Abstract

Optical tweezers combined with various microscopy techniques are a versatile tool for single-molecule force spectroscopy. However, some combinations may compromise measurements. Here, we combined optical tweezers with total-internal-reflection-fluorescence (TIRF) and interference-reflection microscopy (IRM). Using a light-emitting diode (LED) for IRM illumination, we show that single microtubules can be imaged with high contrast. Furthermore, we converted the IRM interference pattern of an upward bent microtubule to its three-dimensional (3D) profile calibrated against the optical tweezers and evanescent TIRF field. In general, LED-based IRM is a powerful method for high-contrast 3D microscopy.

© 2018 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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2018 (2)

M. D. Koch and A. Rohrbach, “Label-free Imaging and Bending Analysis of Microtubules by ROCS Microscopy and Optical Trapping,” Biophys. J. 114, 168–177 (2018).
[Crossref] [PubMed]

M. Bugiel, A. Mitra, S. Girardo, S. Diez, and E. Schäffer, “Measuring microtubule supertwist and defects by three-dimensional-force-clamp tracking of single kinesin-1 motors,” Nano Lett. 18, 1290–1295 (2018).
[Crossref] [PubMed]

2017 (4)

A. Ramaiya, B. Roy, M. Bugiel, and E. Schäffer, “Kinesin rotates unidirectionally and generates torque while walking on microtubules,” Proc. Natl. Acad. Sci. U. S. A. 114, 10894–10899 (2017).
[PubMed]

M. Bugiel, A. Jannasch, and E. Schäffer, “Implementation and tuning of an optical tweezers force-clamp feedback system,” Methods Mol. Biol. 1486, 109–136 (2017).
[Crossref]

C. Jiang, N. Kaul, J. Campbell, and E. Meyhofer, “A novel dual-color bifocal imaging system for single-molecule studies,” Rev. Sci. Instrum. 88, 053705 (2017).
[Crossref] [PubMed]

M. Liebel, J. T. Hugall, and N. F. van Hulst, “Ultrasensitive label-free nanosensing and high-speed tracking of single proteins,” Nano Lett. 17, 1277–1281 (2017).
[Crossref] [PubMed]

2016 (1)

J. Andrecka, J. Ortega Arroyo, K. Lewis, R. Cross, and P. Kukura, “Label-free imaging of microtubules with sub-nm precision using interferometric scattering microscopy,” Biophys. J. 110, 214–217 (2016).
[Crossref] [PubMed]

2015 (1)

M. Bugiel, H. Fantana, V. Bormuth, F. Schiemann, J. Howard, E. Schäffer, and A. Jannasch, “Versatile microsphere attachment of GFP-labeled proteins with preserved functionality Microsphere preparation,” J. Biol. Methods 2, 1–12 (2015).
[Crossref]

2014 (2)

J. Ortega Arroyo, J. Andrecka, K. M. Spillane, N. Billington, Y. Takagi, J. R. Sellers, and P. Kukura, “Label-free, all-optical detection, imaging, and tracking of a single protein,” Nano Lett. 14, 2065–2070 (2014).
[Crossref] [PubMed]

M. Piliarik and V. Sandoghdar, “Direct optical sensing of single unlabelled proteins and super-resolution imaging of their binding sites,” Nat. Commun. 5, 1–8 (2014).
[Crossref]

2013 (1)

I. Heller, G. Sitters, O. D. Broekmans, G. Farge, C. Menges, W. Wende, S. W. Hell, E. J. G. Peterman, and G. J. L. Wuite, “STED nanoscopy combined with optical tweezers reveals protein dynamics on densely covered DNA,” Nat. Methods 10, 910–916 (2013).
[Crossref] [PubMed]

2012 (2)

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J.-Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods 9, 676–682 (2012).
[Crossref] [PubMed]

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

2011 (3)

K. G. Lee, X. W. Chen, H. Eghlidi, P. Kukura, R. Lettow, A. Renn, V. Sandoghdar, and S. Götzinger, “A planar dielectric antenna for directional single-photon emission and near-unity collection efficiency,” Nat. Photonics 5, 166 (2011).
[Crossref]

M. Mahamdeh, C. P. Campos, and E. Schäffer, “Under-filling trapping objectives optimizes the use of the available laser power in optical tweezers,” Opt. Express 19, 11759–11768 (2011).
[Crossref] [PubMed]

M. J. Comstock, T. Ha, and Y. R. Chemla, “Ultrahigh-resolution optical trap with single-fluorophore sensitivity,” Nat. Methods 8, 335–340 (2011).
[Crossref] [PubMed]

2010 (2)

L. Kong, P. Zhang, P. Setlow, and Y.-Q. Li, “Characterization of Bacterial Spore Germination Using Integrated Phase Contrast Microscopy, Raman Spectroscopy, and Optical Tweezers,” Anal. Chem. 82, 3840–3847 (2010).
[Crossref] [PubMed]

B. Gutiérrez-Medina and S. M. Block, “Visualizing individual microtubules by bright field microscopy,” Am. J. Phys. 78, 1152 (2010).
[Crossref]

2009 (4)

M. Mahamdeh and E. Schäffer, “Optical tweezers with millikelvin precision of temperature-controlled objectives and base-pair resolution,” Opt. Express 17, 17190–17199 (2009).
[Crossref] [PubMed]

Y. Huang, J. Wan, M. C. Cheng, Z. Zhang, S. M. Jhiang, and C. H. Menq, “Three-axis rapid steering of optically propelled micro/nanoparticles,” Rev. Sci. Instrum. 80, 1–8 (2009).
[Crossref]

L. Limozin and K. Sengupta, “Quantitative Reflection Interference Contrast Microscopy (RICM) in Soft Matter and Cell Adhesion,” ChemPhysChem 10, 2752–2768 (2009).
[Crossref] [PubMed]

C. Gell, M. Berndt, J. Enderlein, and S. Diez, “TIRF microscopy evanescent field calibration using tilted fluorescent microtubules,” J. Microsc. 234, 38–46 (2009).
[Crossref] [PubMed]

2008 (4)

A. Sischka, C. Kleimann, W. Hachmann, M. M. Schäfer, I. Seuffert, K. Tönsing, and D. Anselmetti, “Single beam optical tweezers setup with backscattered light detection for three-dimensional measurements on dna and nanopores,” Rev. Sci. Instrum. 79, 063702 (2008).
[Crossref] [PubMed]

K. Kim and O. A. Saleh, “Stabilizing method for reflection interference contrast microscopy,” Appl. Opt. 47, 2070–2075 (2008).
[Crossref] [PubMed]

U. Rothbauer, K. Zolghadr, S. Muyldermans, A. Schepers, M. C. Cardoso, and H. Leonhardt, “A versatile nanotrap for biochemical and functional studies with fluorescent fusion proteins,” Mol. Cell. Proteomics 7, 282–289 (2008).
[Crossref]

V. Bormuth, A. Jannasch, M. Ander, C. M. van Kats, A. van Blaaderen, J. Howard, and E. Schäffer, “Optical trapping of coated microspheres,” Opt. Express 16, 13831–13844 (2008).
[Crossref] [PubMed]

2007 (3)

V. Bormuth, J. Howard, and E. Schäffer, “LED illumination for video-enhanced DIC imaging of single microtubules,” J. Microsc. 226, 1–5 (2007).
[Crossref] [PubMed]

J. D. Hunter, “Matplotlib: A 2D graphics environment,” Comput. Sci. Eng. 9, 90–95 (2007).
[Crossref]

E. Schäffer, S. F. Nørrelykke, and J. Howard, “Surface forces and drag coefficients of microspheres near a plane surface measured with optical tweezers,” Langmuir 23, 3654–3665 (2007).
[Crossref] [PubMed]

2006 (4)

J. Kerssemakers, J. Howard, H. Hess, and S. Diez, “The distance that kinesin-1 holds its cargo from the microtubule surface measured by fluorescence interference contrast microscopy,” Proc. Natl. Acad. Sci. U. S. A. 103, 15812 (2006).
[Crossref] [PubMed]

M. Shribak and S. Inoué, “Orientation-independent differential interference contrast microscopy,” Appl. Opt. 45, 460–469 (2006).
[Crossref] [PubMed]

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

L. J. Friedman, J. Chung, and J. Gelles, “Viewing dynamic assembly of molecular complexes by multi-wavelength single-molecule fluorescence,” Biophys. J. 91, 1023–1031 (2006).
[Crossref] [PubMed]

2004 (1)

A. La Porta and M. D. Wang, “Optical torque wrench: Angular trapping, rotation, and torque detection of quartz microparticles,” Phys. Rev. Lett. 92, 190801 (2004).
[Crossref] [PubMed]

2003 (2)

M. Castoldi and A. V. Popov, “Purification of brain tubulin through two cycles of polymerization–depolymerization in a high-molarity buffer,” Protein Expr. Purif. 32, 83– 88 (2003).
[Crossref] [PubMed]

M. J. Lang, P. M. Fordyce, and S. M. Block, “Combined optical trapping and single-molecule fluorescence,” J. Biol. 2, 6 (2003).
[Crossref] [PubMed]

1998 (1)

R. Oldenbourg, E. Salmon, and P. Tran, “Birefringence of Single and Bundled Microtubules,” Biophys. J. 74, 645–654 (1998).
[Crossref] [PubMed]

1996 (1)

1993 (3)

F. Gittes, B. Mickey, J. Nettleton, and J. Howard, “Flexural rigidity of microtubules and actin filaments measured from thermal fluctuations in shape,” J. Cell Biol. 120, 923–934 (1993).
[Crossref] [PubMed]

K. Visscher, G. J. Brakenhoff, and J. J. Krol, “Micromanipulation by “multiple” optical traps created by a single fast scanning trap integrated with the bilateral confocal scanning laser microscope,” Cytometry 14, 105–114 (1993).
[Crossref]

J. Rädler and E. Sackmann, “Imaging optical thicknesses and separation distances of phospholipid vesicles at solid surfaces,” J. Phys. II France 3, 727–748 (1993).
[Crossref]

1991 (1)

L. A. Amos and W. B. Amos, “The bending of sliding microtubules imaged by confocal light microscopy and negative stain electron microscopy,” J. Cell Sci. Suppl. 14, 95–101 (1991).
[Crossref]

1988 (1)

R. A. Walker, E. T. O’Brien, N. K. Pryer, M. F. Soboeiro, W. A. Voter, H. P. Erickson, and E. D. Salmon, “Dynamic instability of individual microtubules analyzed by video light microscopy: rate constants and transition frequencies,” J. Cell Biol. 107, 1437–1448 (1988).
[Crossref] [PubMed]

1986 (1)

1964 (1)

A. S. G. Curtis, “A Study by Interference Reflection Microscopy,” J. Cell Biol. 20, 199–215 (1964).
[Crossref] [PubMed]

Amos, L. A.

L. A. Amos and W. B. Amos, “The bending of sliding microtubules imaged by confocal light microscopy and negative stain electron microscopy,” J. Cell Sci. Suppl. 14, 95–101 (1991).
[Crossref]

Amos, W. B.

L. A. Amos and W. B. Amos, “The bending of sliding microtubules imaged by confocal light microscopy and negative stain electron microscopy,” J. Cell Sci. Suppl. 14, 95–101 (1991).
[Crossref]

Ander, M.

Andrecka, J.

J. Andrecka, J. Ortega Arroyo, K. Lewis, R. Cross, and P. Kukura, “Label-free imaging of microtubules with sub-nm precision using interferometric scattering microscopy,” Biophys. J. 110, 214–217 (2016).
[Crossref] [PubMed]

J. Ortega Arroyo, J. Andrecka, K. M. Spillane, N. Billington, Y. Takagi, J. R. Sellers, and P. Kukura, “Label-free, all-optical detection, imaging, and tracking of a single protein,” Nano Lett. 14, 2065–2070 (2014).
[Crossref] [PubMed]

Anselmetti, D.

A. Sischka, C. Kleimann, W. Hachmann, M. M. Schäfer, I. Seuffert, K. Tönsing, and D. Anselmetti, “Single beam optical tweezers setup with backscattered light detection for three-dimensional measurements on dna and nanopores,” Rev. Sci. Instrum. 79, 063702 (2008).
[Crossref] [PubMed]

Arganda-Carreras, I.

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J.-Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods 9, 676–682 (2012).
[Crossref] [PubMed]

Ashkin, A.

Berndt, M.

C. Gell, M. Berndt, J. Enderlein, and S. Diez, “TIRF microscopy evanescent field calibration using tilted fluorescent microtubules,” J. Microsc. 234, 38–46 (2009).
[Crossref] [PubMed]

Billington, N.

J. Ortega Arroyo, J. Andrecka, K. M. Spillane, N. Billington, Y. Takagi, J. R. Sellers, and P. Kukura, “Label-free, all-optical detection, imaging, and tracking of a single protein,” Nano Lett. 14, 2065–2070 (2014).
[Crossref] [PubMed]

Bjorkholm, J. E.

Block, S. M.

B. Gutiérrez-Medina and S. M. Block, “Visualizing individual microtubules by bright field microscopy,” Am. J. Phys. 78, 1152 (2010).
[Crossref]

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M. Liebel, J. T. Hugall, and N. F. van Hulst, “Ultrasensitive label-free nanosensing and high-speed tracking of single proteins,” Nano Lett. 17, 1277–1281 (2017).
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M. Piliarik and V. Sandoghdar, “Direct optical sensing of single unlabelled proteins and super-resolution imaging of their binding sites,” Nat. Commun. 5, 1–8 (2014).
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Figures (5)

Fig. 1
Fig. 1 Schematic of the combined IRM–TIRF-microscope–optical-tweezers setup.
Fig. 2
Fig. 2 Schematic of the IRM design and principle. The optical path is drawn to scale and shows the marginal rays of the LED (blue lines), the sample (black lines), and the field iris (dashed gray lines). The inset shows the principle of the IRM contrast formation. The incident light of the Köhler-illuminated sample, here a microtubule, is reflected from the glass-water interface (reference) and the specimen (sample), which interfere to form the final IRM signal.
Fig. 3
Fig. 3 Background subtraction and SNR measurement of a microtubule. (A) Raw IRM image (top) of microtubules on a glass surface and background image (middle). Background subtraction leads to the image of the IRM signal (bottom). Note that microtubules are visible without background subtraction. Also note the signature of an interference pattern: a partially unbound microtubule has black and white regions (arrows in (A) top and bottom). (B) Region of interest of the microtubule indicated in A. The black spots are impurities. (C) Median-intensity profile calculated along the microtubule axis of B (black) and a Gaussian fit (orange). (D) Residual noise image after subtraction of the Gaussian fit shown in C from each column of the microtubule image in B. Values above or below the threshold (vertical, dashed lines in C) are indicated in red or blue, respectively. (E) Histogram of the gray values in D (light gray bars). The image noise was calculated from the gray values within the threshold (dark gray bars) excluding signals from impurities. The threshold (*) was calculated as ±1.5× the interquartile range around the median gray level.
Fig. 4
Fig. 4 Optimization of the IRM signal-to-noise ratio. (A) Analyzed microtubule images (top) and residual images (middle) at varying LED currents. The measured SNR is plotted versus the applied LED current (bottom). A power-law fit (dashed line) showed near shot-noise limited imaging. Inset: Measured noise vs. LED current. The noise scaled with an exponent 0.46 ± 0.1. (B) Analyzed microtubule images (top) and residual images (middle) for an increasing number N of averaged frames. The solid line indicates a power-law slope with exponent 0.5. Inset: IRM signal vs. number of averages. (C) Top 2 panels: section 10 images of the microtubule shown in D with increasing INA and the respective residual images. Bottom panels: Legend of sections. Signal of all microtubule-sections (indicated in D) and the corresponding noise is plotted vs. INA. The averaged SNR is normalized by the SNR at INA = 1.3 at the very bottom. (D) An averaged image of a microtubule (N = 50), its line intensity profile (bottom left) and the corresponding histogram (bottom right). The analyzed microtubule-sections of C are indicated (dashed lines).
Fig. 5
Fig. 5 IRM and evanescent field calibration using bent microtubules. (A) Schematic drawing not to scale. A microsphere functionalized with non-motile kinesin-1–GFP motor proteins is trapped and attached to a loose microtubule end, which is pulled upward by the trap. (B) TIRF (red channel, left) and IRM images (right) of a bent microtubule and attached microsphere at increasing trap heights. Note that the bright intensity around the microsphere is due to scattering of the illumination light and not due to the trapping laser. The latter is blocked by an infrared filter. Scale bar: 2 μm. (C) IRM line profiles along the microtubule shown in B (symbols) and the global fit of Eq. (1) (solid lines). The trap height and axial force are indicated. For clarity, data points are offset vertically. (D) Weighted linear fit (dashed line) to the microtubule tip height hMT (circles) plotted versus the trap height htrap (error bars are SEM, gray lines). Inset: Calculated microtubule profile vs. height. (E) Fluorescence intensity line profiles along the microtubule shown in B for different tip heights. (F) Normalized fluorescence intensity line profiles (symbols). Profiles were normalized to the average intensity of the first 20 points and to the line profile at ht = 0.0 μm (shaded area and blue circles in E, respectively). A global fit (solid lines) of the data to Eq. (3) determined the depth of the evanescent field.

Tables (1)

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Table 1 Fit parameters of the global fit to the IRM and TIRF intensity profiles.

Equations (3)

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I ( x ) = B D sin y y cos ( 2 k h ( x ) [ 1 sin 2 ( α 2 ) ] ) ,
h ( x ) = A ( x t x 0 2 ( x x 0 ) 2 ( x x 0 ) 3 6 ) ,
I TIRF ( x ) = exp [ h ( x ) / δ ] ,

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