Dual Detection of Chromosomes and Microtubules by the Chromosomal Passenger Complex Drives Spindle Assembly

SummaryChromosome-dependent spindle assembly requires the chromosomal recruitment and activation of Aurora B, the kinase subunit of the chromosomal passenger complex (CPC). It remains unclear how the chromosome-activated kinase spatially transmits signals to organize the micron-scale spindle. Here we reveal that the CPC must detect two structures, chromosomes and microtubules, to support spindle assembly in Xenopus egg extracts. While Aurora B is enriched on chromosomes in metaphase, we establish that a fraction of Aurora B is targeted to the metaphase spindle and phosphorylates microtubule-bound substrates. We demonstrate that chromosomally activated Aurora B must be targeted to microtubules to drive spindle assembly. Moreover, although the CPC-microtubule interaction can activate Aurora B, which further promotes microtubule assembly, this positive feedback is not initiated without chromosomes. We propose that the dual detection of chromosomes and microtubules by the CPC is a critical step in assembling spindles around and only around chromosomes.

Graphical AbstractFigure optionsDownload high-quality image (238 K)Download as PowerPoint slideHighlights
► A FRET sensor reveals Aurora B-dependent phosphorylation on metaphase spindles
► INCENP mediates chromosome-induced Aurora B activation and microtubule targeting
► Targeting activated Aurora B to microtubules drives spindle assembly
► The microtubule targeting is tuned to prevent chromosome-independent activation