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Morphometric analysis of loading-induced changes in collagen-fibril populations in young tendons

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Summary

This study was designed to gain more detailed morphological information on skeletal tendons in the course of adaptation to physical loading. The effect on collagen fibrils was investigated in 6-week-old mice by means of electron microscopy. Physical loading was performed on a treadmill 5 days a week for 1, 3, 5, 7 and 10 weeks. Morphometric analysis of collagen fibrils revealed the mean diameter, the diameter distribution, the number and the cross-sectional area. The principal observations included:

  1. 1.

    After one week of physical loading an increase in mean fibril diameter (30%, p≦0.01), in number (15%, p≦ 0.05), and in cross-sectional area (15%, p≦0.05), as well as a change in mean fibril diameter distribution.

  2. 2.

    From the third to the seventh week a fall under the level of the controls in mean diameter (26%, p≦0.01), in number (26%, p≦0.01), and a reduced cross-sectional area (17%, p≦0.01), accompanied by signs of splitting of individual collagen fibrils.

  3. 3.

    In the long-term study an increase in fibril number (29%, p≦0.01), a fall in mean diameter from 189 nm in the controls to 179 nm (p≦0.05) but no statistically significant change in the relative cross-sectional area (32%) per unit in comparison to unloaded tendons.

The possible physiological implications of the findings are discussed in the light of several regulatory mechanisms known to appear during the course of physical loading in connective tissues.

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References

  • Anderson JC, Eriksson C (1968) Electrical properties of wet collagen. Nature 278:166–168

    Google Scholar 

  • Aureli G, Castellani AA, Balduine C, Bonucci E, Cetta G, De Luca G, Rizzotti M, Ruggeri A (1981) Structural and metabolic aspects of macromolecules in the connective tissue. Bas Appl Histochem 25:217–254

    Google Scholar 

  • Bassett CAL (1971a) Effect of force on skeletal tissue. In: Darling RE, Downey J (eds) Physical basis for rehabilitation. Saunders WB, Philadelphia, pp 283–316

    Google Scholar 

  • Bassett CAL (1971b) Biophysical principles affecting bone structure. In: Downey JA, Darling RC (eds) The biochemistry and physiology of bone. Academic Press, London New York, pp 1–76

    Google Scholar 

  • Bassett CAL, Becker RO (1962) Generation of electric potentials by bone in response to mechanical stress. Science 137:1063–1064

    CAS  PubMed  Google Scholar 

  • Bassett CAL, Pawluk RJ (1972) Electrical behaviour of cartilage during loading. Science 178:982–983

    Google Scholar 

  • Bonner JT (1982) Evolution and development. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Bowes JH, Cater CW (1968) The interactions of aldehydes with collagen. Biochem Biophys Acta 168:341–352

    Google Scholar 

  • Byrd RJ (1973) The effect of controlled mild exercise on the rate of physiological aging of rats. J Sports Med Phys Fitness 13:1–3

    Google Scholar 

  • Caplan AJ (1981) The molecular control of muscle and cartilage development. In: Liss AR (ed) Levels of genetic control in development. Academic Press, New York, pp 37–68

    Google Scholar 

  • Dobzhansky T (1951) Genetics and the origin of the species. University Press, New York

    Google Scholar 

  • Dyer RF, Enna CD (1976) Ultrastructural features of adult human tendon. Cell Tissue Res 168:247–259

    Google Scholar 

  • Eikenberry EF, Brodsky BB, Craig AS, Parry DAD (1982) Collagen fibril morphometry in developing chick metatarsal tendon: 2. Electron microscope studies. Int J Biol Macromol 4:393–398

    Google Scholar 

  • Evans JH, Barbenel JC (1975) Structural and mechanical properties of tendon related to function. Equ Vet J 7:1–8

    Google Scholar 

  • Eyre DR, Muir H (1974) Collagen polymorphism. Two molecular species in pig intervertebral disc. FEBS Lett 42:192–196

    Google Scholar 

  • Eyre DR, Muir H (1976) Types I and II collagens in intervertébral disc. Biochem J 157:267–270

    CAS  PubMed  Google Scholar 

  • Finlay JB, Hunter JAA, Steven FS (1971) Preparation of human skin for high resolution scanning electron microscopy using phosphate buffered crude bacterial χ-amylase. J Microsc 93:73–76

    Google Scholar 

  • Fitton-Jackson S (1968) Morphogenesis of collagen. In: Gould BS (ed) Treatise on collagen. Vol 2. Academic Press, London, pp 1–66

    Google Scholar 

  • Flint MH (1976) The role of environmental factors on connective tissue cell metabolism. In: Longrace JJ (ed) The ultrastructure of collagen. Springfield, Illinois, pp 191–198

  • Franzblau C, Schmid K, Faris B, Beldekas J, Garvin P, Kagan H, Baum B (1976) The interaction of collagen with α1-acid glycoprotein. Biochem Biophys Acta 427:302–314

    Google Scholar 

  • Fukuda E, Yasuda J (1957) On the piezoelectric effect of bone. J Phys Soc Jpn 12:1158–1162

    Google Scholar 

  • Fukuda E, Yasuda J (1964) Piezoelectric effects in collagen. Jpn J Appl Phys 3:117–121

    Google Scholar 

  • Gillard GC, Birnbaum P, Reilly HC, Merrilees MJ, Flint MH (1979) The effect of charged synthetic polymers on proteoglycan synthesis and sequestration in chick embryo fibroblasts in culture. Biochim Biophys Acta (Gen Sub) 584:520–528

    Google Scholar 

  • Herbert CM, Lindberg KA, Jayson MJV, Bailey AJ (1975) Changes in the collagen of human intervertebral disc during ageing and degenerative disc disease. J Mol Med 1:79–91

    Google Scholar 

  • Hickey DS, Hukins DWL (1979) Effects of methods of preservation on the arrangement of collagen fibrils in extracellular matrices: an X-ray diffraction study of annulus fibrosus. Connect Tissue Res 6:223–228

    Google Scholar 

  • Hickey DS, Hukins DWL (1981) Collagen fibril diameters and elastic fibres in the annulus fibrosus of human fetal intervertebral disc. J Anat 133:351–357

    Google Scholar 

  • Hickey DS, Hukins DWL (1982) Aging changes in the macromolecular organization of the intervertebral disc. Spine Vol 7, No 3: 234–242

    Google Scholar 

  • Leung DYM, Glagov S, Mathews MB (1977a) A new “in vitro” system for studying cell response to mechanical stimulation. Different effects of cyclic stretching and agitation on smooth muscle cell biosynthesis. Exp Cell Res 109:285–298

    Google Scholar 

  • Leung DYM, Glagov S, Mathews MB (1977b) Elastin and collagen accumulation in rabbit ascending aorta and pulmonary trunk during postnatal growth. Correlation of cellular synthetic response with medial tension. Circ Res 41:316–323

    Google Scholar 

  • Liesen H, Dufaux B, Hollmann W (1977) Modification of serum glycoproteins the days following a prolonged physical exercise and the influence of physical training. Eur J Appl Physiol 37:243–254

    Google Scholar 

  • Light ND, Bailey AJ (1979) Changes in cross-linking during ageing in bovine tendon collagen. FEBS Lett 97:183–187

    Google Scholar 

  • Light ND, Bailey AJ (1980) Molecular structure and stabilization of the collagen fibre. In: Viidik A, Vuust J (eds) Biology of collagen. Academic Press, London New York, pp 15–39

    Google Scholar 

  • Merker H-J, Barrach H-J (1982) Stoffwechsel und Physiologie der Sehne. In: Groher W, Noack W (eds) Sportliche Belastungsfähigkeit des Haltungs- und Bewegungsapparates. Thieme, Stuttgart, pp 295–312

    Google Scholar 

  • Merrilees MJ, Flint MH (1980) Ultrastructural study of tension and pressure zones in a rabbit flexor tendon. Am J Anat 157:87–106

    Google Scholar 

  • Michna H (1983) A peculiar myofibrillar pattern in the murine muscle-tendon junction. Cell Tissue Res 233:227–231

    Google Scholar 

  • Miller A (1980) Structural studies on connective tissue. In: Viidik A, Vuust J (eds) Biology of collagen. Academic Press, London New York, pp 39–53

    Google Scholar 

  • Miller EJ (1976) Biochemical characteristics and biological significance of the genetically-distinct collagens. Molec Cell Biochem 13:165–192

    Google Scholar 

  • Oakes BH, Parker AE, Norman J (1982) Changes in collagen fiber populations in young rat cruciate ligaments in response to a one month intensive exercise program (Abstract). Connect Tissue Res 9:212

    Google Scholar 

  • Parry DAD, Craig AS (1977) Quantitative electron microscope observations of the collagen fibrils in rat-tail tendon. Biopolymers 16:1015–1031

    Google Scholar 

  • Parry DAD, Craig AS (1978) Collagen fibrils and elastic fibers in rat-tail tendon: An electron microscopic investigation. Biopolymers 27:843–855

    Google Scholar 

  • Parry DAD, Craig AS, Barnes GRG (1978a) Tendon and ligament from the horse: an ultrastructural study of collagen fibrils and elastic fibres as a function of age. Proc R Soc Lond B 203:293–303

    Google Scholar 

  • Parry DAD, Barnes GRG, Craig AS (1978b) A comparison of the size distribution of collagen fibrils in connective tissues as a function of age and a possible relation between fibril size distribution and mechanical properties. Proc R Soc Lond B 203:305–321

    Google Scholar 

  • Parry DAD, Craig AS, Barnes GRG (1980) Fibrillar collagen in connective tissues. In: Parry DAD, Creamer LK (eds) Fibrous proteins: Scientific, industrial and metabolic aspects, Vol 2. Academic Press, New York, pp 107–119

    Google Scholar 

  • Parry DAD, Flint MH, Gillard GC, Craig AS (1982) Hypothesis: a role for glycosaminoglycans in the development of collagen fibrils. FEBS Lett 149:1–7

    Google Scholar 

  • Penttinen R, Frey H, Aalto M, Vuorio E, Marttala T (1980) Collagen synthesis in cultured cells. In: Viidik A, Vuust J (eds) Biology of collagen. Academic Press, London New York, pp 87–105

    Google Scholar 

  • Pollack SR, Korostoff E, Sternberg ME (1977) Stress generated potentials in bone: Effects of collagen modification. J Biomed Mat Res Vol II: 677–700

    Google Scholar 

  • Rollhäuser H (1954) Funktionelle Anpassung der Sehnenfasern im submikroskopischen Bereich. 51. Verh Anat Ges ErgH 100:318–322

    Google Scholar 

  • Roth S, Freund J (1981a) Optical second-harmonic scattering in rat-tail tendon. Biopolymers 20:1271–1290

    Google Scholar 

  • Roth S, Freund J (1981b) Optical second-harmonic generation in collagen: Evidence for a macroscopic polarity in rat-tail tendon. In: Balaban M, Sussman JL, Traub W, Yonath A, Balaban JSS (eds) Structural aspects of recognition and assembly in biological macromolecules. Rehovot, Philadelphia, pp 447–461

    Google Scholar 

  • Roth S, Freund J (1982) Second harmonic generation and orientational order in connective tissue: A mosaic model for fibril orientational ordering in rat-tail tendon. J Appl Cryst 15:72–78

    Google Scholar 

  • Rowe RWD (1969) The effect of senility on skeletal muscles in the mouse. Exp Gerontol 4:119–126

    Google Scholar 

  • Sachs L (1978) Angewandte Statistik, 5th ed. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Slavkin H, Greulich R (eds) (1975) Extracellular matrix influences on gene expression. Academic Press, New York

    Google Scholar 

  • Steven FS (1967) The effect of chelating agents on collagen interfibrillar matrix interactions in connective tissue. Biochim Biophys Acta 140:522–528

    Google Scholar 

  • Steven FS, Minns RJ, Finlay JB (1975) Evidence for the local denaturation of collagen fibrils during the mechanical rupture of human tendons. Injury 6:317–319

    Google Scholar 

  • Suominen H, Heikkinen E (1975a) Effect of physical training on collagen. Ital J Biochem 24:64–65

    Google Scholar 

  • Suominen H, Heikkinen E (1975b) 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

    Google Scholar 

  • Suominen H, Heikkinen E, Parkatti T (1977) Effect of eight weeks' physical training on muscle and connective tissue of the m. vastus lateralis in 69-year-old men and women. J Gerontol 32:33–37

    Google Scholar 

  • Suominen H, Kiiskinen A, Heikkinen E (1980) Effects of physical training on metabolism of connective tissues in young mice. Acta Physiol Scand 108:17–22

    Google Scholar 

  • Tittel K, Otto H (1970) Der Einfluß eines Lauftrainings unterschiedlicher Dauer und Intensität auf die Hypertrophie, Zugfestigkeit und Dehnungsfähigkeit des straffen kollagenen Bindegewebes (am Beispiel der Achillessehne). Medizin und Sport 10:308–315

    Google Scholar 

  • Torp S, Baer E, Friedman B (1975) Effects of age and of mechanical deformation on the ultrastructure of tendon. In: Atkins EDT, Keller A (eds) Structure of fibrous biopolymers. Colston papers No. 26, Butterworths, London, pp 223–250

    Google Scholar 

  • Udén A (1980) Collagen abnormalities in idiopathic scoliosis. In: Viidik A, Vuust J (eds) Biology of collagen. Academic Press, London New York, pp 175–183

    Google Scholar 

  • Viidik A (1973) Functional properties of collagenous tissues. In: Hall DA, Jackson DS (eds) International review of connective tissue research. Vol VI, Academic Press, New York London, pp 127–215

    Google Scholar 

  • Weibel ER (1969) Stereological principles for morphometry in electron microscopic cytology. Int Rev Cytol 26:235–302

    Google Scholar 

  • Weibel ER (1979) Stereological methods. Vol I, Academic Press, London New York

    Google Scholar 

  • Woodward RH (1972) Correlation. In: Davies OL, Goldsmith PI (eds) Statistical methods in research and development, 4th ed., Oliver and Boyd, Edinburgh, pp 229–235

    Google Scholar 

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  1. Institut für Experimentelle Morphologie, Deutsche Sporthochschule Köln, Köln, Bundesrepublik Deutschland

    H. Michna

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Dedicated to Professor Dr. Dr. Karl-Heinrich Knese, Stuttgart-Hohenheim, in honour of his 70th birthday

Head: Professor Dr. C. Stang-Voss

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Michna, H. Morphometric analysis of loading-induced changes in collagen-fibril populations in young tendons. Cell Tissue Res. 236, 465–470 (1984). https://doi.org/10.1007/BF00214251

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