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Unclearing Microscopy

Ons M’Saad, Michael Shribak, Joerg Bewersdorf

Preprint posted on 2 December 2022 https://www.biorxiv.org/content/10.1101/2022.11.29.518361v1

Unclearing microscopy: seeing human cells directly by eye

Selected by Robert Mahen

Background

With the invention of the microscope in the 17th century, a previously unimagined microscopic world came into view. Robert Hooke first used the term “cells” to describe what he saw in cork when using magnifying lenses to see beyond the resolution of the human eye [1].

In a recent preprint, M’Saad et al. have developed a method to visualise single human cells directly, without a microscope. This technique, which they call Unclearing Microscopy, also allows super resolution imaging without fluorescence or advanced microscopy.

 

Seeing human cells directly by eye

Most human cells are too small to be visible to the naked eye, generally being around 40 µm in length. Expansion microscopy physically expands cells up to 20-fold in size with swellable hydrogels [2,3]. This 20-fold expansion is sufficient to make human cells large enough to be visible by eye (~0.8 mm). In this preprint, M’Saad et al. developed techniques to impart contrast and colour to expanded cells, such that they are visible either with the unaided eye or with transmitted light imaging, in a technique they call Unclearing Microscopy.

 

unclearing microscopy

A schematic of the concept of Unclearing microscopy, taken directly from Fig. 1b of M’Saad et al. 2022 under a CC-BY-NC-ND 4.0 International license.

 

In previous work, M’Saad and Bewersdorf developed pan-expansion microscopy, which uses bulk labelling of the proteome to visualise cellular architecture, resulting in images similar to electron microscopy [4]. Here, they first non-selectively labelled proteins with NHS-ester ligands conjugated to biotin, and then incubated with streptavidin conjugated to horseradish peroxidase before adding either the chromogenic substrates 3,3’-diaminobenzidine (DAB) or silver. This workflow deposits contrast and colour throughout expanded cells using chemistries which have long been used in other techniques, such as immunohistochemistry, electron microscopy, and western blotting. In the case of DAB, a brown coloured precipitate forms at sites where peroxidase is present [5]. This resulted in expanded HeLa or mouse tissue cells with sufficient contrast to be seen with the naked eye. It is likely that cells have never been seen directly like this, allowing one to see features such as nuclei without a microscope.

 

Fig 1c-f taken from M’Saad et al. 2022 under a CC-BY-NC-ND 4.0 International license. Metallic silver (c) and DAB (d) uncleared HeLa cells on a glass bottom dish, imaged with a cell phone camera. e, f, Magnified views of the areas outlined by the black and brown boxes in c and d, respectively.

 

Super resolution microscopy without fluorescence

Super resolution microscopy usually relies both on advanced instrumentation and fluorescent labelling techniques. Imaging the uncleared samples just with conventional phase contrast microscopy allowed cellular organelles such as mitochondria to be visible, however. Distinct mitochondrial cristae could be imaged, despite only being ~70 nm apart, suggesting resolution beyond the diffraction limit, achieved without fluorescence and on a standard transmitted light microscope.

 

Histology at the nanoscale

In a second unclearing method, contrast in the expanded cells was amplified with a photopolymerization-based signal amplification method using eosin staining. This again resulted in cells visible by eye, but also mechanically more solid than standard expansion microscopy hydrogels, allowing them to be excised with tweezers. To improve resolution over standard differential interference contrast imaging, this photopolymerization-based unclearing method was combined with orientation-independent differential interference contrast imaging (OI-DIC). OI-DIC is a quantitative phase contrast transmitted light imaging modality with 3D optical sectioning. OI-DIC imaging of mouse synapses in ~1 mm thick tissue sections revealed similar detail to transmission electron microscopy or pan-expansion microscopy, on the tens of nanometers level.

 

Panels n-q of Figure 3 M’Saad et al. 2022. n, Schematic of a synapse highlighting synaptic densities. o, PBA uncleared putative synapse (inverted color table). p, fluorescence pan-ExM-t image of a putative synapse. q, Transmission Electron Microscopy (TEM) image of a PTA-stained putative synapse prepared as described in [6]. This figure and legend are taken directly from M’Saad et al 2022 under a CC-BY-NC-ND 4.0 International license.

 

Implications

M’Saad et al. point out various interesting implications of their work. Firstly, super resolution imaging is possible without using either fluorescence or advanced instrumentation. This will bypass some well-known disadvantages of fluorescence such as bleaching and make large field of view ultrastructure imaging both faster and potentially cheaper. In clinical settings, they suggest it could replace standard H&E staining, with increased resolution and good long-term storage. Secondly, single human cells can be visualised directly by eye without a microscope. This will be useful in research settings where microscopes are limited, or in other areas such as science outreach. Although current expansion microscopy protocols cannot expand samples arbitrarily to any size, it is possible that they will allow expansion of cells beyond ~ 1 mm in the future. Since “seeing is believing”, and we can now more directly see cells, it will be interesting to see where these developments lead, both for fundamental biology and in clinical settings.

 

References

  1. Robert Hooke. Micrographia, or some physiological descriptions of minute bodies made by magnifying glasses, with observations and inquiries thereupon. By R. Hooke. London: Printed by Jo. Martyn, and Ja. Allestry, printers to the Royal Society.; 1665.
  2. Chen F, Tillberg PW, Boyden ES. Optical imaging. Expansion microscopy. Science. 2015;347: 543–548. doi:10.1126/science.1260088
  3. Tillberg PW, Chen F, Piatkevich KD, Zhao Y, Yu C-CJ, English BP, et al. Protein-retention expansion microscopy of cells and tissues labeled using standard fluorescent proteins and antibodies. Nat Biotechnol. 2016;34: 987–992. doi:10.1038/nbt.3625
  4. M’Saad O, Bewersdorf J. Light microscopy of proteins in their ultrastructural context. Nat Commun. 2020;11: 3850. doi:10.1038/s41467-020-17523-8
  5. Graham RC, Karnovsky MJ. The early stages of absorption of injected horseradish peroxidase in the proximal tubules of mouse kidney: ultrastructural cytochemistry by a new technique. J Histochem Cytochem Off J Histochem Soc. 1966;14: 291–302. doi:10.1177/14.4.291
  6. M’Saad O, Kasula R, Kondratiuk I, Kidd P, Falahati H, Gentile JE, et al. All-optical visualization of specific molecules in the ultrastructural context of brain tissue. bioRxiv; 2022. p. 2022.04.04.486901. doi:10.1101/2022.04.04.486901

Tags: electron microscopy, expansion microscopy, hela, hydrogel, super-resolution microscopy, synapse, unclearing microscopy

Posted on: 2 March 2023 , updated on: 3 March 2023

doi: https://doi.org/10.1242/prelights.33947

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