Unique virulence role of post-translocational chaperone PrsA in shaping Streptococcus pyogenes secretome

References

• Carapetis JR, Steer AC, Mulholland EK, et al. The global burden of group A streptococcal diseases. Lancet Infect Dis. 2005;5(11):685–694.
   PubMed Web of Science ®Google Scholar
• Walker MJ, Barnett TC, McArthur JD, et al. Disease manifestations and pathogenic mechanisms of group A Streptococcus. Clin Microbiol Rev. 2014;27(2):264–301.
   PubMed Web of Science ®Google Scholar
• Freudl R. Leaving home ain’t easy: protein export systems in Gram-positive bacteria. Res Microbiol. 2013;164(6):664–674.
   PubMed Web of Science ®Google Scholar
• Sarvas M, Harwood CR, Bron S, et al. Post-translocational folding of secretory proteins in Gram-positive bacteria. Biochim Biophys Acta. 2004;1694(1-3):311–327.
   PubMed Web of Science ®Google Scholar
• Rosch J, Caparon M. A microdomain for protein secretion in Gram-positive bacteria. Science. 2004;304(5676):1513–1515.
   PubMed Web of Science ®Google Scholar
• Galeotti CL, Bove E, Pezzicoli A, et al. Surface interactome in Streptococcus pyogenes. Mol Cell Proteomics. 2012;11(4):M111 015206.
   PubMed Web of Science ®Google Scholar
• Unal CM, Steinert M. Microbial peptidyl-prolylcis/trans isomerases (PPIases): virulence factors and potential alternative drug targets. Microbiol Mol Biol Rev. 2014;78(3):544–571.
   PubMed Web of Science ®Google Scholar
• Guo L, Wu T, Hu W, et al. Phenotypic characterization of the foldase homologue PrsA in Streptococcus mutans. Mol Oral Microbiol. 2013;28(2):154–165.
   PubMed Web of Science ®Google Scholar
• Hyyrylainen HL, Marciniak BC, Dahncke K, et al. Penicillin-binding protein folding is dependent on the PrsA peptidyl-prolyl cis-trans isomerase in Bacillus subtilis. Mol Microbiol. 2010;77(1):108–127.
   PubMed Web of Science ®Google Scholar
• Jousselin A, Manzano C, Biette A, et al. The Staphylococcus aureus chaperone PrsA is a new auxiliary factor of oxacillin resistance affecting penicillin-binding protein 2A. Antimicrob Agents Chemother. 2015;60(3):1656–1666.
   PubMed Web of Science ®Google Scholar
• Jousselin A, Renzoni A, Andrey DO, et al. The posttranslocational chaperone lipoprotein PrsA is involved in both glycopeptide and oxacillin resistance in Staphylococcus aureus. Antimicrob Agents Chemother. 2012;56(7):3629–3640.
   PubMed Web of Science ®Google Scholar
• Lee CR, Lee JH, Park KS, et al. Quantitative proteomic view associated with resistance to clinically important antibiotics in Gram-positive bacteria: a systematic review. Front Microbiol. 2015;6:828.
   PubMed Web of Science ®Google Scholar
• Pardos de la Gandara M, Borges V, Chung M, et al. Genetic determinants of high-level oxacillin resistance in methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother. 2018;62(6):e00206–18.
   Web of Science ®Google Scholar
• Renzoni A, Kelley WL, Rosato RR, et al. Molecular bases determining daptomycin resistance-mediated resensitization to beta-Lactams (Seesaw effect) in methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother. 2017;61(1):e01634-16.
   Web of Science ®Google Scholar
• Cahoon LA, Freitag NE. Listeria monocytogenes virulence factor secretion: don’t leave the cell without a chaperone. Front Cell Infect Microbiol. 2014;4:13.
   PubMed Web of Science ®Google Scholar
• Cahoon LA, Freitag NE. Identification of conserved and species-specific functions of the Listeria monocytogenes PrsA2 secretion chaperone. Infect Immun. 2015;83(10):4028–4041.
   PubMed Web of Science ®Google Scholar
• Alonzo F 3rd, Freitag NE. Listeria monocytogenes PrsA2 is required for virulence factor secretion and bacterial viability within the host cell cytosol. Infect Immun. 2010;78(11):4944–4957.
   PubMed Web of Science ®Google Scholar
• Alonzo F 3rd, Xayarath B, Whisstock JC, et al. Functional analysis of the listeria monocytogenes secretion chaperone PrsA2 and its multiple contributions to bacterial virulence. Mol Microbiol. 2011;80(6):1530–1548.
   PubMed Web of Science ®Google Scholar
• Cahoon LA, Freitag NE, Prehna G. A structural comparison of Listeria monocytogenes protein chaperones PrsA1 and PrsA2 reveals molecular features required for virulence. Mol Microbiol. 2016;101(1):42–61.
   PubMed Web of Science ®Google Scholar
• Ma Y, Bryant AE, Salmi DB, et al. Identification and characterization of bicistronic speB and prsA gene expression in the group A Streptococcus. J Bacteriol. 2006;188(21):7626–7634.
   PubMed Web of Science ®Google Scholar
• Flores AR, Jewell BE, Fittipaldi N, et al. Human disease isolates of serotype m4 and m22 group a streptococcus lack genes required for hyaluronic acid capsule biosynthesis. mBio. 2012;3(6):e00413–12.
   PubMed Web of Science ®Google Scholar
• Henningham A, Yamaguchi M, Aziz RK, et al. Mutual exclusivity of hyaluronan and hyaluronidase in invasive group A Streptococcus. J Biol Chem. 2014;289(46):32303–32315.
   PubMed Web of Science ®Google Scholar
• Kim S, Lee S, Park H, et al. Predominance of emm4 and antibiotic resistance of Streptococcus pyogenes in acute pharyngitis in a southern region of Korea. J Med Microbiol. 2019;68(7):1053–1058.
   PubMed Web of Science ®Google Scholar
• Whitehead BD, Smith HV, Nourse C. Invasive group A streptococcal disease in children in Queensland. Epidemiol Infect. 2011;139(4):623–628.
   PubMed Web of Science ®Google Scholar
• Alonzo F 3rd, Port GC, Cao M, et al. The posttranslocation chaperone PrsA2 contributes to multiple facets of Listeria monocytogenes pathogenesis. Infect Immun. 2009;77(7):2612–2623.
   PubMed Web of Science ®Google Scholar
• Bessen DE, McGregor KF, Whatmore AM. Relationships between emm and multilocus sequence types within a global collection of Streptococcus pyogenes. BMC Microbiol. 2008;8(1):59.
   PubMedGoogle Scholar
• Cron LE, Bootsma HJ, Noske N, et al. Surface-associated lipoprotein PpmA of Streptococcus pneumoniae is involved in colonization in a strain-specific manner. Microbiology. 2009;155(7):2401–2410.
   PubMedGoogle Scholar
• Lin MH, Li CC, Shu JC, et al. Exoproteome profiling reveals the involvement of the foldase PrsA in the cell surface properties and pathogenesis of Staphylococcus aureus. Proteomics. 2018;18(5–6):e1700195.
   PubMed Web of Science ®Google Scholar
• Wiemels RE, Cech SM, Meyer NM, et al. An intracellular peptidyl-prolyl cis/trans isomerase is required for folding and activity of the Staphylococcus aureus secreted virulence factor nuclease. J Bacteriol. 2017;199(1):e00453–16.
   Web of Science ®Google Scholar
• Williams RC, Rees ML, Jacobs MF, et al. Production of Bacillus anthracis protective antigen is dependent on the extracellular chaperone, PrsA. J Biol Chem. 2003;278(20):18056–18062.
   PubMed Web of Science ®Google Scholar
• Hamilton A, Robinson C, Sutcliffe IC, et al. Mutation of the maturase lipoprotein attenuates the virulence of Streptococcus equi to a greater extent than does loss of general lipoprotein lipidation. Infect Immun. 2006;74(12):6907–6919.
   PubMed Web of Science ®Google Scholar
• Crowley PJ, Brady LJ. Evaluation of the effects of Streptococcus mutans chaperones and protein secretion machinery components on cell surface protein biogenesis, competence, and mutacin production. Mol Oral Microbiol. 2016;31(1):59–77.
   PubMed Web of Science ®Google Scholar
• Liu H, Fu H, Jiang X, et al. PrsA contributes to Streptococcus suis serotype 2 pathogenicity by modulating secretion of selected virulence factors. Vet Microbiol. 2019;236:108375.
   PubMed Web of Science ®Google Scholar
• Drouault S, Anba J, Bonneau S, et al. The peptidyl-prolyl isomerase motif is lacking in PmpA, the PrsA-like protein involved in the secretion machinery of Lactococcus lactis. Appl Environ Microbiol. 2002;68(8):3932–3942.
   PubMed Web of Science ®Google Scholar
• Vitikainen M, Lappalainen I, Seppala R, et al. Structure-function analysis of PrsA reveals roles for the parvulin-like and flanking N- and C-terminal domains in protein folding and secretion in Bacillus subtilis. J Biol Chem. 2004;279(18):19302–19314.
   PubMed Web of Science ®Google Scholar
• Jakob RP, Koch JR, Burmann BM, et al. Dimeric structure of the bacterial extracellular foldase PrsA. J Biol Chem. 2015;290(6):3278–3292.
   PubMed Web of Science ®Google Scholar
• Aziz RK, Pabst MJ, Jeng A, et al. Invasive M1T1 group A Streptococcus undergoes a phase-shift in vivo to prevent proteolytic degradation of multiple virulence factors by SpeB. Mol Microbiol. 2004;51(1):123–134.
   PubMed Web of Science ®Google Scholar
• Zheng PX, Chung KT, Chiang-Ni C, et al. Complete genome sequence of emm1 Streptococcus pyogenes A20, a strain with an intact two-component system, CovRS, isolated from a patient with necrotizing fasciitis. Genome Announc. 2013;1(1):e00149–12.
   Google Scholar
• Boukamp P, Petrussevska RT, Breitkreutz D, et al. Normal keratinization in a spontaneously immortalized aneuploid human keratinocyte cell line. J Cell Biol. 1988;106(3):761-771.
   PubMed Web of Science ®Google Scholar
• Jeng A, Sakota V, Li Z, et al. Molecular genetic analysis of a group A Streptococcus operon encoding serum opacity factor and a novel fibronectin-binding protein, SfbX. J Bacteriol. 2003;185(4):1208–1217.
   PubMed Web of Science ®Google Scholar
• Yamaguchi M, Terao Y, Mori Y, et al. PfbA, a novel plasmin- and fibronectin-binding protein of Streptococcus pneumoniae, contributes to fibronectin-dependent adhesion and antiphagocytosis. J Biol Chem. 2008;283(52):36272-36279.
   Web of Science ®Google Scholar
• Yamaguchi M, Terao Y, Mori-Yamaguchi Y, et al. Streptococcus pneumoniae invades erythrocytes and utilizes them to evade human innate immunity. PLoS One. 2013;8(10):e77282.
   PubMed Web of Science ®Google Scholar
• Wang Y, Yang F, Gritsenko MA, et al. Reversed-phase chromatography with multiple fraction concatenation strategy for proteome profiling of human MCF10A cells. Proteomics. 2011;11(10):2019–2026.
   PubMed Web of Science ®Google Scholar
• Wierzbicki IH, Campeau A, Dehaini D, et al. Group A Streptococcal S protein utilizes red blood cells as immune camouflage and is a critical determinant for immune evasion. Cell Rep. 2019;29(10):2979–2989 e15.
   PubMed Web of Science ®Google Scholar
• Eng JK, McCormack AL, Yates JR. An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database. J Am Soc Mass Spectrom. 1994;5(11):976–989.
   PubMed Web of Science ®Google Scholar
• Elias JE, Gygi SP. Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry. Nat Methods. 2007;4(3):207–214.
   PubMed Web of Science ®Google Scholar
• Xiao Y, Hsiao TH, Suresh U, et al. A novel significance score for gene selection and ranking. Bioinformatics. 2014;30(6):801–807.
   PubMed Web of Science ®Google Scholar
• Hulsen T, de Vlieg J, Alkema W. BioVenn – a web application for the comparison and visualization of biological lists using area-proportional Venn diagrams. BMC Genomics. 2008;9(1):488.
   PubMed Web of Science ®Google Scholar
• Svensson MD, Scaramuzzino DA, Sjobring U, et al. Role for a secreted cysteine proteinase in the establishment of host tissue tropism by group A streptococci. Mol Microbiol. 2000;38(2):242-253.
   PubMed Web of Science ®Google Scholar