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Nat Cell Biol. 2017 Apr;19(4):399-406. doi: 10.1038/ncb3490. Epub 2017 Mar 13.

Endoplasmic-reticulum-mediated microtubule alignment governs cytoplasmic streaming.

Author information

1
Cell Architecture Laboratory, Structural Biology Center, National Institute of Genetics, Mishima 411-8540, Japan.
2
Department of Genetics, School of Life Science, SOKENDAI (The Graduate University for Advanced Studies), Mishima 411-8540, Japan.
3
Physicochimie Curie (Centre National de la Recherche Scientifique-UMR168, UPMC), Institut Curie, PSL Research University, Section de Recherche, Paris 75248, France.
4
Human Interface Laboratory, Department of Advanced Information Technology, Kyushu University, Fukuoka 819-0395, Japan.
5
Quantitative Mechanobiology Laboratory, Center for Frontier Research, National Institute of Genetics, Mishima 411-8540, Japan.
6
Cell Biology and Biophysics Unit, European Molecular Biology Laboratory, Heidelberg 69117, Germany.

Abstract

Cytoplasmic streaming refers to a collective movement of cytoplasm observed in many cell types. The mechanism of meiotic cytoplasmic streaming (MeiCS) in Caenorhabditis elegans zygotes is puzzling as the direction of the flow is not predefined by cell polarity and occasionally reverses. Here, we demonstrate that the endoplasmic reticulum (ER) network structure is required for the collective flow. Using a combination of RNAi, microscopy and image processing of C. elegans zygotes, we devise a theoretical model, which reproduces and predicts the emergence and reversal of the flow. We propose a positive-feedback mechanism, where a local flow generated along a microtubule is transmitted to neighbouring regions through the ER. This, in turn, aligns microtubules over a broader area to self-organize the collective flow. The proposed model could be applicable to various cytoplasmic streaming phenomena in the absence of predefined polarity. The increased mobility of cortical granules by MeiCS correlates with the efficient exocytosis of the granules to protect the zygotes from osmotic and mechanical stresses.

PMID:
28288129
DOI:
10.1038/ncb3490
[Indexed for MEDLINE]

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