Abstract

Traction force microscopy (TFM) is a method used to study the forces exerted by cells as they sense and interact with their environment. Cell forces play a role in processes that take place over a wide range of spatiotemporal scales, and so it is desirable that TFM makes use of imaging modalities that can effectively capture the dynamics associated with these processes. To date, confocal microscopy has been the imaging modality of choice to perform TFM in 3D settings, although multiple factors limit its spatiotemporal coverage. We propose traction force optical coherence microscopy (TF-OCM) as a novel technique that may offer enhanced spatial coverage and temporal sampling compared to current methods used for volumetric TFM studies. Reconstructed volumetric OCM data sets were used to compute time-lapse extracellular matrix deformations resulting from cell forces in 3D culture. These matrix deformations revealed clear differences that can be attributed to the dynamic forces exerted by normal versus contractility-inhibited NIH-3T3 fibroblasts embedded within 3D Matrigel matrices. Our results are the first step toward the realization of 3D TF-OCM, and they highlight the potential use of OCM as a platform for advancing cell mechanics research.

© 2017 Optical Society of America

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2016 (11)

W. J. Polacheck and C. S. Chen, “Measuring cell-generated forces: a guide to the available tools,” Nat. Methods 13(5), 415–423 (2016).
[Crossref] [PubMed]

M. J. Siedlik, V. D. Varner, and C. M. Nelson, “Pushing, pulling, and squeezing our way to understanding mechanotransduction,” Methods 94, 4–12 (2016).
[Crossref] [PubMed]

J. Fujimoto and E. Swanson, “The Development, Commercialization, and Impact of Optical Coherence Tomography,” Invest. Ophthalmol. Vis. Sci. 57(9), OCT1–OCT13 (2016).
[Crossref] [PubMed]

J. A. Mulligan, G. R. Untracht, S. N. Chandrasekaran, C. N. Brown, and S. G. Adie, “Emerging Approaches for High-Resolution Imaging of Tissue Biomechanics with Optical Coherence Elastography,” IEEE J. Sel. Top. Quantum Electron. 22(3), 246 (2016).
[Crossref]

C. Apelian, F. Harms, O. Thouvenin, and A. C. Boccara, “Dynamic full field optical coherence tomography: subcellular metabolic contrast revealed in tissues by interferometric signals temporal analysis,” Biomed. Opt. Express 7(4), 1511–1524 (2016).
[Crossref] [PubMed]

R. L. Blackmon, R. Sandhu, B. S. Chapman, P. Casbas-Hernandez, J. B. Tracy, M. A. Troester, and A. L. Oldenburg, “Imaging Extracellular Matrix Remodeling In Vitro by Diffusion-Sensitive Optical Coherence Tomography,” Biophys. J. 110(8), 1858–1868 (2016).
[Crossref] [PubMed]

H. Tang, J. A. Mulligan, G. R. Untracht, X. Zhang, and S. G. Adie, “GPU-based computational adaptive optics for volumetric optical coherence microscopy,” Proc. SPIE 9720, 97200O (2016).

D. A. Stout, E. Bar-Kochba, J. B. Estrada, J. Toyjanova, H. Kesari, J. S. Reichner, and C. Franck, “Mean deformation metrics for quantifying 3D cell-matrix interactions without requiring information about matrix material properties,” Proc. Natl. Acad. Sci. U.S.A. 113(11), 2898–2903 (2016).
[Crossref] [PubMed]

D. Hillmann, H. Spahr, C. Hain, H. Sudkamp, G. Franke, C. Pfäffle, C. Winter, and G. Hüttmann, “Aberration-free volumetric highspeed imaging of in vivo retina,” Sci. Rep. 6, 35209 (2016).
[Crossref]

A. Curatolo, P. R. T. Munro, D. Lorenser, P. Sreekumar, C. C. Singe, B. F. Kennedy, and D. D. Sampson, “Quantifying the influence of Bessel beams on image quality in optical coherence tomography,” Sci. Rep. 6, 23483 (2016).
[Crossref] [PubMed]

P. Meemon, J. Widjaja, and J. P. Rolland, “Spectral fusing Gabor domain optical coherence microscopy,” Opt. Lett. 41(3), 508–511 (2016).
[Crossref] [PubMed]

2015 (7)

N. D. Shemonski, F. A. South, Y.-Z. Liu, S. G. Adie, P. S. Carney, and S. A. Boppart, “Computational high-resolution optical imaging of the living human retina,” Nat. Photonics 9(7), 440–443 (2015).
[Crossref] [PubMed]

A. Kumar, T. Kamali, R. Platzer, A. Unterhuber, W. Drexler, and R. A. Leitgeb, “Anisotropic aberration correction using region of interest based digital adaptive optics in Fourier domain OCT,” Biomed. Opt. Express 6(4), 1124–1134 (2015).
[Crossref] [PubMed]

O. Chaudhuri, L. Gu, M. Darnell, D. Klumpers, S. A. Bencherif, J. C. Weaver, N. Huebsch, and D. J. Mooney, “Substrate stress relaxation regulates cell spreading,” Nat. Commun. 6, 6365 (2015).
[Crossref] [PubMed]

U. S. Schwarz and J. R. D. Soiné, “Traction force microscopy on soft elastic substrates: A guide to recent computational advances,” Biochim. Biophys. Acta 1853(11), 3095–3104 (2015).
[Crossref] [PubMed]

S. Wang and K. V. Larin, “Optical coherence elastography for tissue characterization: a review,” J. Biophotonics 8(4), 279–302 (2015).
[Crossref] [PubMed]

M. B. Bouchard, V. Voleti, C. S. Mendes, C. Lacefield, W. B. Grueber, R. S. Mann, R. M. Bruno, and E. M. C. Hillman, “Swept confocally-aligned planar excitation (SCAPE) microscopy for high speed volumetric imaging of behaving organisms,” Nat. Photonics 9(2), 113–119 (2015).
[Crossref] [PubMed]

B. R. Seo, P. Bhardwaj, S. Choi, J. Gonzalez, R. C. Andresen Eguiluz, K. Wang, S. Mohanan, P. G. Morris, B. Du, X. K. Zhou, L. T. Vahdat, A. Verma, O. Elemento, C. A. Hudis, R. M. Williams, D. Gourdon, A. J. Dannenberg, and C. Fischbach, “Obesity-dependent changes in interstitial ECM mechanics promote breast tumorigenesis,” Sci. Transl. Med. 7(301), 301ra130 (2015).
[Crossref] [PubMed]

2014 (5)

Y.-Z. Liu, N. D. Shemonski, S. G. Adie, A. Ahmad, A. J. Bower, P. S. Carney, and S. A. Boppart, “Computed optical interferometric tomography for high-speed volumetric cellular imaging,” Biomed. Opt. Express 5(9), 2988–3000 (2014).
[Crossref] [PubMed]

J. L. Compton, J. C. Luo, H. Ma, E. Botvinick, and V. Venugopalan, “High-throughput optical screening of cellular mechanotransduction,” Nat. Photonics 8(9), 710–715 (2014).
[Crossref] [PubMed]

J. Toyjanova, E. Bar-Kochba, C. López-Fagundo, J. Reichner, D. Hoffman-Kim, and C. Franck, “High resolution, large deformation 3D traction force microscopy,” PLoS One 9(4), e90976 (2014).
[Crossref] [PubMed]

B. F. Kennedy, K. M. Kennedy, and D. D. Sampson, “A Review of Optical Coherence Elastography: Fundamentals, Techniques and Prospects,” IEEE J. Sel. Top. Quantum Electron. 20(2), 272–288 (2014).
[Crossref]

R. F. van Oers, E. G. Rens, D. J. LaValley, C. A. Reinhart-King, and R. M. H. Merks, “Mechanical cell-matrix feedback explains pairwise and collective endothelial cell behavior in vitro,” PLOS Comput. Biol. 10(8), e1003774 (2014).
[Crossref] [PubMed]

2013 (11)

T. Klein, W. Wieser, L. Reznicek, A. Neubauer, A. Kampik, and R. Huber, “Multi-MHz retinal OCT,” Biomed. Opt. Express 4(10), 1890–1908 (2013).
[Crossref] [PubMed]

M. B. Ahrens, M. B. Orger, D. N. Robson, J. M. Li, and P. J. Keller, “Whole-brain functional imaging at cellular resolution using light-sheet microscopy,” Nat. Methods 10(5), 413–420 (2013).
[Crossref] [PubMed]

C. Sun, B. Standish, B. Vuong, X.-Y. Wen, and V. Yang, “Digital image correlation-based optical coherence elastography,” J. Biomed. Opt. 18(12), 121515 (2013).
[Crossref] [PubMed]

J. Fu, F. Pierron, and P. D. Ruiz, “Elastic stiffness characterization using three-dimensional full-field deformation obtained with optical coherence tomography and digital volume correlation,” J. Biomed. Opt. 18(12), 121512 (2013).
[Crossref] [PubMed]

J. H. Kim, X. Serra-Picamal, D. T. Tambe, E. H. Zhou, C. Y. Park, M. Sadati, J.-A. Park, R. Krishnan, B. Gweon, E. Millet, J. P. Butler, X. Trepat, and J. J. Fredberg, “Propulsion and navigation within the advancing monolayer sheet,” Nat. Mater. 12(9), 856–863 (2013).
[Crossref] [PubMed]

W. R. Legant, C. K. Choi, J. S. Miller, L. Shao, L. Gao, E. Betzig, and C. S. Chen, “Multidimensional traction force microscopy reveals out-of-plane rotational moments about focal adhesions,” Proc. Natl. Acad. Sci. U.S.A. 110(3), 881–886 (2013).
[Crossref] [PubMed]

M. S. Hall, R. Long, X. Feng, Y. Huang, C.-Y. Hui, and M. Wu, “Toward single cell traction microscopy within 3D collagen matrices,” Exp. Cell Res. 319(16), 2396–2408 (2013).
[Crossref] [PubMed]

M. Sadati, N. Taheri Qazvini, R. Krishnan, C. Y. Park, and J. J. Fredberg, “Collective migration and cell jamming,” Differentiation 86(3), 121–125 (2013).
[Crossref] [PubMed]

L. G. Vincent, Y. S. Choi, B. Alonso-Latorre, J. C. del Álamo, and A. J. Engler, “Mesenchymal stem cell durotaxis depends on substrate stiffness gradient strength,” Biotechnol. J. 8(4), 472–484 (2013).
[Crossref] [PubMed]

S. P. Carey, A. Starchenko, A. L. McGregor, and C. A. Reinhart-King, “Leading malignant cells initiate collective epithelial cell invasion in a three-dimensional heterotypic tumor spheroid model,” Clin. Exp. Metastasis 30(5), 615–630 (2013).
[Crossref] [PubMed]

U. S. Schwarz and S. A. Safran, “Physics of adherent cells,” Rev. Mod. Phys. 85(3), 1327–1381 (2013).
[Crossref]

2012 (7)

C. M. Kraning-Rush, J. P. Califano, and C. A. Reinhart-King, “Cellular Traction Stresses Increase with Increasing Metastatic Potential,” PLoS One 7(2), e32572 (2012).
[Crossref] [PubMed]

S. P. Carey, T. M. D’Alfonso, S. J. Shin, and C. A. Reinhart-King, “Mechanobiology of tumor invasion: engineering meets oncology,” Crit. Rev. Oncol. Hematol. 83(2), 170–183 (2012).
[Crossref] [PubMed]

X. Serra-Picamal, V. Conte, R. Vincent, E. Anon, D. T. Tambe, E. Bazellieres, J. P. Butler, J. J. Fredberg, and X. Trepat, “Mechanical waves during tissue expansion,” Nat. Phys. 8(8), 628–634 (2012).
[Crossref]

S. G. Adie, B. W. Graf, A. Ahmad, P. S. Carney, and S. A. Boppart, “Computational adaptive optics for broadband optical interferometric tomography of biological tissue,” Proc. Natl. Acad. Sci. U.S.A. 109(19), 7175–7180 (2012).
[Crossref] [PubMed]

X. Yu, M. Cross, C. Liu, D. C. Clark, D. T. Haynie, and M. K. Kim, “Measurement of the traction force of biological cells by digital holography,” Biomed. Opt. Express 3(1), 153–159 (2012).
[Crossref] [PubMed]

T. M. Koch, S. Münster, N. Bonakdar, J. P. Butler, and B. Fabry, “3D Traction Forces in Cancer Cell Invasion,” PLoS One 7(3), e33476 (2012).
[Crossref] [PubMed]

S. G. Adie, N. D. Shemonski, B. W. Graf, A. Ahmad, P. Scott Carney, and S. A. Boppart, “Guide-star-based computational adaptive optics for broadband interferometric tomography,” Appl. Phys. Lett. 101(22), 221117 (2012).
[Crossref] [PubMed]

2011 (5)

C. Blatter, B. Grajciar, C. M. Eigenwillig, W. Wieser, B. R. Biedermann, R. Huber, and R. A. Leitgeb, “Extended focus high-speed swept source OCT with self-reconstructive illumination,” Opt. Express 19(13), 12141–12155 (2011).
[Crossref] [PubMed]

K. M. Hakkinen, J. S. Harunaga, A. D. Doyle, and K. M. Yamada, “Direct Comparisons of the Morphology, Migration, Cell Adhesions, and Actin Cytoskeleton of Fibroblasts in Four Different Three-Dimensional Extracellular Matrices,” Tissue Eng. Part A 17(5-6), 713–724 (2011).
[Crossref] [PubMed]

D. T. Tambe, C. C. Hardin, T. E. Angelini, K. Rajendran, C. Y. Park, X. Serra-Picamal, E. H. Zhou, M. H. Zaman, J. P. Butler, D. A. Weitz, J. J. Fredberg, and X. Trepat, “Collective cell guidance by cooperative intercellular forces,” Nat. Mater. 10(6), 469–475 (2011).
[Crossref] [PubMed]

C. Franck, S. A. Maskarinec, D. A. Tirrell, and G. Ravichandran, “Three-Dimensional Traction Force Microscopy: A New Tool for Quantifying Cell-Matrix Interactions,” PLoS One 6(3), e17833 (2011).
[Crossref] [PubMed]

D. Wirtz, K. Konstantopoulos, and P. C. Searson, “The physics of cancer: the role of physical interactions and mechanical forces in metastasis,” Nat. Rev. Cancer 11(7), 512–522 (2011).
[Crossref] [PubMed]

2010 (2)

W. R. Legant, J. S. Miller, B. L. Blakely, D. M. Cohen, G. M. Genin, and C. S. Chen, “Measurement of mechanical tractions exerted by cells in three-dimensional matrices,” Nat. Methods 7(12), 969–971 (2010).
[Crossref] [PubMed]

N. Mohan, I. Stojanovic, W. C. Karl, B. E. A. Saleh, and M. C. Teich, “Compressed sensing in optical coherence tomography,” Proc. SPIE 7570, 75700L (2010).

2009 (6)

B. Pan, K. Qian, H. Xie, and A. Asundi, “Two-dimensional digital image correlation for in-plane displacement and strain measurement: a review,” Meas. Sci. Technol. 20(6), 062001 (2009).
[Crossref]

J. P. Winer, S. Oake, and P. A. Janmey, “Non-linear elasticity of extracellular matrices enables contractile cells to communicate local position and orientation,” PLoS One 4(7), e6382 (2009).
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D. T. Butcher, T. Alliston, and V. M. Weaver, “A tense situation: forcing tumour progression,” Nat. Rev. Cancer 9(2), 108–122 (2009).
[Crossref] [PubMed]

K. R. Levental, H. Yu, L. Kass, J. N. Lakins, M. Egeblad, J. T. Erler, S. F. T. Fong, K. Csiszar, A. Giaccia, W. Weninger, M. Yamauchi, D. L. Gasser, and V. M. Weaver, “Matrix crosslinking forces tumor progression by enhancing integrin signaling,” Cell 139(5), 891–906 (2009).
[Crossref] [PubMed]

X. Trepat, M. R. Wasserman, T. E. Angelini, E. Millet, D. A. Weitz, J. P. Butler, and J. J. Fredberg, “Physical forces during collective cell migration,” Nat. Phys. 5(6), 426–430 (2009).
[Crossref]

S. M. Rey, B. Povazay, B. Hofer, A. Unterhuber, B. Hermann, A. Harwood, and W. Drexler, “Three- and four-dimensional visualization of cell migration using optical coherence tomography,” J. Biophotonics 2(6-7), 370–379 (2009).
[Crossref] [PubMed]

2008 (4)

R. J. Bloom, J. P. George, A. Celedon, S. X. Sun, and D. Wirtz, “Mapping Local Matrix Remodeling Induced by a Migrating Tumor Cell Using Three-Dimensional Multiple-Particle Tracking,” Biophys. J. 95(8), 4077–4088 (2008).
[Crossref] [PubMed]

P. P. Provenzano, D. R. Inman, K. W. Eliceiri, J. G. Knittel, L. Yan, C. T. Rueden, J. G. White, and P. J. Keely, “Collagen density promotes mammary tumor initiation and progression,” BMC Med. 6(1), 11 (2008).
[Crossref] [PubMed]

R. G. Chelliyil, T. S. Ralston, D. L. Marks, and S. A. Boppart, “High-speed processing architecture for spectral-domain optical coherence microscopy,” J. Biomed. Opt. 13(4), 044013 (2008).
[Crossref] [PubMed]

K.-S. Lee and J. P. Rolland, “Bessel beam spectral-domain high-resolution optical coherence tomography with micro-optic axicon providing extended focusing range,” Opt. Lett. 33(15), 1696–1698 (2008).
[Crossref] [PubMed]

2007 (2)

F. Pampaloni, E. G. Reynaud, and E. H. K. Stelzer, “The third dimension bridges the gap between cell culture and live tissue,” Nat. Rev. Mol. Cell Biol. 8(10), 839–845 (2007).
[Crossref] [PubMed]

T. S. Ralston, D. L. Marks, P. S. Carney, and S. A. Boppart, “Interferometric synthetic aperture microscopy,” Nat. Phys. 3(2), 129–134 (2007).
[Crossref] [PubMed]

2006 (3)

2005 (3)

2004 (1)

2003 (4)

P. J. Hunter and T. K. Borg, “Integration from proteins to organs: the Physiome Project,” Nat. Rev. Mol. Cell Biol. 4(3), 237–243 (2003).
[Crossref] [PubMed]

D. L. Marks, A. L. Oldenburg, J. J. Reynolds, and S. A. Boppart, “Autofocus algorithm for dispersion correction in optical coherence tomography,” Appl. Opt. 42(16), 3038–3046 (2003).
[Crossref] [PubMed]

V. D. Gordon, M. T. Valentine, M. L. Gardel, D. Andor-Ardó, S. Dennison, A. A. Bogdanov, D. A. Weitz, and T. S. Deisboeck, “Measuring the mechanical stress induced by an expanding multicellular tumor system: a case study,” Exp. Cell Res. 289(1), 58–66 (2003).
[Crossref] [PubMed]

J. L. Tan, J. Tien, D. M. Pirone, D. S. Gray, K. Bhadriraju, and C. S. Chen, “Cells lying on a bed of microneedles: an approach to isolate mechanical force,” Proc. Natl. Acad. Sci. U.S.A. 100(4), 1484–1489 (2003).
[Crossref] [PubMed]

2001 (1)

T. Wakatsuki, B. Schwab, N. C. Thompson, and E. L. Elson, “Effects of cytochalasin D and latrunculin B on mechanical properties of cells,” J. Cell Sci. 114(Pt 5), 1025–1036 (2001).
[PubMed]

1998 (1)

Adie, S. G.

J. A. Mulligan, G. R. Untracht, S. N. Chandrasekaran, C. N. Brown, and S. G. Adie, “Emerging Approaches for High-Resolution Imaging of Tissue Biomechanics with Optical Coherence Elastography,” IEEE J. Sel. Top. Quantum Electron. 22(3), 246 (2016).
[Crossref]

H. Tang, J. A. Mulligan, G. R. Untracht, X. Zhang, and S. G. Adie, “GPU-based computational adaptive optics for volumetric optical coherence microscopy,” Proc. SPIE 9720, 97200O (2016).

N. D. Shemonski, F. A. South, Y.-Z. Liu, S. G. Adie, P. S. Carney, and S. A. Boppart, “Computational high-resolution optical imaging of the living human retina,” Nat. Photonics 9(7), 440–443 (2015).
[Crossref] [PubMed]

Y.-Z. Liu, N. D. Shemonski, S. G. Adie, A. Ahmad, A. J. Bower, P. S. Carney, and S. A. Boppart, “Computed optical interferometric tomography for high-speed volumetric cellular imaging,” Biomed. Opt. Express 5(9), 2988–3000 (2014).
[Crossref] [PubMed]

S. G. Adie, N. D. Shemonski, B. W. Graf, A. Ahmad, P. Scott Carney, and S. A. Boppart, “Guide-star-based computational adaptive optics for broadband interferometric tomography,” Appl. Phys. Lett. 101(22), 221117 (2012).
[Crossref] [PubMed]

S. G. Adie, B. W. Graf, A. Ahmad, P. S. Carney, and S. A. Boppart, “Computational adaptive optics for broadband optical interferometric tomography of biological tissue,” Proc. Natl. Acad. Sci. U.S.A. 109(19), 7175–7180 (2012).
[Crossref] [PubMed]

Ahmad, A.

Y.-Z. Liu, N. D. Shemonski, S. G. Adie, A. Ahmad, A. J. Bower, P. S. Carney, and S. A. Boppart, “Computed optical interferometric tomography for high-speed volumetric cellular imaging,” Biomed. Opt. Express 5(9), 2988–3000 (2014).
[Crossref] [PubMed]

S. G. Adie, N. D. Shemonski, B. W. Graf, A. Ahmad, P. Scott Carney, and S. A. Boppart, “Guide-star-based computational adaptive optics for broadband interferometric tomography,” Appl. Phys. Lett. 101(22), 221117 (2012).
[Crossref] [PubMed]

S. G. Adie, B. W. Graf, A. Ahmad, P. S. Carney, and S. A. Boppart, “Computational adaptive optics for broadband optical interferometric tomography of biological tissue,” Proc. Natl. Acad. Sci. U.S.A. 109(19), 7175–7180 (2012).
[Crossref] [PubMed]

Ahrens, M. B.

M. B. Ahrens, M. B. Orger, D. N. Robson, J. M. Li, and P. J. Keller, “Whole-brain functional imaging at cellular resolution using light-sheet microscopy,” Nat. Methods 10(5), 413–420 (2013).
[Crossref] [PubMed]

Alliston, T.

D. T. Butcher, T. Alliston, and V. M. Weaver, “A tense situation: forcing tumour progression,” Nat. Rev. Cancer 9(2), 108–122 (2009).
[Crossref] [PubMed]

Alonso-Latorre, B.

L. G. Vincent, Y. S. Choi, B. Alonso-Latorre, J. C. del Álamo, and A. J. Engler, “Mesenchymal stem cell durotaxis depends on substrate stiffness gradient strength,” Biotechnol. J. 8(4), 472–484 (2013).
[Crossref] [PubMed]

Andor-Ardó, D.

V. D. Gordon, M. T. Valentine, M. L. Gardel, D. Andor-Ardó, S. Dennison, A. A. Bogdanov, D. A. Weitz, and T. S. Deisboeck, “Measuring the mechanical stress induced by an expanding multicellular tumor system: a case study,” Exp. Cell Res. 289(1), 58–66 (2003).
[Crossref] [PubMed]

Andresen Eguiluz, R. C.

B. R. Seo, P. Bhardwaj, S. Choi, J. Gonzalez, R. C. Andresen Eguiluz, K. Wang, S. Mohanan, P. G. Morris, B. Du, X. K. Zhou, L. T. Vahdat, A. Verma, O. Elemento, C. A. Hudis, R. M. Williams, D. Gourdon, A. J. Dannenberg, and C. Fischbach, “Obesity-dependent changes in interstitial ECM mechanics promote breast tumorigenesis,” Sci. Transl. Med. 7(301), 301ra130 (2015).
[Crossref] [PubMed]

Angelini, T. E.

D. T. Tambe, C. C. Hardin, T. E. Angelini, K. Rajendran, C. Y. Park, X. Serra-Picamal, E. H. Zhou, M. H. Zaman, J. P. Butler, D. A. Weitz, J. J. Fredberg, and X. Trepat, “Collective cell guidance by cooperative intercellular forces,” Nat. Mater. 10(6), 469–475 (2011).
[Crossref] [PubMed]

X. Trepat, M. R. Wasserman, T. E. Angelini, E. Millet, D. A. Weitz, J. P. Butler, and J. J. Fredberg, “Physical forces during collective cell migration,” Nat. Phys. 5(6), 426–430 (2009).
[Crossref]

Anon, E.

X. Serra-Picamal, V. Conte, R. Vincent, E. Anon, D. T. Tambe, E. Bazellieres, J. P. Butler, J. J. Fredberg, and X. Trepat, “Mechanical waves during tissue expansion,” Nat. Phys. 8(8), 628–634 (2012).
[Crossref]

Apelian, C.

Asundi, A.

B. Pan, K. Qian, H. Xie, and A. Asundi, “Two-dimensional digital image correlation for in-plane displacement and strain measurement: a review,” Meas. Sci. Technol. 20(6), 062001 (2009).
[Crossref]

Bachmann, A. H.

Bar-Kochba, E.

D. A. Stout, E. Bar-Kochba, J. B. Estrada, J. Toyjanova, H. Kesari, J. S. Reichner, and C. Franck, “Mean deformation metrics for quantifying 3D cell-matrix interactions without requiring information about matrix material properties,” Proc. Natl. Acad. Sci. U.S.A. 113(11), 2898–2903 (2016).
[Crossref] [PubMed]

J. Toyjanova, E. Bar-Kochba, C. López-Fagundo, J. Reichner, D. Hoffman-Kim, and C. Franck, “High resolution, large deformation 3D traction force microscopy,” PLoS One 9(4), e90976 (2014).
[Crossref] [PubMed]

Bazellieres, E.

X. Serra-Picamal, V. Conte, R. Vincent, E. Anon, D. T. Tambe, E. Bazellieres, J. P. Butler, J. J. Fredberg, and X. Trepat, “Mechanical waves during tissue expansion,” Nat. Phys. 8(8), 628–634 (2012).
[Crossref]

Beaurepaire, E.

Bencherif, S. A.

O. Chaudhuri, L. Gu, M. Darnell, D. Klumpers, S. A. Bencherif, J. C. Weaver, N. Huebsch, and D. J. Mooney, “Substrate stress relaxation regulates cell spreading,” Nat. Commun. 6, 6365 (2015).
[Crossref] [PubMed]

Betzig, E.

W. R. Legant, C. K. Choi, J. S. Miller, L. Shao, L. Gao, E. Betzig, and C. S. Chen, “Multidimensional traction force microscopy reveals out-of-plane rotational moments about focal adhesions,” Proc. Natl. Acad. Sci. U.S.A. 110(3), 881–886 (2013).
[Crossref] [PubMed]

Bhadriraju, K.

J. L. Tan, J. Tien, D. M. Pirone, D. S. Gray, K. Bhadriraju, and C. S. Chen, “Cells lying on a bed of microneedles: an approach to isolate mechanical force,” Proc. Natl. Acad. Sci. U.S.A. 100(4), 1484–1489 (2003).
[Crossref] [PubMed]

Bhardwaj, P.

B. R. Seo, P. Bhardwaj, S. Choi, J. Gonzalez, R. C. Andresen Eguiluz, K. Wang, S. Mohanan, P. G. Morris, B. Du, X. K. Zhou, L. T. Vahdat, A. Verma, O. Elemento, C. A. Hudis, R. M. Williams, D. Gourdon, A. J. Dannenberg, and C. Fischbach, “Obesity-dependent changes in interstitial ECM mechanics promote breast tumorigenesis,” Sci. Transl. Med. 7(301), 301ra130 (2015).
[Crossref] [PubMed]

Biedermann, B. R.

Blackmon, R. L.

R. L. Blackmon, R. Sandhu, B. S. Chapman, P. Casbas-Hernandez, J. B. Tracy, M. A. Troester, and A. L. Oldenburg, “Imaging Extracellular Matrix Remodeling In Vitro by Diffusion-Sensitive Optical Coherence Tomography,” Biophys. J. 110(8), 1858–1868 (2016).
[Crossref] [PubMed]

Blakely, B. L.

W. R. Legant, J. S. Miller, B. L. Blakely, D. M. Cohen, G. M. Genin, and C. S. Chen, “Measurement of mechanical tractions exerted by cells in three-dimensional matrices,” Nat. Methods 7(12), 969–971 (2010).
[Crossref] [PubMed]

Blanchot, L.

Blatter, C.

Bloom, R. J.

R. J. Bloom, J. P. George, A. Celedon, S. X. Sun, and D. Wirtz, “Mapping Local Matrix Remodeling Induced by a Migrating Tumor Cell Using Three-Dimensional Multiple-Particle Tracking,” Biophys. J. 95(8), 4077–4088 (2008).
[Crossref] [PubMed]

Boccara, A. C.

Boettiger, D.

M. J. Paszek, N. Zahir, K. R. Johnson, J. N. Lakins, G. I. Rozenberg, A. Gefen, C. A. Reinhart-King, S. S. Margulies, M. Dembo, D. Boettiger, D. A. Hammer, and V. M. Weaver, “Tensional homeostasis and the malignant phenotype,” Cancer Cell 8(3), 241–254 (2005).
[Crossref] [PubMed]

Bogdanov, A. A.

V. D. Gordon, M. T. Valentine, M. L. Gardel, D. Andor-Ardó, S. Dennison, A. A. Bogdanov, D. A. Weitz, and T. S. Deisboeck, “Measuring the mechanical stress induced by an expanding multicellular tumor system: a case study,” Exp. Cell Res. 289(1), 58–66 (2003).
[Crossref] [PubMed]

Bonakdar, N.

T. M. Koch, S. Münster, N. Bonakdar, J. P. Butler, and B. Fabry, “3D Traction Forces in Cancer Cell Invasion,” PLoS One 7(3), e33476 (2012).
[Crossref] [PubMed]

Boppart, S. A.

N. D. Shemonski, F. A. South, Y.-Z. Liu, S. G. Adie, P. S. Carney, and S. A. Boppart, “Computational high-resolution optical imaging of the living human retina,” Nat. Photonics 9(7), 440–443 (2015).
[Crossref] [PubMed]

Y.-Z. Liu, N. D. Shemonski, S. G. Adie, A. Ahmad, A. J. Bower, P. S. Carney, and S. A. Boppart, “Computed optical interferometric tomography for high-speed volumetric cellular imaging,” Biomed. Opt. Express 5(9), 2988–3000 (2014).
[Crossref] [PubMed]

S. G. Adie, N. D. Shemonski, B. W. Graf, A. Ahmad, P. Scott Carney, and S. A. Boppart, “Guide-star-based computational adaptive optics for broadband interferometric tomography,” Appl. Phys. Lett. 101(22), 221117 (2012).
[Crossref] [PubMed]

S. G. Adie, B. W. Graf, A. Ahmad, P. S. Carney, and S. A. Boppart, “Computational adaptive optics for broadband optical interferometric tomography of biological tissue,” Proc. Natl. Acad. Sci. U.S.A. 109(19), 7175–7180 (2012).
[Crossref] [PubMed]

R. G. Chelliyil, T. S. Ralston, D. L. Marks, and S. A. Boppart, “High-speed processing architecture for spectral-domain optical coherence microscopy,” J. Biomed. Opt. 13(4), 044013 (2008).
[Crossref] [PubMed]

T. S. Ralston, D. L. Marks, P. S. Carney, and S. A. Boppart, “Interferometric synthetic aperture microscopy,” Nat. Phys. 3(2), 129–134 (2007).
[Crossref] [PubMed]

W. Tan, A. L. Oldenburg, J. J. Norman, T. A. Desai, and S. A. Boppart, “Optical coherence tomography of cell dynamics in three-dimensional tissue models,” Opt. Express 14(16), 7159–7171 (2006).
[Crossref] [PubMed]

D. L. Marks, A. L. Oldenburg, J. J. Reynolds, and S. A. Boppart, “Autofocus algorithm for dispersion correction in optical coherence tomography,” Appl. Opt. 42(16), 3038–3046 (2003).
[Crossref] [PubMed]

Borg, T. K.

P. J. Hunter and T. K. Borg, “Integration from proteins to organs: the Physiome Project,” Nat. Rev. Mol. Cell Biol. 4(3), 237–243 (2003).
[Crossref] [PubMed]

Botvinick, E.

J. L. Compton, J. C. Luo, H. Ma, E. Botvinick, and V. Venugopalan, “High-throughput optical screening of cellular mechanotransduction,” Nat. Photonics 8(9), 710–715 (2014).
[Crossref] [PubMed]

Bouchard, M. B.

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J. Fu, F. Pierron, and P. D. Ruiz, “Elastic stiffness characterization using three-dimensional full-field deformation obtained with optical coherence tomography and digital volume correlation,” J. Biomed. Opt. 18(12), 121512 (2013).
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N. Mohan, I. Stojanovic, W. C. Karl, B. E. A. Saleh, and M. C. Teich, “Compressed sensing in optical coherence tomography,” Proc. SPIE 7570, 75700L (2010).

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A. Kumar, T. Kamali, R. Platzer, A. Unterhuber, W. Drexler, and R. A. Leitgeb, “Anisotropic aberration correction using region of interest based digital adaptive optics in Fourier domain OCT,” Biomed. Opt. Express 6(4), 1124–1134 (2015).
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J. A. Mulligan, G. R. Untracht, S. N. Chandrasekaran, C. N. Brown, and S. G. Adie, “Emerging Approaches for High-Resolution Imaging of Tissue Biomechanics with Optical Coherence Elastography,” IEEE J. Sel. Top. Quantum Electron. 22(3), 246 (2016).
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X. Trepat, M. R. Wasserman, T. E. Angelini, E. Millet, D. A. Weitz, J. P. Butler, and J. J. Fredberg, “Physical forces during collective cell migration,” Nat. Phys. 5(6), 426–430 (2009).
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M. S. Hall, R. Long, X. Feng, Y. Huang, C.-Y. Hui, and M. Wu, “Toward single cell traction microscopy within 3D collagen matrices,” Exp. Cell Res. 319(16), 2396–2408 (2013).
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P. P. Provenzano, D. R. Inman, K. W. Eliceiri, J. G. Knittel, L. Yan, C. T. Rueden, J. G. White, and P. J. Keely, “Collagen density promotes mammary tumor initiation and progression,” BMC Med. 6(1), 11 (2008).
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C. Sun, B. Standish, B. Vuong, X.-Y. Wen, and V. Yang, “Digital image correlation-based optical coherence elastography,” J. Biomed. Opt. 18(12), 121515 (2013).
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K. R. Levental, H. Yu, L. Kass, J. N. Lakins, M. Egeblad, J. T. Erler, S. F. T. Fong, K. Csiszar, A. Giaccia, W. Weninger, M. Yamauchi, D. L. Gasser, and V. M. Weaver, “Matrix crosslinking forces tumor progression by enhancing integrin signaling,” Cell 139(5), 891–906 (2009).
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M. J. Paszek, N. Zahir, K. R. Johnson, J. N. Lakins, G. I. Rozenberg, A. Gefen, C. A. Reinhart-King, S. S. Margulies, M. Dembo, D. Boettiger, D. A. Hammer, and V. M. Weaver, “Tensional homeostasis and the malignant phenotype,” Cancer Cell 8(3), 241–254 (2005).
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D. T. Tambe, C. C. Hardin, T. E. Angelini, K. Rajendran, C. Y. Park, X. Serra-Picamal, E. H. Zhou, M. H. Zaman, J. P. Butler, D. A. Weitz, J. J. Fredberg, and X. Trepat, “Collective cell guidance by cooperative intercellular forces,” Nat. Mater. 10(6), 469–475 (2011).
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H. Tang, J. A. Mulligan, G. R. Untracht, X. Zhang, and S. G. Adie, “GPU-based computational adaptive optics for volumetric optical coherence microscopy,” Proc. SPIE 9720, 97200O (2016).

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J. H. Kim, X. Serra-Picamal, D. T. Tambe, E. H. Zhou, C. Y. Park, M. Sadati, J.-A. Park, R. Krishnan, B. Gweon, E. Millet, J. P. Butler, X. Trepat, and J. J. Fredberg, “Propulsion and navigation within the advancing monolayer sheet,” Nat. Mater. 12(9), 856–863 (2013).
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D. T. Tambe, C. C. Hardin, T. E. Angelini, K. Rajendran, C. Y. Park, X. Serra-Picamal, E. H. Zhou, M. H. Zaman, J. P. Butler, D. A. Weitz, J. J. Fredberg, and X. Trepat, “Collective cell guidance by cooperative intercellular forces,” Nat. Mater. 10(6), 469–475 (2011).
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S. G. Adie, N. D. Shemonski, B. W. Graf, A. Ahmad, P. Scott Carney, and S. A. Boppart, “Guide-star-based computational adaptive optics for broadband interferometric tomography,” Appl. Phys. Lett. 101(22), 221117 (2012).
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R. L. Blackmon, R. Sandhu, B. S. Chapman, P. Casbas-Hernandez, J. B. Tracy, M. A. Troester, and A. L. Oldenburg, “Imaging Extracellular Matrix Remodeling In Vitro by Diffusion-Sensitive Optical Coherence Tomography,” Biophys. J. 110(8), 1858–1868 (2016).
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L. G. Vincent, Y. S. Choi, B. Alonso-Latorre, J. C. del Álamo, and A. J. Engler, “Mesenchymal stem cell durotaxis depends on substrate stiffness gradient strength,” Biotechnol. J. 8(4), 472–484 (2013).
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P. P. Provenzano, D. R. Inman, K. W. Eliceiri, J. G. Knittel, L. Yan, C. T. Rueden, J. G. White, and P. J. Keely, “Collagen density promotes mammary tumor initiation and progression,” BMC Med. 6(1), 11 (2008).
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M. J. Paszek, N. Zahir, K. R. Johnson, J. N. Lakins, G. I. Rozenberg, A. Gefen, C. A. Reinhart-King, S. S. Margulies, M. Dembo, D. Boettiger, D. A. Hammer, and V. M. Weaver, “Tensional homeostasis and the malignant phenotype,” Cancer Cell 8(3), 241–254 (2005).
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Cell (1)

K. R. Levental, H. Yu, L. Kass, J. N. Lakins, M. Egeblad, J. T. Erler, S. F. T. Fong, K. Csiszar, A. Giaccia, W. Weninger, M. Yamauchi, D. L. Gasser, and V. M. Weaver, “Matrix crosslinking forces tumor progression by enhancing integrin signaling,” Cell 139(5), 891–906 (2009).
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S. P. Carey, A. Starchenko, A. L. McGregor, and C. A. Reinhart-King, “Leading malignant cells initiate collective epithelial cell invasion in a three-dimensional heterotypic tumor spheroid model,” Clin. Exp. Metastasis 30(5), 615–630 (2013).
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V. D. Gordon, M. T. Valentine, M. L. Gardel, D. Andor-Ardó, S. Dennison, A. A. Bogdanov, D. A. Weitz, and T. S. Deisboeck, “Measuring the mechanical stress induced by an expanding multicellular tumor system: a case study,” Exp. Cell Res. 289(1), 58–66 (2003).
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M. S. Hall, R. Long, X. Feng, Y. Huang, C.-Y. Hui, and M. Wu, “Toward single cell traction microscopy within 3D collagen matrices,” Exp. Cell Res. 319(16), 2396–2408 (2013).
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J. A. Mulligan, G. R. Untracht, S. N. Chandrasekaran, C. N. Brown, and S. G. Adie, “Emerging Approaches for High-Resolution Imaging of Tissue Biomechanics with Optical Coherence Elastography,” IEEE J. Sel. Top. Quantum Electron. 22(3), 246 (2016).
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R. G. Chelliyil, T. S. Ralston, D. L. Marks, and S. A. Boppart, “High-speed processing architecture for spectral-domain optical coherence microscopy,” J. Biomed. Opt. 13(4), 044013 (2008).
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S. Wang and K. V. Larin, “Optical coherence elastography for tissue characterization: a review,” J. Biophotonics 8(4), 279–302 (2015).
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T. Wakatsuki, B. Schwab, N. C. Thompson, and E. L. Elson, “Effects of cytochalasin D and latrunculin B on mechanical properties of cells,” J. Cell Sci. 114(Pt 5), 1025–1036 (2001).
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O. Chaudhuri, L. Gu, M. Darnell, D. Klumpers, S. A. Bencherif, J. C. Weaver, N. Huebsch, and D. J. Mooney, “Substrate stress relaxation regulates cell spreading,” Nat. Commun. 6, 6365 (2015).
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J. H. Kim, X. Serra-Picamal, D. T. Tambe, E. H. Zhou, C. Y. Park, M. Sadati, J.-A. Park, R. Krishnan, B. Gweon, E. Millet, J. P. Butler, X. Trepat, and J. J. Fredberg, “Propulsion and navigation within the advancing monolayer sheet,” Nat. Mater. 12(9), 856–863 (2013).
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M. B. Bouchard, V. Voleti, C. S. Mendes, C. Lacefield, W. B. Grueber, R. S. Mann, R. M. Bruno, and E. M. C. Hillman, “Swept confocally-aligned planar excitation (SCAPE) microscopy for high speed volumetric imaging of behaving organisms,” Nat. Photonics 9(2), 113–119 (2015).
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J. L. Compton, J. C. Luo, H. Ma, E. Botvinick, and V. Venugopalan, “High-throughput optical screening of cellular mechanotransduction,” Nat. Photonics 8(9), 710–715 (2014).
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Supplementary Material (2)

NameDescription
» Visualization 1: MP4 (1468 KB)      Tracking of 3D deformations induced by NIH-3T3 fibroblasts cultured in a Matrigel-derived ECM. This animation accompanies Figure 2a-2c in the text. Each frame corresponds to the system state at the time denoted in (a).
» Visualization 2: MP4 (1301 KB)      Tracking of 3D deformations induced by NIH-3T3 fibroblasts cultured in a Matrigel-derived ECM. This animation accompanies Figure 2d-2f in the text. Each frame corresponds to the system state at the time denoted in (a).

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Figures (5)

Fig. 1
Fig. 1

Measurement noise floor of the DIC-based ECM displacement tracking algorithm (described in Section 2.6) in the (a) xy-plane and (b) zx-plane, respectively. The variable ‘correlation window side length’ refers to the side length of the windowed deformed-state image. The different curves represent the use of median filters of different sizes following the cross-correlation operation. Displacement noise floors corresponding to the final parameters used in the tracking of cell-induced displacements are denoted by black arrows.

Fig. 2
Fig. 2

Automated tracking of 3D deformations induced by NIH-3T3 fibroblasts cultured in a Matrigel-derived ECM. These images represent the deformations accumulated over a 90 minute imaging time, with reagents introduced to the sample after the first 30 minutes of imaging. Cells were exposed to pure DMSO (a-c), or cytochalasin D solution (d-f). Each subfigure depicts displacements in the en face (upper panels) and vertical (lower panels) orientations. (a,d) Superposition of the initial (t = 0 minutes, red channel) and final (t = 90 minutes, green channel) states of the sample, obtained from the initial and final registered maximum intensity projection images described in Section 2.4. (b,e) Cumulative displacement magnitude of the extracellular matrix (in µm) from a given initial location. (c,f) Cumulative displacement field depicting the direction and relative magnitude of ECM displacement (with arrow lengths exaggerated for visibility), superimposed on the initial maximum intensity projection images. Scale bars = 50 µm. Refer to the text for a discussion of the arrows in (a), (d), and (e).

Fig. 3
Fig. 3

Automated and manual tracking of embedded polystyrene bead cumulative displacement magnitudes in time (top) at varying locations around the cells (bottom) exposed to (a) pure DMSO, or (b) cytochalasin D dissolved in DMSO. All displacement magnitudes are defined with respect to the initial location of a given bead. Solid curves depict results of manual single particle tracking; dashed curves depict results of automated DIC-based displacement tracking. The vertical dashed lines in the displacement plots mark the time at which the DMSO or cytochalasin D was added to the samples. Scale bars = 50 µm.

Fig. 4
Fig. 4

Automated and manual tracking of cumulative displacement magnitudes undergone by embedded polystyrene beads at various selected locations around fibroblasts exposed to the control conditions (DMSO). Each subplot (a-h) depicts the results obtained from independent trials of the experimental protocol. The first subplot (a) depicts the same data discussed in Fig. 3(a). All displacement magnitudes are defined with respect to the initial location of a given bead. Solid curves depict results of manual single particle tracking; dashed curves depict results of automated DIC-based displacement tracking. The vertical dotted lines mark the time at which the samples were exposed to DMSO.

Fig. 5
Fig. 5

Automated and manual tracking of cumulative displacement magnitudes undergone by embedded polystyrene beads at various selected locations around fibroblasts exposed to the contractility inhibiting conditions (cytochalasin D + DMSO). Each subplot (a-h) depicts the results obtained from independent trials of the experimental protocol. The first subplot (a) depicts the same data discussed in Fig. 3(b). All displacement magnitudes are defined with respect to the initial location of a given bead. Solid curves depict results of manual single particle tracking; dashed curves depict results of automated DIC-based displacement tracking. The vertical dotted lines mark the time at which the samples were exposed to cytochalasin D solution.

Equations (1)

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U 0,n ( r )= U 0,n1 ( r )+ u n ( r+ U 0,n1 ( r ) ), for n=1,...,N1 and U 0,0 ( r )=0,

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