Structure of the ER membrane complex, a transmembrane-domain insertase

The endoplasmic reticulum (ER) membrane complex (EMC) cooperates with the Sec61 translocon to co-translationally insert a transmembrane helix (TMH) of many multi-pass integral membrane proteins into the ER membrane, and it is also responsible for inserting the TMH of some tail-anchored proteins 1 –...

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Veröffentlicht in:Nature (London) Jg. 584; H. 7821; S. 475 - 478
Hauptverfasser: Bai, Lin, You, Qinglong, Feng, Xiang, Kovach, Amanda, Li, Huilin
Format: Journal Article
Sprache:Englisch
Veröffentlicht: London Nature Publishing Group UK 20.08.2020
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ISSN:0028-0836, 1476-4687, 1476-4687
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Abstract The endoplasmic reticulum (ER) membrane complex (EMC) cooperates with the Sec61 translocon to co-translationally insert a transmembrane helix (TMH) of many multi-pass integral membrane proteins into the ER membrane, and it is also responsible for inserting the TMH of some tail-anchored proteins 1 – 3 . How EMC accomplishes this feat has been unclear. Here we report the first, to our knowledge, cryo-electron microscopy structure of the eukaryotic EMC. We found that the Saccharomyces cerevisiae EMC contains eight subunits (Emc1–6, Emc7 and Emc10), has a large lumenal region and a smaller cytosolic region, and has a transmembrane region formed by Emc4, Emc5 and Emc6 plus the transmembrane domains of Emc1 and Emc3. We identified a five-TMH fold centred around Emc3 that resembles the prokaryotic YidC insertase and that delineates a largely hydrophilic client protein pocket. The transmembrane domain of Emc4 tilts away from the main transmembrane region of EMC and is partially mobile. Mutational studies demonstrated that the flexibility of Emc4 and the hydrophilicity of the client pocket are required for EMC function. The EMC structure reveals notable evolutionary conservation with the prokaryotic insertases 4 , 5 , suggests that eukaryotic TMH insertion involves a similar mechanism, and provides a framework for detailed understanding of membrane insertion for numerous eukaryotic integral membrane proteins and tail-anchored proteins. The cryo-electron microscopy structure of the ER membrane complex provides insight into its overall architecture, evolution and function in co-translational protein insertion.
AbstractList The endoplasmic reticulum (ER) membrane complex (EMC) cooperates with the Sec61 translocon to co-translationally insert a transmembrane helix (TMH) of many multi-pass integral membrane proteins into the ER membrane, and it is also responsible for inserting the TMH of some tail-anchored proteins1-3. How EMC accomplishes this feat has been unclear. Here we report the first, to our knowledge, cryo-electron microscopy structure of the eukaryotic EMC. We found that the Saccharomyces cerevisiae EMC contains eight subunits (Emc1-6, Emc7 and Emc10), has a large lumenal region and a smaller cytosolic region, and has a transmembrane region formed by Emc4, Emc5 and Emc6 plus the transmembrane domains of Emc1 and Emc3. We identified a five-TMH fold centred around Emc3 that resembles the prokaryotic YidC insertase and that delineates a largely hydrophilic client protein pocket. The transmembrane domain of Emc4 tilts away from the main transmembrane region ofEMC and is partially mobile. Mutational studies demonstrated that the flexibility of Emc4 and the hydrophilicity of the client pocket are required for EMC function. The EMC structure reveals notable evolutionary conservation with the prokaryotic insertases4,5, suggests that eukaryotic TMH insertion involves a similar mechanism, and provides a framework for detailed understanding of membrane insertion for numerous eukaryotic integral membrane proteins and tail-anchored proteins.
The ER membrane complex (EMC) cooperates with the Sec61 translocon to co-translationally insert a transmembrane helix (TMH) of many multi-pass integral membrane proteins into the ER membrane, and it is also responsible for inserting the TMH of some tail-anchored proteins 1–3. How EMC accomplishes this feat has been unclear. Here we report the first cryo-EM structure of the eukaryotic EMC. We found that the Saccharomyces cerevisiae EMC contains eight subunits (Emc1–6, 7, and 10); has a large lumenal region and a smaller cytosolic region; and has a transmembrane region formed by Emc4, 5, and 6 plus the transmembrane domains (TMDs) of Emc1 and 3. We identified a 5-TMH fold centered around Emc3 that resembles the prokaryotic insertase YidC and that delineates a largely hydrophilic client pocket. The TMD of Emc4 tilts away from the main transmembrane region of EMC and is partially mobile. Mutational studies demonstrated that Emc4 flexibility and the hydrophilicity of the client pocket are required for EMC function. The EMC structure reveals a remarkable evolutionary conservation with the prokaryotic insertases 4,5; suggests a similar mechanism of TMH insertion; and provides a framework for detailed understanding of membrane insertion for numerous eukaryotic integral membrane proteins and tail-anchored proteins.
The endoplasmic reticulum (ER) membrane complex (EMC) cooperates with the Sec61 translocon to co-translationally insert a transmembrane helix (TMH) of many multi-pass integral membrane proteins into the ER membrane, and it is also responsible for inserting the TMH of some tail-anchored proteins 1 – 3 . How EMC accomplishes this feat has been unclear. Here we report the first, to our knowledge, cryo-electron microscopy structure of the eukaryotic EMC. We found that the Saccharomyces cerevisiae EMC contains eight subunits (Emc1–6, Emc7 and Emc10), has a large lumenal region and a smaller cytosolic region, and has a transmembrane region formed by Emc4, Emc5 and Emc6 plus the transmembrane domains of Emc1 and Emc3. We identified a five-TMH fold centred around Emc3 that resembles the prokaryotic YidC insertase and that delineates a largely hydrophilic client protein pocket. The transmembrane domain of Emc4 tilts away from the main transmembrane region of EMC and is partially mobile. Mutational studies demonstrated that the flexibility of Emc4 and the hydrophilicity of the client pocket are required for EMC function. The EMC structure reveals notable evolutionary conservation with the prokaryotic insertases 4 , 5 , suggests that eukaryotic TMH insertion involves a similar mechanism, and provides a framework for detailed understanding of membrane insertion for numerous eukaryotic integral membrane proteins and tail-anchored proteins. The cryo-electron microscopy structure of the ER membrane complex provides insight into its overall architecture, evolution and function in co-translational protein insertion.
The endoplasmic reticulum (ER) membrane complex (EMC) cooperates with the Sec61 translocon to co-translationally insert a transmembrane helix (TMH) of many multi-pass integral membrane proteins into the ER membrane, and it is also responsible for inserting the TMH of some tail-anchored proteins . How EMC accomplishes this feat has been unclear. Here we report the first, to our knowledge, cryo-electron microscopy structure of the eukaryotic EMC. We found that the Saccharomyces cerevisiae EMC contains eight subunits (Emc1-6, Emc7 and Emc10), has a large lumenal region and a smaller cytosolic region, and has a transmembrane region formed by Emc4, Emc5 and Emc6 plus the transmembrane domains of Emc1 and Emc3. We identified a five-TMH fold centred around Emc3 that resembles the prokaryotic YidC insertase and that delineates a largely hydrophilic client protein pocket. The transmembrane domain of Emc4 tilts away from the main transmembrane region of EMC and is partially mobile. Mutational studies demonstrated that the flexibility of Emc4 and the hydrophilicity of the client pocket are required for EMC function. The EMC structure reveals notable evolutionary conservation with the prokaryotic insertases , suggests that eukaryotic TMH insertion involves a similar mechanism, and provides a framework for detailed understanding of membrane insertion for numerous eukaryotic integral membrane proteins and tail-anchored proteins.
The endoplasmic reticulum (ER) membrane complex (EMC) cooperates with the Sec61 translocon to co-translationally insert a transmembrane helix (TMH) of many multi-pass integral membrane proteins into the ER membrane, and it is also responsible for inserting the TMH of some tail-anchored proteins1-3. How EMC accomplishes this feat has been unclear. Here we report the first, to our knowledge, cryo-electron microscopy structure of the eukaryotic EMC. We found that the Saccharomyces cerevisiae EMC contains eight subunits (Emc1-6, Emc7 and Emc10), has a large lumenal region and a smaller cytosolic region, and has a transmembrane region formed by Emc4, Emc5 and Emc6 plus the transmembrane domains of Emc1 and Emc3. We identified a five-TMH fold centred around Emc3 that resembles the prokaryotic YidC insertase and that delineates a largely hydrophilic client protein pocket. The transmembrane domain of Emc4 tilts away from the main transmembrane region of EMC and is partially mobile. Mutational studies demonstrated that the flexibility of Emc4 and the hydrophilicity of the client pocket are required for EMC function. The EMC structure reveals notable evolutionary conservation with the prokaryotic insertases4,5, suggests that eukaryotic TMH insertion involves a similar mechanism, and provides a framework for detailed understanding of membrane insertion for numerous eukaryotic integral membrane proteins and tail-anchored proteins.The endoplasmic reticulum (ER) membrane complex (EMC) cooperates with the Sec61 translocon to co-translationally insert a transmembrane helix (TMH) of many multi-pass integral membrane proteins into the ER membrane, and it is also responsible for inserting the TMH of some tail-anchored proteins1-3. How EMC accomplishes this feat has been unclear. Here we report the first, to our knowledge, cryo-electron microscopy structure of the eukaryotic EMC. We found that the Saccharomyces cerevisiae EMC contains eight subunits (Emc1-6, Emc7 and Emc10), has a large lumenal region and a smaller cytosolic region, and has a transmembrane region formed by Emc4, Emc5 and Emc6 plus the transmembrane domains of Emc1 and Emc3. We identified a five-TMH fold centred around Emc3 that resembles the prokaryotic YidC insertase and that delineates a largely hydrophilic client protein pocket. The transmembrane domain of Emc4 tilts away from the main transmembrane region of EMC and is partially mobile. Mutational studies demonstrated that the flexibility of Emc4 and the hydrophilicity of the client pocket are required for EMC function. The EMC structure reveals notable evolutionary conservation with the prokaryotic insertases4,5, suggests that eukaryotic TMH insertion involves a similar mechanism, and provides a framework for detailed understanding of membrane insertion for numerous eukaryotic integral membrane proteins and tail-anchored proteins.
Author Bai, Lin
Feng, Xiang
Kovach, Amanda
You, Qinglong
Li, Huilin
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  givenname: Lin
  orcidid: 0000-0002-7535-7819
  surname: Bai
  fullname: Bai, Lin
  email: lin.bai@vai.org
  organization: Structural Biology Program, Van Andel Institute
– sequence: 2
  givenname: Qinglong
  surname: You
  fullname: You, Qinglong
  organization: Structural Biology Program, Van Andel Institute
– sequence: 3
  givenname: Xiang
  surname: Feng
  fullname: Feng, Xiang
  organization: Structural Biology Program, Van Andel Institute
– sequence: 4
  givenname: Amanda
  surname: Kovach
  fullname: Kovach, Amanda
  organization: Structural Biology Program, Van Andel Institute
– sequence: 5
  givenname: Huilin
  orcidid: 0000-0001-8085-8928
  surname: Li
  fullname: Li, Huilin
  email: huilin.li@vai.org
  organization: Structural Biology Program, Van Andel Institute
BackLink https://www.ncbi.nlm.nih.gov/pubmed/32494008$$D View this record in MEDLINE/PubMed
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CONTRIBUTIONS. L.B. and H.L. conceived and designed experiments. L.B. performed most of the experiments. Q.Y, X. F., and A.K. helped with sample preparation and functional assays. L.B. and H.L. analyzed the data and wrote the manuscript.
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– reference: 33346928 - EMBO J. 2021 Jan 15;40(2):e107407
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Snippet The endoplasmic reticulum (ER) membrane complex (EMC) cooperates with the Sec61 translocon to co-translationally insert a transmembrane helix (TMH) of many...
The ER membrane complex (EMC) cooperates with the Sec61 translocon to co-translationally insert a transmembrane helix (TMH) of many multi-pass integral...
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springer
SourceType Open Access Repository
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Publisher
StartPage 475
SubjectTerms 101/28
101/58
14/19
631/45/173
631/535/1258/1259
631/80/2023/2022
82/16
82/83
Binding Sites
Conservation
Cryoelectron Microscopy
Electron microscopy
Endoplasmic reticulum
Endoplasmic Reticulum - chemistry
Endoplasmic Reticulum - enzymology
Endoplasmic Reticulum - ultrastructure
Evolution, Molecular
Evolutionary conservation
Humanities and Social Sciences
Hydrophobic and Hydrophilic Interactions
Insertion
Integral membrane proteins
Integrals
Intracellular Membranes - chemistry
Intracellular Membranes - enzymology
Intracellular Membranes - ultrastructure
Membranes
Microscopy
Models, Molecular
multidisciplinary
Multiprotein Complexes - chemistry
Multiprotein Complexes - genetics
Multiprotein Complexes - metabolism
Multiprotein Complexes - ultrastructure
Mutation
Protein Domains
Protein Subunits - chemistry
Protein Subunits - genetics
Protein Subunits - metabolism
Proteins
Saccharomyces cerevisiae - chemistry
Saccharomyces cerevisiae - enzymology
Saccharomyces cerevisiae - genetics
Saccharomyces cerevisiae - ultrastructure
Saccharomyces cerevisiae Proteins - chemistry
Saccharomyces cerevisiae Proteins - genetics
Saccharomyces cerevisiae Proteins - metabolism
Saccharomyces cerevisiae Proteins - ultrastructure
Science
Science (multidisciplinary)
Structure-function relationships
Substrate Specificity
Transmembrane domains
Yeast
Title Structure of the ER membrane complex, a transmembrane-domain insertase
URI https://link.springer.com/article/10.1038/s41586-020-2389-3
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https://pubmed.ncbi.nlm.nih.gov/PMC7442705
Volume 584
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