Cargando…

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

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 N...

Descripción completa

Detalles Bibliográficos
Autores principales: Steinberg, Gero, Schuster, Martin, Theisen, Ulrike, Kilaru, Sreedhar, Forge, Andrew, Martin-Urdiroz, Magdalena
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Rockefeller University Press 2012
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3413351/
https://www.ncbi.nlm.nih.gov/pubmed/22851316
http://dx.doi.org/10.1083/jcb.201201087
_version_ 1782240047391571968
author Steinberg, Gero
Schuster, Martin
Theisen, Ulrike
Kilaru, Sreedhar
Forge, Andrew
Martin-Urdiroz, Magdalena
author_facet Steinberg, Gero
Schuster, Martin
Theisen, Ulrike
Kilaru, Sreedhar
Forge, Andrew
Martin-Urdiroz, Magdalena
author_sort Steinberg, Gero
collection PubMed
description 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.
format Online
Article
Text
id pubmed-3413351
institution National Center for Biotechnology Information
language English
publishDate 2012
publisher The Rockefeller University Press
record_format MEDLINE/PubMed
spelling pubmed-34133512013-02-06 Motor-driven motility of fungal nuclear pores organizes chromosomes and fosters nucleocytoplasmic transport Steinberg, Gero Schuster, Martin Theisen, Ulrike Kilaru, Sreedhar Forge, Andrew Martin-Urdiroz, Magdalena J Cell Biol Research Articles 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. The Rockefeller University Press 2012-08-06 /pmc/articles/PMC3413351/ /pubmed/22851316 http://dx.doi.org/10.1083/jcb.201201087 Text en © 2012 Steinberg et al. 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/).
spellingShingle Research Articles
Steinberg, Gero
Schuster, Martin
Theisen, Ulrike
Kilaru, Sreedhar
Forge, Andrew
Martin-Urdiroz, Magdalena
Motor-driven motility of fungal nuclear pores organizes chromosomes and fosters nucleocytoplasmic transport
title Motor-driven motility of fungal nuclear pores organizes chromosomes and fosters nucleocytoplasmic transport
title_full Motor-driven motility of fungal nuclear pores organizes chromosomes and fosters nucleocytoplasmic transport
title_fullStr Motor-driven motility of fungal nuclear pores organizes chromosomes and fosters nucleocytoplasmic transport
title_full_unstemmed Motor-driven motility of fungal nuclear pores organizes chromosomes and fosters nucleocytoplasmic transport
title_short Motor-driven motility of fungal nuclear pores organizes chromosomes and fosters nucleocytoplasmic transport
title_sort motor-driven motility of fungal nuclear pores organizes chromosomes and fosters nucleocytoplasmic transport
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3413351/
https://www.ncbi.nlm.nih.gov/pubmed/22851316
http://dx.doi.org/10.1083/jcb.201201087
work_keys_str_mv AT steinberggero motordrivenmotilityoffungalnuclearporesorganizeschromosomesandfostersnucleocytoplasmictransport
AT schustermartin motordrivenmotilityoffungalnuclearporesorganizeschromosomesandfostersnucleocytoplasmictransport
AT theisenulrike motordrivenmotilityoffungalnuclearporesorganizeschromosomesandfostersnucleocytoplasmictransport
AT kilarusreedhar motordrivenmotilityoffungalnuclearporesorganizeschromosomesandfostersnucleocytoplasmictransport
AT forgeandrew motordrivenmotilityoffungalnuclearporesorganizeschromosomesandfostersnucleocytoplasmictransport
AT martinurdirozmagdalena motordrivenmotilityoffungalnuclearporesorganizeschromosomesandfostersnucleocytoplasmictransport