Centriole elimination during <i>Caenorhabditis elegans</i> oogenesis initiates with loss of the central tube protein <scp>SAS</scp>‐1

Pierron, Marie; Woglar, Alexander; Busso, Coralie; Jha, Keshav; Mikeladze‐Dvali, Tamara; Croisier, Marie; Gönczy, Pierre

doi:10.15252/embj.2023115076

Cited by 5 publications

(2 citation statements)

References 78 publications

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“…Using expansion microscopy, we find that centriole loss is correlated with loss of the SASS6 cartwheel in mitosis. In this regard, mutant centrioles with singlet microtubules resemble centriole loss within C. elegans oocytes, in which an analogous structure to the cartwheel named the central tube is lost prior to centriole widening and subsequent loss of the centriolar microtubules (Pierron et al, 2023). In addition, centriole loss in our mutant cells occurs through a stereotyped progression of architectural changes in mitosis, starting with centriole over elongation in prometaphase and culminating with centriole fragmentation and loss.…”

Section: Discussionmentioning

confidence: 78%

“…Centriole loss is not unique to centrioles lacking compound microtubules: mammalian cells engineered to lack CEP295 also form centrioles that are lost through the cell cycle, due to an inability to undergo centriole to centrosome conversion (Izquierdo et al, 2014). Similarly, in Drosophila oocytes, down-regulation of Polo kinase and pericentriolar material triggers centriole elimination (Pimenta-Marques et al, 2016). We find that CEP295 is properly localized in mutant centrioles with singlet microtubules, indicating that centriole loss in this context may be independent of centriole to centrosome conversion and pericentriolar material recruitment.…”

Section: Discussionmentioning

confidence: 99%

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A delta-tubulin/epsilon-tubulin/Ted protein complex is required for centriole architecture

Pudlowski,

Xu,

Milenkovic

et al. 2024

Preprint

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Centrioles have a unique, conserved architecture formed by three linked triplet microtubules arranged in nine-fold symmetry. The mechanisms by which these triplet microtubules are formed are not understood, but likely involve the noncanonical tubulins delta-tubulin and epsilon-tubulin. Previously, we found that human cells deficient in delta-tubulin or epsilon-tubulin form abnormal centrioles, characterized by an absence of triplet microtubules, lack of central core protein POC5, and a futile cycle of centriole formation and disintegration (Wang et al., 2017). Here, we show that human cells lacking either of the associated proteins TEDC1 and TEDC2 have these same phenotypes. Using ultrastructure expansion microscopy, we identified the roles of these proteins and triplet microtubules in centriole architecture by mapping the locations of centriolar proteins throughout the cell cycle. We find that mutant centrioles have normal architecture during S-phase. By G2-phase, mutant centrioles grow to the same length as control centrioles, but fail to recruit inner scaffold proteins of the central core. Instead, the inner lumen of centrioles is filled with an expanded proximal region, indicating that these proteins, or the triplet microtubules themselves, may be required for recruiting central core proteins and restricting the length of the proximal end. During mitosis, the mutant centrioles elongate further before fragmenting and disintegrating. All four proteins physically interact and TEDC1 and TEDC2 are capable of interacting in the absence of the tubulins. These results support an AlphaFold Multimer structural prediction model for the tetrameric complex, in which delta-tubulin and epsilon-tubulin are predicted to form a heterodimer. TEDC1 and TEDC2 localize to centrosomes and are mutually dependent on each other and on delta-tubulin and epsilon-tubulin for localization. These results indicate that delta-tubulin, epsilon-tubulin, TEDC1, and TEDC2 function together in promoting robust centriole architecture. This work also lays the groundwork for future dissection of this complex, which will provide a basis for determining the mechanisms that underlie the assembly and interplay between compound microtubules and inner centriole structure.

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Section: Discussionmentioning

confidence: 78%

Section: Discussionmentioning

confidence: 99%

A delta-tubulin/epsilon-tubulin/Ted protein complex is required for centriole architecture

Pudlowski,

Xu,

Milenkovic

et al. 2024

Preprint

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Maternal inheritance of functional centrioles in two parthenogenetic nematodes

Perrier,

Guiglielmoni,

Naquin

et al. 2024

Nat Commun

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Centrioles are the core constituent of centrosomes, microtubule-organizing centers involved in directing mitotic spindle assembly and chromosome segregation in animal cells. In sexually reproducing species, centrioles degenerate during oogenesis and female meiosis is usually acentrosomal. Centrioles are retained during male meiosis and, in most species, are reintroduced with the sperm during fertilization, restoring centriole numbers in embryos. In contrast, the presence, origin, and function of centrioles in parthenogenetic species is unknown. We found that centrioles are maternally inherited in two species of asexual parthenogenetic nematodes and identified two different strategies for maternal inheritance evolved in the two species. In Rhabditophanes diutinus, centrioles organize the poles of the meiotic spindle and are inherited by both the polar body and embryo. In Disploscapter pachys, the two pairs of centrioles remain close together and are inherited by the embryo only. Our results suggest that maternally-inherited centrioles organize the embryonic spindle poles and act as a symmetry-breaking cue to induce embryo polarization. Thus, in these parthenogenetic nematodes, centrioles are maternally-inherited and functionally replace their sperm-inherited counterparts in sexually reproducing species.

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Mechanisms of axoneme and centriole elimination inNaegleria gruberi

Woglar,

Busso,

Garcia-Rodriguez

et al. 2024

Preprint

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The excavate Naegleria gruberi, a basal eukaryote related to the "brain eating" Naegleria fowleri, can transform transiently from an amoeboid life form lacking flagella and centrioles to a flagellate life form where these elements are present, followed by reversion to an amoeboid state. The mechanisms imparting elimination of axonemes and centrioles during this reversion process are not known. Here, we uncover that flagella primarily fold onto the cell surface and fuse within milliseconds with the plasma membrane. Once internalized, axonemes are severed by Spastin into equally-sized fragments, which are then enclosed by membranes, after which their contents are eliminated through the lysosomal pathway. Moreover, we discovered that centrioles undergo progressive K63 autophagy-linked poly-ubiquitination and K48 proteasome-promoting poly-ubiquitination, and that ubiquitination occurs next to centriolar microtubules. Most centrioles are eliminated in lysosomes or the cytoplasm in a lysosomal- and proteasome-dependent manner. Strikingly, we uncover in addition that centrioles can be shed in the extracellular milieu and taken up by other cells. Collectively, these findings reveal fundamental mechanisms governing the elimination of essential cellular constituents in Naegleria that may operate broadly in eukaryotic systems.

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Centriole elimination during Caenorhabditis elegans oogenesis initiates with loss of the central tube protein SAS‐1

Cited by 5 publications

References 78 publications

A delta-tubulin/epsilon-tubulin/Ted protein complex is required for centriole architecture

A delta-tubulin/epsilon-tubulin/Ted protein complex is required for centriole architecture

Maternal inheritance of functional centrioles in two parthenogenetic nematodes

Mechanisms of axoneme and centriole elimination inNaegleria gruberi

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