CRISPR-dependent endogenous gene regulation is required for virulence in piscine Streptococcus agalactiae

References

• Jinek M, Chylinski K, Fonfara I, et al. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science. 2012;337(6096):816–821.
   PubMed Web of Science ®Google Scholar
• Makarova KS, Koonin EV. Annotation and classification of CRISPR-Cas systems. Methods Mol Biol. 2015;1311:47–75.
   PubMedGoogle Scholar
• Makarova KS, Wolf YI, Iranzo J, et al. Evolutionary classification of CRISPR-Cas systems: a burst of class 2 and derived variants. Nat Rev Microbiol. 2020;18(2):67–83.
   PubMed Web of Science ®Google Scholar
• Marraffini LA. CRISPR-Cas immunity in prokaryotes. Nature. 2015;526(7571):55–61.
   PubMed Web of Science ®Google Scholar
• Chylinski K, Le Rhun A, Charpentier E. The tracrRNA and Cas9 families of type II CRISPR-Cas immunity systems. RNA Biol. 2013;10(5):726–737.
   PubMed Web of Science ®Google Scholar
• Fonfara I, Le Rhun A, Chylinski K, et al. Phylogeny of Cas9 determines functional exchangeability of dual-RNA and Cas9 among orthologous type II CRISPR-Cas systems. Nucleic Acids Res. 2014;42(4):2577–2590.
   PubMed Web of Science ®Google Scholar
• Heidrich N, Hagmann A, Bauriedl S, et al. The CRISPR/Cas system in Neisseria meningitidis affects bacterial adhesion to human nasopharyngeal epithelial cells. RNA Biol. 2019;16(4):390–396.
   PubMed Web of Science ®Google Scholar
• Sampson TR, Saroj SD, Llewellyn AC, et al. A CRISPR/Cas system mediates bacterial innate immune evasion and virulence. Nature. 2013;497(7448):254–257.
   PubMed Web of Science ®Google Scholar
• Heussler GE, Cady KC, Koeppen K, et al. Clustered regularly interspaced short palindromic repeat-dependent, biofilm-specific death of Pseudomonas aeruginosa mediated by increased expression of phage-related genes. mBio. 2015;6(3):e00129–15.
   PubMed Web of Science ®Google Scholar
• Li R, Fang L, Tan S, et al. Type I CRISPR-Cas targets endogenous genes and regulates virulence to evade mammalian host immunity. Cell Res. 2016;26(12):1273–1287.
   PubMed Web of Science ®Google Scholar
• Robinson JA, Meyer FP. Streptococcal fish pathogen. J Bacteriol. 1966;92(2):512.
   Web of Science ®Google Scholar
• Eldar A, Bejerano Y, Livoff A, et al. Experimental streptococcal meningo-encephalitis in cultured fish. Vet Microbiol. 1995;43(1):33–40.
   Web of Science ®Google Scholar
• Evans JJ, Klesius PH, Pasnik DJ, et al. Human Streptococcus agalactiae isolate in Nile tilapia (Oreochromis niloticus). Emerg Infect Dis. 2009;15(5):774–776.
   Web of Science ®Google Scholar
• Lopez-Sanchez MJ, Sauvage E, Da Cunha V, et al. The highly dynamic CRISPR1 system of Streptococcus agalactiae controls the diversity of its mobilome. Mol Microbiol. 2012;85(6):1057–1071.
   Web of Science ®Google Scholar
• Lier C, Baticle E, Horvath P, et al. Analysis of the type II-A CRISPR-Cas system of Streptococcus agalactiae reveals distinctive features according to genetic lineages. Front Genet. 2015;6:214.
   Web of Science ®Google Scholar
• Liu G, Zhang W, Lu C. Complete genome sequence of Streptococcus agalactiae GD201008-001, isolated In China from tilapia with meningoencephalitis. J Bacteriol. 2012;194(23):6653.
   PubMed Web of Science ®Google Scholar
• Ma K, Cao Q, Luo S, et al. Cas9 enhances bacterial virulence by repressing the regR transcriptional regulator in Streptococcus agalactiae. Infect Immun. 2018;86(3):e00552–17.
   Web of Science ®Google Scholar
• Takamatsu D, Osaki M, Sekizaki T. Thermosensitive suicide vectors for gene replacement in Streptococcus suis. Plasmid. 2001;46(2):140–148.
   PubMed Web of Science ®Google Scholar
• Levican A, Alkeskas A, Gunter C, et al. Adherence to and invasion of human intestinal cells by Arcobacter species and their virulence genotypes. Appl Environ Microbiol. 2013;79(16):4951–4957.
   Web of Science ®Google Scholar
• Chabot-Roy G, Willson P, Segura M, et al. Phagocytosis and killing of Streptococcus suis by porcine neutrophils. Microb Pathog. 2006;41(1):21–32.
   PubMed Web of Science ®Google Scholar
• Westerfield M. The Zebrafish Book. A guide for the laboratory use of zebrafish (Danio rerio). 2000.
   Google Scholar
• Dong Y, Geng J, Liu J, et al. Roles of three TonB systems in the iron utilization and virulence of the Aeromonas hydrophila Chinese epidemic strain NJ-35. Appl Microbiol Biotechnol. 2019 May;103(10):4203–4215.
   Web of Science ®Google Scholar
• Luo S, Cao Q, Ma K, et al. Quantitative assessment of the blood-brain barrier opening caused by Streptococcus agalactiae hyaluronidase in a BALB/c mouse model. Sci Rep. 2017;7(1):13529.
   Google Scholar
• Wang Z, Guo C, Xu Y, et al. Two novel functions of hyaluronidase from Streptococcus agalactiae are enhanced intracellular survival and inhibition of proinflammatory cytokine expression. Infect Immun. 2014;82(6):2615–2625.
   PubMed Web of Science ®Google Scholar
• Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods. 2001;25(4):402–408.
   PubMed Web of Science ®Google Scholar
• Nizet V, Gibson RL, Chi EY, et al. Group B streptococcal beta-hemolysin expression is associated with injury of lung epithelial cells. Infect Immun. 1996;64(9):3818–3826.
   Web of Science ®Google Scholar
• Lembo A, Gurney MA, Burnside K, et al. Regulation of CovR expression in Group B Streptococcus impacts blood-brain barrier penetration. Mol Microbiol. 2010;77(2):431–433.
   Web of Science ®Google Scholar
• Patras KA, Wang NY, Fletcher EM, et al. Group B Streptococcus CovR regulation modulates host immune signalling pathways to promote vaginal colonization. Cell Microbiol. 2013;15(7):1154–1167.
   Web of Science ®Google Scholar
• Rajagopal L, Vo A, Silvestroni A, et al. Regulation of cytotoxin expression by converging eukaryotic-type and two-component signalling mechanisms in Streptococcus agalactiae. Mol Microbiol. 2006;62(4):941–957.
   Web of Science ®Google Scholar
• Rosa-Fraile M, Dramsi S, Spellerberg B. Group B streptococcal haemolysin and pigment, a tale of twins. FEMS Microbiol Rev. 2014;38(5):932–946.
   Web of Science ®Google Scholar
• Liu GY, Doran KS, Lawrence T, et al. Sword and shield: linked group B streptococcal β-hemolysin/cytolysin and carotenoid pigment function to subvert host phagocyte defense. Proc Natl Acad Sci USA. 2004;101(40):14491–14496.
   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(5):736–744.
   PubMed Web of Science ®Google Scholar
• Leclercq SY, Sullivan MJ, Ipe DS, et al. Pathogenesis of Streptococcus urinary tract infection depends on bacterial strain and β-hemolysin/cytolysin that mediates cytotoxicity, cytokine synthesis, inflammation and virulence. Sci Rep. 2016;6:29000.
   PubMed Web of Science ®Google Scholar
• Aliprantis AO, Yang RB, Mark MR, et al. Cell activation and apoptosis by bacterial lipoproteins through toll-like receptor-2. Science. 1999;285(5428):736–739.
   PubMed Web of Science ®Google Scholar
• Louwen R, Staals RH, Endtz HP, et al. The role of CRISPR-Cas systems in virulence of pathogenic bacteria. Microbiol Mol Biol Rev. 2014;78(1):74–88.
   PubMed Web of Science ®Google Scholar
• Abbott NJ. Astrocyte–endothelial interactions and blood–brain barrier permeability. J Anat. 2002;200(6):629–638.
   PubMed Web of Science ®Google Scholar
• Abbott NJ, Ronnback L, Hansson E. Astrocyte-endothelial interactions at the blood-brain barrier. Nat Rev Neurosci. 2006;7(1):41–53.
   PubMed Web of Science ®Google Scholar
• Toledo-Arana A, Dussurget O, Nikitas G, et al. The Listeria transcriptional landscape from saprophytism to virulence. Nature. 2009;459:950–956.
   PubMed Web of Science ®Google Scholar
• Jiang SM, Ishmael N, Dunning Hotopp J, et al. Variation in the group B Streptococcus CsrRS regulon and effects on pathogenicity. J Bacteriol. 2008;190(6):1956–1965.
   Web of Science ®Google Scholar
• Sullivan MJ, Leclercq SY, Ipe DS, et al. Effect of the Streptococcus agalactiae virulence regulator CovR on the pathogenesis of urinary tract infection. J Infect Dis. 2017;215(3):475–483.
   Web of Science ®Google Scholar
• Jiang SM, Cieslewicz MJ, Kasper DL, et al. Regulation of virulence by a two-component system in group B streptococcus. J Bacteriol. 2005;187(3):1105–1113.
   Web of Science ®Google Scholar
• Dalrymple SA, Lucian LA, Slattery R, et al. Interleukin-6-deficient mice are highly susceptible to Listeria monocytogenes infection: correlation with inefficient neutrophilia. Infect Immun. 1995;63(6):2262–2268.
   PubMed Web of Science ®Google Scholar
• Williams DM, Grubbs BG, Darville T, et al. A role for interleukin-6 in host defense against murine Chlamydia trachomatis infection. Infect Immun. 1998;66(9):4564–4567.
   Web of Science ®Google Scholar
• Dalrymple SA, Slattery R, Aud DM, et al. Interleukin-6 is required for a protective immune response to systemic Escherichia coli infection. Infect Immun. 1996;64(8):3231–3235.
   PubMed Web of Science ®Google Scholar