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...
Main Authors: | , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
Elsevier
2016-08-01
|
Series: | Cell Reports |
Online Access: | http://www.sciencedirect.com/science/article/pii/S2211124716308385 |
id |
doaj-37922f7e5c5b4cfe90a084fafd58416c |
---|---|
record_format |
Article |
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 |
work_keys_str_mv |
AT minheekim promotionandsuppressionofcentrioleduplicationarecatalyticallycoupledthroughplk4toensurecentriolehomeostasis AT brianporourke promotionandsuppressionofcentrioleduplicationarecatalyticallycoupledthroughplk4toensurecentriolehomeostasis AT rajeshkumarsoni promotionandsuppressionofcentrioleduplicationarecatalyticallycoupledthroughplk4toensurecentriolehomeostasis AT prasadvjallepalli promotionandsuppressionofcentrioleduplicationarecatalyticallycoupledthroughplk4toensurecentriolehomeostasis AT ronaldchendrickson promotionandsuppressionofcentrioleduplicationarecatalyticallycoupledthroughplk4toensurecentriolehomeostasis AT mengfubryantsou promotionandsuppressionofcentrioleduplicationarecatalyticallycoupledthroughplk4toensurecentriolehomeostasis |
_version_ |
1725961852672802816 |