Sfr1, a <named-content content-type="genus-species">Tetrahymena thermophila</named-content> Sfi1 Repeat Protein, Modulates the Production of Cortical Row Basal Bodies

ABSTRACT Basal bodies are essential microtubule-based structures that template, anchor, and orient cilia at the cell surface. Cilia act primarily in the generation of directional fluid flow and sensory reception, both of which are utilized for a broad spectrum of cellular processes. Although basal b...

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Autores principales:	Westley Heydeck, Alexander J. Stemm-Wolf, Janin Knop, Christina C. Poh, Mark Winey
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2016
Materias:	basal body centrin centriole Sfi1 repeat Tetrahymena ciliates Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/8bc5984034164c4f82ea927b3a321722
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spelling	oai:doaj.org-article:8bc5984034164c4f82ea927b3a3217222021-11-15T15:22:03ZSfr1, a <named-content content-type="genus-species">Tetrahymena thermophila</named-content> Sfi1 Repeat Protein, Modulates the Production of Cortical Row Basal Bodies10.1128/mSphere.00257-162379-5042https://doaj.org/article/8bc5984034164c4f82ea927b3a3217222016-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00257-16https://doaj.org/toc/2379-5042ABSTRACT Basal bodies are essential microtubule-based structures that template, anchor, and orient cilia at the cell surface. Cilia act primarily in the generation of directional fluid flow and sensory reception, both of which are utilized for a broad spectrum of cellular processes. Although basal bodies contribute to vital cell functions, the molecular contributors of their assembly and maintenance are poorly understood. Previous studies of the ciliate Tetrahymena thermophila revealed important roles for two centrin family members in basal body assembly, separation of new basal bodies, and stability. Here, we characterize the basal body function of a centrin-binding protein, Sfr1, in Tetrahymena. Sfr1 is part of a large family of 13 proteins in Tetrahymena that contain Sfi1 repeats (SFRs), a motif originally identified in Saccharomyces cerevisiae Sfi1 that binds centrin. Sfr1 is the only SFR protein in Tetrahymena that localizes to all cortical row and oral apparatus basal bodies. In addition, Sfr1 resides predominantly at the microtubule scaffold from the proximal cartwheel to the distal transition zone. Complete genomic knockout of SFR1 (sfr1Δ) causes a significant increase in both cortical row basal body density and the number of cortical rows, contributing to an overall overproduction of basal bodies. Reintroduction of Sfr1 into sfr1Δ mutant cells leads to a marked reduction of cortical row basal body density and the total number of cortical row basal bodies. Therefore, Sfr1 directly modulates cortical row basal body production. This study reveals an inhibitory role for Sfr1, and potentially centrins, in Tetrahymena basal body production. IMPORTANCE Basal bodies and centrioles are structurally similar and, when rendered dysfunctional as a result of improper assembly or maintenance, are associated with human diseases. Centrins are conserved and abundant components of both structures whose basal body and centriolar functions remain incompletely understood. Despite the extensive study of centrins in Tetrahymena thermophila, little is known about how centrin-binding proteins contribute to centrin’s roles in basal body assembly, stability, and orientation. The sole previous study of the large centrin-binding protein family in Tetrahymena revealed a role for Sfr13 in the stabilization and separation of basal bodies. In this study, we found that Sfr1 localizes to all Tetrahymena basal bodies and complete genetic deletion of SFR1 leads to overproduction of basal bodies. The uncovered inhibitory role of Sfr1 in basal body production suggests that centrin-binding proteins, as well as centrins, may influence basal body number both positively and negatively.Westley HeydeckAlexander J. Stemm-WolfJanin KnopChristina C. PohMark WineyAmerican Society for Microbiologyarticlebasal bodycentrincentrioleSfi1 repeatTetrahymenaciliatesMicrobiologyQR1-502ENmSphere, Vol 1, Iss 6 (2016)
institution	DOAJ
collection	DOAJ
language	EN
topic	basal body centrin centriole Sfi1 repeat Tetrahymena ciliates Microbiology QR1-502
spellingShingle	basal body centrin centriole Sfi1 repeat Tetrahymena ciliates Microbiology QR1-502 Westley Heydeck Alexander J. Stemm-Wolf Janin Knop Christina C. Poh Mark Winey Sfr1, a <named-content content-type="genus-species">Tetrahymena thermophila</named-content> Sfi1 Repeat Protein, Modulates the Production of Cortical Row Basal Bodies
description	ABSTRACT Basal bodies are essential microtubule-based structures that template, anchor, and orient cilia at the cell surface. Cilia act primarily in the generation of directional fluid flow and sensory reception, both of which are utilized for a broad spectrum of cellular processes. Although basal bodies contribute to vital cell functions, the molecular contributors of their assembly and maintenance are poorly understood. Previous studies of the ciliate Tetrahymena thermophila revealed important roles for two centrin family members in basal body assembly, separation of new basal bodies, and stability. Here, we characterize the basal body function of a centrin-binding protein, Sfr1, in Tetrahymena. Sfr1 is part of a large family of 13 proteins in Tetrahymena that contain Sfi1 repeats (SFRs), a motif originally identified in Saccharomyces cerevisiae Sfi1 that binds centrin. Sfr1 is the only SFR protein in Tetrahymena that localizes to all cortical row and oral apparatus basal bodies. In addition, Sfr1 resides predominantly at the microtubule scaffold from the proximal cartwheel to the distal transition zone. Complete genomic knockout of SFR1 (sfr1Δ) causes a significant increase in both cortical row basal body density and the number of cortical rows, contributing to an overall overproduction of basal bodies. Reintroduction of Sfr1 into sfr1Δ mutant cells leads to a marked reduction of cortical row basal body density and the total number of cortical row basal bodies. Therefore, Sfr1 directly modulates cortical row basal body production. This study reveals an inhibitory role for Sfr1, and potentially centrins, in Tetrahymena basal body production. IMPORTANCE Basal bodies and centrioles are structurally similar and, when rendered dysfunctional as a result of improper assembly or maintenance, are associated with human diseases. Centrins are conserved and abundant components of both structures whose basal body and centriolar functions remain incompletely understood. Despite the extensive study of centrins in Tetrahymena thermophila, little is known about how centrin-binding proteins contribute to centrin’s roles in basal body assembly, stability, and orientation. The sole previous study of the large centrin-binding protein family in Tetrahymena revealed a role for Sfr13 in the stabilization and separation of basal bodies. In this study, we found that Sfr1 localizes to all Tetrahymena basal bodies and complete genetic deletion of SFR1 leads to overproduction of basal bodies. The uncovered inhibitory role of Sfr1 in basal body production suggests that centrin-binding proteins, as well as centrins, may influence basal body number both positively and negatively.
format	article
author	Westley Heydeck Alexander J. Stemm-Wolf Janin Knop Christina C. Poh Mark Winey
author_facet	Westley Heydeck Alexander J. Stemm-Wolf Janin Knop Christina C. Poh Mark Winey
author_sort	Westley Heydeck
title	Sfr1, a <named-content content-type="genus-species">Tetrahymena thermophila</named-content> Sfi1 Repeat Protein, Modulates the Production of Cortical Row Basal Bodies
title_short	Sfr1, a <named-content content-type="genus-species">Tetrahymena thermophila</named-content> Sfi1 Repeat Protein, Modulates the Production of Cortical Row Basal Bodies
title_full	Sfr1, a <named-content content-type="genus-species">Tetrahymena thermophila</named-content> Sfi1 Repeat Protein, Modulates the Production of Cortical Row Basal Bodies
title_fullStr	Sfr1, a <named-content content-type="genus-species">Tetrahymena thermophila</named-content> Sfi1 Repeat Protein, Modulates the Production of Cortical Row Basal Bodies
title_full_unstemmed	Sfr1, a <named-content content-type="genus-species">Tetrahymena thermophila</named-content> Sfi1 Repeat Protein, Modulates the Production of Cortical Row Basal Bodies
title_sort	sfr1, a <named-content content-type="genus-species">tetrahymena thermophila</named-content> sfi1 repeat protein, modulates the production of cortical row basal bodies
publisher	American Society for Microbiology
publishDate	2016
url	https://doaj.org/article/8bc5984034164c4f82ea927b3a321722
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Sfr1, a <named-content content-type="genus-species">Tetrahymena thermophila</named-content> Sfi1 Repeat Protein, Modulates the Production of Cortical Row Basal Bodies

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