Amoeboid Swimming Is Propelled by Molecular Paddling in Lymphocytes

Laurene Aoun, Alexander Farutin, Nicolas Garcia-Seyda, Paulin Nègre, Mohd Suhail Rizvi, Sham Tlili, Solene Song, Xuan Luo, Martine Biarnes-Pelicot, Rémi Galland, Jean-Baptiste Sibarita, Alphée Michelot, Claire Hivroz, Salima Rafai, Marie-Pierre Valignat, Chaouqi Misbah, Olivier Theodoly
Biophysical Journal. 2020-09-01; 119(6): 1157-1177
DOI: 10.1016/j.bpj.2020.07.033

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Aoun L(1), Farutin A(2), Garcia-Seyda N(1), Nègre P(1), Rizvi MS(2), Tlili S(3), Song S(1), Luo X(1), Biarnes-Pelicot M(1), Galland R(4), Sibarita JB(4), Michelot A(5), Hivroz C(6), Rafai S(2), Valignat MP(1), Misbah C(7), Theodoly
O(8).

Author information:
(1)Aix Marseille University, CNRS, INSERM, LAI, Turing Centre for Living
Systems, Marseille, France.
(2)University Grenoble Alpes, CNRS, LIPhy, Grenoble, France.
(3)Aix Marseille University, CNRS, INSERM, LAI, Turing Centre for Living
Systems, Marseille, France; Aix Marseille University, CNRS, IBDM, Turing Centre
for Living Systems, Marseille, France.
(4)Univ. Bordeaux, CNRS, Interdisciplinary Institute for Neuroscience, IINS, UMR
5297, Bordeaux, France.
(5)Aix Marseille University, CNRS, IBDM, Turing Centre for Living Systems,
Marseille, France.
(6)Institut Curie, PSL Research University, INSERM U932, Integrative analysis of
T cell activation team, Paris, France.
(7)University Grenoble Alpes, CNRS, LIPhy, Grenoble, France. Electronic address:
.
(8)Aix Marseille University, CNRS, INSERM, LAI, Turing Centre for Living
Systems, Marseille, France. Electronic address: .

Comment in
Biophys J. 2020 Sep 15;119(6):1048-1049.

Mammalian cells developed two main migration modes. The slow mesenchymatous
mode, like crawling of fibroblasts, relies on maturation of adhesion complexes
and actin fiber traction, whereas the fast amoeboid mode, observed exclusively
for leukocytes and cancer cells, is characterized by weak adhesion, highly
dynamic cell shapes, and ubiquitous motility on two-dimensional and in
three-dimensional 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 experimental and computational
evidence that leukocytes do swim, and that efficient propulsion is not fueled by
waves of cell deformation but by a rearward and inhomogeneous treadmilling of
the cell external membrane. Our model consists of a molecular paddling by
transmembrane proteins linked to and advected by the actin cortex, whereas
freely diffusing transmembrane proteins hinder swimming. Furthermore, continuous
paddling is enabled by a combination of external treadmilling and selective
recycling by internal vesicular transport of cortex-bound transmembrane
proteins. This mechanism explains observations that swimming is five times
slower than the retrograde flow of cortex and also that lymphocytes are motile
in nonadherent confined environments. Resultantly, the ubiquitous ability of
mammalian amoeboid cells to migrate in two dimensions or three dimensions and
with or without adhesion can be explained for lymphocytes by a single machinery
of heterogeneous membrane treadmilling.

Copyright © 2020. Published by Elsevier Inc.

 

Auteurs Bordeaux Neurocampus