YidC is in involved in the biogenesis of the secreted autotransporter Hemoglobin Protease

Research output: Contribution to JournalArticleAcademicpeer-review

Abstract

Autotransporters (ATs) constitute an important family of virulence factors secreted by Gram-negative bacteria. Following their translocation across the inner membrane (IM), ATs temporarily reside in the periplasmic space after which they are secreted into the extracellular environment. Previous studies have shown that the AT hemoglobin protease (Hbp) of Escherichia coli requires a functional signal recognition particle pathway and Sec translocon for optimal targeting to and translocation across the IM. Here, we analyzed the mode of IM translocation of Hbp in more detail. Using site-directed photocross-linking, we found that the Hbp signal peptide is adjacent to YidC early during biogenesis. Notably, YidC is in part associated with the Sec translocon but has until now primarily been implicated in the biogenesis of IM proteins. In vivo, YidC appeared critical for the biogenesis of the ATs Hbp and EspC. For Hbp, depletion of YidC resulted in the formation of secretion-incompetent intermediates that were sensitive to degradation by the periplasmic protease DegP, indicating that YidC activity affects Hbp biogenesis at a late stage, after translocation across the IM. This is the first demonstration of a role for YidC in the biogenesis of an extracellular protein. We propose that YidC is required for maintenance of the translocation-competent state of certain ATs in the periplasm. The large periplasmic domain of YidC is not critical for this novel functionality as it can be deleted without affecting Hbp biogenesis. © 2010 by The American Society for Biochemistry and Molecular Biology, Inc.
LanguageEnglish
Pages39682-39690
Number of pages9
JournalJournal of Biological Chemistry
Volume285
Issue number51
DOIs
Publication statusPublished - 2010

Fingerprint

Hemoglobins
Peptide Hydrolases
Membranes
Periplasm
Signal Recognition Particle
Virulence Factors
Protein Sorting Signals
Type V Secretion Systems
Gram-Negative Bacteria
Escherichia coli
Bacteria
Membrane Proteins
Demonstrations
Maintenance
Degradation
Proteins

Cite this

@article{d75d7c65d05745a794902887aef4fe22,
title = "YidC is in involved in the biogenesis of the secreted autotransporter Hemoglobin Protease",
abstract = "Autotransporters (ATs) constitute an important family of virulence factors secreted by Gram-negative bacteria. Following their translocation across the inner membrane (IM), ATs temporarily reside in the periplasmic space after which they are secreted into the extracellular environment. Previous studies have shown that the AT hemoglobin protease (Hbp) of Escherichia coli requires a functional signal recognition particle pathway and Sec translocon for optimal targeting to and translocation across the IM. Here, we analyzed the mode of IM translocation of Hbp in more detail. Using site-directed photocross-linking, we found that the Hbp signal peptide is adjacent to YidC early during biogenesis. Notably, YidC is in part associated with the Sec translocon but has until now primarily been implicated in the biogenesis of IM proteins. In vivo, YidC appeared critical for the biogenesis of the ATs Hbp and EspC. For Hbp, depletion of YidC resulted in the formation of secretion-incompetent intermediates that were sensitive to degradation by the periplasmic protease DegP, indicating that YidC activity affects Hbp biogenesis at a late stage, after translocation across the IM. This is the first demonstration of a role for YidC in the biogenesis of an extracellular protein. We propose that YidC is required for maintenance of the translocation-competent state of certain ATs in the periplasm. The large periplasmic domain of YidC is not critical for this novel functionality as it can be deleted without affecting Hbp biogenesis. {\circledC} 2010 by The American Society for Biochemistry and Molecular Biology, Inc.",
author = "W.S.P. Jong and {ten Hagen-Jongman ten}, C.M. and E. Ruijter and R.V.A. Orru and P. Genevaux and S. Luirink",
year = "2010",
doi = "10.1074/jbc.M110.167650",
language = "English",
volume = "285",
pages = "39682--39690",
journal = "Journal of Biological Chemistry",
issn = "0021-9258",
publisher = "American Society for Biochemistry and Molecular Biology Inc.",
number = "51",

}

YidC is in involved in the biogenesis of the secreted autotransporter Hemoglobin Protease. / Jong, W.S.P.; ten Hagen-Jongman ten, C.M.; Ruijter, E.; Orru, R.V.A.; Genevaux, P.; Luirink, S.

In: Journal of Biological Chemistry, Vol. 285, No. 51, 2010, p. 39682-39690.

Research output: Contribution to JournalArticleAcademicpeer-review

TY - JOUR

T1 - YidC is in involved in the biogenesis of the secreted autotransporter Hemoglobin Protease

AU - Jong, W.S.P.

AU - ten Hagen-Jongman ten, C.M.

AU - Ruijter, E.

AU - Orru, R.V.A.

AU - Genevaux, P.

AU - Luirink, S.

PY - 2010

Y1 - 2010

N2 - Autotransporters (ATs) constitute an important family of virulence factors secreted by Gram-negative bacteria. Following their translocation across the inner membrane (IM), ATs temporarily reside in the periplasmic space after which they are secreted into the extracellular environment. Previous studies have shown that the AT hemoglobin protease (Hbp) of Escherichia coli requires a functional signal recognition particle pathway and Sec translocon for optimal targeting to and translocation across the IM. Here, we analyzed the mode of IM translocation of Hbp in more detail. Using site-directed photocross-linking, we found that the Hbp signal peptide is adjacent to YidC early during biogenesis. Notably, YidC is in part associated with the Sec translocon but has until now primarily been implicated in the biogenesis of IM proteins. In vivo, YidC appeared critical for the biogenesis of the ATs Hbp and EspC. For Hbp, depletion of YidC resulted in the formation of secretion-incompetent intermediates that were sensitive to degradation by the periplasmic protease DegP, indicating that YidC activity affects Hbp biogenesis at a late stage, after translocation across the IM. This is the first demonstration of a role for YidC in the biogenesis of an extracellular protein. We propose that YidC is required for maintenance of the translocation-competent state of certain ATs in the periplasm. The large periplasmic domain of YidC is not critical for this novel functionality as it can be deleted without affecting Hbp biogenesis. © 2010 by The American Society for Biochemistry and Molecular Biology, Inc.

AB - Autotransporters (ATs) constitute an important family of virulence factors secreted by Gram-negative bacteria. Following their translocation across the inner membrane (IM), ATs temporarily reside in the periplasmic space after which they are secreted into the extracellular environment. Previous studies have shown that the AT hemoglobin protease (Hbp) of Escherichia coli requires a functional signal recognition particle pathway and Sec translocon for optimal targeting to and translocation across the IM. Here, we analyzed the mode of IM translocation of Hbp in more detail. Using site-directed photocross-linking, we found that the Hbp signal peptide is adjacent to YidC early during biogenesis. Notably, YidC is in part associated with the Sec translocon but has until now primarily been implicated in the biogenesis of IM proteins. In vivo, YidC appeared critical for the biogenesis of the ATs Hbp and EspC. For Hbp, depletion of YidC resulted in the formation of secretion-incompetent intermediates that were sensitive to degradation by the periplasmic protease DegP, indicating that YidC activity affects Hbp biogenesis at a late stage, after translocation across the IM. This is the first demonstration of a role for YidC in the biogenesis of an extracellular protein. We propose that YidC is required for maintenance of the translocation-competent state of certain ATs in the periplasm. The large periplasmic domain of YidC is not critical for this novel functionality as it can be deleted without affecting Hbp biogenesis. © 2010 by The American Society for Biochemistry and Molecular Biology, Inc.

U2 - 10.1074/jbc.M110.167650

DO - 10.1074/jbc.M110.167650

M3 - Article

VL - 285

SP - 39682

EP - 39690

JO - Journal of Biological Chemistry

T2 - Journal of Biological Chemistry

JF - Journal of Biological Chemistry

SN - 0021-9258

IS - 51

ER -