Centriole translocation and degeneration during ciliogenesis in Caenorhabditis elegans neurons

Abstract

Neuronal cilia that are formed at the dendritic endings of sensory neurons are essential for sensory perception. However, it remains unclear how the centriole-derived basal body is positioned to form a template for cilium formation. Using fluorescence time-lapse microscopy, we show that the centriole translocates from the cell body to the dendrite tip in the sensory neurons. The centriolar protein SAS-5 interacts with the dynein light-chain LC8 and conditional mutations of cytoplasmic dynein-1 block centriole translocation and ciliogenesis. The components of the central tube are essential for the biogenesis of centrioles, which later drive ciliogenesis in the dendrite; however, the centriole loses these components at the late stage of centriole translocation and subsequently recruits transition zone and intraflagellar transport proteins. Together, our results provide a comprehensive model of ciliogenesis in sensory neurons and reveal the importance of the dynein-dependent centriole translocation in this process.

Role for intraflagellar transport in building a functional transition zone

“…Notably, temperature‐sensitive mutations in C. elegans DHC‐1, the cytoplasmic dynein‐1 motor subunit, were previously studied by Schmidt and colleagues . Dynein‐1 is thought to act independently from that of the IFT‐associated dynein‐2, and consistent with this notion, the disruption of DHC‐1 in C. elegans results in a centriole translocation defect that is not observed in the ts‐che‐3 mutant we describe herein.…”

DNAH6is a novel candidate gene associated with sperm head anomaly

“…Rare mutation in DNAH6 has been shown to be associated with human azoospermia (Gershoni et al., ). Dynein proteins have been shown to play important roles in centriole functions including centriole translocation, maintenance of centriole cohesion (Jones et al., ; Li, Yi, Zhu, Zhang, & Ou, ). Centriole is the important structure for sperm head‐neck connexion.…”

Separation and Loss of Centrioles From Primordidal Germ Cells to Mature Oocytes in the Mouse

“…Centriole destruction may be prerequisite for terminal differentiation, and the retention of centrioles is associated with proliferation, regeneration, pluripotency, perhaps even totipotency. Skeletal muscle differentiation results in centriole loss (Tassin et al, 1985;Srsen et al, 2009) as during neuron differentiation (Li et al, 2017). Cardiomyocyte differentiation is particularly instructive, since centrioles are lost during terminal differentiation in murine hearts, which do not regenerate (Poss et al, 2002;Bettencourt-Dias et al, 2003).…”