The art of barrel coopery

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The centriole proteins SPD-2 and ZYG-1 are required for the duplication of these barrel-shaped structures in single-cell Caenorhabditis elegans embryos.

Centrioles are involved in many cellular processes and duplicate once per cell cycle. Using electron tomography and other microscopy techniques, Pelletier et al. have analysed the duplication process of these barrel-shaped structures in single-cell Caenorhabditis elegans embryos.


A three-dimensional representation of daughter centriole assembly that is orthogonal to the older mother centriole. Image courtesy of L. Pelletier, Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany.

Oocytes of C. elegans lack centrioles, but fertilization by sperm contributes a centriole pair to the single-cell embryo. After completing meiosis, the embryo enters the first mitotic division, which is characterized by distinct stages — pronuclear appearance (PNA), pronuclear migration (PNM), pronuclear rotation (PNR) and metaphase — during which a daughter centriole is assembled orthogonally to each mother centriole.

To visualize the recruitment of known centriole proteins during the centriole-assembly process, the authors used oocytes that expressed GFP-tagged centriole proteins. The centriole proteins SPD-2 and ZYG-1 were recruited soon after fertilization, whereas SAS-4, SAS-5 and SAS-6 were recruited later, during PNA. By depleting individual proteins and assessing the effect on the recruitment of the other proteins, the authors deduced that SPD-2 functions upstream of ZYG-1 and that these two proteins are required for the recruitment of SAS-5 and SAS-6, which, in turn, promotes the recruitment of SAS-4.

Centrioles in C. elegans consist of a central tube surrounded by nine single microtubules. By carrying out electron tomography studies at different stages during the first cell division, Pelletier and colleagues observed the first daughter centriole intermediate — the central tube — at the PNA stage. The central tube continued to elongate and increase in diameter during PNM, and single microtubules started to assemble around the central tube at hook-like appendages during PNR.

So, which centriole proteins are required for which step in the assembly process? No daughter centriole structures were detected in sas-5 and sas-6 (RNA interference) embryos, but formation and elongation of the central centriole tube still occurred in sas-4 (RNAi) embryos, although no single microtubules were observed. This implies that SAS-4 is needed to assemble or maintain single microtubules on the central tube, which is consistent with the previously reported ring-like distribution of SAS-4 around the central tube. By contrast, SAS-5 and SAS-6 are required for tube formation and elongation, and SPD-2 and ZYG-1 function further upstream as possible triggers for duplication or direct drivers of the assembly process, as the recruitment of the SAS proteins was blocked in their absence.

As several of the known C. elegans centriole proteins have mammalian homologues, aspects of the centriole-assembly process are likely to be conserved.

Arianne Heinrichs

References

Pelletier, L. et al. Centriole assembly in Caenorhabditis elegans. Nature 444, 619–623 (2006) | Article | PubMed |