Active Diffusion and Microtubule-Based Transport Oppose Myosin Forces to Position Organelles in Cells
ARTICLE Received 13 Nov 2015 | Accepted 3 May 2016 | Published 2 Jun 2016 DOI: 10.1038/ncomms11814 OPEN Active diffusion and microtubule-based transport oppose myosin forces to position organelles in cells Congping Lin1,2,*, Martin Schuster1,*, Sofia Cunha Guimaraes1,w, Peter Ashwin2, Michael Schrader1, Jeremy Metz1, Christian Hacker1, Sarah Jane Gurr1 & Gero Steinberg1 Even distribution of peroxisomes (POs) and lipid droplets (LDs) is critical to their role in lipid and reactive oxygen species homeostasis. How even distribution is achieved remains elusive, but diffusive motion and directed motility may play a role. Here we show that in the fungus Ustilago maydis B95% of POs and LDs undergo diffusive motions. These movements require ATP and involve bidirectional early endosome motility, indicating that microtubule-associated membrane trafficking enhances diffusion of organelles. When early endosome transport is abolished, POs and LDs drift slowly towards the growing cell end. This pole-ward drift is facilitated by anterograde delivery of secretory cargo to the cell tip by myosin-5. Modelling reveals that microtubule-based directed transport and active diffusion support distribution, mobility and mixing of POs. In mammalian COS-7 cells, microtubules and F-actin also counteract each other to distribute POs. This highlights the importance of opposing cytoskeletal forces in organelle positioning in eukaryotes. 1 School of Biosciences, University of Exeter, Stocker Road, Exeter EX4 4QD, UK. 2 Mathematics, University of Exeter, North Park Road, Exeter EX4 4QF, UK. * These authors contributed equally to this work. w Present address: Department of Biology, University of Aveiro, 3810-193 Aveiro, Portugal. Correspondence and requests for materials should be addressed to G.S.
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