Early endosome motility spatially organizes polysome distribution.
Early endosomes (EEs) mediate protein sorting, and their cytoskeleton-dependent motility supports long-distance signaling in neurons. Here, we report an unexpected role of EE motility in distributing the translation machinery in a fungal model system. We visualize ribosomal subunit proteins and show that the large subunits diffused slowly throughout the cytoplasm (Dc,60S = 0.311 µm(2)/s), whereas entire polysomes underwent long-range motility along microtubules. This movement was mediated by "hitchhiking" on kinesin-3 and dynein-driven EEs, where the polysomes appeared to translate EE-associated mRNA into proteins. Modeling indicates that this motor-driven transport is required for even cellular distribution of newly formed ribosomes. Indeed, impaired EE motility in motor mutants, or their inability to bind EEs in mutants lacking the RNA-binding protein Rrm4, reduced ribosome transport and induced ribosome aggregation near the nucleus. As a consequence, cell growth was severely restricted. Collectively, our results indicate that polysomes associate with moving EEs and that "off- and reloading" distributes the protein translation machinery.
Biosciences and 2 Mathematics Research Institute, University of Exeter, Exeter EX4 4QD, England, UK.
Yujiro
Y
Higuchi
Peter
P
Ashwin
Yvonne
Y
Roger
Gero
G
Steinberg
D001693:Biological Transport, Active / Q000187:drug effects; D004058:Diffusion / Q000187:drug effects; D004398:Dyneins / Q000378:metabolism; D011992:Endosomes / Q000187:drug effects / Q000378:metabolism* / Q000648:ultrastructure; D005656:Fungal Proteins / Q000378:metabolism; D049452:Green Fluorescent Proteins / Q000378:metabolism; D025301:Hyphae / Q000378:metabolism / Q000648:ultrastructure; D016547:Kinesins / Q000378:metabolism; D008870:Microtubules / Q000187:drug effects / Q000378:metabolism; D008954:Models, Biological; D009154:Mutation / Q000235:genetics; D011132:Polyribosomes / Q000187:drug effects / Q000378:metabolism* / Q000648:ultrastructure; D011500:Protein Synthesis Inhibitors / Q000494:pharmacology; D021381:Protein Transport / Q000187:drug effects; D016601:RNA-Binding Proteins / Q000378:metabolism; D013312:Stress, Physiological / Q000187:drug effects; D014588:Ustilago / Q000166:cytology / Q000187:drug effects / Q000378:metabolism*
D005656:Fungal Proteins; D011500:Protein Synthesis Inhibitors; D016601:RNA-Binding Proteins; D049452:Green Fluorescent Proteins; D004398:Dyneins; D016547:Kinesins