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Motor-driven motility of fungal nuclear pores organizes chromosomes and fosters nucleocytoplasmic transport

Steinberg, G; Schuster, M; Theisen, U; Kilaru, S; Forge, A; Martin-Urdiroz, M; (2012) Motor-driven motility of fungal nuclear pores organizes chromosomes and fosters nucleocytoplasmic transport. Journal of Cell Biology , 198 (3) 343 - 355. 10.1083/jcb.201201087. Green open access

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[thumbnail of Video 1. Motility of nuclear pores in U. maydis.] QuickTime Movie (Video 1. Motility of nuclear pores in U. maydis.)
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[thumbnail of Video 2. Directed motility of nuclear pores in U. maydis.] QuickTime Movie (Video 2. Directed motility of nuclear pores in U. maydis.)
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[thumbnail of Video 3. Directed motility of nuclear pores into the cytoplasm in U. maydis.] QuickTime Movie (Video 3. Directed motility of nuclear pores into the cytoplasm in U. maydis.)
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[thumbnail of Video 4. Formation of nuclear extensions by directed motility of nuclear pores in U. maydis.] QuickTime Movie (Video 4. Formation of nuclear extensions by directed motility of nuclear pores in U. maydis.)
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[thumbnail of Video 5. Directed motility of NPCs in S. cerevisiae.] QuickTime Movie (Video 5. Directed motility of NPCs in S. cerevisiae.)
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[thumbnail of Video 6. Directed motility of groups of nuclear pores in A. nidulans. ] QuickTime Movie (Video 6. Directed motility of groups of nuclear pores in A. nidulans. )
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[thumbnail of Video 7. Motility of nuclear pores along microtubules.] QuickTime Movie (Video 7. Motility of nuclear pores along microtubules.)
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[thumbnail of Video 8. Colocalization of dynein (green, Dyn2) and NPCs (red, Nup107).] QuickTime Movie (Video 8. Colocalization of dynein (green, Dyn2) and NPCs (red, Nup107).)
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[thumbnail of Video 9. Motility of chromosomes in U. maydis.] QuickTime Movie (Video 9. Motility of chromosomes in U. maydis.)
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[thumbnail of Video 10. Motility of NPCs and chromosomes in U. maydis.] QuickTime Movie (Video 10. Motility of NPCs and chromosomes in U. maydis.)
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Abstract

Exchange between the nucleus and the cytoplasm is controlled by nuclear pore complexes (NPCs). In animals, NPCs are anchored by the nuclear lamina, which ensures their even distribution and proper organization of chromosomes. Fungi do not possess a lamina and how they arrange their chromosomes and NPCs is unknown. Here, we show that motor-driven motility of NPCs organizes the fungal nucleus. In Ustilago maydis, Aspergillus nidulans, and Saccharomyces cerevisiae fluorescently labeled NPCs showed ATP-dependent movements at ~1.0 µm/s. In S. cerevisiae and U. maydis, NPC motility prevented NPCs from clustering. In budding yeast, NPC motility required F-actin, whereas in U. maydis, microtubules, kinesin-1, and dynein drove pore movements. In the latter, pore clustering resulted in chromatin organization defects and led to a significant reduction in both import and export of GFP reporter proteins. This suggests that fungi constantly rearrange their NPCs and corresponding chromosomes to ensure efficient nuclear transport and thereby overcome the need for a structural lamina.

Type: Article
Title: Motor-driven motility of fungal nuclear pores organizes chromosomes and fosters nucleocytoplasmic transport
Location: United States
Open access status: An open access version is available from UCL Discovery
DOI: 10.1083/jcb.201201087
Publisher version: http://dx.doi.org/10.1083/jcb.201201087
Language: English
Additional information: This article is distributed under the terms of an Attribution–Noncommercial–Share Alike–No Mirror Sites license for the first six months after the publication date (see http://www.rupress.org/terms). After six months it is available under a Creative Commons License (Attribution–Noncommercial–Share Alike 3.0 Unported license, as described at http://creativecommons.org/licenses/by-nc-sa/3.0/). PMCID: PMC3413351
Keywords: Actins, Active transport, Cell nucleus, Adenosine triphosphate, Aspergillus nidulans, Chromatin, Chromosomes, Fluorescent dyes, Fungi, Genes, Reporter, Green fluorescent Proteins, Kinesin, Light, Microscopy, Fluorescence, Microtubules, Nuclear lamina, Nuclear pore, Photochemistry, Plasmids, Saccharomyces cerevisiae, Ustilago
UCL classification: UCL
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Brain Sciences
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Brain Sciences > The Ear Institute
URI: https://discovery-pp.ucl.ac.uk/id/eprint/1362653
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