Cargando…

Proteomic analysis of multiple primary cilia reveals a novel mode of ciliary development in mammals

Cilia are structurally and functionally diverse organelles, whose malfunction leads to ciliopathies. While recent studies have uncovered common ciliary transport mechanisms, limited information is available on the proteome of cilia, particularly that of sensory subtypes, which could provide insight...

Descripción completa

Detalles Bibliográficos
Autores principales: Narita, Keishi, Kozuka-Hata, Hiroko, Nonami, Yuta, Ao-Kondo, Hiroko, Suzuki, Toshimitsu, Nakamura, Hideki, Yamakawa, Kazuhiro, Oyama, Masaaki, Inoue, Takafumi, Takeda, Sen
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Company of Biologists 2012
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3507226/
https://www.ncbi.nlm.nih.gov/pubmed/23213475
http://dx.doi.org/10.1242/bio.20121081
_version_ 1782251043805986816
author Narita, Keishi
Kozuka-Hata, Hiroko
Nonami, Yuta
Ao-Kondo, Hiroko
Suzuki, Toshimitsu
Nakamura, Hideki
Yamakawa, Kazuhiro
Oyama, Masaaki
Inoue, Takafumi
Takeda, Sen
author_facet Narita, Keishi
Kozuka-Hata, Hiroko
Nonami, Yuta
Ao-Kondo, Hiroko
Suzuki, Toshimitsu
Nakamura, Hideki
Yamakawa, Kazuhiro
Oyama, Masaaki
Inoue, Takafumi
Takeda, Sen
author_sort Narita, Keishi
collection PubMed
description Cilia are structurally and functionally diverse organelles, whose malfunction leads to ciliopathies. While recent studies have uncovered common ciliary transport mechanisms, limited information is available on the proteome of cilia, particularly that of sensory subtypes, which could provide insight into their functional and developmental diversities. In the present study, we performed proteomic analysis of unique, multiple 9+0 cilia in choroid plexus epithelial cells (CPECs). The analysis of juvenile swine CPEC cilia identified 868 proteins. Among them, 396 were shared with the proteome of 9+0 photoreceptor cilia (outer segment), whereas only 152 were shared with the proteome of 9+2 cilia and flagella. Various signaling molecules were enriched in a CPEC-specific ciliome subset, implicating multiplicity of sensory functions. The ciliome also included molecules for ciliary motility such as Rsph9. In CPECs from juvenile swine or adult mouse, Rsph9 was localized to a subpopulation of cilia, whereas they were non-motile. Live imaging of mouse choroid plexus revealed that neonatal CPEC cilia could beat vigorously, and the motility waned and was lost within 1–2 weeks. The beating characteristics of neonatal CPEC cilia were variable and different from those of typical 9+2 cilia of ependyma, yet an Efhc1-mediated mechanism to regulate the beating frequency was shared in both types of cilia. Notably, ultrastructural analysis revealed the presence of not only 9+0 but also 9+2 and atypical ciliary subtypes in neonatal CPEC. Overall, these results identified both conserved and variable components of sensory cilia, and demonstrated a novel mode of ciliary development in mammals.
format Online
Article
Text
id pubmed-3507226
institution National Center for Biotechnology Information
language English
publishDate 2012
publisher The Company of Biologists
record_format MEDLINE/PubMed
spelling pubmed-35072262012-12-04 Proteomic analysis of multiple primary cilia reveals a novel mode of ciliary development in mammals Narita, Keishi Kozuka-Hata, Hiroko Nonami, Yuta Ao-Kondo, Hiroko Suzuki, Toshimitsu Nakamura, Hideki Yamakawa, Kazuhiro Oyama, Masaaki Inoue, Takafumi Takeda, Sen Biol Open Research Article Cilia are structurally and functionally diverse organelles, whose malfunction leads to ciliopathies. While recent studies have uncovered common ciliary transport mechanisms, limited information is available on the proteome of cilia, particularly that of sensory subtypes, which could provide insight into their functional and developmental diversities. In the present study, we performed proteomic analysis of unique, multiple 9+0 cilia in choroid plexus epithelial cells (CPECs). The analysis of juvenile swine CPEC cilia identified 868 proteins. Among them, 396 were shared with the proteome of 9+0 photoreceptor cilia (outer segment), whereas only 152 were shared with the proteome of 9+2 cilia and flagella. Various signaling molecules were enriched in a CPEC-specific ciliome subset, implicating multiplicity of sensory functions. The ciliome also included molecules for ciliary motility such as Rsph9. In CPECs from juvenile swine or adult mouse, Rsph9 was localized to a subpopulation of cilia, whereas they were non-motile. Live imaging of mouse choroid plexus revealed that neonatal CPEC cilia could beat vigorously, and the motility waned and was lost within 1–2 weeks. The beating characteristics of neonatal CPEC cilia were variable and different from those of typical 9+2 cilia of ependyma, yet an Efhc1-mediated mechanism to regulate the beating frequency was shared in both types of cilia. Notably, ultrastructural analysis revealed the presence of not only 9+0 but also 9+2 and atypical ciliary subtypes in neonatal CPEC. Overall, these results identified both conserved and variable components of sensory cilia, and demonstrated a novel mode of ciliary development in mammals. The Company of Biologists 2012-06-29 /pmc/articles/PMC3507226/ /pubmed/23213475 http://dx.doi.org/10.1242/bio.20121081 Text en © 2012. Published by The Company of Biologists Ltd http://creativecommons.org/licenses/by-nc-sa/3.0 This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial Share Alike License (http://creativecommons.org/licenses/by-nc-sa/3.0/).
spellingShingle Research Article
Narita, Keishi
Kozuka-Hata, Hiroko
Nonami, Yuta
Ao-Kondo, Hiroko
Suzuki, Toshimitsu
Nakamura, Hideki
Yamakawa, Kazuhiro
Oyama, Masaaki
Inoue, Takafumi
Takeda, Sen
Proteomic analysis of multiple primary cilia reveals a novel mode of ciliary development in mammals
title Proteomic analysis of multiple primary cilia reveals a novel mode of ciliary development in mammals
title_full Proteomic analysis of multiple primary cilia reveals a novel mode of ciliary development in mammals
title_fullStr Proteomic analysis of multiple primary cilia reveals a novel mode of ciliary development in mammals
title_full_unstemmed Proteomic analysis of multiple primary cilia reveals a novel mode of ciliary development in mammals
title_short Proteomic analysis of multiple primary cilia reveals a novel mode of ciliary development in mammals
title_sort proteomic analysis of multiple primary cilia reveals a novel mode of ciliary development in mammals
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3507226/
https://www.ncbi.nlm.nih.gov/pubmed/23213475
http://dx.doi.org/10.1242/bio.20121081
work_keys_str_mv AT naritakeishi proteomicanalysisofmultipleprimaryciliarevealsanovelmodeofciliarydevelopmentinmammals
AT kozukahatahiroko proteomicanalysisofmultipleprimaryciliarevealsanovelmodeofciliarydevelopmentinmammals
AT nonamiyuta proteomicanalysisofmultipleprimaryciliarevealsanovelmodeofciliarydevelopmentinmammals
AT aokondohiroko proteomicanalysisofmultipleprimaryciliarevealsanovelmodeofciliarydevelopmentinmammals
AT suzukitoshimitsu proteomicanalysisofmultipleprimaryciliarevealsanovelmodeofciliarydevelopmentinmammals
AT nakamurahideki proteomicanalysisofmultipleprimaryciliarevealsanovelmodeofciliarydevelopmentinmammals
AT yamakawakazuhiro proteomicanalysisofmultipleprimaryciliarevealsanovelmodeofciliarydevelopmentinmammals
AT oyamamasaaki proteomicanalysisofmultipleprimaryciliarevealsanovelmodeofciliarydevelopmentinmammals
AT inouetakafumi proteomicanalysisofmultipleprimaryciliarevealsanovelmodeofciliarydevelopmentinmammals
AT takedasen proteomicanalysisofmultipleprimaryciliarevealsanovelmodeofciliarydevelopmentinmammals