Regulation of the Total Cell Surface Area in Dividing Dictyostelium Cells

When a cell divides into two daughter cells, the total cell surface area should increase. There are two models for membrane supply to support cell division: (1) unfolding of small surface membrane reservoirs such as microvilli or wrinkles and (2) exocytosis of intracellular vesicles. Here, we precis...

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Main Authors: Masahito Tanaka, Koushiro Fujimoto, Shigehiko Yumura
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-04-01
Series:Frontiers in Cell and Developmental Biology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fcell.2020.00238/full
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author Masahito Tanaka
Koushiro Fujimoto
Shigehiko Yumura
author_facet Masahito Tanaka
Koushiro Fujimoto
Shigehiko Yumura
author_sort Masahito Tanaka
collection DOAJ
description When a cell divides into two daughter cells, the total cell surface area should increase. There are two models for membrane supply to support cell division: (1) unfolding of small surface membrane reservoirs such as microvilli or wrinkles and (2) exocytosis of intracellular vesicles. Here, we precisely measured the total cell surface area in dividing Dictyostelium cells, flattened by the agar overlay that eliminated the complexity of unfolding surface membrane reservoirs. Because the cells divided normally under the agar overlay, unfolding of surface membrane reservoirs was not required for cell division. Under the agar overlay, the total cell surface area slightly decreased from the interphase to the metaphase and then increased about 20% during cytokinesis. Both endocytosis and exocytosis were suppressed in the early mitotic phase but recovered during cytokinesis. The imbalance of endocytosis and exocytosis could contribute to the changes observed in the cell surface area. Clathrin-dependent endocytosis was also substantially suppressed during cytokinesis, but contrary to previous reports in cultured animal cells, it did not significantly contribute to the regulation of the cell surface area. Furrowing during cytokinesis was indispensable for the cell membrane increase, and vice versa.
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spelling doaj.art-42d7239d1ffc4df6bf3c77af98c7132c2022-12-22T01:31:07ZengFrontiers Media S.A.Frontiers in Cell and Developmental Biology2296-634X2020-04-01810.3389/fcell.2020.00238527391Regulation of the Total Cell Surface Area in Dividing Dictyostelium CellsMasahito TanakaKoushiro FujimotoShigehiko YumuraWhen a cell divides into two daughter cells, the total cell surface area should increase. There are two models for membrane supply to support cell division: (1) unfolding of small surface membrane reservoirs such as microvilli or wrinkles and (2) exocytosis of intracellular vesicles. Here, we precisely measured the total cell surface area in dividing Dictyostelium cells, flattened by the agar overlay that eliminated the complexity of unfolding surface membrane reservoirs. Because the cells divided normally under the agar overlay, unfolding of surface membrane reservoirs was not required for cell division. Under the agar overlay, the total cell surface area slightly decreased from the interphase to the metaphase and then increased about 20% during cytokinesis. Both endocytosis and exocytosis were suppressed in the early mitotic phase but recovered during cytokinesis. The imbalance of endocytosis and exocytosis could contribute to the changes observed in the cell surface area. Clathrin-dependent endocytosis was also substantially suppressed during cytokinesis, but contrary to previous reports in cultured animal cells, it did not significantly contribute to the regulation of the cell surface area. Furrowing during cytokinesis was indispensable for the cell membrane increase, and vice versa.https://www.frontiersin.org/article/10.3389/fcell.2020.00238/fullcell divisioncell membranecytokinesisendocytosisexocytosis
spellingShingle Masahito Tanaka
Koushiro Fujimoto
Shigehiko Yumura
Regulation of the Total Cell Surface Area in Dividing Dictyostelium Cells
Frontiers in Cell and Developmental Biology
cell division
cell membrane
cytokinesis
endocytosis
exocytosis
title Regulation of the Total Cell Surface Area in Dividing Dictyostelium Cells
title_full Regulation of the Total Cell Surface Area in Dividing Dictyostelium Cells
title_fullStr Regulation of the Total Cell Surface Area in Dividing Dictyostelium Cells
title_full_unstemmed Regulation of the Total Cell Surface Area in Dividing Dictyostelium Cells
title_short Regulation of the Total Cell Surface Area in Dividing Dictyostelium Cells
title_sort regulation of the total cell surface area in dividing dictyostelium cells
topic cell division
cell membrane
cytokinesis
endocytosis
exocytosis
url https://www.frontiersin.org/article/10.3389/fcell.2020.00238/full
work_keys_str_mv AT masahitotanaka regulationofthetotalcellsurfaceareaindividingdictyosteliumcells
AT koushirofujimoto regulationofthetotalcellsurfaceareaindividingdictyosteliumcells
AT shigehikoyumura regulationofthetotalcellsurfaceareaindividingdictyosteliumcells