Molecular basis for unidirectional scaffold switching of human Plk4 in centriole biogenesis

Park, Suk Youl; Park, Jung Eun; Kim, Tae Sung; Kim, Ju Hee; Kwak, Mi Jeong; Ku, Bonsu; Tian, Lei; Murugan, Ravichandran N.; Ahn, Mok-Ryeon; Komiya, Shinobu; Hojo, Hironobu; Kim, Nam Hyung; Kim, Bo Yeon; Bang, Jeong Kyu; Erikson, Raymond L.; Lee, Ki Won; Kim, Seung Jun; Oh, Byung Ha; Yang, Wei; Lee, Kyung S.

doi:10.1038/nsmb.2846

Cited by 96 publications

(177 citation statements)

References 41 publications

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“…In dividing cells, Asl serves as a receptor recruiting Plk4 to the centriole for centriole duplication [24, 27, 30, 31]. However, Asl’s interaction with Plk4 is complex and mediated via two distinct domains (Asl C-terminus and N-terminus), which have distinct functions during centriole duplication [22].…”

Section: Resultsmentioning

confidence: 99%

Asterless Reduction during Spermiogenesis Is Regulated by Plk4 and Is Essential for Zygote Development in Drosophila

et al. 2015

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SUMMARY Centrosome reduction is the decrease in centrosomal components during spermatid differentiation (spermiogenesis) [1, 2]. It is one of several dramatic subcellular reorganizations that leads to spermatozoa formation common to a wide range of animals [3]. However, the mechanism underlying centrosome reduction is unknown and its functions are unclear. Here, we show that in Drosophila melanogaster spermiogenesis, the quantity of centrosomal proteins is dramatically reduced [4, 5];for example, Asterless (Asl) is reduced ~500-fold and is barely detected in spermatozoa. Asl reduction is regulated through a subset of its domains by the master regulator of centriole duplication Plk4[6–8] and by the ubiquitin ligase that targets Plk4 for degradation: Slimb [9, 10]. When Asl reduction is attenuated by Asl overexpression, plk4 mutations, Plk4 RNAi, or Slimb overexpression, Asl levels are higher in spermatozoa, resulting in embryo’s with reduced viability. Significantly, overexpressing Plk4 and Asl simultaneously, or combining plk4 and slimb mutations, balances their opposing effects on Asl reduction, restoring seemingly normal fertility. This suggests that increased Asl levels cause the observed reduced fertility, and not other pleotropic effects. Attenuation of Asl reduction also causes delayed development and a failure to form astral microtubules in the zygote. Together, we provide the first insight into a molecular mechanism that regulates centrosome reduction and the first direct evidence that centrosome reduction is essential for postfertilization development.

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Section: Resultsmentioning

confidence: 99%

Asterless Reduction during Spermiogenesis Is Regulated by Plk4 and Is Essential for Zygote Development in Drosophila

et al. 2015

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“…In mammalian cells, CEP295 directly binds to CEP192 and contributes to the stabilization of centrioles after the loss of the cartwheel upon mitotic exit 89,94 . Considering that CEP152 and CEP192 form scaffolds for the recruitment of PLK4 95–99 , the kinase essential for centriole duplication (see below), these results explain why post-mitotic PCM assembly is required to confer duplication competence to procentrioles 91 . While C.elegans lack an obvious CEP295/Ana1 homolog, recent work has shown that the SAS-7 protein interacts with SPD-2 and is required for procentrioles to acquire competence to duplicate, suggesting SAS-7 may function analogously to CEP295 100 .…”

Section: Control Of Centriole Numbermentioning

confidence: 92%

“…In mammalian cells, PLK4 is recruited to centrioles through binding to two distinct scaffolding proteins, CEP152 and CEP192 95–99 . Super-resolution microscopy shows that both CEP152 and CEP192 form rings around parent centrioles and, accordingly, PLK4 can also be seen to form rings in G1 phase.…”

Section: Control Of Centriole Numbermentioning

confidence: 99%

Once and only once: mechanisms of centriole duplication and their deregulation in disease

Nigg

Holland

2018

Nat Rev Mol Cell Biol

407

546

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Centrioles are conserved microtubule-based organelles that form the core of the centrosome and act as templates for the formation of cilia and flagella. Centrioles have important roles in most microtubule related processes, including motility, cell division and cell signaling. To coordinate these diverse cellular processes, centriole number must be tightly controlled. In cycling cells, one new centriole is formed next to each preexisting centriole in every cell cycle. Advances in imaging, proteomics, structural biology and genome editing have revealed new insights into centriole biogenesis, how centriole numbers are controlled and how alterations in these structures contribute to diseases such as cancer and neurodevelopmental disorders. Moreover, recent work has uncovered the existence of surveillance pathways that limit proliferation of cells with numerical centriole aberrations. Here we discuss recent progress in this field with a focus on signaling pathways and molecular mechanisms.

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“…Two polo‐like kinases (PLKs), PLK4 and PLK1, play crucial roles in centriole duplication and microtubule nucleation (20). PLK4 interacts with Cep192 and then switches to Cep152 in the subsequent centriole replication cycle (19, 21). Chemical inhibition of PLK4 kinase activity reversibly depletes the centrioles in somatic cells (22), suggesting the importance of PLK4 in centriole duplication.…”

mentioning

confidence: 99%

Distinct roles of Cep192 and Cep152 in acentriolar MTOCs and spindle formation during mouse oocyte maturation

Lee

Jung

et al. 2018

FASEB j.

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Mammalian oocytes lack a centriole that acts as a microtubule organization center (MTOC) in most somatic cells. During oocyte maturation, MTOCs undergo remodeling processes, including decondensation, fragmentation, and self-organization. However, the underlying mechanisms of MTOC remodeling in mouse oocytes are not well understood. We showed that two pericentriolar proteins, Cep192 and Cep152, play crucial roles during MTOC remodeling in mouse oocytes. Cep192 is present in MTOCs at all stages of oocyte maturation, and its depletion induces ablation of MTOCs, delay in spindle formation, and abnormal chromosomal alignment in spindles. In the case of Cep152, its localization on MTOCs is limited at the germinal vesicle stage and then disappears from the MTOCs after the germinal vesicle breakdown stage. Cep152 exclusion from MTOCs is involved in the fragmentation of MTOCs, and it is regulated by cyclin-dependent kinase 1 activity. Our results demonstrate the different roles of Cep192 and Cep152 in MTOC remodeling and a novel regulatory mechanism during meiotic spindle formation in mouse oocytes.-Lee, I.-W., Jo, Y.-J., Jung, S.-M., Wang, H.-Y., Kim, N.-H., Namgoong, S. Distinct roles of Cep192 and Cep152 in acentriolar MTOCs and spindle formation during mouse oocyte maturation.

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Molecular basis for unidirectional scaffold switching of human Plk4 in centriole biogenesis

Cited by 96 publications

References 41 publications

Asterless Reduction during Spermiogenesis Is Regulated by Plk4 and Is Essential for Zygote Development in Drosophila

Asterless Reduction during Spermiogenesis Is Regulated by Plk4 and Is Essential for Zygote Development in Drosophila

Once and only once: mechanisms of centriole duplication and their deregulation in disease

Distinct roles of Cep192 and Cep152 in acentriolar MTOCs and spindle formation during mouse oocyte maturation

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