Formation of Transient Protein Aggregate-like Centers Is a General Strategy Postponing Degradation of Misfolded Intermediates
When misfolded intermediates accumulate during heat shock, the protein quality control system promotes cellular adaptation strategies. In <i>Schizosaccharomyces pombe</i>, thermo-sensitive proteins assemble upon stress into protein aggregate-like centers, PACs, to escape from degradation...
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| Format: | Article |
| Language: | English |
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MDPI AG
2023-07-01
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| Series: | International Journal of Molecular Sciences |
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| Online Access: | https://www.mdpi.com/1422-0067/24/13/11202 |
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| author | Susanna Boronat Margarita Cabrera Montserrat Vega Jorge Alcalá Silvia Salas-Pino Rafael R. Daga José Ayté Elena Hidalgo |
| author_facet | Susanna Boronat Margarita Cabrera Montserrat Vega Jorge Alcalá Silvia Salas-Pino Rafael R. Daga José Ayté Elena Hidalgo |
| author_sort | Susanna Boronat |
| collection | DOAJ |
| description | When misfolded intermediates accumulate during heat shock, the protein quality control system promotes cellular adaptation strategies. In <i>Schizosaccharomyces pombe</i>, thermo-sensitive proteins assemble upon stress into protein aggregate-like centers, PACs, to escape from degradation. The role of this protein deposition strategy has been elusive due to the use of different model systems and reporters, and to the addition of artificial inhibitors, which made interpretation of the results difficult. Here, we compare fission and budding yeast model systems, expressing the same misfolding reporters in experiments lacking proteasome or translation inhibitors. We demonstrate that mild heat shock triggers reversible PAC formation, with the collapse of both reporters and chaperones in a process largely mediated by chaperones. This assembly postpones proteasomal degradation of the misfolding reporters, and their Hsp104-dependent disassembly occurs during stress recovery. Severe heat shock induces formation of cytosolic PACs, but also of nuclear structures resembling nucleolar rings, NuRs, presumably to halt nuclear functions. Our study demonstrates that these distantly related yeasts use very similar strategies to adapt and survive to mild and severe heat shock and that aggregate-like formation is a general cellular scheme to postpone protein degradation and facilitate exit from stress. |
| first_indexed | 2024-03-11T01:38:25Z |
| format | Article |
| id | doaj.art-bf3d4bdde12d421fbb002ef627b63ffe |
| institution | Directory Open Access Journal |
| issn | 1661-6596 1422-0067 |
| language | English |
| last_indexed | 2024-03-11T01:38:25Z |
| publishDate | 2023-07-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | International Journal of Molecular Sciences |
| spelling | doaj.art-bf3d4bdde12d421fbb002ef627b63ffe2023-11-18T16:49:36ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672023-07-0124131120210.3390/ijms241311202Formation of Transient Protein Aggregate-like Centers Is a General Strategy Postponing Degradation of Misfolded IntermediatesSusanna Boronat0Margarita Cabrera1Montserrat Vega2Jorge Alcalá3Silvia Salas-Pino4Rafael R. Daga5José Ayté6Elena Hidalgo7Oxidative Stress and Cell Cycle Group, Universitat Pompeu Fabra, C/Doctor Aiguader 88, 08003 Barcelona, SpainOxidative Stress and Cell Cycle Group, Universitat Pompeu Fabra, C/Doctor Aiguader 88, 08003 Barcelona, SpainOxidative Stress and Cell Cycle Group, Universitat Pompeu Fabra, C/Doctor Aiguader 88, 08003 Barcelona, SpainOxidative Stress and Cell Cycle Group, Universitat Pompeu Fabra, C/Doctor Aiguader 88, 08003 Barcelona, SpainCentro Andaluz de Biología del Desarrollo, Universidad Pablo de Olavide-Consejo Superior de Investigaciones Científicas-Junta de Andalucía, Carretera de Utrera, km1, 41013 Seville, SpainCentro Andaluz de Biología del Desarrollo, Universidad Pablo de Olavide-Consejo Superior de Investigaciones Científicas-Junta de Andalucía, Carretera de Utrera, km1, 41013 Seville, SpainOxidative Stress and Cell Cycle Group, Universitat Pompeu Fabra, C/Doctor Aiguader 88, 08003 Barcelona, SpainOxidative Stress and Cell Cycle Group, Universitat Pompeu Fabra, C/Doctor Aiguader 88, 08003 Barcelona, SpainWhen misfolded intermediates accumulate during heat shock, the protein quality control system promotes cellular adaptation strategies. In <i>Schizosaccharomyces pombe</i>, thermo-sensitive proteins assemble upon stress into protein aggregate-like centers, PACs, to escape from degradation. The role of this protein deposition strategy has been elusive due to the use of different model systems and reporters, and to the addition of artificial inhibitors, which made interpretation of the results difficult. Here, we compare fission and budding yeast model systems, expressing the same misfolding reporters in experiments lacking proteasome or translation inhibitors. We demonstrate that mild heat shock triggers reversible PAC formation, with the collapse of both reporters and chaperones in a process largely mediated by chaperones. This assembly postpones proteasomal degradation of the misfolding reporters, and their Hsp104-dependent disassembly occurs during stress recovery. Severe heat shock induces formation of cytosolic PACs, but also of nuclear structures resembling nucleolar rings, NuRs, presumably to halt nuclear functions. Our study demonstrates that these distantly related yeasts use very similar strategies to adapt and survive to mild and severe heat shock and that aggregate-like formation is a general cellular scheme to postpone protein degradation and facilitate exit from stress.https://www.mdpi.com/1422-0067/24/13/11202heat shock responseprotein aggregation-like centersbudding yeastW303 vs. BY4741fission yeastMas5 |
| spellingShingle | Susanna Boronat Margarita Cabrera Montserrat Vega Jorge Alcalá Silvia Salas-Pino Rafael R. Daga José Ayté Elena Hidalgo Formation of Transient Protein Aggregate-like Centers Is a General Strategy Postponing Degradation of Misfolded Intermediates International Journal of Molecular Sciences heat shock response protein aggregation-like centers budding yeast W303 vs. BY4741 fission yeast Mas5 |
| title | Formation of Transient Protein Aggregate-like Centers Is a General Strategy Postponing Degradation of Misfolded Intermediates |
| title_full | Formation of Transient Protein Aggregate-like Centers Is a General Strategy Postponing Degradation of Misfolded Intermediates |
| title_fullStr | Formation of Transient Protein Aggregate-like Centers Is a General Strategy Postponing Degradation of Misfolded Intermediates |
| title_full_unstemmed | Formation of Transient Protein Aggregate-like Centers Is a General Strategy Postponing Degradation of Misfolded Intermediates |
| title_short | Formation of Transient Protein Aggregate-like Centers Is a General Strategy Postponing Degradation of Misfolded Intermediates |
| title_sort | formation of transient protein aggregate like centers is a general strategy postponing degradation of misfolded intermediates |
| topic | heat shock response protein aggregation-like centers budding yeast W303 vs. BY4741 fission yeast Mas5 |
| url | https://www.mdpi.com/1422-0067/24/13/11202 |
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