Hostname: page-component-76fb5796d-22dnz Total loading time: 0 Render date: 2024-04-27T06:22:18.927Z Has data issue: false hasContentIssue false

Influence of growth rate and muscle type on muscle fibre type characteristics, protein synthesis capacity and activity of the calpain system in Friesian calves

Published online by Cambridge University Press:  18 August 2016

M. Therkildsen*
Affiliation:
Danish Institute of Agricultural Sciences, DK-8830 Tjele, Denmark
L. Melchior Larsen
Affiliation:
Royal Veterinary and Agricultural University, DK-1871 Frederiksberg C, Denmark
M. Vestergaard
Affiliation:
Danish Institute of Agricultural Sciences, DK-8830 Tjele, Denmark
Get access

Abstract

The objective of this study was to determine the effect of growth rate on muscle fibre characteristics, concentration of nucleic acids (RNA and DNA) as indicators of muscle protein synthesis capacity and activity of the calpain system at time of slaughter in m. longissimus lumborum (LL) and m. supraspinatus (SS) from calves, in order to elucidate the effect of growth rate on muscle protein turn-over at time of slaughter. Twenty-four Friesian heifer calves were allocated to two different feeding regimens that allowed for a moderate/moderate (MM) or high/high (HH) growth rate from 5 days of age to 90 kg body weight (BW) (period I) and from 90 kg BW to slaughter at 250 kg BW (period II), respectively. The growth rates in the two periods and the weight of LL and SS at slaughter were recorded. Within 30 min after exsanguination, samples were removed from LL and SS, snap-frozen, and later analysed for muscle fibre type frequency and cross-sectional area, DNA and RNA concentration and the activity of the calpain system. High growth rate (i.e. 895 g/day and 1204 g/day in periods I and II, respectively), compared with moderate growth rate (678 g/day and 770 g/day in periods I and II, respectively) had a marked effect on muscle weight and muscle characteristics. High compared with moderate growth rate resulted in hypertrophic growth of type I, IIA and IIB fibres in LL and of type IIA and type IIB fibres in SS, but had no effect on the muscle fibre type frequency in either of the muscles. High growth rate increased total DNA and RNA content and the RNA: DNA ratio in LL, indicating a greater potential for protein synthesis in this muscle, whereas the effect of growth rate was smaller in SS. The activity of µ-calpain, m-calpain and calpastatin was higher in the red SS muscle compared with the whiter LL muscle. However, these enzyme activities were not affected by growth rate, and thus, did not indicate a higher myofibrillar proteolysis in vivo in calves exhibiting high growth rate compared with moderate growth rate. Overall the results showed that different types of muscles react differently to high versus moderate growth rate. High growth rate induced muscle hypertrophy and increased protein synthesis capacity especially in LL and less in SS, but the activities of the enzymes in the calpain system did not show any concomitant increase in muscle protein degradation that would be in favour of improved meat tenderness.

Type
Growth, development and meat science
Copyright
Copyright © British Society of Animal Science 2002

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

Andersen, H. R. 1975. The influence of slaughter weight and level of feeding on growth rate, feed conversion and carcass composition of bulls. Livestock Production Science 2: 341355.CrossRefGoogle Scholar
Becker, W. A. 1992. Manual of quantitative genetics, fifth edition. Academic Enterprises, Pullman, WA.Google Scholar
Beermann, D. H., Butler, W. R., Hogue, D. E., Fishell, V. K., Dalrymple, R. H., Ricks, C. A. and Scanes, C. G. 1987. Cimaterol-induced muscle hypertrophy and altered endocrine status in lambs. Journal of Animal Science 65: 15141524.CrossRefGoogle ScholarPubMed
Brooke, M. H. and Kaiser, K. K. 1970. Muscle fibre types: how many and what kind? Archives of Neurology 23: 369379.CrossRefGoogle ScholarPubMed
Crouse, J. D., Koohmaraie, M. and Seideman, S. C. 1991. The relationship of muscle fibre size to tenderness of beef. Meat Science 30: 295302.CrossRefGoogle ScholarPubMed
Eenaeme, C. van, Clinquart, A., Uytterhaegen, L., Hornick, J., Demeyer, D. and Istasse, L. 1994. Post mortem proteases activity in relation to muscle protein turn-over in Belgian Blue bulls with different growth rates. Sciences des Aliments 14: 475483.Google Scholar
Garlick, P. J., Maltin, C. A., Baillie, A. G. S., Delday, M. I. and Grubb, D. A. 1989. Fibre-type composition of nine rat muscles. II. Relationship to protein turn-over. American Journal of Physiology 257: 828832.Google Scholar
Geesink, G. and Koohmaraie, M. 1999. Technical note: a rapid method for quantification of calpain and calpastatin activities in muscle. Journal of Animal Science 77: 32253229.CrossRefGoogle ScholarPubMed
Goll, D. E., Kleese, W. C. and Szpacenko, A. 1989. Skeletal muscle proteases and protein turn-over. In Animal growth regulation (ed. G., D. R. Campion Hausman, J. and Martin, R. J.), pp. 141182. Plenum Publishing, New York.CrossRefGoogle Scholar
Henckel, P., Ducro, B., Oksbjerg, N. and Hassing, L. 1998. Objectivity of two methods of differentiating fibre types and repeatability of measurements by application of the TEMA image analysis system. European Journal of Histochemistry 42: 4962.Google ScholarPubMed
Higgins, J. A., Lasslett, Y. V., Bardsley, R. G. and Buttery, P. J. 1988. The relation between dietary restriction or clenbuterol (a selective β2 agonist) treatment on muscle growth and calpain proteinase (EC 3.4.22.17) and calpastatin activities in lambs. British Journal of Nutrition 60: 645652.CrossRefGoogle Scholar
Howarth, R. E. and Baldwin, R. L. 1971. Synthesis and accumulation of protein and nucleic acid in rat gastrocnemius muscles during normal growth, restricted growth, and recovery from restricted growth. Journal of Nutrition 101: 477484.CrossRefGoogle ScholarPubMed
Hutson, N. J. and Mortimore, G. E. 1982. Suppression of cytoplasmic protein uptake by lysosomes as the mechanism of protein regain in livers of starved-refed mice. The Journal of Biological Chemistry 257: 95489554.CrossRefGoogle ScholarPubMed
Johnston, J. D., Moody, W. G., Boling, J. A. and Bradley, N. W. 1981. Influence of breed type, sex, feeding systems, and muscle bundle size on bovine fibre type characteristics. Journal of Food Science 46: 17601765.CrossRefGoogle Scholar
Koohmaraie, M. 1990. Quantification of Ca2+-dependent protease activities by hydrophobic and ion-exchange chromatography. Journal of Animal Science 68: 659665.CrossRefGoogle ScholarPubMed
Koohmaraie, M. 1996. Biochemical factors regulating the toughening and tenderization processes of meat. Meat Science 43: 193201.CrossRefGoogle Scholar
Koohmaraie, M., Shackelford, S.D., Muggli-Crockett, N. E. and Stone, R. T. 1991. Effect of the β-adrenergic agonist L644, 969 on muscle growth, endogenous proteinase activities, postmortem proteolysis in wether lambs. Journal of Animal Science 69: 48234835.CrossRefGoogle ScholarPubMed
Koohmaraie, M., Shackelford, S.D., Wheeler, T. L., Lonergan, S. M. and Doumit, M. E. 1995. A muscle hypertrophy condition in lamb (callipyge): characterization of effects on muscle growth and meat quality traits. Journal of Animal Science 73: 35963607.CrossRefGoogle ScholarPubMed
Maltin, C. A., Sinclair, K. D., Warriss, P. D., Grant, C. M., Porter, A. D., Delday, M. I. and Warkup, C. C. 1998. The effects of age at slaughter, genotype and finishing system on the biochemical properties, muscle fibre type characteristics and eating quality of bull beef from suckled calves. Animal Science 66: 341348.CrossRefGoogle Scholar
Millward, D. J., Garlick, P. J., James, W. P. T., Nnanyelugo, D. O. and Ryatt, J. S. 1973. Relationship between protein synthesis and RNA content in skeletal muscle. Nature 241: 204205.CrossRefGoogle ScholarPubMed
Millward, D. J., Garlick, P. J., Stewart, R. J. C., Nnanyelugo, D. O. and Waterlow, J. C. 1975. Skeletal-muscle growth and protein turn-over. Biochemical Journal 150: 235243.CrossRefGoogle Scholar
Moody, W. K., Kemp, J. D., Mahyuddin, M., Johnston, D. M. and Ely, D. G. 1980. Effect of feeding systems, slaughter weight and sex on histological properties of lamb carcasses. Journal of Animal Science 50: 249256.CrossRefGoogle Scholar
Morgan, J. B., Wheeler, T. L., Koohmaraie, M., Crouse, J. D. and Savell, J. W. 1993. Effect of castration on myofibrillar protein turn-over, endogenous proteinase activities, and muscle growth in bovine skeletal muscle. Journal of Animal Science 71: 408414.CrossRefGoogle Scholar
Oksbjerg, N., Petersen, J. S., Sørensen, I. L., Henckel, P., Vestergaard, M., Ertbjerg, P., Møller, A. J., Bejerholm, C. and Støier, S. 2000. Long-term changes in performance and meat quality of Danish Landrace pigs: a study on a current compared with an unimproved genotype. Animal Science 71: 8192.CrossRefGoogle Scholar
Ouali, A. 1990. Meat tenderization: possible causes and mechanisms. A review. Journal of Muscle Foods 1: 129265.CrossRefGoogle Scholar
Ouali, A. and Talmant, A. 1990. Calpains and calpastatin distribution in bovine, porcine and ovine skeletal muscles. Meat Science 28: 331348.CrossRefGoogle ScholarPubMed
Payne, C. A., Hunt, M. C., Warren, K. E., Hayden, J. M., Williams, J. E. and Hedrick, H. B. 1992. Histochemical properties of four bovine muscles as influenced by compensatory gain and growth impetus. Proceedings of the 38th international congress on meat science and technology, Clermont-Ferrand, vol. 2, pp. 121124.Google Scholar
Seideman, S. C. and Crouse, J. D. 1986. The effects of sex condition, genotype and diet on bovine muscle fibre characteristics. Meat Science 17: 5572.CrossRefGoogle Scholar
Seideman, S. C., Koohmaraie, J. D. and Crouse, J. D. 1987. Factors associated with tenderness in young beef. Meat Science 21: 281291.CrossRefGoogle Scholar
Solomon, M. B. and Lynch, G. P. 1988. Biochemical, histochemical and palatability characteristics of young ram lambs as affected by diet and electrical stimulation. Journal of Animal Science 66: 19551962.CrossRefGoogle Scholar
Speck, P. A., Thomson, B. C., Collingwood, K. M., Gilmour, R. S., Sainz, R. D., Bardsley, R. G., Buttery, P. J. and Oddy, H. V. 1993. Effect of genotype and nutrition on calpastatin inhibitory activity and mRNA abundance in milk-fed lambs. Biochimie 75: 925929.CrossRefGoogle ScholarPubMed
Statistical Analysis Systems Institute. 1992. SAS technical report P-229, SAS/STAT software: changes and enhancements, release 6. 07. SAS Institute Inc., Cary, NC.Google Scholar
Therkildsen, M., L., Melchior Larsen, Bang, H. G. and Vestergaard, M. 2002. Effect of growth rate on tenderness development and final tenderness of meat from Friesian calves. Animal Science 74: 253264.CrossRefGoogle Scholar
Thomson, B. C., Muir, P. D. and Dobbie, P. M. 1999. Effect of growth path and breed on the calpain system in steers finished in a feedlot. Journal of Agricultural Science, Cambridge 133: 209215.CrossRefGoogle Scholar
Thomson, B. C., Oddy, V. H. and Sainz, R. D. 1992. Nutritional effects on the calpain system in skeletal muscle of sheep. Proceedings of the New Zealand Society of Animal Production 52: 101102.Google Scholar
Trenkle, A., DeWitt, D. L. and Topel, D. G. 1978. Influence of age, nutrition and genotype on carcass traits and cellular development of the m. longissimus lumborum of cattle. Journal of Animal Science 46: 15971603.CrossRefGoogle Scholar
Wheeler, T. L. and Koohmaraie, M. 1991. A modified procedure for simultaneous extraction and subsequent assay of calcium-dependent and lysosomal protease systems for skeletal muscle biopsy. Journal of Animal Science 69: 15591565.CrossRefGoogle ScholarPubMed
Wheeler, T. L. and Koohmaraie, M. 1992. Effects of the β-adrenergic agonist L644,969 on muscle protein turn-over, endogenous proteinases activities, and meat tenderness in steers. Journal of Animal Science 70: 30353043.CrossRefGoogle Scholar