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Hemodynamic forces tune the arrest, adhesion and extravasation of circulating tumor cells

Gautier Follain, Naël Osmani, Sofia Azevedo, Guillaume Allio, Luc Mercier, Matthia A. Karreman, Gergely Solecki, Nina Fekonja, Claudia Hille, Vincent Chabannes, Guillaume Dollé, Thibaut Metivet, Christophe Prudhomme, Bernhard Ruthensteiner, André Kemmling, Susanne Siemonsen, Tanja Schneider, Jens Fiehler, Markus Glatzel, Frank Winkler, Yannick Schwab, Klaus Pantel, Sébastien Harlepp, Jacky G. Goetz
doi: https://doi.org/10.1101/183046
Gautier Follain
1INSERM UMR_S1109, MN3T, Strasbourg, F-67200, France.
4Fédération de Médecine Translationnelle de Strasbourg (FMTS), Strasbourg, F-67000, France.
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Naël Osmani
1INSERM UMR_S1109, MN3T, Strasbourg, F-67200, France.
4Fédération de Médecine Translationnelle de Strasbourg (FMTS), Strasbourg, F-67000, France.
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Sofia Azevedo
1INSERM UMR_S1109, MN3T, Strasbourg, F-67200, France.
4Fédération de Médecine Translationnelle de Strasbourg (FMTS), Strasbourg, F-67000, France.
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Guillaume Allio
1INSERM UMR_S1109, MN3T, Strasbourg, F-67200, France.
4Fédération de Médecine Translationnelle de Strasbourg (FMTS), Strasbourg, F-67000, France.
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Luc Mercier
1INSERM UMR_S1109, MN3T, Strasbourg, F-67200, France.
4Fédération de Médecine Translationnelle de Strasbourg (FMTS), Strasbourg, F-67000, France.
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Matthia A. Karreman
5Cell Biology and Biophysics Unit, European Molecular Biology Laboratory, Heidelberg, 69117, Germany.
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Gergely Solecki
6Department of Neurooncology, University Hospital Heidelberg, Heidelberg, 69120, Germany and Clinical Cooperation Unit Neurooncology, German Cancer Research Center (DKFZ), Heidelberg, 69120, Germany.
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Nina Fekonja
1INSERM UMR_S1109, MN3T, Strasbourg, F-67200, France.
4Fédération de Médecine Translationnelle de Strasbourg (FMTS), Strasbourg, F-67000, France.
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Claudia Hille
7Institute of Tumor Biology, University Medical Center Hamburg-Eppendorf, Martinistrasse 52, Hamburg, 20246, Germany.
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Vincent Chabannes
8LabEx IRMIA, CEMOSIS, Université de Strasbourg, Strasbourg, F-67000 France.
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Guillaume Dollé
8LabEx IRMIA, CEMOSIS, Université de Strasbourg, Strasbourg, F-67000 France.
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Thibaut Metivet
8LabEx IRMIA, CEMOSIS, Université de Strasbourg, Strasbourg, F-67000 France.
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Christophe Prudhomme
8LabEx IRMIA, CEMOSIS, Université de Strasbourg, Strasbourg, F-67000 France.
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Bernhard Ruthensteiner
9Zoologische Staatssammlung München, Munich, 81247, Germany.
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André Kemmling
10Department of Neuroradiology, University Medical Center Schleswig-Holstein, Campus Lübeck, 23535 Lübeck, Germany
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Susanne Siemonsen
11Department of Diagnostic and Interventional Neuroradiology, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany
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Tanja Schneider
11Department of Diagnostic and Interventional Neuroradiology, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany
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Jens Fiehler
11Department of Diagnostic and Interventional Neuroradiology, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany
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Markus Glatzel
12Center for Diagnostics, Institute of Neuropathology, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany
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Frank Winkler
6Department of Neurooncology, University Hospital Heidelberg, Heidelberg, 69120, Germany and Clinical Cooperation Unit Neurooncology, German Cancer Research Center (DKFZ), Heidelberg, 69120, Germany.
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Yannick Schwab
5Cell Biology and Biophysics Unit, European Molecular Biology Laboratory, Heidelberg, 69117, Germany.
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Klaus Pantel
7Institute of Tumor Biology, University Medical Center Hamburg-Eppendorf, Martinistrasse 52, Hamburg, 20246, Germany.
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Sébastien Harlepp
2Université de Strasbourg, Strasbourg, F-67000, France.
13CNRS UMR7504, Institut de Physique et Chimie des Matériaux de Strasbourg (IPCMS), Strasbourg, F-67000, France.
14LabEx NIE, Université de Strasbourg, Strasbourg, F-67000, France.
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Jacky G. Goetz
1INSERM UMR_S1109, MN3T, Strasbourg, F-67200, France.
4Fédération de Médecine Translationnelle de Strasbourg (FMTS), Strasbourg, F-67000, France.
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  • For correspondence: jacky.goetz@inserm.fr
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ABSTRACT

Metastatic seeding is driven by cell-intrinsic and environmental cues, yet the contribution of biomechanics is poorly known. We aim to elucidate the impact of blood flow on the arrest and the extravasation of circulating tumor cells (CTCs) in vivo. Using the zebrafish embryo, we show that arrest of CTCs occurs mostly in vessels with favorable flow profiles where flow forces control the adhesion efficacy of CTCs to the endothelium. We biophysically identified the threshold values of flow and adhesion forces allowing successful arrest of CTCs. In addition, flow forces fine-tune tumor cell extravasation by impairing the remodeling properties of the endothelium. Importantly, we also observe endothelial remodeling at arrest sites of CTCs in mouse brain capillaries. Finally, we observed that human supratentorial brain metastases preferably develop in areas with low perfusion. Altogether, these results demonstrate that hemodynamic profiles at metastatic sites regulate key steps of extravasation preceding metastatic outgrowth.

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Posted August 31, 2017.
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Hemodynamic forces tune the arrest, adhesion and extravasation of circulating tumor cells
Gautier Follain, Naël Osmani, Sofia Azevedo, Guillaume Allio, Luc Mercier, Matthia A. Karreman, Gergely Solecki, Nina Fekonja, Claudia Hille, Vincent Chabannes, Guillaume Dollé, Thibaut Metivet, Christophe Prudhomme, Bernhard Ruthensteiner, André Kemmling, Susanne Siemonsen, Tanja Schneider, Jens Fiehler, Markus Glatzel, Frank Winkler, Yannick Schwab, Klaus Pantel, Sébastien Harlepp, Jacky G. Goetz
bioRxiv 183046; doi: https://doi.org/10.1101/183046
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Hemodynamic forces tune the arrest, adhesion and extravasation of circulating tumor cells
Gautier Follain, Naël Osmani, Sofia Azevedo, Guillaume Allio, Luc Mercier, Matthia A. Karreman, Gergely Solecki, Nina Fekonja, Claudia Hille, Vincent Chabannes, Guillaume Dollé, Thibaut Metivet, Christophe Prudhomme, Bernhard Ruthensteiner, André Kemmling, Susanne Siemonsen, Tanja Schneider, Jens Fiehler, Markus Glatzel, Frank Winkler, Yannick Schwab, Klaus Pantel, Sébastien Harlepp, Jacky G. Goetz
bioRxiv 183046; doi: https://doi.org/10.1101/183046

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