Literature DB >> 23148222

Hsp33 controls elongation factor-Tu stability and allows Escherichia coli growth in the absence of the major DnaK and trigger factor chaperones.

Nicolas Bruel1, Marie-Pierre Castanié-Cornet, Anne-Marie Cirinesi, Gregory Koningstein, Costa Georgopoulos, Joen Luirink, Pierre Genevaux.   

Abstract

Intracellular de novo protein folding is assisted by cellular networks of molecular chaperones. In Escherichia coli, cooperation between the chaperones trigger factor (TF) and DnaK is central to this process. Accordingly, the simultaneous deletion of both chaperone-encoding genes leads to severe growth and protein folding defects. Herein, we took advantage of such defective phenotypes to further elucidate the interactions of chaperone networks in vivo. We show that disruption of the TF/DnaK chaperone pathway is efficiently rescued by overexpression of the redox-regulated chaperone Hsp33. Consistent with this observation, the deletion of hslO, the Hsp33 structural gene, is no longer tolerated in the absence of the TF/DnaK pathway. However, in contrast with other chaperones like GroEL or SecB, suppression by Hsp33 was not attributed to its potential overlapping general chaperone function(s). Instead, we show that overexpressed Hsp33 specifically binds to elongation factor-Tu (EF-Tu) and targets it for degradation by the protease Lon. This synergistic action of Hsp33 and Lon was responsible for the rescue of bacterial growth in the absence of TF and DnaK, by presumably restoring the coupling between translation and the downstream folding capacity of the cell. In support of this hypothesis, we show that overexpression of the stress-responsive toxin HipA, which inhibits EF-Tu, also rescues bacterial growth and protein folding in the absence of TF and DnaK. The relevance for such a convergence of networks of chaperones and proteases acting directly on EF-Tu to modulate the intracellular rate of protein synthesis in response to protein aggregation is discussed.

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Year:  2012        PMID: 23148222      PMCID: PMC3531757          DOI: 10.1074/jbc.M112.418525

Source DB:  PubMed          Journal:  J Biol Chem        ISSN: 0021-9258            Impact factor:   5.157


  65 in total

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Journal:  Nature       Date:  1992-10-22       Impact factor: 49.962

2.  Sequence and structure of Clp P, the proteolytic component of the ATP-dependent Clp protease of Escherichia coli.

Authors:  M R Maurizi; W P Clark; Y Katayama; S Rudikoff; J Pumphrey; B Bowers; S Gottesman
Journal:  J Biol Chem       Date:  1990-07-25       Impact factor: 5.157

3.  Transposition and fusion of the lac genes to selected promoters in Escherichia coli using bacteriophage lambda and Mu.

Authors:  M J Casadaban
Journal:  J Mol Biol       Date:  1976-07-05       Impact factor: 5.469

4.  The groES and groEL heat shock gene products of Escherichia coli are essential for bacterial growth at all temperatures.

Authors:  O Fayet; T Ziegelhoffer; C Georgopoulos
Journal:  J Bacteriol       Date:  1989-03       Impact factor: 3.490

5.  The reaction of ribosomes with elongation factor Tu.GTP complexes. Aminoacyl-tRNA-independent reactions in the elongation cycle determine the accuracy of protein synthesis.

Authors:  R C Thompson; D B Dix; A M Karim
Journal:  J Biol Chem       Date:  1986-04-15       Impact factor: 5.157

6.  Characterization of twenty-six new heat shock genes of Escherichia coli.

Authors:  S E Chuang; F R Blattner
Journal:  J Bacteriol       Date:  1993-08       Impact factor: 3.490

7.  Trigger factor: a soluble protein that folds pro-OmpA into a membrane-assembly-competent form.

Authors:  E Crooke; W Wickner
Journal:  Proc Natl Acad Sci U S A       Date:  1987-08       Impact factor: 11.205

8.  Delta dnaK52 mutants of Escherichia coli have defects in chromosome segregation and plasmid maintenance at normal growth temperatures.

Authors:  B Bukau; G C Walker
Journal:  J Bacteriol       Date:  1989-11       Impact factor: 3.490

Review 9.  Selective translation during stress in Escherichia coli.

Authors:  Isabella Moll; Hanna Engelberg-Kulka
Journal:  Trends Biochem Sci       Date:  2012-08-30       Impact factor: 13.807

10.  Mutations altering heat shock specific subunit of RNA polymerase suppress major cellular defects of E. coli mutants lacking the DnaK chaperone.

Authors:  B Bukau; G C Walker
Journal:  EMBO J       Date:  1990-12       Impact factor: 11.598

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  15 in total

Review 1.  Stress-induced remodeling of the bacterial proteome.

Authors:  Monica S Guo; Carol A Gross
Journal:  Curr Biol       Date:  2014-05-19       Impact factor: 10.834

2.  Directed evolution of SecB chaperones toward toxin-antitoxin systems.

Authors:  Ambre Julie Sala; Patricia Bordes; Sara Ayala; Nawel Slama; Samuel Tranier; Michèle Coddeville; Anne-Marie Cirinesi; Marie-Pierre Castanié-Cornet; Lionel Mourey; Pierre Genevaux
Journal:  Proc Natl Acad Sci U S A       Date:  2017-11-07       Impact factor: 11.205

3.  Proteotoxic stress induces a cell-cycle arrest by stimulating Lon to degrade the replication initiator DnaA.

Authors:  Kristina Jonas; Jing Liu; Peter Chien; Michael T Laub
Journal:  Cell       Date:  2013-08-01       Impact factor: 41.582

Review 4.  Stress-Activated Chaperones: A First Line of Defense.

Authors:  Wilhelm Voth; Ursula Jakob
Journal:  Trends Biochem Sci       Date:  2017-09-08       Impact factor: 13.807

5.  Protein unfolding as a switch from self-recognition to high-affinity client binding.

Authors:  Bastian Groitl; Scott Horowitz; Karl A T Makepeace; Evgeniy V Petrotchenko; Christoph H Borchers; Dana Reichmann; James C A Bardwell; Ursula Jakob
Journal:  Nat Commun       Date:  2016-01-20       Impact factor: 14.919

6.  Multilevel interaction of the DnaK/DnaJ(HSP70/HSP40) stress-responsive chaperone machine with the central metabolism.

Authors:  Fréderic Anglès; Marie-Pierre Castanié-Cornet; Nawel Slama; Mickael Dinclaux; Anne-Marie Cirinesi; Jean-Charles Portais; Fabien Létisse; Pierre Genevaux
Journal:  Sci Rep       Date:  2017-01-27       Impact factor: 4.379

7.  TAC from Mycobacterium tuberculosis: a paradigm for stress-responsive toxin-antitoxin systems controlled by SecB-like chaperones.

Authors:  Ambre Sala; Virginie Calderon; Patricia Bordes; Pierre Genevaux
Journal:  Cell Stress Chaperones       Date:  2012-12-22       Impact factor: 3.667

Review 8.  Multiple toxin-antitoxin systems in Mycobacterium tuberculosis.

Authors:  Ambre Sala; Patricia Bordes; Pierre Genevaux
Journal:  Toxins (Basel)       Date:  2014-03-06       Impact factor: 4.546

9.  Genome-wide identification of genes essential for the survival of Streptococcus pneumoniae in human saliva.

Authors:  Lilly M Verhagen; Marien I de Jonge; Peter Burghout; Kiki Schraa; Lorenza Spagnuolo; Svenja Mennens; Marc J Eleveld; Christa E van der Gaast-de Jongh; Aldert Zomer; Peter W M Hermans; Hester J Bootsma
Journal:  PLoS One       Date:  2014-02-25       Impact factor: 3.240

10.  An essential nonredundant role for mycobacterial DnaK in native protein folding.

Authors:  Allison Fay; Michael S Glickman
Journal:  PLoS Genet       Date:  2014-07-24       Impact factor: 5.917

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