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Philosophical Transactions of the Royal Society B: Biological Sciences logoLink to Philosophical Transactions of the Royal Society B: Biological Sciences
. 2002 Feb 28;357(1418):191–197. doi: 10.1098/rstb.2001.1033

Viscoelastic properties of collagen: synchrotron radiation investigations and structural model.

R Puxkandl 1, I Zizak 1, O Paris 1, J Keckes 1, W Tesch 1, S Bernstorff 1, P Purslow 1, P Fratzl 1
PMCID: PMC1692933  PMID: 11911776

Abstract

Collagen type I is the most abundant structural protein in tendon, skin and bone, and largely determines the mechanical behaviour of these connective tissues. To obtain a better understanding of the relationship between structure and mechanical properties, tensile tests and synchrotron X-ray scattering have been carried out simultaneously, correlating the mechanical behaviour with changes in the microstructure. Because intermolecular cross-links are thought to have a great influence on the mechanical behaviour of collagen, we also carried out experiments using cross-link-deficient tail-tendon collagen from rats fed with beta-APN, in addition to normal controls. The load-elongation curve of tendon collagen has a characteristic shape with, initially, an increasing slope, corresponding to an increasing stiffness, followed by yielding and then fracture. Cross-link-deficient collagen produces a quite different curve with a marked plateau appearing in some cases, where the length of the tendon increases at constant stress. With the use of in situ X-ray diffraction, it was possible to measure simultaneously the elongation of the collagen fibrils inside the tendon and of the tendon as a whole. The overall strain of the tendon was always larger than the strain in the individual fibrils, which demonstrates that some deformation is taking place in the matrix between fibrils. Moreover, the ratio of fibril strain to tendon strain was dependent on the applied strain rate. When the speed of deformation was increased, this ratio increased in normal collagen but generally decreased in cross-link-deficient collagen, correlating to the appearance of a plateau in the force-elongation curve indicating creep. We proposed a simple structural model, which describes the tendon at a hierarchical level, where fibrils and interfibrillar matrix act as coupled viscoelastic systems. All qualitative features of the strain-rate dependence of both normal and cross-link-deficient collagen can be reproduced within this model. This complements earlier models that considered the next smallest level of hierarchy, describing the deformation of collagen fibrils in terms of changes in their molecular packing.

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Selected References

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  1. Bailey A. J., Paul R. G., Knott L. Mechanisms of maturation and ageing of collagen. Mech Ageing Dev. 1998 Dec 1;106(1-2):1–56. doi: 10.1016/s0047-6374(98)00119-5. [DOI] [PubMed] [Google Scholar]
  2. Cribb A. M., Scott J. E. Tendon response to tensile stress: an ultrastructural investigation of collagen:proteoglycan interactions in stressed tendon. J Anat. 1995 Oct;187(Pt 2):423–428. [PMC free article] [PubMed] [Google Scholar]
  3. Davison P. F. The contribution of labile crosslinks to the tensile behavior of tendons. Connect Tissue Res. 1989;18(4):293–305. doi: 10.3109/03008208909019078. [DOI] [PubMed] [Google Scholar]
  4. Diamant J., Keller A., Baer E., Litt M., Arridge R. G. Collagen; ultrastructure and its relation to mechanical properties as a function of ageing. Proc R Soc Lond B Biol Sci. 1972 Mar 14;180(1060):293–315. doi: 10.1098/rspb.1972.0019. [DOI] [PubMed] [Google Scholar]
  5. Eyre D. R., Paz M. A., Gallop P. M. Cross-linking in collagen and elastin. Annu Rev Biochem. 1984;53:717–748. doi: 10.1146/annurev.bi.53.070184.003441. [DOI] [PubMed] [Google Scholar]
  6. Fratzl P., Fratzl-Zelman N., Klaushofer K. Collagen packing and mineralization. An x-ray scattering investigation of turkey leg tendon. Biophys J. 1993 Jan;64(1):260–266. doi: 10.1016/S0006-3495(93)81362-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Fratzl P., Misof K., Zizak I., Rapp G., Amenitsch H., Bernstorff S. Fibrillar structure and mechanical properties of collagen. J Struct Biol. 1998;122(1-2):119–122. doi: 10.1006/jsbi.1998.3966. [DOI] [PubMed] [Google Scholar]
  8. Hulmes D. J., Wess T. J., Prockop D. J., Fratzl P. Radial packing, order, and disorder in collagen fibrils. Biophys J. 1995 May;68(5):1661–1670. doi: 10.1016/S0006-3495(95)80391-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Kastelic J., Baer E. Deformation in tendon collagen. Symp Soc Exp Biol. 1980;34:397–435. [PubMed] [Google Scholar]
  10. Lees S., Eyre D. R., Barnard S. M. BAPN dose dependence of mature crosslinking in bone matrix collagen of rabbit compact bone: corresponding variation of sonic velocity and equatorial diffraction spacing. Connect Tissue Res. 1990;24(2):95–105. doi: 10.3109/03008209009152426. [DOI] [PubMed] [Google Scholar]
  11. Light N. D., Bailey A. J. Covalent cross-links in collagen. Methods Enzymol. 1982;82(Pt A):360–372. doi: 10.1016/0076-6879(82)82073-9. [DOI] [PubMed] [Google Scholar]
  12. Misof K., Rapp G., Fratzl P. A new molecular model for collagen elasticity based on synchrotron X-ray scattering evidence. Biophys J. 1997 Mar;72(3):1376–1381. doi: 10.1016/S0006-3495(97)78783-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Mosler E., Folkhard W., Knörzer E., Nemetschek-Gansler H., Nemetschek T., Koch M. H. Stress-induced molecular rearrangement in tendon collagen. J Mol Biol. 1985 Apr 20;182(4):589–596. doi: 10.1016/0022-2836(85)90244-x. [DOI] [PubMed] [Google Scholar]
  14. Sasaki N., Odajima S. Elongation mechanism of collagen fibrils and force-strain relations of tendon at each level of structural hierarchy. J Biomech. 1996 Sep;29(9):1131–1136. doi: 10.1016/0021-9290(96)00024-3. [DOI] [PubMed] [Google Scholar]
  15. Sasaki N., Shukunami N., Matsushima N., Izumi Y. Time-resolved X-ray diffraction from tendon collagen during creep using synchrotron radiation. J Biomech. 1999 Mar;32(3):285–292. doi: 10.1016/s0021-9290(98)00174-2. [DOI] [PubMed] [Google Scholar]
  16. Scott J. E. Proteoglycan: collagen interactions in connective tissues. Ultrastructural, biochemical, functional and evolutionary aspects. Int J Biol Macromol. 1991 Jun;13(3):157–161. doi: 10.1016/0141-8130(91)90041-r. [DOI] [PubMed] [Google Scholar]
  17. Tang S. S., Trackman P. C., Kagan H. M. Reaction of aortic lysyl oxidase with beta-aminopropionitrile. J Biol Chem. 1983 Apr 10;258(7):4331–4338. [PubMed] [Google Scholar]

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