Endosome and Golgi‐associated degradation (EGAD) of membrane proteins regulates sphingolipid metabolism
Cellular homeostasis requires the ubiquitin‐dependent degradation of membrane proteins. This was assumed to be mediated exclusively either by endoplasmic reticulum‐associated degradation (ERAD) or by endosomal sorting complexes required for transport (ESCRT)‐dependent lysosomal degradation. We ident...
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| Vydané v: | The EMBO journal Ročník 38; číslo 15; s. e101433 - n/a |
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| Hlavní autori: | , , , , , , , , , , , |
| Médium: | Journal Article |
| Jazyk: | English |
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London
Nature Publishing Group UK
01.08.2019
Springer Nature B.V EMBO Press |
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| ISSN: | 0261-4189, 1460-2075, 1460-2075 |
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| Abstract | Cellular homeostasis requires the ubiquitin‐dependent degradation of membrane proteins. This was assumed to be mediated exclusively either by endoplasmic reticulum‐associated degradation (ERAD) or by endosomal sorting complexes required for transport (ESCRT)‐dependent lysosomal degradation. We identified in
Saccharomyces cerevisiae
an additional pathway that selectively extracts membrane proteins at Golgi and endosomes for degradation by cytosolic proteasomes. One endogenous substrate of this endosome and Golgi‐associated degradation pathway (EGAD) is the ER‐resident membrane protein Orm2, a negative regulator of sphingolipid biosynthesis. Orm2 degradation is initiated by phosphorylation, which triggers its ER export. Once on Golgi and endosomes, Orm2 is poly‐ubiquitinated by the membrane‐embedded “Defective in SREBP cleavage” (Dsc) ubiquitin ligase complex. Cdc48/VCP then extracts ubiquitinated Orm2 from membranes, which is tightly coupled to the proteasomal degradation of Orm2. Thereby, EGAD prevents the accumulation of Orm2 at the ER and in post‐ER compartments and promotes the controlled de‐repression of sphingolipid biosynthesis. Thus, the selective degradation of membrane proteins by EGAD contributes to proteostasis and lipid homeostasis in eukaryotic cells.
Synopsis
Ubiquitin‐dependent membrane protein degradation is thought to occur primarily via ERAD or ESCRT pathways. Endosome and Golgi‐associated degradation (EGAD) of membrane proteins from post‐ER compartments represents a novel mechanisms contributing to proteostasis and lipid homeostasis in
S. cerevisiae
.
EGAD selectively extracts membrane proteins from Golgi and endosomes for degradation by cytosolic proteases.
Orm2, a repressor of sphingolipid synthesis, represents the first endogenous EGAD substrate.
Cdc48/VCP extracts Orm2 from membranes following its ubiquitination by the Dsc ubiquitin ligase complex.
EGAD‐dependent Orm2 degradation is essential for a controlled de‐repression of sphingolipid synthesis.
Graphical Abstract
A novel mechanism for ubiquitin‐dependent extraction from post‐ER compartments regulates proteostasis of yeast membrane protein in addition to ERAD and ESCRT pathways. |
|---|---|
| AbstractList | Cellular homeostasis requires the ubiquitin‐dependent degradation of membrane proteins. This was assumed to be mediated exclusively either by endoplasmic reticulum‐associated degradation (ERAD) or by endosomal sorting complexes required for transport (ESCRT)‐dependent lysosomal degradation. We identified in
Saccharomyces cerevisiae
an additional pathway that selectively extracts membrane proteins at Golgi and endosomes for degradation by cytosolic proteasomes. One endogenous substrate of this endosome and Golgi‐associated degradation pathway (EGAD) is the ER‐resident membrane protein Orm2, a negative regulator of sphingolipid biosynthesis. Orm2 degradation is initiated by phosphorylation, which triggers its ER export. Once on Golgi and endosomes, Orm2 is poly‐ubiquitinated by the membrane‐embedded “Defective in SREBP cleavage” (Dsc) ubiquitin ligase complex. Cdc48/VCP then extracts ubiquitinated Orm2 from membranes, which is tightly coupled to the proteasomal degradation of Orm2. Thereby, EGAD prevents the accumulation of Orm2 at the ER and in post‐ER compartments and promotes the controlled de‐repression of sphingolipid biosynthesis. Thus, the selective degradation of membrane proteins by EGAD contributes to proteostasis and lipid homeostasis in eukaryotic cells.
Synopsis
Ubiquitin‐dependent membrane protein degradation is thought to occur primarily via ERAD or ESCRT pathways. Endosome and Golgi‐associated degradation (EGAD) of membrane proteins from post‐ER compartments represents a novel mechanisms contributing to proteostasis and lipid homeostasis in
S. cerevisiae
.
EGAD selectively extracts membrane proteins from Golgi and endosomes for degradation by cytosolic proteases.
Orm2, a repressor of sphingolipid synthesis, represents the first endogenous EGAD substrate.
Cdc48/VCP extracts Orm2 from membranes following its ubiquitination by the Dsc ubiquitin ligase complex.
EGAD‐dependent Orm2 degradation is essential for a controlled de‐repression of sphingolipid synthesis.
Graphical Abstract
A novel mechanism for ubiquitin‐dependent extraction from post‐ER compartments regulates proteostasis of yeast membrane protein in addition to ERAD and ESCRT pathways. Cellular homeostasis requires the ubiquitin‐dependent degradation of membrane proteins. This was assumed to be mediated exclusively either by endoplasmic reticulum‐associated degradation (ERAD) or by endosomal sorting complexes required for transport (ESCRT)‐dependent lysosomal degradation. We identified in Saccharomyces cerevisiae an additional pathway that selectively extracts membrane proteins at Golgi and endosomes for degradation by cytosolic proteasomes. One endogenous substrate of this endosome and Golgi‐associated degradation pathway (EGAD) is the ER‐resident membrane protein Orm2, a negative regulator of sphingolipid biosynthesis. Orm2 degradation is initiated by phosphorylation, which triggers its ER export. Once on Golgi and endosomes, Orm2 is poly‐ubiquitinated by the membrane‐embedded “Defective in SREBP cleavage” (Dsc) ubiquitin ligase complex. Cdc48/VCP then extracts ubiquitinated Orm2 from membranes, which is tightly coupled to the proteasomal degradation of Orm2. Thereby, EGAD prevents the accumulation of Orm2 at the ER and in post‐ER compartments and promotes the controlled de‐repression of sphingolipid biosynthesis. Thus, the selective degradation of membrane proteins by EGAD contributes to proteostasis and lipid homeostasis in eukaryotic cells. Cellular homeostasis requires the ubiquitin-dependent degradation of membrane proteins. This was assumed to be mediated exclusively either by endoplasmic reticulum-associated degradation (ERAD) or by endosomal sorting complexes required for transport (ESCRT)-dependent lysosomal degradation. We identified in Saccharomyces cerevisiae an additional pathway that selectively extracts membrane proteins at Golgi and endosomes for degradation by cytosolic proteasomes. One endogenous substrate of this endosome and Golgi-associated degradation pathway (EGAD) is the ER-resident membrane protein Orm2, a negative regulator of sphingolipid biosynthesis. Orm2 degradation is initiated by phosphorylation, which triggers its ER export. Once on Golgi and endosomes, Orm2 is poly-ubiquitinated by the membrane-embedded "Defective in SREBP cleavage" (Dsc) ubiquitin ligase complex. Cdc48/VCP then extracts ubiquitinated Orm2 from membranes, which is tightly coupled to the proteasomal degradation of Orm2. Thereby, EGAD prevents the accumulation of Orm2 at the ER and in post-ER compartments and promotes the controlled de-repression of sphingolipid biosynthesis. Thus, the selective degradation of membrane proteins by EGAD contributes to proteostasis and lipid homeostasis in eukaryotic cells.Cellular homeostasis requires the ubiquitin-dependent degradation of membrane proteins. This was assumed to be mediated exclusively either by endoplasmic reticulum-associated degradation (ERAD) or by endosomal sorting complexes required for transport (ESCRT)-dependent lysosomal degradation. We identified in Saccharomyces cerevisiae an additional pathway that selectively extracts membrane proteins at Golgi and endosomes for degradation by cytosolic proteasomes. One endogenous substrate of this endosome and Golgi-associated degradation pathway (EGAD) is the ER-resident membrane protein Orm2, a negative regulator of sphingolipid biosynthesis. Orm2 degradation is initiated by phosphorylation, which triggers its ER export. Once on Golgi and endosomes, Orm2 is poly-ubiquitinated by the membrane-embedded "Defective in SREBP cleavage" (Dsc) ubiquitin ligase complex. Cdc48/VCP then extracts ubiquitinated Orm2 from membranes, which is tightly coupled to the proteasomal degradation of Orm2. Thereby, EGAD prevents the accumulation of Orm2 at the ER and in post-ER compartments and promotes the controlled de-repression of sphingolipid biosynthesis. Thus, the selective degradation of membrane proteins by EGAD contributes to proteostasis and lipid homeostasis in eukaryotic cells. Cellular homeostasis requires the ubiquitin-dependent degradation of membrane proteins. This was assumed to be mediated exclusively either by endoplasmic reticulum-associated degradation (ERAD) or by endosomal sorting complexes required for transport (ESCRT)-dependent lysosomal degradation. We identified in an additional pathway that selectively extracts membrane proteins at Golgi and endosomes for degradation by cytosolic proteasomes. One endogenous substrate of this endosome and Golgi-associated degradation pathway (EGAD) is the ER-resident membrane protein Orm2, a negative regulator of sphingolipid biosynthesis. Orm2 degradation is initiated by phosphorylation, which triggers its ER export. Once on Golgi and endosomes, Orm2 is poly-ubiquitinated by the membrane-embedded "Defective in SREBP cleavage" (Dsc) ubiquitin ligase complex. Cdc48/VCP then extracts ubiquitinated Orm2 from membranes, which is tightly coupled to the proteasomal degradation of Orm2. Thereby, EGAD prevents the accumulation of Orm2 at the ER and in post-ER compartments and promotes the controlled de-repression of sphingolipid biosynthesis. Thus, the selective degradation of membrane proteins by EGAD contributes to proteostasis and lipid homeostasis in eukaryotic cells. Cellular homeostasis requires the ubiquitin‐dependent degradation of membrane proteins. This was assumed to be mediated exclusively either by endoplasmic reticulum‐associated degradation (ERAD) or by endosomal sorting complexes required for transport (ESCRT)‐dependent lysosomal degradation. We identified in Saccharomyces cerevisiae an additional pathway that selectively extracts membrane proteins at Golgi and endosomes for degradation by cytosolic proteasomes. One endogenous substrate of this endosome and Golgi‐associated degradation pathway (EGAD) is the ER‐resident membrane protein Orm2, a negative regulator of sphingolipid biosynthesis. Orm2 degradation is initiated by phosphorylation, which triggers its ER export. Once on Golgi and endosomes, Orm2 is poly‐ubiquitinated by the membrane‐embedded “Defective in SREBP cleavage” (Dsc) ubiquitin ligase complex. Cdc48/VCP then extracts ubiquitinated Orm2 from membranes, which is tightly coupled to the proteasomal degradation of Orm2. Thereby, EGAD prevents the accumulation of Orm2 at the ER and in post‐ER compartments and promotes the controlled de‐repression of sphingolipid biosynthesis. Thus, the selective degradation of membrane proteins by EGAD contributes to proteostasis and lipid homeostasis in eukaryotic cells. Synopsis Ubiquitin‐dependent membrane protein degradation is thought to occur primarily via ERAD or ESCRT pathways. Endosome and Golgi‐associated degradation (EGAD) of membrane proteins from post‐ER compartments represents a novel mechanisms contributing to proteostasis and lipid homeostasis in S. cerevisiae. EGAD selectively extracts membrane proteins from Golgi and endosomes for degradation by cytosolic proteases. Orm2, a repressor of sphingolipid synthesis, represents the first endogenous EGAD substrate. Cdc48/VCP extracts Orm2 from membranes following its ubiquitination by the Dsc ubiquitin ligase complex. EGAD‐dependent Orm2 degradation is essential for a controlled de‐repression of sphingolipid synthesis. A novel mechanism for ubiquitin‐dependent extraction from post‐ER compartments regulates proteostasis of yeast membrane protein in addition to ERAD and ESCRT pathways. |
| Author | Teis, David Widerin, Michael A Angelova, Mihaela Fröhlich, Florian Schmidt, Oliver Kremser, Leopold Lindner, Herbert Baumann, Verena Weyer, Yannick Eising, Sebastian Schleiffer, Alexander Peter, Matthias |
| Author_xml | – sequence: 1 givenname: Oliver orcidid: 0000-0002-7921-4663 surname: Schmidt fullname: Schmidt, Oliver organization: Division of Cell Biology, Biocenter, Medical University of Innsbruck – sequence: 2 givenname: Yannick surname: Weyer fullname: Weyer, Yannick organization: Division of Cell Biology, Biocenter, Medical University of Innsbruck – sequence: 3 givenname: Verena surname: Baumann fullname: Baumann, Verena organization: Division of Cell Biology, Biocenter, Medical University of Innsbruck, MFPL, University of Vienna – sequence: 4 givenname: Michael A surname: Widerin fullname: Widerin, Michael A organization: Division of Cell Biology, Biocenter, Medical University of Innsbruck – sequence: 5 givenname: Sebastian surname: Eising fullname: Eising, Sebastian organization: Department of Biology/Chemistry, University of Osnabrück – sequence: 6 givenname: Mihaela orcidid: 0000-0002-0495-9695 surname: Angelova fullname: Angelova, Mihaela organization: INSERM, Laboratory of Integrative Cancer Immunology, Sorbonne Université, Sorbonne Paris Cité, Université Paris Descartes, Centre de Recherche des Cordeliers, Université Paris Diderot – sequence: 7 givenname: Alexander orcidid: 0000-0001-6251-2747 surname: Schleiffer fullname: Schleiffer, Alexander organization: Research Institute of Molecular Pathology (IMP), Vienna Biocenter (VBC), Institute of Molecular Biotechnology of the Austrian Academy of Sciences (IMBA), Vienna Biocenter (VBC) – sequence: 8 givenname: Leopold surname: Kremser fullname: Kremser, Leopold organization: Division of Clinical Biochemistry, Protein Micro‐Analysis Facility, Biocenter, Medical University of Innsbruck – sequence: 9 givenname: Herbert surname: Lindner fullname: Lindner, Herbert organization: Division of Clinical Biochemistry, Protein Micro‐Analysis Facility, Biocenter, Medical University of Innsbruck – sequence: 10 givenname: Matthias surname: Peter fullname: Peter, Matthias organization: Institute of Biochemistry, ETH‐Zürich – sequence: 11 givenname: Florian orcidid: 0000-0001-8307-2189 surname: Fröhlich fullname: Fröhlich, Florian organization: Department of Biology/Chemistry, University of Osnabrück – sequence: 12 givenname: David orcidid: 0000-0002-8181-0253 surname: Teis fullname: Teis, David email: david.teis@i-med.ac.at organization: Division of Cell Biology, Biocenter, Medical University of Innsbruck |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/31133554$$D View this record in MEDLINE/PubMed https://hal.sorbonne-universite.fr/hal-02282147$$DView record in HAL |
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| ISSN | 0261-4189 1460-2075 |
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| Issue | 15 |
| Keywords | proteasome endosomes Golgi sphingolipids ubiquitin |
| Language | English |
| License | Attribution 2019 The Authors. Published under the terms of the CC BY 4.0 license. Distributed under a Creative Commons Attribution 4.0 International License: http://creativecommons.org/licenses/by/4.0 |
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| SubjectTerms | Biochemistry Biochemistry, Molecular Biology Biodegradation Biosynthesis Cellular Biology Compartments Degradation EMBO20 EMBO31 Endoplasmic reticulum Endosomes Golgi Golgi apparatus Homeostasis Life Sciences Lipid metabolism Lipids Lysosomes Membrane proteins Membranes Phosphorylation proteasome Proteasomes Proteins Saccharomyces cerevisiae sphingolipids Sterol regulatory element-binding protein Substrates Ubiquitin Ubiquitin-protein ligase Ubiquitination |
| Title | Endosome and Golgi‐associated degradation (EGAD) of membrane proteins regulates sphingolipid metabolism |
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