Lon Protease Quality Control of Presecretory Proteins in Escherichia coli and Its Dependence on the SecB and DnaJ (Hsp40) Chaperones

Various environmental insults result in irreversible damage to proteins and protein complexes. To cope, cells have evolved dedicated protein quality control mechanisms involving molecular chaperones and proteases. Here, we provide both genetic and biochemical evidence that the Lon protease and the S...

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Bibliographic Details
Published in:The Journal of biological chemistry 2010-07, Vol.285 (30), p.23506-23514
Main Authors: Sakr, Samer, Cirinesi, Anne-Marie, Ullers, Ronald S., Schwager, Françoise, Georgopoulos, Costa, Genevaux, Pierre
Format: Article
Language:English
Subjects:
Bacterial Proteins - metabolism
Cold Temperature
DnaJ
DnaK
Escherichia coli
Escherichia coli - enzymology
Escherichia coli - metabolism
Escherichia coli - physiology
Escherichia coli Proteins - metabolism
Gene Deletion
HSP40 Heat-Shock Proteins - metabolism
Lon
Microbiology
Mutation
Protease La - deficiency
Protease La - genetics
Protease La - metabolism
Protein Degradation
Protein Export
Protein Folding
Protein Secretion
Protein Structure and Folding
Protein Targeting
Quality Control
SecB
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Summary:Various environmental insults result in irreversible damage to proteins and protein complexes. To cope, cells have evolved dedicated protein quality control mechanisms involving molecular chaperones and proteases. Here, we provide both genetic and biochemical evidence that the Lon protease and the SecB and DnaJ/Hsp40 chaperones are involved in the quality control of presecretory proteins in Escherichia coli. We showed that mutations in the lon gene alleviate the cold-sensitive phenotype of a secB mutant. Such suppression was not observed with either clpP or clpQ protease mutants. In comparison to the respective single mutants, the double secB lon mutant strongly accumulates aggregates of SecB substrates at physiological temperatures, suggesting that the chaperone and the protease share substrates. These observations were extended in vitro by showing that the main substrates identified in secB lon aggregates, namely proOmpF and proOmpC, are highly sensitive to specific degradation by Lon. In contrast, both substrates are significantly protected from Lon degradation by SecB. Interestingly, the chaperone DnaJ by itself protects substrates better from Lon degradation than SecB or the complete DnaK/DnaJ/GrpE chaperone machinery. In agreement with this finding, a DnaJ mutant protein that does not functionally interact in vivo with DnaK efficiently suppresses the SecB cold-sensitive phenotype, highlighting the role of DnaJ in assisting presecretory proteins. Taken together, our data suggest that when the Sec secretion pathway is compromised, a pool of presecretory proteins is transiently maintained in a translocation-competent state and, thus, protected from Lon degradation by either the SecB or DnaJ chaperones.
ISSN:0021-9258
1083-351X
DOI:10.1074/jbc.M110.133058