9,821
Views
20
CrossRef citations to date
0
Altmetric
Review Article

Pathogenicity and virulence of Streptococcus pneumoniae: Cutting to the chase on proteases

Pages 766-787 | Received 14 Aug 2020, Accepted 09 Feb 2021, Published online: 04 Mar 2021

References

  • Anderton JM, Rajam G, Romero-Steiner S, et al. E-cadherin is a receptor for the common protein pneumococcal surface adhesin A (PsaA) of Streptococcus pneumoniae. Microb Pathog. 2007;42(5–6):225–236.
  • Rosenow C, Ryan P, Weiser JN, et al. Contribution of novel choline-binding proteins to adherence, colonization and immunogenicity of Streptococcus pneumoniae. Mol Microbiol. 1997;25(5):819–829.
  • Voss S, Hallström T, Saleh M, et al. The choline-binding protein PspC of Streptococcus pneumoniae interacts with the C-terminal heparin-binding domain of vitronectin. J Biol Chem. 2013;288(22):15614–15627.
  • Zhang JR, Mostov KE, Lamm ME, et al. The polymeric immunoglobulin receptor translocates pneumococci across human nasopharyngeal epithelial cells. Cell. 2000;102(6):827–837.
  • King SJ, Hippe KR, Weiser JN. Deglycosylation of human glycoconjugates by the sequential activities of exoglycosidases expressed by Streptococcus pneumoniae. Mol Microbiol. 2006;59(3):961–974.
  • Tong HH, McIver MA, Fisher LM, et al. Effect of lacto-N-neotetraose, asialoganglioside-GM1 and neuraminidase on adherence of otitis media-associated serotypes ofStreptococcus pneumoniaeto chinchilla tracheal epithelium. Microbial Pathogen. 1999;26(2):111–119.
  • Feldman C, Munro NC, Jeffery PK, et al. Pneumolysin induces the salient histologic features of pneumococcal infection in the rat lung in vivo. Am J Respir Cell Mol Biol. 1991;5(5):416–423.
  • Houldsworth S, Andrew PW, Mitchell TJ. Pneumolysin stimulates production of tumor necrosis factor alpha and interleukin-1 beta by human mononuclear phagocytes. Infect Immun. 1994;62(4):1501–1503.
  • Subramanian K, Neill DR, Malak H, et al. Pneumolysin binds to the mannose-receptor C type 1 (MRC-1) leading to anti-inflammatory responses and enhanced pneumococcal survival. Nat Microbiol. 2019;4(1):62–70.
  • Ren B, Szalai AJ, Thomas O, et al. Both family 1 and family 2 PspA proteins can inhibit complement deposition and confer virulence to a capsular serotype 3 strain of Streptococcus pneumoniae. Infect Immun. 2003;71(1):75–85.
  • Brown EJ, Joiner KA, Cole RM, et al. Localization of complement component 3 on Streptococcus pneumoniae: anti-capsular antibody causes complement deposition on the pneumococcal capsule.. Infect Immun. 1983;39(1):403–409.
  • Wood WB, Smith MR. The inhibition of surface phagocytosis by the capsular slime layer of pneumococcus type III. J Exp Med. 1949;90(1):85–96.
  • Wartha F, Beiter K, Albiger B, et al. Capsule and d-alanylated lipoteichoic acids protect Streptococcus pneumoniae against neutrophil extracellular traps. Cell Microbiol. 2007;9(5):1162–1171.
  • Thibodeaux BA, Caballero AR, Marquart ME, et al. Corneal virulence of Pseudomonas aeruginosa elastase B and alkaline protease produced by Pseudomonas putida. Curr Eye Res. 2007;32(4):373–386.
  • Le Berre R, Nguyen S, Nowak E, et al. Relative contribution of three main virulence factors in Pseudomonas aeruginosa pneumonia. Crit Care Med. 2011;39(9):2113–2120.
  • Maestro B, Sanz JM. Choline binding proteins from Streptococcus pneumoniae: a dual role as enzybiotics and targets for the design of new antimicrobials. Antibiotics (Basel). 2016;5(2):21.
  • Johnson MK. Characterization of a peptidase from Diplococcus pneumoniae. Antonie Van Leeuwenhoek. 1973;39(1):599–608.
  • Johnson MK. Physiological roles of pneumococcal peptidases. J Bacteriol. 1974;119(3):844–847.
  • Kilian M, Mestecky J, Schrohenloher RE. Pathogenic species of the genus Haemophilus and Streptococcus pneumoniae produce immunoglobulin A1 protease. Infect Immun. 1979;26(1):143–149.
  • Male CJ. Immunoglobulin A1 protease production by Haemophilus influenzae and Streptococcus pneumoniae. Infect Immun. 1979;156(1):254–261.
  • Courtney HS. Degradation of connective tissue proteins by serine proteases from Streptococcus pneumoniae. Biochem Biophys Res Commun. 1991;175(3):1023–1028.
  • Kwon K, Hasseman J, Latham S, et al. Recombinant expression and functional analysis of proteases from Streptococcus pneumoniae, Bacillus anthracis, and Yersinia pestis. BMC Biochem. 2011;12(1):17.
  • Nganje CN, Haynes SA, Qabar CM, et al. PepN is a non-essential, cell wall-localized protein that contributes to neutrophil elastase-mediated killing of Streptococcus pneumoniae. PLoS One. 2019;14(2):e0211632.
  • Blevins LK, Parsonage D, Oliver MB, et al. A novel function for the Streptococcus pneumoniae aminopeptidase N: inhibition of T cell effector function through the regulation of TCR signaling. Front Immunol. 2017;8:1610.
  • Wang L, Zhang X, Wu G, et al. Streptococcus pneumoniae aminopeptidase N contributes to bacterial virulence and elicits a strong innate immune response through MAPK and PI3K/AKT signaling. J Microbiol. 2020;58(4):330–339.
  • Pei J, Mitchell DA, Dixon JE, et al. Expansion of type II CAAX proteases reveals evolutionary origin of gamma-secretase subunit APH-1. J Mol Biol. 2011;410(1):18–26.
  • Bek-Thomsen M, Poulsen K, Kilian M. Occurrence and evolution of the paralogous zinc metalloproteases IgA1 protease, ZmpB, ZmpC, and ZmpD in Streptococcus pneumoniae and related commensal species. mBio. 2012;3(5):e00303–12.
  • Bergé M, García P, Iannelli F, et al. The puzzle of zmpB and extensive chain formation, autolysis defect and non-translocation of choline-binding proteins in Streptococcus pneumoniae. Mol Microbiol. 2001;39(6):1651–1660.
  • Löfling J, Vimberg V, Battig P, et al. Cellular interactions by LPxTG-anchored pneumococcal adhesins and their streptococcal homologues. Cell Microbiol. 2011;13(2):186–197.
  • Håvarstein LS, Coomaraswamy G, Morrison DA. An unmodified heptadecapeptide pheromone induces competence for genetic transformation in Streptococcus pneumoniae.. Proc Natl Acad Sci U S A. 1995;92(24):11140–11144.
  • Håvarstein LS, Martin B, Johnsborg O, et al. New insights into the pneumococcal fratricide: relationship to clumping and identification of a novel immunity factor. Mol Microbiol. 2006;59(4):1297–1307.
  • Gosink KK, Mann ER, Guglielmo C, et al. Role of novel choline binding proteins in virulence of Streptococcus pneumoniae. Infect Immun. 2000;68(10):5690–5695.
  • Straume D, Stamsås GA, Salehian Z, et al. Overexpression of the fratricide immunity protein ComM leads to growth inhibition and morphological abnormalities in Streptococcus pneumoniae. Microbiology. 2017;163(1):9–21.
  • Mann B, Orihuela C, Antikainen J, et al. Multifunctional role of choline binding protein G in pneumococcal pathogenesis. Infect Immun. 2006;74(2):821–829.
  • Meinel C, Spartà G, Dahse H-M, et al. Streptococcus pneumoniae from patients with hemolytic uremic syndrome binds human plasminogen via the surface protein PspC and uses plasmin to damage human endothelial cells. J Infect Dis. 2018;217(3):358–370.
  • Cao J, Gong Y, Li D, et al. CD4+ T lymphocytes mediated protection against invasive pneumococcal infection induced by mucosal immunization with ClpP and CbpA. Vaccine. 2009;27(21):2838–2844.
  • Cao J, Gong Y, Dong S, et al. Pneumococcal ClpP modulates the maturation and activation of human dendritic cells: implications for pneumococcal infections. J Leukoc Biol. 2013;93(5):737–749.
  • Park C-Y, Kim E-H, Choi S-Y, et al. Virulence attenuation of Streptococcus pneumoniae clpP mutant by sensitivity to oxidative stress in macrophages via an NO-mediated pathway. J Microbiol. 2010;48(2):229–235.
  • Cao J, Li D, Gong Y, et al. Caseinolytic protease: a protein vaccine which could elicit serotype-independent protection against invasive pneumococcal infection. Clin Exp Immunol. 2009;156(1):52–60.
  • Pestova EV, Håvarstein LS, Morrison DA. Regulation of competence for genetic transformation in Streptococcus pneumoniae by an auto-induced peptide pheromone and a two-component regulatory system. Mol Microbiol. 1996;21(4):853–862.
  • Chastanet A, Prudhomme M, Claverys JP, et al. Regulation of Streptococcus pneumoniae clp genes and their role in competence development and stress survival. J Bacteriol. 2001;183(24):7295–7307.
  • Robertson GT, Ng WL, Foley J, et al. Global transcriptional analysis of clpP mutations of type 2 Streptococcus pneumoniae and their effects on physiology and virulence. J Bacteriol. 2002;184(13):3508–3520.
  • Liu X, Gallay C, Kjos M, et al. High-throughput CRISPRi phenotyping identifies new essential genes in Streptococcus pneumoniae. Mol Syst Biol. 2017;13(5):931.
  • Turgay K, Hahn J, Burghoorn J, et al. Competence in Bacillus subtilis is controlled by regulated proteolysis of a transcription factor. Embo J. 1998;17:6730–6738.
  • Sung CK, Morrison DA. Two distinct functions of ComW in stabilization and activation of the alternative sigma factor ComX in Streptococcus pneumoniae. J Bacteriol. 2005;187(9):3052–3061.
  • Hui FM, Morrison DA. Genetic transformation in Streptococcus pneumoniae: nucleotide sequence analysis shows comA, a gene required for competence induction, to be a member of the bacterial ATP-dependent transport protein family. J Bacteriol. 1991;173(1):372–381.
  • Ishii S, Yano T, Hayash H. Expression and characterization of the peptidase domain of Streptococcus pneumoniae ComA, a bifunctional ATP-binding cassette transporter involved in quorum sensing pathway. J Biol Chem. 2006;281(8):4726–4731.
  • Kwon H-Y, Kim S-W, Choi M-H, et al. Effect of heat shock and mutations in ClpL and ClpP on virulence gene expression in Streptococcus pneumoniae. Infect Immun. 2003;71(7):3757–3765.
  • Kwon H-Y, Ogunniyi AD, Choi M-H, et al. The ClpP protease of Streptococcus pneumoniae modulates virulence gene expression and protects against fatal pneumococcal challenge. Infect Immun. 2004;72(10):5646–5653.
  • Wu K, Zhang X, Shi J, et al. Immunization with a combination of three pneumococcal proteins confers additive and broad protection against Streptococcus pneumoniae infections in mice. Infect Immun. 2010;78(3):1276–1283.
  • Lee J-O, Kim J-Y, Rhee D-K D-K. Streptococcus pneumoniae ClpP protease induces apoptosis via caspase-independent pathway in human neuroblastoma cells: cytoplasmic relocalization of p53. Toxicon. 2013;70:142–152.
  • Ritchie ND, Evans TJ, Dual RNA-seq in Streptococcus pneumoniae infection reveals compartmentalized neutrophil responses in lung and pleural space. mSystems. 2019;4(4):e00216–19.
  • Angel CS, Ruzek M, Hostetter MK. Degradation of C3 by Streptococcus pneumoniae. J Infect Dis. 1994;170(3):600–608.
  • Hostetter MK, Dunny G, Nandiwada L Human complement C3-degrading protein from Streptococcus pneumoniae. United States patent number 6, 676,943; 2004 Jan 13.
  • Armstrong RN. Mechanistic diversity in a metalloenzyme superfamily. Biochemistry. 2000;39(45):13625–13632.
  • Carter R, Wolf J, Van Opijnen T, et al. Genomic analyses of pneumococci from children with sickle cell disease expose host-specific bacterial adaptations and deficits in current interventions. Cell Host Microbe. 2014;15(5):587–599.
  • Rowe HM, Karlsson E, Echlin H, et al. Bacterial factors required for transmission of Streptococcus pneumoniae in mammalian hosts. Cell Host Microbe. 2019;25(6):884–891.
  • Kim D, San BH, Moh SH, et al. Structural basis for the substrate specificity of PepA from Streptococcus pneumoniae, a dodecameric tetrahedral protease. Biochem Biophys Res Commun. 2010;391(1):431–436.
  • Lipinska B, Zylicz M, Georgopoulos C. The HtrA (DegP) protein, essential for Escherichia coli survival at high temperatures, is an endopeptidase.. J Bacteriol. 1990;172(4):1791–1797.
  • De Stoppelaar SF, Bootsma HJ, Zomer A, et al. Streptococcus pneumoniae serine protease HtrA, but not SFP or PrtA, is a major virulence factor in pneumonia. PLoS One. 2013;8(11):e80062.
  • European Molecular Biology Laboratory-European Bioinformatics Institute (EMBL-EBI) InterPro. https://www.ebi.ac.uk/interpro/
  • Spiess C, Beil A, Ehrmann M. A temperature-dependent switch from chaperone to protease in a widely conserved heat shock protein. Cell. 1999;97(3):339–347.
  • Peters K, Schweizer I, Beilharz K, et al. Streptococcus pneumoniae PBP2x mid-cell localization requires the C-terminal PASTA domains and is essential for cell shape maintenance. Mol Microbiol. 2014;93(4):733–755.
  • Ibrahim YM, Kerr AR, McCluskey J, et al. Role of HtrA in the virulence and competence of Streptococcus pneumoniae. Infect Immun. 2004;72(6):3584–3591.
  • Sebert ME, Patel KP, Plotnick M, et al. Pneumococcal HtrA protease mediates inhibition of competence by the CiaRH two-component signaling system. J Bacteriol. 2005;187(12):3969–3979.
  • Cassone M, Gagne AL, Spruce LA, et al. The HtrA protease from Streptococcus pneumoniae digests both denatured proteins and the competence-stimulating peptide. J Biol Chem. 2012;287(46):38449–38459.
  • Liu Y, Zeng Y, Huang Y, et al. HtrA-mediated selective degradation of DNA uptake apparatus accelerates termination of pneumococcal transformation. Mol Microbiol. 2019;112(4):1308–1325.
  • Schnorpfeil A, Kranz M, Kovács M, et al. Target evaluation of the non-coding csRNAs reveals a link of the two-component regulatory system CiaRH to competence control in Streptococcus pneumonia R6. Mol Microbiol. 2013;89(2):334–349.
  • Stevens KE, Chang D, Zwack EE, et al. Competence in Streptococcus pneumoniae is regulated by the rate of ribosomal decoding errors. mBio. 2011;2(5):e00071–11.
  • Dawid S, Sebert ME, Weiser JN. Bacteriocin activity of Streptococcus pneumoniae is controlled by the serine protease HtrA via posttranscriptional regulation. J Bacteriol. 2009;191(5):1509–1518.
  • Kochan TJ, Dawid S. The HtrA protease of Streptococcus pneumoniae controls density-dependent stimulation of the bacteriocin blp locus via disruption of pheromone secretion. J Bacteriol. 2013;195(7):1561–1572.
  • Sebert ME, Palmer LM, Rosenberg M, et al. Microarray-based identification of htrA, a Streptococcus pneumoniae gene that is regulated by the CiaRH two-component system and contributes to nasopharyngeal colonization. Infect Immun. 2002;70(8):4059–4067.
  • Wikström MB, Dahlén G, Kaijser B, et al. Degradation of human immunoglobulins by proteases from Streptococcus pneumoniae obtained from various human sources.. Infect Immun. 1984;44(1):33–37.
  • Reinholdt J, Kilian M. Comparative analysis of immunoglobulin A1 protease activity among bacteria representing different genera, species, and strains. Infect Immun. 1997;65(11):4452–4459.
  • Wani JH, Gilbert JV, Plaut AG, et al. Identification, cloning, and sequencing of the immunoglobulin A1 protease gene of Streptococcus pneumoniae.. Infect Immun. 1996;64(10):3967–3974.
  • Poulsen K, Reinholdt J, Jespersgaard C, et al. A comprehensive genetic study of streptococcal immunoglobulin A1 proteases: evidence for recombination within and between species. Infect Immun. 1998;66(1):181–190.
  • Poulsen K, Reinholdt J, Kilian M. Characterization of the Streptococcus pneumoniae immunoglobulin A1 protease (iga) and its translation product. Infect Immun. 1996;64(10):3957–3966.
  • Chi YC, Rahkola JT, Kendrick AA, et al. Streptococcus pneumoniae IgA1 protease: a metalloprotease that can catalyze in a split manner in vitro. Protein Sci. 2017;26(3):600–610.
  • Kilian M, Mestecky J, Kulhavy R, et al. IgA1 proteases from Haemophilus influenzae, Streptococcus pneumoniae, Neisseria meningitidis, and Streptococcus sanguis: comparative immunochemical studies. J Immunol. 1980;124(6):2596–2600.
  • Batten MR, Senior BW, Kilian M, et al. Amino acid sequence requirements in the hinge of human immunoglobulin A1 (IgA1) for cleavage by streptococcal IgA1 proteases. Infect Immun. 2003;72(3):1462–1469.
  • Senior BW, Batten MR, Kilian M, et al. Amino acid sequence requirements in the human IgA1 hinge for cleavage by streptococcal IgA1 proteases. Biochem Soc Trans. 2002;30(3):A92.
  • Janoff EN, Rubins JB, Fasching C, et al. Pneumococcal IgA1 protease subverts specific protection by human IgA1. Mucosal Immunol. 2014;7(2):249–256.
  • Weiser JN, Bae D, Fasching C, et al. Antibody-enhanced pneumococcal adherence requires IgA1 protease. Proc Natl Acad Sci U S A. 2003;100(7):4215–4220.
  • Chiavolini D, Memmi G, Maggi T, et al. The three extra-cellular zinc metalloproteinases of Streptococcus pneumoniae have a different impact on virulence in mice. BMC Microbiol. 2003;3(1):14.
  • Audouy SAL, Van Selm S, Van Roosmalen ML, et al. Development of lactococcal GEM-based pneumococcal vaccines. Vaccine. 2007;25(13):2497–2506.
  • Abdullah MR, Gutiérrez-Fernández J, Pribyl T, et al. Structure of the pneumococcal l-d-carboxypeptidase DacB and the pathophysiological effects of disabled cell wall hydrolases DacA and DacB. Mol Microbiol. 2014;93(6):1183–1206.
  • Morlot C, Pernot L, Le Gouellec A, et al. Crystal structure of apeptidoglycan synthesis regulatory factor (PBP3) from Streptococcus pneumoniae. J Biol Chem. 2005;280(16):15984–15991.
  • Severin A, Schuster C, Hakenbeck R, et al. Altered murein composition in a DD-carboxypeptidase mutant of Streptococcus pneumoniae.. J Bacteriol. 1992;174(15):5152–5155.
  • Barendt SM, Sham L-T, Winkler ME. Characterization of mutants deficient in the L,D-carboxypeptidase (DacB) and WalRK (VicRK) regulon, involved in peptidoglycan maturation of Streptococcus pneumoniae serotype 2 strain D39. J Bacteriol. 2011;193(9):2290–2300.
  • Hoyland CN, Aldridge C, Cleverley RM, et al. Structure of the LdcB LD-carboxypeptidase reveals the molecular basis of peptidoglycan recognition. Structure. 2014;22(7):949–960.
  • Zhang J, Yang YH, Jiang YL, et al. Structural and biochemical analyses of the Streptococcus pneumoniae L,D-carboxypeptidase DacB. Acta Crystallogr D Biol Crystallogr. 2015;71(Pt 2):283–292.
  • Agarwal V, Kuchipudi A, Fulde M, et al. Streptococcus pneumoniae endopeptidase O (PepO) is a multifunctional plasminogen- and fibronectin-binding protein, facilitating evasion of innate immunity and invasion of host cells. J Biol Chem. 2013;288(10):6849–6863.
  • Agarwal V, Sroka M, Fulde M, et al. Binding of Streptococcus pneumoniae endopeptidase O (PepO) to complement component C1q modulates the complement attack and promotes host cell adherence. J Biol Chem. 2014;289(22):15833–15844.
  • Bergmann S, Rohde M, Preer KT, et al. The nine residue plasminogen-binding motif of the pneumococcal enolase is the major cofactor of plasmin-mediated degradation of extracellular matrix, dissolution of fibrin and transmigration. Thromb Haemost. 2005;94(2):304–311.
  • Shu Z, Yuan J, Wang H, et al. Streptococcus pneumonia PepO promotes host anti-infection defense via autophagy in a Toll-like receptor 2/4 dependent manner. Virulence. 2020;11(1):270–282.
  • Yao H, Zhang H, Lan K, et al. Streptococcus pneumoniae endopeptidase O (PepO) enhances particle uptake by macrophages in a Toll-like receptor 2- and miR-155-dependent manner. Infect Immun. 2017;85(4):e01012–16.
  • Zhang H, Kang L, Yao H, et al. Streptococcus pneumoniae endopeptidase O (PepO) elicits a strong innate immune response in mice via TLR2 and TLR4 signaling pathways. Front Cell Infect Microbiol. 2016;6:23.
  • Hostetter MK. Opsonic and nonopsonic interactions of C3 with Streptococcus pneumoniae. Microb Drug Resist. 1999;5(2):85–89.
  • Zhang Y, Masi AW, Barniak V, et al. Recombinant PhpA protein, a unique histidine motif-containing protein from Streptococcus pneumoniae, protects mice against intranasal pneumococcal challenge. Infect Immun. 2001;69(6):3827–3836.
  • Adamou JE, Heinrichs JH, Erwin AL, et al. Identification and characterization of a novel family of pneumococcal proteins that are protective against sepsis. Infect Immun. 2001;69(2):949–958.
  • Melin M, Di Paolo E, Tikkanen L, et al. Interaction of pneumococcal histidine triad proteins with human complement. Infect Immun. 2010;78(5):2089–2098.
  • Ogunniyi AD, Grabowicz M, Mahdi LK, et al. Pneumococcal histidine triad proteins are regulated by the Zn 2+++ -dependent repressor AdcR and inhibit complement deposition through the recruitment of complement factor H. Faseb J. 2009;23(3):731–738.
  • Bethe G, Nau R, Wellmer A, et al. The cell wall-associated serine protease PrtA: a highly conserved virulence factor of Streptococcus pneumoniae. FEMS Microbiol Lett. 2001;205(1):99–104.
  • Mahdi LK, Van Der Hoek MB, Ebrahimie E, et al. Characterization of pneumococcal genes involved in bloodstream invasion in a mouse model. PLoS One. 2015;10(11):e0141816.
  • Frolet C, Beniazza M, Roux L, et al. New adhesin functions of surface-exposed pneumococcal proteins. BMC Microbiol. 2010;10(1):190.
  • Mirza S, Wilson L, Benjamin WH, et al. Serine protease PrtA from Streptococcus pneumoniae plays a role in the killing of S. pneumoniae by apolactoferrin. Infect Immun. 2011;79(6):2440–2450.
  • Zhang YB, Greenberg B, Lacks SA. Analysis of a Streptococcus pneumoniae gene encoding signal peptidase I and overproduction of the enzyme. Gene. 1997;194(2):249–255.
  • Khandavilli S, Homer KA, Yuste J, et al. Maturation of Streptococcus pneumoniae lipoproteins by a type II signal peptidase is required for ABC transporter function and full virulence. Mol Microbiol. 2008;67(3):541–557.
  • Pribyl T, Moche M, Dreisbach A, et al. Influence of impaired lipoprotein biogenesis on surface and exoproteome of Streptococcus pneumoniae. J Proteome Res. 2014;13(2):650–667.
  • Camilli R, Pettini E, Del Grosso M, et al. Zinc metalloproteinase genes in clinical isolates of Streptococcus pneumoniae: association of the full array with a clonal cluster comprising serotypes 8 and 11A. Microbiology. 2006;152(Pt 2):313–321.
  • Novak R, Charpentier E, Braun JS, et al. Extracellular targeting of choline-binding proteins in Streptococcus pneumoniae by a zinc metalloprotease. Mol Microbiol. 2000;36(2):366–376.
  • Gong Y, Xu W, Cui Y, et al. Immunization with a ZmpB-based protein vaccine could protect against pneumococcal diseases in mice. Infect Immun. 2011;79(2):867–878.
  • Blue CE, Paterson GK, Kerr AR, et al. ZmpB, a novel virulence factor of Streptococcus pneumoniae that induces tumor necrosis factor alpha production in the respiratory tract. Infect Immun. 2003;71(9):4925–4935.
  • Hsieh YC, Tsao PN, Chen CL, et al. Establishment of a young mouse model and identification of an allelic variation of zmpB in complicated pneumonia caused by Streptococcus pneumoniae. Crit Care Med. 2008;36(4):1248–1255.
  • Cremers AJ, Kokmeijer I, Groh L, et al. The role of ZmpC in the clinical manifestation of invasive pneumococcal disease. Int J Med Microbiol. 2014;304(8):984–989.
  • Surewaard BG, Trzciński K, Jacobino SR, et al. Pneumococcal immune evasion: zmpC inhibits neutrophil influx. Cell Microbiol. 2013;15(10):1753–1765.
  • Oggioni MR, Memmi G, Maggi T, et al. Pneumococcal zinc metalloproteinase ZmpC cleaves human matrix metalloproteinase 9 and is a virulence factor in experimental pneumonia. Mol Microbiol. 2003;49(3):795–805.
  • Yamaguchi M, Nakata M, Sumioka R, et al. Zinc metalloproteinase ZmpC suppresses experimental pneumococcal meningitis by inhibiting bacterial invasion of central nervous system. Virulence. 2017;8(8):1516–1524.
  • Chen Y, Hayashida A, Bennett AE, et al. Streptococcus pneumoniae sheds syndecan-1 ectodomains through ZmpC, a metalloproteinase virulence factor. J Biol Chem. 2007;282(1):159–167.
  • Govindarajan B, Menon BB, Spurr-Michaud S, et al. A metalloproteinase secreted by Streptococcus pneumoniae removes membrane mucin MUC16 from the epithelial glycocalyx barrier. PLoS One. 2012;7(3):e32418.
  • Andre GO, Converso TR, Politano WR, et al. Role of Streptococcus pneumoniae proteins in evasion of complement-mediated immunity. Front Microbiol. 2017;8:224.
  • Lanie JA, Ng WL, Kazmierczak KM, et al. Genome sequence of Avery’s virulent serotype 2 strain D39 of Streptococcus pneumoniae and comparison with that of unencapsulated laboratory strain R6. J Bacteriol. 2007;189(1):38–51.
  • Tettelin H, Nelson KE, Paulsen IT, et al. Complete genome sequence of a virulent isolate of Streptococcus pneumoniae. Science. 2001;293(5529):498–506.
  • Slager J, Aprianto R, Veening J-W. Deep genome annotation of the opportunistic human pathogen Streptococcus pneumoniae D39. Nucleic Acids Res. 2018;46(19):9971–9989.