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  • Review Article
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Chromosomal passengers: conducting cell division

Key Points

  • The chromosomal passenger complex (CPC) is involved in the proper orchestration of both mitosis and meiosis. The CPC comprises Aurora-B protein kinase, the inner centromere protein (INCENP), survivin and borealin (also known as Dasra-B). The non-enzymatic members of the complex control the targeting, enzymatic activity and stability of Aurora-B. A fifth protein, TD-60, while not part of the complex, may also have an important role in regulating Aurora-B activity.

  • In early mitosis, the CPC appears on chromosome arms and subsequently concentrates at centromeres. It promotes the loading of condensin I onto mitotic chromosomes as well as the phosphorylation of histone H3. The CPC is also required for assembly and stability of a bipolar mitotic spindle via the phosphorylation of substrates such as stathmin (also known as oncoprotein-18; OP18) and mitotic centromere-associated kinesin (MCAK), as well as for the correction of kinetochore–microtubule attachment errors via the phosphorylation of substrates such as MCAK and HEC1 (highly expressed in cancer-1; known as Ndc80 in budding yeast).

  • The CPC is required for spindle checkpoint function when tension within the spindle is abnormal. The CPC is thought to be required for the recruitment of the checkpoint protein BUBR1 to the kinetochore and, together with the BUB1 checkpoint kinase, to promote the association of BUBR1 with the anaphase promoting complex/cyclosome.

  • In late mitosis, the CPC transfers from centromeres to the spindle midzone during anaphase to finally concentrate in the midbody during telophase and cytokinesis. CPC activity is essential for cytokinesis. It is thought that phosphorylation of vimentin and Rac GTPase activating protein-1 (MgcRacGAP/CYK-4) by Aurora-B are required for cleavage furrow formation and the completion of cytokinesis, respectively.

  • In both mitosis and meiosis, the CPC is required for the correct centromeric localization of the Shugoshin family of proteins. During meiosis, Shugoshin proteins cooperate with protein phosphatase-2A (PP2A) to promote the maintenance of sister centromere cohesion until the metaphase–anaphase transition of the second meiotic division. They also regulate centromeric cohesion in mitotic cells.

Abstract

Mitosis and meiosis are remarkable processes during which cells undergo profound changes in their structure and physiology. These events are orchestrated with a precision that is worthy of a classical symphony, with different activities being switched on and off at precise times and locations throughout the cell. One essential 'conductor' of this symphony is the chromosomal passenger complex (CPC), which comprises Aurora-B protein kinase, the inner centromere protein INCENP, survivin and borealin (also known as Dasra-B). Studies of the CPC are providing insights into its functions, which range from chromosome–microtubule interactions to sister chromatid cohesion to cytokinesis, and constitute one of the most dynamic areas of ongoing mitosis and meiosis research.

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Figure 1: Chromosomal passenger complex localization during mitosis.
Figure 2: Interactions within the chromosomal passenger complex and Aurora-B activation.
Figure 3: Chromosomal passenger complex localization and function during mitosis.
Figure 4: Regulation of kinetochore binding to microtubules by the chromosomal passenger complex (CPC).
Figure 5: Chromosomal passenger complex localization during meiosis.
Figure 6: Localization and function of the chromosomal passenger complex during meiosis I.

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Cell Biology (2nd edition), a textbook by T.D. Pollard and W.C. Earnshaw with J. Lippincott-Schwartz and G. T. Johnson

Glossary

Polo family

A family of Ser/Thr protein kinases that have crucial roles in cell-cycle regulation, in the regulation of sister chromatid pairing and in the assembly and function of the mitotic spindle.

Inner centromere

The heterochromatin-rich region of the chromosome that is situated in between the two kinetochores of the paired sister chromatids.

Spindle midzone

Organized bundles of antiparallel microtubules at the centre of the spindle that form during anaphase and telophase.

Equatorial cell cortex

A region of the cell membrane where actin and myosin fibres assemble to form the contractile ring during anaphase.

Metaphase plate

A dynamic grouping of chromosomes positioned on a plane that is perpendicular to the spindle axis midway between spindle poles.

Inhibitor of apoptosis protein (IAP) family

Proteins that are characterized by their baculovirus IAP repeat (BIR) domains. They suppress apoptosis by interacting with and inhibiting the enzymatic activity of caspases.

Baculovirus IAP repeat (BIR) domain

This Zn2+-finger domain is important for protein–protein interactions and is specific to all proteins of the inhibitor of apoptosis (IAP) family.

CBF3 complex

A multisubunit protein complex in Saccharomyces cerevisiae that binds to centromeric DNA and initiates kinetochore assembly.

FRAP

(Fluorescence recovery after photobleaching). A technique that measures the dynamics of fluorescently tagged macromolecules within cellular substructures.

FLIP

(Fluorescence loss in photobleaching). A technique that measures the mobility of molecules by bleaching a defined region of cytoplasm and watching how this affects the population of fluorescent molecules in other regions of the cell.

Chromodomain

A conserved motif that is present in various chromatin proteins and is involved in binding methylated histone tails.

Condensin complex

A complex of two structural maintenance of chromosomes (SMC) subunits and three auxiliary non-SMC subunits. It is essential for the structural integrity of chromosomes.

Taxol

Also known as paclitaxel. A drug of major importance in cancer chemotherapy that suppresses microtubule dynamic instability, thereby stabilizing microtubules.

Dam1 complex

A multiprotein complex in budding yeast that encircles the plus ends of microtubules proximal to the kinetochore and which is important for kinetochore–microtubule interactions.

Aneuploidy

A condition in which the number of chromosomes is not an exact multiple of the haploid set.

Anaphase promoting complex/cyclosome

(APC/C). A multisubunit E3 ubiquitin ligase that targets proteins for proteasome-mediated degradation by attaching polyubiquitin chains to them. It has a key role in regulating the eukaryotic cell cycle.

Chromosome congression

The movement of correctly attached chromosomes to form a metaphase plate at the midplane of the mitotic spindle.

Shugoshin family

A family of proteins that protect centromeric cohesin from cleavage by separase, possibly by recruiting protein phosphatase-2A to centromeres.

Midbody

A dense structure that is derived from the remains of the central spindle during late telophase and is present at the intercellular bridge during cytokinesis.

Bivalent

A pair of homologous (maternal plus paternal) chromosomes that are linked together after prophase of meiosis I.

Chiasmata

Chromosomal structures that interlink homologous chromosomes at the site of mature crossovers during meiosis I.

Synaptonemal complex

A proteinaceous complex that links pairs of homologous chromosomes during pachytene of meiosis I. It forms during zygotene and disassembles during diplotene stages of meiosis I prophase.

Pachytene

A stage of the prophase of meiosis I during which the homologous chromosomes are paired lengthwise, forming thick threads, and are linked by the synaptonemal complex.

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Ruchaud, S., Carmena, M. & Earnshaw, W. Chromosomal passengers: conducting cell division. Nat Rev Mol Cell Biol 8, 798–812 (2007). https://doi.org/10.1038/nrm2257

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