scholarly journals A unicellular relative of animals generates an epithelium-like cell layer by actomyosin-dependent cellularization

2019 ◽  
Author(s):  
Omaya Dudin ◽  
Andrej Ondracka ◽  
Xavier Grau-Bové ◽  
Arthur A. B. Haraldsen ◽  
Atsushi Toyoda ◽  
...  

SummaryIn animals, cellularization of a coenocyte is a specialized form of cytokinesis that results in the formation of a polarized epithelium during early embryonic development. It is characterized by coordinated assembly of an actomyosin network, which drives inward membrane invaginations. However, whether coordinated cellularization driven by membrane invagination exists outside animals is not known. To that end, we investigate cellularization in the ichthyosporean Sphaeroforma arctica, a close unicellular relative of animals. We show that the process of cellularization involves coordinated inward plasma membrane invaginations dependent on an actomyosin network, and reveal the temporal order of its assembly. This leads to the formation of a polarized layer of cells resembling an epithelium. We show that this epithelium-like stage is associated with tightly regulated transcriptional activation of genes involved in cell adhesion. Hereby we demonstrate the presence of a selforganized, clonally-generated, polarized layer of cells in a unicellular relative of animals.

eLife ◽  
2019 ◽  
Vol 8 ◽  
Author(s):  
Omaya Dudin ◽  
Andrej Ondracka ◽  
Xavier Grau-Bové ◽  
Arthur AB Haraldsen ◽  
Atsushi Toyoda ◽  
...  

In animals, cellularization of a coenocyte is a specialized form of cytokinesis that results in the formation of a polarized epithelium during early embryonic development. It is characterized by coordinated assembly of an actomyosin network, which drives inward membrane invaginations. However, whether coordinated cellularization driven by membrane invagination exists outside animals is not known. To that end, we investigate cellularization in the ichthyosporean Sphaeroforma arctica, a close unicellular relative of animals. We show that the process of cellularization involves coordinated inward plasma membrane invaginations dependent on an actomyosin network and reveal the temporal order of its assembly. This leads to the formation of a polarized layer of cells resembling an epithelium. We show that this stage is associated with tightly regulated transcriptional activation of genes involved in cell adhesion. Hereby we demonstrate the presence of a self-organized, clonally-generated, polarized layer of cells in a unicellular relative of animals.


2000 ◽  
Vol 150 (4) ◽  
pp. 849-860 ◽  
Author(s):  
Thomas Lecuit ◽  
Eric Wieschaus

Cellularization of the Drosophila embryo is a specialized form of cytokinesis that results in the formation of a polarized epithelium. The mechanisms of membrane growth during cytokinesis are largely unknown. It is also unclear whether membrane growth and polarization represent distinct processes that occur simultaneously or whether growth of the membrane is involved in the emergence of polarity. Using a combination of surface labeling and particles tracking techniques, we monitored the dynamics of marked membrane regions during cellularization. We find that the major source of membrane is intracellular, rather than in the form of a plasma membrane reservoir. Depolymerization of microtubules inhibits the export of a newly synthesized transmembrane protein from the Golgi apparatus to the plasma membrane and simultaneously blocks membrane growth. Membrane insertion occurs in a defined sequence at specific sites, first apical, then apical–lateral. Diffusion of the membrane appears insufficient to compete with the massive local insertion of new membrane. We thus identify a tightly regulated scheme of polarized membrane insertion during cellularization. We propose that such a mechanism could participate in the progressive emergence of apical–basal polarity.


2012 ◽  
Vol 36 (2) ◽  
pp. 272 ◽  
Author(s):  
Jie TAN ◽  
Hui-ling SUN ◽  
Fei GAO ◽  
Jing-ping YAN ◽  
Ying-hui DONG ◽  
...  

2010 ◽  
Vol 34 (5) ◽  
pp. 777-785 ◽  
Author(s):  
Wei SONG ◽  
Jia-kun SONG ◽  
Chun-xin FAN ◽  
Tao ZHANG ◽  
Bin WANG

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