Spindle assembly checkpoint-dependent mitotic delay is required for cell division in absence of centrosomes

Farrell, KC; Wang, Jennifer T.; Stearns, Tim

doi:10.7554/elife.84875.1

Cited by 4 publications

(3 citation statements)

References 54 publications

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“…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. Prolonged mitotic arrest has been reported to result in centriole over elongation through Plk1 activity (Kong et al, 2020), and it is possible that a lengthened mitosis, as observed in these mutant cells and cells lacking centrioles (Farrell et al, 2023;, may also result in over elongation of mutant centrioles with just Atubules. In addition, we note that CPAP has an expanded domain in mutant centrioles compared to controls (Fig 4 and Vásquez-Limeta et al, 2022).…”

Section: Discussionmentioning

confidence: 91%

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: 91%

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

Pudlowski,

Xu,

Milenkovic

et al. 2024

Preprint

Self Cite

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“…To ensure accurate chromosome segregation during germ cell division and to produce 2 genetically identical cells during PM II, while further cell division of the vegetative cell is prevented, highly accurate cell cycle checkpoint mechanisms must be executed along these processes. During mitosis, the spindle assembly checkpoint (SAC) is one of these mechanisms that safeguards the transition from metaphase to anaphase ( Lara-Gonzalez et al 2021 ; Farrell et al 2023 ). SAC monitors proper attachment of spindle microtubules to the surface of the kinetochores.…”

Section: Introductionmentioning

confidence: 99%

Heat stress at the bicellular stage inhibits sperm cell development and transport into pollen tubes

Li,

Bruckmann,

Dresselhaus

et al. 2024

Plant Physiology

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For successful double fertilization in flowering plants (angiosperms), pollen tubes deliver two non-motile sperm cells towards female gametes (egg and central cell, respectively). Heatwaves, especially during the reproduction period, threaten male gametophyte (pollen) development, resulting in severe yield losses. Using maize (Zea mays) as a crop and grass model system, we found strong seed set reduction when moderate heat stress was applied for two days during the uni- and bicellular stages of pollen development. We show that heat stress accelerates pollen development and impairs pollen germination capabilities when applied at the unicellular stage. Heat stress at the bicellular stage impairs sperm cell development and transport into pollen tubes. To understand the course of the latter defects, we used marker lines and analyzed the transcriptomes of isolated sperm cells. Heat stress affected the expression of genes associated with transcription, RNA processing and translation, DNA replication, and the cell cycle. This included the genes encoding centromeric histone 3 (CENH3) and α-tubulin. Most genes that were mis-regulated encode proteins involved in the transition from metaphase to anaphase during pollen mitosis II (PM II). Heat stress also activated spindle assembly check point and meta- to anaphase transition genes in sperm cells. In summary, mis-regulation of the identified genes during heat stress at the bicellular stage results in sperm cell development and transport defects ultimately leading to sterility.

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“…To ensure accurate chromosome segregation during germ cell division and to produce two genetically identical cells during PM II, while further cell division of the vegetative cell is prevented, highly accurate cell cycle checkpoint mechanisms must be executed along these processes. During mitosis, the spindle-assembly checkpoint (SAC) is one of these mechanisms that safeguards the transition from metaphase to anaphase (Lara-Gonzalez et al, 2021; Farrell et al, 2023). SAC monitors proper attachment of spindle microtubules to the surface of the kinetochores.…”

Section: Introductionmentioning

confidence: 99%

Heat stress at the bicellular stage inhibits sperm cell development and their transport into pollen tubes

Li,

Bruckmann,

Dresselhaus

et al. 2023

Preprint

View full text Add to dashboard Cite

For a successful double fertilization process in flowering plants (angiosperms), pollen tubes each deliver two non-motile sperm cells towards female gametes (egg and central cell, respectively). Heatwaves especially during the reproduction period are threatening male gametophyte (pollen) development, which results in severe yield losses. By using maize as a crop and grass model system, we found strong seed set reduction when moderate heat stress was applied for two days during the uni- and bicellular stages of pollen development. We show that heat stress accelerates pollen development and impairs pollen germination capabilities, when applied at the unicellular stage. Heat stress at the bicellular stage impairs sperm cell development and their transport into pollen tubes. To understand the course of the latter defects, we used marker lines and analyzed the transcriptomes of isolated sperm cells. While heat stress also affects the expression of genes involved in transcription, RNA processing and translation, especially genes in DNA replication and the cell cycle were mis-regulated. This includes centromeric histone CENH3 and alpha-tubulin. Most mis-regulated genes are involved in transition from metaphase to anaphase during pollen mitosis II (PM II). Heat stress activates spindle assembly check point and meta- to anaphase transition genes in sperm cells. In summary, mis-regulation of the identified genes during heat stress at the bicellular stage explains sperm cell development and transport defects ultimately leading to sterility.

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Spindle assembly checkpoint-dependent mitotic delay is required for cell division in absence of centrosomes

Cited by 4 publications

References 54 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

Heat stress at the bicellular stage inhibits sperm cell development and transport into pollen tubes

Heat stress at the bicellular stage inhibits sperm cell development and their transport into pollen tubes

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