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Cell Cycle-Dependent Dynamics of the Golgi-Centrosome Association in Motile Cells

Here, we characterize spatial distribution of the Golgi complex in human cells. In contrast to the prevailing view that the Golgi compactly surrounds the centrosome throughout interphase, we observe characteristic differences in the morphology of Golgi ribbons and their association with the centroso...

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Autores principales: Frye, Keyada, Renda, Fioranna, Fomicheva, Maria, Zhu, Xiaodong, Gong, Lisa, Khodjakov, Alexey, Kaverina, Irina
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7290758/
https://www.ncbi.nlm.nih.gov/pubmed/32344866
http://dx.doi.org/10.3390/cells9051069
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author Frye, Keyada
Renda, Fioranna
Fomicheva, Maria
Zhu, Xiaodong
Gong, Lisa
Khodjakov, Alexey
Kaverina, Irina
author_facet Frye, Keyada
Renda, Fioranna
Fomicheva, Maria
Zhu, Xiaodong
Gong, Lisa
Khodjakov, Alexey
Kaverina, Irina
author_sort Frye, Keyada
collection PubMed
description Here, we characterize spatial distribution of the Golgi complex in human cells. In contrast to the prevailing view that the Golgi compactly surrounds the centrosome throughout interphase, we observe characteristic differences in the morphology of Golgi ribbons and their association with the centrosome during various periods of the cell cycle. The compact Golgi complex is typical in G1; during S-phase, Golgi ribbons lose their association with the centrosome and extend along the nuclear envelope to largely encircle the nucleus in G2. Interestingly, pre-mitotic separation of duplicated centrosomes always occurs after dissociation from the Golgi. Shortly before the nuclear envelope breakdown, scattered Golgi ribbons reassociate with the separated centrosomes restoring two compact Golgi complexes. Transitions between the compact and distributed Golgi morphologies are microtubule-dependent. However, they occur even in the absence of centrosomes, which implies that Golgi reorganization is not driven by the centrosomal microtubule asters. Cells with different Golgi morphology exhibit distinct differences in the directional persistence and velocity of migration. These data suggest that changes in the radial distribution of the Golgi around the nucleus define the extent of cell polarization and regulate cell motility in a cell cycle-dependent manner.
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spelling pubmed-72907582020-06-17 Cell Cycle-Dependent Dynamics of the Golgi-Centrosome Association in Motile Cells Frye, Keyada Renda, Fioranna Fomicheva, Maria Zhu, Xiaodong Gong, Lisa Khodjakov, Alexey Kaverina, Irina Cells Article Here, we characterize spatial distribution of the Golgi complex in human cells. In contrast to the prevailing view that the Golgi compactly surrounds the centrosome throughout interphase, we observe characteristic differences in the morphology of Golgi ribbons and their association with the centrosome during various periods of the cell cycle. The compact Golgi complex is typical in G1; during S-phase, Golgi ribbons lose their association with the centrosome and extend along the nuclear envelope to largely encircle the nucleus in G2. Interestingly, pre-mitotic separation of duplicated centrosomes always occurs after dissociation from the Golgi. Shortly before the nuclear envelope breakdown, scattered Golgi ribbons reassociate with the separated centrosomes restoring two compact Golgi complexes. Transitions between the compact and distributed Golgi morphologies are microtubule-dependent. However, they occur even in the absence of centrosomes, which implies that Golgi reorganization is not driven by the centrosomal microtubule asters. Cells with different Golgi morphology exhibit distinct differences in the directional persistence and velocity of migration. These data suggest that changes in the radial distribution of the Golgi around the nucleus define the extent of cell polarization and regulate cell motility in a cell cycle-dependent manner. MDPI 2020-04-25 /pmc/articles/PMC7290758/ /pubmed/32344866 http://dx.doi.org/10.3390/cells9051069 Text en © 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Frye, Keyada
Renda, Fioranna
Fomicheva, Maria
Zhu, Xiaodong
Gong, Lisa
Khodjakov, Alexey
Kaverina, Irina
Cell Cycle-Dependent Dynamics of the Golgi-Centrosome Association in Motile Cells
title Cell Cycle-Dependent Dynamics of the Golgi-Centrosome Association in Motile Cells
title_full Cell Cycle-Dependent Dynamics of the Golgi-Centrosome Association in Motile Cells
title_fullStr Cell Cycle-Dependent Dynamics of the Golgi-Centrosome Association in Motile Cells
title_full_unstemmed Cell Cycle-Dependent Dynamics of the Golgi-Centrosome Association in Motile Cells
title_short Cell Cycle-Dependent Dynamics of the Golgi-Centrosome Association in Motile Cells
title_sort cell cycle-dependent dynamics of the golgi-centrosome association in motile cells
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7290758/
https://www.ncbi.nlm.nih.gov/pubmed/32344866
http://dx.doi.org/10.3390/cells9051069
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