Unclearing Microscopy
Preprint posted on 2 December 2022 https://www.biorxiv.org/content/10.1101/2022.11.29.518361v1
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.
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
- 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.
- Chen F, Tillberg PW, Boyden ES. Optical imaging. Expansion microscopy. Science. 2015;347: 543–548. doi:10.1126/science.1260088
- 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
- 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
- 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
- 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
Posted on: 2 March 2023 , updated on: 3 March 2023
doi: https://doi.org/10.1242/prelights.33947
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| List by | Nadja Hümpfer et al. |
EMBL Synthetic Morphogenesis: From Gene Circuits to Tissue Architecture (2021)
A list of preprints mentioned at the #EESmorphoG virtual meeting in 2021.
| List by | Alex Eve |
FENS 2020
A collection of preprints presented during the virtual meeting of the Federation of European Neuroscience Societies (FENS) in 2020
| List by | Ana Dorrego-Rivas |
ECFG15 – Fungal biology
Preprints presented at 15th European Conference on Fungal Genetics 17-20 February 2020 Rome
| List by | Hiral Shah |
ASCB EMBO Annual Meeting 2019
A collection of preprints presented at the 2019 ASCB EMBO Meeting in Washington, DC (December 7-11)
| List by | Madhuja Samaddar et al. |
Lung Disease and Regeneration
This preprint list compiles highlights from the field of lung biology.
| List by | Rob Hynds |
MitoList
This list of preprints is focused on work expanding our knowledge on mitochondria in any organism, tissue or cell type, from the normal biology to the pathology.
| List by | Sandra Franco Iborra |
Also in the neuroscience category:
‘In preprints’ from Development 2022-2023
A list of the preprints featured in Development's 'In preprints' articles between 2022-2023
| List by | Alex Eve, Katherine Brown |
CSHL 87th Symposium: Stem Cells
Preprints mentioned by speakers at the #CSHLsymp23
| List by | Alex Eve |
Journal of Cell Science meeting ‘Imaging Cell Dynamics’
This preList highlights the preprints discussed at the JCS meeting 'Imaging Cell Dynamics'. The meeting was held from 14 - 17 May 2023 in Lisbon, Portugal and was organised by Erika Holzbaur, Jennifer Lippincott-Schwartz, Rob Parton and Michael Way.
| List by | Helen Zenner |
FENS 2020
A collection of preprints presented during the virtual meeting of the Federation of European Neuroscience Societies (FENS) in 2020
| List by | Ana Dorrego-Rivas |
ASCB EMBO Annual Meeting 2019
A collection of preprints presented at the 2019 ASCB EMBO Meeting in Washington, DC (December 7-11)
| List by | Madhuja Samaddar et al. |
SDB 78th Annual Meeting 2019
A curation of the preprints presented at the SDB meeting in Boston, July 26-30 2019. The preList will be updated throughout the duration of the meeting.
| List by | Alex Eve |
Autophagy
Preprints on autophagy and lysosomal degradation and its role in neurodegeneration and disease. Includes molecular mechanisms, upstream signalling and regulation as well as studies on pharmaceutical interventions to upregulate the process.
| List by | Sandra Malmgren Hill |
Young Embryologist Network Conference 2019
Preprints presented at the Young Embryologist Network 2019 conference, 13 May, The Francis Crick Institute, London
| List by | Alex Eve |
Also in the physiology category:
Fibroblasts
The advances in fibroblast biology preList explores the recent discoveries and preprints of the fibroblast world. Get ready to immerse yourself with this list created for fibroblasts aficionados and lovers, and beyond. Here, my goal is to include preprints of fibroblast biology, heterogeneity, fate, extracellular matrix, behavior, topography, single-cell atlases, spatial transcriptomics, and their matrix!
| List by | Osvaldo Contreras |
FENS 2020
A collection of preprints presented during the virtual meeting of the Federation of European Neuroscience Societies (FENS) in 2020
| List by | Ana Dorrego-Rivas |
TAGC 2020
Preprints recently presented at the virtual Allied Genetics Conference, April 22-26, 2020. #TAGC20
| List by | Maiko Kitaoka et al. |
Autophagy
Preprints on autophagy and lysosomal degradation and its role in neurodegeneration and disease. Includes molecular mechanisms, upstream signalling and regulation as well as studies on pharmaceutical interventions to upregulate the process.
| List by | Sandra Malmgren Hill |
Cellular metabolism
A curated list of preprints related to cellular metabolism at Biorxiv by Pablo Ranea Robles from the Prelights community. Special interest on lipid metabolism, peroxisomes and mitochondria.
| List by | Pablo Ranea Robles |
Also in the systems biology category:
‘In preprints’ from Development 2022-2023
A list of the preprints featured in Development's 'In preprints' articles between 2022-2023
| List by | Alex Eve, Katherine Brown |
EMBL Synthetic Morphogenesis: From Gene Circuits to Tissue Architecture (2021)
A list of preprints mentioned at the #EESmorphoG virtual meeting in 2021.
| List by | Alex Eve |
Single Cell Biology 2020
A list of preprints mentioned at the Wellcome Genome Campus Single Cell Biology 2020 meeting.
| List by | Alex Eve |
ASCB EMBO Annual Meeting 2019
A collection of preprints presented at the 2019 ASCB EMBO Meeting in Washington, DC (December 7-11)
| List by | Madhuja Samaddar et al. |
EMBL Seeing is Believing – Imaging the Molecular Processes of Life
Preprints discussed at the 2019 edition of Seeing is Believing, at EMBL Heidelberg from the 9th-12th October 2019
| List by | Dey Lab |
Pattern formation during development
The aim of this preList is to integrate results about the mechanisms that govern patterning during development, from genes implicated in the processes to theoritical models of pattern formation in nature.
| List by | Alexa Sadier |