Isoform-specific functions of Mud/NuMA mediate binucleation of Drosophila male accessory gland cells

BMC Developmental Biology

Takashi Adachi-Yamada²  Hideki Nakagoshi³  Ryunosuke Minami³  Takao Imano²  Akihiko Kokuryo²  Kiichiro Taniguchi¹ 

[1] Department of Life Science, Faculty of Science, Gakushuin University, Tokyo 171-8588, Japan;Department of Biology, Graduate School of Science, Kobe University, Kobe 657-8501, Japan;Graduate School of Natural Science and Technology, Okayama University, Okayama 700-8530, Japan

关键词: Mud;    Spindle orientation;    Cell rounding;    Central spindle;    Cytokinesis;    Binucleation;    Male accessory gland;    Drosophila;   

Others  :  1118599
DOI  :  10.1186/s12861-014-0046-5

 received in 2014-05-13, accepted in 2014-12-11,  发布年份 2014

【 摘 要 】

Background

In standard cell division, the cells undergo karyokinesis and then cytokinesis. Some cells, however, such as cardiomyocytes and hepatocytes, can produce binucleate cells by going through mitosis without cytokinesis. This cytokinesis skipping is thought to be due to the inhibition of cytokinesis machinery such as the central spindle or the contractile ring, but the mechanisms regulating it are unclear. We investigated them by characterizing the binucleation event during development of the Drosophila male accessory gland, in which all cells are binucleate.

Results

The accessory gland cells arrested the cell cycle at 50 hours after puparium formation (APF) and in the middle of the pupal stage stopped proliferating for 5 hours. They then restarted the cell cycle and at 55 hours APF entered the M-phase synchronously. At this stage, accessory gland cells binucleated by mitosis without cytokinesis. Binucleating cells displayed the standard karyokinesis progression but also showed unusual features such as a non-round shape, spindle orientation along the apico-basal axis, and poor assembly of the central spindle. Mud, a Drosophila homolog of NuMA, regulated the processes responsible for these three features, the classical isoform Mud^PBD and the two newly characterized isoforms Mud^L and Mud^S regulated them differently: Mud^L repressed cell rounding, Mud^PBD and Mud^S oriented the spindle along the apico-basal axis, and Mud^S and Mud^L repressed central spindle assembly. Importantly, overexpression of Mud^S induced binucleation even in standard proliferating cells such as those in imaginal discs.

Conclusions

We characterized the binucleation in the Drosophila male accessory gland and examined mechanisms that regulated unusual morphologies of binucleating cells. We demonstrated that Mud, a microtubule binding protein regulating spindle orientation, was involved in this binucleation. We suggest that atypical functions exerted by three structurally different isoforms of Mud regulate cell rounding, spindle orientation and central spindle assembly in binucleation. We also propose that Mud^S is a key regulator triggering cytokinesis skipping in binucleation processes.

【 授权许可】

   
2014 Taniguchi et al.; licensee BioMed Central.

【 图 表 】

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