Abstract

Single plane illumination microscopy based fluorescence correlation spectroscopy (SPIM-FCS) is a new method for imaging FCS in 3D samples, providing diffusion coefficients, flow velocities and concentrations in an imaging mode. Here we extend this technique to two-color fluorescence cross-correlation spectroscopy (SPIM-FCCS), which allows to measure molecular interactions in an imaging mode. We present a theoretical framework for SPIM-FCCS fitting models, which is subsequently used to evaluate several test measurements of in-vitro (labeled microspheres, several DNAs and small unilamellar vesicles) and in-vivo samples (dimeric and monomeric dual-color fluorescent proteins, as well as membrane bound proteins). Our method yields the same quantitative results as the well-established confocal FCCS, but in addition provides unmatched statistics and true imaging capabilities.

© 2014 Optical Society of America

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2013 (4)

M. Kloster-Landsberg, D. Tyndall, I. Wang, R. Walker, J. Richardson, R. Henderson, A. Delon, “Note: Multi-confocal fluorescence correlation spectroscopy in living cells using a complementary metal oxide semiconductor-single photon avalanche diode array,” Rev. Sci. Instrum. 84, 076105 (2013).
[CrossRef] [PubMed]

A. P. Singh, J. W. Krieger, J. Buchholz, E. Charbon, J. Langowski, T. Wohland, “The performance of 2D array detectors for light sheet based fluorescence correlation spectroscopy,” Opt. Express 21, 8652–8668 (2013).
[CrossRef] [PubMed]

J. Sankaran, N. Bag, R. S. Kraut, T. Wohland, “Accuracy and precision in camera-based fluorescence correlation spectroscopy measurements,” Anal. Chem. 85, 3948–3954 (2013).
[CrossRef] [PubMed]

S. Talwar, A. Kumar, M. Rao, G. I. Menon, G. V. Shivashankar, “Correlated spatio-temporal fluctuations in chromatin compaction states characterize stem cells.” Biophys. J. 104, 553–564 (2013).
[CrossRef] [PubMed]

2012 (6)

N. Bag, J. Sankaran, A. Paul, R. S. Kraut, T. Wohland, “Calibration and limits of camera-based fluorescence correlation spectroscopy: A supported lipid bilayer study,” ChemPhysChem 13, 2784–2794 (2012).
[CrossRef] [PubMed]

J. Buchholz, J. W. Krieger, G. Mocsár, B. Kreith, E. Charbon, G. Vámosi, U. Kebschull, J. Langowski, “Fpga implementation of a 32×32 autocorrelator array for analysis of fast image series,” Opt. Express 20, 17767–17782 (2012).
[CrossRef] [PubMed]

Y. H. Foo, N. Naredi-Rainer, D. C. Lamb, S. Ahmed, T. Wohland, “Factors affecting the quantification of biomolecular interactions by fluorescence cross-correlation spectroscopy,” Biophys. J. 102, 1174–1183 (2012).
[CrossRef] [PubMed]

V. Betaneli, E. P. Petrov, P. Schwille, “The role of lipids in VDAC oligomerization,” Biophys. J. 102, 523–531 (2012).
[CrossRef] [PubMed]

T. Toplak, E. Pandzic, L. Chen, M. Vicente-Manzanares, A. R. Horwitz, P. W. Wiseman, “STICCS reveals matrix-dependent adhesion slipping and gripping in migrating cells,” Biophys. J. 103, 1672–1682 (2012).
[CrossRef] [PubMed]

D. M. Shcherbakova, M. A. Hink, L. Joosen, T. W. J. Gadella, V. V. Verkhusha, “An orange fluorescent protein with a large stokes shift for single-excitation multicolor FCCS and FRET imaging,” J. Am. Chem. Soc. 134, 7913–7923 (2012).
[CrossRef]

2011 (1)

J. Capoulade, M. Wachsmuth, L. Hufnagel, M. Knop, “Quantitative fluorescence imaging of protein diffusion and interaction in living cells,” Nat. Biotechnol. 29, 835—839 (2011).
[CrossRef] [PubMed]

2010 (6)

R. A. Colyer, G. Scalia, I. Rech, A. Gulinatti, M. Ghioni, S. Cova, S. Weiss, X. Michalet, “High-throughput FCS using an LCOS spatial light modulator and an 8×1 spad array,” Biomed. Opt. Express 1, 1408–1431 (2010).
[CrossRef]

T. Wohland, X. Shi, J. Sankaran, E. H. K. Stelzer, “Single plane illumination fluorescence correlation spectroscopy (SPIM-FCS) probes inhomogeneous three-dimensional environments,” Opt. Express 10, 10627–10641 (2010).
[CrossRef]

J. Sankaran, X. Shi, L. Ho, E. Stelzer, T. Wohland, “ImFCS: A software for imaging FCS data analysis and visualization,” Opt. Express 18, 25468–25481 (2010). Available at http://staff.science.nus.edu.sg/~chmwt/resources/imfcs_software.html .
[CrossRef]

J. Ries, Z. Petrášek, A. J. García-Sáez, P. Schwille, “A comprehensive framework for fluorescence cross-correlation spectroscopy,” New J. Phys. 12, 113009 (2010).
[CrossRef]

F. Bestvater, Z. Seghiri, M. S. Kang, N. Gröner, J. Y. Lee, I. Kang-Bin, M. Wachsmuth, “EMCCD-based spectrally resolved fluorescence correlation spectroscopy,” Opt. Express 18, 23818–23828 (2010).
[CrossRef]

A. Edelstein, N. Amodaj, K. Hoover, R. Vale, N. Stuurman, “Computer control of microscopes using μManager,” Curr. Protoc. Mol. Biol. 14, 1–14 (2010).

2009 (7)

T. Wocjan, J. Krieger, O. Krichevsky, J. Langowski, “Dynamics of a fluorophore attached to superhelical DNA: Fcs experiments simulated by brownian dynamics,” Phys. Chem. Chem. Phys. 11, 10671–10681 (2009).
[CrossRef]

J. Roszik, D. Lisboa, J. Szöllősi, G. Vereb, “Evaluation of intensity-based ratiometric FRET in image cytometry—approaches and a software solution,” Cytometry A 75A, 761–767 (2009).
[CrossRef]

N. Dross, C. Spriet, M. Zwerger, G. Müller, W. Waldeck, J. Langowski, “Mapping eGFP oligomer mobility in living cell nuclei,” PLoS ONE 4, e5041 (2009).
[CrossRef]

J. Ries, S. Chiantia, P. Schwille, “Accurate determination of membrane dynamics with line-scan FCS,” Biophys. J. 96, 1999–2008 (2009).
[CrossRef] [PubMed]

G. Heuvelman, F. Erdel, M. Wachsmuth, K. Rippe, “Analysis of protein mobilities and interactions in living cells by multifocal fluorescence fluctuation microscopy,” Eur. Biophys. J. 38, 813–828 (2009).
[CrossRef] [PubMed]

D. J. Needleman, Y. Xu, T. J. Mitchison, “Pin-hole array correlation imaging: Highly parallel fluorescence correlation spectroscopy,” Biophys. J. 96, 5050–5059 (2009).
[CrossRef] [PubMed]

M. A. Digman, P. W. Wiseman, A. R. Horwitz, E. Gratton, “Detecting protein complexes in living cells from laser scanning confocal image sequences by the cross correlation raster image spectroscopy method,” Biophys. J. 96, 707–716 (2009).
[CrossRef] [PubMed]

2008 (2)

G. Vámosi, N. Baudendistel, C.-W. von der Lieth, N. Szalóki, G. Mocsár, G. Müller, P. Brázda, W. Waldeck, S. Damjanovich, J. Langowski, K. Tóth, “Conformation of the c-Fos/c-Jun complex in vivo: A combined FRET, FCCS, and MD-modeling study,” Biophys. J. 94, 2859–2868 (2008).
[CrossRef]

J. R. Unruh, E. Gratton, “Analysis of molecular concentration and brightness from fluorescence fluctuation data with an electron multiplied ccd camera,” Biophys. J. 95, 5385–5398 (2008).
[CrossRef] [PubMed]

2007 (4)

B. Kannan, L. Guo, T. Sudhaharan, S. Ahmed, I. Maruyama, T. Wohland, “Spatially resolved total internal reflection fluorescence correlation microscopy using an electron multiplying charge-coupled device camera,” Anal. Chem. 79, 4463–4470 (2007).
[CrossRef] [PubMed]

P. Liu, T. Sudhaharan, R. M. Koh, L. C. Hwang, S. Ahmed, I. N. Maruyama, T. Wohland, “Investigation of the dimerization of proteins from the epidermal growth factor receptor family by single wavelength fluorescence cross-correlation spectroscopy,” Biophys. J. 93, 684–698 (2007).
[CrossRef] [PubMed]

K. Greger, J. Swoger, E. H. K. Stelzer, “Basic building units and properties of a fluorescence single plane illumination microscope,” Rev. Sci. Instrum. 78, 023705 (2007).
[CrossRef] [PubMed]

E. Haustein, P. Schwille, “Fluorescence correlation spectroscopy: novel variations of an established technique,” Annu. Rev. Biophys. Biomol. Struct. 36, 151–169 (2007).
[CrossRef] [PubMed]

2006 (2)

K. Bacia, S. A. Kim, P. Schwille, “Fluorescence cross-correlation spectroscopy in living cells,” Nat. Methods 3, 83–89 (2006).
[CrossRef]

L. C. Hwang, M. Gösch, T. Lasser, T. Wohland, “Simultaneous multicolor fluorescence cross-correlation spectroscopy to detect higher order molecular interactions using single wavelength laser excitation,” Biophys. J. 91, 715–727 (2006).
[CrossRef] [PubMed]

2005 (5)

L. C. Hwang, T. Wohland, “Single wavelength excitation fluorescence cross-correlation spectroscopy with spectrally similar fluorophores: Resolution for binding studies,” J. Chem. Phys. 122, 114708 (2005).
[CrossRef] [PubMed]

M. Gösch, A. Magnusson, S. Hård, H. Blom, S. Anderegg, K. Korn, P. Thyberg, M. Wells, T. Lasser, R. Rigler, “Parallel dual-color fluorescence cross-correlation spectroscopy using diffractive optical elements,” J. Biomed. Opt. 10, 054008 (2005).
[CrossRef] [PubMed]

N. Baudendistel, G. Müller, W. Waldeck, P. Angel, J. Langowski, “Two-hybrid fluorescence cross-correlation spectroscopy detects protein–protein interactions in vivo,” ChemPhysChem 6, 984–990 (2005).
[CrossRef] [PubMed]

B. K. Müller, E. Zaychikov, C. Bräuchle, D. C. Lamb, “Pulsed interleaved excitation,” Biophys. J. 89, 3508–3522 (2005).
[CrossRef] [PubMed]

A. N. Kapanidis, T. A. Laurence, N. K. Lee, E. Margeat, X. Kong, S. Weiss, “Alternating-laser excitation of single molecules,” Acc. Chem. Res. 38, 523–533 (2005).
[CrossRef] [PubMed]

2004 (2)

K. G. Heinze, M. Jahnz, P. Schwille, “Triple-color coincidence analysis: One step further in following higher order molecular complex formation,” Biophys. J. 86, 506–516 (2004).
[CrossRef]

Q. Ruan, M. A. Cheng, M. Levi, E. Gratton, W. W. Mantulin, “Spatial-temporal studies of membrane dynamics: Scanning fluorescence correlation spectroscopy (SFCS),” Biophys. J. 87, 1260–1267 (2004).
[CrossRef] [PubMed]

2003 (1)

L. A. Maguire, H. Zhang, P. A. Shamlou, “Preparation of small unilamellar vesicles (SUV) and biophysical characterization of their complexes with poly-l-lysine-condensed plasmid DNA,” Biotechnol Appl. Biochem. 37, 73–81 (2003).
[CrossRef] [PubMed]

2002 (1)

O. Krichevsky, G. Bonnet, “Fluorescence correlation spectroscopy: the technique and its applications,” Rep. Prog. Phys. 65, 251–297 (2002).
[CrossRef]

1998 (1)

U. Kettling, A. Koltermann, P. Schwille, M. Eigen, “Real-time enzyme kinetics monitored by dual-color fluorescence cross-correlation spectroscopy,” Proc. Natl. Acad. Sci. 95, 1416–1420 (1998).
[CrossRef] [PubMed]

1997 (1)

P. Schwille, F. Meyer-Almes, R. Rigler, “Dual-color fluorescence cross-correlation spectroscopy for multi-component diffusional analysis in solution,” Biophys. J. 72, 1878–1886 (1997).
[CrossRef] [PubMed]

1995 (1)

K. M. Berland, P. T. So, E. Gratton, “Two-photon fluorescence correlation spectroscopy: method and application to the intracellular environment,” Biophys. J. 68, 694–701 (1995).
[CrossRef] [PubMed]

1993 (1)

E. M. M. Manders, F. J. Verbeek, J. A. Aten, “Measurement of co-localization of objects in dual-colour confocal images,” J. Microsc. 169, 375–382 (1993).
[CrossRef]

1987 (1)

A. Corana, M. Marchesi, C. Martini, S. Ridella, “Minimizing multimodal functions of continuous variables with the ’simulated annealing’ algorithm corrigenda for this article is available here,” ACM T. Math. Software 13, 262–280 (1987).
[CrossRef]

1974 (2)

D. Magde, E. L. Elson, W. W. Webb, “Fluorescence correlation spectroscopy I: Conceptual basis and theory,” Biopolymers 13, 1–27 (1974).
[CrossRef]

D. Magde, E. L. Elson, W. W. Webb, “Fluorescence correlation spectroscopy. II. an experimental realization.” Biopolymers 13, 29–61 (1974).
[CrossRef] [PubMed]

1969 (1)

C.-H. Huang, “Phosphatidylcholine vesicles. formation and physical characteristics,” Biochemistry 8, 344–352 (1969). PMID: .
[CrossRef] [PubMed]

1963 (1)

D. W. Marquardt, “An algorithm for least-squares estimation of nonlinear parameters,” J. Soc. Ind. Appl. Math. 11, 431–441 (1963).
[CrossRef]

1944 (1)

K. Levenberg, “A method for the solution of certain nonlinear problems in least squares,” Quart. Appl. Math. 2, 164–168 (1944).

Ahmed, S.

Y. H. Foo, N. Naredi-Rainer, D. C. Lamb, S. Ahmed, T. Wohland, “Factors affecting the quantification of biomolecular interactions by fluorescence cross-correlation spectroscopy,” Biophys. J. 102, 1174–1183 (2012).
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QuickFit 3.0 can be downloaded free of charge from http://www.dkfz.de/Macromol/quickfit/ .

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Figures (7)

Fig. 1
Fig. 1

Schematic view of the SPIMs described in this article: (A) shows the detailed optical setup and (B) shows three possible sample mounting schemes: Solid samples (e.g. beads for calibration) can be embedded in a gel cylinder, liquid samples are sealed into small thermoplastic bags and adherent cells are grown onto small glass pieces.

Fig. 2
Fig. 2

FCCS data evaluation chain. The left column shows the progression from the raw input data to the statistically analyzed results. The right column gives typical numbers for the size of the dataset in each step.

Fig. 3
Fig. 3

Fit results when assuming no shift δx = 0 in the fit model, given that a shift δx > 0 actually is present in the microscope setup. (A) The graph shows the relative error, as defined by Eq. (21) at different crosstalk coefficients κκgr and focal shifts δx (color-coded green-orange or blue-red). the thick orange line marks an error level of 5% which is still acceptable. (B) depicts the simulated foci (as 1/e2-isosurfaces) at different shifts δx. The camera pixels in the object space (pixel size a = 400 nm) are shown as gray squares inside the foci.

Fig. 4
Fig. 4

Example auto- (green/red) and cross-correlation curves (blue) of FCCS standard samples: (A) TetraSpec beads [150,000 frames, 128 × 20 pixel, τmin = 0.53 ms, 3 runs], (B) 170bp dsDNA [700,000 frames, 128 × 6 pixel, τmin = 0.29 ms], (C) 40bp- dsDNA [100,000 frames, 128 × 4 pixel, 2×-binning, τmin = 0.27 ms], (D) double labeled SUV [60,000 frames, τmin = 128 × 20 pixel, τmin = 1.04 ms]. The graphs show the correlation functions of a single pixel and where available average and standard deviation over several runs. Dashed lines are fits to the data.

Fig. 5
Fig. 5

Comparison between confocal and SPIM-FCCS measurements. (A) shows the relative dimer concentration pAB and (B) the relative cross-correlation amplitude q. The black dashed line represents the ideal result (slope 1). Different mixtures of single- and double-labeled 607bp long dsDNA strands were measured on both instruments. For the SPIM, the acquisition setting were: 700,000 frames, 128 × 6 pixels, no binning (red crosses) or 2 × 2 pixel binning (green circles), τmin = 0.33 ms. Data from the confocal measurements are average and standard deviation (SD) over 7 consecutive runs (30 s each). For SPIM they are average and SD over all pixels from 3 – 4 separate experiments. Green lines in (A) represent robust regressions to the 2×-binning data.

Fig. 6
Fig. 6

SPIM-FCCS control measurement of eGFP-mRFP1-dimers and eGFP- + mRFP1-monomers expressed in HeLa cells. (A) and (B) show example correlation functions and fits for the dimer and monomer sample, horizontal dashed lines are the level of cross-correlation explained by crosstalk (C) shows histograms of the relative dimer concentration pABand of the diffusion coefficient DA = DB = DAB in two exemplary cells. (D) shows intensity (blue circles mark position of CFs in A,B), (E) shows relative concentration images (same data as in C) and (F) shows the diffusion coefficient maps. The acquisition settings were: 128 × 20 pixel, 2 × 2 binning, 1.06 ms temporal resolution, 211 s measurement duration (200,000 frames) for the each cell.

Fig. 7
Fig. 7

SPIM-FCCS control measurement of eGFP-EGFR-mRFP1 and PMT-eGFP- + PMT-mRFP1-monomers expressed in CHO cells. (A) and (B) show example correlation functions and fits for the dimer and monomer sample, horizontal dashed lines are the level of cross-correlation explained by crosstalk (C) shows histograms of the relative dimer concentration pAB, (D) shows intensity (red circles mark position of CFs in A,B), and (E) shows relative concentration images (same data as in C) The acquisition settings were: 128 × 20 pixel, 2 × 2 binning, 0.53 ms temporal resolution, 99 s measurement duration (100,000 frames) for the each cell.

Tables (1)

Tables Icon

Table 1 Summary of typical diffusion coefficients recalculated to their value D20,W at 20°C in water and of the relative cross-correlation amplitudes q (not crosstalk-corrected) obtained with different samples. The diffusion coefficients of single dyes (Alexa-488, eGFP etc.), as typically measured in SPIM-FCS, are given for comparison.

Equations (21)

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g γ ρ ( τ ; r ) = I γ ( t ; r ) I ρ ( t + τ ; r ) I γ ( t ; r ) I ρ ( t ; r ) 1 = G γ ρ ( τ ) I γ ( t ; r ) I ρ ( t ; r )
I γ ( t ) = MDE γ ( r ) χ 𝕊 η γ χ c χ ( t , r ) d V , δ I γ ( t ) = MDE γ ( r ) χ 𝕊 η γ χ δ c χ ( t , r ) d V
MDE γ ( r ) = MDE γ ( x , y , z ) = 1 𝒩 I LS ( z ) 0 a 0 a PSF γ ( x μ , y ν , z ) d ν d μ ,
g γ ρ ( τ ) = χ 𝕊 η γ χ η ρ χ G γ ρ χ ( τ ) ( χ 𝕊 η γ χ c χ ) ( χ 𝕊 η ρ χ c χ ) .
G γ ρ χ ( τ ) = δ I γ ( t ) δ I ρ ( t + τ ) η γ χ η ρ χ = c χ MDE γ ( r ) MDE ρ ( r ) ϕ χ ( r , r , τ ) d V d V .
ϕ χ ( r , r , τ ) = 1 ( 4 π D χ τ ) 3 / 2 exp [ ( r r ) 2 4 D χ τ ]
G γ ρ ; x χ ( τ ) = G γ ρ ; y χ ( τ ) = 1 a { erf ( 2 a 8 D χ τ + w γ 2 + w ρ 2 ) + 8 D χ τ + w γ 2 + w ρ 2 a 2 π [ e 2 a 2 8 D χ τ + w γ 2 + w ρ 2 1 ] }
G γ ρ ; z χ ( τ ) = 2 / π 8 D χ τ + z γ 2 + z ρ 2 .
η g A η g η g B = 0 η g AB = η g η r A = κ gr η g η r B η r η r AB = η r + κ gr η g .
η g = I g ( t ) c A + c AB , η r = I r ( t ) κ gr I g ( t ) c B + c AB ,
g gg ( τ ) = η g 2 G gg A ( τ ) + η g 2 G gg AB ( τ ) η g 2 ( c A + c AB ) 2
g rr ( τ ) = η r 2 [ G rr B ( τ ) + G rr AB ( τ ) ] + κ gr 2 η g 2 [ G gg A ( τ ) + G gg AB ( τ ) ] + 2 κ gr η r η g G gr AB ( τ ) ( κ gr η g c A + ( η r + κ gr η g ) c AB + η r c B ) 2
g gr ( τ ) = g rg ( τ ) = η g η r G gr AB ( τ ) + κ gr η g η r G gr A ( τ ) + κ gr η g 2 G gg AB ( τ ) ( η g c A + η g c AB ) ( κ gr η g c A + ( η r + κ gr η g ) c AB + η r c B )
p AB = c AB min ( c A , c B )
q = g gr ( τ min ) min [ g gg ( τ min ) , g rr ( τ min ) ] ,
β * = argmin β γ ρ = { gg , rr , gr , rg } i [ g ^ γ ρ , i g γ ρ ( τ i ; π γ ρ ( β ) ) σ ^ γ ρ , i ] 2 ,
g gg ( τ ) = η g 2 c A + η g 2 c AB η g 2 ( c A + c AB ) 2 Ǧ gg G ( τ )
g rr ( τ ) = η r 2 [ c B + c AB ] + κ gr 2 η g 2 [ c A + c AB ] + 2 κ gr η r η g c AB ( κ gr η g c A + ( η r + κ gr η g ) c AB + η r c B ) 2 Ǧ rr R ( τ )
g gr ( τ ) = g rg ( τ ) = η g η r c AB + κ gr η g η r c A + κ gr η g 2 c AB ( η g c A + η g c AB ) ( κ gr η g c A + ( η r + κ gr η g ) c AB + η r c B ) Ǧ gr GR ( τ ) ,
p AB ( δ x ) = c AB ( δ x ) c all ( δ x ) = c AB ( δ x ) c A ( δ x ) + c B ( δ x ) + c AB ( δ x )
err ( δ x ) = | p AB ( δ x ) p AB ( 0 ) | p AB ( 0 ) .

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