Interplay between the Hsp90 Chaperone and the HslVU Protease To Regulate the Level of an Essential Protein in <named-content content-type="genus-species">Shewanella oneidensis</named-content>

ABSTRACT Protein synthesis, folding, and degradation are an accurately regulated process occurring in every organism and called proteostasis. This process is essential to maintain a healthy proteome since proteostasis dysregulation is responsible for devastating cellular issues. Proteostasis is cont...

Descripción completa

Guardado en:

Detalles Bibliográficos
Autores principales:	Flora Ambre Honoré, Nathanael Jean Maillot, Vincent Méjean, Olivier Genest
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	heat shock proteases protein chaperone protein folding proteostasis stress adaptation Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/60f76403c6114addb001c5df69694c35
Etiquetas:	Agregar Etiqueta Sin Etiquetas, Sea el primero en etiquetar este registro!

id	oai:doaj.org-article:60f76403c6114addb001c5df69694c35
record_format	dspace
spelling	oai:doaj.org-article:60f76403c6114addb001c5df69694c352021-11-15T15:55:25ZInterplay between the Hsp90 Chaperone and the HslVU Protease To Regulate the Level of an Essential Protein in <named-content content-type="genus-species">Shewanella oneidensis</named-content>10.1128/mBio.00269-192150-7511https://doaj.org/article/60f76403c6114addb001c5df69694c352019-06-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00269-19https://doaj.org/toc/2150-7511ABSTRACT Protein synthesis, folding, and degradation are an accurately regulated process occurring in every organism and called proteostasis. This process is essential to maintain a healthy proteome since proteostasis dysregulation is responsible for devastating cellular issues. Proteostasis is controlled by a complex network of molecular chaperones and proteases. Among them, eukaryotic Hsp90, assisted by many cochaperones and the Hsp70 chaperone system, plays a major role in activating hundreds of client proteins, and Hsp90 inhibition usually leads to proteasomal degradation of these clients. In bacteria, however, the precise function of Hsp90 remains quite unclear, and only a few clients are known. Recently, we have shown that Hsp90 is essential at elevated temperature in the aquatic model bacterium Shewanella oneidensis, and we have identified a client of Hsp90, TilS, involved in tRNA modification. Here we found that two members of the proteostasis network with antagonist activities, the Hsp90 chaperone and the HslVU protease, which is considered the proteasome ancestor, together regulate the level of TilS. In particular, we show that deletion of the genes coding for the HslVU protease suppresses the growth defect of an S. oneidensis strain with hsp90 deleted, by increasing the cellular level of the essential TilS protein. These results open up new avenues for understanding how proteostasis is controlled in bacteria, and new Hsp90 clients are much needed now to confirm the interplay between Hsp90 and proteases. IMPORTANCE Maintaining a healthy proteome is essential in every living cell from bacteria to humans. For example, proteostasis (protein homeostasis) imbalance in humans leads to devastating diseases, including neurodegenerative diseases and cancers. Therefore, proteins need to be assisted from their synthesis to their native folding and ultimately to their degradation. To ensure efficient protein turnover, cells possess an intricate network of molecular chaperones and proteases for protein folding and degradation. However, these networks need to be better defined and understood. Here, using the aquatic bacterium Shewanella oneidensis as a model organism, we demonstrate interplay between two proteins with antagonist activities, the Hsp90 chaperone and the HslVU protease, to finely regulate the level of an essential client of Hsp90. Therefore, this work provides a new bacterial model to better study protein regulation and turnover, and it sheds light on how proteostasis by Hsp90 and proteases could be controlled in bacteria.Flora Ambre HonoréNathanael Jean MaillotVincent MéjeanOlivier GenestAmerican Society for Microbiologyarticleheat shockproteasesprotein chaperoneprotein foldingproteostasisstress adaptationMicrobiologyQR1-502ENmBio, Vol 10, Iss 3 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	heat shock proteases protein chaperone protein folding proteostasis stress adaptation Microbiology QR1-502
spellingShingle	heat shock proteases protein chaperone protein folding proteostasis stress adaptation Microbiology QR1-502 Flora Ambre Honoré Nathanael Jean Maillot Vincent Méjean Olivier Genest Interplay between the Hsp90 Chaperone and the HslVU Protease To Regulate the Level of an Essential Protein in <named-content content-type="genus-species">Shewanella oneidensis</named-content>
description	ABSTRACT Protein synthesis, folding, and degradation are an accurately regulated process occurring in every organism and called proteostasis. This process is essential to maintain a healthy proteome since proteostasis dysregulation is responsible for devastating cellular issues. Proteostasis is controlled by a complex network of molecular chaperones and proteases. Among them, eukaryotic Hsp90, assisted by many cochaperones and the Hsp70 chaperone system, plays a major role in activating hundreds of client proteins, and Hsp90 inhibition usually leads to proteasomal degradation of these clients. In bacteria, however, the precise function of Hsp90 remains quite unclear, and only a few clients are known. Recently, we have shown that Hsp90 is essential at elevated temperature in the aquatic model bacterium Shewanella oneidensis, and we have identified a client of Hsp90, TilS, involved in tRNA modification. Here we found that two members of the proteostasis network with antagonist activities, the Hsp90 chaperone and the HslVU protease, which is considered the proteasome ancestor, together regulate the level of TilS. In particular, we show that deletion of the genes coding for the HslVU protease suppresses the growth defect of an S. oneidensis strain with hsp90 deleted, by increasing the cellular level of the essential TilS protein. These results open up new avenues for understanding how proteostasis is controlled in bacteria, and new Hsp90 clients are much needed now to confirm the interplay between Hsp90 and proteases. IMPORTANCE Maintaining a healthy proteome is essential in every living cell from bacteria to humans. For example, proteostasis (protein homeostasis) imbalance in humans leads to devastating diseases, including neurodegenerative diseases and cancers. Therefore, proteins need to be assisted from their synthesis to their native folding and ultimately to their degradation. To ensure efficient protein turnover, cells possess an intricate network of molecular chaperones and proteases for protein folding and degradation. However, these networks need to be better defined and understood. Here, using the aquatic bacterium Shewanella oneidensis as a model organism, we demonstrate interplay between two proteins with antagonist activities, the Hsp90 chaperone and the HslVU protease, to finely regulate the level of an essential client of Hsp90. Therefore, this work provides a new bacterial model to better study protein regulation and turnover, and it sheds light on how proteostasis by Hsp90 and proteases could be controlled in bacteria.
format	article
author	Flora Ambre Honoré Nathanael Jean Maillot Vincent Méjean Olivier Genest
author_facet	Flora Ambre Honoré Nathanael Jean Maillot Vincent Méjean Olivier Genest
author_sort	Flora Ambre Honoré
title	Interplay between the Hsp90 Chaperone and the HslVU Protease To Regulate the Level of an Essential Protein in <named-content content-type="genus-species">Shewanella oneidensis</named-content>
title_short	Interplay between the Hsp90 Chaperone and the HslVU Protease To Regulate the Level of an Essential Protein in <named-content content-type="genus-species">Shewanella oneidensis</named-content>
title_full	Interplay between the Hsp90 Chaperone and the HslVU Protease To Regulate the Level of an Essential Protein in <named-content content-type="genus-species">Shewanella oneidensis</named-content>
title_fullStr	Interplay between the Hsp90 Chaperone and the HslVU Protease To Regulate the Level of an Essential Protein in <named-content content-type="genus-species">Shewanella oneidensis</named-content>
title_full_unstemmed	Interplay between the Hsp90 Chaperone and the HslVU Protease To Regulate the Level of an Essential Protein in <named-content content-type="genus-species">Shewanella oneidensis</named-content>
title_sort	interplay between the hsp90 chaperone and the hslvu protease to regulate the level of an essential protein in <named-content content-type="genus-species">shewanella oneidensis</named-content>
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/60f76403c6114addb001c5df69694c35
work_keys_str_mv	AT floraambrehonore interplaybetweenthehsp90chaperoneandthehslvuproteasetoregulatethelevelofanessentialproteininnamedcontentcontenttypegenusspeciesshewanellaoneidensisnamedcontent AT nathanaeljeanmaillot interplaybetweenthehsp90chaperoneandthehslvuproteasetoregulatethelevelofanessentialproteininnamedcontentcontenttypegenusspeciesshewanellaoneidensisnamedcontent AT vincentmejean interplaybetweenthehsp90chaperoneandthehslvuproteasetoregulatethelevelofanessentialproteininnamedcontentcontenttypegenusspeciesshewanellaoneidensisnamedcontent AT oliviergenest interplaybetweenthehsp90chaperoneandthehslvuproteasetoregulatethelevelofanessentialproteininnamedcontentcontenttypegenusspeciesshewanellaoneidensisnamedcontent
_version_	1718427152048717824

Interplay between the Hsp90 Chaperone and the HslVU Protease To Regulate the Level of an Essential Protein in <named-content content-type="genus-species">Shewanella oneidensis</named-content>

Ejemplares similares