Abstract

Cell adhesion is a crucial biological and biomedical parameter defining cell differentiation, cell migration, cell survival, and state of disease. Because of its importance in cellular function, several tools have been developed in order to monitor cell adhesion in response to various biochemical and mechanical cues. However, there remains a need to monitor cell adhesion and cell-substrate separation with a method that allows real-time measurements on accessible equipment. In this article, we present a method to monitor cell-substrate separation at the single cell level using a plasmonic extraordinary optical transmission substrate, which has a high sensitivity to refractive index changes at the metal-dielectric interface. We show how refractive index changes can be detected using intensity peaks in color channel histograms from RGB images taken of the device surface with a brightfield microscope. This allows mapping of the nonuniform refractive index pattern of a single cell cultured on the plasmonic substrate and therefore high-throughput detection of cell-substrate adhesion with observations in real time.

© 2017 Optical Society of America

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References

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    [Crossref] [PubMed]
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    [PubMed]
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    [PubMed]
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  10. 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(9), 1836–1843 (2008).
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    [Crossref] [PubMed]
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    [Crossref] [PubMed]
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    [Crossref]
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    [Crossref]
  31. C. Genet and T. W. Ebbesen, “Light in tiny holes,” Nature 445(7123), 39–46 (2007).
    [Crossref] [PubMed]
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    [Crossref]
  33. L. S. Jung, C. T. Campbell, T. M. Chinowsky, M. N. Mar, and S. S. Yee, “Quantitative interpretation of the response of surface plasmon resonance sensors to adsorbed films,” Langmuir 14(19), 5636–5648 (1998).
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    [Crossref] [PubMed]

2016 (1)

L. Plucinski, M. Ranjan Gartia, W. R. Arnold, A. Ameen, T. W. Chang, A. Hsiao, G. Logan Liu, and A. Das, “Substrate binding to cytochrome P450-2J2 in Nanodiscs detected by nanoplasmonic Lycurgus cup arrays,” Biosens. Bioelectron. 75, 337–346 (2016).
[Crossref] [PubMed]

2015 (2)

T. W. Chang, X. H. Wang, A. Hsiao, Z. D. Xu, G. H. Lin, M. R. Gartia, X. R. Liu, and G. L. Liu, “Bifunctional Nano Lycurgus Cup Array Plasmonic Sensor for Colorimetric Sensing and Surface-Enhanced Raman Spectroscopy,” Adv. Opt. Mater. 3(10), 1397–1404 (2015).
[Crossref]

A. A. Khalili and M. R. Ahmad, “A Review of Cell Adhesion Studies for Biomedical and Biological Applications,” Int. J. Mol. Sci. 16(8), 18149–18184 (2015).
[Crossref] [PubMed]

2013 (1)

M. R. Gartia, A. Hsiao, A. Pokhriyal, S. Seo, G. Kulsharova, B. T. Cunningham, T. C. Bond, and G. L. Liu, “Colorimetric plasmon resonance imaging using nano lycurgus cup arrays,” Adv. Opt. Mater. 1(4), 281 (2013).
[Crossref]

2012 (2)

X. M. Zhang, Z. B. Li, S. S. Ye, S. Wu, J. H. Zhang, L. Y. Cui, A. R. Li, T. Q. Wang, S. Z. Li, and B. Yang, “Elevated Ag nanohole arrays for high performance plasmonic sensors based on extraordinary optical transmission,” J. Mater. Chem. 22(18), 8903–8910 (2012).
[Crossref]

K. Watanabe, K. Matsuura, F. Kawata, K. Nagata, J. Ning, and H. Kano, “Scanning and non-scanning surface plasmon microscopy to observe cell adhesion sites,” Biomed. Opt. Express 3(2), 354–359 (2012).
[Crossref] [PubMed]

2011 (1)

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]

2008 (3)

B. Sabass, M. L. Gardel, C. M. Waterman, and U. S. Schwarz, “High resolution traction force microscopy based on experimental and computational advances,” Biophys. J. 94(1), 207–220 (2008).
[Crossref] [PubMed]

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(9), 1836–1843 (2008).
[Crossref]

R. Gordon, D. Sinton, K. L. Kavanagh, and A. G. Brolo, “A new generation of sensors based on extraordinary optical transmission,” Acc. Chem. Res. 41(8), 1049–1057 (2008).
[Crossref] [PubMed]

2007 (1)

C. Genet and T. W. Ebbesen, “Light in tiny holes,” Nature 445(7123), 39–46 (2007).
[Crossref] [PubMed]

2006 (1)

P. H. Puech, K. Poole, D. Knebel, and D. J. Muller, “A new technical approach to quantify cell-cell adhesion forces by AFM,” Ultramicroscopy 106(8-9), 637–644 (2006).
[Crossref] [PubMed]

2005 (3)

S. Sen, S. Subramanian, and D. E. Discher, “Indentation and adhesive probing of a cell membrane with AFM: theoretical model and experiments,” Biophys. J. 89(5), 3203–3213 (2005).
[Crossref] [PubMed]

D. E. Discher, P. Janmey, and Y. L. Wang, “Tissue cells feel and respond to the stiffness of their substrate,” Science 310(5751), 1139–1143 (2005).
[Crossref] [PubMed]

G. Liu, J. Doll, and L. Lee, “High-speed multispectral imaging of nanoplasmonic array,” Opt. Express 13(21), 8520–8525 (2005).
[Crossref] [PubMed]

2004 (1)

A. G. Brolo, R. Gordon, B. Leathem, and K. L. Kavanagh, “Surface plasmon sensor based on the enhanced light transmission through arrays of nanoholes in gold films,” Langmuir 20(12), 4813–4815 (2004).
[Crossref] [PubMed]

2001 (1)

S. Munevar, Y. Wang, and M. Dembo, “Traction force microscopy of migrating normal and H-ras transformed 3T3 fibroblasts,” Biophys. J. 80(4), 1744–1757 (2001).
[Crossref] [PubMed]

2000 (2)

C. Zhu, “Kinetics and mechanics of cell adhesion,” J. Biomech. 33(1), 23–33 (2000).
[Crossref] [PubMed]

G. Maheshwari, G. Brown, D. A. Lauffenburger, A. Wells, and L. G. Griffith, “Cell adhesion and motility depend on nanoscale RGD clustering,” J. Cell Sci. 113(Pt 10), 1677–1686 (2000).
[PubMed]

1999 (1)

K. Giebel, C. Bechinger, S. Herminghaus, M. Riedel, P. Leiderer, U. Weiland, and M. Bastmeyer, “Imaging of cell/substrate contacts of living cells with surface plasmon resonance microscopy,” Biophys. J. 76(1), 509–516 (1999).
[Crossref] [PubMed]

1998 (2)

R. J. Pelham and Y. L. Wang, “Cell locomotion and focal adhesions are regulated by substrate flexibility (vol 94, pg 13661, 1997),” Proc. Natl. Acad. Sci. U.S.A. 95, 12070 (1998).

L. S. Jung, C. T. Campbell, T. M. Chinowsky, M. N. Mar, and S. S. Yee, “Quantitative interpretation of the response of surface plasmon resonance sensors to adsorbed films,” Langmuir 14(19), 5636–5648 (1998).
[Crossref]

1996 (1)

B. M. Gumbiner, “Cell adhesion: the molecular basis of tissue architecture and morphogenesis,” Cell 84(3), 345–357 (1996).
[Crossref] [PubMed]

1995 (1)

U. Dammer, O. Popescu, P. Wagner, D. Anselmetti, H. J. Güntherodt, and G. N. Misevic, “Binding strength between cell adhesion proteoglycans measured by atomic force microscopy,” Science 267(5201), 1173–1175 (1995).
[Crossref] [PubMed]

1993 (2)

S. M. Albelda, “Role of integrins and other cell adhesion molecules in tumor progression and metastasis,” Lab. Invest. 68(1), 4–17 (1993).
[PubMed]

B. R. Zetter, “Adhesion Molecules in Tumor Metastasis,” Semin. Cancer Biol. 4(4), 219–229 (1993).
[PubMed]

1992 (1)

R. O. Hynes, “Integrins: Versatility, Modulation, and Signaling in Cell Adhesion,” Cell 69(1), 11–25 (1992).
[Crossref] [PubMed]

1987 (1)

E. Ruoslahti and M. D. Pierschbacher, “New perspectives in cell adhesion: RGD and integrins,” Science 238(4826), 491–497 (1987).
[Crossref] [PubMed]

1985 (1)

H. Verschueren, “Interference reflection microscopy in cell biology: methodology and applications,” J. Cell Sci. 75, 279–301 (1985).
[PubMed]

1976 (1)

C. S. Izzard and L. R. Lochner, “Cell-to-Substrate Contacts in Living Fibroblasts: an Interference Reflexion Study with an Evaluation of the Technique,” J. Cell Sci. 21(1), 129–159 (1976).
[PubMed]

1974 (1)

P. B. Johnson and R. W. Christy, “Optical-Constants of Transition-Metals - Ti, V, Cr, Mn, Fe, Co, Ni, and Pd,” Phys. Rev. B 9(12), 5056–5070 (1974).
[Crossref]

1972 (1)

P. B. Johnson and R. W. Christy, “Optical Constants of Noble Metals,” Phys. Rev. B 6(12), 4370–4379 (1972).
[Crossref]

1964 (1)

A. S. Curtis, “The mechanism of adhesion of cells to glass. a study by interference reflection microscopy,” J. Cell Biol. 20(2), 199–215 (1964).
[Crossref] [PubMed]

Ahmad, M. R.

A. A. Khalili and M. R. Ahmad, “A Review of Cell Adhesion Studies for Biomedical and Biological Applications,” Int. J. Mol. Sci. 16(8), 18149–18184 (2015).
[Crossref] [PubMed]

Albelda, S. M.

S. M. Albelda, “Role of integrins and other cell adhesion molecules in tumor progression and metastasis,” Lab. Invest. 68(1), 4–17 (1993).
[PubMed]

Ameen, A.

L. Plucinski, M. Ranjan Gartia, W. R. Arnold, A. Ameen, T. W. Chang, A. Hsiao, G. Logan Liu, and A. Das, “Substrate binding to cytochrome P450-2J2 in Nanodiscs detected by nanoplasmonic Lycurgus cup arrays,” Biosens. Bioelectron. 75, 337–346 (2016).
[Crossref] [PubMed]

Anselmetti, D.

U. Dammer, O. Popescu, P. Wagner, D. Anselmetti, H. J. Güntherodt, and G. N. Misevic, “Binding strength between cell adhesion proteoglycans measured by atomic force microscopy,” Science 267(5201), 1173–1175 (1995).
[Crossref] [PubMed]

Arnold, W. R.

L. Plucinski, M. Ranjan Gartia, W. R. Arnold, A. Ameen, T. W. Chang, A. Hsiao, G. Logan Liu, and A. Das, “Substrate binding to cytochrome P450-2J2 in Nanodiscs detected by nanoplasmonic Lycurgus cup arrays,” Biosens. Bioelectron. 75, 337–346 (2016).
[Crossref] [PubMed]

Bastmeyer, M.

K. Giebel, C. Bechinger, S. Herminghaus, M. Riedel, P. Leiderer, U. Weiland, and M. Bastmeyer, “Imaging of cell/substrate contacts of living cells with surface plasmon resonance microscopy,” Biophys. J. 76(1), 509–516 (1999).
[Crossref] [PubMed]

Bechinger, C.

K. Giebel, C. Bechinger, S. Herminghaus, M. Riedel, P. Leiderer, U. Weiland, and M. Bastmeyer, “Imaging of cell/substrate contacts of living cells with surface plasmon resonance microscopy,” Biophys. J. 76(1), 509–516 (1999).
[Crossref] [PubMed]

Bond, T. C.

M. R. Gartia, A. Hsiao, A. Pokhriyal, S. Seo, G. Kulsharova, B. T. Cunningham, T. C. Bond, and G. L. Liu, “Colorimetric plasmon resonance imaging using nano lycurgus cup arrays,” Adv. Opt. Mater. 1(4), 281 (2013).
[Crossref]

Brolo, A. G.

R. Gordon, D. Sinton, K. L. Kavanagh, and A. G. Brolo, “A new generation of sensors based on extraordinary optical transmission,” Acc. Chem. Res. 41(8), 1049–1057 (2008).
[Crossref] [PubMed]

A. G. Brolo, R. Gordon, B. Leathem, and K. L. Kavanagh, “Surface plasmon sensor based on the enhanced light transmission through arrays of nanoholes in gold films,” Langmuir 20(12), 4813–4815 (2004).
[Crossref] [PubMed]

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(9), 1836–1843 (2008).
[Crossref]

Brown, G.

G. Maheshwari, G. Brown, D. A. Lauffenburger, A. Wells, and L. G. Griffith, “Cell adhesion and motility depend on nanoscale RGD clustering,” J. Cell Sci. 113(Pt 10), 1677–1686 (2000).
[PubMed]

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(9), 1836–1843 (2008).
[Crossref]

Campbell, C. T.

L. S. Jung, C. T. Campbell, T. M. Chinowsky, M. N. Mar, and S. S. Yee, “Quantitative interpretation of the response of surface plasmon resonance sensors to adsorbed films,” Langmuir 14(19), 5636–5648 (1998).
[Crossref]

Chang, T. W.

L. Plucinski, M. Ranjan Gartia, W. R. Arnold, A. Ameen, T. W. Chang, A. Hsiao, G. Logan Liu, and A. Das, “Substrate binding to cytochrome P450-2J2 in Nanodiscs detected by nanoplasmonic Lycurgus cup arrays,” Biosens. Bioelectron. 75, 337–346 (2016).
[Crossref] [PubMed]

T. W. Chang, X. H. Wang, A. Hsiao, Z. D. Xu, G. H. Lin, M. R. Gartia, X. R. Liu, and G. L. Liu, “Bifunctional Nano Lycurgus Cup Array Plasmonic Sensor for Colorimetric Sensing and Surface-Enhanced Raman Spectroscopy,” Adv. Opt. Mater. 3(10), 1397–1404 (2015).
[Crossref]

Chinowsky, T. M.

L. S. Jung, C. T. Campbell, T. M. Chinowsky, M. N. Mar, and S. S. Yee, “Quantitative interpretation of the response of surface plasmon resonance sensors to adsorbed films,” Langmuir 14(19), 5636–5648 (1998).
[Crossref]

Christy, R. W.

P. B. Johnson and R. W. Christy, “Optical-Constants of Transition-Metals - Ti, V, Cr, Mn, Fe, Co, Ni, and Pd,” Phys. Rev. B 9(12), 5056–5070 (1974).
[Crossref]

P. B. Johnson and R. W. Christy, “Optical Constants of Noble Metals,” Phys. Rev. B 6(12), 4370–4379 (1972).
[Crossref]

Cui, L. Y.

X. M. Zhang, Z. B. Li, S. S. Ye, S. Wu, J. H. Zhang, L. Y. Cui, A. R. Li, T. Q. Wang, S. Z. Li, and B. Yang, “Elevated Ag nanohole arrays for high performance plasmonic sensors based on extraordinary optical transmission,” J. Mater. Chem. 22(18), 8903–8910 (2012).
[Crossref]

Cunningham, B. T.

M. R. Gartia, A. Hsiao, A. Pokhriyal, S. Seo, G. Kulsharova, B. T. Cunningham, T. C. Bond, and G. L. Liu, “Colorimetric plasmon resonance imaging using nano lycurgus cup arrays,” Adv. Opt. Mater. 1(4), 281 (2013).
[Crossref]

Curtis, A. S.

A. S. Curtis, “The mechanism of adhesion of cells to glass. a study by interference reflection microscopy,” J. Cell Biol. 20(2), 199–215 (1964).
[Crossref] [PubMed]

Dammer, U.

U. Dammer, O. Popescu, P. Wagner, D. Anselmetti, H. J. Güntherodt, and G. N. Misevic, “Binding strength between cell adhesion proteoglycans measured by atomic force microscopy,” Science 267(5201), 1173–1175 (1995).
[Crossref] [PubMed]

Das, A.

L. Plucinski, M. Ranjan Gartia, W. R. Arnold, A. Ameen, T. W. Chang, A. Hsiao, G. Logan Liu, and A. Das, “Substrate binding to cytochrome P450-2J2 in Nanodiscs detected by nanoplasmonic Lycurgus cup arrays,” Biosens. Bioelectron. 75, 337–346 (2016).
[Crossref] [PubMed]

Dembo, M.

S. Munevar, Y. Wang, and M. Dembo, “Traction force microscopy of migrating normal and H-ras transformed 3T3 fibroblasts,” Biophys. J. 80(4), 1744–1757 (2001).
[Crossref] [PubMed]

Discher, D. E.

S. Sen, S. Subramanian, and D. E. Discher, “Indentation and adhesive probing of a cell membrane with AFM: theoretical model and experiments,” Biophys. J. 89(5), 3203–3213 (2005).
[Crossref] [PubMed]

D. E. Discher, P. Janmey, and Y. L. Wang, “Tissue cells feel and respond to the stiffness of their substrate,” Science 310(5751), 1139–1143 (2005).
[Crossref] [PubMed]

Doll, J.

Ebbesen, T. W.

C. Genet and T. W. Ebbesen, “Light in tiny holes,” Nature 445(7123), 39–46 (2007).
[Crossref] [PubMed]

Franck, C.

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]

Gardel, M. L.

B. Sabass, M. L. Gardel, C. M. Waterman, and U. S. Schwarz, “High resolution traction force microscopy based on experimental and computational advances,” Biophys. J. 94(1), 207–220 (2008).
[Crossref] [PubMed]

Gartia, M. R.

T. W. Chang, X. H. Wang, A. Hsiao, Z. D. Xu, G. H. Lin, M. R. Gartia, X. R. Liu, and G. L. Liu, “Bifunctional Nano Lycurgus Cup Array Plasmonic Sensor for Colorimetric Sensing and Surface-Enhanced Raman Spectroscopy,” Adv. Opt. Mater. 3(10), 1397–1404 (2015).
[Crossref]

M. R. Gartia, A. Hsiao, A. Pokhriyal, S. Seo, G. Kulsharova, B. T. Cunningham, T. C. Bond, and G. L. Liu, “Colorimetric plasmon resonance imaging using nano lycurgus cup arrays,” Adv. Opt. Mater. 1(4), 281 (2013).
[Crossref]

Genet, C.

C. Genet and T. W. Ebbesen, “Light in tiny holes,” Nature 445(7123), 39–46 (2007).
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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(9), 1836–1843 (2008).
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K. Giebel, C. Bechinger, S. Herminghaus, M. Riedel, P. Leiderer, U. Weiland, and M. Bastmeyer, “Imaging of cell/substrate contacts of living cells with surface plasmon resonance microscopy,” Biophys. J. 76(1), 509–516 (1999).
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R. Gordon, D. Sinton, K. L. Kavanagh, and A. G. Brolo, “A new generation of sensors based on extraordinary optical transmission,” Acc. Chem. Res. 41(8), 1049–1057 (2008).
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A. G. Brolo, R. Gordon, B. Leathem, and K. L. Kavanagh, “Surface plasmon sensor based on the enhanced light transmission through arrays of nanoholes in gold films,” Langmuir 20(12), 4813–4815 (2004).
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Griffith, L. G.

G. Maheshwari, G. Brown, D. A. Lauffenburger, A. Wells, and L. G. Griffith, “Cell adhesion and motility depend on nanoscale RGD clustering,” J. Cell Sci. 113(Pt 10), 1677–1686 (2000).
[PubMed]

Gumbiner, B. M.

B. M. Gumbiner, “Cell adhesion: the molecular basis of tissue architecture and morphogenesis,” Cell 84(3), 345–357 (1996).
[Crossref] [PubMed]

Güntherodt, H. J.

U. Dammer, O. Popescu, P. Wagner, D. Anselmetti, H. J. Güntherodt, and G. N. Misevic, “Binding strength between cell adhesion proteoglycans measured by atomic force microscopy,” Science 267(5201), 1173–1175 (1995).
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Herminghaus, S.

K. Giebel, C. Bechinger, S. Herminghaus, M. Riedel, P. Leiderer, U. Weiland, and M. Bastmeyer, “Imaging of cell/substrate contacts of living cells with surface plasmon resonance microscopy,” Biophys. J. 76(1), 509–516 (1999).
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Hsiao, A.

L. Plucinski, M. Ranjan Gartia, W. R. Arnold, A. Ameen, T. W. Chang, A. Hsiao, G. Logan Liu, and A. Das, “Substrate binding to cytochrome P450-2J2 in Nanodiscs detected by nanoplasmonic Lycurgus cup arrays,” Biosens. Bioelectron. 75, 337–346 (2016).
[Crossref] [PubMed]

T. W. Chang, X. H. Wang, A. Hsiao, Z. D. Xu, G. H. Lin, M. R. Gartia, X. R. Liu, and G. L. Liu, “Bifunctional Nano Lycurgus Cup Array Plasmonic Sensor for Colorimetric Sensing and Surface-Enhanced Raman Spectroscopy,” Adv. Opt. Mater. 3(10), 1397–1404 (2015).
[Crossref]

M. R. Gartia, A. Hsiao, A. Pokhriyal, S. Seo, G. Kulsharova, B. T. Cunningham, T. C. Bond, and G. L. Liu, “Colorimetric plasmon resonance imaging using nano lycurgus cup arrays,” Adv. Opt. Mater. 1(4), 281 (2013).
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R. O. Hynes, “Integrins: Versatility, Modulation, and Signaling in Cell Adhesion,” Cell 69(1), 11–25 (1992).
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Izzard, C. S.

C. S. Izzard and L. R. Lochner, “Cell-to-Substrate Contacts in Living Fibroblasts: an Interference Reflexion Study with an Evaluation of the Technique,” J. Cell Sci. 21(1), 129–159 (1976).
[PubMed]

Janmey, P.

D. E. Discher, P. Janmey, and Y. L. Wang, “Tissue cells feel and respond to the stiffness of their substrate,” Science 310(5751), 1139–1143 (2005).
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Johnson, P. B.

P. B. Johnson and R. W. Christy, “Optical-Constants of Transition-Metals - Ti, V, Cr, Mn, Fe, Co, Ni, and Pd,” Phys. Rev. B 9(12), 5056–5070 (1974).
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P. B. Johnson and R. W. Christy, “Optical Constants of Noble Metals,” Phys. Rev. B 6(12), 4370–4379 (1972).
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L. S. Jung, C. T. Campbell, T. M. Chinowsky, M. N. Mar, and S. S. Yee, “Quantitative interpretation of the response of surface plasmon resonance sensors to adsorbed films,” Langmuir 14(19), 5636–5648 (1998).
[Crossref]

Kano, H.

Kavanagh, K. L.

R. Gordon, D. Sinton, K. L. Kavanagh, and A. G. Brolo, “A new generation of sensors based on extraordinary optical transmission,” Acc. Chem. Res. 41(8), 1049–1057 (2008).
[Crossref] [PubMed]

A. G. Brolo, R. Gordon, B. Leathem, and K. L. Kavanagh, “Surface plasmon sensor based on the enhanced light transmission through arrays of nanoholes in gold films,” Langmuir 20(12), 4813–4815 (2004).
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Kawata, F.

Khalili, A. A.

A. A. Khalili and M. R. Ahmad, “A Review of Cell Adhesion Studies for Biomedical and Biological Applications,” Int. J. Mol. Sci. 16(8), 18149–18184 (2015).
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Knebel, D.

P. H. Puech, K. Poole, D. Knebel, and D. J. Muller, “A new technical approach to quantify cell-cell adhesion forces by AFM,” Ultramicroscopy 106(8-9), 637–644 (2006).
[Crossref] [PubMed]

Kulsharova, G.

M. R. Gartia, A. Hsiao, A. Pokhriyal, S. Seo, G. Kulsharova, B. T. Cunningham, T. C. Bond, and G. L. Liu, “Colorimetric plasmon resonance imaging using nano lycurgus cup arrays,” Adv. Opt. Mater. 1(4), 281 (2013).
[Crossref]

Ladoux, B.

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(9), 1836–1843 (2008).
[Crossref]

Lauffenburger, D. A.

G. Maheshwari, G. Brown, D. A. Lauffenburger, A. Wells, and L. G. Griffith, “Cell adhesion and motility depend on nanoscale RGD clustering,” J. Cell Sci. 113(Pt 10), 1677–1686 (2000).
[PubMed]

Leathem, B.

A. G. Brolo, R. Gordon, B. Leathem, and K. L. Kavanagh, “Surface plasmon sensor based on the enhanced light transmission through arrays of nanoholes in gold films,” Langmuir 20(12), 4813–4815 (2004).
[Crossref] [PubMed]

Lee, L.

Leiderer, P.

K. Giebel, C. Bechinger, S. Herminghaus, M. Riedel, P. Leiderer, U. Weiland, and M. Bastmeyer, “Imaging of cell/substrate contacts of living cells with surface plasmon resonance microscopy,” Biophys. J. 76(1), 509–516 (1999).
[Crossref] [PubMed]

Li, A. R.

X. M. Zhang, Z. B. Li, S. S. Ye, S. Wu, J. H. Zhang, L. Y. Cui, A. R. Li, T. Q. Wang, S. Z. Li, and B. Yang, “Elevated Ag nanohole arrays for high performance plasmonic sensors based on extraordinary optical transmission,” J. Mater. Chem. 22(18), 8903–8910 (2012).
[Crossref]

Li, S. Z.

X. M. Zhang, Z. B. Li, S. S. Ye, S. Wu, J. H. Zhang, L. Y. Cui, A. R. Li, T. Q. Wang, S. Z. Li, and B. Yang, “Elevated Ag nanohole arrays for high performance plasmonic sensors based on extraordinary optical transmission,” J. Mater. Chem. 22(18), 8903–8910 (2012).
[Crossref]

Li, Z. B.

X. M. Zhang, Z. B. Li, S. S. Ye, S. Wu, J. H. Zhang, L. Y. Cui, A. R. Li, T. Q. Wang, S. Z. Li, and B. Yang, “Elevated Ag nanohole arrays for high performance plasmonic sensors based on extraordinary optical transmission,” J. Mater. Chem. 22(18), 8903–8910 (2012).
[Crossref]

Lin, G. H.

T. W. Chang, X. H. Wang, A. Hsiao, Z. D. Xu, G. H. Lin, M. R. Gartia, X. R. Liu, and G. L. Liu, “Bifunctional Nano Lycurgus Cup Array Plasmonic Sensor for Colorimetric Sensing and Surface-Enhanced Raman Spectroscopy,” Adv. Opt. Mater. 3(10), 1397–1404 (2015).
[Crossref]

Liu, G.

Liu, G. L.

T. W. Chang, X. H. Wang, A. Hsiao, Z. D. Xu, G. H. Lin, M. R. Gartia, X. R. Liu, and G. L. Liu, “Bifunctional Nano Lycurgus Cup Array Plasmonic Sensor for Colorimetric Sensing and Surface-Enhanced Raman Spectroscopy,” Adv. Opt. Mater. 3(10), 1397–1404 (2015).
[Crossref]

M. R. Gartia, A. Hsiao, A. Pokhriyal, S. Seo, G. Kulsharova, B. T. Cunningham, T. C. Bond, and G. L. Liu, “Colorimetric plasmon resonance imaging using nano lycurgus cup arrays,” Adv. Opt. Mater. 1(4), 281 (2013).
[Crossref]

Liu, X. R.

T. W. Chang, X. H. Wang, A. Hsiao, Z. D. Xu, G. H. Lin, M. R. Gartia, X. R. Liu, and G. L. Liu, “Bifunctional Nano Lycurgus Cup Array Plasmonic Sensor for Colorimetric Sensing and Surface-Enhanced Raman Spectroscopy,” Adv. Opt. Mater. 3(10), 1397–1404 (2015).
[Crossref]

Lochner, L. R.

C. S. Izzard and L. R. Lochner, “Cell-to-Substrate Contacts in Living Fibroblasts: an Interference Reflexion Study with an Evaluation of the Technique,” J. Cell Sci. 21(1), 129–159 (1976).
[PubMed]

Logan Liu, G.

L. Plucinski, M. Ranjan Gartia, W. R. Arnold, A. Ameen, T. W. Chang, A. Hsiao, G. Logan Liu, and A. Das, “Substrate binding to cytochrome P450-2J2 in Nanodiscs detected by nanoplasmonic Lycurgus cup arrays,” Biosens. Bioelectron. 75, 337–346 (2016).
[Crossref] [PubMed]

Maheshwari, G.

G. Maheshwari, G. Brown, D. A. Lauffenburger, A. Wells, and L. G. Griffith, “Cell adhesion and motility depend on nanoscale RGD clustering,” J. Cell Sci. 113(Pt 10), 1677–1686 (2000).
[PubMed]

Mar, M. N.

L. S. Jung, C. T. Campbell, T. M. Chinowsky, M. N. Mar, and S. S. Yee, “Quantitative interpretation of the response of surface plasmon resonance sensors to adsorbed films,” Langmuir 14(19), 5636–5648 (1998).
[Crossref]

Maskarinec, S. A.

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]

Matsuura, K.

Misevic, G. N.

U. Dammer, O. Popescu, P. Wagner, D. Anselmetti, H. J. Güntherodt, and G. N. Misevic, “Binding strength between cell adhesion proteoglycans measured by atomic force microscopy,” Science 267(5201), 1173–1175 (1995).
[Crossref] [PubMed]

Muller, D. J.

P. H. Puech, K. Poole, D. Knebel, and D. J. Muller, “A new technical approach to quantify cell-cell adhesion forces by AFM,” Ultramicroscopy 106(8-9), 637–644 (2006).
[Crossref] [PubMed]

Munevar, S.

S. Munevar, Y. Wang, and M. Dembo, “Traction force microscopy of migrating normal and H-ras transformed 3T3 fibroblasts,” Biophys. J. 80(4), 1744–1757 (2001).
[Crossref] [PubMed]

Nagata, K.

Ning, J.

Pelham, R. J.

R. J. Pelham and Y. L. Wang, “Cell locomotion and focal adhesions are regulated by substrate flexibility (vol 94, pg 13661, 1997),” Proc. Natl. Acad. Sci. U.S.A. 95, 12070 (1998).

Pierschbacher, M. D.

E. Ruoslahti and M. D. Pierschbacher, “New perspectives in cell adhesion: RGD and integrins,” Science 238(4826), 491–497 (1987).
[Crossref] [PubMed]

Plucinski, L.

L. Plucinski, M. Ranjan Gartia, W. R. Arnold, A. Ameen, T. W. Chang, A. Hsiao, G. Logan Liu, and A. Das, “Substrate binding to cytochrome P450-2J2 in Nanodiscs detected by nanoplasmonic Lycurgus cup arrays,” Biosens. Bioelectron. 75, 337–346 (2016).
[Crossref] [PubMed]

Pokhriyal, A.

M. R. Gartia, A. Hsiao, A. Pokhriyal, S. Seo, G. Kulsharova, B. T. Cunningham, T. C. Bond, and G. L. Liu, “Colorimetric plasmon resonance imaging using nano lycurgus cup arrays,” Adv. Opt. Mater. 1(4), 281 (2013).
[Crossref]

Poole, K.

P. H. Puech, K. Poole, D. Knebel, and D. J. Muller, “A new technical approach to quantify cell-cell adhesion forces by AFM,” Ultramicroscopy 106(8-9), 637–644 (2006).
[Crossref] [PubMed]

Popescu, O.

U. Dammer, O. Popescu, P. Wagner, D. Anselmetti, H. J. Güntherodt, and G. N. Misevic, “Binding strength between cell adhesion proteoglycans measured by atomic force microscopy,” Science 267(5201), 1173–1175 (1995).
[Crossref] [PubMed]

Puech, P. H.

P. H. Puech, K. Poole, D. Knebel, and D. J. Muller, “A new technical approach to quantify cell-cell adhesion forces by AFM,” Ultramicroscopy 106(8-9), 637–644 (2006).
[Crossref] [PubMed]

Ranjan Gartia, M.

L. Plucinski, M. Ranjan Gartia, W. R. Arnold, A. Ameen, T. W. Chang, A. Hsiao, G. Logan Liu, and A. Das, “Substrate binding to cytochrome P450-2J2 in Nanodiscs detected by nanoplasmonic Lycurgus cup arrays,” Biosens. Bioelectron. 75, 337–346 (2016).
[Crossref] [PubMed]

Ravichandran, G.

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]

Riedel, M.

K. Giebel, C. Bechinger, S. Herminghaus, M. Riedel, P. Leiderer, U. Weiland, and M. Bastmeyer, “Imaging of cell/substrate contacts of living cells with surface plasmon resonance microscopy,” Biophys. J. 76(1), 509–516 (1999).
[Crossref] [PubMed]

Ruoslahti, E.

E. Ruoslahti and M. D. Pierschbacher, “New perspectives in cell adhesion: RGD and integrins,” Science 238(4826), 491–497 (1987).
[Crossref] [PubMed]

Sabass, B.

B. Sabass, M. L. Gardel, C. M. Waterman, and U. S. Schwarz, “High resolution traction force microscopy based on experimental and computational advances,” Biophys. J. 94(1), 207–220 (2008).
[Crossref] [PubMed]

Saez, 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(9), 1836–1843 (2008).
[Crossref]

Schwarz, U. S.

B. Sabass, M. L. Gardel, C. M. Waterman, and U. S. Schwarz, “High resolution traction force microscopy based on experimental and computational advances,” Biophys. J. 94(1), 207–220 (2008).
[Crossref] [PubMed]

Sen, S.

S. Sen, S. Subramanian, and D. E. Discher, “Indentation and adhesive probing of a cell membrane with AFM: theoretical model and experiments,” Biophys. J. 89(5), 3203–3213 (2005).
[Crossref] [PubMed]

Seo, S.

M. R. Gartia, A. Hsiao, A. Pokhriyal, S. Seo, G. Kulsharova, B. T. Cunningham, T. C. Bond, and G. L. Liu, “Colorimetric plasmon resonance imaging using nano lycurgus cup arrays,” Adv. Opt. Mater. 1(4), 281 (2013).
[Crossref]

Silberzan, P.

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(9), 1836–1843 (2008).
[Crossref]

Sinton, D.

R. Gordon, D. Sinton, K. L. Kavanagh, and A. G. Brolo, “A new generation of sensors based on extraordinary optical transmission,” Acc. Chem. Res. 41(8), 1049–1057 (2008).
[Crossref] [PubMed]

Subramanian, S.

S. Sen, S. Subramanian, and D. E. Discher, “Indentation and adhesive probing of a cell membrane with AFM: theoretical model and experiments,” Biophys. J. 89(5), 3203–3213 (2005).
[Crossref] [PubMed]

Tirrell, D. A.

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]

Trichet, L.

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(9), 1836–1843 (2008).
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H. Verschueren, “Interference reflection microscopy in cell biology: methodology and applications,” J. Cell Sci. 75, 279–301 (1985).
[PubMed]

Wagner, P.

U. Dammer, O. Popescu, P. Wagner, D. Anselmetti, H. J. Güntherodt, and G. N. Misevic, “Binding strength between cell adhesion proteoglycans measured by atomic force microscopy,” Science 267(5201), 1173–1175 (1995).
[Crossref] [PubMed]

Wang, T. Q.

X. M. Zhang, Z. B. Li, S. S. Ye, S. Wu, J. H. Zhang, L. Y. Cui, A. R. Li, T. Q. Wang, S. Z. Li, and B. Yang, “Elevated Ag nanohole arrays for high performance plasmonic sensors based on extraordinary optical transmission,” J. Mater. Chem. 22(18), 8903–8910 (2012).
[Crossref]

Wang, X. H.

T. W. Chang, X. H. Wang, A. Hsiao, Z. D. Xu, G. H. Lin, M. R. Gartia, X. R. Liu, and G. L. Liu, “Bifunctional Nano Lycurgus Cup Array Plasmonic Sensor for Colorimetric Sensing and Surface-Enhanced Raman Spectroscopy,” Adv. Opt. Mater. 3(10), 1397–1404 (2015).
[Crossref]

Wang, Y.

S. Munevar, Y. Wang, and M. Dembo, “Traction force microscopy of migrating normal and H-ras transformed 3T3 fibroblasts,” Biophys. J. 80(4), 1744–1757 (2001).
[Crossref] [PubMed]

Wang, Y. L.

D. E. Discher, P. Janmey, and Y. L. Wang, “Tissue cells feel and respond to the stiffness of their substrate,” Science 310(5751), 1139–1143 (2005).
[Crossref] [PubMed]

R. J. Pelham and Y. L. Wang, “Cell locomotion and focal adhesions are regulated by substrate flexibility (vol 94, pg 13661, 1997),” Proc. Natl. Acad. Sci. U.S.A. 95, 12070 (1998).

Watanabe, K.

Waterman, C. M.

B. Sabass, M. L. Gardel, C. M. Waterman, and U. S. Schwarz, “High resolution traction force microscopy based on experimental and computational advances,” Biophys. J. 94(1), 207–220 (2008).
[Crossref] [PubMed]

Weiland, U.

K. Giebel, C. Bechinger, S. Herminghaus, M. Riedel, P. Leiderer, U. Weiland, and M. Bastmeyer, “Imaging of cell/substrate contacts of living cells with surface plasmon resonance microscopy,” Biophys. J. 76(1), 509–516 (1999).
[Crossref] [PubMed]

Wells, A.

G. Maheshwari, G. Brown, D. A. Lauffenburger, A. Wells, and L. G. Griffith, “Cell adhesion and motility depend on nanoscale RGD clustering,” J. Cell Sci. 113(Pt 10), 1677–1686 (2000).
[PubMed]

Wu, S.

X. M. Zhang, Z. B. Li, S. S. Ye, S. Wu, J. H. Zhang, L. Y. Cui, A. R. Li, T. Q. Wang, S. Z. Li, and B. Yang, “Elevated Ag nanohole arrays for high performance plasmonic sensors based on extraordinary optical transmission,” J. Mater. Chem. 22(18), 8903–8910 (2012).
[Crossref]

Xayaphoummine, 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(9), 1836–1843 (2008).
[Crossref]

Xu, Z. D.

T. W. Chang, X. H. Wang, A. Hsiao, Z. D. Xu, G. H. Lin, M. R. Gartia, X. R. Liu, and G. L. Liu, “Bifunctional Nano Lycurgus Cup Array Plasmonic Sensor for Colorimetric Sensing and Surface-Enhanced Raman Spectroscopy,” Adv. Opt. Mater. 3(10), 1397–1404 (2015).
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Yang, B.

X. M. Zhang, Z. B. Li, S. S. Ye, S. Wu, J. H. Zhang, L. Y. Cui, A. R. Li, T. Q. Wang, S. Z. Li, and B. Yang, “Elevated Ag nanohole arrays for high performance plasmonic sensors based on extraordinary optical transmission,” J. Mater. Chem. 22(18), 8903–8910 (2012).
[Crossref]

Ye, S. S.

X. M. Zhang, Z. B. Li, S. S. Ye, S. Wu, J. H. Zhang, L. Y. Cui, A. R. Li, T. Q. Wang, S. Z. Li, and B. Yang, “Elevated Ag nanohole arrays for high performance plasmonic sensors based on extraordinary optical transmission,” J. Mater. Chem. 22(18), 8903–8910 (2012).
[Crossref]

Yee, S. S.

L. S. Jung, C. T. Campbell, T. M. Chinowsky, M. N. Mar, and S. S. Yee, “Quantitative interpretation of the response of surface plasmon resonance sensors to adsorbed films,” Langmuir 14(19), 5636–5648 (1998).
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B. R. Zetter, “Adhesion Molecules in Tumor Metastasis,” Semin. Cancer Biol. 4(4), 219–229 (1993).
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X. M. Zhang, Z. B. Li, S. S. Ye, S. Wu, J. H. Zhang, L. Y. Cui, A. R. Li, T. Q. Wang, S. Z. Li, and B. Yang, “Elevated Ag nanohole arrays for high performance plasmonic sensors based on extraordinary optical transmission,” J. Mater. Chem. 22(18), 8903–8910 (2012).
[Crossref]

Zhang, X. M.

X. M. Zhang, Z. B. Li, S. S. Ye, S. Wu, J. H. Zhang, L. Y. Cui, A. R. Li, T. Q. Wang, S. Z. Li, and B. Yang, “Elevated Ag nanohole arrays for high performance plasmonic sensors based on extraordinary optical transmission,” J. Mater. Chem. 22(18), 8903–8910 (2012).
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Zhu, C.

C. Zhu, “Kinetics and mechanics of cell adhesion,” J. Biomech. 33(1), 23–33 (2000).
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Acc. Chem. Res. (1)

R. Gordon, D. Sinton, K. L. Kavanagh, and A. G. Brolo, “A new generation of sensors based on extraordinary optical transmission,” Acc. Chem. Res. 41(8), 1049–1057 (2008).
[Crossref] [PubMed]

Adv. Opt. Mater. (2)

M. R. Gartia, A. Hsiao, A. Pokhriyal, S. Seo, G. Kulsharova, B. T. Cunningham, T. C. Bond, and G. L. Liu, “Colorimetric plasmon resonance imaging using nano lycurgus cup arrays,” Adv. Opt. Mater. 1(4), 281 (2013).
[Crossref]

T. W. Chang, X. H. Wang, A. Hsiao, Z. D. Xu, G. H. Lin, M. R. Gartia, X. R. Liu, and G. L. Liu, “Bifunctional Nano Lycurgus Cup Array Plasmonic Sensor for Colorimetric Sensing and Surface-Enhanced Raman Spectroscopy,” Adv. Opt. Mater. 3(10), 1397–1404 (2015).
[Crossref]

Biomed. Opt. Express (1)

Biophys. J. (4)

K. Giebel, C. Bechinger, S. Herminghaus, M. Riedel, P. Leiderer, U. Weiland, and M. Bastmeyer, “Imaging of cell/substrate contacts of living cells with surface plasmon resonance microscopy,” Biophys. J. 76(1), 509–516 (1999).
[Crossref] [PubMed]

S. Munevar, Y. Wang, and M. Dembo, “Traction force microscopy of migrating normal and H-ras transformed 3T3 fibroblasts,” Biophys. J. 80(4), 1744–1757 (2001).
[Crossref] [PubMed]

B. Sabass, M. L. Gardel, C. M. Waterman, and U. S. Schwarz, “High resolution traction force microscopy based on experimental and computational advances,” Biophys. J. 94(1), 207–220 (2008).
[Crossref] [PubMed]

S. Sen, S. Subramanian, and D. E. Discher, “Indentation and adhesive probing of a cell membrane with AFM: theoretical model and experiments,” Biophys. J. 89(5), 3203–3213 (2005).
[Crossref] [PubMed]

Biosens. Bioelectron. (1)

L. Plucinski, M. Ranjan Gartia, W. R. Arnold, A. Ameen, T. W. Chang, A. Hsiao, G. Logan Liu, and A. Das, “Substrate binding to cytochrome P450-2J2 in Nanodiscs detected by nanoplasmonic Lycurgus cup arrays,” Biosens. Bioelectron. 75, 337–346 (2016).
[Crossref] [PubMed]

Cell (2)

B. M. Gumbiner, “Cell adhesion: the molecular basis of tissue architecture and morphogenesis,” Cell 84(3), 345–357 (1996).
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Figures (6)

Fig. 1
Fig. 1 (a) Schematic of a single cell cultured on the Au plasmonic nanocup device. (b) Top-down SEM image of the EOT sensor to show the morphology experienced by the cell. (c) Simulated transmission spectra when the superstrate RI is increased. (d) Simulated transmission spectra when the cell-substrate separation distance is decreased. (e) Electromagnetic near field components at the resonance conditions.
Fig. 2
Fig. 2 (a) Transmission spectra of the nanocup array for air, PBS, and PBS with a cultured cell. (b-c) Histograms of the red, green, blue, and green-red color channels for RGB images of the nanocup array with air and PBS, respectively. (d) Relationship between spectral peak position and superstrate RI. (e-h) Histograms for red, green, blue, and green-red color channels for different superstrate RI. (i) Relationship between color channel peak intensity and superstrate RI.
Fig. 3
Fig. 3 RGB image before (a) and after (b) filtering. (c-e) Red channel, green channel, and green-red channel images, respectively. The scale bar is 10 µm.
Fig. 4
Fig. 4 RGB image of one cell before (a) and after (b) filtering. (c-e) Red channel, green channel, and difference channel images, respectively. RGB image of another cell before (f) and after (g) filtering. (h-j) Red, green, and difference channel images, respectively. The second color bar in (e) and (j) gives the cell-substrate separation distance. The scale bar is 10 µm.
Fig. 5
Fig. 5 (a-e) Cells cultured on the plasmonic device with images taken once every thirty minutes. (e-h) The same images are shown with a closer view of the cell body and smaller intensity range to increase contrast. The second colorbar indicates the cell-substrate separation distance. The scale bar is 10 µm.
Fig. 6
Fig. 6 (a) Schematic of the multispectral imaging setup. (b) Image taken at λ = 625 nm. (c-h) Contrast stretched difference image, I(λ1-I(λ2), between λ2 = 625 nm and λ1 = 450 nm, λ1 = 475 nm, λ1 = 500 nm, λ1 = 525 nm, λ1 = 550 nm, and λ1 = 575 nm, respectively. (i-k) Visualization of single cells for the difference image between λ1 = 575 nm and λ2 = 625 nm. The scale bar for (a)-(h) is 50 µm. The scale bar for (i)-(k) is 10 µm.

Equations (2)

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ΔI=m(R I eff R I c )
R I eff = 2 l 0 RI(z) e 2z/l dz

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