Abstract

Thanks to its non-invasive nature, X-ray phase contrast tomography is a very versatile imaging tool for biomedical studies. In contrast, histology is a well-established method, though having its limitations: it requires extensive sample preparation and it is quite time consuming. Therefore, the development of nano-imaging techniques for studying anatomic details at the cellular level is gaining more and more importance. In this article, full field transmission X-ray nanotomography is used in combination with Zernike phase contrast to image millimeter sized unstained tissue samples at high spatial resolution. The regions of interest (ROI) scans of different tissues were obtained from mouse kidney, spleen and mammalian carcinoma. Thanks to the relatively large field of view and effective pixel sizes down to 36 nm, this 3D approach enabled the visualization of the specific morphology of each tissue type without staining or complex sample preparation. As a proof of concept technique, we show that the high-quality images even permitted the 3D segmentation of multiple structures down to a sub-cellular level. Using stitching techniques, volumes larger than the field of view are accessible. This method can lead to a deeper understanding of the organs’ nano-anatomy, filling the resolution gap between histology and transmission electron microscopy.

Published by The Optical Society under the terms of the Creative Commons Attribution 4.0 License. Further distribution of this work must maintain attribution to the author(s) and the published article's title, journal citation, and DOI.

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2020 (1)

M. Töpperwien, F. van der Meer, C. Stadelmann, and T. Salditt, “Correlative x-ray phase-contrast tomography and histology of human brain tissue affected by Alzheimer’s disease,” NeuroImage 210, 116523 (2020).
[Crossref]

2019 (7)

L. Massimi, I. Bukreeva, G. Santamaria, M. Fratini, A. Corbelli, F. Brun, S. Fumagalli, L. Maugeri, A. Pacureanu, P. Cloetens, N. Pieroni, F. Fiordaliso, G. Forloni, A. Uccelli, N. Kerlero de Rosbo, C. Balducci, and A. Cedola, “Exploring Alzheimer’s disease mouse brain through X-ray phase contrast tomography: From the cell to the organ,” NeuroImage 184, 490–495 (2019).
[Crossref]

E. Larsson, D. Gürsoy, F. De Carlo, E. Lilleodden, M. Storm, F. Wilde, K. Hu, M. Müller, and I. Greving, “Nanoporous gold: a hierarchical and multiscale 3D test pattern for characterizing X-ray nano-tomography systems,” J. Synchrotron Radiat. 26(1), 194–204 (2019).
[Crossref]

I. Costantini, R. Cicchi, L. Silvestri, F. Vanzi, and F. S. Pavone, “In-vivo and ex-vivo optical clearing methods for biological tissues: review,” Biomed. Opt. Express 10(10), 5251–5267 (2019).
[Crossref]

X. Zhu, L. Huang, Y. Zheng, Y. Song, Q. Xu, J. Wang, K. Si, S. Duan, and W. Gong, “Ultrafast optical clearing method for three-dimensional imaging with cellular resolution,” Proc. Natl. Acad. Sci. 116(23), 11480–11489 (2019).
[Crossref]

A. Kazarine, K. Kolosova, A. A. Gopal, H. Wang, R. Tahara, A. Rammal, K. Kost, L. Mongeau, N. Y. K. Li-Jessen, and P. W. Wiseman, “Multimodal virtual histology of rabbit vocal folds by nonlinear microscopy and nano computed tomography,” Biomed. Opt. Express 10(3), 1151–1164 (2019).
[Crossref]

J. F. Dekkers, M. Alieva, L. M. Wellens, H. C. R. Ariese, P. R. Jamieson, A. M. Vonk, G. D. Amatngalim, H. Hu, K. C. Oost, H. J. G. Snippert, J. M. Beekman, E. J. Wehrens, J. E. Visvader, H. Clevers, and A. C. Rios, “High-resolution 3d imaging of fixed and cleared organoids,” Nat. Protoc. 14(6), 1756–1771 (2019).
[Crossref]

A. Miettinen, I. V. Oikonomidis, A. Bonnin, and M. Stampanoni, “Nrstitcher: non-rigid stitching of terapixel-scale volumetric images,” Bioinformatics 35(24), 5290–5297 (2019).
[Crossref]

2018 (3)

M. Töpperwien, F. van der Meer, C. Stadelmann, and T. Salditt, “Three-dimensional virtual histology of human cerebellum by X-ray phase-contrast tomography,” Proc. Natl. Acad. Sci. U. S. A. 115(27), 6940–6945 (2018).
[Crossref]

A. Khimchenko, C. Bikis, A. Pacureanu, S. E. Hieber, P. Thalmann, H. Deyhle, G. Schweighauser, J. Hench, S. Frank, M. Müller-Gerbl, G. Schulz, P. Cloetens, and B. Müller, “Hard X-Ray Nanoholotomography: Large-Scale, Label-Free, 3D Neuroimaging beyond Optical Limit,” Adv. Sci. 5(6), 1700694 (2018).
[Crossref]

M. Busse, M. Müller, M. A. Kimm, S. Ferstl, S. Allner, K. Achterhold, J. Herzen, and F. Pfeiffer, “Three-dimensional virtual histology enabled through cytoplasm-specific X-ray stain for microscopic and nanoscopic computed tomography,” Proc. Natl. Acad. Sci. U. S. A. 115(10), 2293–2298 (2018).
[Crossref]

2017 (1)

A. Cedola, A. Bravin, I. Bukreeva, M. Fratini, A. Pacureanu, A. Mittone, L. Massimi, P. Cloetens, P. Coan, G. Campi, R. Spanò, F. Brun, V. Grigoryev, V. Petrosino, C. Venturi, M. Mastrogiacomo, N. Kerlero De Rosbo, and A. Uccelli, “X-Ray Phase Contrast Tomography Reveals Early Vascular Alterations and Neuronal Loss in a Multiple Sclerosis Model,” Sci. Rep. 7(1), 5890 (2017).
[Crossref]

2016 (1)

A. Karageorgis, S. Dufort, L. Sancey, M. Henry, S. Hirsjärvi, C. Passirani, J.-P. Benoit, J. Gravier, I. Texier, O. Montigon, M. Benmerad, V. Siroux, E. L. Barbier, and J.-L. Coll, “An MRI-based classification scheme to predict passive access of 5 to 50-nm large nanoparticles to tumors,” Sci. Rep. 6(1), 21417 (2016).
[Crossref]

2015 (3)

J. A. McCormick and D. H. Ellison Division, “The Distal Convoluted Tubule,” Compr Physiol. 5, 45–98 (2015).

M. Sivaguru, G. Fried, B. S. Sivaguru, V. A. Sivaguru, X. Lu, K. H. Choi, M. T. A. Saif, B. Lin, and S. Sadayappan, “Cardiac muscle organization revealed in 3-d by imaging whole-mount mouse hearts using twophoton fluorescence and confocal microscopy,” BioTechniques 59(5), 295–308 (2015).
[Crossref]

I. Vartiainen, C. Holzner, I. Mohacsi, P. Karvinen, A. Diaz, and C. David, “Artifact characterization and reduction in scanning X-ray Zernike phase contrast microscopy,” Opt. Express 23(10), 13278–13294 (2015).
[Crossref]

2014 (3)

I. Greving, F. Wilde, M. Ogurreck, J. Herzen, J. U. Hammel, A. Hipp, F. Friedrich, L. Lottermoser, T. Dose, H. Burmester, M. Müller, and F. Beckmann, “P05 imaging beamline at PETRA III: first results,” Dev. X-Ray Tomogr. IX 9212, 92120O (2014).
[Crossref]

A. R. Subramanya and D. H. Ellison, “Distal convoluted tubule,” Clin. J. Am. Soc. Nephrol. 9(12), 2147–2163 (2014).
[Crossref]

D. Gürsoy, F. De Carlo, X. Xiao, and C. Jacobsen, “TomoPy: A framework for the analysis of synchrotron tomographic data,” J. Synchrotron Radiat. 21(5), 1188–1193 (2014).
[Crossref]

2013 (4)

R. P. J. Nieuwenhuizen, K. A. Lidke, M. Bates, D. L. Puig, D. Grünwald, S. Stallinga, and B. Rieger, “Measuring image resolution in optical nanoscopy,” Nat. Methods 10(6), 557–562 (2013).
[Crossref]

J. L. Zhuo and X. C. Li, “Proximal Nephron,” Compr. Physiol. 3(3), 1079–1123 (2013).
[Crossref]

M. Ogurreck, F. Wilde, J. Herzen, F. Beckmann, V. Nazmov, J. Mohr, A. Haibel, M. Müller, and A. Schreyer, “The nanotomography endstation at the PETRA III imaging beamline,” J. Phys.: Conf. Ser. 425(18), 182002 (2013).
[Crossref]

A. Bravin, P. Coan, and P. Suortti, “X-ray phase-contrast imaging: From pre-clinical applications towards clinics,” Phys. Med. Biol. 58(1), R1–R35 (2013).
[Crossref]

2012 (5)

C. C. Chien, C. C. Cheng, H. H. Chen, Y. Hwu, Y. S. Chu, C. Petibois, A. Chen, Y. T. Ching, and G. Margaritondo, “X-ray microscopy and tomography detect the accumulation of bare and PEG-coated gold nanoparticles in normal and tumor mouse tissues,” Anal. Bioanal. Chem. 404(5), 1287–1296 (2012).
[Crossref]

R. Mokso, L. Quaroni, F. Marone, S. Irvine, J. Vila-Comamala, A. Blanke, and M. Stampanoni, “X-ray mosaic nanotomography of large microorganisms,” J. Struct. Biol. 177(2), 233–238 (2012).
[Crossref]

L. Silvestri, A. Bria, L. Sacconi, G. Iannello, and F. S. Pavone, “Confocal light sheet microscopy: micron-scale neuroanatomy of the entire mouse brain,” Opt. Express 20(18), 20582–20598 (2012).
[Crossref]

J. J. Lombardo, R. A. Ristau, W. M. Harris, and W. K. Chiu, “Focused ion beam preparation of samples for X-ray nanotomography,” J. Synchrotron Radiat. 19(5), 789–796 (2012).
[Crossref]

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J. Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: An open-source platform for biological-image analysis,” Nat. Methods 9(7), 676–682 (2012).
[Crossref]

2011 (1)

J. C. Andrews, F. Meirer, Y. Liu, Z. Mester, and P. Pianetta, “Transmission x-ray microscopy for full-field nano imaging of biomaterials,” Microsc. Res. Tech. 74(7), 671–681 (2011).
[Crossref]

2010 (3)

M. Stampanoni, R. Mokso, F. Marone, J. Vila-Comamala, S. Gorelick, P. Trtik, K. Jefimovs, and C. David, “Phase-contrast tomography at the nanoscale using hard x rays,” Phys. Rev. B 81(14), 140105 (2010).
[Crossref]

C. Larabell and K. A. Nugent, “Imaging Cellular Architecture with X-rays,” Curr. Opin. Struct. Biol. 20(5), 623–631 (2010).
[Crossref]

C. Holzner, M. Feser, S. Vogt, B. Hornberger, S. B. Baines, and C. Jacobsen, “Zernike phase contrast in scanning microscopy with X-rays,” Nat. Phys. 6(11), 883–887 (2010).
[Crossref]

2009 (2)

B. Münch, P. Trtik, F. Marone, and M. Stampanoni, “Stripe and ring artifact removal with combined wavelet - Fourier filtering,” Opt. Express 17(10), 8567 (2009).
[Crossref]

G. McDermott, M. A. Le Gros, C. G. Knoechel, M. Uchida, and C. A. Larabell, “Soft X-ray Tomography and Cryogenic Light Microscopy: The Cool Combination in Cellular Imaging,” Trends Cell Biol. 19(11), 587–595 (2009).
[Crossref]

2005 (3)

M. A. Le Gros, G. McDermott, and C. A. Larabell, “X-ray tomography of whole cells,” Curr. Opin. Struct. Biol. 15(5), 593–600 (2005).
[Crossref]

T. Weitkamp, A. Diaz, C. David, F. Pfeiffer, M. Stampanoni, P. Cloetens, and E. Ziegler, “X-ray phase imaging with a grating interferometer,” Opt. Express 13(16), 6296 (2005).
[Crossref]

M. van Heel and M. Schatz, “Fourier shell correlation threshold criteria,” J. Struct. Biol. 151(3), 250–262 (2005).
[Crossref]

2004 (1)

P. Thurner, F. Beckmann, and B. Müller, “An optimization procedure for spatial and density resolution in hard X-ray micro-computed tomography,” Nucl. Instrum. Methods Phys. Res., Sect. B 225(4), 599–603 (2004).
[Crossref]

2003 (1)

U. Neuhäusler, G. Schneider, W. Ludwig, M. A. Meyer, E. Zschech, and D. Hambach, “X-ray microscopy in Zernike phase contrast mode at 4 keV photon energy with 60 nm resolution,” J. Phys. D: Appl. Phys. 36(10A), A79–A82 (2003).
[Crossref]

2002 (2)

M. Awaji, Y. Suzuki, A. Takeuchi, H. Takano, N. Kamijo, S. Tamura, and M. Yasumoto, “Zernike-type X-ray imaging microscopy at 25 keV with Fresnel zone plate optics,” J. Synchrotron Rad. 9(3), 125–127 (2002).
[Crossref]

D. Paganin, S. C. Mayo, T. E. Gureyev, P. R. Miller, and S. W. Wilkins, “Simultaneous phase and amplitude extraction from a single defocused image of a homogeneous object,” J. Microsc. 206(1), 33–40 (2002).
[Crossref]

1999 (2)

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A. Pacureanu, J. Maniates-Selvin, A. T. Kuan, L. A. Thomas, C.-L. Chen, P. Cloetens, and W.-C. A. Lee, “Dense neuronal reconstruction through x-ray holographic nano-tomography,” bioRxiv (2019).

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D. Paganin, S. C. Mayo, T. E. Gureyev, P. R. Miller, and S. W. Wilkins, “Simultaneous phase and amplitude extraction from a single defocused image of a homogeneous object,” J. Microsc. 206(1), 33–40 (2002).
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A. Karageorgis, S. Dufort, L. Sancey, M. Henry, S. Hirsjärvi, C. Passirani, J.-P. Benoit, J. Gravier, I. Texier, O. Montigon, M. Benmerad, V. Siroux, E. L. Barbier, and J.-L. Coll, “An MRI-based classification scheme to predict passive access of 5 to 50-nm large nanoparticles to tumors,” Sci. Rep. 6(1), 21417 (2016).
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Petibois, C.

C. C. Chien, C. C. Cheng, H. H. Chen, Y. Hwu, Y. S. Chu, C. Petibois, A. Chen, Y. T. Ching, and G. Margaritondo, “X-ray microscopy and tomography detect the accumulation of bare and PEG-coated gold nanoparticles in normal and tumor mouse tissues,” Anal. Bioanal. Chem. 404(5), 1287–1296 (2012).
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A. Cedola, A. Bravin, I. Bukreeva, M. Fratini, A. Pacureanu, A. Mittone, L. Massimi, P. Cloetens, P. Coan, G. Campi, R. Spanò, F. Brun, V. Grigoryev, V. Petrosino, C. Venturi, M. Mastrogiacomo, N. Kerlero De Rosbo, and A. Uccelli, “X-Ray Phase Contrast Tomography Reveals Early Vascular Alterations and Neuronal Loss in a Multiple Sclerosis Model,” Sci. Rep. 7(1), 5890 (2017).
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M. Busse, M. Müller, M. A. Kimm, S. Ferstl, S. Allner, K. Achterhold, J. Herzen, and F. Pfeiffer, “Three-dimensional virtual histology enabled through cytoplasm-specific X-ray stain for microscopic and nanoscopic computed tomography,” Proc. Natl. Acad. Sci. U. S. A. 115(10), 2293–2298 (2018).
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R. P. J. Nieuwenhuizen, K. A. Lidke, M. Bates, D. L. Puig, D. Grünwald, S. Stallinga, and B. Rieger, “Measuring image resolution in optical nanoscopy,” Nat. Methods 10(6), 557–562 (2013).
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R. Mokso, L. Quaroni, F. Marone, S. Irvine, J. Vila-Comamala, A. Blanke, and M. Stampanoni, “X-ray mosaic nanotomography of large microorganisms,” J. Struct. Biol. 177(2), 233–238 (2012).
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Rieger, B.

R. P. J. Nieuwenhuizen, K. A. Lidke, M. Bates, D. L. Puig, D. Grünwald, S. Stallinga, and B. Rieger, “Measuring image resolution in optical nanoscopy,” Nat. Methods 10(6), 557–562 (2013).
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J. F. Dekkers, M. Alieva, L. M. Wellens, H. C. R. Ariese, P. R. Jamieson, A. M. Vonk, G. D. Amatngalim, H. Hu, K. C. Oost, H. J. G. Snippert, J. M. Beekman, E. J. Wehrens, J. E. Visvader, H. Clevers, and A. C. Rios, “High-resolution 3d imaging of fixed and cleared organoids,” Nat. Protoc. 14(6), 1756–1771 (2019).
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J. J. Lombardo, R. A. Ristau, W. M. Harris, and W. K. Chiu, “Focused ion beam preparation of samples for X-ray nanotomography,” J. Synchrotron Radiat. 19(5), 789–796 (2012).
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G. Schmahl, D. Rudolph, G. Schneider, P. Guttmann, and B. Niemann, “Phase contrast X-ray microscopy studies,” Optik 97, 181–182 (1994).

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J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J. Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: An open-source platform for biological-image analysis,” Nat. Methods 9(7), 676–682 (2012).
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J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J. Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: An open-source platform for biological-image analysis,” Nat. Methods 9(7), 676–682 (2012).
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Sadayappan, S.

M. Sivaguru, G. Fried, B. S. Sivaguru, V. A. Sivaguru, X. Lu, K. H. Choi, M. T. A. Saif, B. Lin, and S. Sadayappan, “Cardiac muscle organization revealed in 3-d by imaging whole-mount mouse hearts using twophoton fluorescence and confocal microscopy,” BioTechniques 59(5), 295–308 (2015).
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Saif, M. T. A.

M. Sivaguru, G. Fried, B. S. Sivaguru, V. A. Sivaguru, X. Lu, K. H. Choi, M. T. A. Saif, B. Lin, and S. Sadayappan, “Cardiac muscle organization revealed in 3-d by imaging whole-mount mouse hearts using twophoton fluorescence and confocal microscopy,” BioTechniques 59(5), 295–308 (2015).
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Supplementary Material (1)

NameDescription
» Visualization 1       Video showing the stitched slices through the volume

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Figures (6)

Fig. 1.
Fig. 1. Schematic drawing of the Zernike TXM installed at the P05 imaging beamline, at PETRA III (DESY, Germany). The components "OSA" and "FZP" are the short abbreviation for "order sorting apertures" and "Fresnel Zone Plate", respectively.
Fig. 2.
Fig. 2. (a) Virtual nanotomography slice of the mouse kidney. (b) Zoomed view over one tubule cells group. The tubular structure is indicated by the blue dashed line, the lumen by the green dashed line and the nuclei by the yellow one. The orange arrow points at the nucleolus inside the nucleus. The two red arrows indicate a structure similar to a glomerulus. (c) Virtual tomographic slice enhancing tubule cells of different shape. (d) Minimum intensity projection image showing a distal tubule (blue dashed lines) surrounded by three proximal tubules (purple arrows). (e) Histological slice showing the kidney cortex anatomy. (f) Magnified view of the region within the black rectangle in (e).
Fig. 3.
Fig. 3. (a) 3D volume rendering in grey-scale of a volume of interest derived from the kidney tomographic dataset. (b) 3D rendering with segmented tubule cells. (c) Rendering of the 3D segmented tubule cells and sub-structures: the tubule is displayed in blue, the lumen in green and the nuclei in yellow.
Fig. 4.
Fig. 4. (a) Reconstructed tomographic slice showing the cellular arrangement in the red pulp area of the spleen. (b) Reconstructed tomographic slice representing the cellular arrangement in the white pulp area of the spleen. (c) Histological image showing the cellular arrangement at the interface between red pulp (RP) and white pulp (WP). (d) Magnified imaged showing the cell nuclei belonging to the red pulp (RP) and to the white pulp (WP).
Fig. 5.
Fig. 5. (a) Minimum intensity projection image of 14 reconstructed nanotomography slices. The image shows the chaotic organization of tumor cells surrounding a typical healthy mouse cell, whose nucleus is pointed out by a yellow arrow. (b) Minimum intensity projection image of 14 nanotomography slices selected at another depth of the reconstructed dataset. (c) 3D rendering of a volume of interest with 51 µm in height. (d) Histological image of the same tumor tissue.
Fig. 6.
Fig. 6. Slice with enlarged FoV obtained by stitching four reconstructed nanotomographic slices.