Centriole foci persist in starfish oocytes despite Polo-like kinase 1 inactivation or loss of microtubule nucleation activity

Pierron, Marie; Kalbfuß, Nils; Borrego-Pinto, Joana; Lénárt, Péter; Gönczy, Pierre

doi:10.1091/mbc.e19-06-0346

Cited by 7 publications

(10 citation statements)

References 30 publications

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“…The centriolar complex is reported to be eliminated in late oogenesis, a process triggered by reduction in Polo-like kinase (Plk) activity ( Pimenta-Marques et al, 2016 ). In starfish oocytes, three centrioles are selectively removed by extrusion into polar bodies, while the sole remaining daughter centriole is degraded in anaphase II, and this process is independent of Plk1 ( Borrego-Pinto et al, 2016 ; Pierron et al, 2020 ). To sum up, although centriole elimination is a hallmark feature of oocytes, the mechanism manipulating the process varies.…”

Section: Centrosomes In Germ Cells and Centrosome Abnormalities In Infertilitymentioning

confidence: 99%

Multifaceted roles of centrosomes in development, health, and disease

Zhou

2021

Journal of Molecular Cell Biology

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The centrosome is a membrane-less organelle consisting of a pair of barrel-shaped centrioles and pericentriolar material and functions as the major microtubule-organizing center and signaling hub in animal cells. The past decades have witnessed the functional complexity and importance of centrosomes in various cellular processes such as cell shaping, division, and migration. In addition, centrosome abnormalities are linked to a wide range of human diseases and pathological states, such as cancer, reproductive disorder, brain disease, and ciliopathies. Herein, we discuss various functions of centrosomes in development and health, with an emphasis on their roles in germ cells, stem cells, and immune responses. We also discuss how centrosome dysfunctions are involved in diseases. A better understanding of the mechanisms regulating centrosome functions may lead the way to potential therapeutic targeting of this organelle in disease treatment.

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Section: Centrosomes In Germ Cells and Centrosome Abnormalities In Infertilitymentioning

confidence: 99%

Multifaceted roles of centrosomes in development, health, and disease

Zhou

2021

Journal of Molecular Cell Biology

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“…Perhaps a large PCM surrounding a cluster of 64 centrioles would prevent the elimination machinery to reach centrioles in Drosophila , such that prior PCM disassembly is a prerequisite for organelle removal in that case. Inhibiting Plk1 in starfish oocytes does not alter disappearance timing of foci bearing the centriolar marker Centrin2, suggesting that centriole elimination is not regulated by this kinase in this system either (Pierron et al , 2020). Future work should help clarify why the requirement of Polo and the PCM revealed in Drosophila oogenesis may not be deployed in other centriole elimination settings.…”

Section: Discussionmentioning

confidence: 99%

“…In the first mode, maternal centrioles are removed following the meiotic divisions (Crowder et al , 2015). This is the case in starfish, for example, where centrioles are present at spindle poles during the two female meiotic divisions, such that three maternal centrioles are eliminated through polar body extrusion, with the last one being removed in the zygote (Sluder et al , 1989; Shirato et al , 2006; Borrego‐Pinto et al , 2016; Pierron et al , 2020). In the second and most prevalent mode, which occurs notably in worms, flies, and vertebrates, maternal centrioles are removed during oogenesis, before the meiotic divisions.…”

Section: Introductionmentioning

confidence: 99%

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

Pierron,

Woglar,

Busso

et al. 2023

The EMBO Journal

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In most metazoans, centrioles are lost during oogenesis, ensuring that the zygote is endowed with the correct number of two centrioles, which are paternally contributed. How centriole architecture is dismantled during oogenesis is not understood. Here, we analyze with unprecedent detail the ultrastructural and molecular changes during oogenesis centriole elimination in Caenorhabditis elegans. Centriole elimination begins with loss of the so‐called central tube and organelle widening, followed by microtubule disassembly. The resulting cluster of centriolar proteins then disappears gradually, usually moving in a microtubule‐ and dynein‐dependent manner to the plasma membrane. Our analysis indicates that neither Polo‐like kinases nor the PCM, which modulate oogenesis centriole elimination in Drosophila, do so in C. elegans. Furthermore, we demonstrate that the central tube protein SAS‐1 normally departs initially from the organelle, which loses integrity earlier in sas‐1 mutants. Overall, our work provides novel mechanistic insights regarding the fundamental process of oogenesis centriole elimination.

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“…Only one daughter centriole remains in the zygote, which is rapidly eliminated in the fertilized egg. Modified with permission from [82]. …”

Section: Centriole Elimination In the Female Germlinementioning

confidence: 99%

“…Intriguingly, neither the PCM nor the activity of the Polo-like-kinase Plk1 seem sufficient to protect centrioles in other systems. Thus, mother centrioles in A. forbesi persist after their experimental retention in the oocyte, although they do not nucleate microtubules [82]. Furthermore, pharmacological inhibition of Plk1 does not lead to premature elimination of centrioles in P. miniata [82].…”

Section: Which Factors Induce Centriole Destabilization?mentioning

confidence: 99%

Towards understanding centriole elimination

Kalbfuss,

Gönczy

2023

Open Biol.

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Centrioles are microtubule-based structures crucial for forming flagella, cilia and centrosomes. Through these roles, centrioles are critical notably for proper cell motility, signalling and division. Recent years have advanced significantly our understanding of the mechanisms governing centriole assembly and architecture. Although centrioles are typically very stable organelles, persisting over many cell cycles, they can also be eliminated in some cases. Here, we review instances of centriole elimination in a range of species and cell types. Moreover, we discuss potential mechanisms that enable the switch from a stable organelle to a vanishing one. Further work is expected to provide novel insights into centriole elimination mechanisms in health and disease, thereby also enabling scientists to readily manipulate organelle fate.

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Centriole foci persist in starfish oocytes despite Polo-like kinase 1 inactivation or loss of microtubule nucleation activity

Cited by 7 publications

References 30 publications

Multifaceted roles of centrosomes in development, health, and disease

Multifaceted roles of centrosomes in development, health, and disease

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

Towards understanding centriole elimination

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