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Structure of the Peritenons of the Paravertebral Tendons Treated with Hyaluronic Acid

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Abstract

The tendon sheaths (peritenons) of the paravertebral tendons of the tails of Wistar rats were studied using scanning electron microscopy. A phenomenological classification of the osteoid structures of the peritenons is given, with the identification of their persistent and permanent varieties. Sesamoid islets, needle-like and lamellar growths, and rudiments of osteons are classified as persistent. Persistent osteoid structures are well prepared for transformations aimed at strengthening the intracellular matrix under mechanical stress. Permanent osteoid structures are microgranules and faceted deposits of calcium phosphates involved in structural and mechanical processes and hetero- and homogeneous nucleation. Hyaluronate loosens the matrix of sesamoid islets, which increases the mobility of sesamoid globules and creates the prerequisites for their directed migration to areas of increased mechanical stress and foci of possible mineralization of extracellular substance, including fibrillar collagen. Hyaluronate sticks together granules and deposits of structured calcium phosphates and contributes to their growth and fixation in areas of increased risk of mechanical stress. This is a fundamentally important adaptive mechanism for strengthening the tendon tissue, acting in advance.

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REFERENCES

  1. Almond, A., Deangelis, P.L., and Blundell, C.D., Hyaluronan: The local solution conformation determined by NMR and computer modeling is close to a contracted left-handed 4-fold helix, J. Mol. Biol., 2006, vol. 358, no. 5, рр. 1256−1269.

  2. Amizuka, N., Hasegawa, T., Oda, K., et al., Histology of epiphyseal cartilage calcification and endochondral ossification, Front. Biosci., 2012, vol. 4, no. 6, pp. 2085−2100.

    Article  Google Scholar 

  3. Amizuka, N., Hasegawa, T., Yamamoto, T., and Oda, K., Microscopic aspects on biomineralization in bone, Clin. Calcium, 2014, vol. 24, no. 2, pp. 203−214.

    CAS  PubMed  Google Scholar 

  4. Anandagoda, N., Ezra, D.G., Cheema, U., et al., Hyaluronan hydration generates three-dimensional meso-scale structure in engineered collagen tissues, J. R. Soc., Interface, 2012, vol. 9, no. 75, pp. 2680−2687.

    Article  CAS  PubMed  Google Scholar 

  5. Benjamin, M., Toumi, H., Ralphs, J.R., et al., Where tendons and ligaments meet bone: Attachment sites (‘entheses’) in relation to exercise and/or mechanical load, J. Anat., 2006, vol. 208, pp. 471−490.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Caspersen, M.B., Roubroeks, J.P., Qun, L., et al., Thermal degradation and stability of sodium hyaluronate in solid state, Carbohydr. Res., 2014, vol. 107, pp. 25−30.

    Article  CAS  Google Scholar 

  7. Cowman, M.K., Schmidt, T.A., Raghavan, P., and Stecco, A., Viscoelastic properties of hyaluronan in physiological conditions, F1000Res, 2015, vol. 4, pp. 622−634.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Donati, A., Magnani, A., Bonechi, C., et al., Solution structure of hyaluronic acid oligomers by experimental and theoretical NMR, and molecular dynamics simulation, Biopolymers, 2001, vol. 59, no. 6, pp. 434−445.

    Article  CAS  PubMed  Google Scholar 

  9. Frayssinet, A., Petta, D., Eglin, D., et al., Development of collagen/hyaluronic acid-tyramine (COLL/THA) composite hydrogels with tunable gelling kinetic and THA content for the treatment of nucleus pulposus, Orthopaedic Proc., 2018, vol. 100-B, suppl. 14, p. 96.

  10. Gaidash, A.A., Krut’ko, V.K., Blinova, M.I., et al., Structure and physicochemical properties of paravertebral tendons, Tsitologiya, 2022, vol. 64, no. 3, pp. 249−261.

    Google Scholar 

  11. Gatej, I., Popa, M., and Rinaudo, M., Role of the pH on hyaluronan behavior in aqueous solution, Biomacromolecules, 2015, vol. 6, no. 1, pp. 61−67.

    Article  Google Scholar 

  12. Gemballa, S., Ebmeyer, L., Hagen, K., et al., Evolutionary transformations of myoseptal tendons in gnathostomes, Proc. Biol. Sci., 2003, vol. 270, pp. 1229−1235.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Hardingham, T., Heng, B.C., and Gribbon, P., Analysis of the concentrated solution properties of hyaluronan by confocal-frap show no evidence of chain-chain association, in Hyaluronan, Proc. Int. Meet. (September 2000, North East Wales Institute), Cambridge: Woodhead Publ. Ltd, 2002, vol. 1, pp. 123−136.

  14. Hasegawa, T., Yamamoto, T., Tsuchiya, E., et al., Ultrastructural and biochemical aspects of matrix vesicle-mediated mineralization, Jpn. Dent. Sci. Rev., 2017, vol. 53, pp. 34−45.

    Article  PubMed  Google Scholar 

  15. Hoefting, J.M., Cowman, M.K., Matsuoka, S., and Balazs, E.A., Temperature effect on the dynamic rheological characteristics of hyaluronan, hylan A and Synvisc, in Hyaluronan, Proc. Int. Meet. (September 2000, North East Wales Institute), Cambridge: Woodhead Publ. Ltd, 2002, vol. 1, pp. 103−108.

  16. Huang-Lee, L.L., Wu, J.H., and Nimni, M.E., Effects of hyaluronan on collagen fibrillar matrix contraction by fibroblasts, J. Biomed. Mater. Res., 1994, vol. 28, no. 1, pp. 123−132.

    Article  CAS  PubMed  Google Scholar 

  17. Jansen, K.A., Licup, A.J., Sharma, A., et al., The role of network architecture in collagen mechanics, Biophys. J., 2018, vol. 114, pp. 2665−2678.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Kastelic, J., Galeski, A., and Baer, E., The multicomposite structure of tendon, Connect. Tissue Res., 1978, vol. 6, pp. 11−23.

    Article  CAS  PubMed  Google Scholar 

  19. Knepper, P.A., Covici, S., Fadel, J.R., et al., Surface-tension properties of hyaluronic acid, J. Glaucoma, 1995, vol. 4, no. 3, pp. 194−199.

    Article  CAS  PubMed  Google Scholar 

  20. Knill, C.J., Kennedy, J.F., Latif, Y., and Ellwood, D., Effect of metal ions on the rheological flow profiles of hyaluronate solutions, in Hyaluronan, Proc. Int. Meet. (September 2000, North East Wales Institute), Cambridge: Woodhead Publ. Ltd, 2002, vol. 1, pp. 175−180.

  21. Kraft, D., Bindslev, D., Melsen, B., et al., Mechano-sensitivity of dental pulp stem cells is related to their osteogenic maturity European, Eur. J. Oral Sci., 2010, vol. 118, no. 1, pp. 29−38.

    Article  CAS  PubMed  Google Scholar 

  22. Landis, W.J. and Silver, F.H., Mineral deposition in the extracellular matrices of vertebrate tissues: Identification of possible apatite nucleation sites on type i collagen, Cells Tissues Organs, 2009, vol. 189, pp. 20−24.

    Article  CAS  PubMed  Google Scholar 

  23. Lanir, Y., Structure-strength relations in mammalian tendon, Biophys. J., 1978, vol. 24, pp. 541−554.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Mikelsaar, R.H. and Scott, J.E., Molecular modelling of secondary and tertiary structures of hyaluronan, compared with electron microscopy and NMR data. Possible sheets and tubular structures in aqueous solution, Glycoconj. J., 1994, vol. 11, no. 2, pp. 65−71.

    Article  CAS  PubMed  Google Scholar 

  25. Nonogaki, T., Xu, S., Kugimiya, S.M., et al., Two dimensional auto-organized nanostructure formation of hyaluronate on bovine serum albumin monolayer and its surface tension, Langmuir, 2000, vol. 16, no. 9, pp. 4272−4278.

    Article  CAS  Google Scholar 

  26. Nudelman, F., Pieterse, K., George, A., et al., The role of collagen in bone apatite formation in the presence of hydroxyapatite nucleation inhibitors, Nat. Mater., 2010, vol. 9, pp. 1004−1009.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Prusova, A., Šmejkalová, D., Chytil, M., et al., An alternative DSC approach to study hydration of hyaluronan, Carbohydr. Polym., 2010, vol. 82, no. 2, pp. 498−503.

    Article  CAS  Google Scholar 

  28. Scott, J.E., Cummings, C., Brass, A., and Chen, Y., Secondary and tertiary structures of hyaluronan in aqueous solution, investigated by rotary shadowing-electron microscopy and computer simulation. Hyaluronan is a very efficient network-forming polymer, Biochem. J., 1991, vol. 274, pp. 699−705.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Shimazu, A., Jikko, A., Iwamoto, M., et al., Effects of hyaluronic acid on the release of proteoglycan from the cell matrix in rabbit chondrocyte cultures in the presence and absence of cytokines, Arthritis Rheum., 1993, vol. 36, no. 2, pp. 247−253.

    Article  CAS  PubMed  Google Scholar 

  30. Suh, H. and Lee, J.E., Behavior of fibroblasts on a porous hyaluronic acid incorporated collagen matrix, Yonsei Med. J., 2002, vol. 43, no. 2, pp. 193−202.

    Article  CAS  PubMed  Google Scholar 

  31. Summers, A.P. and Koob, T.J., The evolution of tendon ? morphology and material properties, Comp. Biochem. Physiol., Part A: Mol. Integr. Physiol., 2002, vol. 133, pp. 1159−1170.

    Article  Google Scholar 

  32. Wu, T., Yin, F., Wang, N., et al., Involvement of mechanosensitive ion channels in the effects of mechanical stretch induces osteogenic differentiation in mouse bone marrow mesenchymal stem cells, J. Cell Physiol., 2021, vol. 236, no. 1, pp. 284−293.

    Article  CAS  PubMed  Google Scholar 

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Funding

This work was performed with financial support of the State Program of Scientific Research “Chemical Processes, Reagents, and Technologies, Bioregulators, and Bioorganic Chemistry” under task 2.1.04.7 for 2021–2025.

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Correspondence to A. A. Gaidash.

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The authors declare that they have no conflicts of interest.

The authors did not conduct experiments with human participation. All procedures performed in animal research comply with the ethical standards of the National Committee for Research Ethics and the Helsinki Declaration on Bioethics and Human Rights (WMA Declaration of Helsinki—Ethical Principles for Medical Research Involving Human Subjects, 2013).

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Gaidash, A.A., Krut’ko, V.K., Kulak, A.I. et al. Structure of the Peritenons of the Paravertebral Tendons Treated with Hyaluronic Acid. Biol Bull Rev 13, 559–571 (2023). https://doi.org/10.1134/S2079086423060075

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  • DOI: https://doi.org/10.1134/S2079086423060075

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