Cell and Nucleus Shape as an Indicator of Tissue Fluidity in Carcinoma

Tissue, cell, and nucleus morphology change during tumor progression. In 2D confluent cell cultures, different tissue states, such as fluid (unjammed) and solid (jammed), are correlated with cell shapes. These results do not have to apply a priori to three dimensions. Cancer cell motility requires a...

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Autores principales:	Steffen Grosser, Jürgen Lippoldt, Linda Oswald, Matthias Merkel, Daniel M. Sussman, Frédéric Renner, Pablo Gottheil, Erik W. Morawetz, Thomas Fuhs, Xiaofan Xie, Steve Pawlizak, Anatol W. Fritsch, Benjamin Wolf, Lars-Christian Horn, Susanne Briest, Bahriye Aktas, M. Lisa Manning, Josef A. Käs
Formato:	article
Lenguaje:	EN
Publicado:	American Physical Society 2021
Materias:	Physics QC1-999
Acceso en línea:	https://doaj.org/article/d2bc1c5286d3438697d2a8671f69ec4e
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spelling	oai:doaj.org-article:d2bc1c5286d3438697d2a8671f69ec4e2021-12-02T14:07:13ZCell and Nucleus Shape as an Indicator of Tissue Fluidity in Carcinoma10.1103/PhysRevX.11.0110332160-3308https://doaj.org/article/d2bc1c5286d3438697d2a8671f69ec4e2021-02-01T00:00:00Zhttp://doi.org/10.1103/PhysRevX.11.011033http://doi.org/10.1103/PhysRevX.11.011033https://doaj.org/toc/2160-3308Tissue, cell, and nucleus morphology change during tumor progression. In 2D confluent cell cultures, different tissue states, such as fluid (unjammed) and solid (jammed), are correlated with cell shapes. These results do not have to apply a priori to three dimensions. Cancer cell motility requires and corresponds to a fluidization of the tumor tissue on the bulk level. Here, we investigate bulk tissue fluidity in 3D and determine how it correlates with cell and nucleus shape. In patient samples of mamma and cervix carcinoma, we find areas where cells can move or are immobile. We compare 3D cell spheroids composed of cells from a cancerous and a noncancerous cell line. Through bulk mechanical spheroid-fusion experiments and single live-cell tracking, we show that the cancerous sample is fluidized by active cells moving through the tissue. The healthy, epithelial sample with immobile cells behaves more solidlike. 3D segmentations of the samples show that the degree of tissue fluidity correlates with elongated cell and nucleus shapes. This correlation links cell shapes to cell motility and bulk mechanical behavior. We find two active states of matter in solid tumors: an amorphous glasslike state with characteristics of 3D cell jamming and a disordered fluid state. Individual cell and nucleus shape may serve as a marker for metastatic potential to foster personalized cancer treatment.Steffen GrosserJürgen LippoldtLinda OswaldMatthias MerkelDaniel M. SussmanFrédéric RennerPablo GottheilErik W. MorawetzThomas FuhsXiaofan XieSteve PawlizakAnatol W. FritschBenjamin WolfLars-Christian HornSusanne BriestBahriye AktasM. Lisa ManningJosef A. KäsAmerican Physical SocietyarticlePhysicsQC1-999ENPhysical Review X, Vol 11, Iss 1, p 011033 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Physics QC1-999
spellingShingle	Physics QC1-999 Steffen Grosser Jürgen Lippoldt Linda Oswald Matthias Merkel Daniel M. Sussman Frédéric Renner Pablo Gottheil Erik W. Morawetz Thomas Fuhs Xiaofan Xie Steve Pawlizak Anatol W. Fritsch Benjamin Wolf Lars-Christian Horn Susanne Briest Bahriye Aktas M. Lisa Manning Josef A. Käs Cell and Nucleus Shape as an Indicator of Tissue Fluidity in Carcinoma
description	Tissue, cell, and nucleus morphology change during tumor progression. In 2D confluent cell cultures, different tissue states, such as fluid (unjammed) and solid (jammed), are correlated with cell shapes. These results do not have to apply a priori to three dimensions. Cancer cell motility requires and corresponds to a fluidization of the tumor tissue on the bulk level. Here, we investigate bulk tissue fluidity in 3D and determine how it correlates with cell and nucleus shape. In patient samples of mamma and cervix carcinoma, we find areas where cells can move or are immobile. We compare 3D cell spheroids composed of cells from a cancerous and a noncancerous cell line. Through bulk mechanical spheroid-fusion experiments and single live-cell tracking, we show that the cancerous sample is fluidized by active cells moving through the tissue. The healthy, epithelial sample with immobile cells behaves more solidlike. 3D segmentations of the samples show that the degree of tissue fluidity correlates with elongated cell and nucleus shapes. This correlation links cell shapes to cell motility and bulk mechanical behavior. We find two active states of matter in solid tumors: an amorphous glasslike state with characteristics of 3D cell jamming and a disordered fluid state. Individual cell and nucleus shape may serve as a marker for metastatic potential to foster personalized cancer treatment.
format	article
author	Steffen Grosser Jürgen Lippoldt Linda Oswald Matthias Merkel Daniel M. Sussman Frédéric Renner Pablo Gottheil Erik W. Morawetz Thomas Fuhs Xiaofan Xie Steve Pawlizak Anatol W. Fritsch Benjamin Wolf Lars-Christian Horn Susanne Briest Bahriye Aktas M. Lisa Manning Josef A. Käs
author_facet	Steffen Grosser Jürgen Lippoldt Linda Oswald Matthias Merkel Daniel M. Sussman Frédéric Renner Pablo Gottheil Erik W. Morawetz Thomas Fuhs Xiaofan Xie Steve Pawlizak Anatol W. Fritsch Benjamin Wolf Lars-Christian Horn Susanne Briest Bahriye Aktas M. Lisa Manning Josef A. Käs
author_sort	Steffen Grosser
title	Cell and Nucleus Shape as an Indicator of Tissue Fluidity in Carcinoma
title_short	Cell and Nucleus Shape as an Indicator of Tissue Fluidity in Carcinoma
title_full	Cell and Nucleus Shape as an Indicator of Tissue Fluidity in Carcinoma
title_fullStr	Cell and Nucleus Shape as an Indicator of Tissue Fluidity in Carcinoma
title_full_unstemmed	Cell and Nucleus Shape as an Indicator of Tissue Fluidity in Carcinoma
title_sort	cell and nucleus shape as an indicator of tissue fluidity in carcinoma
publisher	American Physical Society
publishDate	2021
url	https://doaj.org/article/d2bc1c5286d3438697d2a8671f69ec4e
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Cell and Nucleus Shape as an Indicator of Tissue Fluidity in Carcinoma

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