Experimental and Computational Investigation of the Role of Stress Fiber Contractility in the Resistance of Osteoblasts to Compression

Bulletin of Mathematical Biology

Volumn 75, Issue 8, 2013, Pages 1284-1303

  Weafer, P P ^a   Ronan, W ^a   Jarvis, S P ^b   McGarry, J P ^a  

^a NATIONAL UNIVERSITY OF IRELAND   (Ireland)

^b UNIVERSITY COLLEGE DUBLIN   (Ireland)

Author keywords

Active stress fiber model; In vitro cell compression

Indexed keywords

ACTIN FILAMENT; ANIMAL; ARTICLE; ATOMIC FORCE MICROSCOPY; BIOLOGICAL MODEL; BIOMECHANICS; CELL SHAPE; CELL STRAIN 3T3; COMPRESSIVE STRENGTH; COMPUTER SIMULATION; CYTOLOGY; MOUSE; OSTEOBLAST; PHYSIOLOGY; STRESS FIBER;

3T3 CELLS; ACTIN CYTOSKELETON; ANIMALS; BIOMECHANICAL PHENOMENA; CELL SHAPE; COMPRESSIVE STRENGTH; COMPUTER SIMULATION; MICE; MICROSCOPY, ATOMIC FORCE; MODELS, BIOLOGICAL; OSTEOBLASTS; STRESS FIBERS;

EID: 84881367992     PISSN: 00928240     EISSN: 15229602     Source Type: Journal    
DOI: 10.1007/s11538-013-9812-y     Document Type: Article

References (47)

1. Avalos, P. G., Reichenzeller, M., Eils, R., & Gladilin, E. (2011). Probing compressibility of the nuclear interior in wild-type and lamin deficient cells using microscopic imaging and computational modeling. J. Biomech., 44(15), 2642-2648.
2. Broers, J. L. V., Peeters, E. A. G., Kuijpers, H. J. H., Endert, J., Bouten, C. V. C., Oomens, C. W. J., Baaijens, F. P. T., & Ramaekers, F. C. S. (2004). Decreased mechanical stiffness in lmna-/- cells is caused by defective nucleo-cytoskeletal integrity: implications for the development of laminopathies. Hum. Mol. Genet., 13(21), 2567-2580.
3. Butt, H. J., & Jaschke, M. (1995). Calculation of thermal noise in atomic force microscopy. Nanotechnology, 6(1), 1-7.
4. Caille, N., Thoumine, O., Tardy, Y., & Meister, J. J. (2002). Contribution of the nucleus to the mechanical properties of endothelial cells. J. Biomech., 35(2), 177-187.
5. Chancellor, T., Lee, J., Thodeti, C. K., & Lele, T. (2010). Actomyosin tension exerted on the nucleus through nesprin-1 connections influences endothelial cell adhesion, migration, and cyclic strain-induced reorientation. Biophys. J., 99(1), 115-123.
6. Cleveland, J. P., Manne, S., Bocek, D., & Hansma, P. K. (1993). A nondestructive method for determining the spring constant of cantilevers for scanning force microscopy. Rev. Sci. Instrum., 64(2), 403-405.
7. Darling, E. M., Topel, M., Zauscher, S., Vail, T. P., & Guilak, F. (2008). Viscoelastic properties of human mesenchymally-derived stem cells and primary osteoblasts, chondrocytes, and adipocytes. J. Biomech., 41(2), 454-464.
8. Deng, Z., Lulevich, V., Liu, F.-T., & Liu, G.-Y. (2010). Applications of atomic force microscopy in biophysical chemistry of cells. J. Phys. Chem. B, 114(18), 5971-5982.
9. Deshpande, V. S., McMeeking, R. M., & Evans, A. G. (2006). A bio-chemo-mechanical model for cell contractility. Proc. Natl. Acad. Sci., 103(38), 14015-14020.
10. Deshpande, V. S., McMeeking, R. M., & Evans, A. G. (2007). A model for the contractility of the cytoskeleton including the effects of stress-fibre formation and dissociation. Proc. R. Soc. A, Math. Phys. Eng. Sci., 463(2079), 787-815.
11. Dowling, E. P., Ronan, W., Ofek, G., Deshpande, V. S., Athanasiou, K. A., McMeeking, R. M., & McGarry, J. P. (2012). The effect of remodelling and contractility of the actin cytoskeleton on the shear resistance of single cells: a computational and experimental investigation. J. R. Soc. Interface, 9(77), 3469-3479.
12. Duncan, R., & Turner, C. (1995). Mechanotransduction and the functional response of bone to mechanical strain. Calcif. Tissue Int., 57(5), 344-358.
13. Franke, R. P., Grafe, M., Schnittler, H., Seiffge, D., Mittermayer, C., & Drenckhahn, D. (1984). Induction of human vascular endothelial stress fibres by fluid shear stress. Nature, 307(5952), 648-649.
14. Frost, H. M. (2004). A 2003 update of bone physiology and Wolff's law for clinicians. Angle Orthod., 74(1), 3-15.
15. Gabbay, J. S., Zuk, P. A., Tahernia, A., Askari, M., O'Hara, C. M., Karthikeyan, T., Azari, K., Hollinger, J. O., & Bradley, J. P. (2006). In vitro microdistraction of preosteoblasts: distraction promotes proliferation and oscillation promotes differentiation. Tissue Eng., 12(11), 3055-3065.
16. Guilak, F., & Mow, V. C. (2000). The mechanical environment of the chondrocyte: a biphasic finite element model of cell-matrix interactions in articular cartilage. J. Biomech., 33(12), 1663-1673.
17. Guilak, F., Tedrow, J. R., & Burgkart, R. (2000). Viscoelastic properties of the cell nucleus. Biochem. Biophys. Res. Commun., 269(3), 781-786.
18. Haider, M. A., & Guilak, F. (2002). An axisymmetric boundary integral model for assessing elastic cell properties in the micropipette aspiration contact problem. J. Biomech. Eng., 124(5), 586-595.
19. Higuchi, C., Nakamura, N., Yoshikawa, H., & Itoh, K. (2009). Transient dynamic actin cytoskeletal change stimulates the osteoblastic differentiation. J. Bone Miner. Metab., 27(2), 158-167.
20. Hofmann, U. G., Rotsch, C., Parak, W. J., & Radmacher, M. (1997). Investigating the cytoskeleton of chicken cardiocytes with the atomic force microscope. J. Struct. Biol., 119(2), 84-91.
21. Houben, F., Ramaekers, F. C. S., Snoeckx, L. H. E. H., & Broers, J. L. V. (2007). Role of nuclear lamina-cytoskeleton interactions in the maintenance of cellular strength. Biochim. Biophys. Acta, Mol. Cell Res., 1773(5), 675-686.
22. Kelly, G. M., Kilpatrick, J. I., van Es, M. H., Weafer, P. P., Prendergast, P. J., & Jarvis, S. P. (2011). Bone cell elasticity and morphology changes during the cell cycle. J. Biomech., 44(8), 1484-1490.
23. Khatau, S. B., Hale, C. M., Stewart-Hutchinson, P. J., Patel, M. S., Stewart, C. L., Searson, P. C., Hodzic, D., & Wirtz, D. (2009). A perinuclear actin cap regulates nuclear shape. Proc. Natl. Acad. Sci., 106(45), 19017-19022.
24. Kolega, J. (1986). Effects of mechanical tension on protrusive activity and microfilament and intermediate filament organization in an epidermal epithelium moving in culture. J. Cell Biol., 102(4), 1400-1411.
25. Lulevich, V., Zink, T., Chen, H.-Y., Liu, F.-T., & Liu, G.-Y. (2006). Cell mechanics using atomic force microscopy-based single-cell compression. Langmuir, 22(19), 8151-8155.
26. McGarry, J. P. (2009). Characterization of cell mechanical properties by computational modeling of parallel plate compression. Ann. Biomed. Eng., 37(11), 2317-2325.
27. McGarry, J. P., & McHugh, P. E. (2008). Modelling of in vitro chondrocyte detachment. J. Mech. Phys. Solids, 56(4), 1554-1565.
28. McGarry, J. P., Murphy, B. P., & McHugh, P. E. (2005). Computational mechanics modelling of cell-substrate contact during cyclic substrate deformation. J. Mech. Phys. Solids, 53(12), 2597-2637.
29. McGarry, J. G., Maguire, P., Campbell, V. A., O'Connell, B. C., Prendergast, P. J., & Jarvis, S. P. (2008). Stimulation of nitric oxide mechanotransduction in single osteoblasts using atomic force microscopy. J. Orthop. Res., 26(4), 513-521.
30. McGarry, J. P., Fu, J., Yang, M. T., Chen, C. S., McMeeking, R. M., Evans, A. G., & Deshpande, V. S. (2009). Simulation of the contractile response of cells on an array of micro-posts. Philos. Trans. R. Soc., Math. Phys. Eng. Sci., 367(1902), 3477-3497.
31. Mohrdieck, C., Wanner, A., Roos, W., Roth, A., Sackmann, E., Spatz, J. P., & Arzt, E. (2005). A theoretical description of elastic pillar substrates in biophysical experiments. ChemPhysChem, 6(8), 1492-1498.
32. Ofek, G., Natoli, R. M., & Athanasiou, K. A. (2009a). In situ mechanical properties of the chondrocyte cytoplasm and nucleus. J. Biomech., 42(7), 873-877.
33. Ofek, G., Wiltz, D. C., & Athanasiou, K. A. (2009b). Contribution of the cytoskeleton to the compressive properties and recovery behavior of single cells. Biophys. J., 97(7), 1873-1882.
34. Owan, I., Burr, D. B., Turner, C. H., Qiu, J., Tu, Y., Onyia, J. E., & Duncan, R. L. (1997). Mechanotransduction in bone: osteoblasts are more responsive to fluid forces than mechanical strain. Am. J. Physiol., Cell Physiol., 273(3), C810-C815.
35. Pathak, A., Deshpande, V. S., McMeeking, R. M., & Evans, A. G. (2008). The simulation of stress fibre and focal adhesion development in cells on patterned substrates. J. R. Soc. Interface, 5(22), 507-524.
36. Peeters, E. A., Oomens, C. W., Bouten, C. V., Bader, D. L., & Baaijens, F. P. (2005a). Viscoelastic properties of single attached cells under compression. J. Biomech. Eng., 127(2), 237-243.
37. Peeters, E. A., Oomens, C. W., Bouten, C. V., Bader, D. L., & Baaijens, F. P. (2005b). Mechanical and failure properties of single attached cells under compression. J. Biomech., 38(8), 1685-1693.
38. Rath, B., Nam, J., Knobloch, T. J., Lannutti, J. J., & Agarwal, S. (2008). Compressive forces induce osteogenic gene expression in calvarial osteoblasts. J. Biomech., 41(5), 1095-1103.
39. Ronan, W., Deshpande, V. S., McMeeking, R. M., & McGarry, J. P. (2011). Simulation of stress fiber remodeling and mixed mode focal adhesion assembly during cell spreading and for cells adhered to elastic substrates. In: Proceedings of the ASME 2011 summer bioengineering conference, SBC2011-53878, Farmington, PA, USA.
40. Ronan, W., Deshpande, V. S., McMeeking, R. M., & McGarry, J. P. (2012). Numerical investigation of the active role of the actin cytoskeleton in the compression resistance of cells. J. Mech. Behav. Biomed. Mater., 14, 143-157.
41. Rotsch, C., & Radmacher, M. (2000). Drug-induced changes of cytoskeletal structure and mechanics in fibroblasts: an atomic force microscopy study. Biophys. J., 78(1), 520-535.
42. Rowat, A. C., Foster, L. J., Nielsen, M. M., Weiss, M., & Ipsen, J. H. (2005). Characterization of the elastic properties of the nuclear envelope. J. R. Soc. Interface, 2(2), 63-69.
43. Shieh, A. C., & Athanasiou, K. A. (2007). Dynamic compression of single cells. Osteoarthr. Cartil., 15(3), 328-334.
44. Storm, C., Pastore, J. J., MacKintosh, F. C., Lubensky, T. C., & Janmey, P. A. (2005). Nonlinear elasticity in biological gels. Nature, 435(7039), 191-194.
45. Thoumine, O., Cardoso, O., & Meister, J. J. (1999). Changes in the mechanical properties of fibroblasts during spreading: a micromanipulation study. Eur. Biophys. J. Biophys. Lett., 28(3), 222-234.
46. Warshaw, D. M., Desrosiers, J. M., Work, S. S., & Trybus, K. M. (1990). Smooth muscle myosin cross-bridge interactions modulate actin filament sliding velocity in vitro. J. Cell Biol., 111(2), 453-463.
47. Weafer, P., McGarry, J., van Es, M., Kilpatrick, J., Ronan, W., Nolan, D., & Jarvis, S. (2012). Stability enhancement of an atomic force microscope for long-term force measurement including cantilever modification for whole cell deformation. Rev. Sci. Instrum., 83(9), 093709.