Structural diversity in twin-arginine signal peptide-binding proteins

Maillard, Julien; Spronk, Chris A. E. M.; Buchanan, Grant; Lyall, Verity; Richardson, David J.; Palmer, Tracy; Vuister, Geerten W.; Sargent, Frank

doi:10.1073/pnas.0703967104

Cited by 70 publications

(93 citation statements)

References 45 publications

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“…The mode of action of PceT resembles that of other chaperones involved in the maturation of Tat-dependent proteins such as TorD (Genest et al, 2009;Sargent, 2007b), DmsD (Guymer et al, 2009;Li et al, 2010) or NapD proteins (Kern et al, 2007;Maillard et al, 2007;Potter & Cole, 1999). Although belonging to very distinct protein families, these chaperones specifically recognize the signal peptide of their cognate Tat-dependent protein and participate in their maturation process.…”

Section: Dedicated Chaperone Function Of Dha-pcetmentioning

confidence: 99%

Redundancy and specificity of multiple trigger factor chaperones in Desulfitobacteria

2011

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The ribosome-bound trigger factor (TF) chaperone assists folding of newly synthesized polypeptides and participates in the assembly of macromolecular complexes. In the present study we showed that multiple distinct TF paralogues are present in genomes of Desulfitobacteria, a bacterial genus known for its ability to grow using organohalide respiration. Two full-length TF chaperones and at least one truncated TF (lacking the N-terminal ribosome-binding domain) were identified, the latter being systematically linked to clusters of reductive dehalogenase genes encoding the key enzymes in organohalide respiration. Using a well-characterized heterologous chaperone-deficient Escherichia coli strain lacking both TF and DnaK chaperones, we demonstrated that all three TF chaperones were functional in vivo, as judged by their ability to partially suppress bacterial growth defects and protein aggregation in the absence of both major E. coli chaperones. Next, we found that the N-terminal truncated TF-like protein PceT functions as a dedicated chaperone for the cognate reductive dehalogenase PceA by solubilizing and stabilizing it in the heterologous system. Finally, we showed that PceT specifically interacts with the twin-arginine signal peptide of PceA. Taken together, our data define PceT (and more generally the new RdhT family) as a class of TF-like chaperones involved in the maturation of proteins secreted by the twin-arginine translocation pathway. INTRODUCTIONFolding of newly synthesized polypeptides in the cytosol is assisted by molecular chaperones (Hartl & Hayer-Hartl, 2009). In bacteria, the ribosome-bound chaperone trigger factor (TF) plays a major role in this process. In Escherichia coli, it is believed that most nascent polypeptides emerging from the ribosome interact with TF before completing their folding (Hoffmann et al., 2010;Kramer et al., 2009). TF chaperone specifically binds to L23 protein at the polypeptide exit tunnel of active ribosomes with a 1 : 1 stoichiometry (Ferbitz et al., 2004;Kramer et al., 2002b;Patzelt et al., 2001). Remarkably, it has been recently shown that TF cycles the ribosome on and off and that ribosome-free TF may stay bound to elongating polypeptides for a prolonged period (Kaiser et al., 2006;Rutkowska et al., 2008).In agreement with such a property, it has recently been proposed that TF participates in the post-translational assembly of large protein complexes in the cytosol (Martinez-Hackert & Hendrickson, 2009). The TF chaperone is composed of three distinct protein domains, which have been functionally and structurally determined. The Nterminal domain (NTD) consists of a ribosome-binding domain containing a conserved motif responsible for binding to ribosomal proteins (Hesterkamp et al., 1997;Kramer et al., 2002aKramer et al., , 2004. The central module in the TF structure corresponds to the C-terminal domain (CTD) and harbours the core of the chaperone activity (Genevaux et al., 2004;Kramer et al., 2004). Finally the domain encoded at the centre of the tig gene exhibits a ...

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Section: Dedicated Chaperone Function Of Dha-pcetmentioning

confidence: 99%

Redundancy and specificity of multiple trigger factor chaperones in Desulfitobacteria

2011

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“…The cytoplasmic protein NapD is involved in NapA relocation by binding to the NapA twin-arginine signal peptide (Maillard et al, 2007). The NapAB form heteromeric complex catalyses by the reduction of nitrate to nitrite.…”

Section: Introductionmentioning

confidence: 99%

Physiological and evolutionary studies of NAP systems in Shewanella piezotolerans WP3

Chen

Wang

et al. 2010

The ISME Journal

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Most of the Shewanella species contain two periplasmic nitrate reductases (NAP-a and NAP-b), which is a unique feature of this genus. In the present study, the physiological function and evolutionary relationship of the two NAP systems were studied in the deep-sea bacterium Shewanella piezotolerans WP3. Both of the WP3 nap gene clusters: nap-a (napD1A1B1C) and nap-b (napD2A2B2) were shown to be involved in nitrate respiration. Phylogenetic analyses suggest that NAP-b originated earlier than NAP-a. Tetraheme cytochromes NapC and CymA were found to be the major electron deliver proteins, and CymA also served as a sole electron transporter towards nitrite reductase. Interestingly, a DnapA2 mutant with the single functional NAP-a system showed better growth than the wild-type strain, when grown in nitrate medium, and it had a selective advantage to the wild-type strain. On the basis of these results, we proposed the evolution direction of nitrate respiration system in Shewanella: from a single NAP-b to NAP-b and NAP-a both, followed by the evolution to a single NAP-a. Moreover, the data presented here will be very useful for the designed engineering of Shewanella for more efficient respiring capabilities for environmental bioremediation.

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“…Rather, they 'escort' their CISM substrates though the entire maturation process as implied by their interactome (30) (Figure 1). Accordingly, many potential roles for REMPs have been proposed, including functioning as: (i) foldases to ensure correct secondary and tertiary structure (25,31); (ii) unfoldases to correct folding mistakes (25); (iii) avoidance chaperones to prevent incorrect membrane targeting during folding and assembly (32); (iv) cofactor-assembly chaperones to maintain apoenzymes in a cofactor-binding competent conformation (30,31); (v) cofactor-binding proteins, which bind the cofactor prior to its transfer to the apoenzyme (30,33); (vi) targeting proteins directing substrates to specific cellular locations (34,35); (vii) escort chaperones to promote transmembrane transport of enzyme complexes (30,31,34); (viii) proofreading chaperones to suppress transport until essential prior steps in the assembly process are complete (33,36,37); and (ix) protease protection chaperones to prevent degradation during assembly (38). Yet despite these proposed roles, a detailed path of actions for REMPs has yet to be defined.…”

Section: So Dmso] (4)mentioning

confidence: 99%

Assembly pathway of a bacterial complex iron sulfur molybdoenzyme

Cherak

Turner

2017

Biomolecular Concepts

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Protein folding and assembly into macromolecule complexes within the living cell are complex processes requiring intimate coordination. The biogenesis of complex iron sulfur molybdoenzymes (CISM) requires use of a system specific chaperone -a redox enzyme maturation protein (REMP) -to help mediate final folding and assembly. The CISM dimethyl sulfoxide (DMSO) reductase is a bacterial oxidoreductase that utilizes DMSO as a final electron acceptor for anaerobic respiration. The REMP DmsD strongly interacts with DMSO reductase to facilitate folding, cofactor-insertion, subunit assembly and targeting of the multi-subunit enzyme prior to membrane translocation and final assembly and maturation into a bioenergetic catalytic unit. In this article, we discuss the biogenesis of DMSO reductase as an example of the participant network for bacterial CISM maturation pathways.

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Structural diversity in twin-arginine signal peptide-binding proteins

Cited by 70 publications

References 45 publications

Redundancy and specificity of multiple trigger factor chaperones in Desulfitobacteria

Redundancy and specificity of multiple trigger factor chaperones in Desulfitobacteria

Physiological and evolutionary studies of NAP systems in Shewanella piezotolerans WP3

Assembly pathway of a bacterial complex iron sulfur molybdoenzyme

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