Abstract

Single-particle tracking (SPT) is a powerful approach to investigate dynamics without ensemble average. Continuing effort has been made to track smaller particles with better spatial precision at higher speed. In this work, we demonstrate SPT of 20 nm gold nanoparticle (GNP) with 2 nm spatial precision up to 500 kHz by using microsecond interferometric scattering (μs-iSCAT) microscopy. The linear scattering signal from single GNPs is detected by a high-speed CMOS camera via interference. Through this homodyne detection, shot-noise limited sensitivity, and therefore optimal localization precision are achieved at high speed where considerable electronic noise is present. Using μs-iSCAT microscopy, we observe anomalous diffusion of GNPs labeled to lipid molecules in a supported bilayer membrane prepared on a glass substrate. The combination of nanometer spatial precision and microsecond temporal resolution provides the opportunity to study rapid motions of nano-objects on molecular scale with unprecedented clarity.

© 2014 Optical Society of America

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2014

C. L. Hsieh, S. Spindler, J. Ehrig, V. Sandoghdar, “Tracking single particles on supported lipid membranes: multimobility diffusion and nanoscopic confinement,” J. Phys. Chem. B 118(6), 1545–1554 (2014).
[CrossRef] [PubMed]

2013

J. Andrecka, K. M. Spillane, J. Ortega-Arroyo, P. Kukura, “Direct observation and control of supported lipid bilayer formation with interferometric scattering microscopy,” ACS Nano 7(12), 10662–10670 (2013).
[CrossRef] [PubMed]

G. Kucsko, P. C. Maurer, N. Y. Yao, M. Kubo, H. J. Noh, P. K. Lo, H. Park, M. D. Lukin, “Nanometre-scale thermometry in a living cell,” Nature 500(7460), 54–58 (2013).
[CrossRef] [PubMed]

Y. Gu, W. Sun, G. F. Wang, M. T. Zimmermann, R. L. Jernigan, N. Fang, “Revealing rotational modes of functionalized gold nanorods on live cell membranes,” Small 9(5), 785–792 (2013).
[CrossRef] [PubMed]

W. Li, R. Liu, Y. L. Wang, Y. L. Zhao, X. Y. Gao, “Temporal techniques: dynamic tracking of nanomaterials in live cells,” Small 9(9-10), 1585–1594 (2013).
[CrossRef] [PubMed]

2012

P. Mascalchi, E. Haanappel, K. Carayon, S. Mazères, L. Salomé, “Probing the influence of the particle in Single Particle Tracking measurements of lipid diffusion,” Soft Matter 8(16), 4462–4470 (2012).
[CrossRef]

J. Ortega-Arroyo, P. Kukura, “Interferometric scattering microscopy (iSCAT): new frontiers in ultrafast and ultrasensitive optical microscopy,” Phys. Chem. Chem. Phys. 14(45), 15625–15636 (2012).
[CrossRef] [PubMed]

2011

M. J. Skaug, R. Faller, M. L. Longo, “Correlating anomalous diffusion with lipid bilayer membrane structure using single molecule tracking and atomic force microscopy,” J. Chem. Phys. 134(21), 215101 (2011).
[CrossRef] [PubMed]

R. Tero, G. Sazaki, T. Ujihara, T. Urisu, “Anomalous diffusion in supported lipid bilayers induced by oxide surface nanostructures,” Langmuir 27(16), 9662–9665 (2011).
[CrossRef] [PubMed]

M. P. Clausen, B. C. Lagerholm, “The probe rules in single particle tracking,” Curr. Protein Pept. Sci. 12(8), 699–713 (2011).
[CrossRef] [PubMed]

2010

H. Ueno, S. Nishikawa, R. Iino, K. V. Tabata, S. Sakakihara, T. Yanagida, H. Noji, “Simple dark-field microscopy with nanometer spatial precision and microsecond temporal resolution,” Biophys. J. 98(9), 2014–2023 (2010).
[CrossRef] [PubMed]

S. T. Wereley, C. D. Meinhart, “Recent advances in micro-particle image velocimetry,” Annu. Rev. Fluid Mech. 42(1), 557–576 (2010).
[CrossRef]

X. Michalet, “Mean square displacement analysis of single-particle trajectories with localization error: Brownian motion in an isotropic medium,” Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 82(4), 041914 (2010).
[CrossRef] [PubMed]

K. Simons, M. J. Gerl, “Revitalizing membrane rafts: new tools and insights,” Nat. Rev. Mol. Cell Biol. 11(10), 688–699 (2010).
[CrossRef] [PubMed]

M. Krishnan, N. Mojarad, P. Kukura, V. Sandoghdar, “Geometry-induced electrostatic trapping of nanometric objects in a fluid,” Nature 467(7316), 692–695 (2010).
[CrossRef] [PubMed]

2009

P. Kukura, H. Ewers, C. Müller, A. Renn, A. Helenius, V. Sandoghdar, “High-speed nanoscopic tracking of the position and orientation of a single virus,” Nat. Methods 6(12), 923–927 (2009).
[CrossRef] [PubMed]

2008

X. L. Nan, P. A. Sims, X. S. Xie, “Organelle tracking in a living cell with microsecond time resolution and nanometer spatial precision,” ChemPhysChem 9(5), 707–712 (2008).
[CrossRef] [PubMed]

H. M. van der Schaar, M. J. Rust, C. Chen, H. van der Ende-Metselaar, J. Wilschut, X. Zhuang, J. M. Smit, “Dissecting the cell entry pathway of dengue virus by single-particle tracking in living cells,” PLoS Pathog. 4(12), e1000244 (2008).
[CrossRef] [PubMed]

2007

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

2006

D. Lasne, G. A. Blab, S. Berciaud, M. Heine, L. Groc, D. Choquet, L. Cognet, B. Lounis, “Single nanoparticle photothermal tracking (SNaPT) of 5-nm gold beads in live cells,” Biophys. J. 91(12), 4598–4604 (2006).
[CrossRef] [PubMed]

V. Jacobsen, P. Stoller, C. Brunner, V. Vogel, V. Sandoghdar, “Interferometric optical detection and tracking of very small gold nanoparticles at a water-glass interface,” Opt. Express 14(1), 405–414 (2006).
[CrossRef] [PubMed]

P. K. Jain, K. S. Lee, I. H. El-Sayed, M. A. El-Sayed, “Calculated absorption and scattering properties of gold nanoparticles of different size, shape, and composition: applications in biological imaging and biomedicine,” J. Phys. Chem. B 110(14), 7238–7248 (2006).
[CrossRef] [PubMed]

M. A. van Dijk, A. L. Tchebotareva, M. Orrit, M. Lippitz, S. Berciaud, D. Lasne, L. Cognet, B. Lounis, “Absorption and scattering microscopy of single metal nanoparticles,” Phys. Chem. Chem. Phys. 8(30), 3486–3495 (2006).
[CrossRef] [PubMed]

2005

A. Kusumi, C. Nakada, K. Ritchie, K. Murase, K. Suzuki, H. Murakoshi, R. S. Kasai, J. Kondo, T. Fujiwara, “Paradigm shift of the plasma membrane concept from the two-dimensional continuum fluid to the partitioned fluid: high-speed single-molecule tracking of membrane molecules,” Annu. Rev. Biophys. Biomol. Struct. 34, 351–378 (2005).
[CrossRef] [PubMed]

2004

K. Lindfors, T. Kalkbrenner, P. Stoller, V. Sandoghdar, “Detection and spectroscopy of gold nanoparticles using supercontinuum white light confocal microscopy,” Phys. Rev. Lett. 93(3), 037401 (2004).
[CrossRef] [PubMed]

2002

R. E. Thompson, D. R. Larson, W. W. Webb, “Precise nanometer localization analysis for individual fluorescent probes,” Biophys. J. 82(5), 2775–2783 (2002).
[CrossRef] [PubMed]

D. S. Martin, M. B. Forstner, J. A. Käs, “Apparent subdiffusion inherent to single particle tracking,” Biophys. J. 83(4), 2109–2117 (2002).
[CrossRef] [PubMed]

1997

M. J. Saxton, K. Jacobson, “Single-particle tracking: applications to membrane dynamics,” Annu. Rev. Biophys. Biomol. Struct. 26(1), 373–399 (1997).
[CrossRef] [PubMed]

1991

H. Qian, M. P. Sheetz, E. L. Elson, “Single particle tracking. Analysis of diffusion and flow in two-dimensional systems,” Biophys. J. 60(4), 910–921 (1991).
[CrossRef] [PubMed]

1986

N. Bobroff, “Position measurement with a resolution and noise-limited instrument,” Rev. Sci. Instrum. 57(6), 1152–1157 (1986).
[CrossRef]

1985

M. De Brabander, G. Geuens, R. Nuydens, M. Moeremans, J. De Mey, “Probing microtubule-dependent intracellular motility with nanometre particle video ultramicroscopy (nanovid ultramicroscopy),” Cytobios 43(174S), 273–283 (1985).
[PubMed]

1984

A. A. Brian, H. M. McConnell, “Allogeneic stimulation of cytotoxic T cells by supported planar membranes,” Proc. Natl. Acad. Sci. U.S.A. 81(19), 6159–6163 (1984).
[CrossRef] [PubMed]

1983

M. P. Sheetz, J. A. Spudich, “Movement of myosin-coated fluorescent beads on actin cables in vitro,” Nature 303(5912), 31–35 (1983).
[CrossRef] [PubMed]

1979

1975

C. H. Chan, “Effective absorption for thermal blooming due to aerosols,” Appl. Phys. Lett. 26(11), 628–630 (1975).
[CrossRef]

Andrecka, J.

J. Andrecka, K. M. Spillane, J. Ortega-Arroyo, P. Kukura, “Direct observation and control of supported lipid bilayer formation with interferometric scattering microscopy,” ACS Nano 7(12), 10662–10670 (2013).
[CrossRef] [PubMed]

Berciaud, S.

D. Lasne, G. A. Blab, S. Berciaud, M. Heine, L. Groc, D. Choquet, L. Cognet, B. Lounis, “Single nanoparticle photothermal tracking (SNaPT) of 5-nm gold beads in live cells,” Biophys. J. 91(12), 4598–4604 (2006).
[CrossRef] [PubMed]

M. A. van Dijk, A. L. Tchebotareva, M. Orrit, M. Lippitz, S. Berciaud, D. Lasne, L. Cognet, B. Lounis, “Absorption and scattering microscopy of single metal nanoparticles,” Phys. Chem. Chem. Phys. 8(30), 3486–3495 (2006).
[CrossRef] [PubMed]

Blab, G. A.

D. Lasne, G. A. Blab, S. Berciaud, M. Heine, L. Groc, D. Choquet, L. Cognet, B. Lounis, “Single nanoparticle photothermal tracking (SNaPT) of 5-nm gold beads in live cells,” Biophys. J. 91(12), 4598–4604 (2006).
[CrossRef] [PubMed]

Bobroff, N.

N. Bobroff, “Position measurement with a resolution and noise-limited instrument,” Rev. Sci. Instrum. 57(6), 1152–1157 (1986).
[CrossRef]

Brian, A. A.

A. A. Brian, H. M. McConnell, “Allogeneic stimulation of cytotoxic T cells by supported planar membranes,” Proc. Natl. Acad. Sci. U.S.A. 81(19), 6159–6163 (1984).
[CrossRef] [PubMed]

Brunner, C.

Carayon, K.

P. Mascalchi, E. Haanappel, K. Carayon, S. Mazères, L. Salomé, “Probing the influence of the particle in Single Particle Tracking measurements of lipid diffusion,” Soft Matter 8(16), 4462–4470 (2012).
[CrossRef]

Chan, C. H.

C. H. Chan, “Effective absorption for thermal blooming due to aerosols,” Appl. Phys. Lett. 26(11), 628–630 (1975).
[CrossRef]

Chen, C.

H. M. van der Schaar, M. J. Rust, C. Chen, H. van der Ende-Metselaar, J. Wilschut, X. Zhuang, J. M. Smit, “Dissecting the cell entry pathway of dengue virus by single-particle tracking in living cells,” PLoS Pathog. 4(12), e1000244 (2008).
[CrossRef] [PubMed]

Choquet, D.

D. Lasne, G. A. Blab, S. Berciaud, M. Heine, L. Groc, D. Choquet, L. Cognet, B. Lounis, “Single nanoparticle photothermal tracking (SNaPT) of 5-nm gold beads in live cells,” Biophys. J. 91(12), 4598–4604 (2006).
[CrossRef] [PubMed]

Clausen, M. P.

M. P. Clausen, B. C. Lagerholm, “The probe rules in single particle tracking,” Curr. Protein Pept. Sci. 12(8), 699–713 (2011).
[CrossRef] [PubMed]

Cognet, L.

M. A. van Dijk, A. L. Tchebotareva, M. Orrit, M. Lippitz, S. Berciaud, D. Lasne, L. Cognet, B. Lounis, “Absorption and scattering microscopy of single metal nanoparticles,” Phys. Chem. Chem. Phys. 8(30), 3486–3495 (2006).
[CrossRef] [PubMed]

D. Lasne, G. A. Blab, S. Berciaud, M. Heine, L. Groc, D. Choquet, L. Cognet, B. Lounis, “Single nanoparticle photothermal tracking (SNaPT) of 5-nm gold beads in live cells,” Biophys. J. 91(12), 4598–4604 (2006).
[CrossRef] [PubMed]

De Brabander, M.

M. De Brabander, G. Geuens, R. Nuydens, M. Moeremans, J. De Mey, “Probing microtubule-dependent intracellular motility with nanometre particle video ultramicroscopy (nanovid ultramicroscopy),” Cytobios 43(174S), 273–283 (1985).
[PubMed]

De Mey, J.

M. De Brabander, G. Geuens, R. Nuydens, M. Moeremans, J. De Mey, “Probing microtubule-dependent intracellular motility with nanometre particle video ultramicroscopy (nanovid ultramicroscopy),” Cytobios 43(174S), 273–283 (1985).
[PubMed]

Ehrig, J.

C. L. Hsieh, S. Spindler, J. Ehrig, V. Sandoghdar, “Tracking single particles on supported lipid membranes: multimobility diffusion and nanoscopic confinement,” J. Phys. Chem. B 118(6), 1545–1554 (2014).
[CrossRef] [PubMed]

El-Sayed, I. H.

P. K. Jain, K. S. Lee, I. H. El-Sayed, M. A. El-Sayed, “Calculated absorption and scattering properties of gold nanoparticles of different size, shape, and composition: applications in biological imaging and biomedicine,” J. Phys. Chem. B 110(14), 7238–7248 (2006).
[CrossRef] [PubMed]

El-Sayed, M. A.

P. K. Jain, K. S. Lee, I. H. El-Sayed, M. A. El-Sayed, “Calculated absorption and scattering properties of gold nanoparticles of different size, shape, and composition: applications in biological imaging and biomedicine,” J. Phys. Chem. B 110(14), 7238–7248 (2006).
[CrossRef] [PubMed]

Elson, E. L.

H. Qian, M. P. Sheetz, E. L. Elson, “Single particle tracking. Analysis of diffusion and flow in two-dimensional systems,” Biophys. J. 60(4), 910–921 (1991).
[CrossRef] [PubMed]

Ewers, H.

P. Kukura, H. Ewers, C. Müller, A. Renn, A. Helenius, V. Sandoghdar, “High-speed nanoscopic tracking of the position and orientation of a single virus,” Nat. Methods 6(12), 923–927 (2009).
[CrossRef] [PubMed]

Faller, R.

M. J. Skaug, R. Faller, M. L. Longo, “Correlating anomalous diffusion with lipid bilayer membrane structure using single molecule tracking and atomic force microscopy,” J. Chem. Phys. 134(21), 215101 (2011).
[CrossRef] [PubMed]

Fang, N.

Y. Gu, W. Sun, G. F. Wang, M. T. Zimmermann, R. L. Jernigan, N. Fang, “Revealing rotational modes of functionalized gold nanorods on live cell membranes,” Small 9(5), 785–792 (2013).
[CrossRef] [PubMed]

Forstner, M. B.

D. S. Martin, M. B. Forstner, J. A. Käs, “Apparent subdiffusion inherent to single particle tracking,” Biophys. J. 83(4), 2109–2117 (2002).
[CrossRef] [PubMed]

Fujiwara, T.

A. Kusumi, C. Nakada, K. Ritchie, K. Murase, K. Suzuki, H. Murakoshi, R. S. Kasai, J. Kondo, T. Fujiwara, “Paradigm shift of the plasma membrane concept from the two-dimensional continuum fluid to the partitioned fluid: high-speed single-molecule tracking of membrane molecules,” Annu. Rev. Biophys. Biomol. Struct. 34, 351–378 (2005).
[CrossRef] [PubMed]

Gao, X. Y.

W. Li, R. Liu, Y. L. Wang, Y. L. Zhao, X. Y. Gao, “Temporal techniques: dynamic tracking of nanomaterials in live cells,” Small 9(9-10), 1585–1594 (2013).
[CrossRef] [PubMed]

Gerl, M. J.

K. Simons, M. J. Gerl, “Revitalizing membrane rafts: new tools and insights,” Nat. Rev. Mol. Cell Biol. 11(10), 688–699 (2010).
[CrossRef] [PubMed]

Geuens, G.

M. De Brabander, G. Geuens, R. Nuydens, M. Moeremans, J. De Mey, “Probing microtubule-dependent intracellular motility with nanometre particle video ultramicroscopy (nanovid ultramicroscopy),” Cytobios 43(174S), 273–283 (1985).
[PubMed]

Groc, L.

D. Lasne, G. A. Blab, S. Berciaud, M. Heine, L. Groc, D. Choquet, L. Cognet, B. Lounis, “Single nanoparticle photothermal tracking (SNaPT) of 5-nm gold beads in live cells,” Biophys. J. 91(12), 4598–4604 (2006).
[CrossRef] [PubMed]

Gu, Y.

Y. Gu, W. Sun, G. F. Wang, M. T. Zimmermann, R. L. Jernigan, N. Fang, “Revealing rotational modes of functionalized gold nanorods on live cell membranes,” Small 9(5), 785–792 (2013).
[CrossRef] [PubMed]

Haanappel, E.

P. Mascalchi, E. Haanappel, K. Carayon, S. Mazères, L. Salomé, “Probing the influence of the particle in Single Particle Tracking measurements of lipid diffusion,” Soft Matter 8(16), 4462–4470 (2012).
[CrossRef]

Heine, M.

D. Lasne, G. A. Blab, S. Berciaud, M. Heine, L. Groc, D. Choquet, L. Cognet, B. Lounis, “Single nanoparticle photothermal tracking (SNaPT) of 5-nm gold beads in live cells,” Biophys. J. 91(12), 4598–4604 (2006).
[CrossRef] [PubMed]

Helenius, A.

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C. L. Hsieh, S. Spindler, J. Ehrig, V. Sandoghdar, “Tracking single particles on supported lipid membranes: multimobility diffusion and nanoscopic confinement,” J. Phys. Chem. B 118(6), 1545–1554 (2014).
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Wang, G. F.

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Figures (7)

Fig. 1
Fig. 1

Schematics of the experimental setup. AOD1 and AOD2: acoustic optical deflectors for beam scanning in two directions; L1: wide-field lens (f1 = 20 cm) focusing laser beam at the back focal plane of the objective lens; BS: 50:50 non-polarizing beamsplitter; OBJ: 100x oil-immersion objective (NA 1.4); L2: camera lens (f2 = 75 cm), placed at a position such that its front focal plane coincides with the back focal plane of the OBJ; M1 and M2: mirrors. The CMOS camera records the iSCAT image formed via interference between the backscattered light from GNPs and the reflection from the glass-water interface (see inset and text for details).

Fig. 2
Fig. 2

(a) iSCAT image of 20 nm GNPs randomly deposited on a coverslip embedded in water. (b) Normalized intensity line profile of a selected particle shown in (a). Squares are the measured data, and the red curve is the corresponding Gaussian fit. (c) Histogram of the amplitude of the normalized intensity measured from 115 particles. The mean amplitude of the normalized intensity is 0.13, and the standard deviation is 0.04.

Fig. 3
Fig. 3

Noise amplitude ( σ det ) measured at different illumination intensities. The experimental data are shown as dots. The red solid curve shows the theoretical noise amplitude considering the camera noise and the photon noise. The cyan dashed line shows the noise fluctuation only due to the photon noise. It is clear that the measured noise is dominated by the shot noise of photon at high intensities.

Fig. 4
Fig. 4

(a) iSCAT image of a 20 nm GNP deposited on a coverslip embedded in water acquired at 500 kHz. (b) Histogram of localization precision of the GNP displayed in (a). The average localization precision is 2.01 nm, and the standard deviation is 0.24 nm.

Fig. 5
Fig. 5

(a) Localization precision and (b) normalized intensity of a 20 nm GNP measured at various acquisition rates. In (a) and (b), squares are the average values and error bars are the standard deviations of the measurements of 1,000 images. The localization precision and the normalized intensity show no dependency on the acquisition rate. The small variation in the values measured at different acquisition rates is thought to be due to the slight difference in the axial position of the sample, leading to small changes in the spot size and the contrast of the point-spread functions.

Fig. 6
Fig. 6

(a) Schematics of a GNP labeled to biotinylated lipid molecules in a supported bilayer membrane. (b) Snapshot of iSCAT image of a 20 nm GNP diffusing on the membrane. (c) Diffusion trajectory of a GNP labeled to biotin-cap-DPPE in DOPC membrane, recorded at 100,000 fps for 1 second. Inset: close-up view revealing details of the diffusion trajectory. (d) Measured MSD data of the trajectory displayed in (c) (shown as squares) and the corresponding fit with a model of anomalous diffusion (red curve). The blue line connects the first two MSD data points and extrapolates for longer time delays, which illustrates the nonlinear dependency of the measured MSD data with respect to time delays. (e) Measured diffusion rate as a function of time delay. The diffusion rate of the GNP remains constant at long timescale (> 150 μs) and starts to show a gradual increase at short timescale (< 150 μs), which is a typical diffusion characteristic of anomalous diffusion.

Fig. 7
Fig. 7

(a) Raw iSCAT image of a 20 nm GNP. (b) Background image (see text for details). (c) Background corrected image from (a).

Equations (5)

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σ det = σ camera 2 + σ laser 2 + σ photon 2 .
N det = N r + N s +2 N r N s cosθ
SNR= 2 N r N s / σ det 2 N r N s / σ photon = 2 N r N s / N r =2 N s ,
MSD( Δt )=4 D α Δ t α + ε off
MSD( Δt )=4D( Δt )Δt+ ε off

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