Periprotein lipidomes of Saccharomyces cerevisiae provide a flexible environment for conformational changes of membrane proteins
Yeast tolerates a low pH and high solvent concentrations. The permeability of the plasma membrane (PM) for small molecules is low and lateral diffusion of proteins is slow. These findings suggest a high degree of lipid order, which raises the question of how membrane proteins function in such an env...
| Main Authors: | , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
eLife Sciences Publications Ltd
2020-04-01
|
| Series: | eLife |
| Subjects: | |
| Online Access: | https://elifesciences.org/articles/57003 |
| _version_ | 1811201242844626944 |
|---|---|
| author | Joury S van 't Klooster Tan-Yun Cheng Hendrik R Sikkema Aike Jeucken Branch Moody Bert Poolman |
| author_facet | Joury S van 't Klooster Tan-Yun Cheng Hendrik R Sikkema Aike Jeucken Branch Moody Bert Poolman |
| author_sort | Joury S van 't Klooster |
| collection | DOAJ |
| description | Yeast tolerates a low pH and high solvent concentrations. The permeability of the plasma membrane (PM) for small molecules is low and lateral diffusion of proteins is slow. These findings suggest a high degree of lipid order, which raises the question of how membrane proteins function in such an environment. The yeast PM is segregated into the Micro-Compartment-of-Can1 (MCC) and Pma1 (MCP), which have different lipid compositions. We extracted proteins from these microdomains via stoichiometric capture of lipids and proteins in styrene-maleic-acid-lipid-particles (SMALPs). We purified SMALP-lipid-protein complexes by chromatography and quantitatively analyzed periprotein lipids located within the diameter defined by one SMALP. Phospholipid and sterol concentrations are similar for MCC and MCP, but sphingolipids are enriched in MCP. Ergosterol is depleted from this periprotein lipidome, whereas phosphatidylserine is enriched relative to the bulk of the plasma membrane. Direct detection of PM lipids in the 'periprotein space' supports the conclusion that proteins function in the presence of a locally disordered lipid state. |
| first_indexed | 2024-04-12T02:18:51Z |
| format | Article |
| id | doaj.art-51119df5db0440f5a4a92bf00b7bc3e5 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-12T02:18:51Z |
| publishDate | 2020-04-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-51119df5db0440f5a4a92bf00b7bc3e52022-12-22T03:52:11ZengeLife Sciences Publications LtdeLife2050-084X2020-04-01910.7554/eLife.57003Periprotein lipidomes of Saccharomyces cerevisiae provide a flexible environment for conformational changes of membrane proteinsJoury S van 't Klooster0https://orcid.org/0000-0002-1232-8615Tan-Yun Cheng1https://orcid.org/0000-0002-5178-6985Hendrik R Sikkema2Aike Jeucken3Branch Moody4Bert Poolman5https://orcid.org/0000-0002-1455-531XDepartment of Biochemistry, University of Groningen Groningen Biomolecular Sciences and Biotechnology Institute, Groningen, NetherlandsDivision of Rheumatology, Inflammation and Immunity Brigham and Women's Hospital, Harvard Medical School, Boston, United StatesDepartment of Biochemistry, University of Groningen Groningen Biomolecular Sciences and Biotechnology Institute, Groningen, NetherlandsDepartment of Biochemistry, University of Groningen Groningen Biomolecular Sciences and Biotechnology Institute, Groningen, NetherlandsDivision of Rheumatology, Inflammation and Immunity Brigham and Women's Hospital, Harvard Medical School, Boston, United States; Department of Medicine, Harvard Medical School, Boston, United StatesDepartment of Biochemistry, University of Groningen Groningen Biomolecular Sciences and Biotechnology Institute, Groningen, NetherlandsYeast tolerates a low pH and high solvent concentrations. The permeability of the plasma membrane (PM) for small molecules is low and lateral diffusion of proteins is slow. These findings suggest a high degree of lipid order, which raises the question of how membrane proteins function in such an environment. The yeast PM is segregated into the Micro-Compartment-of-Can1 (MCC) and Pma1 (MCP), which have different lipid compositions. We extracted proteins from these microdomains via stoichiometric capture of lipids and proteins in styrene-maleic-acid-lipid-particles (SMALPs). We purified SMALP-lipid-protein complexes by chromatography and quantitatively analyzed periprotein lipids located within the diameter defined by one SMALP. Phospholipid and sterol concentrations are similar for MCC and MCP, but sphingolipids are enriched in MCP. Ergosterol is depleted from this periprotein lipidome, whereas phosphatidylserine is enriched relative to the bulk of the plasma membrane. Direct detection of PM lipids in the 'periprotein space' supports the conclusion that proteins function in the presence of a locally disordered lipid state.https://elifesciences.org/articles/57003lipidomicsplasma membraneSaccharomyces cerevisiaeeisosomemembrane proteinsmembrane domains |
| spellingShingle | Joury S van 't Klooster Tan-Yun Cheng Hendrik R Sikkema Aike Jeucken Branch Moody Bert Poolman Periprotein lipidomes of Saccharomyces cerevisiae provide a flexible environment for conformational changes of membrane proteins eLife lipidomics plasma membrane Saccharomyces cerevisiae eisosome membrane proteins membrane domains |
| title | Periprotein lipidomes of Saccharomyces cerevisiae provide a flexible environment for conformational changes of membrane proteins |
| title_full | Periprotein lipidomes of Saccharomyces cerevisiae provide a flexible environment for conformational changes of membrane proteins |
| title_fullStr | Periprotein lipidomes of Saccharomyces cerevisiae provide a flexible environment for conformational changes of membrane proteins |
| title_full_unstemmed | Periprotein lipidomes of Saccharomyces cerevisiae provide a flexible environment for conformational changes of membrane proteins |
| title_short | Periprotein lipidomes of Saccharomyces cerevisiae provide a flexible environment for conformational changes of membrane proteins |
| title_sort | periprotein lipidomes of saccharomyces cerevisiae provide a flexible environment for conformational changes of membrane proteins |
| topic | lipidomics plasma membrane Saccharomyces cerevisiae eisosome membrane proteins membrane domains |
| url | https://elifesciences.org/articles/57003 |
| work_keys_str_mv | AT jourysvantklooster periproteinlipidomesofsaccharomycescerevisiaeprovideaflexibleenvironmentforconformationalchangesofmembraneproteins AT tanyuncheng periproteinlipidomesofsaccharomycescerevisiaeprovideaflexibleenvironmentforconformationalchangesofmembraneproteins AT hendrikrsikkema periproteinlipidomesofsaccharomycescerevisiaeprovideaflexibleenvironmentforconformationalchangesofmembraneproteins AT aikejeucken periproteinlipidomesofsaccharomycescerevisiaeprovideaflexibleenvironmentforconformationalchangesofmembraneproteins AT branchmoody periproteinlipidomesofsaccharomycescerevisiaeprovideaflexibleenvironmentforconformationalchangesofmembraneproteins AT bertpoolman periproteinlipidomesofsaccharomycescerevisiaeprovideaflexibleenvironmentforconformationalchangesofmembraneproteins |