Outer kinetochore protein Dam1 promotes centromere clustering in parallel with Slk19 in budding yeast

Mittal, Priyanka; Chavan, Ankita; Trakroo, Deepika; Shah, Sanket; Ghosh, Santanu

doi:10.1007/s00412-019-00694-9

Cited by 10 publications

(14 citation statements)

References 102 publications

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“…Due to the difference in chromosome segregation patterns between mitosis and meiosis, several kinetochore proteins have altered essentiality (Mehta et al, 2014, Agarwal et al, 2015). Likewise, earlier we reported absence of Cin8 and Kip3 severely compromises genome stability specifically in meiosis (Mittal et al, 2019). Here, we add to that list by showing a meiosis-specific kinetochore stabilizing function of the kinesin motors.…”

Section: Discussionsupporting

confidence: 79%

“…We and others have earlier reported that the inner and outer kinetochore proteins are interdependent for centromeric localization (Thakur and Sanyal, 2012; Mittal et al ., 2019) in contrast to the notional hierarchical organization of the kinetochore at the centromeres. Therefore, it is plausible that the improper localization of outer kinetochore protein (Ndc80) at the centromeres in the motor mutant may hinder the maintenance of inner kinetochore proteins at the centromeres.…”

Section: Resultsmentioning

confidence: 96%

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Evidence of kinesin motors involved in stable kinetochore assembly during early meiosis

Shah

Mittal

Kumar

et al. 2022

Preprint

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The characteristic bi-lobed organization of the kinetochores observed during mitotic metaphase is a result of separation of the sister kinetochores into two clusters upon their stable end-on attachment to the microtubules emanating from opposite spindle poles. In contrast, during metaphase I of meiosis despite bi-orientation of the homologs, we observe that the kinetochores are linearly dispersed between the two spindle poles indicating that pole-distal and pole-proximal kinetochores are attached laterally and end-on, respectively to the microtubules. Colocalization studies of kinetochores and kinesin motors suggest that budding yeast kinesin 5, Cin8 and Kip1 perhaps localize to the end-on attached kinetochores while kinesin 8, Kip3 resides at all the kinetochores. Unlike mitosis in budding yeast, in meiosis, the outer kinetochores assemble much later after prophase I. From the findings including co-appearance of kinesin 5 and the outer kinetochore protein Ndc80 at the centromeres after prophase I and a reduction in Ndc80 level in Cin8 null mutant, we propose that kinesin motors are required for reassembly and stability of the kinetochores during early meiosis. Thus, this work reports yet another meiosis specific function of kinesin motor.

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Section: Discussionsupporting

confidence: 79%

Section: Resultsmentioning

confidence: 96%

Evidence of kinesin motors involved in stable kinetochore assembly during early meiosis

Shah

Mittal

Kumar

et al. 2022

Preprint

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“…Images were generated by merging the planes projecting maximum intensity and further analyzed. The quantification of the fluorescence intensity of the images, acquired using a Zeiss AxioObserver Z1 microscope, was performed using ImageJ software (92). A region of interest covering the fluorescence signal was defined, and the integrated intensity of that region was estimated, following background reduction, by averaging the integrated intensities of three random nonfluorescent areas multiplied by the area of the fluorescent signal region.…”

Section: Methodsmentioning

confidence: 99%

Meiosis-Specific Functions of Kinesin Motors in Cohesin Removal and Maintenance of Chromosome Integrity in Budding Yeast

Mittal

Ghule

Trakroo

et al. 2020

Molecular and Cellular Biology

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Kinesin motors provide the molecular forces at the kinetochore-microtubule interface and along the spindle to control chromosome segregation. During meiosis with two rounds of microtubule assembly-disassembly, the roles of motor proteins remain unexplored. We observed that in contrast to mitosis, Cin8 and Kip3 together are indispensable for meiosis. While examining meiosis in cin8Δ kip3Δ cells, we detected chromosome breakage in the meiosis II cells. The double mutant exhibits a delay in cohesin removal during anaphase I. Consequently, some cells fail to undergo meiosis II and form dyads, while some, as they progress through meiosis II, cause a defect in chromosome integrity. We believe that in the latter cells, an imbalance of spindle-mediated force and the simultaneous persistence of cohesin on chromosomes cause their breakage. We provide evidence that tension generated by Cin8 and Kip3 through microtubule cross-linking is essential for signaling efficient cohesin removal and the maintenance of chromosome integrity during meiosis.

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“…Slk19 was originally identified as a centromere associated protein that functions to stabilize the mitotic spindle (Zeng et al, 1999). At the centromere, Slk19 contributes to the clustering of kinetochores (KTs) (Richmond et al, 2013;Mittal et al, 2019), to centromeric elasticity (Zhang et al, 2006) and to the regulation of the activity of the separase Esp1 (Lianga et al, 2018). Furthermore Slk19, together and interdependently with Stu1, is sequestered at unattached KTs (Kolenda et al, 2018).…”

Section: Introductionmentioning

confidence: 99%

“…At the centromere, Slk19 contributes to the clustering of kinetochores (KTs) ( Richmond et al. , 2013 ; Mittal et al. , 2019 ), to centromeric elasticity ( Zhang et al.…”

Section: Introductionmentioning

confidence: 99%

Slk19 enhances cross-linking of microtubules by Ase1 and Stu1

Norell

Ortiz

Lechner

2021

MBoC

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The S. cerevisiae protein Slk19 has been shown to localize to kinetochores throughout mitosis and to the spindle midzone in anaphase. However, Slk19 clearly also has an important role for spindle formation and stabilization in prometaphase and metaphase. Albeit this role is unresolved. Here we show that Slk19’s localization to metaphase spindles in vivo and to microtubules in vitro depends on the microtubule crosslinking protein Ase1 and the MT crosslinking and stabilizing protein Stu1. By analyzing a slk19 mutant that specifically fails to localize to spindles and microtubules, we surprisingly found that the presence of Slk19 amplified the amount of Ase1 strongly and that of Stu1 moderately at the metaphase spindle in vivo and at microtubules in vitro. Furthermore, Slk19 markedly enhanced the crosslinking of microtubules in vitro, when added together with Ase1 or Stu1. We therefore suggest that Slk19 recruits additional Ase1 and Stu1 to the interpolar microtubules of metaphase spindles and thus increases their crosslinking and stabilization. This is in agreement with our observation that cells with defective Slk19 localization exhibit shorter metaphase spindles, an increased number of unaligned nuclear microtubules and most likely reduced interpolar microtubule overlaps.

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Outer kinetochore protein Dam1 promotes centromere clustering in parallel with Slk19 in budding yeast

Cited by 10 publications

References 102 publications

Evidence of kinesin motors involved in stable kinetochore assembly during early meiosis

Evidence of kinesin motors involved in stable kinetochore assembly during early meiosis

Meiosis-Specific Functions of Kinesin Motors in Cohesin Removal and Maintenance of Chromosome Integrity in Budding Yeast

Slk19 enhances cross-linking of microtubules by Ase1 and Stu1

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