Complement evasion factor (CEF), a novel immune evasion factor of Streptococcus pyogenes

References

• Botteaux A, Budnik I, Smeesters PR. Group A Streptococcus infections in children: from virulence to clinical management. Curr Opin Infect Dis. 2018;31(3):224–230.
   PubMed Web of Science ®Google Scholar
• Cunningham MW. Pathogenesis of group A streptococcal infections. Clin Microbiol Rev. 2000;13(3):470–511.
   PubMed Web of Science ®Google Scholar
• Stevens DL, Bryant AE. Severe group a streptococcal infections. In: Ferretti JJ, Stevens DL, Fischetti VA, editors. Streptococcus pyogenes: basic biology to clinical manifestations. Oklahoma City: University of Oklahoma Health Sciences Center(c) The University of Oklahoma Health Sciences Center; 2016.
   Google Scholar
• Cunningham MW. Streptococcus and rheumatic fever. Curr Opin Rheumatol. 2012;24(4):408–416.
   PubMed Web of Science ®Google Scholar
• Martin WJ, Steer AC, Smeesters PR, et al. Post-infectious group A streptococcal autoimmune syndromes and the heart. Autoimmun Rev. 2015;14(8):710–725.
   PubMed Web of Science ®Google Scholar
• Mosquera J, Pedreanez A. Acute post-streptococcal glomerulonephritis: analysis of the pathogenesis. Int Rev Immunol. 2021; 40(6):381–400.
   Web of Science ®Google Scholar
• 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
• Brouwer S, Barnett TC, Rivera-Hernandez T, et al. Streptococcus pyogenes adhesion and colonization. FEBS Lett. 2016;590(21):3739–3757.
   PubMed Web of Science ®Google Scholar
• Cole JN, Barnett TC, Nizet V, et al. Molecular insight into invasive group A streptococcal disease. Nature Rev Microbiol. 2011;9(10):724–736.
   PubMed Web of Science ®Google Scholar
• Laabei M, Ermert D. Catch me if you can: streptococcus pyogenes complement evasion strategies. J Innate Immun. 2019;11(1):3–12.
   PubMed Web of Science ®Google Scholar
• Olsen RJ, Shelburne SA, Musser JM. Molecular mechanisms underlying group A streptococcal pathogenesis. Cell Microbiol. 2009;11(1):1–12.
   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
• Proft T, Fraser J. Superantigens: just like peptides only different. J Exp Med. 1998;187(6):819–821.
   PubMed Web of Science ®Google Scholar
• Proft T, Fraser JD. Streptococcal superantigens. Chem Immunol Allergy. 2007;93:1–23.
   PubMedGoogle Scholar
• Chang A, Khemlani A, Kang H, et al. Functional analysis of Streptococcus pyogenes nuclease A (SpnA), a novel group A streptococcal virulence factor. Mol Microbiol. 2011;79(6):1629–1642.
   PubMed Web of Science ®Google Scholar
• Korczynska JE, Turkenburg JP, Taylor EJ. The structural characterization of a prophage-encoded extracellular DNase from Streptococcus pyogenes. Nucleic Acids Res. 2012;40(2):928–938.
   PubMed Web of Science ®Google Scholar
• Tanaka M, Kinoshita-Daitoku R, Kiga K, et al. Group A Streptococcus establishes pharynx infection by degrading the deoxyribonucleic acid of neutrophil extracellular traps. Sci Rep. 2020;10(1):3251.
   PubMed Web of Science ®Google Scholar
• Alouf JE. Streptococcal toxins (streptolysin O, streptolysin S, erythrogenic toxin). Pharmacol Ther. 1980;11(3):661–717.
   PubMed Web of Science ®Google Scholar
• LaRock DL, Russell R, Johnson AF, et al. Group A streptococcus infection of the nasopharynx requires proinflammatory signaling through the interleukin-1 receptor. Infect Immun. 2020;88.
   Web of Science ®Google Scholar
• Kurupati P, Turner CE, Tziona I, et al. Chemokine-cleaving Streptococcus pyogenes protease SpyCEP is necessary and sufficient for bacterial dissemination within soft tissues and the respiratory tract. Mol Microbiol. 2010;76(6):1387–1397.
   PubMed Web of Science ®Google Scholar
• Turner CE, Kurupati P, Jones MD, et al. Emerging Role of the Interleukin-8 cleaving enzyme SpyCEP in clinical streptococcus pyogenes infection. J Infect Dis. 2009;200(4):555–563.
   PubMed Web of Science ®Google Scholar
• Reis ES, Mastellos DC, Hajishengallis G, et al. New insights into the immune functions of complement. Nat Rev Immunol. 2019;19(8):503–516.
   PubMed Web of Science ®Google Scholar
• Pandey S, Maharana J, Li XX, et al. Emerging insights into the structure and function of complement C5a receptors. Trends Biochem Sci. 2020;45(8):693–705.
   PubMed Web of Science ®Google Scholar
• Merle NS, Church SE, Fremeaux-Bacchi V, et al. Complement system part I - molecular mechanisms of activation and regulation. Front Immunol. 2015;6:262.
   PubMed Web of Science ®Google Scholar
• Merle NS, Noe R, Halbwachs-Mecarelli L, et al. Complement system part II: role in immunity. Front Immunol. 2015;6:257.
   PubMed Web of Science ®Google Scholar
• Agniswamy J, Lei B, Musser JM, et al. Insight of host immune evasion mediated by two variants of group a Streptococcus Mac protein. J Biol Chem. 2004;279(50):52789–52796.
   PubMed Web of Science ®Google Scholar
• Collin M, Olsen A. EndoS, a novel secreted protein from Streptococcus pyogenes with endoglycosidase activity on human IgG. EMBO J. 2001;20(12):3046–3055.
   PubMed Web of Science ®Google Scholar
• Von Pawel-rammingen U. Streptococcal IdeS and its impact on immune response and inflammation. J Innate Immun. 2012;4(2):132–140.
   PubMed Web of Science ®Google Scholar
• Honda-Ogawa M, Sumitomo T, Mori Y, et al. Streptococcus pyogenes endopeptidase O contributes to evasion from complement-mediated bacteriolysis via binding to human complement factor C1q. J Biol Chem. 2017;292(10):4244–4254.
   PubMed Web of Science ®Google Scholar
• Fernie-King BA, Seilly DJ, Willers C, et al. Streptococcal inhibitor of complement (SIC) inhibits the membrane attack complex by preventing uptake of C567 onto cell membranes. Immunology. 2001;103(3):390–398.
   PubMed Web of Science ®Google Scholar
• Cleary PP, Prahbu U, Dale JB, et al. Streptococcal C5a peptidase is a highly specific endopeptidase. Infect Immun. 1992;60(12):5219–5223.
   PubMed Web of Science ®Google Scholar
• Lynskey NN, Reglinski M, Calay D, et al. Multi-functional mechanisms of immune evasion by the streptococcal complement inhibitor C5a peptidase. PLoS Pathog. 2017;13(8):e1006493.
   PubMed Web of Science ®Google Scholar
• Honda-Ogawa M, Ogawa T, Terao Y, et al. Cysteine proteinase from Streptococcus pyogenes enables evasion of innate immunity via degradation of complement factors. J Biol Chem. 2013;288(22):15854–15864.
   PubMed Web of Science ®Google Scholar
• Caswell CC, Han R, Hovis KM, et al. The Scl1 protein of M6-type group A Streptococcus binds the human complement regulatory protein, factor H, and inhibits the alternative pathway of complement. Mol Microbiol. 2008;67(3):584–596.
   PubMed Web of Science ®Google Scholar
• Pandiripally V, Gregory E, Cue D. Acquisition of regulators of complement activation by Streptococcus pyogenes serotype M1. Infect Immun. 2002;70(11):6206–6214.
   PubMed Web of Science ®Google Scholar
• Ting YT, Batot G, Baker EN, et al. Expression, purification and crystallization of a membrane-associated, catalytically active type I signal peptidase from staphylococcus aureus. Acta Crystallogr F Struct Biol Commun. 2015;71(1):61–65.
   PubMedGoogle Scholar
• Podbielski A, Spellerberg B, Woischnik M, et al. Novel series of plasmid vectors for gene inactivation and expression analysis in group A streptococci (GAS). Gene. 1996;177(1–2):137–147.
   PubMed Web of Science ®Google Scholar
• Okada N, Tatsuno I, Hanski E, et al. Streptococcus pyogenes protein F promotes invasion of HeLa cells. Microbiology. 1998;144(Pt 11):3079–3086.
   Google Scholar
• Loh JM, Adenwalla N, Wiles S, et al. Galleria mellonella larvae as an infection model for group A streptococcus. Virulence. 2013;4(5):419–428.
   PubMed Web of Science ®Google Scholar
• Nakata M, Kreikemeyer B. Genetics, structure, and function of group A streptococcal pili. Front Microbiol. 2021;12:616508.
   PubMed Web of Science ®Google Scholar
• Tsai JC, Loh JM, Clow F, et al. The Group A Streptococcus serotype M2 pilus plays a role in host cell adhesion and immune evasion. Mol Microbiol. 2017;103(2):282–298.
   PubMed Web of Science ®Google Scholar
• Bessen DE, Kalia A. Genomic localization of a t serotype locus to a recombinatorial zone encoding extracellular matrix-binding proteins in Streptococcus pyogenes. Infect Immun. 2002;70(3):1159–1167.
   PubMed Web of Science ®Google Scholar
• Ritchie GE, Moffatt BE, Sim RB, et al. Glycosylation and the complement system. Chem Rev. 2002;102(2):305–320.
   PubMed Web of Science ®Google Scholar
• Wang T, Voglmeir J. PNGases as valuable tools in glycoprotein analysis. Protein Pept Lett. 2014;21(10):976–985.
   PubMed Web of Science ®Google Scholar
• Langley R, Wines B, Willoughby N, et al. The staphylococcal superantigen-like protein 7 binds IgA and complement C5 and inhibits IgA-Fc alpha RI binding and serum killing of bacteria. J Immunol. 2005;174(5):2926–2933.
   PubMed Web of Science ®Google Scholar
• Laursen NS, Gordon N, Hermans S, et al. Structural basis for inhibition of complement C5 by the SSL7 protein from Staphylococcus aureus. Proc Natl Acad Sci U S A. 2010;107(8):3681–3686.
   PubMed Web of Science ®Google Scholar
• Brown EJ. Interaction of gram-positive microorganisms with complement. Curr Top Microbiol Immunol. 1985;121:159–187.
   PubMed Web of Science ®Google Scholar
• Tsai CJ, Loh JM, Proft T. Galleria mellonella infection models for the study of bacterial diseases and for antimicrobial drug testing. Virulence. 2016;7(3):214–229.
   PubMed Web of Science ®Google Scholar
• Loh JM, Adenwalla N, Wiles S, et al. Galleria mellonella larvae as an infection model for group A streptococcus. Virulence. 2013;4(5):419–428.
   PubMed Web of Science ®Google Scholar
• Lorenz N, Clow F, Radcliff FJ, et al. Full functional activity of SSL7 requires binding of both complement C5 and IgA. Immunol Cell Biol. 2013;91(7):469–476.
   PubMed Web of Science ®Google Scholar
• Berends ET, Dekkers JF, Nijland R, et al. Distinct localization of the complement C5b-9 complex on Gram-positive bacteria. Cell Microbiol. 2013;15(12):1955–1968.
   PubMed Web of Science ®Google Scholar
• Fernie-King BA, Seilly DJ, Lachmann PJ. Inhibition of antimicrobial peptides by group A streptococci: SIC and DRS. Biochem Soc Trans. 2006;34(2):273–275.
   PubMedGoogle Scholar
• Frick IM, Shannon O, Neumann A, et al. Streptococcal inhibitor of complement (SIC) modulates fibrinolysis and enhances bacterial survival within fibrin clots. J Biol Chem. 2018;293(35):13578–13591.
   PubMed Web of Science ®Google Scholar
• Neumann A, Happonen L, Karlsson C, et al. Streptococcal protein SIC activates monocytes and induces inflammation. iScience. 2021;24(4):102339.
   PubMed Web of Science ®Google Scholar
• Tran-Winkler HJ, Love JF, Gryllos I, et al. Signal transduction through CsrRS confers an invasive phenotype in group A Streptococcus. PLoS Pathog. 2011;7(10):e1002361.
   PubMed Web of Science ®Google Scholar
• Graham MR, Virtaneva K, Porcella SF, et al. Analysis of the transcriptome of group A Streptococcus in mouse soft tissue infection. Am J Pathol. 2006;169(3):927–942.
   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
• Kansal RG, Datta V, Aziz RK, et al. Dissection of the molecular basis for hypervirulence of an In Vivo–Selected Phenotype of the Widely Disseminated M1T1 strain of group A Streptococcus Bacteria. J Infect Dis. 2010;201(6):855–865.
   PubMed Web of Science ®Google Scholar
• Virtaneva K, Porcella SF, Graham MR, et al. Longitudinal analysis of the group A Streptococcus transcriptome in experimental pharyngitis in cynomolgus macaques. Proc Natl Acad Sci U S A. 2005;102(25):9014–9019.
   PubMed Web of Science ®Google Scholar