary & Biomedical Science, Murdoch University, Murdoch, WA 6150, Australia
*
†E-mail: [email protected]
Get access

Abstract

The aim of this experiment was to evaluate the impact of selection for greater muscling on whole body insulin responsiveness in cattle, as reflected by greater uptake of glucose in response to constant insulin infusion and greater glucose disappearance following an intravenous glucose tolerance test. This study used 18-month-old steers from an Angus herd visually assessed and selected for divergence in muscling over 15 years. Eleven high-muscled (High), 10 low-muscled (Low) and 3 high-muscled steers, which were heterozygous for a myostatin polymorphism (HighHet), were infused with insulin using the hyperinsulineamic-euglyceamic clamp technique. Insulin was constantly infused at two levels, 0.6 μIU/kg per min and 6.0 μIU/kg per min. Glucose was concurrently infused to maintain euglyceamia and the steady state glucose infusion rate (SSGIR) indicated insulin responsiveness. An intravenous glucose tolerance test was also administered at 200 mg/kg live weight. Sixteen blood samples were collected from each animal between −30 and 130 min relative to the administration of intravenous glucose, plasma glucose and insulin concentration was determined in order to analyse insulin secretion and glucose disappearance. Insulin-like growth factor-1 (IGF-1) was also measured in basal plasma samples. At the low insulin infusion rate of 0.6 mU/kg per min, the SSGIR was 73% higher for the High muscling genotype animals when compared to the Low (P < 0.05). At the high insulin infusion rate of 6.0 mU/kg per min, these differences were proportionately less with the High and the HighHet genotypes having only 27% and 34% higher SSGIR (P < 0.05) than the Low-muscled genotype. The High-muscled cattle also had 30% higher plasma IGF-1 concentrations compared to the Low-muscled cattle. There was no effect of muscling genotype on basal insulin or basal glucose concentrations, glucose disappearance or insulin secretion following an intravenous glucose tolerance test. The increased whole body insulin responsiveness in combination with higher IGF-1 concentrations in the High-muscled steers is likely to initiate a greater level of protein synthesis, which may partially explain the increased muscle accretion in these animals.

Keywords

muscling genotypeglucose disappearanceinsulin responsivenessbeef yieldhyperinsulinaemic-euglycaemic clamp
Type
Full Paper
Information
animal , Volume 5 , Issue 10 , 26 August 2011 , pp. 1579 - 1586
Copyright
Copyright © The Animal Consortium 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ballard, FJ, Read, LC, Francis, GL, Bagley, CJ, Wallace, JC 1986. Binding properties and biological potencies of insulin-like growth factors in L6 myoblasts. Biochemical Journal 233, 223–230.Google Scholar
Bassett, JM, Wallace, ALC 1966. Diluents for insulin standards in immunoassay of insulin in undiluted ovine plasma by a double antibody technique. Journal of Endocrinology 36, 99–100.Google Scholar
Bergman, EN, Reulein, SS, Corlett, RE 1989. Effects of obesity on insulin sensitivity and responsiveness in sheep. American Journal of Physiology (Endocrinology & Metabolism) 257, E772–E781.Google Scholar
Breier, BH, Gallaher, BW, Gluckman, PD 1991. Radioimmunoassay for insulin-like growth factor-I: solutions to some potential problems and pitfalls. Journal of Endocrinology 128, 347–357.Google Scholar
DeFronzo, RA, Tobin, JD, Andres, R 1979. Glucose clamp technique: a method for quantifying insulin secretion and resistance. American Journal of Physiology (Endocrinology, Metabolism and Gastrointestinal Physiology) 237, E214–E223.Google Scholar
Elliot, M, Gahan, R, Sundstrom, B 1987. Assessing cattle for muscle. In Agfact A2.3.27 (ed. R Gaden), pp. 1–5. NSW Department of Agriculture, Orange, NSW, Australia.Google Scholar
Etherton, TD 1982. The role of insulin-receptor in interactions in regulation of nutrient utilization by skeletal muscle and adipose tissue; a review. Journal of Animal Science 54, 58–67.Google Scholar
Francis, SM, Bickerstaffe, R 1996. The insulin status of sheep with genetic differences in glucose clearance. Domestic Animal Endocrinology 13, 171–184.CrossRefGoogle ScholarPubMed
Goodyear, LJ, Hirshman, MF, Smith, RJ, Horton, ES 1991. Glucose transporter number, activity, and isoform content in plasma membranes of red and white skeletal muscle. American Journal of Physiology, Endocrinology and Metabolism 261, E556–E561.CrossRefGoogle ScholarPubMed
Greenwood, PL, Cafe, LM, O'Rourke, BA, McKiernan, WA 2006. Myofibre characteristics in M. semitendinosus of steers from Angus muscling selection lines with normal and mutant myostatin alleles. Proceeding of Australian Society of Animal Production 26th Biennial Conference, Short communication, Perth, WA, Australia, 15pp.Google Scholar
Gregory, NG, Christopherson, RJ, Lister, D 1986. Adipose tissue capillary blood flow in relation to fatness in sheep. Research in Veterinary Science 40, 352–356.CrossRefGoogle ScholarPubMed
Hales, CN, Randle, PJ 1963. Immunoassay of insulin with insulin-antibody precipitate. Biochemical Journal 88, 137–146.CrossRefGoogle ScholarPubMed
Henriksen, EJ, Bourey, RE, Rodnick, KJ, Koranyi, L, Permutt, MA, Holloszy, JO 1990. Glucose transporter protein content and glucose transport capacity in rat skeletal muscles. American Journal of Physiology, Endocrinology and Metabolism 259, E593–E598.Google Scholar
Hocquette, JF, Bornes, F, Balage, M, Ferre, P, Grizard, J, Vermorel, M 1995. Glucose-transporter (GLUT4) protein content in oxidative and glycolytic skeletal muscles from calf and goat. Biochemistry Journal 305, 465–470.CrossRefGoogle ScholarPubMed
James, DE, Strube, M, Muecdler, M 1989. Molecular cloning and characterization of an insulin-regulatable glucose transporter. Nature 338, 83–87.CrossRefGoogle ScholarPubMed
Kraegen, EW, James, DE, Jenkins, AB, Chisholm, DJ 1985. Dose-responsive curves for in vivo insulin sensitivity in individual tissues in rats. American Journal of Physiology, Endocrinology and Metabolism 248, E353–E362.CrossRefGoogle Scholar
Kunst, A, Draeger, B, Ziegenhorn, J 1984. Colorimetric methods with glucose oxidase and peroxidase. In Methods of enzymatic analysis (ed. HU Bergmeyer), pp. 163–172. Verlag Chemie Academic Press, Inc., Weinheim, Basel, Switzerland.Google Scholar
Lillioja, S, Young, AA, Culter, CL, Ivy, JL, Abbott, WG, Zawadzki, JK, Yki, JH, Christin, L, Secomb, TW, Bogardus, C 1987. Skeletal muscle capillary density and fiber type are possible determinants of in vivo insulin resistance in man. Journal of Clinical Investigation 80, 415–424.CrossRefGoogle ScholarPubMed
Marette, A, Richardson, JM, Ramlal, T, Balon, TW, Vranic, M, Pessin, JE, Klip, A 1992. Abundance, localization, and insulin-induced translocation of glucose transporters in red and white muscle. American Journal of Physiology. Cell Physiology 263, C443–C452.Google Scholar
McCann, JP, Reimers, TJ 1985. Glucose response to exogenous insulin and kinetics of insulin metabolism in obese and lean heifers. Journal of Animal Science 61, 612–618.CrossRefGoogle ScholarPubMed
McGilchrist, P, Pethick, DW, Bonny, SPF, Greenwood, PL, Gardner, GE 2011. Beef cattle selected for increased muscularity have a reduced muscle response and increased adipose tissue response to adrenaline. Animal. Available on CJO 2010. doi:10.1017/S1751731110002508. FirstView, 1–10.Google Scholar
McKiernan, WA 1990. New developments in live animal appraisal of meat quantity in beef cattle. 8th Proceedings of the Australian Association of Animal Breeding and Genetics, Hamilton, New Zealand, 447–450pp.Google Scholar
McKiernan, WA 2001. Breeding for divergence in muscling. Proceedings of Beef Products Conference, Orange, NSW, Australia, 42–45pp.Google Scholar
Nolan, JJ, Ludvik, B, Beerdsen, P, Joyce, M, Olefsky, J 1994. Improvement in glucose tolerance and insulin resistance in obese subjects treated with troglitazone. New England Journal of Medicine 331, 1188–1193.Google Scholar
O'Rourke, BA, Dennis, JA, Healy, PJ, McKiernan, WA, Greenwood, PL, Cafe, LM, Perry, D, Walker, KH, Marsh, I, Parnell, PF, Arthur, PF 2009. Quantitative analysis of performance, carcass and meat quality traits in cattle from two Australian beef herds in which a null myostatin allele is segregating. Animal Production Science 49, 297–305.Google Scholar
Perry, D, Yeates, AP, McKiernan, WA 1993. Meat yield and subjective muscle scores in medium weight steers. Australian Journal of Experimental Agriculture 33, 825–831.CrossRefGoogle Scholar
Perry, D, Shorthose, WR, Ferguson, DM, Thompson, JM 2001. Methods used in the CRC program for the determination of carcass yield and beef quality. Australian Journal of Experimental Agriculture 41, 953–957.Google Scholar
Prior, RL, Smith, SB 1982. Hormonal effects on partitioning of nutrients for tissue growth: role of insulin. Federation Proceedings 40, 2545–2549.Google Scholar
Proud, CG 2006. Regulation of protein synthesis by insulin. Biochemical Society Transactions 34, 213–216.CrossRefGoogle ScholarPubMed
Roeder, RA, Hossner, KL, Sasser, RG, Gunn, JM 1988. Regulation of protein turnover by recombinant human insulin-like growth factor-I in L6 myotube cultures. Hormone Metabolism Research 20, 698–700.Google Scholar
Russell-Jones, DL, Umpleby, AM, Hennessy, TRea 1994. Use of a leucine clamp to demonstrate that IGF-I actively stimulates protein synthesis in normal humans. American Journal of Physiology 267, E591–E598.Google ScholarPubMed
Salans, LB, Knittle, JL, Hirsch, J 1968. The role of adipose cell size and adipose tissue insulin sensitivity in the carbohydrate intolerance of human obesity. The Journal of Clinical Investigation 47, 153–165.CrossRefGoogle ScholarPubMed
SAS 2001. Statistical analysis system. SAS Institute Incorporated, Cary, North Carolina, USA.Google Scholar
Tindal, JS, Knaggs, GS, Hart, IC, Blake, LA 1978. Release of growth hormone in lactating and non-lactating goats in relation to behaviour, stages of sleep, electroencephalographs, environmental stimuli and levels of prolactin, insulin, glucose and free fatty acids in the circulation. Journal of Endocrinology 76, 333–346.CrossRefGoogle Scholar
Umpleby, AM, Russell-Jones, DL 1996. The hormonal control of protein metabolism. Baillière's Clinical Endocrinology and Metabolism 10, 551–570.CrossRefGoogle ScholarPubMed
Vasconcelos, JT, Sawyer, JE, Tedeschi, LO, McCollum, FT, Greene, LW 2009. Effects of different growing diets on performance, carcass characteristics, insulin sensitivity, and accretion of intramuscular and subcutaneous adipose tissue of feedlot cattle. Journal of Animal Science 87, 1540–1547.Google Scholar
Weekes, TEC 1991. Hormonal control of glucose metabolism. In Proceedings of 7th International Symposium on Ruminant Physiology (ed. T Tsuda, Y Sasaki and R Kawashima), pp. 183. Academic Press, San Diego, CA, USA.Google Scholar
Wegner, J, Albrecht, E, Fiedler, I, Teuscher, F, Papstein, HJ, Ender, K 2000. Growth- and breed-related changes of muscle fiber characteristics in cattle. Journal of Animal Science 78, 1485–1496.CrossRefGoogle ScholarPubMed
Ziel, FH, Venkatesan, N, Davidson, MB 1988. Glucose transport is rate limiting for skeletal muscle glucose metabolism in normal and STZ-induced diabetic rats. Diabetes 37, 885–890.CrossRefGoogle ScholarPubMed
Zierler, K 1999. Whole body glucose metabolism. American Journal of Physiology, Endocrinology and Metabolism 276, E409–E426.Google Scholar