An Autonomous Oscillation Times and Executes Centriole Biogenesis

Aydogan, Mustafa G.; Steinacker, Thomas L.; Mofatteh, Mohammad; Wilmott, Zachary M.; Zhou, Felix; Gartenmann, Lisa; Wainman, Alan; Saurya, Saroj; Novak, Zsofia A.; Wong, Siu‐Shing; Goriely, Alain; Boemo, Michael A.; Raff, Jordan W.

doi:10.1016/j.cell.2020.05.018

Cited by 35 publications

(101 citation statements)

References 85 publications

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“…These results suggest that phosphorylation of NEDD1 by PLK4 is critical for NEDD1 to switch its binding target from γ-TuRC to SAS-6 to facilitate cartwheel assembly initiation. Recent research has revealed that an autonomous PLK4 oscillation at the base of the growing centriole initiates and executes centriole biogenesis in fly embryos, and while S phase progresses, the centriolar PLK4 level grows to a critical concentration that triggers its destruction until its concentration is too low to support Sas-6 and Ana2 recruitment for cartwheel growth ( Aydogan et al, 2020 ; Aydogan et al, 2018 ). In addition, another study showed that reduced PLK4 activity relieves the SCF–FBXW5 complex activity to degrade centriolar SAS-6 to restrict centrosome reduplication ( Puklowski et al, 2011 ).…”

Section: Resultsmentioning

confidence: 99%

PLK4-phosphorylated NEDD1 facilitates cartwheel assembly and centriole biogenesis initiations

Chi

Wang

Xin

et al. 2020

Journal of Cell Biology

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Centrosome duplication occurs under strict spatiotemporal regulation once per cell cycle, and it begins with cartwheel assembly and daughter centriole biogenesis at the lateral sites of the mother centrioles. However, although much of this process is understood, how centrosome duplication is initiated remains unclear. Here, we show that cartwheel assembly followed by daughter centriole biogenesis is initiated on the NEDD1-containing layer of the pericentriolar material (PCM) by the recruitment of SAS-6 to the mother centriole under the regulation of PLK4. We found that PLK4-mediated phosphorylation of NEDD1 at its S325 amino acid residue directly promotes both NEDD1 binding to SAS-6 and recruiting SAS-6 to the centrosome. Overexpression of phosphomimicking NEDD1 mutant S325E promoted cartwheel assembly and daughter centriole biogenesis initiations, whereas overexpression of nonphosphorylatable NEDD1 mutant S325A abolished the initiations. Collectively, our results demonstrate that PLK4-regulated NEDD1 facilitates initiation of the cartwheel assembly and of daughter centriole biogenesis in mammals.

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Section: Resultsmentioning

confidence: 99%

PLK4-phosphorylated NEDD1 facilitates cartwheel assembly and centriole biogenesis initiations

Chi

Wang

Xin

et al. 2020

Journal of Cell Biology

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“…It is in this model system where an organelle ‘clock’ has recently been demonstrated to regulate the timing of centriole formation – an oscillatory mechanism that is normally entrained by the cell cycle progression, but can also run autonomously ( Aydogan et al, 2020 ; Figure 2 ). Centrioles are cytoskeletal organelles that form centrosomes – the major microtubule organizing centers (MTOCs) that aid the assembly of mitotic spindles in dividing cells (reviewed in Banterle and Gönczy, 2017 ; Conduit et al, 2015 ).…”

Section: The Emerging Concept Of Autonomous Clocks and Their Mechanisms At Different Scales And Complexitiesmentioning

confidence: 99%

Autonomous clocks that regulate organelle biogenesis, cytoskeletal organization, and intracellular dynamics

Mofatteh

Iturra

Alamban

et al. 2021

eLife

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How do cells perceive time? Do cells use temporal information to regulate the production/degradation of their enzymes, membranes, and organelles? Does controlling biological time influence cytoskeletal organization and cellular architecture in ways that confer evolutionary and physiological advantages? Potential answers to these fundamental questions of cell biology have historically revolved around the discussion of ‘master’ temporal programs, such as the principal cyclin-dependent kinase/cyclin cell division oscillator and the circadian clock. In this review, we provide an overview of the recent evidence supporting an emerging concept of ‘autonomous clocks,’ which under normal conditions can be entrained by the cell cycle and/or the circadian clock to run at their pace, but can also run independently to serve their functions if/when these major temporal programs are halted/abrupted. We begin the discussion by introducing recent developments in the study of such clocks and their roles at different scales and complexities. We then use current advances to elucidate the logic and molecular architecture of temporal networks that comprise autonomous clocks, providing important clues as to how these clocks may have evolved to run independently and, sometimes at the cost of redundancy, have strongly coupled to run under the full command of the cell cycle and/or the circadian clock. Next, we review a list of important recent findings that have shed new light onto potential hallmarks of autonomous clocks, suggestive of prospective theoretical and experimental approaches to further accelerate their discovery. Finally, we discuss their roles in health and disease, as well as possible therapeutic opportunities that targeting the autonomous clocks may offer.

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“…Biological oscillators can also entrain each other to create an oscillator hierarchy. This is the case with the circadian oscillators in peripheral organs, which take their cue from the master circadian oscillator in the brain (Brown et al, 2019), and the PLK4driven centriole biogenesis oscillator, which is entrained by the cell-cycle oscillator (Aydogan et al, 2020).…”

Section: Entrainmentmentioning

confidence: 99%

“…Circadian oscillators ( Bell-Pedersen et al, 2005 ) and Cyclin/CDK cell cycle oscillators ( Örd and Loog, 2019 ) are perhaps the best known examples of this style of clock, but oscillators are also found in other contexts in which biological processes are regularly repeated or require periodicity. Take, for example, the formation of a new procentriole during centriole duplication in Drosophila embryos ( Aydogan et al, 2020 ). The amount of material integrated into the new procentriole is controlled by oscillations in the recruitment of the master regulator Polo-like kinase 4 (PLK4) by its receptor Asterless.…”

Section: The Fundamentals Of Cellular Clocksmentioning

confidence: 99%

Keeping track of time: The fundamentals of cellular clocks

Gliech

Holland

2020

Journal of Cell Biology

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Biological timekeeping enables the coordination and execution of complex cellular processes such as developmental programs, day/night organismal changes, intercellular signaling, and proliferative safeguards. While these systems are often considered separately owing to a wide variety of mechanisms, time frames, and outputs, all clocks are built by calibrating or delaying the rate of biochemical reactions and processes. In this review, we explore the common themes and core design principles of cellular clocks, giving special consideration to the challenges associated with building timers from biochemical components. We also outline how evolution has coopted time to increase the reliability of a diverse range of biological systems.

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An Autonomous Oscillation Times and Executes Centriole Biogenesis

Cited by 35 publications

References 85 publications

PLK4-phosphorylated NEDD1 facilitates cartwheel assembly and centriole biogenesis initiations

PLK4-phosphorylated NEDD1 facilitates cartwheel assembly and centriole biogenesis initiations

Autonomous clocks that regulate organelle biogenesis, cytoskeletal organization, and intracellular dynamics

Keeping track of time: The fundamentals of cellular clocks

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