Re-establishment of cytoskeletal tensional homeostasis in lax tendons occurs through an actin-mediated cellular contraction of the extracellular matrix

Journal of Orthopaedic Research

Volumn 30, Issue 11, 2012, Pages 1695-1701

  Gardner, Keri ^a   Lavagnino, Michael ^a   Egerbacher, Monika ^b   Arnoczky, Steven P ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b UNIVERSITY OF VETERINARY MEDICINE   (Austria)

Author keywords

contraction; cytoskeleton; MMP 13; smooth muscle actin; tendon cells

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; COLLAGENASE; CYTOCHALASIAN D; MYCOTOXIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL CULTURE; CYTOSKELETON; EXTRACELLULAR MATRIX; HOMEOSTASIS; LAX TENDON; NONHUMAN; PRIORITY JOURNAL; RAT; TENDON;

ACTIN CYTOSKELETON; ACTINS; ANIMALS; EXTRACELLULAR MATRIX; HOMEOSTASIS; MATRIX METALLOPROTEINASE 13; RATS; RATS, SPRAGUE-DAWLEY; TAIL; TENDONS;

EID: 84867233142     PISSN: 07360266     EISSN: 1554527X     Source Type: Journal    
DOI: 10.1002/jor.22131     Document Type: Article

References (44)

1. Banes AJ, Tsuzali M, Yamamoto J, et al. 1995. Mechanoreception at the cellular level: the detection, interpretation, and diversity of responses to mechanical signals. Biochem Cell Biol 73: 349-365.
2. Chen CS, Ingber DE., 1999. Tensegrity and mechanoregulation: from skeleton to cytoskeleton. Osteoarthritis Cartilage 7: 81-94.
3. Ingber DE., 1997. Tensegrity: the architectural basis of cellular mechanotransduction. Annu Rev Physiol 59: 575-599.
4. Wang N, Tytell JD, Ingber DE., 2009. Mechanotransduction at a distance: mechanically coupling the extracellular matrix with the nucleus. Nat Rev Mol Cell Biol 10: 75-82.
5. Arora PD, McCulloch CA., 1994. Dependence of collagen remodeling on alpha-smooth muscle actin expression by fibroblasts. J Cell Physiol 159: 161-175.
6. Brown RA, Prajapati R, McGrouther DA, et al. 1998. Tensional homeostasis in dermal fibroblasts: mechanical responses to mechanical loading in three-dimensional substrates. J Cell Physiol 175: 322-332.
7. Lavagnino M, Arnoczky SP., 2005. In vitro alterations in cytoskeletal tensional homeostasis control gene expression in tendon cells. J Orthop Res 23: 1211-1218.
8. Sawhney RK, Howard J., 2004. Molecular dissection of the fibroblast traction machinery. Cell Motil Cytoskeleton 58: 175-185.
9. Arnoczky SP, Lavagnino M, Egerbacher M, et al. 2008. Loss of homeostatic strain alters mechanostat 'set point' of tendon cells in vitro. Clin Orthop Relat Res 466: 1583-1591.
10. Arnoczky SP, Tian T, Lavagnino M, et al. 2004. Ex vivo static tensile loading inhibits MMP-1 expression in rat tail tendon cells through a cytoskeletally based mechanotransduction mechanism. J Orthop Res 22: 328-333.
11. Egerbacher M, Arnoczky SP, Caballero O, et al. 2008. Loss of homeostatic tension induces apoptosis in tendon cells. Clin Orthop Relat Res 466: 1562-1568.
12. Lavagnino M, Arnoczky SP, Egerbacher M, et al. 2006. Isolated fibrillar damage in tendons stimulates local collagenase mRNA expression protein synthesis. J Biomech 39: 2355-2362.
13. Lavagnino M, Arnoczky SP, Tian T, et al. 2003. Effect of amplitude frequency of cyclic tensile strain on the inhibition of MMP-1 mRNA expression in tendon cells: an in vitro study. Connect Tissue Res 44: 181-187.
14. Hartzel DK, Arnoczky SP, Kilfoyles SJ, et al. 2001. Myofibroblasts in the accessory ligament (distal check ligament) the deep digital flexor tendon of foals. Am J Vet Res 62: 823-827.
15. Ippolito E, Natali PG, Postacchini F, et al. 1977. Ultrastructural immunochemical evidence of actin in the tendon cells. Clin Orthop Relat Res 126: 282-284.
16. Murray MM, Spector M., 1999. Fibroblast distribution in the anteromedial bundle of the human anterior cruciate ligament: the presence of α-smooth muscle active-positive cells. J Orthop Res 17: 18-27.
17. Premdas J, Tang J-B, Warner JP, et al. 2001. The presence of smooth muscle actin in fibroblasts in the torn human rotator cuff. J Orthop Res 19: 221-228.
18. Weiler A, Unterhaiser FN, Hail J-J, et al. 2002. α-Smooth muscle actin is expressed by fibroblastic cells of the ovine anterior cruciate ligament and its free tendon graft during remodeling. J Orthop Res 20: 310-317.
19. Harris AK., 1986. Cell traction and its relationship to morphorgenesis and malignancy. Amer Zool 26: 559-560.
20. Kalson NS, Holmes DF, Kapacee Z, et al. 2010. An experimental model for studying the biomechanics of embryonic tendon: evidence that the development of mechanical properties depends on the actinomyosin machinery. Matrix Biol 29: 678-689.
21. Stopak D, Harris AK., 1982. Connective tissue morphogenesis by fibroblast traction. I. Tissue culture observations. Dev Biol 90: 383-398, 1982.
22. Stopak D, Wessells NK, Harris AK., 1985. Morphogenetic rearrangement of injected collagen in developing chicken limb buds. Proc Natl Acad Sci 82: 2804-2808.
23. Farshad M, Gerber C, Snedeker JG, et al. 2011. Structure of retracted tendons after staged repair following continuous traction. Knee Surg Sports Traumatol Arthrosc 19: 2131-2137.
24. Meyer DC, Lajtai G, von Rechenberg B, et al. 2006. Tendon retracts more than muscle in experimental chronic tears of the rotator cuff. J Bone and Jt Surg 88B: 1533-1538.
25. Murray MM, Martin SD, Martin TL, et al. 2000. Histological changes in the human anterior cruciate ligament after rupture. J Bone Jt Surg 82A: 1387-1397.
26. King GJW, Edwards P, Brant RF, et al. 1995. Intraoperative graft tensioning alters viscoelastic but not failure behaviours of rabbit medial collateral ligament autografts. J Orthop Res 13: 915-922.
27. Arnoczky SP, Lavagnino M, Egerbacher M., 2007. The mechanobiological aetiopathogenesis of tendinoptahy: is it the over-stimulation or the under-stimulation of tendon cells ? Int J Exp Path 88: 217-226.
28. Galatz LM, Charlton N, Das R, et al. 2009. Complete removal of load is detrimental to rotator cuff healing. J Shoulder Elbow Surg 18: 669-675.
29. Frost HM., 1987. Bone "mass" and the "mechanostat" A proposal. Anat Rec 219: 1-9.
30. Crisco JJ, Chelikani S, Brown RK, et al,. 1997. The effects of exercise on ligamentous stiffness in the wrist. J Hand Surg 22A: 44-48.
31. Grana WA, Muse G., 1988. The effect of exercise on laxity in the anterior cruciate ligament deficient knee. Am J Sports Med 16: 586-588.
32. Dahners LE, Banes AJ, Burridge KWT., 1986. The relationship of actin to ligament contraction. Clin Orthop 210: 246-251.
33. Cooper JA., 1987. Effects of cytochalasin and phalloidin on actin. J Cell Biol 105: 1473-1478.
34. Bruijns RHJ, Bult H., 2001. Effects of local cytochalasin D delivery on smooth muscle cell migration and on collar-induced intimal hyperplasia in the rabbit carotid artery. Br J Phamacol 134: 473-483.
35. Kinner B, Zaleska JM, Spector M., 2002. Regulation of smooth muscle actin expression and contraction in adult human mesenchymal cells. Exp Cell Res 278: 72-83.
36. 2-terminal peptide of α-smooth muscle actin inhibits force generation by the myofibroblast in vitro and in vivo. J Cell Biol 157: 657-663.
37. Brown RA., 2006. Cytomechanics in connective tissue repair and engineering. In:, Chaponnier C, Desmouliere A, Gabbiani G, editors. Tissue repair, contraction and the myofibroblast. New York: Springer; pp 7-24.
38. Clark RAF., 1996. Wound repair: overview and general considerations,. In:, Clark RAF, editor. The molecular and cell biology of wound repair, 2nd edition. New York: Plenum Press; pp 3-50.
39. Faryniarz DA, Chaponnier C, Gabbiani G, et al. 1996. Myofibroblasts in the healing laprine medial collateral ligament: possible mechanisms of contraction. J Orthop Res 14: 228-237.
40. Meller R, Schiborra F, Brandes G, et al. 2009. Postnatal maturation of tendon, cruciate ligament, meniscus and articyulr cartilage: a histological study in sheep. Ann Anat 191: 575-585.
41. Tomasek JJ, Gabbiani G, Hinz B, et al. 2002. Myofibroblasts and mechanoregulation of connective tissue remodeling. Nat Rev Mol Cell Biol 3: 349-363.
42. Ghassemifar MR, Tarnuzzer RW, Chegini N, et al. 1997. Expression of alpha-smooth muscle actin, TGF-β1 and TGFβ type II receptor during connective tissue contraction. In vitro Cell Dev Biol 33: 622-627.
43. O'Brien TD, Reeves ND, Baltzopoulos V, et al. 2010. Mechanical properties of the patellar tendon in adults and children. J Biomech 43: 1190-1195.
44. Waugh CM, Blazevich AJ, Fath F, et al. 2012. Age-related changes in mechanical properties of the Achilles tendon. J Anat 220: 144-155.