Hierarchical Model for the Role of J-Domain Proteins in Distinct Cellular Functions

[Display omitted] •The specific role of JDPs in bacterial cellular functions is unclear.•DnaJ, one of the JDPs in E. coli, is essential for survival at high temperature.•Either DnaJ or CbpA is sufficient to activate DnaK in bacterial amyloid production.•DnaJ and CbpA promote the DnaK-regulated produ...

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Bibliographic Details
Published in:	Journal of molecular biology Vol. 433; no. 3; p. 166750
Main Authors:	Sugimoto, Shinya, Yamanaka, Kunitoshi, Niwa, Tatsuya, Terasawa, Yurika, Kinjo, Yuki, Mizunoe, Yoshimitsu, Ogura, Teru
Format:	Journal Article
Language:	English
Published:	England Elsevier Ltd 05-02-2021
Subjects:	chaperone curli DNA-Binding Proteins - genetics DNA-Binding Proteins - metabolism Escherichia coli - physiology Escherichia coli Proteins - chemistry Escherichia coli Proteins - metabolism hierarchy HSP70 Heat-Shock Proteins - chemistry HSP70 Heat-Shock Proteins - metabolism Hsp70/DnaK JDPs Models, Biological Protein Binding Protein Domains Protein Interaction Domains and Motifs Protein Transport Proteins - chemistry Proteins - genetics Proteins - metabolism Sequence Deletion Solubility TSB Hsp HFIP hierarchy KJE NEF KAE CR NBD TBS-T curli chaperone SBD JDP Hsp70/DnaK JDPs
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Summary:	[Display omitted] •The specific role of JDPs in bacterial cellular functions is unclear.•DnaJ, one of the JDPs in E. coli, is essential for survival at high temperature.•Either DnaJ or CbpA is sufficient to activate DnaK in bacterial amyloid production.•DnaJ and CbpA promote the DnaK-regulated production of curli at multiple steps.•The role of JDPs in the DnaK system differs in different cellular functions. In Escherichia coli, the major bacterial Hsp70 system consists of DnaK, three J-domain proteins (JDPs: DnaJ, CbpA, and DjlA), and nucleotide exchange factor GrpE. JDPs determine substrate specificity for the Hsp70 system; however, knowledge on their specific role in bacterial cellular functions is limited. In this study, we demonstrated the role of JDPs in bacterial survival during heat stress and the DnaK-regulated formation of curli—extracellular amyloid fibers involved in biofilm formation. Genetic analysis demonstrate that only DnaJ is essential for survival at high temperature. On the other hand, either DnaJ or CbpA, but not DjlA, is sufficient to activate DnaK in curli production. Additionally, several DnaK mutants with reduced activity are able to complement the loss of curli production in E. coli ΔdnaK, whereas they do not recover the growth defect of the mutant strain at high temperature. Biochemical analyses reveal that DnaJ and CbpA are involved in the expression of the master regulator CsgD through the solubilization of MlrA, a DNA-binding transcriptional activator for the csgD promoter. Furthermore, DnaJ and CbpA also keep CsgA in a translocation-competent state by preventing its aggregation in the cytoplasm. Our findings support a hierarchical model wherein the role of JDPs in the Hsp70 system differs according to individual cellular functions.
ISSN:	0022-2836 1089-8638
DOI:	10.1016/j.jmb.2020.166750