Streptococcus suis subtilisin-like serine proteases SspA-1 and SspA-2 interplay with complement C3a and C5a to facilitate bacterial immune evasion and infection

References

• Haas B, Grenier D. Understanding the virulence of Streptococcus suis: a veterinary, medical, and economic challenge. Med Mal Infect. 2018;48(3):159–17. doi: 10.1016/j.medmal.2017.10.001
   PubMed Web of Science ®Google Scholar
• Segura M, Zheng H, de Greeff A, et al. Latest developments on Streptococcus suis: an emerging zoonotic pathogen: part 1. Future Microbiol. 2014;9(4):441–444. doi: 10.2217/fmb.14.14
   PubMed Web of Science ®Google Scholar
• Tan C, Zhang A, Chen H, et al. Recent proceedings on prevalence and pathogenesis of Streptococcus suis. Curr Issues Mol Biol. 2019;32:473–520. doi: 10.21775/cimb.032.473
   PubMed Web of Science ®Google Scholar
• Bleuze M, Gottschalk M, Segura M. Neutrophils in Streptococcus suis infection: from host defense to pathology. Microorganisms. 2021;9(11):2392. doi: 10.3390/microorganisms9112392
   PubMed Web of Science ®Google Scholar
• Goyette-Desjardins G, Auger JP, Xu J, et al. Streptococcus suis, an important pig pathogen and emerging zoonotic agent-an update on the worldwide distribution based on serotyping and sequence typing. Emerg Microbes Infect. 2014;3(6):e45. doi: 10.1038/emi.2014.45
   PubMed Web of Science ®Google Scholar
• Feng Y, Zhang H, Ma Y, et al. Uncovering newly emerging variants of Streptococcus suis, an important zoonotic agent. Trends Microbiol. 2010;18(3):124–31. doi: 10.1016/j.tim.2009.12.003
   PubMed Web of Science ®Google Scholar
• Liu P, Pian Y, Li X, et al. Streptococcus suis adenosine synthase functions as an effector in evasion of PMN-mediated innate immunit. J Infect Dis. 2014;210(1):35–45. doi: 10.1093/infdis/jiu050
   PubMed Web of Science ®Google Scholar
• Doran KS, Fulde M, Gratz N, et al. Host-pathogen interactions in bacterial meningitis. Acta Neuropathol. 2016;131(2):185–209. doi: 10.1007/s00401-015-1531-z
   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. doi: 10.3389/fimmu.2015.00262
   PubMed Web of Science ®Google Scholar
• Ghebrehiwet B. The complement system: an evolution in progress. F1000Res. 2016;5:2840. doi: 10.12688/f1000research.10065.1
   PubMedGoogle Scholar
• Laarman A, Milder F, van Strijp J, et al. Complement inhibition by gram-positive pathogens: molecular mechanisms and therapeutic implications. J Mol Med (Berl). 2010;88(2):115–20. doi: 10.1007/s00109-009-0572-y
   PubMed Web of Science ®Google Scholar
• Pausa M, Pellis V, Cinco M, et al. Serum-resistant strains of borrelia burgdorferi evade complement-mediated killing by expressing a CD59-like complement inhibitory molecule. J Immunol. 2003;170(6):3214–22. doi: 10.4049/jimmunol.170.6.3214
   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):15854–64. doi: 10.1074/jbc.M113.469106
   PubMed Web of Science ®Google Scholar
• Dai S, Rajaram MV, Curry HM, et al. Fine tuning inflammation at the front door: macrophage complement receptor 3-mediates phagocytosis and immune suppression for Francisella tularensis. PLOS Pathog. 2013;9(1):e1003114. doi: 10.1371/journal.ppat.1003114
   PubMed Web of Science ®Google Scholar
• Jongerius I, Kohl J, Pandey MK, et al. Staphylococcal complement evasion by various convertase-blocking molecules. J Exp Med. 2007;204(10):2461–2471. doi: 10.1084/jem.20070818
   PubMed Web of Science ®Google Scholar
• Lathem WW, Bergsbaken T, Welch RA. Potentiation of C1 esterase inhibitor by StcE, a metalloprotease secreted by Escherichia coli O157: H7. J Exp Med. 2004;199(8):1077–87. doi: 10.1084/jem.20030255
   PubMed Web of Science ®Google Scholar
• Cartwright K. Pneumococcal disease in western Europe: burden of disease, antibiotic resistance and management. Eur J Pediatr. 2002;161(4):188–95. doi: 10.1007/s00431-001-0907-3
   PubMed Web of Science ®Google Scholar
• Li X, Liu P, Gan S, et al. Mechanisms of host-pathogen protein complex formation and bacterial immune evasion of Streptococcus suis Protein Fhb. J Biol Chem. 2016;291(33):17122–32. doi: 10.1074/jbc.M116.719443
   PubMed Web of Science ®Google Scholar
• Fittipaldi N, Segura M, Grenier D, et al. Virulence factors involved in the pathogenesis of the infection caused by the swine pathogen and zoonotic agent Streptococcus suis. Future Microbiol. 2012;7(2):259–279. doi: 10.2217/fmb.11.149
   PubMed Web of Science ®Google Scholar
• Deng S, Xu T, Fang Q, et al. The surface-exposed protein SntA contributes to complement evasion in zoonotic Streptococcus suis. Front Immunol. 2018;9:1063. doi: 10.3389/fimmu.2018.01063
   PubMed Web of Science ®Google Scholar
• Seele J, Beineke A, Hillermann LM, et al. The immunoglobulin M-degrading enzyme of Streptococcus suis, IdeSsuis, is involved in complement evasion. Vet Res. 2015;46(1):45. doi: 10.1186/s13567-015-0171-6
   PubMedGoogle Scholar
• Deng S, Zhao L, Zhu J, et al. Complement C3aR/C5aR-binding protein Suilysin of Streptococcus suis contributes to monocyte chemotaxis. Vet Microbiol. 2020;242:108599. doi: 10.1016/j.vetmic.2020.108599
   PubMed Web of Science ®Google Scholar
• Lo MW, Woodruff TM. Complement: bridging the innate and adaptive immune systems in sterile inflammation. J Leukocyte Biol. 2020;108(1):339–351. doi: 10.1002/JLB.3MIR0220-270R
   PubMed Web of Science ®Google Scholar
• Ward PA, Fattahi F. New strategies for treatment of infectious sepsis. J Leukocyte Biol. 2019;106(1):187–192. doi: 10.1002/JLB.4MIR1118-425R
   PubMed Web of Science ®Google Scholar
• Yin S, Li M, Rao X, et al. Subtilisin-like protease-1 secreted through type IV secretion system contributes to high virulence of Streptococcus suis 2. Sci Rep. 2016;6(1):27369. doi: 10.1038/srep27369
   PubMedGoogle Scholar
• Bonifait L, Grenier D. The SspA subtilisin-like protease of Streptococcus suis triggers a pro-inflammatory response in macrophages through a non-proteolytic mechanism. BMC Microbiol. 2011;11(1):47. doi: 10.1186/1471-2180-11-47
   PubMedGoogle Scholar
• Hu Q, Liu P, Yu Z, et al. Identification of a cell wall-associated subtilisin-like serine protease involved in the pathogenesis of Streptococcus suis serotype 2. Microb Pathog. 2010;48(3–4):103–9. doi: 10.1016/j.micpath.2009.11.005
   PubMed Web of Science ®Google Scholar
• Bonifait L, de la Cruz Dominguez-Punaro M, Vaillancourt K, et al. The cell envelope subtilisin-like proteinase is a virulence determinant for Streptococcus suis. BMC Microbiol. 2010;10(1):42. doi: 10.1186/1471-2180-10-42
   PubMedGoogle Scholar
• Holden MT, Hauser H, Sanders M, et al. Rapid evolution of virulence and drug resistance in the emerging zoonotic pathogen Streptococcus suis. PloS One. 2009;4(7):e6072. doi: 10.1371/journal.pone.0006072
   PubMed Web of Science ®Google Scholar
• Li Q, Liu H, Du D, et al. Identification of novel laminin- and fibronectin-binding proteins by Far-Western Blot: capturing the adhesins of Streptococcus suis type 2. Front Cell Infect Microbiol. 2015;5:82. doi: 10.3389/fcimb.2015.00082
   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. doi: 10.1371/journal.ppat.1006493
   PubMed Web of Science ®Google Scholar
• Zheng C, Wei M, Qiu J, et al. A markerless gene deletion system in Streptococcus suis by using the Copper-Inducible Vibrio parahaemolyticus YoeB Toxin as a counterselectable marker. Microorganisms. 2021;9(5):1095. doi: 10.3390/microorganisms9051095
   PubMed Web of Science ®Google Scholar
• Li H, Li T, Hu Q, et al. Inhibitors targeting the autophosphorylation of serine/threonine kinase of Streptococcus suis show potent antimicrobial activity. Front Microbiol. 2022;13:990091. doi: 10.3389/fmicb.2022.990091
   PubMed Web of Science ®Google Scholar
• Wertheim HF, Nghia HD, Taylor W, et al. Streptococcus suis: an emerging human pathogen. Clin Infect Dis. 2009;48(5):617–25. doi: 10.1086/596763
   PubMed Web of Science ®Google Scholar
• Gottschalk M, Xu J, Calzas C, et al. Streptococcus suis: a new emerging or an old neglected zoonotic pathogen? Future Microbiol. 2010;5(3):371–391. doi: 10.2217/fmb.10.2
   PubMed Web of Science ®Google Scholar
• Segura M, Fittipaldi N, Calzas C, et al. Critical Streptococcus suis virulence factors: are they all really critical? Trends Microbiol. 2017;25(7):585–599. doi: 10.1016/j.tim.2017.02.005
   PubMed Web of Science ®Google Scholar
• Baums CG, Valentin-Weigand P. Surface-associated and secreted factors of Streptococcus suis in epidemiology, pathogenesis and vaccine development. Anim Health Res Rev. 2009;10(1):65–83. doi: 10.1017/S146625230999003X
   PubMedGoogle Scholar
• Li H, Dang G, Liu H, et al. Characterization of a novel mycobacterium tuberculosis serine protease (Rv3194c) activity and pathogenicity. Tuberculosis (Edinb). 2019;119:101880. doi: 10.1016/j.tube.2019.101880
   PubMed Web of Science ®Google Scholar
• Chen C, Tang J, Dong W, et al. A glimpse of streptococcal toxic shock syndrome from comparative genomics of S. suis 2 Chinese isolates. PloS One. 2007;2(3):e315. doi: 10.1371/journal.pone.0000315
   PubMed Web of Science ®Google Scholar
• Jobichen C, Tan YC, Prabhakar MT, et al. Structure of ScpC, a virulence protease from Streptococcus pyogenes, reveals the functional domains and maturation mechanism. Biochem J. 2018;475(17):2847–2860. doi: 10.1042/BCJ20180145
   PubMedGoogle Scholar
• Chmouryguina I, Suvorov A, Ferrieri P, et al. Conservation of the C5a peptidase genes in group a and B streptococci. Infect Immun. 1996;64(7):2387–90. doi: 10.1128/iai.64.7.2387-2390.1996
   PubMed Web of Science ®Google Scholar
• Terao Y, Yamaguchi M, Hamada S, et al. Multifunctional glyceraldehyde-3-phosphate dehydrogenase of Streptococcus pyogenes is essential for evasion from neutrophils. J Biol Chem. 2006;281(20):14215–23. doi: 10.1074/jbc.M513408200
   PubMed Web of Science ®Google Scholar
• Mishra R, Das A, Rana S. Resveratrol binding to human complement fragment 5a ((h)C5a) may modulate the C5aR signaling axes. J Biomol Struct Dyn. 2021;39(5):1766–1780. doi: 10.1080/07391102.2020.1738958
   PubMed Web of Science ®Google Scholar
• Haynes DR, Harkin DG, Bignold LP, et al. Inhibition of C5a-induced neutrophil chemotaxis and macrophage cytokine production in vitro by a new C5a receptor antagonist. Biochem Pharmacol. 2000;60(5):729–33. doi: 10.1016/S0006-2952(00)00361-0
   PubMed Web of Science ®Google Scholar
• Liu Y, Xu SQ, Long WJ, et al. C5aR antagonist inhibits occurrence and progression of complement C5a induced inflammatory response of microglial cells through activating p38MAPK and ERK1/2 signaling pathway. Eur Rev Med Pharmacol Sci. 2018;22(22):7994–8003. doi: 10.26355/eurrev_201811_16428
   PubMed Web of Science ®Google Scholar
• Fan J, Zhao L, Hu Q, et al. Screening for Virulence-Related Genes via a Transposon Mutant Library of Streptococcus suis Serotype 2 Using a Galleria mellonella Larvae Infection Model. Microorganisms. 2022;10(5):868. doi: 10.3390/microorganisms10050868
   PubMed Web of Science ®Google Scholar
• Heath DS, Axelrad AA, McLeod DL, et al. Separation of the erythropoietin-responsive progenitors BFU-E and CFU-E in mouse bone marrow by unit gravity sedimentation. Blood. 1976;47(5):777–92. doi: 10.1182/blood.V47.5.777.777
   PubMed Web of Science ®Google Scholar
• Yang R, Wang J, Wang F, et al. Blood–brain barrier integrity damage in bacterial meningitis: the underlying link, mechanisms, and therapeutic targets. Int J Mol Sci. 2023;24(3):2852. doi: 10.3390/ijms24032852
   PubMed Web of Science ®Google Scholar