BUB-1 promotes amphitelic chromosome biorientation via multiple activities at the kinetochore

Edwards, Frances A.; Maton, Gilliane; Gareil, Nelly; Canman, Julie C.; Dumont, Julien

doi:10.7554/elife.40690

Cited by 23 publications

(34 citation statements)

References 88 publications

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“…Therefore, HCP-1 (and its paralogue HCP-2) could be regulating events during early anaphase, in addition to recruiting CLS-2 during mid-anaphase. While more experiments are needed to test this hypothesis, an intricate interaction between BUB-1, HCP-1/2 and CLS-2 has recently been shown to be involved in the regulating kinetochore–MT attachments during mitosis (Edwards et al, 2018).…”

Section: Discussionmentioning

confidence: 99%

Sumoylation regulates protein dynamics during meiotic chromosome segregation in C. elegans oocytes

Pelisch

Borja

Jaffray

et al. 2019

Journal of Cell Science

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Oocyte meiotic spindles in most species lack centrosomes and the mechanisms that underlie faithful chromosome segregation in acentrosomal meiotic spindles are not well understood. In C. elegans oocytes, spindle microtubules exert a poleward force on chromosomes that is dependent on the microtubule-stabilising protein CLS-2, the orthologue of the mammalian CLASP proteins. The checkpoint kinase BUB-1 and CLS-2 localise in the central spindle and display a dynamic localisation pattern throughout anaphase, but the signals regulating their anaphase-specific localisation remains unknown. We have shown previously that SUMO regulates BUB-1 localisation during metaphase I. Here, we found that SUMO modification of BUB-1 is regulated by the SUMO E3 ligase GEI-17 and the SUMO protease ULP-1. SUMO and GEI-17 are required for BUB-1 localisation between segregating chromosomes during early anaphase I. We also show that CLS-2 is subject to SUMO-mediated regulation; CLS-2 precociously localises in the midbivalent when either SUMO or GEI-17 are depleted. Overall, we provide evidence for a novel, SUMO-mediated control of protein dynamics during early anaphase I in oocytes.

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Section: Discussionmentioning

confidence: 99%

Sumoylation regulates protein dynamics during meiotic chromosome segregation in C. elegans oocytes

Pelisch

Borja

Jaffray

et al. 2019

Journal of Cell Science

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“…Next, we analyzed the domains of BUB-1, HCP-1, and CLS-2 necessary for BHC module assembly. During mitosis, CENP-F in mammals and HCP-1 in C. elegans , are recruited to kinetochores through the BUB-1 kinase domain 39, 46 . We first tested if that was also the case during meiosis by analyzing HCP-1 and CLS-2 localization in C. elegans oocytes expressing RNAi-resistant transgenes encoding full length BUB-1 (BUB-1 FL ) or a kinase domain-deleted mutant of BUB-1 (BUB-1 ΔKD ) after depletion of endogenous BUB-1 (Figure 2A) 39 .…”

Section: Resultsmentioning

confidence: 99%

Synergistic stabilization of microtubules by BUB-1, HCP-1 and CLS-2 controls meiotic spindle assembly in C. elegans oocytes

Macaisne

Bellutti

Laband

et al. 2022

Preprint

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During cell division, chromosome segregation is orchestrated by a microtubule-based spindle. Interaction between spindle microtubules and kinetochores is central to the bi-orientation of chromosomes. Initially dynamic to allow spindle assembly and kinetochore attachments, which is essential for chromosome alignment, microtubules are eventually stabilized for efficient segregation of sister chromatids and homologous chromosomes during mitosis and meiosis I respectively. Therefore, the precise control of microtubule dynamics is of utmost importance during mitosis and meiosis. Here, we study the assembly and role of a kinetochore module, comprised of the kinase BUB-1, the two redundant CENP-F orthologs HCP-1/2, and the CLASP family member CLS-2 (hereafter termed the BHC module), in the control of microtubule dynamics in Caenorhabditis elegans oocytes. Using a combination of in vivo structure-function analyses of BHC components and in vitro microtubule-based assays, we show that BHC components stabilize microtubules, which is essential for meiotic spindle formation and accurate chromosome segregation. Overall, our results show that BUB-1 and HCP-1/2 do not only act as targeting components for CLS-2 at kinetochores, but also synergistically control kinetochore-microtubule dynamics by promoting microtubule pause. Together, our results suggest that BUB-1 and HCP-1/2 actively participate in the control of kinetochore-microtubule dynamics in the context of the BHC module to promote accurate chromosome segregation in meiosis.

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“…After chromosome replication, microtubules connect sister chromatids and direct them to the middle of the cell (Primorac et al, 2013). Accurate chromosome segregation relies on bioriented, amphitelic attachments of chromosomes to microtubules of the mitotic spindle, in which the sister chromatids must be attached to opposite spindle poles (Edwards et al, 2018; Primorac et al, 2013). The SAC is activated when improper attachment occurs.…”

Section: Bub3 Overviewmentioning

confidence: 99%

“…attachments of chromosomes to microtubules of the mitotic spindle, in which the sister chromatids must be attached to opposite spindle poles (Edwards et al, 2018;Primorac et al, 2013). The SAC is activated when improper attachment occurs.…”

mentioning

confidence: 99%

Research progress of Bub3 gene in malignant tumors

Wang

Chen

Pan

et al. 2022

Cell Biology International

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The spindle assembly checkpoint (SAC) is a highly conserved monitoring system that ensures a fidelity of chromosome segregation during mitosis. Bub3, a mitotic Checkpoint Protein, is a member of the Bub protein family, and an important factor in the SAC. Abnormal expression of Bub3 results in mitotic defects, defective spindle gate function, chromosomal instability and the development of aneuploidy cells. Aneuploidy is a state of abnormal karyotype that has long been considered as a marker of tumorigenesis.Karyotypic heterogeneity in tumor cells, known as "chromosomal instability" (CIN), can be used to distinguish cancerous cells from their normal tissue counterpart. In this review, we summarize the expression and clinical significance of Bub3 in a variety of tumors and suggest that it has potential in the treatment of cancer.

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BUB-1 promotes amphitelic chromosome biorientation via multiple activities at the kinetochore

Cited by 23 publications

References 88 publications

Sumoylation regulates protein dynamics during meiotic chromosome segregation in C. elegans oocytes

Sumoylation regulates protein dynamics during meiotic chromosome segregation in C. elegans oocytes

Synergistic stabilization of microtubules by BUB-1, HCP-1 and CLS-2 controls meiotic spindle assembly in C. elegans oocytes

Research progress of Bub3 gene in malignant tumors

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