Cancer cell viscoelasticity measurement by quantitative phase and flow stress induction
Language English Country United States Media print-electronic
Document type Journal Article, Research Support, Non-U.S. Gov't
PubMed
35390297
PubMed Central
PMC9117928
DOI
10.1016/j.bpj.2022.04.002
PII: S0006-3495(22)00276-4
Knihovny.cz E-resources
- MeSH
- Cytochalasin D MeSH
- Elastic Modulus MeSH
- Neoplasms * MeSH
- Elasticity MeSH
- Reproducibility of Results MeSH
- Viscosity MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- Cytochalasin D MeSH
Cell viscoelastic properties are affected by the cell cycle, differentiation, and pathological processes such as malignant transformation. Therefore, evaluation of the mechanical properties of the cells proved to be an approach to obtaining information on the functional state of the cells. Most of the currently used methods for cell mechanophenotyping are limited by low robustness or the need for highly expert operation. In this paper, the system and method for viscoelasticity measurement using shear stress induction by fluid flow is described and tested. Quantitative phase imaging (QPI) is used for image acquisition because this technique enables one to quantify optical path length delays introduced by the sample, thus providing a label-free objective measure of morphology and dynamics. Viscosity and elasticity determination were refined using a new approach based on the linear system model and parametric deconvolution. The proposed method allows high-throughput measurements during live-cell experiments and even through a time lapse, whereby we demonstrated the possibility of simultaneous extraction of shear modulus, viscosity, cell morphology, and QPI-derived cell parameters such as circularity or cell mass. Additionally, the proposed method provides a simple approach to measure cell refractive index with the same setup, which is required for reliable cell height measurement with QPI, an essential parameter for viscoelasticity calculation. Reliability of the proposed viscoelasticity measurement system was tested in several experiments including cell types of different Young/shear modulus and treatment with cytochalasin D or docetaxel, and an agreement with atomic force microscopy was observed. The applicability of the proposed approach was also confirmed by a time-lapse experiment with cytochalasin D washout, whereby an increase of stiffness corresponded to actin repolymerization in time.
See more in PubMed
Coughlin M.F., Bielenberg D.R., et al. Fredberg J.J. Cytoskeletal stiffness, friction, and fluidity of cancer cell lines with different metastatic potential. Clin. Exp. metastasis. 2013;30:237–250. PubMed PMC
Wirtz D., Konstantopoulos K., Searson P.C. The physics of cancer: the role of physical interactions and mechanical forces in metastasis. Nat. Rev. Cancer. 2011;11:512–522. PubMed PMC
Bufi N., Saitakis M., et al. Asnacios A. Human primary immune cells exhibit distinct mechanical properties that are modified by inflammation. Biophysical J. 2015;108:2181–2190. PubMed PMC
Jacobi A., Rosendahl P., et al. Guck J. Stem Cell Mobilization. Springer; 2019. Analysis of biomechanical properties of hematopoietic stem and progenitor cells using real-time fluorescence and deformability cytometry; pp. 135–148. PubMed
Moeendarbary E., Harris A.R. Cell mechanics: principles, practices, and prospects. Wiley Interdiscip. Rev. Syst. Biol. Med. 2014;6:371–388. PubMed PMC
Hao Y., Cheng S., et al. Li M. Mechanical properties of single cells: measurement methods and applications. Biotechnol. Adv. 2020;45:107648. PubMed
Wu P.-H., Aroush D.R.-B., et al. Wirtz D. A comparison of methods to assess cell mechanical properties. Nat. Methods. 2018;15:491–498. PubMed PMC
Alibert C., Goud B., Manneville J.-B. Are cancer cells really softer than normal cells? Biol. Cell. 2017;109:167–189. PubMed
Rother J., Nöding H., et al. Janshoff A. Atomic force microscopy-based microrheology reveals significant differences in the viscoelastic response between malign and benign cell lines. Open Biol. 2014;4:140046. PubMed PMC
Raudenska M., Kratochvilova M., et al. Masarik M. Cisplatin enhances cell stiffness and decreases invasiveness rate in prostate cancer cells by actin accumulation. Scientific Rep. 2019;9:1–11. PubMed PMC
Eaton P., Batziou K. Artifacts and practical issues in atomic force microscopy. At. force Microsc. 2019;1886:3–28. PubMed
Eldridge W.J., Sheinfeld A., et al. Wax A. Imaging deformation of adherent cells due to shear stress using quantitative phase imaging. Opt. Lett. 2016;41:352–355. PubMed
Eldridge W.J., Ceballos S., et al. Wax A. Shear modulus measurement by quantitative phase imaging and correlation with atomic force microscopy. Biophysical J. 2019;117:696–705. PubMed PMC
Rappaz B., Marquet P., et al. Magistretti P.J. Measurement of the integral refractive index and dynamic cell morphometry of living cells with digital holographic microscopy. Opt. Express. 2005;13:9361–9373. PubMed
Slaby T., Kolman P., et al. Chmelik R. Off-axis setup taking full advantage of incoherent illumination in coherence-controlled holographic microscope. Opt. Express. 2013;21:14747–14762. PubMed
ibidi GmbH Application Note 11 Shear Stress and Shear Rates for Ibidi Μ-Slides Based on Numerical Calculations Version 5.0. 2021. https://ibidi.com/img/cms/support/AN/AN11_Shear_stress.pdf
Park Y., Depeursinge C., Popescu G. Quantitative phase imaging in biomedicine. Nat. Photon. 2018;12:578–589.
Wu T., Feng J.J. A biomechanical model for fluidization of cells under dynamic strain. Biophysical J. 2015;108:43–52. PubMed PMC
Vicar T., Gumulec J., et al. Masarik M. 2021 43rd Annual International Conference of the IEEE Engineering in Medicine Biology Society. EMBC; 2021. Parametric deconvolution for cancer cells viscoelasticity measurements from quantitative phase images; pp. 439–442. PubMed
Boothe T., Hilbert L., et al. Rink J.C. A tunable refractive index matching medium for live imaging cells, tissues and model organisms. Elife. 2017;6:e27240. PubMed PMC
Wakatsuki T., Schwab B., et al. Elson E.L. Effects of cytochalasin D and latrunculin B on mechanical properties of cells. J. Cel. Sci. 2001;114:1025–1036. PubMed
Wang K., Sun X.H., et al. Chen J. Characterization of cytoplasmic viscosity of hundreds of single tumour cells based on micropipette aspiration. R. Soc. Open Sci. 2019;6:181707. PubMed PMC
Xiao H., Verdier-Pinard P., et al. Orr G.A. Insights into the mechanism of microtubule stabilization by Taxol. Proc. Natl. Acad. Sci. U S A. 2006;103:10166–10173. https://www.pnas.org/content/103/27/10166 PubMed PMC
Thurston G., Jaggi B., Palcic B. Measurement of cell motility and morphology with an automated microscope system. Cytometry: J. Int. Soc. Anal. Cytol. 1988;9:411–417. PubMed
Vicar T., Raudenska M., et al. Balvan J. The quantitative-phase dynamics of apoptosis and lytic cell death. Scientific Rep. 2020;10:1–12. PubMed PMC
Ojima K., Lin Z.-X., et al. Mermelstein C. Distinctive effects of cytochalasin B in chick primary myoblasts and fibroblasts. PloS one. 2016;11:e0154109. PubMed PMC
Kim K., Park W.S., et al. Park Y. Correlative three-dimensional fluorescence and refractive index tomography: bridging the gap between molecular specificity and quantitative bioimaging. Biomed. Opt. express. 2017;8:5688–5697. PubMed PMC
Liu P.Y., Chin L.K., et al. Leprince-Wang Y. Cell refractive index for cell biology and disease diagnosis: past, present and future. Lab Chip. 2016;16:634–644. doi: 10.1039/C5LC01445J. PubMed DOI
Nehls S., Nöding H., et al. Janshoff A. Stiffness of MDCK II cells depends on confluency and cell size. Biophysical J. 2019;116:2204–2211. PubMed PMC
Chiou Y.-W., Lin H.-K., et al. Yeh M.-L. The influence of physical and physiological cues on atomic force microscopy-based cell stiffness assessment. PloS one. 2013;8:e77384. PubMed PMC
Spedden E., White J.D., et al. Staii C. Elasticity maps of living neurons measured by combined fluorescence and atomic force microscopy. Biophysical J. 2012;103:868–877. PubMed PMC
Zemła J., Bobrowska J., et al. Lekka M. Indenting soft samples (hydrogels and cells) with cantilevers possessing various shapes of probing tip. Eur. Biophys. J. 2020;49:485–495. PubMed PMC
Adeniba O.O., Corbin E.A., et al. Bashir R. Simultaneous time-varying viscosity, elasticity, and mass measurements of single adherent cancer cells across cell cycle. Scientific Rep. 2020;10:1–12. PubMed PMC
Yun X., Tang M., et al. Wang H. Interrogation of drug effects on HeLa cells by exploiting new AFM mechanical biomarkers. RSC Adv. 2017;7:43764–43771. doi: 10.1039/C7RA06233H. DOI
Shimolina L.E., Gulin A.A., et al. Shirmanova M.V. Mapping cisplatin-induced viscosity alterations in cancer cells using molecular rotor and fluorescence lifetime imaging microscopy. J. Biomed. Opt. 2020;25:1–16. doi: 10.1117/1.JBO.25.12.126004. PubMed DOI PMC
Guyer M., Claus P.E. Increased viscosity of cells of induced tumors. Cancer Res. 1942;2:16–18.
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