Abstract

Most structured illumination microscopes use a physical or syn–thetic grating that is projected into the sample plane to generate a periodic illumination pattern. Albeit simple and cost-effective, this arrangement hampers fast or multi-color acquisition, which is a critical requirement for time-lapse imaging of cellular and sub-cellular dynamics. In this study, we designed and implemented an interferometric approach allowing large-field, fast, dual-color imaging at an isotropic 100-nm resolution based on a sub-diffraction fringe pattern generated by the interference of two colliding evanescent waves. Our all-mirror-based system generates illumination pat-terns of arbitrary orientation and period, limited only by the illumination aperture (NA = 1.45), the response time of a fast, piezo-driven tip-tilt mirror (10 ms) and the available fluorescence signal. At low µW laser powers suitable for long-period observation of life cells and with a camera exposure time of 20 ms, our system permits the acquisition of super-resolved 50 µm by 50 µm images at 3.3 Hz. The possibility it offers for rapidly adjusting the pattern between images is particularly advantageous for experiments that require multi-scale and multi-color information. We demonstrate the performance of our instrument by imaging mitochondrial dynamics in cultured cortical astrocytes. As an illustration of dual-color excitation dual-color detection, we also resolve interaction sites between near-membrane mitochondria and the endoplasmic reticulum. Our TIRF-SIM microscope provides a versatile, compact and cost-effective arrangement for super-resolution imaging, allowing the investigation of co-localization and dynamic interactions between organelles – important questions in both cell biology and neurophysiology

© 2013 Optical Society of America

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  1. R. Heintzmann and M. G. L. Gustafsson, “Subdiffraction resolution in continuous samples,” Nat. Photonics3(7), 362–364 (2009).
    [CrossRef]
  2. B. Huang, “Super-resolution optical microscopy: multiple choices,” Curr. Opin. Chem. Biol.14(1), 10–14 (2010).
    [CrossRef] [PubMed]
  3. B. O. Leung and K. C. Chou, “Review of super-resolution fluorescence microscopy for biology,” Appl. Spectrosc.65(9), 967–980 (2011).
    [CrossRef] [PubMed]
  4. S. W. Hell and J. Wichmann, “Breaking the diffraction resolution limit by stimulated emission: stimulated-emission-depletion fluorescence microscopy,” Opt. Lett.19(11), 780–782 (1994).
    [CrossRef] [PubMed]
  5. 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,” Science313(5793), 1642–1645 (2006).
    [CrossRef] [PubMed]
  6. M. J. Rust, M. Bates, and X. Zhuang, “Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM),” Nat. Methods3(10), 793–796 (2006).
    [CrossRef] [PubMed]
  7. W. Lukosz, “Optical systems with resolving powers exceeding the classical limit,” J. Opt. Soc. Am.56(11), 1463–1471 (1966).
    [CrossRef]
  8. R. Heintzmann and C. Cremer, “Laterally modulated excitation microscopy: improvement of resolution by using a diffraction grating,” Proc. SPIE3568, 185–196 (1999).
    [CrossRef]
  9. M. G. L. Gustafsson, “Surpassing the lateral resolution limit by a factor of two using structured illumination microscopy,” J. Microsc.198(2), 82–87 (2000).
    [CrossRef] [PubMed]
  10. J. T. Frohn, “Super-resolution fluorescence microscopy by structured light illumination,” (Ph.D. thesis, Eidgenössische Technische Hochschule (ETH), Zürich, 2000).
  11. L. M. Hirvonen, K. Wicker, O. Mandula, and R. Heintzmann, “Structured illumination microscopy of a living cell,” Eur. Biophys. J.38(6), 807–812 (2009).
    [CrossRef] [PubMed]
  12. O. Gliko, G. D. Reddy, B. Anvari, W. E. Brownell, and P. Saggau, “Standing wave total internal reflection fluorescence microscopy to measure the size of nanostructures in living cells,” J. Biomed. Opt.11(6), 064013 (2006).
    [CrossRef] [PubMed]
  13. E. Chung, D. Kim, and P. T. C. So, “Extended resolution wide-field optical imaging: objective-launched standing-wave total internal reflection fluorescence microscopy,” Opt. Lett.31(7), 945–947 (2006).
    [CrossRef] [PubMed]
  14. M. Beck, M. Aschwanden, and A. Stemmer, “Sub-100-nanometre resolution in total internal reflection fluorescence microscopy,” J. Microsc.232(1), 99–105 (2008).
    [CrossRef] [PubMed]
  15. E. Chung, D. Kim, Y. Cui, Y. H. Kim, and P. T. C. So, “Two-dimensional standing wave total internal reflection fluorescence microscopy: superresolution imaging of single molecular and biological specimens,” Biophys. J.93(5), 1747–1757 (2007).
    [CrossRef] [PubMed]
  16. R. Fiolka, M. Beck, and A. Stemmer, “Structured illumination in total internal reflection fluorescence microscopy using a spatial light modulator,” Opt. Lett.33(14), 1629–1631 (2008).
    [CrossRef] [PubMed]
  17. O. Gliko, W. E. Brownell, and P. Saggau, “Fast two-dimensional standing-wave total-internal-reflection fluorescence microscopy using acousto-optic deflectors,” Opt. Lett.34(6), 836–838 (2009).
    [CrossRef] [PubMed]
  18. P. Kner, B. B. Chhun, E. R. Griffis, L. Winoto, and M. G. L. Gustafsson, “Super-resolution video microscopy of live cells by structured illumination,” Nat. Methods6(5), 339–342 (2009).
    [CrossRef] [PubMed]
  19. Z. Huang and N. L. Thompson, “Theory for two-photon excitation in pattern photobleaching with evanescent illumination,” Biophys. Chem.47(3), 241–249 (1993).
    [CrossRef] [PubMed]
  20. G. E. Cragg and P. T. C. So, “Lateral resolution enhancement with standing evanescent waves,” Opt. Lett.25(1), 46–48 (2000).
    [CrossRef] [PubMed]
  21. A. L. Stout and D. Axelrod, “Evanescent field excitation of fluorescence by epi-illumination microscopy,” Appl. Opt.28(24), 5237–5242 (1989).
    [CrossRef] [PubMed]
  22. F. Orieux, E. Sepulveda, V. Loriette, B. Dubertret, and J. C. Olivo-Marin, “Bayesian estimation for optimized structured illumination microscopy,” IEEE Trans. Image Process.21(2), 601–614 (2012).
    [CrossRef] [PubMed]
  23. K. Wicker, O. Mandula, G. Best, R. Fiolka, and R. Heintzmann, “Phase optimisation for structured illumination microscopy,” Opt. Express21(2), 2032–2049 (2013).
    [CrossRef] [PubMed]
  24. D. Li, K. Hérault, M. Oheim, and N. Ropert, “FM dyes enter via a store-operated calcium channel and modify calcium signaling of cultured astrocytes,” Proc. Natl. Acad. Sci. U.S.A.106(51), 21960–21965 (2009).
    [CrossRef] [PubMed]
  25. M. Brunstein, M. Teremetz, C. Tourain, and M. Oheim, “Combined evanescent-wave excitation and supercritical-angle fluorescence detection improves optical sectioning,” (arXiv.org>physics> http://arxiv.org/abs/1302.1615 , 2013).
  26. R. Rizzuto, M. R. Duchen, and T. Pozzan, “Flirting in little space: the ER/mitochondria Ca2+ liaison,” Sci. STKE2004(215), re1 (2004).
    [PubMed]
  27. D. A. Rusakov, K. Zheng, and C. Henneberger, “Astrocytes as regulators of synaptic function: A quest for the Ca2+ master key,” Neuroscientist17(5), 513–523 (2011).
    [CrossRef] [PubMed]
  28. R. T. Doyle, M. J. Szulzcewski, and P. G. Haydon, “Extraction of near-field fluorescence from composite signals to provide high resolution images of glial cells,” Biophys. J.80(5), 2477–2482 (2001).
    [CrossRef] [PubMed]
  29. A. Rossi, T. J. Moritz, J. Ratelade, and A. S. Verkman, “Super-resolution imaging of aquaporin-4 orthogonal arrays of particles in cell membranes,” J. Cell Sci.125(18), 4405–4412 (2012).
    [CrossRef] [PubMed]
  30. S. Takahashi, S. Okada, H. Nishioka, S. Usuki, and K. Takamasu, “Theoretical and numerical analysis of lateral resolution improvement characteristics for fluorescence microscopy using standing evanescent light with image retrieval,” Meas. Sci. Technol.19(8), 084006 (2008).
    [CrossRef]
  31. G. Best, R. Amberger, D. Baddeley, T. Ach, S. Dithmar, R. Heintzmann, and C. Cremer, “Structured illumination microscopy of autofluorescent aggregations in human tissue,” Micron42(4), 330–335 (2011).
    [CrossRef] [PubMed]
  32. E. H. Rego, L. Shao, J. J. Macklin, L. Winoto, G. A. Johansson, N. Kamps-Hughes, M. W. Davidson, and M. G. L. Gustafsson, “Nonlinear structured-illumination microscopy with a photoswitchable protein reveals cellular structures at 50-nm resolution,” Proc. Natl. Acad. Sci. U.S.A.109(3), E135–E143 (2012).
    [CrossRef] [PubMed]
  33. E. Mudry, K. Belkebir, J. Girard, E. Le Moal, C. Nicoletti, M. Allain, and A. Sentenac, “Structured illumination microscopy using unknown speckle patterns,” Nat. Photonics6(5), 312–315 (2012).
    [CrossRef]
  34. F. Spira, N. S. Mueller, G. Beck, P. von Olshausen, J. Beig, and R. Wedlich-Söldner, “Patchwork organization of the yeast plasma membrane into numerous coexisting domains,” Nat. Cell Biol.14(6), 640–648 (2012).
    [CrossRef] [PubMed]
  35. M. van ’t Hoff, V. de Sars, and M. Oheim, “A programmable light engine for quantitative single molecule TIRF and HILO imaging,” Opt. Express16(22), 18495–18504 (2008).
    [CrossRef] [PubMed]
  36. S. Chowdhury, A.-H. Dhalla, and J. Izatt, “Structured oblique illumination microscopy for enhanced resolution imaging of non-fluorescent, coherently scattering samples,” Biomed. Opt. Express3(8), 1841–1854 (2012).
    [CrossRef] [PubMed]
  37. K. O’Holleran and M. Shaw, “Polarization effects on contrast in structured illumination microscopy,” Opt. Lett.37(22), 4603–4605 (2012).
    [CrossRef] [PubMed]
  38. A. Sentenac, K. Belkebir, H. Giovannini, and P. C. Chaumet, “Subdiffraction resolution in total internal reflection fluorescence microscopy with a grating substrate,” Opt. Lett.33(3), 255–257 (2008).
    [CrossRef] [PubMed]
  39. F. Schapper, J. T. Gonçalves, and M. Oheim, “Fluorescence imaging with two-photon evanescent wave excitation,” Eur. Biophys. J.32(7), 635–643 (2003).
    [CrossRef] [PubMed]
  40. R. Heintzmann, T. M. Jovin, and C. Cremer, “Saturated patterned excitation microscopy--a concept for optical resolution improvement,” J. Opt. Soc. Am. A19(8), 1599–1609 (2002).
    [CrossRef] [PubMed]
  41. A. Gur, Z. Zalevsky, V. Micó, J. García, and D. Fixler, “The limitations of nonlinear fluorescence effect in super resolution saturated structured illumination microscopy system,” J. Fluoresc.21(3), 1075–1082 (2011).
    [CrossRef] [PubMed]

2013 (1)

2012 (7)

S. Chowdhury, A.-H. Dhalla, and J. Izatt, “Structured oblique illumination microscopy for enhanced resolution imaging of non-fluorescent, coherently scattering samples,” Biomed. Opt. Express3(8), 1841–1854 (2012).
[CrossRef] [PubMed]

K. O’Holleran and M. Shaw, “Polarization effects on contrast in structured illumination microscopy,” Opt. Lett.37(22), 4603–4605 (2012).
[CrossRef] [PubMed]

E. H. Rego, L. Shao, J. J. Macklin, L. Winoto, G. A. Johansson, N. Kamps-Hughes, M. W. Davidson, and M. G. L. Gustafsson, “Nonlinear structured-illumination microscopy with a photoswitchable protein reveals cellular structures at 50-nm resolution,” Proc. Natl. Acad. Sci. U.S.A.109(3), E135–E143 (2012).
[CrossRef] [PubMed]

E. Mudry, K. Belkebir, J. Girard, E. Le Moal, C. Nicoletti, M. Allain, and A. Sentenac, “Structured illumination microscopy using unknown speckle patterns,” Nat. Photonics6(5), 312–315 (2012).
[CrossRef]

F. Spira, N. S. Mueller, G. Beck, P. von Olshausen, J. Beig, and R. Wedlich-Söldner, “Patchwork organization of the yeast plasma membrane into numerous coexisting domains,” Nat. Cell Biol.14(6), 640–648 (2012).
[CrossRef] [PubMed]

F. Orieux, E. Sepulveda, V. Loriette, B. Dubertret, and J. C. Olivo-Marin, “Bayesian estimation for optimized structured illumination microscopy,” IEEE Trans. Image Process.21(2), 601–614 (2012).
[CrossRef] [PubMed]

A. Rossi, T. J. Moritz, J. Ratelade, and A. S. Verkman, “Super-resolution imaging of aquaporin-4 orthogonal arrays of particles in cell membranes,” J. Cell Sci.125(18), 4405–4412 (2012).
[CrossRef] [PubMed]

2011 (4)

G. Best, R. Amberger, D. Baddeley, T. Ach, S. Dithmar, R. Heintzmann, and C. Cremer, “Structured illumination microscopy of autofluorescent aggregations in human tissue,” Micron42(4), 330–335 (2011).
[CrossRef] [PubMed]

A. Gur, Z. Zalevsky, V. Micó, J. García, and D. Fixler, “The limitations of nonlinear fluorescence effect in super resolution saturated structured illumination microscopy system,” J. Fluoresc.21(3), 1075–1082 (2011).
[CrossRef] [PubMed]

D. A. Rusakov, K. Zheng, and C. Henneberger, “Astrocytes as regulators of synaptic function: A quest for the Ca2+ master key,” Neuroscientist17(5), 513–523 (2011).
[CrossRef] [PubMed]

B. O. Leung and K. C. Chou, “Review of super-resolution fluorescence microscopy for biology,” Appl. Spectrosc.65(9), 967–980 (2011).
[CrossRef] [PubMed]

2010 (1)

B. Huang, “Super-resolution optical microscopy: multiple choices,” Curr. Opin. Chem. Biol.14(1), 10–14 (2010).
[CrossRef] [PubMed]

2009 (5)

R. Heintzmann and M. G. L. Gustafsson, “Subdiffraction resolution in continuous samples,” Nat. Photonics3(7), 362–364 (2009).
[CrossRef]

L. M. Hirvonen, K. Wicker, O. Mandula, and R. Heintzmann, “Structured illumination microscopy of a living cell,” Eur. Biophys. J.38(6), 807–812 (2009).
[CrossRef] [PubMed]

D. Li, K. Hérault, M. Oheim, and N. Ropert, “FM dyes enter via a store-operated calcium channel and modify calcium signaling of cultured astrocytes,” Proc. Natl. Acad. Sci. U.S.A.106(51), 21960–21965 (2009).
[CrossRef] [PubMed]

P. Kner, B. B. Chhun, E. R. Griffis, L. Winoto, and M. G. L. Gustafsson, “Super-resolution video microscopy of live cells by structured illumination,” Nat. Methods6(5), 339–342 (2009).
[CrossRef] [PubMed]

O. Gliko, W. E. Brownell, and P. Saggau, “Fast two-dimensional standing-wave total-internal-reflection fluorescence microscopy using acousto-optic deflectors,” Opt. Lett.34(6), 836–838 (2009).
[CrossRef] [PubMed]

2008 (5)

A. Sentenac, K. Belkebir, H. Giovannini, and P. C. Chaumet, “Subdiffraction resolution in total internal reflection fluorescence microscopy with a grating substrate,” Opt. Lett.33(3), 255–257 (2008).
[CrossRef] [PubMed]

R. Fiolka, M. Beck, and A. Stemmer, “Structured illumination in total internal reflection fluorescence microscopy using a spatial light modulator,” Opt. Lett.33(14), 1629–1631 (2008).
[CrossRef] [PubMed]

M. van ’t Hoff, V. de Sars, and M. Oheim, “A programmable light engine for quantitative single molecule TIRF and HILO imaging,” Opt. Express16(22), 18495–18504 (2008).
[CrossRef] [PubMed]

S. Takahashi, S. Okada, H. Nishioka, S. Usuki, and K. Takamasu, “Theoretical and numerical analysis of lateral resolution improvement characteristics for fluorescence microscopy using standing evanescent light with image retrieval,” Meas. Sci. Technol.19(8), 084006 (2008).
[CrossRef]

M. Beck, M. Aschwanden, and A. Stemmer, “Sub-100-nanometre resolution in total internal reflection fluorescence microscopy,” J. Microsc.232(1), 99–105 (2008).
[CrossRef] [PubMed]

2007 (1)

E. Chung, D. Kim, Y. Cui, Y. H. Kim, and P. T. C. So, “Two-dimensional standing wave total internal reflection fluorescence microscopy: superresolution imaging of single molecular and biological specimens,” Biophys. J.93(5), 1747–1757 (2007).
[CrossRef] [PubMed]

2006 (4)

O. Gliko, G. D. Reddy, B. Anvari, W. E. Brownell, and P. Saggau, “Standing wave total internal reflection fluorescence microscopy to measure the size of nanostructures in living cells,” J. Biomed. Opt.11(6), 064013 (2006).
[CrossRef] [PubMed]

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,” Science313(5793), 1642–1645 (2006).
[CrossRef] [PubMed]

M. J. Rust, M. Bates, and X. Zhuang, “Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM),” Nat. Methods3(10), 793–796 (2006).
[CrossRef] [PubMed]

E. Chung, D. Kim, and P. T. C. So, “Extended resolution wide-field optical imaging: objective-launched standing-wave total internal reflection fluorescence microscopy,” Opt. Lett.31(7), 945–947 (2006).
[CrossRef] [PubMed]

2004 (1)

R. Rizzuto, M. R. Duchen, and T. Pozzan, “Flirting in little space: the ER/mitochondria Ca2+ liaison,” Sci. STKE2004(215), re1 (2004).
[PubMed]

2003 (1)

F. Schapper, J. T. Gonçalves, and M. Oheim, “Fluorescence imaging with two-photon evanescent wave excitation,” Eur. Biophys. J.32(7), 635–643 (2003).
[CrossRef] [PubMed]

2002 (1)

2001 (1)

R. T. Doyle, M. J. Szulzcewski, and P. G. Haydon, “Extraction of near-field fluorescence from composite signals to provide high resolution images of glial cells,” Biophys. J.80(5), 2477–2482 (2001).
[CrossRef] [PubMed]

2000 (2)

M. G. L. Gustafsson, “Surpassing the lateral resolution limit by a factor of two using structured illumination microscopy,” J. Microsc.198(2), 82–87 (2000).
[CrossRef] [PubMed]

G. E. Cragg and P. T. C. So, “Lateral resolution enhancement with standing evanescent waves,” Opt. Lett.25(1), 46–48 (2000).
[CrossRef] [PubMed]

1999 (1)

R. Heintzmann and C. Cremer, “Laterally modulated excitation microscopy: improvement of resolution by using a diffraction grating,” Proc. SPIE3568, 185–196 (1999).
[CrossRef]

1994 (1)

1993 (1)

Z. Huang and N. L. Thompson, “Theory for two-photon excitation in pattern photobleaching with evanescent illumination,” Biophys. Chem.47(3), 241–249 (1993).
[CrossRef] [PubMed]

1989 (1)

1966 (1)

Ach, T.

G. Best, R. Amberger, D. Baddeley, T. Ach, S. Dithmar, R. Heintzmann, and C. Cremer, “Structured illumination microscopy of autofluorescent aggregations in human tissue,” Micron42(4), 330–335 (2011).
[CrossRef] [PubMed]

Allain, M.

E. Mudry, K. Belkebir, J. Girard, E. Le Moal, C. Nicoletti, M. Allain, and A. Sentenac, “Structured illumination microscopy using unknown speckle patterns,” Nat. Photonics6(5), 312–315 (2012).
[CrossRef]

Amberger, R.

G. Best, R. Amberger, D. Baddeley, T. Ach, S. Dithmar, R. Heintzmann, and C. Cremer, “Structured illumination microscopy of autofluorescent aggregations in human tissue,” Micron42(4), 330–335 (2011).
[CrossRef] [PubMed]

Anvari, B.

O. Gliko, G. D. Reddy, B. Anvari, W. E. Brownell, and P. Saggau, “Standing wave total internal reflection fluorescence microscopy to measure the size of nanostructures in living cells,” J. Biomed. Opt.11(6), 064013 (2006).
[CrossRef] [PubMed]

Aschwanden, M.

M. Beck, M. Aschwanden, and A. Stemmer, “Sub-100-nanometre resolution in total internal reflection fluorescence microscopy,” J. Microsc.232(1), 99–105 (2008).
[CrossRef] [PubMed]

Axelrod, D.

Baddeley, D.

G. Best, R. Amberger, D. Baddeley, T. Ach, S. Dithmar, R. Heintzmann, and C. Cremer, “Structured illumination microscopy of autofluorescent aggregations in human tissue,” Micron42(4), 330–335 (2011).
[CrossRef] [PubMed]

Bates, M.

M. J. Rust, M. Bates, and X. Zhuang, “Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM),” Nat. Methods3(10), 793–796 (2006).
[CrossRef] [PubMed]

Beck, G.

F. Spira, N. S. Mueller, G. Beck, P. von Olshausen, J. Beig, and R. Wedlich-Söldner, “Patchwork organization of the yeast plasma membrane into numerous coexisting domains,” Nat. Cell Biol.14(6), 640–648 (2012).
[CrossRef] [PubMed]

Beck, M.

R. Fiolka, M. Beck, and A. Stemmer, “Structured illumination in total internal reflection fluorescence microscopy using a spatial light modulator,” Opt. Lett.33(14), 1629–1631 (2008).
[CrossRef] [PubMed]

M. Beck, M. Aschwanden, and A. Stemmer, “Sub-100-nanometre resolution in total internal reflection fluorescence microscopy,” J. Microsc.232(1), 99–105 (2008).
[CrossRef] [PubMed]

Beig, J.

F. Spira, N. S. Mueller, G. Beck, P. von Olshausen, J. Beig, and R. Wedlich-Söldner, “Patchwork organization of the yeast plasma membrane into numerous coexisting domains,” Nat. Cell Biol.14(6), 640–648 (2012).
[CrossRef] [PubMed]

Belkebir, K.

E. Mudry, K. Belkebir, J. Girard, E. Le Moal, C. Nicoletti, M. Allain, and A. Sentenac, “Structured illumination microscopy using unknown speckle patterns,” Nat. Photonics6(5), 312–315 (2012).
[CrossRef]

A. Sentenac, K. Belkebir, H. Giovannini, and P. C. Chaumet, “Subdiffraction resolution in total internal reflection fluorescence microscopy with a grating substrate,” Opt. Lett.33(3), 255–257 (2008).
[CrossRef] [PubMed]

Best, G.

K. Wicker, O. Mandula, G. Best, R. Fiolka, and R. Heintzmann, “Phase optimisation for structured illumination microscopy,” Opt. Express21(2), 2032–2049 (2013).
[CrossRef] [PubMed]

G. Best, R. Amberger, D. Baddeley, T. Ach, S. Dithmar, R. Heintzmann, and C. Cremer, “Structured illumination microscopy of autofluorescent aggregations in human tissue,” Micron42(4), 330–335 (2011).
[CrossRef] [PubMed]

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,” Science313(5793), 1642–1645 (2006).
[CrossRef] [PubMed]

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,” Science313(5793), 1642–1645 (2006).
[CrossRef] [PubMed]

Brownell, W. E.

O. Gliko, W. E. Brownell, and P. Saggau, “Fast two-dimensional standing-wave total-internal-reflection fluorescence microscopy using acousto-optic deflectors,” Opt. Lett.34(6), 836–838 (2009).
[CrossRef] [PubMed]

O. Gliko, G. D. Reddy, B. Anvari, W. E. Brownell, and P. Saggau, “Standing wave total internal reflection fluorescence microscopy to measure the size of nanostructures in living cells,” J. Biomed. Opt.11(6), 064013 (2006).
[CrossRef] [PubMed]

Chaumet, P. C.

Chhun, B. B.

P. Kner, B. B. Chhun, E. R. Griffis, L. Winoto, and M. G. L. Gustafsson, “Super-resolution video microscopy of live cells by structured illumination,” Nat. Methods6(5), 339–342 (2009).
[CrossRef] [PubMed]

Chou, K. C.

Chowdhury, S.

Chung, E.

E. Chung, D. Kim, Y. Cui, Y. H. Kim, and P. T. C. So, “Two-dimensional standing wave total internal reflection fluorescence microscopy: superresolution imaging of single molecular and biological specimens,” Biophys. J.93(5), 1747–1757 (2007).
[CrossRef] [PubMed]

E. Chung, D. Kim, and P. T. C. So, “Extended resolution wide-field optical imaging: objective-launched standing-wave total internal reflection fluorescence microscopy,” Opt. Lett.31(7), 945–947 (2006).
[CrossRef] [PubMed]

Cragg, G. E.

Cremer, C.

G. Best, R. Amberger, D. Baddeley, T. Ach, S. Dithmar, R. Heintzmann, and C. Cremer, “Structured illumination microscopy of autofluorescent aggregations in human tissue,” Micron42(4), 330–335 (2011).
[CrossRef] [PubMed]

R. Heintzmann, T. M. Jovin, and C. Cremer, “Saturated patterned excitation microscopy--a concept for optical resolution improvement,” J. Opt. Soc. Am. A19(8), 1599–1609 (2002).
[CrossRef] [PubMed]

R. Heintzmann and C. Cremer, “Laterally modulated excitation microscopy: improvement of resolution by using a diffraction grating,” Proc. SPIE3568, 185–196 (1999).
[CrossRef]

Cui, Y.

E. Chung, D. Kim, Y. Cui, Y. H. Kim, and P. T. C. So, “Two-dimensional standing wave total internal reflection fluorescence microscopy: superresolution imaging of single molecular and biological specimens,” Biophys. J.93(5), 1747–1757 (2007).
[CrossRef] [PubMed]

Davidson, M. W.

E. H. Rego, L. Shao, J. J. Macklin, L. Winoto, G. A. Johansson, N. Kamps-Hughes, M. W. Davidson, and M. G. L. Gustafsson, “Nonlinear structured-illumination microscopy with a photoswitchable protein reveals cellular structures at 50-nm resolution,” Proc. Natl. Acad. Sci. U.S.A.109(3), E135–E143 (2012).
[CrossRef] [PubMed]

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,” Science313(5793), 1642–1645 (2006).
[CrossRef] [PubMed]

de Sars, V.

Dhalla, A.-H.

Dithmar, S.

G. Best, R. Amberger, D. Baddeley, T. Ach, S. Dithmar, R. Heintzmann, and C. Cremer, “Structured illumination microscopy of autofluorescent aggregations in human tissue,” Micron42(4), 330–335 (2011).
[CrossRef] [PubMed]

Doyle, R. T.

R. T. Doyle, M. J. Szulzcewski, and P. G. Haydon, “Extraction of near-field fluorescence from composite signals to provide high resolution images of glial cells,” Biophys. J.80(5), 2477–2482 (2001).
[CrossRef] [PubMed]

Dubertret, B.

F. Orieux, E. Sepulveda, V. Loriette, B. Dubertret, and J. C. Olivo-Marin, “Bayesian estimation for optimized structured illumination microscopy,” IEEE Trans. Image Process.21(2), 601–614 (2012).
[CrossRef] [PubMed]

Duchen, M. R.

R. Rizzuto, M. R. Duchen, and T. Pozzan, “Flirting in little space: the ER/mitochondria Ca2+ liaison,” Sci. STKE2004(215), re1 (2004).
[PubMed]

Fiolka, R.

Fixler, D.

A. Gur, Z. Zalevsky, V. Micó, J. García, and D. Fixler, “The limitations of nonlinear fluorescence effect in super resolution saturated structured illumination microscopy system,” J. Fluoresc.21(3), 1075–1082 (2011).
[CrossRef] [PubMed]

García, J.

A. Gur, Z. Zalevsky, V. Micó, J. García, and D. Fixler, “The limitations of nonlinear fluorescence effect in super resolution saturated structured illumination microscopy system,” J. Fluoresc.21(3), 1075–1082 (2011).
[CrossRef] [PubMed]

Giovannini, H.

Girard, J.

E. Mudry, K. Belkebir, J. Girard, E. Le Moal, C. Nicoletti, M. Allain, and A. Sentenac, “Structured illumination microscopy using unknown speckle patterns,” Nat. Photonics6(5), 312–315 (2012).
[CrossRef]

Gliko, O.

O. Gliko, W. E. Brownell, and P. Saggau, “Fast two-dimensional standing-wave total-internal-reflection fluorescence microscopy using acousto-optic deflectors,” Opt. Lett.34(6), 836–838 (2009).
[CrossRef] [PubMed]

O. Gliko, G. D. Reddy, B. Anvari, W. E. Brownell, and P. Saggau, “Standing wave total internal reflection fluorescence microscopy to measure the size of nanostructures in living cells,” J. Biomed. Opt.11(6), 064013 (2006).
[CrossRef] [PubMed]

Gonçalves, J. T.

F. Schapper, J. T. Gonçalves, and M. Oheim, “Fluorescence imaging with two-photon evanescent wave excitation,” Eur. Biophys. J.32(7), 635–643 (2003).
[CrossRef] [PubMed]

Griffis, E. R.

P. Kner, B. B. Chhun, E. R. Griffis, L. Winoto, and M. G. L. Gustafsson, “Super-resolution video microscopy of live cells by structured illumination,” Nat. Methods6(5), 339–342 (2009).
[CrossRef] [PubMed]

Gur, A.

A. Gur, Z. Zalevsky, V. Micó, J. García, and D. Fixler, “The limitations of nonlinear fluorescence effect in super resolution saturated structured illumination microscopy system,” J. Fluoresc.21(3), 1075–1082 (2011).
[CrossRef] [PubMed]

Gustafsson, M. G. L.

E. H. Rego, L. Shao, J. J. Macklin, L. Winoto, G. A. Johansson, N. Kamps-Hughes, M. W. Davidson, and M. G. L. Gustafsson, “Nonlinear structured-illumination microscopy with a photoswitchable protein reveals cellular structures at 50-nm resolution,” Proc. Natl. Acad. Sci. U.S.A.109(3), E135–E143 (2012).
[CrossRef] [PubMed]

P. Kner, B. B. Chhun, E. R. Griffis, L. Winoto, and M. G. L. Gustafsson, “Super-resolution video microscopy of live cells by structured illumination,” Nat. Methods6(5), 339–342 (2009).
[CrossRef] [PubMed]

R. Heintzmann and M. G. L. Gustafsson, “Subdiffraction resolution in continuous samples,” Nat. Photonics3(7), 362–364 (2009).
[CrossRef]

M. G. L. Gustafsson, “Surpassing the lateral resolution limit by a factor of two using structured illumination microscopy,” J. Microsc.198(2), 82–87 (2000).
[CrossRef] [PubMed]

Haydon, P. G.

R. T. Doyle, M. J. Szulzcewski, and P. G. Haydon, “Extraction of near-field fluorescence from composite signals to provide high resolution images of glial cells,” Biophys. J.80(5), 2477–2482 (2001).
[CrossRef] [PubMed]

Heintzmann, R.

K. Wicker, O. Mandula, G. Best, R. Fiolka, and R. Heintzmann, “Phase optimisation for structured illumination microscopy,” Opt. Express21(2), 2032–2049 (2013).
[CrossRef] [PubMed]

G. Best, R. Amberger, D. Baddeley, T. Ach, S. Dithmar, R. Heintzmann, and C. Cremer, “Structured illumination microscopy of autofluorescent aggregations in human tissue,” Micron42(4), 330–335 (2011).
[CrossRef] [PubMed]

L. M. Hirvonen, K. Wicker, O. Mandula, and R. Heintzmann, “Structured illumination microscopy of a living cell,” Eur. Biophys. J.38(6), 807–812 (2009).
[CrossRef] [PubMed]

R. Heintzmann and M. G. L. Gustafsson, “Subdiffraction resolution in continuous samples,” Nat. Photonics3(7), 362–364 (2009).
[CrossRef]

R. Heintzmann, T. M. Jovin, and C. Cremer, “Saturated patterned excitation microscopy--a concept for optical resolution improvement,” J. Opt. Soc. Am. A19(8), 1599–1609 (2002).
[CrossRef] [PubMed]

R. Heintzmann and C. Cremer, “Laterally modulated excitation microscopy: improvement of resolution by using a diffraction grating,” Proc. SPIE3568, 185–196 (1999).
[CrossRef]

Hell, S. W.

Henneberger, C.

D. A. Rusakov, K. Zheng, and C. Henneberger, “Astrocytes as regulators of synaptic function: A quest for the Ca2+ master key,” Neuroscientist17(5), 513–523 (2011).
[CrossRef] [PubMed]

Hérault, K.

D. Li, K. Hérault, M. Oheim, and N. Ropert, “FM dyes enter via a store-operated calcium channel and modify calcium signaling of cultured astrocytes,” Proc. Natl. Acad. Sci. U.S.A.106(51), 21960–21965 (2009).
[CrossRef] [PubMed]

Hess, H. F.

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,” Science313(5793), 1642–1645 (2006).
[CrossRef] [PubMed]

Hirvonen, L. M.

L. M. Hirvonen, K. Wicker, O. Mandula, and R. Heintzmann, “Structured illumination microscopy of a living cell,” Eur. Biophys. J.38(6), 807–812 (2009).
[CrossRef] [PubMed]

Huang, B.

B. Huang, “Super-resolution optical microscopy: multiple choices,” Curr. Opin. Chem. Biol.14(1), 10–14 (2010).
[CrossRef] [PubMed]

Huang, Z.

Z. Huang and N. L. Thompson, “Theory for two-photon excitation in pattern photobleaching with evanescent illumination,” Biophys. Chem.47(3), 241–249 (1993).
[CrossRef] [PubMed]

Izatt, J.

Johansson, G. A.

E. H. Rego, L. Shao, J. J. Macklin, L. Winoto, G. A. Johansson, N. Kamps-Hughes, M. W. Davidson, and M. G. L. Gustafsson, “Nonlinear structured-illumination microscopy with a photoswitchable protein reveals cellular structures at 50-nm resolution,” Proc. Natl. Acad. Sci. U.S.A.109(3), E135–E143 (2012).
[CrossRef] [PubMed]

Jovin, T. M.

Kamps-Hughes, N.

E. H. Rego, L. Shao, J. J. Macklin, L. Winoto, G. A. Johansson, N. Kamps-Hughes, M. W. Davidson, and M. G. L. Gustafsson, “Nonlinear structured-illumination microscopy with a photoswitchable protein reveals cellular structures at 50-nm resolution,” Proc. Natl. Acad. Sci. U.S.A.109(3), E135–E143 (2012).
[CrossRef] [PubMed]

Kim, D.

E. Chung, D. Kim, Y. Cui, Y. H. Kim, and P. T. C. So, “Two-dimensional standing wave total internal reflection fluorescence microscopy: superresolution imaging of single molecular and biological specimens,” Biophys. J.93(5), 1747–1757 (2007).
[CrossRef] [PubMed]

E. Chung, D. Kim, and P. T. C. So, “Extended resolution wide-field optical imaging: objective-launched standing-wave total internal reflection fluorescence microscopy,” Opt. Lett.31(7), 945–947 (2006).
[CrossRef] [PubMed]

Kim, Y. H.

E. Chung, D. Kim, Y. Cui, Y. H. Kim, and P. T. C. So, “Two-dimensional standing wave total internal reflection fluorescence microscopy: superresolution imaging of single molecular and biological specimens,” Biophys. J.93(5), 1747–1757 (2007).
[CrossRef] [PubMed]

Kner, P.

P. Kner, B. B. Chhun, E. R. Griffis, L. Winoto, and M. G. L. Gustafsson, “Super-resolution video microscopy of live cells by structured illumination,” Nat. Methods6(5), 339–342 (2009).
[CrossRef] [PubMed]

Le Moal, E.

E. Mudry, K. Belkebir, J. Girard, E. Le Moal, C. Nicoletti, M. Allain, and A. Sentenac, “Structured illumination microscopy using unknown speckle patterns,” Nat. Photonics6(5), 312–315 (2012).
[CrossRef]

Leung, B. O.

Li, D.

D. Li, K. Hérault, M. Oheim, and N. Ropert, “FM dyes enter via a store-operated calcium channel and modify calcium signaling of cultured astrocytes,” Proc. Natl. Acad. Sci. U.S.A.106(51), 21960–21965 (2009).
[CrossRef] [PubMed]

Lindwasser, O. W.

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,” Science313(5793), 1642–1645 (2006).
[CrossRef] [PubMed]

Lippincott-Schwartz, J.

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,” Science313(5793), 1642–1645 (2006).
[CrossRef] [PubMed]

Loriette, V.

F. Orieux, E. Sepulveda, V. Loriette, B. Dubertret, and J. C. Olivo-Marin, “Bayesian estimation for optimized structured illumination microscopy,” IEEE Trans. Image Process.21(2), 601–614 (2012).
[CrossRef] [PubMed]

Lukosz, W.

Macklin, J. J.

E. H. Rego, L. Shao, J. J. Macklin, L. Winoto, G. A. Johansson, N. Kamps-Hughes, M. W. Davidson, and M. G. L. Gustafsson, “Nonlinear structured-illumination microscopy with a photoswitchable protein reveals cellular structures at 50-nm resolution,” Proc. Natl. Acad. Sci. U.S.A.109(3), E135–E143 (2012).
[CrossRef] [PubMed]

Mandula, O.

K. Wicker, O. Mandula, G. Best, R. Fiolka, and R. Heintzmann, “Phase optimisation for structured illumination microscopy,” Opt. Express21(2), 2032–2049 (2013).
[CrossRef] [PubMed]

L. M. Hirvonen, K. Wicker, O. Mandula, and R. Heintzmann, “Structured illumination microscopy of a living cell,” Eur. Biophys. J.38(6), 807–812 (2009).
[CrossRef] [PubMed]

Micó, V.

A. Gur, Z. Zalevsky, V. Micó, J. García, and D. Fixler, “The limitations of nonlinear fluorescence effect in super resolution saturated structured illumination microscopy system,” J. Fluoresc.21(3), 1075–1082 (2011).
[CrossRef] [PubMed]

Moritz, T. J.

A. Rossi, T. J. Moritz, J. Ratelade, and A. S. Verkman, “Super-resolution imaging of aquaporin-4 orthogonal arrays of particles in cell membranes,” J. Cell Sci.125(18), 4405–4412 (2012).
[CrossRef] [PubMed]

Mudry, E.

E. Mudry, K. Belkebir, J. Girard, E. Le Moal, C. Nicoletti, M. Allain, and A. Sentenac, “Structured illumination microscopy using unknown speckle patterns,” Nat. Photonics6(5), 312–315 (2012).
[CrossRef]

Mueller, N. S.

F. Spira, N. S. Mueller, G. Beck, P. von Olshausen, J. Beig, and R. Wedlich-Söldner, “Patchwork organization of the yeast plasma membrane into numerous coexisting domains,” Nat. Cell Biol.14(6), 640–648 (2012).
[CrossRef] [PubMed]

Nicoletti, C.

E. Mudry, K. Belkebir, J. Girard, E. Le Moal, C. Nicoletti, M. Allain, and A. Sentenac, “Structured illumination microscopy using unknown speckle patterns,” Nat. Photonics6(5), 312–315 (2012).
[CrossRef]

Nishioka, H.

S. Takahashi, S. Okada, H. Nishioka, S. Usuki, and K. Takamasu, “Theoretical and numerical analysis of lateral resolution improvement characteristics for fluorescence microscopy using standing evanescent light with image retrieval,” Meas. Sci. Technol.19(8), 084006 (2008).
[CrossRef]

O’Holleran, K.

Oheim, M.

D. Li, K. Hérault, M. Oheim, and N. Ropert, “FM dyes enter via a store-operated calcium channel and modify calcium signaling of cultured astrocytes,” Proc. Natl. Acad. Sci. U.S.A.106(51), 21960–21965 (2009).
[CrossRef] [PubMed]

M. van ’t Hoff, V. de Sars, and M. Oheim, “A programmable light engine for quantitative single molecule TIRF and HILO imaging,” Opt. Express16(22), 18495–18504 (2008).
[CrossRef] [PubMed]

F. Schapper, J. T. Gonçalves, and M. Oheim, “Fluorescence imaging with two-photon evanescent wave excitation,” Eur. Biophys. J.32(7), 635–643 (2003).
[CrossRef] [PubMed]

Okada, S.

S. Takahashi, S. Okada, H. Nishioka, S. Usuki, and K. Takamasu, “Theoretical and numerical analysis of lateral resolution improvement characteristics for fluorescence microscopy using standing evanescent light with image retrieval,” Meas. Sci. Technol.19(8), 084006 (2008).
[CrossRef]

Olenych, 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,” Science313(5793), 1642–1645 (2006).
[CrossRef] [PubMed]

Olivo-Marin, J. C.

F. Orieux, E. Sepulveda, V. Loriette, B. Dubertret, and J. C. Olivo-Marin, “Bayesian estimation for optimized structured illumination microscopy,” IEEE Trans. Image Process.21(2), 601–614 (2012).
[CrossRef] [PubMed]

Orieux, F.

F. Orieux, E. Sepulveda, V. Loriette, B. Dubertret, and J. C. Olivo-Marin, “Bayesian estimation for optimized structured illumination microscopy,” IEEE Trans. Image Process.21(2), 601–614 (2012).
[CrossRef] [PubMed]

Patterson, G. H.

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,” Science313(5793), 1642–1645 (2006).
[CrossRef] [PubMed]

Pozzan, T.

R. Rizzuto, M. R. Duchen, and T. Pozzan, “Flirting in little space: the ER/mitochondria Ca2+ liaison,” Sci. STKE2004(215), re1 (2004).
[PubMed]

Ratelade, J.

A. Rossi, T. J. Moritz, J. Ratelade, and A. S. Verkman, “Super-resolution imaging of aquaporin-4 orthogonal arrays of particles in cell membranes,” J. Cell Sci.125(18), 4405–4412 (2012).
[CrossRef] [PubMed]

Reddy, G. D.

O. Gliko, G. D. Reddy, B. Anvari, W. E. Brownell, and P. Saggau, “Standing wave total internal reflection fluorescence microscopy to measure the size of nanostructures in living cells,” J. Biomed. Opt.11(6), 064013 (2006).
[CrossRef] [PubMed]

Rego, E. H.

E. H. Rego, L. Shao, J. J. Macklin, L. Winoto, G. A. Johansson, N. Kamps-Hughes, M. W. Davidson, and M. G. L. Gustafsson, “Nonlinear structured-illumination microscopy with a photoswitchable protein reveals cellular structures at 50-nm resolution,” Proc. Natl. Acad. Sci. U.S.A.109(3), E135–E143 (2012).
[CrossRef] [PubMed]

Rizzuto, R.

R. Rizzuto, M. R. Duchen, and T. Pozzan, “Flirting in little space: the ER/mitochondria Ca2+ liaison,” Sci. STKE2004(215), re1 (2004).
[PubMed]

Ropert, N.

D. Li, K. Hérault, M. Oheim, and N. Ropert, “FM dyes enter via a store-operated calcium channel and modify calcium signaling of cultured astrocytes,” Proc. Natl. Acad. Sci. U.S.A.106(51), 21960–21965 (2009).
[CrossRef] [PubMed]

Rossi, A.

A. Rossi, T. J. Moritz, J. Ratelade, and A. S. Verkman, “Super-resolution imaging of aquaporin-4 orthogonal arrays of particles in cell membranes,” J. Cell Sci.125(18), 4405–4412 (2012).
[CrossRef] [PubMed]

Rusakov, D. A.

D. A. Rusakov, K. Zheng, and C. Henneberger, “Astrocytes as regulators of synaptic function: A quest for the Ca2+ master key,” Neuroscientist17(5), 513–523 (2011).
[CrossRef] [PubMed]

Rust, M. J.

M. J. Rust, M. Bates, and X. Zhuang, “Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM),” Nat. Methods3(10), 793–796 (2006).
[CrossRef] [PubMed]

Saggau, P.

O. Gliko, W. E. Brownell, and P. Saggau, “Fast two-dimensional standing-wave total-internal-reflection fluorescence microscopy using acousto-optic deflectors,” Opt. Lett.34(6), 836–838 (2009).
[CrossRef] [PubMed]

O. Gliko, G. D. Reddy, B. Anvari, W. E. Brownell, and P. Saggau, “Standing wave total internal reflection fluorescence microscopy to measure the size of nanostructures in living cells,” J. Biomed. Opt.11(6), 064013 (2006).
[CrossRef] [PubMed]

Schapper, F.

F. Schapper, J. T. Gonçalves, and M. Oheim, “Fluorescence imaging with two-photon evanescent wave excitation,” Eur. Biophys. J.32(7), 635–643 (2003).
[CrossRef] [PubMed]

Sentenac, A.

E. Mudry, K. Belkebir, J. Girard, E. Le Moal, C. Nicoletti, M. Allain, and A. Sentenac, “Structured illumination microscopy using unknown speckle patterns,” Nat. Photonics6(5), 312–315 (2012).
[CrossRef]

A. Sentenac, K. Belkebir, H. Giovannini, and P. C. Chaumet, “Subdiffraction resolution in total internal reflection fluorescence microscopy with a grating substrate,” Opt. Lett.33(3), 255–257 (2008).
[CrossRef] [PubMed]

Sepulveda, E.

F. Orieux, E. Sepulveda, V. Loriette, B. Dubertret, and J. C. Olivo-Marin, “Bayesian estimation for optimized structured illumination microscopy,” IEEE Trans. Image Process.21(2), 601–614 (2012).
[CrossRef] [PubMed]

Shao, L.

E. H. Rego, L. Shao, J. J. Macklin, L. Winoto, G. A. Johansson, N. Kamps-Hughes, M. W. Davidson, and M. G. L. Gustafsson, “Nonlinear structured-illumination microscopy with a photoswitchable protein reveals cellular structures at 50-nm resolution,” Proc. Natl. Acad. Sci. U.S.A.109(3), E135–E143 (2012).
[CrossRef] [PubMed]

Shaw, M.

So, P. T. C.

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,” Science313(5793), 1642–1645 (2006).
[CrossRef] [PubMed]

Spira, F.

F. Spira, N. S. Mueller, G. Beck, P. von Olshausen, J. Beig, and R. Wedlich-Söldner, “Patchwork organization of the yeast plasma membrane into numerous coexisting domains,” Nat. Cell Biol.14(6), 640–648 (2012).
[CrossRef] [PubMed]

Stemmer, A.

R. Fiolka, M. Beck, and A. Stemmer, “Structured illumination in total internal reflection fluorescence microscopy using a spatial light modulator,” Opt. Lett.33(14), 1629–1631 (2008).
[CrossRef] [PubMed]

M. Beck, M. Aschwanden, and A. Stemmer, “Sub-100-nanometre resolution in total internal reflection fluorescence microscopy,” J. Microsc.232(1), 99–105 (2008).
[CrossRef] [PubMed]

Stout, A. L.

Szulzcewski, M. J.

R. T. Doyle, M. J. Szulzcewski, and P. G. Haydon, “Extraction of near-field fluorescence from composite signals to provide high resolution images of glial cells,” Biophys. J.80(5), 2477–2482 (2001).
[CrossRef] [PubMed]

Takahashi, S.

S. Takahashi, S. Okada, H. Nishioka, S. Usuki, and K. Takamasu, “Theoretical and numerical analysis of lateral resolution improvement characteristics for fluorescence microscopy using standing evanescent light with image retrieval,” Meas. Sci. Technol.19(8), 084006 (2008).
[CrossRef]

Takamasu, K.

S. Takahashi, S. Okada, H. Nishioka, S. Usuki, and K. Takamasu, “Theoretical and numerical analysis of lateral resolution improvement characteristics for fluorescence microscopy using standing evanescent light with image retrieval,” Meas. Sci. Technol.19(8), 084006 (2008).
[CrossRef]

Thompson, N. L.

Z. Huang and N. L. Thompson, “Theory for two-photon excitation in pattern photobleaching with evanescent illumination,” Biophys. Chem.47(3), 241–249 (1993).
[CrossRef] [PubMed]

Usuki, S.

S. Takahashi, S. Okada, H. Nishioka, S. Usuki, and K. Takamasu, “Theoretical and numerical analysis of lateral resolution improvement characteristics for fluorescence microscopy using standing evanescent light with image retrieval,” Meas. Sci. Technol.19(8), 084006 (2008).
[CrossRef]

van ’t Hoff, M.

Verkman, A. S.

A. Rossi, T. J. Moritz, J. Ratelade, and A. S. Verkman, “Super-resolution imaging of aquaporin-4 orthogonal arrays of particles in cell membranes,” J. Cell Sci.125(18), 4405–4412 (2012).
[CrossRef] [PubMed]

von Olshausen, P.

F. Spira, N. S. Mueller, G. Beck, P. von Olshausen, J. Beig, and R. Wedlich-Söldner, “Patchwork organization of the yeast plasma membrane into numerous coexisting domains,” Nat. Cell Biol.14(6), 640–648 (2012).
[CrossRef] [PubMed]

Wedlich-Söldner, R.

F. Spira, N. S. Mueller, G. Beck, P. von Olshausen, J. Beig, and R. Wedlich-Söldner, “Patchwork organization of the yeast plasma membrane into numerous coexisting domains,” Nat. Cell Biol.14(6), 640–648 (2012).
[CrossRef] [PubMed]

Wichmann, J.

Wicker, K.

K. Wicker, O. Mandula, G. Best, R. Fiolka, and R. Heintzmann, “Phase optimisation for structured illumination microscopy,” Opt. Express21(2), 2032–2049 (2013).
[CrossRef] [PubMed]

L. M. Hirvonen, K. Wicker, O. Mandula, and R. Heintzmann, “Structured illumination microscopy of a living cell,” Eur. Biophys. J.38(6), 807–812 (2009).
[CrossRef] [PubMed]

Winoto, L.

E. H. Rego, L. Shao, J. J. Macklin, L. Winoto, G. A. Johansson, N. Kamps-Hughes, M. W. Davidson, and M. G. L. Gustafsson, “Nonlinear structured-illumination microscopy with a photoswitchable protein reveals cellular structures at 50-nm resolution,” Proc. Natl. Acad. Sci. U.S.A.109(3), E135–E143 (2012).
[CrossRef] [PubMed]

P. Kner, B. B. Chhun, E. R. Griffis, L. Winoto, and M. G. L. Gustafsson, “Super-resolution video microscopy of live cells by structured illumination,” Nat. Methods6(5), 339–342 (2009).
[CrossRef] [PubMed]

Zalevsky, Z.

A. Gur, Z. Zalevsky, V. Micó, J. García, and D. Fixler, “The limitations of nonlinear fluorescence effect in super resolution saturated structured illumination microscopy system,” J. Fluoresc.21(3), 1075–1082 (2011).
[CrossRef] [PubMed]

Zheng, K.

D. A. Rusakov, K. Zheng, and C. Henneberger, “Astrocytes as regulators of synaptic function: A quest for the Ca2+ master key,” Neuroscientist17(5), 513–523 (2011).
[CrossRef] [PubMed]

Zhuang, X.

M. J. Rust, M. Bates, and X. Zhuang, “Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM),” Nat. Methods3(10), 793–796 (2006).
[CrossRef] [PubMed]

Appl. Opt. (1)

Appl. Spectrosc. (1)

Biomed. Opt. Express (1)

Biophys. Chem. (1)

Z. Huang and N. L. Thompson, “Theory for two-photon excitation in pattern photobleaching with evanescent illumination,” Biophys. Chem.47(3), 241–249 (1993).
[CrossRef] [PubMed]

Biophys. J. (2)

E. Chung, D. Kim, Y. Cui, Y. H. Kim, and P. T. C. So, “Two-dimensional standing wave total internal reflection fluorescence microscopy: superresolution imaging of single molecular and biological specimens,” Biophys. J.93(5), 1747–1757 (2007).
[CrossRef] [PubMed]

R. T. Doyle, M. J. Szulzcewski, and P. G. Haydon, “Extraction of near-field fluorescence from composite signals to provide high resolution images of glial cells,” Biophys. J.80(5), 2477–2482 (2001).
[CrossRef] [PubMed]

Curr. Opin. Chem. Biol. (1)

B. Huang, “Super-resolution optical microscopy: multiple choices,” Curr. Opin. Chem. Biol.14(1), 10–14 (2010).
[CrossRef] [PubMed]

Eur. Biophys. J. (2)

L. M. Hirvonen, K. Wicker, O. Mandula, and R. Heintzmann, “Structured illumination microscopy of a living cell,” Eur. Biophys. J.38(6), 807–812 (2009).
[CrossRef] [PubMed]

F. Schapper, J. T. Gonçalves, and M. Oheim, “Fluorescence imaging with two-photon evanescent wave excitation,” Eur. Biophys. J.32(7), 635–643 (2003).
[CrossRef] [PubMed]

IEEE Trans. Image Process. (1)

F. Orieux, E. Sepulveda, V. Loriette, B. Dubertret, and J. C. Olivo-Marin, “Bayesian estimation for optimized structured illumination microscopy,” IEEE Trans. Image Process.21(2), 601–614 (2012).
[CrossRef] [PubMed]

J. Biomed. Opt. (1)

O. Gliko, G. D. Reddy, B. Anvari, W. E. Brownell, and P. Saggau, “Standing wave total internal reflection fluorescence microscopy to measure the size of nanostructures in living cells,” J. Biomed. Opt.11(6), 064013 (2006).
[CrossRef] [PubMed]

J. Cell Sci. (1)

A. Rossi, T. J. Moritz, J. Ratelade, and A. S. Verkman, “Super-resolution imaging of aquaporin-4 orthogonal arrays of particles in cell membranes,” J. Cell Sci.125(18), 4405–4412 (2012).
[CrossRef] [PubMed]

J. Fluoresc. (1)

A. Gur, Z. Zalevsky, V. Micó, J. García, and D. Fixler, “The limitations of nonlinear fluorescence effect in super resolution saturated structured illumination microscopy system,” J. Fluoresc.21(3), 1075–1082 (2011).
[CrossRef] [PubMed]

J. Microsc. (2)

M. Beck, M. Aschwanden, and A. Stemmer, “Sub-100-nanometre resolution in total internal reflection fluorescence microscopy,” J. Microsc.232(1), 99–105 (2008).
[CrossRef] [PubMed]

M. G. L. Gustafsson, “Surpassing the lateral resolution limit by a factor of two using structured illumination microscopy,” J. Microsc.198(2), 82–87 (2000).
[CrossRef] [PubMed]

J. Opt. Soc. Am. (1)

J. Opt. Soc. Am. A (1)

Meas. Sci. Technol. (1)

S. Takahashi, S. Okada, H. Nishioka, S. Usuki, and K. Takamasu, “Theoretical and numerical analysis of lateral resolution improvement characteristics for fluorescence microscopy using standing evanescent light with image retrieval,” Meas. Sci. Technol.19(8), 084006 (2008).
[CrossRef]

Micron (1)

G. Best, R. Amberger, D. Baddeley, T. Ach, S. Dithmar, R. Heintzmann, and C. Cremer, “Structured illumination microscopy of autofluorescent aggregations in human tissue,” Micron42(4), 330–335 (2011).
[CrossRef] [PubMed]

Nat. Cell Biol. (1)

F. Spira, N. S. Mueller, G. Beck, P. von Olshausen, J. Beig, and R. Wedlich-Söldner, “Patchwork organization of the yeast plasma membrane into numerous coexisting domains,” Nat. Cell Biol.14(6), 640–648 (2012).
[CrossRef] [PubMed]

Nat. Methods (2)

P. Kner, B. B. Chhun, E. R. Griffis, L. Winoto, and M. G. L. Gustafsson, “Super-resolution video microscopy of live cells by structured illumination,” Nat. Methods6(5), 339–342 (2009).
[CrossRef] [PubMed]

M. J. Rust, M. Bates, and X. Zhuang, “Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM),” Nat. Methods3(10), 793–796 (2006).
[CrossRef] [PubMed]

Nat. Photonics (2)

R. Heintzmann and M. G. L. Gustafsson, “Subdiffraction resolution in continuous samples,” Nat. Photonics3(7), 362–364 (2009).
[CrossRef]

E. Mudry, K. Belkebir, J. Girard, E. Le Moal, C. Nicoletti, M. Allain, and A. Sentenac, “Structured illumination microscopy using unknown speckle patterns,” Nat. Photonics6(5), 312–315 (2012).
[CrossRef]

Neuroscientist (1)

D. A. Rusakov, K. Zheng, and C. Henneberger, “Astrocytes as regulators of synaptic function: A quest for the Ca2+ master key,” Neuroscientist17(5), 513–523 (2011).
[CrossRef] [PubMed]

Opt. Express (2)

Opt. Lett. (7)

Proc. Natl. Acad. Sci. U.S.A. (2)

D. Li, K. Hérault, M. Oheim, and N. Ropert, “FM dyes enter via a store-operated calcium channel and modify calcium signaling of cultured astrocytes,” Proc. Natl. Acad. Sci. U.S.A.106(51), 21960–21965 (2009).
[CrossRef] [PubMed]

E. H. Rego, L. Shao, J. J. Macklin, L. Winoto, G. A. Johansson, N. Kamps-Hughes, M. W. Davidson, and M. G. L. Gustafsson, “Nonlinear structured-illumination microscopy with a photoswitchable protein reveals cellular structures at 50-nm resolution,” Proc. Natl. Acad. Sci. U.S.A.109(3), E135–E143 (2012).
[CrossRef] [PubMed]

Proc. SPIE (1)

R. Heintzmann and C. Cremer, “Laterally modulated excitation microscopy: improvement of resolution by using a diffraction grating,” Proc. SPIE3568, 185–196 (1999).
[CrossRef]

Sci. STKE (1)

R. Rizzuto, M. R. Duchen, and T. Pozzan, “Flirting in little space: the ER/mitochondria Ca2+ liaison,” Sci. STKE2004(215), re1 (2004).
[PubMed]

Science (1)

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,” Science313(5793), 1642–1645 (2006).
[CrossRef] [PubMed]

Other (2)

J. T. Frohn, “Super-resolution fluorescence microscopy by structured light illumination,” (Ph.D. thesis, Eidgenössische Technische Hochschule (ETH), Zürich, 2000).

M. Brunstein, M. Teremetz, C. Tourain, and M. Oheim, “Combined evanescent-wave excitation and supercritical-angle fluorescence detection improves optical sectioning,” (arXiv.org>physics> http://arxiv.org/abs/1302.1615 , 2013).

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Figures (6)

Fig. 1
Fig. 1

, Schematic layout of the excitation optical path of our compact custom TIRF-SIM. Laser: 488-nm OPSL/561-nm DPPS, λ/2: wave plate, TT: tip/tilt-mirror, BS: 50/50-beam splitter, RE: retro-reflector, PI: piezoelectric actuator, M1, M2: mirrors, FL: f = 300-mm focusing lens, DC: dichroic, TL: tube lens (f = 300mm), obj: × 60/NA1.45 PlanApo objective, BFP: back-focal plane, CS: coverslip. See main text for details. Inset, measured interference patterns created at the sample plane and schematic focused-spot positions in the objective BFP.

Fig. 2
Fig. 2

TIRF-SIM multi-color imaging at 100-nm resolution. TIRF (A) and TIRF-SIM (B) images of 93-nm diameter green-fluorescent beads (ex./em. maxima 505/515 nm), integration time 20 ms per image. Insets (top), zoom on individual bead, scale bar: 0.5 µm. (bottom), Fourier transforms (FT) of the TIRF and TIRF-SIM images show the increased spatial-frequency band-pass. (C), Representative fluorescence-intensity profiles of beads imaged in TIRF and TIRF-SIM, respectively. Excitation was at 488 for the left (same green-fluorescent bead as depicted in (A),(B), red line), and middle panel (red-emitting bead). Right: 561-nm excitation of a yellow-green emitting bead. Images were taken with a pattern period s of 175 nm at 20-ms integration time (i.e., 306 ms for acquisition of nine images used for the calculation of final super-resolved image). We used low µW laser powers in the sample plane.

Fig. 3
Fig. 3

Resistance to sample movement. Sequence of TIRF (A) and TIRF-SIM (B) images of green-fluorescent beads (505/515nm) moving at 230 nm/s. The whole sample was translated on a piezo-stage and 20-ms images were acquired at 3.3 Hz. Red dashed line serves as a reference for the eye. Note the sample displacement to the right (red arrow). Contrast inverted for better clarity in print. Scale bar: 1 µm.

Fig. 4
Fig. 4

TIRF-SIM imaging of near-membrane mitochondrial dynamics. (A), whole-filed image of an astrocyte expressing mito-EGFP, integration time 20 ms per image (306 ms per to obtain the super-resolved full-field image, s = 180 nm). (B), 3.3-Hz time-lapse sequences showing mitochondrial dynamics in the zoom region shown in (A). Scale bar: 1 µm. (C), Distance travelled vs. time of the leading edge of the mitochondrium identified with a red arrow head on panel (B). The speed of tip displacement obtained from a linear fit was υ = 1.24 ± 0.06 µm/s.

Fig. 5
Fig. 5

Dual-color superresolution imaging. TIRF (A) and TIRF-SIM (B) images of an astrocyte expressing ER-EGFP, a marker of the endoplasmic reticulum, and labeled with Mito-Tracker-Deep-Red, a marker of mitochondria. Images were taken sequentially upon 488- and 561-nm excitation, respectively, with no emission filter. Exposure time was 200 ms per frame (total time: 3.8s for the acquisition of the two colors). Pattern period was 180 nm (206 nm) for the green (red) channel, respectively. (C) Zoom on the region of interest shown in (A), (B). Scale bar: 1 µm. (D) Intensity profiles, along the line region of interest shown in (A) and (B), for the ER (green) and mitochondria (red) reveal the increase in image contrast and resolution.

Fig. 6
Fig. 6

Different options for optimizing fringe pattern contrast. Left, unrotated “vertical polarization” provides high contrast vertical fringes but low contrast in other directions. Middle left, ideally, polarization would rotate with the pattern to assure tangential s-polarization to give optimal contrast. Middle right, circular polarization produces constant but low fringe contrast. We used instead an unrotated “horizontal polarization” (right) corresponding to a local maximum in fringe contrast. The precise polarization angle depends on the given objective NA, beam angle and pattern directions. See ref [37]. for details.

Tables (1)

Tables Icon

Table 1 Measured full-width at half-maximum diameters (FWHMmeas) of 93-nm fluorescent beads excited at 488 or 561 nm. FWHMPSF values are corrected for the finite bead size. Numbers are means ± SD for n = 10 beads for each color.

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