Skip to main content
SpringerLink
Log in

Effects of cyclic strain on rat tail tenocytes

  • Published:
Molecular Biology Reports Aims and scope Submit manuscript

Abstract

Cyclical mechanical strain is considered an important component in flexor tendon cell activation to prevent adhesions and enhance the healing process after tissue injury or surgery, but the biochemical events associated with this remain unclear. To address this, we examined the effects of cyclic tension on the expression of hyaluronic acid, an important lubricant and signal transducer in tendon, on its receptor (CD44), and on total glycosaminoglycan content in rat tail derived tendon fibroblasts in vitro. Tenocytes were plated on fibronectin coated silastic membranes and the cultures were held static or subjected to vacuum induced deformation for a period of 5 min once every 8 h as a model of cyclic mechanical stress. After 24 h medium and cell layers were collected for analyses by product specific ELISA, Western blot, and colorimetric dye-binding assays. Strained tenocytes produced a nearly two-fold increase in hyaluronic acid and a greater than 60% increase in CD44, but had an insignificant effect on total glycosaminoglycan content. Our results predict that high levels of strain may therefore rapidly enhance the expression of hyaluronic acid and cause, albeit still unresolved, downstream effects on CD44 activation, to influence tendon cell activity and enhance the process of tendon repair.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  1. Kubota H, Manske PR, Aoki M, Pruitt DL, Larson BJ (1996) Effect of motion and tension on injured flexor tendons in chickens. J Hand Surg [Am] 21:456–463

    Article  CAS  Google Scholar 

  2. Tanaka H, Manske PR, Pruitt DL, Larson BJ (1995) Effect of cyclic tension on lacerated flexor tendons in vitro. J Hand Surg [Am] 20:467–473

    Article  CAS  Google Scholar 

  3. Mass DP, Tuel RJ, Labarbera M, Greenwald DP (1993) Effects of constant mechanical tension on the healing of rabbit flexor tendons. Clin Orthop Relat Res 296:301–306

    PubMed  Google Scholar 

  4. Wray RC Jr, Ollinger H, Lowrey R, Weeks PM (1981) Effect of continuous load on the mechanical properties of tendon adhesions. Hand 13:92–96

    Article  PubMed  Google Scholar 

  5. Tang JB (2005) Clinical outcomes associated with flexor tendon repair. Hand Clin 21:199–210

    Article  PubMed  Google Scholar 

  6. Tammi MI, Day AJ, Turley EA (2002) Hyaluronan and homeostasis: a balancing act. J Biol Chem 277:4581–4584

    Article  CAS  PubMed  Google Scholar 

  7. Collis L, Hall C, Lange L, Ziebell M, Prestwich R, Turley EA (1998) Rapid hyaluronan uptake is associated with enhanced motility: implications for an intracellular mode of action. FEBS Lett 440:444–449

    Article  CAS  PubMed  Google Scholar 

  8. Evanko SP, Wight TN (1999) Intracellular localization of hyaluronan in proliferating cells. J Histochem Cytochem 47:1331–1342

    CAS  PubMed  Google Scholar 

  9. Yuzawa K (1985) Experimental studies on the healing and restoration of gliding function of the injured digital flexor tendon, part 9: the use of drugs to prevent adhesion formation of the injured tendon. Nippon Seikeigeka Gakkai Zasshi 59:1107–1118

    CAS  PubMed  Google Scholar 

  10. Chen Z, Gu J (1995) Experimental research on using macromolecule sodium hyaluronate to prevent flexior tendon adhesion. Zhonghua Wai Ke Za Zhi 33:526–528

    CAS  PubMed  Google Scholar 

  11. Karakurum G, Buyukbebeci O, Kalender M, Gulec A (2003) Seprafilm interposition for preventing adhesion formation after tenolysis, an experimental study on the chicken flexor tendons. J Surg Res 113:195–200

    Article  PubMed  Google Scholar 

  12. Thomas SC, Jones LC, Hungerford DS (1986) Hyaluronic acid and its effect on postoperative adhesions in the rabbit flexor tendon, a preliminary look. Clin Orthop Relat Res 206:281–289

    CAS  PubMed  Google Scholar 

  13. Xu J, Gu Y, Wang H (1995) Experimental study of sodium hyaluronate products on prevention of tendon adhesion. Zhonghua Wai Ke Za Zhi 33:529–531

    CAS  PubMed  Google Scholar 

  14. Menderes A, Mola F, Tayfur V, Vayvada H, Barutcu A (2004) Prevention of peritendinous adhesions following flexor tendon injury with seprafilm. Ann Plast Surg 53:560–564

    Article  PubMed  Google Scholar 

  15. Wiig M, Abrahamsson SO, Lundborg G (1996) Effects of hyaluronan on cell proliferation and collagen synthesis: a study of rabbit flexor tendons in vitro. J Hand Surg [Am] 21:599–604

    Article  CAS  Google Scholar 

  16. Weiss C, Levy HJ, Denlinger J, Suros JM, Weiss HE (1986) The role of Na-hylan in reducing postsurgical tendon adhesions. Bull Hosp Jt Dis Orthop Inst 46:9–15

    CAS  PubMed  Google Scholar 

  17. Amiel D, Ishizue K, Billings E Jr, Wiig M, Vande Berg J, Akeson WH et al (1989) Hyaluronan in flexor tendon repair. J Hand Surg [Am] 14:837–843

    Article  CAS  Google Scholar 

  18. Gaughan EM, Nixon AJ, Krook LP, Yeager AE, Mann KA, Mohammed H et al (1991) Effects of sodium hyaluronate on tendon healing and adhesion formation in horses. Am J Vet Res 52:764–773

    CAS  PubMed  Google Scholar 

  19. St Onge R, Weiss C, Denlinger JL, Balazs EA (1980) A preliminary assessment of Na- hyaluronate injection into “no man’s land” for primary flexor tendon repair. Clin Orthop Relat Res 146:269–275

    PubMed  Google Scholar 

  20. Strickland JW (2000) Development of flexor tendon surgery: twenty-five years of progress. J Hand Surg [Am] 25:214–235

    Article  CAS  Google Scholar 

  21. Hagberg L (1992) Exogenous hyaluronate as an adjunct in the prevention of adhesions after flexor tendon surgery: a controlled clinical trial. J Hand Surg [Am] 17:132–136

    Article  CAS  Google Scholar 

  22. Taras JS, Lamb MJ (1999) Treatment of flexor tendon injuries: surgeons’ perspective. J Hand Ther 12:141–148

    CAS  PubMed  Google Scholar 

  23. Pankov R, Yamada KM (2002) Fibronectin at a glance. J Cell Sci 115:3861–3863

    Article  CAS  PubMed  Google Scholar 

  24. Banes AJ, Tsuzaki M, Hu P, Brigman B, Brown T, Almekinders L et al (1995) PDGF- BB, IGF-I and mechanical load stimulate DNA synthesis in avian tendon fibroblasts in vitro. J Biomech 28:1505–1513

    Article  CAS  PubMed  Google Scholar 

  25. Arnoczky SP, Tian T, Lavagnino M, Gardner K, Schuler P, Morse P (2002) Activation of stress-activated protein kinases (SAPK) in tendon cells following cyclic strain: the effects of strain frequency, strain magnitude, and cytosolic calcium. J Orthop Res 20:947–952

    Article  CAS  PubMed  Google Scholar 

  26. Zeichen J, van Griensven M, Bosch U (2000) The proliferative response of isolated human tendon fibroblasts to cyclic biaxial mechanical strain. Am J Sports Med 28:888–892

    CAS  PubMed  Google Scholar 

  27. Qin TW, Yang ZM, Wu ZZ, Xie HQ, Qin J, Cai SX (2005) Adhesion strength of human tenocytes to extracellular matrix component-modified poly(dl-lactide-co-glycolide) substrates. Biomaterials 26:6635–6642

    Article  CAS  PubMed  Google Scholar 

  28. Koob TJ (2002) Biomimetic approaches to tendon repair. Comp Biochem Physiol A Mol Integr Physiol 133:1171–1192

    Article  PubMed  Google Scholar 

  29. Yamamoto E, Iwanaga W, Miyazaki H, Hayashi K (2002) Effects of static stress on the mechanical properties of cultured collagen fascicles from the rabbit patellar tendon. J Biomech Eng 124:85–93

    Article  PubMed  Google Scholar 

  30. Ralphs JR, Waggett AD, Benjamin M (2002) Actin stress fibres and cell–cell adhesion molecules in tendons: organisation in vivo and response to mechanical loading of tendon cells in vitro. Matrix Biol 21:67–74

    Article  CAS  PubMed  Google Scholar 

  31. Hannafin JA, Arnoczky SP, Hoonjan A, Torzilli PA (1995) Effect of stress deprivation and cyclic tensile loading on the material and morphologic properties of canine flexor digitorum profundus tendon: an in vitro study. J Orthop Res 13:907–914

    Article  CAS  PubMed  Google Scholar 

  32. Koob TJ, Clark PE, Hernandez DJ, Thurmond FA, Vogel KG (1992) Compression loading in vitro regulates proteoglycan synthesis by tendon fibrocartilage. Arch Biochem Biophys 298:303–312

    Article  CAS  PubMed  Google Scholar 

  33. Slack C, Bradley G, Beaumont B, Poole A, Flint M (1986) Changes in the morphology and synthetic activity of cultured rat tail tendon. Cell Tissue Res 245:359–368

    Article  CAS  PubMed  Google Scholar 

  34. Slack C, Flint MH, Thompson BM (1984) The effect of tensional load on isolated embryonic chick tendons in organ culture. Connect Tissue Res 12:229–247

    Article  CAS  PubMed  Google Scholar 

  35. Gillard GC, Reilly HC, Bell-Booth PG, Flint MH (1979) The influence of mechanical forces on the glycosaminoglycan content of the rabbit flexor digitorum profundus tendon. Connect Tissue Res 7:37–46

    Article  CAS  PubMed  Google Scholar 

  36. Woo SL, Gomez MA, Amiel D, Ritter MA, Gelberman RH, Akeson WH (1981) The effects of exercise on the biomechanical and biochemical properties of swine digital flexor tendons. J Biomech Eng 103:51–56

    Article  CAS  PubMed  Google Scholar 

  37. Malaviya P, Butler DL, Boivin GP, Smith FN, Barry FP, Murphy JM et al (2000) An in vivo model for load-modulated remodeling in the rabbit flexor tendon. J Orthop Res 18:116–125

    Article  CAS  PubMed  Google Scholar 

  38. Buchanan CI, Marsh RL (2002) Effects of exercise on the biomechanical, biochemical and structural properties of tendons. Comp Biochem Physiol A Mol Integr Physiol 133:1101–1107

    Article  PubMed  Google Scholar 

  39. Packer DL, Dombi GW, Yu PY, Zidel P, Sullivan WG (1994) An in vitro model of fibroblast activity and adhesion formation during flexor tendon healing. J Hand Surg [Am] 19:769–776

    Article  CAS  Google Scholar 

  40. Falk K, Lindman B, Bengmark S, Larsson K, Holmdahl L (2001) Prevention of adhesions by surfactants and cellulose derivatives in mice. Eur J Surg 167:136–141

    Article  CAS  PubMed  Google Scholar 

  41. Khitrina GV (1968) The effect of hyaluronidase on adhesive processes in the pleural cavity under experimental conditions. Biull Eksp Biol Med 65:115–117

    CAS  PubMed  Google Scholar 

  42. Stoehr BJ, Gutierrez JE, Close AS (1966) Effect of intraperitoneal hyaluronidase on the reformation of intestinal adhesions. Am J Surg 111:881–883

    Article  CAS  PubMed  Google Scholar 

  43. Adamian LV, Mynbaev OA, Strugatskii VM (1995) An experimental validation of hyaluronidase electrophoresis for the prevention of postoperative adhesions. Vopr Kurortol Fizioter Lech Fiz Kult 3:18–20

    PubMed  Google Scholar 

  44. Zimmerman E, Geiger B, Addadi L (2002) Initial stages of cell–matrix adhesion can be mediated and modulated by cell-surface hyaluronan. Biophys J 82:1848–1857

    Article  CAS  PubMed  Google Scholar 

  45. Yang C, Amadio PC, Sun YL, Zhao C, Zobitz ME, An KN (2004) Tendon surface modification by chemically modified HA coating after flexor digitorum profundus tendon repair. J Biomed Mater Res B Appl Biomater 68:15–20

    Article  PubMed  CAS  Google Scholar 

  46. Kelly MA, Moskowitz RW, Lieberman JR (2004) Hyaluronan therapy: looking toward the future. Am J Orthop 33(Suppl 2):23–28

    PubMed  Google Scholar 

  47. Pitt WG, Morris RN, Mason ML, Hall MW, Luo Y, Prestwich GD (2004) Attachment of hyaluronan to metallic surfaces. J Biomed Mater Res A 68:95–106

    Article  PubMed  CAS  Google Scholar 

  48. Bulpitt P, Aeschlimann D (1999) New strategy for chemical modification of hyaluronic acid: preparation of functionalized derivatives and their use in the formation of novel biocompatible hydrogels. J Biomed Mater Res 47:152–169

    Article  CAS  PubMed  Google Scholar 

  49. Tsai SW, Fang JF, Yang C, Chen JH, Su LT, Jan SH (2005) Preparation and evaluation of a hyaluronate-collagen film for preventing post-surgical adhesion. J Int Med Res 33:68–76

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

These studies were supported by a grant from the Plastic Surgery Educational Foundation. We are especially grateful to Drs. Martijn van Griensven, Michael Skutek, and Tanja Barkhausen (Hannover Medical School, Germany) for their technical advice on tendon fibroblast cultures.

Author information

Authors and Affiliations

  1. Department of Surgery (Section of Plastic Surgery), Yale University School of Medicine, P.O. Box 208041, New Haven, CT, 06520-8041, USA

    Richard J. Crockett, Michael Centrella, Thomas L. McCarthy & J. Grant Thomson

Authors
  1. Richard J. Crockett
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Michael Centrella
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Thomas L. McCarthy
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. J. Grant Thomson
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to J. Grant Thomson.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Crockett, R.J., Centrella, M., McCarthy, T.L. et al. Effects of cyclic strain on rat tail tenocytes. Mol Biol Rep 37, 2629–2634 (2010). https://doi.org/10.1007/s11033-009-9788-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11033-009-9788-8

Keywords

Search

Navigation