Abstract

We have demonstrated a new method of 3D elastography based on 3D light microscopy and micro-scale manipulation. We used custom-built micromanipulators to apply a mechanical force onto multicellular tumor spheroids (200-300 µm in size) and recorded the induced compression with a differential interference contrast (DIC)/confocal microscope to obtain a 4D (x, y, z, and indentation steps) image sequence. Deformation analysis made through 3D pattern tracking without using fluorescence revealed 3D structural and spatial heterogeneity in tumor spheroids. We observed a 20-30 µm-sized spot of locally-induced large deformation within a tumor spheroid. We also found solid fibroblast cores formed in a tumor-fibroblast co-culture spheroid to be stiffer than surrounding cancer cells, which would not have been discovered using only conventional fluorescence. Our new method of 3D elastography may be used to better understand structural composition in multicellular spheroids through analysis of mechanical heterogeneity.

© 2019 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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References

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    [Crossref] [PubMed]
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2018 (2)

P. Grasland-Mongrain, A. Zorgani, S. Nakagawa, S. Bernard, L. G. Paim, G. Fitzharris, S. Catheline, and G. Cloutier, “Ultrafast imaging of cell elasticity with optical microelastography,” Proc. Natl. Acad. Sci. U.S.A. 115(5), 861–866 (2018).
[Crossref] [PubMed]

D. Jaiswal, M. D. Tang-Schomer, D. Sood, D. L. Kaplan, and K. Hoshino, “Nondestructive, Label-Free Characterization of Mechanical Microheterogeneity in Biomimetic Materials,” ACS Biomater. Sci. Eng. 4(9), 3259–3267 (2018).
[Crossref]

2017 (4)

D. Jaiswal, N. Cowley, Z. Bian, G. Zheng, K. P. Claffey, and K. Hoshino, “Stiffness analysis of 3D spheroids using microtweezers,” PLoS One 12(11), e0188346 (2017).
[Crossref] [PubMed]

R. M. S. Sigrist, J. Liau, A. E. Kaffas, M. C. Chammas, and J. K. Willmann, “Ultrasound Elastography: Review of Techniques and Clinical Applications,” Theranostics 7(5), 1303–1329 (2017).
[Crossref] [PubMed]

K. V. Larin and D. D. Sampson, “Optical coherence elastography - OCT at work in tissue biomechanics [Invited],” Biomed. Opt. Express 8(2), 1172–1202 (2017).
[Crossref] [PubMed]

B. F. Kennedy, P. Wijesinghe, and D. D. Sampson, “The emergence of optical elastography in biomedicine,” Nat. Photonics 11(4), 205 (2017).
[Crossref]

2016 (2)

A. Curatolo, M. Villiger, D. Lorenser, P. Wijesinghe, A. Fritz, B. F. Kennedy, and D. D. Sampson, “Ultrahigh-resolution optical coherence elastography,” Opt. Lett. 41(1), 21–24 (2016).
[Crossref] [PubMed]

S. Yamaguchi, R. Morizane, K. Homma, T. Monkawa, S. Suzuki, S. Fujii, M. Koda, K. Hiratsuka, M. Yamashita, T. Yoshida, S. Wakino, K. Hayashi, J. Sasaki, S. Hori, and H. Itoh, “Generation of kidney tubular organoids from human pluripotent stem cells,” Sci. Rep. 6(1), 38353 (2016).
[Crossref] [PubMed]

2015 (4)

Y. Jamin, J. K. R. Boult, J. Li, S. Popov, P. Garteiser, J. L. Ulloa, C. Cummings, G. Box, S. A. Eccles, C. Jones, J. C. Waterton, J. C. Bamber, R. Sinkus, and S. P. Robinson, “Exploring the biomechanical properties of brain malignancies and their pathologic determinants in vivo with magnetic resonance elastography,” Cancer Res. 75(7), 1216–1224 (2015).
[Crossref] [PubMed]

C. Leroux, J. Palmier, A. C. Boccara, G. Cappello, and S. Monnier, “Elastography of multicellular aggregates submitted to osmo-mechanical stress,” New J. Phys. 17(7), 073035 (2015).
[Crossref]

S. Bartfeld, T. Bayram, M. van de Wetering, M. Huch, H. Begthel, P. Kujala, R. Vries, P. J. Peters, and H. Clevers, “In vitro expansion of human gastric epithelial stem cells and their responses to bacterial infection,” Gastroenterology 148(1), 126–136 (2015).
[Crossref] [PubMed]

T. Dehoux, M. Abi Ghanem, O. F. Zouani, J. M. Rampnoux, Y. Guillet, S. Dilhaire, M. C. Durrieu, and B. Audoin, “All-optical broadband ultrasonography of single cells,” Sci. Rep. 5(1), 8650 (2015).
[Crossref] [PubMed]

2014 (2)

C. Wenzel, B. Riefke, S. Gründemann, A. Krebs, S. Christian, F. Prinz, M. Osterland, S. Golfier, S. Räse, N. Ansari, M. Esner, M. Bickle, F. Pampaloni, C. Mattheyer, E. H. Stelzer, K. Parczyk, S. Prechtl, and P. Steigemann, “3D high-content screening for the identification of compounds that target cells in dormant tumor spheroid regions,” Exp. Cell Res. 323(1), 131–143 (2014).
[Crossref] [PubMed]

R. L. DiMarco, J. Su, K. S. Yan, R. Dewi, C. J. Kuo, and S. C. Heilshorn, “Engineering of three-dimensional microenvironments to promote contractile behavior in primary intestinal organoids,” Integr. Biol. 6(2), 127–142 (2014).
[Crossref] [PubMed]

2013 (2)

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]

K. M. Kennedy, C. Ford, B. F. Kennedy, M. B. Bush, and D. D. Sampson, “Analysis of mechanical contrast in optical coherence elastography,” J. Biomed. Opt. 18(12), 121508 (2013).
[Crossref] [PubMed]

2012 (3)

E. S. Nakasone, H. A. Askautrud, T. Kees, J. H. Park, V. Plaks, A. J. Ewald, M. Fein, M. G. Rasch, Y. X. Tan, J. Qiu, J. Park, P. Sinha, M. J. Bissell, E. Frengen, Z. Werb, and M. Egeblad, “Imaging tumor-stroma interactions during chemotherapy reveals contributions of the microenvironment to resistance,” Cancer Cell 21(4), 488–503 (2012).
[Crossref] [PubMed]

A. L. Correia and M. J. Bissell, “The tumor microenvironment is a dominant force in multidrug resistance,” Drug Resist. Updat. 15(1-2), 39–49 (2012).
[Crossref] [PubMed]

G. Mehta, A. Y. Hsiao, M. Ingram, G. D. Luker, and S. Takayama, “Opportunities and challenges for use of tumor spheroids as models to test drug delivery and efficacy,” J. Control. Release 164(2), 192–204 (2012).
[Crossref] [PubMed]

2011 (1)

A. Sarvazyan, T. J. Hall, M. W. Urban, M. Fatemi, S. R. Aglyamov, and B. S. Garra, “An overview of elastography-an emerging branch of medical imaging,” Curr. Med. Imaging Rev. 7(4), 255–282 (2011).
[Crossref] [PubMed]

2010 (1)

T. Liu, B. Lin, and J. Qin, “Carcinoma-associated fibroblasts promoted tumor spheroid invasion on a microfluidic 3D co-culture device,” Lab Chip 10(13), 1671–1677 (2010).
[Crossref] [PubMed]

2009 (1)

M. B. Meads, R. A. Gatenby, and W. S. Dalton, “Environment-mediated drug resistance: a major contributor to minimal residual disease,” Nat. Rev. Cancer 9(9), 665–674 (2009).
[Crossref] [PubMed]

2008 (2)

J. E. Visvader and G. J. Lindeman, “Cancer stem cells in solid tumours: accumulating evidence and unresolved questions,” Nat. Rev. Cancer 8(10), 755–768 (2008).
[Crossref] [PubMed]

C. Tatsumi, M. Kudo, K. Ueshima, S. Kitai, S. Takahashi, T. Inoue, Y. Minami, H. Chung, K. Maekawa, K. Fujimoto, T. Akiko, and M. Takeshi, “Noninvasive evaluation of hepatic fibrosis using serum fibrotic markers, transient elastography (FibroScan) and real-time tissue elastography,” Intervirology 51(Suppl 1), 27–33 (2008).
[Crossref] [PubMed]

2007 (4)

T. Vargo-Gogola and J. M. Rosen, “Modelling breast cancer: one size does not fit all,” Nat. Rev. Cancer 7(9), 659–672 (2007).
[Crossref] [PubMed]

S. E. Cross, Y. S. Jin, J. Rao, and J. K. Gimzewski, “Nanomechanical analysis of cells from cancer patients,” Nat. Nanotechnol. 2(12), 780–783 (2007).
[Crossref] [PubMed]

A. Ivascu and M. Kubbies, “Diversity of cell-mediated adhesions in breast cancer spheroids,” Int. J. Oncol. 31(6), 1403–1413 (2007).
[Crossref] [PubMed]

M. Zietarska, C. M. Maugard, A. Filali-Mouhim, M. Alam-Fahmy, P. N. Tonin, D. M. Provencher, and A. M. Mes-Masson, “Molecular description of a 3D in vitro model for the study of epithelial ovarian cancer (EOC),” Mol. Carcinog. 46(10), 872–885 (2007).
[Crossref] [PubMed]

2006 (1)

A. S. Khalil, B. E. Bouma, and M. R. Kaazempur Mofrad, “A combined FEM/genetic algorithm for vascular soft tissue elasticity estimation,” Cardiovasc. Eng. 6(3), 93–102 (2006).
[Crossref] [PubMed]

2005 (1)

A. S. Khalil, R. C. Chan, A. H. Chau, B. E. Bouma, and M. R. K. Mofrad, “Tissue elasticity estimation with optical coherence elastography: toward mechanical characterization of in vivo soft tissue,” Ann. Biomed. Eng. 33(11), 1631–1639 (2005).
[Crossref] [PubMed]

2004 (1)

Y. Tseng, J. S. Lee, T. P. Kole, I. Jiang, and D. Wirtz, “Micro-organization and visco-elasticity of the interphase nucleus revealed by particle nanotracking,” J. Cell Sci. 117(Pt 10), 2159–2167 (2004).
[Crossref] [PubMed]

2002 (1)

P. Seidl, R. Huettinger, R. Knuechel, and L. A. Kunz-Schughart, “Three-dimensional fibroblast-tumor cell interaction causes downregulation of RACK1 mRNA expression in breast cancer cells in vitro,” Int. J. Cancer 102(2), 129–136 (2002).
[Crossref] [PubMed]

2001 (1)

K. R. Nightingale, M. L. Palmeri, R. W. Nightingale, and G. E. Trahey, “On the feasibility of remote palpation using acoustic radiation force,” J. Acoust. Soc. Am. 110(1), 625–634 (2001).
[Crossref] [PubMed]

1999 (1)

S. N. Bhatia and C. S. Chen, “Tissue engineering at the micro-scale,” Biomed. Microdevices 2(2), 131–144 (1999).
[Crossref] [PubMed]

1998 (1)

1995 (1)

R. Muthupillai, D. J. Lomas, P. J. Rossman, J. F. Greenleaf, A. Manduca, and R. L. Ehman, “Magnetic resonance elastography by direct visualization of propagating acoustic strain waves,” Science 269(5232), 1854–1857 (1995).
[Crossref] [PubMed]

1989 (1)

H. Bruck, S. McNeill, M. A. Sutton, and W. Peters, “Digital image correlation using Newton-Raphson method of partial differential correction,” Exp. Mech. 29(3), 261–267 (1989).
[Crossref]

Abi Ghanem, M.

T. Dehoux, M. Abi Ghanem, O. F. Zouani, J. M. Rampnoux, Y. Guillet, S. Dilhaire, M. C. Durrieu, and B. Audoin, “All-optical broadband ultrasonography of single cells,” Sci. Rep. 5(1), 8650 (2015).
[Crossref] [PubMed]

Aglyamov, S. R.

A. Sarvazyan, T. J. Hall, M. W. Urban, M. Fatemi, S. R. Aglyamov, and B. S. Garra, “An overview of elastography-an emerging branch of medical imaging,” Curr. Med. Imaging Rev. 7(4), 255–282 (2011).
[Crossref] [PubMed]

Akiko, T.

C. Tatsumi, M. Kudo, K. Ueshima, S. Kitai, S. Takahashi, T. Inoue, Y. Minami, H. Chung, K. Maekawa, K. Fujimoto, T. Akiko, and M. Takeshi, “Noninvasive evaluation of hepatic fibrosis using serum fibrotic markers, transient elastography (FibroScan) and real-time tissue elastography,” Intervirology 51(Suppl 1), 27–33 (2008).
[Crossref] [PubMed]

Alam-Fahmy, M.

M. Zietarska, C. M. Maugard, A. Filali-Mouhim, M. Alam-Fahmy, P. N. Tonin, D. M. Provencher, and A. M. Mes-Masson, “Molecular description of a 3D in vitro model for the study of epithelial ovarian cancer (EOC),” Mol. Carcinog. 46(10), 872–885 (2007).
[Crossref] [PubMed]

Ansari, N.

C. Wenzel, B. Riefke, S. Gründemann, A. Krebs, S. Christian, F. Prinz, M. Osterland, S. Golfier, S. Räse, N. Ansari, M. Esner, M. Bickle, F. Pampaloni, C. Mattheyer, E. H. Stelzer, K. Parczyk, S. Prechtl, and P. Steigemann, “3D high-content screening for the identification of compounds that target cells in dormant tumor spheroid regions,” Exp. Cell Res. 323(1), 131–143 (2014).
[Crossref] [PubMed]

Askautrud, H. A.

E. S. Nakasone, H. A. Askautrud, T. Kees, J. H. Park, V. Plaks, A. J. Ewald, M. Fein, M. G. Rasch, Y. X. Tan, J. Qiu, J. Park, P. Sinha, M. J. Bissell, E. Frengen, Z. Werb, and M. Egeblad, “Imaging tumor-stroma interactions during chemotherapy reveals contributions of the microenvironment to resistance,” Cancer Cell 21(4), 488–503 (2012).
[Crossref] [PubMed]

Audoin, B.

T. Dehoux, M. Abi Ghanem, O. F. Zouani, J. M. Rampnoux, Y. Guillet, S. Dilhaire, M. C. Durrieu, and B. Audoin, “All-optical broadband ultrasonography of single cells,” Sci. Rep. 5(1), 8650 (2015).
[Crossref] [PubMed]

Bamber, J. C.

Y. Jamin, J. K. R. Boult, J. Li, S. Popov, P. Garteiser, J. L. Ulloa, C. Cummings, G. Box, S. A. Eccles, C. Jones, J. C. Waterton, J. C. Bamber, R. Sinkus, and S. P. Robinson, “Exploring the biomechanical properties of brain malignancies and their pathologic determinants in vivo with magnetic resonance elastography,” Cancer Res. 75(7), 1216–1224 (2015).
[Crossref] [PubMed]

Bartfeld, S.

S. Bartfeld, T. Bayram, M. van de Wetering, M. Huch, H. Begthel, P. Kujala, R. Vries, P. J. Peters, and H. Clevers, “In vitro expansion of human gastric epithelial stem cells and their responses to bacterial infection,” Gastroenterology 148(1), 126–136 (2015).
[Crossref] [PubMed]

Bayram, T.

S. Bartfeld, T. Bayram, M. van de Wetering, M. Huch, H. Begthel, P. Kujala, R. Vries, P. J. Peters, and H. Clevers, “In vitro expansion of human gastric epithelial stem cells and their responses to bacterial infection,” Gastroenterology 148(1), 126–136 (2015).
[Crossref] [PubMed]

Begthel, H.

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P. Grasland-Mongrain, A. Zorgani, S. Nakagawa, S. Bernard, L. G. Paim, G. Fitzharris, S. Catheline, and G. Cloutier, “Ultrafast imaging of cell elasticity with optical microelastography,” Proc. Natl. Acad. Sci. U.S.A. 115(5), 861–866 (2018).
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S. N. Bhatia and C. S. Chen, “Tissue engineering at the micro-scale,” Biomed. Microdevices 2(2), 131–144 (1999).
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D. Jaiswal, N. Cowley, Z. Bian, G. Zheng, K. P. Claffey, and K. Hoshino, “Stiffness analysis of 3D spheroids using microtweezers,” PLoS One 12(11), e0188346 (2017).
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C. Wenzel, B. Riefke, S. Gründemann, A. Krebs, S. Christian, F. Prinz, M. Osterland, S. Golfier, S. Räse, N. Ansari, M. Esner, M. Bickle, F. Pampaloni, C. Mattheyer, E. H. Stelzer, K. Parczyk, S. Prechtl, and P. Steigemann, “3D high-content screening for the identification of compounds that target cells in dormant tumor spheroid regions,” Exp. Cell Res. 323(1), 131–143 (2014).
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A. L. Correia and M. J. Bissell, “The tumor microenvironment is a dominant force in multidrug resistance,” Drug Resist. Updat. 15(1-2), 39–49 (2012).
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E. S. Nakasone, H. A. Askautrud, T. Kees, J. H. Park, V. Plaks, A. J. Ewald, M. Fein, M. G. Rasch, Y. X. Tan, J. Qiu, J. Park, P. Sinha, M. J. Bissell, E. Frengen, Z. Werb, and M. Egeblad, “Imaging tumor-stroma interactions during chemotherapy reveals contributions of the microenvironment to resistance,” Cancer Cell 21(4), 488–503 (2012).
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C. Leroux, J. Palmier, A. C. Boccara, G. Cappello, and S. Monnier, “Elastography of multicellular aggregates submitted to osmo-mechanical stress,” New J. Phys. 17(7), 073035 (2015).
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Y. Jamin, J. K. R. Boult, J. Li, S. Popov, P. Garteiser, J. L. Ulloa, C. Cummings, G. Box, S. A. Eccles, C. Jones, J. C. Waterton, J. C. Bamber, R. Sinkus, and S. P. Robinson, “Exploring the biomechanical properties of brain malignancies and their pathologic determinants in vivo with magnetic resonance elastography,” Cancer Res. 75(7), 1216–1224 (2015).
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A. S. Khalil, B. E. Bouma, and M. R. Kaazempur Mofrad, “A combined FEM/genetic algorithm for vascular soft tissue elasticity estimation,” Cardiovasc. Eng. 6(3), 93–102 (2006).
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Box, G.

Y. Jamin, J. K. R. Boult, J. Li, S. Popov, P. Garteiser, J. L. Ulloa, C. Cummings, G. Box, S. A. Eccles, C. Jones, J. C. Waterton, J. C. Bamber, R. Sinkus, and S. P. Robinson, “Exploring the biomechanical properties of brain malignancies and their pathologic determinants in vivo with magnetic resonance elastography,” Cancer Res. 75(7), 1216–1224 (2015).
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H. Bruck, S. McNeill, M. A. Sutton, and W. Peters, “Digital image correlation using Newton-Raphson method of partial differential correction,” Exp. Mech. 29(3), 261–267 (1989).
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K. M. Kennedy, C. Ford, B. F. Kennedy, M. B. Bush, and D. D. Sampson, “Analysis of mechanical contrast in optical coherence elastography,” J. Biomed. Opt. 18(12), 121508 (2013).
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Cappello, G.

C. Leroux, J. Palmier, A. C. Boccara, G. Cappello, and S. Monnier, “Elastography of multicellular aggregates submitted to osmo-mechanical stress,” New J. Phys. 17(7), 073035 (2015).
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Catheline, S.

P. Grasland-Mongrain, A. Zorgani, S. Nakagawa, S. Bernard, L. G. Paim, G. Fitzharris, S. Catheline, and G. Cloutier, “Ultrafast imaging of cell elasticity with optical microelastography,” Proc. Natl. Acad. Sci. U.S.A. 115(5), 861–866 (2018).
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Chammas, M. C.

R. M. S. Sigrist, J. Liau, A. E. Kaffas, M. C. Chammas, and J. K. Willmann, “Ultrasound Elastography: Review of Techniques and Clinical Applications,” Theranostics 7(5), 1303–1329 (2017).
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A. S. Khalil, R. C. Chan, A. H. Chau, B. E. Bouma, and M. R. K. Mofrad, “Tissue elasticity estimation with optical coherence elastography: toward mechanical characterization of in vivo soft tissue,” Ann. Biomed. Eng. 33(11), 1631–1639 (2005).
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Chau, A. H.

A. S. Khalil, R. C. Chan, A. H. Chau, B. E. Bouma, and M. R. K. Mofrad, “Tissue elasticity estimation with optical coherence elastography: toward mechanical characterization of in vivo soft tissue,” Ann. Biomed. Eng. 33(11), 1631–1639 (2005).
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Chen, C. S.

S. N. Bhatia and C. S. Chen, “Tissue engineering at the micro-scale,” Biomed. Microdevices 2(2), 131–144 (1999).
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Christian, S.

C. Wenzel, B. Riefke, S. Gründemann, A. Krebs, S. Christian, F. Prinz, M. Osterland, S. Golfier, S. Räse, N. Ansari, M. Esner, M. Bickle, F. Pampaloni, C. Mattheyer, E. H. Stelzer, K. Parczyk, S. Prechtl, and P. Steigemann, “3D high-content screening for the identification of compounds that target cells in dormant tumor spheroid regions,” Exp. Cell Res. 323(1), 131–143 (2014).
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Chung, H.

C. Tatsumi, M. Kudo, K. Ueshima, S. Kitai, S. Takahashi, T. Inoue, Y. Minami, H. Chung, K. Maekawa, K. Fujimoto, T. Akiko, and M. Takeshi, “Noninvasive evaluation of hepatic fibrosis using serum fibrotic markers, transient elastography (FibroScan) and real-time tissue elastography,” Intervirology 51(Suppl 1), 27–33 (2008).
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Claffey, K. P.

D. Jaiswal, N. Cowley, Z. Bian, G. Zheng, K. P. Claffey, and K. Hoshino, “Stiffness analysis of 3D spheroids using microtweezers,” PLoS One 12(11), e0188346 (2017).
[Crossref] [PubMed]

Clevers, H.

S. Bartfeld, T. Bayram, M. van de Wetering, M. Huch, H. Begthel, P. Kujala, R. Vries, P. J. Peters, and H. Clevers, “In vitro expansion of human gastric epithelial stem cells and their responses to bacterial infection,” Gastroenterology 148(1), 126–136 (2015).
[Crossref] [PubMed]

Cloutier, G.

P. Grasland-Mongrain, A. Zorgani, S. Nakagawa, S. Bernard, L. G. Paim, G. Fitzharris, S. Catheline, and G. Cloutier, “Ultrafast imaging of cell elasticity with optical microelastography,” Proc. Natl. Acad. Sci. U.S.A. 115(5), 861–866 (2018).
[Crossref] [PubMed]

Correia, A. L.

A. L. Correia and M. J. Bissell, “The tumor microenvironment is a dominant force in multidrug resistance,” Drug Resist. Updat. 15(1-2), 39–49 (2012).
[Crossref] [PubMed]

Cowley, N.

D. Jaiswal, N. Cowley, Z. Bian, G. Zheng, K. P. Claffey, and K. Hoshino, “Stiffness analysis of 3D spheroids using microtweezers,” PLoS One 12(11), e0188346 (2017).
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Cross, S. E.

S. E. Cross, Y. S. Jin, J. Rao, and J. K. Gimzewski, “Nanomechanical analysis of cells from cancer patients,” Nat. Nanotechnol. 2(12), 780–783 (2007).
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Cummings, C.

Y. Jamin, J. K. R. Boult, J. Li, S. Popov, P. Garteiser, J. L. Ulloa, C. Cummings, G. Box, S. A. Eccles, C. Jones, J. C. Waterton, J. C. Bamber, R. Sinkus, and S. P. Robinson, “Exploring the biomechanical properties of brain malignancies and their pathologic determinants in vivo with magnetic resonance elastography,” Cancer Res. 75(7), 1216–1224 (2015).
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Curatolo, A.

Dalton, W. S.

M. B. Meads, R. A. Gatenby, and W. S. Dalton, “Environment-mediated drug resistance: a major contributor to minimal residual disease,” Nat. Rev. Cancer 9(9), 665–674 (2009).
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T. Dehoux, M. Abi Ghanem, O. F. Zouani, J. M. Rampnoux, Y. Guillet, S. Dilhaire, M. C. Durrieu, and B. Audoin, “All-optical broadband ultrasonography of single cells,” Sci. Rep. 5(1), 8650 (2015).
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R. L. DiMarco, J. Su, K. S. Yan, R. Dewi, C. J. Kuo, and S. C. Heilshorn, “Engineering of three-dimensional microenvironments to promote contractile behavior in primary intestinal organoids,” Integr. Biol. 6(2), 127–142 (2014).
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T. Dehoux, M. Abi Ghanem, O. F. Zouani, J. M. Rampnoux, Y. Guillet, S. Dilhaire, M. C. Durrieu, and B. Audoin, “All-optical broadband ultrasonography of single cells,” Sci. Rep. 5(1), 8650 (2015).
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Y. Jamin, J. K. R. Boult, J. Li, S. Popov, P. Garteiser, J. L. Ulloa, C. Cummings, G. Box, S. A. Eccles, C. Jones, J. C. Waterton, J. C. Bamber, R. Sinkus, and S. P. Robinson, “Exploring the biomechanical properties of brain malignancies and their pathologic determinants in vivo with magnetic resonance elastography,” Cancer Res. 75(7), 1216–1224 (2015).
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Egeblad, M.

E. S. Nakasone, H. A. Askautrud, T. Kees, J. H. Park, V. Plaks, A. J. Ewald, M. Fein, M. G. Rasch, Y. X. Tan, J. Qiu, J. Park, P. Sinha, M. J. Bissell, E. Frengen, Z. Werb, and M. Egeblad, “Imaging tumor-stroma interactions during chemotherapy reveals contributions of the microenvironment to resistance,” Cancer Cell 21(4), 488–503 (2012).
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R. Muthupillai, D. J. Lomas, P. J. Rossman, J. F. Greenleaf, A. Manduca, and R. L. Ehman, “Magnetic resonance elastography by direct visualization of propagating acoustic strain waves,” Science 269(5232), 1854–1857 (1995).
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Esner, M.

C. Wenzel, B. Riefke, S. Gründemann, A. Krebs, S. Christian, F. Prinz, M. Osterland, S. Golfier, S. Räse, N. Ansari, M. Esner, M. Bickle, F. Pampaloni, C. Mattheyer, E. H. Stelzer, K. Parczyk, S. Prechtl, and P. Steigemann, “3D high-content screening for the identification of compounds that target cells in dormant tumor spheroid regions,” Exp. Cell Res. 323(1), 131–143 (2014).
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Ewald, A. J.

E. S. Nakasone, H. A. Askautrud, T. Kees, J. H. Park, V. Plaks, A. J. Ewald, M. Fein, M. G. Rasch, Y. X. Tan, J. Qiu, J. Park, P. Sinha, M. J. Bissell, E. Frengen, Z. Werb, and M. Egeblad, “Imaging tumor-stroma interactions during chemotherapy reveals contributions of the microenvironment to resistance,” Cancer Cell 21(4), 488–503 (2012).
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Fatemi, M.

A. Sarvazyan, T. J. Hall, M. W. Urban, M. Fatemi, S. R. Aglyamov, and B. S. Garra, “An overview of elastography-an emerging branch of medical imaging,” Curr. Med. Imaging Rev. 7(4), 255–282 (2011).
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E. S. Nakasone, H. A. Askautrud, T. Kees, J. H. Park, V. Plaks, A. J. Ewald, M. Fein, M. G. Rasch, Y. X. Tan, J. Qiu, J. Park, P. Sinha, M. J. Bissell, E. Frengen, Z. Werb, and M. Egeblad, “Imaging tumor-stroma interactions during chemotherapy reveals contributions of the microenvironment to resistance,” Cancer Cell 21(4), 488–503 (2012).
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M. Zietarska, C. M. Maugard, A. Filali-Mouhim, M. Alam-Fahmy, P. N. Tonin, D. M. Provencher, and A. M. Mes-Masson, “Molecular description of a 3D in vitro model for the study of epithelial ovarian cancer (EOC),” Mol. Carcinog. 46(10), 872–885 (2007).
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Fitzharris, G.

P. Grasland-Mongrain, A. Zorgani, S. Nakagawa, S. Bernard, L. G. Paim, G. Fitzharris, S. Catheline, and G. Cloutier, “Ultrafast imaging of cell elasticity with optical microelastography,” Proc. Natl. Acad. Sci. U.S.A. 115(5), 861–866 (2018).
[Crossref] [PubMed]

Ford, C.

K. M. Kennedy, C. Ford, B. F. Kennedy, M. B. Bush, and D. D. Sampson, “Analysis of mechanical contrast in optical coherence elastography,” J. Biomed. Opt. 18(12), 121508 (2013).
[Crossref] [PubMed]

Frengen, E.

E. S. Nakasone, H. A. Askautrud, T. Kees, J. H. Park, V. Plaks, A. J. Ewald, M. Fein, M. G. Rasch, Y. X. Tan, J. Qiu, J. Park, P. Sinha, M. J. Bissell, E. Frengen, Z. Werb, and M. Egeblad, “Imaging tumor-stroma interactions during chemotherapy reveals contributions of the microenvironment to resistance,” Cancer Cell 21(4), 488–503 (2012).
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Fritz, A.

Fujii, S.

S. Yamaguchi, R. Morizane, K. Homma, T. Monkawa, S. Suzuki, S. Fujii, M. Koda, K. Hiratsuka, M. Yamashita, T. Yoshida, S. Wakino, K. Hayashi, J. Sasaki, S. Hori, and H. Itoh, “Generation of kidney tubular organoids from human pluripotent stem cells,” Sci. Rep. 6(1), 38353 (2016).
[Crossref] [PubMed]

Fujimoto, K.

C. Tatsumi, M. Kudo, K. Ueshima, S. Kitai, S. Takahashi, T. Inoue, Y. Minami, H. Chung, K. Maekawa, K. Fujimoto, T. Akiko, and M. Takeshi, “Noninvasive evaluation of hepatic fibrosis using serum fibrotic markers, transient elastography (FibroScan) and real-time tissue elastography,” Intervirology 51(Suppl 1), 27–33 (2008).
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Garra, B. S.

A. Sarvazyan, T. J. Hall, M. W. Urban, M. Fatemi, S. R. Aglyamov, and B. S. Garra, “An overview of elastography-an emerging branch of medical imaging,” Curr. Med. Imaging Rev. 7(4), 255–282 (2011).
[Crossref] [PubMed]

Garteiser, P.

Y. Jamin, J. K. R. Boult, J. Li, S. Popov, P. Garteiser, J. L. Ulloa, C. Cummings, G. Box, S. A. Eccles, C. Jones, J. C. Waterton, J. C. Bamber, R. Sinkus, and S. P. Robinson, “Exploring the biomechanical properties of brain malignancies and their pathologic determinants in vivo with magnetic resonance elastography,” Cancer Res. 75(7), 1216–1224 (2015).
[Crossref] [PubMed]

Gatenby, R. A.

M. B. Meads, R. A. Gatenby, and W. S. Dalton, “Environment-mediated drug resistance: a major contributor to minimal residual disease,” Nat. Rev. Cancer 9(9), 665–674 (2009).
[Crossref] [PubMed]

Gimzewski, J. K.

S. E. Cross, Y. S. Jin, J. Rao, and J. K. Gimzewski, “Nanomechanical analysis of cells from cancer patients,” Nat. Nanotechnol. 2(12), 780–783 (2007).
[Crossref] [PubMed]

Golfier, S.

C. Wenzel, B. Riefke, S. Gründemann, A. Krebs, S. Christian, F. Prinz, M. Osterland, S. Golfier, S. Räse, N. Ansari, M. Esner, M. Bickle, F. Pampaloni, C. Mattheyer, E. H. Stelzer, K. Parczyk, S. Prechtl, and P. Steigemann, “3D high-content screening for the identification of compounds that target cells in dormant tumor spheroid regions,” Exp. Cell Res. 323(1), 131–143 (2014).
[Crossref] [PubMed]

Grasland-Mongrain, P.

P. Grasland-Mongrain, A. Zorgani, S. Nakagawa, S. Bernard, L. G. Paim, G. Fitzharris, S. Catheline, and G. Cloutier, “Ultrafast imaging of cell elasticity with optical microelastography,” Proc. Natl. Acad. Sci. U.S.A. 115(5), 861–866 (2018).
[Crossref] [PubMed]

Greenleaf, J. F.

R. Muthupillai, D. J. Lomas, P. J. Rossman, J. F. Greenleaf, A. Manduca, and R. L. Ehman, “Magnetic resonance elastography by direct visualization of propagating acoustic strain waves,” Science 269(5232), 1854–1857 (1995).
[Crossref] [PubMed]

Gründemann, S.

C. Wenzel, B. Riefke, S. Gründemann, A. Krebs, S. Christian, F. Prinz, M. Osterland, S. Golfier, S. Räse, N. Ansari, M. Esner, M. Bickle, F. Pampaloni, C. Mattheyer, E. H. Stelzer, K. Parczyk, S. Prechtl, and P. Steigemann, “3D high-content screening for the identification of compounds that target cells in dormant tumor spheroid regions,” Exp. Cell Res. 323(1), 131–143 (2014).
[Crossref] [PubMed]

Guillet, Y.

T. Dehoux, M. Abi Ghanem, O. F. Zouani, J. M. Rampnoux, Y. Guillet, S. Dilhaire, M. C. Durrieu, and B. Audoin, “All-optical broadband ultrasonography of single cells,” Sci. Rep. 5(1), 8650 (2015).
[Crossref] [PubMed]

Hall, T. J.

A. Sarvazyan, T. J. Hall, M. W. Urban, M. Fatemi, S. R. Aglyamov, and B. S. Garra, “An overview of elastography-an emerging branch of medical imaging,” Curr. Med. Imaging Rev. 7(4), 255–282 (2011).
[Crossref] [PubMed]

Hayashi, K.

S. Yamaguchi, R. Morizane, K. Homma, T. Monkawa, S. Suzuki, S. Fujii, M. Koda, K. Hiratsuka, M. Yamashita, T. Yoshida, S. Wakino, K. Hayashi, J. Sasaki, S. Hori, and H. Itoh, “Generation of kidney tubular organoids from human pluripotent stem cells,” Sci. Rep. 6(1), 38353 (2016).
[Crossref] [PubMed]

Heilshorn, S. C.

R. L. DiMarco, J. Su, K. S. Yan, R. Dewi, C. J. Kuo, and S. C. Heilshorn, “Engineering of three-dimensional microenvironments to promote contractile behavior in primary intestinal organoids,” Integr. Biol. 6(2), 127–142 (2014).
[Crossref] [PubMed]

Hiratsuka, K.

S. Yamaguchi, R. Morizane, K. Homma, T. Monkawa, S. Suzuki, S. Fujii, M. Koda, K. Hiratsuka, M. Yamashita, T. Yoshida, S. Wakino, K. Hayashi, J. Sasaki, S. Hori, and H. Itoh, “Generation of kidney tubular organoids from human pluripotent stem cells,” Sci. Rep. 6(1), 38353 (2016).
[Crossref] [PubMed]

Homma, K.

S. Yamaguchi, R. Morizane, K. Homma, T. Monkawa, S. Suzuki, S. Fujii, M. Koda, K. Hiratsuka, M. Yamashita, T. Yoshida, S. Wakino, K. Hayashi, J. Sasaki, S. Hori, and H. Itoh, “Generation of kidney tubular organoids from human pluripotent stem cells,” Sci. Rep. 6(1), 38353 (2016).
[Crossref] [PubMed]

Hori, S.

S. Yamaguchi, R. Morizane, K. Homma, T. Monkawa, S. Suzuki, S. Fujii, M. Koda, K. Hiratsuka, M. Yamashita, T. Yoshida, S. Wakino, K. Hayashi, J. Sasaki, S. Hori, and H. Itoh, “Generation of kidney tubular organoids from human pluripotent stem cells,” Sci. Rep. 6(1), 38353 (2016).
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Hoshino, K.

D. Jaiswal, M. D. Tang-Schomer, D. Sood, D. L. Kaplan, and K. Hoshino, “Nondestructive, Label-Free Characterization of Mechanical Microheterogeneity in Biomimetic Materials,” ACS Biomater. Sci. Eng. 4(9), 3259–3267 (2018).
[Crossref]

D. Jaiswal, N. Cowley, Z. Bian, G. Zheng, K. P. Claffey, and K. Hoshino, “Stiffness analysis of 3D spheroids using microtweezers,” PLoS One 12(11), e0188346 (2017).
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Hsiao, A. Y.

G. Mehta, A. Y. Hsiao, M. Ingram, G. D. Luker, and S. Takayama, “Opportunities and challenges for use of tumor spheroids as models to test drug delivery and efficacy,” J. Control. Release 164(2), 192–204 (2012).
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Huch, M.

S. Bartfeld, T. Bayram, M. van de Wetering, M. Huch, H. Begthel, P. Kujala, R. Vries, P. J. Peters, and H. Clevers, “In vitro expansion of human gastric epithelial stem cells and their responses to bacterial infection,” Gastroenterology 148(1), 126–136 (2015).
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Huettinger, R.

P. Seidl, R. Huettinger, R. Knuechel, and L. A. Kunz-Schughart, “Three-dimensional fibroblast-tumor cell interaction causes downregulation of RACK1 mRNA expression in breast cancer cells in vitro,” Int. J. Cancer 102(2), 129–136 (2002).
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Ingram, M.

G. Mehta, A. Y. Hsiao, M. Ingram, G. D. Luker, and S. Takayama, “Opportunities and challenges for use of tumor spheroids as models to test drug delivery and efficacy,” J. Control. Release 164(2), 192–204 (2012).
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Inoue, T.

C. Tatsumi, M. Kudo, K. Ueshima, S. Kitai, S. Takahashi, T. Inoue, Y. Minami, H. Chung, K. Maekawa, K. Fujimoto, T. Akiko, and M. Takeshi, “Noninvasive evaluation of hepatic fibrosis using serum fibrotic markers, transient elastography (FibroScan) and real-time tissue elastography,” Intervirology 51(Suppl 1), 27–33 (2008).
[Crossref] [PubMed]

Itoh, H.

S. Yamaguchi, R. Morizane, K. Homma, T. Monkawa, S. Suzuki, S. Fujii, M. Koda, K. Hiratsuka, M. Yamashita, T. Yoshida, S. Wakino, K. Hayashi, J. Sasaki, S. Hori, and H. Itoh, “Generation of kidney tubular organoids from human pluripotent stem cells,” Sci. Rep. 6(1), 38353 (2016).
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A. Ivascu and M. Kubbies, “Diversity of cell-mediated adhesions in breast cancer spheroids,” Int. J. Oncol. 31(6), 1403–1413 (2007).
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Jaiswal, D.

D. Jaiswal, M. D. Tang-Schomer, D. Sood, D. L. Kaplan, and K. Hoshino, “Nondestructive, Label-Free Characterization of Mechanical Microheterogeneity in Biomimetic Materials,” ACS Biomater. Sci. Eng. 4(9), 3259–3267 (2018).
[Crossref]

D. Jaiswal, N. Cowley, Z. Bian, G. Zheng, K. P. Claffey, and K. Hoshino, “Stiffness analysis of 3D spheroids using microtweezers,” PLoS One 12(11), e0188346 (2017).
[Crossref] [PubMed]

Jamin, Y.

Y. Jamin, J. K. R. Boult, J. Li, S. Popov, P. Garteiser, J. L. Ulloa, C. Cummings, G. Box, S. A. Eccles, C. Jones, J. C. Waterton, J. C. Bamber, R. Sinkus, and S. P. Robinson, “Exploring the biomechanical properties of brain malignancies and their pathologic determinants in vivo with magnetic resonance elastography,” Cancer Res. 75(7), 1216–1224 (2015).
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H. Bruck, S. McNeill, M. A. Sutton, and W. Peters, “Digital image correlation using Newton-Raphson method of partial differential correction,” Exp. Mech. 29(3), 261–267 (1989).
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T. Liu, B. Lin, and J. Qin, “Carcinoma-associated fibroblasts promoted tumor spheroid invasion on a microfluidic 3D co-culture device,” Lab Chip 10(13), 1671–1677 (2010).
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K. V. Larin and D. D. Sampson, “Optical coherence elastography - OCT at work in tissue biomechanics [Invited],” Biomed. Opt. Express 8(2), 1172–1202 (2017).
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K. M. Kennedy, C. Ford, B. F. Kennedy, M. B. Bush, and D. D. Sampson, “Analysis of mechanical contrast in optical coherence elastography,” J. Biomed. Opt. 18(12), 121508 (2013).
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A. Sarvazyan, T. J. Hall, M. W. Urban, M. Fatemi, S. R. Aglyamov, and B. S. Garra, “An overview of elastography-an emerging branch of medical imaging,” Curr. Med. Imaging Rev. 7(4), 255–282 (2011).
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S. Yamaguchi, R. Morizane, K. Homma, T. Monkawa, S. Suzuki, S. Fujii, M. Koda, K. Hiratsuka, M. Yamashita, T. Yoshida, S. Wakino, K. Hayashi, J. Sasaki, S. Hori, and H. Itoh, “Generation of kidney tubular organoids from human pluripotent stem cells,” Sci. Rep. 6(1), 38353 (2016).
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P. Seidl, R. Huettinger, R. Knuechel, and L. A. Kunz-Schughart, “Three-dimensional fibroblast-tumor cell interaction causes downregulation of RACK1 mRNA expression in breast cancer cells in vitro,” Int. J. Cancer 102(2), 129–136 (2002).
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R. M. S. Sigrist, J. Liau, A. E. Kaffas, M. C. Chammas, and J. K. Willmann, “Ultrasound Elastography: Review of Techniques and Clinical Applications,” Theranostics 7(5), 1303–1329 (2017).
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E. S. Nakasone, H. A. Askautrud, T. Kees, J. H. Park, V. Plaks, A. J. Ewald, M. Fein, M. G. Rasch, Y. X. Tan, J. Qiu, J. Park, P. Sinha, M. J. Bissell, E. Frengen, Z. Werb, and M. Egeblad, “Imaging tumor-stroma interactions during chemotherapy reveals contributions of the microenvironment to resistance,” Cancer Cell 21(4), 488–503 (2012).
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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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ACS Biomater. Sci. Eng. (1)

D. Jaiswal, M. D. Tang-Schomer, D. Sood, D. L. Kaplan, and K. Hoshino, “Nondestructive, Label-Free Characterization of Mechanical Microheterogeneity in Biomimetic Materials,” ACS Biomater. Sci. Eng. 4(9), 3259–3267 (2018).
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Ann. Biomed. Eng. (1)

A. S. Khalil, R. C. Chan, A. H. Chau, B. E. Bouma, and M. R. K. Mofrad, “Tissue elasticity estimation with optical coherence elastography: toward mechanical characterization of in vivo soft tissue,” Ann. Biomed. Eng. 33(11), 1631–1639 (2005).
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Biomed. Microdevices (1)

S. N. Bhatia and C. S. Chen, “Tissue engineering at the micro-scale,” Biomed. Microdevices 2(2), 131–144 (1999).
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Biomed. Opt. Express (1)

Cancer Cell (1)

E. S. Nakasone, H. A. Askautrud, T. Kees, J. H. Park, V. Plaks, A. J. Ewald, M. Fein, M. G. Rasch, Y. X. Tan, J. Qiu, J. Park, P. Sinha, M. J. Bissell, E. Frengen, Z. Werb, and M. Egeblad, “Imaging tumor-stroma interactions during chemotherapy reveals contributions of the microenvironment to resistance,” Cancer Cell 21(4), 488–503 (2012).
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Cancer Res. (1)

Y. Jamin, J. K. R. Boult, J. Li, S. Popov, P. Garteiser, J. L. Ulloa, C. Cummings, G. Box, S. A. Eccles, C. Jones, J. C. Waterton, J. C. Bamber, R. Sinkus, and S. P. Robinson, “Exploring the biomechanical properties of brain malignancies and their pathologic determinants in vivo with magnetic resonance elastography,” Cancer Res. 75(7), 1216–1224 (2015).
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Cardiovasc. Eng. (1)

A. S. Khalil, B. E. Bouma, and M. R. Kaazempur Mofrad, “A combined FEM/genetic algorithm for vascular soft tissue elasticity estimation,” Cardiovasc. Eng. 6(3), 93–102 (2006).
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Curr. Med. Imaging Rev. (1)

A. Sarvazyan, T. J. Hall, M. W. Urban, M. Fatemi, S. R. Aglyamov, and B. S. Garra, “An overview of elastography-an emerging branch of medical imaging,” Curr. Med. Imaging Rev. 7(4), 255–282 (2011).
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A. L. Correia and M. J. Bissell, “The tumor microenvironment is a dominant force in multidrug resistance,” Drug Resist. Updat. 15(1-2), 39–49 (2012).
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Exp. Cell Res. (1)

C. Wenzel, B. Riefke, S. Gründemann, A. Krebs, S. Christian, F. Prinz, M. Osterland, S. Golfier, S. Räse, N. Ansari, M. Esner, M. Bickle, F. Pampaloni, C. Mattheyer, E. H. Stelzer, K. Parczyk, S. Prechtl, and P. Steigemann, “3D high-content screening for the identification of compounds that target cells in dormant tumor spheroid regions,” Exp. Cell Res. 323(1), 131–143 (2014).
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Exp. Mech. (1)

H. Bruck, S. McNeill, M. A. Sutton, and W. Peters, “Digital image correlation using Newton-Raphson method of partial differential correction,” Exp. Mech. 29(3), 261–267 (1989).
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Gastroenterology (1)

S. Bartfeld, T. Bayram, M. van de Wetering, M. Huch, H. Begthel, P. Kujala, R. Vries, P. J. Peters, and H. Clevers, “In vitro expansion of human gastric epithelial stem cells and their responses to bacterial infection,” Gastroenterology 148(1), 126–136 (2015).
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Int. J. Cancer (1)

P. Seidl, R. Huettinger, R. Knuechel, and L. A. Kunz-Schughart, “Three-dimensional fibroblast-tumor cell interaction causes downregulation of RACK1 mRNA expression in breast cancer cells in vitro,” Int. J. Cancer 102(2), 129–136 (2002).
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Integr. Biol. (1)

R. L. DiMarco, J. Su, K. S. Yan, R. Dewi, C. J. Kuo, and S. C. Heilshorn, “Engineering of three-dimensional microenvironments to promote contractile behavior in primary intestinal organoids,” Integr. Biol. 6(2), 127–142 (2014).
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Intervirology (1)

C. Tatsumi, M. Kudo, K. Ueshima, S. Kitai, S. Takahashi, T. Inoue, Y. Minami, H. Chung, K. Maekawa, K. Fujimoto, T. Akiko, and M. Takeshi, “Noninvasive evaluation of hepatic fibrosis using serum fibrotic markers, transient elastography (FibroScan) and real-time tissue elastography,” Intervirology 51(Suppl 1), 27–33 (2008).
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J. Acoust. Soc. Am. (1)

K. R. Nightingale, M. L. Palmeri, R. W. Nightingale, and G. E. Trahey, “On the feasibility of remote palpation using acoustic radiation force,” J. Acoust. Soc. Am. 110(1), 625–634 (2001).
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J. Biomed. Opt. (2)

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]

K. M. Kennedy, C. Ford, B. F. Kennedy, M. B. Bush, and D. D. Sampson, “Analysis of mechanical contrast in optical coherence elastography,” J. Biomed. Opt. 18(12), 121508 (2013).
[Crossref] [PubMed]

J. Cell Sci. (1)

Y. Tseng, J. S. Lee, T. P. Kole, I. Jiang, and D. Wirtz, “Micro-organization and visco-elasticity of the interphase nucleus revealed by particle nanotracking,” J. Cell Sci. 117(Pt 10), 2159–2167 (2004).
[Crossref] [PubMed]

J. Control. Release (1)

G. Mehta, A. Y. Hsiao, M. Ingram, G. D. Luker, and S. Takayama, “Opportunities and challenges for use of tumor spheroids as models to test drug delivery and efficacy,” J. Control. Release 164(2), 192–204 (2012).
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Lab Chip (1)

T. Liu, B. Lin, and J. Qin, “Carcinoma-associated fibroblasts promoted tumor spheroid invasion on a microfluidic 3D co-culture device,” Lab Chip 10(13), 1671–1677 (2010).
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Mol. Carcinog. (1)

M. Zietarska, C. M. Maugard, A. Filali-Mouhim, M. Alam-Fahmy, P. N. Tonin, D. M. Provencher, and A. M. Mes-Masson, “Molecular description of a 3D in vitro model for the study of epithelial ovarian cancer (EOC),” Mol. Carcinog. 46(10), 872–885 (2007).
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Nat. Nanotechnol. (1)

S. E. Cross, Y. S. Jin, J. Rao, and J. K. Gimzewski, “Nanomechanical analysis of cells from cancer patients,” Nat. Nanotechnol. 2(12), 780–783 (2007).
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Nat. Photonics (1)

B. F. Kennedy, P. Wijesinghe, and D. D. Sampson, “The emergence of optical elastography in biomedicine,” Nat. Photonics 11(4), 205 (2017).
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Nat. Rev. Cancer (3)

T. Vargo-Gogola and J. M. Rosen, “Modelling breast cancer: one size does not fit all,” Nat. Rev. Cancer 7(9), 659–672 (2007).
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M. B. Meads, R. A. Gatenby, and W. S. Dalton, “Environment-mediated drug resistance: a major contributor to minimal residual disease,” Nat. Rev. Cancer 9(9), 665–674 (2009).
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J. E. Visvader and G. J. Lindeman, “Cancer stem cells in solid tumours: accumulating evidence and unresolved questions,” Nat. Rev. Cancer 8(10), 755–768 (2008).
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New J. Phys. (1)

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Supplementary Material (5)

NameDescription
» Visualization 1       Analysis of a tumor spheroid
» Visualization 2       Detailed strain analysis
» Visualization 3       Analysis of a tumor-fibroblast co-culture spheroid
» Visualization 4       3D strain map
» Visualization 5       3D fluorescence overlay

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Figures (5)

Fig. 1
Fig. 1 Image tracking and deformation analysis. (a) The bottom half of the spheroid was imaged by the Nikon DIC/confocal microscope as it was gently compressed by a pair of tweezers. (b) A meshed model was built based on the obtained 3D image. (c) Nodal displacement was found by image-tracking a voxel. (d) The strain vector of each element was found from the displacement vectors of the eight nodes.
Fig. 2
Fig. 2 (a) A cell-sized spot with a localized, large deformation was visualized in the strain analysis of a tumor spheroid. (b) Fluorescence image of the same layer. The white arrow indicates the position of the soft spot. (c) The soft spot was not observed in distant layers. Scale bars = 50 µm. A movie clip (Visualization 1) is available.
Fig. 3
Fig. 3 (a1-a3) Von Mises strain analysis and (b1-b3) corresponding fluorescence images of the further indentation sequence. When a large compression was added, cell displacement is observed as the balloon-like deflation and inflation from (b2) to (b3). The strain analysis detected the displacement at an early step of indentation in (a1). (c) Analysis of axial (x’), lateral (y’), and elevational (z) and shear (xy’, zx’, and yz) strain components. The direction of the indentation was chosen as the x’ axis. Scale bars = 50 µm. See also Visualization 1 and Visualization 2.
Fig. 4
Fig. 4 Analysis of tumor-fibroblast co-culture spheroid. HDFa cells were added to the T47D spheroid at day 7 of incubation, allowing for fibroblast infiltration, and imaged at day 11. (a) Von Mises strain calculated from DIC images. (b) Overlay fluorescence image of tracking dyes used to identify cell types (T47D: red, HDFa: green). Three distinctive regions of fibroblast cells are visible in both images. The strain analysis indicates that fibroblast regions are stiffer than cancer cells. Scale bars = 100 µm. A movie clip (Visualization 3) is available.
Fig. 5
Fig. 5 Analysis of the fibroblast-infiltrated tumor spheroid with (a) 3D strain map and (b) 3D fluorescence overlay of (c) fibroblast (green) and (d) tumor cells (red). Scale bars = 100 µm. Movie clips (Visualization 4 andVisualization 5) are available.

Equations (10)

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{ ε }= [ B ]{ u }
{ ε }= { ε x ;  ε y ;  ε z ; γ xy ; γ zx ; γ yz },
[ B ]=[ N X O O O N Y O O O N Z N Y N X O N Z O N X O N Z N Y ]
N X = 2 Δx [ 1/8 1/8 1/8 1/8 1/8 1/8 1/8 1/8 ]
N Y = 2 Δy [ 1/8 1/8 1/8 1/8 1/8 1/8 1/8 1/8 ]
N Z = 2 Δz [ 1/8 1/8 1/8 1/8 1/8 1/8 1/8 1/8 ]
O=[ 0 0 0 0 0 0 0 0 ]
{ u }= { u 1 ; u 2 ; u 3 ;; u 8 ;  v 1 ;  v 2 ; v 3 ;; v 8 ;  w 1 ;  w 2 ; w 3 ;; w 8 }
ε VM = 2 3 3( e xx 2 + e yy 2 + e zz 2 ) 2 + 3( γ xy 2 + γ zx 2 + γ yz 2 ) 4 ,
e xx =(2 ε xx ε yy ε zz )/3; e yy =( ε xx +2 ε yy ε zz )/; e zz =( ε xx ε yy +2 ε zz )/3.

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