Hostname: page-component-586b7cd67f-2plfb Total loading time: 0 Render date: 2024-11-24T07:19:33.290Z Has data issue: false hasContentIssue false

Growth equations for skeletal muscle derived from the cytonuclear ratio and growth constraining supplementary functions

Published online by Cambridge University Press:  18 August 2016

C. Z. Roux*
Affiliation:
Department of Genetics, University of Pretoria, Pretoria, 0002, Republic of South Africa
Get access

Abstract

For purely hypertrophic muscle it is postulated that the growth rate in number of nuclei is proportional to the cytoplasmic mass per nucleus multiplied by a growth constraining supplementary function. Growth constraint depends on the distance from any one of the limit number of nuclei, the limit muscle mass or the limit cytoplasmic mass per nucleus. Furthermore, theory and evidence are presented for a power (allometric) relationship between total number of nuclei (n) and muscle mass (m) given by the equation n = gmh. Evidence points to two clusters of values for h, one in the vicinity of h = 2/3 and the other h = 1/2. Both may depend on a linear relationship between number of nuclei inside muscle fibre and fibre cross-sectional area. The difference between the two situations can be derived from basic assumptions on either local or systemic diffusion mediated control of the number or division of satellite cell nuclei, leading directly to values of h either equal to 2/3 or V2. For likely values of h and suitable choices of growth constraints, almost all well known growth functions in the literature are derived as potentially applicable to total number of nuclei, or muscle mass or their ratio. Muscle mass growth will show a sigmoidal form for h = 1. This explains sigmoidal growth in body mass as it is mostly dominated by muscle mass. A possible linear growth phase before maturity is explicable from the cessation of either length (h = 1) or nuclear (h = 0) growth in muscle fibres, while cytoplasmic growth continues to maturity. Furthermore, two rat examples indicate that whole body protein growth can be described by the equations derived for muscle mass growth.

Type
Research Article
Copyright
Copyright © British Society of Animal Science 1999

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

Adams, R. D., Denny-Brown, D. and Pearson, L. M. 1962. Diseases of muscle: a study in pathology, second edition. Henry Kimpton, London.Google Scholar
Allen, R. E., Dodson, M. V., Boxhorn, L. K., Davis, S. L. and Hossner, K. L. 1986. Satellite cell proliferation in response to pituitary hormones. Journal of Animal Science 62: 15961601.CrossRefGoogle ScholarPubMed
Baldwin, R. L. and Sainz, R. D. 1995. Energy partitioning and modelling in animal nutrition. Annual Review of Nutrition 15: 191211.CrossRefGoogle ScholarPubMed
Baserga, R. 1984. Growth in size and cell DNA replication. Experimental Cell Research 151: 14.CrossRefGoogle ScholarPubMed
Bertalanffy, L. von. 1960. Principles and theory of growth.In Fundamental aspects of normal and malignant growth (ed. Nowinski, W. W.), pp. 137259. Elsevier, Amsterdam.Google Scholar
Brody, S. 1945. Bioenergetics and growth. Reinhold, New York.Google Scholar
Brown, J. E., Fitzhugh, H. A. and Cartwright, T. C. 1976. A comparison of nonlinear models for describing weight-age relationships in cattle. Journal of Animal Science 42: 810818.CrossRefGoogle Scholar
Bullough, W. S. 1975. Mitotic control in adult mammalian tissues. Biological Reviews 50: 99127.CrossRefGoogle ScholarPubMed
Cardasis, A. and Cooper, G. W. 1975. An analysis of nuclear numbers in individual muscle fibres during differentiation and growth: satellite cell-muscle fibre growth unit. Journal of Experimental Zoology 191: 347358.CrossRefGoogle ScholarPubMed
Cheek, D. B. 1971. Hormonal and nutritional factors influencing muscle cell growth. Journal of Dental Research 6: (supplement) 13851391.CrossRefGoogle Scholar
Eisen, E. J., Lang, B. J. and Legates, J. E. 1969. Comparison of growth functions within and between lines of mice selected for large and small body weight. Theoretical and Applied Genetics 39: 251 260.CrossRefGoogle ScholarPubMed
Glore, S. R. and Layman, D. K. 1983. Cellular growth of skeletal muscle in weanling rats during dietary restrictions. Growth 47: 403410.Google ScholarPubMed
Harbison, S. A., Goll, D. E., Parish, F. C,. Wang, V. and Kline, E. A. 1976. Muscle growth in two genetically different lines of swine. Growth 40: 253283.Google ScholarPubMed
Hogberg, M. G. and Zimmerman, D. R. 1979. Effects of protein nutrition in young pigs on developmental changes in the body and skeletal muscles during growth. Journal of Animal Science 49: 472481.CrossRefGoogle Scholar
Huggett, A. St G. and Widdas, W. F. 1951. The relationship between mammalian foetal weight and conception age. Journal of Physiology 114: 306317.Google ScholarPubMed
Konigsberg, I. R. 1971. Diffusion mediated control of my oblast fusion. Developmental Biology 26: 133152.CrossRefGoogle Scholar
Laird, A. K. 1966. Postnatal growth of birds and mammals. Growth 30: 349363.Google ScholarPubMed
Latimer, H. B. 1944. The prenatal growth of the cat. XV. The weight of the musculature in the fetal and in the adult cat Growth 8: 205219.Google Scholar
Laurent, G. J., Sparrow, M. P. and Millward, D. J. 1978. Turnover of muscle protein in the fowl: changes in rates of protein synthesis and breakdown during hypertrophy of the anterior and posterior latissimus dorsi muscles. Biochemical Journal 176: 407417.CrossRefGoogle ScholarPubMed
Le Cren, E. D. 1951. The length-weight relationship and seasonal cycle in gonad weight and condition in the perch (Perca fluviatillis). Journal of Animal Ecology 20: 201 219.CrossRefGoogle Scholar
Medawar, P. B. 1940. The growth, growth energy, and aging of the chickens heart. Proceedings of the Royal Society, Series B 129: 332355.Google Scholar
Millward, D. J. 1980. Protein turnover in skeletal and cardiac muscle during normal growth and hypertrophy. In Research monographs in cell and tissue physiology (ed. Wildenthal, K.), vol. 3, pp. 161199. Elsevier/North Holland, Amsterdam.Google Scholar
Millward, D. J., Garlick, P. J., Steward, R. J. C., Nnanyelugo, D. O. and Waterlow, J. C. 1975. Skeletal-muscle growth and protein turnover. Biochemical Journal 150: 235243.CrossRefGoogle ScholarPubMed
Moss, F. P. 1968. The relationship between the dimensions of the fibres and the number of nuclei during normal growth of the skeletal muscle in the domestic fowl. American Journal of Anatomy 122: 555564.CrossRefGoogle ScholarPubMed
Munro, H. N. 1969. Evolution of protein metabolism in mammals. In Mammalian protein metabolism (ed. Munro, H. N.), vol. 3, pp. 133182. Academic Press, New York.CrossRefGoogle ScholarPubMed
Nurse, P. 1980. Cell cycle control — both deterministic and probabilistic? Nature 286: 910.CrossRefGoogle ScholarPubMed
Oltjen, J. W., Bywater, A. C. and Baldwin, R. L. 1985. Simulation of normal protein accretion in rats. Journal of Nutrition 115: 4552.CrossRefGoogle ScholarPubMed
Pearson, A. M. and Young, R. B. 1989. Muscle and meat biochemistry. Academic Press, San Diego.Google Scholar
Richards, F. J. 1959. A flexible growth function for empirical use. Journal of Experimental Botany 10: 290300.CrossRefGoogle Scholar
Robelin, J. and Geay, Y. 1984. Body composition of cattle as affected by physiological status, breed, sex and diet. In Herbivore nutition in the subtropics and tropics (ed. Gilchrist, F. M. C. and Mackie, R. I.), pp. 525548. The Science Press, Craighall, South Africa.Google Scholar
Robinson, E. W. and Bradford, G. E. 1969. Cellular response to selection for rapid growth in mice. Growth 33: 221229.Google ScholarPubMed
Salmon-Legagneur, E. 1968. Prenatal development in the pig and some other multiparous animals. In Growth and development of mammals (ed. Lodge, G. A. and Lamming, G. E.), pp. 158191. Butterworths, London.Google Scholar
Siebrits, F. K. and Barnes, P. M. 1989. The change in the rate of muscle protein metabolism of rats from weaning to 90 days of age. Comparative Biochemistry and Physiology 92A: 485488.CrossRefGoogle ScholarPubMed
Swatland, H. J. 1984. Structure and development of meat animals. Prentice Hall, Englewood Cliffs, NJ.Google Scholar
Taylor, St C. S. 1968. Time taken to mature in relation to mature weight for sexes, strains and species of domesticated mammals and birds. Animal Production 10: 157169.Google Scholar
Taylor, St C. S. 1980. Live-weight growth from embryo to adult in domesticated mammals. Animal Production 31: 223235.Google Scholar
Timon, V. M. and Eisen, E. J. 1969. Comparison of growth curves of mice selected and unselected for postweaning gain. Theoretical and Applied Genetics 39: 345351.CrossRefGoogle ScholarPubMed
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 of cattle. Journal of Animal Science 46: 15971603.CrossRefGoogle Scholar
Tyson, J. J. 1987. Size control of cell division. Journal of Theoretical Biology 126: 381391.CrossRefGoogle ScholarPubMed
Ursin, E. 1967. A mathematical model of some aspects of fish growth, respiration and mortality. Journal of the Fisheries Research Board of Canada 24: 23552453.CrossRefGoogle Scholar
Ursin, E. 1979. Principles of growth in fishes. Symposia of the Zoological Society, London 44: 6387.Google Scholar
Weatherley, A. H. and Gill, H. S. 1987. The biology offish growth. Academic Press, London.Google Scholar
Winick, M. and Noble, A. 1965. Quantitative changes in DNA, RNA and protein during prenatal and postnatal growth in the rat. Developmental Biology 12: 451466.CrossRefGoogle ScholarPubMed
Winick, M. and Noble, A. 1966. Cellular response in rats during malnutrition at various ages. Journal of Nutrition 89: 300306.CrossRefGoogle ScholarPubMed
Winick, M. and Noble, A. 1967. Cellular response with increased feeding in neonatal rats. Journal of Nutrition 91: 179182.CrossRefGoogle ScholarPubMed