The Dysferlin Domain-Only Protein, Spo73, Is Required for Prospore Membrane Extension in <named-content content-type="genus-species">Saccharomyces cerevisiae</named-content>

ABSTRACT Sporulation of Saccharomyces cerevisiae is a developmental process in which an ascus containing four haploid spores forms from a diploid cell. During this process, newly formed membrane structures called prospore membranes extend along the nuclear envelope and engulf and package daughter nu...

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Autores principales:	Yuuya Okumura, Tsuyoshi S. Nakamura, Takayuki Tanaka, Ichiro Inoue, Yasuyuki Suda, Tetsuo Takahashi, Hideki Nakanishi, Shugo Nakamura, Xiao-Dong Gao, Hiroyuki Tachikawa
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2016
Materias:	Saccharomyces cerevisiae sporulation prospore membrane dysferlin domain Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/631119e5fd6e42daaba70fd1e0dbbb16
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spelling	oai:doaj.org-article:631119e5fd6e42daaba70fd1e0dbbb162021-11-15T15:21:38ZThe Dysferlin Domain-Only Protein, Spo73, Is Required for Prospore Membrane Extension in <named-content content-type="genus-species">Saccharomyces cerevisiae</named-content>10.1128/mSphere.00038-152379-5042https://doaj.org/article/631119e5fd6e42daaba70fd1e0dbbb162016-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00038-15https://doaj.org/toc/2379-5042ABSTRACT Sporulation of Saccharomyces cerevisiae is a developmental process in which an ascus containing four haploid spores forms from a diploid cell. During this process, newly formed membrane structures called prospore membranes extend along the nuclear envelope and engulf and package daughter nuclei along with cytosol and organelles to form precursors of spores. Proteins involved in prospore membrane extension, Vps13 and Spo71, have recently been reported; however, the overall mechanism of membrane extension remains unclear. Here, we identified Spo73 as an additional factor involved in prospore membrane extension. Analysis of a spo73∆ mutant revealed that it shows defects similar to those of a spo71∆ mutant during prospore membrane formation. Spo73 localizes to the prospore membrane, and this localization is independent of Spo71 and Vps13. In contrast, a Spo73 protein carrying mutations in a surface basic patch mislocalizes to the cytoplasm and overexpression of Spo71 can partially rescue localization to the prospore membrane. Similar to spo71∆ mutants, spo73∆ mutants display genetic interactions with the mutations in the SMA2 and SPO1 genes involved in prospore membrane bending. Further, our bioinformatic analysis revealed that Spo73 is a dysferlin domain-only protein. Thus, these results suggest that a dysferlin domain-only protein, Spo73, functions with a dual pleckstrin homology domain protein, Spo71, in prospore membrane extension. Analysis of Spo73 will provide insights into the conserved function of dysferlin domains, which is related to dysferlinopathy. IMPORTANCE Prospore membrane formation consists of de novo double-membrane formation, which occurs during the developmental process of sporulation in Saccharomyces cerevisiae. Membranes are formed into their proper size and shape, and thus, prospore membrane formation has been studied as a general model of membrane formation. We identified SPO73, previously shown to be required for spore wall formation, as an additional gene involved in prospore membrane extension. Genetic and cell biological analyses suggested that Spo73 functions on the prospore membrane with other factors in prospore membrane extension, counteracting the bending force of the prospore membrane. Spo73 is the first dysferlin domain-only protein ever analyzed. The dysferlin domain is conserved from yeast to mammals and is found in dysferlin proteins, which are involved in dysferlinopathy, although the precise function of the domain is unknown. Continued analysis of Spo73 will contribute to our understanding of the function of dysferlin domains and dysferlinopathy.Yuuya OkumuraTsuyoshi S. NakamuraTakayuki TanakaIchiro InoueYasuyuki SudaTetsuo TakahashiHideki NakanishiShugo NakamuraXiao-Dong GaoHiroyuki TachikawaAmerican Society for MicrobiologyarticleSaccharomyces cerevisiaesporulationprospore membranedysferlin domainMicrobiologyQR1-502ENmSphere, Vol 1, Iss 1 (2016)
institution	DOAJ
collection	DOAJ
language	EN
topic	Saccharomyces cerevisiae sporulation prospore membrane dysferlin domain Microbiology QR1-502
spellingShingle	Saccharomyces cerevisiae sporulation prospore membrane dysferlin domain Microbiology QR1-502 Yuuya Okumura Tsuyoshi S. Nakamura Takayuki Tanaka Ichiro Inoue Yasuyuki Suda Tetsuo Takahashi Hideki Nakanishi Shugo Nakamura Xiao-Dong Gao Hiroyuki Tachikawa The Dysferlin Domain-Only Protein, Spo73, Is Required for Prospore Membrane Extension in <named-content content-type="genus-species">Saccharomyces cerevisiae</named-content>
description	ABSTRACT Sporulation of Saccharomyces cerevisiae is a developmental process in which an ascus containing four haploid spores forms from a diploid cell. During this process, newly formed membrane structures called prospore membranes extend along the nuclear envelope and engulf and package daughter nuclei along with cytosol and organelles to form precursors of spores. Proteins involved in prospore membrane extension, Vps13 and Spo71, have recently been reported; however, the overall mechanism of membrane extension remains unclear. Here, we identified Spo73 as an additional factor involved in prospore membrane extension. Analysis of a spo73∆ mutant revealed that it shows defects similar to those of a spo71∆ mutant during prospore membrane formation. Spo73 localizes to the prospore membrane, and this localization is independent of Spo71 and Vps13. In contrast, a Spo73 protein carrying mutations in a surface basic patch mislocalizes to the cytoplasm and overexpression of Spo71 can partially rescue localization to the prospore membrane. Similar to spo71∆ mutants, spo73∆ mutants display genetic interactions with the mutations in the SMA2 and SPO1 genes involved in prospore membrane bending. Further, our bioinformatic analysis revealed that Spo73 is a dysferlin domain-only protein. Thus, these results suggest that a dysferlin domain-only protein, Spo73, functions with a dual pleckstrin homology domain protein, Spo71, in prospore membrane extension. Analysis of Spo73 will provide insights into the conserved function of dysferlin domains, which is related to dysferlinopathy. IMPORTANCE Prospore membrane formation consists of de novo double-membrane formation, which occurs during the developmental process of sporulation in Saccharomyces cerevisiae. Membranes are formed into their proper size and shape, and thus, prospore membrane formation has been studied as a general model of membrane formation. We identified SPO73, previously shown to be required for spore wall formation, as an additional gene involved in prospore membrane extension. Genetic and cell biological analyses suggested that Spo73 functions on the prospore membrane with other factors in prospore membrane extension, counteracting the bending force of the prospore membrane. Spo73 is the first dysferlin domain-only protein ever analyzed. The dysferlin domain is conserved from yeast to mammals and is found in dysferlin proteins, which are involved in dysferlinopathy, although the precise function of the domain is unknown. Continued analysis of Spo73 will contribute to our understanding of the function of dysferlin domains and dysferlinopathy.
format	article
author	Yuuya Okumura Tsuyoshi S. Nakamura Takayuki Tanaka Ichiro Inoue Yasuyuki Suda Tetsuo Takahashi Hideki Nakanishi Shugo Nakamura Xiao-Dong Gao Hiroyuki Tachikawa
author_facet	Yuuya Okumura Tsuyoshi S. Nakamura Takayuki Tanaka Ichiro Inoue Yasuyuki Suda Tetsuo Takahashi Hideki Nakanishi Shugo Nakamura Xiao-Dong Gao Hiroyuki Tachikawa
author_sort	Yuuya Okumura
title	The Dysferlin Domain-Only Protein, Spo73, Is Required for Prospore Membrane Extension in <named-content content-type="genus-species">Saccharomyces cerevisiae</named-content>
title_short	The Dysferlin Domain-Only Protein, Spo73, Is Required for Prospore Membrane Extension in <named-content content-type="genus-species">Saccharomyces cerevisiae</named-content>
title_full	The Dysferlin Domain-Only Protein, Spo73, Is Required for Prospore Membrane Extension in <named-content content-type="genus-species">Saccharomyces cerevisiae</named-content>
title_fullStr	The Dysferlin Domain-Only Protein, Spo73, Is Required for Prospore Membrane Extension in <named-content content-type="genus-species">Saccharomyces cerevisiae</named-content>
title_full_unstemmed	The Dysferlin Domain-Only Protein, Spo73, Is Required for Prospore Membrane Extension in <named-content content-type="genus-species">Saccharomyces cerevisiae</named-content>
title_sort	dysferlin domain-only protein, spo73, is required for prospore membrane extension in <named-content content-type="genus-species">saccharomyces cerevisiae</named-content>
publisher	American Society for Microbiology
publishDate	2016
url	https://doaj.org/article/631119e5fd6e42daaba70fd1e0dbbb16
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The Dysferlin Domain-Only Protein, Spo73, Is Required for Prospore Membrane Extension in <named-content content-type="genus-species">Saccharomyces cerevisiae</named-content>

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