An autonomous oscillation times and executes centriole biogenesis

The accurate timing and execution of organelle biogenesis is crucial for cell physiology. Centriole biogenesis is regulated by Polo-like kinase 4 (Plk4) and initiates in S-phase when a daughter centriole grows from the side of a pre-existing mother. Here, we show that a Plk4 oscillation at the base...

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Main Authors: Aydogan, MG, Steinacker, TL, Mofatteh, M, Wilmott, ZM, Zhou, FY, Gartenmann, L, Wainman, A, Saurya, S, Novak, ZA, Wong, SS, Goriely, A, Boemo, MA, Raff, JW
Format: Journal article
Language:English
Published: Elsevier 2020
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author Aydogan, MG
Steinacker, TL
Mofatteh, M
Wilmott, ZM
Zhou, FY
Gartenmann, L
Wainman, A
Saurya, S
Novak, ZA
Wong, SS
Goriely, A
Boemo, MA
Raff, JW
author_facet Aydogan, MG
Steinacker, TL
Mofatteh, M
Wilmott, ZM
Zhou, FY
Gartenmann, L
Wainman, A
Saurya, S
Novak, ZA
Wong, SS
Goriely, A
Boemo, MA
Raff, JW
author_sort Aydogan, MG
collection OXFORD
description The accurate timing and execution of organelle biogenesis is crucial for cell physiology. Centriole biogenesis is regulated by Polo-like kinase 4 (Plk4) and initiates in S-phase when a daughter centriole grows from the side of a pre-existing mother. Here, we show that a Plk4 oscillation at the base of the growing centriole initiates and times centriole biogenesis to ensure that centrioles grow at the right time and to the right size. The Plk4 oscillation is normally entrained to the cell-cycle oscillator but can run autonomously of it—potentially explaining why centrioles can duplicate independently of cell-cycle progression. Mathematical modeling indicates that the Plk4 oscillation can be generated by a time-delayed negative feedback loop in which Plk4 inactivates the interaction with its centriolar receptor through multiple rounds of phosphorylation. We hypothesize that similar organelle-specific oscillations could regulate the timing and execution of organelle biogenesis more generally.
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spelling oxford-uuid:6d37f4e8-b887-40fa-a41a-b421903396422022-03-26T19:16:30ZAn autonomous oscillation times and executes centriole biogenesisJournal articlehttp://purl.org/coar/resource_type/c_dcae04bcuuid:6d37f4e8-b887-40fa-a41a-b42190339642EnglishSymplectic ElementsElsevier2020Aydogan, MGSteinacker, TLMofatteh, MWilmott, ZMZhou, FYGartenmann, LWainman, ASaurya, SNovak, ZAWong, SSGoriely, ABoemo, MARaff, JWThe accurate timing and execution of organelle biogenesis is crucial for cell physiology. Centriole biogenesis is regulated by Polo-like kinase 4 (Plk4) and initiates in S-phase when a daughter centriole grows from the side of a pre-existing mother. Here, we show that a Plk4 oscillation at the base of the growing centriole initiates and times centriole biogenesis to ensure that centrioles grow at the right time and to the right size. The Plk4 oscillation is normally entrained to the cell-cycle oscillator but can run autonomously of it—potentially explaining why centrioles can duplicate independently of cell-cycle progression. Mathematical modeling indicates that the Plk4 oscillation can be generated by a time-delayed negative feedback loop in which Plk4 inactivates the interaction with its centriolar receptor through multiple rounds of phosphorylation. We hypothesize that similar organelle-specific oscillations could regulate the timing and execution of organelle biogenesis more generally.
spellingShingle Aydogan, MG
Steinacker, TL
Mofatteh, M
Wilmott, ZM
Zhou, FY
Gartenmann, L
Wainman, A
Saurya, S
Novak, ZA
Wong, SS
Goriely, A
Boemo, MA
Raff, JW
An autonomous oscillation times and executes centriole biogenesis
title An autonomous oscillation times and executes centriole biogenesis
title_full An autonomous oscillation times and executes centriole biogenesis
title_fullStr An autonomous oscillation times and executes centriole biogenesis
title_full_unstemmed An autonomous oscillation times and executes centriole biogenesis
title_short An autonomous oscillation times and executes centriole biogenesis
title_sort autonomous oscillation times and executes centriole biogenesis
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