Abstract

Though structured illumination (SI) microscopy is a popular imaging technique conventionally associated with fluorescent super-resolution, recent works have suggested its applicability towards sub-diffraction resolution coherent imaging with quantitative endogenous biological contrast. Here, we demonstrate that SI can efficiently integrate together the principles of fluorescent super-resolution and coherent synthetic aperture to achieve 3D dual-modality sub-diffraction resolution, fluorescence and refractive-index (RI) visualizations of biological samples. We experimentally demonstrate this framework by introducing a SI microscope capable of 3D sub-diffraction resolution fluorescence and RI imaging, and verify its biological visualization capabilities by experimentally reconstructing 3D RI/fluorescence visualizations of fluorescent calibration microspheres as well as alveolar basal epithelial adenocarcinoma (A549) and human colorectal adenocarcinmoa (HT-29) cells, fluorescently stained for F-actin. This demonstration may suggest SI as an especially promising imaging technique to enable future biological studies that explore synergistically operating biophysical/biochemical and molecular mechanisms at sub-diffraction resolutions.

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

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2017 (5)

2016 (4)

2015 (2)

2014 (7)

Y. Kim, H. Shim, K. Kim, H. Park, J. H. Heo, J. Yoon, C. Choi, S. Jang, and Y. Park, “Common-path diffraction optical tomography for investigation of three-dimensional structures and dynamics of biological cells,” Opt. Express 22(9), 10398–10407 (2014).
[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, 87–91 (2014).

E. Sánchez-Ortiga, M. Martínez-Corral, G. Saavedra, and J. Garcia-Sucerquia, “Enhancing spatial resolution in digital holographic microscopy by biprism structured illumination,” Opt. Lett. 39(7), 2086–2089 (2014).
[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).
[PubMed]

T. Kim, R. Zhou, M. Mir, S. D. Babacan, P. S. Carney, L. L. Goddard, and G. Popescu, “White-light diffraction tomography of unlabelled live cells,” Nat. Photonics 8, 256–263 (2014).

K. Kim, H. Yoon, M. Diez-Silva, M. Dao, R. R. Dasari, and Y. Park, “High-resolution three-dimensional imaging of red blood cells parasitized by Plasmodium falciparum and in situ hemozoin crystals using optical diffraction tomography,” J. Biomed. Opt. 19(1), 011005 (2014).
[PubMed]

B.-C. Chen, W. R. Legant, K. Wang, L. Shao, D. E. Milkie, M. W. Davidson, C. Janetopoulos, X. S. Wu, J. A. Hammer, Z. Liu, B. P. English, Y. Mimori-Kiyosue, D. P. Romero, A. T. Ritter, J. Lippincott-Schwartz, L. Fritz-Laylin, R. D. Mullins, D. M. Mitchell, J. N. Bembenek, A. C. Reymann, R. Böhme, S. W. Grill, J. T. Wang, G. Seydoux, U. S. Tulu, D. P. Kiehart, and E. Betzig, “Lattice light-sheet microscopy: Imaging molecules to embryos at high spatiotemporal resolution,” Science 346(6208), 1257998 (2014).
[PubMed]

2013 (8)

K. Xu, G. Zhong, and X. Zhuang, “Actin, spectrin, and associated proteins form a periodic cytoskeletal structure in axons,” Science 339(6118), 452–456 (2013).
[PubMed]

Y. Cotte, F. Toy, P. Jourdain, N. Pavillon, D. Boss, P. Magistretti, P. Marquet, and C. Depeursinge, “Marker-free phase nanoscopy,” Nat. Photonics 7, 113–117 (2013).

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

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).
[PubMed]

J. C. Akers, D. Gonda, R. Kim, B. S. Carter, and C. C. Chen, “Biogenesis of extracellular vesicles (EV): exosomes, microvesicles, retrovirus-like vesicles, and apoptotic bodies,” J. Neurooncol. 113(1), 1–11 (2013).
[PubMed]

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).
[PubMed]

J. Chen, Y. Xu, X. Lv, X. Lai, and S. Zeng, “Super-resolution differential interference contrast microscopy by structured illumination,” Opt. Express 21(1), 112–121 (2013).
[PubMed]

S. Chowdhury and J. Izatt, “Structured illumination quantitative phase microscopy for enhanced resolution amplitude and phase imaging,” Biomed. Opt. Express 4(10), 1795–1805 (2013).
[PubMed]

2012 (6)

E. H. Rego, L. Shao, J. J. Macklin, L. Winoto, G. A. Johansson, N. Kamps-Hughes, M. W. Davidson, and M. G. 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).
[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).
[PubMed]

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).
[PubMed]

Y. Sung, W. Choi, N. Lue, R. R. Dasari, and Z. Yaqoob, “Stain-free quantification of chromosomes in live cells using regularized tomographic phase microscopy,” PLoS One 7(11), e49502 (2012).
[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).
[PubMed]

F. de Chaumont, S. Dallongeville, N. Chenouard, N. Hervé, S. Pop, T. Provoost, V. Meas-Yedid, P. Pankajakshan, T. Lecomte, Y. Le Montagner, T. Lagache, A. Dufour, and J. C. Olivo-Marin, “Icy: an open bioimage informatics platform for extended reproducible research,” Nat. Methods 9(7), 690–696 (2012).
[PubMed]

2011 (2)

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).
[PubMed]

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).
[PubMed]

2010 (1)

2009 (5)

B. Rappaz, E. Cano, T. Colomb, J. Kühn, C. Depeursinge, V. Simanis, P. J. Magistretti, and P. Marquet, “Noninvasive characterization of the fission yeast cell cycle by monitoring dry mass with digital holographic microscopy,” J. Biomed. Opt. 14, 034049 (2009).

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).
[PubMed]

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).
[PubMed]

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).
[PubMed]

R. Fiolka, K. Wicker, R. Heintzmann, and A. Stemmer, “Simplified approach to diffraction tomography in optical microscopy,” Opt. Express 17(15), 12407–12417 (2009).
[PubMed]

2008 (4)

G. Popescu, Y. Park, W. Choi, R. R. Dasari, M. S. Feld, and K. Badizadegan, “Imaging red blood cell dynamics by quantitative phase microscopy,” Blood Cells Mol. Dis. 41(1), 10–16 (2008).
[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).
[PubMed]

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).
[PubMed]

Y. Park, M. Diez-Silva, G. Popescu, G. Lykotrafitis, W. Choi, M. S. Feld, and S. Suresh, “Refractive index maps and membrane dynamics of human red blood cells parasitized by Plasmodium falciparum,” Proc. Natl. Acad. Sci. U.S.A. 105(37), 13730–13735 (2008).
[PubMed]

2007 (1)

2006 (3)

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

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).
[PubMed]

2005 (4)

2004 (1)

A. Rustom, R. Saffrich, I. Markovic, P. Walther, and H.-H. Gerdes, “Nanotubular highways for intercellular organelle transport,” Science 303(5660), 1007–1010 (2004).
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2002 (2)

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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V. Lauer, “New approach to optical diffraction tomography yielding a vector equation of diffraction tomography and a novel tomographic microscope,” J. Microsc. 205(Pt 2), 165–176 (2002).
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2000 (2)

D. T. Ross, U. Scherf, M. B. Eisen, C. M. Perou, C. Rees, P. Spellman, V. Iyer, S. S. Jeffrey, M. Van de Rijn, M. Waltham, A. Pergamenschikov, J. C. Lee, D. Lashkari, D. Shalon, T. G. Myers, J. N. Weinstein, D. Botstein, and P. O. Brown, “Systematic variation in gene expression patterns in human cancer cell lines,” Nat. Genet. 24(3), 227–235 (2000).
[PubMed]

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

1998 (1)

K. A. Foster, C. G. Oster, M. M. Mayer, M. L. Avery, and K. L. Audus, “Characterization of the A549 cell line as a type II pulmonary epithelial cell model for drug metabolism,” Exp. Cell Res. 243(2), 359–366 (1998).
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1997 (1)

B. P. Cormack, G. Bertram, M. Egerton, N. A. Gow, S. Falkow, and A. J. Brown, “Yeast-enhanced green fluorescent protein (yEGFP): a reporter of gene expression in Candida albicans,” Microbiology 143(Pt 2), 303–311 (1997).
[PubMed]

1995 (1)

R. Rizzuto, M. Brini, P. Pizzo, M. Murgia, and T. Pozzan, “Chimeric green fluorescent protein as a tool for visualizing subcellular organelles in living cells,” Curr. Biol. 5(6), 635–642 (1995).
[PubMed]

1994 (1)

1991 (1)

F. N. Jiang, D. J. Liu, H. Neyndorff, M. Chester, S. Y. Jiang, and J. G. Levy, “Photodynamic killing of human squamous cell carcinoma cells using a monoclonal antibody-photosensitizer conjugate,” J. Natl. Cancer Inst. 83(17), 1218–1225 (1991).
[PubMed]

1986 (1)

M. Rousset, “The human colon carcinoma cell lines HT-29 and Caco-2: two in vitro models for the study of intestinal differentiation,” Biochimie 68(9), 1035–1040 (1986).
[PubMed]

1985 (1)

A. Zweibaum, M. Pinto, G. Chevalier, E. Dussaulx, N. Triadou, B. Lacroix, K. Haffen, J. L. Brun, and M. Rousset, “Enterocytic differentiation of a subpopulation of the human colon tumor cell line HT-29 selected for growth in sugar-free medium and its inhibition by glucose,” J. Cell. Physiol. 122(1), 21–29 (1985).
[PubMed]

1980 (1)

R. J. Mason and M. C. Williams, “Phospholipid composition and ultrastructure of A549 cells and other cultured pulmonary epithelial cells of presumed type II cell origin,” Biochimica et Biophysica Acta (BBA)- Lipids and Lipid Metabolism 617, 36–50 (1980).

1978 (1)

D. L. Shapiro, L. L. Nardone, S. A. Rooney, E. K. Motoyama, and J. L. Munoz, “Phospholipid biosynthesis and secretion by a cell line (A549) which resembles type II alveolar epithelial cells,” Biochimica et Biophysica Acta (BBA)- Lipids and Lipid Metabolism 530, 197–207 (1978).

1967 (1)

1966 (1)

W. Lukosz, “Optical systems with resolving powers exceeding the classical limit,” J. Opt. Soc. A. 56, 1463–1471 (1966).

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).
[PubMed]

Akers, J. C.

J. C. Akers, D. Gonda, R. Kim, B. S. Carter, and C. C. Chen, “Biogenesis of extracellular vesicles (EV): exosomes, microvesicles, retrovirus-like vesicles, and apoptotic bodies,” J. Neurooncol. 113(1), 1–11 (2013).
[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).
[PubMed]

Audus, K. L.

K. A. Foster, C. G. Oster, M. M. Mayer, M. L. Avery, and K. L. Audus, “Characterization of the A549 cell line as a type II pulmonary epithelial cell model for drug metabolism,” Exp. Cell Res. 243(2), 359–366 (1998).
[PubMed]

Avery, M. L.

K. A. Foster, C. G. Oster, M. M. Mayer, M. L. Avery, and K. L. Audus, “Characterization of the A549 cell line as a type II pulmonary epithelial cell model for drug metabolism,” Exp. Cell Res. 243(2), 359–366 (1998).
[PubMed]

Babacan, S. D.

T. Kim, R. Zhou, M. Mir, S. D. Babacan, P. S. Carney, L. L. Goddard, and G. Popescu, “White-light diffraction tomography of unlabelled live cells,” Nat. Photonics 8, 256–263 (2014).

Badizadegan, K.

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).
[PubMed]

G. Popescu, Y. Park, W. Choi, R. R. Dasari, M. S. Feld, and K. Badizadegan, “Imaging red blood cell dynamics by quantitative phase microscopy,” Blood Cells Mol. Dis. 41(1), 10–16 (2008).
[PubMed]

Beard, M. R.

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).
[PubMed]

Beemiller, P.

E. Cai, K. Marchuk, P. Beemiller, C. Beppler, M. G. Rubashkin, V. M. Weaver, A. Gérard, T.-L. Liu, B.-C. Chen, and E. Betzig, “Visualizing dynamic microvillar search and stabilization during ligand detection by T cells,” Science 356, 3118 (2017).

Bembenek, J. N.

B.-C. Chen, W. R. Legant, K. Wang, L. Shao, D. E. Milkie, M. W. Davidson, C. Janetopoulos, X. S. Wu, J. A. Hammer, Z. Liu, B. P. English, Y. Mimori-Kiyosue, D. P. Romero, A. T. Ritter, J. Lippincott-Schwartz, L. Fritz-Laylin, R. D. Mullins, D. M. Mitchell, J. N. Bembenek, A. C. Reymann, R. Böhme, S. W. Grill, J. T. Wang, G. Seydoux, U. S. Tulu, D. P. Kiehart, and E. Betzig, “Lattice light-sheet microscopy: Imaging molecules to embryos at high spatiotemporal resolution,” Science 346(6208), 1257998 (2014).
[PubMed]

Beppler, C.

E. Cai, K. Marchuk, P. Beemiller, C. Beppler, M. G. Rubashkin, V. M. Weaver, A. Gérard, T.-L. Liu, B.-C. Chen, and E. Betzig, “Visualizing dynamic microvillar search and stabilization during ligand detection by T cells,” Science 356, 3118 (2017).

Bertram, G.

B. P. Cormack, G. Bertram, M. Egerton, N. A. Gow, S. Falkow, and A. J. Brown, “Yeast-enhanced green fluorescent protein (yEGFP): a reporter of gene expression in Candida albicans,” Microbiology 143(Pt 2), 303–311 (1997).
[PubMed]

Betzig, E.

E. Cai, K. Marchuk, P. Beemiller, C. Beppler, M. G. Rubashkin, V. M. Weaver, A. Gérard, T.-L. Liu, B.-C. Chen, and E. Betzig, “Visualizing dynamic microvillar search and stabilization during ligand detection by T cells,” Science 356, 3118 (2017).

B.-C. Chen, W. R. Legant, K. Wang, L. Shao, D. E. Milkie, M. W. Davidson, C. Janetopoulos, X. S. Wu, J. A. Hammer, Z. Liu, B. P. English, Y. Mimori-Kiyosue, D. P. Romero, A. T. Ritter, J. Lippincott-Schwartz, L. Fritz-Laylin, R. D. Mullins, D. M. Mitchell, J. N. Bembenek, A. C. Reymann, R. Böhme, S. W. Grill, J. T. Wang, G. Seydoux, U. S. Tulu, D. P. Kiehart, and E. Betzig, “Lattice light-sheet microscopy: Imaging molecules to embryos at high spatiotemporal resolution,” Science 346(6208), 1257998 (2014).
[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).
[PubMed]

Böhme, R.

B.-C. Chen, W. R. Legant, K. Wang, L. Shao, D. E. Milkie, M. W. Davidson, C. Janetopoulos, X. S. Wu, J. A. Hammer, Z. Liu, B. P. English, Y. Mimori-Kiyosue, D. P. Romero, A. T. Ritter, J. Lippincott-Schwartz, L. Fritz-Laylin, R. D. Mullins, D. M. Mitchell, J. N. Bembenek, A. C. Reymann, R. Böhme, S. W. Grill, J. T. Wang, G. Seydoux, U. S. Tulu, D. P. Kiehart, and E. Betzig, “Lattice light-sheet microscopy: Imaging molecules to embryos at high spatiotemporal resolution,” Science 346(6208), 1257998 (2014).
[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,” Science 313(5793), 1642–1645 (2006).
[PubMed]

Borejdo, J.

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).
[PubMed]

Boss, D.

Y. Cotte, F. Toy, P. Jourdain, N. Pavillon, D. Boss, P. Magistretti, P. Marquet, and C. Depeursinge, “Marker-free phase nanoscopy,” Nat. Photonics 7, 113–117 (2013).

Botstein, D.

D. T. Ross, U. Scherf, M. B. Eisen, C. M. Perou, C. Rees, P. Spellman, V. Iyer, S. S. Jeffrey, M. Van de Rijn, M. Waltham, A. Pergamenschikov, J. C. Lee, D. Lashkari, D. Shalon, T. G. Myers, J. N. Weinstein, D. Botstein, and P. O. Brown, “Systematic variation in gene expression patterns in human cancer cell lines,” Nat. Genet. 24(3), 227–235 (2000).
[PubMed]

Brini, M.

R. Rizzuto, M. Brini, P. Pizzo, M. Murgia, and T. Pozzan, “Chimeric green fluorescent protein as a tool for visualizing subcellular organelles in living cells,” Curr. Biol. 5(6), 635–642 (1995).
[PubMed]

Brown, A. J.

B. P. Cormack, G. Bertram, M. Egerton, N. A. Gow, S. Falkow, and A. J. Brown, “Yeast-enhanced green fluorescent protein (yEGFP): a reporter of gene expression in Candida albicans,” Microbiology 143(Pt 2), 303–311 (1997).
[PubMed]

Brown, P. O.

D. T. Ross, U. Scherf, M. B. Eisen, C. M. Perou, C. Rees, P. Spellman, V. Iyer, S. S. Jeffrey, M. Van de Rijn, M. Waltham, A. Pergamenschikov, J. C. Lee, D. Lashkari, D. Shalon, T. G. Myers, J. N. Weinstein, D. Botstein, and P. O. Brown, “Systematic variation in gene expression patterns in human cancer cell lines,” Nat. Genet. 24(3), 227–235 (2000).
[PubMed]

Brun, J. L.

A. Zweibaum, M. Pinto, G. Chevalier, E. Dussaulx, N. Triadou, B. Lacroix, K. Haffen, J. L. Brun, and M. Rousset, “Enterocytic differentiation of a subpopulation of the human colon tumor cell line HT-29 selected for growth in sugar-free medium and its inhibition by glucose,” J. Cell. Physiol. 122(1), 21–29 (1985).
[PubMed]

Bursac, N.

Cai, E.

E. Cai, K. Marchuk, P. Beemiller, C. Beppler, M. G. Rubashkin, V. M. Weaver, A. Gérard, T.-L. Liu, B.-C. Chen, and E. Betzig, “Visualizing dynamic microvillar search and stabilization during ligand detection by T cells,” Science 356, 3118 (2017).

Cande, W. Z.

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).
[PubMed]

Cano, E.

B. Rappaz, E. Cano, T. Colomb, J. Kühn, C. Depeursinge, V. Simanis, P. J. Magistretti, and P. Marquet, “Noninvasive characterization of the fission yeast cell cycle by monitoring dry mass with digital holographic microscopy,” J. Biomed. Opt. 14, 034049 (2009).

Carlton, P. M.

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).
[PubMed]

Carney, P. S.

T. Kim, R. Zhou, M. Mir, S. D. Babacan, P. S. Carney, L. L. Goddard, and G. Popescu, “White-light diffraction tomography of unlabelled live cells,” Nat. Photonics 8, 256–263 (2014).

Carter, B. S.

J. C. Akers, D. Gonda, R. Kim, B. S. Carter, and C. C. Chen, “Biogenesis of extracellular vesicles (EV): exosomes, microvesicles, retrovirus-like vesicles, and apoptotic bodies,” J. Neurooncol. 113(1), 1–11 (2013).
[PubMed]

Chan, C. J.

M. Schürmann, J. Scholze, P. Müller, J. Guck, and C. J. Chan, “Cell nuclei have lower refractive index and mass density than cytoplasm,” J. Biophotonics 9(10), 1068–1076 (2016).
[PubMed]

Chen, B.-C.

E. Cai, K. Marchuk, P. Beemiller, C. Beppler, M. G. Rubashkin, V. M. Weaver, A. Gérard, T.-L. Liu, B.-C. Chen, and E. Betzig, “Visualizing dynamic microvillar search and stabilization during ligand detection by T cells,” Science 356, 3118 (2017).

B.-C. Chen, W. R. Legant, K. Wang, L. Shao, D. E. Milkie, M. W. Davidson, C. Janetopoulos, X. S. Wu, J. A. Hammer, Z. Liu, B. P. English, Y. Mimori-Kiyosue, D. P. Romero, A. T. Ritter, J. Lippincott-Schwartz, L. Fritz-Laylin, R. D. Mullins, D. M. Mitchell, J. N. Bembenek, A. C. Reymann, R. Böhme, S. W. Grill, J. T. Wang, G. Seydoux, U. S. Tulu, D. P. Kiehart, and E. Betzig, “Lattice light-sheet microscopy: Imaging molecules to embryos at high spatiotemporal resolution,” Science 346(6208), 1257998 (2014).
[PubMed]

Chen, C. C.

J. C. Akers, D. Gonda, R. Kim, B. S. Carter, and C. C. Chen, “Biogenesis of extracellular vesicles (EV): exosomes, microvesicles, retrovirus-like vesicles, and apoptotic bodies,” J. Neurooncol. 113(1), 1–11 (2013).
[PubMed]

Chen, J.

Chenouard, N.

F. de Chaumont, S. Dallongeville, N. Chenouard, N. Hervé, S. Pop, T. Provoost, V. Meas-Yedid, P. Pankajakshan, T. Lecomte, Y. Le Montagner, T. Lagache, A. Dufour, and J. C. Olivo-Marin, “Icy: an open bioimage informatics platform for extended reproducible research,” Nat. Methods 9(7), 690–696 (2012).
[PubMed]

Chester, M.

F. N. Jiang, D. J. Liu, H. Neyndorff, M. Chester, S. Y. Jiang, and J. G. Levy, “Photodynamic killing of human squamous cell carcinoma cells using a monoclonal antibody-photosensitizer conjugate,” J. Natl. Cancer Inst. 83(17), 1218–1225 (1991).
[PubMed]

Chevalier, G.

A. Zweibaum, M. Pinto, G. Chevalier, E. Dussaulx, N. Triadou, B. Lacroix, K. Haffen, J. L. Brun, and M. Rousset, “Enterocytic differentiation of a subpopulation of the human colon tumor cell line HT-29 selected for growth in sugar-free medium and its inhibition by glucose,” J. Cell. Physiol. 122(1), 21–29 (1985).
[PubMed]

Chhun, B. B.

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).
[PubMed]

Choi, C.

Choi, W.

Y. Sung, W. Choi, N. Lue, R. R. Dasari, and Z. Yaqoob, “Stain-free quantification of chromosomes in live cells using regularized tomographic phase microscopy,” PLoS One 7(11), e49502 (2012).
[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).
[PubMed]

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).
[PubMed]

Y. Park, M. Diez-Silva, G. Popescu, G. Lykotrafitis, W. Choi, M. S. Feld, and S. Suresh, “Refractive index maps and membrane dynamics of human red blood cells parasitized by Plasmodium falciparum,” Proc. Natl. Acad. Sci. U.S.A. 105(37), 13730–13735 (2008).
[PubMed]

G. Popescu, Y. Park, W. Choi, R. R. Dasari, M. S. Feld, and K. Badizadegan, “Imaging red blood cell dynamics by quantitative phase microscopy,” Blood Cells Mol. Dis. 41(1), 10–16 (2008).
[PubMed]

Choi, Y.

Chowdhury, S.

Chung, J.

Colomb, T.

B. Rappaz, E. Cano, T. Colomb, J. Kühn, C. Depeursinge, V. Simanis, P. J. Magistretti, and P. Marquet, “Noninvasive characterization of the fission yeast cell cycle by monitoring dry mass with digital holographic microscopy,” J. Biomed. Opt. 14, 034049 (2009).

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).
[PubMed]

Cormack, B. P.

B. P. Cormack, G. Bertram, M. Egerton, N. A. Gow, S. Falkow, and A. J. Brown, “Yeast-enhanced green fluorescent protein (yEGFP): a reporter of gene expression in Candida albicans,” Microbiology 143(Pt 2), 303–311 (1997).
[PubMed]

Cotte, Y.

Y. Cotte, F. Toy, P. Jourdain, N. Pavillon, D. Boss, P. Magistretti, P. Marquet, and C. Depeursinge, “Marker-free phase nanoscopy,” Nat. Photonics 7, 113–117 (2013).

Cuche, E.

Dallongeville, S.

F. de Chaumont, S. Dallongeville, N. Chenouard, N. Hervé, S. Pop, T. Provoost, V. Meas-Yedid, P. Pankajakshan, T. Lecomte, Y. Le Montagner, T. Lagache, A. Dufour, and J. C. Olivo-Marin, “Icy: an open bioimage informatics platform for extended reproducible research,” Nat. Methods 9(7), 690–696 (2012).
[PubMed]

Dan, D.

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, 87–91 (2014).

Dao, M.

K. Kim, H. Yoon, M. Diez-Silva, M. Dao, R. R. Dasari, and Y. Park, “High-resolution three-dimensional imaging of red blood cells parasitized by Plasmodium falciparum and in situ hemozoin crystals using optical diffraction tomography,” J. Biomed. Opt. 19(1), 011005 (2014).
[PubMed]

Dasari, R. R.

K. Kim, H. Yoon, M. Diez-Silva, M. Dao, R. R. Dasari, and Y. Park, “High-resolution three-dimensional imaging of red blood cells parasitized by Plasmodium falciparum and in situ hemozoin crystals using optical diffraction tomography,” J. Biomed. Opt. 19(1), 011005 (2014).
[PubMed]

Y. Sung, W. Choi, N. Lue, R. R. Dasari, and Z. Yaqoob, “Stain-free quantification of chromosomes in live cells using regularized tomographic phase microscopy,” PLoS One 7(11), e49502 (2012).
[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).
[PubMed]

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).
[PubMed]

G. Popescu, Y. Park, W. Choi, R. R. Dasari, M. S. Feld, and K. Badizadegan, “Imaging red blood cell dynamics by quantitative phase microscopy,” Blood Cells Mol. Dis. 41(1), 10–16 (2008).
[PubMed]

Davidson, M. W.

B.-C. Chen, W. R. Legant, K. Wang, L. Shao, D. E. Milkie, M. W. Davidson, C. Janetopoulos, X. S. Wu, J. A. Hammer, Z. Liu, B. P. English, Y. Mimori-Kiyosue, D. P. Romero, A. T. Ritter, J. Lippincott-Schwartz, L. Fritz-Laylin, R. D. Mullins, D. M. Mitchell, J. N. Bembenek, A. C. Reymann, R. Böhme, S. W. Grill, J. T. Wang, G. Seydoux, U. S. Tulu, D. P. Kiehart, and E. Betzig, “Lattice light-sheet microscopy: Imaging molecules to embryos at high spatiotemporal resolution,” Science 346(6208), 1257998 (2014).
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T. Kim, R. Zhou, M. Mir, S. D. Babacan, P. S. Carney, L. L. Goddard, and G. Popescu, “White-light diffraction tomography of unlabelled live cells,” Nat. Photonics 8, 256–263 (2014).

G. Popescu, Y. Park, W. Choi, R. R. Dasari, M. S. Feld, and K. Badizadegan, “Imaging red blood cell dynamics by quantitative phase microscopy,” Blood Cells Mol. Dis. 41(1), 10–16 (2008).
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Rees, C.

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Figures (9)

Fig. 1
Fig. 1 Three-dimensional (a) coherent and (b) fluorescent diffraction-limited transfer functions are shown. (c) SI can fill out sub-diffraction regions in coherent 3D k-space by using incremented spatial frequencies, analogous to diffraction tomography. (d) SI can also fill out sub-diffraction regions in fluorescent 3D k-space [31]. Because the fluorescent transfer function shown in (b) is filled (not of infinitesimal axial thickness), SI spatial frequencies do not have to be incremented for fluorescent super-resolution, as is required in (c).
Fig. 2
Fig. 2 (a) Experimental dual-modality system enabling both 3D fluorescence and refractive-index imaging. Examples of raw (b) fluorescent and (c) coherent-interferometric acquisitions required for SI reconstructions. (d) Zoom of interferogram shows both the SI and off-axis interference patterns. (e) Fourier-transform of interferogram shows the sample’s complex electric-field distribution.
Fig. 3
Fig. 3 (a) SI-enabled RI and (b) widefield diffraction-limited QP lateral visualizations of a cluster of 300 nm polystyrene microspheres. (c) Associated axial RI and (d) QP cross-sections are also shown. Lateral and axial visualizations are shown at identical size scales.
Fig. 4
Fig. 4 SI-enabled (a) RI and (b) fluorescent lateral visualizations of a monolayer sample of 2.0 um fluorescently tagged polystyrene microspheres. Associated axial (c) RI and (d) fluorescent cross-sections are also shown. (e) RI and (f) fluorescent volume-renderings are also shown.
Fig. 5
Fig. 5 Three-dimensional (a) RI and (b) fluorescence volumes are shown after SI reconstruction for a single A549 cell. (c,d) Corresponding 3D RI and fluorescent tomograms are shown [56]. Cross-sectional z-planes are compared through the (e,g,i) RI and (f,h,j) general QP volume reconstructions. Analogously, cross-sectional z-planes are also compared between the (k,m,o) SI-enabled super-resolution and (l,n,p) diffraction-limited widefield fluorescent volumes.
Fig. 6
Fig. 6 (a) RI slice and (b) fluorescence maximum intensity projection shown for a HT-29 cell cluster, along with (c,d) associated axial cross-sections, respectively. Red and yellow arrows in (a) indicate nuclear periphery and nucleoli boundaries, respectively. From the coherent arm of the optical system, (e-g) RI and (h-j) standard QP visualization is compared for the cell cluster at select axial positions. Similarly, for the fluorescent arm of the system, fluorescent (k-m) super-resolution and (n-p) diffraction-limited widefield visualization of the cell cluster is also compared. 3D Tomograms are visualized with (q-s) different RI-thresholded opacity constraints (to visualize different intracellular components of varying RI) as well as with (t) general super-resolved fluorescent contrast.
Fig. 7
Fig. 7 (a) SI-enabled RI and (b) widefield diffraction-limited QP lateral visualizations of a conjoined pair of A549 cells. (c) Associated axial RI and (d) QP cross-sections are also shown. 3D QP signal was reconstructed by using Fresnel kernels to digitally propagate the in-focus QP image in (b).
Fig. 8
Fig. 8 Lateral visualizations of two samples of (a,b) A549 and (c,d) HT-29 cells. Yellow and red arrows in (b) indicate fully formed cell nuclei and nucleoli, respectively. Yellow arrows in (d) indicate cell blebs, an indication of apoptosis.
Fig. 9
Fig. 9 Lateral visualizations of a 3-cell cluster of HT-29 cells undergoing apoptosis. Lateral (a) RI and (b) fluorescence visualizations are shown.

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