Interactions of N- and C-terminal parts of Ana1 permitting centriole duplication but not elongation

The conserved process of centriole duplication requires the establishment of a Sas6-centred cartwheel initiated by Plk4’s phosphorylation of Ana1/STIL. Subsequently, the centriole undergoes conversion to a centrosome requiring its radial expansion and elongation, mediated by a network requiring inte...

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Main Authors: Agota Nagy, Levente Kovacs, Helene Rangone, Jingyan Fu, Mark Ladinsky, David M. Glover
Format: Article
Language:English
Published: The Royal Society 2025-02-01
Series:Open Biology
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Online Access:https://royalsocietypublishing.org/doi/10.1098/rsob.240325
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author Agota Nagy
Levente Kovacs
Helene Rangone
Jingyan Fu
Mark Ladinsky
David M. Glover
author_facet Agota Nagy
Levente Kovacs
Helene Rangone
Jingyan Fu
Mark Ladinsky
David M. Glover
author_sort Agota Nagy
collection DOAJ
description The conserved process of centriole duplication requires the establishment of a Sas6-centred cartwheel initiated by Plk4’s phosphorylation of Ana1/STIL. Subsequently, the centriole undergoes conversion to a centrosome requiring its radial expansion and elongation, mediated by a network requiring interactions between Cep135, Ana1/Cep295 and Asterless/Cep152. Here, we show that mutant alleles encoding overlapping N- and C-terminal parts of Ana1 are capable of intragenic complementation to rescue radial expansion. This permits the recruitment of Asl and thereby centriole duplication and mechanosensory cilia formation to restore the coordination defects of these mutants. This genetic combination also rescues centriole duplication in the male germ line but does not rescue the elongation of the triplet microtubule-containing centrioles of primary spermatocytes. Consequently, these males are coordinated but sterile. Such centriole elongation is rescued by the continuous, full-length Ana1 sequence. We define a region that when deleted within otherwise intact Ana1 does not permit primary spermatocyte centrioles to elongate but still allows recruitment of Asl. Our findings point to differing demands upon the physical organization of Ana1 for the distinct processes of radial expansion and elongation of centrioles.
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spelling doaj-art-00a6c2a4a24c491eace5a92f8e53b09f2025-02-05T00:05:21ZengThe Royal SocietyOpen Biology2046-24412025-02-0115210.1098/rsob.240325Interactions of N- and C-terminal parts of Ana1 permitting centriole duplication but not elongationAgota Nagy0Levente Kovacs1Helene Rangone2Jingyan Fu3Mark Ladinsky4David M. Glover5Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA 91125, USADivision of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA 91125, USADepartment of Genetics, University of Cambridge, Cambridge CB2 3EH, UKDepartment of Genetics, University of Cambridge, Cambridge CB2 3EH, UKDivision of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA 91125, USADivision of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA 91125, USAThe conserved process of centriole duplication requires the establishment of a Sas6-centred cartwheel initiated by Plk4’s phosphorylation of Ana1/STIL. Subsequently, the centriole undergoes conversion to a centrosome requiring its radial expansion and elongation, mediated by a network requiring interactions between Cep135, Ana1/Cep295 and Asterless/Cep152. Here, we show that mutant alleles encoding overlapping N- and C-terminal parts of Ana1 are capable of intragenic complementation to rescue radial expansion. This permits the recruitment of Asl and thereby centriole duplication and mechanosensory cilia formation to restore the coordination defects of these mutants. This genetic combination also rescues centriole duplication in the male germ line but does not rescue the elongation of the triplet microtubule-containing centrioles of primary spermatocytes. Consequently, these males are coordinated but sterile. Such centriole elongation is rescued by the continuous, full-length Ana1 sequence. We define a region that when deleted within otherwise intact Ana1 does not permit primary spermatocyte centrioles to elongate but still allows recruitment of Asl. Our findings point to differing demands upon the physical organization of Ana1 for the distinct processes of radial expansion and elongation of centrioles.https://royalsocietypublishing.org/doi/10.1098/rsob.240325Ana1centriolecentrosomeDrosophila
spellingShingle Agota Nagy
Levente Kovacs
Helene Rangone
Jingyan Fu
Mark Ladinsky
David M. Glover
Interactions of N- and C-terminal parts of Ana1 permitting centriole duplication but not elongation
Open Biology
Ana1
centriole
centrosome
Drosophila
title Interactions of N- and C-terminal parts of Ana1 permitting centriole duplication but not elongation
title_full Interactions of N- and C-terminal parts of Ana1 permitting centriole duplication but not elongation
title_fullStr Interactions of N- and C-terminal parts of Ana1 permitting centriole duplication but not elongation
title_full_unstemmed Interactions of N- and C-terminal parts of Ana1 permitting centriole duplication but not elongation
title_short Interactions of N- and C-terminal parts of Ana1 permitting centriole duplication but not elongation
title_sort interactions of n and c terminal parts of ana1 permitting centriole duplication but not elongation
topic Ana1
centriole
centrosome
Drosophila
url https://royalsocietypublishing.org/doi/10.1098/rsob.240325
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AT jingyanfu interactionsofnandcterminalpartsofana1permittingcentrioleduplicationbutnotelongation
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