Collective rotational motion of freely expanding T84 epithelial cell colonies
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Collective rotational motion of freely expanding T84 epithelial cell colonies. / Ascione, Flora; Caserta, Sergio; Esposito, Speranza; Rachela, Valeria Villella; Maiuri, Luigi; Nejad, Mehrana R.; Doostmohammadi, Amin; Yeomans, Julia M.; Guido, Stefano.
I: Journal of the Royal Society Interface, Bind 20, Nr. 199, 20220719, 22.02.2023.Publikation: Bidrag til tidsskrift › Tidsskriftartikel › Forskning › fagfællebedømt
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T1 - Collective rotational motion of freely expanding T84 epithelial cell colonies
AU - Ascione, Flora
AU - Caserta, Sergio
AU - Esposito, Speranza
AU - Rachela, Valeria Villella
AU - Maiuri, Luigi
AU - Nejad, Mehrana R.
AU - Doostmohammadi, Amin
AU - Yeomans, Julia M.
AU - Guido, Stefano
PY - 2023/2/22
Y1 - 2023/2/22
N2 - Coordinated rotational motion is an intriguing, yet still elusive mode of collective cell migration, which is relevant in pathological and morphogenetic processes. Most of the studies on this topic have been carried out on epithelial cells plated on micropatterned substrates, where cell motion is confined in regions of well-defined shapes coated with extracellular matrix adhesive proteins. The driver of collective rotation in such conditions has not been clearly elucidated, although it has been speculated that spatial confinement can play an essential role in triggering cell rotation. Here, we study the growth of epithelial cell colonies freely expanding (i.e. with no physical constraints) on the surface of cell culture plates and focus on collective cell rotation in such conditions, a case which has received scarce attention in the literature. One of the main findings of our work is that coordinated cell rotation spontaneously occurs in cell clusters in the free growth regime, thus implying that cell confinement is not necessary to elicit collective rotation as previously suggested. The extent of collective rotation was size and shape dependent: a highly coordinated disc-like rotation was found in small cell clusters with a round shape, while collective rotation was suppressed in large irregular cell clusters generated by merging of different clusters in the course of their growth. The angular motion was persistent in the same direction, although clockwise and anticlockwise rotations were equally likely to occur among different cell clusters. Radial cell velocity was quite low as compared to the angular velocity, in agreement with the free expansion regime where cluster growth is essentially governed by cell proliferation. A clear difference in morphology was observed between cells at the periphery and the ones in the core of the clusters, the former being more elongated and spread out as compared to the latter. Overall, our results, to our knowledge, provide the first quantitative and systematic evidence that coordinated cell rotation does not require a spatial confinement and occurs spontaneously in freely expanding epithelial cell colonies, possibly as a mechanism for the system.
AB - Coordinated rotational motion is an intriguing, yet still elusive mode of collective cell migration, which is relevant in pathological and morphogenetic processes. Most of the studies on this topic have been carried out on epithelial cells plated on micropatterned substrates, where cell motion is confined in regions of well-defined shapes coated with extracellular matrix adhesive proteins. The driver of collective rotation in such conditions has not been clearly elucidated, although it has been speculated that spatial confinement can play an essential role in triggering cell rotation. Here, we study the growth of epithelial cell colonies freely expanding (i.e. with no physical constraints) on the surface of cell culture plates and focus on collective cell rotation in such conditions, a case which has received scarce attention in the literature. One of the main findings of our work is that coordinated cell rotation spontaneously occurs in cell clusters in the free growth regime, thus implying that cell confinement is not necessary to elicit collective rotation as previously suggested. The extent of collective rotation was size and shape dependent: a highly coordinated disc-like rotation was found in small cell clusters with a round shape, while collective rotation was suppressed in large irregular cell clusters generated by merging of different clusters in the course of their growth. The angular motion was persistent in the same direction, although clockwise and anticlockwise rotations were equally likely to occur among different cell clusters. Radial cell velocity was quite low as compared to the angular velocity, in agreement with the free expansion regime where cluster growth is essentially governed by cell proliferation. A clear difference in morphology was observed between cells at the periphery and the ones in the core of the clusters, the former being more elongated and spread out as compared to the latter. Overall, our results, to our knowledge, provide the first quantitative and systematic evidence that coordinated cell rotation does not require a spatial confinement and occurs spontaneously in freely expanding epithelial cell colonies, possibly as a mechanism for the system.
KW - epithelial cells
KW - active matter
KW - collective rotation
KW - living matter
KW - active nematics
KW - COHERENT ANGULAR MOTION
KW - MIGRATION
KW - MONOLAYER
KW - DIFFUSION
KW - DYNAMICS
KW - DIVISION
KW - GUIDANCE
KW - BEHAVIOR
KW - FLOW
U2 - 10.1098/rsif.2022.0719
DO - 10.1098/rsif.2022.0719
M3 - Journal article
C2 - 36872917
VL - 20
JO - Journal of the Royal Society Interface
JF - Journal of the Royal Society Interface
SN - 2042-8898
IS - 199
M1 - 20220719
ER -
ID: 340974205