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Unbalanced Charge Distribution as a Determinant for Dependence of a Subset of Escherichia coli Membrane Proteins on the Membrane Insertase YidC

Membrane proteins are involved in numerous essential cell processes, including transport, gene regulation, motility, and metabolism. To function properly, they must be inserted into the membrane and folded correctly. YidC, an essential protein in Escherichia coli with homologues in other bacteria, A...

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Autores principales: Gray, Andrew N., Henderson-Frost, Josephine M., Boyd, Dana, Shirafi, Shirin, Niki, Hironori, Goldberg, Marcia B.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society of Microbiology 2011
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3225971/
https://www.ncbi.nlm.nih.gov/pubmed/22108384
http://dx.doi.org/10.1128/mBio.00238-11
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author Gray, Andrew N.
Henderson-Frost, Josephine M.
Boyd, Dana
Shirafi, Shirin
Niki, Hironori
Goldberg, Marcia B.
author_facet Gray, Andrew N.
Henderson-Frost, Josephine M.
Boyd, Dana
Shirafi, Shirin
Niki, Hironori
Goldberg, Marcia B.
author_sort Gray, Andrew N.
collection PubMed
description Membrane proteins are involved in numerous essential cell processes, including transport, gene regulation, motility, and metabolism. To function properly, they must be inserted into the membrane and folded correctly. YidC, an essential protein in Escherichia coli with homologues in other bacteria, Archaea, mitochondria, and chloroplasts, functions by incompletely understood mechanisms in the insertion and folding of certain membrane proteins. Using a genome-scale approach, we identified 69 E. coli membrane proteins that, in the absence of YidC, exhibited aberrant localization by microscopy. Further examination of a subset revealed biochemical defects in membrane insertion in the absence of YidC, indicating their dependence on YidC for proper membrane insertion or folding. Membrane proteins possessing an unfavorable distribution of positively charged residues were significantly more likely to depend on YidC for membrane insertion. Correcting the charge distribution of a charge-unbalanced YidC-dependent membrane protein abrogated its requirement for YidC, while perturbing the charge distribution of a charge-balanced YidC-independent membrane protein rendered it YidC dependent, demonstrating that charge distribution can be a necessary and sufficient determinant of YidC dependence. These findings provide insights into a mechanism by which YidC promotes proper membrane protein biogenesis and suggest a critical function of YidC in all organisms and organelles that express it.
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spelling pubmed-32259712011-11-30 Unbalanced Charge Distribution as a Determinant for Dependence of a Subset of Escherichia coli Membrane Proteins on the Membrane Insertase YidC Gray, Andrew N. Henderson-Frost, Josephine M. Boyd, Dana Shirafi, Shirin Niki, Hironori Goldberg, Marcia B. mBio Research Article Membrane proteins are involved in numerous essential cell processes, including transport, gene regulation, motility, and metabolism. To function properly, they must be inserted into the membrane and folded correctly. YidC, an essential protein in Escherichia coli with homologues in other bacteria, Archaea, mitochondria, and chloroplasts, functions by incompletely understood mechanisms in the insertion and folding of certain membrane proteins. Using a genome-scale approach, we identified 69 E. coli membrane proteins that, in the absence of YidC, exhibited aberrant localization by microscopy. Further examination of a subset revealed biochemical defects in membrane insertion in the absence of YidC, indicating their dependence on YidC for proper membrane insertion or folding. Membrane proteins possessing an unfavorable distribution of positively charged residues were significantly more likely to depend on YidC for membrane insertion. Correcting the charge distribution of a charge-unbalanced YidC-dependent membrane protein abrogated its requirement for YidC, while perturbing the charge distribution of a charge-balanced YidC-independent membrane protein rendered it YidC dependent, demonstrating that charge distribution can be a necessary and sufficient determinant of YidC dependence. These findings provide insights into a mechanism by which YidC promotes proper membrane protein biogenesis and suggest a critical function of YidC in all organisms and organelles that express it. American Society of Microbiology 2011-11-22 /pmc/articles/PMC3225971/ /pubmed/22108384 http://dx.doi.org/10.1128/mBio.00238-11 Text en Copyright © 2011 Gray et al. http://creativecommons.org/licenses/by-nc-sa/3.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial-Share Alike 3.0 Unported License (http://creativecommons.org/licenses/by-nc-sa/3.0/) , which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Gray, Andrew N.
Henderson-Frost, Josephine M.
Boyd, Dana
Shirafi, Shirin
Niki, Hironori
Goldberg, Marcia B.
Unbalanced Charge Distribution as a Determinant for Dependence of a Subset of Escherichia coli Membrane Proteins on the Membrane Insertase YidC
title Unbalanced Charge Distribution as a Determinant for Dependence of a Subset of Escherichia coli Membrane Proteins on the Membrane Insertase YidC
title_full Unbalanced Charge Distribution as a Determinant for Dependence of a Subset of Escherichia coli Membrane Proteins on the Membrane Insertase YidC
title_fullStr Unbalanced Charge Distribution as a Determinant for Dependence of a Subset of Escherichia coli Membrane Proteins on the Membrane Insertase YidC
title_full_unstemmed Unbalanced Charge Distribution as a Determinant for Dependence of a Subset of Escherichia coli Membrane Proteins on the Membrane Insertase YidC
title_short Unbalanced Charge Distribution as a Determinant for Dependence of a Subset of Escherichia coli Membrane Proteins on the Membrane Insertase YidC
title_sort unbalanced charge distribution as a determinant for dependence of a subset of escherichia coli membrane proteins on the membrane insertase yidc
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3225971/
https://www.ncbi.nlm.nih.gov/pubmed/22108384
http://dx.doi.org/10.1128/mBio.00238-11
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