A homeostatic clock sets daughter centriole size in flies

Mustafa G Aydogan; Alan Wainman; Saroj Saurya; Thomas L Steinacker; Anna Caballe; Zsofia A Novak; Janina Baumbach; Nadine Muschalik; Jordan W Raff

doi:10.1083/jcb.201801014

A homeostatic clock sets daughter centriole size in flies

J Cell Biol. 2018 Apr 2;217(4):1233-1248. doi: 10.1083/jcb.201801014. Epub 2018 Mar 2.

Authors

Mustafa G Aydogan¹, Alan Wainman^{1

2}, Saroj Saurya¹, Thomas L Steinacker¹, Anna Caballe¹, Zsofia A Novak¹, Janina Baumbach¹, Nadine Muschalik¹, Jordan W Raff³

Affiliations

¹ Sir William Dunn School of Pathology, University of Oxford, Oxford, England, UK.
² Micron Oxford Advanced Bioimaging Unit, Department of Biochemistry, University of Oxford, Oxford, England, UK.
³ Sir William Dunn School of Pathology, University of Oxford, Oxford, England, UK [email protected].

Abstract

Centrioles are highly structured organelles whose size is remarkably consistent within any given cell type. New centrioles are born when Polo-like kinase 4 (Plk4) recruits Ana2/STIL and Sas-6 to the side of an existing "mother" centriole. These two proteins then assemble into a cartwheel, which grows outwards to form the structural core of a new daughter. Here, we show that in early Drosophila melanogaster embryos, daughter centrioles grow at a linear rate during early S-phase and abruptly stop growing when they reach their correct size in mid- to late S-phase. Unexpectedly, the cartwheel grows from its proximal end, and Plk4 determines both the rate and period of centriole growth: the more active the centriolar Plk4, the faster centrioles grow, but the faster centriolar Plk4 is inactivated and growth ceases. Thus, Plk4 functions as a homeostatic clock, establishing an inverse relationship between growth rate and period to ensure that daughter centrioles grow to the correct size.

Publication types

Research Support, Non-U.S. Gov't
Video-Audio Media

MeSH terms

Animals
Behavior, Animal
Cell Cycle Proteins / genetics
Cell Cycle Proteins / metabolism
Centrioles / enzymology*
Centrioles / genetics
Circadian Rhythm Signaling Peptides and Proteins / genetics
Circadian Rhythm Signaling Peptides and Proteins / metabolism*
Drosophila Proteins / genetics
Drosophila Proteins / metabolism*
Drosophila melanogaster / embryology
Drosophila melanogaster / enzymology*
Drosophila melanogaster / genetics
Embryo, Nonmammalian / enzymology
Homeostasis
Locomotion
Microtubule-Associated Proteins / genetics
Microtubule-Associated Proteins / metabolism
Mutation
Protein Binding
Protein Serine-Threonine Kinases / genetics
Protein Serine-Threonine Kinases / metabolism*
Protein Transport
S Phase*
Signal Transduction
Time Factors

Substances

Ana2 protein, Drosophila
Cell Cycle Proteins
Circadian Rhythm Signaling Peptides and Proteins
Drosophila Proteins
Microtubule-Associated Proteins
Sas-6 protein, Drosophila
Protein Serine-Threonine Kinases
Sak protein, Drosophila

Abstract

Publication types

MeSH terms

Substances

Grants and funding