Twist1-positive epithelial cells retain adhesive and proliferative capacity throughout dissemination

Shamir, Eliah R.; Coutinho, Kester; Georgess, Dan; Auer, Manfred; Ewald, Andrew J.

doi:10.1242/bio.019703

Title: Twist1-positive epithelial cells retain adhesive and proliferative capacity throughout dissemination

Journal Article · 10 July 2016 · Biology Open

DOI: https://doi.org/10.1242/bio.019703 · OSTI ID:1627081

Shamir, Eliah R. ^[1]; Coutinho, Kester ^[2]; Georgess, Dan ^[3]; Auer, Manfred ^[3];

^[3]

Johns Hopkins University School of Medicine, Baltimore, MD (United States). Departments of Cell Biology and Oncology, Center for Cell Dynamics; DOE/OSTI
Johns Hopkins University School of Medicine, Baltimore, MD (United States). Departments of Cell Biology and Oncology, Center for Cell Dynamics; Lawrence Berkeley National Laboratory, Berkeley, CA United States). Molecular Biophysics and Integrated Bioimaging Division
Johns Hopkins University School of Medicine, Baltimore, MD (United States). Departments of Cell Biology and Oncology, Center for Cell Dynamics

Dissemination is the process by which cells detach and migrate away from a multicellular tissue. The epithelial-to-mesenchymal transition (EMT) conceptualizes dissemination in a stepwise fashion, with downregulation of E-cadherin leading to loss of intercellular junctions, induction of motility, and then escape from the epithelium. This gain of migratory activity is proposed to be mutually exclusive with proliferation. We previously developed a dissemination assay based on inducible expression of the transcription factor Twist1 and here utilize it to characterize the timing and dynamics of intercellular adhesion, proliferation and migration during dissemination. Surprisingly, Twist1+ epithelium displayed extensive intercellular junctions, and Twist1– luminal epithelial cells could still adhere to disseminating Twist1+ cells. Although proteolysis and proliferation were both observed throughout dissemination, neither was absolutely required. Finally, Twist1+ cells exhibited a hybrid migration mode; their morphology and nuclear deformation were characteristic of amoeboid cells, whereas their dynamic protrusive activity, pericellular proteolysis and migration speeds were more typical of mesenchymal cells. Our data reveal that epithelial cells can disseminate while retaining competence to adhere and proliferate.

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Sponsoring Organization:: USDOE

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1627081

Journal Information:: Biology Open, Journal Name: Biology Open Journal Issue: 9 Vol. 5; ISSN 2046-6390

Country of Publication:: United States

Language:: English

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Twist1-induced dissemination preserves epithelial identity and requires E-cadherin Shamir, Eliah R.; Pappalardo, Elisa; Jorgens, Danielle M. Journal of Cell Biology, Vol. 204, Issue 5 https://doi.org/10.1083/jcb.201306088	journal	March 2014
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Controversies around epithelial–mesenchymal plasticity in cancer metastasis Williams, Elizabeth D.; Gao, Dingcheng; Redfern, Andrew Nature Reviews Cancer, Vol. 19, Issue 12 https://doi.org/10.1038/s41568-019-0213-x	journal	October 2019
Bulk tumour cell migration in lung carcinomas might be more common than epithelial-mesenchymal transition and be differently regulated Zacharias, Martin; Brcic, Luka; Eidenhammer, Sylvia BMC Cancer, Vol. 18, Issue 1 https://doi.org/10.1186/s12885-018-4640-y	journal	July 2018
Control of Invasion by Epithelial-to-Mesenchymal Transition Programs during Metastasis Pearson, Gray W. Journal of Clinical Medicine, Vol. 8, Issue 5 https://doi.org/10.3390/jcm8050646	journal	May 2019
Bulk tumour cell migration in lung carcinomas might be more common than epithelial-mesenchymal transition and be differently regulated Zacharias, Martin; Brcic, Luka; Eidenhammer, Sylvia BMC Cancer, Vol. 18, Issue 1 https://doi.org/10.1186/s12885-018-4640-y	journal	July 2018

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