Abstract

We present a two-color two-photon stimulated emission depletion microscopy technique (2C2P-STED) that correlates a confocal image with a super-resolved image employing the inherent self-referencing mechanism of nonlinear excitation. The novel approach overcomes the substantial challenge posed by two different imaging modalities in laser-scanning fluorescence microscopy for colocalization on the nanometer scale. Demonstrating the principle of 2C2P-STED, we show for the first time super-resolved images of the gram-positive bacteria Streptococcus pneumoniae TIGR4 pilus type-1. A signal-to-noise ratio (SNR) greater than 10 was achieved in 2C2P excitation mode and approximately 70 nm details were resolved in 2P-STED.

© 2019 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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2018 (2)

T. Ando, S. P. Bhamidimarri, N. Brending, H. Colin-York, L. Collinson, N. De Jonge, P. J. de Pablo, E. Debroye, C. Eggeling, C. Franck, M. Fritzsche, H. Gerritsen, B. N. G. Giepmans, K. Grunewald, J. Hofkens, J. P. Hoogenboom, K. P. F. Janssen, R. Kaufmann, J. Klumpermann, N. Kurniawan, J. Kusch, N. Liv, V. Parekh, D. B. Peckys, F. Rehfeldt, D. C. Reutens, M. B. J. Roeffaers, T. Salditt, I. A. T. Schaap, U. S. Schwarz, P. Verkade, M. W. Vogel, R. Wagner, M. Winterhalter, H. Yuan, and G. Zifarelli, “The 2018 correlative microscopy techniques roadmap,” J. Phys. D: Appl. Phys. 51(44), 443001 (2018).
[Crossref]

M. Mohseni, C. Polzer, and T. Hellerer, “Resolution of spectral focusing in coherent Raman imaging,” Opt. Express 26(8), 10230–10241 (2018).
[Crossref]

2017 (1)

2013 (1)

P. Bethge, R. Chéreau, E. Avignone, G. Marsicano, and U. V. Nägerl, “Two-Photon Excitation STED Microscopy in Two Colors in Acute Brain Slices,” Biophys. J. 104(4), 778–785 (2013).
[Crossref]

2012 (4)

P. Mahou, M. Zimmerley, K. Loulier, K. S. Matho, G. Labroille, X. Morin, W. Supatto, J. Livet, D. Débarre, and E. Beaurepaire, “Multicolor two-photon tissue imaging by wavelength mixing,” Nat. Methods 9(8), 815–818 (2012).
[Crossref]

J. Schindelin, “Fiji: An Open-Source Platform for Biological-Image Analysis,” Nat. Methods 9(7), 676–682 (2012).
[Crossref]

T. J. Gould, D. Burke, J. Bewersdorf, and M. J. Booth, “Adaptive optics enables 3D STED microscopy in aberrating specimens,” Opt. Express 20(19), 20998–21009 (2012).
[Crossref]

P. Bianchini, B. Harke, S. Galiani, G. Vicidomini, and A. Diaspro, “Single-wavelength two-photon excitation-stimulated emission depletion (SW2PE-STED) superresolution imaging,” Proc. Natl. Acad. Sci. 109(17), 6390–6393 (2012).
[Crossref]

2011 (3)

G. Vicidomini, G. Moneron, K. Y. Han, V. Westphal, H. Ta, M. Reuss, J. Engelhardt, C. Eggeling, and S. W. Hell, “Sharper low-power STED nanoscopy by time gating,” Nat. Methods 8(7), 571–573 (2011).
[Crossref]

T. Scheul, C. D’Amico, I. Wang, and J.-C. Vial, “Two-photon excitation and stimulated emission depletion by a single wavelength,” Opt. Express 19(19), 18036–18048 (2011).
[Crossref]

J. Caplan, M. Niethammer, R. M. Taylor, and K. J. Czymmek, “The Power of Correlative Microscopy: Multi-modal, Multi-scale, Multi-dimensional,” Curr. Opin. Struct. Biol. 21(5), 686–693 (2011).
[Crossref]

2010 (2)

S. Deng, L. Liu, Y. Cheng, R. Li, and Z. Xu, “Effects of primary aberrations on the fluorescence depletion patterns of STED microscopy,” Opt. Express 18(2), 1657–1666 (2010).
[Crossref]

X. Hao, C. Kuang, T. Wang, and X. Liu, “Effects of polarization on the de-excitation dark focal spot in STED microscopy,” J. Opt. 12(11), 115707 (2010).
[Crossref]

2009 (3)

E. Rittweger, K. Y. Han, S. E. Irvine, C. Eggeling, and S. W. Hell, “STED microscopy reveals crystal colour centres with nanometric resolution,” Nat. Photonics 3(3), 144–147 (2009).
[Crossref]

G. Moneron and S. W. Hell, “Two-photon excitation STED microscopy,” Opt. Express 17(17), 14567 (2009).
[Crossref]

M. Hilleringmann, P. Ringler, S. A. Müller, G. De Angelis, R. Rappuoli, I. Ferlenghi, and A. Engel, “Molecular architecture of Streptococcus pneumoniae TIGR4 pili,” EMBO J. 28(24), 3921–3930 (2009).
[Crossref]

2008 (3)

2007 (3)

J. Keller, A. Schönle, and S. W. Hell, “Efficient fluorescence inhibition patterns for RESOLFT microscopy,” Opt. Express 15(6), 3361 (2007).
[Crossref]

S. W. Hell, “Far-Field Optical Nanoscopy,” Single Mol. 316(5828), 1153–1158 (2007).
[Crossref]

L. Bonacina, Y. Mugnier, F. Courvoisier, R. Le Dantec, J. Extermann, Y. Lambert, V. Boutou, C. Galez, and J.-P. Wolf, “Polar Fe(IO3)3 nanocrystals as local probes for nonlinear microscopy,” Appl. Phys. B: Lasers Opt. 87(3), 399–403 (2007).
[Crossref]

2006 (5)

M. J. Rust, M. Bates, and X. Zhuang, “Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM),” Nat. Methods 3(10), 793–796 (2006).
[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]

K. I. Willig, S. O. Rizzoli, V. Westphal, R. Jahn, and S. W. Hell, “STED microscopy reveals that synaptotagmin remains clustered after synaptic vesicle exocytosis,” Nature 440(7086), 935–939 (2006).
[Crossref]

M. A. Barocchi, J. Ries, X. Zogaj, C. Hemsley, B. Albiger, A. Kanth, S. Dahlberg, J. Fernebro, M. Moschioni, and V. Masignani, “A pneumococcal pilus influences virulence and host inflammatory responses,” Proc. Natl. Acad. Sci. 103(8), 2857–2862 (2006).
[Crossref]

K. I. Willig, J. Keller, M. Bossi, and S. W. Hell, “STED microscopy resolves nanoparticle assemblies,” New J. Phys. 8(6), 106 (2006).
[Crossref]

2005 (1)

F. Helmchen and W. Denk, “Deep tissue two-photon microscopy,” Nat. Methods 2(12), 932–940 (2005).
[Crossref]

2004 (1)

2002 (1)

L. E. Helseth, “Focusing of atoms with strongly confined light potentials,” Opt. Commun. 212(4-6), 343–352 (2002).
[Crossref]

2001 (1)

T. A. Klar, E. Engel, and S. W. Hell, “Breaking Abbe’s diffraction resolution limit in fluorescence microscopy with stimulated emission depletion beams of various shapes,” Phys. Rev. E 64(6), 066613 (2001).
[Crossref]

2000 (1)

P. T. C. So, C. Y. Dong, B. R. Masters, and K. M. Berland, “Two-Photon Excitation Fluorescence Microscopy,” Annu. Rev. Biomed. Eng. 2(1), 399–429 (2000).
[Crossref]

1996 (1)

J. R. Lakowicz, I. Gryczynski, H. Malak, and Z. Gryczynski, “Two-color two-photon excitation of fluorescence,” Photochem. Photobiol. 64(4), 632–635 (1996).
[Crossref]

1990 (1)

W. Denk, J. H. Strickler, and W. W. Webb, “Two-photon laser scanning fluorescence microscopy,” Science 248(4951), 73–76 (1990).
[Crossref]

1959 (2)

E. Wolf, “Electromagnetic diffraction in optical systems-I. An integral representation of the image field,” Proc. R. Soc. London, Ser. A 253(1274), 349–357 (1959).
[Crossref]

B. Richards and E. Wolf, “Electromagnetic diffraction in optical systems, II. Structure of the image field in an aplanatic system,” Proc. R. Soc. London, Ser. A 253(1274), 358–379 (1959).
[Crossref]

1873 (1)

E. Abbe, “Beiträge zur Theorie des Mikroskops und der mikroskopischen Wahrnehmung,” Archiv für mikroskopische Anatomie 9(1), 413–418 (1873).
[Crossref]

Abbe, E.

E. Abbe, “Beiträge zur Theorie des Mikroskops und der mikroskopischen Wahrnehmung,” Archiv für mikroskopische Anatomie 9(1), 413–418 (1873).
[Crossref]

Albiger, B.

M. A. Barocchi, J. Ries, X. Zogaj, C. Hemsley, B. Albiger, A. Kanth, S. Dahlberg, J. Fernebro, M. Moschioni, and V. Masignani, “A pneumococcal pilus influences virulence and host inflammatory responses,” Proc. Natl. Acad. Sci. 103(8), 2857–2862 (2006).
[Crossref]

Ando, T.

T. Ando, S. P. Bhamidimarri, N. Brending, H. Colin-York, L. Collinson, N. De Jonge, P. J. de Pablo, E. Debroye, C. Eggeling, C. Franck, M. Fritzsche, H. Gerritsen, B. N. G. Giepmans, K. Grunewald, J. Hofkens, J. P. Hoogenboom, K. P. F. Janssen, R. Kaufmann, J. Klumpermann, N. Kurniawan, J. Kusch, N. Liv, V. Parekh, D. B. Peckys, F. Rehfeldt, D. C. Reutens, M. B. J. Roeffaers, T. Salditt, I. A. T. Schaap, U. S. Schwarz, P. Verkade, M. W. Vogel, R. Wagner, M. Winterhalter, H. Yuan, and G. Zifarelli, “The 2018 correlative microscopy techniques roadmap,” J. Phys. D: Appl. Phys. 51(44), 443001 (2018).
[Crossref]

Artigas, D.

Auksorius, E.

Avignone, E.

P. Bethge, R. Chéreau, E. Avignone, G. Marsicano, and U. V. Nägerl, “Two-Photon Excitation STED Microscopy in Two Colors in Acute Brain Slices,” Biophys. J. 104(4), 778–785 (2013).
[Crossref]

Barocchi, M. A.

M. A. Barocchi, J. Ries, X. Zogaj, C. Hemsley, B. Albiger, A. Kanth, S. Dahlberg, J. Fernebro, M. Moschioni, and V. Masignani, “A pneumococcal pilus influences virulence and host inflammatory responses,” Proc. Natl. Acad. Sci. 103(8), 2857–2862 (2006).
[Crossref]

Bates, M.

M. J. Rust, M. Bates, and X. Zhuang, “Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM),” Nat. Methods 3(10), 793–796 (2006).
[Crossref]

Beaurepaire, E.

P. Mahou, M. Zimmerley, K. Loulier, K. S. Matho, G. Labroille, X. Morin, W. Supatto, J. Livet, D. Débarre, and E. Beaurepaire, “Multicolor two-photon tissue imaging by wavelength mixing,” Nat. Methods 9(8), 815–818 (2012).
[Crossref]

Berland, K. M.

P. T. C. So, C. Y. Dong, B. R. Masters, and K. M. Berland, “Two-Photon Excitation Fluorescence Microscopy,” Annu. Rev. Biomed. Eng. 2(1), 399–429 (2000).
[Crossref]

Bethge, P.

P. Bethge, R. Chéreau, E. Avignone, G. Marsicano, and U. V. Nägerl, “Two-Photon Excitation STED Microscopy in Two Colors in Acute Brain Slices,” Biophys. J. 104(4), 778–785 (2013).
[Crossref]

Betzig, E.

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]

Bewersdorf, J.

Bhamidimarri, S. P.

T. Ando, S. P. Bhamidimarri, N. Brending, H. Colin-York, L. Collinson, N. De Jonge, P. J. de Pablo, E. Debroye, C. Eggeling, C. Franck, M. Fritzsche, H. Gerritsen, B. N. G. Giepmans, K. Grunewald, J. Hofkens, J. P. Hoogenboom, K. P. F. Janssen, R. Kaufmann, J. Klumpermann, N. Kurniawan, J. Kusch, N. Liv, V. Parekh, D. B. Peckys, F. Rehfeldt, D. C. Reutens, M. B. J. Roeffaers, T. Salditt, I. A. T. Schaap, U. S. Schwarz, P. Verkade, M. W. Vogel, R. Wagner, M. Winterhalter, H. Yuan, and G. Zifarelli, “The 2018 correlative microscopy techniques roadmap,” J. Phys. D: Appl. Phys. 51(44), 443001 (2018).
[Crossref]

Bianchini, P.

P. Bianchini, B. Harke, S. Galiani, G. Vicidomini, and A. Diaspro, “Single-wavelength two-photon excitation-stimulated emission depletion (SW2PE-STED) superresolution imaging,” Proc. Natl. Acad. Sci. 109(17), 6390–6393 (2012).
[Crossref]

Bonacina, L.

L. Bonacina, Y. Mugnier, F. Courvoisier, R. Le Dantec, J. Extermann, Y. Lambert, V. Boutou, C. Galez, and J.-P. Wolf, “Polar Fe(IO3)3 nanocrystals as local probes for nonlinear microscopy,” Appl. Phys. B: Lasers Opt. 87(3), 399–403 (2007).
[Crossref]

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).
[Crossref]

Booth, M. J.

Boruah, B. R.

Bossi, M.

K. I. Willig, J. Keller, M. Bossi, and S. W. Hell, “STED microscopy resolves nanoparticle assemblies,” New J. Phys. 8(6), 106 (2006).
[Crossref]

Boutou, V.

L. Bonacina, Y. Mugnier, F. Courvoisier, R. Le Dantec, J. Extermann, Y. Lambert, V. Boutou, C. Galez, and J.-P. Wolf, “Polar Fe(IO3)3 nanocrystals as local probes for nonlinear microscopy,” Appl. Phys. B: Lasers Opt. 87(3), 399–403 (2007).
[Crossref]

Brending, N.

T. Ando, S. P. Bhamidimarri, N. Brending, H. Colin-York, L. Collinson, N. De Jonge, P. J. de Pablo, E. Debroye, C. Eggeling, C. Franck, M. Fritzsche, H. Gerritsen, B. N. G. Giepmans, K. Grunewald, J. Hofkens, J. P. Hoogenboom, K. P. F. Janssen, R. Kaufmann, J. Klumpermann, N. Kurniawan, J. Kusch, N. Liv, V. Parekh, D. B. Peckys, F. Rehfeldt, D. C. Reutens, M. B. J. Roeffaers, T. Salditt, I. A. T. Schaap, U. S. Schwarz, P. Verkade, M. W. Vogel, R. Wagner, M. Winterhalter, H. Yuan, and G. Zifarelli, “The 2018 correlative microscopy techniques roadmap,” J. Phys. D: Appl. Phys. 51(44), 443001 (2018).
[Crossref]

Burke, D.

Caplan, J.

J. Caplan, M. Niethammer, R. M. Taylor, and K. J. Czymmek, “The Power of Correlative Microscopy: Multi-modal, Multi-scale, Multi-dimensional,” Curr. Opin. Struct. Biol. 21(5), 686–693 (2011).
[Crossref]

Cheng, Y.

Chéreau, R.

P. Bethge, R. Chéreau, E. Avignone, G. Marsicano, and U. V. Nägerl, “Two-Photon Excitation STED Microscopy in Two Colors in Acute Brain Slices,” Biophys. J. 104(4), 778–785 (2013).
[Crossref]

Colin-York, H.

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T. Ando, S. P. Bhamidimarri, N. Brending, H. Colin-York, L. Collinson, N. De Jonge, P. J. de Pablo, E. Debroye, C. Eggeling, C. Franck, M. Fritzsche, H. Gerritsen, B. N. G. Giepmans, K. Grunewald, J. Hofkens, J. P. Hoogenboom, K. P. F. Janssen, R. Kaufmann, J. Klumpermann, N. Kurniawan, J. Kusch, N. Liv, V. Parekh, D. B. Peckys, F. Rehfeldt, D. C. Reutens, M. B. J. Roeffaers, T. Salditt, I. A. T. Schaap, U. S. Schwarz, P. Verkade, M. W. Vogel, R. Wagner, M. Winterhalter, H. Yuan, and G. Zifarelli, “The 2018 correlative microscopy techniques roadmap,” J. Phys. D: Appl. Phys. 51(44), 443001 (2018).
[Crossref]

So, P. T. C.

P. T. C. So, C. Y. Dong, B. R. Masters, and K. M. Berland, “Two-Photon Excitation Fluorescence Microscopy,” Annu. Rev. Biomed. Eng. 2(1), 399–429 (2000).
[Crossref]

Sougrat, R.

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]

Strickler, J. H.

W. Denk, J. H. Strickler, and W. W. Webb, “Two-photon laser scanning fluorescence microscopy,” Science 248(4951), 73–76 (1990).
[Crossref]

Supatto, W.

P. Mahou, M. Zimmerley, K. Loulier, K. S. Matho, G. Labroille, X. Morin, W. Supatto, J. Livet, D. Débarre, and E. Beaurepaire, “Multicolor two-photon tissue imaging by wavelength mixing,” Nat. Methods 9(8), 815–818 (2012).
[Crossref]

Ta, H.

G. Vicidomini, G. Moneron, K. Y. Han, V. Westphal, H. Ta, M. Reuss, J. Engelhardt, C. Eggeling, and S. W. Hell, “Sharper low-power STED nanoscopy by time gating,” Nat. Methods 8(7), 571–573 (2011).
[Crossref]

Taylor, R. M.

J. Caplan, M. Niethammer, R. M. Taylor, and K. J. Czymmek, “The Power of Correlative Microscopy: Multi-modal, Multi-scale, Multi-dimensional,” Curr. Opin. Struct. Biol. 21(5), 686–693 (2011).
[Crossref]

Török, P.

Ullal, C. K.

Verkade, P.

T. Ando, S. P. Bhamidimarri, N. Brending, H. Colin-York, L. Collinson, N. De Jonge, P. J. de Pablo, E. Debroye, C. Eggeling, C. Franck, M. Fritzsche, H. Gerritsen, B. N. G. Giepmans, K. Grunewald, J. Hofkens, J. P. Hoogenboom, K. P. F. Janssen, R. Kaufmann, J. Klumpermann, N. Kurniawan, J. Kusch, N. Liv, V. Parekh, D. B. Peckys, F. Rehfeldt, D. C. Reutens, M. B. J. Roeffaers, T. Salditt, I. A. T. Schaap, U. S. Schwarz, P. Verkade, M. W. Vogel, R. Wagner, M. Winterhalter, H. Yuan, and G. Zifarelli, “The 2018 correlative microscopy techniques roadmap,” J. Phys. D: Appl. Phys. 51(44), 443001 (2018).
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Vial, J.-C.

Vicidomini, G.

P. Bianchini, B. Harke, S. Galiani, G. Vicidomini, and A. Diaspro, “Single-wavelength two-photon excitation-stimulated emission depletion (SW2PE-STED) superresolution imaging,” Proc. Natl. Acad. Sci. 109(17), 6390–6393 (2012).
[Crossref]

G. Vicidomini, G. Moneron, K. Y. Han, V. Westphal, H. Ta, M. Reuss, J. Engelhardt, C. Eggeling, and S. W. Hell, “Sharper low-power STED nanoscopy by time gating,” Nat. Methods 8(7), 571–573 (2011).
[Crossref]

Vogel, M. W.

T. Ando, S. P. Bhamidimarri, N. Brending, H. Colin-York, L. Collinson, N. De Jonge, P. J. de Pablo, E. Debroye, C. Eggeling, C. Franck, M. Fritzsche, H. Gerritsen, B. N. G. Giepmans, K. Grunewald, J. Hofkens, J. P. Hoogenboom, K. P. F. Janssen, R. Kaufmann, J. Klumpermann, N. Kurniawan, J. Kusch, N. Liv, V. Parekh, D. B. Peckys, F. Rehfeldt, D. C. Reutens, M. B. J. Roeffaers, T. Salditt, I. A. T. Schaap, U. S. Schwarz, P. Verkade, M. W. Vogel, R. Wagner, M. Winterhalter, H. Yuan, and G. Zifarelli, “The 2018 correlative microscopy techniques roadmap,” J. Phys. D: Appl. Phys. 51(44), 443001 (2018).
[Crossref]

Wagner, R.

T. Ando, S. P. Bhamidimarri, N. Brending, H. Colin-York, L. Collinson, N. De Jonge, P. J. de Pablo, E. Debroye, C. Eggeling, C. Franck, M. Fritzsche, H. Gerritsen, B. N. G. Giepmans, K. Grunewald, J. Hofkens, J. P. Hoogenboom, K. P. F. Janssen, R. Kaufmann, J. Klumpermann, N. Kurniawan, J. Kusch, N. Liv, V. Parekh, D. B. Peckys, F. Rehfeldt, D. C. Reutens, M. B. J. Roeffaers, T. Salditt, I. A. T. Schaap, U. S. Schwarz, P. Verkade, M. W. Vogel, R. Wagner, M. Winterhalter, H. Yuan, and G. Zifarelli, “The 2018 correlative microscopy techniques roadmap,” J. Phys. D: Appl. Phys. 51(44), 443001 (2018).
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Wang, T.

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W. Denk, J. H. Strickler, and W. W. Webb, “Two-photon laser scanning fluorescence microscopy,” Science 248(4951), 73–76 (1990).
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G. Vicidomini, G. Moneron, K. Y. Han, V. Westphal, H. Ta, M. Reuss, J. Engelhardt, C. Eggeling, and S. W. Hell, “Sharper low-power STED nanoscopy by time gating,” Nat. Methods 8(7), 571–573 (2011).
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B. Harke, J. Keller, C. K. Ullal, V. Westphal, A. Schönle, and S. W. Hell, “Resolution scaling in STED microscopy,” Opt. Express 16(6), 4154–4162 (2008).
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K. I. Willig, S. O. Rizzoli, V. Westphal, R. Jahn, and S. W. Hell, “STED microscopy reveals that synaptotagmin remains clustered after synaptic vesicle exocytosis,” Nature 440(7086), 935–939 (2006).
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K. I. Willig, J. Keller, M. Bossi, and S. W. Hell, “STED microscopy resolves nanoparticle assemblies,” New J. Phys. 8(6), 106 (2006).
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Winterhalter, M.

T. Ando, S. P. Bhamidimarri, N. Brending, H. Colin-York, L. Collinson, N. De Jonge, P. J. de Pablo, E. Debroye, C. Eggeling, C. Franck, M. Fritzsche, H. Gerritsen, B. N. G. Giepmans, K. Grunewald, J. Hofkens, J. P. Hoogenboom, K. P. F. Janssen, R. Kaufmann, J. Klumpermann, N. Kurniawan, J. Kusch, N. Liv, V. Parekh, D. B. Peckys, F. Rehfeldt, D. C. Reutens, M. B. J. Roeffaers, T. Salditt, I. A. T. Schaap, U. S. Schwarz, P. Verkade, M. W. Vogel, R. Wagner, M. Winterhalter, H. Yuan, and G. Zifarelli, “The 2018 correlative microscopy techniques roadmap,” J. Phys. D: Appl. Phys. 51(44), 443001 (2018).
[Crossref]

Wolf, E.

B. Richards and E. Wolf, “Electromagnetic diffraction in optical systems, II. Structure of the image field in an aplanatic system,” Proc. R. Soc. London, Ser. A 253(1274), 358–379 (1959).
[Crossref]

E. Wolf, “Electromagnetic diffraction in optical systems-I. An integral representation of the image field,” Proc. R. Soc. London, Ser. A 253(1274), 349–357 (1959).
[Crossref]

Wolf, J.-P.

L. Bonacina, Y. Mugnier, F. Courvoisier, R. Le Dantec, J. Extermann, Y. Lambert, V. Boutou, C. Galez, and J.-P. Wolf, “Polar Fe(IO3)3 nanocrystals as local probes for nonlinear microscopy,” Appl. Phys. B: Lasers Opt. 87(3), 399–403 (2007).
[Crossref]

Xu, Z.

Yuan, H.

T. Ando, S. P. Bhamidimarri, N. Brending, H. Colin-York, L. Collinson, N. De Jonge, P. J. de Pablo, E. Debroye, C. Eggeling, C. Franck, M. Fritzsche, H. Gerritsen, B. N. G. Giepmans, K. Grunewald, J. Hofkens, J. P. Hoogenboom, K. P. F. Janssen, R. Kaufmann, J. Klumpermann, N. Kurniawan, J. Kusch, N. Liv, V. Parekh, D. B. Peckys, F. Rehfeldt, D. C. Reutens, M. B. J. Roeffaers, T. Salditt, I. A. T. Schaap, U. S. Schwarz, P. Verkade, M. W. Vogel, R. Wagner, M. Winterhalter, H. Yuan, and G. Zifarelli, “The 2018 correlative microscopy techniques roadmap,” J. Phys. D: Appl. Phys. 51(44), 443001 (2018).
[Crossref]

Zhuang, X.

M. J. Rust, M. Bates, and X. Zhuang, “Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM),” Nat. Methods 3(10), 793–796 (2006).
[Crossref]

Zifarelli, G.

T. Ando, S. P. Bhamidimarri, N. Brending, H. Colin-York, L. Collinson, N. De Jonge, P. J. de Pablo, E. Debroye, C. Eggeling, C. Franck, M. Fritzsche, H. Gerritsen, B. N. G. Giepmans, K. Grunewald, J. Hofkens, J. P. Hoogenboom, K. P. F. Janssen, R. Kaufmann, J. Klumpermann, N. Kurniawan, J. Kusch, N. Liv, V. Parekh, D. B. Peckys, F. Rehfeldt, D. C. Reutens, M. B. J. Roeffaers, T. Salditt, I. A. T. Schaap, U. S. Schwarz, P. Verkade, M. W. Vogel, R. Wagner, M. Winterhalter, H. Yuan, and G. Zifarelli, “The 2018 correlative microscopy techniques roadmap,” J. Phys. D: Appl. Phys. 51(44), 443001 (2018).
[Crossref]

Zimmerley, M.

P. Mahou, M. Zimmerley, K. Loulier, K. S. Matho, G. Labroille, X. Morin, W. Supatto, J. Livet, D. Débarre, and E. Beaurepaire, “Multicolor two-photon tissue imaging by wavelength mixing,” Nat. Methods 9(8), 815–818 (2012).
[Crossref]

Zogaj, X.

M. A. Barocchi, J. Ries, X. Zogaj, C. Hemsley, B. Albiger, A. Kanth, S. Dahlberg, J. Fernebro, M. Moschioni, and V. Masignani, “A pneumococcal pilus influences virulence and host inflammatory responses,” Proc. Natl. Acad. Sci. 103(8), 2857–2862 (2006).
[Crossref]

Annu. Rev. Biomed. Eng. (1)

P. T. C. So, C. Y. Dong, B. R. Masters, and K. M. Berland, “Two-Photon Excitation Fluorescence Microscopy,” Annu. Rev. Biomed. Eng. 2(1), 399–429 (2000).
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Appl. Phys. B: Lasers Opt. (1)

L. Bonacina, Y. Mugnier, F. Courvoisier, R. Le Dantec, J. Extermann, Y. Lambert, V. Boutou, C. Galez, and J.-P. Wolf, “Polar Fe(IO3)3 nanocrystals as local probes for nonlinear microscopy,” Appl. Phys. B: Lasers Opt. 87(3), 399–403 (2007).
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E. Abbe, “Beiträge zur Theorie des Mikroskops und der mikroskopischen Wahrnehmung,” Archiv für mikroskopische Anatomie 9(1), 413–418 (1873).
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Biophys. J. (1)

P. Bethge, R. Chéreau, E. Avignone, G. Marsicano, and U. V. Nägerl, “Two-Photon Excitation STED Microscopy in Two Colors in Acute Brain Slices,” Biophys. J. 104(4), 778–785 (2013).
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Curr. Opin. Struct. Biol. (1)

J. Caplan, M. Niethammer, R. M. Taylor, and K. J. Czymmek, “The Power of Correlative Microscopy: Multi-modal, Multi-scale, Multi-dimensional,” Curr. Opin. Struct. Biol. 21(5), 686–693 (2011).
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EMBO J. (1)

M. Hilleringmann, P. Ringler, S. A. Müller, G. De Angelis, R. Rappuoli, I. Ferlenghi, and A. Engel, “Molecular architecture of Streptococcus pneumoniae TIGR4 pili,” EMBO J. 28(24), 3921–3930 (2009).
[Crossref]

J. Opt. (1)

X. Hao, C. Kuang, T. Wang, and X. Liu, “Effects of polarization on the de-excitation dark focal spot in STED microscopy,” J. Opt. 12(11), 115707 (2010).
[Crossref]

J. Phys. D: Appl. Phys. (1)

T. Ando, S. P. Bhamidimarri, N. Brending, H. Colin-York, L. Collinson, N. De Jonge, P. J. de Pablo, E. Debroye, C. Eggeling, C. Franck, M. Fritzsche, H. Gerritsen, B. N. G. Giepmans, K. Grunewald, J. Hofkens, J. P. Hoogenboom, K. P. F. Janssen, R. Kaufmann, J. Klumpermann, N. Kurniawan, J. Kusch, N. Liv, V. Parekh, D. B. Peckys, F. Rehfeldt, D. C. Reutens, M. B. J. Roeffaers, T. Salditt, I. A. T. Schaap, U. S. Schwarz, P. Verkade, M. W. Vogel, R. Wagner, M. Winterhalter, H. Yuan, and G. Zifarelli, “The 2018 correlative microscopy techniques roadmap,” J. Phys. D: Appl. Phys. 51(44), 443001 (2018).
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Mol. Microbiol. (1)

S. Fälker, A. L. Nelson, E. Morfeldt, K. Jonas, K. Hultenby, J. Ries, Ö Melefors, S. Normark, and B. Henriques-Normark, “Sortase-mediated assembly and surface topology of adhesive pneumococcal pili,” Mol. Microbiol. 70(3), 595–607 (2008).
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Nat. Methods (5)

G. Vicidomini, G. Moneron, K. Y. Han, V. Westphal, H. Ta, M. Reuss, J. Engelhardt, C. Eggeling, and S. W. Hell, “Sharper low-power STED nanoscopy by time gating,” Nat. Methods 8(7), 571–573 (2011).
[Crossref]

M. J. Rust, M. Bates, and X. Zhuang, “Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM),” Nat. Methods 3(10), 793–796 (2006).
[Crossref]

P. Mahou, M. Zimmerley, K. Loulier, K. S. Matho, G. Labroille, X. Morin, W. Supatto, J. Livet, D. Débarre, and E. Beaurepaire, “Multicolor two-photon tissue imaging by wavelength mixing,” Nat. Methods 9(8), 815–818 (2012).
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Nat. Photonics (1)

E. Rittweger, K. Y. Han, S. E. Irvine, C. Eggeling, and S. W. Hell, “STED microscopy reveals crystal colour centres with nanometric resolution,” Nat. Photonics 3(3), 144–147 (2009).
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Nature (1)

K. I. Willig, S. O. Rizzoli, V. Westphal, R. Jahn, and S. W. Hell, “STED microscopy reveals that synaptotagmin remains clustered after synaptic vesicle exocytosis,” Nature 440(7086), 935–939 (2006).
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New J. Phys. (1)

K. I. Willig, J. Keller, M. Bossi, and S. W. Hell, “STED microscopy resolves nanoparticle assemblies,” New J. Phys. 8(6), 106 (2006).
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Opt. Lett. (1)

Optica (1)

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Proc. Natl. Acad. Sci. (2)

P. Bianchini, B. Harke, S. Galiani, G. Vicidomini, and A. Diaspro, “Single-wavelength two-photon excitation-stimulated emission depletion (SW2PE-STED) superresolution imaging,” Proc. Natl. Acad. Sci. 109(17), 6390–6393 (2012).
[Crossref]

M. A. Barocchi, J. Ries, X. Zogaj, C. Hemsley, B. Albiger, A. Kanth, S. Dahlberg, J. Fernebro, M. Moschioni, and V. Masignani, “A pneumococcal pilus influences virulence and host inflammatory responses,” Proc. Natl. Acad. Sci. 103(8), 2857–2862 (2006).
[Crossref]

Proc. R. Soc. London, Ser. A (2)

E. Wolf, “Electromagnetic diffraction in optical systems-I. An integral representation of the image field,” Proc. R. Soc. London, Ser. A 253(1274), 349–357 (1959).
[Crossref]

B. Richards and E. Wolf, “Electromagnetic diffraction in optical systems, II. Structure of the image field in an aplanatic system,” Proc. R. Soc. London, Ser. A 253(1274), 358–379 (1959).
[Crossref]

Science (2)

W. Denk, J. H. Strickler, and W. W. Webb, “Two-photon laser scanning fluorescence microscopy,” Science 248(4951), 73–76 (1990).
[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).
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C. Polzer, S. Ness, M. Mohseni, J. Rädler, M. Hilleringmann, and T. Hellerer, “Nanometer-scale colocalization microscopy of Streptococcus pneumoniae filaments,” in Multiphoton Microscopy in the Biomedical Sciences XIX (International Society for Optics and Photonics, 2019), Vol. 10882, p. 108822S.

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Figures (6)

Fig. 1.
Fig. 1. Principle of the 2C2P-STED technique. (a) Simplified Jablonski diagram of the two-color two-photon excitation by absorption of two photons with different wavelengths ${\lambda _1}$ and ${\lambda _2}$. The sum of the photon energies excites the molecule, which in turn requires the spatial overlap of both laser foci. 2C2P is used for excitation of a counterstain in a biological specimen. (b) Jablonski diagram showing the two-photon absorption of photons with wavelength ${\lambda _2}$ and the stimulated emission induced by a photon with wavelength ${\lambda _1}$. This leads to an effective point spread function (PSF) beyond the diffraction limit, if a donut-shaped intensity distribution is applied. 2P-STED is applied for imaging the sub-structure of interest. (c) Despite switching between 2C2P (a) and 2P-STED (b), the laser alignment is well preserved. The overlay of the counterstain and the sub-structure image reveals the spatial correlation of the different components.
Fig. 2.
Fig. 2. (a) Schematic drawing of the experimental setup: DIODE: 775 nm laser, FEMTO: 1034 nm laser, PSD: Picosecond delayer, M: Mirror, T1: Telescope, PBSC: Polarization beam splitter, SLM: spatial light modulator, HWP1/HWP2: zero-order half-waveplates, D1, D2; D3: dichroic mirrors, QWP: achromatic quarter-waveplate, G: resonant-galvo scanner, SL/TL: scan lens/tube lens, OL: objective lens, C: Condensor lens MF: Multiphoton filter, FB/FR/FF: Bandpass filter, PMT: photomultiplier tubes, MPM: Multiphoton microscope. (b) Visualization of the different imaging modalities. 2C2P Imaging: SLM phase is set to a homogeneous gray value of 127 (8-bit), the DIODE laser is set to PICO mode (37 ps), and the time delay is set to zero. STED imaging: A vortex phase from 0 to 2π is applied on the SLM, the DIODE laser is set to STED mode (538 ps), and a time delay of approximately 250 ps is induced.
Fig. 3.
Fig. 3. 2C2P-STED of S. pneumoniae TIGR4 and pili type-1. a) Intensity images of the two separate detector channels. a.1) AlexaFluor594 labeled RrgB components with 2P excitation. a.2) ATTO425 labeled cellular shape applying 2C2P excitation. a.3) STED image of AlexaFluor594 labeled RrgB components. b) Merged images acquired with 2C2P and 2P mode in diffraction limited resolution (left) and with STED microscopy (right). Images are shown in false color (Cyan: ATTO425, Red: AlexaFluor594). Here, the pili or subunits of the pili are predominantly localized at the polar and midcell region. c) The magnified 2C2P-STED image of the bacterium (white arrow in (b)) reveals a separated sub-structure of labeled RrgB pilus-1 components along the equatorial plane. d) Intensity profiles for STED and 2C2P fluorescence along the lines that span between the red and green arrows, respectively. RrgB labeled components in the distance of 70 nm can be clearly distinguished. Scale bar a) and b) 1 µm; c) 500 nm.
Fig. 4.
Fig. 4. Simulation of the intensity distribution in the XY-plane for 2C2P imaging and STED imaging modality. Upper part (2C2P imaging): Normalized intensity distribution of each singular process with $\lambda = 775\; \textrm{nm}$ and $\lambda = 1034\; \textrm{nm}$ for 2C2P imaging. Here, the effective PSF results as the product of the intensity distributions of each focused laser ${I_{2C2P}} = {I_{1034}} \cdot {I_{775}}$ (right column). Lower part (STED imaging): Two-photon excitation intensity distribution with $\lambda = 1034\; \textrm{nm}$ and donut-shaped intensity distribution used for stimulated emission depletion with $\lambda = 775\; \textrm{nm}$. The full width at half maximum (FWHM) of the effective PSFs in each imaging modality is given in the images. In STED imaging the resolution increases with higher STED laser intensities shown in the lower row in the right column.
Fig. 5.
Fig. 5. Cross-correlation of the FEMTO and the PICO laser in steps of 10 ps using SFG. The sample used is Fe(IO3)3. a) Microscopic images of the SFG signal at different time delays (images 1-5). The time dependent intensity signal is evaluated in the region of interest (ROI) shown in image 3. Scale bar: 2 µm b) The cross-correlation directly gives the pulse shape of the PICO laser. Inset: Schematic energy diagram of the SFG process. The main peak has a FWHM of 37 ps. The peak (position 3) is defined as “time-zero”.
Fig. 6.
Fig. 6. a) Phase contrast images of Streptococcus pneumoniae TIGR4. b) 2C2P image of S. pneumoniae cellular shapes. c) 2P image of pilus-1 related RrgB components. d) Energy schemes of potential excitation processes considering 2C2P excitation of ATTO425 at the wavelengths λ1 and λ2. Unwanted background via direct 2P excitation can be avoided if no transition using either λ1 or λ2 is possible. e) Intensity profile along the orange arrow (shown in b)) with 2C2P and direct 2P excitation of ATTO425. Continuous purple: 2C2P. Dashed green: 775 nm. Dotted red: 1030 nm. Scale bar a) – c) 1 µm.

Equations (5)

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

E ( r , ϕ , θ ) = ( E x E y E z ) = i f λ θ ϕ A 0 e γ 2 ( s i n 2 θ s i n 2 α ) c o s θ e i k ( x s i n θ c o s ϕ + y s i n θ s i n ϕ + z c o s θ ) ( c o s θ c o s 2 ϕ + s i n 2 ϕ + i ( c o s ϕ s i n ϕ ( c o s θ 1 ) ) c o s ϕ s i n ϕ ( c o s θ 1 ) + i ( c o s 2 ϕ + c o s θ s i n 2 ϕ ) s i n θ ( c o s ϕ + i s i n ϕ ) ) e i Δ α s i n θ d ϕ d θ
I = | E x | 2 + | E y | 2 + | E z | 2
I 2 C 2 P = I 1 I 2
I 2 P = I 2 2
d = λ 2 N A 1 + ( I I S T E D )

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