Active cargo positioning in antiparallel transport networks

Mathieu Richard (1) , Carles Blanch-Mercader (1) , Hajer Ennomani (2) , Wenxiang Cao (3) , Enrique de La Cruz (3) , Jean-François Joanny (1, 4, 5) , Frank Jülicher (6, 7) , Laurent Blanchoin (2) , Pascal Martin (1)

1 PCC - Laboratoire Physico-Chimie Curie [Institut Curie]
2 CytoMorphoLab
3 Department of Molecular Biophysics and Biochemistry
4 ESPCI Paris - Ecole Superieure de Physique et de Chimie Industrielles de la Ville de Paris
5 Collège de France - Chaire Matière molle et biophysique
6 MPI-PKS - Max Planck Institute for the Physics of Complex Systems
7 TU Dresden - Technische Universität Dresden = Dresden University of Technology

Cytoskeletal filaments assemble into dense parallel, antiparallel, or disordered networks, providing a complex environment for active cargo transport and positioning by molecular motors. The interplay between the network architecture and intrinsic motor properties clearly affects transport properties but remains poorly understood. Here, by using surface micropatterns of actin polymerization, we investigate stochastic transport properties of colloidal beads in antiparallel networks of overlapping actin filaments. We found that 200-nm beads coated with myosin Va motors displayed directed movements toward positions where the net polarity of the actin network vanished, accumulating there. The bead distribution was dictated by the spatial profiles of local bead velocity and diffusion coefficient, indicating that a diffusion-drift process was at work. Remarkably, beads coated with heavy-mero-myosin II motors showed a similar behavior. However, although velocity gradients were steeper with myosin II, the much larger bead diffusion observed with this motor resulted in less precise positioning. Our observations are well described by a 3-state model, in which active beads locally sense the net polarity of the network by frequently detaching from and reattaching to the filaments. A stochastic sequence of processive runs and diffusive searches results in a biased random walk. The precision of bead positioning is set by the gradient of net actin polarity in the network and by the run length of the cargo in an attached state. Our results unveiled physical rules for cargo transport and positioning in networks of mixed polarity.

Mots clés: stochastic processes; myosin; actin cytoskeleton; diffusion-drift process; intracellular transport

Domaines: Biologie cellulaire; Biophysique

Mathieu Richard, Carles Blanch-Mercader, Hajer Ennomani, Wenxiang Cao, Enrique de La Cruz, et al.. Active cargo positioning in antiparallel transport networks. Proceedings of the National Academy of Sciences of the United States of America, 2019, 116 (30), pp.14835-14842. ⟨10.1073/pnas.1900416116⟩. ⟨hal-02185109⟩