Abstract

We report the observation of chromatin dynamics in living budding yeast (Saccharomyces cerevisiae) cells, in three-dimensions (3D). Using dual color localization microscopy and employing a Tetrapod point spread function, we analyze the spatio-temporal dynamics of two fluorescently labeled DNA loci surrounding the GAL locus. From the measured trajectories, we obtain different dynamical characteristics in terms of inter-loci distance and temporal variance; when the GAL locus is activated, the 3D inter-loci distance and temporal variance increase compared to the inactive state. These changes are visible in spite of the large thermally- and biologically-driven heterogeneity in the relative motion of the two loci. Our observations are consistent with current euchromatin vs. heterochromatin models.

© 2017 Optical Society of America

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References

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    [PubMed]

2017 (1)

2016 (1)

Y. Shechtman, L. E. Weiss, A. S. Backer, M. Y. Lee, and W. E. Moerner, “Multicolour localization microscopy by point-spread-function engineering,” Nat. Photonics 10, 590–594 (2016).
[PubMed]

2015 (3)

A. von Diezmann, M. Y. Lee, M. D. Lew, and W. E. Moerner, “Correcting field-dependent aberrations with nanoscale accuracy in three-dimensional single-molecule localization microscopy,” Optica 2(11), 985–993 (2015).
[PubMed]

Y. Shechtman, L. E. Weiss, A. S. Backer, S. J. Sahl, and W. E. Moerner, “Precise 3D scan-free multiple-particle tracking over large axial ranges with Tetrapod point spread functions,” Nano Lett. 15, 4194–4199 (2015).
[PubMed]

L. Carlini, S. J. Holden, K. M. Douglass, and S. Manley, “Correction of a depth-dependent lateral distortion in 3D super-resolution imaging,” PLoS One 10(11), e0142949 (2015).
[PubMed]

2014 (6)

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]

Y. Shechtman, S. J. Sahl, A. S. Backer, and W. E. Moerner, “Optimal Point Spread Function Design for 3D Imaging,” Phys. Rev. Lett. 113(13), 133902 (2014).
[PubMed]

A. S. Backer and W. E. Moerner, “Extending Single-Molecule Microscopy Using Optical Fourier Processing,” J. Phys. Chem. B 118(28), 8313–8329 (2014).
[PubMed]

M. K. Lee, P. Rai, J. Williams, R. J. Twieg, and W. E. Moerner, “Small-molecule labeling of live cell surfaces for three-dimensional super-resolution microscopy,” J. Am. Chem. Soc. 136(40), 14003–14006 (2014).
[PubMed]

S. Jia, J. C. Vaughan, and X. Zhuang, “Isotropic three-dimensional super-resolution imaging with a self-bending point spread function,” Nat. Photonics 8, 302–306 (2014).
[PubMed]

M. P. Backlund, R. Joyner, K. Weis, and W. E. Moerner, “Correlations of three-dimensional motion of chromosomal loci in yeast revealed by the Double-Helix Point Spread Function microscope,” Mol. Biol. Cell 25(22), 3619–3629 (2014).
[PubMed]

2013 (3)

W. A. Bickmore and B. van Steensel, “Genome architecture: domain organization of interphase chromosomes,” Cell 152(6), 1270–1284 (2013).
[PubMed]

S. Abrahamsson, J. Chen, B. Hajj, S. Stallinga, A. Y. Katsov, J. Wisniewski, G. Mizuguchi, P. Soule, F. Mueller, C. Dugast Darzacq, X. Darzacq, C. Wu, C. I. Bargmann, D. A. Agard, M. Dahan, and M. G. L. Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10(1), 60–63 (2013).
[PubMed]

A. Gahlmann, J. L. Ptacin, G. Grover, S. Quirin, A. R. S. von Diezmann, M. K. Lee, M. P. Backlund, L. Shapiro, R. Piestun, and W. E. Moerner, “Quantitative multicolor subdiffraction imaging of bacterial protein ultrastructures in three dimensions,” Nano Lett. 13(3), 987–993 (2013).
[PubMed]

2012 (1)

L. S. Churchman and J. A. Spudich, “Single-molecule high-resolution colocalization of single probes,” Cold Spring Harb. Protoc. 2012(2), 242–245 (2012).
[PubMed]

2011 (1)

P. A. Santi, “Light Sheet Fluorescence Microscopy: A Review,” J. Histochem. Cytochem. 59(2), 129–138 (2011).
[PubMed]

2010 (1)

M. A. Thompson, J. M. Casolari, M. Badieirostami, P. O. Brown, and W. E. Moerner, “Three-dimensional tracking of single mRNA particles in Saccharomyces cerevisiae using a double-helix point spread function,” Proc. Natl. Acad. Sci. U.S.A. 107(42), 17864–17871 (2010).
[PubMed]

2009 (3)

S. R. P. Pavani, M. A. Thompson, J. S. Biteen, S. J. Lord, N. Liu, R. J. Twieg, R. Piestun, and W. E. Moerner, “Three-dimensional, single-molecule fluorescence imaging beyond the diffraction limit by using a double-helix point spread function,” Proc. Natl. Acad. Sci. U.S.A. 106(9), 2995–2999 (2009).
[PubMed]

A. V. Abraham, S. Ram, J. Chao, E. S. Ward, and R. J. Ober, “Quantitative study of single molecule location estimation techniques,” Opt. Express 17(26), 23352–23373 (2009).
[PubMed]

E. Lieberman-Aiden, N. L. van Berkum, L. Williams, M. Imakaev, T. Ragoczy, A. Telling, I. Amit, B. R. Lajoie, P. J. Sabo, M. O. Dorschner, R. Sandstrom, B. Bernstein, M. A. Bender, M. Groudine, A. Gnirke, J. Stamatoyannopoulos, L. A. Mirny, E. S. Lander, and J. Dekker, “Comprehensive mapping of long-range interactions reveals folding principles of the human genome,” Science 326(5950), 289–293 (2009).
[PubMed]

2008 (1)

B. Huang, W. Wang, M. Bates, and X. Zhuang, “Three-dimensional super-resolution imaging by stochastic optical reconstruction microscopy,” Science 319(5864), 810–813 (2008).
[PubMed]

2007 (1)

L. Holtzer, T. Meckel, and T. Schmidt, “Nanometric three-dimensional tracking of individual quantum dots in cells,” Appl. Phys. Lett. 90, 053902 (2007).

2004 (2)

P. Prabhat, S. Ram, E. S. Ward, and R. J. Ober, “Simultaneous imaging of different focal planes in fluorescence microscopy for the study of cellular dynamics in three dimensions,” IEEE Trans. Nanobioscience 3(4), 237–242 (2004).
[PubMed]

J. Huisken, J. Swoger, F. Del Bene, J. Wittbrodt, and E. H. Stelzer, “Optical sectioning deep inside live embryos by selective plane illumination microscopy,” Science 305(5686), 1007–1009 (2004).
[PubMed]

2002 (1)

J. Dekker, K. Rippe, M. Dekker, and N. Kleckner, “Capturing Chromosome Conformation,” Science 295(5558), 1306–1311 (2002).
[PubMed]

2001 (1)

R. Bash and D. Lohr, “Yeast chromatin structure and regulation of GAL gene expression,” Prog. Nucleic Acid Res. Mol. Biol. 65, 197–259 (2001).
[PubMed]

1999 (1)

M. Johnston, “Feasting, fasting and fermenting. glucose sensing in yeast and other cells,” Trends Genet. 15(1), 29–33 (1999).
[PubMed]

1998 (1)

C. B. Brachmann, A. Davies, G. J. Cost, E. Caputo, J. Li, P. Hieter, and J. D. Boeke, “Designer deletion strains derived from Saccharomyces cerevisiae S288C: a useful set of strains and plasmids for PCR-mediated gene disruption and other applications,” Yeast 14(2), 115–132 (1998).
[PubMed]

1996 (1)

R. H. Webb, “Confocal optical microscopy,” Rep. Prog. Phys. 59, 427 (1996).

1994 (1)

H. P. Kao and A. S. Verkman, “Tracking of single fluorescent particles in three dimensions: use of cylindrical optics to encode particle position,” Biophys. J. 67(3), 1291–1300 (1994).
[PubMed]

1991 (1)

1962 (1)

L. A. Goodman, “The variance of the product of K random variables,” J. Am. Stat. Assoc. 57, 54–60 (1962).

1959 (1)

B. Richards and E. Wolf, “Electromagnetic Diffraction in optical systems. II. Structure of the image field in an aplanatic system,” Proc. R. Soc. Lond. A 253, 358–379 (1959).

Abraham, A. V.

Abrahamsson, S.

S. Abrahamsson, J. Chen, B. Hajj, S. Stallinga, A. Y. Katsov, J. Wisniewski, G. Mizuguchi, P. Soule, F. Mueller, C. Dugast Darzacq, X. Darzacq, C. Wu, C. I. Bargmann, D. A. Agard, M. Dahan, and M. G. L. Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10(1), 60–63 (2013).
[PubMed]

Agard, D. A.

S. Abrahamsson, J. Chen, B. Hajj, S. Stallinga, A. Y. Katsov, J. Wisniewski, G. Mizuguchi, P. Soule, F. Mueller, C. Dugast Darzacq, X. Darzacq, C. Wu, C. I. Bargmann, D. A. Agard, M. Dahan, and M. G. L. Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10(1), 60–63 (2013).
[PubMed]

Alber, F.

E. Dultz, R. Mancini, G. Polles, P. Vallotton, F. Alber, and K. Weis, “Quantitative imaging of chromatin decompaction in living cells,” bioRxiv (2017), doi:.
[Crossref]

Amit, I.

E. Lieberman-Aiden, N. L. van Berkum, L. Williams, M. Imakaev, T. Ragoczy, A. Telling, I. Amit, B. R. Lajoie, P. J. Sabo, M. O. Dorschner, R. Sandstrom, B. Bernstein, M. A. Bender, M. Groudine, A. Gnirke, J. Stamatoyannopoulos, L. A. Mirny, E. S. Lander, and J. Dekker, “Comprehensive mapping of long-range interactions reveals folding principles of the human genome,” Science 326(5950), 289–293 (2009).
[PubMed]

Backer, A. S.

Y. Shechtman, L. E. Weiss, A. S. Backer, M. Y. Lee, and W. E. Moerner, “Multicolour localization microscopy by point-spread-function engineering,” Nat. Photonics 10, 590–594 (2016).
[PubMed]

Y. Shechtman, L. E. Weiss, A. S. Backer, S. J. Sahl, and W. E. Moerner, “Precise 3D scan-free multiple-particle tracking over large axial ranges with Tetrapod point spread functions,” Nano Lett. 15, 4194–4199 (2015).
[PubMed]

A. S. Backer and W. E. Moerner, “Extending Single-Molecule Microscopy Using Optical Fourier Processing,” J. Phys. Chem. B 118(28), 8313–8329 (2014).
[PubMed]

Y. Shechtman, S. J. Sahl, A. S. Backer, and W. E. Moerner, “Optimal Point Spread Function Design for 3D Imaging,” Phys. Rev. Lett. 113(13), 133902 (2014).
[PubMed]

Backlund, M. P.

M. P. Backlund, R. Joyner, K. Weis, and W. E. Moerner, “Correlations of three-dimensional motion of chromosomal loci in yeast revealed by the Double-Helix Point Spread Function microscope,” Mol. Biol. Cell 25(22), 3619–3629 (2014).
[PubMed]

A. Gahlmann, J. L. Ptacin, G. Grover, S. Quirin, A. R. S. von Diezmann, M. K. Lee, M. P. Backlund, L. Shapiro, R. Piestun, and W. E. Moerner, “Quantitative multicolor subdiffraction imaging of bacterial protein ultrastructures in three dimensions,” Nano Lett. 13(3), 987–993 (2013).
[PubMed]

Badieirostami, M.

M. A. Thompson, J. M. Casolari, M. Badieirostami, P. O. Brown, and W. E. Moerner, “Three-dimensional tracking of single mRNA particles in Saccharomyces cerevisiae using a double-helix point spread function,” Proc. Natl. Acad. Sci. U.S.A. 107(42), 17864–17871 (2010).
[PubMed]

Bargmann, C. I.

S. Abrahamsson, J. Chen, B. Hajj, S. Stallinga, A. Y. Katsov, J. Wisniewski, G. Mizuguchi, P. Soule, F. Mueller, C. Dugast Darzacq, X. Darzacq, C. Wu, C. I. Bargmann, D. A. Agard, M. Dahan, and M. G. L. Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10(1), 60–63 (2013).
[PubMed]

Bash, R.

R. Bash and D. Lohr, “Yeast chromatin structure and regulation of GAL gene expression,” Prog. Nucleic Acid Res. Mol. Biol. 65, 197–259 (2001).
[PubMed]

Bates, M.

B. Huang, W. Wang, M. Bates, and X. Zhuang, “Three-dimensional super-resolution imaging by stochastic optical reconstruction microscopy,” Science 319(5864), 810–813 (2008).
[PubMed]

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]

Bender, M. A.

E. Lieberman-Aiden, N. L. van Berkum, L. Williams, M. Imakaev, T. Ragoczy, A. Telling, I. Amit, B. R. Lajoie, P. J. Sabo, M. O. Dorschner, R. Sandstrom, B. Bernstein, M. A. Bender, M. Groudine, A. Gnirke, J. Stamatoyannopoulos, L. A. Mirny, E. S. Lander, and J. Dekker, “Comprehensive mapping of long-range interactions reveals folding principles of the human genome,” Science 326(5950), 289–293 (2009).
[PubMed]

Bernstein, B.

E. Lieberman-Aiden, N. L. van Berkum, L. Williams, M. Imakaev, T. Ragoczy, A. Telling, I. Amit, B. R. Lajoie, P. J. Sabo, M. O. Dorschner, R. Sandstrom, B. Bernstein, M. A. Bender, M. Groudine, A. Gnirke, J. Stamatoyannopoulos, L. A. Mirny, E. S. Lander, and J. Dekker, “Comprehensive mapping of long-range interactions reveals folding principles of the human genome,” Science 326(5950), 289–293 (2009).
[PubMed]

Betzig, E.

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]

Bickmore, W. A.

W. A. Bickmore and B. van Steensel, “Genome architecture: domain organization of interphase chromosomes,” Cell 152(6), 1270–1284 (2013).
[PubMed]

Biteen, J. S.

S. R. P. Pavani, M. A. Thompson, J. S. Biteen, S. J. Lord, N. Liu, R. J. Twieg, R. Piestun, and W. E. Moerner, “Three-dimensional, single-molecule fluorescence imaging beyond the diffraction limit by using a double-helix point spread function,” Proc. Natl. Acad. Sci. U.S.A. 106(9), 2995–2999 (2009).
[PubMed]

Boeke, J. D.

C. B. Brachmann, A. Davies, G. J. Cost, E. Caputo, J. Li, P. Hieter, and J. D. Boeke, “Designer deletion strains derived from Saccharomyces cerevisiae S288C: a useful set of strains and plasmids for PCR-mediated gene disruption and other applications,” Yeast 14(2), 115–132 (1998).
[PubMed]

Böhme, R.

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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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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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Y. Shechtman, L. E. Weiss, A. S. Backer, M. Y. Lee, and W. E. Moerner, “Multicolour localization microscopy by point-spread-function engineering,” Nat. Photonics 10, 590–594 (2016).
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Y. Shechtman, L. E. Weiss, A. S. Backer, S. J. Sahl, and W. E. Moerner, “Precise 3D scan-free multiple-particle tracking over large axial ranges with Tetrapod point spread functions,” Nano Lett. 15, 4194–4199 (2015).
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A. von Diezmann, M. Y. Lee, M. D. Lew, and W. E. Moerner, “Correcting field-dependent aberrations with nanoscale accuracy in three-dimensional single-molecule localization microscopy,” Optica 2(11), 985–993 (2015).
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M. P. Backlund, R. Joyner, K. Weis, and W. E. Moerner, “Correlations of three-dimensional motion of chromosomal loci in yeast revealed by the Double-Helix Point Spread Function microscope,” Mol. Biol. Cell 25(22), 3619–3629 (2014).
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M. K. Lee, P. Rai, J. Williams, R. J. Twieg, and W. E. Moerner, “Small-molecule labeling of live cell surfaces for three-dimensional super-resolution microscopy,” J. Am. Chem. Soc. 136(40), 14003–14006 (2014).
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A. Gahlmann, J. L. Ptacin, G. Grover, S. Quirin, A. R. S. von Diezmann, M. K. Lee, M. P. Backlund, L. Shapiro, R. Piestun, and W. E. Moerner, “Quantitative multicolor subdiffraction imaging of bacterial protein ultrastructures in three dimensions,” Nano Lett. 13(3), 987–993 (2013).
[PubMed]

M. A. Thompson, J. M. Casolari, M. Badieirostami, P. O. Brown, and W. E. Moerner, “Three-dimensional tracking of single mRNA particles in Saccharomyces cerevisiae using a double-helix point spread function,” Proc. Natl. Acad. Sci. U.S.A. 107(42), 17864–17871 (2010).
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S. R. P. Pavani, M. A. Thompson, J. S. Biteen, S. J. Lord, N. Liu, R. J. Twieg, R. Piestun, and W. E. Moerner, “Three-dimensional, single-molecule fluorescence imaging beyond the diffraction limit by using a double-helix point spread function,” Proc. Natl. Acad. Sci. U.S.A. 106(9), 2995–2999 (2009).
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Piestun, R.

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S. R. P. Pavani, M. A. Thompson, J. S. Biteen, S. J. Lord, N. Liu, R. J. Twieg, R. Piestun, and W. E. Moerner, “Three-dimensional, single-molecule fluorescence imaging beyond the diffraction limit by using a double-helix point spread function,” Proc. Natl. Acad. Sci. U.S.A. 106(9), 2995–2999 (2009).
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E. Dultz, R. Mancini, G. Polles, P. Vallotton, F. Alber, and K. Weis, “Quantitative imaging of chromatin decompaction in living cells,” bioRxiv (2017), doi:.
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P. Prabhat, S. Ram, E. S. Ward, and R. J. Ober, “Simultaneous imaging of different focal planes in fluorescence microscopy for the study of cellular dynamics in three dimensions,” IEEE Trans. Nanobioscience 3(4), 237–242 (2004).
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M. K. Lee, P. Rai, J. Williams, R. J. Twieg, and W. E. Moerner, “Small-molecule labeling of live cell surfaces for three-dimensional super-resolution microscopy,” J. Am. Chem. Soc. 136(40), 14003–14006 (2014).
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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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E. Lieberman-Aiden, N. L. van Berkum, L. Williams, M. Imakaev, T. Ragoczy, A. Telling, I. Amit, B. R. Lajoie, P. J. Sabo, M. O. Dorschner, R. Sandstrom, B. Bernstein, M. A. Bender, M. Groudine, A. Gnirke, J. Stamatoyannopoulos, L. A. Mirny, E. S. Lander, and J. Dekker, “Comprehensive mapping of long-range interactions reveals folding principles of the human genome,” Science 326(5950), 289–293 (2009).
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Y. Shechtman, L. E. Weiss, A. S. Backer, S. J. Sahl, and W. E. Moerner, “Precise 3D scan-free multiple-particle tracking over large axial ranges with Tetrapod point spread functions,” Nano Lett. 15, 4194–4199 (2015).
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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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P. N. Petrov, Y. Shechtman, and W. E. Moerner, “Measurement-based estimation of global pupil functions in 3D localization microscopy,” Opt. Express 25(7), 7945–7959 (2017).
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Y. Shechtman, L. E. Weiss, A. S. Backer, M. Y. Lee, and W. E. Moerner, “Multicolour localization microscopy by point-spread-function engineering,” Nat. Photonics 10, 590–594 (2016).
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S. R. P. Pavani, M. A. Thompson, J. S. Biteen, S. J. Lord, N. Liu, R. J. Twieg, R. Piestun, and W. E. Moerner, “Three-dimensional, single-molecule fluorescence imaging beyond the diffraction limit by using a double-helix point spread function,” Proc. Natl. Acad. Sci. U.S.A. 106(9), 2995–2999 (2009).
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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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M. K. Lee, P. Rai, J. Williams, R. J. Twieg, and W. E. Moerner, “Small-molecule labeling of live cell surfaces for three-dimensional super-resolution microscopy,” J. Am. Chem. Soc. 136(40), 14003–14006 (2014).
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S. R. P. Pavani, M. A. Thompson, J. S. Biteen, S. J. Lord, N. Liu, R. J. Twieg, R. Piestun, and W. E. Moerner, “Three-dimensional, single-molecule fluorescence imaging beyond the diffraction limit by using a double-helix point spread function,” Proc. Natl. Acad. Sci. U.S.A. 106(9), 2995–2999 (2009).
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Figures (8)

Fig. 1
Fig. 1

Dual-color Tetrapod imaging. (a) Optical setup (main components). A split-color 4f system is added to a standard inverted microscope, starting from the image plane (IP), yielding a dual-color image illuminating two corners of the camera (CAM). L = lens, DM = dichroic mirror, M = mirror, PM = phase mask. (b) A 6 µm Tetrapod phase pattern, implemented by photo-lithographically etched dielectric phase-masks placed in the Fourier plane, one for each color channel. (c) Experimental calibration measurements of a fluorescent microsphere imaged over a 6 µm range in the green channel (top) and red channel (bottom). Lateral orientation angle of the PSF is calibrated in the fitting procedure. Scale bar = 1 µm.

Fig. 2
Fig. 2

Yeast labeling scheme. Engineered yeast strain (KWY5028) contains two fluorescently labeled loci on opposite sides of the GAL locus. Dual color labeling is achieved using the LacO/LacI-GFP system (green) and TetO/TetR-mCherry system (red).

Fig. 3
Fig. 3

Fitting with strong background: example. (a) Raw data: yeast measurement with strong cellular background (red channel). (b) Model used for fitting, consisting of the Tetrapod PSF (c) combined with cellular background modeled as a 2D Gaussian (d). Scale bar = 1 µm. Color scales are normalized per figure.

Fig. 4
Fig. 4

3D trajectories and co-localization trace: example. 3D trajectories of red (a) and green (b) loci, taken from a KWY5028 cell in galactose, over five minutes, in a time-lapse video with 6 second intervals. Time is encoded in color-value (dark = start, light = end). (c) The obtained 3D distance trace.

Fig. 5
Fig. 5

3D co-localization results. (a) Statistical comparison between galactose and dextrose conditions, in KWY5028, where the two labeled loci are on opposite sides of the GAL locus. 3D distance distribution using all data points (left) and temporal standard deviation per cell, derived from co-localization traces such as in Fig. 4(c). (b) Control: 3D distance distribution (left) and temporal standard deviation per cell (right) for control strain KWY4067, where the two labeled loci are on same side of GAL locus.

Fig. 6
Fig. 6

Localization precision estimates per channel. Two example cells are shown - one in each color channel. Localization traces are shown in the top panel, along with low-order polynomial fits in red. The bottom panel shows the localization histograms after subtracting the polynomial fits.

Fig. 7
Fig. 7

Experimental determination of registration error. A fluorescent bead embedded in agarose (~2 µm deep) is scanned axially over a 3.75 µm range, imaged in both color channels and co-localized using our depth dependent affine registration procedure. The resulting localization errors in x,y,z and a 3D error histogram are shown.

Fig. 8
Fig. 8

Numerical simulation of inter-locus distance precision.

Tables (1)

Tables Icon

Table 1 Yeast strains used in this study. Both KWY strains listed are derived from S288c and are of the BY varieties BY4742 (MATα his3Δ1 leu2Δ0 lys2Δ0 ura3Δ0) and BY4741 (MATa his3Δ1 leu2Δ0 met15Δ0 ura3Δ0), respectively [34].

Equations (9)

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

P(x',y')= circ(ρ) { 1 [(NA/ n 1 )ρ] 2 } 1/4 exp[ iM( ρ,φ ) ],
ψ depth ( ρ,φ| z 0 , f n )=k n 1 f n 1 ( NA n 1  ρ ) 2 +k n 2 z 0 1 ( NA n 2 ρ ) 2 .
P aberr ( ρ,φ )=P( ρ,φ )exp{ i[ ψ depth ( ρ,φ|z, f n )+ ψ aberr ( ρ,φ ) ] }.
NLL= m ( μ m +b ) I m log( μ m +b ),
μ ^ | F{ P aberr ( ρ,φ; z 0 , f n , n 1 , n 2 )exp[ ik NA M 2 N A 2   ρ( x 0 cosφ+ y 0 sinφ ) ] } | 2 ,
R= ( x green x red ) 2 + ( y green y red ) 2 + ( z green z red ) 2 ,
x= x green x red = x ^ green x ^ red +Δ x green +Δ x red +Δ x reg y= y green y red = y ^ green y ^ red +Δ y green +Δ y red +Δ y reg z= z green z red = z ^ green z ^ red +Δ z green +Δ z red +Δ z reg
Δ( R 2 )= (Δ ( x 2 ) 2 +Δ ( y 2 ) 2 +Δ ( z 2 ) 2 ) =2 (xΔx) 2 + (yΔy) 2 + (zΔz) 2 ) Δ( R 2 )=Δ(RR)2RΔR
ΔR1/R (xΔx) 2 + (yΔy) 2 + (zΔy) 2 .