Nine‐fold symmetry of centriole: The joint efforts of its core proteins

Tian, Yuan; Yan, Yuxuan; Fu, Jingyan

doi:10.1002/bies.202100262

Cited by 3 publications

(3 citation statements)

References 164 publications

(243 reference statements)

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“…Finally, a potentially crucial benefit of our modelling approach is that it does not rely on PLK4 being recruited to centrioles by a number of discrete compartments, as was the case in previous models. While there is some data supporting the idea that centriolar CEP152/Asl, a major recruiter of PLK4 to the centriole (Hatch et al, 2010; Dzhindzhev et al, 2010; Cizmecioglu et al, 2010) may be organised in discrete compartments, the precise number and organisation of these compartments is unclear (Takao et al, 2019; Tian et al, 2021; Wainman, 2021; Gao et al, 2021; Tian et al, 2022; Wilmerding et al, 2023). Moreover, it has also been proposed that CEP152 may be able to self-assemble around the centriole as a continuous ring (Kim et al, 2019; Lee et al, 2020).…”

Section: Discussionmentioning

confidence: 99%

A simple Turing reaction-diffusion model can explain how mother centrioles break symmetry to generate a single daughter

Wilmott

Goriely

Raff

2023

Preprint

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Centrioles are barrel-shaped structures that duplicate when a mother centriole gives birth to a single daughter that grows from its side. Polo-like-kinase 4 (PLK4), the master regulator of centriole biogenesis, is initially recruited around the mother centriole but it quickly concentrates at a single focus that defines the daughter centriole assembly site. How this PLK4 asymmetry is generated is unclear. Two previous studies used different molecular and mathematical models to simulate PLK4 symmetry breaking. Here, we extract the core biological ideas from both models to formulate a new and much simpler mathematical model where phosphorylated and unphosphorylated species of PLK4 (either on their own, or in complexes with other centriole duplication proteins) form the two-components of a classic Turing reaction-diffusion system. These two components bind/unbind from the mother at different rates, and so effectively diffuse around the mother at different rates. This allows a slow-diffusing activator species to accumulate at a single site on the mother, while a fast-diffusing inhibitor species rapidly diffuses around the centriole to suppress activator accumulation. Our analysis suggests that phosphorylated and unphosphorylated species of PLK4 can form a Turing reaction-diffusion system to break symmetry and generate a single daughter centriole.

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Section: Discussionmentioning

confidence: 99%

A simple Turing reaction-diffusion model can explain how mother centrioles break symmetry to generate a single daughter

Wilmott

Goriely

Raff

2023

Preprint

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“…This sets the ground for centriole duplication in the following S-phase. A picture emerges in which CEP135 is spotted as the communication point (“pinpoint” [ 29 ]) of the central cartwheel structure and the centriolar MT, stabilizes the centriole after cartwheel removal, fosters CCC, and improves competence for further duplication.…”

Section: Discussionmentioning

confidence: 99%

Mitotic Maturation Compensates for Premature Centrosome Splitting and PCM Loss in Human cep135 Knockout Cells

Chu

Gruß

2022

Cells

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Centrosomes represent main microtubule organizing centers (MTOCs) in animal cells. Their duplication in S-phase enables the establishment of two MTOCs in M-phase that define the poles of the spindle and ensure equal distribution of chromosomes and centrosomes to the two daughter cells. While key functions of many centrosomal proteins have been addressed in RNAi experiments and chronic knockdown, knockout experiments with complete loss of function in all cells enable quantitative analysis of cellular phenotypes at all cell-cycle stages. Here, we show that the centriolar satellite proteins SSX2IP and WDR8 and the centriolar protein CEP135 form a complex before centrosome assembly in vertebrate oocytes and further functionally interact in somatic cells with established centrosomes. We present stable knockouts of SSX2IP, WDR8, and CEP135 in human cells. While loss of SSX2IP and WDR8 are compensated for, cep135 knockout cells display compromised PCM recruitment, reduced MTOC function, and premature centrosome splitting with imbalanced PCMs. Defective cep135 knockout centrosomes, however, manage to establish balanced spindle poles, allowing unperturbed mitosis and regular cell proliferation. Our data show essential functions of CEP135 in interphase MTOCs and demonstrate that loss of individual functions of SSX2IP, WDR8, and CEP135 are fully compensated for in mitosis.

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“…A final potential advantage of our modelling approach is that it does not rely on PLK4 being recruited to centrioles by receptors that are organised into discrete compartments that compete with each other for PLK4 binding, as was the case in both previous models. While there is some data supporting the idea that CEP152/Asl may be organised into discrete compartments, the number and organisation of these compartments is unclear [13,[21][22][23][24]75]. Moreover, it has been proposed that CEP152, together with its binding partner CEP63, can assemble into a continuous ring around the centriole [76,77].…”

Section: Plos Biologymentioning

confidence: 99%

A simple Turing reaction–diffusion model explains how PLK4 breaks symmetry during centriole duplication and assembly

Wilmott,

Goriely,

Raff

2023

PLoS Biol

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Centrioles duplicate when a mother centriole gives birth to a daughter that grows from its side. Polo-like-kinase 4 (PLK4), the master regulator of centriole duplication, is recruited symmetrically around the mother centriole, but it then concentrates at a single focus that defines the daughter centriole assembly site. How PLK4 breaks symmetry is unclear. Here, we propose that phosphorylated and unphosphorylated species of PLK4 form the 2 components of a classical Turing reaction–diffusion system. These 2 components bind to/unbind from the surface of the mother centriole at different rates, allowing a slow-diffusing activator species of PLK4 to accumulate at a single site on the mother, while a fast-diffusing inhibitor species of PLK4 suppresses activator accumulation around the rest of the centriole. This “short-range activation/long-range inhibition,” inherent to Turing systems, can drive PLK4 symmetry breaking on a either a continuous or compartmentalised Plk4-binding surface, with PLK4 overexpression producing multiple PLK4 foci and PLK4 kinase inhibition leading to a lack of symmetry-breaking and PLK4 accumulation—as observed experimentally.

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Nine‐fold symmetry of centriole: The joint efforts of its core proteins

Cited by 3 publications

References 164 publications

A simple Turing reaction-diffusion model can explain how mother centrioles break symmetry to generate a single daughter

A simple Turing reaction-diffusion model can explain how mother centrioles break symmetry to generate a single daughter

Mitotic Maturation Compensates for Premature Centrosome Splitting and PCM Loss in Human cep135 Knockout Cells

A simple Turing reaction–diffusion model explains how PLK4 breaks symmetry during centriole duplication and assembly

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