An Autonomous Oscillation Times and Executes Centriole Biogenesis.


Journal

Cell
ISSN: 1097-4172
Titre abrégé: Cell
Pays: United States
ID NLM: 0413066

Informations de publication

Date de publication:
25 06 2020
Historique:
received: 05 04 2019
revised: 19 12 2019
accepted: 08 05 2020
pubmed: 13 6 2020
medline: 22 1 2021
entrez: 13 6 2020
Statut: ppublish

Résumé

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.

Identifiants

pubmed: 32531200
pii: S0092-8674(20)30613-9
doi: 10.1016/j.cell.2020.05.018
pmc: PMC7327525
pii:
doi:

Substances chimiques

Cell Cycle Proteins 0
Drosophila Proteins 0
Protein Serine-Threonine Kinases EC 2.7.11.1
Sak protein, Drosophila EC 2.7.11.1

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1566-1581.e27

Subventions

Organisme : Wellcome Trust
ID : 107457
Pays : United Kingdom
Organisme : Cancer Research UK
ID : C5255/A23225
Pays : United Kingdom
Organisme : Biotechnology and Biological Sciences Research Council
ID : BB/N016858/1
Pays : United Kingdom
Organisme : Wellcome Trust
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 104575
Pays : United Kingdom

Informations de copyright

Copyright © 2020 The Author(s). Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of Interests The authors declare no competing interests.

Références

Science. 2008 Jul 4;321(5885):126-9
pubmed: 18599789
Elife. 2019 Sep 09;8:
pubmed: 31498081
J Microsc. 2008 Nov;232(2):343-52
pubmed: 19017233
Cell. 2010 Apr 16;141(2):224-6
pubmed: 20403319
J Cell Biol. 2009 Jan 26;184(2):225-39
pubmed: 19171756
Cell. 2010 Apr 16;141(2):268-79
pubmed: 20403323
Wiley Interdiscip Rev Syst Biol Med. 2015 Sep-Oct;7(5):301-16
pubmed: 26033862
Cell Rep. 2018 Jul 10;24(2):503-514
pubmed: 29996109
Methods. 2017 Feb 15;115:80-90
pubmed: 27713081
Curr Biol. 2013 Nov 18;23(22):2255-2261
pubmed: 24184097
Cell. 2011 Feb 4;144(3):364-75
pubmed: 21277013
J Cell Biol. 2018 Apr 2;217(4):1233-1248
pubmed: 29500190
J Cell Biol. 2015 Feb 16;208(4):401-14
pubmed: 25688134
Nature. 1997 Jul 3;388(6637):93-7
pubmed: 9214509
Annu Rev Biophys. 2016 Jul 5;45:49-64
pubmed: 27145879
Biol Open. 2019 Sep 18;8(9):
pubmed: 31533936
Genetics. 2000 May;155(1):159-66
pubmed: 10790391
Curr Biol. 2008 Feb 26;18(4):245-54
pubmed: 18291653
Cell. 2016 Dec 15;167(7):1750-1761.e16
pubmed: 27984725
J Cell Biol. 2010 Nov 15;191(4):721-9
pubmed: 21059850
Proc Natl Acad Sci U S A. 2001 Feb 27;98(5):2399-406
pubmed: 11226251
Curr Biol. 2012 May 8;22(9):R330-9
pubmed: 22575475
J Cell Sci. 2019 Feb 20;132(4):
pubmed: 30787112
Dev Cell. 2016 Aug 22;38(4):399-412
pubmed: 27554859
Nat Commun. 2019 Apr 18;10(1):1810
pubmed: 31000710
iScience. 2018 Oct 26;8:222-235
pubmed: 30340068
J Cell Sci. 2010 Jul 1;123(Pt 13):2163-9
pubmed: 20516151
Nat Commun. 2014 Oct 24;5:5267
pubmed: 25342035
PLoS Genet. 2015 May 28;11(5):e1005261
pubmed: 26020779
Biophys J. 2008 Feb 15;94(4):1437-48
pubmed: 17933881
Biochem Soc Trans. 2016 Oct 15;44(5):1253-1263
pubmed: 27911707
Bioinformatics. 2016 Mar 15;32(6):958-60
pubmed: 26589275
Nat Commun. 2018 Apr 19;9(1):1553
pubmed: 29674717
Elife. 2014 Jun 10;3:e02678
pubmed: 24916159
Cell Syst. 2016 Feb 24;2(2):62-7
pubmed: 27135159
Curr Biol. 2004 Dec 14;14(23):2143-8
pubmed: 15589158
Biol Open. 2015 Feb 20;4(3):370-7
pubmed: 25701666
FEBS Lett. 2007 Jan 9;581(1):77-83
pubmed: 17174311
Curr Biol. 2009 Jan 13;19(1):43-9
pubmed: 19084407
J Evol Biol. 2009 Feb;22(2):430-4
pubmed: 19032497
Trends Genet. 2011 Aug;27(8):307-15
pubmed: 21680046
Nat Rev Mol Cell Biol. 2008 Dec;9(12):981-91
pubmed: 18971947
Curr Biol. 2014 Jun 2;24(11):1276-82
pubmed: 24835456
Mol Biol Cell. 2008 Jul;19(7):3163-78
pubmed: 18463166
Annu Rev Cell Dev Biol. 2017 Oct 6;33:23-49
pubmed: 28813178
J Cell Biol. 2010 Jan 25;188(2):191-8
pubmed: 20100909
J Cell Biol. 2010 Nov 15;191(4):731-9
pubmed: 21059844
Curr Biol. 2007 Feb 20;17(4):293-303
pubmed: 17306545
Curr Biol. 2013 Nov 18;23(22):2245-2254
pubmed: 24184099
Elife. 2014 Jan 01;3:e01812
pubmed: 24596152
Genes Dev. 1998 Dec 1;12(23):3741-51
pubmed: 9851980
Curr Biol. 2014 Nov 3;24(21):2526-32
pubmed: 25264260
Nat Commun. 2019 Oct 31;10(1):4959
pubmed: 31672968
J Biol Chem. 2000 Jan 28;275(4):2247-50
pubmed: 10644669
Science. 2011 Mar 4;331(6021):1196-9
pubmed: 21273447
J Cell Biol. 1995 Jul;130(1):105-15
pubmed: 7790366
J Cell Biol. 1990 Jun;110(6):2033-42
pubmed: 2190990
Science. 2010 Mar 19;327(5972):1522-6
pubmed: 20299597
Science. 1943 May 21;97(2525):451-6
pubmed: 17789864
Trends Genet. 1996 Sep;12(9):345-50
pubmed: 8855663
J Cell Biol. 2019 Feb 4;218(2):395-409
pubmed: 30446607
Cell. 2008 Jun 13;133(6):1032-42
pubmed: 18555779
Genetics. 2008 Dec;180(4):2081-94
pubmed: 18854586
J Cell Biol. 1990 Jun;110(6):2025-32
pubmed: 2351692
J Cell Biol. 2018 Apr 2;217(4):1217-1231
pubmed: 29496738
Nature. 2013 Aug 29;500(7464):603-7
pubmed: 23863935
Cell. 2009 Nov 13;139(4):663-78
pubmed: 19914163
PLoS Biol. 2008 Sep 16;6(9):e224
pubmed: 18798690
Biochem J. 2009 Mar 15;418(3):567-74
pubmed: 19143658
Science. 2018 Apr 20;360(6386):
pubmed: 29674564
Sci Rep. 2015 Nov 03;5:15915
pubmed: 26525406
Mol Biol Cell. 2018 Nov 15;29(23):2874-2886
pubmed: 30256714
Philos Trans R Soc Lond B Biol Sci. 2014 Sep 5;369(1650):
pubmed: 25047614
Elife. 2015 Nov 04;4:
pubmed: 26530814
Microsc Res Tech. 2014 Jul;77(7):528-36
pubmed: 24729575
Nature. 2010 Oct 7;467(7316):714-8
pubmed: 20852615
Nat Rev Mol Cell Biol. 2018 May;19(5):297-312
pubmed: 29363672
Nat Methods. 2013 May;10(5):407-9
pubmed: 23524392
Science. 2003 Oct 10;302(5643):255-9
pubmed: 12934012

Auteurs

Mustafa G Aydogan (MG)

Sir William Dunn School of Pathology, University of Oxford, Oxford OX1 3RE, UK. Electronic address: mustafa.aydogan@path.ox.ac.uk.

Thomas L Steinacker (TL)

Sir William Dunn School of Pathology, University of Oxford, Oxford OX1 3RE, UK.

Mohammad Mofatteh (M)

Sir William Dunn School of Pathology, University of Oxford, Oxford OX1 3RE, UK.

Zachary M Wilmott (ZM)

Sir William Dunn School of Pathology, University of Oxford, Oxford OX1 3RE, UK; Mathematical Institute, University of Oxford, Oxford OX2 6GG, UK.

Felix Y Zhou (FY)

Ludwig Institute for Cancer Research, University of Oxford, Oxford OX3 7DQ, UK.

Lisa Gartenmann (L)

Sir William Dunn School of Pathology, University of Oxford, Oxford OX1 3RE, UK.

Alan Wainman (A)

Sir William Dunn School of Pathology, University of Oxford, Oxford OX1 3RE, UK.

Saroj Saurya (S)

Sir William Dunn School of Pathology, University of Oxford, Oxford OX1 3RE, UK.

Zsofia A Novak (ZA)

Sir William Dunn School of Pathology, University of Oxford, Oxford OX1 3RE, UK.

Siu-Shing Wong (SS)

Sir William Dunn School of Pathology, University of Oxford, Oxford OX1 3RE, UK.

Alain Goriely (A)

Mathematical Institute, University of Oxford, Oxford OX2 6GG, UK.

Michael A Boemo (MA)

Sir William Dunn School of Pathology, University of Oxford, Oxford OX1 3RE, UK. Electronic address: mb915@cam.ac.uk.

Jordan W Raff (JW)

Sir William Dunn School of Pathology, University of Oxford, Oxford OX1 3RE, UK. Electronic address: jordan.raff@path.ox.ac.uk.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH