The Hcp proteins fused with diverse extended-toxin domains represent a novel pattern of antibacterial effectors in type VI secretion systems

References

• Hayes CS, Aoki SK, Low DA. Bacterial contact-dependent delivery systems. Ann Rev Genet 2010; 44:71-90; PMID:21047256; http://dx.doi.org/10.1146/annurev.genet.42.110807.091449
   PubMed Web of Science ®Google Scholar
• Konovalova A, Sogaard-Andersen L. Close encounters: contact-dependent interactions in bacteria. Mol Microbiol 2011; 81:297-301; PMID:21651624; http://dx.doi.org/10.1111/j.1365-2958.2011.07711.x
   PubMed Web of Science ®Google Scholar
• Ho BT, Dong TG, Mekalanos JJ. A view to a kill: the bacterial type VI secretion system. Cell Host Microbe 2014; 15:9-21; http://dx.doi.org/10.1016/j.chom.2013.11.008
   PubMed Web of Science ®Google Scholar
• LeRoux M, Kirkpatrick RL, Montauti EI, Tran BQ, Peterson SB, Harding BN, Whitney JC, Russell AB, Traxler B, Goo YA, et al. Kin cell lysis is a danger signal that activates antibacterial pathways of Pseudomonas aeruginosa. eLife 2015; 4:e05701; PMID:25643398; http://dx.doi.org/10.7554/eLife.05701
   PubMed Web of Science ®Google Scholar
• Russell AB, Hood RD, Bui NK, LeRoux M, Vollmer W, Mougous JD. Type VI secretion delivers bacteriolytic effectors to target cells. Nature 2011; 475:343-7; PMID:21776080; http://dx.doi.org/10.1038/nature10244
   PubMed Web of Science ®Google Scholar
• Schwarz S, Singh P, Robertson JD, LeRoux M, Skerrett SJ, Goodlett DR, West TE, Mougous JD. VgrG-5 is a Burkholderia type VI secretion system-exported protein required for multinucleated giant cell formation and virulence. Infect Immun 2014; 82:1445-52; PMID:24452686; http://dx.doi.org/10.1128/IAI.01368-13
   PubMed Web of Science ®Google Scholar
• Sana TG, Flaugnatti N, Lugo KA, Lam LH, Jacobson A, Baylot V, Durand E, Journet L, Cascales E, Monack DM. Salmonella Typhimurium utilizes a T6SS-mediated antibacterial weapon to establish in the host gut. Proc Natl Acad Sci U S A 2016; 113:E5044-51; PMID:27503894; http://dx.doi.org/10.1073/pnas.1608858113
   PubMed Web of Science ®Google Scholar
• Hecht AL, Casterline BW, Earley ZM, Goo YA, Goodlett DR, Bubeck Wardenburg J. Strain competition restricts colonization of an enteric pathogen and prevents colitis. EMBO Rep 2016; 17:1281-91; PMID:27432285; http://dx.doi.org/10.15252/embr.201642282
   PubMed Web of Science ®Google Scholar
• Wenren LM, Sullivan NL, Cardarelli L, Septer AN, Gibbs KA. Two independent pathways for self-recognition in Proteus mirabilis are linked by type VI-dependent export. mBio 2013; 4; PMID:23882014; http://dx.doi.org/10.1128/mBio.00374-13
   PubMed Web of Science ®Google Scholar
• Unterweger D, Miyata ST, Bachmann V, Brooks TM, Mullins T, Kostiuk B, Provenzano D, Pukatzki S. The Vibrio cholerae type VI secretion system employs diverse effector modules for intraspecific competition. Nate Commun 2014; 5:3549; PMID:24686479; http://dx.doi.org/10.1038/ncomms4549
   PubMed Web of Science ®Google Scholar
• Russell AB, Singh P, Brittnacher M, Bui NK, Hood RD, Carl MA, Agnello DM, Schwarz S, Goodlett DR, Vollmer W, et al. A widespread bacterial type VI secretion effector superfamily identified using a heuristic approach. Cell Host Microbe 2012; 11:538-49; http://dx.doi.org/10.1016/j.chom.2012.04.007
   PubMed Web of Science ®Google Scholar
• Dong TG, Ho BT, Yoder-Himes DR, Mekalanos JJ. Identification of T6SS-dependent effector and immunity proteins by Tn-seq in Vibrio cholerae. Proc Natl Acad Sci U S A 2013; 110:2623-8; PMID:23362380; http://dx.doi.org/10.1073/pnas.1222783110
   PubMed Web of Science ®Google Scholar
• Salomon D, Kinch LN, Trudgian DC, Guo X, Klimko JA, Grishin NV, Mirzaei H, Orth K. Marker for type VI secretion system effectors. Proc Natl Acad Sci U S A 2014; 111:9271-6; PMID:24927539; http://dx.doi.org/10.1073/pnas.1406110111
   PubMed Web of Science ®Google Scholar
• Russell AB, LeRoux M, Hathazi K, Agnello DM, Ishikawa T, Wiggins PA, Wai SN, Mougous JD. Diverse type VI secretion phospholipases are functionally plastic antibacterial effectors. Nature 2013; 496:508-12; PMID:23552891; http://dx.doi.org/10.1038/nature12074
   PubMed Web of Science ®Google Scholar
• Whitney JC, Chou S, Russell AB, Biboy J, Gardiner TE, Ferrin MA, Brittnacher M, Vollmer W, Mougous JD. Identification, structure, and function of a novel type VI secretion peptidoglycan glycoside hydrolase effector-immunity pair. J Biol Chem 2013; 288:26616-24; PMID:23878199; http://dx.doi.org/10.1074/jbc.M113.488320
   PubMed Web of Science ®Google Scholar
• Brooks TM, Unterweger D, Bachmann V, Kostiuk B, Pukatzki S. Lytic activity of the Vibrio cholerae type VI secretion toxin VgrG-3 is inhibited by the antitoxin TsaB. J Biol Chem 2013; 288:7618-25; PMID:23341465; http://dx.doi.org/10.1074/jbc.M112.436725
   PubMed Web of Science ®Google Scholar
• Ma LS, Hachani A, Lin JS, Filloux A, Lai EM. Agrobacterium tumefaciens deploys a superfamily of type VI secretion DNase effectors as weapons for interbacterial competition in planta. Cell Host Microbe 2014; 16:94-104; http://dx.doi.org/10.1016/j.chom.2014.06.002
   PubMed Web of Science ®Google Scholar
• Whitney JC, Quentin D, Sawai S, LeRoux M, Harding BN, Ledvina HE, Tran BQ, Robinson H, Goo YA, Goodlett DR, et al. An interbacterial NAD(P)(+) glycohydrolase toxin requires elongation factor Tu for delivery to target cells. Cell 2015; 163:607-19; PMID:26456113; http://dx.doi.org/10.1016/j.cell.2015.09.027
   PubMed Web of Science ®Google Scholar
• Miyata ST, Unterweger D, Rudko SP, Pukatzki S. Dual expression profile of type VI secretion system immunity genes protects pandemic Vibrio cholerae. PLoS Pathog 2013; 9:e1003752; PMID:24348240; http://dx.doi.org/10.1371/journal.ppat.1003752
   PubMed Web of Science ®Google Scholar
• Bingle LE, Bailey CM, Pallen MJ. Type VI secretion: a beginner's guide. Curr Opin Microbiol 2008; 11:3-8; PMID:18289922; http://dx.doi.org/10.1016/j.mib.2008.01.006
   PubMed Web of Science ®Google Scholar
• Costa TR, Felisberto-Rodrigues C, Meir A, Prevost MS, Redzej A, Trokter M, Waksman G. Secretion systems in Gram-negative bacteria: structural and mechanistic insights. Nat Rev Microbiol 2015; 13:343-59; PMID:25978706; http://dx.doi.org/10.1038/nrmicro3456
   PubMed Web of Science ®Google Scholar
• Mougous JD, Cuff ME, Raunser S, Shen A, Zhou M, Gifford CA, Goodman AL, Joachimiak G, Ordoñez CL, Lory S, et al. A virulence locus of Pseudomonas aeruginosa encodes a protein secretion apparatus. Science 2006; 312:1526-30; PMID:16763151; http://dx.doi.org/10.1126/science.1128393
   PubMed Web of Science ®Google Scholar
• Silverman JM, Agnello DM, Zheng H, Andrews BT, Li M, Catalano CE, Gonen T, Mougous JD. Haemolysin coregulated protein is an exported receptor and chaperone of type VI secretion substrates. Mol Cell 2013; 51:584-93; PMID:23954347; http://dx.doi.org/10.1016/j.molcel.2013.07.025
   PubMed Web of Science ®Google Scholar
• Osipiuk J, Xu X, Cui H, Savchenko A, Edwards A, Joachimiak A. Crystal structure of secretory protein Hcp3 from Pseudomonas aeruginosa. J Struct Funct Genomics 2011; 12:21-6; PMID:21476004; http://dx.doi.org/10.1007/s10969-011-9107-1
   PubMedGoogle Scholar
• Pell LG, Kanelis V, Donaldson LW, Howell PL, Davidson AR. The phage lambda major tail protein structure reveals a common evolution for long-tailed phages and the type VI bacterial secretion system. Proc Natl Acad Sci U S A 2009; 106:4160-5; PMID:19251647; http://dx.doi.org/10.1073/pnas.0900044106
   PubMed Web of Science ®Google Scholar
• Brunet YR, Henin J, Celia H, Cascales E. Type VI secretion and bacteriophage tail tubes share a common assembly pathway. EMBO Rep 2014; 15:315-21; PMID:24488256; http://dx.doi.org/10.1002/embr.201337936
   PubMed Web of Science ®Google Scholar
• Journet L, Cascales E. The type VI secretion system in escherichia coli and related species. EcoSal Plus 2016; 7:1-20; PMID:27223818; http://dx.doi.org/10.1128/ecosalplus.ESP-0009-2015
   PubMedGoogle Scholar
• Ma J, Sun M, Bao Y, Pan Z, Zhang W, Lu C, Yao H. Genetic diversity and features analysis of type VI secretion systems loci in avian pathogenic Escherichia coli by wide genomic scanning. Infect Genet Evol 2013; 20:454-64; PMID:24120694; http://dx.doi.org/10.1016/j.meegid.2013.09.031
   PubMed Web of Science ®Google Scholar
• Ma J, Bao Y, Sun M, Dong W, Pan Z, Zhang W, Lu C, Yao H. Two functional type VI secretion systems in avian pathogenic Escherichia coli are involved in different pathogenic pathways. Infect Immun 2014; 82:3867-79; PMID:24980972; http://dx.doi.org/10.1128/IAI.01769-14
   PubMed Web of Science ®Google Scholar
• Barret M, Egan F, Fargier E, Morrissey JP, O'Gara F. Genomic analysis of the type VI secretion systems in Pseudomonas spp.: novel clusters and putative effectors uncovered. Microbiology 2011; 157:1726-39; PMID:21474537; http://dx.doi.org/10.1099/mic.0.048645-0
   PubMed Web of Science ®Google Scholar
• De Maayer P, Venter SN, Kamber T, Duffy B, Coutinho TA, Smits TH. Comparative genomics of the Type VI secretion systems of Pantoea and Erwinia species reveals the presence of putative effector islands that may be translocated by the VgrG and Hcp proteins. BMC Genomics 2011; 12:576; PMID:22115407; http://dx.doi.org/10.1186/1471-2164-12-576
   PubMed Web of Science ®Google Scholar
• Shneider MM, Buth SA, Ho BT, Basler M, Mekalanos JJ, Leiman PG. PAAR-repeat proteins sharpen and diversify the type VI secretion system spike. Nature 2013; 500:350-3; PMID:23925114; http://dx.doi.org/10.1038/nature12453
   PubMed Web of Science ®Google Scholar
• Blondel CJ, Jimenez JC, Contreras I, Santiviago CA. Comparative genomic analysis uncovers 3 novel loci encoding type six secretion systems differentially distributed in Salmonella serotypes. BMC Genomics 2009; 10:354; PMID:19653904; http://dx.doi.org/10.1186/1471-2164-10-354
   PubMed Web of Science ®Google Scholar
• Koskiniemi S, Lamoureux JG, Nikolakakis KC, t'Kint de Roodenbeke C, Kaplan MD, Low DA, Hayes CS. Rhs proteins from diverse bacteria mediate intercellular competition. Proc Natl Acad Sci U S A 2013; 110:7032-7; PMID:23572593; http://dx.doi.org/10.1073/pnas.1300627110
   PubMed Web of Science ®Google Scholar
• Zhang D, de Souza RF, Anantharaman V, Iyer LM, Aravind L. Polymorphic toxin systems: Comprehensive characterization of trafficking modes, processing, mechanisms of action, immunity and ecology using comparative genomics. Biol Direct 2012; 7:18; PMID:22731697; http://dx.doi.org/10.1186/1745-6150-7-18
   PubMed Web of Science ®Google Scholar
• Pukatzki S, Ma AT, Revel AT, Sturtevant D, Mekalanos JJ. Type VI secretion system translocates a phage tail spike-like protein into target cells where it cross-links actin. Proc Natl Acad Sci U S A 2007; 104:15508-13; PMID:17873062; http://dx.doi.org/10.1073/pnas.0706532104
   PubMed Web of Science ®Google Scholar
• Jiang F, Wang X, Wang B, Chen L, Zhao Z, Waterfield NR, Yang G, Jin Q. The pseudomonas aeruginosa Type VI secretion PGAP1-like effector induces host autophagy by activating endoplasmic reticulum stress. Cell reports 2016; 16:1502-9; PMID:27477276; http://dx.doi.org/10.1016/j.celrep.2016.07.012
   PubMed Web of Science ®Google Scholar
• Jiang F, Waterfield NR, Yang J, Yang G, Jin Q. A Pseudomonas aeruginosa type VI secretion phospholipase D effector targets both prokaryotic and eukaryotic cells. Cell Host Microbe 2014; 15:600-10; http://dx.doi.org/10.1016/j.chom.2014.04.010
   PubMed Web of Science ®Google Scholar
• Aoki SK, Diner EJ, de Roodenbeke CT, Burgess BR, Poole SJ, Braaten BA, Jones AM, Webb JS, Hayes CS, Cotter PA, et al. A widespread family of polymorphic contact-dependent toxin delivery systems in bacteria. Nature 2010; 468:439-42; PMID:21085179; http://dx.doi.org/10.1038/nature09490
   PubMed Web of Science ®Google Scholar
• Liang X, Moore R, Wilton M, Wong MJ, Lam L, Dong TG. Identification of divergent type VI secretion effectors using a conserved chaperone domain. Proc Natl Acad Sci U S A 2015; 112:9106-11; PMID:26150500; http://dx.doi.org/10.1073/pnas.1505317112
   PubMed Web of Science ®Google Scholar
• Russell AB, Peterson SB, Mougous JD. Type VI secretion system effectors: poisons with a purpose. Nat Rev Microbiol 2014; 12:137-48; PMID:24384601; http://dx.doi.org/10.1038/nrmicro3185
   PubMed Web of Science ®Google Scholar
• Russell AB, Wexler AG, Harding BN, Whitney JC, Bohn AJ, Goo YA, Tran BQ, Barry NA, Zheng H, Peterson SB, et al. A type VI secretion-related pathway in Bacteroidetes mediates interbacterial antagonism. Cell Host Microbe 2014; 16:227-36; http://dx.doi.org/10.1016/j.chom.2014.07.007
   PubMed Web of Science ®Google Scholar
• Hood RD, Singh P, Hsu F, Guvener T, Carl MA, Trinidad RR, Silverman JM, Ohlson BB, Hicks KG, Plemel RL, et al. A type VI secretion system of Pseudomonas aeruginosa targets a toxin to bacteria. Cell Host Microbe 2010; 7:25-37; http://dx.doi.org/10.1016/j.chom.2009.12.007
   PubMed Web of Science ®Google Scholar
• Ballister ER, Lai AH, Zuckermann RN, Cheng Y, Mougous JD. In vitro self-assembly of tailorable nanotubes from a simple protein building block. Proc Natl Acad Sci U S A 2008; 105:3733-8; PMID:18310321; http://dx.doi.org/10.1073/pnas.0712247105
   PubMed Web of Science ®Google Scholar
• Douzi B, Spinelli S, Blangy S, Roussel A, Durand E, Brunet YR, Cascales E, Cambillau C. Crystal structure and self-interaction of the type VI secretion tail-tube protein from enteroaggregative Escherichia coli. PloS one 2014; 9:e86918; PMID:24551044; http://dx.doi.org/10.1371/journal.pone.0086918
   PubMed Web of Science ®Google Scholar
• Frohlich KS, Papenfort K. Interplay of regulatory RNAs and mobile genetic elements in enteric pathogens. Mol Microbiol 2016; 101:701-13; PMID:27232692
   PubMed Web of Science ®Google Scholar
• Koskiniemi S, Garza-Sanchez F, Sandegren L, Webb JS, Braaten BA, Poole SJ, Andersson DI, Hayes CS, Low DA. Selection of orphan Rhs toxin expression in evolved Salmonella enterica serovar Typhimurium. PLoS Genet 2014; 10:e1004255; PMID:24675981
   PubMed Web of Science ®Google Scholar
• Hayes CS, Koskiniemi S, Ruhe ZC, Poole SJ, Low DA. Mechanisms and biological roles of contact-dependent growth inhibition systems. Cold Spring Harbor perspectives in medicine 2014; a010025; PMID:24492845; http://dx.doi.org/10.1101/cshperspect.a010025
   PubMed Web of Science ®Google Scholar
• Poole SJ, Diner EJ, Aoki SK, Braaten BA, t'Kint de Roodenbeke C, Low DA, Hayes CS. Identification of functional toxin/immunity genes linked to contact-dependent growth inhibition (CDI) and rearrangement hotspot (Rhs) systems. PLoS Genet 2011; 7:e1002217; PMID:21829394
   PubMed Web of Science ®Google Scholar
• Datsenko KA, Wanner BL. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 2000; 97:6640-5; PMID:10829079
   PubMed Web of Science ®Google Scholar
• Alteri CJ, Smith SN, Mobley HL. Fitness of Escherichia coli during urinary tract infection requires gluconeogenesis and the TCA cycle. PLoS pathog 2009; 5:e1000448; PMID:19478872
   PubMed Web of Science ®Google Scholar
• Soding J, Biegert A, Lupas AN. The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res 2005; 33:W244-8; PMID:15980461
   PubMed Web of Science ®Google Scholar
• Kelley LA, Mezulis S, Yates CM, Wass MN, Sternberg MJ. The Phyre2 web portal for protein modeling, prediction and analysis. Nat Protoc 2015; 10:845-58; PMID:25950237
   PubMed Web of Science ®Google Scholar
• Kelley LA, Sternberg MJ. Protein structure prediction on the Web: a case study using the Phyre server. Nat Protoc 2009; 4:363-71; PMID:19247286
   PubMed Web of Science ®Google Scholar
• Geer LY, Domrachev M, Lipman DJ, Bryant SH. CDART: protein homology by domain architecture. Genome Res 2002; 12:1619-23; PMID:12368255
   PubMed Web of Science ®Google Scholar
• Li G, Laturnus C, Ewers C, Wieler LH. Identification of genes required for avian Escherichia coli septicemia by signature-tagged mutagenesis. Infect Immun 2005; 73:2818-27; PMID:15845486
   PubMed Web of Science ®Google Scholar
• Diner EJ, Beck CM, Webb JS, Low DA, Hayes CS. Identification of a target cell permissive factor required for contact-dependent growth inhibition (CDI). Genes Dev 2012; 26:515-25
   PubMed Web of Science ®Google Scholar
• Skyberg JA, Johnson TJ, Nolan LK. Mutational and transcriptional analyses of an avian pathogenic Escherichia coli ColV plasmid. BMC Microbiol 2008; 8:24; PMID:18230176
   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; 25:402-8; PMID:11846609
   PubMed Web of Science ®Google Scholar
• Zhou Y, Tao J, Yu H, Ni J, Zeng L, Teng Q, Kim KS, Zhao GP, Guo X, Yao Y. Hcp family proteins secreted via the type VI secretion system coordinately regulate Escherichia coli K1 interaction with human brain microvascular endothelial cells. Infect Immun 2012; 80:1243-51; PMID:22184413
   PubMed Web of Science ®Google Scholar