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PMID: 26528856 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

Collective cancer cell invasion induced by coordinated contractile stresses.

Oncotarget ·Vol. 6 ·No. 41 ·2015-12-22 ·Pages 43438-51

Jimenez Valencia AM, Wu PH, Yogurtcu ON, Rao P, DiGiacomo J, Godet I, He L, Lee MH, Gilkes D, Sun SX, Wirtz D

Abstract

The physical underpinnings of fibrosarcoma cell dissemination from a tumor in a surrounding collagen-rich matrix are poorly understood. Here we show that a tumor spheroid embedded in a 3D collagen matrix exerts large contractile forces on the matrix before invasion. Cell invasion is accompanied by complex spatially and temporally dependent patterns of cell migration within and at the surface of the spheroids that are fundamentally different from migratory patterns of individual fibrosarcoma cells homogeneously distributed in the same type of matrix. Cells display a continuous transition from a round morphology at the spheroid core, to highly aligned elongated morphology at the spheroid periphery, which depends on both β1-integrin-based cell-matrix adhesion and myosin II/ROCK-based cell contractility. This isotropic-to-anisotropic transition corresponds to a shift in migration, from a slow and unpolarized movement at the core, to a fast, polarized and persistent one at the periphery. Our results also show that the ensuing collective invasion of fibrosarcoma cells is induced by anisotropic contractile stresses exerted on the surrounding matrix.

Keywords
3D invasion model fibrosarcoma spatio-temporal invasion
MeSH Terms
Cell Adhesion Cell Line, Tumor Cell Movement/physiology Collagen/metabolism Extracellular Matrix/metabolism Fibrosarcoma/pathology Humans Microscopy, Fluorescence Neoplasm Invasiveness/pathology Spheroids, Cellular
Chemicals
Collagen
Authors & Affiliations
11 authors, click to expand affiliations / ORCID
Jimenez Valencia Angela M
Department of Chemical and Biomolecular Engineering, The Johns Hopkins University, Baltimore, Maryland, 21218, USA. | Physical Sciences-Oncology Center and Institute for NanoBioTechnology, The Johns Hopkins University, Baltimore, Maryland, 21218, USA.
Wu Pei-Hsun
Department of Chemical and Biomolecular Engineering, The Johns Hopkins University, Baltimore, Maryland, 21218, USA. | Physical Sciences-Oncology Center and Institute for NanoBioTechnology, The Johns Hopkins University, Baltimore, Maryland, 21218, USA.
Yogurtcu Osman N
Department of Mechanical Engineering, The Johns Hopkins University, Baltimore, Maryland, 21218, USA.
Rao Pranay
Department of Chemical and Biomolecular Engineering, The Johns Hopkins University, Baltimore, Maryland, 21218, USA.
DiGiacomo Josh
Department of Chemical and Biomolecular Engineering, The Johns Hopkins University, Baltimore, Maryland, 21218, USA.
Godet Inês
Department of Chemical and Biomolecular Engineering, The Johns Hopkins University, Baltimore, Maryland, 21218, USA.
He Lijuan
Department of Chemical and Biomolecular Engineering, The Johns Hopkins University, Baltimore, Maryland, 21218, USA. | Physical Sciences-Oncology Center and Institute for NanoBioTechnology, The Johns Hopkins University, Baltimore, Maryland, 21218, USA.
Lee Meng-Horng
Department of Chemical and Biomolecular Engineering, The Johns Hopkins University, Baltimore, Maryland, 21218, USA. | Physical Sciences-Oncology Center and Institute for NanoBioTechnology, The Johns Hopkins University, Baltimore, Maryland, 21218, USA.
Gilkes Daniele
Department of Chemical and Biomolecular Engineering, The Johns Hopkins University, Baltimore, Maryland, 21218, USA. | Physical Sciences-Oncology Center and Institute for NanoBioTechnology, The Johns Hopkins University, Baltimore, Maryland, 21218, USA.
Sun Sean X
Physical Sciences-Oncology Center and Institute for NanoBioTechnology, The Johns Hopkins University, Baltimore, Maryland, 21218, USA. | Department of Mechanical Engineering, The Johns Hopkins University, Baltimore, Maryland, 21218, USA.
Wirtz Denis
Department of Chemical and Biomolecular Engineering, The Johns Hopkins University, Baltimore, Maryland, 21218, USA. | Physical Sciences-Oncology Center and Institute for NanoBioTechnology, The Johns Hopkins University, Baltimore, Maryland, 21218, USA. | Department of Oncology and Department of Pathology, The Johns Hopkins School of Medicine, Baltimore, Maryland, 21218, USA.
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Article Info
Journal
Oncotarget
Abbr.
Oncotarget
ISSN
1949-2553
Published
2015-12-22
Pages
43438-51
Language
English
Region
United States
NLM ID
101532965
PMCID
PMC4791242
Subset
IM
Grants
NCI NIH HHS · U54 CA143868 · United States
NCI NIH HHS · R00 CA181352 · United States
NCI NIH HHS · U54CA143868 · United States
NCI NIH HHS · R01CA174388 · United States
NCI NIH HHS · R01 CA174388 · United States
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