Abstract

Real-time optical imaging combined with single-molecule manipulation broadens the horizons for acquiring information about the spatiotemporal localization and the mechanical details of target molecules. To obtain an optical signal outside the focal plane without unintended interruption of the force signal in single-molecule optical imaging-force spectroscopy, we developed an optical method to extend the depth of field in a high numerical aperture objective (≥ 1.2), required to visualize a single fluorophore. By axial scanning, using an electrically tunable lens with a fixed sample, we were successfully able to visualize the epidermal growth factor receptor (EGFR) moving along the three-dimensionally elongated filamentous actin bundles connecting cells (intercellular nanotube), while another EGFR on the intercellular nanotube was trapped by optical tweezers in living cells. Our approach is simple, fast and inexpensive, but it is powerful for imaging target molecules axially in single-molecule optical imaging-force spectroscopy.

© 2017 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

Full Article  |  PDF Article
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References

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  26. A. C. Gradilla, E. González, I. Seijo, G. Andrés, M. Bischoff, L. González-Mendez, V. Sánchez, A. Callejo, C. Ibáñez, M. Guerra, J. R. Ortigão-Farias, J. D. Sutherland, M. González, R. Barrio, J. M. Falcón-Pérez, and I. Guerrero, “Exosomes as hedgehog carriers in cytoneme-mediated transport and secretion,” Nat. Commun. 5, 5649 (2014).
  27. M. Inaba, M. Buszczak, and Y. M. Yamashita, “Nanotubes mediate niche-stem-cell signalling in the Drosophila testis,” Nature 523(7560), 329–332 (2015).
  28. Y. Connor, S. Tekleab, S. Nandakumar, C. Walls, Y. Tekleab, A. Husain, O. Gadish, V. Sabbisetti, S. Kaushik, S. Sehrawat, A. Kulkarni, H. Dvorak, B. Zetter, E. R. Edelman, and S. Sengupta, “Physical nanoscale conduit-mediated communication between tumour cells and the endothelium modulates endothelial phenotype,” Nat. Commun. 6, 8671 (2015).
  29. M. Karlikow, B. Goic, V. Mongelli, A. Salles, C. Schmitt, I. Bonne, C. Zurzolo, and M.-C. Saleh, “Drosophila cells use nanotube-like structures to transfer dsRNA and RNAi machinery between cells,” Sci. Rep. 6, 27085 (2016).
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  31. I. Chung, R. Akita, R. Vandlen, D. Toomre, J. Schlessinger, and I. Mellman, “Spatial control of EGF receptor activation by reversible dimerization on living cells,” Nature 464(7289), 783–787 (2010).
  32. D. S. Lidke, K. A. Lidke, B. Rieger, T. M. Jovin, and D. J. Arndt-Jovin, “Reaching out for signals: filopodia sense EGF and respond by directed retrograde transport of activated receptors,” J. Cell Biol. 170(4), 619–626 (2005).
  33. C. Zuo, Q. Chen, W. Qu, and A. Asundi, “High-speed transport-of-intensity phase microscopy with an electrically tunable lens,” Opt. Express 21(20), 24060–24075 (2013).
  34. F. O. Fahrbach, F. F. Voigt, B. Schmid, F. Helmchen, and J. Huisken, “Rapid 3D light-sheet microscopy with a tunable lens,” Opt. Express 21(18), 21010–21026 (2013).
  35. Y. Nakai, M. Ozeki, T. Hiraiwa, R. Tanimoto, A. Funahashi, N. Hiroi, A. Taniguchi, S. Nonaka, V. Boilot, R. Shrestha, J. Clark, N. Tamura, V. M. Draviam, and H. Oku, “High-speed microscopy with an electrically tunable lens to image the dynamics of in vivo molecular complexes,” Rev. Sci. Instrum. 86(1), 013707 (2015).
  36. B. Li, H. Qin, S. Yang, and D. Xing, “In vivo fast variable focus photoacoustic microscopy using an electrically tunable lens,” Opt. Express 22(17), 20130–20137 (2014).
  37. K. Philipp, A. Smolarski, N. Koukourakis, A. Fischer, M. Stürmer, U. Wallrabe, and J. W. Czarske, “Volumetric HiLo microscopy employing an electrically tunable lens,” Opt. Express 24(13), 15029–15041 (2016).

2016 (5)

Y. Jeon, D. Kim, J. V. Martín-López, R. Lee, J. Oh, J. Hanne, R. Fishel, and J.-B. Lee, “Dynamic control of strand excision during human DNA mismatch repair,” Proc. Natl. Acad. Sci. U.S.A. 113(12), 3281–3286 (2016).

M. Karlikow, B. Goic, V. Mongelli, A. Salles, C. Schmitt, I. Bonne, C. Zurzolo, and M.-C. Saleh, “Drosophila cells use nanotube-like structures to transfer dsRNA and RNAi machinery between cells,” Sci. Rep. 6, 27085 (2016).

F. E. Kemmerich, M. Swoboda, D. J. Kauert, M. S. Grieb, S. Hahn, F. W. Schwarz, R. Seidel, and M. Schlierf, “Simultaneous single-molecule force and fluorescence sampling of DNA nanostructure conformations using magnetic tweezers,” Nano Lett. 16(1), 381–386 (2016).

M. N. Economo, N. G. Clack, L. D. Lavis, C. R. Gerfen, K. Svoboda, E. W. Myers, and J. Chandrashekar, “A platform for brain-wide imaging and reconstruction of individual neurons,” eLife 5, e10566 (2016).

K. Philipp, A. Smolarski, N. Koukourakis, A. Fischer, M. Stürmer, U. Wallrabe, and J. W. Czarske, “Volumetric HiLo microscopy employing an electrically tunable lens,” Opt. Express 24(13), 15029–15041 (2016).

2015 (5)

J. Jiang, D. Zhang, S. Walker, C. Gu, Y. Ke, W. H. Yung, and S.-C. Chen, “Fast 3-D temporal focusing microscopy using an electrically tunable lens,” Opt. Express 23(19), 24362–24368 (2015).

Y. Nakai, M. Ozeki, T. Hiraiwa, R. Tanimoto, A. Funahashi, N. Hiroi, A. Taniguchi, S. Nonaka, V. Boilot, R. Shrestha, J. Clark, N. Tamura, V. M. Draviam, and H. Oku, “High-speed microscopy with an electrically tunable lens to image the dynamics of in vivo molecular complexes,” Rev. Sci. Instrum. 86(1), 013707 (2015).

X. Wang and H. H. Gerdes, “Transfer of mitochondria via tunneling nanotubes rescues apoptotic PC12 cells,” Cell Death Differ. 22(7), 1181–1191 (2015).

M. Inaba, M. Buszczak, and Y. M. Yamashita, “Nanotubes mediate niche-stem-cell signalling in the Drosophila testis,” Nature 523(7560), 329–332 (2015).

Y. Connor, S. Tekleab, S. Nandakumar, C. Walls, Y. Tekleab, A. Husain, O. Gadish, V. Sabbisetti, S. Kaushik, S. Sehrawat, A. Kulkarni, H. Dvorak, B. Zetter, E. R. Edelman, and S. Sengupta, “Physical nanoscale conduit-mediated communication between tumour cells and the endothelium modulates endothelial phenotype,” Nat. Commun. 6, 8671 (2015).

2014 (5)

S. Roy, H. Huang, S. Liu, and T. B. Kornberg, “Cytoneme-mediated contact-dependent transport of the Drosophila decapentaplegic signaling protein,” Science 343(6173), 1244624 (2014).

J. M. Jabbour, B. H. Malik, C. Olsovsky, R. Cuenca, S. Cheng, J. A. Jo, Y.-S. L. Cheng, J. M. Wright, and K. C. Maitland, “Optical axial scanning in confocal microscopy using an electrically tunable lens,” Biomed. Opt. Express 5(2), 645–652 (2014).

N. Koukourakis, M. Finkeldey, M. Stürmer, C. Leithold, N. C. Gerhardt, M. R. Hofmann, U. Wallrabe, J. W. Czarske, and A. Fischer, “Axial scanning in confocal microscopy employing adaptive lenses (CAL),” Opt. Express 22(5), 6025–6039 (2014).

B. Li, H. Qin, S. Yang, and D. Xing, “In vivo fast variable focus photoacoustic microscopy using an electrically tunable lens,” Opt. Express 22(17), 20130–20137 (2014).

A. C. Gradilla, E. González, I. Seijo, G. Andrés, M. Bischoff, L. González-Mendez, V. Sánchez, A. Callejo, C. Ibáñez, M. Guerra, J. R. Ortigão-Farias, J. D. Sutherland, M. González, R. Barrio, J. M. Falcón-Pérez, and I. Guerrero, “Exosomes as hedgehog carriers in cytoneme-mediated transport and secretion,” Nat. Commun. 5, 5649 (2014).

2013 (4)

F. O. Fahrbach, F. F. Voigt, B. Schmid, F. Helmchen, and J. Huisken, “Rapid 3D light-sheet microscopy with a tunable lens,” Opt. Express 21(18), 21010–21026 (2013).

C. Zuo, Q. Chen, W. Qu, and A. Asundi, “High-speed transport-of-intensity phase microscopy with an electrically tunable lens,” Opt. Express 21(20), 24060–24075 (2013).

J. Briscoe and J. P. Vincent, “Hedgehog threads to spread,” Nat. Cell Biol. 15(11), 1265–1267 (2013).

T. A. Sanders, E. Llagostera, and M. Barna, “Specialized filopodia direct long-range transport of SHH during vertebrate tissue patterning,” Nature 497(7451), 628–632 (2013).

2012 (1)

J. Lee, Y. Miyanaga, M. Ueda, and S. Hohng, “Video-rate confocal microscopy for single-molecule imaging in live cells and superresolution fluorescence imaging,” Biophys. J. 103(8), 1691–1697 (2012).

2011 (2)

S. Roy, F. Hsiung, and T. B. Kornberg, “Specificity of Drosophila cytonemes for distinct signaling pathways,” Science 332(6027), 354–358 (2011).

B. F. Grewe, F. F. Voigt, M. van ’t Hoff, and F. Helmchen, “Fast two-layer two-photon imaging of neuronal cell populations using an electrically tunable lens,” Biomed. Opt. Express 2(7), 2035–2046 (2011).

2010 (1)

I. Chung, R. Akita, R. Vandlen, D. Toomre, J. Schlessinger, and I. Mellman, “Spatial control of EGF receptor activation by reversible dimerization on living cells,” Nature 464(7289), 783–787 (2010).

2008 (2)

K. C. Neuman and A. Nagy, “Single-molecule force spectroscopy: optical tweezers, magnetic tweezers and atomic force microscopy,” Nat. Methods 5(6), 491–505 (2008).

S. Sowinski, C. Jolly, O. Berninghausen, M. A. Purbhoo, A. Chauveau, K. Köhler, S. Oddos, P. Eissmann, F. M. Brodsky, C. Hopkins, B. Onfelt, Q. Sattentau, and D. M. Davis, “Membrane nanotubes physically connect T cells over long distances presenting a novel route for HIV-1 transmission,” Nat. Cell Biol. 10(2), 211–219 (2008).

2007 (1)

N. M. Sherer, M. J. Lehmann, L. F. Jimenez-Soto, C. Horensavitz, M. Pypaert, and W. Mothes, “Retroviruses can establish filopodial bridges for efficient cell-to-cell transmission,” Nat. Cell Biol. 9(3), 310–315 (2007).

2006 (2)

B. Onfelt, S. Nedvetzki, R. K. P. Benninger, M. A. Purbhoo, S. Sowinski, A. N. Hume, M. C. Seabra, M. A. A. Neil, P. M. W. French, and D. M. Davis, “Structurally distinct membrane nanotubes between human macrophages support long-distance vesicular traffic or surfing of bacteria,” J. Immunol. 177(12), 8476–8483 (2006).

R. R. Brau, P. B. Tarsa, J. M. Ferrer, P. Lee, and M. J. Lang, “Interlaced optical force-fluorescence measurements for single molecule biophysics,” Biophys. J. 91(3), 1069–1077 (2006).

2005 (4)

D. S. Lidke, K. A. Lidke, B. Rieger, T. M. Jovin, and D. J. Arndt-Jovin, “Reaching out for signals: filopodia sense EGF and respond by directed retrograde transport of activated receptors,” J. Cell Biol. 170(4), 619–626 (2005).

R. Kassies, K. O. van der Werf, A. Lenferink, C. N. Hunter, J. D. Olsen, V. Subramaniam, and C. Otto, “Combined AFM and confocal fluorescence microscope for applications in bio-nanotechnology,” J. Microsc. 217(Pt 1), 109–116 (2005).

W. J. Greenleaf, M. T. Woodside, E. A. Abbondanzieri, and S. M. Block, “Passive all-optical force clamp for high-resolution laser trapping,” Phys. Rev. Lett. 95(20), 208102 (2005).

F. Hsiung, F.-A. Ramirez-Weber, D. D. Iwaki, and T. B. Kornberg, “Dependence of Drosophila wing imaginal disc cytonemes on Decapentaplegic,” Nature 437(7058), 560–563 (2005).

2004 (3)

A. Rustom, R. Saffrich, I. Markovic, P. Walther, and H. H. Gerdes, “Nanotubular highways for intercellular organelle transport,” Science 303(5660), 1007–1010 (2004).

D. L. Vossen, A. van der Horst, M. Dogterom, and A. van Blaaderen, “Optical tweezers and confocal microscopy for simultaneous three-dimensional manipulation and imaging in concentrated colloidal dispersions,” Rev. Sci. Instrum. 75, 2960–2970 (2004).

M. J. Lang, P. M. Fordyce, A. M. Engh, K. C. Neuman, and S. M. Block, “Simultaneous, coincident optical trapping and single-molecule fluorescence,” Nat. Methods 1(2), 133–139 (2004).

2003 (1)

C. De Joussineau, J. Soulé, M. Martin, C. Anguille, P. Montcourrier, and D. Alexandre, “Delta-promoted filopodia mediate long-range lateral inhibition in Drosophila,” Nature 426(6966), 555–559 (2003).

1999 (1)

F.-A. Ramírez-Weber and T. B. Kornberg, “Cytonemes: cellular processes that project to the principal signaling center in Drosophila imaginal discs,” Cell 97(5), 599–607 (1999).

Abbondanzieri, E. A.

W. J. Greenleaf, M. T. Woodside, E. A. Abbondanzieri, and S. M. Block, “Passive all-optical force clamp for high-resolution laser trapping,” Phys. Rev. Lett. 95(20), 208102 (2005).

Akita, R.

I. Chung, R. Akita, R. Vandlen, D. Toomre, J. Schlessinger, and I. Mellman, “Spatial control of EGF receptor activation by reversible dimerization on living cells,” Nature 464(7289), 783–787 (2010).

Alexandre, D.

C. De Joussineau, J. Soulé, M. Martin, C. Anguille, P. Montcourrier, and D. Alexandre, “Delta-promoted filopodia mediate long-range lateral inhibition in Drosophila,” Nature 426(6966), 555–559 (2003).

Andrés, G.

A. C. Gradilla, E. González, I. Seijo, G. Andrés, M. Bischoff, L. González-Mendez, V. Sánchez, A. Callejo, C. Ibáñez, M. Guerra, J. R. Ortigão-Farias, J. D. Sutherland, M. González, R. Barrio, J. M. Falcón-Pérez, and I. Guerrero, “Exosomes as hedgehog carriers in cytoneme-mediated transport and secretion,” Nat. Commun. 5, 5649 (2014).

Anguille, C.

C. De Joussineau, J. Soulé, M. Martin, C. Anguille, P. Montcourrier, and D. Alexandre, “Delta-promoted filopodia mediate long-range lateral inhibition in Drosophila,” Nature 426(6966), 555–559 (2003).

Arndt-Jovin, D. J.

D. S. Lidke, K. A. Lidke, B. Rieger, T. M. Jovin, and D. J. Arndt-Jovin, “Reaching out for signals: filopodia sense EGF and respond by directed retrograde transport of activated receptors,” J. Cell Biol. 170(4), 619–626 (2005).

Asundi, A.

Barna, M.

T. A. Sanders, E. Llagostera, and M. Barna, “Specialized filopodia direct long-range transport of SHH during vertebrate tissue patterning,” Nature 497(7451), 628–632 (2013).

Barrio, R.

A. C. Gradilla, E. González, I. Seijo, G. Andrés, M. Bischoff, L. González-Mendez, V. Sánchez, A. Callejo, C. Ibáñez, M. Guerra, J. R. Ortigão-Farias, J. D. Sutherland, M. González, R. Barrio, J. M. Falcón-Pérez, and I. Guerrero, “Exosomes as hedgehog carriers in cytoneme-mediated transport and secretion,” Nat. Commun. 5, 5649 (2014).

Benninger, R. K. P.

B. Onfelt, S. Nedvetzki, R. K. P. Benninger, M. A. Purbhoo, S. Sowinski, A. N. Hume, M. C. Seabra, M. A. A. Neil, P. M. W. French, and D. M. Davis, “Structurally distinct membrane nanotubes between human macrophages support long-distance vesicular traffic or surfing of bacteria,” J. Immunol. 177(12), 8476–8483 (2006).

Berninghausen, O.

S. Sowinski, C. Jolly, O. Berninghausen, M. A. Purbhoo, A. Chauveau, K. Köhler, S. Oddos, P. Eissmann, F. M. Brodsky, C. Hopkins, B. Onfelt, Q. Sattentau, and D. M. Davis, “Membrane nanotubes physically connect T cells over long distances presenting a novel route for HIV-1 transmission,” Nat. Cell Biol. 10(2), 211–219 (2008).

Bischoff, M.

A. C. Gradilla, E. González, I. Seijo, G. Andrés, M. Bischoff, L. González-Mendez, V. Sánchez, A. Callejo, C. Ibáñez, M. Guerra, J. R. Ortigão-Farias, J. D. Sutherland, M. González, R. Barrio, J. M. Falcón-Pérez, and I. Guerrero, “Exosomes as hedgehog carriers in cytoneme-mediated transport and secretion,” Nat. Commun. 5, 5649 (2014).

Block, S. M.

W. J. Greenleaf, M. T. Woodside, E. A. Abbondanzieri, and S. M. Block, “Passive all-optical force clamp for high-resolution laser trapping,” Phys. Rev. Lett. 95(20), 208102 (2005).

M. J. Lang, P. M. Fordyce, A. M. Engh, K. C. Neuman, and S. M. Block, “Simultaneous, coincident optical trapping and single-molecule fluorescence,” Nat. Methods 1(2), 133–139 (2004).

Boilot, V.

Y. Nakai, M. Ozeki, T. Hiraiwa, R. Tanimoto, A. Funahashi, N. Hiroi, A. Taniguchi, S. Nonaka, V. Boilot, R. Shrestha, J. Clark, N. Tamura, V. M. Draviam, and H. Oku, “High-speed microscopy with an electrically tunable lens to image the dynamics of in vivo molecular complexes,” Rev. Sci. Instrum. 86(1), 013707 (2015).

Bonne, I.

M. Karlikow, B. Goic, V. Mongelli, A. Salles, C. Schmitt, I. Bonne, C. Zurzolo, and M.-C. Saleh, “Drosophila cells use nanotube-like structures to transfer dsRNA and RNAi machinery between cells,” Sci. Rep. 6, 27085 (2016).

Brau, R. R.

R. R. Brau, P. B. Tarsa, J. M. Ferrer, P. Lee, and M. J. Lang, “Interlaced optical force-fluorescence measurements for single molecule biophysics,” Biophys. J. 91(3), 1069–1077 (2006).

Briscoe, J.

J. Briscoe and J. P. Vincent, “Hedgehog threads to spread,” Nat. Cell Biol. 15(11), 1265–1267 (2013).

Brodsky, F. M.

S. Sowinski, C. Jolly, O. Berninghausen, M. A. Purbhoo, A. Chauveau, K. Köhler, S. Oddos, P. Eissmann, F. M. Brodsky, C. Hopkins, B. Onfelt, Q. Sattentau, and D. M. Davis, “Membrane nanotubes physically connect T cells over long distances presenting a novel route for HIV-1 transmission,” Nat. Cell Biol. 10(2), 211–219 (2008).

Buszczak, M.

M. Inaba, M. Buszczak, and Y. M. Yamashita, “Nanotubes mediate niche-stem-cell signalling in the Drosophila testis,” Nature 523(7560), 329–332 (2015).

Callejo, A.

A. C. Gradilla, E. González, I. Seijo, G. Andrés, M. Bischoff, L. González-Mendez, V. Sánchez, A. Callejo, C. Ibáñez, M. Guerra, J. R. Ortigão-Farias, J. D. Sutherland, M. González, R. Barrio, J. M. Falcón-Pérez, and I. Guerrero, “Exosomes as hedgehog carriers in cytoneme-mediated transport and secretion,” Nat. Commun. 5, 5649 (2014).

Chandrashekar, J.

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M. N. Economo, N. G. Clack, L. D. Lavis, C. R. Gerfen, K. Svoboda, E. W. Myers, and J. Chandrashekar, “A platform for brain-wide imaging and reconstruction of individual neurons,” eLife 5, e10566 (2016).

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M. N. Economo, N. G. Clack, L. D. Lavis, C. R. Gerfen, K. Svoboda, E. W. Myers, and J. Chandrashekar, “A platform for brain-wide imaging and reconstruction of individual neurons,” eLife 5, e10566 (2016).

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M. Karlikow, B. Goic, V. Mongelli, A. Salles, C. Schmitt, I. Bonne, C. Zurzolo, and M.-C. Saleh, “Drosophila cells use nanotube-like structures to transfer dsRNA and RNAi machinery between cells,” Sci. Rep. 6, 27085 (2016).

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Guerra, M.

A. C. Gradilla, E. González, I. Seijo, G. Andrés, M. Bischoff, L. González-Mendez, V. Sánchez, A. Callejo, C. Ibáñez, M. Guerra, J. R. Ortigão-Farias, J. D. Sutherland, M. González, R. Barrio, J. M. Falcón-Pérez, and I. Guerrero, “Exosomes as hedgehog carriers in cytoneme-mediated transport and secretion,” Nat. Commun. 5, 5649 (2014).

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A. C. Gradilla, E. González, I. Seijo, G. Andrés, M. Bischoff, L. González-Mendez, V. Sánchez, A. Callejo, C. Ibáñez, M. Guerra, J. R. Ortigão-Farias, J. D. Sutherland, M. González, R. Barrio, J. M. Falcón-Pérez, and I. Guerrero, “Exosomes as hedgehog carriers in cytoneme-mediated transport and secretion,” Nat. Commun. 5, 5649 (2014).

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Y. Jeon, D. Kim, J. V. Martín-López, R. Lee, J. Oh, J. Hanne, R. Fishel, and J.-B. Lee, “Dynamic control of strand excision during human DNA mismatch repair,” Proc. Natl. Acad. Sci. U.S.A. 113(12), 3281–3286 (2016).

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Hohng, S.

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S. Sowinski, C. Jolly, O. Berninghausen, M. A. Purbhoo, A. Chauveau, K. Köhler, S. Oddos, P. Eissmann, F. M. Brodsky, C. Hopkins, B. Onfelt, Q. Sattentau, and D. M. Davis, “Membrane nanotubes physically connect T cells over long distances presenting a novel route for HIV-1 transmission,” Nat. Cell Biol. 10(2), 211–219 (2008).

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N. M. Sherer, M. J. Lehmann, L. F. Jimenez-Soto, C. Horensavitz, M. Pypaert, and W. Mothes, “Retroviruses can establish filopodial bridges for efficient cell-to-cell transmission,” Nat. Cell Biol. 9(3), 310–315 (2007).

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S. Roy, F. Hsiung, and T. B. Kornberg, “Specificity of Drosophila cytonemes for distinct signaling pathways,” Science 332(6027), 354–358 (2011).

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S. Roy, H. Huang, S. Liu, and T. B. Kornberg, “Cytoneme-mediated contact-dependent transport of the Drosophila decapentaplegic signaling protein,” Science 343(6173), 1244624 (2014).

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Hume, A. N.

B. Onfelt, S. Nedvetzki, R. K. P. Benninger, M. A. Purbhoo, S. Sowinski, A. N. Hume, M. C. Seabra, M. A. A. Neil, P. M. W. French, and D. M. Davis, “Structurally distinct membrane nanotubes between human macrophages support long-distance vesicular traffic or surfing of bacteria,” J. Immunol. 177(12), 8476–8483 (2006).

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R. Kassies, K. O. van der Werf, A. Lenferink, C. N. Hunter, J. D. Olsen, V. Subramaniam, and C. Otto, “Combined AFM and confocal fluorescence microscope for applications in bio-nanotechnology,” J. Microsc. 217(Pt 1), 109–116 (2005).

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Y. Connor, S. Tekleab, S. Nandakumar, C. Walls, Y. Tekleab, A. Husain, O. Gadish, V. Sabbisetti, S. Kaushik, S. Sehrawat, A. Kulkarni, H. Dvorak, B. Zetter, E. R. Edelman, and S. Sengupta, “Physical nanoscale conduit-mediated communication between tumour cells and the endothelium modulates endothelial phenotype,” Nat. Commun. 6, 8671 (2015).

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A. C. Gradilla, E. González, I. Seijo, G. Andrés, M. Bischoff, L. González-Mendez, V. Sánchez, A. Callejo, C. Ibáñez, M. Guerra, J. R. Ortigão-Farias, J. D. Sutherland, M. González, R. Barrio, J. M. Falcón-Pérez, and I. Guerrero, “Exosomes as hedgehog carriers in cytoneme-mediated transport and secretion,” Nat. Commun. 5, 5649 (2014).

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F. Hsiung, F.-A. Ramirez-Weber, D. D. Iwaki, and T. B. Kornberg, “Dependence of Drosophila wing imaginal disc cytonemes on Decapentaplegic,” Nature 437(7058), 560–563 (2005).

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Y. Jeon, D. Kim, J. V. Martín-López, R. Lee, J. Oh, J. Hanne, R. Fishel, and J.-B. Lee, “Dynamic control of strand excision during human DNA mismatch repair,” Proc. Natl. Acad. Sci. U.S.A. 113(12), 3281–3286 (2016).

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Jimenez-Soto, L. F.

N. M. Sherer, M. J. Lehmann, L. F. Jimenez-Soto, C. Horensavitz, M. Pypaert, and W. Mothes, “Retroviruses can establish filopodial bridges for efficient cell-to-cell transmission,” Nat. Cell Biol. 9(3), 310–315 (2007).

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Jolly, C.

S. Sowinski, C. Jolly, O. Berninghausen, M. A. Purbhoo, A. Chauveau, K. Köhler, S. Oddos, P. Eissmann, F. M. Brodsky, C. Hopkins, B. Onfelt, Q. Sattentau, and D. M. Davis, “Membrane nanotubes physically connect T cells over long distances presenting a novel route for HIV-1 transmission,” Nat. Cell Biol. 10(2), 211–219 (2008).

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D. S. Lidke, K. A. Lidke, B. Rieger, T. M. Jovin, and D. J. Arndt-Jovin, “Reaching out for signals: filopodia sense EGF and respond by directed retrograde transport of activated receptors,” J. Cell Biol. 170(4), 619–626 (2005).

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M. Karlikow, B. Goic, V. Mongelli, A. Salles, C. Schmitt, I. Bonne, C. Zurzolo, and M.-C. Saleh, “Drosophila cells use nanotube-like structures to transfer dsRNA and RNAi machinery between cells,” Sci. Rep. 6, 27085 (2016).

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R. Kassies, K. O. van der Werf, A. Lenferink, C. N. Hunter, J. D. Olsen, V. Subramaniam, and C. Otto, “Combined AFM and confocal fluorescence microscope for applications in bio-nanotechnology,” J. Microsc. 217(Pt 1), 109–116 (2005).

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F. E. Kemmerich, M. Swoboda, D. J. Kauert, M. S. Grieb, S. Hahn, F. W. Schwarz, R. Seidel, and M. Schlierf, “Simultaneous single-molecule force and fluorescence sampling of DNA nanostructure conformations using magnetic tweezers,” Nano Lett. 16(1), 381–386 (2016).

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Y. Connor, S. Tekleab, S. Nandakumar, C. Walls, Y. Tekleab, A. Husain, O. Gadish, V. Sabbisetti, S. Kaushik, S. Sehrawat, A. Kulkarni, H. Dvorak, B. Zetter, E. R. Edelman, and S. Sengupta, “Physical nanoscale conduit-mediated communication between tumour cells and the endothelium modulates endothelial phenotype,” Nat. Commun. 6, 8671 (2015).

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F. E. Kemmerich, M. Swoboda, D. J. Kauert, M. S. Grieb, S. Hahn, F. W. Schwarz, R. Seidel, and M. Schlierf, “Simultaneous single-molecule force and fluorescence sampling of DNA nanostructure conformations using magnetic tweezers,” Nano Lett. 16(1), 381–386 (2016).

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Y. Jeon, D. Kim, J. V. Martín-López, R. Lee, J. Oh, J. Hanne, R. Fishel, and J.-B. Lee, “Dynamic control of strand excision during human DNA mismatch repair,” Proc. Natl. Acad. Sci. U.S.A. 113(12), 3281–3286 (2016).

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S. Sowinski, C. Jolly, O. Berninghausen, M. A. Purbhoo, A. Chauveau, K. Köhler, S. Oddos, P. Eissmann, F. M. Brodsky, C. Hopkins, B. Onfelt, Q. Sattentau, and D. M. Davis, “Membrane nanotubes physically connect T cells over long distances presenting a novel route for HIV-1 transmission,” Nat. Cell Biol. 10(2), 211–219 (2008).

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S. Roy, H. Huang, S. Liu, and T. B. Kornberg, “Cytoneme-mediated contact-dependent transport of the Drosophila decapentaplegic signaling protein,” Science 343(6173), 1244624 (2014).

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R. R. Brau, P. B. Tarsa, J. M. Ferrer, P. Lee, and M. J. Lang, “Interlaced optical force-fluorescence measurements for single molecule biophysics,” Biophys. J. 91(3), 1069–1077 (2006).

M. J. Lang, P. M. Fordyce, A. M. Engh, K. C. Neuman, and S. M. Block, “Simultaneous, coincident optical trapping and single-molecule fluorescence,” Nat. Methods 1(2), 133–139 (2004).

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M. N. Economo, N. G. Clack, L. D. Lavis, C. R. Gerfen, K. Svoboda, E. W. Myers, and J. Chandrashekar, “A platform for brain-wide imaging and reconstruction of individual neurons,” eLife 5, e10566 (2016).

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J. Lee, Y. Miyanaga, M. Ueda, and S. Hohng, “Video-rate confocal microscopy for single-molecule imaging in live cells and superresolution fluorescence imaging,” Biophys. J. 103(8), 1691–1697 (2012).

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Y. Jeon, D. Kim, J. V. Martín-López, R. Lee, J. Oh, J. Hanne, R. Fishel, and J.-B. Lee, “Dynamic control of strand excision during human DNA mismatch repair,” Proc. Natl. Acad. Sci. U.S.A. 113(12), 3281–3286 (2016).

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R. R. Brau, P. B. Tarsa, J. M. Ferrer, P. Lee, and M. J. Lang, “Interlaced optical force-fluorescence measurements for single molecule biophysics,” Biophys. J. 91(3), 1069–1077 (2006).

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Y. Jeon, D. Kim, J. V. Martín-López, R. Lee, J. Oh, J. Hanne, R. Fishel, and J.-B. Lee, “Dynamic control of strand excision during human DNA mismatch repair,” Proc. Natl. Acad. Sci. U.S.A. 113(12), 3281–3286 (2016).

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N. M. Sherer, M. J. Lehmann, L. F. Jimenez-Soto, C. Horensavitz, M. Pypaert, and W. Mothes, “Retroviruses can establish filopodial bridges for efficient cell-to-cell transmission,” Nat. Cell Biol. 9(3), 310–315 (2007).

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Lenferink, A.

R. Kassies, K. O. van der Werf, A. Lenferink, C. N. Hunter, J. D. Olsen, V. Subramaniam, and C. Otto, “Combined AFM and confocal fluorescence microscope for applications in bio-nanotechnology,” J. Microsc. 217(Pt 1), 109–116 (2005).

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Lidke, D. S.

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M. N. Economo, N. G. Clack, L. D. Lavis, C. R. Gerfen, K. Svoboda, E. W. Myers, and J. Chandrashekar, “A platform for brain-wide imaging and reconstruction of individual neurons,” eLife 5, e10566 (2016).

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M. Karlikow, B. Goic, V. Mongelli, A. Salles, C. Schmitt, I. Bonne, C. Zurzolo, and M.-C. Saleh, “Drosophila cells use nanotube-like structures to transfer dsRNA and RNAi machinery between cells,” Sci. Rep. 6, 27085 (2016).

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S. Sowinski, C. Jolly, O. Berninghausen, M. A. Purbhoo, A. Chauveau, K. Köhler, S. Oddos, P. Eissmann, F. M. Brodsky, C. Hopkins, B. Onfelt, Q. Sattentau, and D. M. Davis, “Membrane nanotubes physically connect T cells over long distances presenting a novel route for HIV-1 transmission,” Nat. Cell Biol. 10(2), 211–219 (2008).

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F. E. Kemmerich, M. Swoboda, D. J. Kauert, M. S. Grieb, S. Hahn, F. W. Schwarz, R. Seidel, and M. Schlierf, “Simultaneous single-molecule force and fluorescence sampling of DNA nanostructure conformations using magnetic tweezers,” Nano Lett. 16(1), 381–386 (2016).

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F. E. Kemmerich, M. Swoboda, D. J. Kauert, M. S. Grieb, S. Hahn, F. W. Schwarz, R. Seidel, and M. Schlierf, “Simultaneous single-molecule force and fluorescence sampling of DNA nanostructure conformations using magnetic tweezers,” Nano Lett. 16(1), 381–386 (2016).

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M. N. Economo, N. G. Clack, L. D. Lavis, C. R. Gerfen, K. Svoboda, E. W. Myers, and J. Chandrashekar, “A platform for brain-wide imaging and reconstruction of individual neurons,” eLife 5, e10566 (2016).

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F. E. Kemmerich, M. Swoboda, D. J. Kauert, M. S. Grieb, S. Hahn, F. W. Schwarz, R. Seidel, and M. Schlierf, “Simultaneous single-molecule force and fluorescence sampling of DNA nanostructure conformations using magnetic tweezers,” Nano Lett. 16(1), 381–386 (2016).

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Cell (1)

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Figures (4)

Fig. 1
Fig. 1 Schematic of the line-scan confocal microscopy (LSCM) combined with optical tweezers (OT). After passing through the cylindrical lens (CL), the shape of the excitation beam changes from an enlarged circle to a thin oval. The box at the bottom displays cross sections perpendicular to the propagation of the excitation beam at each position of a, b, c, and d in the path of the solid (x-axis view) and dashed (y-axis view) lines. The red solid line is the path of the emission signal. The grey solid line is the path of the trapping laser and the optical signal from the trapped bead. GM: Galvano scanning mirror, DM: Dichroic mirror, BX: Beam expander, T1/T2/T3: Telescope. The 3D detection and Trapping system is the part of the NanoTracker2 from JPK Instruments AG.
Fig. 2
Fig. 2 (a) Input voltage control of Scan OFF and ON with a 10 Hz ETL using a triangle wave. The Galvano scanning mirror scans at a frequency of 50 Hz and the sampling rate of the EMCCD is 10 Hz. (b) The offset lens in front of the ETL adjusts the focal length of the ETL to infinity for VETL (=V0) = 3 V, negative for VETL < 3 V, and positive for VETL > 3 V. (c) Magnification of the LSCM in a 100× or 60× objective lens as a function of the focal length of the ETL (VETL). (d) Relative SNR with respect to SNR at VETL = 3.0 V at various VETL. (e) Focal shift in the microscope with a 100× or 60× objective lens at various VETL
Fig. 3
Fig. 3 (a) Sytox Orange-stained dsDNA immobilized on the surface pulled by optical tweezers (left). The stained DNA is imaged at a specific focal length of the ETL (right). (b) VETL varies from 3.0 V to 3.6 V or from 3.1 V to 3.5 V at a frequency of 10 Hz. The depth of field increases (right). (c) The intensity profiles of the stained DNA are presented in Scan OFF (gray), ON (magenta, solid), and the average of the intensities of the DNA at 3.0 V ~ 3.6 V in Scan OFF (magenta, dotted). (d) The depth of field is measured in Scanning OFF and Scan ON (3.3 ± 0.2 V and 3.3 ± 0.3 V).
Fig. 4
Fig. 4 (a) Schematic representation of EGFR imaging on the intercellular nanotube connecting HeLa cells. (b) Kymograph of the EGF–QDs on the intercellular nanotube with the focal shift of 4.1 μm (VETL = 3.1 ~3.5 V, step = 0.1 V). (c) Schematic of an EGFR transport using EGF coated bead as an additional force probe. (d) EGF–QD Kymographs, (e) trapping force, and (f) trap position for three different experiments.

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