ε-tubulin is essential in <i>Tetrahymena thermophila</i> for the assembly and stability of basal bodies

Ross, Ian K.; Clarissa, Christina; Giddings, Thomas H.; Winey, Mark

doi:10.1242/jcs.128694

Cited by 33 publications

(34 citation statements)

References 55 publications

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“…We did not observe a strong defect in centriole number associated with zeta-tubulin depletion, in contrast to previous reports for the ZED tubulins [7, 9, 31–33]. The evolutionary conservation of the ZED module clearly indicates that these tubulins cannot be absolutely required for centriole formation, since organisms such as Drosophila have centrioles but lack all ZED tubulins [34].…”

Section: Discussioncontrasting

confidence: 99%

“…Disruption of ZED tubulins in these organisms results in significant cytoskeletal defects, consistent with the ZED tubulins having a conserved role in basal body-cytoskeleton interactions [31, 32]. For example, disruption of epsilon-tubulin in Tetrahymena resulted in defective orientation and spacing of basal bodies [33], similar to depletion of zeta-tubulin in Xenopus .…”

Section: Discussionmentioning

confidence: 81%

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Zeta-Tubulin Is a Member of a Conserved Tubulin Module and Is a Component of the Centriolar Basal Foot in Multiciliated Cells

et al. 2015

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SUMMARY There are six members of the tubulin superfamily in eukaryotes [1]. Alpha- and beta-tubulin form a heterodimer that polymerizes to form microtubules, and gamma-tubulin nucleates microtubules as a component of the gamma-tubulin ring complex. Alpha-, beta-, and gamma-tubulin are conserved in all eukaryotes. In contrast, delta- and epsilon-tubulin are conserved in many, but not all, eukaryotes and are associated with centrioles, although their molecular function is unclear [2–7]. Zeta-tubulin is the sixth and final member of the tubulin superfamily, and is largely uncharacterized. We find that zeta-, epsilon-, and delta-tubulin form an evolutionarily co-conserved module, the ZED module, that has been lost at several junctions in eukaryotic evolution, and that zeta- and delta-tubulin are evolutionarily interchangeable. Humans lack zeta-tubulin, but have delta-tubulin. In Xenopus multiciliated cells, zeta-tubulin is a component of the basal foot, a centriolar appendage that connects centrioles to the apical cytoskeleton, and co-localizes there with epsilon-tubulin. Depletion of zeta-tubulin results in disorganization of centriole distribution and polarity in multiciliated cells. In contrast with multiciliated cells, zeta-tubulin in cycling cells does not localize to centrioles and is associated with the TRiC/CCT cytoplasmic chaperone complex. We conclude that zeta-tubulin facilitates interactions between the centrioles and the apical cytoskeleton as a component of the basal foot in differentiated cells, and propose that the ZED tubulins are important for centriole functionalization and orientation of centrioles with respect to cellular polarity axes.

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Section: Discussioncontrasting

confidence: 99%

Section: Discussionmentioning

confidence: 81%

Zeta-Tubulin Is a Member of a Conserved Tubulin Module and Is a Component of the Centriolar Basal Foot in Multiciliated Cells

et al. 2015

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“…These results demonstrate that cells lacking either delta-tubulin or epsilon-tubulin form defective centrioles that lack normal triplet microtubules. This is similar to the defects reported for delta-tubulin and epsilon-tubulin mutants in unicellular eukaryotes (DupuisWilliams et al, 2002;Dutcher and Trabuco, 1998;Dutcher et al, 2002;Gadelha et al, 2006;Garreau de Loubresse et al, 2001;Goodenough and StClair, 1975;Ross et al, 2013).…”

Section: Resultssupporting

confidence: 89%

Centriole triplet microtubules are required for stable centriole formation and inheritance in human cells

Wang

Kong²,

Hoerner

et al. 2017

Preprint

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Centrioles are composed of long-lived microtubules arranged in nine triplets.However, the contribution of triplet microtubules to mammalian centriole formation and stability is unknown. Little is known of the mechanism of triplet microtubule formation, but experiments in unicellular eukaryotes indicate that delta-tubulin and epsilon-tubulin, two less-studied tubulin family members, are required. Here, we report that centrioles in delta-tubulin and epsilon-tubulin null mutant human cells lack triplet microtubules and fail to undergo centriole maturation. These aberrant centrioles are formed de novo each cell cycle, but are unstable and do not persist to the next cell cycle, leading to a futile cycle of centriole formation and disintegration. Disintegration can be suppressed by paclitaxel treatment. Delta-tubulin and epsilon-tubulin physically interact, indicating that these tubulins act together to maintain triplet microtubules and that these are necessary for inheritance of centrioles from one cell cycle to the next.

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“…Assembly generally occurs from an extant structure in a 1:1 ratio with the aid of molecular assembly factors (12–15). Additionally, basal bodies and centrioles can be assembled de novo , as well as from a deuterosome serving to mediate the amplification of these structures in specific cell types (16–18).…”

Section: Introductionmentioning

confidence: 99%

Sfr1, a Tetrahymena thermophila Sfi1 Repeat Protein, Modulates the Production of Cortical Row Basal Bodies

Heydeck

Stemm-Wolf

Knop

et al. 2016

mSphere

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Basal bodies and centrioles are structurally similar and, when rendered dysfunctional as a result of improper assembly or maintenance, are associated with human diseases. Centrins are conserved and abundant components of both structures whose basal body and centriolar functions remain incompletely understood. Despite the extensive study of centrins in Tetrahymena thermophila, little is known about how centrin-binding proteins contribute to centrin’s roles in basal body assembly, stability, and orientation. The sole previous study of the large centrin-binding protein family in Tetrahymena revealed a role for Sfr13 in the stabilization and separation of basal bodies. In this study, we found that Sfr1 localizes to all Tetrahymena basal bodies and complete genetic deletion of SFR1 leads to overproduction of basal bodies. The uncovered inhibitory role of Sfr1 in basal body production suggests that centrin-binding proteins, as well as centrins, may influence basal body number both positively and negatively.

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ε-tubulin is essential in Tetrahymena thermophila for the assembly and stability of basal bodies

Cited by 33 publications

References 55 publications

Zeta-Tubulin Is a Member of a Conserved Tubulin Module and Is a Component of the Centriolar Basal Foot in Multiciliated Cells

Zeta-Tubulin Is a Member of a Conserved Tubulin Module and Is a Component of the Centriolar Basal Foot in Multiciliated Cells

Centriole triplet microtubules are required for stable centriole formation and inheritance in human cells

Sfr1, a Tetrahymena thermophila Sfi1 Repeat Protein, Modulates the Production of Cortical Row Basal Bodies

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