Hostname: page-component-cd9895bd7-7cvxr Total loading time: 0 Render date: 2024-12-22T17:17:53.743Z Has data issue: false hasContentIssue false
  • English
  • Français

Beef cattle selected for increased muscularity have a reduced muscle response and increased adipose tissue response to adrenaline

Published online by Cambridge University Press:  05 January 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 the adrenaline responsiveness of muscle, adipose and liver tissue, as reflected by changes in plasma levels of the intermediary metabolites lactate, non-esterified fatty acids (NEFA) and glucose. This study used 18-month-old steers from an Angus herd visually assessed and selected for divergence in muscling for over 15 years. Ten low muscled (Low), 11 high muscled (High) and 3 high muscled heterozygotes for myostatin mutation (HighHet) steers were challenged with adrenaline doses ranging between 0.2 to 3.0 μg/kg live weight. For each challenge, 16 blood samples were taken between −30 and 130 min relative to adrenaline administration. Plasma was analysed for NEFA, lactate and glucose concentration and area under curve (AUC) over time was calculated to reflect the tissue responses to adrenaline. Sixteen basal plasma samples from each animal were also assayed for growth hormone. Muscle glycogen and lactate concentration were analysed from four muscle biopsies taken from the semimembranosus, semitendinosus and longissimus thoracis et lumborum of each animal at 14, 90 and 150 days on an ad libitum grain-based diet and at slaughter on day 157. In response to the adrenaline challenges, the High steers had 30% lower lactate AUC than the Low steers at challenges greater than 2 μg/kg live weight, indicating lower muscle responsiveness at the highest adrenaline doses. Aligning with this decrease in muscle response in the High animals were the muscle glycogen concentrations which were 6.1% higher in the High steers. These results suggest that selection for muscling could reduce the incidence of dark, firm, dry meat that is caused by low levels of glycogen at slaughter. At all levels of adrenaline challenge, the High steers had at least 30% greater NEFA AUC, indicating that their adipose tissue was more responsive to adrenaline, resulting in greater lipolysis. In agreement with this response, the High steers had a higher plasma growth hormone concentration, which is likely to have contributed to the increased lipolysis evident in these animals in response to adrenaline. This difference in lipolysis may in part explain the reduced fatness of muscular cattle. There was no effect of selection for muscling on liver responsiveness to adrenaline.

Keywords

muscularityadrenaline sensitivityglycogenlipolysiscattle
Type
Full Paper
Information
animal , Volume 5 , Issue 6 , June 2011 , pp. 875 - 884
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

Bernard, C, Cassar-Malek, I, Renand, G, Hocquette, JF 2009. Changes in muscle gene expression related to metabolism according to growth potential in young bulls. Meat Science 82, 205–212.CrossRefGoogle ScholarPubMed
Boukhliq, R, Martin, GB, White, CL, Blackberry, MA, Murray, PJ 1997. Role of glucose, fatty acids and protein in regulation of testicular growth and secretion of gonadotrophin, prolactin, somatotrophin and insulin in the mature ram. Reproduction, Fertility and Development 9, 515–524.CrossRefGoogle ScholarPubMed
Briand, M, Talmant, A, Briand, Y, Monin, G, Durand, R 1981. Metabolic types of muscle in sheep: I. Myosin ATPase, glycolytic and mitochondrial enzyme activities. European Journal of Applied Physiology and Occupational Physiology 46, 347–358.CrossRefGoogle ScholarPubMed
Chan, DM, Exton, JH 1976. A rapid method for the dtermination of glycogen content and radioactivity in small quantities of tissue or isolated hepatocytes. Analytical Biochemistry 71, 96–105.CrossRefGoogle ScholarPubMed
Downing, JA, Joss, J, Connell, P, Scaramuzzi, RJ 1995. Ovulation rate and the concentrations of gonadotrophic and metabolic hormones in ewes fed lupin grain. Journal of Reproduction and Fertility 103, 137–145.CrossRefGoogle ScholarPubMed
Drackley, JK, Overton, TR, Douglas, GN 2001. Adaptations of glucose and long-chain fatty acid metabolism in liver of dairy cows during periparturient period. Journal of Dairy Science 84, E100–E112.CrossRefGoogle Scholar
Duncombe, WG 1964. The colorimetric micro-determinations of non-esterified fatty acids in plasma. Clinica Chimica Acta 9, 122–125.CrossRefGoogle Scholar
Eisemann, JH, Hammond, AC, Bauman, DE, Reynolds, PJ, McCutcheon, SN, Tyrrell, HF, Haaland, GL 1986. Effect of bovine growth hormone administration on metabolism of growing Hereford heifers: protein and lipid metabolism and plasma concentrations of metabolites and hormones. Journal of Nutrition 116, 2504–2515.CrossRefGoogle ScholarPubMed
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
Ferguson, DM, Bruce, HL, Thompson, JM, Egan, AF, Perry, D, Shorthose, WR 2001. Factors affecting beef palatability – farmgate to chilled carcass. Australian Journal of Experimental Agriculture 41, 879–891.CrossRefGoogle Scholar
Fiems, LO, Van Hoof, J, Uytterhaegen, L, Boucque, CV, Demeyer, D 1995. Comparative quality of meat from double-muscled and normal beef cattle. In Expression of tissue proteinases and regulation of protein degradation as related to meat quality (ed. A Ouali, D Demeyer and FJM Smulders), pp. 381–393. ECCEAMST, Utrecht, The Netherlands.Google Scholar
Gardner, GE, Kennedy, L, Milton, JTB, Pethick, DW 1999. Glycogen metabolism and ultimate pH of muscle in Merino, first-cross and second-cross wether lambs as affected by stress before slaughter. Australian Journal of Agricultural Research 50, 175–181.CrossRefGoogle Scholar
Greenwood, PL, Gardner, GE, Hegarty, RS 2006a. Lamb myofibre characteristics are influenced by sire estimated breeding values and pastoral nutritional system. Australian Journal of Agricultural Research 57, 627–639.CrossRefGoogle Scholar
Greenwood, PL, Cafe, LM, O'Rourke, BA, McKiernan, WA 2006b. Myofibre characteristics in M. semitendinosus of steers from Angus muscling selection lines with normal and mutant myostatin alleles. In Australian Society of Animal Production 26th Biennial Conference, Short communication 15, Perth.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
Hocquette, JF, Bas, P, Bauchart, D, Vermorel, M, Geay, Y 1999. Fat partitioning and biochemical characteristics of fatty tissues in relation to plasma metabolites and hormones in normal and double-muscled young growing bulls. Comparative Biochemistry and Physiology Part A 122, 127–138.CrossRefGoogle ScholarPubMed
Itaya, K, Ui, M 1965. Colorimetric determination of free fatty acids in biological fluids. Journal Lipid Research 6, 16–20.CrossRefGoogle ScholarPubMed
Jensen, F, Alvardado, S, Pirkusny, I, Geary, C 1995. NBQX blocks the acute and late epileltogenic effects of perinatal hypoxia. Epilepsia 36, 966–972.CrossRefGoogle ScholarPubMed
Jocken, JWE, Blaak, EE 2008. Catecholamine-induced lipolysis in adipose tissue and skeletal muscle in obesity. Physiology & Behavior 94, 219–230.CrossRefGoogle ScholarPubMed
Johnsson, ID, Hart, IC 1985. Pre-pubertal mammogenesis in the sheep. 1. The effects of level of nutrition on growth and mammary development in female lambs. Animal Production 41, 323–332.Google 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
Lacourt, A, Tarrant, PV 1985. Glycogen depletion patterns in myofibres of cattle during stress. Meat Science 15, 85–100.CrossRefGoogle ScholarPubMed
Leenanuruksa, D, McDowell, GH 1985. Effects of prolonged intravenous infusions of adrenaline on glucose utilization, plasma metabolites, hormones and milk production in lactating sheep. Australian Journal of Biological Science 38, 197–208.CrossRefGoogle ScholarPubMed
Marbach, EP, Weil, MH 1967. Rapid enzymatic measurement of blood lactate and pyruvate. Journal of Clinical Chemistry 13, 314–325.CrossRefGoogle ScholarPubMed
Martin, W, Murphree, S, Saffitz, J 1989. Beta-adrenergic receptor distribution among muscle fibre types and resistance arterioles of white, red, and intermediate skeletal muscle. Circulation Research 64, 1096–1105.CrossRefGoogle ScholarPubMed
Martin, KM, McGilchrist, P, Thompson, JM, Gardner, GE 2011. Progeny of high muscling sires have reduced muscle response to adrenaline in sheep. Animal, doi:10.1017/S1751731110002764.CrossRefGoogle ScholarPubMed
McCutcheon, SN, Bauman, DE 1986. Effect of chronic growth hormone treatment on responses to epinephrine and thyrotropin-releasing hormone in lactating cows. Journal of Dairy Science 69, 44–51.CrossRefGoogle ScholarPubMed
McKiernan, WA 1990. New developments in live animal appraisal of meat quantity in beef cattle. In Proceedings of the 8th Conference of the Australian Association for Animal Breeding and Genetics, Hamilton, New Zealand, pp. 447–450.Google Scholar
McKiernan, WA 2001. Breeding for divergence in muscling. In Beef Products Conference (ed. JF Wilkins and JA Archer), pp. 42–45. NSW Department of Agriculture, Orange, NSW, Australia.Google Scholar
Monin, G 1981a. Double-muscling and sensitivity to stress. In The problem of dark-cutting in beef. Current topics in veterinary medicine and animal science, (ed. DE Hood and PV Tarrant), vol. 10, pp. 199–208. Martinus Nijhoff, The Hague, The Netherlands.Google Scholar
Monin, G 1981b. Muscle metabolic type and the DFD condition. In The problem of dark-cutting in beef. Current topics in veterinary medicine and animal science (ed. DE Hood and PV Tarrant), pp. 63–85. Martinus Nijhoff, The Hague, The Netherlands.Google Scholar
Novakofski, J, Brenner, K, Easter, R, McLaren, D, Jones, R, Ingle, D, Bechtel, P 1988. Effects of porcine somatotropin on swine metabolism. FASEB Journal 2, A848.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.CrossRefGoogle Scholar
Perry, D, McKiernan, WA, Yeates, AP 1993a. Muscle score: its usefulness in describing the potential yield of saleable meat from live steers and their carcasses. Australian Journal of Experimental Agriculture 33, 275–281.CrossRefGoogle Scholar
Perry, D, Yeates, AP, McKiernan, WA 1993b. Meat yield and subjective muscle scores in medium weight steers. Australian Journal of Experimental Agriculture 33, 825–831.CrossRefGoogle Scholar
Pethick, DW, Dunshae, FR 1996. The partitioning of fat in farm animals. Proceedings of the Nutrition Society of Australia 20, 3–13.Google Scholar
Pethick, DW, Rowe, JB, Tudor, GD 1995. Glycogen metabolism and meat quality. In Proceedings of recent advances in animal nutrition in Australia (ed. JB Rowe and JV Nolan), pp. 97–103. Department of Animal Science, University of New England, Armidale, NSW, Australia.Google Scholar
Reynisdttir, S, Wahrenberg, H, Carlstrom, K, Rossner, S, Arner, P 1994. Catecholamine resistance in fat cells of women with upper body obesity due to decreased expression of beta 2-adrenoreceptors. Diabetologia 37, 428–435.CrossRefGoogle Scholar
Richter, EA, Ruderman, NB, Haralambos, G, Belur, ER, Galbo, H 1982. Muscle glycogenolysis during exercise: dual control by epinephrine and contractions. American Journal of Physiology 242, E25–E32.Google ScholarPubMed
Saltin, B, Gollnick, P 1983. Skeletal muscle adaptability: significance for metabolisms and performance. In Handbook of physiology – skeletal muscle section 10 (ed. LD Peachy), pp. 555–631. American Physiological Society, Maryland, USA.Google Scholar
Seal, CJ, Reynolds, CK 1993. Nutritional implications of gastrointestinal and liver metabolism in ruminants. Nutrition Research Reviews 6, 185–208.CrossRefGoogle ScholarPubMed
Sechen, SJ, Dunshea, FR, Bauman, DE 1990. Somatotropin in lactating cows: effect on response to epinephrine and insulin. American Journal Physiology Endocrinology and Metabolism 258, E582–E588.CrossRefGoogle Scholar
Sejrsen, K, Huber, JT, Tucker, HA 1983. Influence of amount fed on hormone concentrations and their relationship to mammary growth in heifers. Journal of Dairy Science 66, 845–855.CrossRefGoogle ScholarPubMed
Statistical Analysis System Institute 2001. SAS Institute Incorporated, Cary, NC.Google Scholar
Sudre, K, Cassar-Malek, I, Listrat, A, Ueda, Y, Leroux, C, Jurie, C, Auffray, C, Renand, G, Martin, P, Hocquette, JF 2005. Biochemical and transcriptomic analyses of two bovine skeletal muscles in Charolais bulls divergently selected for muscle growth. Meat Science 70, 267–277.CrossRefGoogle ScholarPubMed
Totland, GK, Kryvi, H 1991. Distribution patterns of muscle fibre types in major muscles of the bull (Bos taurus). Anatomy and Embryology 184, 441–450.CrossRefGoogle ScholarPubMed
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
Wood, JD, Warris, PD 1992. The influence of the manipulation of carcass composition on meat quality. In The control of fat and lean deposition (ed. PJ Buttery, KN Boorman and DB Lindsay), pp. 331–334. Butterworths Heinmann, Oxford, UK.CrossRefGoogle Scholar