Dynamic relocalization of the chromosomal passenger complex proteins inner centromere protein (INCENP) and aurora-B kinase during male mouse meiosis

Aurora B kinase activity is required for successful cell division. In this paper, we show that Aurora B is phosphorylated at serine 331 (Ser331) during mitosis and that phosphorylated Aurora B localizes to kinetochores in prometaphase cells. Chk1 kinase is essential for Ser331 phosphorylation during unperturbed prometaphase or during spindle disruption by taxol but not nocodazole. Phosphorylation at Ser331 is required for optimal phosphorylation of INCENP at TSS residues, for Survivin association with the chromosomal passenger complex, and for complete Aurora B activation, but it is dispensable for Aurora B localization to centromeres, for autophosphorylation at threonine 232, and for association with INCENP. Overexpression of Aurora BS331A, in which Ser331 is mutated to alanine, results in spontaneous chromosome missegregation, cell multinucleation, unstable binding of BubR1 to kinetochores, and impaired mitotic delay in the presence of taxol. We propose that Chk1 phosphorylates Aurora B at Ser331 to fully induce Aurora B kinase activity. These results indicate that phosphorylation at Ser331 is an essential mechanism for Aurora B activation.

Download Full-text

Coordinated regulation of the ESCRT-III component CHMP4C by the chromosomal passenger complex and centralspindlin during cytokinesis

Open Biology ◽

10.1098/rsob.160248 ◽

2016 ◽

Vol 6 (10) ◽

pp. 160248 ◽

Cited By ~ 26

Author(s):

Luisa Capalbo ◽

Ioanna Mela ◽

Maria Alba Abad ◽

A. Arockia Jeyaprakash ◽

J. Michael Edwardson ◽

...

Keyword(s):

Atomic Force Microscopy ◽

Cell Division ◽

Aurora B ◽

Aurora B Kinase ◽

Chromosomal Passenger Complex ◽

Force Microscopy ◽

Daughter Cells ◽

Atomic Force ◽

Chromosomal Passenger

The chromosomal passenger complex (CPC)—composed of Aurora B kinase, Borealin, Survivin and INCENP—surveys the fidelity of genome segregation throughout cell division. The CPC has been proposed to prevent polyploidy by controlling the final separation (known as abscission) of the two daughter cells via regulation of the ESCRT-III CHMP4C component. The molecular details are, however, still unclear. Using atomic force microscopy, we show that CHMP4C binds to and remodels membranes in vitro . Borealin prevents the association of CHMP4C with membranes, whereas Aurora B interferes with CHMP4C's membrane remodelling activity. Moreover, we show that CHMP4C phosphorylation is not required for its assembly into spiral filaments at the abscission site and that two distinctly localized pools of phosphorylated CHMP4C exist during cytokinesis. We also characterized the CHMP4C interactome in telophase cells and show that the centralspindlin complex associates preferentially with unphosphorylated CHMP4C in cytokinesis. Our findings indicate that gradual dephosphorylation of CHMP4C triggers a ‘relay’ mechanism between the CPC and centralspindlin that regulates the timely distribution and activation of CHMP4C for the execution of abscission.

Download Full-text

EB1 enables spindle microtubules to regulate centromeric recruitment of Aurora B

The Journal of Cell Biology ◽

10.1083/jcb.201307119 ◽

2014 ◽

Vol 204 (6) ◽

pp. 947-963 ◽

Cited By ~ 38

Author(s):

Budhaditya Banerjee ◽

Cortney A. Kestner ◽

P. Todd Stukenberg

Keyword(s):

Mitotic Chromosome ◽

Histone H3 ◽

Aurora B ◽

Dependent Manner ◽

Histone H2a ◽

Aurora B Kinase ◽

Chromosomal Passenger Complex ◽

Checkpoint Signaling ◽

Chromosomal Passenger ◽

Spindle Microtubules

The Aurora B kinase coordinates kinetochore–microtubule attachments with spindle checkpoint signaling on each mitotic chromosome. We find that EB1, a microtubule plus end–tracking protein, is required to enrich Aurora B at inner centromeres in a microtubule-dependent manner. This regulates phosphorylation of both kinetochore and chromatin substrates. EB1 regulates the histone phosphorylation marks (histone H2A phospho-Thr120 and histone H3 phospho-Thr3) that localize Aurora B. The chromosomal passenger complex containing Aurora B can be found on a subset of spindle microtubules that exist near prometaphase kinetochores, known as preformed K-fibers (kinetochore fibers). Our data suggest that EB1 enables the spindle microtubules to regulate the phosphorylation of kinetochores through recruitment of the Aurora B kinase.

Download Full-text

Disassembly of actin and keratin networks by Aurora B kinase at the midplane of cleaving Xenopus laevis eggs

10.1101/513200 ◽

2019 ◽

Author(s):

Christine M. Field ◽

James F. Pelletier ◽

Timothy J. Mitchison

Keyword(s):

Xenopus Laevis ◽

Kinase Activity ◽

Flow Patterns ◽

Aurora B ◽

Aurora B Kinase ◽

Chromosomal Passenger Complex ◽

Chromosomal Passenger ◽

Dividing Cells ◽

Local Softening

AbstractWe investigated how bulk cytoplasm prepares for cytokinesis in Xenopus laevis eggs, which are large, rapidly dividing cells. The egg midplane is demarcated by Chromosomal Passenger Complex (CPC) localized on microtubule bundles between asters. Using an extract system and intact eggs we found that local kinase activity of the AURKB subunit of the CPC caused disassembly of F-actin and keratin between asters, and local softening of the cytoplasm as assayed by flow patterns. Beads coated with active CPC mimicked aster boundaries and caused AURKB-dependent disassembly of F-actin and keratin that propagated ~40 μm without microtubules, and much farther with microtubules present, due to CPC auto-activation. We propose that active CPC at aster boundaries locally reduces cytoplasmic stiffness by disassembling actin and keratin networks. This may help sister centrosomes move apart after mitosis, prepare a soft path for furrow ingression and/or release G-actin to build the furrow cortex.

Download Full-text

Borealin

The Journal of Cell Biology ◽

10.1083/jcb.200404001 ◽

2004 ◽

Vol 166 (2) ◽

pp. 179-191 ◽

Cited By ~ 275

Author(s):

Reto Gassmann ◽

Ana Carvalho ◽

Alexander J. Henzing ◽

Sandrine Ruchaud ◽

Damien F. Hudson ◽

...

Keyword(s):

Rna Interference ◽

Histone H3 ◽

Aurora B ◽

Mitotic Progression ◽

Aurora B Kinase ◽

Chromosomal Passenger Complex ◽

Central Spindle ◽

Chromosomal Passenger ◽

Bipolar Spindles

The chromosomal passenger complex of Aurora B kinase, INCENP, and Survivin has essential regulatory roles at centromeres and the central spindle in mitosis. Here, we describe Borealin, a novel member of the complex. Approximately half of Aurora B in mitotic cells is complexed with INCENP, Borealin, and Survivin; and Borealin binds Survivin and INCENP in vitro. A second complex contains Aurora B and INCENP, but no Borealin or Survivin. Depletion of Borealin by RNA interference delays mitotic progression and results in kinetochore–spindle misattachments and an increase in bipolar spindles associated with ectopic asters. The extra poles, which apparently form after chromosomes achieve a bipolar orientation, severely disrupt the partitioning of chromosomes in anaphase. Borealin depletion has little effect on histone H3 serine10 phosphorylation. These results implicate the chromosomal passenger holocomplex in the maintenance of spindle integrity and suggest that histone H3 serine10 phosphorylation is performed by an Aurora B–INCENP subcomplex.

Download Full-text

Development of a Chemical Genetic Approach for Human Aurora B Kinase Identifies Novel Substrates of the Chromosomal Passenger Complex

Molecular & Cellular Proteomics ◽

10.1074/mcp.m111.013912 ◽

2012 ◽

Vol 11 (5) ◽

pp. 47-59 ◽

Cited By ~ 35

Author(s):

Rutger C. C. Hengeveld ◽

Nicholas T. Hertz ◽

Martijn J. M. Vromans ◽

Chao Zhang ◽

Alma L. Burlingame ◽

...

Keyword(s):

Aurora B ◽

Genetic Approach ◽

Aurora B Kinase ◽

Chromosomal Passenger Complex ◽

Chemical Genetic ◽

Chromosomal Passenger

Download Full-text

Chromosome-directed oocyte spindle assembly depends HP1 and the Chromosomal Passenger Complex

10.1101/2020.06.03.132142 ◽

2020 ◽

Author(s):

Lin-Ing Wang ◽

Tyler DeFosse ◽

Rachel A. Battaglia ◽

Victoria F. Wagner ◽

Kim S. McKim

Keyword(s):

Homologous Chromosome ◽

Spindle Assembly ◽

Aurora B ◽

Aurora B Kinase ◽

Chromosomal Passenger Complex ◽

Central Spindle ◽

Bipolar Spindle ◽

Chromosomal Passenger ◽

Spindle Microtubules

AbstractThe chromosomes in the oocytes of many animals appear to promote bipolar spindle assembly. In Drosophila oocytes, spindle assembly requires the chromosomal passenger complex (CPC), which consists of INCENP, Borealin, Survivin and Aurora B. To determine what recruits the CPC to the chromosomes and its role in spindle assembly, we developed a strategy to manipulate the function and localization of INCENP, which is critical for recruiting the Aurora B kinase. We found that an interaction between Borealin and HP1 is crucial for the initial recruitment of the CPC to the chromosomes and is sufficient to build kinetochores and recruit spindle microtubules. We also found that HP1 moves from the chromosomes to the spindle microtubules along with the CPC, and based on this, propose a mechanism for how the CPC moves from the chromosomes to the microtubules. Within the central spindle, rather than at the centromeres, the CPC and HP1 are required for homologous chromosome bi-orientation.

Download Full-text

EVI5 protein associates with the INCENP-aurora B kinase-survivin chromosomal passenger complex and is involved in the completion of cytokinesis

Experimental Cell Research ◽

10.1016/j.yexcr.2006.03.032 ◽

2006 ◽

Vol 312 (12) ◽

pp. 2325-2335 ◽

Cited By ~ 17

Author(s):

Silviu L. Faitar ◽

Khalid Sossey-Alaoui ◽

Tamara A. Ranalli ◽

John K. Cowell

Keyword(s):

Aurora B ◽

Aurora B Kinase ◽

Chromosomal Passenger Complex ◽

Chromosomal Passenger

Download Full-text

Use of DT40 conditional-knockout cell lines to study chromosomal passenger protein function

Biochemical Society Transactions ◽

10.1042/bst0381655 ◽

2010 ◽

Vol 38 (6) ◽

pp. 1655-1659 ◽

Cited By ~ 1

Author(s):

Xavier Fant ◽

Kumiko Samejima ◽

Ana Carvalho ◽

Hiromi Ogawa ◽

Zhenjie Xu ◽

...

Keyword(s):

Cell Lines ◽

Protein Function ◽

Kinase Activity ◽

Current Knowledge ◽

Conditional Knockout ◽

Aurora B ◽

Aurora B Kinase ◽

Chromosomal Passenger ◽

Passenger Protein

The CPC [chromosomal passenger complex; INCENP (inner centromere protein), Aurora B kinase, survivin and borealin] is implicated in many mitotic processes. In the present paper we describe how we generated DT40 conditional-knockout cell lines for incenp1 and survivin1 to better understand the role of these CPC subunits in the control of Aurora B kinase activity. These lines enabled us to reassess current knowledge of survivin function and to show that INCENP acts as a rheostat for Aurora B activity.

Download Full-text