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Research Paper

RopB-regulated SpeB cysteine protease degrades extracellular vesicles-associated streptolysin O and bacterial proteins from group A Streptococcus

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Article: 2249784 | Received 09 May 2023, Accepted 13 Aug 2023, Published online: 24 Aug 2023

References

  • Deatherage BL, Cookson BT, Andrews-Polymenis HL. Membrane vesicle release in bacteria, eukaryotes, and archaea: a conserved yet underappreciated aspect of microbial life. Infect Immun. 2012;80(6):1948–13. doi: 10.1128/IAI.06014-11
  • Beveridge TJ. Structures of gram-negative cell walls and their derived membrane vesicles. J Bacteriol. 1999;181(16):4725–4733. doi: 10.1128/JB.181.16.4725-4733.1999
  • Kulkarni HM, Jagannadham MV. Biogenesis and multifaceted roles of outer membrane vesicles from Gram-negative bacteria. Microbiology (Reading). 2014;160(10):2109–2121. doi: 10.1099/mic.0.079400-0
  • Biagini M, Garibaldi M, Aprea S, et al. The human pathogen Streptococcus pyogenes releases lipoproteins as lipoprotein-rich membrane vesicles. Mol & Cell Proteomics. 2015;14(8):2138–2149. doi: 10.1074/mcp.M114.045880
  • Prados-Rosales R, Baena A, Martinez LR, et al. Mycobacteria release active membrane vesicles that modulate immune responses in a TLR2-dependent manner in mice. J Clin Invest. 2011;121(4):1471–1483. doi: 10.1172/JCI44261
  • Lee EY, Choi DY, Kim DK, et al. Gram-positive bacteria produce membrane vesicles: proteomics-based characterization of Staphylococcus aureus-derived membrane vesicles. Proteomics. 2009;9(24):5425–5436. doi: 10.1002/pmic.200900338
  • Cunningham MW. Pathogenesis of group A streptococcal infections and their sequelae. Adv Exp Med Biol. 2008;609:29–42.
  • Resch U, Tsatsaronis JA, Le Rhun A, et al. A two-component regulatory system impacts extracellular membrane-derived vesicle production in group A Streptococcus. mBio. 2016;7:e00207–16. doi: 10.1128/mBio.00207-16
  • Ikebe T, Ato M, Matsumura T, et al. Highly frequent mutations in negative regulators of multiple virulence genes in group A streptococcal toxic shock syndrome isolates. PLoS Pathog. 2010;6(4):e1000832. doi: 10.1371/journal.ppat.1000832
  • Sumby P, Whitney AR, Graviss EA, et al. Genome-wide analysis of group A streptococci reveals a mutation that modulates global phenotype and disease specificity. PLoS Pathog. 2006;2(1):e5. doi: 10.1371/journal.ppat.0020005
  • Churchward G. The two faces of Janus: virulence gene regulation by CovR/S in group A streptococci. Mol Microbiol. 2007;64(1):34–41. doi: 10.1111/j.1365-2958.2007.05649.x
  • Shi YA, Chen TC, Chen YW, et al. The bacterial markers of identification of invasive CovR/CovS-inactivated group A Streptococcus. Microbiol Spectr. 2022;10:e0203322. doi: 10.1128/spectrum.02033-22
  • Chiang-Ni C, Chen YW, Chen KL, et al. RopB represses the transcription of speB in the absence of SIP in group A Streptococcus. Life Sci Alliance. 2023;6(6):e202201809. doi: 10.26508/lsa.202201809
  • Do H, Makthal N, VanderWal AR, et al. Environmental pH and peptide signaling control virulence of Streptococcus pyogenes via a quorum-sensing pathway. Nat Commun. 2019;10(1):2586. doi: 10.1038/s41467-019-10556-8
  • Do H, Makthal N, VanderWal AR, et al. Leaderless secreted peptide signaling molecule alters global gene expression and increases virulence of a human bacterial pathogen. Proc Natl Acad Sci U S A. 2017;114(40):E8498–E507. doi: 10.1073/pnas.1705972114
  • Wu ZY, Campeau A, Liu CH, et al. Unique virulence role of post-translocational chaperone PrsA in shaping Streptococcus pyogenes secretome. Virulence. 2021;12(1):2633–2647. doi: 10.1080/21505594.2021.1982501
  • LaRock DL, Johnson AF, Wilde S, et al. Group A Streptococcus induces GSDMA-dependent pyroptosis in keratinocytes. Nature. 2022;605(7910):527–531. doi: 10.1038/s41586-022-04717-x
  • Deng W, Bai Y, Deng F, et al. Streptococcal pyrogenic exotoxin B cleaves GSDMA and triggers pyroptosis. Nature. 2022;602(7897):496–502. doi: 10.1038/s41586-021-04384-4
  • Brown L, Wolf JM, Prados-Rosales R, et al. Through the wall: extracellular vesicles in Gram-positive bacteria, mycobacteria and fungi. Nat Rev Microbiol. 2015;13(10):620–630. doi: 10.1038/nrmicro3480
  • Chaussee MS, Watson RO, Smoot JC, et al. Identification of Rgg-regulated exoproteins of Streptococcus pyogenes. Infect Immun. 2001;69(2):822–831. doi: 10.1128/IAI.69.2.822-831.2001
  • Tjia-Fleck S, Readnour BM, Ayinuola YA, et al. High-resolution single-particle cryo-EM hydrated structure of Streptococcus pyogenes enolase offers insights into its function as a plasminogen receptor. Biochemistry. 2023;62(3):735–746. doi: 10.1021/acs.biochem.2c00637
  • Derbise A, Song YP, Parikh S, et al. Role of the C-terminal lysine residues of streptococcal surface enolase in Glu- and Lys-plasminogen-binding activities of group A streptococci. Infect Immun. 2004;72(1):94–105. doi: 10.1128/IAI.72.1.94-105.2004
  • Antikainen J, Kuparinen V, Lahteenmaki K, et al. Enolases from Gram-positive bacterial pathogens and commensal lactobacilli share functional similarity in virulence-associated traits. FEMS Immunol Med Microbiol. 2007;51(3):526–534. doi: 10.1111/j.1574-695X.2007.00330.x
  • von Pawel-Rammingen U, Bjorck L. IdeS and SpeB: immunoglobulin-degrading cysteine proteinases of Streptococcus pyogenes. Curr Opin Microbiol. 2003;6(1):50–55. doi: 10.1016/S1369-5274(03)00003-1
  • Bisno AL, Brito MO, Collins CM. Molecular basis of group A streptococcal virulence. Lancet Infect Dis. 2003;3(4):191–200. doi: 10.1016/S1473-3099(03)00576-0
  • Graham MR, Smoot LM, Migliaccio CA, et al. Virulence control in group A Streptococcus by a two-component gene regulatory system: global expression profiling and in vivo infection modeling. Proc Natl Acad Sci U S A. 2002;99:13855–13860. doi: 10.1073/pnas.202353699
  • Chiang-Ni C, Kao CY, Hsu CY, et al. Phosphorylation at the D53 but not the T65 residue of CovR determines the repression of rgg and speB transcription in emm1- and emm49-type group A streptococci. J Bacteriol. 2019;201(4):e00681–18. doi: 10.1128/JB.00681-18
  • Murase K, Aikawa C, Nozawa T, et al. Biological effect of Streptococcus pyogenes-released extracellular vesicles on human monocytic cells, induction of cytotoxicity, and inflammatory response. Front Cell Infect Microbiol. 2021;11:711144. doi: 10.3389/fcimb.2021.711144
  • 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;51:123–134. doi: 10.1046/j.1365-2958.2003.03797.x
  • Doran JD, Nomizu M, Takebe S, et al. Autocatalytic processing of the streptococcal cysteine protease zymogen: processing mechanism and characterization of the autoproteolytic cleavage sites. Eur J Biochem. 1999;263:145–151. doi: 10.1046/j.1432-1327.1999.00473.x
  • Chen CY, Luo SC, Kuo CF, et al. Maturation processing and characterization of streptopain. J Biol Chem. 2003;278(19):17336–17343. doi: 10.1074/jbc.M209038200
  • Wang X, Eagen WJ, Lee JC. Orchestration of human macrophage NLRP3 inflammasome activation by Staphylococcus aureus extracellular vesicles. Proc Natl Acad Sci U S A. 2020;117(6):3174–3184. doi: 10.1073/pnas.1915829117
  • Rasmussen M, Bjorck L. Proteolysis and its regulation at the surface of Streptococcus pyogenes. Mol Microbiol. 2002;43(3):537–544. doi: 10.1046/j.1365-2958.2002.02766.x
  • Pancholi V, Fischetti VA. α-enolase, a novel strong plasmin(ogen) binding protein on the surface of pathogenic streptococci. J Biol Chem. 1998;273(23):14503–14515. doi: 10.1074/jbc.273.23.14503
  • Fontan PA, Pancholi V, Nociari MM, et al. Antibodies to streptococcal surface enolase react with human alpha-enolase: implications in poststreptococcal sequelae. J Infect Dis. 2000;182:1712–1721. doi: 10.1086/317604
  • Marsollier L, Brodin P, Jackson M, et al. Impact of Mycobacterium ulcerans biofilm on transmissibility to ecological niches and buruli ulcer pathogenesis. PLoS Pathog. 2007;3(5):e62. doi: 10.1371/journal.ppat.0030062
  • Thay B, Wai SN, Oscarsson J, et al. Staphylococcus aureus α-toxin-dependent Induction of host cell death by membrane-derived vesicles. PLoS One. 2013;8:e54661. doi: 10.1371/journal.pone.0054661
  • Sun H, Ringdahl U, Homeister JW, et al. Plasminogen is a critical host pathogenicity factor for group A streptococcal infection. Science. 2004;305(5688):1283–1286. doi: 10.1126/science.1101245
  • Briaud P, Carroll RK, Richardson AR. Extracellular vesicle biogenesis and functions in gram-positive bacteria. Infect Immun. 2020;88(12):88. doi: 10.1128/IAI.00433-20
  • Coelho C, Brown L, Maryam M, et al. Listeria monocytogenes virulence factors, including listeriolysin O, are secreted in biologically active extracellular vesicles. J Biol Chem. 2019;294(4):1202–1217. doi: 10.1074/jbc.RA118.006472
  • Chiang-Ni C, Zheng PX, Ho YR, et al. emm1/sequence type 28 strains of group A streptococci that express covR at early stationary phase are associated with increased growth and earlier SpeB secretion. J Clin Microbiol. 2009;47(10):3161–3169. doi: 10.1128/JCM.00202-09
  • Chiang-Ni C, Chu TP, Wu JJ, et al. Repression of Rgg but not upregulation of LacD.1 in emm1-type covS mutant mediates the SpeB repression in group A Streptococcus. Front Microbiol. 2016;7:1935. doi: 10.3389/fmicb.2016.01935
  • Chiang-Ni C, Shi YA, Lai CH, et al. Cytotoxicity and survival fitness of Invasive covS mutant of group A Streptococcus in phagocytic cells. Front Microbiol. 2018;9:2592. doi: 10.3389/fmicb.2018.02592
  • Tsai WJ, Lai YH, Shi YA, et al. Structural basis underlying the synergism of NADase and SLO during group A Streptococcus infection. Commun Biol. 2023;6(1):124. doi: 10.1038/s42003-023-04502-0
  • Wang CH, Chiang-Ni C, Kuo HT, et al. Peroxide responsive regulator PerR of group A Streptococcus is required for the expression of phage-associated DNase Sda1 under oxidative stress. PLoS One. 2013;8(12):e81882. doi: 10.1371/journal.pone.0081882
  • Chiang-Ni C, Tseng HC, Hung CH, et al. Acidic stress enhances CovR/S-dependent gene repression through activation of the covR/S promoter in emm1-type group A Streptococcus. Int J Med Microbiol. 2017;307(6):329–339. doi: 10.1016/j.ijmm.2017.06.002
  • Valcu M, Valcu CM. Data transformation practices in biomedical sciences. Nat Methods. 2011;8(2):104–105. doi: 10.1038/nmeth0211-104
  • Tsou CC, Chiang-Ni C, Lin YS, et al. Oxidative stress and metal ions regulate a ferritin-like gene, dpr, in Streptococcus pyogenes. Int J Med Microbiol. 2010;300(4):259–264. doi: 10.1016/j.ijmm.2009.09.002