Abstract

Sub-diffraction resolution imaging has played a pivotal role in biological research by visualizing key, but previously unresolvable, sub-cellular structures. Unfortunately, applications of far-field sub-diffraction resolution are currently divided between fluorescent and coherent-diffraction regimes, and a multimodal sub-diffraction technique that bridges this gap has not yet been demonstrated. Here we report that structured illumination (SI) allows multimodal sub-diffraction imaging of both coherent quantitative-phase (QP) and fluorescence. Due to SI’s conventionally fluorescent applications, we first demonstrate the principle of SI-enabled three-dimensional (3D) QP sub-diffraction imaging with calibration microspheres. Image analysis confirmed enhanced lateral and axial resolutions over diffraction-limited QP imaging, and established striking parallels between coherent SI and conventional optical diffraction tomography. We next introduce an optical system utilizing SI to achieve 3D sub-diffraction, multimodal QP/fluorescent visualization of A549 biological cells fluorescently tagged for F-actin. Our results suggest that SI has a unique utility in studying biological phenomena with significant molecular, biophysical, and biochemical components.

© 2017 Optical Society of America

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References

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2016 (2)

W. J. Eldridge, A. Sheinfeld, M. T. Rinehart, and A. Wax, “Imaging deformation of adherent cells due to shear stress using quantitative phase imaging,” Opt. Lett. 41(2), 352–355 (2016).
[Crossref] [PubMed]

R. Horstmeyer, R. Heintzmann, G. Popescu, L. Waller, and C. Yang, “Standardizing the resolution claims for coherent microscopy,” Nat. Photonics 10(2), 68–71 (2016).
[Crossref]

2015 (5)

2014 (4)

L. Tian, X. Li, K. Ramchandran, and L. Waller, “Multiplexed coded illumination for Fourier Ptychography with an LED array microscope,” Biomed. Opt. Express 5(7), 2376–2389 (2014).
[Crossref] [PubMed]

S. Chowdhury and J. Izatt, “Structured illumination diffraction phase microscopy for broadband, subdiffraction resolution, quantitative phase imaging,” Opt. Lett. 39(4), 1015–1018 (2014).
[Crossref] [PubMed]

J. Zheng, P. Gao, B. Yao, T. Ye, M. Lei, J. Min, D. Dan, Y. Yang, and S. Yan, “Digital holographic microscopy with phase-shift-free structured illumination,” Photonics Research 2(3), 87–91 (2014).
[Crossref]

B. Bhaduri, C. Edwards, H. Pham, R. Zhou, T. H. Nguyen, L. L. Goddard, and G. Popescu, “Diffraction phase microscopy: principles and applications in materials and life sciences,” Adv. Opt. Photonics 6(1), 57–119 (2014).
[Crossref]

2013 (6)

2012 (3)

R. Fiolka, L. Shao, E. H. Rego, M. W. Davidson, and M. G. Gustafsson, “Time-lapse two-color 3D imaging of live cells with doubled resolution using structured illumination,” Proc. Natl. Acad. Sci. U.S.A. 109(14), 5311–5315 (2012).
[Crossref] [PubMed]

S. Chowdhury, A.-H. Dhalla, and J. Izatt, “Structured oblique illumination microscopy for enhanced resolution imaging of non-fluorescent, coherently scattering samples,” Biomed. Opt. Express 3(8), 1841–1854 (2012).
[Crossref] [PubMed]

I. Akopova, S. Tatur, M. Grygorczyk, R. Luchowski, I. Gryczynski, Z. Gryczynski, J. Borejdo, and R. Grygorczyk, “Imaging exocytosis of ATP-containing vesicles with TIRF microscopy in lung epithelial A549 cells,” Purinergic Signal. 8(1), 59–70 (2012).
[Crossref] [PubMed]

2011 (4)

L. Shao, P. Kner, E. H. Rego, and M. G. Gustafsson, “Super-resolution 3D microscopy of live whole cells using structured illumination,” Nat. Methods 8(12), 1044–1046 (2011).
[Crossref] [PubMed]

F. E. Robles, C. Wilson, G. Grant, and A. Wax, “Molecular imaging true-colour spectroscopic optical coherence tomography,” Nat. Photonics 5(12), 744–747 (2011).
[Crossref] [PubMed]

R. Wang, Z. Wang, L. Millet, M. U. Gillette, A. J. Levine, and G. Popescu, “Dispersion-relation phase spectroscopy of intracellular transport,” Opt. Express 19(21), 20571–20579 (2011).
[Crossref] [PubMed]

M. Kim, Y. Choi, C. Fang-Yen, Y. Sung, R. R. Dasari, M. S. Feld, and W. Choi, “High-speed synthetic aperture microscopy for live cell imaging,” Opt. Lett. 36(2), 148–150 (2011).
[Crossref] [PubMed]

2010 (3)

2009 (4)

2008 (4)

M. G. Gustafsson, L. Shao, P. M. Carlton, C. J. Wang, I. N. Golubovskaya, W. Z. Cande, D. A. Agard, and J. W. Sedat, “Three-dimensional resolution doubling in wide-field fluorescence microscopy by structured illumination,” Biophys. J. 94(12), 4957–4970 (2008).
[Crossref] [PubMed]

G. Popescu, Y. Park, N. Lue, C. Best-Popescu, L. Deflores, R. R. Dasari, M. S. Feld, and K. Badizadegan, “Optical imaging of cell mass and growth dynamics,” Am. J. Physiol. Cell Physiol. 295(2), C538–C544 (2008).
[Crossref] [PubMed]

B. Hein, K. I. Willig, and S. W. Hell, “Stimulated emission depletion (STED) nanoscopy of a fluorescent protein-labeled organelle inside a living cell,” Proc. Natl. Acad. Sci. U.S.A. 105(38), 14271–14276 (2008).
[Crossref] [PubMed]

P. Langehanenberg, B. Kemper, D. Dirksen, and G. von Bally, “Autofocusing in digital holographic phase contrast microscopy on pure phase objects for live cell imaging,” Appl. Opt. 47(19), D176–D182 (2008).
[Crossref] [PubMed]

2007 (1)

2006 (6)

V. Mico, Z. Zalevsky, P. García-Martínez, and J. García, “Synthetic aperture superresolution with multiple off-axis holograms,” J. Opt. Soc. Am. A 23(12), 3162–3170 (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,” Science 313(5793), 1642–1645 (2006).
[Crossref] [PubMed]

Y. L. Jin, J. Y. Chen, L. Xu, and P. N. Wang, “Refractive index measurement for biomaterial samples by total internal reflection,” Phys. Med. Biol. 51(20), N371–N379 (2006).
[Crossref] [PubMed]

Y. Park, G. Popescu, K. Badizadegan, R. R. Dasari, and M. S. Feld, “Diffraction phase and fluorescence microscopy,” Opt. Express 14(18), 8263–8268 (2006).
[Crossref] [PubMed]

R. Heintzmann and G. Ficz, “Breaking the resolution limit in light microscopy,” Brief. Funct. Genomics Proteomics 5(4), 289–301 (2006).
[Crossref] [PubMed]

S. Van Aert, D. Van Dyck, and A. J. den Dekker, “Resolution of coherent and incoherent imaging systems reconsidered - Classical criteria and a statistical alternative,” Opt. Express 14(9), 3830–3839 (2006).
[Crossref] [PubMed]

2005 (2)

2003 (1)

S. Hu, J. Chen, B. Fabry, Y. Numaguchi, A. Gouldstone, D. E. Ingber, J. J. Fredberg, J. P. Butler, and N. Wang, “Intracellular stress tomography reveals stress focusing and structural anisotropy in cytoskeleton of living cells,” Am. J. Physiol. Cell Physiol. 285(5), C1082–C1090 (2003).
[Crossref] [PubMed]

2002 (2)

V. Lauer, “New approach to optical diffraction tomography yielding a vector equation of diffraction tomography and a novel tomographic microscope,” J. Microsc. 205(2), 165–176 (2002).
[Crossref] [PubMed]

M. Okuda, K. Li, M. R. Beard, L. A. Showalter, F. Scholle, S. M. Lemon, and S. A. Weinman, “Mitochondrial injury, oxidative stress, and antioxidant gene expression are induced by hepatitis C virus core protein,” Gastroenterology 122(2), 366–375 (2002).
[Crossref] [PubMed]

2001 (1)

N. Wang, K. Naruse, D. Stamenović, J. J. Fredberg, S. M. Mijailovich, I. M. Tolić-Nørrelykke, T. Polte, R. Mannix, and D. E. Ingber, “Mechanical behavior in living cells consistent with the tensegrity model,” Proc. Natl. Acad. Sci. U.S.A. 98(14), 7765–7770 (2001).
[Crossref] [PubMed]

2000 (2)

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

V. Backman, M. B. Wallace, L. T. Perelman, J. T. Arendt, R. Gurjar, M. G. Müller, Q. Zhang, G. Zonios, E. Kline, J. A. McGilligan, S. Shapshay, T. Valdez, K. Badizadegan, J. M. Crawford, M. Fitzmaurice, S. Kabani, H. S. Levin, M. Seiler, R. R. Dasari, I. Itzkan, J. Van Dam, and M. S. Feld, “Detection of preinvasive cancer cells,” Nature 406(6791), 35–36 (2000).
[Crossref] [PubMed]

1998 (1)

P. A. Janmey, “The cytoskeleton and cell signaling: component localization and mechanical coupling,” Physiol. Rev. 78(3), 763–781 (1998).
[PubMed]

1997 (2)

J. G. Flannery, S. Zolotukhin, M. I. Vaquero, M. M. LaVail, N. Muzyczka, and W. W. Hauswirth, “Efficient photoreceptor-targeted gene expression in vivo by recombinant adeno-associated virus,” Proc. Natl. Acad. Sci. U.S.A. 94(13), 6916–6921 (1997).
[Crossref] [PubMed]

O. Seksek, J. Biwersi, and A. S. Verkman, “Translational diffusion of macromolecule-sized solutes in cytoplasm and nucleus,” J. Cell Biol. 138(1), 131–142 (1997).
[Crossref] [PubMed]

1992 (1)

1975 (1)

V. Nayyar, “Rayleigh two-point resolution by a semi-transparent and φ-phase annular optical system operating in partially coherent light,” Opt. Commun. 13(3), 254–258 (1975).
[Crossref]

1962 (1)

R. Barakat, “Application of apodization to increase two-point resolution by the Sparrow criterion. I. Coherent illumination,” JOSA 52(3), 276–283 (1962).
[Crossref]

Agard, D. A.

M. G. Gustafsson, L. Shao, P. M. Carlton, C. J. Wang, I. N. Golubovskaya, W. Z. Cande, D. A. Agard, and J. W. Sedat, “Three-dimensional resolution doubling in wide-field fluorescence microscopy by structured illumination,” Biophys. J. 94(12), 4957–4970 (2008).
[Crossref] [PubMed]

Akopova, I.

I. Akopova, S. Tatur, M. Grygorczyk, R. Luchowski, I. Gryczynski, Z. Gryczynski, J. Borejdo, and R. Grygorczyk, “Imaging exocytosis of ATP-containing vesicles with TIRF microscopy in lung epithelial A549 cells,” Purinergic Signal. 8(1), 59–70 (2012).
[Crossref] [PubMed]

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V. Backman, M. B. Wallace, L. T. Perelman, J. T. Arendt, R. Gurjar, M. G. Müller, Q. Zhang, G. Zonios, E. Kline, J. A. McGilligan, S. Shapshay, T. Valdez, K. Badizadegan, J. M. Crawford, M. Fitzmaurice, S. Kabani, H. S. Levin, M. Seiler, R. R. Dasari, I. Itzkan, J. Van Dam, and M. S. Feld, “Detection of preinvasive cancer cells,” Nature 406(6791), 35–36 (2000).
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Van Dam, J.

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Van Dyck, D.

Vaquero, M. I.

J. G. Flannery, S. Zolotukhin, M. I. Vaquero, M. M. LaVail, N. Muzyczka, and W. W. Hauswirth, “Efficient photoreceptor-targeted gene expression in vivo by recombinant adeno-associated virus,” Proc. Natl. Acad. Sci. U.S.A. 94(13), 6916–6921 (1997).
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O. Seksek, J. Biwersi, and A. S. Verkman, “Translational diffusion of macromolecule-sized solutes in cytoplasm and nucleus,” J. Cell Biol. 138(1), 131–142 (1997).
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V. Backman, M. B. Wallace, L. T. Perelman, J. T. Arendt, R. Gurjar, M. G. Müller, Q. Zhang, G. Zonios, E. Kline, J. A. McGilligan, S. Shapshay, T. Valdez, K. Badizadegan, J. M. Crawford, M. Fitzmaurice, S. Kabani, H. S. Levin, M. Seiler, R. R. Dasari, I. Itzkan, J. Van Dam, and M. S. Feld, “Detection of preinvasive cancer cells,” Nature 406(6791), 35–36 (2000).
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Waller, L.

R. Horstmeyer, R. Heintzmann, G. Popescu, L. Waller, and C. Yang, “Standardizing the resolution claims for coherent microscopy,” Nat. Photonics 10(2), 68–71 (2016).
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M. G. Gustafsson, L. Shao, P. M. Carlton, C. J. Wang, I. N. Golubovskaya, W. Z. Cande, D. A. Agard, and J. W. Sedat, “Three-dimensional resolution doubling in wide-field fluorescence microscopy by structured illumination,” Biophys. J. 94(12), 4957–4970 (2008).
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Wang, N.

S. Hu, J. Chen, B. Fabry, Y. Numaguchi, A. Gouldstone, D. E. Ingber, J. J. Fredberg, J. P. Butler, and N. Wang, “Intracellular stress tomography reveals stress focusing and structural anisotropy in cytoskeleton of living cells,” Am. J. Physiol. Cell Physiol. 285(5), C1082–C1090 (2003).
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N. Wang, K. Naruse, D. Stamenović, J. J. Fredberg, S. M. Mijailovich, I. M. Tolić-Nørrelykke, T. Polte, R. Mannix, and D. E. Ingber, “Mechanical behavior in living cells consistent with the tensegrity model,” Proc. Natl. Acad. Sci. U.S.A. 98(14), 7765–7770 (2001).
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Wang, P. N.

Y. L. Jin, J. Y. Chen, L. Xu, and P. N. Wang, “Refractive index measurement for biomaterial samples by total internal reflection,” Phys. Med. Biol. 51(20), N371–N379 (2006).
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Wang, R.

Wang, Z.

Wax, A.

Weinman, S. A.

M. Okuda, K. Li, M. R. Beard, L. A. Showalter, F. Scholle, S. M. Lemon, and S. A. Weinman, “Mitochondrial injury, oxidative stress, and antioxidant gene expression are induced by hepatitis C virus core protein,” Gastroenterology 122(2), 366–375 (2002).
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Wicker, K.

Willig, K. I.

B. Hein, K. I. Willig, and S. W. Hell, “Stimulated emission depletion (STED) nanoscopy of a fluorescent protein-labeled organelle inside a living cell,” Proc. Natl. Acad. Sci. U.S.A. 105(38), 14271–14276 (2008).
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Wilson, C.

F. E. Robles, C. Wilson, G. Grant, and A. Wax, “Molecular imaging true-colour spectroscopic optical coherence tomography,” Nat. Photonics 5(12), 744–747 (2011).
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Winoto, L.

P. Kner, B. B. Chhun, E. R. Griffis, L. Winoto, and M. G. Gustafsson, “Super-resolution video microscopy of live cells by structured illumination,” Nat. Methods 6(5), 339–342 (2009).
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Xu, L.

Y. L. Jin, J. Y. Chen, L. Xu, and P. N. Wang, “Refractive index measurement for biomaterial samples by total internal reflection,” Phys. Med. Biol. 51(20), N371–N379 (2006).
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Xu, P.

D. Li, L. Shao, B.-C. Chen, X. Zhang, M. Zhang, B. Moses, D. E. Milkie, J. R. Beach, J. A. Hammer, M. Pasham, T. Kirchhausen, M. A. Baird, M. W. Davidson, P. Xu, and E. Betzig, “Extended-resolution structured illumination imaging of endocytic and cytoskeletal dynamics,” Science 349(6251), aab3500 (2015).
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Yan, S.

J. Zheng, P. Gao, B. Yao, T. Ye, M. Lei, J. Min, D. Dan, Y. Yang, and S. Yan, “Digital holographic microscopy with phase-shift-free structured illumination,” Photonics Research 2(3), 87–91 (2014).
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R. Horstmeyer, R. Heintzmann, G. Popescu, L. Waller, and C. Yang, “Standardizing the resolution claims for coherent microscopy,” Nat. Photonics 10(2), 68–71 (2016).
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J. Zheng, P. Gao, B. Yao, T. Ye, M. Lei, J. Min, D. Dan, Y. Yang, and S. Yan, “Digital holographic microscopy with phase-shift-free structured illumination,” Photonics Research 2(3), 87–91 (2014).
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Yao, B.

J. Zheng, P. Gao, B. Yao, T. Ye, M. Lei, J. Min, D. Dan, Y. Yang, and S. Yan, “Digital holographic microscopy with phase-shift-free structured illumination,” Photonics Research 2(3), 87–91 (2014).
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Ye, J. C.

Ye, T.

J. Zheng, P. Gao, B. Yao, T. Ye, M. Lei, J. Min, D. Dan, Y. Yang, and S. Yan, “Digital holographic microscopy with phase-shift-free structured illumination,” Photonics Research 2(3), 87–91 (2014).
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Zhang, M.

D. Li, L. Shao, B.-C. Chen, X. Zhang, M. Zhang, B. Moses, D. E. Milkie, J. R. Beach, J. A. Hammer, M. Pasham, T. Kirchhausen, M. A. Baird, M. W. Davidson, P. Xu, and E. Betzig, “Extended-resolution structured illumination imaging of endocytic and cytoskeletal dynamics,” Science 349(6251), aab3500 (2015).
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Zhang, X.

D. Li, L. Shao, B.-C. Chen, X. Zhang, M. Zhang, B. Moses, D. E. Milkie, J. R. Beach, J. A. Hammer, M. Pasham, T. Kirchhausen, M. A. Baird, M. W. Davidson, P. Xu, and E. Betzig, “Extended-resolution structured illumination imaging of endocytic and cytoskeletal dynamics,” Science 349(6251), aab3500 (2015).
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Zheng, G.

G. Zheng, R. Horstmeyer, and C. Yang, “Wide-field, high-resolution Fourier ptychographic microscopy,” Nat. Photonics 7(9), 739–745 (2013).
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Zheng, J.

J. Zheng, P. Gao, B. Yao, T. Ye, M. Lei, J. Min, D. Dan, Y. Yang, and S. Yan, “Digital holographic microscopy with phase-shift-free structured illumination,” Photonics Research 2(3), 87–91 (2014).
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Zhou, R.

B. Bhaduri, C. Edwards, H. Pham, R. Zhou, T. H. Nguyen, L. L. Goddard, and G. Popescu, “Diffraction phase microscopy: principles and applications in materials and life sciences,” Adv. Opt. Photonics 6(1), 57–119 (2014).
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J. G. Flannery, S. Zolotukhin, M. I. Vaquero, M. M. LaVail, N. Muzyczka, and W. W. Hauswirth, “Efficient photoreceptor-targeted gene expression in vivo by recombinant adeno-associated virus,” Proc. Natl. Acad. Sci. U.S.A. 94(13), 6916–6921 (1997).
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Zonios, G.

V. Backman, M. B. Wallace, L. T. Perelman, J. T. Arendt, R. Gurjar, M. G. Müller, Q. Zhang, G. Zonios, E. Kline, J. A. McGilligan, S. Shapshay, T. Valdez, K. Badizadegan, J. M. Crawford, M. Fitzmaurice, S. Kabani, H. S. Levin, M. Seiler, R. R. Dasari, I. Itzkan, J. Van Dam, and M. S. Feld, “Detection of preinvasive cancer cells,” Nature 406(6791), 35–36 (2000).
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Adv. Opt. Photonics (1)

B. Bhaduri, C. Edwards, H. Pham, R. Zhou, T. H. Nguyen, L. L. Goddard, and G. Popescu, “Diffraction phase microscopy: principles and applications in materials and life sciences,” Adv. Opt. Photonics 6(1), 57–119 (2014).
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Am. J. Physiol. Cell Physiol. (2)

S. Hu, J. Chen, B. Fabry, Y. Numaguchi, A. Gouldstone, D. E. Ingber, J. J. Fredberg, J. P. Butler, and N. Wang, “Intracellular stress tomography reveals stress focusing and structural anisotropy in cytoskeleton of living cells,” Am. J. Physiol. Cell Physiol. 285(5), C1082–C1090 (2003).
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G. Popescu, Y. Park, N. Lue, C. Best-Popescu, L. Deflores, R. R. Dasari, M. S. Feld, and K. Badizadegan, “Optical imaging of cell mass and growth dynamics,” Am. J. Physiol. Cell Physiol. 295(2), C538–C544 (2008).
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Appl. Opt. (2)

Biomed. Opt. Express (4)

Biophys. J. (1)

M. G. Gustafsson, L. Shao, P. M. Carlton, C. J. Wang, I. N. Golubovskaya, W. Z. Cande, D. A. Agard, and J. W. Sedat, “Three-dimensional resolution doubling in wide-field fluorescence microscopy by structured illumination,” Biophys. J. 94(12), 4957–4970 (2008).
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R. Heintzmann and G. Ficz, “Breaking the resolution limit in light microscopy,” Brief. Funct. Genomics Proteomics 5(4), 289–301 (2006).
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Gastroenterology (1)

M. Okuda, K. Li, M. R. Beard, L. A. Showalter, F. Scholle, S. M. Lemon, and S. A. Weinman, “Mitochondrial injury, oxidative stress, and antioxidant gene expression are induced by hepatitis C virus core protein,” Gastroenterology 122(2), 366–375 (2002).
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J. Cell Biol. (2)

O. Seksek, J. Biwersi, and A. S. Verkman, “Translational diffusion of macromolecule-sized solutes in cytoplasm and nucleus,” J. Cell Biol. 138(1), 131–142 (1997).
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L. Schermelleh, R. Heintzmann, and H. Leonhardt, “A guide to super-resolution fluorescence microscopy,” J. Cell Biol. 190(2), 165–175 (2010).
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V. Lauer, “New approach to optical diffraction tomography yielding a vector equation of diffraction tomography and a novel tomographic microscope,” J. Microsc. 205(2), 165–176 (2002).
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M. G. Gustafsson, “Surpassing the lateral resolution limit by a factor of two using structured illumination microscopy,” J. Microsc. 198(2), 82–87 (2000).
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J. Opt. Soc. Am. A (1)

JOSA (1)

R. Barakat, “Application of apodization to increase two-point resolution by the Sparrow criterion. I. Coherent illumination,” JOSA 52(3), 276–283 (1962).
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Nat. Methods (2)

L. Shao, P. Kner, E. H. Rego, and M. G. Gustafsson, “Super-resolution 3D microscopy of live whole cells using structured illumination,” Nat. Methods 8(12), 1044–1046 (2011).
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P. Kner, B. B. Chhun, E. R. Griffis, L. Winoto, and M. G. Gustafsson, “Super-resolution video microscopy of live cells by structured illumination,” Nat. Methods 6(5), 339–342 (2009).
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Nat. Photonics (4)

Y. Cotte, F. Toy, P. Jourdain, N. Pavillon, D. Boss, P. Magistretti, P. Marquet, and C. Depeursinge, “Marker-free phase nanoscopy,” Nat. Photonics 7(2), 113–117 (2013).
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G. Zheng, R. Horstmeyer, and C. Yang, “Wide-field, high-resolution Fourier ptychographic microscopy,” Nat. Photonics 7(9), 739–745 (2013).
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F. E. Robles, C. Wilson, G. Grant, and A. Wax, “Molecular imaging true-colour spectroscopic optical coherence tomography,” Nat. Photonics 5(12), 744–747 (2011).
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R. Horstmeyer, R. Heintzmann, G. Popescu, L. Waller, and C. Yang, “Standardizing the resolution claims for coherent microscopy,” Nat. Photonics 10(2), 68–71 (2016).
[Crossref]

Nature (1)

V. Backman, M. B. Wallace, L. T. Perelman, J. T. Arendt, R. Gurjar, M. G. Müller, Q. Zhang, G. Zonios, E. Kline, J. A. McGilligan, S. Shapshay, T. Valdez, K. Badizadegan, J. M. Crawford, M. Fitzmaurice, S. Kabani, H. S. Levin, M. Seiler, R. R. Dasari, I. Itzkan, J. Van Dam, and M. S. Feld, “Detection of preinvasive cancer cells,” Nature 406(6791), 35–36 (2000).
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Opt. Express (9)

T. Slabý, P. Kolman, Z. Dostál, M. Antoš, M. Lošťák, and R. Chmelík, “Off-axis setup taking full advantage of incoherent illumination in coherence-controlled holographic microscope,” Opt. Express 21(12), 14747–14762 (2013).
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P. Girshovitz and N. T. Shaked, “Fast phase processing in off-axis holography using multiplexing with complex encoding and live-cell fluctuation map calculation in real-time,” Opt. Express 23(7), 8773–8787 (2015).
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J. Lim, K. Lee, K. H. Jin, S. Shin, S. Lee, Y. Park, and J. C. Ye, “Comparative study of iterative reconstruction algorithms for missing cone problems in optical diffraction tomography,” Opt. Express 23(13), 16933–16948 (2015).
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S. Van Aert, D. Van Dyck, and A. J. den Dekker, “Resolution of coherent and incoherent imaging systems reconsidered - Classical criteria and a statistical alternative,” Opt. Express 14(9), 3830–3839 (2006).
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R. Fiolka, K. Wicker, R. Heintzmann, and A. Stemmer, “Simplified approach to diffraction tomography in optical microscopy,” Opt. Express 17(15), 12407–12417 (2009).
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Y. Sung, W. Choi, C. Fang-Yen, K. Badizadegan, R. R. Dasari, and M. S. Feld, “Optical diffraction tomography for high resolution live cell imaging,” Opt. Express 17(1), 266–277 (2009).
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Y. Park, G. Popescu, K. Badizadegan, R. R. Dasari, and M. S. Feld, “Diffraction phase and fluorescence microscopy,” Opt. Express 14(18), 8263–8268 (2006).
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R. Wang, Z. Wang, L. Millet, M. U. Gillette, A. J. Levine, and G. Popescu, “Dispersion-relation phase spectroscopy of intracellular transport,” Opt. Express 19(21), 20571–20579 (2011).
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S. S. Kou and C. J. Sheppard, “Imaging in digital holographic microscopy,” Opt. Express 15(21), 13640–13648 (2007).
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Opt. Lett. (10)

M. Debailleul, V. Georges, B. Simon, R. Morin, and O. Haeberlé, “High-resolution three-dimensional tomographic diffractive microscopy of transparent inorganic and biological samples,” Opt. Lett. 34(1), 79–81 (2009).
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W. J. Eldridge, A. Sheinfeld, M. T. Rinehart, and A. Wax, “Imaging deformation of adherent cells due to shear stress using quantitative phase imaging,” Opt. Lett. 41(2), 352–355 (2016).
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F. E. Robles and A. Wax, “Separating the scattering and absorption coefficients using the real and imaginary parts of the refractive index with low-coherence interferometry,” Opt. Lett. 35(17), 2843–2845 (2010).
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S. Chowdhury, W. J. Eldridge, A. Wax, and J. A. Izatt, “Spatial frequency-domain multiplexed microscopy for simultaneous, single-camera, one-shot, fluorescent, and quantitative-phase imaging,” Opt. Lett. 40(21), 4839–4842 (2015).
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M. Habaza, B. Gilboa, Y. Roichman, and N. T. Shaked, “Tomographic phase microscopy with 180° rotation of live cells in suspension by holographic optical tweezers,” Opt. Lett. 40(8), 1881–1884 (2015).
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S. Chowdhury and J. Izatt, “Structured illumination diffraction phase microscopy for broadband, subdiffraction resolution, quantitative phase imaging,” Opt. Lett. 39(4), 1015–1018 (2014).
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P. Gao, G. Pedrini, and W. Osten, “Structured illumination for resolution enhancement and autofocusing in digital holographic microscopy,” Opt. Lett. 38(8), 1328–1330 (2013).
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M. Kim, Y. Choi, C. Fang-Yen, Y. Sung, R. R. Dasari, M. S. Feld, and W. Choi, “High-speed synthetic aperture microscopy for live cell imaging,” Opt. Lett. 36(2), 148–150 (2011).
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P. Marquet, B. Rappaz, P. J. Magistretti, E. Cuche, Y. Emery, T. Colomb, and C. Depeursinge, “Digital holographic microscopy: a noninvasive contrast imaging technique allowing quantitative visualization of living cells with subwavelength axial accuracy,” Opt. Lett. 30(5), 468–470 (2005).
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P. von Olshausen and A. Rohrbach, “Coherent total internal reflection dark-field microscopy: label-free imaging beyond the diffraction limit,” Opt. Lett. 38(20), 4066–4069 (2013).
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Photonics Research (1)

J. Zheng, P. Gao, B. Yao, T. Ye, M. Lei, J. Min, D. Dan, Y. Yang, and S. Yan, “Digital holographic microscopy with phase-shift-free structured illumination,” Photonics Research 2(3), 87–91 (2014).
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Phys. Med. Biol. (1)

Y. L. Jin, J. Y. Chen, L. Xu, and P. N. Wang, “Refractive index measurement for biomaterial samples by total internal reflection,” Phys. Med. Biol. 51(20), N371–N379 (2006).
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N. Wang, K. Naruse, D. Stamenović, J. J. Fredberg, S. M. Mijailovich, I. M. Tolić-Nørrelykke, T. Polte, R. Mannix, and D. E. Ingber, “Mechanical behavior in living cells consistent with the tensegrity model,” Proc. Natl. Acad. Sci. U.S.A. 98(14), 7765–7770 (2001).
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M. G. Gustafsson, “Nonlinear structured-illumination microscopy: wide-field fluorescence imaging with theoretically unlimited resolution,” Proc. Natl. Acad. Sci. U.S.A. 102(37), 13081–13086 (2005).
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B. Hein, K. I. Willig, and S. W. Hell, “Stimulated emission depletion (STED) nanoscopy of a fluorescent protein-labeled organelle inside a living cell,” Proc. Natl. Acad. Sci. U.S.A. 105(38), 14271–14276 (2008).
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R. Fiolka, L. Shao, E. H. Rego, M. W. Davidson, and M. G. Gustafsson, “Time-lapse two-color 3D imaging of live cells with doubled resolution using structured illumination,” Proc. Natl. Acad. Sci. U.S.A. 109(14), 5311–5315 (2012).
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J. G. Flannery, S. Zolotukhin, M. I. Vaquero, M. M. LaVail, N. Muzyczka, and W. W. Hauswirth, “Efficient photoreceptor-targeted gene expression in vivo by recombinant adeno-associated virus,” Proc. Natl. Acad. Sci. U.S.A. 94(13), 6916–6921 (1997).
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D. Li, L. Shao, B.-C. Chen, X. Zhang, M. Zhang, B. Moses, D. E. Milkie, J. R. Beach, J. A. Hammer, M. Pasham, T. Kirchhausen, M. A. Baird, M. W. Davidson, P. Xu, and E. Betzig, “Extended-resolution structured illumination imaging of endocytic and cytoskeletal dynamics,” Science 349(6251), aab3500 (2015).
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Figures (8)

Fig. 1
Fig. 1

3D transfer functions in QP and fluorescence imaging, assuming equal excitation and emission wavelengths. (a,b) Cross-sectional plot and 3D rendering demonstrate that the transfer function in QP imaging forms a spherical cap (commonly referred to as Ewald’s Sphere). Dimensional parameters of this cap are determined by wavelength, microscope objective NA, and immersion oil refractive index. Autocorrelation of this cap corresponds to the transfer function for fluorescence imaging. (c,d) Cross-sectional plot and 3D render show this region to have a filled torus-like shape. Note that direct comparisons between (a) and (c) are inappropriate because spatial frequencies in QP and fluorescence imaging are measured in the electric-field and intensity regimes.

Fig. 2
Fig. 2

Filling out 3D frequency space with structured illumination. Cross-sectional plots show how axial frequency space is filled with (a) uniform illumination, (b) sinusoidal illumination with maximum allowable spatial frequency, and (c) a summation of sinusoidal illuminations of varying spatial frequencies. Note that illuminating with simply one spatial frequency is not sufficient to fill out axial frequency space in coherent-diffraction imaging, as it is in fluorescent imaging. (d,e,f) Corresponding 3D renderings show 3D frequency space being filled by Ewald caps.

Fig. 3
Fig. 3

(a) Optical system diagram is shown, and consolidates conventional fluorescent structured illumination (SI) microscopy with SI diffraction phase microscopy (SI-DPM) for sub-diffraction resolution quantitative-phase (QP) and fluorescent imaging. (b) Conventional widefield illumination is achieved when all the SLM pixels are turned ‘ON’, resulting in a single focused spot at the back focal plane (BFP) of the imaging objective and a single collimated beam illuminating the sample. Sinusoidal structured illumination is achieved when the SLM is programmed to display a sinusoidal pattern. This results in three focused spots at the BFP of the imaging objective and a three beam coherent interference through the imaging volume. (c) The diffracted excitation beam from the sample is spectrally separated from the fluorescence, and is fed through a diffraction-phase-microscope (DPM). An asymmetric mask (M) is used to physically completely block the −1st diffraction order from DG while passing the + 1st diffraction order. Note that in the case of SI, each diffraction order from the DG contains the 0th and ± 1st diffraction orders from the SLM. To generate a uniform wavefront reference beam necessary for off-axis holography, the mask also applies a pinhole spatial filter to the 0th diffraction order from the SLM contained in the 0th diffraction order from the DG. Due to the broadband spectrum of the NKT-illumination source, this diffraction order is the only undispersed component suitable for spatial filtering.

Fig. 4
Fig. 4

(a) SI QP imaging is compared with (b) WF QP imaging when taking an optical image section through a sample consisting of a monolayer of 400 nm diameter polystyrene spheres. Lateral sub-diffraction imaging capabilities are clearly demonstrated when comparing the SI and WF zooms (c and d, respectively) of the 400 nm microspheres.

Fig. 5
Fig. 5

Demonstrating SI’s capabilities for enabling 3D quantitative-phase (QP) imaging. (a,b) We compare SI-enhanced and conventional widefield (WF) QP imaging volumes when visualizing 520nm diameter microspheres. Clear improvements allowed by SI include increased lateral resolution and depth-localization. (c,d) Axial cross-sections from the SI-enhanced and WF imaging volumes (location marked by dashed yellow line in (a,b)) show the microspheres depth-localized to a resolution of 1.2um with SI-enhancement, while no depth-localization is apparent with conventional WF. (e,f) The axial cross-sections of radially-averaged Fourier transforms show the 3D frequency content of the SI-enhanced and WF imaging volumes. The Fourier transform of the WF imaging volume clearly shows the Ewald cap associated with conventional coherent imaging. In contrast, the Fourier transform of the SI-enhanced imaging volume depicts the distinct butterfly shape associated with ODT. (g,h) Zooms of the region outlined in yellow from (a,b), respectively, are shown. The 520nm diameter beads fall just within the bound set by the diffraction limit, and so are theoretically resolvable – however, coherent noise and out-of-focus diffraction artifacts deem sections of the zoom (indicated by yellow arrows in (h)) practically irresolvable without the enhancements allowed by SI.

Fig. 6
Fig. 6

3D visualization capabilities of QP and fluorescent imaging. (a,k) SI and (b,l) WF imaging performances are compared when visualizing an individual A549 cell. SI-enhanced QP sub-diffraction resolution is clearly evident from a zoom of the region outlined in yellow in (a,b), which shows several high phase-delay structures clearly resolvable with (c) SI but not (d) WF QP imaging. 3D imaging capabilities between SI and WF are compared when considering defocused sample planes through the (c,e,g,i) SI and (d,f,h,j) WF image volumes. In the SI volume, the sharp QP signal from the high phase-delay structures attenuated with increasing defocus, indicating optical depth sectioning. In contrast, the WF volume showed the QP signal from the high phase-delay structures diffracting out into the defocused planes, leading to diffraction artifacts indistinguishable from in-focus QP signal. Fluorescent resolution was also enhanced when comparing (k) SI to (l) WF imaging, respectively. (m,o,q,s) Defocused planes show that SI fluorescence imaging demonstrates clear optical sectioning and shows the actin morphology undergoing clear organizational changes through different depths of the cell. In contrast, defocused planes through the (n,p,r,t) WF fluorescence volume show a strong defocused signal throughout the volume stack, which hinders visualization of important high-resolution features.

Fig. 7
Fig. 7

Illustration depicting transfer of spatial frequencies in a coherent imaging system. (a) Illustration depicting imaging setup for orthogonal, widefield, coherent illumination. (b) Fourier diagram illustrating the illumination wave-vector, the Ewald sphere (in dashed outline) for all possible diffracted spatial frequencies, as well as the set of all detected spatial frequencies k s . (c) Fourier diagram illustrating the coherent system’s transfer function as the region of the sample’s 3D spatial-frequency spectrum that give rise to the set of all k s .

Fig. 8
Fig. 8

(a-c) Illustration of the relationship between illumination axial and lateral harmonic components, I m ( k z ) and J m ( k x,y ) respectively, and H m ( k ) for component orders m=0,1,2 . (d-f) Illustration of the relative positioning between the sample spectrum S( k ) and the image system’s region of accepted spatial frequencies H m ( k ) for components Y 0 ( k ), Y 1 ( k ), Y 2 ( k ) . (g-i) Illustrating the regions of accepted sample spectrum after correcting for the original spatial-frequency shifts present in the sample information in components Y 0 ( k ), Y 1 ( k ), Y 2 ( k ) . (j) Illustrating that the synthesized region of accepted sample spectrum contains more information than allowed by simple widefield coherent imaging (as is illustrated in (d)).

Equations (11)

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y(r)=h(r)[s(r)i(r)]
 i( r x,y ,z )= m c m   i m ( z ) j m ( r x,y )
 y( r )=[ h( si ) ]( r ) =h( r )[ s( r ) m c m   i m ( z ) j m ( r x,y ) ] = m c m h( rr' ) s( r' )  i m ( z' )  j m ( r ' x,y ) dr'
 y( r )= m c m h( rr' )  i m ( zz' ) s( r' )   j m ( r ' x,y ) dr' = m c m [ ( h( r ) i m ( z ) )( s( r ) j m (r x,y ) ) ] = m c m y m ( r )
Y m ( k )= H m ( k )[ S( k ) J m ( k x,y ) ]
i SI ( r )=exp( j ( k 0 r+ ϕ 0 ) )+exp( j ( k 1 r+ ϕ 1 ) ) +exp( j ( k 2 r+ ϕ 2 ) )
  i SI ( r )=exp( j  k λ z )+exp( j ( k T r x,y + k T,z z+ϕ ) ) +exp( j ( k T r x,y + k T,z zϕ ) )  =exp( j  k λ z )+ e jϕ exp( j  k T r x,y )exp( j  k T,z z ) + e jϕ exp( j  k T r x,y )exp( j  k T,z z )
  i 0 ( z )=exp( j  k λ z )      FFT       I 0 ( k z )=δ( k z k λ ) j 0 ( r x,y )=1      FFT       J 0 ( k x,y )=δ( k x,y ) i 1 ( z )=exp( j  k T,z z )      FFT       I 1 ( k z )=δ( k z k T,z ) j 1 ( r x,y )=exp( j  k T r x,y )      FFT       J 1 ( k x,y )=δ( k x,y k T )   i 2 ( z )=exp( j  k T,z z )      FFT       I 2 ( k z )=δ( k z k T,z ) j 2 ( r x,y )=exp( j  k T r x,y )      FFT       J 2 ( k x,y )=δ( k x,y + k T )
   Y 0 ( k )= H 0 ( k )S( k ) H 0 ( k )= H p ( k k λ )   Y 1 ( k )= H 1 ( k )S( k k T,3D ) H 1 ( k )= H p ( k k T,z,3D ) Y 2 ( k )= H 2 ( k )S( k+ k T,3D )   H 2 ( k )= H p ( k k T,z,3D )
Y( k )= Y 0 ( k )+ e jϕ Y 1 ( k )+ e jϕ Y 2 ( k )
Y SI ( k )= Y 0 ( k )+ Y 1 ( k+ k T,3D )+ Y 2 ( k k T,3D ) =[ H 0 ( k )+ H 1 ( k+ k T,3D )+ H 2 ( k k T,3D ) ]S( k )

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