Abstract

Cells sense and respond to external physical forces and substrate rigidity by regulating their cell shape, internal cytoskeletal tension, and stiffness. Here we show that the combination of micropillar traction force and noncontact Brillouin microscopy provides access to cell-generated forces and intracellular mechanical properties at optical resolution. Actin-rich cytoplasmic domains of 3T3 fibroblasts showed significantly higher Brillouin shifts, indicating a potential increase in stiffness when adhering on fibronectin-coated glass compared to soft PDMS micropillars. Our findings demonstrate the complementarity of micropillar traction force and Brillouin microscopy to better understand the relation between cell force generation and the intracellular mechanical properties.

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

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References

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2018 (6)

W. Pomp, K. Schakenraad, H. E. Balcğlu, H. van Hoorn, E. H. Danen, R. M. Merks, T. Schmidt, and L. Giomi, “Cytoskeletal anisotropy controls geometry and forces of adherent cells,” Phys. review letters 121, 178101 (2018).
[Crossref]

M. Abi Ghanem, T. Dehoux, L. Liu, G. Le Saux, L. Plawinski, M.-C. Durrieu, and B. Audoin, “Opto-acoustic microscopy reveals adhesion mechanics of single cells,” Rev. Sci. Instruments 89, 014901 (2018).
[Crossref]

P.-J. Wu, I. V. Kabakova, J. W. Ruberti, J. M. Sherwood, I. E. Dunlop, C. Paterson, P. Török, and D. R. Overby, “Water content, not stiffness, dominates brillouin spectroscopy measurements in hydrated materials,” Nat. methods 15, 561 (2018).
[Crossref] [PubMed]

G. Scarcelli and S. H. Yun, “Reply to ‘water content, not stiffness, dominates brillouin spectroscopy measurements in hydrated materials’,” Nat. methods 15, 562 (2018).
[Crossref] [PubMed]

R. Schlüßler, S. Möllmert, S. Abuhattum, G. Cojoc, P. Müller, K. Kim, C. Möckel, C. Zimmermann, J. Czarske, and J. Guck, “Mechanical mapping of spinal cord growth and repair in living zebrafish larvae by brillouin imaging,” Biophys. journal 115, 911–923 (2018).
[Crossref]

G. Antonacci, V. de Turris, A. Rosa, and G. Ruocco, “Background-deflection brillouin microscopy reveals altered biomechanics of intracellular stress granules by als protein fus,” Commun. biology 1, 139 (2018).
[Crossref]

2017 (5)

F. Scarponi, S. Mattana, S. Corezzi, S. Caponi, L. Comez, P. Sassi, A. Morresi, M. Paolantoni, L. Urbanelli, C. Emiliani, and et al., “High-performance versatile setup for simultaneous brillouin-raman microspectroscopy,” Phys. Rev. X 7, 031015 (2017).

S. Mattana, S. Caponi, F. Tamagnini, D. Fioretto, and F. Palombo, “Viscoelasticity of amyloid plaques in transgenic mouse brain studied by brillouin microspectroscopy and correlative raman analysis,” J. innovative optical health sciences 10, 1742001 (2017).
[Crossref]

G. Antonacci, “Dark-field brillouin microscopy,” Opt. letters 42, 1432–1435 (2017).
[Crossref]

E. Edrei, M. C. Gather, and G. Scarcelli, “Integration of spectral coronagraphy within vipa-based spectrometers for high extinction brillouin imaging,” Opt. express 25, 6895–6903 (2017).
[Crossref] [PubMed]

J. J. Northey, L. Przybyla, and V. M. Weaver, “Tissue force programs cell fate and tumor aggression,” Cancer discovery 7, 1224–1237 (2017).
[Crossref] [PubMed]

2016 (9)

H. Laklai, Y. A. Miroshnikova, M. W. Pickup, E. A. Collisson, G. E. Kim, A. S. Barrett, R. C. Hill, J. N. Lakins, D. D. Schlaepfer, J. K. Mouw, and et al., “Genotype tunes pancreatic ductal adenocarcinoma tissue tension to induce matricellular fibrosis and tumor progression,” Nat. medicine 22, 497 (2016).
[Crossref]

R. Sunyer, V. Conte, J. Escribano, A. Elosegui-Artola, A. Labernadie, L. Valon, D. Navajas, J. M. García-Aznar, J. J. Muñoz, P. Roca-Cusachs, and et al., “Collective cell durotaxis emerges from long-range intercellular force transmission,” Science 353, 1157–1161 (2016).
[Crossref] [PubMed]

Y. A. Miroshnikova, J. K. Mouw, J. M. Barnes, M. W. Pickup, J. N. Lakins, Y. Kim, K. Lobo, A. I. Persson, G. F. Reis, T. R. McKnight, and et al., “Tissue mechanics promote idh1-dependent hif1α–tenascin c feedback to regulate glioblastoma aggression,” Nat. cell biology 18, 1336 (2016).
[Crossref]

G. Antonacci and S. Braakman, “Biomechanics of subcellular structures by non-invasive brillouin microscopy,” Sci. reports 6, 37217 (2016).
[Crossref]

K. Elsayad, S. Werner, M. Gallemí, J. Kong, E. R. S. Guajardo, L. Zhang, Y. Jaillais, T. Greb, and Y. Belkhadir, “Mapping the subcellular mechanical properties of live cells in tissues with fluorescence emission–brillouin imaging,” Sci. Signal. 9, rs5 (2016).
[Crossref]

H. Wolfenson, G. Meacci, S. Liu, M. R. Stachowiak, T. Iskratsch, S. Ghassemi, P. Roca-Cusachs, B. O’Shaughnessy, J. Hone, and M. P. Sheetz, “Tropomyosin controls sarcomere-like contractions for rigidity sensing and suppressing growth on soft matrices,” Nat. cell biology 18, 33 (2016).
[Crossref]

J. Zhang, A. Fiore, S.-H. Yun, H. Kim, and G. Scarcelli, “Line-scanning brillouin microscopy for rapid non-invasive mechanical imaging,” Sci. reports 6, 35398 (2016).
[Crossref]

I. Remer and A. Bilenca, “High-speed stimulated brillouin scattering spectroscopy at 780 nm,” APL Photonics 1, 061301 (2016).
[Crossref]

G. Antonacci, S. De Panfilis, G. Di Domenico, E. DelRe, and G. Ruocco, “Breaking the contrast limit in single-pass fabry-pérot spectrometers,” Phys. Rev. Appl. 6, 054020 (2016).
[Crossref]

2015 (8)

G. Antonacci, G. Lepert, C. Paterson, and P. Török, “Elastic suppression in brillouin imaging by destructive interference,” Appl. Phys. Lett. 107, 061102 (2015).
[Crossref]

G. Antonacci, R. M. Pedrigi, A. Kondiboyina, V. V. Mehta, R. De Silva, C. Paterson, R. Krams, and P. Török, “Quantification of plaque stiffness by brillouin microscopy in experimental thin cap fibroatheroma,” J. Royal Soc. Interface 12, 20150843 (2015).
[Crossref]

M. J. Girard, W. J. Dupps, M. Baskaran, G. Scarcelli, S. H. Yun, H. A. Quigley, I. A. Sigal, and N. G. Strouthidis, “Translating ocular biomechanics into clinical practice: current state and future prospects,” Curr. eye research 40, 1–18 (2015).
[Crossref]

Z. Steelman, Z. Meng, A. J. Traverso, and V. V. Yakovlev, “Brillouin spectroscopy as a new method of screening for increased csf total protein during bacterial meningitis,” J. Biophotonics 8, 408–414 (2015).
[Crossref]

M. Gupta, B. R. Sarangi, J. Deschamps, Y. Nematbakhsh, A. Callan-Jones, F. Margadant, R.-M. Mège, C. T. Lim, R. Voituriez, and B. Ladoux, “Adaptive rheology and ordering of cell cytoskeleton govern matrix rigidity sensing,” Nat. communications 6, 7525 (2015).
[Crossref]

G. Scarcelli, W. J. Polacheck, H. T. Nia, K. Patel, A. J. Grodzinsky, R. D. Kamm, and S. H. Yun, “Noncontact three-dimensional mapping of intracellular hydromechanical properties by brillouin microscopy,” Nat. methods 12, 1132 (2015).
[Crossref] [PubMed]

U. S. Schwarz and J. R. Soiné, “Traction force microscopy on soft elastic substrates: A guide to recent computational advances,” Biochimica et Biophys. Acta (BBA)-Molecular Cell Res. 1853, 3095–3104 (2015).
[Crossref]

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

2014 (3)

M. Abi Ghanem, T. Dehoux, O. F. Zouani, A. Gadalla, M.-C. Durrieu, and B. Audoin, “Remote opto-acoustic probing of single-cell adhesion on metallic surfaces,” J. biophotonics 7, 453–459 (2014).
[Crossref]

H. van Hoorn, R. Harkes, E. M. Spiesz, C. Storm, D. van Noort, B. Ladoux, and T. Schmidt, “The nanoscale architecture of force-bearing focal adhesions,” Nano letters 14, 4257–4262 (2014).
[Crossref] [PubMed]

F. Palombo, M. Madami, N. Stone, and D. Fioretto, “Mechanical mapping with chemical specificity by confocal brillouin and raman microscopy,” Analyst 139, 729–733 (2014).
[Crossref] [PubMed]

2013 (2)

K. J. Koski, P. Akhenblit, K. McKiernan, and J. L. Yarger, “Non-invasive determination of the complete elastic moduli of spider silks,” Nat. Mater. 12, 262 (2013).
[Crossref] [PubMed]

G. Antonacci, M. R. Foreman, C. Paterson, and P. Török, “Spectral broadening in brillouin imaging,” Appl. Phys. Lett. 103, 221105 (2013).
[Crossref]

2012 (2)

S. Ghassemi, G. Meacci, S. Liu, A. A. Gondarenko, A. Mathur, P. Roca-Cusachs, M. P. Sheetz, and J. Hone, “Cells test substrate rigidity by local contractions on submicrometer pillars,” Proc. Natl. Acad. Sci. 109, 5328–5333 (2012).
[Crossref] [PubMed]

F. Bosveld, I. Bonnet, B. Guirao, S. Tlili, Z. Wang, A. Petitalot, R. Marchand, P.-L. Bardet, P. Marcq, F. Graner, and et al., “Mechanical control of morphogenesis by fat/dachsous/four-jointed planar cell polarity pathway,” Science 336, 724–727 (2012).
[Crossref] [PubMed]

2011 (3)

S.-Y. Tee, J. Fu, C. S. Chen, and P. A. Janmey, “Cell shape and substrate rigidity both regulate cell stiffness,” Biophys. journal 100, L25–L27 (2011).
[Crossref]

J. Le Digabel, N. Biais, J. Fresnais, J.-F. Berret, P. Hersen, and B. Ladoux, “Magnetic micropillars as a tool to govern substrate deformations,” Lab on a Chip 11, 2630–2636 (2011).
[Crossref] [PubMed]

G. Scarcelli and S. H. Yun, “Multistage vipa etalons for high-extinction parallel brillouin spectroscopy,” Opt. express 19, 10913–10922 (2011).
[Crossref] [PubMed]

2009 (1)

S. W. Moore, N. Biais, and M. P. Sheetz, “Traction on immobilized netrin-1 is sufficient to reorient axons,” Science 325, 166 (2009).
[Crossref] [PubMed]

2008 (2)

G. Scarcelli and S. H. Yun, “Confocal brillouin microscopy for three-dimensional mechanical imaging,” Nat. photonics 2, 39 (2008).
[Crossref]

M. Ghibaudo, A. Saez, L. Trichet, A. Xayaphoummine, J. Browaeys, P. Silberzan, A. Buguin, and B. Ladoux, “Traction forces and rigidity sensing regulate cell functions,” Soft Matter 4, 1836–1843 (2008).
[Crossref]

2007 (3)

A. Saez, M. Ghibaudo, A. Buguin, P. Silberzan, and B. Ladoux, “Rigidity-driven growth and migration of epithelial cells on microstructured anisotropic substrates,” Proc. Natl. Acad. Sci. 104, 8281–8286 (2007).
[Crossref] [PubMed]

N. J. Sniadecki, A. Anguelouch, M. T. Yang, C. M. Lamb, Z. Liu, S. B. Kirschner, Y. Liu, D. H. Reich, and C. S. Chen, “Magnetic microposts as an approach to apply forces to living cells,” Proc. Natl. Acad. Sci. 104, 14553–14558 (2007).
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I. Levental, P. C. Georges, and P. A. Janmey, “Soft biological materials and their impact on cell function,” Soft Matter 3, 299–306 (2007).
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2006 (1)

A. J. Engler, S. Sen, H. L. Sweeney, and D. E. Discher, “Matrix elasticity directs stem cell lineage specification,” Cell 126, 677–689 (2006).
[Crossref] [PubMed]

2005 (4)

D. E. Discher, P. Janmey, and Y.-l. Wang, “Tissue cells feel and respond to the stiffness of their substrate,” Science 310, 1139–1143 (2005).
[Crossref] [PubMed]

T. Yeung, P. C. Georges, L. A. Flanagan, B. Marg, M. Ortiz, M. Funaki, N. Zahir, W. Ming, V. Weaver, and P. A. Janmey, “Effects of substrate stiffness on cell morphology, cytoskeletal structure, and adhesion,” Cell motility cytoskeleton 60, 24–34 (2005).
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O. Du Roure, A. Saez, A. Buguin, R. H. Austin, P. Chavrier, P. Siberzan, and B. Ladoux, “Force mapping in epithelial cell migration,” Proc. Natl. Acad. Sci. 102, 2390–2395 (2005).
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2004 (1)

D. York, N. M. Evensen, M. L. Martınez, and J. De Basabe Delgado, “Unified equations for the slope, intercept, and standard errors of the best straight line,” Am. J. Phys. 72, 367–375 (2004).
[Crossref]

2003 (2)

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. 100, 1484–1489 (2003).
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1996 (1)

M. Shirasaki, “Large angular dispersion by a virtually imaged phased array and its application to a wavelength demultiplexer,” Opt. letters 21, 366–368 (1996).
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1977 (1)

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Abi Ghanem, M.

M. Abi Ghanem, T. Dehoux, L. Liu, G. Le Saux, L. Plawinski, M.-C. Durrieu, and B. Audoin, “Opto-acoustic microscopy reveals adhesion mechanics of single cells,” Rev. Sci. Instruments 89, 014901 (2018).
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M. Abi Ghanem, T. Dehoux, O. F. Zouani, A. Gadalla, M.-C. Durrieu, and B. Audoin, “Remote opto-acoustic probing of single-cell adhesion on metallic surfaces,” J. biophotonics 7, 453–459 (2014).
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Abuhattum, S.

R. Schlüßler, S. Möllmert, S. Abuhattum, G. Cojoc, P. Müller, K. Kim, C. Möckel, C. Zimmermann, J. Czarske, and J. Guck, “Mechanical mapping of spinal cord growth and repair in living zebrafish larvae by brillouin imaging,” Biophys. journal 115, 911–923 (2018).
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Alfano, V.

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Anguelouch, A.

N. J. Sniadecki, A. Anguelouch, M. T. Yang, C. M. Lamb, Z. Liu, S. B. Kirschner, Y. Liu, D. H. Reich, and C. S. Chen, “Magnetic microposts as an approach to apply forces to living cells,” Proc. Natl. Acad. Sci. 104, 14553–14558 (2007).
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Antonacci, G.

G. Antonacci, V. de Turris, A. Rosa, and G. Ruocco, “Background-deflection brillouin microscopy reveals altered biomechanics of intracellular stress granules by als protein fus,” Commun. biology 1, 139 (2018).
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G. Antonacci, “Dark-field brillouin microscopy,” Opt. letters 42, 1432–1435 (2017).
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G. Antonacci, S. De Panfilis, G. Di Domenico, E. DelRe, and G. Ruocco, “Breaking the contrast limit in single-pass fabry-pérot spectrometers,” Phys. Rev. Appl. 6, 054020 (2016).
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G. Antonacci and S. Braakman, “Biomechanics of subcellular structures by non-invasive brillouin microscopy,” Sci. reports 6, 37217 (2016).
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G. Antonacci, R. M. Pedrigi, A. Kondiboyina, V. V. Mehta, R. De Silva, C. Paterson, R. Krams, and P. Török, “Quantification of plaque stiffness by brillouin microscopy in experimental thin cap fibroatheroma,” J. Royal Soc. Interface 12, 20150843 (2015).
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G. Antonacci, G. Lepert, C. Paterson, and P. Török, “Elastic suppression in brillouin imaging by destructive interference,” Appl. Phys. Lett. 107, 061102 (2015).
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G. Antonacci, M. R. Foreman, C. Paterson, and P. Török, “Spectral broadening in brillouin imaging,” Appl. Phys. Lett. 103, 221105 (2013).
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R. Prevedel, A. Diz-Muñoz, G. Ruocco, and G. Antonacci, “Brillouin microscopy-a revolutionary tool for mechanobiology?” arXiv preprint arXiv:1901.02006 (2019).

R. De Santis, V. Alfano, V. de Turris, A. Colantoni, L. Santini, M. G. Garone, G. Antonacci, G. Peruzzi, E. Sudria-Lopez, E. Wyler, and et al., “Mutant fus and elavl4 (hud) aberrant crosstalk in amyotrophic lateral sclerosis,” Available at SSRN 3261820 (2018).

Audoin, B.

M. Abi Ghanem, T. Dehoux, L. Liu, G. Le Saux, L. Plawinski, M.-C. Durrieu, and B. Audoin, “Opto-acoustic microscopy reveals adhesion mechanics of single cells,” Rev. Sci. Instruments 89, 014901 (2018).
[Crossref]

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

M. Abi Ghanem, T. Dehoux, O. F. Zouani, A. Gadalla, M.-C. Durrieu, and B. Audoin, “Remote opto-acoustic probing of single-cell adhesion on metallic surfaces,” J. biophotonics 7, 453–459 (2014).
[Crossref]

Austin, R. H.

O. Du Roure, A. Saez, A. Buguin, R. H. Austin, P. Chavrier, P. Siberzan, and B. Ladoux, “Force mapping in epithelial cell migration,” Proc. Natl. Acad. Sci. 102, 2390–2395 (2005).
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Balcglu, H. E.

W. Pomp, K. Schakenraad, H. E. Balcğlu, H. van Hoorn, E. H. Danen, R. M. Merks, T. Schmidt, and L. Giomi, “Cytoskeletal anisotropy controls geometry and forces of adherent cells,” Phys. review letters 121, 178101 (2018).
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F. Bosveld, I. Bonnet, B. Guirao, S. Tlili, Z. Wang, A. Petitalot, R. Marchand, P.-L. Bardet, P. Marcq, F. Graner, and et al., “Mechanical control of morphogenesis by fat/dachsous/four-jointed planar cell polarity pathway,” Science 336, 724–727 (2012).
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Y. A. Miroshnikova, J. K. Mouw, J. M. Barnes, M. W. Pickup, J. N. Lakins, Y. Kim, K. Lobo, A. I. Persson, G. F. Reis, T. R. McKnight, and et al., “Tissue mechanics promote idh1-dependent hif1α–tenascin c feedback to regulate glioblastoma aggression,” Nat. cell biology 18, 1336 (2016).
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M. J. Girard, W. J. Dupps, M. Baskaran, G. Scarcelli, S. H. Yun, H. A. Quigley, I. A. Sigal, and N. G. Strouthidis, “Translating ocular biomechanics into clinical practice: current state and future prospects,” Curr. eye research 40, 1–18 (2015).
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Belkhadir, Y.

K. Elsayad, S. Werner, M. Gallemí, J. Kong, E. R. S. Guajardo, L. Zhang, Y. Jaillais, T. Greb, and Y. Belkhadir, “Mapping the subcellular mechanical properties of live cells in tissues with fluorescence emission–brillouin imaging,” Sci. Signal. 9, rs5 (2016).
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Berret, J.-F.

J. Le Digabel, N. Biais, J. Fresnais, J.-F. Berret, P. Hersen, and B. Ladoux, “Magnetic micropillars as a tool to govern substrate deformations,” Lab on a Chip 11, 2630–2636 (2011).
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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. 100, 1484–1489 (2003).
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Biais, N.

J. Le Digabel, N. Biais, J. Fresnais, J.-F. Berret, P. Hersen, and B. Ladoux, “Magnetic micropillars as a tool to govern substrate deformations,” Lab on a Chip 11, 2630–2636 (2011).
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S. W. Moore, N. Biais, and M. P. Sheetz, “Traction on immobilized netrin-1 is sufficient to reorient axons,” Science 325, 166 (2009).
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N. Biais, D. Higashi, M. So, and B. Ladoux, “Techniques to measure pilus retraction forces,” in Neisseria meningitidis, (Springer, 2012), pp. 197–216.
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Bilenca, A.

I. Remer and A. Bilenca, “High-speed stimulated brillouin scattering spectroscopy at 780 nm,” APL Photonics 1, 061301 (2016).
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Bonnet, I.

F. Bosveld, I. Bonnet, B. Guirao, S. Tlili, Z. Wang, A. Petitalot, R. Marchand, P.-L. Bardet, P. Marcq, F. Graner, and et al., “Mechanical control of morphogenesis by fat/dachsous/four-jointed planar cell polarity pathway,” Science 336, 724–727 (2012).
[Crossref] [PubMed]

Bosveld, F.

F. Bosveld, I. Bonnet, B. Guirao, S. Tlili, Z. Wang, A. Petitalot, R. Marchand, P.-L. Bardet, P. Marcq, F. Graner, and et al., “Mechanical control of morphogenesis by fat/dachsous/four-jointed planar cell polarity pathway,” Science 336, 724–727 (2012).
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Braakman, S.

G. Antonacci and S. Braakman, “Biomechanics of subcellular structures by non-invasive brillouin microscopy,” Sci. reports 6, 37217 (2016).
[Crossref]

Browaeys, J.

M. Ghibaudo, A. Saez, L. Trichet, A. Xayaphoummine, J. Browaeys, P. Silberzan, A. Buguin, and B. Ladoux, “Traction forces and rigidity sensing regulate cell functions,” Soft Matter 4, 1836–1843 (2008).
[Crossref]

Buguin, A.

M. Ghibaudo, A. Saez, L. Trichet, A. Xayaphoummine, J. Browaeys, P. Silberzan, A. Buguin, and B. Ladoux, “Traction forces and rigidity sensing regulate cell functions,” Soft Matter 4, 1836–1843 (2008).
[Crossref]

A. Saez, M. Ghibaudo, A. Buguin, P. Silberzan, and B. Ladoux, “Rigidity-driven growth and migration of epithelial cells on microstructured anisotropic substrates,” Proc. Natl. Acad. Sci. 104, 8281–8286 (2007).
[Crossref] [PubMed]

O. Du Roure, A. Saez, A. Buguin, R. H. Austin, P. Chavrier, P. Siberzan, and B. Ladoux, “Force mapping in epithelial cell migration,” Proc. Natl. Acad. Sci. 102, 2390–2395 (2005).
[Crossref] [PubMed]

Callan-Jones, A.

M. Gupta, B. R. Sarangi, J. Deschamps, Y. Nematbakhsh, A. Callan-Jones, F. Margadant, R.-M. Mège, C. T. Lim, R. Voituriez, and B. Ladoux, “Adaptive rheology and ordering of cell cytoskeleton govern matrix rigidity sensing,” Nat. communications 6, 7525 (2015).
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Caponi, S.

F. Scarponi, S. Mattana, S. Corezzi, S. Caponi, L. Comez, P. Sassi, A. Morresi, M. Paolantoni, L. Urbanelli, C. Emiliani, and et al., “High-performance versatile setup for simultaneous brillouin-raman microspectroscopy,” Phys. Rev. X 7, 031015 (2017).

S. Mattana, S. Caponi, F. Tamagnini, D. Fioretto, and F. Palombo, “Viscoelasticity of amyloid plaques in transgenic mouse brain studied by brillouin microspectroscopy and correlative raman analysis,” J. innovative optical health sciences 10, 1742001 (2017).
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Chavrier, P.

O. Du Roure, A. Saez, A. Buguin, R. H. Austin, P. Chavrier, P. Siberzan, and B. Ladoux, “Force mapping in epithelial cell migration,” Proc. Natl. Acad. Sci. 102, 2390–2395 (2005).
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Chen, C. S.

S.-Y. Tee, J. Fu, C. S. Chen, and P. A. Janmey, “Cell shape and substrate rigidity both regulate cell stiffness,” Biophys. journal 100, L25–L27 (2011).
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N. J. Sniadecki, A. Anguelouch, M. T. Yang, C. M. Lamb, Z. Liu, S. B. Kirschner, Y. Liu, D. H. Reich, and C. S. Chen, “Magnetic microposts as an approach to apply forces to living cells,” Proc. Natl. Acad. Sci. 104, 14553–14558 (2007).
[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. 100, 1484–1489 (2003).
[Crossref] [PubMed]

Cojoc, G.

R. Schlüßler, S. Möllmert, S. Abuhattum, G. Cojoc, P. Müller, K. Kim, C. Möckel, C. Zimmermann, J. Czarske, and J. Guck, “Mechanical mapping of spinal cord growth and repair in living zebrafish larvae by brillouin imaging,” Biophys. journal 115, 911–923 (2018).
[Crossref]

Colantoni, A.

R. De Santis, V. Alfano, V. de Turris, A. Colantoni, L. Santini, M. G. Garone, G. Antonacci, G. Peruzzi, E. Sudria-Lopez, E. Wyler, and et al., “Mutant fus and elavl4 (hud) aberrant crosstalk in amyotrophic lateral sclerosis,” Available at SSRN 3261820 (2018).

Collisson, E. A.

H. Laklai, Y. A. Miroshnikova, M. W. Pickup, E. A. Collisson, G. E. Kim, A. S. Barrett, R. C. Hill, J. N. Lakins, D. D. Schlaepfer, J. K. Mouw, and et al., “Genotype tunes pancreatic ductal adenocarcinoma tissue tension to induce matricellular fibrosis and tumor progression,” Nat. medicine 22, 497 (2016).
[Crossref]

Comez, L.

F. Scarponi, S. Mattana, S. Corezzi, S. Caponi, L. Comez, P. Sassi, A. Morresi, M. Paolantoni, L. Urbanelli, C. Emiliani, and et al., “High-performance versatile setup for simultaneous brillouin-raman microspectroscopy,” Phys. Rev. X 7, 031015 (2017).

Conte, V.

R. Sunyer, V. Conte, J. Escribano, A. Elosegui-Artola, A. Labernadie, L. Valon, D. Navajas, J. M. García-Aznar, J. J. Muñoz, P. Roca-Cusachs, and et al., “Collective cell durotaxis emerges from long-range intercellular force transmission,” Science 353, 1157–1161 (2016).
[Crossref] [PubMed]

Corezzi, S.

F. Scarponi, S. Mattana, S. Corezzi, S. Caponi, L. Comez, P. Sassi, A. Morresi, M. Paolantoni, L. Urbanelli, C. Emiliani, and et al., “High-performance versatile setup for simultaneous brillouin-raman microspectroscopy,” Phys. Rev. X 7, 031015 (2017).

Czarske, J.

R. Schlüßler, S. Möllmert, S. Abuhattum, G. Cojoc, P. Müller, K. Kim, C. Möckel, C. Zimmermann, J. Czarske, and J. Guck, “Mechanical mapping of spinal cord growth and repair in living zebrafish larvae by brillouin imaging,” Biophys. journal 115, 911–923 (2018).
[Crossref]

Danen, E. H.

W. Pomp, K. Schakenraad, H. E. Balcğlu, H. van Hoorn, E. H. Danen, R. M. Merks, T. Schmidt, and L. Giomi, “Cytoskeletal anisotropy controls geometry and forces of adherent cells,” Phys. review letters 121, 178101 (2018).
[Crossref]

De Basabe Delgado, J.

D. York, N. M. Evensen, M. L. Martınez, and J. De Basabe Delgado, “Unified equations for the slope, intercept, and standard errors of the best straight line,” Am. J. Phys. 72, 367–375 (2004).
[Crossref]

De Panfilis, S.

G. Antonacci, S. De Panfilis, G. Di Domenico, E. DelRe, and G. Ruocco, “Breaking the contrast limit in single-pass fabry-pérot spectrometers,” Phys. Rev. Appl. 6, 054020 (2016).
[Crossref]

De Santis, R.

R. De Santis, V. Alfano, V. de Turris, A. Colantoni, L. Santini, M. G. Garone, G. Antonacci, G. Peruzzi, E. Sudria-Lopez, E. Wyler, and et al., “Mutant fus and elavl4 (hud) aberrant crosstalk in amyotrophic lateral sclerosis,” Available at SSRN 3261820 (2018).

De Silva, R.

G. Antonacci, R. M. Pedrigi, A. Kondiboyina, V. V. Mehta, R. De Silva, C. Paterson, R. Krams, and P. Török, “Quantification of plaque stiffness by brillouin microscopy in experimental thin cap fibroatheroma,” J. Royal Soc. Interface 12, 20150843 (2015).
[Crossref]

de Turris, V.

G. Antonacci, V. de Turris, A. Rosa, and G. Ruocco, “Background-deflection brillouin microscopy reveals altered biomechanics of intracellular stress granules by als protein fus,” Commun. biology 1, 139 (2018).
[Crossref]

R. De Santis, V. Alfano, V. de Turris, A. Colantoni, L. Santini, M. G. Garone, G. Antonacci, G. Peruzzi, E. Sudria-Lopez, E. Wyler, and et al., “Mutant fus and elavl4 (hud) aberrant crosstalk in amyotrophic lateral sclerosis,” Available at SSRN 3261820 (2018).

Dehoux, T.

M. Abi Ghanem, T. Dehoux, L. Liu, G. Le Saux, L. Plawinski, M.-C. Durrieu, and B. Audoin, “Opto-acoustic microscopy reveals adhesion mechanics of single cells,” Rev. Sci. Instruments 89, 014901 (2018).
[Crossref]

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

M. Abi Ghanem, T. Dehoux, O. F. Zouani, A. Gadalla, M.-C. Durrieu, and B. Audoin, “Remote opto-acoustic probing of single-cell adhesion on metallic surfaces,” J. biophotonics 7, 453–459 (2014).
[Crossref]

DelRe, E.

G. Antonacci, S. De Panfilis, G. Di Domenico, E. DelRe, and G. Ruocco, “Breaking the contrast limit in single-pass fabry-pérot spectrometers,” Phys. Rev. Appl. 6, 054020 (2016).
[Crossref]

Deschamps, J.

M. Gupta, B. R. Sarangi, J. Deschamps, Y. Nematbakhsh, A. Callan-Jones, F. Margadant, R.-M. Mège, C. T. Lim, R. Voituriez, and B. Ladoux, “Adaptive rheology and ordering of cell cytoskeleton govern matrix rigidity sensing,” Nat. communications 6, 7525 (2015).
[Crossref]

Di Domenico, G.

G. Antonacci, S. De Panfilis, G. Di Domenico, E. DelRe, and G. Ruocco, “Breaking the contrast limit in single-pass fabry-pérot spectrometers,” Phys. Rev. Appl. 6, 054020 (2016).
[Crossref]

Dilhaire, S.

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

Discher, D. E.

A. J. Engler, S. Sen, H. L. Sweeney, and D. E. Discher, “Matrix elasticity directs stem cell lineage specification,” Cell 126, 677–689 (2006).
[Crossref] [PubMed]

D. E. Discher, P. Janmey, and Y.-l. Wang, “Tissue cells feel and respond to the stiffness of their substrate,” Science 310, 1139–1143 (2005).
[Crossref] [PubMed]

Diz-Muñoz, A.

R. Prevedel, A. Diz-Muñoz, G. Ruocco, and G. Antonacci, “Brillouin microscopy-a revolutionary tool for mechanobiology?” arXiv preprint arXiv:1901.02006 (2019).

Du Roure, O.

O. Du Roure, A. Saez, A. Buguin, R. H. Austin, P. Chavrier, P. Siberzan, and B. Ladoux, “Force mapping in epithelial cell migration,” Proc. Natl. Acad. Sci. 102, 2390–2395 (2005).
[Crossref] [PubMed]

Dunlop, I. E.

P.-J. Wu, I. V. Kabakova, J. W. Ruberti, J. M. Sherwood, I. E. Dunlop, C. Paterson, P. Török, and D. R. Overby, “Water content, not stiffness, dominates brillouin spectroscopy measurements in hydrated materials,” Nat. methods 15, 561 (2018).
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Dupps, W. J.

M. J. Girard, W. J. Dupps, M. Baskaran, G. Scarcelli, S. H. Yun, H. A. Quigley, I. A. Sigal, and N. G. Strouthidis, “Translating ocular biomechanics into clinical practice: current state and future prospects,” Curr. eye research 40, 1–18 (2015).
[Crossref]

Durrieu, M.-C.

M. Abi Ghanem, T. Dehoux, L. Liu, G. Le Saux, L. Plawinski, M.-C. Durrieu, and B. Audoin, “Opto-acoustic microscopy reveals adhesion mechanics of single cells,” Rev. Sci. Instruments 89, 014901 (2018).
[Crossref]

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

M. Abi Ghanem, T. Dehoux, O. F. Zouani, A. Gadalla, M.-C. Durrieu, and B. Audoin, “Remote opto-acoustic probing of single-cell adhesion on metallic surfaces,” J. biophotonics 7, 453–459 (2014).
[Crossref]

Edrei, E.

Elosegui-Artola, A.

R. Sunyer, V. Conte, J. Escribano, A. Elosegui-Artola, A. Labernadie, L. Valon, D. Navajas, J. M. García-Aznar, J. J. Muñoz, P. Roca-Cusachs, and et al., “Collective cell durotaxis emerges from long-range intercellular force transmission,” Science 353, 1157–1161 (2016).
[Crossref] [PubMed]

Elsayad, K.

K. Elsayad, S. Werner, M. Gallemí, J. Kong, E. R. S. Guajardo, L. Zhang, Y. Jaillais, T. Greb, and Y. Belkhadir, “Mapping the subcellular mechanical properties of live cells in tissues with fluorescence emission–brillouin imaging,” Sci. Signal. 9, rs5 (2016).
[Crossref]

Emiliani, C.

F. Scarponi, S. Mattana, S. Corezzi, S. Caponi, L. Comez, P. Sassi, A. Morresi, M. Paolantoni, L. Urbanelli, C. Emiliani, and et al., “High-performance versatile setup for simultaneous brillouin-raman microspectroscopy,” Phys. Rev. X 7, 031015 (2017).

Engler, A. J.

A. J. Engler, S. Sen, H. L. Sweeney, and D. E. Discher, “Matrix elasticity directs stem cell lineage specification,” Cell 126, 677–689 (2006).
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Z. Steelman, Z. Meng, A. J. Traverso, and V. V. Yakovlev, “Brillouin spectroscopy as a new method of screening for increased csf total protein during bacterial meningitis,” J. Biophotonics 8, 408–414 (2015).
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R. Schlüßler, S. Möllmert, S. Abuhattum, G. Cojoc, P. Müller, K. Kim, C. Möckel, C. Zimmermann, J. Czarske, and J. Guck, “Mechanical mapping of spinal cord growth and repair in living zebrafish larvae by brillouin imaging,” Biophys. journal 115, 911–923 (2018).
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T. Dehoux, M. A. Ghanem, O. Zouani, J.-M. Rampnoux, Y. Guillet, S. Dilhaire, M.-C. Durrieu, and B. Audoin, “All-optical broadband ultrasonography of single cells,” Sci. reports 5, 8650 (2015).
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M. Abi Ghanem, T. Dehoux, O. F. Zouani, A. Gadalla, M.-C. Durrieu, and B. Audoin, “Remote opto-acoustic probing of single-cell adhesion on metallic surfaces,” J. biophotonics 7, 453–459 (2014).
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Am. J. Phys. (1)

D. York, N. M. Evensen, M. L. Martınez, and J. De Basabe Delgado, “Unified equations for the slope, intercept, and standard errors of the best straight line,” Am. J. Phys. 72, 367–375 (2004).
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Analyst (1)

F. Palombo, M. Madami, N. Stone, and D. Fioretto, “Mechanical mapping with chemical specificity by confocal brillouin and raman microscopy,” Analyst 139, 729–733 (2014).
[Crossref] [PubMed]

APL Photonics (1)

I. Remer and A. Bilenca, “High-speed stimulated brillouin scattering spectroscopy at 780 nm,” APL Photonics 1, 061301 (2016).
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Appl. Phys. Lett. (3)

G. Antonacci, G. Lepert, C. Paterson, and P. Török, “Elastic suppression in brillouin imaging by destructive interference,” Appl. Phys. Lett. 107, 061102 (2015).
[Crossref]

G. Antonacci, M. R. Foreman, C. Paterson, and P. Török, “Spectral broadening in brillouin imaging,” Appl. Phys. Lett. 103, 221105 (2013).
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K. Koski and J. Yarger, “Brillouin imaging,” Appl. Phys. Lett. 87, 061903 (2005).
[Crossref]

Biochimica et Biophys. Acta (BBA)-Molecular Cell Res. (1)

U. S. Schwarz and J. R. Soiné, “Traction force microscopy on soft elastic substrates: A guide to recent computational advances,” Biochimica et Biophys. Acta (BBA)-Molecular Cell Res. 1853, 3095–3104 (2015).
[Crossref]

Biophys. journal (2)

S.-Y. Tee, J. Fu, C. S. Chen, and P. A. Janmey, “Cell shape and substrate rigidity both regulate cell stiffness,” Biophys. journal 100, L25–L27 (2011).
[Crossref]

R. Schlüßler, S. Möllmert, S. Abuhattum, G. Cojoc, P. Müller, K. Kim, C. Möckel, C. Zimmermann, J. Czarske, and J. Guck, “Mechanical mapping of spinal cord growth and repair in living zebrafish larvae by brillouin imaging,” Biophys. journal 115, 911–923 (2018).
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Cancer discovery (1)

J. J. Northey, L. Przybyla, and V. M. Weaver, “Tissue force programs cell fate and tumor aggression,” Cancer discovery 7, 1224–1237 (2017).
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Cell (1)

A. J. Engler, S. Sen, H. L. Sweeney, and D. E. Discher, “Matrix elasticity directs stem cell lineage specification,” Cell 126, 677–689 (2006).
[Crossref] [PubMed]

Cell motility cytoskeleton (1)

T. Yeung, P. C. Georges, L. A. Flanagan, B. Marg, M. Ortiz, M. Funaki, N. Zahir, W. Ming, V. Weaver, and P. A. Janmey, “Effects of substrate stiffness on cell morphology, cytoskeletal structure, and adhesion,” Cell motility cytoskeleton 60, 24–34 (2005).
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Commun. biology (1)

G. Antonacci, V. de Turris, A. Rosa, and G. Ruocco, “Background-deflection brillouin microscopy reveals altered biomechanics of intracellular stress granules by als protein fus,” Commun. biology 1, 139 (2018).
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Curr. biology (1)

E. Farge, “Mechanical induction of twist in the drosophila foregut/stomodeal primordium,” Curr. biology 13, 1365–1377 (2003).
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Curr. eye research (1)

M. J. Girard, W. J. Dupps, M. Baskaran, G. Scarcelli, S. H. Yun, H. A. Quigley, I. A. Sigal, and N. G. Strouthidis, “Translating ocular biomechanics into clinical practice: current state and future prospects,” Curr. eye research 40, 1–18 (2015).
[Crossref]

J. Biophotonics (1)

Z. Steelman, Z. Meng, A. J. Traverso, and V. V. Yakovlev, “Brillouin spectroscopy as a new method of screening for increased csf total protein during bacterial meningitis,” J. Biophotonics 8, 408–414 (2015).
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M. Abi Ghanem, T. Dehoux, O. F. Zouani, A. Gadalla, M.-C. Durrieu, and B. Audoin, “Remote opto-acoustic probing of single-cell adhesion on metallic surfaces,” J. biophotonics 7, 453–459 (2014).
[Crossref]

J. Histochem. & Cytochem. (1)

G. Zack, W. Rogers, and S. Latt, “Automatic measurement of sister chromatid exchange frequency,” J. Histochem. & Cytochem. 25, 741–753 (1977).
[Crossref]

J. innovative optical health sciences (1)

S. Mattana, S. Caponi, F. Tamagnini, D. Fioretto, and F. Palombo, “Viscoelasticity of amyloid plaques in transgenic mouse brain studied by brillouin microspectroscopy and correlative raman analysis,” J. innovative optical health sciences 10, 1742001 (2017).
[Crossref]

J. Royal Soc. Interface (1)

G. Antonacci, R. M. Pedrigi, A. Kondiboyina, V. V. Mehta, R. De Silva, C. Paterson, R. Krams, and P. Török, “Quantification of plaque stiffness by brillouin microscopy in experimental thin cap fibroatheroma,” J. Royal Soc. Interface 12, 20150843 (2015).
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Lab on a Chip (1)

J. Le Digabel, N. Biais, J. Fresnais, J.-F. Berret, P. Hersen, and B. Ladoux, “Magnetic micropillars as a tool to govern substrate deformations,” Lab on a Chip 11, 2630–2636 (2011).
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Nano letters (1)

H. van Hoorn, R. Harkes, E. M. Spiesz, C. Storm, D. van Noort, B. Ladoux, and T. Schmidt, “The nanoscale architecture of force-bearing focal adhesions,” Nano letters 14, 4257–4262 (2014).
[Crossref] [PubMed]

Nat. cell biology (2)

H. Wolfenson, G. Meacci, S. Liu, M. R. Stachowiak, T. Iskratsch, S. Ghassemi, P. Roca-Cusachs, B. O’Shaughnessy, J. Hone, and M. P. Sheetz, “Tropomyosin controls sarcomere-like contractions for rigidity sensing and suppressing growth on soft matrices,” Nat. cell biology 18, 33 (2016).
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Y. A. Miroshnikova, J. K. Mouw, J. M. Barnes, M. W. Pickup, J. N. Lakins, Y. Kim, K. Lobo, A. I. Persson, G. F. Reis, T. R. McKnight, and et al., “Tissue mechanics promote idh1-dependent hif1α–tenascin c feedback to regulate glioblastoma aggression,” Nat. cell biology 18, 1336 (2016).
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Nat. communications (1)

M. Gupta, B. R. Sarangi, J. Deschamps, Y. Nematbakhsh, A. Callan-Jones, F. Margadant, R.-M. Mège, C. T. Lim, R. Voituriez, and B. Ladoux, “Adaptive rheology and ordering of cell cytoskeleton govern matrix rigidity sensing,” Nat. communications 6, 7525 (2015).
[Crossref]

Nat. Mater. (1)

K. J. Koski, P. Akhenblit, K. McKiernan, and J. L. Yarger, “Non-invasive determination of the complete elastic moduli of spider silks,” Nat. Mater. 12, 262 (2013).
[Crossref] [PubMed]

Nat. medicine (1)

H. Laklai, Y. A. Miroshnikova, M. W. Pickup, E. A. Collisson, G. E. Kim, A. S. Barrett, R. C. Hill, J. N. Lakins, D. D. Schlaepfer, J. K. Mouw, and et al., “Genotype tunes pancreatic ductal adenocarcinoma tissue tension to induce matricellular fibrosis and tumor progression,” Nat. medicine 22, 497 (2016).
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Figures (6)

Fig. 1
Fig. 1 Correlative micropillar traction force and Brillouin microscopy. (A) Schematic of the optical fluorescence (’SETUP 1’) and Brillouin (’SETUP 2’) independent setups. Cells adhere to a hexagonal patterned elastic micropillar array. The fluorescence setup (’SETUP 1’) was used to collect the fluorescence signal emitted by the micropillars and therefore to measure the cellular adhesion forces from the pillar displacements [21]. The same sample was then moved to the Brillouin imaging setup (’SETUP 2’) where the scattered signal was collected in a backscattering geometry and delivered to the background-deflection (BD) spectrometer. This is a single-stage VIPA spectrometer integrating a diffraction mask (DM) to deflect the elastic background signal from the dispersion axis [48]. (B) Sensitivity histogram of the Brillouin setup. N=1000 spectra were acquired on a PDMS sample. System sensitivity was evaluated to be σ = 0.025 GHz.
Fig. 2
Fig. 2 Correlative high-resolution contractile forces and biomechanical properties of 3T3 fibroblasts. (A) Representative fluorescence confocal image of a 3T3 fibroblast cell (green and blue for actin and nucleus staining, respectively) adhering on fibronectin-coated (red) elastic micropillar arrays. The white arrows indicate the contractile forces quantified by multiplying the pillar displacements by the spring constant. The total cellular force was measured to be 60.8 ±0.9 nN. (B) Representative fluorescence confocal image of a 3T3 fibroblast cell (green and blue for actin and nucleus staining, respectively) adhering on fibronectin-coated glass. (C–D) High-resolution confocal Brillouin images of the representative cells in (A–B). The reported average cell Brillouin shifts νB of 7.51±0.05 GHz and 7.57±0.08 GHz are significantly different (p-value<0.05 from a two-sample t-test, N=3146 and 4715 Brillouin shift values respectively). The cell Brillouin shifts were determined by using the triangle method [57]. Scale bar: 10 μm.
Fig. 3
Fig. 3 Intracellular Brillouin frequency shifts increase as a function of substrate stiffness. (A) Normalized probability density function (PDF) of Brillouin shifts νB for cells on soft PDMS micropillars (solid blue line) and glass (solid red line). The Brillouin shifts components for PDMS, PBS buffer and cells are indicated by the arrows. A Gaussian fit of the ’Buffer’ peak (black dashed line) is performed to set a threshold value ν B T = 7.466 GHz (see Methods in 2.4). (B) PDF plot of cellular Brillouin shift ν B > ν B T. A three-Gaussian fit (solid lines) is performed for Brillouin shift profiles of cells on both soft PDMS micropillars (solid blue line) and glass (solid red line). Results are reported in Table 1. The choice of such model is clarified in Fig. 6 in the Appendix.
Fig. 4
Fig. 4 Label- and contact-free Brillouin imaging of actin stress fibers. (A) Confocal image of 3T3 fibroblast adhering on fibronectin-coated glass. Actin filaments are labeled with AF532-conjugated phalloidin (grayscale). The dashed red line indicates where the Brillouin line scan was performed. Scale bar: 10 μm. (B) Brillouin shifts νB from the line scan across the cell (dashed red line in A) measured with an increased data acquisition time of 500 ms per spectrum. The dashed grey lines report the Brillouin shift values μ1, μ2, and μ3 from Table 1.
Fig. 5
Fig. 5 Actin Brillouin shifts and force per pillar of cells on soft PDMS micropillars. Data are reported as mean ±SD. A linear fit (solid red line) using the York method [58] gives a slope of 0.003±0.004 GHz/nN and an intercept of 7.54±0.01 GHz (R2=0.14).
Fig. 6
Fig. 6 Comparison of non-linear least squares fits with one, two or three component Gaussian functions for soft PDMS micropillars (A) and Glass (B) conditions. The optimal model (i.e. three-component Gaussian fit) was chosen after the Akaike information criterion (AIC) values that are reported in the plots. The AIC values were determined as AIC =2k +n ln(RSS), where k is the number of parameters (e.g. k =3 for one-component Gaussian), n the sample size, and RSS the residual sum of squares (i.e. i ( y i f ( x i ) ) 2).

Tables (1)

Tables Icon

Table 1 Parameters from a non-linear least squares fit with three independent Gaussian functions of the Brillouin shifts PDF reported in Fig. 3B. A*, μ* and σ* are the amplitude, mean and standard deviation (±95% CI) of the Gaussian functions. The p-values were obtained from a t-test for which the significance level was set to p-value<0.05 (N=5 cells and 6 cells for soft PDMS micropillars and glass, respectively).

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