Polo kinase Cdc5 associates with centromeres to facilitate the removal of centromeric cohesin during mitosis

Mishra, Prashant; Ciftci-Yilmaz, Sultan; Reynolds, David; Au, Wei-Chun; Boeckmann, Lars; Dittman, Lauren E.; Jowhar, Ziad J.; Pachpor, Tejaswini; Yeh, Elaine; Baker, Richard E.; Hoyt, M. Andrew; D’Amours, Damien; Bloom, Kerry; Basrai, Munira A.

doi:10.1091/mbc.e16-01-0004

Cited by 20 publications

(30 citation statements)

References 97 publications

(109 reference statements)

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“…Upon Mcd1p-AID depletion, the binding of Cdc5p was abolished genome-wide (Figure 3 and Figure 3-figure supplement 1, Figure 3-figure supplement 2, Figure 3-figure supplement 3), despite similar levels of total Cdc5p(Figure 3-figure supplement 4). This result recapitulated previous work showing the cohesin-dependent binding of Cdc5p at CARs(Mishra et al, 2016;Pakchuen et al, 2016). A few small peaks of binding were observed at centromere and RDN regions, but they coincided with false positives in the GFP-control.…”

supporting

confidence: 89%

“…In this study, we provide important clues on how the regulation of condensin by cohesin and Cdc5p is important for the folding of the RDN. First, cohesin is required for the initial recruitment of Cdc5p to chromosomes in mid-M (this study, and (Mishra et al, 2016;Pakchuen et al, 2016)). We showed that cohesin recruitment of Cdc5p to chromosomes promotes Cdc5p binding to neighboring condensin.…”

Section: Cdc5 Recruitment To the Condensin-bound Region Of The Rdn Stmentioning

confidence: 84%

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The Spatial Regulation of Condensin Activity in Chromosome Condensation

Lamothe

Costantino

Koshland

2019

Preprint

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AbstractCondensin mediates chromosome condensation, which is essential for proper chromosome segregation during mitosis. Prior to anaphase of budding yeast, the ribosomal DNA (RDN) condenses to a thin loop that is distinct from the rest of the chromosomes. We provide evidence that the establishment and maintenance of this RDN condensation require the regulation of condensin by Cdc5p (polo) kinase. We show that Cdc5p is recruited to the site of condensin binding in the RDN by cohesin, a complex related to condensin. Cdc5p and cohesin prevent condensin from misfolding the RDN into an irreversibly decondensed state. From these and other observations, we propose that the spatial regulation of Cdc5p by cohesin modulates condensin activity to ensure proper RDN folding into a thin loop. This mechanism may be evolutionarily conserved, promoting the thinly condensed constrictions that occur at centromeres and RDN of mitotic chromosomes in plants and animals.

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supporting

confidence: 89%

Section: Cdc5 Recruitment To the Condensin-bound Region Of The Rdn Stmentioning

confidence: 84%

The Spatial Regulation of Condensin Activity in Chromosome Condensation

Lamothe

Costantino

Koshland

2019

Preprint

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“…Furthermore, two foreign genes, including those encoding HAUS augmin-like complex subunit 5 (ESA01078.1) and polo kinase (ESA11624.1), are functionally related to mitosis. Polo kinases can regulate mitosis by triggering mitotic exit and facilitating removing centromeric cohesin (Mishra et al, 2016 ; Rodriguez-Rodriguez et al, 2016 ). The HAUS augmin-like complex plays an important role in mitotic spindle formation, chromosome integrity maintenance, and cytokinesis completion (Goshima et al, 2008 ; Lawo et al, 2009 ; Uehara et al, 2009 ).…”

Section: Resultsmentioning

confidence: 99%

Horizontal Gene Transfer From Bacteria and Plants to the Arbuscular Mycorrhizal Fungus Rhizophagus irregularis

Zhao

Tang

et al. 2018

Front. Plant Sci.

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Arbuscular mycorrhizal fungi (AMF) belong to Glomeromycotina, and are mutualistic symbionts of many land plants. Associated bacteria accompany AMF during their lifecycle to establish a robust tripartite association consisting of fungi, plants and bacteria. Physical association among this trinity provides possibilities for the exchange of genetic materials. However, very few horizontal gene transfer (HGT) from bacteria or plants to AMF has been reported yet. In this study, we complement existing algorithms by developing a new pipeline, Blast2hgt, to efficiently screen for putative horizontally derived genes from a whole genome. Genome analyses of the glomeromycete Rhizophagus irregularis identified 19 fungal genes that had been transferred between fungi and bacteria/plants, of which seven were obtained from bacteria. Another 18 R. irregularis genes were found to be recently acquired from either plants or bacteria. In the R. irregularis genome, gene duplication has contributed to the expansion of three foreign genes. Importantly, more than half of the R. irregularis foreign genes were expressed in various transcriptomic experiments, suggesting that these genes are functional in R. irregularis. Functional annotation and available evidence showed that these acquired genes may participate in diverse but fundamental biological processes such as regulation of gene expression, mitosis and signal transduction. Our study suggests that horizontal gene influx through endosymbiosis is a source of new functions for R. irregularis, and HGT might have played a role in the evolution and symbiotic adaptation of this arbuscular mycorrhizal fungus.

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“…For cell cycle assays, logarithmically grown cultures at 25˚C were treated with alpha factor for G1 arrest (3 μM), hydroxyurea (HU, 0.1 M) for S-phase and nocodazole (20 μg/ml) for G2/M arrest, respectively for 90 to 120 minutes. Cell cycle arrest was confirmed by FACS and microscopic analysis for nuclear morphology as described previously [8,90]. Anti-HA antibody (12CA5, Roche Inc) was used to detect HA-tagged Cse4, rabbit polyclonal antibodies against histone H3 (ab1791, Abcam) to detect histones.…”

Section: Protein Stability Assaysmentioning

confidence: 99%

Skp, Cullin, F-box (SCF)-Met30 and SCF-Cdc4-Mediated Proteolysis of CENP-A Prevents Mislocalization of CENP-A for Chromosomal Stability in Budding Yeast

Zhang

Mishra

et al. 2020

PLoS Genet

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Restricting the localization of the histone H3 variant CENP-A (Cse4 in yeast, CID in flies) to centromeres is essential for faithful chromosome segregation. Mislocalization of CENP-A leads to chromosomal instability (CIN) in yeast, fly and human cells. Overexpression and mislocalization of CENP-A has been observed in many cancers and this correlates with increased invasiveness and poor prognosis. Yet genes that regulate CENP-A levels and localization under physiological conditions have not been defined. In this study we used a genome-wide genetic screen to identify essential genes required for Cse4 homeostasis to prevent its mislocalization for chromosomal stability. We show that two Skp, Cullin, Fbox (SCF) ubiquitin ligases with the evolutionarily conserved F-box proteins Met30 and Cdc4 interact and cooperatively regulate proteolysis of endogenous Cse4 and prevent its mislocalization for faithful chromosome segregation under physiological conditions. The interaction of Met30 with Cdc4 is independent of the D domain, which is essential for their homodimerization and ubiquitination of other substrates. The requirement for both Cdc4 and Met30 for ubiquitination is specifc for Cse4; and a common substrate for Cdc4 and Met30 has not previously been described. Met30 is necessary for the interaction between Cdc4 and Cse4, and defects in this interaction lead to stabilization and mislocalization of Cse4, which in turn contributes to CIN. We provide the first direct link between Cse4 mislocalization to defects in kinetochore structure and show that SCF-mediated proteolysis of

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Polo kinase Cdc5 associates with centromeres to facilitate the removal of centromeric cohesin during mitosis

Abstract: Cdc5 associates with centromeric chromatin during mitosis. Cdc5 plays a critical role in the differential removal of cohesin from centromeric chromatin compared to chromosome arms.

Cited by 20 publications

References 97 publications

The Spatial Regulation of Condensin Activity in Chromosome Condensation

The Spatial Regulation of Condensin Activity in Chromosome Condensation

Horizontal Gene Transfer From Bacteria and Plants to the Arbuscular Mycorrhizal Fungus Rhizophagus irregularis

Skp, Cullin, F-box (SCF)-Met30 and SCF-Cdc4-Mediated Proteolysis of CENP-A Prevents Mislocalization of CENP-A for Chromosomal Stability in Budding Yeast

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