Abstract
Centrosomes, the predominant sites of microtubule nucleation and anchorage, coordinate spindle assembly and cell division in animal cells. At the onset of mitosis, centrioles accumulate microtubule-organizing pericentriolar material (PCM) in a process termed centrosome maturation. To what extent centrosome maturation depends on the continued activity of mitotic regulators or the presence of centrioles has hitherto been unclear. Using the C.elegans early embryo, we show that PCM expansion requires the Polo-like kinase PLK-1 and CEP192 (SPD-2 in C.elegans), but not its upstream regulator Aurora A (AIR-1), while maintenance of the PCM polymer depends exclusively on PLK-1. SPD-2 and PLK-1 are highly concentrated at centrioles. Unexpectedly, laser microsurgery reveals that while centrioles are required for PCM recruitment and centrosome structural integrity they are dispensable for PCM maintenance. We propose a model whereby centrioles promote centrosome maturation by recruiting PLK-1, but subsequent maintenance occurs via PLK-1 acting directly within the PCM.
Highlights
Centrosomes are cytoplasmic structures that organize the microtubule network of animal cells, thereby directing the positioning of organelles, intracellular traffic, polarity, morphogenesis, and cell division
Depletion of all three proteins strongly impairs the mitotic accumulation of the pericentriolar material (PCM) scaffold component SPD-5, while leaving interphase levels largely unchanged (Figures 1B and 1C). This is in contrast to depletion of SPD-5 itself, which entirely eliminates PCM assembly (Figure S1B). Both SPD-2 and PLK-1 are highly concentrated at centrioles, while AIR-1 localizes throughout the PCM and on astral microtubules (Figure 1A; see Figure S1B)
When applied to mitotically arrested embryos, PLK-1 inhibition induced a marked loss of centrosomal SPD-5, with levels dropping to those found in S phase (Figures 2A and 2B; Video S2B), revealing an ongoing requirement for PLK-1 activity to maintain the PCM polymer
Summary
Centrioles are essential for the formation of centrosomes. Here, Cabral et al use the C. elegans early embryo to show centrioles to be required for mitotic expansion of the pericentriolar material (PCM) and centrosome structural integrity, but dispensable for maintenance of the PCM scaffold polymer once recruited.
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