An ancestral role of pericentrin in centriole formation through SAS-6 recruitment

Abstract

Short summaryThe pericentriolar matrix (PCM) is not only important for microtubule-nucleation but also can regulate centriole biogenesis. Ito et al. reveal an ancestral interaction between the centriole protein SAS-6 and the PCM component pericentrin, which regulates centriole biogenesis and elongation. AbstractThe centrosome is composed of two centrioles surrounded by a microtubule-nucleating pericentriolar matrix (PCM). Centrioles regulate matrix assembly. Here we ask whether the matrix also regulates centriole assembly. To define the interaction between the matrix and individual centriole components, we take advantage of a heterologous expression system using fission yeast. Importantly, its centrosome, the spindle pole body (SPB), has matrix but no centrioles. Surprisingly, we observed that the SPB can recruit several animal centriole components. Pcp1/pericentrin, a conserved matrix component that is often upregulated in cancer, recruits a critical centriole constituent, SAS-6. We further show that this novel interaction is conserved and important for centriole biogenesis and elongation in animals. We speculate that the Pcp1/pericentrin-SAS-6 interaction surface was conserved for one billion years of evolution after centriole loss in yeasts, due to its conserved binding to calmodulin. This study reveals an ancestral relationship between pericentrin and the centriole, where both regulate each other assembly, ensuring mutual localisation.

Centrosome Remodelling in Evolution

“…We searched for orthologues of components of the human centrosome localizing to centrioles and PCM and the fission yeast SPB components by using reciprocal pairwise sequence-based (BLASTP and phmmer) and domain-based (hmmsearch) methods [ 87 , 88 ]. Black circles represent the presence of orthologues; blue circles indicate that previous studies showed the presence of a protein with short conserved motifs [ 47 , 56 , 60 ] although we failed to identify it by the above-mentioned computational methods; white circles indicate no detectable orthologue ([ 89 ] and our unpublished results).…”

Dynamics of centriole amplification in centrosome-depleted brain multiciliated progenitors

“…Overexpression of Pericentrin leads to overduplication of centrioles in human transformed cells 27 . More recently, Pericentrin was shown to recruit Sas6 and to be involved in centriole biogenesis and stability in drosophila 28,29 . The increasing expression of Pericentrin during A-phase, visible by the increasing surface of the Pericentrin cloud, may be involved in the sequential formation of procentrioles we observed, even in the absence of centrosomal centrioles.…”