Promotion and Suppression of Centriole Duplication Are Catalytically Coupled through PLK4 to Ensure Centriole Homeostasis

PLK4 is the major kinase driving centriole duplication. Duplication occurs only once per cell cycle, forming one new (or daughter) centriole that is tightly engaged to the preexisting (or mother) centriole. Centriole engagement is known to block the reduplication of mother centrioles, but the molecu...

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Main Authors: Minhee Kim, Brian P. O’Rourke, Rajesh Kumar Soni, Prasad V. Jallepalli, Ronald C. Hendrickson, Meng-Fu Bryan Tsou
Format: Article
Language:English
Published: Elsevier 2016-08-01
Series:Cell Reports
Online Access:http://www.sciencedirect.com/science/article/pii/S2211124716308385
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spelling doaj-37922f7e5c5b4cfe90a084fafd58416c2020-11-24T21:30:46ZengElsevierCell Reports2211-12472016-08-011651195120310.1016/j.celrep.2016.06.069Promotion and Suppression of Centriole Duplication Are Catalytically Coupled through PLK4 to Ensure Centriole HomeostasisMinhee Kim0Brian P. O’Rourke1Rajesh Kumar Soni2Prasad V. Jallepalli3Ronald C. Hendrickson4Meng-Fu Bryan Tsou5Cell Biology Program, Memorial Sloan-Kettering Cancer Center, New York, NY 10065, USACell Biology Program, Memorial Sloan-Kettering Cancer Center, New York, NY 10065, USAMicrochemistry and Proteomics Core Facility, Memorial Sloan-Kettering Cancer Center, New York, NY 10065 USAMolecular Biology Program, Memorial Sloan-Kettering Cancer Center, New York, NY 10065, USAMicrochemistry and Proteomics Core Facility, Memorial Sloan-Kettering Cancer Center, New York, NY 10065 USACell Biology Program, Memorial Sloan-Kettering Cancer Center, New York, NY 10065, USAPLK4 is the major kinase driving centriole duplication. Duplication occurs only once per cell cycle, forming one new (or daughter) centriole that is tightly engaged to the preexisting (or mother) centriole. Centriole engagement is known to block the reduplication of mother centrioles, but the molecular identity responsible for the block remains unclear. Here, we show that the centriolar cartwheel, the geometric scaffold for centriole assembly, forms the identity of daughter centrioles essential for the block, ceasing further duplication of the mother centriole to which it is engaged. To ensure a steady block, we found that the cartwheel requires constant maintenance by PLK4 through phosphorylation of the same substrate that drives centriole assembly, revealing a parsimonious control in which “assembly” and “block for new assembly” are linked through the same catalytic reaction to achieve homeostasis. Our results support a recently deduced model that the cartwheel-bound PLK4 directly suppresses centriole reduplication.http://www.sciencedirect.com/science/article/pii/S2211124716308385
collection DOAJ
language English
format Article
sources DOAJ
author Minhee Kim
Brian P. O’Rourke
Rajesh Kumar Soni
Prasad V. Jallepalli
Ronald C. Hendrickson
Meng-Fu Bryan Tsou
spellingShingle Minhee Kim
Brian P. O’Rourke
Rajesh Kumar Soni
Prasad V. Jallepalli
Ronald C. Hendrickson
Meng-Fu Bryan Tsou
Promotion and Suppression of Centriole Duplication Are Catalytically Coupled through PLK4 to Ensure Centriole Homeostasis
Cell Reports
author_facet Minhee Kim
Brian P. O’Rourke
Rajesh Kumar Soni
Prasad V. Jallepalli
Ronald C. Hendrickson
Meng-Fu Bryan Tsou
author_sort Minhee Kim
title Promotion and Suppression of Centriole Duplication Are Catalytically Coupled through PLK4 to Ensure Centriole Homeostasis
title_short Promotion and Suppression of Centriole Duplication Are Catalytically Coupled through PLK4 to Ensure Centriole Homeostasis
title_full Promotion and Suppression of Centriole Duplication Are Catalytically Coupled through PLK4 to Ensure Centriole Homeostasis
title_fullStr Promotion and Suppression of Centriole Duplication Are Catalytically Coupled through PLK4 to Ensure Centriole Homeostasis
title_full_unstemmed Promotion and Suppression of Centriole Duplication Are Catalytically Coupled through PLK4 to Ensure Centriole Homeostasis
title_sort promotion and suppression of centriole duplication are catalytically coupled through plk4 to ensure centriole homeostasis
publisher Elsevier
series Cell Reports
issn 2211-1247
publishDate 2016-08-01
description PLK4 is the major kinase driving centriole duplication. Duplication occurs only once per cell cycle, forming one new (or daughter) centriole that is tightly engaged to the preexisting (or mother) centriole. Centriole engagement is known to block the reduplication of mother centrioles, but the molecular identity responsible for the block remains unclear. Here, we show that the centriolar cartwheel, the geometric scaffold for centriole assembly, forms the identity of daughter centrioles essential for the block, ceasing further duplication of the mother centriole to which it is engaged. To ensure a steady block, we found that the cartwheel requires constant maintenance by PLK4 through phosphorylation of the same substrate that drives centriole assembly, revealing a parsimonious control in which “assembly” and “block for new assembly” are linked through the same catalytic reaction to achieve homeostasis. Our results support a recently deduced model that the cartwheel-bound PLK4 directly suppresses centriole reduplication.
url http://www.sciencedirect.com/science/article/pii/S2211124716308385
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