Crystal structure of a substrate-engaged SecY protein-translocation channel
Abstract
Hydrophobic signal sequences target secretory polypeptides to a protein-conducting channel formed by a heterotrimeric membrane protein complex, the prokaryotic SecY or eukaryotic Sec61 complex. How signal sequences are recognized is poorly understood, particularly because they are diverse in sequence and length. Structures of the inactive channel show that the largest subunit, SecY or Sec61α, consists of two halves that form an hourglass-shaped pore with a constriction in the middle of the membrane and a lateral gate that faces lipid. The cytoplasmic funnel is empty, while the extracellular funnel is filled with a plug domain. In bacteria, the SecY channel associates with the translating ribosome in co-translational translocation, and with the SecA ATPase in post-translational translocation. How a translocating polypeptide inserts into the channel is uncertain, as cryo-electron microscopy structures of the active channel have a relatively low resolution (~10 Å) or are of insufficient quality. Here we report a crystal structure of the active channel, assembled from SecY complex, the SecA ATPase, and a segment of a secretory protein fused into SecA. The translocating protein segment inserts into the channel as a loop, displacing the plug domain. The hydrophobic core of the signal sequence forms a helix that sits inmore »
- Authors:
-
- Howard Hughes Medical Institute and Harvard Medical School, Boston, MA (United States)
- The Rockefeller University and Howard Hughes Medical Inst., New York, NY (United States); Howard Hughes Medical Institute and Harvard Medical School, Boston, MA (United States)
- Whitehead Inst. for Biomedical Research, Cambridge, MA (United States)
- Publication Date:
- Research Org.:
- Argonne National Laboratory (ANL), Argonne, IL (United States)
- Sponsoring Org.:
- National Inst. of Health
- OSTI Identifier:
- 1243126
- Grant/Contract Number:
- GM052586
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Nature (London)
- Additional Journal Information:
- Journal Name: Nature (London); Journal Volume: 531; Journal Issue: 7594; Journal ID: ISSN 0028-0836
- Publisher:
- Nature Publishing Group
- Country of Publication:
- United States
- Language:
- ENGLISH
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Protein translocation; X-ray crystallography
Citation Formats
Li, Long, Park, Eunyong, Ling, JingJing, Ingram, Jessica, Ploegh, Hidde, and Rapoport, Tom A. Crystal structure of a substrate-engaged SecY protein-translocation channel. United States: N. p., 2016.
Web. doi:10.1038/nature17163.
Li, Long, Park, Eunyong, Ling, JingJing, Ingram, Jessica, Ploegh, Hidde, & Rapoport, Tom A. Crystal structure of a substrate-engaged SecY protein-translocation channel. United States. https://doi.org/10.1038/nature17163
Li, Long, Park, Eunyong, Ling, JingJing, Ingram, Jessica, Ploegh, Hidde, and Rapoport, Tom A. Mon .
"Crystal structure of a substrate-engaged SecY protein-translocation channel". United States. https://doi.org/10.1038/nature17163. https://www.osti.gov/servlets/purl/1243126.
@article{osti_1243126,
title = {Crystal structure of a substrate-engaged SecY protein-translocation channel},
author = {Li, Long and Park, Eunyong and Ling, JingJing and Ingram, Jessica and Ploegh, Hidde and Rapoport, Tom A.},
abstractNote = {Hydrophobic signal sequences target secretory polypeptides to a protein-conducting channel formed by a heterotrimeric membrane protein complex, the prokaryotic SecY or eukaryotic Sec61 complex. How signal sequences are recognized is poorly understood, particularly because they are diverse in sequence and length. Structures of the inactive channel show that the largest subunit, SecY or Sec61α, consists of two halves that form an hourglass-shaped pore with a constriction in the middle of the membrane and a lateral gate that faces lipid. The cytoplasmic funnel is empty, while the extracellular funnel is filled with a plug domain. In bacteria, the SecY channel associates with the translating ribosome in co-translational translocation, and with the SecA ATPase in post-translational translocation. How a translocating polypeptide inserts into the channel is uncertain, as cryo-electron microscopy structures of the active channel have a relatively low resolution (~10 Å) or are of insufficient quality. Here we report a crystal structure of the active channel, assembled from SecY complex, the SecA ATPase, and a segment of a secretory protein fused into SecA. The translocating protein segment inserts into the channel as a loop, displacing the plug domain. The hydrophobic core of the signal sequence forms a helix that sits in a groove outside the lateral gate, while the following polypeptide segment intercalates into the gate. The carboxy (C)-terminal section of the polypeptide loop is located in the channel, surrounded by residues of the pore ring. Furthermore, during translocation, the hydrophobic segments of signal sequences, and probably bilayer-spanning domains of nascent membrane proteins, exit the lateral gate and dock at a specific site that faces the lipid phase.},
doi = {10.1038/nature17163},
journal = {Nature (London)},
number = 7594,
volume = 531,
place = {United States},
year = {Mon Mar 07 00:00:00 EST 2016},
month = {Mon Mar 07 00:00:00 EST 2016}
}
Web of Science
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Dynamic action of the Sec machinery during initiation, protein translocation and termination
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Protein Translocation: SecA–SecY Conformational Crosstalk Opens Channel
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Voltage Sensing in Bacterial Protein Translocation
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Protein Transport Across the Bacterial Plasma Membrane by the Sec Pathway
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Two-way communication between SecY and SecA suggests a Brownian ratchet mechanism for protein translocation
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ZMPSTE24 missense mutations that cause progeroid diseases decrease prelamin A cleavage activity and/or protein stability
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