Distinct roles of centriole distal appendage proteins in ciliary assembly and disassembly

Abstract The primary cilium is a cellular organelle whose assembly and disassembly are closely linked to the cell cycle. The centriole distal appendage (DA) is essential for the early stages of ciliogenesis by anchoring the mother centriole to the cell surface. Despite the identification of over twe...

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Main Authors: Su-yeon Je, Hyuk Wan Ko
Format: Article
Language:English
Published: BMC 2024-12-01
Series:Cell Communication and Signaling
Subjects:
Online Access:https://doi.org/10.1186/s12964-024-01962-7
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author Su-yeon Je
Hyuk Wan Ko
author_facet Su-yeon Je
Hyuk Wan Ko
author_sort Su-yeon Je
collection DOAJ
description Abstract The primary cilium is a cellular organelle whose assembly and disassembly are closely linked to the cell cycle. The centriole distal appendage (DA) is essential for the early stages of ciliogenesis by anchoring the mother centriole to the cell surface. Despite the identification of over twelve proteins constituting the DA, including CEP83, CEP89, CEP164, FBF1, and SCLT1, their specific functions in ciliary dynamics are not fully understood. Here, we elucidate the precise role of DA proteins in ciliary assembly and disassembly. While Cep89 mutant cells exhibit normal ciliogenesis, the kinetics of ciliary disassembly is significantly delayed. Through siRNA-mediated knockdown of DA proteins, we identified two functional subgroups within DA proteins: CEP83, SCLT1, and CEP164, which are primarily essential for ciliary assembly and centriole docking, and CEP89 and FBF1, which specifically regulate ciliary disassembly. Notably, the depletion of CEP89 and FBF1 not only impedes ciliary disassembly but also disrupts the Aurora A kinase signaling pathway, leading to its downregulation and mislocalization at the basal body during serum-induced cell cycle re-entry. These findings suggest that DA components can be functionally categorized into two modules responsible for distinct aspects of ciliary dynamics, with broad implications for cellular signaling, homeostasis, and development.
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spelling doaj-art-e7885eeb1f3841568daed75ca9e858d32025-08-20T01:57:16ZengBMCCell Communication and Signaling1478-811X2024-12-0122111010.1186/s12964-024-01962-7Distinct roles of centriole distal appendage proteins in ciliary assembly and disassemblySu-yeon Je0Hyuk Wan Ko1Department of Biochemistry, College of Life Science and Biotechnology, Yonsei UniversityDepartment of Biochemistry, College of Life Science and Biotechnology, Yonsei UniversityAbstract The primary cilium is a cellular organelle whose assembly and disassembly are closely linked to the cell cycle. The centriole distal appendage (DA) is essential for the early stages of ciliogenesis by anchoring the mother centriole to the cell surface. Despite the identification of over twelve proteins constituting the DA, including CEP83, CEP89, CEP164, FBF1, and SCLT1, their specific functions in ciliary dynamics are not fully understood. Here, we elucidate the precise role of DA proteins in ciliary assembly and disassembly. While Cep89 mutant cells exhibit normal ciliogenesis, the kinetics of ciliary disassembly is significantly delayed. Through siRNA-mediated knockdown of DA proteins, we identified two functional subgroups within DA proteins: CEP83, SCLT1, and CEP164, which are primarily essential for ciliary assembly and centriole docking, and CEP89 and FBF1, which specifically regulate ciliary disassembly. Notably, the depletion of CEP89 and FBF1 not only impedes ciliary disassembly but also disrupts the Aurora A kinase signaling pathway, leading to its downregulation and mislocalization at the basal body during serum-induced cell cycle re-entry. These findings suggest that DA components can be functionally categorized into two modules responsible for distinct aspects of ciliary dynamics, with broad implications for cellular signaling, homeostasis, and development.https://doi.org/10.1186/s12964-024-01962-7Primary ciliumCiliogenesisDistal appendageCEP89Ciliary disassemblyAurora A
spellingShingle Su-yeon Je
Hyuk Wan Ko
Distinct roles of centriole distal appendage proteins in ciliary assembly and disassembly
Cell Communication and Signaling
Primary cilium
Ciliogenesis
Distal appendage
CEP89
Ciliary disassembly
Aurora A
title Distinct roles of centriole distal appendage proteins in ciliary assembly and disassembly
title_full Distinct roles of centriole distal appendage proteins in ciliary assembly and disassembly
title_fullStr Distinct roles of centriole distal appendage proteins in ciliary assembly and disassembly
title_full_unstemmed Distinct roles of centriole distal appendage proteins in ciliary assembly and disassembly
title_short Distinct roles of centriole distal appendage proteins in ciliary assembly and disassembly
title_sort distinct roles of centriole distal appendage proteins in ciliary assembly and disassembly
topic Primary cilium
Ciliogenesis
Distal appendage
CEP89
Ciliary disassembly
Aurora A
url https://doi.org/10.1186/s12964-024-01962-7
work_keys_str_mv AT suyeonje distinctrolesofcentrioledistalappendageproteinsinciliaryassemblyanddisassembly
AT hyukwanko distinctrolesofcentrioledistalappendageproteinsinciliaryassemblyanddisassembly