Cargando…
Chaperone requirements for de novo folding of Saccharomyces cerevisiae septins
Polymers of septin protein complexes play cytoskeletal roles in eukaryotic cells. The specific subunit composition within complexes controls functions and higher-order structural properties. All septins have globular GTPase domains. The other eukaryotic cytoskeletal NTPases strictly require assistan...
Autores principales: | , , , , , , , |
---|---|
Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
The American Society for Cell Biology
2022
|
Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9635297/ https://www.ncbi.nlm.nih.gov/pubmed/35947497 http://dx.doi.org/10.1091/mbc.E22-07-0262 |
_version_ | 1784824683137335296 |
---|---|
author | Hassell, Daniel Denney, Ashley Singer, Emily Benson, Aleyna Roth, Andrew Ceglowski, Julia Steingesser, Marc McMurray, Michael |
author_facet | Hassell, Daniel Denney, Ashley Singer, Emily Benson, Aleyna Roth, Andrew Ceglowski, Julia Steingesser, Marc McMurray, Michael |
author_sort | Hassell, Daniel |
collection | PubMed |
description | Polymers of septin protein complexes play cytoskeletal roles in eukaryotic cells. The specific subunit composition within complexes controls functions and higher-order structural properties. All septins have globular GTPase domains. The other eukaryotic cytoskeletal NTPases strictly require assistance from molecular chaperones of the cytosol, particularly the cage-like chaperonins, to fold into oligomerization-competent conformations. We previously identified cytosolic chaperones that bind septins and influence the oligomerization ability of septins carrying mutations linked to human disease, but it was unknown to what extent wild-type septins require chaperone assistance for their native folding. Here we use a combination of in vivo and in vitro approaches to demonstrate chaperone requirements for de novo folding and complex assembly by budding yeast septins. Individually purified septins adopted nonnative conformations and formed nonnative homodimers. In chaperonin- or Hsp70-deficient cells, septins folded slower and were unable to assemble posttranslationally into native complexes. One septin, Cdc12, was so dependent on cotranslational chaperonin assistance that translation failed without it. Our findings point to distinct translation elongation rates for different septins as a possible mechanism to direct a stepwise, cotranslational assembly pathway in which general cytosolic chaperones act as key intermediaries. |
format | Online Article Text |
id | pubmed-9635297 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | The American Society for Cell Biology |
record_format | MEDLINE/PubMed |
spelling | pubmed-96352972022-12-07 Chaperone requirements for de novo folding of Saccharomyces cerevisiae septins Hassell, Daniel Denney, Ashley Singer, Emily Benson, Aleyna Roth, Andrew Ceglowski, Julia Steingesser, Marc McMurray, Michael Mol Biol Cell Articles Polymers of septin protein complexes play cytoskeletal roles in eukaryotic cells. The specific subunit composition within complexes controls functions and higher-order structural properties. All septins have globular GTPase domains. The other eukaryotic cytoskeletal NTPases strictly require assistance from molecular chaperones of the cytosol, particularly the cage-like chaperonins, to fold into oligomerization-competent conformations. We previously identified cytosolic chaperones that bind septins and influence the oligomerization ability of septins carrying mutations linked to human disease, but it was unknown to what extent wild-type septins require chaperone assistance for their native folding. Here we use a combination of in vivo and in vitro approaches to demonstrate chaperone requirements for de novo folding and complex assembly by budding yeast septins. Individually purified septins adopted nonnative conformations and formed nonnative homodimers. In chaperonin- or Hsp70-deficient cells, septins folded slower and were unable to assemble posttranslationally into native complexes. One septin, Cdc12, was so dependent on cotranslational chaperonin assistance that translation failed without it. Our findings point to distinct translation elongation rates for different septins as a possible mechanism to direct a stepwise, cotranslational assembly pathway in which general cytosolic chaperones act as key intermediaries. The American Society for Cell Biology 2022-09-22 /pmc/articles/PMC9635297/ /pubmed/35947497 http://dx.doi.org/10.1091/mbc.E22-07-0262 Text en © 2022 Hassell et al. “ASCB®,” “The American Society for Cell Biology®,” and “Molecular Biology of the Cell®” are registered trademarks of The American Society for Cell Biology. https://creativecommons.org/licenses/by-nc-sa/4.0/This article is distributed by The American Society for Cell Biology under license from the author(s). Two months after publication it is available to the public under an Attribution–Noncommercial-Share Alike 4.0 International Creative Commons License. |
spellingShingle | Articles Hassell, Daniel Denney, Ashley Singer, Emily Benson, Aleyna Roth, Andrew Ceglowski, Julia Steingesser, Marc McMurray, Michael Chaperone requirements for de novo folding of Saccharomyces cerevisiae septins |
title | Chaperone requirements for de novo folding of Saccharomyces cerevisiae septins |
title_full | Chaperone requirements for de novo folding of Saccharomyces cerevisiae septins |
title_fullStr | Chaperone requirements for de novo folding of Saccharomyces cerevisiae septins |
title_full_unstemmed | Chaperone requirements for de novo folding of Saccharomyces cerevisiae septins |
title_short | Chaperone requirements for de novo folding of Saccharomyces cerevisiae septins |
title_sort | chaperone requirements for de novo folding of saccharomyces cerevisiae septins |
topic | Articles |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9635297/ https://www.ncbi.nlm.nih.gov/pubmed/35947497 http://dx.doi.org/10.1091/mbc.E22-07-0262 |
work_keys_str_mv | AT hasselldaniel chaperonerequirementsfordenovofoldingofsaccharomycescerevisiaeseptins AT denneyashley chaperonerequirementsfordenovofoldingofsaccharomycescerevisiaeseptins AT singeremily chaperonerequirementsfordenovofoldingofsaccharomycescerevisiaeseptins AT bensonaleyna chaperonerequirementsfordenovofoldingofsaccharomycescerevisiaeseptins AT rothandrew chaperonerequirementsfordenovofoldingofsaccharomycescerevisiaeseptins AT ceglowskijulia chaperonerequirementsfordenovofoldingofsaccharomycescerevisiaeseptins AT steingessermarc chaperonerequirementsfordenovofoldingofsaccharomycescerevisiaeseptins AT mcmurraymichael chaperonerequirementsfordenovofoldingofsaccharomycescerevisiaeseptins |