The spindle pole bodies facilitate nuclear envelope division during closed mitosis in fission yeast.
Many organisms divide chromosomes within the confines of the nuclear envelope (NE) in a process known as closed mitosis. Thus, they must ensure coordination between segregation of the genetic material and division of the NE itself. Although many years of work have led to a reasonably clear understanding of mitotic spindle function in chromosome segregation, the NE division mechanism remains obscure. Here, we show that fission yeast cells overexpressing the transforming acid coiled coil (TACC)-related protein, Mia1p/Alp7p, failed to separate the spindle pole bodies (SPBs) at the onset of mitosis, but could assemble acentrosomal bipolar and antiparallel spindle structures. Most of these cells arrested in anaphase with fully extended spindles and nonsegregated chromosomes. Spindle poles that lacked the SPBs did not lead the division of the NE during spindle elongation, but deformed it, trapping the chromosomes within. When the SPBs were severed by laser microsurgery in wild-type cells, we observed analogous deformations of the NE by elongating spindle remnants, resulting in NE division failure. Analysis of dis1Delta cells that elongate spindles despite unattached kinetochores indicated that the SPBs were required for maintaining nuclear shape at anaphase onset. Strikingly, when the NE was disassembled by utilizing a temperature-sensitive allele of the Ran GEF, Pim1p, the abnormal spindles induced by Mia1p overexpression were capable of segregating sister chromatids to daughter cells, suggesting that the failure to divide the NE prevents chromosome partitioning. Our results imply that the SPBs preclude deformation of the NE during spindle elongation and thus serve as specialized structures enabling nuclear division during closed mitosis in fission yeast.
Zheng
Liling
L
Cell Dynamics Group, Temasek Life Sciences Laboratory, Singapore.
Schwartz
Cindi
C
Magidson
Valentin
V
Khodjakov
Alexey
A
Oliferenko
Snezhana
S
D048750:Cell Nucleus Division / Q000235:genetics / Q000502:physiology*; D015825:Chromosomes, Fungal / Q000235:genetics; D005800:Genes, Fungal; D046529:Microscopy, Electron, Transmission; D008869:Microtubule-Associated Proteins / Q000235:genetics / Q000502:physiology; D008938:Mitosis / Q000235:genetics / Q000502:physiology*; D009154:Mutation; D009685:Nuclear Envelope / Q000235:genetics / Q000502:physiology*; D012568:Schizosaccharomyces / Q000166:cytology* / Q000235:genetics / Q000502:physiology*; D029702:Schizosaccharomyces pombe Proteins / Q000235:genetics / Q000502:physiology; D008941:Spindle Apparatus / Q000235:genetics / Q000502:physiology* / Q000648:ultrastructure
C479626:Alp7 protein, S pombe; C502827:Ase1 protein, S pombe; D008869:Microtubule-Associated Proteins; D029702:Schizosaccharomyces pombe Proteins; C094879:dis1 protein, S pombe