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Superresolution microscopy reveals a dynamic picture of cell polarity maintenance during directional growth

Polar (directional) cell growth, a key cellular mechanism shared among a wide range of species, relies on targeted insertion of new material at specific locations of the plasma membrane. How these cell polarity sites are stably maintained during massive membrane insertion has remained elusive. Conve...

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Autores principales: Ishitsuka, Yuji, Savage, Natasha, Li, Yiming, Bergs, Anna, Grün, Nathalie, Kohler, Daria, Donnelly, Rebecca, Nienhaus, G. Ulrich, Fischer, Reinhard, Takeshita, Norio
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Association for the Advancement of Science 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4673053/
https://www.ncbi.nlm.nih.gov/pubmed/26665168
http://dx.doi.org/10.1126/sciadv.1500947
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author Ishitsuka, Yuji
Savage, Natasha
Li, Yiming
Bergs, Anna
Grün, Nathalie
Kohler, Daria
Donnelly, Rebecca
Nienhaus, G. Ulrich
Fischer, Reinhard
Takeshita, Norio
author_facet Ishitsuka, Yuji
Savage, Natasha
Li, Yiming
Bergs, Anna
Grün, Nathalie
Kohler, Daria
Donnelly, Rebecca
Nienhaus, G. Ulrich
Fischer, Reinhard
Takeshita, Norio
author_sort Ishitsuka, Yuji
collection PubMed
description Polar (directional) cell growth, a key cellular mechanism shared among a wide range of species, relies on targeted insertion of new material at specific locations of the plasma membrane. How these cell polarity sites are stably maintained during massive membrane insertion has remained elusive. Conventional live-cell optical microscopy fails to visualize polarity site formation in the crowded cell membrane environment because of its limited resolution. We have used advanced live-cell imaging techniques to directly observe the localization, assembly, and disassembly processes of cell polarity sites with high spatiotemporal resolution in a rapidly growing filamentous fungus, Aspergillus nidulans. We show that the membrane-associated polarity site marker TeaR is transported on microtubules along with secretory vesicles and forms a protein cluster at that point of the apical membrane where the plus end of the microtubule touches. There, a small patch of membrane is added through exocytosis, and the TeaR cluster gets quickly dispersed over the membrane. There is an incessant disassembly and reassembly of polarity sites at the growth zone, and each new polarity site locus is slightly offset from preceding ones. On the basis of our imaging results and computational modeling, we propose a transient polarity model that explains how cell polarity is stably maintained during highly active directional growth.
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spelling pubmed-46730532015-12-10 Superresolution microscopy reveals a dynamic picture of cell polarity maintenance during directional growth Ishitsuka, Yuji Savage, Natasha Li, Yiming Bergs, Anna Grün, Nathalie Kohler, Daria Donnelly, Rebecca Nienhaus, G. Ulrich Fischer, Reinhard Takeshita, Norio Sci Adv Research Articles Polar (directional) cell growth, a key cellular mechanism shared among a wide range of species, relies on targeted insertion of new material at specific locations of the plasma membrane. How these cell polarity sites are stably maintained during massive membrane insertion has remained elusive. Conventional live-cell optical microscopy fails to visualize polarity site formation in the crowded cell membrane environment because of its limited resolution. We have used advanced live-cell imaging techniques to directly observe the localization, assembly, and disassembly processes of cell polarity sites with high spatiotemporal resolution in a rapidly growing filamentous fungus, Aspergillus nidulans. We show that the membrane-associated polarity site marker TeaR is transported on microtubules along with secretory vesicles and forms a protein cluster at that point of the apical membrane where the plus end of the microtubule touches. There, a small patch of membrane is added through exocytosis, and the TeaR cluster gets quickly dispersed over the membrane. There is an incessant disassembly and reassembly of polarity sites at the growth zone, and each new polarity site locus is slightly offset from preceding ones. On the basis of our imaging results and computational modeling, we propose a transient polarity model that explains how cell polarity is stably maintained during highly active directional growth. American Association for the Advancement of Science 2015-11-13 /pmc/articles/PMC4673053/ /pubmed/26665168 http://dx.doi.org/10.1126/sciadv.1500947 Text en Copyright © 2015, The Authors http://creativecommons.org/licenses/by-nc/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial license (http://creativecommons.org/licenses/by-nc/4.0/) , which permits use, distribution, and reproduction in any medium, so long as the resultant use is not for commercial advantage and provided the original work is properly cited.
spellingShingle Research Articles
Ishitsuka, Yuji
Savage, Natasha
Li, Yiming
Bergs, Anna
Grün, Nathalie
Kohler, Daria
Donnelly, Rebecca
Nienhaus, G. Ulrich
Fischer, Reinhard
Takeshita, Norio
Superresolution microscopy reveals a dynamic picture of cell polarity maintenance during directional growth
title Superresolution microscopy reveals a dynamic picture of cell polarity maintenance during directional growth
title_full Superresolution microscopy reveals a dynamic picture of cell polarity maintenance during directional growth
title_fullStr Superresolution microscopy reveals a dynamic picture of cell polarity maintenance during directional growth
title_full_unstemmed Superresolution microscopy reveals a dynamic picture of cell polarity maintenance during directional growth
title_short Superresolution microscopy reveals a dynamic picture of cell polarity maintenance during directional growth
title_sort superresolution microscopy reveals a dynamic picture of cell polarity maintenance during directional growth
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4673053/
https://www.ncbi.nlm.nih.gov/pubmed/26665168
http://dx.doi.org/10.1126/sciadv.1500947
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