Solution structure of the parvulin-type PPIase domain of Staphylococcus aureus PrsA – Implications for the catalytic mechanism of parvulins

Heikkinen, Outi; Seppälä, Raili; Tossavainen, Helena; Heikkinen, Sami; Koskela, Harri; Permi, Perttu; Kilpeläinen, Ilkka

doi:10.1186/1472-6807-9-17

Cited by 41 publications

(48 citation statements)

References 38 publications

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“…Saturation could not be reached in these titration experiments, indicating that the dissociation constant of the complex between the peptide and PpiD* is in the range of 1 mM. Similar values were observed previously for other parvulins 25,30 and for cyclophilin18.…”

Section: Ppid* Does Not Catalyze Prolyl Isomerization In Peptides or supporting

confidence: 67%

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The prolyl isomerase domain of PpiD fromEscherichia colishows a parvulin fold but is devoid of catalytic activity

et al. 2009

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PpiD is a periplasmic folding helper protein of Escherichia coli. It consists of an N-terminal helix that anchors PpiD in the inner membrane near the SecYEG translocon, followed by three periplasmic domains. The second domain (residues 264-357) shows homology to parvulinlike prolyl isomerases. This domain is a well folded, stable protein and follows a simple two-state folding mechanism. In its solution structure, as determined by NMR spectroscopy, it resembles most closely the first parvulin domain of the SurA protein, which resides in the periplasm of E. coli as well. A previously reported prolyl isomerase activity of PpiD could not be reproduced when using improved protease-free peptide assays or assays with refolding proteins as substrates. The parvulin domain of PpiD interacts, however, with a proline-containing tetrapeptide, and the binding site, as identified by NMR resonance shift analysis, colocalized with the catalytic sites of other parvulins. In its structure, the parvulin domain of PpiD resembles most closely the inactive first parvulin domain of SurA, which is part of the chaperone unit of this protein and presumably involved in substrate recognition.Keywords: parvulin; Pin1; prolyl isomerase; SurA; protein maturation; periplasm; SecYEG Abbreviations: PpiD, periplasmic folding helper protein from Escherichia coli; PpiD*, parvulin-like domain of PpiD (residues 264-357); PPIase, peptidyl-prolyl cis/trans isomerase; CD, circular dichroism; T M , midpoint of a thermal unfolding transition; DH D , vań t Hoff enthalpy of denaturation at T M ; DG D , Gibbs free energy of denaturation; m, cooperativity value of a denaturant-induced equilibrium unfolding transition; Ds, time constant of a folding reaction; k u , microscopic rate constant and m u (¼ qlnk u /q[urea]), kinetic m-value of unfolding; k f , m f , microscopic rate constant and kinetic m-value of refolding; NOESY, nuclear Overhauser enhancement and exchange spectroscopy; HSQC, hetero single quantum coherence; hNOE, 15 N hetero nuclear NOE; HX, hydrogen exchange; NH, amide proton; RCM-T1, reduced and carboxymethylated form of the S54G/P55N double mutant of ribonuclease T 1 ; N2, N2 domain of the gene 3 protein of phage fd.Additional Supporting Information may be found in the online version of this article.

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Section: Ppid* Does Not Catalyze Prolyl Isomerization In Peptides or supporting

confidence: 67%

“…20 At present, structures of eight parvulins are available in the Protein Data Bank. 9,[23][24][25][26][27][28][29][30] The different subtypes differ in the length and the composition of the loop between the strand b1 and the helix a1. Human Pin1 is the most prominent member of the parvulin family.…”

Section: Introductionmentioning

confidence: 99%

The prolyl isomerase domain of PpiD fromEscherichia colishows a parvulin fold but is devoid of catalytic activity

et al. 2009

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“…Structural characterization by solution NMR of the PrsA PPD domains of S. aureus and B. subtillis revealed a typical parvullin fold for these domains [335,336]. The fold showed highly similar structures reported for trigger factor and SurA PPD domains from Gram-negative bacteria [130,272].…”

Section: Other Chaperonesmentioning

confidence: 87%

Chaperones and chaperone–substrate complexes: Dynamic playgrounds for NMR spectroscopists

Burmann¹,

Hiller²

2015

Progress in Nuclear Magnetic Resonance Spectroscopy

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“…PrsA is a lipid-anchored protein located on the outer face of the plasma membrane, found ubiquitously in Grampositive species (68,75), and contains a peptidyl-prolyl cis-trans isomerase (PPIase) domain. PPIases catalyze cis-trans isomerization of peptide bonds, and S. aureus PrsA has been shown to function as a prolyl isomerase (34,80). PrsA is thought to assist folding of proteins destined for secretion, and a PrsA homolog in Bacillus subtilis has been shown to be directly involved in folding penicillin-binding proteins (41).…”

Section: Discussionmentioning

confidence: 99%

A Mutation in the PP2C Phosphatase Gene in a Staphylococcus aureus USA300 Clinical Isolate with Reduced Susceptibility to Vancomycin and Daptomycin

Passalacqua

Satola

Crispell

et al. 2012

Antimicrob Agents Chemother

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c Methicillin-resistant Staphylococcus aureus (MRSA) strains with reduced susceptibility to vancomycin (MIC of 4 to 8 g/ml) are referred to as vancomycin-intermediate S. aureus (VISA). In this study, we characterized two isogenic USA300 S. aureus isolates collected sequentially from a single patient with endocarditis where the S. aureus isolate changed from being susceptible to vancomycin (VSSA) (1 g/ml) to VISA (8 g/ml). In addition, the VISA isolate lost beta-lactamase activity and showed increased resistance to daptomycin and linezolid. The two strains did not differ in growth rate, but the VISA isolate had a thickened cell wall and was less autolytic. Transcriptome sequencing (RNA-seq) analysis comparing the two isolates grown to late exponential phase showed significant differences in transcription of cell surface protein genes (spa, SBI [second immunoglobulin-binding protein of S. aureus], and fibrinogen-binding proteins), regulatory genes (agrBCA, RNAIII, sarT, and saeRS), and others. Using whole-genome shotgun resequencing, we identified 6 insertion/deletion mutations between the VSSA and VISA isolates. A protein phosphatase 2C (PP2C) family phosphatase had a 6-bp (nonframeshift) insertion mutation in a highly conserved metal binding domain. Complementation of the clinical VISA isolate with a wild-type copy of the PP2C gene reduced the vancomycin and daptomycin MICs and increased autolytic activity, suggesting that this gene contributed to the reduced vancomycin susceptibility phenotype acquired in vivo. Creation of de novo mutants from the VSSA strain resulted in different mutations, demonstrating that reduced susceptibility to vancomycin in USA300 strains can occur via multiple routes, highlighting the complex nature of the VISA phenotype.

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Solution structure of the parvulin-type PPIase domain of Staphylococcus aureus PrsA – Implications for the catalytic mechanism of parvulins

Cited by 41 publications

References 38 publications

The prolyl isomerase domain of PpiD fromEscherichia colishows a parvulin fold but is devoid of catalytic activity

The prolyl isomerase domain of PpiD fromEscherichia colishows a parvulin fold but is devoid of catalytic activity

Chaperones and chaperone–substrate complexes: Dynamic playgrounds for NMR spectroscopists

A Mutation in the PP2C Phosphatase Gene in a Staphylococcus aureus USA300 Clinical Isolate with Reduced Susceptibility to Vancomycin and Daptomycin

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