Abstract

Characterising and understanding the mechanisms involved in cell death are especially important to combating threats to human health, particularly for the study of antimicrobial peptides and their effectiveness against pathogenic fungi. However, imaging these processes often relies on the use of synthetic molecules which bind to specific cellular targets to produce contrast. Here we study yeast cell death, induced by the anti-fungal peptide, NaD1. By treating yeast as a model organism we aim to understand anti-fungal cell death processes without relying on sample modification. Using a quantitative phase imaging technique, ptychography, we were able to produce label free images of yeast cells during death and use them to investigate the mode of action of NaD1. Using this technique we were able to identify a significant phase shift which provided a clear signature of yeast cell death. Additionally, ptychography identifies cell death much earlier than a comparative fluorescence study, providing new insights into the cellular changes that occur during cell death. The results indicate ptychography has great potential as a means of providing additional information about cellular processes which otherwise may be masked by indirect labelling approaches.

© 2019 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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2018 (4)

A. Le Gratiet, L. Pesce, M. Oneto, R. Marongiu, G. Zanini, P. Bianchini, and A. Diaspro, “Circular intensity differential scattering (CIDS) scanning microscopy to image chromatin-DNA nuclear organization,” OSA Continuum 1(3), 1068 (2018).
[Crossref]

M. Odstrčil, M. Holler, and M. Guizar-Sicairos, “Arbitrary-path fly-scan ptychography,” Opt. Express 26(10), 12585 (2018).
[Crossref]

J. Sun, C. Zuo, J. Zhang, Y. Fan, and Q. Chen, “High-speed Fourier ptychographic microscopy based on programmable annular illuminations,” Sci. Rep. 8(1), 7669 (2018).
[Crossref]

B. M. E. Hayes, M. R. Bleackley, M. A. Anderson, and N. L. V. D. Weerden, “The Plant Defensin NaD1 Enters the Cytoplasm of Candida albicans via Endocytosis,” J. Fungi 4(1), 20 (2018).
[Crossref]

2017 (1)

Y. Yao, S. P. Veetil, C. Liu, and J. Zhu, “Ptychographic phase microscope based on high-speed modulation on the illumination beam,” J. Biomed. Opt. 22(3), 036010 (2017).
[Crossref]

2016 (8)

C. Falcone and C. Mazzoni, “External and internal triggers of cell death in yeast,” Cell. Mol. Life Sci. 73(11-12), 2237–2250 (2016).
[Crossref]

N. Anthony, G. Cadenazzi, K. A. Nugent, and B. Abbey, “Optical ptychographic microscopy for quantitative anisotropic phase imaging,” Proc. SPIE 10013, 1001331 (2016).
[Crossref]

N. Anthony, G. Cadenazzi, H. Kirkwood, E. Huwald, K. A. Nugent, and B. Abbey, “A Direct Approach to In-Plane Stress Separation using Photoelastic Ptychography,” Sci. Rep. 6(1), 30541 (2016).
[Crossref]

R. Suman, G. Smith, K. E. A. Hazel, R. Kasprowicz, M. Coles, P. O’Toole, and S. Chawla, “Label-free imaging to study phenotypic behavioural traits of cells in complex co-cultures,” Sci. Rep. 6(1), 22032 (2016).
[Crossref]

L. M. Almassalha, G. M. Bauer, J. E. Chandler, S. Gladstein, L. Cherkezyan, Y. Stypula-Cyrus, S. Weinberg, D. Zhang, P. Thusgaard Ruhoff, H. K. Roy, H. Subramanian, N. S. Chandel, I. Szleifer, and V. Backman, “Label-free imaging of the native, living cellular nanoarchitecture using partial-wave spectroscopic microscopy,” Proc. Natl. Acad. Sci. 113(42), E6372–E6381 (2016).
[Crossref]

L. Ma, G. Rajshekhar, R. Wang, B. Bhaduri, S. Sridharan, M. Mir, A. Chakraborty, R. Iyer, S. Prasanth, L. Millet, M. U. Gillette, and G. K. Popescu, “Phase correlation imaging of unlabeled cell dynamics,” Sci. Rep. 6(1), 32702 (2016).
[Crossref]

R. Horstmeyer, J. Chung, X. Ou, G. Zheng, and C. Yang, “Diffraction tomography with Fourier ptychography,” Optica 3(8), 827 (2016).
[Crossref]

W. Yu, S. Wang, S. Veetil, S. Gao, C. Liu, and J. Zhu, “High-quality image reconstruction method for ptychography with partially coherent illumination,” Phys. Rev. B 93(24), 241105 (2016).
[Crossref]

2015 (1)

F. Lu, S. Basu, V. Igras, M. P. Hoang, M. Ji, D. Fu, G. R. Holtom, V. A. Neel, C. W. Freudiger, D. E. Fisher, and X. S. Xie, “Label-free DNA imaging in vivo with stimulated Raman scattering microscopy,” Proc. Natl. Acad. Sci. 112(37), 11624–11629 (2015).
[Crossref]

2014 (3)

2013 (7)

B. M. E. Hayes, M. R. Bleackley, J. L. Wiltshire, M. A. Anderson, A. Traven, and N. L. van der Weerden, “Identification and Mechanism of Action of the Plant Defensin NaD1 as a New Member of the Antifungal Drug Arsenal against Candida albicans,” Antimicrob. Agents Chemother. 57(8), 3667–3675 (2013).
[Crossref]

W. Chen, K. D. Long, M. Lu, V. Chaudhery, H. Yu, J. S. Choi, J. Polans, Y. Zhuo, B. A. Harley, and B. T. Cunningham, “Photonic crystal enhanced microscopy for imaging of live cell adhesion,” Analyst 138(20), 5886–5894 (2013).
[Crossref]

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

J. Marrison, L. Ráty, P. Marriott, and P. O’Toole, “Ptychography – a label free, high-contrast imaging technique for live cells using quantitative phase information,” Sci. Rep. 3(1), 2369 (2013).
[Crossref]

D. L. Coutu and T. Schroeder, “Probing cellular processes by long-term live imaging - historic problems and current solutions,” J. Cell Sci. 126(17), 3805–3815 (2013).
[Crossref]

M. W. M. Jones, G. A. van Riessen, B. Abbey, C. T. Putkunz, M. D. Junker, E. Balaur, D. J. Vine, I. McNulty, B. Chen, B. D. Arhatari, S. Frankland, K. A. Nugent, L. Tilley, and A. G. Peele, “Whole-cell phase contrast imaging at the nanoscale using Fresnel Coherent Diffractive Imaging Tomography,” Sci. Rep. 3(1), 2288 (2013).
[Crossref]

D. M. Wloch-Salamon and A. E. Bem, “Types of cell death and methods of their detection in yeast Saccharomyces cerevisiae,” J. Appl. Microbiol. 114(2), 287–298 (2013).
[Crossref]

2012 (1)

2011 (3)

2010 (3)

A. M. Maiden, J. M. Rodenburg, and M. J. Humphry, “Optical ptychography: a practical implementation with useful resolution,” Opt. Lett. 35(15), 2585–2587 (2010).
[Crossref]

K. Giewekemeyer, P. Thibault, S. Kalbfleisch, A. Beerlink, C. M. Kewish, M. Dierolf, F. Pfeiffer, and T. Salditt, “Quantitative biological imaging by ptychographic x-ray diffraction microscopy,” Proc. Natl. Acad. Sci. 107(2), 529–534 (2010).
[Crossref]

T. Eisenberg, D. Carmona-Gutierrez, S. Búttner, N. Tavernarakis, and F. Madeo, “Necrosis in yeast,” Apoptosis 15(3), 257–268 (2010).
[Crossref]

2009 (1)

P. Thibault, M. Dierolf, O. Bunk, A. Menzel, and F. Pfeiffer, “Probe retrieval in ptychographic coherent diffractive imaging,” Ultramicroscopy 109(4), 338–343 (2009).
[Crossref]

2008 (3)

N. L. van der Weerden, F. T. Lay, and M. A. Anderson, “The Plant Defensin, NaD1, Enters the Cytoplasm of Fusarium Oxysporum Hyphae,” J. Biol. Chem. 283(21), 14445–14452 (2008).
[Crossref]

B. Abbey, K. A. Nugent, G. J. Williams, J. N. Clark, A. G. Peele, M. A. Pfeifer, M. D. De Jonge, and I. McNulty, “Keyhole coherent diffractive imaging,” Nat. Phys. 4(5), 394–398 (2008).
[Crossref]

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. 105(37), 13730–13735 (2008).
[Crossref]

2007 (1)

J. M. Rodenburg, A. C. Hurst, A. G. Cullis, B. Dobson, F. Pfeiffer, O. Bunk, C. David, K. Jefimovs, and I. Johnson, “Hard-X-Ray Lensless Imaging of Extended Objects,” Phys. Rev. Lett. 98(3), 034801 (2007).
[Crossref]

1991 (1)

A. Diaspro, M. Bertolotto, L. Vergani, and C. Nicolini, “Polarized light scattering of nucleosomes and polynucleosomes-in situ and in vitro studies,” IEEE Trans. Biomed. Eng. 38(7), 670–678 (1991).
[Crossref]

Abbey, B.

N. Anthony, G. Cadenazzi, H. Kirkwood, E. Huwald, K. A. Nugent, and B. Abbey, “A Direct Approach to In-Plane Stress Separation using Photoelastic Ptychography,” Sci. Rep. 6(1), 30541 (2016).
[Crossref]

N. Anthony, G. Cadenazzi, K. A. Nugent, and B. Abbey, “Optical ptychographic microscopy for quantitative anisotropic phase imaging,” Proc. SPIE 10013, 1001331 (2016).
[Crossref]

N. W. Phillips, C. T. Putkunz, G. van Riessen, H. D. Coughlan, M. W. M. Jones, and B. Abbey, “Ptychographic Fresnel coherent diffraction tomography at the nanoscale,” Int. J. Mater. Res. 105(7), 655–663 (2014).
[Crossref]

M. W. M. Jones, G. A. van Riessen, B. Abbey, C. T. Putkunz, M. D. Junker, E. Balaur, D. J. Vine, I. McNulty, B. Chen, B. D. Arhatari, S. Frankland, K. A. Nugent, L. Tilley, and A. G. Peele, “Whole-cell phase contrast imaging at the nanoscale using Fresnel Coherent Diffractive Imaging Tomography,” Sci. Rep. 3(1), 2288 (2013).
[Crossref]

B. Abbey, K. A. Nugent, G. J. Williams, J. N. Clark, A. G. Peele, M. A. Pfeifer, M. D. De Jonge, and I. McNulty, “Keyhole coherent diffractive imaging,” Nat. Phys. 4(5), 394–398 (2008).
[Crossref]

Almassalha, L. M.

L. M. Almassalha, G. M. Bauer, J. E. Chandler, S. Gladstein, L. Cherkezyan, Y. Stypula-Cyrus, S. Weinberg, D. Zhang, P. Thusgaard Ruhoff, H. K. Roy, H. Subramanian, N. S. Chandel, I. Szleifer, and V. Backman, “Label-free imaging of the native, living cellular nanoarchitecture using partial-wave spectroscopic microscopy,” Proc. Natl. Acad. Sci. 113(42), E6372–E6381 (2016).
[Crossref]

Anderson, M. A.

B. M. E. Hayes, M. R. Bleackley, M. A. Anderson, and N. L. V. D. Weerden, “The Plant Defensin NaD1 Enters the Cytoplasm of Candida albicans via Endocytosis,” J. Fungi 4(1), 20 (2018).
[Crossref]

B. M. E. Hayes, M. R. Bleackley, J. L. Wiltshire, M. A. Anderson, A. Traven, and N. L. van der Weerden, “Identification and Mechanism of Action of the Plant Defensin NaD1 as a New Member of the Antifungal Drug Arsenal against Candida albicans,” Antimicrob. Agents Chemother. 57(8), 3667–3675 (2013).
[Crossref]

N. L. van der Weerden, F. T. Lay, and M. A. Anderson, “The Plant Defensin, NaD1, Enters the Cytoplasm of Fusarium Oxysporum Hyphae,” J. Biol. Chem. 283(21), 14445–14452 (2008).
[Crossref]

Anthony, N.

N. Anthony, G. Cadenazzi, K. A. Nugent, and B. Abbey, “Optical ptychographic microscopy for quantitative anisotropic phase imaging,” Proc. SPIE 10013, 1001331 (2016).
[Crossref]

N. Anthony, G. Cadenazzi, H. Kirkwood, E. Huwald, K. A. Nugent, and B. Abbey, “A Direct Approach to In-Plane Stress Separation using Photoelastic Ptychography,” Sci. Rep. 6(1), 30541 (2016).
[Crossref]

Arhatari, B. D.

M. W. M. Jones, G. A. van Riessen, B. Abbey, C. T. Putkunz, M. D. Junker, E. Balaur, D. J. Vine, I. McNulty, B. Chen, B. D. Arhatari, S. Frankland, K. A. Nugent, L. Tilley, and A. G. Peele, “Whole-cell phase contrast imaging at the nanoscale using Fresnel Coherent Diffractive Imaging Tomography,” Sci. Rep. 3(1), 2288 (2013).
[Crossref]

Backman, V.

L. M. Almassalha, G. M. Bauer, J. E. Chandler, S. Gladstein, L. Cherkezyan, Y. Stypula-Cyrus, S. Weinberg, D. Zhang, P. Thusgaard Ruhoff, H. K. Roy, H. Subramanian, N. S. Chandel, I. Szleifer, and V. Backman, “Label-free imaging of the native, living cellular nanoarchitecture using partial-wave spectroscopic microscopy,” Proc. Natl. Acad. Sci. 113(42), E6372–E6381 (2016).
[Crossref]

Balaur, E.

M. W. M. Jones, G. A. van Riessen, B. Abbey, C. T. Putkunz, M. D. Junker, E. Balaur, D. J. Vine, I. McNulty, B. Chen, B. D. Arhatari, S. Frankland, K. A. Nugent, L. Tilley, and A. G. Peele, “Whole-cell phase contrast imaging at the nanoscale using Fresnel Coherent Diffractive Imaging Tomography,” Sci. Rep. 3(1), 2288 (2013).
[Crossref]

Basu, S.

F. Lu, S. Basu, V. Igras, M. P. Hoang, M. Ji, D. Fu, G. R. Holtom, V. A. Neel, C. W. Freudiger, D. E. Fisher, and X. S. Xie, “Label-free DNA imaging in vivo with stimulated Raman scattering microscopy,” Proc. Natl. Acad. Sci. 112(37), 11624–11629 (2015).
[Crossref]

Bauer, G. M.

L. M. Almassalha, G. M. Bauer, J. E. Chandler, S. Gladstein, L. Cherkezyan, Y. Stypula-Cyrus, S. Weinberg, D. Zhang, P. Thusgaard Ruhoff, H. K. Roy, H. Subramanian, N. S. Chandel, I. Szleifer, and V. Backman, “Label-free imaging of the native, living cellular nanoarchitecture using partial-wave spectroscopic microscopy,” Proc. Natl. Acad. Sci. 113(42), E6372–E6381 (2016).
[Crossref]

Beckers, M.

M. Beckers, T. Senkbeil, T. Gorniak, M. Reese, K. Giewekemeyer, S. C. Gleber, T. Salditt, and A. Rosenhahn, “Chemical Contrast in Soft X-Ray Ptychography,” Phys. Rev. Lett. 107(20), 208101 (2011).
[Crossref]

Beerlink, A.

K. Giewekemeyer, P. Thibault, S. Kalbfleisch, A. Beerlink, C. M. Kewish, M. Dierolf, F. Pfeiffer, and T. Salditt, “Quantitative biological imaging by ptychographic x-ray diffraction microscopy,” Proc. Natl. Acad. Sci. 107(2), 529–534 (2010).
[Crossref]

Bem, A. E.

D. M. Wloch-Salamon and A. E. Bem, “Types of cell death and methods of their detection in yeast Saccharomyces cerevisiae,” J. Appl. Microbiol. 114(2), 287–298 (2013).
[Crossref]

Bertolotto, M.

A. Diaspro, M. Bertolotto, L. Vergani, and C. Nicolini, “Polarized light scattering of nucleosomes and polynucleosomes-in situ and in vitro studies,” IEEE Trans. Biomed. Eng. 38(7), 670–678 (1991).
[Crossref]

Bhaduri, B.

L. Ma, G. Rajshekhar, R. Wang, B. Bhaduri, S. Sridharan, M. Mir, A. Chakraborty, R. Iyer, S. Prasanth, L. Millet, M. U. Gillette, and G. K. Popescu, “Phase correlation imaging of unlabeled cell dynamics,” Sci. Rep. 6(1), 32702 (2016).
[Crossref]

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F. Lu, S. Basu, V. Igras, M. P. Hoang, M. Ji, D. Fu, G. R. Holtom, V. A. Neel, C. W. Freudiger, D. E. Fisher, and X. S. Xie, “Label-free DNA imaging in vivo with stimulated Raman scattering microscopy,” Proc. Natl. Acad. Sci. 112(37), 11624–11629 (2015).
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W. Chen, K. D. Long, M. Lu, V. Chaudhery, H. Yu, J. S. Choi, J. Polans, Y. Zhuo, B. A. Harley, and B. T. Cunningham, “Photonic crystal enhanced microscopy for imaging of live cell adhesion,” Analyst 138(20), 5886–5894 (2013).
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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. 105(37), 13730–13735 (2008).
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T. Eisenberg, D. Carmona-Gutierrez, S. Búttner, N. Tavernarakis, and F. Madeo, “Necrosis in yeast,” Apoptosis 15(3), 257–268 (2010).
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A. Diaspro, M. Bertolotto, L. Vergani, and C. Nicolini, “Polarized light scattering of nucleosomes and polynucleosomes-in situ and in vitro studies,” IEEE Trans. Biomed. Eng. 38(7), 670–678 (1991).
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Zhang, D.

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Zhang, F.

Zhang, J.

J. Sun, C. Zuo, J. Zhang, Y. Fan, and Q. Chen, “High-speed Fourier ptychographic microscopy based on programmable annular illuminations,” Sci. Rep. 8(1), 7669 (2018).
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Y. Yao, S. P. Veetil, C. Liu, and J. Zhu, “Ptychographic phase microscope based on high-speed modulation on the illumination beam,” J. Biomed. Opt. 22(3), 036010 (2017).
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J. Sun, C. Zuo, J. Zhang, Y. Fan, and Q. Chen, “High-speed Fourier ptychographic microscopy based on programmable annular illuminations,” Sci. Rep. 8(1), 7669 (2018).
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Analyst (1)

W. Chen, K. D. Long, M. Lu, V. Chaudhery, H. Yu, J. S. Choi, J. Polans, Y. Zhuo, B. A. Harley, and B. T. Cunningham, “Photonic crystal enhanced microscopy for imaging of live cell adhesion,” Analyst 138(20), 5886–5894 (2013).
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Antimicrob. Agents Chemother. (1)

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Int. J. Mater. Res. (1)

N. W. Phillips, C. T. Putkunz, G. van Riessen, H. D. Coughlan, M. W. M. Jones, and B. Abbey, “Ptychographic Fresnel coherent diffraction tomography at the nanoscale,” Int. J. Mater. Res. 105(7), 655–663 (2014).
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Opt. Express (4)

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OSA Continuum (1)

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Figures (5)

Fig. 1.
Fig. 1. Ptychographic Imaging Configuration. a) A 5 mm beam ($\lambda$ = 660 nm) is incident on an objective lens with the sample placed at a defocused distance of 150 ${\mu }$m and the detector placed 16 mm from the focus. Selected reconstructions of the b) amplitude and c) phase of the recovered probe.
Fig. 2.
Fig. 2. Comparison between the characteristics of alive (a-c) and dead (d-f) cells. Reconstructed amplitude (a,d) and phase (b, e) using ptychography, and optical fluorescence measurements (green) overlaid on bright-field (greyscale) images (c, f), of S. cerevisiae yeast cells. g) Boxplot of the average phase for both the alive and dead cell samples.
Fig. 3.
Fig. 3. Confocal fluorescence measurements showing the uptake of SYTOX green by S. cerevisiae cells in the presence of NaD1 over time. a) The distribution of the SYTOX dye, used as an indicator of membrane permeabilisation, is shown for a series of time points for a large number of cells. Shown are (top) Differential interference contrast microscopy (DIC), (middle) confocal microscopy, and (bottom) confocal overlaid on DIC. Inset: An example enlargement of two individual cells highlighting the SYTOX fluorescence distribution over time. Scale bar is 5 $\mu$m.
Fig. 4.
Fig. 4. Ptychographically reconstructed phase distribution of S. cerevisiae yeast cells over time. Reconstructed phase at a) t=3 mins, b) t=20 mins, and c) t=54 mins. d) A plot of the average phase for each of the four cells shown in a-c. Note that the colour of the lines is matched to the corresponding box around each cell.
Fig. 5.
Fig. 5. Phase distribution of an individual S. cerevisiae cell from Fig. 3(a). The evolution of the phase distribution is shown for the same cell at 6 different time points a) t=3 mins, b) t=10 mins, c) t=20 mins, d) t=30 mins, e) t=40 mins, and f) t=50 mins. The phase distribution along slices taken through the g) horizontal and h) vertical centre of the cell. The approximate point of cell death is indicated with an arrow in g).