bims-micesi Biomed News
on Mitotic cell signalling
Issue of 2023‒04‒23
twelve papers selected by
Valentina Piano
Uniklinik Köln


  1. J Biol Chem. 2023 Apr 13. pii: S0021-9258(23)01739-8. [Epub ahead of print] 104711
      Mitotic kinetochores are initially captured by dynamic microtubules via a 'search-and-capture' mechanism. The microtubule motor, dynein, is critical for kinetochore capture as it has been shown to transport microtubule-attached chromosomes towards the spindle pole during early mitosis. The microtubule-binding Ndc80 complex that is recruited to kinetochores in prophase is known to play a central role in forming kinetochore-microtubule (kMT) attachments in metaphase. It is not yet clear, however, how Ndc80 contributes to initial kMT capture during prometaphase. Here, by combining CRISPR/Cas9-mediated knockout and RNAi technology with assays specifically targeted to study kMT capture, we show that mitotic cells lacking Ndc80 exhibit severe defects in this function during prometaphase. Rescue experiments show that Ndc80 mutants deficient in microtubule-binding are unable to execute proper kMT capture. While cells inhibited of dynein alone are predominantly able to make initial kMT attachments, cells co-depleted of Ndc80 and dynein show severe defects in kMT capture. Further, we use an in vitro TIR-FM assay to reconstitute microtubule capture events, which suggest that Ndc80 and dynein coordinate with each other for microtubule plus-end capture and that the phosphorylation status of Ndc80 is critical for productive kMT capture. A novel physical interaction between Ndc80 and dynein that we identify in prometaphase extracts might be critical for efficient kMT plus-end capture. Thus, our studies, for the first time, identify a distinct event in the formation of initial kMT attachments, which is directly mediated by Ndc80, and in coordination with dynein is required for efficient kMT capture and chromosome alignment.
    DOI:  https://doi.org/10.1016/j.jbc.2023.104711
  2. EMBO J. 2023 Apr 17. e111587
      Cancer cells display persistent underlying chromosomal instability, with individual tumour types intriguingly exhibiting characteristic subsets of whole, and subchromosomal aneuploidies. Few methods to induce specific aneuploidies will exist, hampering investigation of functional consequences of recurrent aneuploidies, as well as the acute consequences of specific chromosome mis-segregation. We therefore investigated the possibility of sabotaging the mitotic segregation of specific chromosomes using nuclease-dead CRISPR-Cas9 (dCas9) as a cargo carrier to specific genomic loci. We recruited the kinetochore-nucleating domain of centromere protein CENP-T to assemble ectopic kinetochores either near the centromere of chromosome 9, or the telomere of chromosome 1. Ectopic kinetochore assembly led to increased chromosome instability and partial aneuploidy of the target chromosomes, providing the potential to induce specific chromosome mis-segregation events in a range of cell types. We also provide an analysis of putative endogenous repeats that could support ectopic kinetochore formation. Overall, our findings provide new insights into ectopic kinetochore biology and represent an important step towards investigating the role of specific aneuploidy and chromosome mis-segregation events in diseases associated with aneuploidy.
    Keywords:  aneuploidy; centromere; chromosomal instability; chromosome mis-segregation; kinetochore
    DOI:  https://doi.org/10.15252/embj.2022111587
  3. Elife. 2023 Apr 17. pii: e84057. [Epub ahead of print]12
      Phosphorylation is a key post-translational modification that is utilised in many biological processes for the rapid and reversible regulation of protein localisation and activity. Polo-like kinase 1 (PLK-1) is essential for both mitotic and meiotic cell divisions, with key functions being conserved in eukaryotes. The roles and regulation of PLK-1 during mitosis have been well characterised. However, the discrete roles and regulation of PLK-1 during meiosis have remained obscure. Here, we used Caenorhabditis elegans (C. elegans) oocytes to show that PLK-1 plays distinct roles in meiotic spindle assembly and/or stability, chromosome alignment and segregation, and polar body extrusion during meiosis I. Furthermore, by a combination of live imaging and biochemical analysis we identified the chromosomal recruitment mechanisms of PLK-1 during C. elegans oocyte meiosis. The spindle assembly checkpoint kinase BUB-1 directly recruits PLK-1 to the kinetochore and midbivalent while the chromosome arm population of PLK-1 depends on a direct interaction with the centromeric-associated protein CENP-CHCP-4. We found that perturbing both BUB-1 and CENP-CHCP-4 recruitment of PLK-1 leads to severe meiotic defects, resulting in highly aneuploid oocytes. Overall, our results shed light on the roles played by PLK-1 during oocyte meiosis and provide a mechanistic understanding of PLK-1 targeting to meiotic chromosomes.
    Keywords:  C. elegans; cell biology
    DOI:  https://doi.org/10.7554/eLife.84057
  4. Front Cell Dev Biol. 2023 ;11 1191987
      
    Keywords:  abscission; actomyosin; cancer; central spindle; contractile ring; microtubules; midbody; phosphorylation
    DOI:  https://doi.org/10.3389/fcell.2023.1191987
  5. Nat Struct Mol Biol. 2023 Apr 20.
      In the early stages of mitosis, cohesin is released from chromosome arms but not from centromeres. The protection of centromeric cohesin by SGO1 maintains the sister chromatid cohesion that resists the pulling forces of microtubules until all chromosomes are attached in a bipolar manner to the mitotic spindle. Here we present the X-ray crystal structure of a segment of human SGO1 bound to a conserved surface of the cohesin complex. SGO1 binds to a composite interface formed by the SA2 and SCC1RAD21 subunits of cohesin. SGO1 shares this binding interface with CTCF, indicating that these distinct chromosomal regulators control cohesin through a universal principle. This interaction is essential for the localization of SGO1 to centromeres and protects centromeric cohesin against WAPL-mediated cohesin release. SGO1-cohesin binding is maintained until the formation of microtubule-kinetochore attachments and is required for faithful chromosome segregation and the maintenance of a stable karyotype.
    DOI:  https://doi.org/10.1038/s41594-023-00968-y
  6. Sci Adv. 2023 Apr 21. 9(16): eadf8582
      Aurora kinase A (AURKA) performs critical functions in mitosis. Thus, the activity and subcellular localization of AURKA are tightly regulated and depend on diverse factors including interactions with the multiple binding cofactors. How these different cofactors regulate AURKA to elicit different levels of activity at distinct subcellular locations and times is poorly understood. Here, we identified a conserved region of CEP192, the major cofactor of AURKA, that mediates the interaction with AURKA. Quantitative binding studies were performed to map the interactions of a conserved helix (Helix-1) within CEP192. The crystal structure of Helix-1 bound to AURKA revealed a distinct binding site that is different from other cofactor proteins such as TPX2. Inhibiting the interaction between Helix-1 and AURKA in cells led to the mitotic defects, demonstrating the importance of the interaction. Collectively, we revealed a structural basis for the CEP192-mediated AURKA regulation at the centrosome, which is distinct from TPX2-mediated regulation on the spindle microtubule.
    DOI:  https://doi.org/10.1126/sciadv.adf8582
  7. Biophys J. 2023 Apr 20. pii: S0006-3495(23)00268-0. [Epub ahead of print]
      Cell division during early embryogenesis is linked to key morphogenic events such as embryo symmetry breaking and tissue patterning. It is thought that the physical surrounding of cells together with cell intrinsic cues act as a mechanical "mold", guiding cell division to ensure these events are robust. To quantify how cell division is affected by the mechanical and geometrical environment, we present a novel computational mechanical model of cytokinesis, the final phase of cell division. Simulations with the model reproduced experimentally observed furrow dynamics and describe the volume ratio of daughter cells in asymmetric cell divisions, based on the position and orientation of the mitotic spindle. For dividing cells in geometrically confined environments, we show how the orientation of confinement relative to the division axis modulates the volume ratio in asymmetric cell division. Further, we quantified how cortex viscosity and surface tension determine the shape of a dividing cell and govern bubble-instabilities in asymmetric cell division. Finally, we simulated the formation of the three body axes via sequential (a)symmetric divisions up until the 6-cell stage of early C. elegans development, which proceeds within the confines of an eggshell. We demonstrate how model input parameters spindle position and orientation provide sufficient information to reliably predict the volume ratio of daughter cells during the cleavage phase of development. However, for egg geometries perturbed by compression, the model predicts that a change in confinement alone is insufficient to explain experimentally observed differences in cell volume. This points to an effect of the compression on the spindle positioning mechanism. Additionally, the model predicts that confinement stabilizes asymmetric cell divisions against bubble-instabilities.
    DOI:  https://doi.org/10.1016/j.bpj.2023.04.017
  8. Curr Opin Plant Biol. 2023 Apr 15. pii: S1369-5266(23)00031-6. [Epub ahead of print]73 102366
      The preprophase band (PPB) is a transient cytokinetic structure that marks the future division plane at the onset of mitosis. The PPB forms a dense cortical ring of mainly microtubules, actin filaments, endoplasmic reticulum, and associated proteins that encircles the nucleus of mitotic cells. After PPB disassembly, the positional information is preserved by the cortical division zone (CDZ). The formation of the PPB and its contribution to timely CDZ set-up involves activities of functionally distinct microtubule-associated proteins (MAPs) that interact physically and genetically to support robust division plane orientation in plants. Recent studies identified two types of plant-specific MAPs as key regulators of PPB formation, the TON1 RECRUITMENT MOTIF (TRM) and IQ67 DOMAIN (IQD) families. Both families share hallmarks of disordered scaffold proteins. Interactions of IQDs and TRMs with multiple binding partners, including the microtubule severing KATANIN1, may provide a molecular framework to coordinate PPB formation, maturation, and disassembly.
    Keywords:  Cell division; Division plane positioning; Intrinsic disorder; Microtubule-associated proteins; Preprophase band; Scaffolds
    DOI:  https://doi.org/10.1016/j.pbi.2023.102366
  9. Elife. 2023 Apr 19. pii: e80254. [Epub ahead of print]12
      The trapping of Poly-ADP-ribose polymerase (PARP) on DNA caused by PARP inhibitors (PARPi) triggers acute DNA replication stress and synthetic lethality (SL) in BRCA2-deficient cells. Hence, DNA damage is accepted as a prerequisite for SL in BRCA2-deficient cells. In contrast, here we show that inhibiting ROCK in BRCA2-deficient cells triggers SL independently from acute replication stress. Such SL is preceded by polyploidy and binucleation resulting from cytokinesis failure. Such initial mitosis abnormalities are followed by other M-phase defects, including anaphase bridges and abnormal mitotic figures associated with multipolar spindles, supernumerary centrosomes and multinucleation. SL was also triggered by inhibiting Citron Rho-interacting kinase, another enzyme that, similarly to ROCK, regulates cytokinesis. Together, these observations demonstrate that cytokinesis failure triggers mitotic abnormalities and SL in BRCA2-deficient cells. Furthermore, the prevention of mitotic entry by depletion of Early mitotic inhibitor 1 (EMI1) augmented the survival of BRCA2-deficient cells treated with ROCK inhibitors, thus reinforcing the association between M-phase and cell death in BRCA2-deficient cells. This novel SL differs from the one triggered by PARPi and uncovers mitosis as an Achilles heel of BRCA2-deficient cells.
    Keywords:  cancer biology; cell biology
    DOI:  https://doi.org/10.7554/eLife.80254
  10. FASEB J. 2023 05;37(5): e22922
      Age-related oocyte aneuploidy occurs as a result of chromosome segregation errors in female meiosis-I and meiosis-II, and is caused by a progressive age-related deterioration of the chromosome segregation machinery. Here, we assess the impact of age upon the kinetochore, the multi-protein structure that forms the link between the chromosome and spindle microtubules. We find that in meiosis-I the outer kinetochore assembles at germinal vesicle breakdown, but that a substantially smaller outer kinetochore is assembled in oocytes from aged mice. We show this correlates with a weaker centromere in aged oocytes and, using nuclear transfer approaches to generate young-aged hybrid oocytes, we show that outer kinetochore assembly always mirrors the status of the centromere, regardless of cytoplasmic age. Finally, we show that weaker kinetochores in aged oocytes are associated with thinner microtubule bundles, that are more likely to be mis-attached. We conclude that progressive loss of the centromere with advancing maternal age underpins a loss of the outer kinetochore in meiosis-I, which likely contributes to chromosome segregation fallibility in oocytes from older females.
    Keywords:  aging; aneuploidy; centromere; kinetochore; oocyte
    DOI:  https://doi.org/10.1096/fj.202300062R
  11. Cells Dev. 2023 Apr 14. pii: S2667-2901(23)00015-3. [Epub ahead of print] 203839
      Centrosomes are microtubule organizing centers involved in chromosome segregation, spindle orientation, cell motility and cilia formation. In recent years, they have also emerged as key modulators of asymmetric cell division. Centrosomes are composed of two centrioles that initiate duplication in S phase. The conservative nature of centriole duplication means that the two centrioles of a G1 cell are of different ages. They are also structurally different as only the older centriole carry appendages, an assembly of a subset of proteins primarily required for cilia formation. In a growing tissue, the non-motile, primary cilium acts as a mechano- and sensory organelle that influences cell behavior via modulation of signaling pathways. Here, we discuss the most recent findings about distal appendage composition and function, as well as cell cycle-specific regulation and their implications in various diseases.
    Keywords:  Basal body; Cell cycle; Centriole maturation; Centrosome; Cilia; Distal appendages; NEK2; PLK1
    DOI:  https://doi.org/10.1016/j.cdev.2023.203839
  12. Invest Ophthalmol Vis Sci. 2023 Apr 03. 64(4): 23
      Purpose: Uveal melanoma (UM) is the most common intraocular malignancy in adults developing liver metastases, threatening a patient's life. Current therapeutics failed to significantly improve the survival of patients with UM. Thus, the discovery of potent drugs is imminent.Methods: Integrated bioinformatic analysis of The Cancer Genome Atlas and immunohistochemistry staining of patients' tissues revealed the oncogenic role of aurora kinase B (AURKB) in UM. Drug sensitivity assays and an orthotopic intraocular animal model were used to test the efficacy of AURKB inhibitors. RNA sequencing and immunoblotting were performed to identify the downstream effector. A chromatin immunoprecipitation assay was conducted to elucidate AURKB's transcriptional regulation on the target gene.
    Results: AURKB was found overexpressed in patients with UM, resulting in a poor prognosis. Luckily, the AURKB-specific inhibitor, hesperadin, achieved prominent pharmacological efficiency in UM in vitro and in vivo. Mechanically, hesperadin compromised phosphorylation of histone H3 at serine 10 (H3S10ph) at the promoter of telomerase reverse transcriptase, accompanied by methylation of histone H3 at lysine 9. This methylated status of the promoter region forced chromatin condensation and consequently halted the transcription of telomerase reverse transcriptase.
    Conclusions: Collectively, our data demonstrated that AURKB inhibitors decelerated UM tumorigenesis by epigenetically silencing the expression of oncogenic telomerase reverse transcriptase, indicating AURKB as a potential therapeutic target in UM.
    DOI:  https://doi.org/10.1167/iovs.64.4.23