Abstract

Fluorescence fluctuation-based superresolution techniques can achieve fast superresolution imaging on a cost-effective wide-field platform at a low light level with reduced phototoxicity. However, the current methods exhibit certain imaging deficiencies that misinterpret nanoscale features reconstructed from fluctuating image sequences, thus degrading the superresolution imaging quality and performance. Here we propose cross-cumulant enhanced radiality nanoscopy (CERN), which employs cross-cumulant analysis in tandem with radiality processing. We demonstrated that CERN can significantly improve the spatial resolution at a low light level while eliminating the misinterpretations of nanoscale features of the existing fluctuation-based superresolution methods. In the experiment, we further verified the superior performance of CERN over the current methods through performing multicolor superresolution imaging of subcellular microtubule networks and clathrin-coated pits as well as the high-precision reconstruction of densely packed RNA transcripts.

© 2020 Chinese Laser Press

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2018 (8)

Y. M. Sigal, R. Zhou, and X. Zhuang, “Visualizing and discovering cellular structures with super-resolution microscopy,” Science 361, 880–887 (2018).
[Crossref]

X. Huang, J. Fan, L. Li, H. Liu, R. Wu, Y. Wu, L. Wei, H. Mao, A. Lal, P. Xi, L. Tang, Y. Zhang, Y. Liu, S. Tan, and L. Chen, “Fast, long-term, super-resolution imaging with Hessian structured illumination microscopy,” Nat. Biotechnol. 36, 451–459 (2018).
[Crossref]

L. Zou, S. Zhang, B. Wang, and J. Tan, “High-order super-resolution optical fluctuation imaging based on low-pass denoising,” Opt. Lett. 43, 707–710 (2018).
[Crossref]

S. Culley, K. L. Tosheva, P. M. Pereira, and R. Henriques, “SRRF: universal live-cell super-resolution microscopy,” Int. J. Biochem. Cell Biol. 101, 74–79 (2018).
[Crossref]

Z. Zeng, J. Ma, P. Xi, and C. Xu, “Joint tagging assisted fluctuation nanoscopy enables fast high-density super-resolution imaging,” J. Biophoton. 11, e201800020 (2018).
[Crossref]

S. Culley, D. Albrecht, C. Jacobs, P. M. Pereira, C. Leterrier, J. Mercer, and R. Henriques, “Quantitative mapping and minimization of super-resolution optical imaging artifacts,” Nat. Meth. 15, 263–266 (2018).
[Crossref]

R. Li, X. Chen, Z. Lin, Y. Wang, and Y. Sun, “Expansion enhanced nanoscopy,” Nanoscale 10, 17552–17556 (2018).
[Crossref]

T. Lukes, J. Pospisil, K. Fliegel, T. Lasser, and G. M. Hagen, “Quantitative super-resolution single molecule microscopy dataset of YFP-tagged growth factor receptors,” GigaScience 7, giy002 (2018).
[Crossref]

2017 (3)

X. Chen, Z. Liu, R. Li, C. Shan, Z. Zeng, B. Xue, W. Yuan, C. Mo, P. Xi, and C. Wu, “Multicolor super-resolution fluorescence microscopy with blue and carmine small photoblinking polymer dots,” ACS Nano 11, 8084–8091 (2017).
[Crossref]

S. J. Sahl, S. W. Hell, and S. Jakobs, “Fluorescence nanoscopy in cell biology,” Nat. Rev. Mol. Cell Biol. 18, 685–701 (2017).
[Crossref]

W. Yan, Y. Yang, Y. Tan, X. Chen, Y. Li, J. Qu, and T. Ye, “Coherent optical adaptive technique improves the spatial resolution of STED microscopy in thick samples,” Photon. Res. 5, 176–181 (2017).
[Crossref]

2016 (5)

Z. Zeng and P. Xi, “Advances in three-dimensional super-resolution nanoscopy,” Microsc. Res. Tech. 79, 893–898 (2016).
[Crossref]

A. L. Efros and D. J. Nesbitt, “Origin and control of blinking in quantum dots,” Nat. Nanotechnol. 11, 661–671 (2016).
[Crossref]

N. Gustafsson, S. Culley, G. Ashdown, D. M. Owen, P. M. Pereira, and R. Henriques, “Fast live-cell conventional fluorophore nanoscopy with ImageJ through super-resolution radial fluctuations,” Nat. Commun. 7, 12471 (2016).
[Crossref]

S. Jiang, Y. Zhang, H. Yang, Y. Xiao, X. Miao, R. Li, Y. Xu, and X. Zhang, “Enhanced SOFI algorithm achieved with modified optical fluctuating signal extraction,” Opt. Express 24, 3037–3045 (2016).
[Crossref]

W. Xuehua, C. Danni, Y. Bin, and N. Hanben, “Statistical precision in super-resolution optical fluctuation imaging,” Appl. Opt. 55, 7911–7916 (2016).
[Crossref]

2015 (4)

F. Chen, P. W. Tillberg, and E. S. Boyden, “Expansion microscopy,” Science 347, 543–548 (2015).
[Crossref]

Z. Zeng, X. Chen, H. Wang, N. Huang, C. Shan, H. Zhang, J. Teng, and P. Xi, “Fast super-resolution imaging with ultra-high labeling density achieved by joint tagging super-resolution optical fluctuation imaging,” Sci. Rep. 5, 8359 (2015).
[Crossref]

I. Yahiatene, S. Hennig, M. Müller, and T. Huser, “Entropy-based super-resolution imaging (ESI): from disorder to fine detail,” ACS Photon. 2, 1049–1056 (2015).
[Crossref]

X. Chen, Z. Zeng, H. Wang, and P. Xi, “Three-dimensional multimodal sub-diffraction imaging with spinning-disk confocal microscopy using blinking/fluctuating probes,” Nano Res. 8, 2251–2260 (2015).
[Crossref]

2014 (1)

S. Geissbuehler, A. Sharipov, A. Godinat, N. L. Bocchio, P. A. Sandoz, A. Huss, N. A. Jensen, S. Jakobs, J. Enderlein, and F. G. Van Der Goot, “Live-cell multiplane three-dimensional super-resolution optical fluctuation imaging,” Nat. Commun. 5, 5830 (2014).
[Crossref]

2013 (1)

T. Dertinger, A. Pallaoro, G. Braun, S. Ly, T. A. Laurence, and S. Weiss, “Advances in superresolution optical fluctuation imaging (SOFI),” Quart. Rev. Biophys. 46, 210–221 (2013).
[Crossref]

2012 (3)

S. Geissbuehler, N. L. Bocchio, C. Dellagiacoma, C. Berclaz, M. Leutenegger, and T. Lasser, “Mapping molecular statistics with balanced super-resolution optical fluctuation imaging (bSOFI),” Opt. Nanosc. 1, 4–7 (2012).
[Crossref]

S. Cox, E. Rosten, J. Monypenny, T. Jovanovic-Talisman, D. T. Burnette, J. Lippincott-Schwartz, G. E. Jones, and R. Heintzmann, “Bayesian localization microscopy reveals nanoscale podosome dynamics,” Nat. Meth. 9, 195–200 (2012).
[Crossref]

J. Chojnacki, T. Staudt, B. Glass, P. Bingen, J. Engelhardt, M. Anders, J. Schneider, B. Müller, S. W. Hell, and H.-G. Kräusslich, “Maturation-dependent HIV-1 surface protein redistribution revealed by fluorescence nanoscopy,” Science 338, 524–528 (2012).
[Crossref]

2011 (1)

D. T. Burnette, P. Sengupta, Y. Dai, J. Lippincott-Schwartz, and B. Kachar, “Bleaching/blinking assisted localization microscopy for superresolution imaging using standard fluorescent molecules,” Proc. Natl. Acad. Sci. USA 108, 21081–21086 (2011).
[Crossref]

2010 (2)

T. Dertinger, R. Colyer, R. Vogel, J. Enderlein, and S. Weiss, “Achieving increased resolution and more pixels with Superresolution Optical Fluctuation Imaging (SOFI),” Opt. Express 18, 18875–18885 (2010).
[Crossref]

T. M. Watanabe, S. Fukui, T. Jin, F. Fujii, and T. Yanagida, “Real-time nanoscopy by using blinking enhanced quantum dots,” Biophys. J. 99, L50–L52 (2010).
[Crossref]

2009 (1)

T. Dertinger, R. Colyer, G. Iyer, S. Weiss, and J. Enderlein, “Fast, background-free, 3D super-resolution optical fluctuation imaging (SOFI),” Proc. Natl. Acad. Sci. USA 106, 22287–22292 (2009).
[Crossref]

2006 (3)

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, 1642–1645 (2006).
[Crossref]

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

S. T. Hess, T. P. Girirajan, and M. D. Mason, “Ultra-high resolution imaging by fluorescence photoactivation localization microscopy,” Biophys. J. 91, 4258–4272 (2006).
[Crossref]

2000 (1)

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

1994 (1)

Albrecht, D.

S. Culley, D. Albrecht, C. Jacobs, P. M. Pereira, C. Leterrier, J. Mercer, and R. Henriques, “Quantitative mapping and minimization of super-resolution optical imaging artifacts,” Nat. Meth. 15, 263–266 (2018).
[Crossref]

Anders, M.

J. Chojnacki, T. Staudt, B. Glass, P. Bingen, J. Engelhardt, M. Anders, J. Schneider, B. Müller, S. W. Hell, and H.-G. Kräusslich, “Maturation-dependent HIV-1 surface protein redistribution revealed by fluorescence nanoscopy,” Science 338, 524–528 (2012).
[Crossref]

Ashdown, G.

N. Gustafsson, S. Culley, G. Ashdown, D. M. Owen, P. M. Pereira, and R. Henriques, “Fast live-cell conventional fluorophore nanoscopy with ImageJ through super-resolution radial fluctuations,” Nat. Commun. 7, 12471 (2016).
[Crossref]

Bates, M.

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

Berclaz, C.

S. Geissbuehler, N. L. Bocchio, C. Dellagiacoma, C. Berclaz, M. Leutenegger, and T. Lasser, “Mapping molecular statistics with balanced super-resolution optical fluctuation imaging (bSOFI),” Opt. Nanosc. 1, 4–7 (2012).
[Crossref]

Betzig, E.

E. Betzig, G. H. Patterson, R. Sougrat, O. W. Lindwasser, S. Olenych, J. S. Bonifacino, M. W. Davidson, J. Lippincott-Schwartz, and H. F. Hess, “Imaging intracellular fluorescent proteins at nanometer resolution,” Science 313, 1642–1645 (2006).
[Crossref]

Bin, Y.

Bingen, P.

J. Chojnacki, T. Staudt, B. Glass, P. Bingen, J. Engelhardt, M. Anders, J. Schneider, B. Müller, S. W. Hell, and H.-G. Kräusslich, “Maturation-dependent HIV-1 surface protein redistribution revealed by fluorescence nanoscopy,” Science 338, 524–528 (2012).
[Crossref]

Bocchio, N. L.

S. Geissbuehler, A. Sharipov, A. Godinat, N. L. Bocchio, P. A. Sandoz, A. Huss, N. A. Jensen, S. Jakobs, J. Enderlein, and F. G. Van Der Goot, “Live-cell multiplane three-dimensional super-resolution optical fluctuation imaging,” Nat. Commun. 5, 5830 (2014).
[Crossref]

S. Geissbuehler, N. L. Bocchio, C. Dellagiacoma, C. Berclaz, M. Leutenegger, and T. Lasser, “Mapping molecular statistics with balanced super-resolution optical fluctuation imaging (bSOFI),” Opt. Nanosc. 1, 4–7 (2012).
[Crossref]

Bonifacino, J. S.

E. Betzig, G. H. Patterson, R. Sougrat, O. W. Lindwasser, S. Olenych, J. S. Bonifacino, M. W. Davidson, J. Lippincott-Schwartz, and H. F. Hess, “Imaging intracellular fluorescent proteins at nanometer resolution,” Science 313, 1642–1645 (2006).
[Crossref]

Boyden, E. S.

F. Chen, P. W. Tillberg, and E. S. Boyden, “Expansion microscopy,” Science 347, 543–548 (2015).
[Crossref]

Braun, G.

T. Dertinger, A. Pallaoro, G. Braun, S. Ly, T. A. Laurence, and S. Weiss, “Advances in superresolution optical fluctuation imaging (SOFI),” Quart. Rev. Biophys. 46, 210–221 (2013).
[Crossref]

Burnette, D. T.

S. Cox, E. Rosten, J. Monypenny, T. Jovanovic-Talisman, D. T. Burnette, J. Lippincott-Schwartz, G. E. Jones, and R. Heintzmann, “Bayesian localization microscopy reveals nanoscale podosome dynamics,” Nat. Meth. 9, 195–200 (2012).
[Crossref]

D. T. Burnette, P. Sengupta, Y. Dai, J. Lippincott-Schwartz, and B. Kachar, “Bleaching/blinking assisted localization microscopy for superresolution imaging using standard fluorescent molecules,” Proc. Natl. Acad. Sci. USA 108, 21081–21086 (2011).
[Crossref]

Chen, F.

F. Chen, P. W. Tillberg, and E. S. Boyden, “Expansion microscopy,” Science 347, 543–548 (2015).
[Crossref]

Chen, L.

X. Huang, J. Fan, L. Li, H. Liu, R. Wu, Y. Wu, L. Wei, H. Mao, A. Lal, P. Xi, L. Tang, Y. Zhang, Y. Liu, S. Tan, and L. Chen, “Fast, long-term, super-resolution imaging with Hessian structured illumination microscopy,” Nat. Biotechnol. 36, 451–459 (2018).
[Crossref]

Chen, X.

R. Li, X. Chen, Z. Lin, Y. Wang, and Y. Sun, “Expansion enhanced nanoscopy,” Nanoscale 10, 17552–17556 (2018).
[Crossref]

W. Yan, Y. Yang, Y. Tan, X. Chen, Y. Li, J. Qu, and T. Ye, “Coherent optical adaptive technique improves the spatial resolution of STED microscopy in thick samples,” Photon. Res. 5, 176–181 (2017).
[Crossref]

X. Chen, Z. Liu, R. Li, C. Shan, Z. Zeng, B. Xue, W. Yuan, C. Mo, P. Xi, and C. Wu, “Multicolor super-resolution fluorescence microscopy with blue and carmine small photoblinking polymer dots,” ACS Nano 11, 8084–8091 (2017).
[Crossref]

X. Chen, Z. Zeng, H. Wang, and P. Xi, “Three-dimensional multimodal sub-diffraction imaging with spinning-disk confocal microscopy using blinking/fluctuating probes,” Nano Res. 8, 2251–2260 (2015).
[Crossref]

Z. Zeng, X. Chen, H. Wang, N. Huang, C. Shan, H. Zhang, J. Teng, and P. Xi, “Fast super-resolution imaging with ultra-high labeling density achieved by joint tagging super-resolution optical fluctuation imaging,” Sci. Rep. 5, 8359 (2015).
[Crossref]

Chojnacki, J.

J. Chojnacki, T. Staudt, B. Glass, P. Bingen, J. Engelhardt, M. Anders, J. Schneider, B. Müller, S. W. Hell, and H.-G. Kräusslich, “Maturation-dependent HIV-1 surface protein redistribution revealed by fluorescence nanoscopy,” Science 338, 524–528 (2012).
[Crossref]

Colyer, R.

T. Dertinger, R. Colyer, R. Vogel, J. Enderlein, and S. Weiss, “Achieving increased resolution and more pixels with Superresolution Optical Fluctuation Imaging (SOFI),” Opt. Express 18, 18875–18885 (2010).
[Crossref]

T. Dertinger, R. Colyer, G. Iyer, S. Weiss, and J. Enderlein, “Fast, background-free, 3D super-resolution optical fluctuation imaging (SOFI),” Proc. Natl. Acad. Sci. USA 106, 22287–22292 (2009).
[Crossref]

Cox, S.

S. Cox, E. Rosten, J. Monypenny, T. Jovanovic-Talisman, D. T. Burnette, J. Lippincott-Schwartz, G. E. Jones, and R. Heintzmann, “Bayesian localization microscopy reveals nanoscale podosome dynamics,” Nat. Meth. 9, 195–200 (2012).
[Crossref]

Culley, S.

S. Culley, D. Albrecht, C. Jacobs, P. M. Pereira, C. Leterrier, J. Mercer, and R. Henriques, “Quantitative mapping and minimization of super-resolution optical imaging artifacts,” Nat. Meth. 15, 263–266 (2018).
[Crossref]

S. Culley, K. L. Tosheva, P. M. Pereira, and R. Henriques, “SRRF: universal live-cell super-resolution microscopy,” Int. J. Biochem. Cell Biol. 101, 74–79 (2018).
[Crossref]

N. Gustafsson, S. Culley, G. Ashdown, D. M. Owen, P. M. Pereira, and R. Henriques, “Fast live-cell conventional fluorophore nanoscopy with ImageJ through super-resolution radial fluctuations,” Nat. Commun. 7, 12471 (2016).
[Crossref]

Dai, Y.

D. T. Burnette, P. Sengupta, Y. Dai, J. Lippincott-Schwartz, and B. Kachar, “Bleaching/blinking assisted localization microscopy for superresolution imaging using standard fluorescent molecules,” Proc. Natl. Acad. Sci. USA 108, 21081–21086 (2011).
[Crossref]

Danni, C.

Davidson, M. 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,” Science 313, 1642–1645 (2006).
[Crossref]

Dellagiacoma, C.

S. Geissbuehler, N. L. Bocchio, C. Dellagiacoma, C. Berclaz, M. Leutenegger, and T. Lasser, “Mapping molecular statistics with balanced super-resolution optical fluctuation imaging (bSOFI),” Opt. Nanosc. 1, 4–7 (2012).
[Crossref]

Dertinger, T.

T. Dertinger, A. Pallaoro, G. Braun, S. Ly, T. A. Laurence, and S. Weiss, “Advances in superresolution optical fluctuation imaging (SOFI),” Quart. Rev. Biophys. 46, 210–221 (2013).
[Crossref]

T. Dertinger, R. Colyer, R. Vogel, J. Enderlein, and S. Weiss, “Achieving increased resolution and more pixels with Superresolution Optical Fluctuation Imaging (SOFI),” Opt. Express 18, 18875–18885 (2010).
[Crossref]

T. Dertinger, R. Colyer, G. Iyer, S. Weiss, and J. Enderlein, “Fast, background-free, 3D super-resolution optical fluctuation imaging (SOFI),” Proc. Natl. Acad. Sci. USA 106, 22287–22292 (2009).
[Crossref]

Efros, A. L.

A. L. Efros and D. J. Nesbitt, “Origin and control of blinking in quantum dots,” Nat. Nanotechnol. 11, 661–671 (2016).
[Crossref]

Enderlein, J.

S. Geissbuehler, A. Sharipov, A. Godinat, N. L. Bocchio, P. A. Sandoz, A. Huss, N. A. Jensen, S. Jakobs, J. Enderlein, and F. G. Van Der Goot, “Live-cell multiplane three-dimensional super-resolution optical fluctuation imaging,” Nat. Commun. 5, 5830 (2014).
[Crossref]

T. Dertinger, R. Colyer, R. Vogel, J. Enderlein, and S. Weiss, “Achieving increased resolution and more pixels with Superresolution Optical Fluctuation Imaging (SOFI),” Opt. Express 18, 18875–18885 (2010).
[Crossref]

T. Dertinger, R. Colyer, G. Iyer, S. Weiss, and J. Enderlein, “Fast, background-free, 3D super-resolution optical fluctuation imaging (SOFI),” Proc. Natl. Acad. Sci. USA 106, 22287–22292 (2009).
[Crossref]

Engelhardt, J.

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T. Dertinger, A. Pallaoro, G. Braun, S. Ly, T. A. Laurence, and S. Weiss, “Advances in superresolution optical fluctuation imaging (SOFI),” Quart. Rev. Biophys. 46, 210–221 (2013).
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T. Dertinger, R. Colyer, G. Iyer, S. Weiss, and J. Enderlein, “Fast, background-free, 3D super-resolution optical fluctuation imaging (SOFI),” Proc. Natl. Acad. Sci. USA 106, 22287–22292 (2009).
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Wu, C.

X. Chen, Z. Liu, R. Li, C. Shan, Z. Zeng, B. Xue, W. Yuan, C. Mo, P. Xi, and C. Wu, “Multicolor super-resolution fluorescence microscopy with blue and carmine small photoblinking polymer dots,” ACS Nano 11, 8084–8091 (2017).
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Wu, R.

X. Huang, J. Fan, L. Li, H. Liu, R. Wu, Y. Wu, L. Wei, H. Mao, A. Lal, P. Xi, L. Tang, Y. Zhang, Y. Liu, S. Tan, and L. Chen, “Fast, long-term, super-resolution imaging with Hessian structured illumination microscopy,” Nat. Biotechnol. 36, 451–459 (2018).
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Wu, Y.

X. Huang, J. Fan, L. Li, H. Liu, R. Wu, Y. Wu, L. Wei, H. Mao, A. Lal, P. Xi, L. Tang, Y. Zhang, Y. Liu, S. Tan, and L. Chen, “Fast, long-term, super-resolution imaging with Hessian structured illumination microscopy,” Nat. Biotechnol. 36, 451–459 (2018).
[Crossref]

Xi, P.

X. Huang, J. Fan, L. Li, H. Liu, R. Wu, Y. Wu, L. Wei, H. Mao, A. Lal, P. Xi, L. Tang, Y. Zhang, Y. Liu, S. Tan, and L. Chen, “Fast, long-term, super-resolution imaging with Hessian structured illumination microscopy,” Nat. Biotechnol. 36, 451–459 (2018).
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Z. Zeng, J. Ma, P. Xi, and C. Xu, “Joint tagging assisted fluctuation nanoscopy enables fast high-density super-resolution imaging,” J. Biophoton. 11, e201800020 (2018).
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X. Chen, Z. Liu, R. Li, C. Shan, Z. Zeng, B. Xue, W. Yuan, C. Mo, P. Xi, and C. Wu, “Multicolor super-resolution fluorescence microscopy with blue and carmine small photoblinking polymer dots,” ACS Nano 11, 8084–8091 (2017).
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Z. Zeng and P. Xi, “Advances in three-dimensional super-resolution nanoscopy,” Microsc. Res. Tech. 79, 893–898 (2016).
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X. Chen, Z. Zeng, H. Wang, and P. Xi, “Three-dimensional multimodal sub-diffraction imaging with spinning-disk confocal microscopy using blinking/fluctuating probes,” Nano Res. 8, 2251–2260 (2015).
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Z. Zeng, X. Chen, H. Wang, N. Huang, C. Shan, H. Zhang, J. Teng, and P. Xi, “Fast super-resolution imaging with ultra-high labeling density achieved by joint tagging super-resolution optical fluctuation imaging,” Sci. Rep. 5, 8359 (2015).
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Xiao, Y.

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Z. Zeng, J. Ma, P. Xi, and C. Xu, “Joint tagging assisted fluctuation nanoscopy enables fast high-density super-resolution imaging,” J. Biophoton. 11, e201800020 (2018).
[Crossref]

Xu, Y.

Xue, B.

X. Chen, Z. Liu, R. Li, C. Shan, Z. Zeng, B. Xue, W. Yuan, C. Mo, P. Xi, and C. Wu, “Multicolor super-resolution fluorescence microscopy with blue and carmine small photoblinking polymer dots,” ACS Nano 11, 8084–8091 (2017).
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Xuehua, W.

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I. Yahiatene, S. Hennig, M. Müller, and T. Huser, “Entropy-based super-resolution imaging (ESI): from disorder to fine detail,” ACS Photon. 2, 1049–1056 (2015).
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Yan, W.

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T. M. Watanabe, S. Fukui, T. Jin, F. Fujii, and T. Yanagida, “Real-time nanoscopy by using blinking enhanced quantum dots,” Biophys. J. 99, L50–L52 (2010).
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Yang, H.

Yang, Y.

Ye, T.

Yuan, W.

X. Chen, Z. Liu, R. Li, C. Shan, Z. Zeng, B. Xue, W. Yuan, C. Mo, P. Xi, and C. Wu, “Multicolor super-resolution fluorescence microscopy with blue and carmine small photoblinking polymer dots,” ACS Nano 11, 8084–8091 (2017).
[Crossref]

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Z. Zeng, J. Ma, P. Xi, and C. Xu, “Joint tagging assisted fluctuation nanoscopy enables fast high-density super-resolution imaging,” J. Biophoton. 11, e201800020 (2018).
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X. Chen, Z. Liu, R. Li, C. Shan, Z. Zeng, B. Xue, W. Yuan, C. Mo, P. Xi, and C. Wu, “Multicolor super-resolution fluorescence microscopy with blue and carmine small photoblinking polymer dots,” ACS Nano 11, 8084–8091 (2017).
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Z. Zeng and P. Xi, “Advances in three-dimensional super-resolution nanoscopy,” Microsc. Res. Tech. 79, 893–898 (2016).
[Crossref]

X. Chen, Z. Zeng, H. Wang, and P. Xi, “Three-dimensional multimodal sub-diffraction imaging with spinning-disk confocal microscopy using blinking/fluctuating probes,” Nano Res. 8, 2251–2260 (2015).
[Crossref]

Z. Zeng, X. Chen, H. Wang, N. Huang, C. Shan, H. Zhang, J. Teng, and P. Xi, “Fast super-resolution imaging with ultra-high labeling density achieved by joint tagging super-resolution optical fluctuation imaging,” Sci. Rep. 5, 8359 (2015).
[Crossref]

Zhang, H.

Z. Zeng, X. Chen, H. Wang, N. Huang, C. Shan, H. Zhang, J. Teng, and P. Xi, “Fast super-resolution imaging with ultra-high labeling density achieved by joint tagging super-resolution optical fluctuation imaging,” Sci. Rep. 5, 8359 (2015).
[Crossref]

Zhang, S.

Zhang, X.

Zhang, Y.

X. Huang, J. Fan, L. Li, H. Liu, R. Wu, Y. Wu, L. Wei, H. Mao, A. Lal, P. Xi, L. Tang, Y. Zhang, Y. Liu, S. Tan, and L. Chen, “Fast, long-term, super-resolution imaging with Hessian structured illumination microscopy,” Nat. Biotechnol. 36, 451–459 (2018).
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S. Jiang, Y. Zhang, H. Yang, Y. Xiao, X. Miao, R. Li, Y. Xu, and X. Zhang, “Enhanced SOFI algorithm achieved with modified optical fluctuating signal extraction,” Opt. Express 24, 3037–3045 (2016).
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Y. M. Sigal, R. Zhou, and X. Zhuang, “Visualizing and discovering cellular structures with super-resolution microscopy,” Science 361, 880–887 (2018).
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Zhuang, X.

Y. M. Sigal, R. Zhou, and X. Zhuang, “Visualizing and discovering cellular structures with super-resolution microscopy,” Science 361, 880–887 (2018).
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M. J. Rust, M. Bates, and X. Zhuang, “Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM),” Nat. Meth. 3, 793–796 (2006).
[Crossref]

Zou, L.

ACS Nano (1)

X. Chen, Z. Liu, R. Li, C. Shan, Z. Zeng, B. Xue, W. Yuan, C. Mo, P. Xi, and C. Wu, “Multicolor super-resolution fluorescence microscopy with blue and carmine small photoblinking polymer dots,” ACS Nano 11, 8084–8091 (2017).
[Crossref]

ACS Photon. (1)

I. Yahiatene, S. Hennig, M. Müller, and T. Huser, “Entropy-based super-resolution imaging (ESI): from disorder to fine detail,” ACS Photon. 2, 1049–1056 (2015).
[Crossref]

Appl. Opt. (1)

Biophys. J. (2)

T. M. Watanabe, S. Fukui, T. Jin, F. Fujii, and T. Yanagida, “Real-time nanoscopy by using blinking enhanced quantum dots,” Biophys. J. 99, L50–L52 (2010).
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S. T. Hess, T. P. Girirajan, and M. D. Mason, “Ultra-high resolution imaging by fluorescence photoactivation localization microscopy,” Biophys. J. 91, 4258–4272 (2006).
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GigaScience (1)

T. Lukes, J. Pospisil, K. Fliegel, T. Lasser, and G. M. Hagen, “Quantitative super-resolution single molecule microscopy dataset of YFP-tagged growth factor receptors,” GigaScience 7, giy002 (2018).
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Int. J. Biochem. Cell Biol. (1)

S. Culley, K. L. Tosheva, P. M. Pereira, and R. Henriques, “SRRF: universal live-cell super-resolution microscopy,” Int. J. Biochem. Cell Biol. 101, 74–79 (2018).
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J. Biophoton. (1)

Z. Zeng, J. Ma, P. Xi, and C. Xu, “Joint tagging assisted fluctuation nanoscopy enables fast high-density super-resolution imaging,” J. Biophoton. 11, e201800020 (2018).
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J. Microsc. (1)

M. G. Gustafsson, “Surpassing the lateral resolution limit by a factor of two using structured illumination microscopy,” J. Microsc. 198, 82–87 (2000).
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Microsc. Res. Tech. (1)

Z. Zeng and P. Xi, “Advances in three-dimensional super-resolution nanoscopy,” Microsc. Res. Tech. 79, 893–898 (2016).
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Nano Res. (1)

X. Chen, Z. Zeng, H. Wang, and P. Xi, “Three-dimensional multimodal sub-diffraction imaging with spinning-disk confocal microscopy using blinking/fluctuating probes,” Nano Res. 8, 2251–2260 (2015).
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Nanoscale (1)

R. Li, X. Chen, Z. Lin, Y. Wang, and Y. Sun, “Expansion enhanced nanoscopy,” Nanoscale 10, 17552–17556 (2018).
[Crossref]

Nat. Biotechnol. (1)

X. Huang, J. Fan, L. Li, H. Liu, R. Wu, Y. Wu, L. Wei, H. Mao, A. Lal, P. Xi, L. Tang, Y. Zhang, Y. Liu, S. Tan, and L. Chen, “Fast, long-term, super-resolution imaging with Hessian structured illumination microscopy,” Nat. Biotechnol. 36, 451–459 (2018).
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Nat. Commun. (2)

N. Gustafsson, S. Culley, G. Ashdown, D. M. Owen, P. M. Pereira, and R. Henriques, “Fast live-cell conventional fluorophore nanoscopy with ImageJ through super-resolution radial fluctuations,” Nat. Commun. 7, 12471 (2016).
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Nat. Meth. (3)

S. Culley, D. Albrecht, C. Jacobs, P. M. Pereira, C. Leterrier, J. Mercer, and R. Henriques, “Quantitative mapping and minimization of super-resolution optical imaging artifacts,” Nat. Meth. 15, 263–266 (2018).
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M. J. Rust, M. Bates, and X. Zhuang, “Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM),” Nat. Meth. 3, 793–796 (2006).
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S. Cox, E. Rosten, J. Monypenny, T. Jovanovic-Talisman, D. T. Burnette, J. Lippincott-Schwartz, G. E. Jones, and R. Heintzmann, “Bayesian localization microscopy reveals nanoscale podosome dynamics,” Nat. Meth. 9, 195–200 (2012).
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Nat. Nanotechnol. (1)

A. L. Efros and D. J. Nesbitt, “Origin and control of blinking in quantum dots,” Nat. Nanotechnol. 11, 661–671 (2016).
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Nat. Rev. Mol. Cell Biol. (1)

S. J. Sahl, S. W. Hell, and S. Jakobs, “Fluorescence nanoscopy in cell biology,” Nat. Rev. Mol. Cell Biol. 18, 685–701 (2017).
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Opt. Express (2)

Opt. Lett. (2)

Opt. Nanosc. (1)

S. Geissbuehler, N. L. Bocchio, C. Dellagiacoma, C. Berclaz, M. Leutenegger, and T. Lasser, “Mapping molecular statistics with balanced super-resolution optical fluctuation imaging (bSOFI),” Opt. Nanosc. 1, 4–7 (2012).
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Photon. Res. (1)

Proc. Natl. Acad. Sci. USA (2)

D. T. Burnette, P. Sengupta, Y. Dai, J. Lippincott-Schwartz, and B. Kachar, “Bleaching/blinking assisted localization microscopy for superresolution imaging using standard fluorescent molecules,” Proc. Natl. Acad. Sci. USA 108, 21081–21086 (2011).
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T. Dertinger, R. Colyer, G. Iyer, S. Weiss, and J. Enderlein, “Fast, background-free, 3D super-resolution optical fluctuation imaging (SOFI),” Proc. Natl. Acad. Sci. USA 106, 22287–22292 (2009).
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Quart. Rev. Biophys. (1)

T. Dertinger, A. Pallaoro, G. Braun, S. Ly, T. A. Laurence, and S. Weiss, “Advances in superresolution optical fluctuation imaging (SOFI),” Quart. Rev. Biophys. 46, 210–221 (2013).
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Sci. Rep. (1)

Z. Zeng, X. Chen, H. Wang, N. Huang, C. Shan, H. Zhang, J. Teng, and P. Xi, “Fast super-resolution imaging with ultra-high labeling density achieved by joint tagging super-resolution optical fluctuation imaging,” Sci. Rep. 5, 8359 (2015).
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Science (4)

Y. M. Sigal, R. Zhou, and X. Zhuang, “Visualizing and discovering cellular structures with super-resolution microscopy,” Science 361, 880–887 (2018).
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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, 1642–1645 (2006).
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Figures (4)

Fig. 1.
Fig. 1. (a) Simulated 2D array of ring-like structures with varying radii; (b) wide-field imaging of the simulated ring-like structures; (c) distribution of different SNRs by adding different levels of Poisson noise in a discrete manner along the vertical direction; (d) second-order SOFI of the simulated ring-like structures; (e)–(g) SRRF of the simulated ring-like structures with TRA, TRM, and TRPPM calculation modes; (h)–(j) SRRF of the simulated ring-like structures with TRAC 2, TRAC 3, and TRAC 4 calculation modes; (k) CERN imaging of the simulated ring-like structures; (l) RSP coefficient evaluation of the reconstructed ring-like structures by different imaging methods in the high SNR and low SNR regions; (m)–(p) RSE evaluation of the reconstructed ring-like structures in the low SNR region with TRAC 2, TRAC 3, TRAC 4, and CERN imaging methods. The histograms of (b) and (d) were equalized for clear visualization of the low SNR structures. The source code and data set are available on Github, https://github.com/zhipingzeng/CERN. Scale bar, 500 nm.
Fig. 2.
Fig. 2. (a) Wide-field image of the simulated tubulin-like network with dynamic doughnut-shaped and point-like nanoscale cargoes moving along network lines; (b), (c) second-order SOFI and SRRF (TRA) images of the simulated dynamic structure; (d) CERN image of the simulated dynamic structure, precisely discerning the doughnut-shaped cargoes (marked by “D”) from the point-like cargoes (marked by “P”); (e)–(h) magnified images indicated by the white dotted regions from (a) to (d). For the cargoes marked by “P,” we generated the cargo images by convolving point-like structures (30 nm radii) with a Gaussian PSF. For the cargoes marked by “D,” we generated the cargo images by convolving ring-like structures (90 nm radii) with a smaller Gaussian PSF. Different PSFs indicated the labeling of two different types of fluorophores with distinct wavelengths for imaging different targets. The blue and red arrows represent the different moving directions of the cargoes along the network lines. Scale bars, 1 μm in (a)–(d); 300 nm in (e)–(h).
Fig. 3.
Fig. 3. (a), (b) Multicolor wide-field and second-order SOFI images of the subcellular microtubule network and CCPs [33]; (c) SRRF image with TRAC 2 calculation mode of the microtubule network and CCPs; (d) CERN image of the microtubule network and CCPs; (e) line profiles of the wide-field, second SOFI-, SRRF (TRAC 2)-, and CERN-reconstructed CCPs indicated by the white arrows in (f)–(i); (f)–(i) magnified images of the white dotted regions from (a)–(d); (j)–(k) RSE evaluation of the reconstructed CCP in TRAC 2 and CERN imaging; (l) line profiles of the second SOFI-, SRRF (TRAC 2)-, and CERN-reconstructed closely separated filaments located by the red arrows in (b)–(d). Scale bars, 1 μm in (a)–(d); 500 nm in (f)–(i).
Fig. 4.
Fig. 4. (a) Wide-field image of the densely pack RNA transcripts; (b)–(d) second-order SOFI, SRRF (TRPPM), and SRRF (TRAC 2) images of the RNA molecule distribution; (e) ThunderSTORM image of the RNA molecule distribution [34]; (f) CERN image of the RNA molecules; (g) line profiles of the SRRF (TRPPM)-, SRRF (TRAC 2)-, ThunderSTORM-, and CERN-reconstructed RNA molecules indicated by the white arrows in (c)–(f). (h) FRC comparison of the reconstructed superresolution images from SRRF (TRPPM), SRRF (TRAC 2), ThunderSTORM, and CERN methods. The standard deviations were calculated by using three different image sequences for image reconstructions. Raw data courtesy of the GigaScience Database [34]. Scale bars, 1 μm in (a)–(f).

Equations (6)

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

XCn(r=1ni=1nri)=m=1MAmnPSFn(rrm)Cn{δfm(t)}.
XC2(X,Y)={XC2(2x+i,2y+j)i,j=0,1ij=α·δF(x,y,t+τ)·δF(x+i,y+j,t)tXC2(2x+i,2y+j)i,j=0=α·δF(x,y,t+τ)·δF(x+i+1,y+j+1,t)tXC2(2x+i,2y+j)i,j=1=α·δF(x+i,y,t+τ)·δF(x,y+j,t)t}.
(XYi)GYi(XYi)GXi=0.
R(X,Y)=1Ni=1Nsgn(Gi·ri|Gi||ri|)·(1di|ri|)2.
RSE=x,y[ID(x,y)IRS(x,y)]2n.
RSP=x,y[ID(x,y)I¯D][IRS(x,y)I¯RS]x,y[ID(x,y)I¯D]2x,y[IRS(x,y)I¯RS]2.