European Society of Biomechanics S.M. Perren Award 2010: An adaptation mechanism for fibrous tissue to sustained shortening

Journal of Biomechanics

Volumn 43, Issue 16, 2010, Pages 3168-3176

  Foolen, Jasper ^a   Van Donkelaar, Corrinus C ^a   Soekhradj Soechit, Sarita ^a   Ito, Keita ^a  

^a EINDHOVEN UNIVERSITY OF TECHNOLOGY   (Netherlands)

Author keywords

Collagen; Cycloheximide; Cytochalasin; Mechanics; Tissue remodeling

Indexed keywords

ACTIN FILAMENT; ADAPTATION MECHANISM; ADAPTATION PROCESS; ADAPTIVE RESPONSE; CELL CONTRACTION; CHICK EMBRYO; COLLAGEN FIBER; CYCLOHEXIMIDES; CYTOCHALASIN; DEVELOPMENTAL STAGE; EQUILIBRIUM STATE; FIBROUS TISSUE; FORCE-STRAIN CURVES; IN-VITRO; MECHANICAL ENVIRONMENT; MECHANICAL EQUILIBRIUM; MECHANICAL STATE; MULTI-PHOTON MICROSCOPY; PROTEIN SYNTHESIS; RESIDUAL TISSUES; TIME POINTS; TISSUE REMODELING;

BIOMECHANICS; COLLAGEN; HIP PROSTHESES; MULTIPHOTON PROCESSES; VISUALIZATION;

TISSUE;

COLLAGEN FIBER; CYCLOHEXIMIDE; CYTOCHALASIN D;

ACTIN FILAMENT; ADAPTIVE BEHAVIOR; ANIMAL TISSUE; ARTICLE; CHICK EMBRYO; CONTROLLED STUDY; EMBRYO; FIBROUS TISSUE; IN VITRO STUDY; MULTIPHOTON MICROSCOPY; NONHUMAN; PERIOSTEUM; PRIORITY JOURNAL; PROTEIN SYNTHESIS; TISSUE REGENERATION; TISSUE TYPES;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; AWARDS AND PRIZES; BIOMECHANICS; CHICK EMBRYO; COLLAGEN; CONNECTIVE TISSUE; EUROPE; MICROFILAMENTS; PERIOSTEUM; SOCIETIES, SCIENTIFIC; STRESS, MECHANICAL;

EID: 78549280473     PISSN: 00219290     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jbiomech.2010.07.040     Document Type: Article

References (63)

1. Abreu E.L., Leigh D., Derwin K.A. Effect of altered mechanical load conditions on the structure and function of cultured tendon fascicles. J. Orthop. Res. 2008, 26:364-373.
2. Arnoczky S.P., Lavagnino M., Egerbacher M., Caballero O., Gardner K. Matrix metalloproteinase inhibitors prevent a decrease in the mechanical properties of stress-deprived tendons: an in vitro experimental study. Am. J. Sports Med. 2007, 35:763-769.
3. Augustin G., Antabak A., Davila S. The periosteum part 1: anatomy, histology and molecular biology. Injury 2007, 38:1115-1130.
4. Balguid A., Rubbens M.P., Mol A., Bank R.A., Bogers A.J., van Kats J.P., de Mol B.A., Baaijens F.P., Bouten C.V. The role of collagen cross-links in biomechanical behavior of human aortic heart valve leaflets-relevance for tissue engineering. Tissue Eng. 2007, 13:1501-1511.
5. Bank R.A., Beekman B., Verzijl N., de Roos J.A., Sakkee A.N., TeKoppele J.M. Sensitive fluorimetric quantitation of pyridinium and pentosidine crosslinks in biological samples in a single high-performance liquid chromatographic run. J. Chromatogr. B Biomed. Sci. Appl. 1997, 703:37-44.
6. Bank R.A., Jansen E.J., Beekman B., te Koppele J.M. Amino acid analysis by reverse-phase high-performance liquid chromatography: improved derivatization and detection conditions with 9-fluorenylmethyl chloroformate. Anal. Biochem. 1996, 240:167-176.
7. Bell E., Ivarsson B., Merrill C. Production of a tissue-like structure by contraction of collagen lattices by human fibroblasts of different proliferative potential in vitro. Proc. Natl. Acad Sci. USA 1979, 76:1274-1278.
8. Bertram J.E., Polevoy Y., Cullinane D.M. Mechanics of avian fibrous periosteum: tensile and adhesion properties during growth. Bone 1998, 22:669-675.
9. Binkley J.M., Peat M. The effects of immobilization on the ultrastructure and mechanical properties of the medial collateral ligament of rats. Clin. Orthop. Relat. Res. 1986, 301-308.
10. Boerboom R.A., Krahn K.N., Megens R.T., van Zandvoort M.A., Merkx M., Bouten C.V. High resolution imaging of collagen organisation and synthesis using a versatile collagen specific probe. J. Struct. Biol. 2007, 159:392-399.
11. Brown R.A., Prajapati R., McGrouther D.A., Yannas I.V., Eastwood M. Tensional homeostasis in dermal fibroblasts: mechanical responses to mechanical loading in three-dimensional substrates. J. Cell Physiol. 1998, 175:323-332.
12. Cesarone C.F., Bolognesi C., Santi L. Improved microfluorometric DNA determination in biological material using 33258 Hoechst. Anal. Biochem. 1979, 100:188-197.
13. Church L.E., Johnson L.C. Growth of long bones in the chicken. Rates of growth in length and diameter of the humerus, tibia and metatarsus. Am. J. Anat. 1964, 114:521-538.
14. Curwin S.L., Vailas A.C., Wood J. Immature tendon adaptation to strenuous exercise. J. Appl. Physiol 1988, 65:2297-2301.
15. Dodd N.J., Schor S.L., Rushton G. The effects of a collagenous extracellular matrix on fibroblast membrane organization. An ESR spin label study. Exp. Cell Res. 1982, 141:421-431.
16. Eastwood M., Porter R., Khan U., McGrouther G., Brown R. Quantitative analysis of collagen gel contractile forces generated by dermal fibroblasts and the relationship to cell morphology. J. Cell Physiol. 1996, 166:33-42.
17. Ellsmere J.C., Khanna R.A., Lee J.M. Mechanical loading of bovine pericardium accelerates enzymatic degradation. Biomaterials 1999, 20:1143-1150.
18. Emans P.J., Surtel D.A., Frings E.J., Bulstra S.K., Kuijer R. In vivo generation of cartilage from periosteum. Tissue Eng. 2005, 11:369-377.
19. Farndale R.W., Buttle D.J., Barrett A.J. Improved quantitation and discrimination of sulphated glycosaminoglycans by use of dimethylmethylene blue. Biochim. Biophys. Acta 1986, 883:173-177.
20. Feng Z., Ishibashi M., Nomura Y., Kitajima T., Nakamura T. Constraint stress, microstructural characteristics, and enhanced mechanical properties of a special fibroblast-embedded collagen construct. Artif. Organs 2006, 30:870-877.
21. Feng Z., Tateishi Y., Nomura Y., Kitajima T., Nakamura T. Construction of fibroblast-collagen gels with orientated fibrils induced by static or dynamic stress: toward the fabrication of small tendon grafts. J. Artif. Organs 2006, 9:220-225.
22. Foolen J., van Donkelaar C.C., Murphy P., Huiskes R., Ito K. Residual periosteum tension is insufficient to directly modulate bone growth. J. Biomech. 2009, 42:152-157.
23. Foolen J., van Donkelaar C.C., Nowlan N., Murphy P., Huiskes R., Ito K. Collagen orientation in periosteum and perichondrium is aligned with preferential directions of tissue growth. J. Orthop. Res. 2008, 26:1263-1268.
24. Grinnell F., Lamke C.R. Reorganization of hydrated collagen lattices by human skin fibroblasts. J. Cell Sci. 1984, 66:51-63.
25. Grinnell F., Zhu M., Carlson M.A., Abrams J.M. Release of mechanical tension triggers apoptosis of human fibroblasts in a model of regressing granulation tissue. Exp. Cell Res. 1999, 248:608-619.
26. Guidry C. Extracellular matrix contraction by fibroblasts: peptide promoters and second messengers. Cancer Metastasis Rev. 1992, 11:45-54.
27. Guidry C., Grinnell F. Studies on the mechanism of hydrated collagen gel reorganization by human skin fibroblasts. J. Cell Sci. 1985, 79:67-81.
28. Guidry C., Grinnell F. Contraction of hydrated collagen gels by fibroblasts: evidence for two mechanisms by which collagen fibrils are stabilized. Collagen Relat. Res. 1987, 6:515-529.
29. Guidry C., Hohn S., Hook M. Endothelial cells secrete a factor that promotes fibroblast contraction of hydrated collagen gels. J. Cell Biol. 1990, 110:519-528.
30. Hamburger V., Hamilton H.L. A series of normal stages in the development of the chick embryo. 1951. Dev. Dyn. 1992, 195:231-272.
31. Harris A.K., Stopak D., Wild P. Fibroblast traction as a mechanism for collagen morphogenesis. Nature 1981, 290:249-251.
32. Henshaw D.R., Attia E., Bhargava M., Hannafin J.A. Canine ACL fibroblast integrin expression and cell alignment in response to cyclic tensile strain in three-dimensional collagen gels. J. Orthop. Res. 2006, 24:481-490.
33. Huang C., Yannas I.V. Mechanochemical studies of enzymatic degradation of insoluble collagen fibers. J. Biomed. Mater. Res. 1977, 11:137-154.
34. Huang D., Chang T.R., Aggarwal A., Lee R.C., Ehrlich H.P. Mechanisms and dynamics of mechanical strengthening in ligament-equivalent fibroblast-populated collagen matrices. Ann. Biomed. Eng. 1993, 21:289-305.
35. Kim S.G., Akaike T., Sasagaw T., Atomi Y., Kurosawa H. Gene expression of type I and type III collagen by mechanical stretch in anterior cruciate ligament cells. Cell Struct. Funct. 2002, 27:139-144.
36. Krahn K.N., Bouten C.V.C., van Tuijl S., van Zandvoort M.A.M.J., Merkx M. Fluorescently labeled collagen binding proteins allow specific visualization of collagen in tissues and live cell culture. Anal. Biochem. 2006, 350:177-185.
37. Lavagnino M., Arnoczky S.P. In vitro alterations in cytoskeletal tensional homeostasis control gene expression in tendon cells. J. Orthop. Res. 2005, 23:1211-1218.
38. Loitz B.J., Zernicke R.F., Vailas A.C., Kody M.H., Meals R.A. Effects of short-term immobilization versus continuous passive motion on the biomechanical and biochemical properties of the rabbit tendon. Clin. Orthop. Relat. Res. 1989, 265-271.
39. Meshel A.S., Wei Q., Adelstein R.S., Sheetz M.P. Basic mechanism of three-dimensional collagen fibre transport by fibroblasts. Nat. Cell Biol. 2005, 7:157-164.
40. Michna H. Morphometric analysis of loading-induced changes in collagen-fibril populations in young tendons. Cell Tissue Res. 1984, 236:465-470.
41. Michna H., Hartmann G. Adaptation of tendon collagen to exercise. Int. Orthop. 1989, 13:161-165.
42. Mochitate K., Pawelek P., Grinnell F. Stress relaxation of contracted collagen gels: disruption of actin filament bundles, release of cell surface fibronectin, and down-regulation of DNA and protein synthesis. Exp. Cell Res. 1991, 193:198-207.
43. Nabeshima Y., Grood E.S., Sakurai A., Herman J.H. Uniaxial tension inhibits tendon collagen degradation by collagenase in vitro. J. Orthop. Res. 1996, 14:123-130.
44. Nakagawa S., Pawelek P., Grinnell F. Long-term culture of fibroblasts in contracted collagen gels: effects on cell growth and biosynthetic activity. J. Invest Dermatol. 1989, 93:792-798.
45. O'Driscoll S.W., Recklies A.D., Poole A.R. Chondrogenesis in periosteal explants. An organ culture model for in vitro study. J. Bone Joint Surg. Am. 1994, 76:1042-1051.
46. Parsons M., Kessler E., Laurent G.J., Brown R.A., Bishop J.E. Mechanical load enhances procollagen processing in dermal fibroblasts by regulating levels of procollagen C-proteinase. Exp. Cell Res. 1999, 252:319-331.
47. Petroll W.M., Vishwanath M., Ma L. Corneal fibroblasts respond rapidly to changes in local mechanical stress. Invest. Ophthalmol. Vis. Sci. 2004, 45:3466-3474.
48. Popowics T.E., Zhu Z., Herring S.W. Mechanical properties of the periosteum in the pig, Sus scrofa. Arch. Oral Biol. 2002, 47:733-741.
49. Puxkandl R., Zizak I., Paris O., Keckes J., Tesch W., Bernstorff S., Purslow P., Fratzl P. Viscoelastic properties of collagen: synchrotron radiation investigations and structural model. Philos. Trans. R. Soc. London B Biol. Sci. 2002, 357:191-197.
50. Rath N.C., Huff G.R., Huff W.E., Balog J.M. Factors regulating bone maturity and strength in poultry. Poult. Sci. 2000, 79:1024-1032.
51. Ravetto, A., Kock, L.M., Donkelaar, C.C., Ito, K., 2009. Mechanical stimulation enhances collagen synthesis in periosteum-derived cartilage. In: Proceedings of the ASME 2009 Summer Bioengineering Conference SBC2009-204245.
52. Robins S.P., Duncan A., Wilson N., Evans B.J. Standardization of pyridinium crosslinks, pyridinoline and deoxypyridinoline, for use as biochemical markers of collagen degradation. Clin. Chem. 1996, 42:1621-1626.
53. Ruberti J.W., Hallab N.J. Strain-controlled enzymatic cleavage of collagen in loaded matrix. Biochem. Biophys. Res. Commun. 2005, 336:483-489.
54. Sawhney R.K., Howard J. Slow local movements of collagen fibers by fibroblasts drive the rapid global self-organization of collagen gels. J. Cell Biol. 2002, 157:1083-1091.
55. Stopak D., Harris A.K. Connective tissue morphogenesis by fibroblast traction. I. Tissue culture observations. Dev. Biol. 1982, 90:383-398.
56. Thomopoulos S., Fomovsky G.M., Holmes J.W. The development of structural and mechanical anisotropy in fibroblast populated collagen gels. J. Biomech. Eng. 2005, 127:742-750.
57. Tomasek J.J., Haaksma C.J., Eddy R.J., Vaughan M.B. Fibroblast contraction occurs on release of tension in attached collagen lattices: dependency on an organized actin cytoskeleton and serum. Anat. Rec. 1992, 232:359-368.
58. Wakatsuki T., Elson E.L. Reciprocal interactions between cells and extracellular matrix during remodeling of tissue constructs. Biophys. Chem. 2003, 100:593-605.
59. Wang J.H.C., Jia F., Gilbert T.W., Woo S.L.Y. Cell orientation determines the alignment of cell-produced collagenous matrix. J. Biomech. 2003, 36:97-102.
60. Yamamoto E., Iwanaga W., Miyazaki H., Hayashi K. Effects of static stress on the mechanical properties of cultured collagen fascicles from the rabbit patellar tendon. J. Biomech. Eng. 2002, 124:85-93.
61. Yamamoto N., Ohno K., Hayashi K., Kuriyama H., Yasuda K., Kaneda K. Effects of stress shielding on the mechanical properties of rabbit patellar tendon. J. Biomech. Eng. 1993, 115:23-28.
62. Yang G., Crawford R.C., Wang J.H.C. Proliferation and collagen production of human patellar tendon fibroblasts in response to cyclic uniaxial stretching in serum-free conditions. J. Biomech. 2004, 37:1543-1550.
63. Zhu Y.K., Umino T., Liu X.D., Wang H.J., Romberger D.J., Spurzem J.R., Rennard S.I. Contraction of fibroblast-containing collagen gels: initial collagen concentration regulates the degree of contraction and cell survival. In Vitro Cell Dev. Biol. Anim 2001, 37:10-16.