Emergence of a Bilaterally Symmetric Pattern from Chiral Components in the Planarian Epidermis

Abstract

Highlights d Centrioles form a bilaterally symmetric pattern across the planarian epidermis d Within cells, centrioles are organized into a chiral asymmetric network d ODF2 and VFL1/3 help in establishing asymmetric connections between centrioles d Bilaterally symmetric patterns can emerge from chiral cellular structures

CCDC61/VFL3 Is a Paralog of SAS6 and Promotes Ciliary Functions

“…Recent studies on CCDC61 in the unicellular ciliate Paramecium tetraurelia showed that the protein plays a crucial role in the orientation of basal bodies and localizes at the interface between basal bodies and ciliary rootlets (Bengueddach et al, 2017). Consistent with these observations, CCDC61 was also shown to be important for the basal body orientation, and the generation of basal feet and ciliary rootlets in the multiciliated ventral epidermis of the flatworm Schmidtea mediterranea (Azimzadeh et al, 2012;Basquin et al, 2019), where its absence results in movement defects. Finally, in Xenopus laevis, the gene expression of CCDC61 was found to be upregulated by the expression of Multicilin, which promotes centriole biogenesis in multiciliated cells (Stubbs et al, 2012).…”

Lrrcc1 and Ccdc61 are conserved effectors of multiciliated cell function

“…The distribution of Lrrcc1 and Ccdc61 at BBs is consistent with their observed requirement for correct MCC organization. This function is shared with Vfl1 (Lrrcc1) and Vfl3 (Ccdc61) orthologs, which are required to organize flagella/cilia in Chlamydomonas, Paramecium and planarians (Adams et al, 1985;Basquin et al, 2019;Bengueddach et al, 2017;Hoops et al, 1984;Wright et al, 1983). In contrast to studies in these species, however, we did not detect major rootlet structural defects upon Lrrcc1 and Ccdc61 depletion, suggesting the existence of redundant mechanisms to build up Xenopus BB appendages.…”

“…In this model, polarization of BBs relies on their chiral construction, which mobilizes Lrrcc1 and Ccd61. This polarization allows the establishment of bilateral symmetry of the ventral multiciliated epidermis, which in turns governs the orientation of the worm movement (Basquin et al, 2019). In addition, retro-control loops exist between the different scales.…”

“…Here, we used the Xenopus laevis ciliated epidermis as a model to shed light on this issue. We decided to comparatively study Lrrcc1 and Ccdc61, based on their shared biological functions in Chlamydomonas and Schmidtea (Adams et al, 1985;Basquin et al, 2019;Hoops et al, 1984;Wright et al, 1983), and their reported physical interaction in an unbiased human proteomic screen (Hein et al, 2015). In Xenopus, MCCs are specified deeply, in the inner cellular layer of the epidermis before intercalating at regular intervals into the outer cellular layer.…”

“…Lrrcc1 (Leucine rich repeat coiled-coil domain containing 1) and Ccdc61 (Coiled-coil domaincontaining protein 61) are structural proteins, conserved from Chlamydomonas to human, which are involved in centriole appendage biogenesis and function, both at the centrosome and at ciliary BBs (Adams et al, 1985;Barenz et al, 2018;Basquin et al, 2019;Bengueddach et al, 2017;Hoops et al, 1984;Muto et al, 2008;Ochi et al, 2020;Pizon et al, 2020;Silflow et al, 2001;Wright et al, 1983). In MCCs of the planarian epidermis, Lrrcc1 (Vfl1) and Ccdc61 (Vfl3) depletion causes structural BB defects, thus perturbing cilia orientation, and altering the direction of locomotion (Basquin et al, 2019). The importance of Lrrcc1 and Ccdc61 in vertebrate MCCs remains unknown.…”