Targeting the type III secretion system to treat bacterial infections

Bibliography

• Clatworthy A, Pierson E, Hung D. Targeting virulence: a new paradigm for antimicrobial therapy. Nat Chem Biol 2007;3:541-8
   PubMed Web of Science ®Google Scholar
• Watanabe T. Infective heredity of multiple drug resistance in bacteria. Bacteriol Rev 1963;27:87-115
   PubMedGoogle Scholar
• Jabes D. The antibiotic R&D pipeline: an update. Curr Opin Microbiol 2011;14:564-9
   PubMed Web of Science ®Google Scholar
• Lautenbach E, Polk R. Resistant gram-negative bacilli: a neglected healthcare crisis? Am J Health Syst Pharm 2007;64:S3-21. quiz S22
   Google Scholar
• Coates A, Halls G. Antibiotics in Phase II and III clinical trials. Handb Exp Pharmacol 2012;211:167-83
   Google Scholar
• Keyser P, Elofsson M, Rosell S, Wolf-Watz H. Virulence blockers as alternatives to antibiotics: type III secretion inhibitors against Gram-negative bacteria. J Intern Med 2008;264:17-29
   PubMed Web of Science ®Google Scholar
• Chang J, Antonopoulos D, Kalra A, et al. Decreased diversity of the fecal microbiome in recurrent Clostridium difficile-associated diarrhea. J Infect Dis 2008;197:435-8
   PubMed Web of Science ®Google Scholar
• Sekirov I, Russell S, Antunes L, Finlay B. Gut microbiota in health and disease. Physiol Rev 2010;90:859-904
   PubMed Web of Science ®Google Scholar
• Von Behring E, Kitasato S. On the acquisition of immunity against diptheria and tetanus in animals. Dtsch Med Wochensch 1890;16:1145-8
   Google Scholar
• Büttner D. Protein export according to schedule: architecture, assembly, and regulation of type III secretion systems from plant- and animal-pathogenic bacteria. Microbiol Mol Biol Rev 2012;76:262-310
   PubMed Web of Science ®Google Scholar
• Cornelis G. The type III secretion injectisome. Nat Rev Microbiol 2006;4:811-25
   PubMed Web of Science ®Google Scholar
• Zhou D, Galán J. Salmonella entry into host cells: the work in concert of type III secreted effector proteins. Microbes Infect Inst Pasteur 2001;3:1293-8
   PubMed Web of Science ®Google Scholar
• Collier-Hyams L, Zeng H, Sun J, et al. Cutting edge: salmonella AvrA effector inhibits the key proinflammatory, anti-apoptotic NF-kappa B pathway. J Immunol Baltim Md 1950;169:2846-50
   Google Scholar
• Holmes A, Mühlen S, Roe AJ, Dean P. The EspF effector, a bacterial pathogen's Swiss army knife. Infect Immun 2010;78:4445-53
   PubMed Web of Science ®Google Scholar
• Kim D, Lenzen G, Page A-L, et al. The Shigella flexneri effector OspG interferes with innate immune responses by targeting ubiquitin-conjugating enzymes. Proc Natl Acad Sci USA 2005;102:14046-51
   PubMed Web of Science ®Google Scholar
• Swietnicki W, Carmany D, Retford M, et al. Identification of small-molecule inhibitors of Yersinia pestis type III secretion system YscN ATPase. PLoS ONE 2011;6:e19716
   PubMedGoogle Scholar
• Gauthier A, Robertson M, Lowden M, et al. Transcriptional inhibitor of virulence factors in enteropathogenic Escherichia coli. Antimicrob Agents Chemother 2005;49:4101-9
   PubMed Web of Science ®Google Scholar
• Perry R, Fetherston J. Yersinia pestis–etiologic agent of plague. Clin Microbiol Rev 1997;10:35-66
   PubMed Web of Science ®Google Scholar
• Galindo C, Rosenzweig J, Kirtley M, Chopra A. Pathogenesis of Y. enterocolitica and Y. pseudotuberculosis in human Yersiniosis. J Pathog 2011;2011:182051
   PubMedGoogle Scholar
• Majowicz S, Musto J, Scallan E, et al. The global burden of nontyphoidal Salmonella gastroenteritis. Clin Infect Dis Off Publ Infect Dis Soc Am 2010;50:882-9
   PubMed Web of Science ®Google Scholar
• Bhutta Z, Threlfall J. Addressing the global disease burden of typhoid fever. JAMA J Am Med Assoc 2009;302:898-9
   Google Scholar
• Croxen M, Finlay B. Molecular mechanisms of Escherichia coli pathogenicity. Nat Rev Microbiol 2010;8:26-38
   PubMed Web of Science ®Google Scholar
• Smith K, Wilker P, Reiter P, et al. Antibiotic treatment of Escherichia coli O157 infection and the risk of hemolytic uremic syndrome, Minnesota. Pediatr Infect Dis J 2012;31:37-41
   Google Scholar
• Peng J, Yang J, Jin Q. Research progress in Shigella in the postgenomic era. Sci China Life Sci 2010;53:1284-90
   Google Scholar
• Grier M, Garrity-Ryan L, Bartlett V, et al. N-Hydroxybenzimidazole inhibitors of ExsA MAR transcription factor in Pseudomonas aeruginosa: in vitro anti-virulence activity and metabolic stability. Bioorg Med Chem Lett 2010;20:3380-3
   PubMed Web of Science ®Google Scholar
• Cornelis G. The type III secretion injectisome, a complex nanomachine for intracellular “toxin” delivery. Biol Chem 2010;391:745-51
   PubMedGoogle Scholar
• Sekiya K, Ohishi M, Ogino T, et al. Supermolecular structure of the enteropathogenic Escherichia coli type III secretion system and its direct interaction with the EspA-sheath-like structure. Proc Natl Acad Sci USA 2001;98:11638-43
   PubMed Web of Science ®Google Scholar
• Izoré T, Job V, Dessen A. Biogenesis, regulation, and targeting of the type III secretion system. Struct Lond Engl 1993;19:603-12
   Google Scholar
• Kubori T, Sukhan A, Aizawa S, Galán J. Molecular characterization and assembly of the needle complex of the Salmonella Typhimurium type III protein secretion system. Proc Natl Acad Sci USA 2000;97:10225-30
   PubMed Web of Science ®Google Scholar
• Pettersson J, Nordfelth R, Dubinina E, et al. Modulation of virulence factor expression by pathogen target cell contact. Science 1996;273:1231-3
   Google Scholar
• Sorg I, Wagner S, Amstutz M, et al. YscU recognizes translocators as export substrates of the Yersinia injectisome. EMBO J 2007;26:3015-24
   Google Scholar
• Deng W, Li Y, Hardwidge P, et al. Regulation of type III secretion hierarchy of translocators and effectors in attaching and effacing bacterial pathogens. Infect Immun 2005;73:2135-46
   PubMed Web of Science ®Google Scholar
• Barta M, Guragain M, Adam P, et al. Identification of the bile salt binding site on IpaD from Shigella flexneri and the influence of ligand binding on IpaD structure. Proteins 2012;80:935-45
   Google Scholar
• Akeda Y, Galán J. Chaperone release and unfolding of substrates in type III secretion. Nature 2005;437:911-15
   PubMed Web of Science ®Google Scholar
• Schlumberger M, Müller AJ, Ehrbar K, et al. Real-time imaging of type III secretion: salmonella SipA injection into host cells. Proc Natl Acad Sci USA 2005;102:12548-53
   PubMedGoogle Scholar
• Andersson K, Carballeira N, Magnusson K, et al. YopH of Yersinia pseudotuberculosis interrupts early phosphotyrosine signalling associated with phagocytosis. Mol Microbiol 1996;20:1057-69
   PubMed Web of Science ®Google Scholar
• Lee P-C, Stopford C, Svenson A, Rietsch A. Control of effector export by the Pseudomonas aeruginosa type III secretion proteins PcrG and PcrV. Mol Microbiol 2010;75:924-41
   Google Scholar
• Veenendaal A, Hodgkinson J, Schwarzer L, et al. The type III secretion system needle tip complex mediates host cell sensing and translocon insertion. Mol Microbiol 2007;63:1719-30
   PubMed Web of Science ®Google Scholar
• Chen Y, Anderson D. Expression hierarchy in the Yersinia type III secretion system established through YopD recognition of RNA. Mol Microbiol 2011;80:966-80
   Google Scholar
• Anderson D, Ramamurthi K, Tam C, Schneewind O. YopD and LcrH regulate expression of Yersinia enterocolitica YopQ by a posttranscriptional mechanism and bind to yopQ RNA. J Bacteriol 2002;184:1287-95
   Google Scholar
• Cambronne E, Schneewind O. Yersinia enterocolitica type III secretion: yscM1 and yscM2 regulate yop gene expression by a posttranscriptional mechanism that targets the 5' untranslated region of yop mRNA. J Bacteriol 2002;184:5880-93
   Google Scholar
• Kauppi A, Nordfelth R, Uvell H, et al. Targeting bacterial virulence: inhibitors of type III secretion in Yersinia. Chem Biol 2003;10:241-9
   PubMed Web of Science ®Google Scholar
• Pan N, Brady M, Leong J, Goguen J. Targeting type III secretion in Yersinia pestis. Antimicrob Agents Chemother 2009;53:385-92
   PubMed Web of Science ®Google Scholar
• Felise H, Nguyen H, Pfuetzner R, et al. An inhibitor of gram-negative bacterial virulence protein secretion. Cell Host Microbe 2008;4:325-36
   PubMed Web of Science ®Google Scholar
• Linington R, Robertson M, Gauthier A, et al. Caminoside A, an antimicrobial glycolipid isolated from the marine sponge Caminus sphaeroconia. Org Lett 2002;4:4089-92
   PubMed Web of Science ®Google Scholar
• Michiels T, Wattiau P, Brasseur R, et al. Secretion of Yop proteins by Yersiniae. Infect Immun 1990;58:2840-9
   PubMed Web of Science ®Google Scholar
• Li X, Kang F, Macielag M. Triazine compounds as inhibitors of bacterial type III protein secretion systems. WO 2005111017 A1; 2005
   Google Scholar
• Yount J, Tsou L, Dossa P, et al. Visible fluorescence detection of type III protein secretion from bacterial pathogens. J Am Chem Soc 2010;132:8244-5
   Google Scholar
• Van Engelenburg S, Palmer A. Imaging type-III secretion reveals dynamics and spatial segregation of Salmonella effectors. Nat Methods 2010;7:325-30
   PubMed Web of Science ®Google Scholar
• Van Engelenburg S, Palmer A. Quantification of real-time Salmonella effector type III secretion kinetics reveals differential secretion rates for SopE2 and SptP. Chem Biol 2008;15:619-28
   Google Scholar
• Enninga J, Mounier J, Sansonetti P, Tran Van Nhieu G. Secretion of type III effectors into host cells in real time. Nat Methods 2005;2:959-65
   PubMed Web of Science ®Google Scholar
• Tsou L, Dossa P, Hang H. Small molecules aimed at type III secretion systems to inhibit bacterial virulence. Med Chem Comm 2013;4:68-79
   Google Scholar
• Li J, Lv C, Sun W, et al. Cytosporone B, an inhibitor of the type III secretion system of Salmonella enterica serovar Typhimurium. Antimicrob Agents Chemother 2013;57:2191-8
   PubMed Web of Science ®Google Scholar
• Kimura K, Iwatsuki M, Nagai T, et al. A small-molecule inhibitor of the bacterial type III secretion system protects against in vivo infection with Citrobacter rodentium. J Antibiot (Tokyo) 2011;64:197-203
   PubMed Web of Science ®Google Scholar
• Vikram A, Jayaprakasha G, Jesudhasan P, et al. Suppression of bacterial cell-cell signalling, biofilm formation and type III secretion system by citrus flavonoids. J Appl Microbiol 2010;109:515-27
   PubMed Web of Science ®Google Scholar
• Willing B, Antunes L, Keeney K, et al. Harvesting the biological potential of the human gut microbiome. BioEssays News Rev Mol Cell Dev Biol 2011;33:414-18
   Google Scholar
• Gallegos M, Schleif R, Bairoch A, et al. Arac/XylS family of transcriptional regulators. Microbiol Mol Biol Rev MMBR 1997;61:393-410
   PubMed Web of Science ®Google Scholar
• Garrity-Ryan L, Kim O, Balada-Llasat J-M, et al. Small molecule inhibitors of LcrF, a Yersinia pseudotuberculosis transcription factor, attenuate virulence and limit infection in a murine pneumonia model. Infect Immun 2010;78:4683-90
   PubMed Web of Science ®Google Scholar
• Ozawa I, Takeuchi I, Yamamoto K, et al. Synthesis and antimicrobial activity of salicylanilide derivatives. II. Chem Pharm Bull (Tokyo) 1984;32:305-12
   Google Scholar
• Bowser T, Bartlett V, Grier M, et al. Novel anti-infection agents: small-molecule inhibitors of bacterial transcription factors. Bioorg Med Chem Lett 2007;17:5652-5
   PubMed Web of Science ®Google Scholar
• Kim O, Garrity-Ryan L, Bartlett V, et al. N-hydroxybenzimidazole inhibitors of the transcription factor LcrF in Yersinia: novel antivirulence agents. J Med Chem 2009;52:5626-34
   PubMed Web of Science ®Google Scholar
• Dahlgren M, Kauppi A, Olsson I-M, et al. Design, synthesis, and multivariate quantitative structure-activity relationship of salicylanilides–potent inhibitors of type III secretion in Yersinia. J Med Chem 2007;50:6177-88
   PubMed Web of Science ®Google Scholar
• Chène P. AT Pases as drug targets: learning from their structure. Nat Rev Drug Discov 2002;1:665-73
   PubMed Web of Science ®Google Scholar
• Hilleringmann M, Pansegrau W, Doyle M, et al. Inhibitors of Helicobacter pylori ATPase Cagalpha block CagA transport and cag virulence. Microbiol Read Engl 2006;152:2919-30
   Google Scholar
• Young G, Schmiel D, Miller V. A new pathway for the secretion of virulence factors by bacteria: the flagellar export apparatus functions as a protein-secretion system. Proc Natl Acad Sci USA 1999;96:6456-61
   PubMed Web of Science ®Google Scholar
• Vijay-Kumar M, Aitken J, Carvalho F, et al. Metabolic syndrome and altered gut microbiota in mice lacking Toll-like receptor 5. Science 2010;328:228-31
   PubMed Web of Science ®Google Scholar
• Kline T, Felise H, Barry K, et al. Substituted 2-imino-5-arylidenethiazolidin-4-one inhibitors of bacterial type III secretion. J Med Chem 2008;51:7065-74
   PubMed Web of Science ®Google Scholar
• Veenendaal A, Sundin C, Blocker A. Small-molecule type III secretion system inhibitors block assembly of the Shigella type III secreton. J Bacteriol 2009;191:563-70
   PubMed Web of Science ®Google Scholar
• Larzábal M, Mercado E, Vilte D, et al. Designed coiled-coil peptides inhibit the type three secretion system of enteropathogenic Escherichia coli. PLoS ONE 2010;5:e9046
   PubMed Web of Science ®Google Scholar
• Larzábal M, Zotta E, Ibarra C, et al. Effect of coiled-coil peptides on the function of the type III secretion system-dependent activity of enterohemorrhagic Escherichia coli O157:H7 and Citrobacter rodentium. Int J Med Microbiol IJMM 2013;303:9-15
   PubMed Web of Science ®Google Scholar
• Goure J, Broz P, Attree O, et al. Protective anti-V antibodies inhibit Pseudomonas and Yersinia translocon assembly within host membranes. J Infect Dis 2005;192:218-25
   PubMed Web of Science ®Google Scholar
• Heath D, Anderson G, Mauro J, et al. Protection against experimental bubonic and pneumonic plague by a recombinant capsular F1-V antigen fusion protein vaccine. Vaccine 1998;16:1131-7
   PubMed Web of Science ®Google Scholar
• Sawa T, Yahr T, Ohara M, et al. Active and passive immunization with the Pseudomonas V antigen protects against type III intoxication and lung injury. Nat Med 1999;5:392-8
   PubMed Web of Science ®Google Scholar
• Shime N, Sawa T, Fujimoto J, et al. Therapeutic administration of anti-PcrV F(ab')(2) in sepsis associated with Pseudomonas aeruginosa. J Immunol Baltim Md 1950;167:5880-6
   Google Scholar
• François B, Luyt C-E, Dugard A, et al. Safety and pharmacokinetics of an anti-PcrV PEGylated monoclonal antibody fragment in mechanically ventilated patients colonized with Pseudomonas aeruginosa: a randomized, double-blind, placebo-controlled trial. Crit Care Med 2012;40:2320-6
   PubMed Web of Science ®Google Scholar
• Clinical Trials. Study to Evaluate the Effect of KB001-A on Time-to-Need for Antibiotic Treatment. US National Institutes of Health, Bethesda, MD. Available from: http://clinicaltrials.gov/ct2/show/NCT01695343 [Last accessed 28 August 2013]
   Google Scholar
• Surnamexu G, Surnameduggineni G, Surnameespitia G, et al. A synthetic bivalent ligand of CXCR4 inhibits HIV infection. Biochem Biophys Res Commun 2013;435:646-50
   Google Scholar
• Kenny B, DeVinney R, Stein M, et al. Enteropathogenic E. coli (EPEC) transfers its receptor for intimate adherence into mammalian cells. Cell 1997;91:511-20
   PubMed Web of Science ®Google Scholar
• Donnenberg M, Tzipori S, McKee M, et al. The role of the eae gene of enterohemorrhagic Escherichia coli in intimate attachment in vitro and in a porcine model. J Clin Invest 1993;92:1418-24
   PubMedGoogle Scholar
• Harmon D, Davis A, Castillo C, Mecsas J. Identification and characterization of small-molecule inhibitors of Yop translocation in Yersinia pseudotuberculosis. Antimicrob Agents Chemother 2010;54:3241-54
   PubMed Web of Science ®Google Scholar
• Bliska J, Copass M, Falkow S. The Yersinia pseudotuberculosis adhesin YadA mediates intimate bacterial attachment to and entry into HEp-2 cells. Infect Immun 1993;61:3914-21
   Google Scholar
• Hudson D, Layton A, Field T, et al. Inhibition of type III secretion in Salmonella enterica serovar Typhimurium by small-molecule inhibitors. Antimicrob Agents Chemother 2007;51:2631-5
   PubMed Web of Science ®Google Scholar
• Negrea A, Bjur E, Ygberg S, et al. Salicylidene acylhydrazides that affect type III protein secretion in Salmonella enterica serovar typhimurium. Antimicrob Agents Chemother 2007;51:2867-76
   PubMed Web of Science ®Google Scholar
• Muschiol S, Normark S, Henriques-Normark B, Subtil A. Small molecule inhibitors of the Yersinia type III secretion system impair the development of Chlamydia after entry into host cells. BMC Microbiol 2009;9:75
   PubMed Web of Science ®Google Scholar
• Slepenkin A, Enquist P-A, Hägglund U, et al. Reversal of the antichlamydial activity of putative type III secretion inhibitors by iron. Infect Immun 2007;75:3478-89
   PubMed Web of Science ®Google Scholar
• Tree J, Wang D, McInally C, et al. Characterization of the effects of salicylidene acylhydrazide compounds on type III secretion in Escherichia coli O157:H7. Infect Immun 2009;77:4209-20
   PubMed Web of Science ®Google Scholar
• Nordfelth R, Kauppi A, Norberg H, et al. Small-molecule inhibitors specifically targeting type III secretion. Infect Immun 2005;73:3104-14
   PubMed Web of Science ®Google Scholar
• Abe H, Miyahara A, Oshima T, et al. Global regulation by horizontally transferred regulators establishes the pathogenicity of Escherichia coli. DNA Res Int J Rapid Publ Rep Genes Genomes 2008;15:25-38
   Google Scholar
• Layton A, Hudson D, Thompson A, et al. Salicylidene acylhydrazide-mediated inhibition of type III secretion system-1 in Salmonella enterica serovar Typhimurium is associated with iron restriction and can be reversed by free iron. FEMS Microbiol Lett 2010;302:114-22
   PubMed Web of Science ®Google Scholar
• Gabrielsen M, Beckham KS, Feher VA, et al. Structural characterisation of Tpx from Yersinia pseudotuberculosis reveals insights into the binding of salicylidene acylhydrazide compounds. PLoS One 2012;7:e32217
   Google Scholar
• Wang D, Zetterström CE, Gabrielsen M, et al. Identification of bacterial target proteins for the salicylidene acylhydrazide class of virulence-blocking compounds. J Biol Chem 2011;286:29922-31
   PubMed Web of Science ®Google Scholar
• Martinez-Argudo I, Veenendaal A, Liu X, et al. Isolation of Salmonella mutants resistant to the inhibitory effect of Salicylidene acylhydrazides on flagella-mediated motility. PloS One 2013;8:e52179
   PubMedGoogle Scholar
• Wolf K, Betts H, Chellas-Géry B, et al. Treatment of Chlamydia trachomatis with a small molecule inhibitor of the Yersinia type III secretion system disrupts progression of the chlamydial developmental cycle. Mol Microbiol 2006;61:1543-55
   PubMed Web of Science ®Google Scholar
• Slepenkin A, Chu H, Elofsson M, et al. Protection of mice from a Chlamydia trachomatis vaginal infection using a Salicylidene acylhydrazide, a potential microbicide. J Infect Dis 2011;204:1313-20
   PubMed Web of Science ®Google Scholar
• Engström P, Nguyen BD, Normark J, et al. Mutations in hemG mediate resistance to Salicylidene acylhydrazides: a novel link between protoporphyrinogen oxidase (HemG) and Chlamydia trachomatis infectivity. J Bacteriol 2013;195:4221-30
   PubMed Web of Science ®Google Scholar
• Ochoa T, Clearly T. Lactoferrin disruption of bacterial type III secretion systems. Biometals Int J Role Met Ions Biol Biochem Med 2004;17:257-60
   Google Scholar
• Mahmood F, Hakimiyan A, Jayaraman V, et al. A novel human antimicrobial factor targets Pseudomonas aeruginosa through its type III secretion system. J Med Microbiol 2013;62:531-9
   PubMedGoogle Scholar
• Cantón R, Lumb J. Emerging resistance in Gram-negative pathogens and implications for clinical practice. Future Microbiol 2011;6:19-22
   Google Scholar
• Bergeron J, Worrall L, Sgourakis N, et al. A refined model of the prototypical Salmonella SPI-1 T3SS basal body reveals the molecular basis for its assembly. PLoS Pathog 2013;9:e1003307
   Google Scholar
• Marlovits T, Kubori T, Sukhan A, et al. Structural insights into the assembly of the type III secretion needle complex. Science 2004;306:1040-2
   PubMed Web of Science ®Google Scholar
• Schraidt O, Marlovits T. Three-dimensional model of Salmonella's needle complex at subnanometer resolution. Science 2011;331:1192-5
   Google Scholar
• Dewoody R, Merritt P, Marketon M. Regulation of the Yersinia type III secretion system: traffic control. Front Cell Infect Microbiol 2013;3:4
   Google Scholar
• Berger C, Crepin V, Baruch K, et al. EspZ of enteropathogenic and enterohemorrhagic Escherichia coli regulates type III secretion system protein translocation. mBio 2012;3:e00317-12
   Google Scholar
• Huang Z, Sutton S, Wallenfang A, et al. Structural insights into host GTPase isoform selection by a family of bacterial GEF mimics. Nat Struct Mol Biol 2009;16:853-60
   PubMed Web of Science ®Google Scholar
• Heine S, Diaz-McNair J, Martinez-Becerra F, et al. Evaluation of immunogenicity and protective efficacy of orally delivered Shigella type III secretion system proteins IpaB and IpaD. Vaccine 2013;31:2919-29
   PubMed Web of Science ®Google Scholar
• Potter A, Klashinsky S, Li Y, et al. Decreased shedding of Escherichia coli O157:H7 by cattle following vaccination with type III secreted proteins. Vaccine 2004;22:362-9
   PubMed Web of Science ®Google Scholar
• Worrall L, Bergeron J, Strynadka N. Chapter 14 - Type 3 secretion systems. In: Donnenberg M, editor. Escherichia coli: Pathotypes and principles of pathogenesis. 2nd revised edition. Academic Press, Salt Lake City, Utah. Elsevier Science & Technology Books 2013. p. 417-50
   Google Scholar
• Yang J, Hocking DM, Cheng C, et al. Disarming bacterial virulence through chemical inhibition of the DNA-binding domain of an AraC-like transcriptional activator. J Biol Chem 2013; doi:10.1074/jbc.M113.503912
   Google Scholar