Abstract

In spite of the advantages associated with the molecular specificity of fluorescence imaging, there is still a significant need to augment these approaches with label-free imaging. Therefore, we have implemented a form of interference microscopy based upon phase-shifted, laser-feedback interferometry and developed an algorithm that can be used to separate the contribution of the elastically scattered light by sub-cellular structures from the reflection at the coverslip-buffer interface. The method offers an opportunity to probe protein aggregation, index of refraction variations and structure. We measure the topography and reflection from calibration spheres and from stress fibers and adhesions in both fixed and motile cells. Unlike the data acquired with reflection interference contrast microscopy, where the reflection from adhesions can appear dark, our approach demonstrates that these regions have high reflectivity. The data acquired from fixed and live cells show the presence of a dense actin layer located ≈ 100 nm above the coverslip interface. Finally, the measured dynamics of filopodia and the lamella in a live cell supports retrograde flow as the dominate mechanism responsible for filopodia retraction.

© 2011 OSA

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2010 (4)

K. Salaita, P. M. Nair, R. S. Petit, R. M. Neve, D. Das, J. W. Gray, and J. T. Groves, “Restriction of receptor movement alters cellular response: physical force sensing by EphA2,” Science 327(5971), 1380–1385 (2010).
[CrossRef] [PubMed]

H. Ding, L. J. Millet, M. U. Gillette, and G. Popescu, “Actin-driven cell dynamics probed by Fourier transform light scattering,” Biomed. Opt. Express 1(1), 260–267 (2010).
[CrossRef]

N. T. Shaked, L. L. Satterwhite, N. Bursac, and A Wax, “Whole-cell-analysis of live cardiomyocytes using wide-field interferometric phase microscopy,” Biomed. Opt. Express 1(2), 706–719 (2010)
[CrossRef]

P. Kanchanawong, G. Shtengel, A. M. G. Pasapera, E. B Ramko, M. W. Davidson, H. F. Hess, and C. M. Waterman, “Nanoscale architecture of integrin-based cell adhesions,” Nature 468(7323), 580–584 (2010).
[CrossRef] [PubMed]

2009 (11)

G. Shtengel, J. A. Galbraith, C. G. Galbraith, J. Lippincott-Schwartz, J. M. Gillette, S. Manley, R. Sougrat, C. M. Waterman, P. Kanchanawong, M. W. Davidson, R. D. Fetter, and H. F. Hess, “Interferometric fluorescent super-resolution microscopy resolves 3D cellular ultrastructure,” Proc. Nat. Acad. Sci. U.S.A. 106(9), 3125–3130 (2009).
[CrossRef]

E. Atilgan and B. Ovryn, “Nucleation and growth of integrin adhesions,” Biophys. J. 96, 3555–3572 (2009).
[CrossRef] [PubMed]

C. H. Chen, F. C. Tsai, C. C. Wang, and C. H. Lee, “Three-dimensional characterization of active membrane waves on living cells,” Phys. Rev. Lett. 103238101 (2009).
[CrossRef]

N. T. Shaked, Y. Zhu, M. T. Rinehart, and A. Wax, “Two-step-only phase-shifting interferometry with optimized detector bandwidth for microscopy of live cells,” Opt. Express 17(18), 15585–15591 (2009)
[CrossRef] [PubMed]

E. Atilgan and B. Ovryn, “Membrane deformation at integrin adhesions,” Curr. Pharma. Biotechnol. 10(5), 508–514 (2009).
[CrossRef]

H. Wolfenson, Y. I. Henis, B. Geiger, and A. D. Bershadsky, “The heel and toe of the cells foot: a multifaceted approach for understanding the structure and dynamics of focal adhesions,” Cell Motil. Cytoskeleton. 66(11), 1017–1029 (2009).
[CrossRef] [PubMed]

A. D. Dubash, M. M. Menold, T. Samson, E. Boulter, R. Garcia-Mata, R. Doughman, and K. Burridge, “Focal adhesions: new angles on an old structure,” Int. Rev. Cell Mol. Biol. 277, 1–65 (2009).
[CrossRef] [PubMed]

A. S. Smith and E. Sackmann, “Progress in mimetic studies of cell adhesion and the mechanosensing,” ChemPhysChem 10(1), 66–78 (2009).
[CrossRef]

L. Limozin and K. Sengupta, “Quantitative reflection interference contrast microscopy (RICM) in soft matter and cell adhesion,” ChemPhysChem 10(16), 2752–2768 (2009).
[CrossRef] [PubMed]

P. V. Ganesan and S. G. Boxer, “A membrane interferometer,” Proc. Nat. Acad. Sci. U.S.A. 106(14), 5627–5632 (2009).
[CrossRef]

B. Geiger, J. P. Spatz, and A. D. Bershadsky, “Environmental sensing through focal adhesions,” Nat. Rev. Mol. Cell Biol. 10(1), 21–33 (2009).
[CrossRef] [PubMed]

2008 (9)

P. K. Mattila and P. Lappalainen, “Filopodia: molecular architecture and cellular functions,” Nat. Rev. Mol. Cell Biol. 9, 446–454 (2008).
[CrossRef] [PubMed]

A. S. Smith, K. Sengupta, S. Goennenwein, U. Seifert, and E. Sackmann, “Force-induced growth of adhesion domains is controlled by receptor mobility,” Proc. Nat. Acad. Sci. U.S.A. 105, 6906–6911 (2008).
[CrossRef]

G. Shroff, C. G Hari, and E. Betzig, “Live-cell photoactivated localization microscopy of nanoscale adhesion dynamics,” Nat. Meth. 5, 417–423 (2008).
[CrossRef]

G. Gauglitz and G. Proll, “Strategies for label-free optical detection,” Adv. Biochem. Eng. Biotech. 109, 395–432 (2008).

H. F. Ding, Z. Wang, F. Nguyen, S. A. Boppart, and G. Popescu, “Fourier transform light scattering of inhomogeneous and dynamic structures,” Phys. Rev. Lett. 101(23), 238102 (2008).
[CrossRef] [PubMed]

J. T. Groves, R. Parthasarathy, and M. B. Forstner, “Fluorescence imaging of membrane dynamics,” Annu. Rev. Biomed. Eng. 10, 311–338 (2008).
[CrossRef] [PubMed]

A. A. M. Pierres, D. Benoliel, D. Touchard, and P. Bongrand, “How cells tiptoe on adhesive surfaces before sticking,” Biophys. J. 94, 4114–4122 (2008).
[CrossRef] [PubMed]

C. Le Clainche and M. F. Carlier, “Regulation of actin assembly associated with protrusion and adhesion in cell migration,” Physiol. Rev. 88(2), 489–513 (2008).
[CrossRef] [PubMed]

I. G. E. Renhorn and G. D. Boreman, “Analytical fitting model for rough-surface BRDF,” Opt. Express 16(17), 12892–12898 (2008).
[CrossRef] [PubMed]

2007 (7)

L. Limozin and K. Sengupta, “Modulation of vesicle adhesion and spreading kinetics by Hyaluronan cushions,” Biophys. J. 93, 3300–3313 (2007).
[CrossRef] [PubMed]

A. Boulbitch, Z. Guttenberg, and E. Sackmann, “Kinetics of membrane adhesion mediated by Ligand-receptor interaction studied with a biomimetic system,” Biophys. J. 81, 2743–2751 (2007).
[CrossRef]

J. Hwang and W. Moerner, “Interferometry of a single nanoparticle using the Gouy phase of a focused laser beam,” Opt. Commun. 280(2), 487–491 (2007).
[CrossRef]

S. Pellegrin and H. Mellor, “Actin stress fibres,” J. Cell Sci. 120(20), 3491–3499 (2007).
[CrossRef] [PubMed]

M. Rueckel and W. Denk, “Properties of coherence-gated wavefront sensing,” J. Opt. Soc. Am. A 24(11), 3517–3529 (2007).
[CrossRef]

H. Shroff, C. G. Galbraith, J. A. Galbraith, H. White, J. Gillette, S. Olenych, M. W. Davidson, and E. Betzig, “Dual-color superresolution imaging of genetically expressed probes within individual adhesion complexes,” Proc. Nat. Acad. Sci. U.S.A. 104(51), 20308–20313 (2007).
[CrossRef]

D. J. Bornhop, J. C. Latham, A. Kussrow, D. A. Markov, R. D. Jones, and H. S. Sorensen, “Free-solution, label-free molecular interactions studied by back-scattering interferometry,” Science 317(5845), 1732 (2007).
[CrossRef] [PubMed]

2006 (2)

E. Betzig, G. H. Patterson, R. Sougrat, O. W. Lindwasser, S. Olenych, J. S. Bonifacino, M. W. Davidson, J. Lippincott-Schwartz, and H. F. Hess, “Imaging intracellular fluorescent proteins at nanometer resolution,” Science 313(5793), 1642–1645 (2006).
[CrossRef] [PubMed]

A. Zidovska and E. Sackmann, “Brownian Motion of nucleated cell envelopes impedes adhesion,” Phys. Rev. Lett. 96, 048103 (2006).
[CrossRef] [PubMed]

2005 (3)

C. H. Wang, J. Y. Lin, and C. H. Lee, “Membrane ripples of a living cell measured by non-interferometric wide-field optical profilometry,” Opt. Express 13(26), 10665–10672 (2005).
[CrossRef] [PubMed]

S. K. Mitra, D. A. Hanson, and D. D. Schlaepfer, “Focal adhesion kinase: in command and control of cell motility,” Nat. Rev. Mol. Cell Biol. 6(1), 56–68 (2005).
[CrossRef] [PubMed]

N. G. Clack and J. T. Groves, “Many-particle tracking with nanometer resolution in three dimensions by reflection interference contrast microscopy,” Langmuir 21(14), 6430–6435 (2005).
[CrossRef] [PubMed]

2004 (2)

C. J. R. Sheppard, M. Roy, and M. D. Sharma, “Image formation in low-coherence and confocal interference microscopes,” Appl. Opt. 43(7), 1493–1502 (2004).
[CrossRef] [PubMed]

R. Parthasarathy and J. T. Groves, “Optical techniques for imaging membrane topography,” Cell. Biochem. Biophys. 1(3), 391–414 (2004).
[CrossRef]

2003 (2)

I. Weber, “Reflection interference contrast microscopy,” Meth. Enzymol. 361, 34–47 (2003).
[CrossRef] [PubMed]

X. Ma, J.Q. Lu, R. S. Brock, K. M. Jacobs, and X.H. Hu, “Determination of complex refractive index of polystyrene microspheres from 370 to 1610 nm,” Phys. Med. Biol. 48(24), 4165–4172 (2003).
[CrossRef]

2002 (3)

W. Wang, J. B. Wycko, V. C. Frohlich, Y. Oleynikov, S. Huttelmaier, J. Zavadil, L. Cermak, E. P. Bottinger, R. H. Singer, J. G. White, J. E. Segall, and J. S. Condeelis, “Single cell behavior in metastatic primary mammary tumors correlated with gene expression patterns revealed by molecular profiling,” Cancer Res. 62, 6278–6288 (2002).
[PubMed]

S. T. Hess and W. W. Webb, “Focal volume optics and experimental artifacts in confocal fluorescence correlation spectroscopy,” Biophys. J. 83(4), 2300–2317 (2002).
[CrossRef] [PubMed]

M. B. Steketee and K. W. Tosney, “Three functionally distinct adhesions in filopodia: shaft adhesions control Lamellar extension,” J. Neurol. 22(18), 8071–8083 (2002).

2001 (2)

J. R. Mourant, T. M. Johnson, and J. P. Freyer, “Characterizing mammalian cells and cell phantoms by polarized backscattering fiber-optic measurements,” Appl. Opt. 40(28), 5114–5123 (2001).
[CrossRef]

Y. Iwanaga, Y. D. Braun, and P. Fromherz, “No correlation of focal contacts and close adhesion by comparing GFP-vinculin and fluorescence interference of DiI,” Eur. Biophys. J. 30(1), 17–26 (2001).
[CrossRef] [PubMed]

2000 (2)

B. Ovryn, “Three-dimensional forward scattering particle image velocimetry applied to a microscopic field-of-view,” Exp. Fluids 29(1), S175–S184 (2000).
[CrossRef]

D. G. Fischer and B. Ovryn, “Interfacial shape and contact-angle measurement of transparent samples with confocal interference microscopy,” Opt. Lett. 25(7), 478–480 (2000).
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1999 (2)

A. Mallavarapu and T. J. Mitchison, “Regulated actin cytoskeleton assembly at filopodium tips controls their extension and retraction,” Cell Biol. 146(5), 1097–1106 (1999).
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B. Ovryn and J. H. Andrews, “Measurement of changes in optical path length and reflectivity with phase-shifting laser feedback interferometry,” Appl. Opt. 38(10), 1959–1967 (1999).
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1998 (4)

M. Born and E. Wolf, Principles of Optics (Cambridge University Press, 1998).

J. M. Schmitt and G. Kumar , “Optical scattering properties of soft tissue: a discrete particle model,” Appl. Opt. 37(13), 2788–2797 (1998).
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B. Ovryn and J. H. Andrews, “Phase-shifted laser feedback interferometry,” Opt. Lett. 23(14), 1078–1080 (1998).
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D. Zuckerman and R. Bruinsma, “Vesicle-vesicle adhesion by mobile lock-and-key molecules: Debye-Huckel theory and Monte Carlo simulation,” Phys. Rev. E 57, 964–977 (1998).
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1995 (2)

J. O. Radler, T. J. Feder, H. H. Strey, and E. Sackmann, “Fluctuation analysis of tension-controlled undulation forces between giant vesicles and solid substrates,” Phys. Rev. E 51, 4526–4536 (1995).
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C. J. R. Sheppard and K. G. Larkin, “Effect of numerical aperture on interference fringe spacing,” Appl. Opt. 34(22), 4731–4734 (1995).
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1993 (3)

J J. Radler and E. Sackmann, “Imaging optical thicknesses and separation distances of phospholipid vesicles at solid surfaces,” J. Phys. II France 3(5), 727–748 (1993).
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A. Bearden, M. P. O’Neill, L. C. Osborne, and T. L. Wong, “Imaging and vibrational analysis with laser-feedback interferometry,” Opt. Lett. 18(3), 238–240 (1993).
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R. Juskaitis, N. Rea, and T. Wilson, “Fibre-optic based confocal microscopy using laser detection,” Opt. Commun. 99(1), 105–113 (1993).
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1992 (1)

J. Radler and E. Sackmann, “On the measurement of weak repulsive and frictional colloidal forces by reflection interference contrast microscopy,” Langmuir 8(3), 848–853 (1992).
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1991 (1)

X. D. He, K. E. Torrance, F. X. Sillion, and D. P. Greenberg, “A comprehensive physical model for light reflection,” SIGGRAPH Comput. Graph. 25(4), 175–186 (1991).
[CrossRef]

1988 (4)

K. Creath, “Phase measurement interferometry techniques,” in Progress in Optics , E. Wolf eds. (North-Holland, 1988) XXVI349–393.
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I. I. Singer, S. Scott, D. W. Kawka, D. M. Kazazis, J. Gailit, and E. Ruoslahti, “Cell surface distribution of fibronectin and vitronectin receptors depends on substrate composition and extracellular matrix accumulation.” J. Cell Biol. 106(6), 2171–2182 (1988).
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G. L. Nicolson, “Differential organ tissue adhesion, invasion, and growth properties of metastatic rat mammary adenocarcinoma cells,” Breast Cancer Res. Treat. 12(2), 167–176 (1988).
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J. Bailey and D. Gingell, “Contacts of chick fibroblasts on glass: results and limitations of quantitative interferometry,” J. Cell Sci. 90(2), 215–224 (1988).
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1987 (2)

1985 (1)

H. Verschueren, “Interference reflection microscopy in cell biology: Methodology and applications,” J. Cell Sci. 75(1), 279–301 (1985).
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1984 (1)

Y. Y. Cheng and J. C. Wyant, “Two-wavelength phase shifting interferometry,” Appl. Oct. 23(24), 4539–4543 (1984).
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1976 (2)

C. Izzard and L. Lochner, “Cell-to-substrate contacts in living fibroblasts: an interference reflexion study with an evaluation of the technique,” J. Cell Sci. 21, 129–159 (1976).
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J. B. Keller, “Inverse problems,” A. Math. Mon. 83(2), 107–118 (1976).
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1967 (1)

T. H. Peek, P. T. Bolwijn, and C. T. J. Alkemade, “Axial mode number of gas lasers from moving-mirror experiments,” Am. J. Phys. 35(9), 820–831 (1967).
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1964 (1)

A. S. G. Curtis, “The mechanism of adhesion of cells to glass. A study by interference reflection microscopy,” J. Cell Biol. 20(2), 199–215 (1964).
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Alkemade, C. T. J.

T. H. Peek, P. T. Bolwijn, and C. T. J. Alkemade, “Axial mode number of gas lasers from moving-mirror experiments,” Am. J. Phys. 35(9), 820–831 (1967).
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Andrews, J. H.

Atilgan, E.

E. Atilgan and B. Ovryn, “Membrane deformation at integrin adhesions,” Curr. Pharma. Biotechnol. 10(5), 508–514 (2009).
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E. Atilgan and B. Ovryn, “Nucleation and growth of integrin adhesions,” Biophys. J. 96, 3555–3572 (2009).
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Bailey, J.

J. Bailey and D. Gingell, “Contacts of chick fibroblasts on glass: results and limitations of quantitative interferometry,” J. Cell Sci. 90(2), 215–224 (1988).
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Bearden, A.

Benoliel, D.

A. A. M. Pierres, D. Benoliel, D. Touchard, and P. Bongrand, “How cells tiptoe on adhesive surfaces before sticking,” Biophys. J. 94, 4114–4122 (2008).
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Bershadsky, A. D.

B. Geiger, J. P. Spatz, and A. D. Bershadsky, “Environmental sensing through focal adhesions,” Nat. Rev. Mol. Cell Biol. 10(1), 21–33 (2009).
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H. Wolfenson, Y. I. Henis, B. Geiger, and A. D. Bershadsky, “The heel and toe of the cells foot: a multifaceted approach for understanding the structure and dynamics of focal adhesions,” Cell Motil. Cytoskeleton. 66(11), 1017–1029 (2009).
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Betzig, E.

G. Shroff, C. G Hari, and E. Betzig, “Live-cell photoactivated localization microscopy of nanoscale adhesion dynamics,” Nat. Meth. 5, 417–423 (2008).
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H. Shroff, C. G. Galbraith, J. A. Galbraith, H. White, J. Gillette, S. Olenych, M. W. Davidson, and E. Betzig, “Dual-color superresolution imaging of genetically expressed probes within individual adhesion complexes,” Proc. Nat. Acad. Sci. U.S.A. 104(51), 20308–20313 (2007).
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E. Betzig, G. H. Patterson, R. Sougrat, O. W. Lindwasser, S. Olenych, J. S. Bonifacino, M. W. Davidson, J. Lippincott-Schwartz, and H. F. Hess, “Imaging intracellular fluorescent proteins at nanometer resolution,” Science 313(5793), 1642–1645 (2006).
[CrossRef] [PubMed]

Bolwijn, P. T.

T. H. Peek, P. T. Bolwijn, and C. T. J. Alkemade, “Axial mode number of gas lasers from moving-mirror experiments,” Am. J. Phys. 35(9), 820–831 (1967).
[CrossRef]

Bongrand, P.

A. A. M. Pierres, D. Benoliel, D. Touchard, and P. Bongrand, “How cells tiptoe on adhesive surfaces before sticking,” Biophys. J. 94, 4114–4122 (2008).
[CrossRef] [PubMed]

Bonifacino, J. S.

E. Betzig, G. H. Patterson, R. Sougrat, O. W. Lindwasser, S. Olenych, J. S. Bonifacino, M. W. Davidson, J. Lippincott-Schwartz, and H. F. Hess, “Imaging intracellular fluorescent proteins at nanometer resolution,” Science 313(5793), 1642–1645 (2006).
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Boppart, S. A.

H. F. Ding, Z. Wang, F. Nguyen, S. A. Boppart, and G. Popescu, “Fourier transform light scattering of inhomogeneous and dynamic structures,” Phys. Rev. Lett. 101(23), 238102 (2008).
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Boreman, G. D.

Born, M.

M. Born and E. Wolf, Principles of Optics (Cambridge University Press, 1998).

Bornhop, D. J.

D. J. Bornhop, J. C. Latham, A. Kussrow, D. A. Markov, R. D. Jones, and H. S. Sorensen, “Free-solution, label-free molecular interactions studied by back-scattering interferometry,” Science 317(5845), 1732 (2007).
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Bottinger, E. P.

W. Wang, J. B. Wycko, V. C. Frohlich, Y. Oleynikov, S. Huttelmaier, J. Zavadil, L. Cermak, E. P. Bottinger, R. H. Singer, J. G. White, J. E. Segall, and J. S. Condeelis, “Single cell behavior in metastatic primary mammary tumors correlated with gene expression patterns revealed by molecular profiling,” Cancer Res. 62, 6278–6288 (2002).
[PubMed]

Boulbitch, A.

A. Boulbitch, Z. Guttenberg, and E. Sackmann, “Kinetics of membrane adhesion mediated by Ligand-receptor interaction studied with a biomimetic system,” Biophys. J. 81, 2743–2751 (2007).
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Boulter, E.

A. D. Dubash, M. M. Menold, T. Samson, E. Boulter, R. Garcia-Mata, R. Doughman, and K. Burridge, “Focal adhesions: new angles on an old structure,” Int. Rev. Cell Mol. Biol. 277, 1–65 (2009).
[CrossRef] [PubMed]

Boxer, S. G.

P. V. Ganesan and S. G. Boxer, “A membrane interferometer,” Proc. Nat. Acad. Sci. U.S.A. 106(14), 5627–5632 (2009).
[CrossRef]

Braun, Y. D.

Y. Iwanaga, Y. D. Braun, and P. Fromherz, “No correlation of focal contacts and close adhesion by comparing GFP-vinculin and fluorescence interference of DiI,” Eur. Biophys. J. 30(1), 17–26 (2001).
[CrossRef] [PubMed]

Brock, R. S.

X. Ma, J.Q. Lu, R. S. Brock, K. M. Jacobs, and X.H. Hu, “Determination of complex refractive index of polystyrene microspheres from 370 to 1610 nm,” Phys. Med. Biol. 48(24), 4165–4172 (2003).
[CrossRef]

Bruinsma, R.

D. Zuckerman and R. Bruinsma, “Vesicle-vesicle adhesion by mobile lock-and-key molecules: Debye-Huckel theory and Monte Carlo simulation,” Phys. Rev. E 57, 964–977 (1998).
[CrossRef]

Burridge, K.

A. D. Dubash, M. M. Menold, T. Samson, E. Boulter, R. Garcia-Mata, R. Doughman, and K. Burridge, “Focal adhesions: new angles on an old structure,” Int. Rev. Cell Mol. Biol. 277, 1–65 (2009).
[CrossRef] [PubMed]

Bursac, N.

Carlier, M. F.

C. Le Clainche and M. F. Carlier, “Regulation of actin assembly associated with protrusion and adhesion in cell migration,” Physiol. Rev. 88(2), 489–513 (2008).
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Cermak, L.

W. Wang, J. B. Wycko, V. C. Frohlich, Y. Oleynikov, S. Huttelmaier, J. Zavadil, L. Cermak, E. P. Bottinger, R. H. Singer, J. G. White, J. E. Segall, and J. S. Condeelis, “Single cell behavior in metastatic primary mammary tumors correlated with gene expression patterns revealed by molecular profiling,” Cancer Res. 62, 6278–6288 (2002).
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Chen, C. H.

C. H. Chen, F. C. Tsai, C. C. Wang, and C. H. Lee, “Three-dimensional characterization of active membrane waves on living cells,” Phys. Rev. Lett. 103238101 (2009).
[CrossRef]

Cheng, Y. Y.

Y. Y. Cheng and J. C. Wyant, “Two-wavelength phase shifting interferometry,” Appl. Oct. 23(24), 4539–4543 (1984).
[CrossRef]

Clack, N. G.

N. G. Clack and J. T. Groves, “Many-particle tracking with nanometer resolution in three dimensions by reflection interference contrast microscopy,” Langmuir 21(14), 6430–6435 (2005).
[CrossRef] [PubMed]

Condeelis, J. S.

W. Wang, J. B. Wycko, V. C. Frohlich, Y. Oleynikov, S. Huttelmaier, J. Zavadil, L. Cermak, E. P. Bottinger, R. H. Singer, J. G. White, J. E. Segall, and J. S. Condeelis, “Single cell behavior in metastatic primary mammary tumors correlated with gene expression patterns revealed by molecular profiling,” Cancer Res. 62, 6278–6288 (2002).
[PubMed]

Creath, K.

K. Creath, “Phase measurement interferometry techniques,” in Progress in Optics , E. Wolf eds. (North-Holland, 1988) XXVI349–393.
[CrossRef]

Curtis, A. S. G.

A. S. G. 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]

Das, D.

K. Salaita, P. M. Nair, R. S. Petit, R. M. Neve, D. Das, J. W. Gray, and J. T. Groves, “Restriction of receptor movement alters cellular response: physical force sensing by EphA2,” Science 327(5971), 1380–1385 (2010).
[CrossRef] [PubMed]

Davidson, M. W.

P. Kanchanawong, G. Shtengel, A. M. G. Pasapera, E. B Ramko, M. W. Davidson, H. F. Hess, and C. M. Waterman, “Nanoscale architecture of integrin-based cell adhesions,” Nature 468(7323), 580–584 (2010).
[CrossRef] [PubMed]

G. Shtengel, J. A. Galbraith, C. G. Galbraith, J. Lippincott-Schwartz, J. M. Gillette, S. Manley, R. Sougrat, C. M. Waterman, P. Kanchanawong, M. W. Davidson, R. D. Fetter, and H. F. Hess, “Interferometric fluorescent super-resolution microscopy resolves 3D cellular ultrastructure,” Proc. Nat. Acad. Sci. U.S.A. 106(9), 3125–3130 (2009).
[CrossRef]

H. Shroff, C. G. Galbraith, J. A. Galbraith, H. White, J. Gillette, S. Olenych, M. W. Davidson, and E. Betzig, “Dual-color superresolution imaging of genetically expressed probes within individual adhesion complexes,” Proc. Nat. Acad. Sci. U.S.A. 104(51), 20308–20313 (2007).
[CrossRef]

E. Betzig, G. H. Patterson, R. Sougrat, O. W. Lindwasser, S. Olenych, J. S. Bonifacino, M. W. Davidson, J. Lippincott-Schwartz, and H. F. Hess, “Imaging intracellular fluorescent proteins at nanometer resolution,” Science 313(5793), 1642–1645 (2006).
[CrossRef] [PubMed]

Denk, W.

Ding, H.

Ding, H. F.

H. F. Ding, Z. Wang, F. Nguyen, S. A. Boppart, and G. Popescu, “Fourier transform light scattering of inhomogeneous and dynamic structures,” Phys. Rev. Lett. 101(23), 238102 (2008).
[CrossRef] [PubMed]

Doughman, R.

A. D. Dubash, M. M. Menold, T. Samson, E. Boulter, R. Garcia-Mata, R. Doughman, and K. Burridge, “Focal adhesions: new angles on an old structure,” Int. Rev. Cell Mol. Biol. 277, 1–65 (2009).
[CrossRef] [PubMed]

Dubash, A. D.

A. D. Dubash, M. M. Menold, T. Samson, E. Boulter, R. Garcia-Mata, R. Doughman, and K. Burridge, “Focal adhesions: new angles on an old structure,” Int. Rev. Cell Mol. Biol. 277, 1–65 (2009).
[CrossRef] [PubMed]

Eiju, T.

Feder, T. J.

J. O. Radler, T. J. Feder, H. H. Strey, and E. Sackmann, “Fluctuation analysis of tension-controlled undulation forces between giant vesicles and solid substrates,” Phys. Rev. E 51, 4526–4536 (1995).
[CrossRef]

Fetter, R. D.

G. Shtengel, J. A. Galbraith, C. G. Galbraith, J. Lippincott-Schwartz, J. M. Gillette, S. Manley, R. Sougrat, C. M. Waterman, P. Kanchanawong, M. W. Davidson, R. D. Fetter, and H. F. Hess, “Interferometric fluorescent super-resolution microscopy resolves 3D cellular ultrastructure,” Proc. Nat. Acad. Sci. U.S.A. 106(9), 3125–3130 (2009).
[CrossRef]

Fischer, D. G.

Forstner, M. B.

J. T. Groves, R. Parthasarathy, and M. B. Forstner, “Fluorescence imaging of membrane dynamics,” Annu. Rev. Biomed. Eng. 10, 311–338 (2008).
[CrossRef] [PubMed]

Freyer, J. P.

Frohlich, V. C.

W. Wang, J. B. Wycko, V. C. Frohlich, Y. Oleynikov, S. Huttelmaier, J. Zavadil, L. Cermak, E. P. Bottinger, R. H. Singer, J. G. White, J. E. Segall, and J. S. Condeelis, “Single cell behavior in metastatic primary mammary tumors correlated with gene expression patterns revealed by molecular profiling,” Cancer Res. 62, 6278–6288 (2002).
[PubMed]

Fromherz, P.

Y. Iwanaga, Y. D. Braun, and P. Fromherz, “No correlation of focal contacts and close adhesion by comparing GFP-vinculin and fluorescence interference of DiI,” Eur. Biophys. J. 30(1), 17–26 (2001).
[CrossRef] [PubMed]

Gailit, J.

I. I. Singer, S. Scott, D. W. Kawka, D. M. Kazazis, J. Gailit, and E. Ruoslahti, “Cell surface distribution of fibronectin and vitronectin receptors depends on substrate composition and extracellular matrix accumulation.” J. Cell Biol. 106(6), 2171–2182 (1988).
[CrossRef] [PubMed]

Galbraith, C. G.

G. Shtengel, J. A. Galbraith, C. G. Galbraith, J. Lippincott-Schwartz, J. M. Gillette, S. Manley, R. Sougrat, C. M. Waterman, P. Kanchanawong, M. W. Davidson, R. D. Fetter, and H. F. Hess, “Interferometric fluorescent super-resolution microscopy resolves 3D cellular ultrastructure,” Proc. Nat. Acad. Sci. U.S.A. 106(9), 3125–3130 (2009).
[CrossRef]

H. Shroff, C. G. Galbraith, J. A. Galbraith, H. White, J. Gillette, S. Olenych, M. W. Davidson, and E. Betzig, “Dual-color superresolution imaging of genetically expressed probes within individual adhesion complexes,” Proc. Nat. Acad. Sci. U.S.A. 104(51), 20308–20313 (2007).
[CrossRef]

Galbraith, J. A.

G. Shtengel, J. A. Galbraith, C. G. Galbraith, J. Lippincott-Schwartz, J. M. Gillette, S. Manley, R. Sougrat, C. M. Waterman, P. Kanchanawong, M. W. Davidson, R. D. Fetter, and H. F. Hess, “Interferometric fluorescent super-resolution microscopy resolves 3D cellular ultrastructure,” Proc. Nat. Acad. Sci. U.S.A. 106(9), 3125–3130 (2009).
[CrossRef]

H. Shroff, C. G. Galbraith, J. A. Galbraith, H. White, J. Gillette, S. Olenych, M. W. Davidson, and E. Betzig, “Dual-color superresolution imaging of genetically expressed probes within individual adhesion complexes,” Proc. Nat. Acad. Sci. U.S.A. 104(51), 20308–20313 (2007).
[CrossRef]

Ganesan, P. V.

P. V. Ganesan and S. G. Boxer, “A membrane interferometer,” Proc. Nat. Acad. Sci. U.S.A. 106(14), 5627–5632 (2009).
[CrossRef]

Garcia-Mata, R.

A. D. Dubash, M. M. Menold, T. Samson, E. Boulter, R. Garcia-Mata, R. Doughman, and K. Burridge, “Focal adhesions: new angles on an old structure,” Int. Rev. Cell Mol. Biol. 277, 1–65 (2009).
[CrossRef] [PubMed]

Gauglitz, G.

G. Gauglitz and G. Proll, “Strategies for label-free optical detection,” Adv. Biochem. Eng. Biotech. 109, 395–432 (2008).

Geiger, B.

H. Wolfenson, Y. I. Henis, B. Geiger, and A. D. Bershadsky, “The heel and toe of the cells foot: a multifaceted approach for understanding the structure and dynamics of focal adhesions,” Cell Motil. Cytoskeleton. 66(11), 1017–1029 (2009).
[CrossRef] [PubMed]

B. Geiger, J. P. Spatz, and A. D. Bershadsky, “Environmental sensing through focal adhesions,” Nat. Rev. Mol. Cell Biol. 10(1), 21–33 (2009).
[CrossRef] [PubMed]

Gillette, J.

H. Shroff, C. G. Galbraith, J. A. Galbraith, H. White, J. Gillette, S. Olenych, M. W. Davidson, and E. Betzig, “Dual-color superresolution imaging of genetically expressed probes within individual adhesion complexes,” Proc. Nat. Acad. Sci. U.S.A. 104(51), 20308–20313 (2007).
[CrossRef]

Gillette, J. M.

G. Shtengel, J. A. Galbraith, C. G. Galbraith, J. Lippincott-Schwartz, J. M. Gillette, S. Manley, R. Sougrat, C. M. Waterman, P. Kanchanawong, M. W. Davidson, R. D. Fetter, and H. F. Hess, “Interferometric fluorescent super-resolution microscopy resolves 3D cellular ultrastructure,” Proc. Nat. Acad. Sci. U.S.A. 106(9), 3125–3130 (2009).
[CrossRef]

Gillette, M. U.

Gingell, D.

J. Bailey and D. Gingell, “Contacts of chick fibroblasts on glass: results and limitations of quantitative interferometry,” J. Cell Sci. 90(2), 215–224 (1988).
[PubMed]

Goennenwein, S.

A. S. Smith, K. Sengupta, S. Goennenwein, U. Seifert, and E. Sackmann, “Force-induced growth of adhesion domains is controlled by receptor mobility,” Proc. Nat. Acad. Sci. U.S.A. 105, 6906–6911 (2008).
[CrossRef]

Gray, J. W.

K. Salaita, P. M. Nair, R. S. Petit, R. M. Neve, D. Das, J. W. Gray, and J. T. Groves, “Restriction of receptor movement alters cellular response: physical force sensing by EphA2,” Science 327(5971), 1380–1385 (2010).
[CrossRef] [PubMed]

Greenberg, D. P.

X. D. He, K. E. Torrance, F. X. Sillion, and D. P. Greenberg, “A comprehensive physical model for light reflection,” SIGGRAPH Comput. Graph. 25(4), 175–186 (1991).
[CrossRef]

Groves, J. T.

K. Salaita, P. M. Nair, R. S. Petit, R. M. Neve, D. Das, J. W. Gray, and J. T. Groves, “Restriction of receptor movement alters cellular response: physical force sensing by EphA2,” Science 327(5971), 1380–1385 (2010).
[CrossRef] [PubMed]

J. T. Groves, R. Parthasarathy, and M. B. Forstner, “Fluorescence imaging of membrane dynamics,” Annu. Rev. Biomed. Eng. 10, 311–338 (2008).
[CrossRef] [PubMed]

N. G. Clack and J. T. Groves, “Many-particle tracking with nanometer resolution in three dimensions by reflection interference contrast microscopy,” Langmuir 21(14), 6430–6435 (2005).
[CrossRef] [PubMed]

R. Parthasarathy and J. T. Groves, “Optical techniques for imaging membrane topography,” Cell. Biochem. Biophys. 1(3), 391–414 (2004).
[CrossRef]

Guttenberg, Z.

A. Boulbitch, Z. Guttenberg, and E. Sackmann, “Kinetics of membrane adhesion mediated by Ligand-receptor interaction studied with a biomimetic system,” Biophys. J. 81, 2743–2751 (2007).
[CrossRef]

Hanson, D. A.

S. K. Mitra, D. A. Hanson, and D. D. Schlaepfer, “Focal adhesion kinase: in command and control of cell motility,” Nat. Rev. Mol. Cell Biol. 6(1), 56–68 (2005).
[CrossRef] [PubMed]

Hari, C. G

G. Shroff, C. G Hari, and E. Betzig, “Live-cell photoactivated localization microscopy of nanoscale adhesion dynamics,” Nat. Meth. 5, 417–423 (2008).
[CrossRef]

Hariharan, P.

He, X. D.

X. D. He, K. E. Torrance, F. X. Sillion, and D. P. Greenberg, “A comprehensive physical model for light reflection,” SIGGRAPH Comput. Graph. 25(4), 175–186 (1991).
[CrossRef]

Henis, Y. I.

H. Wolfenson, Y. I. Henis, B. Geiger, and A. D. Bershadsky, “The heel and toe of the cells foot: a multifaceted approach for understanding the structure and dynamics of focal adhesions,” Cell Motil. Cytoskeleton. 66(11), 1017–1029 (2009).
[CrossRef] [PubMed]

Hess, H. F.

P. Kanchanawong, G. Shtengel, A. M. G. Pasapera, E. B Ramko, M. W. Davidson, H. F. Hess, and C. M. Waterman, “Nanoscale architecture of integrin-based cell adhesions,” Nature 468(7323), 580–584 (2010).
[CrossRef] [PubMed]

G. Shtengel, J. A. Galbraith, C. G. Galbraith, J. Lippincott-Schwartz, J. M. Gillette, S. Manley, R. Sougrat, C. M. Waterman, P. Kanchanawong, M. W. Davidson, R. D. Fetter, and H. F. Hess, “Interferometric fluorescent super-resolution microscopy resolves 3D cellular ultrastructure,” Proc. Nat. Acad. Sci. U.S.A. 106(9), 3125–3130 (2009).
[CrossRef]

E. Betzig, G. H. Patterson, R. Sougrat, O. W. Lindwasser, S. Olenych, J. S. Bonifacino, M. W. Davidson, J. Lippincott-Schwartz, and H. F. Hess, “Imaging intracellular fluorescent proteins at nanometer resolution,” Science 313(5793), 1642–1645 (2006).
[CrossRef] [PubMed]

Hess, S. T.

S. T. Hess and W. W. Webb, “Focal volume optics and experimental artifacts in confocal fluorescence correlation spectroscopy,” Biophys. J. 83(4), 2300–2317 (2002).
[CrossRef] [PubMed]

Hu, X.H.

X. Ma, J.Q. Lu, R. S. Brock, K. M. Jacobs, and X.H. Hu, “Determination of complex refractive index of polystyrene microspheres from 370 to 1610 nm,” Phys. Med. Biol. 48(24), 4165–4172 (2003).
[CrossRef]

Huttelmaier, S.

W. Wang, J. B. Wycko, V. C. Frohlich, Y. Oleynikov, S. Huttelmaier, J. Zavadil, L. Cermak, E. P. Bottinger, R. H. Singer, J. G. White, J. E. Segall, and J. S. Condeelis, “Single cell behavior in metastatic primary mammary tumors correlated with gene expression patterns revealed by molecular profiling,” Cancer Res. 62, 6278–6288 (2002).
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Figures (7)

Fig. 1
Fig. 1

Schematic diagram of experimental configuration of the laser feedback interference microscope. Linearly polarized light from a low power continuous-wave helium-neon laser passes through a broadband electro-optic phase-modulator and is subsequently expanded so that the TEM00 mode fills the back aperture of a high numerical microscope objective. The modulated intensity due to laser feedback of light from the sample is monitored with a photodetector at the back mirror. A single computer controls the phase shifts to the modulator, reads the photodetector signal and controls the piezoelectric stage that moves the sample.

Fig. 2
Fig. 2

Effect of defocus on visibility of the interference fringes from a coverslip-buffer interface. (a) Change in the measured visibility, m, (dotted lines) as the coverslip-buffer interface was translated by Δz; solid line is based upon a solution to the forward problem (Eq. (6)). (b) Position of the interface, Δzm = λγ/(4π n), as a function of defocus (dotted); solid line is based upon Eq. (7). (c) Difference between measured and predicted phase, Δγ = γ – (4π n/λz, near focus (dotted). Plot of ΔγG = – tan−1(2Δz/zo ) (solid black line) where zo = 0.3μm. Predicted variation (solid red line) on the basis of Eq. (7) with θ = (4π n/λz – tan−1(2Δz/zo ) + π.

Fig. 3
Fig. 3

Imaging geometry when scanning a sphere. When the scan position is directly beneath the center of the sphere, light is reflected from a tangent plane that is parallel to the plane of the coverslip-buffer interface, consequently the optical path will be parallel to the optical (z) axis. As the scan position moves outward from the center of the sphere, the optical path can be determined by tracing the path of the ray from the microscope objective that intersects the sphere normal to the tangent plane and reflects back into the objective. Therefore, the optical path, δ = OPL/(2n), at the scan position, x and the perpendicular distance, h, from the interface (at x′) to the tangent plane.

Fig. 4
Fig. 4

(A) Visibility of the fringes from the surface of a 7.7μm radius polystyrene sphere in water. (B) Fringe visibility and (C) phase from a single row of pixels; the analytical fits (solid lines) are based upon analysis of the forward problem and dotted lines are experiment.

Fig. 5
Fig. 5

Inverse method used to determine the visibility and height of the surface of a sphere above an interface. (A & B) visibility and (C) δ (black squares) and height (red squares) as a function of the virtual scan position, x′ (h = h(x′)). The fit to δ (black line) and predicted height of sphere, h = h(x′) (red line) is also shown based upon a sphere with radius R = 7.7μm and ho = 0.005μm above the interface. Fit to visibility using Eq. (8) (solid line in B).

Fig. 6
Fig. 6

Fluorescence and interference images obtained near the ventral plasma membrane of fixed cells. (A) Immunofluorescence image showing F-actin localization near the periphery of the cell. (scale bar: 5μm). (B) Immunofluorescence image of the density of paxillin. (C) Fringe visibility and (D) height of the reflective features above the coverslip-buffer interface at discrete scan points that cover the same region as the fluorescence images calculated using the inverse method (Eqs. (8) and (9)). The height, z, was determined from the phase, θ, as: z = f λ 4 π n b θ with λ = 0.6328 μm, nb = 1.333 and f = 1.2. Using this method, the height map represents the distance above the coverslip.

Fig. 7
Fig. 7

Visibility and topography reconstructed for a live cell using the inverse method. The cell may be observed to be moving towards the south-east (lower-right) of the image. Top row: six scans of the visibility. Bottom row: six scans of the topography. Each of the scans contains 60 x 40 pixels and was acquired in approximately 25 seconds. The temporal separation between scans was about 6 minutes and the total time elapsed time was approximately 40 minutes.

Equations (14)

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

I i ( x ) = I o ( x ) { 1 + V ( x ) cos ( Φ ( x ) + ψ i ) }
V = 3 ( [ 2 ( I 2 I 4 ) ] 2 + [ 2 I 3 ( I 1 + I 5 ) ] 2 ) 1 / 2 2 ( I 1 + I 2 + 2 I 3 + I 4 + I 5 )
Φ = tan 1 ( 2 ( I 2 I 4 ) 2 I 3 ( I 1 + I 5 ) )
I i = I o { 1 + A cos ( φ + ψ i ) + B cos ( φ + θ + ψ i ) }
I i = I o { 1 + m cos ( γ + ψ i ) }
m = A 2 + B 2 + 2 A B cos ( θ )
γ = tan 1 ( B sin ( θ ) A + B cos ( θ ) ) + φ
B = m 2 + A 2 2 m A cos ( γ φ )
θ = tan 1 ( m sin ( γ φ ) m cos ( γ φ ) A ) .
ϑ = tan 1 ( x R + h o ) .
δ = ( R + h o ) 2 + x 2 R .
θ = 2 π λ OPL + π .
h = δ cos ( ϑ ) ,
x ' = x δ sin ( ϑ ) ,

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