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Age- and training-related changes in the collagen metabolism of rat skeletal muscle

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The effects of ageing and life-long endurance training on the collagen metabolism of skeletal muscle were evaluated in a longitudinal study. Wistar rats performed treadmill running 5 days a week for 2 years. The activities of collagen biosynthesis enzymes, prolyl-4-hydroxylase and galactosylhydroxylysyl glucosyltransferase, were highest in the muscles of the youngest animals, decreased up to the age of 2 months and from then on remained virtually unchanged. The enzyme activity in young animals was higher in the slow collagenous soleus muscle than in the rectus femoris muscle. The enzyme activity in the soleus muscle was higher for older trained rats than older untrained rats. The relative proportion of type I collagen increased and that of type III collagen decreased with age, suggesting a more marked contribution by type I collagen to the agerelated accumulation of total muscular collagen. The results show that collagen biosynthesis decreases with maturation and that life-long endurance training maintains a higher level of biosynthesis in slow muscles.

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  1. Alnageeb MA, Zaid NS, Goldspink G (1984) Connective tissue changes and physical properties of developing and ageing skeletal muscle. J Anat 139:677–689

  2. Anttinen H, Oikarinen A, Kivirikko KI (1977) Age-related changes in human skin collagen galactosyltransferase and collagen glucosyltransferase activities. Clin Chim Acta 76:95–101

  3. Anttinen H, Järvensivu PH, Sovalainen E-R (1981) Serum galactosylhydroxylysyl glucosyltransferase in acute myocardial infarction and during subsequent collagen scar formation. Eur J Clin Invest 11:375–379

  4. Anttinen H, Terho EO, Järvensivu PM, Savolainen E-R (1985) Elevated serum galactosylhydroxylysyl glucosyltransferase, a collagen synthesis marker, in fibrosing lung diseases. Clin Chim Acta 3:3–8

  5. Berg RA, Prockop DJ (1973) The thermal transition of a nonhydroxylated form of collagen. Evidence for a role for hydroxyproline in stabilizing the triplehelix of collagen. Biochem Biophys Res Commun 52:115–119

  6. Booth FW, Gould EW (1975) Effects of training and disuse on connective tissue. In: Willmore JH, Keogh JF (eds) Exercise and sport sciences reviews. Academic Press, New York, p 83–112

  7. Borg TK, Caulfield JB (1980) Morphology of connective tissue in skeletal muscle. Tissue Cell 12:197–207

  8. Bornstein P, Sage H (1980) Structurally distinct collagen types. Annu Rev Biochem 49:957–1003

  9. Duance VC, Restall DJ, Beard H, Bourne FJ, Bailey AJ (1977) The location of three collagen types in skeletal muscle. FEBS Lett 79:248–252

  10. Epstein EH (1974) (α 1 (III))3 Human skin collagen release by pepsin digestion and preponderance in fetal life. J Biol Chem 249:3225–3231

  11. Gutmann E (1977) Muscle. In: Finch CE, Hayflick L (eds) Handbook of the biology of ageing. Van Nostrand, New York, pp 445–469

  12. Hasselbach W, Schneider G (1951) Der L-Myosin-und Aktin-gehalt des Kaninchenmuskels. Biochem Z 321:462–475

  13. Juva K, Prockop DJ (1966) Modified procedure for the assay of H3- or C14-labelled hydroxyproline. Anal Biochem 15:77–83

  14. Kivirikko KI, Myllylä R (1979) Collagen glycosyltransferases. Int Rev Connect Tissue Res 8:23–72

  15. Kivirikko KI, Myllylä R (1980) The hydroxylation of prolyl and lysyl residues. In: Freedman RB, Hawkins HC (eds) The enzymology of posttranslational modifications of proteins. Academic Press, London, pp 53–104

  16. Kivirikko KJ, Myllylä R (1982) Posttranslational enzymes in the biosynthesis of collagen: intracellular enzymes. In: Colowick SP, Kaplan NO (eds) Methods in enzymology, vol 82. Structural and contractile proteins. Academic Press, New York, pp 245–304

  17. Kivirikko KI, Laitinen D, Prockop DJ (1967) Modification of a specific assay for hydroxyproline in urine. Anal Biochem 19:249–255

  18. Kovanen V, Suominen H (1987) Effects of age and lifetime physical training on fibre composition of slow and fast skeletal muscle in rats. Pflügers Arch 408:543–551

  19. Kovanen V, Suominen H, Heikkinen E (1980) Connective tissue of “fast” and “slow” skeletal muscle in rats — effects of endurance training. Acta Physiol Scand 108:173–180

  20. Kovanen V, Suominen H, Heikkinen E (1984a) Collagen of slow twitch and fast twitch muscle fibres in different types of rat skeletal muscle. Eur J Appl Physiol 52:235–242

  21. Kovanen V, Suominen H, Heikkinen E (1984b) Mechanical properties of fast and slow skeletal muscle with special reference to collagen and endurance training. J Biomech 17:725–735

  22. Kovanen V, Suominen H, Peltonen L (1987) Effects of aging and life-long physical training on collagen in slow and fast skeletal muscle in rats. A morphometric and immunohistochemical study. Cell Tissue Res 248:247–255

  23. Kuutti-Savolainen E-R, Anttinen H, Miettinen TA, Kivirikko KI (1979) Collagen biosynthesis enzymes in serum and hepatic tissue in liver disease. II. Galactosylhydroxylysyl glucosyltransferase. Eur J Clin Invest 9:97–101

  24. Laemmli VK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

  25. Laurent GJ (1987) Dynamic state of collagen: pathways of collagen degradation in vivo and their possible role in regulation of collagen mass. Am J Physiol 252:C1-C9

  26. Laurent JL, Cockerill P, McAnulty RJ, Hastings JRB (1981) A simplified method for quantitation of the relative amounts of type I and type III collagen in small tissue samples. Anal Biochem 13:301–312

  27. Lento M (1983) Collagen and fibronectin in a healing skeletal muscle injury: an experimental study in rats under variable states of physical activity. Ann Univ Turk Ser D Med-Odontol

  28. Light ND (1982) Estimation of types I and III collagens in whole tissue by quantitation of CNBr peptides on SDSpolyacrylamide gels. Biochim Biophys Acta 702:30–36

  29. Light ND, Bailey AJ (1979) Covalent crosslinks in collagen: characterization and relationships to connective tissue disorders. In: Parry DAS, Creamer LK (eds) Fibrous proteins: scientific, industrial and medical aspects. Academic Press, London, pp 151–177

  30. Mayne R, Sandersen RD (1985) The extracellular matrix of skeletal muscle. Coll Relat Res 5:449–468

  31. Myllylä R, Myllylä W, Tolonen V, Kivirikko KI (1982) Changes in collagen metabolism in diseased muscle. I. Biochemical studies. Arch Neurol 39:752–755

  32. Peltonen L, Myllylä R, Tolonen V (1983) Changes in collagen metabolism in diseased muscle. II. Immunohistochemical studies. Arch Neurol 39:756–759

  33. Ramshaw JAM (1986) Distribution of type III collagen in bovine skin of various ages. Connect Tissue Res 14:307–314

  34. Savolainen ER, Miettinen TA, Pikkarainen P, Salaspuro MP, Kivirikko KI (1983) Enzymes of collagen synthesis and type III procollagen aminopropeptide in the evaluation of D-penicillamine and medroxyprogesterone treatments of primary biliary cirrhosis. Gut 24:136–142

  35. Suominen H, Heikkinen E (1975) Enzyme activities in muscle and connective tissue of M. vastus lateralis in habitually training and sedentary 33 to 70-year-old men. Eur J Appl Physiol 34:249–254

  36. Suominen H, Heikkinen E, Parkatti T (1977) Effect of eight weeks' physical training on muscle and connective tissue of the m. vastus lateralis in 60-year-old men and women. J Gerontol 32:33–37

  37. Takala TES, Myllylä R, Salminen A, Anttinen H, Vihko V (1983) Increased activities of prolyl-4-hydroxylase and galactosylhydroxylysyl glucosyltransferase, enzymes of collagen biosynthesis in skeletal muscle of endurance-trained mice. Pflügers Arch 399:271–274

  38. Tryggvason K, Majamaa K, Kivirikko KI (1979) Prolyl 3-hydroxylase and 4-hydroxylase activities in certain rat and chick-embryo tissues and age-related changes in their activities in the rat. Biochem J 178:127–131

  39. Tuderman L, Kivirikko KI (1977) Immunoreactive prolyl hydroxylase in human skin, serum and synovial fluid: changes in the content and components with age. Eur J Clin Invest 7:295–299

  40. Vogel HG (1974) Correlation between tensile strength and collagen content in rat skin effect of age and cortisol treatment. Connect Tissue Res 2:177–182

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Kovanen, V., Suominen, H. Age- and training-related changes in the collagen metabolism of rat skeletal muscle. Europ. J. Appl. Physiol. 58, 765–771 (1989). https://doi.org/10.1007/BF00637389

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Key words

  • Collagen biosynthesis
  • Collagen types
  • Slow and fast skeletal muscle
  • Age
  • Endurance training