Stretch-activated force shedding, force recovery, and cytoskeletal remodeling in contractile fibroblasts

Journal of Biomechanics

Volumn 41, Issue 14, 2008, Pages 2964-2971

  Nekouzadeh, Ali ^a   Pryse, Kenneth M ^b   Elson, Elliot L ^b   Genin, Guy M ^b  

^a WASHINGTON UNIVERSITY IN ST LOUIS   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Active cellular mechanics; Myofibroblasts; Stretch activated remodeling

Indexed keywords

ABS RESINS; CALCIUM; CELL CULTURE; FIBERS; FIBROBLASTS; NETWORK PROTOCOLS; SENSOR NETWORKS;

ACTIN FILAMENTS; ACTIVE CELLULAR MECHANICS; CYTOSKELETAL; FIBER NETWORKS; FORCE RECOVERY; MECHANICAL FORCES; MYOFIBROBLASTS; STRESS FIBERS; STRETCH-ACTIVATED REMODELING;

STRESSES;

CALCIUM;

ACTIN FILAMENT; ANIMAL CELL; ARTICLE; CYTOSKELETON; DEPOLYMERIZATION; FIBROBLAST; FORCE; MUSCLE CONTRACTION; MYOFIBROBLAST; NONHUMAN; PRIORITY JOURNAL; TENSION;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; CALCIUM SIGNALING; CELLS, CULTURED; CHICK EMBRYO; CYTOSKELETON; EXTRACELLULAR MATRIX; FIBROBLASTS; HUMANS; MECHANOTRANSDUCTION, CELLULAR; MUSCLE CONTRACTION; MYOBLASTS; STRESS, MECHANICAL;

EID: 53149121240     PISSN: 00219290     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jbiomech.2008.07.033     Document Type: Article

References (40)

1. Brown R.A., Prajapati R., McGrouther D.A., Yannas I.V., and Eastwood M. Tensional homeostasis in dermal fibroblasts: mechanical responses to mechanical loading in three-dimensional substrates. Journal of Cell Physiology 175 3 (1998) 323-332
2. Chrzanowska-Wodnicka M., and Burridge K. Rho-stimulated contractility drives the formation of stress fibers and focal adhesions. Journal of Cell Biology 133 6 (1996) 1403-1415
3. Costa K.D., Hucker W.J., and Yin F.C. Buckling of actin stress fibers: a new wrinkle in the cytoskeletal tapestry. Cell Motility and the Cytoskeleton 52 4 (2002) 266-274
4. Deshpande V.S., McMeeking R.M., and Evans A.G. A bio-chemo-mechanical model for cell contractility. Proceedings of the National. Academy of Sciences of the United States of America 103 38 (2006) 14015-14020
5. Dugina V., Fontao L., Chaponnier C., Vasiliev J., and Gabbiani G. Focal adhesion features during myofibroblastic differentiation are controlled by intracellular and extracellular factors. Journal of Cell Science 114 Pt 18 (2001) 3285-3296
6. Engvall E., Hessle H., and Klier G. Molecular assembly, secretion, and matrix deposition of type VI collagen. Journal of Cell Science 102 3 (1986) 703-710
7. Gabbiani G. The role of contractile proteins in wound healing and fibrocontractive diseases. Methods and Achievements in Experimental Pathology 9 (1979) 187-206
8. Genin G.M., and Hutchinson J.W. Composite laminates in plane stress: constitutive modelling and stress redistribution due to matrix cracking. Journal of the American Ceramic Society 80 5 (1997) 1245-1255
9. Griffith L.G., and Swartz M.A. Capturing complex 3D tissue physiology in vitro. Nature Reviews Molecular Cell Biology 7 3 (2006) 211-224
10. Guinier A. X-Ray Diffraction: In Crystals, Imperfect Crystals, and Amorphous Bodies (1994), Dover, New York
11. He Y., and Grinnell F. Stress relaxation of fibroblasts activates a cyclic AMP signaling pathway. Journal of Cell Biology 126 2 (1994) 457-464
12. Hinz B., and Gabbiani G. Mechanisms of force generation and transmission by myofibroblasts. Current Opinion in Biotechnology 14 5 (2003) 538-546
13. Iba T., and Sumpio B.E. Morphological response of human endothelial cells subjected to cyclic strain in vitro. Microvascular Research 42 3 (1991) 245-254
14. Kolodney M.S., and Elson E.L. Contraction due to microtubule disruption is associated with increased phosphorylation of myosin regulatory light chain. Proceedings of the National Academy of Sciencesof the United States of America 92 22 (1995) 10252-10256
15. Kolodney M.S., and Wysolmerski R.B. Isometric contraction by fibroblasts and endothelial cells in tissue culture: a quantitative study. Journal of Cell Biology 117 1 (1992) 73-82
16. Kreis T.E., and Birchmeier W. Stress fiber sarcomeres of fibroblasts are contractile. Cell 22 2 Pt 2 (1980) 555-561
17. Marquez J.P. Fourier analysis and automated measurement of cell and fiber angular orientation distributions. International Journal of Solids and Structures 43 21 (2005) 6413-6423
18. Marquez J.P., Genin G.M., Zahalak G.I., and Elson E.L. The relationship between cell and tissue strain in three-dimensional bio-artificial tissues. Biophysical Journal 88 2 (2005) 778-789
19. Marquez J.P., Genin G.M., Zahalak G.I., and Elson E.L. Thin bio-artificial tissues in plane stress: the relationship between cell and tissue strain, and an improved constitutive model. Biophysical Journal 88 2 (2005) 765-777
20. Marquez J.P., Genin G.M., Pryse K.M., and Elson E.L. Cellular and matrix contributions to tissue construct stiffness increase with cellular concentration. Annals of Biomedical Engineering 34 9 (2006) 1475-1482
21. Mott R.E., and Helmke B.P. Mapping the dynamics of shear stress-induced structural changes in endothelial cells. American Journal of Physiology-Cell Physiology 293 5 (2007) C1616-C1626
22. Nekouzadeh A., Genin G.M., Bayly P.V., and Elson E.L. Wave motion in relaxation-testing of nonlinear elastic media. Proceedings of the Royal Society A 461 (2005) 1599-1626
23. Nekouzadeh A., Pryse K.M., Elson E.L., and Genin G.M. A simplified approach to quasi-linear viscoelastic modeling. Journal of Biomechanics 40 14 (2007) 3070-3078
24. Nobe H., Nobe K., and Paul R.J. Fibroblast fiber contraction: role of C and Rho kinase in activation by thromboxane A2. American Journal of Physiology Cell Physiology 285 6 (2003) C1411-C1419
25. Parizi M., Howard E.W., and Tomasek J.J. Regulation of LPA-promoted myofibroblast contraction: role of Rho, myosin light chain kinase, and myosin light chain phosphatase. Experimental Cell Research 254 2 (2000) 210-220
26. Prajapati R.T., Chavally-Mis B., Herbage D., Eastwood M., and Brown R.A. Mechanical loading regulates protease production by fibroblasts in three-dimensional collagen substrates. Wound Repair and Regeneration 8 3 (2000) 226-237
27. Pryse K.M., Nekouzadeh A., Genin G.M., Elson E.L., and Zahalak G.I. Incremental mechanics of collagen gels: new experiments and a new viscoelastic model. Annals of Biomedical Engineering 31 10 (2003) 1287-1296
28. Ross R., and Benditt E.P. Wound healing and collagen formation. V. Quantitative electron microscope radioautographic observations of proline-H3 utilization by fibroblasts. Journal of Cell Biology 27 1 (1965) 83-106
29. Serini G., and Gabbiani G. Mechanisms of myofibroblast activity and phenotypic modulation. Experimental Cell Research 250 2 (1999) 273-283
30. Shirinsky V.P., Antonov A.S., Birukov K.G., Sobolevsky A.V., Romanov Y.A., Kabaeva N.V., Antonova G.N., and Smirnov V.N. Mechano-chemical control of human endothelium orientation and size. Journal of Cell Biology 109 1 (1989) 331-339
31. Shreiber D.I., Barocas V.H., and Tranquillo R.T. Temporal variations in cell migration and traction during fibroblast-mediated gel compaction. Biophysical Journal 84 6 (2003) 4102-4114
32. Thastrup O., Cullen P.J., Drobak B.K., Hanley M.R., and Dawson A.P. Thapsigargin, a tumor promoter, discharges intracellular Ca2+ stores by specific inhibition of the endoplasmic reticulum Ca2(+)-ATPase. Proceedings of the National Academy of Sciences of the United States of America 87 7 (1990) 2466-2470
33. Thompson J.B., Kindt J.H., Drake B., Hansma H.G., Morse D.E., and Hansma P.K. Bone indentation recovery time correlates with bond reforming time. Nature 414 6865 (2001) 773-776
34. Tomasek J.J., Gabbiani G., Hinz B., Chaponnier C., and Brown R.A. Myofibroblasts and mechano-regulation of connective tissue remodelling. Nature Reviews Molecular Cell Biology 3 5 (2002) 349-363
35. Tomasek J.J., Vaughan M.B., Kropp B.P., Gabbiani G., Martin M.D., Haaksma C.J., and Hinz B. Contraction of myofibroblasts in granulation tissue is dependent on Rho/Rho kinase/myosin light chain phosphatase activity. Wound Repair and Regeneration 14 3 (2006) 313-320
36. Wakatsuki T., and Elson E.L. Reciprocal interactions between cells and extracellular matrix during remodeling of tissue constructs. Biophysical Chemistry 100 1-3 (2003) 593-605
37. Wakatsuki T., Kolodney M.S., Zahalak G.I., and Elson E.L. Cell mechanics studied by a reconstituted model tissue. Biophysical Journal 79 5 (2000) 2353-2368
38. Wang J.H., Goldschmidt-Clermont P., and Yin F.C. Contractility affects stress fiber remodeling and reorientation of endothelial cells subjected to cyclic mechanical stretching. Annals of Biomedical Engineering 28 10 (2000) 1165-1171
39. Wirtz H.R., and Dobbs L.G. Calcium mobilization and exocytosis after one mechanical stretch of lung epithelial cells. Science 250 4985 (1990) 1266-1269
40. Zahalak G.I., Wagenseil J.E., Wakatsuki T., and Elson E.L. A cell-based constitutive relation for bio-artificial tissues. Biophysical Journal 79 5 (2000) 2369-2381