Cargando…
The Dysferlin Domain-Only Protein, Spo73, Is Required for Prospore Membrane Extension in Saccharomyces cerevisiae
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 alon...
Autores principales: | , , , , , , , , , |
---|---|
Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
American Society for Microbiology
2015
|
Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4863634/ https://www.ncbi.nlm.nih.gov/pubmed/27303688 http://dx.doi.org/10.1128/mSphere.00038-15 |
_version_ | 1782431512284626944 |
---|---|
author | Okumura, Yuuya Nakamura, Tsuyoshi S. Tanaka, Takayuki Inoue, Ichiro Suda, Yasuyuki Takahashi, Tetsuo Nakanishi, Hideki Nakamura, Shugo Gao, Xiao-Dong Tachikawa, Hiroyuki |
author_facet | Okumura, Yuuya Nakamura, Tsuyoshi S. Tanaka, Takayuki Inoue, Ichiro Suda, Yasuyuki Takahashi, Tetsuo Nakanishi, Hideki Nakamura, Shugo Gao, Xiao-Dong Tachikawa, Hiroyuki |
author_sort | Okumura, Yuuya |
collection | PubMed |
description | 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 | Online Article Text |
id | pubmed-4863634 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2015 |
publisher | American Society for Microbiology |
record_format | MEDLINE/PubMed |
spelling | pubmed-48636342016-06-14 The Dysferlin Domain-Only Protein, Spo73, Is Required for Prospore Membrane Extension in Saccharomyces cerevisiae Okumura, Yuuya Nakamura, Tsuyoshi S. Tanaka, Takayuki Inoue, Ichiro Suda, Yasuyuki Takahashi, Tetsuo Nakanishi, Hideki Nakamura, Shugo Gao, Xiao-Dong Tachikawa, Hiroyuki mSphere Research Article 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. American Society for Microbiology 2015-12-16 /pmc/articles/PMC4863634/ /pubmed/27303688 http://dx.doi.org/10.1128/mSphere.00038-15 Text en Copyright © 2015 Okumura et al. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (http://creativecommons.org/licenses/by/4.0/) . |
spellingShingle | Research Article Okumura, Yuuya Nakamura, Tsuyoshi S. Tanaka, Takayuki Inoue, Ichiro Suda, Yasuyuki Takahashi, Tetsuo Nakanishi, Hideki Nakamura, Shugo Gao, Xiao-Dong Tachikawa, Hiroyuki The Dysferlin Domain-Only Protein, Spo73, Is Required for Prospore Membrane Extension in Saccharomyces cerevisiae |
title | The Dysferlin Domain-Only Protein, Spo73, Is Required for Prospore Membrane Extension in Saccharomyces cerevisiae |
title_full | The Dysferlin Domain-Only Protein, Spo73, Is Required for Prospore Membrane Extension in Saccharomyces cerevisiae |
title_fullStr | The Dysferlin Domain-Only Protein, Spo73, Is Required for Prospore Membrane Extension in Saccharomyces cerevisiae |
title_full_unstemmed | The Dysferlin Domain-Only Protein, Spo73, Is Required for Prospore Membrane Extension in Saccharomyces cerevisiae |
title_short | The Dysferlin Domain-Only Protein, Spo73, Is Required for Prospore Membrane Extension in Saccharomyces cerevisiae |
title_sort | dysferlin domain-only protein, spo73, is required for prospore membrane extension in saccharomyces cerevisiae |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4863634/ https://www.ncbi.nlm.nih.gov/pubmed/27303688 http://dx.doi.org/10.1128/mSphere.00038-15 |
work_keys_str_mv | AT okumurayuuya thedysferlindomainonlyproteinspo73isrequiredforprosporemembraneextensioninsaccharomycescerevisiae AT nakamuratsuyoshis thedysferlindomainonlyproteinspo73isrequiredforprosporemembraneextensioninsaccharomycescerevisiae AT tanakatakayuki thedysferlindomainonlyproteinspo73isrequiredforprosporemembraneextensioninsaccharomycescerevisiae AT inoueichiro thedysferlindomainonlyproteinspo73isrequiredforprosporemembraneextensioninsaccharomycescerevisiae AT sudayasuyuki thedysferlindomainonlyproteinspo73isrequiredforprosporemembraneextensioninsaccharomycescerevisiae AT takahashitetsuo thedysferlindomainonlyproteinspo73isrequiredforprosporemembraneextensioninsaccharomycescerevisiae AT nakanishihideki thedysferlindomainonlyproteinspo73isrequiredforprosporemembraneextensioninsaccharomycescerevisiae AT nakamurashugo thedysferlindomainonlyproteinspo73isrequiredforprosporemembraneextensioninsaccharomycescerevisiae AT gaoxiaodong thedysferlindomainonlyproteinspo73isrequiredforprosporemembraneextensioninsaccharomycescerevisiae AT tachikawahiroyuki thedysferlindomainonlyproteinspo73isrequiredforprosporemembraneextensioninsaccharomycescerevisiae AT okumurayuuya dysferlindomainonlyproteinspo73isrequiredforprosporemembraneextensioninsaccharomycescerevisiae AT nakamuratsuyoshis dysferlindomainonlyproteinspo73isrequiredforprosporemembraneextensioninsaccharomycescerevisiae AT tanakatakayuki dysferlindomainonlyproteinspo73isrequiredforprosporemembraneextensioninsaccharomycescerevisiae AT inoueichiro dysferlindomainonlyproteinspo73isrequiredforprosporemembraneextensioninsaccharomycescerevisiae AT sudayasuyuki dysferlindomainonlyproteinspo73isrequiredforprosporemembraneextensioninsaccharomycescerevisiae AT takahashitetsuo dysferlindomainonlyproteinspo73isrequiredforprosporemembraneextensioninsaccharomycescerevisiae AT nakanishihideki dysferlindomainonlyproteinspo73isrequiredforprosporemembraneextensioninsaccharomycescerevisiae AT nakamurashugo dysferlindomainonlyproteinspo73isrequiredforprosporemembraneextensioninsaccharomycescerevisiae AT gaoxiaodong dysferlindomainonlyproteinspo73isrequiredforprosporemembraneextensioninsaccharomycescerevisiae AT tachikawahiroyuki dysferlindomainonlyproteinspo73isrequiredforprosporemembraneextensioninsaccharomycescerevisiae |