PpiD is a player in the network of periplasmic chaperones in <it>Escherichia coli</it>

<p>Abstract</p> <p>Background</p> <p>The inner membrane-anchored periplasmic folding factor PpiD is described as a parvulin-like peptidyl prolyl isomerase (PPIase) that assists in the maturation of the major beta-barrel outer membrane proteins (OMPs) of <it>Escher...

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Main Authors: Behrens-Kneip Susanne, Barion Birgitta, Matern Yvonne
Format: Article
Language:English
Published: BMC 2010-09-01
Series:BMC Microbiology
Online Access:http://www.biomedcentral.com/1471-2180/10/251
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author Behrens-Kneip Susanne
Barion Birgitta
Matern Yvonne
author_facet Behrens-Kneip Susanne
Barion Birgitta
Matern Yvonne
author_sort Behrens-Kneip Susanne
collection DOAJ
description <p>Abstract</p> <p>Background</p> <p>The inner membrane-anchored periplasmic folding factor PpiD is described as a parvulin-like peptidyl prolyl isomerase (PPIase) that assists in the maturation of the major beta-barrel outer membrane proteins (OMPs) of <it>Escherichia coli</it>. More recent work however, calls these findings into question. Here, we re-examined the role of PpiD in the <it>E. coli </it>periplasm by analyzing its functional interplay with other folding factors that influence OMP maturation as well as general protein folding in the periplasmic compartment of the cell, such as SurA, Skp, and DegP.</p> <p>Results</p> <p>The analysis of the effects of both deletion and overexpression of <it>ppiD </it>on cell envelope phenotypes revealed that PpiD in contrast to prior observations plays only a minor role, if any, in the maturation of OMPs and cannot compensate for the lack of SurA in the periplasm. On the other hand, our results show that overproduction of PpiD rescues a <it>surA skp </it>double mutant from lethality. In the presence of increased PpiD levels <it>surA skp </it>cells show reduced activities of both the SigmaE-dependent and the Cpx envelope stress responses, and contain increased amounts of folded species of the major OMP OmpA. These effects require the anchoring of PpiD in the inner membrane but are independent of its parvulin-like PPIase domain. Moreover, a PpiD protein lacking the PPIase domain also complements the growth defects of an <it>fkpA ppiD surA </it>triple PPIase mutant and exhibits chaperone activity <it>in vitro</it>. In addition, PpiD appears to collaborate with DegP, as deletion of <it>ppiD </it>confers a temperature-dependent conditional synthetic phenotype in a <it>degP </it>mutant.</p> <p>Conclusions</p> <p>This study provides first direct evidence that PpiD functions as a chaperone and contributes to the network of periplasmic chaperone activities without being specifically involved in OMP maturation. Consistent with previous work, our data support a model in which the chaperone function of PpiD is used to aid in the early periplasmic folding of many newly translocated proteins.</p>
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spelling doaj.art-444cf5922c604f7fa8316b706fd92da52022-12-21T23:42:15ZengBMCBMC Microbiology1471-21802010-09-0110125110.1186/1471-2180-10-251PpiD is a player in the network of periplasmic chaperones in <it>Escherichia coli</it>Behrens-Kneip SusanneBarion BirgittaMatern Yvonne<p>Abstract</p> <p>Background</p> <p>The inner membrane-anchored periplasmic folding factor PpiD is described as a parvulin-like peptidyl prolyl isomerase (PPIase) that assists in the maturation of the major beta-barrel outer membrane proteins (OMPs) of <it>Escherichia coli</it>. More recent work however, calls these findings into question. Here, we re-examined the role of PpiD in the <it>E. coli </it>periplasm by analyzing its functional interplay with other folding factors that influence OMP maturation as well as general protein folding in the periplasmic compartment of the cell, such as SurA, Skp, and DegP.</p> <p>Results</p> <p>The analysis of the effects of both deletion and overexpression of <it>ppiD </it>on cell envelope phenotypes revealed that PpiD in contrast to prior observations plays only a minor role, if any, in the maturation of OMPs and cannot compensate for the lack of SurA in the periplasm. On the other hand, our results show that overproduction of PpiD rescues a <it>surA skp </it>double mutant from lethality. In the presence of increased PpiD levels <it>surA skp </it>cells show reduced activities of both the SigmaE-dependent and the Cpx envelope stress responses, and contain increased amounts of folded species of the major OMP OmpA. These effects require the anchoring of PpiD in the inner membrane but are independent of its parvulin-like PPIase domain. Moreover, a PpiD protein lacking the PPIase domain also complements the growth defects of an <it>fkpA ppiD surA </it>triple PPIase mutant and exhibits chaperone activity <it>in vitro</it>. In addition, PpiD appears to collaborate with DegP, as deletion of <it>ppiD </it>confers a temperature-dependent conditional synthetic phenotype in a <it>degP </it>mutant.</p> <p>Conclusions</p> <p>This study provides first direct evidence that PpiD functions as a chaperone and contributes to the network of periplasmic chaperone activities without being specifically involved in OMP maturation. Consistent with previous work, our data support a model in which the chaperone function of PpiD is used to aid in the early periplasmic folding of many newly translocated proteins.</p>http://www.biomedcentral.com/1471-2180/10/251
spellingShingle Behrens-Kneip Susanne
Barion Birgitta
Matern Yvonne
PpiD is a player in the network of periplasmic chaperones in <it>Escherichia coli</it>
BMC Microbiology
title PpiD is a player in the network of periplasmic chaperones in <it>Escherichia coli</it>
title_full PpiD is a player in the network of periplasmic chaperones in <it>Escherichia coli</it>
title_fullStr PpiD is a player in the network of periplasmic chaperones in <it>Escherichia coli</it>
title_full_unstemmed PpiD is a player in the network of periplasmic chaperones in <it>Escherichia coli</it>
title_short PpiD is a player in the network of periplasmic chaperones in <it>Escherichia coli</it>
title_sort ppid is a player in the network of periplasmic chaperones in it escherichia coli it
url http://www.biomedcentral.com/1471-2180/10/251
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