Competence-induced protein Ccs4 facilitates pneumococcal invasion into brain tissue and virulence in meningitis

References

• van de Beek D, de Gans J, Spanjaard L, et al. Clinical features and prognostic factors in adults with bacterial meningitis. N Engl J Med. 2004;351:1849–1859.
   PubMed Web of Science ®Google Scholar
• van der Poll T, Opal SM. Pathogenesis, treatment, and prevention of pneumococcal pneumonia. Lancet. 2009;374:1543–1556.
   PubMed Web of Science ®Google Scholar
• Brouwer MC, Tunkel AR, van de Beek D. Epidemiology, diagnosis, and antimicrobial treatment of acute bacterial meningitis. Clin Microbiol Rev. 2010;23:467–492.
   PubMed Web of Science ®Google Scholar
• Hoogman M, van de Beek D, Weisfelt M, et al. Cognitive outcome in adults after bacterial meningitis. J Neurol Neurosurg Psychiatry. 2007;78:1092–1096.
   PubMed Web of Science ®Google Scholar
• Orihuela CJ, Mahdavi J, Thornton J, et al. Laminin receptor initiates bacterial contact with the blood brain barrier in experimental meningitis models. J Clin Invest. 2009;119:1638–1646.
   PubMed Web of Science ®Google Scholar
• Ring A, Jn W, Ei T. Pneumococcal trafficking across the blood-brain barrier. Molecular analysis of a novel bidirectional pathway. J Clin Invest. 1998;102:347–360.
   PubMed Web of Science ®Google Scholar
• Uchiyama S, Carlin AF, Khosravi A, et al. The surface-anchored NanA protein promotes pneumococcal brain endothelial cell invasion. J Exp Med. 2009;206:1845–1852.
   PubMed Web of Science ®Google Scholar
• Chang YC, Uchiyama S, Varki A, et al. Leukocyte inflammatory responses provoked by pneumococcal sialidase. MBio. 2012;3:e00220–11.
   PubMed Web of Science ®Google Scholar
• Banerjee A, Van Sorge NM, Sheen TR, et al. Activation of brain endothelium by pneumococcal neuraminidase NanA promotes bacterial internalization. Cell Microbiol. 2010;12:1576–1588.
   PubMed Web of Science ®Google Scholar
• Iovino F, Hammarlof DL, Garriss G, et al. Pneumococcal meningitis is promoted by single cocci expressing pilus adhesin RrgA. J Clin Invest. 2016;126:2821–2826.
   PubMed Web of Science ®Google Scholar
• Iovino F, Engelen-Lee JY, Brouwer M, et al. pIgR and PECAM-1 bind to pneumococcal adhesins RrgA and PspC mediating bacterial brain invasion. J Exp Med. 2017;214:1619–1630.
   PubMed Web of Science ®Google Scholar
• Yamaguchi M, Nakata M, Sumioka R, et al. Zinc metalloproteinase ZmpC suppresses experimental pneumococcal meningitis by inhibiting bacterial invasion of central nervous systems. Virulence. 2017;8:1516–1524.
   PubMed Web of Science ®Google Scholar
• Havarstein 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;92:11140–11144.
   PubMed Web of Science ®Google Scholar
• Oggioni MR, Trappetti C, Kadioglu A, et al. Switch from planktonic to sessile life: a major event in pneumococcal pathogenesis. Mol Microbiol. 2006;61:1196–1210.
   PubMed Web of Science ®Google Scholar
• Peterson S, Cline RT, Tettelin H, et al. Gene expression analysis of the Streptococcus pneumoniae competence regulons by use of DNA microarrays. J Bacteriol. 2000;182:6192–6202.
   PubMed Web of Science ®Google Scholar
• Aprianto R, Slager J, Holsappel S, et al. Time-resolved dual RNA-seq reveals extensive rewiring of lung epithelial and pneumococcal transcriptomes during early infection. Genome Biol. 2016;17:198.
   PubMed Web of Science ®Google Scholar
• Orihuela CJ, Radin JN, Sublett JE, et al. Microarray analysis of pneumococcal gene expression during invasive disease. Infect Immun. 2004;72:5582–5596.
   PubMed Web of Science ®Google Scholar
• Serruto D, Spadafina T, Ciucchi L, et al. Neisseria meningitidis GNA2132, a heparin-binding protein that induces protective immunity in humans. Proc Natl Acad Sci U S A. 2010;107:3770–3775.
   PubMed Web of Science ®Google Scholar
• Chang YC, Wang Z, Flax LA, et al. Glycosaminoglycan binding facilitates entry of a bacterial pathogen into central nervous systems. PLoS Pathog. 2011;7:e1002082.
   PubMed Web of Science ®Google Scholar
• Meneghetti MC, Hughes AJ, Rudd TR, et al. Heparan sulfate and heparin interactions with proteins. J R Soc Interface. 2015;12:0589.
   PubMed Web of Science ®Google Scholar
• Peschel A, Sahl HG. The co-evolution of host cationic antimicrobial peptides and microbial resistance. Nat Rev Microbiol. 2006;4:529–536.
   PubMed Web of Science ®Google Scholar
• Dando SJ, Mackay-Sim A, Norton R, et al. Pathogens penetrating the central nervous system: infection pathways and the cellular and molecular mechanisms of invasion. Clin Microbiol Rev. 2014;27:691–726.
   PubMed Web of Science ®Google Scholar
• Martin B, Prudhomme M, Alloing G, et al. Cross-regulation of competence pheromone production and export in the early control of transformation in Streptococcus pneumoniae. Mol Microbiol. 2000;38:867–878.
   PubMed Web of Science ®Google Scholar
• Mortier-Barriere I, de Saizieu A, Claverys JP, et al. Competence-specific induction of recA is required for full recombination proficiency during transformation in Streptococcus pneumoniae. Mol Microbiol. 1998;27:159–170.
   PubMed Web of Science ®Google Scholar
• Zhu L, Lin J, Kuang Z, et al. Deletion analysis of Streptococcus pneumoniae late competence genes distinguishes virulence determinants that are dependent or independent of competence induction. Mol Microbiol. 2015;97:151–165.
   PubMed Web of Science ®Google Scholar
• Doran KS, Liu GY, Nizet V. Group B streptococcal β-hemolysin/cytolysin activates neutrophil signaling pathways in brain endothelium and contributes to development of meningitis. J Clin Invest. 2003;112:736–744.
   PubMed Web of Science ®Google Scholar
• Kim KS. Mechanisms of microbial traversal of the blood–brain barrier. Nat Rev Microbiol. 2008;6:625–634.
   PubMed Web of Science ®Google Scholar
• Barichello T, Generoso JS, Simoes LR, et al. Role of oxidative stress in the pathophysiology of pneumococcal meningitis. Oxid Med Cell Longev. 2013;2013:371465.
   PubMed Web of Science ®Google Scholar
• Sarrazin S, Lamanna WC, Esko JD. Heparan sulfate proteoglycans. Cold Spring Harb Perspect Biol. 2011;3:a004952.
   PubMed Web of Science ®Google Scholar
• Esko JD, Kimata K, Lindahl U, et al. Chapter 16. Proteoglycans and sulfated glycosaminoglycans. In: Varki A, Cummings RD, Esko JD, et al., editors. Essentials of glycobiology. Plainview, NY: Cold Spring Harbor Laboratory Press; 2009;16:229–248.
   Google Scholar
• Maruvada R, Kim KS. Extracellular loops of the Eschericia coli outer membrane protein A contribute to the pathogenesis of meningitis. J Infect Dis. 2011;203:131–140.
   PubMed Web of Science ®Google Scholar
• Wang Y, Huang SH, Wass CA, et al. The gene locus yijP contributes to Escherichia coli K1 invasion of brain microvascular endothelial cells. Infect Immun. 1999;67:4751–4756.
   PubMed Web of Science ®Google Scholar
• Pautsch A, Schulz GE. Structure of the outer membrane protein A transmembrane domain. Nat Struct Biol. 1998;5:1013–1017.
   PubMedGoogle Scholar
• Hammerschmidt S, Wolff S, Hocke A, et al. Illustration of pneumococcal polysaccharide capsule during adherence and invasion of epithelial cells. Infect Immun. 2005;73:4653–4667.
   PubMed Web of Science ®Google Scholar
• Kietzman CC, Gao G, Mann B, et al. Dynamic capsule restructuring by the main pneumococcal autolysin LytA in response to the epithelium. Nat Commun. 2016;7:10859.
   PubMed Web of Science ®Google Scholar
• Howard LV, Gooder H. Specificity of the autolysin of Streptococcus (Diplococcus) pneumoniae. J Bacteriol. 1974;117:796–804.
   PubMed Web of Science ®Google Scholar
• Fernebro J, Andersson I, Sublett J, et al. Capsular expression in Streptococcus pneumoniae negatively affects spontaneous and antibiotic-induced lysis and contributes to antibiotic tolerance. J Infect Dis. 2004;189:328–338.
   PubMed Web of Science ®Google Scholar
• Henriques Normark B, Normark S. Antibiotic tolerance in pneumococci. Clin Microbiol Infect. 2002;8:613–622.
   PubMed Web of Science ®Google Scholar
• Lopez R, Garcia E. Recent trends on the molecular biology of pneumococcal capsules, lytic enzymes, and bacteriophage. FEMS Microbiol Rev. 2004;28:553–580.
   PubMed Web of Science ®Google Scholar
• Regev-Yochay G, Trzcinski K, Thompson CM, et al. SpxB is a suicide gene of Streptococcus pneumoniae and confers a selective advantage in an in vivo competitive colonization model. J Bacteriol. 2007;189:6532–6539.
   PubMed Web of Science ®Google Scholar
• Dejana E, Tournier-Lasserve E, Weinstein BM. The control of vascular integrity by endothelial cell junctions: molecular basis and pathological implications. Dev Cell. 2009;16:209–221.
   PubMed Web of Science ®Google Scholar
• Yancopoulos GD, Davis S, Gale NW, et al. Vascular-specific growth factors and blood vessel formation. Nature. 2000;407:242–248.
   PubMed Web of Science ®Google Scholar
• Frerking I, Gunther A, Seeger W, et al. Pulmonary surfactant: functions, abnormalities and therapeutic options. Intensive Care Med. 2001;27:1699–1717.
   PubMed Web of Science ®Google Scholar
• Vaporidi K, Tsatsanis C, Georgopoulos D, et al. Effects of hypoxia and hypercapnia on surfactant protein expression proliferation and apoptosis in A549 alveolar epithelial cells. Life Sci. 2005;78:284–293.
   PubMed Web of Science ®Google Scholar
• Peterson SN, Sung CK, Cline R, et al. Identification of competence pheromone responsive genes in Streptococcus pneumoniae by use of DNA microarrays. Mol Microbiol. 2004;51:1051–1070.
   PubMed Web of Science ®Google Scholar
• Lin J, Zhu L, Lau GW. Disentangling competence for genetic transformation and virulence in Streptococcus pneumoniae. Curr Genet. 2016;62:97–103.
   PubMed Web of Science ®Google Scholar
• Kilian M, Riley DR, Jensen A, et al. Parallel evolution of Streptococcus pneumoniae and Streptococcus mitis to pathogenic and mutualistic lifestyles. MBio. 2014;5:e01490–14.
   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;185:1208–1217.
   PubMed Web of Science ®Google Scholar
• Yamaguchi M, Minamide Y, Terao Y, et al. Nrc of Streptococcus pneumoniae suppresses capsule expression and enhances anti-phagocytosis. Biochem Biophys Res Commun. 2009;390:155–160.
   PubMed Web of Science ®Google Scholar
• Mori Y, Yamaguchi M, Terao Y, et al. α-Enolase of Streptococcus pneumoniae induces formation of neutrophil extracellular traps. J Biol Chem. 2012;287:10472–10481.
   PubMed Web of Science ®Google Scholar
• Bricker AL, Camilli A. Transformation of a type 4 encapsulated strain of Streptococcus pneumoniae. FEMS Microbiol Lett. 1999;172:131–135.
   PubMed Web of Science ®Google Scholar
• Yamaguchi M, Terao Y, Ogawa T, et al. Role of Streptococcus sanguinis sortase A in bacterial colonization. Microbes Infect. 2006;8:2791–2796.
   PubMed Web of Science ®Google Scholar
• Yamaguchi M, Hirose Y, Nakata M, et al. Evolutionary inactivation of a sialidase in group B Streptococcus. Sci Rep. 2016;6:28852.
   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;283:36272–36279.
   PubMed Web of Science ®Google Scholar
• Lancefield RC. Differentiation of group A streptococci with a common R antigen into three serological types, with special reference to the bactericidal test. J Exp Med. 1957;106:525–544.
   PubMed Web of Science ®Google Scholar
• Isaka M, Tatsuno I, Maeyama J, et al. The YvqE two-component system controls biofilm formation and acid production in Streptococcus pyogenes. APMIS. 2016;124:574–585.
   PubMed Web of Science ®Google Scholar
• Okumura CY, Anderson EL, Dohrmann S, et al. IgG protease Mac/IdeS is not essential for phagocyte resistance or mouse virulence of M1T1 group A Streptococcus. MBio. 2013;4:e00499–13.
   PubMed Web of Science ®Google Scholar
• Dohrmann S, LaRock CN, Anderson EL, et al. Group a streptococcal M1 protein provides resistance against the antimicrobial activity of histones. Sci Rep. 2017;7:43039.
   PubMed Web of Science ®Google Scholar