Abstract

It is increasingly important to measure cell mechanical properties in three-dimensional environments. Particle tracking microrheology (PTM) can measure cellular viscoelastic properties; however, out-of-plane data can introduce artifacts into these measurements. We developed a technique that employs HiLo microscopy to reduce out-of-plane contributions. This method eliminated signals from 90% of probes 0.5 μm or further from the focal plane, while retaining all in-plane probes. We used this technique to characterize live-cell bilayers and found that there were significant, frequency-dependent changes to the extracted cell moduli when compared to conventional analysis. Our results indicate that removal of out-of-plane information is vital for accurate assessments of cell mechanical properties.

© 2012 OSA

Full Article  |  PDF Article

References

  • View by:
  • |
  • |
  • |

  1. J. Lammerding and R. T. Lee, “The nuclear membrane and mechanotransduction: impaired nuclear mechanics and mechanotransduction in lamin A/C deficient cells,” in Nuclear Organization in Development and Disease, Novartis Foundation Symposium Vol. 264 (Wiley, 2005), pp. 264–273.
  2. T. P. Kole, Y. Tseng, I. Jiang, J. L. Katz, and D. Wirtz, “Intracellular mechanics of migrating fibroblasts,” Mol. Biol. Cell16(1), 328–338 (2005).
    [CrossRef] [PubMed]
  3. R. G. Wells, “The role of matrix stiffness in regulating cell behavior,” Hepatology47(4), 1394–1400 (2008).
    [CrossRef] [PubMed]
  4. E. U. Azeloglu, J. Bhattacharya, and K. D. Costa, “Atomic force microscope elastography reveals phenotypic differences in alveolar cell stiffness,” J. Appl. Physiol.105(2), 652–661 (2008).
    [CrossRef] [PubMed]
  5. D. Fudge, D. Russell, D. Beriault, W. Moore, E. B. Lane, and A. W. Vogl, “The intermediate filament network in cultured human keratinocytes is remarkably extensible and resilient,” PLoS ONE3(6), e2327 (2008).
    [CrossRef] [PubMed]
  6. H. Huang, A. Asimaki, D. Lo, W. McKenna, and J. Saffitz, “Disparate effects of different mutations in plakoglobin on cell mechanical behavior,” Cell Motil. Cytoskeleton65(12), 964–978 (2008).
    [CrossRef] [PubMed]
  7. J. Lammerding, P. C. Schulze, T. Takahashi, S. Kozlov, T. Sullivan, R. D. Kamm, C. L. Stewart, and R. T. Lee, “Lamin A/C deficiency causes defective nuclear mechanics and mechanotransduction,” J. Clin. Invest.113(3), 370–378 (2004).
    [PubMed]
  8. D. Wirtz, “Particle-tracking microrheology of living cells: principles and applications,” Annu Rev Biophys38(1), 301–326 (2009).
    [CrossRef] [PubMed]
  9. J. C. Crocker and B. D. Hoffman, “Multiple-particle tracking and two-point microrheology in cells,” Methods Cell Biol.83, 141–178 (2007).
    [CrossRef] [PubMed]
  10. M. Jonas, H. Huang, R. D. Kamm, and P. T. So, “Fast fluorescence laser tracking microrheometry, II: quantitative studies of cytoskeletal mechanotransduction,” Biophys. J.95(2), 895–909 (2008).
    [CrossRef] [PubMed]
  11. A. W. Lau, B. D. Hoffman, A. Davies, J. C. Crocker, and T. C. Lubensky, “Microrheology, stress fluctuations, and active behavior of living cells,” Phys. Rev. Lett.91(19), 198101 (2003).
    [CrossRef] [PubMed]
  12. C. M. Hale, A. L. Shrestha, S. B. Khatau, P. J. Stewart-Hutchinson, L. Hernandez, C. L. Stewart, D. Hodzic, and D. Wirtz, “Dysfunctional connections between the nucleus and the actin and microtubule networks in laminopathic models,” Biophys. J.95(11), 5462–5475 (2008).
    [CrossRef] [PubMed]
  13. J. S. Lee, P. Panorchan, C. M. Hale, S. B. Khatau, T. P. Kole, Y. Tseng, and D. Wirtz, “Ballistic intracellular nanorheology reveals ROCK-hard cytoplasmic stiffening response to fluid flow,” J. Cell Sci.119(9), 1760–1768 (2006).
    [CrossRef] [PubMed]
  14. A. Pai, P. Sundd, and D. F. Tees, “In situ microrheological determination of neutrophil stiffening following adhesion in a model capillary,” Ann. Biomed. Eng.36(4), 596–603 (2008).
    [CrossRef] [PubMed]
  15. P. Panorchan, J. S. Lee, B. R. Daniels, T. P. Kole, Y. Tseng, and D. Wirtz, “Probing cellular mechanical responses to stimuli using ballistic intracellular nanorheology,” Methods Cell Biol.83, 113–140 (2007).
    [CrossRef] [PubMed]
  16. P. J. Stewart-Hutchinson, C. M. Hale, D. Wirtz, and D. Hodzic, “Structural requirements for the assembly of LINC complexes and their function in cellular mechanical stiffness,” Exp. Cell Res.314(8), 1892–1905 (2008).
    [CrossRef] [PubMed]
  17. A. D. van der Meer, Y. Li, M. H. Duits, A. A. Poot, J. Feijen, and I. Vermes, “Shear stress induces a transient and VEGFR-2-dependent decrease in the motion of injected particles in endothelial cells,” Biorheology47(3-4), 179–192 (2010).
    [PubMed]
  18. Y. Tseng, T. P. Kole, and D. Wirtz, “Micromechanical mapping of live cells by multiple-particle-tracking microrheology,” Biophys. J.83(6), 3162–3176 (2002).
    [CrossRef] [PubMed]
  19. K. Nishida, M. Yamato, Y. Hayashida, K. Watanabe, K. Yamamoto, E. Adachi, S. Nagai, A. Kikuchi, N. Maeda, H. Watanabe, T. Okano, and Y. Tano, “Corneal reconstruction with tissue-engineered cell sheets composed of autologous oral mucosal epithelium,” N. Engl. J. Med.351(12), 1187–1196 (2004).
    [CrossRef] [PubMed]
  20. S. L. Ishaug-Riley, G. M. Crane-Kruger, M. J. Yaszemski, and A. G. Mikos, “Three-dimensional culture of rat calvarial osteoblasts in porous biodegradable polymers,” Biomaterials19(15), 1405–1412 (1998).
    [CrossRef] [PubMed]
  21. S. L. Ishaug, G. M. Crane, M. J. Miller, A. W. Yasko, M. J. Yaszemski, and A. G. Mikos, “Bone formation by three-dimensional stromal osteoblast culture in biodegradable polymer scaffolds,” J. Biomed. Mater. Res.36(1), 17–28 (1997).
    [CrossRef] [PubMed]
  22. T. Eschenhagen, C. Fink, U. Remmers, H. Scholz, J. Wattchow, J. Weil, W. Zimmermann, H. H. Dohmen, H. Schäfer, N. Bishopric, T. Wakatsuki, and E. L. Elson, “Three-dimensional reconstitution of embryonic cardiomyocytes in a collagen matrix: a new heart muscle model system,” FASEB J.11(8), 683–694 (1997).
    [PubMed]
  23. M. A. Neil, R. Juskaitis, and T. Wilson, “Method of obtaining optical sectioning by using structured light in a conventional microscope,” Opt. Lett.22(24), 1905–1907 (1997).
    [CrossRef] [PubMed]
  24. N. Bozinovic, C. Ventalon, T. Ford, and J. Mertz, “Fluorescence endomicroscopy with structured illumination,” Opt. Express16(11), 8016–8025 (2008).
    [CrossRef] [PubMed]
  25. M. F. Langhorst, J. Schaffer, and B. Goetze, “Structure brings clarity: structured illumination microscopy in cell biology,” Biotechnol. J.4(6), 858–865 (2009).
    [CrossRef] [PubMed]
  26. S. Santos, K. K. Chu, D. Lim, N. Bozinovic, T. N. Ford, C. Hourtoule, A. C. Bartoo, S. K. Singh, and J. Mertz, “Optically sectioned fluorescence endomicroscopy with hybrid-illumination imaging through a flexible fiber bundle,” J. Biomed. Opt.14(3), 030502 (2009).
    [CrossRef] [PubMed]
  27. D. Lim, K. K. Chu, and J. Mertz, “Wide-field fluorescence sectioning with hybrid speckle and uniform-illumination microscopy,” Opt. Lett.33(16), 1819–1821 (2008).
    [CrossRef] [PubMed]
  28. J. Mertz and J. Kim, “Scanning light-sheet microscopy in the whole mouse brain with HiLo background rejection,” J. Biomed. Opt.15(1), 016027 (2010).
    [CrossRef] [PubMed]
  29. J. C. Crocker and D. G. Grier, “When like charges attract: the effects of geometrical confinement on long-range colloidal interactions,” Phys. Rev. Lett.77(9), 1897–1900 (1996).
    [CrossRef] [PubMed]
  30. T. G. Mason, “Estimating the viscoelastic moduli of complex fluids using the generalized Stokes-Einstein equation,” Rheologica Acta39(4), 371–378 (2000).
    [CrossRef]
  31. B. S. Elkin, E. U. Azeloglu, K. D. Costa, and B. Morrison, “Mechanical heterogeneity of the rat hippocampus measured by atomic force microscope indentation,” J. Neurotrauma24(5), 812–822 (2007).
    [CrossRef] [PubMed]
  32. D. C. Lin, E. K. Dimitriadis, and F. Horkay, “Robust strategies for automated AFM force curve analysis--I. Non-adhesive indentation of soft, inhomogeneous materials,” J. Biomech. Eng.129(3), 430–440 (2007).
    [CrossRef] [PubMed]
  33. J. Solon, I. Levental, K. Sengupta, P. C. Georges, and P. A. Janmey, “Fibroblast adaptation and stiffness matching to soft elastic substrates,” Biophys. J.93(12), 4453–4461 (2007).
    [CrossRef] [PubMed]
  34. X. Shi, L. Qin, X. Zhang, K. He, C. Xiong, J. Fang, X. Fang, and Y. Zhang, “Elasticity of cardiac cells on the polymer substrates with different stiffness: an atomic force microscopy study,” Phys. Chem. Chem. Phys.13(16), 7540–7545 (2011).
    [CrossRef] [PubMed]
  35. L. Cao, A. Wu, and G. A. Truskey, “Biomechanical effects of flow and coculture on human aortic and cord blood-derived endothelial cells,” J. Biomech.44(11), 2150–2157 (2011).
    [CrossRef] [PubMed]
  36. J. G. McNally, T. Karpova, J. Cooper, and J. A. Conchello, “Three-dimensional imaging by deconvolution microscopy,” Methods19(3), 373–385 (1999).
    [CrossRef] [PubMed]
  37. A. Ganz, M. Lambert, A. Saez, P. Silberzan, A. Buguin, R. M. Mège, and B. Ladoux, “Traction forces exerted through N-cadherin contacts,” Biol. Cell98(12), 721–730 (2006).
    [CrossRef] [PubMed]
  38. V. Maruthamuthu, B. Sabass, U. S. Schwarz, and M. L. Gardel, “Cell-ECM traction force modulates endogenous tension at cell-cell contacts,” Proc. Natl. Acad. Sci. U.S.A.108(12), 4708–4713 (2011).
    [CrossRef] [PubMed]
  39. M. C. DeSantis, S. K. Zareh, X. Li, R. E. Blankenship, and Y. M. Wang, “Single-image axial localization precision analysis for individual fluorophores,” Opt. Express20(3), 3057–3065 (2012).
    [CrossRef] [PubMed]
  40. P. H. Wu, S. H. Arce, P. R. Burney, and Y. Tseng, “A novel approach to high accuracy of video-based microrheology,” Biophys. J.96(12), 5103–5111 (2009).
    [CrossRef] [PubMed]
  41. P. Prabhat, S. Ram, E. S. Ward, and R. J. Ober, “Simultaneous imaging of different focal planes in fluorescence microscopy for the study of cellular dynamics in three dimensions,” IEEE Trans. Nanobioscience3(4), 237–242 (2004).
    [CrossRef] [PubMed]
  42. H. P. Kao and A. S. Verkman, “Tracking of single fluorescent particles in three dimensions: use of cylindrical optics to encode particle position,” Biophys. J.67(3), 1291–1300 (1994).
    [CrossRef] [PubMed]
  43. V. Levi, Q. Ruan, and E. Gratton, “3-D particle tracking in a two-photon microscope: application to the study of molecular dynamics in cells,” Biophys. J.88(4), 2919–2928 (2005).
    [CrossRef] [PubMed]

2012

2011

X. Shi, L. Qin, X. Zhang, K. He, C. Xiong, J. Fang, X. Fang, and Y. Zhang, “Elasticity of cardiac cells on the polymer substrates with different stiffness: an atomic force microscopy study,” Phys. Chem. Chem. Phys.13(16), 7540–7545 (2011).
[CrossRef] [PubMed]

L. Cao, A. Wu, and G. A. Truskey, “Biomechanical effects of flow and coculture on human aortic and cord blood-derived endothelial cells,” J. Biomech.44(11), 2150–2157 (2011).
[CrossRef] [PubMed]

V. Maruthamuthu, B. Sabass, U. S. Schwarz, and M. L. Gardel, “Cell-ECM traction force modulates endogenous tension at cell-cell contacts,” Proc. Natl. Acad. Sci. U.S.A.108(12), 4708–4713 (2011).
[CrossRef] [PubMed]

2010

J. Mertz and J. Kim, “Scanning light-sheet microscopy in the whole mouse brain with HiLo background rejection,” J. Biomed. Opt.15(1), 016027 (2010).
[CrossRef] [PubMed]

A. D. van der Meer, Y. Li, M. H. Duits, A. A. Poot, J. Feijen, and I. Vermes, “Shear stress induces a transient and VEGFR-2-dependent decrease in the motion of injected particles in endothelial cells,” Biorheology47(3-4), 179–192 (2010).
[PubMed]

2009

D. Wirtz, “Particle-tracking microrheology of living cells: principles and applications,” Annu Rev Biophys38(1), 301–326 (2009).
[CrossRef] [PubMed]

P. H. Wu, S. H. Arce, P. R. Burney, and Y. Tseng, “A novel approach to high accuracy of video-based microrheology,” Biophys. J.96(12), 5103–5111 (2009).
[CrossRef] [PubMed]

M. F. Langhorst, J. Schaffer, and B. Goetze, “Structure brings clarity: structured illumination microscopy in cell biology,” Biotechnol. J.4(6), 858–865 (2009).
[CrossRef] [PubMed]

S. Santos, K. K. Chu, D. Lim, N. Bozinovic, T. N. Ford, C. Hourtoule, A. C. Bartoo, S. K. Singh, and J. Mertz, “Optically sectioned fluorescence endomicroscopy with hybrid-illumination imaging through a flexible fiber bundle,” J. Biomed. Opt.14(3), 030502 (2009).
[CrossRef] [PubMed]

2008

N. Bozinovic, C. Ventalon, T. Ford, and J. Mertz, “Fluorescence endomicroscopy with structured illumination,” Opt. Express16(11), 8016–8025 (2008).
[CrossRef] [PubMed]

D. Lim, K. K. Chu, and J. Mertz, “Wide-field fluorescence sectioning with hybrid speckle and uniform-illumination microscopy,” Opt. Lett.33(16), 1819–1821 (2008).
[CrossRef] [PubMed]

M. Jonas, H. Huang, R. D. Kamm, and P. T. So, “Fast fluorescence laser tracking microrheometry, II: quantitative studies of cytoskeletal mechanotransduction,” Biophys. J.95(2), 895–909 (2008).
[CrossRef] [PubMed]

R. G. Wells, “The role of matrix stiffness in regulating cell behavior,” Hepatology47(4), 1394–1400 (2008).
[CrossRef] [PubMed]

E. U. Azeloglu, J. Bhattacharya, and K. D. Costa, “Atomic force microscope elastography reveals phenotypic differences in alveolar cell stiffness,” J. Appl. Physiol.105(2), 652–661 (2008).
[CrossRef] [PubMed]

D. Fudge, D. Russell, D. Beriault, W. Moore, E. B. Lane, and A. W. Vogl, “The intermediate filament network in cultured human keratinocytes is remarkably extensible and resilient,” PLoS ONE3(6), e2327 (2008).
[CrossRef] [PubMed]

H. Huang, A. Asimaki, D. Lo, W. McKenna, and J. Saffitz, “Disparate effects of different mutations in plakoglobin on cell mechanical behavior,” Cell Motil. Cytoskeleton65(12), 964–978 (2008).
[CrossRef] [PubMed]

P. J. Stewart-Hutchinson, C. M. Hale, D. Wirtz, and D. Hodzic, “Structural requirements for the assembly of LINC complexes and their function in cellular mechanical stiffness,” Exp. Cell Res.314(8), 1892–1905 (2008).
[CrossRef] [PubMed]

C. M. Hale, A. L. Shrestha, S. B. Khatau, P. J. Stewart-Hutchinson, L. Hernandez, C. L. Stewart, D. Hodzic, and D. Wirtz, “Dysfunctional connections between the nucleus and the actin and microtubule networks in laminopathic models,” Biophys. J.95(11), 5462–5475 (2008).
[CrossRef] [PubMed]

A. Pai, P. Sundd, and D. F. Tees, “In situ microrheological determination of neutrophil stiffening following adhesion in a model capillary,” Ann. Biomed. Eng.36(4), 596–603 (2008).
[CrossRef] [PubMed]

2007

P. Panorchan, J. S. Lee, B. R. Daniels, T. P. Kole, Y. Tseng, and D. Wirtz, “Probing cellular mechanical responses to stimuli using ballistic intracellular nanorheology,” Methods Cell Biol.83, 113–140 (2007).
[CrossRef] [PubMed]

J. C. Crocker and B. D. Hoffman, “Multiple-particle tracking and two-point microrheology in cells,” Methods Cell Biol.83, 141–178 (2007).
[CrossRef] [PubMed]

B. S. Elkin, E. U. Azeloglu, K. D. Costa, and B. Morrison, “Mechanical heterogeneity of the rat hippocampus measured by atomic force microscope indentation,” J. Neurotrauma24(5), 812–822 (2007).
[CrossRef] [PubMed]

D. C. Lin, E. K. Dimitriadis, and F. Horkay, “Robust strategies for automated AFM force curve analysis--I. Non-adhesive indentation of soft, inhomogeneous materials,” J. Biomech. Eng.129(3), 430–440 (2007).
[CrossRef] [PubMed]

J. Solon, I. Levental, K. Sengupta, P. C. Georges, and P. A. Janmey, “Fibroblast adaptation and stiffness matching to soft elastic substrates,” Biophys. J.93(12), 4453–4461 (2007).
[CrossRef] [PubMed]

2006

A. Ganz, M. Lambert, A. Saez, P. Silberzan, A. Buguin, R. M. Mège, and B. Ladoux, “Traction forces exerted through N-cadherin contacts,” Biol. Cell98(12), 721–730 (2006).
[CrossRef] [PubMed]

J. S. Lee, P. Panorchan, C. M. Hale, S. B. Khatau, T. P. Kole, Y. Tseng, and D. Wirtz, “Ballistic intracellular nanorheology reveals ROCK-hard cytoplasmic stiffening response to fluid flow,” J. Cell Sci.119(9), 1760–1768 (2006).
[CrossRef] [PubMed]

2005

T. P. Kole, Y. Tseng, I. Jiang, J. L. Katz, and D. Wirtz, “Intracellular mechanics of migrating fibroblasts,” Mol. Biol. Cell16(1), 328–338 (2005).
[CrossRef] [PubMed]

V. Levi, Q. Ruan, and E. Gratton, “3-D particle tracking in a two-photon microscope: application to the study of molecular dynamics in cells,” Biophys. J.88(4), 2919–2928 (2005).
[CrossRef] [PubMed]

2004

J. Lammerding, P. C. Schulze, T. Takahashi, S. Kozlov, T. Sullivan, R. D. Kamm, C. L. Stewart, and R. T. Lee, “Lamin A/C deficiency causes defective nuclear mechanics and mechanotransduction,” J. Clin. Invest.113(3), 370–378 (2004).
[PubMed]

P. Prabhat, S. Ram, E. S. Ward, and R. J. Ober, “Simultaneous imaging of different focal planes in fluorescence microscopy for the study of cellular dynamics in three dimensions,” IEEE Trans. Nanobioscience3(4), 237–242 (2004).
[CrossRef] [PubMed]

K. Nishida, M. Yamato, Y. Hayashida, K. Watanabe, K. Yamamoto, E. Adachi, S. Nagai, A. Kikuchi, N. Maeda, H. Watanabe, T. Okano, and Y. Tano, “Corneal reconstruction with tissue-engineered cell sheets composed of autologous oral mucosal epithelium,” N. Engl. J. Med.351(12), 1187–1196 (2004).
[CrossRef] [PubMed]

2003

A. W. Lau, B. D. Hoffman, A. Davies, J. C. Crocker, and T. C. Lubensky, “Microrheology, stress fluctuations, and active behavior of living cells,” Phys. Rev. Lett.91(19), 198101 (2003).
[CrossRef] [PubMed]

2002

Y. Tseng, T. P. Kole, and D. Wirtz, “Micromechanical mapping of live cells by multiple-particle-tracking microrheology,” Biophys. J.83(6), 3162–3176 (2002).
[CrossRef] [PubMed]

2000

T. G. Mason, “Estimating the viscoelastic moduli of complex fluids using the generalized Stokes-Einstein equation,” Rheologica Acta39(4), 371–378 (2000).
[CrossRef]

1999

J. G. McNally, T. Karpova, J. Cooper, and J. A. Conchello, “Three-dimensional imaging by deconvolution microscopy,” Methods19(3), 373–385 (1999).
[CrossRef] [PubMed]

1998

S. L. Ishaug-Riley, G. M. Crane-Kruger, M. J. Yaszemski, and A. G. Mikos, “Three-dimensional culture of rat calvarial osteoblasts in porous biodegradable polymers,” Biomaterials19(15), 1405–1412 (1998).
[CrossRef] [PubMed]

1997

S. L. Ishaug, G. M. Crane, M. J. Miller, A. W. Yasko, M. J. Yaszemski, and A. G. Mikos, “Bone formation by three-dimensional stromal osteoblast culture in biodegradable polymer scaffolds,” J. Biomed. Mater. Res.36(1), 17–28 (1997).
[CrossRef] [PubMed]

T. Eschenhagen, C. Fink, U. Remmers, H. Scholz, J. Wattchow, J. Weil, W. Zimmermann, H. H. Dohmen, H. Schäfer, N. Bishopric, T. Wakatsuki, and E. L. Elson, “Three-dimensional reconstitution of embryonic cardiomyocytes in a collagen matrix: a new heart muscle model system,” FASEB J.11(8), 683–694 (1997).
[PubMed]

M. A. Neil, R. Juskaitis, and T. Wilson, “Method of obtaining optical sectioning by using structured light in a conventional microscope,” Opt. Lett.22(24), 1905–1907 (1997).
[CrossRef] [PubMed]

1996

J. C. Crocker and D. G. Grier, “When like charges attract: the effects of geometrical confinement on long-range colloidal interactions,” Phys. Rev. Lett.77(9), 1897–1900 (1996).
[CrossRef] [PubMed]

1994

H. P. Kao and A. S. Verkman, “Tracking of single fluorescent particles in three dimensions: use of cylindrical optics to encode particle position,” Biophys. J.67(3), 1291–1300 (1994).
[CrossRef] [PubMed]

Adachi, E.

K. Nishida, M. Yamato, Y. Hayashida, K. Watanabe, K. Yamamoto, E. Adachi, S. Nagai, A. Kikuchi, N. Maeda, H. Watanabe, T. Okano, and Y. Tano, “Corneal reconstruction with tissue-engineered cell sheets composed of autologous oral mucosal epithelium,” N. Engl. J. Med.351(12), 1187–1196 (2004).
[CrossRef] [PubMed]

Arce, S. H.

P. H. Wu, S. H. Arce, P. R. Burney, and Y. Tseng, “A novel approach to high accuracy of video-based microrheology,” Biophys. J.96(12), 5103–5111 (2009).
[CrossRef] [PubMed]

Asimaki, A.

H. Huang, A. Asimaki, D. Lo, W. McKenna, and J. Saffitz, “Disparate effects of different mutations in plakoglobin on cell mechanical behavior,” Cell Motil. Cytoskeleton65(12), 964–978 (2008).
[CrossRef] [PubMed]

Azeloglu, E. U.

E. U. Azeloglu, J. Bhattacharya, and K. D. Costa, “Atomic force microscope elastography reveals phenotypic differences in alveolar cell stiffness,” J. Appl. Physiol.105(2), 652–661 (2008).
[CrossRef] [PubMed]

B. S. Elkin, E. U. Azeloglu, K. D. Costa, and B. Morrison, “Mechanical heterogeneity of the rat hippocampus measured by atomic force microscope indentation,” J. Neurotrauma24(5), 812–822 (2007).
[CrossRef] [PubMed]

Bartoo, A. C.

S. Santos, K. K. Chu, D. Lim, N. Bozinovic, T. N. Ford, C. Hourtoule, A. C. Bartoo, S. K. Singh, and J. Mertz, “Optically sectioned fluorescence endomicroscopy with hybrid-illumination imaging through a flexible fiber bundle,” J. Biomed. Opt.14(3), 030502 (2009).
[CrossRef] [PubMed]

Beriault, D.

D. Fudge, D. Russell, D. Beriault, W. Moore, E. B. Lane, and A. W. Vogl, “The intermediate filament network in cultured human keratinocytes is remarkably extensible and resilient,” PLoS ONE3(6), e2327 (2008).
[CrossRef] [PubMed]

Bhattacharya, J.

E. U. Azeloglu, J. Bhattacharya, and K. D. Costa, “Atomic force microscope elastography reveals phenotypic differences in alveolar cell stiffness,” J. Appl. Physiol.105(2), 652–661 (2008).
[CrossRef] [PubMed]

Bishopric, N.

T. Eschenhagen, C. Fink, U. Remmers, H. Scholz, J. Wattchow, J. Weil, W. Zimmermann, H. H. Dohmen, H. Schäfer, N. Bishopric, T. Wakatsuki, and E. L. Elson, “Three-dimensional reconstitution of embryonic cardiomyocytes in a collagen matrix: a new heart muscle model system,” FASEB J.11(8), 683–694 (1997).
[PubMed]

Blankenship, R. E.

Bozinovic, N.

S. Santos, K. K. Chu, D. Lim, N. Bozinovic, T. N. Ford, C. Hourtoule, A. C. Bartoo, S. K. Singh, and J. Mertz, “Optically sectioned fluorescence endomicroscopy with hybrid-illumination imaging through a flexible fiber bundle,” J. Biomed. Opt.14(3), 030502 (2009).
[CrossRef] [PubMed]

N. Bozinovic, C. Ventalon, T. Ford, and J. Mertz, “Fluorescence endomicroscopy with structured illumination,” Opt. Express16(11), 8016–8025 (2008).
[CrossRef] [PubMed]

Buguin, A.

A. Ganz, M. Lambert, A. Saez, P. Silberzan, A. Buguin, R. M. Mège, and B. Ladoux, “Traction forces exerted through N-cadherin contacts,” Biol. Cell98(12), 721–730 (2006).
[CrossRef] [PubMed]

Burney, P. R.

P. H. Wu, S. H. Arce, P. R. Burney, and Y. Tseng, “A novel approach to high accuracy of video-based microrheology,” Biophys. J.96(12), 5103–5111 (2009).
[CrossRef] [PubMed]

Cao, L.

L. Cao, A. Wu, and G. A. Truskey, “Biomechanical effects of flow and coculture on human aortic and cord blood-derived endothelial cells,” J. Biomech.44(11), 2150–2157 (2011).
[CrossRef] [PubMed]

Chu, K. K.

S. Santos, K. K. Chu, D. Lim, N. Bozinovic, T. N. Ford, C. Hourtoule, A. C. Bartoo, S. K. Singh, and J. Mertz, “Optically sectioned fluorescence endomicroscopy with hybrid-illumination imaging through a flexible fiber bundle,” J. Biomed. Opt.14(3), 030502 (2009).
[CrossRef] [PubMed]

D. Lim, K. K. Chu, and J. Mertz, “Wide-field fluorescence sectioning with hybrid speckle and uniform-illumination microscopy,” Opt. Lett.33(16), 1819–1821 (2008).
[CrossRef] [PubMed]

Conchello, J. A.

J. G. McNally, T. Karpova, J. Cooper, and J. A. Conchello, “Three-dimensional imaging by deconvolution microscopy,” Methods19(3), 373–385 (1999).
[CrossRef] [PubMed]

Cooper, J.

J. G. McNally, T. Karpova, J. Cooper, and J. A. Conchello, “Three-dimensional imaging by deconvolution microscopy,” Methods19(3), 373–385 (1999).
[CrossRef] [PubMed]

Costa, K. D.

E. U. Azeloglu, J. Bhattacharya, and K. D. Costa, “Atomic force microscope elastography reveals phenotypic differences in alveolar cell stiffness,” J. Appl. Physiol.105(2), 652–661 (2008).
[CrossRef] [PubMed]

B. S. Elkin, E. U. Azeloglu, K. D. Costa, and B. Morrison, “Mechanical heterogeneity of the rat hippocampus measured by atomic force microscope indentation,” J. Neurotrauma24(5), 812–822 (2007).
[CrossRef] [PubMed]

Crane, G. M.

S. L. Ishaug, G. M. Crane, M. J. Miller, A. W. Yasko, M. J. Yaszemski, and A. G. Mikos, “Bone formation by three-dimensional stromal osteoblast culture in biodegradable polymer scaffolds,” J. Biomed. Mater. Res.36(1), 17–28 (1997).
[CrossRef] [PubMed]

Crane-Kruger, G. M.

S. L. Ishaug-Riley, G. M. Crane-Kruger, M. J. Yaszemski, and A. G. Mikos, “Three-dimensional culture of rat calvarial osteoblasts in porous biodegradable polymers,” Biomaterials19(15), 1405–1412 (1998).
[CrossRef] [PubMed]

Crocker, J. C.

J. C. Crocker and B. D. Hoffman, “Multiple-particle tracking and two-point microrheology in cells,” Methods Cell Biol.83, 141–178 (2007).
[CrossRef] [PubMed]

A. W. Lau, B. D. Hoffman, A. Davies, J. C. Crocker, and T. C. Lubensky, “Microrheology, stress fluctuations, and active behavior of living cells,” Phys. Rev. Lett.91(19), 198101 (2003).
[CrossRef] [PubMed]

J. C. Crocker and D. G. Grier, “When like charges attract: the effects of geometrical confinement on long-range colloidal interactions,” Phys. Rev. Lett.77(9), 1897–1900 (1996).
[CrossRef] [PubMed]

Daniels, B. R.

P. Panorchan, J. S. Lee, B. R. Daniels, T. P. Kole, Y. Tseng, and D. Wirtz, “Probing cellular mechanical responses to stimuli using ballistic intracellular nanorheology,” Methods Cell Biol.83, 113–140 (2007).
[CrossRef] [PubMed]

Davies, A.

A. W. Lau, B. D. Hoffman, A. Davies, J. C. Crocker, and T. C. Lubensky, “Microrheology, stress fluctuations, and active behavior of living cells,” Phys. Rev. Lett.91(19), 198101 (2003).
[CrossRef] [PubMed]

DeSantis, M. C.

Dimitriadis, E. K.

D. C. Lin, E. K. Dimitriadis, and F. Horkay, “Robust strategies for automated AFM force curve analysis--I. Non-adhesive indentation of soft, inhomogeneous materials,” J. Biomech. Eng.129(3), 430–440 (2007).
[CrossRef] [PubMed]

Dohmen, H. H.

T. Eschenhagen, C. Fink, U. Remmers, H. Scholz, J. Wattchow, J. Weil, W. Zimmermann, H. H. Dohmen, H. Schäfer, N. Bishopric, T. Wakatsuki, and E. L. Elson, “Three-dimensional reconstitution of embryonic cardiomyocytes in a collagen matrix: a new heart muscle model system,” FASEB J.11(8), 683–694 (1997).
[PubMed]

Duits, M. H.

A. D. van der Meer, Y. Li, M. H. Duits, A. A. Poot, J. Feijen, and I. Vermes, “Shear stress induces a transient and VEGFR-2-dependent decrease in the motion of injected particles in endothelial cells,” Biorheology47(3-4), 179–192 (2010).
[PubMed]

Elkin, B. S.

B. S. Elkin, E. U. Azeloglu, K. D. Costa, and B. Morrison, “Mechanical heterogeneity of the rat hippocampus measured by atomic force microscope indentation,” J. Neurotrauma24(5), 812–822 (2007).
[CrossRef] [PubMed]

Elson, E. L.

T. Eschenhagen, C. Fink, U. Remmers, H. Scholz, J. Wattchow, J. Weil, W. Zimmermann, H. H. Dohmen, H. Schäfer, N. Bishopric, T. Wakatsuki, and E. L. Elson, “Three-dimensional reconstitution of embryonic cardiomyocytes in a collagen matrix: a new heart muscle model system,” FASEB J.11(8), 683–694 (1997).
[PubMed]

Eschenhagen, T.

T. Eschenhagen, C. Fink, U. Remmers, H. Scholz, J. Wattchow, J. Weil, W. Zimmermann, H. H. Dohmen, H. Schäfer, N. Bishopric, T. Wakatsuki, and E. L. Elson, “Three-dimensional reconstitution of embryonic cardiomyocytes in a collagen matrix: a new heart muscle model system,” FASEB J.11(8), 683–694 (1997).
[PubMed]

Fang, J.

X. Shi, L. Qin, X. Zhang, K. He, C. Xiong, J. Fang, X. Fang, and Y. Zhang, “Elasticity of cardiac cells on the polymer substrates with different stiffness: an atomic force microscopy study,” Phys. Chem. Chem. Phys.13(16), 7540–7545 (2011).
[CrossRef] [PubMed]

Fang, X.

X. Shi, L. Qin, X. Zhang, K. He, C. Xiong, J. Fang, X. Fang, and Y. Zhang, “Elasticity of cardiac cells on the polymer substrates with different stiffness: an atomic force microscopy study,” Phys. Chem. Chem. Phys.13(16), 7540–7545 (2011).
[CrossRef] [PubMed]

Feijen, J.

A. D. van der Meer, Y. Li, M. H. Duits, A. A. Poot, J. Feijen, and I. Vermes, “Shear stress induces a transient and VEGFR-2-dependent decrease in the motion of injected particles in endothelial cells,” Biorheology47(3-4), 179–192 (2010).
[PubMed]

Fink, C.

T. Eschenhagen, C. Fink, U. Remmers, H. Scholz, J. Wattchow, J. Weil, W. Zimmermann, H. H. Dohmen, H. Schäfer, N. Bishopric, T. Wakatsuki, and E. L. Elson, “Three-dimensional reconstitution of embryonic cardiomyocytes in a collagen matrix: a new heart muscle model system,” FASEB J.11(8), 683–694 (1997).
[PubMed]

Ford, T.

Ford, T. N.

S. Santos, K. K. Chu, D. Lim, N. Bozinovic, T. N. Ford, C. Hourtoule, A. C. Bartoo, S. K. Singh, and J. Mertz, “Optically sectioned fluorescence endomicroscopy with hybrid-illumination imaging through a flexible fiber bundle,” J. Biomed. Opt.14(3), 030502 (2009).
[CrossRef] [PubMed]

Fudge, D.

D. Fudge, D. Russell, D. Beriault, W. Moore, E. B. Lane, and A. W. Vogl, “The intermediate filament network in cultured human keratinocytes is remarkably extensible and resilient,” PLoS ONE3(6), e2327 (2008).
[CrossRef] [PubMed]

Ganz, A.

A. Ganz, M. Lambert, A. Saez, P. Silberzan, A. Buguin, R. M. Mège, and B. Ladoux, “Traction forces exerted through N-cadherin contacts,” Biol. Cell98(12), 721–730 (2006).
[CrossRef] [PubMed]

Gardel, M. L.

V. Maruthamuthu, B. Sabass, U. S. Schwarz, and M. L. Gardel, “Cell-ECM traction force modulates endogenous tension at cell-cell contacts,” Proc. Natl. Acad. Sci. U.S.A.108(12), 4708–4713 (2011).
[CrossRef] [PubMed]

Georges, P. C.

J. Solon, I. Levental, K. Sengupta, P. C. Georges, and P. A. Janmey, “Fibroblast adaptation and stiffness matching to soft elastic substrates,” Biophys. J.93(12), 4453–4461 (2007).
[CrossRef] [PubMed]

Goetze, B.

M. F. Langhorst, J. Schaffer, and B. Goetze, “Structure brings clarity: structured illumination microscopy in cell biology,” Biotechnol. J.4(6), 858–865 (2009).
[CrossRef] [PubMed]

Gratton, E.

V. Levi, Q. Ruan, and E. Gratton, “3-D particle tracking in a two-photon microscope: application to the study of molecular dynamics in cells,” Biophys. J.88(4), 2919–2928 (2005).
[CrossRef] [PubMed]

Grier, D. G.

J. C. Crocker and D. G. Grier, “When like charges attract: the effects of geometrical confinement on long-range colloidal interactions,” Phys. Rev. Lett.77(9), 1897–1900 (1996).
[CrossRef] [PubMed]

Hale, C. M.

P. J. Stewart-Hutchinson, C. M. Hale, D. Wirtz, and D. Hodzic, “Structural requirements for the assembly of LINC complexes and their function in cellular mechanical stiffness,” Exp. Cell Res.314(8), 1892–1905 (2008).
[CrossRef] [PubMed]

C. M. Hale, A. L. Shrestha, S. B. Khatau, P. J. Stewart-Hutchinson, L. Hernandez, C. L. Stewart, D. Hodzic, and D. Wirtz, “Dysfunctional connections between the nucleus and the actin and microtubule networks in laminopathic models,” Biophys. J.95(11), 5462–5475 (2008).
[CrossRef] [PubMed]

J. S. Lee, P. Panorchan, C. M. Hale, S. B. Khatau, T. P. Kole, Y. Tseng, and D. Wirtz, “Ballistic intracellular nanorheology reveals ROCK-hard cytoplasmic stiffening response to fluid flow,” J. Cell Sci.119(9), 1760–1768 (2006).
[CrossRef] [PubMed]

Hayashida, Y.

K. Nishida, M. Yamato, Y. Hayashida, K. Watanabe, K. Yamamoto, E. Adachi, S. Nagai, A. Kikuchi, N. Maeda, H. Watanabe, T. Okano, and Y. Tano, “Corneal reconstruction with tissue-engineered cell sheets composed of autologous oral mucosal epithelium,” N. Engl. J. Med.351(12), 1187–1196 (2004).
[CrossRef] [PubMed]

He, K.

X. Shi, L. Qin, X. Zhang, K. He, C. Xiong, J. Fang, X. Fang, and Y. Zhang, “Elasticity of cardiac cells on the polymer substrates with different stiffness: an atomic force microscopy study,” Phys. Chem. Chem. Phys.13(16), 7540–7545 (2011).
[CrossRef] [PubMed]

Hernandez, L.

C. M. Hale, A. L. Shrestha, S. B. Khatau, P. J. Stewart-Hutchinson, L. Hernandez, C. L. Stewart, D. Hodzic, and D. Wirtz, “Dysfunctional connections between the nucleus and the actin and microtubule networks in laminopathic models,” Biophys. J.95(11), 5462–5475 (2008).
[CrossRef] [PubMed]

Hodzic, D.

C. M. Hale, A. L. Shrestha, S. B. Khatau, P. J. Stewart-Hutchinson, L. Hernandez, C. L. Stewart, D. Hodzic, and D. Wirtz, “Dysfunctional connections between the nucleus and the actin and microtubule networks in laminopathic models,” Biophys. J.95(11), 5462–5475 (2008).
[CrossRef] [PubMed]

P. J. Stewart-Hutchinson, C. M. Hale, D. Wirtz, and D. Hodzic, “Structural requirements for the assembly of LINC complexes and their function in cellular mechanical stiffness,” Exp. Cell Res.314(8), 1892–1905 (2008).
[CrossRef] [PubMed]

Hoffman, B. D.

J. C. Crocker and B. D. Hoffman, “Multiple-particle tracking and two-point microrheology in cells,” Methods Cell Biol.83, 141–178 (2007).
[CrossRef] [PubMed]

A. W. Lau, B. D. Hoffman, A. Davies, J. C. Crocker, and T. C. Lubensky, “Microrheology, stress fluctuations, and active behavior of living cells,” Phys. Rev. Lett.91(19), 198101 (2003).
[CrossRef] [PubMed]

Horkay, F.

D. C. Lin, E. K. Dimitriadis, and F. Horkay, “Robust strategies for automated AFM force curve analysis--I. Non-adhesive indentation of soft, inhomogeneous materials,” J. Biomech. Eng.129(3), 430–440 (2007).
[CrossRef] [PubMed]

Hourtoule, C.

S. Santos, K. K. Chu, D. Lim, N. Bozinovic, T. N. Ford, C. Hourtoule, A. C. Bartoo, S. K. Singh, and J. Mertz, “Optically sectioned fluorescence endomicroscopy with hybrid-illumination imaging through a flexible fiber bundle,” J. Biomed. Opt.14(3), 030502 (2009).
[CrossRef] [PubMed]

Huang, H.

M. Jonas, H. Huang, R. D. Kamm, and P. T. So, “Fast fluorescence laser tracking microrheometry, II: quantitative studies of cytoskeletal mechanotransduction,” Biophys. J.95(2), 895–909 (2008).
[CrossRef] [PubMed]

H. Huang, A. Asimaki, D. Lo, W. McKenna, and J. Saffitz, “Disparate effects of different mutations in plakoglobin on cell mechanical behavior,” Cell Motil. Cytoskeleton65(12), 964–978 (2008).
[CrossRef] [PubMed]

Ishaug, S. L.

S. L. Ishaug, G. M. Crane, M. J. Miller, A. W. Yasko, M. J. Yaszemski, and A. G. Mikos, “Bone formation by three-dimensional stromal osteoblast culture in biodegradable polymer scaffolds,” J. Biomed. Mater. Res.36(1), 17–28 (1997).
[CrossRef] [PubMed]

Ishaug-Riley, S. L.

S. L. Ishaug-Riley, G. M. Crane-Kruger, M. J. Yaszemski, and A. G. Mikos, “Three-dimensional culture of rat calvarial osteoblasts in porous biodegradable polymers,” Biomaterials19(15), 1405–1412 (1998).
[CrossRef] [PubMed]

Janmey, P. A.

J. Solon, I. Levental, K. Sengupta, P. C. Georges, and P. A. Janmey, “Fibroblast adaptation and stiffness matching to soft elastic substrates,” Biophys. J.93(12), 4453–4461 (2007).
[CrossRef] [PubMed]

Jiang, I.

T. P. Kole, Y. Tseng, I. Jiang, J. L. Katz, and D. Wirtz, “Intracellular mechanics of migrating fibroblasts,” Mol. Biol. Cell16(1), 328–338 (2005).
[CrossRef] [PubMed]

Jonas, M.

M. Jonas, H. Huang, R. D. Kamm, and P. T. So, “Fast fluorescence laser tracking microrheometry, II: quantitative studies of cytoskeletal mechanotransduction,” Biophys. J.95(2), 895–909 (2008).
[CrossRef] [PubMed]

Juskaitis, R.

Kamm, R. D.

M. Jonas, H. Huang, R. D. Kamm, and P. T. So, “Fast fluorescence laser tracking microrheometry, II: quantitative studies of cytoskeletal mechanotransduction,” Biophys. J.95(2), 895–909 (2008).
[CrossRef] [PubMed]

J. Lammerding, P. C. Schulze, T. Takahashi, S. Kozlov, T. Sullivan, R. D. Kamm, C. L. Stewart, and R. T. Lee, “Lamin A/C deficiency causes defective nuclear mechanics and mechanotransduction,” J. Clin. Invest.113(3), 370–378 (2004).
[PubMed]

Kao, H. P.

H. P. Kao and A. S. Verkman, “Tracking of single fluorescent particles in three dimensions: use of cylindrical optics to encode particle position,” Biophys. J.67(3), 1291–1300 (1994).
[CrossRef] [PubMed]

Karpova, T.

J. G. McNally, T. Karpova, J. Cooper, and J. A. Conchello, “Three-dimensional imaging by deconvolution microscopy,” Methods19(3), 373–385 (1999).
[CrossRef] [PubMed]

Katz, J. L.

T. P. Kole, Y. Tseng, I. Jiang, J. L. Katz, and D. Wirtz, “Intracellular mechanics of migrating fibroblasts,” Mol. Biol. Cell16(1), 328–338 (2005).
[CrossRef] [PubMed]

Khatau, S. B.

C. M. Hale, A. L. Shrestha, S. B. Khatau, P. J. Stewart-Hutchinson, L. Hernandez, C. L. Stewart, D. Hodzic, and D. Wirtz, “Dysfunctional connections between the nucleus and the actin and microtubule networks in laminopathic models,” Biophys. J.95(11), 5462–5475 (2008).
[CrossRef] [PubMed]

J. S. Lee, P. Panorchan, C. M. Hale, S. B. Khatau, T. P. Kole, Y. Tseng, and D. Wirtz, “Ballistic intracellular nanorheology reveals ROCK-hard cytoplasmic stiffening response to fluid flow,” J. Cell Sci.119(9), 1760–1768 (2006).
[CrossRef] [PubMed]

Kikuchi, A.

K. Nishida, M. Yamato, Y. Hayashida, K. Watanabe, K. Yamamoto, E. Adachi, S. Nagai, A. Kikuchi, N. Maeda, H. Watanabe, T. Okano, and Y. Tano, “Corneal reconstruction with tissue-engineered cell sheets composed of autologous oral mucosal epithelium,” N. Engl. J. Med.351(12), 1187–1196 (2004).
[CrossRef] [PubMed]

Kim, J.

J. Mertz and J. Kim, “Scanning light-sheet microscopy in the whole mouse brain with HiLo background rejection,” J. Biomed. Opt.15(1), 016027 (2010).
[CrossRef] [PubMed]

Kole, T. P.

P. Panorchan, J. S. Lee, B. R. Daniels, T. P. Kole, Y. Tseng, and D. Wirtz, “Probing cellular mechanical responses to stimuli using ballistic intracellular nanorheology,” Methods Cell Biol.83, 113–140 (2007).
[CrossRef] [PubMed]

J. S. Lee, P. Panorchan, C. M. Hale, S. B. Khatau, T. P. Kole, Y. Tseng, and D. Wirtz, “Ballistic intracellular nanorheology reveals ROCK-hard cytoplasmic stiffening response to fluid flow,” J. Cell Sci.119(9), 1760–1768 (2006).
[CrossRef] [PubMed]

T. P. Kole, Y. Tseng, I. Jiang, J. L. Katz, and D. Wirtz, “Intracellular mechanics of migrating fibroblasts,” Mol. Biol. Cell16(1), 328–338 (2005).
[CrossRef] [PubMed]

Y. Tseng, T. P. Kole, and D. Wirtz, “Micromechanical mapping of live cells by multiple-particle-tracking microrheology,” Biophys. J.83(6), 3162–3176 (2002).
[CrossRef] [PubMed]

Kozlov, S.

J. Lammerding, P. C. Schulze, T. Takahashi, S. Kozlov, T. Sullivan, R. D. Kamm, C. L. Stewart, and R. T. Lee, “Lamin A/C deficiency causes defective nuclear mechanics and mechanotransduction,” J. Clin. Invest.113(3), 370–378 (2004).
[PubMed]

Ladoux, B.

A. Ganz, M. Lambert, A. Saez, P. Silberzan, A. Buguin, R. M. Mège, and B. Ladoux, “Traction forces exerted through N-cadherin contacts,” Biol. Cell98(12), 721–730 (2006).
[CrossRef] [PubMed]

Lambert, M.

A. Ganz, M. Lambert, A. Saez, P. Silberzan, A. Buguin, R. M. Mège, and B. Ladoux, “Traction forces exerted through N-cadherin contacts,” Biol. Cell98(12), 721–730 (2006).
[CrossRef] [PubMed]

Lammerding, J.

J. Lammerding, P. C. Schulze, T. Takahashi, S. Kozlov, T. Sullivan, R. D. Kamm, C. L. Stewart, and R. T. Lee, “Lamin A/C deficiency causes defective nuclear mechanics and mechanotransduction,” J. Clin. Invest.113(3), 370–378 (2004).
[PubMed]

Lane, E. B.

D. Fudge, D. Russell, D. Beriault, W. Moore, E. B. Lane, and A. W. Vogl, “The intermediate filament network in cultured human keratinocytes is remarkably extensible and resilient,” PLoS ONE3(6), e2327 (2008).
[CrossRef] [PubMed]

Langhorst, M. F.

M. F. Langhorst, J. Schaffer, and B. Goetze, “Structure brings clarity: structured illumination microscopy in cell biology,” Biotechnol. J.4(6), 858–865 (2009).
[CrossRef] [PubMed]

Lau, A. W.

A. W. Lau, B. D. Hoffman, A. Davies, J. C. Crocker, and T. C. Lubensky, “Microrheology, stress fluctuations, and active behavior of living cells,” Phys. Rev. Lett.91(19), 198101 (2003).
[CrossRef] [PubMed]

Lee, J. S.

P. Panorchan, J. S. Lee, B. R. Daniels, T. P. Kole, Y. Tseng, and D. Wirtz, “Probing cellular mechanical responses to stimuli using ballistic intracellular nanorheology,” Methods Cell Biol.83, 113–140 (2007).
[CrossRef] [PubMed]

J. S. Lee, P. Panorchan, C. M. Hale, S. B. Khatau, T. P. Kole, Y. Tseng, and D. Wirtz, “Ballistic intracellular nanorheology reveals ROCK-hard cytoplasmic stiffening response to fluid flow,” J. Cell Sci.119(9), 1760–1768 (2006).
[CrossRef] [PubMed]

Lee, R. T.

J. Lammerding, P. C. Schulze, T. Takahashi, S. Kozlov, T. Sullivan, R. D. Kamm, C. L. Stewart, and R. T. Lee, “Lamin A/C deficiency causes defective nuclear mechanics and mechanotransduction,” J. Clin. Invest.113(3), 370–378 (2004).
[PubMed]

Levental, I.

J. Solon, I. Levental, K. Sengupta, P. C. Georges, and P. A. Janmey, “Fibroblast adaptation and stiffness matching to soft elastic substrates,” Biophys. J.93(12), 4453–4461 (2007).
[CrossRef] [PubMed]

Levi, V.

V. Levi, Q. Ruan, and E. Gratton, “3-D particle tracking in a two-photon microscope: application to the study of molecular dynamics in cells,” Biophys. J.88(4), 2919–2928 (2005).
[CrossRef] [PubMed]

Li, X.

Li, Y.

A. D. van der Meer, Y. Li, M. H. Duits, A. A. Poot, J. Feijen, and I. Vermes, “Shear stress induces a transient and VEGFR-2-dependent decrease in the motion of injected particles in endothelial cells,” Biorheology47(3-4), 179–192 (2010).
[PubMed]

Lim, D.

S. Santos, K. K. Chu, D. Lim, N. Bozinovic, T. N. Ford, C. Hourtoule, A. C. Bartoo, S. K. Singh, and J. Mertz, “Optically sectioned fluorescence endomicroscopy with hybrid-illumination imaging through a flexible fiber bundle,” J. Biomed. Opt.14(3), 030502 (2009).
[CrossRef] [PubMed]

D. Lim, K. K. Chu, and J. Mertz, “Wide-field fluorescence sectioning with hybrid speckle and uniform-illumination microscopy,” Opt. Lett.33(16), 1819–1821 (2008).
[CrossRef] [PubMed]

Lin, D. C.

D. C. Lin, E. K. Dimitriadis, and F. Horkay, “Robust strategies for automated AFM force curve analysis--I. Non-adhesive indentation of soft, inhomogeneous materials,” J. Biomech. Eng.129(3), 430–440 (2007).
[CrossRef] [PubMed]

Lo, D.

H. Huang, A. Asimaki, D. Lo, W. McKenna, and J. Saffitz, “Disparate effects of different mutations in plakoglobin on cell mechanical behavior,” Cell Motil. Cytoskeleton65(12), 964–978 (2008).
[CrossRef] [PubMed]

Lubensky, T. C.

A. W. Lau, B. D. Hoffman, A. Davies, J. C. Crocker, and T. C. Lubensky, “Microrheology, stress fluctuations, and active behavior of living cells,” Phys. Rev. Lett.91(19), 198101 (2003).
[CrossRef] [PubMed]

Maeda, N.

K. Nishida, M. Yamato, Y. Hayashida, K. Watanabe, K. Yamamoto, E. Adachi, S. Nagai, A. Kikuchi, N. Maeda, H. Watanabe, T. Okano, and Y. Tano, “Corneal reconstruction with tissue-engineered cell sheets composed of autologous oral mucosal epithelium,” N. Engl. J. Med.351(12), 1187–1196 (2004).
[CrossRef] [PubMed]

Maruthamuthu, V.

V. Maruthamuthu, B. Sabass, U. S. Schwarz, and M. L. Gardel, “Cell-ECM traction force modulates endogenous tension at cell-cell contacts,” Proc. Natl. Acad. Sci. U.S.A.108(12), 4708–4713 (2011).
[CrossRef] [PubMed]

Mason, T. G.

T. G. Mason, “Estimating the viscoelastic moduli of complex fluids using the generalized Stokes-Einstein equation,” Rheologica Acta39(4), 371–378 (2000).
[CrossRef]

McKenna, W.

H. Huang, A. Asimaki, D. Lo, W. McKenna, and J. Saffitz, “Disparate effects of different mutations in plakoglobin on cell mechanical behavior,” Cell Motil. Cytoskeleton65(12), 964–978 (2008).
[CrossRef] [PubMed]

McNally, J. G.

J. G. McNally, T. Karpova, J. Cooper, and J. A. Conchello, “Three-dimensional imaging by deconvolution microscopy,” Methods19(3), 373–385 (1999).
[CrossRef] [PubMed]

Mège, R. M.

A. Ganz, M. Lambert, A. Saez, P. Silberzan, A. Buguin, R. M. Mège, and B. Ladoux, “Traction forces exerted through N-cadherin contacts,” Biol. Cell98(12), 721–730 (2006).
[CrossRef] [PubMed]

Mertz, J.

J. Mertz and J. Kim, “Scanning light-sheet microscopy in the whole mouse brain with HiLo background rejection,” J. Biomed. Opt.15(1), 016027 (2010).
[CrossRef] [PubMed]

S. Santos, K. K. Chu, D. Lim, N. Bozinovic, T. N. Ford, C. Hourtoule, A. C. Bartoo, S. K. Singh, and J. Mertz, “Optically sectioned fluorescence endomicroscopy with hybrid-illumination imaging through a flexible fiber bundle,” J. Biomed. Opt.14(3), 030502 (2009).
[CrossRef] [PubMed]

N. Bozinovic, C. Ventalon, T. Ford, and J. Mertz, “Fluorescence endomicroscopy with structured illumination,” Opt. Express16(11), 8016–8025 (2008).
[CrossRef] [PubMed]

D. Lim, K. K. Chu, and J. Mertz, “Wide-field fluorescence sectioning with hybrid speckle and uniform-illumination microscopy,” Opt. Lett.33(16), 1819–1821 (2008).
[CrossRef] [PubMed]

Mikos, A. G.

S. L. Ishaug-Riley, G. M. Crane-Kruger, M. J. Yaszemski, and A. G. Mikos, “Three-dimensional culture of rat calvarial osteoblasts in porous biodegradable polymers,” Biomaterials19(15), 1405–1412 (1998).
[CrossRef] [PubMed]

S. L. Ishaug, G. M. Crane, M. J. Miller, A. W. Yasko, M. J. Yaszemski, and A. G. Mikos, “Bone formation by three-dimensional stromal osteoblast culture in biodegradable polymer scaffolds,” J. Biomed. Mater. Res.36(1), 17–28 (1997).
[CrossRef] [PubMed]

Miller, M. J.

S. L. Ishaug, G. M. Crane, M. J. Miller, A. W. Yasko, M. J. Yaszemski, and A. G. Mikos, “Bone formation by three-dimensional stromal osteoblast culture in biodegradable polymer scaffolds,” J. Biomed. Mater. Res.36(1), 17–28 (1997).
[CrossRef] [PubMed]

Moore, W.

D. Fudge, D. Russell, D. Beriault, W. Moore, E. B. Lane, and A. W. Vogl, “The intermediate filament network in cultured human keratinocytes is remarkably extensible and resilient,” PLoS ONE3(6), e2327 (2008).
[CrossRef] [PubMed]

Morrison, B.

B. S. Elkin, E. U. Azeloglu, K. D. Costa, and B. Morrison, “Mechanical heterogeneity of the rat hippocampus measured by atomic force microscope indentation,” J. Neurotrauma24(5), 812–822 (2007).
[CrossRef] [PubMed]

Nagai, S.

K. Nishida, M. Yamato, Y. Hayashida, K. Watanabe, K. Yamamoto, E. Adachi, S. Nagai, A. Kikuchi, N. Maeda, H. Watanabe, T. Okano, and Y. Tano, “Corneal reconstruction with tissue-engineered cell sheets composed of autologous oral mucosal epithelium,” N. Engl. J. Med.351(12), 1187–1196 (2004).
[CrossRef] [PubMed]

Neil, M. A.

Nishida, K.

K. Nishida, M. Yamato, Y. Hayashida, K. Watanabe, K. Yamamoto, E. Adachi, S. Nagai, A. Kikuchi, N. Maeda, H. Watanabe, T. Okano, and Y. Tano, “Corneal reconstruction with tissue-engineered cell sheets composed of autologous oral mucosal epithelium,” N. Engl. J. Med.351(12), 1187–1196 (2004).
[CrossRef] [PubMed]

Ober, R. J.

P. Prabhat, S. Ram, E. S. Ward, and R. J. Ober, “Simultaneous imaging of different focal planes in fluorescence microscopy for the study of cellular dynamics in three dimensions,” IEEE Trans. Nanobioscience3(4), 237–242 (2004).
[CrossRef] [PubMed]

Okano, T.

K. Nishida, M. Yamato, Y. Hayashida, K. Watanabe, K. Yamamoto, E. Adachi, S. Nagai, A. Kikuchi, N. Maeda, H. Watanabe, T. Okano, and Y. Tano, “Corneal reconstruction with tissue-engineered cell sheets composed of autologous oral mucosal epithelium,” N. Engl. J. Med.351(12), 1187–1196 (2004).
[CrossRef] [PubMed]

Pai, A.

A. Pai, P. Sundd, and D. F. Tees, “In situ microrheological determination of neutrophil stiffening following adhesion in a model capillary,” Ann. Biomed. Eng.36(4), 596–603 (2008).
[CrossRef] [PubMed]

Panorchan, P.

P. Panorchan, J. S. Lee, B. R. Daniels, T. P. Kole, Y. Tseng, and D. Wirtz, “Probing cellular mechanical responses to stimuli using ballistic intracellular nanorheology,” Methods Cell Biol.83, 113–140 (2007).
[CrossRef] [PubMed]

J. S. Lee, P. Panorchan, C. M. Hale, S. B. Khatau, T. P. Kole, Y. Tseng, and D. Wirtz, “Ballistic intracellular nanorheology reveals ROCK-hard cytoplasmic stiffening response to fluid flow,” J. Cell Sci.119(9), 1760–1768 (2006).
[CrossRef] [PubMed]

Poot, A. A.

A. D. van der Meer, Y. Li, M. H. Duits, A. A. Poot, J. Feijen, and I. Vermes, “Shear stress induces a transient and VEGFR-2-dependent decrease in the motion of injected particles in endothelial cells,” Biorheology47(3-4), 179–192 (2010).
[PubMed]

Prabhat, P.

P. Prabhat, S. Ram, E. S. Ward, and R. J. Ober, “Simultaneous imaging of different focal planes in fluorescence microscopy for the study of cellular dynamics in three dimensions,” IEEE Trans. Nanobioscience3(4), 237–242 (2004).
[CrossRef] [PubMed]

Qin, L.

X. Shi, L. Qin, X. Zhang, K. He, C. Xiong, J. Fang, X. Fang, and Y. Zhang, “Elasticity of cardiac cells on the polymer substrates with different stiffness: an atomic force microscopy study,” Phys. Chem. Chem. Phys.13(16), 7540–7545 (2011).
[CrossRef] [PubMed]

Ram, S.

P. Prabhat, S. Ram, E. S. Ward, and R. J. Ober, “Simultaneous imaging of different focal planes in fluorescence microscopy for the study of cellular dynamics in three dimensions,” IEEE Trans. Nanobioscience3(4), 237–242 (2004).
[CrossRef] [PubMed]

Remmers, U.

T. Eschenhagen, C. Fink, U. Remmers, H. Scholz, J. Wattchow, J. Weil, W. Zimmermann, H. H. Dohmen, H. Schäfer, N. Bishopric, T. Wakatsuki, and E. L. Elson, “Three-dimensional reconstitution of embryonic cardiomyocytes in a collagen matrix: a new heart muscle model system,” FASEB J.11(8), 683–694 (1997).
[PubMed]

Ruan, Q.

V. Levi, Q. Ruan, and E. Gratton, “3-D particle tracking in a two-photon microscope: application to the study of molecular dynamics in cells,” Biophys. J.88(4), 2919–2928 (2005).
[CrossRef] [PubMed]

Russell, D.

D. Fudge, D. Russell, D. Beriault, W. Moore, E. B. Lane, and A. W. Vogl, “The intermediate filament network in cultured human keratinocytes is remarkably extensible and resilient,” PLoS ONE3(6), e2327 (2008).
[CrossRef] [PubMed]

Sabass, B.

V. Maruthamuthu, B. Sabass, U. S. Schwarz, and M. L. Gardel, “Cell-ECM traction force modulates endogenous tension at cell-cell contacts,” Proc. Natl. Acad. Sci. U.S.A.108(12), 4708–4713 (2011).
[CrossRef] [PubMed]

Saez, A.

A. Ganz, M. Lambert, A. Saez, P. Silberzan, A. Buguin, R. M. Mège, and B. Ladoux, “Traction forces exerted through N-cadherin contacts,” Biol. Cell98(12), 721–730 (2006).
[CrossRef] [PubMed]

Saffitz, J.

H. Huang, A. Asimaki, D. Lo, W. McKenna, and J. Saffitz, “Disparate effects of different mutations in plakoglobin on cell mechanical behavior,” Cell Motil. Cytoskeleton65(12), 964–978 (2008).
[CrossRef] [PubMed]

Santos, S.

S. Santos, K. K. Chu, D. Lim, N. Bozinovic, T. N. Ford, C. Hourtoule, A. C. Bartoo, S. K. Singh, and J. Mertz, “Optically sectioned fluorescence endomicroscopy with hybrid-illumination imaging through a flexible fiber bundle,” J. Biomed. Opt.14(3), 030502 (2009).
[CrossRef] [PubMed]

Schäfer, H.

T. Eschenhagen, C. Fink, U. Remmers, H. Scholz, J. Wattchow, J. Weil, W. Zimmermann, H. H. Dohmen, H. Schäfer, N. Bishopric, T. Wakatsuki, and E. L. Elson, “Three-dimensional reconstitution of embryonic cardiomyocytes in a collagen matrix: a new heart muscle model system,” FASEB J.11(8), 683–694 (1997).
[PubMed]

Schaffer, J.

M. F. Langhorst, J. Schaffer, and B. Goetze, “Structure brings clarity: structured illumination microscopy in cell biology,” Biotechnol. J.4(6), 858–865 (2009).
[CrossRef] [PubMed]

Scholz, H.

T. Eschenhagen, C. Fink, U. Remmers, H. Scholz, J. Wattchow, J. Weil, W. Zimmermann, H. H. Dohmen, H. Schäfer, N. Bishopric, T. Wakatsuki, and E. L. Elson, “Three-dimensional reconstitution of embryonic cardiomyocytes in a collagen matrix: a new heart muscle model system,” FASEB J.11(8), 683–694 (1997).
[PubMed]

Schulze, P. C.

J. Lammerding, P. C. Schulze, T. Takahashi, S. Kozlov, T. Sullivan, R. D. Kamm, C. L. Stewart, and R. T. Lee, “Lamin A/C deficiency causes defective nuclear mechanics and mechanotransduction,” J. Clin. Invest.113(3), 370–378 (2004).
[PubMed]

Schwarz, U. S.

V. Maruthamuthu, B. Sabass, U. S. Schwarz, and M. L. Gardel, “Cell-ECM traction force modulates endogenous tension at cell-cell contacts,” Proc. Natl. Acad. Sci. U.S.A.108(12), 4708–4713 (2011).
[CrossRef] [PubMed]

Sengupta, K.

J. Solon, I. Levental, K. Sengupta, P. C. Georges, and P. A. Janmey, “Fibroblast adaptation and stiffness matching to soft elastic substrates,” Biophys. J.93(12), 4453–4461 (2007).
[CrossRef] [PubMed]

Shi, X.

X. Shi, L. Qin, X. Zhang, K. He, C. Xiong, J. Fang, X. Fang, and Y. Zhang, “Elasticity of cardiac cells on the polymer substrates with different stiffness: an atomic force microscopy study,” Phys. Chem. Chem. Phys.13(16), 7540–7545 (2011).
[CrossRef] [PubMed]

Shrestha, A. L.

C. M. Hale, A. L. Shrestha, S. B. Khatau, P. J. Stewart-Hutchinson, L. Hernandez, C. L. Stewart, D. Hodzic, and D. Wirtz, “Dysfunctional connections between the nucleus and the actin and microtubule networks in laminopathic models,” Biophys. J.95(11), 5462–5475 (2008).
[CrossRef] [PubMed]

Silberzan, P.

A. Ganz, M. Lambert, A. Saez, P. Silberzan, A. Buguin, R. M. Mège, and B. Ladoux, “Traction forces exerted through N-cadherin contacts,” Biol. Cell98(12), 721–730 (2006).
[CrossRef] [PubMed]

Singh, S. K.

S. Santos, K. K. Chu, D. Lim, N. Bozinovic, T. N. Ford, C. Hourtoule, A. C. Bartoo, S. K. Singh, and J. Mertz, “Optically sectioned fluorescence endomicroscopy with hybrid-illumination imaging through a flexible fiber bundle,” J. Biomed. Opt.14(3), 030502 (2009).
[CrossRef] [PubMed]

So, P. T.

M. Jonas, H. Huang, R. D. Kamm, and P. T. So, “Fast fluorescence laser tracking microrheometry, II: quantitative studies of cytoskeletal mechanotransduction,” Biophys. J.95(2), 895–909 (2008).
[CrossRef] [PubMed]

Solon, J.

J. Solon, I. Levental, K. Sengupta, P. C. Georges, and P. A. Janmey, “Fibroblast adaptation and stiffness matching to soft elastic substrates,” Biophys. J.93(12), 4453–4461 (2007).
[CrossRef] [PubMed]

Stewart, C. L.

C. M. Hale, A. L. Shrestha, S. B. Khatau, P. J. Stewart-Hutchinson, L. Hernandez, C. L. Stewart, D. Hodzic, and D. Wirtz, “Dysfunctional connections between the nucleus and the actin and microtubule networks in laminopathic models,” Biophys. J.95(11), 5462–5475 (2008).
[CrossRef] [PubMed]

J. Lammerding, P. C. Schulze, T. Takahashi, S. Kozlov, T. Sullivan, R. D. Kamm, C. L. Stewart, and R. T. Lee, “Lamin A/C deficiency causes defective nuclear mechanics and mechanotransduction,” J. Clin. Invest.113(3), 370–378 (2004).
[PubMed]

Stewart-Hutchinson, P. J.

C. M. Hale, A. L. Shrestha, S. B. Khatau, P. J. Stewart-Hutchinson, L. Hernandez, C. L. Stewart, D. Hodzic, and D. Wirtz, “Dysfunctional connections between the nucleus and the actin and microtubule networks in laminopathic models,” Biophys. J.95(11), 5462–5475 (2008).
[CrossRef] [PubMed]

P. J. Stewart-Hutchinson, C. M. Hale, D. Wirtz, and D. Hodzic, “Structural requirements for the assembly of LINC complexes and their function in cellular mechanical stiffness,” Exp. Cell Res.314(8), 1892–1905 (2008).
[CrossRef] [PubMed]

Sullivan, T.

J. Lammerding, P. C. Schulze, T. Takahashi, S. Kozlov, T. Sullivan, R. D. Kamm, C. L. Stewart, and R. T. Lee, “Lamin A/C deficiency causes defective nuclear mechanics and mechanotransduction,” J. Clin. Invest.113(3), 370–378 (2004).
[PubMed]

Sundd, P.

A. Pai, P. Sundd, and D. F. Tees, “In situ microrheological determination of neutrophil stiffening following adhesion in a model capillary,” Ann. Biomed. Eng.36(4), 596–603 (2008).
[CrossRef] [PubMed]

Takahashi, T.

J. Lammerding, P. C. Schulze, T. Takahashi, S. Kozlov, T. Sullivan, R. D. Kamm, C. L. Stewart, and R. T. Lee, “Lamin A/C deficiency causes defective nuclear mechanics and mechanotransduction,” J. Clin. Invest.113(3), 370–378 (2004).
[PubMed]

Tano, Y.

K. Nishida, M. Yamato, Y. Hayashida, K. Watanabe, K. Yamamoto, E. Adachi, S. Nagai, A. Kikuchi, N. Maeda, H. Watanabe, T. Okano, and Y. Tano, “Corneal reconstruction with tissue-engineered cell sheets composed of autologous oral mucosal epithelium,” N. Engl. J. Med.351(12), 1187–1196 (2004).
[CrossRef] [PubMed]

Tees, D. F.

A. Pai, P. Sundd, and D. F. Tees, “In situ microrheological determination of neutrophil stiffening following adhesion in a model capillary,” Ann. Biomed. Eng.36(4), 596–603 (2008).
[CrossRef] [PubMed]

Truskey, G. A.

L. Cao, A. Wu, and G. A. Truskey, “Biomechanical effects of flow and coculture on human aortic and cord blood-derived endothelial cells,” J. Biomech.44(11), 2150–2157 (2011).
[CrossRef] [PubMed]

Tseng, Y.

P. H. Wu, S. H. Arce, P. R. Burney, and Y. Tseng, “A novel approach to high accuracy of video-based microrheology,” Biophys. J.96(12), 5103–5111 (2009).
[CrossRef] [PubMed]

P. Panorchan, J. S. Lee, B. R. Daniels, T. P. Kole, Y. Tseng, and D. Wirtz, “Probing cellular mechanical responses to stimuli using ballistic intracellular nanorheology,” Methods Cell Biol.83, 113–140 (2007).
[CrossRef] [PubMed]

J. S. Lee, P. Panorchan, C. M. Hale, S. B. Khatau, T. P. Kole, Y. Tseng, and D. Wirtz, “Ballistic intracellular nanorheology reveals ROCK-hard cytoplasmic stiffening response to fluid flow,” J. Cell Sci.119(9), 1760–1768 (2006).
[CrossRef] [PubMed]

T. P. Kole, Y. Tseng, I. Jiang, J. L. Katz, and D. Wirtz, “Intracellular mechanics of migrating fibroblasts,” Mol. Biol. Cell16(1), 328–338 (2005).
[CrossRef] [PubMed]

Y. Tseng, T. P. Kole, and D. Wirtz, “Micromechanical mapping of live cells by multiple-particle-tracking microrheology,” Biophys. J.83(6), 3162–3176 (2002).
[CrossRef] [PubMed]

van der Meer, A. D.

A. D. van der Meer, Y. Li, M. H. Duits, A. A. Poot, J. Feijen, and I. Vermes, “Shear stress induces a transient and VEGFR-2-dependent decrease in the motion of injected particles in endothelial cells,” Biorheology47(3-4), 179–192 (2010).
[PubMed]

Ventalon, C.

Verkman, A. S.

H. P. Kao and A. S. Verkman, “Tracking of single fluorescent particles in three dimensions: use of cylindrical optics to encode particle position,” Biophys. J.67(3), 1291–1300 (1994).
[CrossRef] [PubMed]

Vermes, I.

A. D. van der Meer, Y. Li, M. H. Duits, A. A. Poot, J. Feijen, and I. Vermes, “Shear stress induces a transient and VEGFR-2-dependent decrease in the motion of injected particles in endothelial cells,” Biorheology47(3-4), 179–192 (2010).
[PubMed]

Vogl, A. W.

D. Fudge, D. Russell, D. Beriault, W. Moore, E. B. Lane, and A. W. Vogl, “The intermediate filament network in cultured human keratinocytes is remarkably extensible and resilient,” PLoS ONE3(6), e2327 (2008).
[CrossRef] [PubMed]

Wakatsuki, T.

T. Eschenhagen, C. Fink, U. Remmers, H. Scholz, J. Wattchow, J. Weil, W. Zimmermann, H. H. Dohmen, H. Schäfer, N. Bishopric, T. Wakatsuki, and E. L. Elson, “Three-dimensional reconstitution of embryonic cardiomyocytes in a collagen matrix: a new heart muscle model system,” FASEB J.11(8), 683–694 (1997).
[PubMed]

Wang, Y. M.

Ward, E. S.

P. Prabhat, S. Ram, E. S. Ward, and R. J. Ober, “Simultaneous imaging of different focal planes in fluorescence microscopy for the study of cellular dynamics in three dimensions,” IEEE Trans. Nanobioscience3(4), 237–242 (2004).
[CrossRef] [PubMed]

Watanabe, H.

K. Nishida, M. Yamato, Y. Hayashida, K. Watanabe, K. Yamamoto, E. Adachi, S. Nagai, A. Kikuchi, N. Maeda, H. Watanabe, T. Okano, and Y. Tano, “Corneal reconstruction with tissue-engineered cell sheets composed of autologous oral mucosal epithelium,” N. Engl. J. Med.351(12), 1187–1196 (2004).
[CrossRef] [PubMed]

Watanabe, K.

K. Nishida, M. Yamato, Y. Hayashida, K. Watanabe, K. Yamamoto, E. Adachi, S. Nagai, A. Kikuchi, N. Maeda, H. Watanabe, T. Okano, and Y. Tano, “Corneal reconstruction with tissue-engineered cell sheets composed of autologous oral mucosal epithelium,” N. Engl. J. Med.351(12), 1187–1196 (2004).
[CrossRef] [PubMed]

Wattchow, J.

T. Eschenhagen, C. Fink, U. Remmers, H. Scholz, J. Wattchow, J. Weil, W. Zimmermann, H. H. Dohmen, H. Schäfer, N. Bishopric, T. Wakatsuki, and E. L. Elson, “Three-dimensional reconstitution of embryonic cardiomyocytes in a collagen matrix: a new heart muscle model system,” FASEB J.11(8), 683–694 (1997).
[PubMed]

Weil, J.

T. Eschenhagen, C. Fink, U. Remmers, H. Scholz, J. Wattchow, J. Weil, W. Zimmermann, H. H. Dohmen, H. Schäfer, N. Bishopric, T. Wakatsuki, and E. L. Elson, “Three-dimensional reconstitution of embryonic cardiomyocytes in a collagen matrix: a new heart muscle model system,” FASEB J.11(8), 683–694 (1997).
[PubMed]

Wells, R. G.

R. G. Wells, “The role of matrix stiffness in regulating cell behavior,” Hepatology47(4), 1394–1400 (2008).
[CrossRef] [PubMed]

Wilson, T.

Wirtz, D.

D. Wirtz, “Particle-tracking microrheology of living cells: principles and applications,” Annu Rev Biophys38(1), 301–326 (2009).
[CrossRef] [PubMed]

C. M. Hale, A. L. Shrestha, S. B. Khatau, P. J. Stewart-Hutchinson, L. Hernandez, C. L. Stewart, D. Hodzic, and D. Wirtz, “Dysfunctional connections between the nucleus and the actin and microtubule networks in laminopathic models,” Biophys. J.95(11), 5462–5475 (2008).
[CrossRef] [PubMed]

P. J. Stewart-Hutchinson, C. M. Hale, D. Wirtz, and D. Hodzic, “Structural requirements for the assembly of LINC complexes and their function in cellular mechanical stiffness,” Exp. Cell Res.314(8), 1892–1905 (2008).
[CrossRef] [PubMed]

P. Panorchan, J. S. Lee, B. R. Daniels, T. P. Kole, Y. Tseng, and D. Wirtz, “Probing cellular mechanical responses to stimuli using ballistic intracellular nanorheology,” Methods Cell Biol.83, 113–140 (2007).
[CrossRef] [PubMed]

J. S. Lee, P. Panorchan, C. M. Hale, S. B. Khatau, T. P. Kole, Y. Tseng, and D. Wirtz, “Ballistic intracellular nanorheology reveals ROCK-hard cytoplasmic stiffening response to fluid flow,” J. Cell Sci.119(9), 1760–1768 (2006).
[CrossRef] [PubMed]

T. P. Kole, Y. Tseng, I. Jiang, J. L. Katz, and D. Wirtz, “Intracellular mechanics of migrating fibroblasts,” Mol. Biol. Cell16(1), 328–338 (2005).
[CrossRef] [PubMed]

Y. Tseng, T. P. Kole, and D. Wirtz, “Micromechanical mapping of live cells by multiple-particle-tracking microrheology,” Biophys. J.83(6), 3162–3176 (2002).
[CrossRef] [PubMed]

Wu, A.

L. Cao, A. Wu, and G. A. Truskey, “Biomechanical effects of flow and coculture on human aortic and cord blood-derived endothelial cells,” J. Biomech.44(11), 2150–2157 (2011).
[CrossRef] [PubMed]

Wu, P. H.

P. H. Wu, S. H. Arce, P. R. Burney, and Y. Tseng, “A novel approach to high accuracy of video-based microrheology,” Biophys. J.96(12), 5103–5111 (2009).
[CrossRef] [PubMed]

Xiong, C.

X. Shi, L. Qin, X. Zhang, K. He, C. Xiong, J. Fang, X. Fang, and Y. Zhang, “Elasticity of cardiac cells on the polymer substrates with different stiffness: an atomic force microscopy study,” Phys. Chem. Chem. Phys.13(16), 7540–7545 (2011).
[CrossRef] [PubMed]

Yamamoto, K.

K. Nishida, M. Yamato, Y. Hayashida, K. Watanabe, K. Yamamoto, E. Adachi, S. Nagai, A. Kikuchi, N. Maeda, H. Watanabe, T. Okano, and Y. Tano, “Corneal reconstruction with tissue-engineered cell sheets composed of autologous oral mucosal epithelium,” N. Engl. J. Med.351(12), 1187–1196 (2004).
[CrossRef] [PubMed]

Yamato, M.

K. Nishida, M. Yamato, Y. Hayashida, K. Watanabe, K. Yamamoto, E. Adachi, S. Nagai, A. Kikuchi, N. Maeda, H. Watanabe, T. Okano, and Y. Tano, “Corneal reconstruction with tissue-engineered cell sheets composed of autologous oral mucosal epithelium,” N. Engl. J. Med.351(12), 1187–1196 (2004).
[CrossRef] [PubMed]

Yasko, A. W.

S. L. Ishaug, G. M. Crane, M. J. Miller, A. W. Yasko, M. J. Yaszemski, and A. G. Mikos, “Bone formation by three-dimensional stromal osteoblast culture in biodegradable polymer scaffolds,” J. Biomed. Mater. Res.36(1), 17–28 (1997).
[CrossRef] [PubMed]

Yaszemski, M. J.

S. L. Ishaug-Riley, G. M. Crane-Kruger, M. J. Yaszemski, and A. G. Mikos, “Three-dimensional culture of rat calvarial osteoblasts in porous biodegradable polymers,” Biomaterials19(15), 1405–1412 (1998).
[CrossRef] [PubMed]

S. L. Ishaug, G. M. Crane, M. J. Miller, A. W. Yasko, M. J. Yaszemski, and A. G. Mikos, “Bone formation by three-dimensional stromal osteoblast culture in biodegradable polymer scaffolds,” J. Biomed. Mater. Res.36(1), 17–28 (1997).
[CrossRef] [PubMed]

Zareh, S. K.

Zhang, X.

X. Shi, L. Qin, X. Zhang, K. He, C. Xiong, J. Fang, X. Fang, and Y. Zhang, “Elasticity of cardiac cells on the polymer substrates with different stiffness: an atomic force microscopy study,” Phys. Chem. Chem. Phys.13(16), 7540–7545 (2011).
[CrossRef] [PubMed]

Zhang, Y.

X. Shi, L. Qin, X. Zhang, K. He, C. Xiong, J. Fang, X. Fang, and Y. Zhang, “Elasticity of cardiac cells on the polymer substrates with different stiffness: an atomic force microscopy study,” Phys. Chem. Chem. Phys.13(16), 7540–7545 (2011).
[CrossRef] [PubMed]

Zimmermann, W.

T. Eschenhagen, C. Fink, U. Remmers, H. Scholz, J. Wattchow, J. Weil, W. Zimmermann, H. H. Dohmen, H. Schäfer, N. Bishopric, T. Wakatsuki, and E. L. Elson, “Three-dimensional reconstitution of embryonic cardiomyocytes in a collagen matrix: a new heart muscle model system,” FASEB J.11(8), 683–694 (1997).
[PubMed]

Ann. Biomed. Eng.

A. Pai, P. Sundd, and D. F. Tees, “In situ microrheological determination of neutrophil stiffening following adhesion in a model capillary,” Ann. Biomed. Eng.36(4), 596–603 (2008).
[CrossRef] [PubMed]

Annu Rev Biophys

D. Wirtz, “Particle-tracking microrheology of living cells: principles and applications,” Annu Rev Biophys38(1), 301–326 (2009).
[CrossRef] [PubMed]

Biol. Cell

A. Ganz, M. Lambert, A. Saez, P. Silberzan, A. Buguin, R. M. Mège, and B. Ladoux, “Traction forces exerted through N-cadherin contacts,” Biol. Cell98(12), 721–730 (2006).
[CrossRef] [PubMed]

Biomaterials

S. L. Ishaug-Riley, G. M. Crane-Kruger, M. J. Yaszemski, and A. G. Mikos, “Three-dimensional culture of rat calvarial osteoblasts in porous biodegradable polymers,” Biomaterials19(15), 1405–1412 (1998).
[CrossRef] [PubMed]

Biophys. J.

Y. Tseng, T. P. Kole, and D. Wirtz, “Micromechanical mapping of live cells by multiple-particle-tracking microrheology,” Biophys. J.83(6), 3162–3176 (2002).
[CrossRef] [PubMed]

J. Solon, I. Levental, K. Sengupta, P. C. Georges, and P. A. Janmey, “Fibroblast adaptation and stiffness matching to soft elastic substrates,” Biophys. J.93(12), 4453–4461 (2007).
[CrossRef] [PubMed]

M. Jonas, H. Huang, R. D. Kamm, and P. T. So, “Fast fluorescence laser tracking microrheometry, II: quantitative studies of cytoskeletal mechanotransduction,” Biophys. J.95(2), 895–909 (2008).
[CrossRef] [PubMed]

C. M. Hale, A. L. Shrestha, S. B. Khatau, P. J. Stewart-Hutchinson, L. Hernandez, C. L. Stewart, D. Hodzic, and D. Wirtz, “Dysfunctional connections between the nucleus and the actin and microtubule networks in laminopathic models,” Biophys. J.95(11), 5462–5475 (2008).
[CrossRef] [PubMed]

H. P. Kao and A. S. Verkman, “Tracking of single fluorescent particles in three dimensions: use of cylindrical optics to encode particle position,” Biophys. J.67(3), 1291–1300 (1994).
[CrossRef] [PubMed]

V. Levi, Q. Ruan, and E. Gratton, “3-D particle tracking in a two-photon microscope: application to the study of molecular dynamics in cells,” Biophys. J.88(4), 2919–2928 (2005).
[CrossRef] [PubMed]

P. H. Wu, S. H. Arce, P. R. Burney, and Y. Tseng, “A novel approach to high accuracy of video-based microrheology,” Biophys. J.96(12), 5103–5111 (2009).
[CrossRef] [PubMed]

Biorheology

A. D. van der Meer, Y. Li, M. H. Duits, A. A. Poot, J. Feijen, and I. Vermes, “Shear stress induces a transient and VEGFR-2-dependent decrease in the motion of injected particles in endothelial cells,” Biorheology47(3-4), 179–192 (2010).
[PubMed]

Biotechnol. J.

M. F. Langhorst, J. Schaffer, and B. Goetze, “Structure brings clarity: structured illumination microscopy in cell biology,” Biotechnol. J.4(6), 858–865 (2009).
[CrossRef] [PubMed]

Cell Motil. Cytoskeleton

H. Huang, A. Asimaki, D. Lo, W. McKenna, and J. Saffitz, “Disparate effects of different mutations in plakoglobin on cell mechanical behavior,” Cell Motil. Cytoskeleton65(12), 964–978 (2008).
[CrossRef] [PubMed]

Exp. Cell Res.

P. J. Stewart-Hutchinson, C. M. Hale, D. Wirtz, and D. Hodzic, “Structural requirements for the assembly of LINC complexes and their function in cellular mechanical stiffness,” Exp. Cell Res.314(8), 1892–1905 (2008).
[CrossRef] [PubMed]

FASEB J.

T. Eschenhagen, C. Fink, U. Remmers, H. Scholz, J. Wattchow, J. Weil, W. Zimmermann, H. H. Dohmen, H. Schäfer, N. Bishopric, T. Wakatsuki, and E. L. Elson, “Three-dimensional reconstitution of embryonic cardiomyocytes in a collagen matrix: a new heart muscle model system,” FASEB J.11(8), 683–694 (1997).
[PubMed]

Hepatology

R. G. Wells, “The role of matrix stiffness in regulating cell behavior,” Hepatology47(4), 1394–1400 (2008).
[CrossRef] [PubMed]

IEEE Trans. Nanobioscience

P. Prabhat, S. Ram, E. S. Ward, and R. J. Ober, “Simultaneous imaging of different focal planes in fluorescence microscopy for the study of cellular dynamics in three dimensions,” IEEE Trans. Nanobioscience3(4), 237–242 (2004).
[CrossRef] [PubMed]

J. Appl. Physiol.

E. U. Azeloglu, J. Bhattacharya, and K. D. Costa, “Atomic force microscope elastography reveals phenotypic differences in alveolar cell stiffness,” J. Appl. Physiol.105(2), 652–661 (2008).
[CrossRef] [PubMed]

J. Biomech.

L. Cao, A. Wu, and G. A. Truskey, “Biomechanical effects of flow and coculture on human aortic and cord blood-derived endothelial cells,” J. Biomech.44(11), 2150–2157 (2011).
[CrossRef] [PubMed]

J. Biomech. Eng.

D. C. Lin, E. K. Dimitriadis, and F. Horkay, “Robust strategies for automated AFM force curve analysis--I. Non-adhesive indentation of soft, inhomogeneous materials,” J. Biomech. Eng.129(3), 430–440 (2007).
[CrossRef] [PubMed]

J. Biomed. Mater. Res.

S. L. Ishaug, G. M. Crane, M. J. Miller, A. W. Yasko, M. J. Yaszemski, and A. G. Mikos, “Bone formation by three-dimensional stromal osteoblast culture in biodegradable polymer scaffolds,” J. Biomed. Mater. Res.36(1), 17–28 (1997).
[CrossRef] [PubMed]

J. Biomed. Opt.

J. Mertz and J. Kim, “Scanning light-sheet microscopy in the whole mouse brain with HiLo background rejection,” J. Biomed. Opt.15(1), 016027 (2010).
[CrossRef] [PubMed]

S. Santos, K. K. Chu, D. Lim, N. Bozinovic, T. N. Ford, C. Hourtoule, A. C. Bartoo, S. K. Singh, and J. Mertz, “Optically sectioned fluorescence endomicroscopy with hybrid-illumination imaging through a flexible fiber bundle,” J. Biomed. Opt.14(3), 030502 (2009).
[CrossRef] [PubMed]

J. Cell Sci.

J. S. Lee, P. Panorchan, C. M. Hale, S. B. Khatau, T. P. Kole, Y. Tseng, and D. Wirtz, “Ballistic intracellular nanorheology reveals ROCK-hard cytoplasmic stiffening response to fluid flow,” J. Cell Sci.119(9), 1760–1768 (2006).
[CrossRef] [PubMed]

J. Clin. Invest.

J. Lammerding, P. C. Schulze, T. Takahashi, S. Kozlov, T. Sullivan, R. D. Kamm, C. L. Stewart, and R. T. Lee, “Lamin A/C deficiency causes defective nuclear mechanics and mechanotransduction,” J. Clin. Invest.113(3), 370–378 (2004).
[PubMed]

J. Neurotrauma

B. S. Elkin, E. U. Azeloglu, K. D. Costa, and B. Morrison, “Mechanical heterogeneity of the rat hippocampus measured by atomic force microscope indentation,” J. Neurotrauma24(5), 812–822 (2007).
[CrossRef] [PubMed]

Methods

J. G. McNally, T. Karpova, J. Cooper, and J. A. Conchello, “Three-dimensional imaging by deconvolution microscopy,” Methods19(3), 373–385 (1999).
[CrossRef] [PubMed]

Methods Cell Biol.

J. C. Crocker and B. D. Hoffman, “Multiple-particle tracking and two-point microrheology in cells,” Methods Cell Biol.83, 141–178 (2007).
[CrossRef] [PubMed]

P. Panorchan, J. S. Lee, B. R. Daniels, T. P. Kole, Y. Tseng, and D. Wirtz, “Probing cellular mechanical responses to stimuli using ballistic intracellular nanorheology,” Methods Cell Biol.83, 113–140 (2007).
[CrossRef] [PubMed]

Mol. Biol. Cell

T. P. Kole, Y. Tseng, I. Jiang, J. L. Katz, and D. Wirtz, “Intracellular mechanics of migrating fibroblasts,” Mol. Biol. Cell16(1), 328–338 (2005).
[CrossRef] [PubMed]

N. Engl. J. Med.

K. Nishida, M. Yamato, Y. Hayashida, K. Watanabe, K. Yamamoto, E. Adachi, S. Nagai, A. Kikuchi, N. Maeda, H. Watanabe, T. Okano, and Y. Tano, “Corneal reconstruction with tissue-engineered cell sheets composed of autologous oral mucosal epithelium,” N. Engl. J. Med.351(12), 1187–1196 (2004).
[CrossRef] [PubMed]

Opt. Express

Opt. Lett.

Phys. Chem. Chem. Phys.

X. Shi, L. Qin, X. Zhang, K. He, C. Xiong, J. Fang, X. Fang, and Y. Zhang, “Elasticity of cardiac cells on the polymer substrates with different stiffness: an atomic force microscopy study,” Phys. Chem. Chem. Phys.13(16), 7540–7545 (2011).
[CrossRef] [PubMed]

Phys. Rev. Lett.

J. C. Crocker and D. G. Grier, “When like charges attract: the effects of geometrical confinement on long-range colloidal interactions,” Phys. Rev. Lett.77(9), 1897–1900 (1996).
[CrossRef] [PubMed]

A. W. Lau, B. D. Hoffman, A. Davies, J. C. Crocker, and T. C. Lubensky, “Microrheology, stress fluctuations, and active behavior of living cells,” Phys. Rev. Lett.91(19), 198101 (2003).
[CrossRef] [PubMed]

PLoS ONE

D. Fudge, D. Russell, D. Beriault, W. Moore, E. B. Lane, and A. W. Vogl, “The intermediate filament network in cultured human keratinocytes is remarkably extensible and resilient,” PLoS ONE3(6), e2327 (2008).
[CrossRef] [PubMed]

Proc. Natl. Acad. Sci. U.S.A.

V. Maruthamuthu, B. Sabass, U. S. Schwarz, and M. L. Gardel, “Cell-ECM traction force modulates endogenous tension at cell-cell contacts,” Proc. Natl. Acad. Sci. U.S.A.108(12), 4708–4713 (2011).
[CrossRef] [PubMed]

Rheologica Acta

T. G. Mason, “Estimating the viscoelastic moduli of complex fluids using the generalized Stokes-Einstein equation,” Rheologica Acta39(4), 371–378 (2000).
[CrossRef]

Other

J. Lammerding and R. T. Lee, “The nuclear membrane and mechanotransduction: impaired nuclear mechanics and mechanotransduction in lamin A/C deficient cells,” in Nuclear Organization in Development and Disease, Novartis Foundation Symposium Vol. 264 (Wiley, 2005), pp. 264–273.

Supplementary Material (2)

» Media 1: AVI (1962 KB)     
» Media 2: AVI (1962 KB)     

Cited By

OSA participates in CrossRef's Cited-By Linking service. Citing articles from OSA journals and other participating publishers are listed here.

Alert me when this article is cited.


Figures (6)

Fig. 1
Fig. 1

For the uniform (A) and HiLo-processed (C) images of the top CM layer, HiLo processing reduces the presence of the background signal from the bottom CF layer. For the uniform (B) and HiLo-processed (D) images of the bottom CF layer, HiLo processing reduces the presence of the signal from the top CM layer, while retaining actin and cytoplasmic fluorescence of the CF layer. For example, the sarcomeres that are seen in the top CM layer (white arrow) are less clear in the HiLo image of the bottom CF layer. Similarly, a circular actin structure that can clearly be seen in the top CM layer (gray arrow) cannot be seen in the HiLo image of the bottom CF layer. Images brightness/contrast adjusted for clarity. Scale bar is 30um.

Fig. 2
Fig. 2

The percentage drop in bead intensity between uniform and HiLo images (relative to HiLo) at increasing distances from the focal plane. Beads 0.5 μm or closer to the image plane have a drop in intensity less than 20%, and 88% of beads 0.5 μm or further from the image plane had a drop in intensity greater than 20%. The asymmetry in the bead distribution results from the inverted configuration of the microscope; objects below the imaging plane could be observed to a far greater out-of-plane distance than objects above the imaging plane.

Fig. 3
Fig. 3

Plot of MSD (nm2) vs. tau (s) (A), G′ (Pa) vs. frequency (Hz) (B), and G″(Pa) vs. frequency (Hz) (C) for bottom (Media 1) and top (Media 2) cell layers with and without HiLo image processing. HiLo processing allows for the removal of out-of-plane beads. Removing the out-of-plane beads from each image produces a small increase in the MSD of the bottom layer and a larger decrease in the MSD of the top layer over all time lags. These alterations in MSD produce a decrease in the storage and loss modulus in bottom layer and an increase of the storage and loss modulus in the top layer. The MSD (D, in nm2), storage modulus (E, in Pa), and loss modulus (F, in Pa) are compared at three different time lags. All data are compared using a student’s t-test (*p < 0.05, **p < 0.01, ^p < 0.001). Statistical analysis at not performed for G′ and G″, as these are derived parameters. G′ drops to zero above 0.2Hz, so was not included in the plot (E).

Fig. 4
Fig. 4

Comparison of the appearance (A,B), trajectory (C,D), and MSD (E) of a single bead as seen at the bottom layer (in-plane) and the top layer (out-of-plane). The out-of-plane bead (B) appears smaller than the in-plane bead (A) with a more uniform intensity distribution. This increases the contribution of signal fluctuations and decreases the centroid-finding resolution of the tracking program. Because of this, short time-lag displacements of the out-of-plane bead (D) are much larger than the displacements of the in-plane bead (C) on the log-log scale. The result is that analysis yields an increase in MSD magnitude and decrease in slope (E), the effect of which of which decreases at longer time lags on a log-log plot as the bead centroid more clearly changes position.

Fig. 5
Fig. 5

AFM testing shows that 3T3 cells plated on a 3T3 monolayer have a significantly higher elastic modulus (kPa) than 3T3 cells plated on glass (n = 11 for both cases; *p < 0.05 as measured by a student’s t-test).

Fig. 6
Fig. 6

MSD (nm2) vs. Tau (s) plot comparing properties of 3T3 cell monolayer with the top and bottom layers of a 3T3 cell bilayer. The monolayer is shown here as having properties similar to the bottom layer of the bilayer, showing that the presence of the top layer of cells does not have a significant effect on the mechanical properties of the bottom layer.

Equations (12)

Equations on this page are rendered with MathJax. Learn more.

I d ( ρ )=| I n ( ρ ) I u ( ρ ) |
I lp ( ρ )=LP[ I d ( ρ ) ].
I hp ( ρ )=HP[ I u ( ρ ) ]
I hilo ( ρ )=η I lp ( ρ )+ I hp ( ρ )
Δ r 2 ( τ ) = ( r( t+τ )r( t ) ) 2 t
G'(ω)=| G * (ω) |cos(πα(ω)/2), G''(ω)=| G * (ω) |sin(πα(ω)/2),
α(ω) ln Δ r 2 (τ) lnτ | τ=1/ω | G * (ω) | 2 k B T 3πa Δ r 2 (1/ω) Γ[ 1+α(ω) ] ,
Γ[ 1+α ]0.457 (1+α) 2 1.36(1+α)+1.90
E= F(1 ν 2 ) πΦ(D)
Φ(D)= 4 3π ( R D 3 ) 1/2
Φ(D)= 4 2π { (aD)[ m( a 2 tanϕ )( π 2 arcsin( b a ) ) ]( a 3 3R )+ ( a 2 b 2 ) 1/2 [ m b tanϕ + a 2 b 2 3R ] }
D+ a R [ ( a 2 b 2 ) 1/2 a ] na tanϕ [ π 2 arcsin( b a ) ]=0

Metrics