Literature DB >> 31699371

Unjamming and collective migration in MCF10A breast cancer cell lines.

Jae Hun Kim1, Adrian F Pegoraro2, Amit Das3, Stephan A Koehler1, Sylvia Ann Ujwary1, Bo Lan1, Jennifer A Mitchel1, Lior Atia1, Shijie He4, Karin Wang5, Dapeng Bi3, Muhammad H Zaman6, Jin-Ah Park1, James P Butler7, Kyu Ha Lee8, Jacqueline R Starr8, Jeffrey J Fredberg9.   

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.
Copyright © 2019 Elsevier Inc. All rights reserved.

Entities:  

Keywords:  Breast carcinoma; Cell shape; Collective migration; Cooperativity; Unjamming

Mesh:

Year:  2019        PMID: 31699371      PMCID: PMC6937379          DOI: 10.1016/j.bbrc.2019.10.188

Source DB:  PubMed          Journal:  Biochem Biophys Res Commun        ISSN: 0006-291X            Impact factor:   3.575


  59 in total

1.  Energy barriers and cell migration in densely packed tissues.

Authors:  Dapeng Bi; Jorge H Lopez; J M Schwarz; M Lisa Manning
Journal:  Soft Matter       Date:  2014-03-28       Impact factor: 3.679

2.  Morphogenesis and oncogenesis of MCF-10A mammary epithelial acini grown in three-dimensional basement membrane cultures.

Authors:  Jayanta Debnath; Senthil K Muthuswamy; Joan S Brugge
Journal:  Methods       Date:  2003-07       Impact factor: 3.608

Review 3.  Collective cell migration in morphogenesis, regeneration and cancer.

Authors:  Peter Friedl; Darren Gilmour
Journal:  Nat Rev Mol Cell Biol       Date:  2009-07       Impact factor: 94.444

4.  Collective invasion in breast cancer requires a conserved basal epithelial program.

Authors:  Kevin J Cheung; Edward Gabrielson; Zena Werb; Andrew J Ewald
Journal:  Cell       Date:  2013-12-12       Impact factor: 41.582

Review 5.  Mechanoreciprocity in cell migration.

Authors:  Sjoerd van Helvert; Cornelis Storm; Peter Friedl
Journal:  Nat Cell Biol       Date:  2017-12-21       Impact factor: 28.824

6.  Cell jamming: collective invasion of mesenchymal tumor cells imposed by tissue confinement.

Authors:  Anna Haeger; Marina Krause; Katarina Wolf; Peter Friedl
Journal:  Biochim Biophys Acta       Date:  2014-04-08

7.  Autocrine Fibronectin Inhibits Breast Cancer Metastasis.

Authors:  Aparna Shinde; Sarah Libring; Aktan Alpsoy; Ammara Abdullah; James A Schaber; Luis Solorio; Michael K Wendt
Journal:  Mol Cancer Res       Date:  2018-06-22       Impact factor: 5.852

8.  Unjamming overcomes kinetic and proliferation arrest in terminally differentiated cells and promotes collective motility of carcinoma.

Authors:  Andrea Palamidessi; Chiara Malinverno; Emanuela Frittoli; Salvatore Corallino; Elisa Barbieri; Sara Sigismund; Galina V Beznoussenko; Emanuele Martini; Massimiliano Garre; Ines Ferrara; Claudio Tripodo; Flora Ascione; Elisabetta A Cavalcanti-Adam; Qingsen Li; Pier Paolo Di Fiore; Dario Parazzoli; Fabio Giavazzi; Roberto Cerbino; Giorgio Scita
Journal:  Nat Mater       Date:  2019-07-22       Impact factor: 47.656

9.  Jamming transitions in cancer.

Authors:  Linda Oswald; Steffen Grosser; David M Smith; Josef A Käs
Journal:  J Phys D Appl Phys       Date:  2017-10-27       Impact factor: 3.207

10.  A fluid-to-solid jamming transition underlies vertebrate body axis elongation.

Authors:  Alessandro Mongera; Payam Rowghanian; Hannah J Gustafson; Elijah Shelton; David A Kealhofer; Emmet K Carn; Friedhelm Serwane; Adam A Lucio; James Giammona; Otger Campàs
Journal:  Nature       Date:  2018-09-05       Impact factor: 49.962

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  12 in total

1.  On the origins of order.

Authors:  Jeffrey J Fredberg
Journal:  Soft Matter       Date:  2022-03-23       Impact factor: 3.679

Review 2.  Contribution of mechanical homeostasis to epithelial-mesenchymal transition.

Authors:  Se Jik Han; Sangwoo Kwon; Kyung Sook Kim
Journal:  Cell Oncol (Dordr)       Date:  2022-09-23       Impact factor: 7.051

Review 3.  Varied solutions to multicellularity: The biophysical and evolutionary consequences of diverse intercellular bonds.

Authors:  Thomas C Day; Pedro Márquez-Zacarías; Pablo Bravo; Aawaz R Pokhrel; Kathryn A MacGillivray; William C Ratcliff; Peter J Yunker
Journal:  Biophys Rev (Melville)       Date:  2022-06-01

Review 4.  Are cell jamming and unjamming essential in tissue development?

Authors:  Lior Atia; Jeffrey J Fredberg; Nir S Gov; Adrian F Pegoraro
Journal:  Cells Dev       Date:  2021-08-04

5.  Topological data analysis of collective and individual epithelial cells using persistent homology of loops.

Authors:  Dhananjay Bhaskar; William Y Zhang; Ian Y Wong
Journal:  Soft Matter       Date:  2021-05-05       Impact factor: 4.046

6.  Distinct roles of tumor associated mutations in collective cell migration.

Authors:  Rachel M Lee; Michele I Vitolo; Wolfgang Losert; Stuart S Martin
Journal:  Sci Rep       Date:  2021-05-13       Impact factor: 4.996

7.  A novel jamming phase diagram links tumor invasion to non-equilibrium phase separation.

Authors:  Wenying Kang; Jacopo Ferruzzi; Catalina-Paula Spatarelu; Yu Long Han; Yasha Sharma; Stephan A Koehler; Jennifer A Mitchel; Adil Khan; James P Butler; Darren Roblyer; Muhammad H Zaman; Jin-Ah Park; Ming Guo; Zi Chen; Adrian F Pegoraro; Jeffrey J Fredberg
Journal:  iScience       Date:  2021-10-12

8.  Epithelial layer unjamming shifts energy metabolism toward glycolysis.

Authors:  Stephen J DeCamp; Victor M K Tsuda; Jacopo Ferruzzi; Stephan A Koehler; John T Giblin; Darren Roblyer; Muhammad H Zaman; Scott T Weiss; Ayşe Kılıç; Margherita De Marzio; Chan Young Park; Nicolas Chiu Ogassavara; Jennifer A Mitchel; James P Butler; Jeffrey J Fredberg
Journal:  Sci Rep       Date:  2020-10-27       Impact factor: 4.379

9.  In primary airway epithelial cells, the unjamming transition is distinct from the epithelial-to-mesenchymal transition.

Authors:  Jennifer A Mitchel; Amit Das; Michael J O'Sullivan; Ian T Stancil; Stephen J DeCamp; Stephan Koehler; Oscar H Ocaña; James P Butler; Jeffrey J Fredberg; M Angela Nieto; Dapeng Bi; Jin-Ah Park
Journal:  Nat Commun       Date:  2020-10-07       Impact factor: 14.919

10.  Tight Junction ZO Proteins Maintain Tissue Fluidity, Ensuring Efficient Collective Cell Migration.

Authors:  Mark Skamrahl; Hongtao Pang; Maximilian Ferle; Jannis Gottwald; Angela Rübeling; Riccardo Maraspini; Alf Honigmann; Tabea A Oswald; Andreas Janshoff
Journal:  Adv Sci (Weinh)       Date:  2021-08-12       Impact factor: 16.806

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