Periplasmic oxidized-protein repair during copper stress in E. coli: A focus on the metallochaperone CusF.
Methionine residues are particularly sensitive to oxidation by reactive oxygen or chlorine species (ROS/RCS), leading to the appearance of methionine sulfoxide in proteins. This post-translational oxidation can be reversed by omnipresent protein repair pathways involving methionine sulfoxide reducta...
| Main Authors: | , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Public Library of Science (PLoS)
2022-07-01
|
| Series: | PLoS Genetics |
| Online Access: | https://doi.org/10.1371/journal.pgen.1010180 |
| _version_ | 1798002678996926464 |
|---|---|
| author | Alexandra Vergnes Camille Henry Gaia Grassini Laurent Loiseau Sara El Hajj Yann Denis Anne Galinier Didier Vertommen Laurent Aussel Benjamin Ezraty |
| author_facet | Alexandra Vergnes Camille Henry Gaia Grassini Laurent Loiseau Sara El Hajj Yann Denis Anne Galinier Didier Vertommen Laurent Aussel Benjamin Ezraty |
| author_sort | Alexandra Vergnes |
| collection | DOAJ |
| description | Methionine residues are particularly sensitive to oxidation by reactive oxygen or chlorine species (ROS/RCS), leading to the appearance of methionine sulfoxide in proteins. This post-translational oxidation can be reversed by omnipresent protein repair pathways involving methionine sulfoxide reductases (Msr). In the periplasm of Escherichia coli, the enzymatic system MsrPQ, whose expression is triggered by the RCS, controls the redox status of methionine residues. Here we report that MsrPQ synthesis is also induced by copper stress via the CusSR two-component system, and that MsrPQ plays a role in copper homeostasis by maintaining the activity of the copper efflux pump, CusCFBA. Genetic and biochemical evidence suggest the metallochaperone CusF is the substrate of MsrPQ and our study reveals that CusF methionines are redox sensitive and can be restored by MsrPQ. Thus, the evolution of a CusSR-dependent synthesis of MsrPQ allows conservation of copper homeostasis under aerobic conditions by maintenance of the reduced state of Met residues in copper-trafficking proteins. |
| first_indexed | 2024-04-11T11:56:03Z |
| format | Article |
| id | doaj.art-15bde4244bf24faeb63a64d50f742a50 |
| institution | Directory Open Access Journal |
| issn | 1553-7390 1553-7404 |
| language | English |
| last_indexed | 2024-04-11T11:56:03Z |
| publishDate | 2022-07-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Genetics |
| spelling | doaj.art-15bde4244bf24faeb63a64d50f742a502022-12-22T04:25:10ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042022-07-01187e101018010.1371/journal.pgen.1010180Periplasmic oxidized-protein repair during copper stress in E. coli: A focus on the metallochaperone CusF.Alexandra VergnesCamille HenryGaia GrassiniLaurent LoiseauSara El HajjYann DenisAnne GalinierDidier VertommenLaurent AusselBenjamin EzratyMethionine residues are particularly sensitive to oxidation by reactive oxygen or chlorine species (ROS/RCS), leading to the appearance of methionine sulfoxide in proteins. This post-translational oxidation can be reversed by omnipresent protein repair pathways involving methionine sulfoxide reductases (Msr). In the periplasm of Escherichia coli, the enzymatic system MsrPQ, whose expression is triggered by the RCS, controls the redox status of methionine residues. Here we report that MsrPQ synthesis is also induced by copper stress via the CusSR two-component system, and that MsrPQ plays a role in copper homeostasis by maintaining the activity of the copper efflux pump, CusCFBA. Genetic and biochemical evidence suggest the metallochaperone CusF is the substrate of MsrPQ and our study reveals that CusF methionines are redox sensitive and can be restored by MsrPQ. Thus, the evolution of a CusSR-dependent synthesis of MsrPQ allows conservation of copper homeostasis under aerobic conditions by maintenance of the reduced state of Met residues in copper-trafficking proteins.https://doi.org/10.1371/journal.pgen.1010180 |
| spellingShingle | Alexandra Vergnes Camille Henry Gaia Grassini Laurent Loiseau Sara El Hajj Yann Denis Anne Galinier Didier Vertommen Laurent Aussel Benjamin Ezraty Periplasmic oxidized-protein repair during copper stress in E. coli: A focus on the metallochaperone CusF. PLoS Genetics |
| title | Periplasmic oxidized-protein repair during copper stress in E. coli: A focus on the metallochaperone CusF. |
| title_full | Periplasmic oxidized-protein repair during copper stress in E. coli: A focus on the metallochaperone CusF. |
| title_fullStr | Periplasmic oxidized-protein repair during copper stress in E. coli: A focus on the metallochaperone CusF. |
| title_full_unstemmed | Periplasmic oxidized-protein repair during copper stress in E. coli: A focus on the metallochaperone CusF. |
| title_short | Periplasmic oxidized-protein repair during copper stress in E. coli: A focus on the metallochaperone CusF. |
| title_sort | periplasmic oxidized protein repair during copper stress in e coli a focus on the metallochaperone cusf |
| url | https://doi.org/10.1371/journal.pgen.1010180 |
| work_keys_str_mv | AT alexandravergnes periplasmicoxidizedproteinrepairduringcopperstressinecoliafocusonthemetallochaperonecusf AT camillehenry periplasmicoxidizedproteinrepairduringcopperstressinecoliafocusonthemetallochaperonecusf AT gaiagrassini periplasmicoxidizedproteinrepairduringcopperstressinecoliafocusonthemetallochaperonecusf AT laurentloiseau periplasmicoxidizedproteinrepairduringcopperstressinecoliafocusonthemetallochaperonecusf AT saraelhajj periplasmicoxidizedproteinrepairduringcopperstressinecoliafocusonthemetallochaperonecusf AT yanndenis periplasmicoxidizedproteinrepairduringcopperstressinecoliafocusonthemetallochaperonecusf AT annegalinier periplasmicoxidizedproteinrepairduringcopperstressinecoliafocusonthemetallochaperonecusf AT didiervertommen periplasmicoxidizedproteinrepairduringcopperstressinecoliafocusonthemetallochaperonecusf AT laurentaussel periplasmicoxidizedproteinrepairduringcopperstressinecoliafocusonthemetallochaperonecusf AT benjaminezraty periplasmicoxidizedproteinrepairduringcopperstressinecoliafocusonthemetallochaperonecusf |