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


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Article Info

DATE

2014-12-20

AUTHORS

Kiichiro Taniguchi, Akihiko Kokuryo, Takao Imano, Ryunosuke Minami, Hideki Nakagoshi, Takashi Adachi-Yamada

ABSTRACT

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. More... »

PAGES

46

Identifiers

URI

http://scigraph.springernature.com/pub.10.1186/s12861-014-0046-5

DOI

http://dx.doi.org/10.1186/s12861-014-0046-5

DIMENSIONS

https://app.dimensions.ai/details/publication/pub.1022792293

PUBMED

https://www.ncbi.nlm.nih.gov/pubmed/25527079


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66 classical isoforms
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74 disk
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76 events
77 features
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80 gland
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82 hepatocytes
83 homolog
84 hours
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86 imaginal discs
87 inhibition
88 isoform-specific functions
89 isoforms
90 karyokinesis
91 karyokinesis progression
92 key regulator
93 machinery
94 male accessory gland cells
95 male accessory glands
96 mechanism
97 mediate binucleation
98 middle
99 mitosis
100 morphology
101 mud
102 non-round shape
103 orientation
104 overexpression
105 phase
106 poor assembly
107 process
108 progression
109 protein
110 pupal stage
111 puparium formation
112 regulator
113 ring
114 rounding
115 shape
116 skipping
117 spindle
118 spindle assembly
119 spindle orientation
120 stage
121 standard cell division
122 standard karyokinesis progression
123 unusual features
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