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Unjamming and collective migration in MCF10A breast cancer cell lines

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Kim, Jae Hun, Pegoraro, Adrian F., Das, Amit, Koehler, Stephan A., Ujwary, Sylvia Ann, Lan, Bo, Mitchel, Jennifer A., Atia, Lior +9 more·2020·Biochemical and Biophysical Research Communications
DOI 10.1016/j.bbrc.2019.10.188PMC PMC6937379
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Abstract

Each cell comprising an intact, healthy, confluent epithelial layer ordinarily remains sedentary, firmly adherent to and caged by its neighbors, and thus defines an elemental constituent of a solid-like cellular collective [1,2]. After malignant transformation, however, the cellular collective can become fluid-like and migratory, as evidenced by collective motions that arise in characteristic swirls, strands, ducts, sheets, or clusters [3,4]. To transition from a solid-like to a fluid-like phase and thereafter to migrate collectively, it has been recently argued that cells comprising the disordered but confluent epithelial collective can undergo changes of cell shape so as to overcome geometric constraints attributable to the newly discovered phenomenon of cell jamming and the associated unjamming transition (UJT) [1,2,5-9]. Relevance of the jamming concept to carcinoma cells lines of graded degrees of invasive potential has never been investigated, however. Using classical in vitro cultures of six breast cancer model systems, here we investigate structural and dynamical signatures of cell jamming, and the relationship between them [1,2,10,11]. In order of roughly increasing invasive potential as previously reported, model systems examined included MCF10A, MCF10A.Vector; MCF10A.14-3-3ζ; MCF10.ErbB2, MCF10AT; and MCF10CA1a [12-15]. Migratory speed depended on the particular cell line. Unsurprisingly, for example, the MCF10CA1a cell line exhibited much faster migratory speed relative to the others. But unexpectedly, across different cell lines higher speeds were associated with enhanced size of cooperative cell packs in a manner reminiscent of a peloton [9]. Nevertheless, within each of the cell lines evaluated, cell shape and shape variability from cell-to-cell conformed with predicted structural signatures of cell layer unjamming [1]. Moreover, both structure and migratory dynamics were compatible with previous theoretical descriptions of the cell jamming mechanism [2,10,11,16,17]. As such, these findings demonstrate the richness of the cell jamming mechanism, which is now seen to apply across these cancer cell lines but remains poorly understood.

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  • Cancer progression, in some stages, is more efficient thanks to the fluidization/rigidification of the involved tissues.

    “This discrete nature comes hand in hand with side effects: cancer progression, in some stages, is more efficient thanks to the fluidization/rigidification of the involved tissues [407].”

    From Fundamental constraints to the logic of living systems (2024) · cites this paper as [407]

    The Discussion (“Shape, speed, and cooperativity”; page not provided) links the transition to a fluid-like, collectively migratory state with a proposed role in cancer progression. It does not show that rigidification makes cancer progression more efficient, or establish increased progression efficiency at particular stages. (LLM, conf=0.84)

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  • Fundamental constraints to the logic of living systems

    Solé, R., Kempes, C. P., Corominas-Murtra, B., De Domenico, M., Kolchinsky, A., Lachmann, M., Libby, E., Saavedra, S., Smith, E., & Wolpert, D. (2024) · Interface Focus · doi:10.1098/rsfs.2024.0010 · Cited by 34 · see citing works

    “This discrete nature comes hand in hand with side effects: cancer progression, in some stages, is more efficient thanks to the fluidization/rigidification of the involved tissues [407].”
    Background

Authors
Kim, J. H., Pegoraro, A. F., Das, A., Koehler, S. A., Ujwary, S. A., Lan, B., Mitchel, J. A., Atia, L., He, S., Wang, K., Bi, D., Zaman, M. H., Park, J.-A., Butler, J. P., Lee, K. H., Starr, J. R., & Fredberg, J. J.
Affiliations
  • Harvard University (US)
  • University of Ottawa (CA)
  • Northeastern University (US)
  • Temple University (US)
  • Boston University (US)
  • Brigham and Women's Hospital (US)
  • The Forsyth Institute (US)
Corresponding author
Fredberg, Jeffrey J.
ORCID
Venue
Biochemical and Biophysical Research Communications
Publisher
Elsevier BV
Published
2020-01
Volume
521
Issue
3
Pages
706-715
ISSN
0006-291X (ISSN-L)
DOI
10.1016/j.bbrc.2019.10.188
PMC
PMC6937379
OpenAlex
W2989175110
Cited by
65
References
2
Citations by year
2026: 5 · 2025: 14 · 2024: 11 · 2023: 11 · 2022: 9 · 2021: 9 · 2020: 5 · 2012: 1
FWCI
3.02
Type
journal article
Language
en
Open access
Licence
Locations
  • Biochemical and Biophysical Research Communications (publishedVersion)
  • PubMed (publishedVersion)
  • Europe PMC (PubMed Central) (acceptedVersion)
  • PubMed Central (acceptedVersion)
Funders
National Institutes of Health
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular Mechanics and Interactions
  • Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
  • Physical Sciences › Materials Science › Materials Chemistry › Material Dynamics and Properties
Keywords
cell jamming, unjamming transition, collective cell migration, breast cancer cell lines, MCF10A, cell shape, cell-cell adhesion, invasive potential
MeSH terms
Breast Neoplasms, Cell Movement, Cell Transformation, Neoplastic, Female, Humans, Neoplasm Invasiveness, Cell Line, Tumor, Cell Shape

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