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Mammalian Amoeboid Swimming is propelled by molecular and not protrusion-based paddling in Lymphocytes

Laurene Aoun, Paulin Negre, Alexander Farutin, Nicolas Garcia-Seyda, Mohd Suhail Rivzi, Remi Galland, Alphee Michelot, Xuan Luo, Martine Biarnes-Pelicot, Claire Hivroz, Salima Rafai, Jean-Baptiste Sibareta, Marie-Pierre Valignat, Chaouqi Misbah, Olivier Theodoly
doi: https://doi.org/10.1101/509182
Laurene Aoun
Aix Marseille Univ, CNRS, INSERM, LAI, Turing Centre for Living Systems, Marseille, France.;
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Paulin Negre
Aix Marseille Univ, CNRS, INSERM, LAI, Turing Centre for Living Systems, Marseille, France.;
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Alexander Farutin
Univ. Grenoble Alpes, CNRS, LIPhy, 38000 Grenoble, France;
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Nicolas Garcia-Seyda
Aix Marseille Univ, CNRS, INSERM, LAI, Turing Centre for Living Systems, Marseille, France.;
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Mohd Suhail Rivzi
Univ. Grenoble Alpes, CNRS, LIPhy, 38000 Grenoble, France;
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Remi Galland
Interdisciplinary Institute for Neuroscience, Centre National de la Recherche Scientifique (CNRS);
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Alphee Michelot
Aix Marseille Univ, CNRS, IBDM, Turing Centre for Living Systems, Marseille, France;
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Xuan Luo
Aix Marseille Univ, CNRS, INSERM, LAI, Turing Centre for Living Systems, Marseille, France.;
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Martine Biarnes-Pelicot
Aix Marseille Univ, CNRS, INSERM, LAI, Turing Centre for Living Systems, Marseille, France.;
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Claire Hivroz
Institute Curie, INSERM U932, PSL Research University, Paris 75005, France
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Salima Rafai
Univ. Grenoble Alpes, CNRS, LIPhy, 38000 Grenoble, France;
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Jean-Baptiste Sibareta
Interdisciplinary Institute for Neuroscience, Centre National de la Recherche Scientifique (CNRS);
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Marie-Pierre Valignat
Aix Marseille Univ, CNRS, INSERM, LAI, Turing Centre for Living Systems, Marseille, France.;
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Chaouqi Misbah
Univ. Grenoble Alpes, CNRS, LIPhy, 38000 Grenoble, France;
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Olivier Theodoly
Aix Marseille Univ, CNRS, INSERM, LAI, Turing Centre for Living Systems, Marseille, France.;
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  • For correspondence: olivier.theodoly@inserm.fr
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Abstract

Mammalian cells developed two main migration modes. The slow mesenchymatous mode, like fibroblasts crawling, relies on maturation of adhesion complexes and actin fiber traction, while the fast amoeboid mode, observed exclusively for leukocytes and cancer cells, is characterized by weak adhesion, highly dynamic cell shapes, and ubiquitous motility on 2D and in 3D solid matrix. In both cases, interactions with the substrate by adhesion or friction are widely accepted as a prerequisite for mammalian cell motility, which precludes swimming. We show here experimentally and computationally that leukocytes do swim, and that propulsion is not fueled by waves of cell deformation but by a rearward and inhomogeneous treadmilling of the cell envelope. We model the propulsion as a molecular paddling by transmembrane proteins linked to and advected by the actin cortex, whereas freely diffusing transmembrane proteins hinder swimming. This mechanism explains that swimming is five times slower than the cortex retrograde flow. Resultantly the ubiquitous ability of mammalian amoeboid cells to migrate in various environments can be explained for lymphocytes by a single machinery of envelope treadmilling.

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Posted January 02, 2019.
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Mammalian Amoeboid Swimming is propelled by molecular and not protrusion-based paddling in Lymphocytes
Laurene Aoun, Paulin Negre, Alexander Farutin, Nicolas Garcia-Seyda, Mohd Suhail Rivzi, Remi Galland, Alphee Michelot, Xuan Luo, Martine Biarnes-Pelicot, Claire Hivroz, Salima Rafai, Jean-Baptiste Sibareta, Marie-Pierre Valignat, Chaouqi Misbah, Olivier Theodoly
bioRxiv 509182; doi: https://doi.org/10.1101/509182
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Mammalian Amoeboid Swimming is propelled by molecular and not protrusion-based paddling in Lymphocytes
Laurene Aoun, Paulin Negre, Alexander Farutin, Nicolas Garcia-Seyda, Mohd Suhail Rivzi, Remi Galland, Alphee Michelot, Xuan Luo, Martine Biarnes-Pelicot, Claire Hivroz, Salima Rafai, Jean-Baptiste Sibareta, Marie-Pierre Valignat, Chaouqi Misbah, Olivier Theodoly
bioRxiv 509182; doi: https://doi.org/10.1101/509182

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