The spindle position checkpoint: how to deal with spindle misalignment during asymmetric cell division in budding yeast

2008 ◽  
Vol 36 (3) ◽  
pp. 416-420 ◽  
Author(s):  
Roberta Fraschini ◽  
Marianna Venturetti ◽  
Elena Chiroli ◽  
Simonetta Piatti
Keyword(s):  
Cell Division ◽  
Genome Stability ◽  
Asymmetric Cell Division ◽  
Budding Yeast ◽  
Spindle Positioning ◽  
Bud Neck ◽  
Mother And Daughter ◽  
Division Spindle ◽  
Division Axis ◽  
Spindle Position

During asymmetric cell division, spindle positioning is critical to ensure the unequal segregation of polarity factors and generate daughter cells with different sizes or fates. In budding yeast the boundary between mother and daughter cell resides at the bud neck, where cytokinesis takes place at the end of the cell cycle. Since budding and bud neck formation occur much earlier than bipolar spindle formation, spindle positioning is a finely regulated process. A surveillance device called the SPOC (spindle position checkpoint) oversees this process and delays mitotic exit and cytokinesis until the spindle is properly oriented along the division axis, thus ensuring genome stability.

The mother-bud neck as a signaling platform for the coordination between spindle position and cytokinesis in budding yeast

2011 ◽  
Vol 392 (8-9) ◽  
pp. 805-812 ◽  
Author(s):  
Laura Merlini ◽  
Simonetta Piatti
Keyword(s):  
Genome Stability ◽  
Asymmetric Cell Division ◽  
Budding Yeast ◽  
Cytoskeletal Proteins ◽  
Spindle Positioning ◽  
Bud Neck ◽  
Mother And Daughter ◽  
Associated Proteins ◽  
Division Axis ◽  
Spindle Position

Abstract During asymmetric cell division, spindle positioning is critical for ensuring the unequal inheritance of polarity factors. In budding yeast, the mother-bud neck determines the cleavage plane and a correct nuclear division between mother and daughter cell requires orientation of the mitotic spindle along the mother-bud axis. A surveillance device called the spindle position/orientation checkpoint (SPOC) oversees this process and delays mitotic exit and cytokinesis until the spindle is properly oriented along the division axis, thus ensuring genome stability. Cytoskeletal proteins called septins form a ring at the bud neck that is essential for cytokinesis. Furthermore, septins and septin-associated proteins are implicated in spindle positioning and SPOC. In this review, we discuss the emerging connections between septins and the SPOC and the role of the mother-bud neck as a signaling platform to couple proper chromosome segregation to cytokinesis.

scholarly journals Mitotic Spindle Positioning in Saccharomyces cerevisiae Is Accomplished by Antagonistically Acting Microtubule Motor Proteins

1997 ◽  
Vol 138 (5) ◽  
pp. 1041-1053 ◽  
Author(s):  
Frank R. Cottingham ◽  
M. Andrew Hoyt
Keyword(s):  
Saccharomyces Cerevisiae ◽  
Cell Division ◽  
Mitotic Spindle ◽  
Asymmetric Cell Division ◽  
Wild Type ◽  
Yeast Saccharomyces Cerevisiae ◽  
Spindle Positioning ◽  
Dynein Motor ◽  
Bud Neck ◽  
Microtubule Motor

Proper positioning of the mitotic spindle is often essential for cell division and differentiation processes. The asymmetric cell division characteristic of budding yeast, Saccharomyces cerevisiae, requires that the spindle be positioned at the mother–bud neck and oriented along the mother–bud axis. The single dynein motor encoded by the S. cerevisiae genome performs an important but nonessential spindle-positioning role. We demonstrate that kinesin-related Kip3p makes a major contribution to spindle positioning in the absence of dynein. The elimination of Kip3p function in dyn1Δ cells severely compromised spindle movement to the mother–bud neck. In dyn1Δ cells that had completed positioning, elimination of Kip3p function caused spindles to mislocalize to distal positions in mother cell bodies. We also demonstrate that the spindle-positioning defects exhibited by dyn1 kip3 cells are caused, to a large extent, by the actions of kinesin- related Kip2p. Microtubules in kip2Δ cells were shorter and more sensitive to benomyl than wild-type, in contrast to the longer and benomyl-resistant microtubules found in dyn1Δ and kip3Δ cells. Most significantly, the deletion of KIP2 greatly suppressed the spindle localization defect and slow growth exhibited by dyn1 kip3 cells. Likewise, induced expression of KIP2 caused spindles to mislocalize in cells deficient for dynein and Kip3p. Our findings indicate that Kip2p participates in normal spindle positioning but antagonizes a positioning mechanism acting in dyn1 kip3 cells. The observation that deletion of KIP2 could also suppress the inviability of dyn1Δ kar3Δ cells suggests that kinesin-related Kar3p also contributes to spindle positioning.

scholarly journals Spindle position dictates division site during asymmetric cell division in moss

2020 ◽  
Author(s):  
Elena Kozgunova ◽  
Mari W. Yoshida ◽  
Gohta Goshima
Keyword(s):  
Cell Division ◽  
Mitotic Spindle ◽  
Actin Filaments ◽  
Asymmetric Cell Division ◽  
Physcomitrella Patens ◽  
Plant Cells ◽  
Spindle Positioning ◽  
Division Site ◽  
Multicellular Organisms ◽  
Spindle Position

AbstractAsymmetric cell division (ACD) underlies the development of multicellular organisms. The division site in plant cells is predetermined prior to mitosis and the localization of the mitotic spindle is considered static, unlike in animal ACD, where the cell division site is defined by active spindle-positioning mechanisms. Here, we isolated a novel mutant of the microtubule-associated protein TPX2 in the moss Physcomitrella patens and observed abnormal spindle motility, which led to inverted asymmetric division during organ development. This phenotype was rescued by restoring endogenous TPX2 function and, unexpectedly, by depolymerizing actin filaments. Thus, we identify an active spindle-positioning mechanism involving microtubules and actin filaments that sets the division site in plants, which is reminiscent of the acentrosomal ACD in animals, and suggests the existence of a common ancestral mechanism.

scholarly journals Spindle-independent condensation-mediated segregation of yeast ribosomal DNA in late anaphase

2005 ◽  
Vol 168 (2) ◽  
pp. 209-219 ◽  
Author(s):  
Félix Machín ◽  
Jordi Torres-Rosell ◽  
Adam Jarmuz ◽  
Luis Aragón
Keyword(s):  
Cell Division ◽  
Ribosomal Dna ◽  
Budding Yeast ◽  
Mitotic Cell ◽  
Yeast Genome ◽  
Daughter Cells ◽  
Late Anaphase ◽  
Mother And Daughter ◽  
The Right ◽  
Chromosome Resolution

Mitotic cell division involves the equal segregation of all chromosomes during anaphase. The presence of ribosomal DNA (rDNA) repeats on the right arm of chromosome XII makes it the longest in the budding yeast genome. Previously, we identified a stage during yeast anaphase when rDNA is stretched across the mother and daughter cells. Here, we show that resolution of sister rDNAs is achieved by unzipping of the locus from its centromere-proximal to centromere-distal regions. We then demonstrate that during this stretched stage sister rDNA arrays are neither compacted nor segregated despite being largely resolved from each other. Surprisingly, we find that rDNA segregation after this period no longer requires spindles but instead involves Cdc14-dependent rDNA axial compaction. These results demonstrate that chromosome resolution is not simply a consequence of compacting chromosome arms and that overall rDNA compaction is necessary to mediate the segregation of the long arm of chromosome XII.

scholarly journals Budding Yeast Dma Proteins Control Septin Dynamics and the Spindle Position Checkpoint by Promoting the Recruitment of the Elm1 Kinase to the Bud Neck

PLoS Genetics ◽  
2012 ◽  
Vol 8 (4) ◽  
pp. e1002670 ◽  
Author(s):  
Laura Merlini ◽  
Roberta Fraschini ◽  
Barbara Boettcher ◽  
Yves Barral ◽  
Giovanna Lucchini ◽  
...  
Keyword(s):  
Budding Yeast ◽  
Bud Neck ◽  
Spindle Position

scholarly journals Cytoplasmic MTOCs control spindle orientation for asymmetric cell division in plants

2017 ◽  
Vol 114 (42) ◽  
pp. E8847-E8854 ◽  
Author(s):  
Ken Kosetsu ◽  
Takashi Murata ◽  
Moé Yamada ◽  
Momoko Nishina ◽  
Joanna Boruc ◽  
...  
Keyword(s):  
Cell Division ◽  
Asymmetric Cell Division ◽  
Physcomitrella Patens ◽  
De Novo ◽  
Critical Role ◽  
Fine Tuning ◽  
Spindle Orientation ◽  
Mitotic Apparatus ◽  
Division Plane ◽  
Division Axis

Proper orientation of the cell division axis is critical for asymmetric cell divisions that underpin cell differentiation. In animals, centrosomes are the dominant microtubule organizing centers (MTOC) and play a pivotal role in axis determination by orienting the mitotic spindle. In land plants that lack centrosomes, a critical role of a microtubular ring structure, the preprophase band (PPB), has been observed in this process; the PPB is required for orienting (before prophase) and guiding (in telophase) the mitotic apparatus. However, plants must possess additional mechanisms to control the division axis, as certain cell types or mutants do not form PPBs. Here, using live imaging of the gametophore of the moss Physcomitrella patens, we identified acentrosomal MTOCs, which we termed “gametosomes,” appearing de novo and transiently in the prophase cytoplasm independent of PPB formation. We show that gametosomes are dispensable for spindle formation but required for metaphase spindle orientation. In some cells, gametosomes appeared reminiscent of the bipolar MT “polar cap” structure that forms transiently around the prophase nucleus in angiosperms. Specific disruption of the polar caps in tobacco cells misoriented the metaphase spindles and frequently altered the final division plane, indicating that they are functionally analogous to the gametosomes. These results suggest a broad use of transient MTOC structures as the spindle orientation machinery in plants, compensating for the evolutionary loss of centrosomes, to secure the initial orientation of the spindle in a spatial window that allows subsequent fine-tuning of the division plane axis by the guidance machinery.

scholarly journals Elm1 kinase activates the spindle position checkpoint kinase Kin4

2010 ◽  
Vol 190 (6) ◽  
pp. 975-989 ◽  
Author(s):  
Ayse Koca Caydasi ◽  
Bahtiyar Kurtulmus ◽  
Maria I.L. Orrico ◽  
Astrid Hofmann ◽  
Bashar Ibrahim ◽  
...  
Keyword(s):  
Cell Cycle ◽  
Cell Cycle Progression ◽  
Kinase Activity ◽  
Asymmetric Cell Division ◽  
Cycle Progression ◽  
Spindle Positioning ◽  
Surveillance Mechanism ◽  
Spindle Position ◽  
Conserved Residue

Budding yeast asymmetric cell division relies upon the precise coordination of spindle orientation and cell cycle progression. The spindle position checkpoint (SPOC) is a surveillance mechanism that prevents cells with misoriented spindles from exiting mitosis. The cortical kinase Kin4 acts near the top of this network. How Kin4 kinase activity is regulated and maintained in respect to spindle positional cues remains to be established. Here, we show that the bud neck–associated kinase Elm1 participates in Kin4 activation and SPOC signaling by phosphorylating a conserved residue within the activation loop of Kin4. Blocking Elm1 function abolishes Kin4 kinase activity in vivo and eliminates the SPOC response to spindle misalignment. These findings establish a novel function for Elm1 in the coordination of spindle positioning with cell cycle progression via its control of Kin4.

scholarly journals Functional Characterization of Dma1 and Dma2, the Budding Yeast Homologues of Schizosaccharomyces pombe Dma1 and Human Chfr

2004 ◽  
Vol 15 (8) ◽  
pp. 3796-3810 ◽  
Author(s):  
Roberta Fraschini ◽  
Denis Bilotta ◽  
Giovanna Lucchini ◽  
Simonetta Piatti
Keyword(s):  
Schizosaccharomyces Pombe ◽  
Budding Yeast ◽  
Functional Characterization ◽  
Ectopic Expression ◽  
Mitotic Exit ◽  
Spindle Positioning ◽  
Septin Ring ◽  
Daughter Cells ◽  
Spindle Position

Proper transmission of genetic information requires correct assembly and positioning of the mitotic spindle, responsible for driving each set of sister chromatids to the two daughter cells, followed by cytokinesis. In case of altered spindle orientation, the spindle position checkpoint inhibits Tem1-dependent activation of the mitotic exit network (MEN), thus delaying mitotic exit and cytokinesis until errors are corrected. We report a functional analysis of two previously uncharacterized budding yeast proteins, Dma1 and Dma2, 58% identical to each other and homologous to human Chfr and Schizosaccharomyces pombe Dma1, both of which have been previously implicated in mitotic checkpoints. We show that Dma1 and Dma2 are involved in proper spindle positioning, likely regulating septin ring deposition at the bud neck. DMA2 overexpression causes defects in septin ring disassembly at the end of mitosis and in cytokinesis. The latter defects can be rescued by either eliminating the spindle position checkpoint protein Bub2 or overproducing its target, Tem1, both leading to MEN hyperactivation. In addition, dma1Δ dma2Δ cells fail to activate the spindle position checkpoint in response to the lack of dynein, whereas ectopic expression of DMA2 prevents unscheduled mitotic exit of spindle checkpoint mutants treated with microtubule-depolymerizing drugs. Although their primary functions remain to be defined, our data suggest that Dma1 and Dma2 might be required to ensure timely MEN activation in telophase.

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