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Annals of Biomedical Engineering

, Volume 33, Issue 8, pp 1090–1099 | Cite as

The Influence of Noncollagenous Matrix Components on the Micromechanical Environment of Tendon Fascicles

  • Hazel R. C. Screen
  • Julia C. Shelton
  • Vivek H. Chhaya
  • Michael V. Kayser
  • Dan L. Bader
  • David A. Lee
Article

Abstract

Tendon is composed of type I collagen fibers, interspersed with proteoglycan matrix and cells. Glycosaminoglycans may play a role in maintaining the structural integrity of tendon, preventing excessive shearing between collagen components. This study tests the hypothesis that tendon extension mechanisms can be altered by modifying the composition of noncollagenous matrix. Tendon explants were treated with phosphate buffered saline (PBS) or PBS + 0.5 U ml−1 chondroitinase ABC. Structural changes were examined using TEM and biochemical analysis, while strain response was examined using confocal microscopy and gross mechanical characterization. Chondroitinase ABC removed 90% of glycosaminoglycans from the matrix. Results demonstrated significant swelling of fibrils and surrounding matrix when incubated in either solution. In response to applied strain, PBS incubated samples demonstrated significantly less sliding between adjacent fibers than nonincubated, and a 33% reduction in maximum force. By contrast, fascicles incubated in chondroitinase ABC demonstrated a similar strain response to nonincubated. Data indicate that collagen-proteoglycan binding characteristics can be influenced by incubation and this, in turn, can influence the preferred extension mechanisms adopted by fascicles. This highlights the importance of maintaining fascicles within their natural environment to prevent structural or mechanical changes prior to subsequent analysis.

Keywords

Collagen Proteoglycan Matrix Strain Tenocyte Cell nuclei 

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References

  1. 1.
    M. Abrahams. Mechanical behaviour of tendon in vitro. Med. Biol. Eng. 5:433–443, 1967.PubMedGoogle Scholar
  2. 2.
    Arnoczky, S. P., M. Lavagnino, J. H. Whallon, and A. Hoonjan. In situ cell nucleus deformation in tendons under tensile load; a mophological analysis using confocal laser microscopy. J.Orthop. Res. 20:29–35, 2002.Google Scholar
  3. 3.
    Bailey, A. J., S. P. Robins, and G. Balian. Biological significance of the intermolecular crosslinks of collagen. Nature 251:105–109, 1974.CrossRefPubMedGoogle Scholar
  4. 4.
    Banes, A. J., M. Tsuzaki, J. Yamamoto, T. Fischer, B. Brigman, T. Brown, and L. Miller. Mechanoreception at the cellular level: The detection, interpretation, and diversity of responses to mechanical signals. Biochem. Cell Biol. 73:349–365, 1995.PubMedGoogle Scholar
  5. 5.
    Benjamin, M., and J. R. Ralphs. Tendons and ligaments: An overview. Histol. Histopathol. 12:1135–1144, 1997.PubMedGoogle Scholar
  6. 6.
    Berenson, M. C., F. T. Blevins, A. H. Plaas, and K. G. Vogel. Proteoglycans of human rotator cuff tendons. J. Orthop. Res. 14:518–525, 1996.CrossRefPubMedGoogle Scholar
  7. 7.
    Blevin, F. T. Structure, function and adaptation of tendon. Curr. Opin. Orthop. 7(5): 57–61, 1996.Google Scholar
  8. 8.
    Blevins, F. T., M. Djurasovic, E. L. Flatow, and K. G. Vogel. Biology of the rotator cuff tendon. Orthop. Clin. N. Am. 28(1):1–15, 1997.CrossRefGoogle Scholar
  9. 9.
    Chimich, D., N. Shrive, C. Frank, L. Marchuk, and R. Bray. Water content alters viscoelastic behavior of the normal adolescent rabbit medial collateral ligament. J. Biomech. 25(8):831–837, 1992.CrossRefPubMedGoogle Scholar
  10. 10.
    Covizi, D. Z., S. L. Felisbino, L. Gomes, E. R. Pimentel, and H. F. Carvalho. Regional adaptations in three rat tendons. Tissue Cell 33(5):483–490, 2001.CrossRefPubMedGoogle Scholar
  11. 11.
    Cribb, A. M., and J. E. Scott. Tendon response to tensile stress: An ultrastructural investigation of collagen: Proteoglycan interactions in stressed tendon. J. Anat. 187:423–428, 1995.PubMedGoogle Scholar
  12. 12.
    Evered, D., and J. Whelan. Function of Proteogylcans. London: Wiley Interscience, 1986.Google Scholar
  13. 13.
    Farndale, R. W., C. A. Sayers, and A. J. Barrett. A direct spectrophotometric microassay for sulphated glycosaminoglycans in cartilage cultures. Connect. Tissue Res. 9:247–248, 1982.PubMedGoogle Scholar
  14. 14.
    Kastelic, J., and E. Baer. Deformation in tendon collagen. Symp. Soc. Exp. Biol. 34:397–435, 1980.PubMedGoogle Scholar
  15. 15.
    Kastelic, J., A. Galeski, and E. Baer. The multicomposite structure of tendon. Connect. Tissue Res. 6:11–23, 1978.PubMedGoogle Scholar
  16. 16.
    Koob, T. Effects of chondroitinase-ABC on proteoglycans and swelling properties of fibrocartilage in bovine flexor tendon. J. Orthop. Res. 7:219–227, 1989.CrossRefPubMedGoogle Scholar
  17. 17.
    Lee, D. A., E. Assoku, and V. Doyle. A specific quantitative assay for collagen synthesis by cells seeded in collagen-based biomaterials using Sirius Red precipitation. J. Mater. Sci. 9:47–51, 1998.CrossRefGoogle Scholar
  18. 18.
    Maganaris, C. N., and J. P. Paul. In vivo human tendon mechanical properties. J. Physiol. 521(1):307–313, 1999.CrossRefPubMedGoogle Scholar
  19. 19.
    McNeilly, C., A. J. Banes, and J. R. Ralphs. Tendon cells in vivo form a three dimensional network of cell processes linked by gap junctions. J. Anat. 189:593–600, 1996.PubMedGoogle Scholar
  20. 20.
    Millesi, H., R. Reihsner, G. Hamilton, and R. Mallinger. Biomechanical properties of normal tendons, normal palmar aponeuroses, and tissues from patients with Dupuytren’s disease subjected to elastase and chondroitinase treatment. Clin. Biomech. 10:29–35, 1995.CrossRefGoogle Scholar
  21. 21.
    Minns, R. J., and P. D. Soden. The role of the fibrous components and ground substance in the mechanical properties of biological tissues: A preliminary investigation. J. Biomech. 6:153–165, 1973.CrossRefPubMedGoogle Scholar
  22. 22.
    Parry, D. A. D., M. H. Flint, G. C. Gillard, and A. S. Craig. A role for glycosaminoglycans in the development of collagen fibrils. FEBS Lett. 149(1):1–7, 1982.CrossRefPubMedGoogle Scholar
  23. 23.
    Pogány, G., D. J. Hernandez, and K. G. Vogel. The in vitro interaction of proteoglycans with type I collagen is modulated by phosphate. Arch. Biochem. Biophys. 313(1):102–111, 1994.CrossRefPubMedGoogle Scholar
  24. 24.
    Puxkandl, R., I. Zizak, O. Paris, J. Keckes, W. Tesch, S. Bernstorff, P. P. Purslow, and P. Fratzl. Viscoelastic properties of collagen: Synchrotron radiation investigations and structural model. Proc. R. Soc. Lond. B 357:191–197, 2002.CrossRefGoogle Scholar
  25. 25.
    Ralphs, J. R. Cell biology of tendons. Eur. Cell. Mater. J. 4(S1):39–40, 2002.Google Scholar
  26. 26.
    Raspanti, M., T. Congiu, A. Alessandrini, P. Gobbi, and A. Ruggeri. Different patterns of collagen–proteoglycan interaction: A scanning electron microscopy and atomic force microscopy study. Eur. J. Histochem. 44:335–343, 2000.PubMedGoogle Scholar
  27. 27.
    The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J. Cell Biol. 17:208–212, 1963.CrossRefPubMedGoogle Scholar
  28. 28.
    Scott, J. E. Proteoglycan–fibrillar collagen interactions. Biochem. J. 252:13–323, 1988.Google Scholar
  29. 29.
    Scott, J. E. Proteoglycan: Collagen interaction and subfibrillar structure in collagen fibrils. Implications in the development and ageing of connective tissues. J. Anat. 169:23–35, 1990.PubMedGoogle Scholar
  30. 30.
    Scott, J. E. Elasticity in extracellular matrix shape modules of tendon, cartilage etc. A sliding proteoglycan-filament model. J. Physiol. 55(2):335–343, 2003.CrossRefGoogle Scholar
  31. 31.
    Scott, J. E., and R. Orford. Dermatan sulphate-rich proteoglycan associates with rat-tail tendon collagen at the d band in the gap region. Biochem. J. 197:213–216, 1981.PubMedGoogle Scholar
  32. 32.
    Scott, J. E., R. Orford, and E. W. Hughes. Proteoglycan-collagen arrangements in developing rat tail tendon. Biochem. J. 195:573–581, 1981.PubMedGoogle Scholar
  33. 33.
    Screen, H. R. C., D. A. Lee, D. L. Bader, and J. C. Shelton. Development of a technique to determine strains in tendons using the cell nuclei. Biorheology 40:361–368, 2003.PubMedGoogle Scholar
  34. 34.
    Screen, H. R. C., D. A. Lee, D. L. Bader, and J. C. Shelton. An investigation into the effects of the hierarchical structure of tendon fascicles on micromechanical properties. J. Eng. Med. 218:109–119, 2004.Google Scholar
  35. 35.
    Vogel, K. G., and A. B. Meyers. Proteins in the tensile region of adult bovine deep flexor tendon. Clin. Orthop. 367:S344–S355, 1999.CrossRefPubMedGoogle Scholar
  36. 36.
    Vogel, K. G., M. Paulsson, and D. Heinegard. Specific inhibition of type I and type II collagen fibrillogenesis by the small proteoglycan of tendon. Biochem. J. 223:587–597, 1984.PubMedGoogle Scholar

Copyright information

© Biomedical Engineering Society 2005

Authors and Affiliations

  • Hazel R. C. Screen
    • 1
  • Julia C. Shelton
    • 1
  • Vivek H. Chhaya
    • 1
  • Michael V. Kayser
    • 2
  • Dan L. Bader
    • 1
  • David A. Lee
    • 1
  1. 1.Medical Engineering Division and IRC in Biomedical Materials, Department of Engineering, Queen MaryUniversity of LondonLondonUnited Kingdom
  2. 2.Institute of OrthopaedicsUniversity College London Medical SchoolStanmoreUnited Kingdom

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