Basal bodies bend in response to ciliary forces

Junker, Anthony D.; Woodhams, Louis G.; Soh, Adam W. J.; O’Toole, Eileen; Bayly, Philip V.; Pearson, Chad G.

doi:10.1091/mbc.e22-10-0468-t

Cited by 11 publications

(8 citation statements)

References 88 publications

(127 reference statements)

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“…We speculate that centrioles with triplet microtubules and the proteins they anchor, including the inner scaffold, may be required for centriole function in organisms with motile cilia, perhaps to help stabilize the basal body against ciliary movement. Such activity has been described for Tetrahymena basal bodies, and mutating an inner scaffold protein, Poc1, results in abnormal bending within basal bodies (Junker et al, 2022). Further supporting this hypothesis, Drosophila spermatocytes, one of the few cells within this species with motile cilia, have basal bodies with triplet microtubules (González et al, 1998).…”

Section: Discussionmentioning

confidence: 87%

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: 87%

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

Pudlowski,

Xu,

Milenkovic

et al. 2024

Preprint

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“…We previously showed that BBs bend in response to the cilia beat stroke, suggesting that BBs balance rigidity with plasticity to ensure they do not disassemble (Junker et al, 2022). To understand how the BB architecture protects itself from ciliary forces, we used UExM-SIM to assess how BBs bend in response to ciliary beating.…”

Section: Resultsmentioning

confidence: 99%

“…Under high force conditions, WT BBs exhibit a gradual bend, whereas dramatic fracturing of the BB through the core region was observed in the absence of Poc1, suggesting poc1Δ BBs lack the structural integrity that can integrate the bending without destructive deformation (Fig. 6E; (Junker et al, 2022)). To determine whether BBs that show structural defects have intact core structures, we used UExM-SIM to visualize Poc16 in BBs in high force conditions.…”

Section: Resultsmentioning

confidence: 99%

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Poc1 is a basal body inner junction protein that promotes triplet microtubule integrity and interconnections

Ruehle,

Li,

Agard

et al. 2023

Preprint

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Basal bodies (BBs) are conserved eukaryotic structures that organize motile and primary cilia. The BB is comprised of nine, cylindrically arranged, triplet microtubules (TMTs) that are connected to each other by inter-TMT linkages which maintain BB structure. During ciliary beating, forces transmitted to the BB must be resisted to prevent BB disassembly. Poc1 is a conserved BB protein important for BBs to resist ciliary forces. To understand how Poc1 confers BB stability, we identified the precise position of Poc1 binding in theTetrahymenaBB and the effect of Poc1 loss on BB structure. Poc1 binds at the TMT inner junctions, stabilizing TMTs directly. From this location, Poc1 also stabilizes inter-TMT linkages throughout the BB, including the cartwheel pinhead and the inner scaffold. Moreover, we identify a molecular response to ciliary forces via a molecular remodeling of the inner scaffold, as determined by differences in Fam161A localization. Thus, while not essential for BB assembly, Poc1 promotes BB interconnections that establish an architecture competent to resist ciliary forces.

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“…Centrioles are subcellular organelles with an evolutionarily conserved, barrel-shaped structure that are found at the base of cilia and flagella (reviewed in Azimzadeh, 2021; Winey and O’Toole, 2014). There, the centriole, also known as the basal body, acts as a shock absorber that resists the movement of axonemal microtubules relative to one other, although they may flex in response to ciliary forces (Junker et al, 2022). Yet, centrioles have evolved diverse structures in the sperm cells of many invertebrate and vertebrate animals, presumably due to divergent selective pressure produced by varying levels of sperm competition (reviewed in Avidor-Reiss and Fishman, 2019), an evolutionary process that drives sperm change due to post-ejaculatory competition between males (reviewed in Birkhead and Hunter, 1990; Humphries et al, 2008; Parker, 1970).…”

Section: Introductionmentioning

confidence: 99%

The Evolution of Centriole Degradation in Mouse Sperm

Khanal

Puente

Chandanayaka

et al. 2023

Preprint

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Centrioles are subcellular organelles with an evolutionarily conserved structure and a shock absorber-like function. In sperm, centrioles are found at the flagellum base and are essential for embryo development in basal animals. Yet, sperm centrioles have evolved diverse forms, sometimes acting like a transmission system, as in cattle, and sometimes becoming dispensable, as in house mice. How the essential sperm centriole evolved to become dispensable in some organisms is unclear. Here, we test the hypothesis that this transition occurred through a cascade of evolutionary changes to the proteins, structure, and function of sperm centrioles and was possibly driven by sperm competition. We found that the last steps in this cascade are associated with a change in the primary structure of the centriolar luminal protein FAM161A in rodents. This information provides the first insight into the molecular mechanisms and adaptive evolution underlying a major evolutionary transition within the internal structure of the mammalian sperm neck.

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Basal bodies bend in response to ciliary forces

Cited by 11 publications

References 88 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

Poc1 is a basal body inner junction protein that promotes triplet microtubule integrity and interconnections

The Evolution of Centriole Degradation in Mouse Sperm

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