High-resolution line-scan Brillouin microscopy for live imaging of mechanical properties during embryo development.
Journal
Nature methods
ISSN: 1548-7105
Titre abrégé: Nat Methods
Pays: United States
ID NLM: 101215604
Informations de publication
Date de publication:
05 2023
05 2023
Historique:
received:
09
02
2022
accepted:
17
02
2023
medline:
12
5
2023
pubmed:
31
3
2023
entrez:
30
3
2023
Statut:
ppublish
Résumé
Brillouin microscopy can assess mechanical properties of biological samples in a three-dimensional (3D), all-optical and hence non-contact fashion, but its weak signals often lead to long imaging times and require an illumination dosage harmful for living organisms. Here, we present a high-resolution line-scanning Brillouin microscope for multiplexed and hence fast 3D imaging of dynamic biological processes with low phototoxicity. The improved background suppression and resolution, in combination with fluorescence light-sheet imaging, enables the visualization of the mechanical properties of cells and tissues over space and time in living organism models such as fruit flies, ascidians and mouse embryos.
Identifiants
pubmed: 36997817
doi: 10.1038/s41592-023-01822-1
pii: 10.1038/s41592-023-01822-1
pmc: PMC10172129
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
755-760Commentaires et corrections
Type : CommentIn
Informations de copyright
© 2023. The Author(s).
Références
Engler, A. J., Sen, S., Sweeney, H. L. & Discher, D. E. Matrix elasticity directs stem cell lineage specification. Cell 126, 677–689 (2006).
doi: 10.1016/j.cell.2006.06.044
pubmed: 16923388
Krieg, M. et al. Atomic force microscopy-based mechanobiology. Nat. Rev. Phys. 1, 41–57 (2019).
doi: 10.1038/s42254-018-0001-7
Hochmuth, R. M. Micropipette aspiration of living cells. J. Biomech. 33, 15–22 (2000).
doi: 10.1016/S0021-9290(99)00175-X
pubmed: 10609514
Kennedy, B. F., Wijesinghe, P. & Sampson, D. D. The emergence of optical elastography in biomedicine. Nat. Photon. 11, 215–221 (2017).
doi: 10.1038/nphoton.2017.6
Palombo, F. & Fioretto, D. Brillouin light scattering: applications in biomedical sciences. Chem. Rev. 119, 7833–7847 (2019).
doi: 10.1021/acs.chemrev.9b00019
pubmed: 31042024
pmcid: 6624783
Prevedel, R., Diz-Muñoz, A., Ruocco, G. & Antonacci, G. Brillouin microscopy: an emerging tool for mechanobiology. Nat. Methods 16, 969–977 (2019).
doi: 10.1038/s41592-019-0543-3
pubmed: 31548707
Antonacci, G. et al. Recent progress and current opinions in Brillouin microscopy for life science applications. Biophys. Rev. 12, 615–624 (2020).
doi: 10.1007/s12551-020-00701-9
pubmed: 32458371
pmcid: 7311586
Scarcelli, G. & Yun, S. H. Confocal Brillouin microscopy for three-dimensional mechanical imaging. Nat. Photon. 2, 39–43 (2008).
doi: 10.1038/nphoton.2007.250
Scarcelli, G. et al. Noncontact three-dimensional mapping of intracellular hydromechanical properties by Brillouin microscopy. Nat. Methods 12, 1132–1134 (2015).
doi: 10.1038/nmeth.3616
pubmed: 26436482
pmcid: 4666809
Mattana, S., Caponi, S., Tamagnini, F., Fioretto, D. & Palombo, F. Viscoelasticity of amyloid plaques in transgenic mouse brain studied by Brillouin microspectroscopy and correlative Raman analysis. J. Innov. Opt. Health Sci. 10, 1742001 (2017).
doi: 10.1142/S1793545817420019
pubmed: 29151920
pmcid: 5687568
Chan, C. J., Bevilacqua, C. & Prevedel, R. Mechanical mapping of mammalian follicle development using Brillouin microscopy. Commun. Biol. 4, 1133 (2021).
doi: 10.1038/s42003-021-02662-5
pubmed: 34580426
pmcid: 8476509
Scarcelli, G. & Yun, S. H. In vivo Brillouin optical microscopy of the human eye. Opt. Express 20, 9197–9202 (2012).
doi: 10.1364/OE.20.009197
pubmed: 22513631
pmcid: 3500092
Schlüßler, R. et al. Mechanical mapping of spinal cord growth and repair in living zebrafish larvae by Brillouin imaging. Biophys. J. 115, 911–923 (2018).
doi: 10.1016/j.bpj.2018.07.027
pubmed: 30122291
pmcid: 6127462
Bevilacqua, C., Sánchez-Iranzo, H., Richter, D., Diz-Muñoz, A. & Prevedel, R. Imaging mechanical properties of sub-micron ECM in live zebrafish using Brillouin microscopy. Biomed. Opt. Express 10, 1420–1431 (2019).
doi: 10.1364/BOE.10.001420
pubmed: 30891356
pmcid: 6420298
Palombo, F., Madami, M., Stone, N. & Fioretto, D. Mechanical mapping with chemical specificity by confocal Brillouin and Raman microscopy. Analyst 139, 729–733 (2014).
doi: 10.1039/C3AN02168H
pubmed: 24396853
Koski, K. J., Akhenblit, P., McKiernan, K. & Yarger, J. L. Non-invasive determination of the complete elastic moduli of spider silks. Nat. Mater. 12, 262–267 (2013).
doi: 10.1038/nmat3549
pubmed: 23353627
Yun, S. H. & Chernyak, D. Brillouin microscopy: assessing ocular tissue biomechanics. Curr. Opin. Ophthalmol. 29, 299–305 (2018).
doi: 10.1097/ICU.0000000000000489
pubmed: 29771749
pmcid: 6012042
Remer, I., Shaashoua, R., Shemesh, N., Ben-Zvi, A. & Bilenca, A. High-sensitivity and high-specificity biomechanical imaging by stimulated Brillouin scattering microscopy. Nat. Methods 17, 913–916 (2020).
doi: 10.1038/s41592-020-0882-0
pubmed: 32747769
Ballmann, C. W. et al. Stimulated Brillouin scattering microscopic imaging. Sci. Rep. 5, 18139 (2015).
doi: 10.1038/srep18139
pubmed: 26691398
pmcid: 4686920
Zhang, J., Fiore, A., Yun, S.-H., Kim, H. & Scarcelli, G. Line-scanning Brillouin microscopy for rapid non-invasive mechanical imaging. Sci. Rep. 6, 35398 (2016).
doi: 10.1038/srep35398
pubmed: 27739499
pmcid: 5064313
Strnad, P. et al. Inverted light-sheet microscope for imaging mouse pre-implantation development. Nat. Methods 13, 139–142 (2016).
doi: 10.1038/nmeth.3690
pubmed: 26657559
Elsayad, K. et al. Mapping the subcellular mechanical properties of live cells in tissues with fluorescence emission–Brillouin imaging. Sci. Signal. 9, rs5 (2016).
doi: 10.1126/scisignal.aaf6326
pubmed: 27382028
Meng, Z., Traverso, A. J. & Yakovlev, V. V. Background clean-up in Brillouin microspectroscopy of scattering medium. Opt. Express 22, 5410–5415 (2014).
doi: 10.1364/OE.22.005410
pubmed: 24663880
pmcid: 4086329
Caponi, S., Fioretto, D. & Mattarelli, M. On the actual spatial resolution of Brillouin imaging. Opt. Lett. 45, 1063–1066 (2020).
doi: 10.1364/OL.385072
pubmed: 32108770
Antonacci, G., Foreman, M. R., Paterson, C. & Török, P. Spectral broadening in Brillouin imaging. Appl. Phys. Lett. 103, 5–8 (2013).
doi: 10.1063/1.4836477
Nikolić, M. & Scarcelli, G. Long-term Brillouin imaging of live cells with reduced absorption-mediated damage at 660 nm wavelength. Biomed. Opt. Express 10, 1567–1580 (2019).
doi: 10.1364/BOE.10.001567
pubmed: 31086695
pmcid: 6484981
Martin, A. C. The physical mechanisms of Drosophila gastrulation: mesoderm and endoderm Invagination. Genetics 214, 543–560 (2020).
doi: 10.1534/genetics.119.301292
pubmed: 32132154
Bhide, S. et al. Mechanical competition alters the cellular interpretation of an endogenous genetic program. J. Cell Biol. 220, e202104107 (2021).
doi: 10.1083/jcb.202104107
pubmed: 34449835
pmcid: 8406609
Liu, T. L. et al. Observing the cell in its native state: imaging subcellular dynamics in multicellular organisms. Science 360, eaaq1392 (2018).
doi: 10.1126/science.aaq1392
pubmed: 29674564
pmcid: 6040645
Krzic, U., Gunther, S., Saunders, T. E., Streichan, S. J. & Hufnagel, L. Multiview light-sheet microscope for rapid in toto imaging. Nat. Methods 9, 730–733 (2012).
doi: 10.1038/nmeth.2064
pubmed: 22660739
Vergara, H. M. et al. Whole-body integration of gene expression and single-cell morphology. Cell 184, 4819–4837 (2021).
doi: 10.1016/j.cell.2021.07.017
pubmed: 34380046
pmcid: 8445025
Bakhshandeh, S. et al. Optical quantification of intracellular mass density and cell mechanics in 3D mechanical confinement. Soft Matter 17, 853–862 (2021).
doi: 10.1039/D0SM01556C
pubmed: 33232425
Przybylski, A., Thiel, B., Keller-Findeisen, J., Stock, B. & Bates, M. Gpufit: an open-source toolkit for GPU-accelerated curve fitting. Sci. Rep. 7, 15722 (2017).
doi: 10.1038/s41598-017-15313-9
pubmed: 29146965
pmcid: 5691161
Bulgakova, N. A., Grigoriev, I., Yap, A. S., Akhmanova, A. & Brown, N. H. Dynamic microtubules produce an asymmetric E-cadherin-Bazooka complex to maintain segment boundaries. J. Cell Biol. 201, 887–901 (2013).
doi: 10.1083/jcb.201211159
pubmed: 23751496
pmcid: 3678168
Campos-Ortega, J. A. & Hartenstein, V. The Embryonic Development of Drosophila melanogaster (Springer, 1997).
Gomez, J. M., Chumakova, L., Bulgakova, N. A. & Brown, N. H. Microtubule organization is determined by the shape of epithelial cells. Nat. Commun. 7, 13172 (2016).
doi: 10.1038/ncomms13172
pubmed: 27779189
pmcid: 5093320
Kölsch, V., Seher, T., Fernandez-Ballester, G. J., Serrano, L. & Leptin, M. Control of Drosophila gastrulation by apical localization of adherens junctions and RhoGEF2. Science 315, 384–386 (2007).
doi: 10.1126/science.1134833
pubmed: 17234948
Robin, F. B. et al. Time-lapse imaging of live Phallusia embryos for creating 3D digital replicas. Cold Spring Harb. Protoc. 2011, 1244–1246 (2011).
pubmed: 21969623
Reichmann, J., Eguren, M., Lin, Y., Schneider, I. & Ellenberg, J. Live imaging of cell division in preimplantation mouse embryos using inverted light-sheet microscopy. Methods Cell Biol. 145, 279–292 (2018).
doi: 10.1016/bs.mcb.2018.03.030
pubmed: 29957209