Pilotins are mobile T3SS components involved in assembly and substrate specificity of the bacterial type III secretion system.
bacterial virulence mechanisms
host pathogen interaction
live cell microscopy
membrane transport
secretion systems
Journal
Molecular microbiology
ISSN: 1365-2958
Titre abrégé: Mol Microbiol
Pays: England
ID NLM: 8712028
Informations de publication
Date de publication:
04 Jan 2024
04 Jan 2024
Historique:
revised:
17
12
2023
received:
23
05
2023
accepted:
20
12
2023
medline:
5
1
2024
pubmed:
5
1
2024
entrez:
5
1
2024
Statut:
aheadofprint
Résumé
In animal pathogens, assembly of the type III secretion system injectisome requires the presence of so-called pilotins, small lipoproteins that assist the formation of the secretin ring in the outer membrane. Using a combination of functional assays, interaction studies, proteomics, and live-cell microscopy, we determined the contribution of the pilotin to the assembly, function, and substrate selectivity of the T3SS and identified potential new downstream roles of pilotin proteins. In absence of its pilotin SctG, Yersinia enterocolitica forms few, largely polar injectisome sorting platforms and needles. Accordingly, most export apparatus subcomplexes are mobile in these strains, suggesting the absence of fully assembled injectisomes. Remarkably, while absence of the pilotin all but prevents export of early T3SS substrates, such as the needle subunits, it has little effect on secretion of late T3SS substrates, including the virulence effectors. We found that although pilotins interact with other injectisome components such as the secretin in the outer membrane, they mostly localize in transient mobile clusters in the bacterial membrane. Together, these findings provide a new view on the role of pilotins in the assembly and function of type III secretion injectisomes.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Max-Planck-Gesellschaft
Informations de copyright
© 2024 The Authors. Molecular Microbiology published by John Wiley & Sons Ltd.
Références
Abby, S.S. & Rocha, E.P.C. (2012) The non-flagellar type III secretion system evolved from the bacterial flagellum and diversified into host-cell adapted systems. PLoS Genetics, 8, e1002983.
Abrusci, P., Vergara-Irigaray, M., Johnson, S., Beeby, M.D., Hendrixson, D.R., Roversi, P. et al. (2013) Architecture of the major component of the type III secretion system export apparatus. Nature Structural & Molecular Biology, 20, 99-104.
Ahrné, E., Glatter, T., Viganò, C., Von Schubert, C., Nigg, E.A. & Schmidt, A. (2016) Evaluation and improvement of quantification accuracy in isobaric mass tag-based protein quantification experiments. Journal of Proteome Research, 15, 2537-2547.
Albrecht, R., Zeth, K., Söding, J., Lupas, A. & Linke, D. (2006) Expression, crystallization and preliminary X-ray crystallographic studies of the outer membrane protein OmpW from Escherichia coli. Acta Crystallographica. Section F, Structural Biology and Crystallization Communications, 62, 415-418.
Allaoui, A., Scheen, R., Lambert de Rouvroit, C. & Cornelis, G.R. (1995) VirG, a Yersinia enterocolitica lipoprotein involved in Ca2+ dependency, is related to exsB of Pseudomonas aeruginosa. Journal of Bacteriology, 177, 4230-4237.
Bange, G., Kümmerer, N., Engel, C., Bozkurt, G., Wild, K. & Sinning, I. (2010) FlhA provides the adaptor for coordinated delivery of late flagella building blocks to the type III secretion system. Proceedings of the National Academy of Sciences of the United States of America, 107, 11295-11300.
Blocker, A.J., Gounon, P., Larquet, E., Niebuhr, K., Cabiaux, V., Parsot, C. et al. (1999) The tripartite type III secreton of Shigella flexneri inserts IpaB and IpaC into host membranes. The Journal of Cell Biology, 147, 683-693.
Böhme, K., Steinmann, R., Kortmann, J., Seekircher, S., Heroven, A.K., Berger, E. et al. (2012) Concerted actions of a thermo-labile regulator and a unique intergenic RNA thermosensor control Yersinia virulence. PLoS Pathogens, 8, e1002518.
Botteaux, A., Sory, M.-P., Biskri, L., Parsot, C. & Allaoui, A. (2009) MxiC is secreted by and controls the substrate specificity of the Shigella flexneri type III secretion apparatus. Molecular Microbiology, 71, 449-460.
Breidenstein, E.B.M., Janot, L., Strehmel, J., Fernandez, L., Taylor, P.K., Kukavica-Ibrulj, I. et al. (2012) The Lon protease is essential for full virulence in Pseudomonas aeruginosa. PLoS One, 7, e49123.
Bretz, J., Losada, L., Lisboa, K. & Hutcheson, S.W. (2002) Lon protease functions as a negative regulator of type III protein secretion in Pseudomonas syringae. Molecular Microbiology, 45, 397-409.
Burgess, J.L., Case, H.B., Burgess, R.A. & Dickenson, N.E. (2020) Dominant negative effects by inactive Spa47 mutants inhibit T3SS function and Shigella virulence. PLoS One, 15, e0228227.
Burghout, P., Beckers, F., de Wit, E., van Boxtel, R., Cornelis, G.R., Tommassen, J. et al. (2004) Role of the pilot protein YscW in the biogenesis of the YscC secretin in Yersinia enterocolitica. Journal of Bacteriology, 186, 5366-5375.
Burkinshaw, B.J. & Strynadka, N.C. (2014) Assembly and structure of the T3SS. Biochimica et Biophysica Acta (BBA)-Molecular Cell Research, 1843, 1648-1693.
Büttner, D. (2012) Protein export according to schedule: architecture, assembly, and regulation of type III secretion systems from plant- and animal-pathogenic bacteria. Microbiology and Molecular Biology Reviews, 76, 262-310.
Carter, P.B., Zahorchak, R.J. & Brubaker, R.R. (1980) Plague virulence antigens from Yersinia enterocolitica. Infection and Immunity, 28, 638-640.
Chakravortty, D., Rohde, M., Jäger, L., Deiwick, J. & Hensel, M. (2005) Formation of a novel surface structure encoded by Salmonella Pathogenicity Island 2. The EMBO Journal, 24, 2043-2052.
Chami, M., Guilvout, I., Gregorini, M., Rémigy, H.W., Müller, S.A., Valerio, M. et al. (2005) Structural insights into the secretin PulD and its trypsin-resistant core. The Journal of Biological Chemistry, 280, 37732-37741.
Chernyatina, A.A. & Low, H.H. (2019) Core architecture of a bacterial type II secretion system. Nature Communications, 10, 1-10.
Coombes, B.K. (2009) Type III secretion systems in symbiotic adaptation of pathogenic and non-pathogenic bacteria. Trends Microbiol, 17, 89-94.
Collin, S., Guilvout, I., Nickerson, N.N. & Pugsley, A.P. (2011) Sorting of an integral outer membrane protein via the lipoprotein-specific Lol pathway and a dedicated lipoprotein pilotin. Molecular Microbiology, 80, 655-665.
Collin, S., Krehenbrink, M., Guilvout, I. & Pugsley, A.P. (2013) The targeting, docking and anti-proteolysis functions of the secretin chaperone PulS. Research in Microbiology, 164, 390-396.
Collins, J., Robinson, C., Danhof, H., Knetsch, C.W., Van Leeuwen, H.C., Lawley, T.D. et al. (2018) Dietary trehalose enhances virulence of epidemic Clostridium difficile. Nature, 553, 291-294.
Cornelis, G.R. (1993) Role of the transcription activator VirF and the histone-like protein YmoA in the thermoregulation of virulence functions in Yersiniae. Zentralblatt für Bakteriologie, 278, 149-164.
Cornelis, G.R. (2006) The type III secretion injectisome. Nature Reviews. Microbiology, 4, 811-825.
Cornelis, G.R., Sluiters, C., Delor, I., Geib, D., Kaniga, K., de Rouvroit, C.L. et al. (1991) ymoA, a Yersinia enterocolitica chromosomal gene modulating the expression of virulence functions. Molecular Microbiology, 5, 1023-1034.
Cox, J. & Mann, M. (2008) MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nature Biotechnology, 26, 1367-1372.
Crago, A. & Koronakis, V. (1998) Salmonella InvG forms a ring-like multimer that requires the InvH lipoprotein for outer membrane localization. Molecular Microbiology, 30, 47-56.
Daefler, S. & Russel, M. (1998) The Salmonella typhimurium InvH protein is an outer membrane lipoprotein required for the proper localization of InvG. Molecular Microbiology, 28, 1367-1380.
Day, J.B. & Plano, G.V. (1998) A complex composed of SycN and YscB functions as a specific chaperone for YopN in Yersinia pestis. Molecular Microbiology, 30, 777-788.
Diepold, A., Amstutz, M., Abel, S., Sorg, I., Jenal, U. & Cornelis, G.R. (2010) Deciphering the assembly of the Yersinia type III secretion injectisome. The EMBO Journal, 29, 1928-1940.
Diepold, A. & Armitage, J.P. (2015) Type III secretion systems: the bacterial flagellum and the injectisome. Philosophical Transactions of the Royal Society B: Biological Sciences, 370, 20150020.
Diepold, A., Kudryashev, M., Delalez, N.J., Berry, R.M. & Armitage, J.P. (2015) Composition, formation, and regulation of the cytosolic C-ring, a dynamic component of the type III secretion Injectisome. PLoS Biology, 13, e1002039.
Diepold, A., Sezgin, E., Huseyin, M., Mortimer, T., Eggeling, C. & Armitage, J.P. (2017) A dynamic and adaptive network of cytosolic interactions governs protein export by the T3SS injectisome. Nature Communications, 8, 15940.
Diepold, A. & Wagner, S. (2014) Assembly of the bacterial type III secretion machinery. FEMS Microbiology Reviews, 38, 802-822.
Diepold, A., Wiesand, U., Amstutz, M. & Cornelis, G.R. (2012) Assembly of the Yersinia injectisome: the missing pieces. Molecular Microbiology, 85, 878-892.
Diepold, A., Wiesand, U. & Cornelis, G.R. (2011) The assembly of the export apparatus (YscR,S,T,U,V) of the Yersinia type III secretion apparatus occurs independently of other structural components and involves the formation of an YscV oligomer. Molecular Microbiology, 82, 502-514.
Erhardt, M., Namba, K. & Hughes, K.T. (2010) Bacterial nanomachines: the flagellum and type III injectisome. Cold Spring Harbor Perspectives in Biology, 2, a000299.
Figaj, D., Czaplewska, P., Przepióra, T., Ambroziak, P., Potrykus, M. & Skorko-Glonek, J. (2020) Lon protease is important for growth under stressful conditions and pathogenicity of the phytopathogen, bacterium Dickeya solani. International Journal of Molecular Sciences, 21, 3687.
Flacht, L., Lunelli, M., Kaszuba, K., Chen, Z.A., O'Reilly, F.J., Rappsilber, J. et al. (2023) Integrative structural analysis of the type III secretion system needle complex from Shigella flexneri. Protein Science, 32, 1-15.
Fuchs, T.M., Brandt, K., Starke, M. & Rattei, T. (2011) Shotgun sequencing of Yersinia enterocolitica strain W22703 (biotype 2, serotype O:9): genomic evidence for oscillation between invertebrates and mammals. BMC Genomics, 12, 168.
Galán, J.E. & Wolf-Watz, H. (2006) Protein delivery into eukaryotic cells by type III secretion machines. Nature, 444, 567-573.
Glatter, T., Ludwig, C., Ahrné, E., Aebersold, R., Heck, A.J.R. & Schmidt, A. (2012) Large-scale quantitative assessment of different in-solution protein digestion protocols reveals superior cleavage efficiency of tandem Lys-C/trypsin proteolysis over trypsin digestion. Journal of Proteome Research, 11, 5145-5156.
Gu, S., Rehman, S., Wang, X., Shevchik, V.E. & Pickersgill, R.W. (2012) Structural and functional insights into the pilotin-secretin complex of the type II secretion system. PLoS Pathogens, 8, e1002531.
Gur, E. & Sauer, R.T. (2008) Recognition of misfolded proteins by Lon, a AAA+ protease. Genes & Development, 22, 2267-2277.
Hardie, K.R., Lory, S. & Pugsley, A.P. (1996) Insertion of an outer membrane protein in Escherichia coli requires a chaperone-like protein. The EMBO Journal, 15, 978-988.
Hoe, N. & Goguen, J.D. (1993) Temperature sensing in Yersinia pestis: translation of the LcrF activator protein is thermally regulated. Journal of Bacteriology, 175, 7901-7909.
Hong, H., Patel, D.R., Tamm, L.K. & van den Berg, B. (2006) The outer membrane protein OmpW forms an eight-stranded β-barrel with a hydrophobic channel. The Journal of Biological Chemistry, 281, 7568-7577.
Hu, B., Lara-Tejero, M., Kong, Q., Galán, J.E. & Liu, J. (2017) In situ molecular architecture of the salmonella type III secretion machine. Cell, 168, 1065-1074.e10.
Hu, B., Morado, D.R., Margolin, W., Rohde, J.R., Arizmendi, O., Picking, W.L. et al. (2015) Visualization of the type III secretion sorting platform of Shigella flexneri. Proceedings of the National Academy of Sciences of the United States of America, 112, 1047-1052.
Hu, J., Worrall, L.J., Hong, C., Vuckovic, M., Atkinson, C.E., Caveney, N. et al. (2018) Cryo-EM analysis of the T3S injectisome reveals the structure of the needle and open secretin. Nature Communications, 9, 3840.
Hueck, C.J. (1998) Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiology and Molecular Biology Reviews, 62, 379-433.
Inoue, Y., Kinoshita, M., Kida, M., Takekawa, N., Namba, K., Imada, K. et al. (2021) The FlhA linker mediates flagellar protein export switching during flagellar assembly. Communications Biology, 4, 646.
Iriarte, M. & Cornelis, G.R. (1999) Identification of SycN, YscX, and YscY, three new elements of the Yersinia yop virulon. Journal of Bacteriology, 181, 675-680.
Jackson, M.W., Silva-Herzog, E. & Plano, G.V. (2004) The ATP-dependent ClpXP and Lon proteases regulate expression of the Yersinia pestis type III secretion system via regulated proteolysis of YmoA, a small histone-like protein. Molecular Microbiology, 54, 1364-1378.
Jeckelmann, J.M. & Erni, B. (2019) Carbohydrate transport by group translocation: the bacterial phosphoenolpyruvate: sugar phosphotransferase system. Basel, Switzerland: Springer International Publishing.
Jeckelmann, J.M. & Erni, B. (2020) Transporters of glucose and other carbohydrates in bacteria. Pflügers Archiv: European Journal of Physiology, 472, 1129-1153.
Journet, L., Agrain, C., Broz, P. & Cornelis, G.R. (2003) The needle length of bacterial injectisomes is determined by a molecular ruler. Science, 302, 1757-1760.
Kaniga, K., Delor, I. & Cornelis, G.R. (1991) A wide-host-range suicide vector for improving reverse genetics in gram-negative bacteria: inactivation of the blaA gene of Yersinia enterocolitica. Gene, 109, 137-141.
Kinoshita, M., Hara, N., Imada, K., Namba, K. & Minamino, T. (2013) Interactions of bacterial flagellar chaperone-substrate complexes with FlhA contribute to co-ordinating assembly of the flagellar filament. Molecular Microbiology, 90, 1249-1261.
Kok, M., Bron, G., Erni, B. & Mukhija, S. (2003) Effect of enzyme I of the bacterial phosphoenolpyruvate: sugar phosphotransferase system (PTS) on virulence in a murine model. Microbiology, 149, 2645-2652.
Konovalova, A. & Silhavy, T.J. (2015) Outer membrane lipoprotein biogenesis: Lol is not the end. Philosophical Transactions of the Royal Society B: Biological Sciences, 370, 20150030.
Koo, J., Burrows, L.L. & Lynne Howell, P. (2012) Decoding the roles of pilotins and accessory proteins in secretin escort services. FEMS Microbiology Letters, 328, 1-12.
Korotkov, K.V., Gonen, T. & Hol, W.G.J. (2011) Secretins: dynamic channels for protein transport across membranes. Trends in Biochemical Sciences, 36(8), 433-443.
Koster, M., Bitter, W., de Cock, H., Allaoui, A., Cornelis, G.R. & Tommassen, J. (1997) The outer membrane component, YscC, of the Yop secretion machinery of Yersinia enterocolitica forms a ring-shaped multimeric complex. Molecular Microbiology, 26, 789-797.
Kudryashev, M., Diepold, A., Amstutz, M., Armitage, J.P., Stahlberg, H. & Cornelis, G.R. (2015) Yersinia enterocolitica type III secretion injectisomes form regularly spaced clusters, which incorporate new machines upon activation. Molecular Microbiology, 95, 875-884.
Kudryashev, M., Stenta, M., Schmelz, S., Amstutz, M., Wiesand, U., Castaño-Díez, D. et al. (2013) In situ structural analysis of the Yersinia enterocolitica injectisome. eLife, 2, e00792.
Kusmierek, M., Hoßmann, J., Witte, R., Opitz, W., Vollmer, I., Volk, M. et al. (2019) A bacterial secreted translocator hijacks riboregulators to control type III secretion in response to host cell contact. PLoS Pathogens, 15, e1007813.
Lambert de Rouvroit, C., Sluiters, C. & Cornelis, G.R. (1992) Role of the transcriptional activator, VirF, and temperature in the expression of the pYV plasmid genes of Yersinia enterocolitica. Molecular Microbiology, 6, 395-409.
Lampaki, D., Diepold, A. & Glatter, T. (2020) A serial sample processing strategy with improved performance for in-depth quantitative analysis of type III secretion events in Pseudomonas aeruginosa. Journal of Proteome Research, 19, 543-553.
Lara-Tejero, M., Kato, J., Wagner, S., Liu, X. & Galán, J.E. (2011) A sorting platform determines the order of protein secretion in bacterial type III systems. Science, 331, 1188-1191.
Lee, J.H., Ancona, V. & Zhao, Y. (2018) Lon protease modulates virulence traits in Erwinia amylovora by direct monitoring of major regulators and indirectly through the Rcs and Gac-Csr regulatory systems. Molecular Plant Pathology, 19, 827-840.
Majewski, D.D., Okon, M., Heinkel, F., Robb, C.S., Vuckovic, M., McIntosh, L.P. et al. (2021) Characterization of the pilotin-secretin complex from the Salmonella enterica type III secretion system using hybrid structural methods. Structure, 29, 125-138.e5.
Mazé, A., Glatter, T. & Bumann, D. (2014) The central metabolism regulator EIIAGlc switches salmonella from growth arrest to acute virulence through activation of virulence factor secretion. Cell Reports, 7, 1426-1433.
Miletic, S., Fahrenkamp, D., Goessweiner-Mohr, N., Wald, J., Pantel, M., Vesper, O. et al. (2021) Substrate-engaged type III secretion system structures reveal gating mechanism for unfolded protein translocation. Nature Communications, 12, 1546.
Milne-Davies, B., Helbig, C., Wimmi, S., Cheng, D.W.C., Paczia, N. & Diepold, A. (2019) Life after secretion-Yersinia enterocolitica rapidly toggles effector secretion and can resume cell division in response to changing external conditions. Frontiers in Microbiology, 10, 2128.
Minamino, T., Inoue, Y., Kinoshita, M. & Namba, K. (2020) FliK-driven conformational rearrangements of FlhA and FlhB are required for export switching of the flagellar protein export apparatus. Journal of Bacteriology, 202, e00637-1.
Miwa, H. & Okazaki, S. (2017) How effectorspromote beneficial interactions. Curr Opin Plant Biol, 38, 148-154.
Nouwen, N., Ranson, N., Saibil, H.R., Wolpensinger, B., Engel, A., Ghazi, A. et al. (1999) Secretin PulD: association with pilot PulS, structure, and ion-conducting channel formation. Proceedings of the National Academy of Sciences of the United States of America, 96, 8173-8177.
Okon, M., Moraes, T.F., Lario, P.I., Creagh, A.L., Haynes, C.A., Strynadka, N.C. et al. (2008) Structural characterization of the type-III pilot-secretin complex from Shigella flexneri. Structure, 16, 1544-1554.
Omnus, D.J., Fink, M.J., Szwedo, K. & Jonas, K. (2021) The lon protease temporally restricts polar cell differentiation events during the caulobacter cell cycle. eLife, 10, 1-24.
Pacheco, A.R. & Sperandio, V. (2015) Enteric pathogens exploit the microbiota-generated nutritional environment of the gut. Metabolism and Bacterial Pathogenesis, 3(3), MBP-0001-2014. https://doi.org/10.1128/microbiolspec.MBP-0001-2014.
Palace, S.G., Proulx, M.K., Lu, S., Baker, R.E. & Goguen, J.D. (2014) Genome-wide mutant fitness profiling identifies nutritional requirements for optimal growth of Yersinia pestis in deep tissue. MBio, 5, e01385-14.
Perdu, C., Huber, P., Bouillot, S., Blocker, A.J., Elsen, S., Attree, I. et al. (2015) ExsB is required for correct assembly of Pseudomonas aeruginosa type III secretion apparatus in the bacterial membrane and full virulence in vivo. Infection and Immunity, 83, 1789-1798.
Pflüger-Grau, K. & Görke, B. (2010) Regulatory roles of the bacterial nitrogen-related phosphotransferase system. Trends in Microbiology, 18, 205-214.
Rau, R. & Darwin, A.J. (2015) Identification of YsaP, the pilotin of the Yersinia enterocolitica Ysa type III secretion system. Journal of Bacteriology, 197, 2770-2779.
Renault, T.T., Guse, A. & Erhardt, M. (2019) Export mechanisms and energy transduction in type-III secretion machines. In: Current topics in microbiology and immunology. Berlin, Heidelberg: Springer, pp. 1-17.
Sasakawa, C., Kamata, K., Sakai, T., Murayama, S.Y., Makino, S. & Yoshikawa, M. (1986) Molecular alteration of the 140-megadalton plasmid associated with loss of virulence and Congo red binding activity in Shigella flexneri. Infection and Immunity, 51, 470-475.
Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T. et al. (2012) Fiji: an open-source platform for biological-image analysis. Nature Methods, 9, 676-682.
Schuch, R. & Maurelli, A.T. (1999) The mxi-Spa type III secretory pathway of Shigella flexneri requires an outer membrane lipoprotein, MxiM, for invasin translocation. Infection and Immunity, 67, 1982-1991.
Schuch, R. & Maurelli, A.T. (2001) MxiM and MxiJ, base elements of the mxi-Spa type III secretion system of Shigella, interact with and stabilize the MxiD secretin in the cell envelope. Journal of Bacteriology, 183, 6991-6998.
Schwiesow, L., Lam, H., Dersch, P. & Auerbuch, V. (2016) Yersinia type III secretion system master regulator LcrF. Journal of Bacteriology, 198, 604-614.
Silva, Y.R.d.O., Contreras-Martel, C., Macheboeuf, P. & Dessen, A. (2020) Bacterial secretins: mechanisms of assembly and membrane targeting. Protein Science, 29, 893-904.
Sorg, I., Wagner, S., Amstutz, M., Müller, S.A., Broz, P., Lussi, Y. et al. (2007) YscU recognizes translocators as export substrates of the Yersinia injectisome. The EMBO Journal, 26, 3015-3024.
Spahn, C., Laine, R.F., Pereira, P. & Gómez-de-mariscal, E. (2021) Supplementary information-DeepBacs: bacterial image analysis using open-source deep learning approaches. bioRxiv, 1-15.
Sturm, A., Heinemann, M., Arnoldini, M., Benecke, A., Ackermann, M., Benz, M. et al. (2011) The cost of virulence: retarded growth of Salmonella Typhimurium cells expressing type III secretion system 1. PLoS Pathogens, 7, e1002143.
Thevenaz, P., Ruttimann, U.E. & Unser, M. (1998) A pyramid approach to subpixel registration based on intensity. IEEE Transactions on Image Processing, 7, 27-41.
Troisfontaines, P. & Cornelis, G.R. (2005) Type III secretion: more systems than you think. Physiology, 20, 326-339.
Tseytin, I., Dagan, A., Oren, S. & Sal-Man, N. (2017) The role of EscD in supporting EscC polymerization in the type III secretion system of enteropathogenic Escherichia coli. Biochimica et Biophysica Acta, 1860, 384-395.
Tsilibaris, V., Maenhaut-Michel, G. & Van Melderen, L. (2006) Biological roles of the Lon ATP-dependent protease. Research in Microbiology, 157, 701-713.
Tyanova, S., Temu, T., Sinitcyn, P., Carlson, A., Hein, M.Y., Geiger, T. et al. (2016) The Perseus computational platform for comprehensive analysis of (prote)omics data. Nature Methods, 13, 731-740.
Wagner, S. & Diepold, A. (2020) A unified nomenclature for injectisome-type type III secretion systems. Current Topics in Microbiology and Immunology, 427, 1-10.
Wagner, S., Grin, I., Malmsheimer, S., Singh, N., Torres-Vargas, C.E. & Westerhausen, S. (2018) Bacterial type III secretion systems: a complex device for the delivery of bacterial effector proteins into eukaryotic host cells. FEMS Microbiology Letters, 365, fny201.
Wallace, I.M., O'Sullivan, O., Higgins, D.G. & Notredame, C. (2006) M-Coffee: combining multiple sequence alignment methods with T-Coffee. Nucleic Acids Research, 34, 1692-1699.
Wang, Q., Millet, Y.A., Chao, M.C., Sasabe, J., Davis, B.M. & Waldor, M.K. (2015) A genome-wide screen reveals that the Vibrio cholerae phosphoenolpyruvate phosphotransferase system modulates virulence gene expression. Infection and Immunity, 83, 3381-3395.
Wee, D.H. & Hughes, K.T. (2015) Molecular ruler determines needle length for the Salmonella Spi-1 injectisome. Proceedings of the National Academy of Sciences of the United States of America, 112, 4098-4103.
Wimmi, S., Balinovic, A., Jeckel, H., Selinger, L., Lampaki, D., Eisemann, E. et al. (2021) Dynamic relocalization of cytosolic type III secretion system components prevents premature protein secretion at low external pH. Nature Communications, 12, 1625.
Wu, X.-B., Tian, L.-H., Zou, H.-J., Wang, C.-Y., Yu, Z.-Q., Tang, C.-H. et al. (2013) Outer membrane protein OmpW of Escherichia coli is required for resistance to phagocytosis. Research in Microbiology, 164, 848-855.
Xing, Q., Shi, K., Portaliou, A.G., Rossi, P., Economou, A. & Kalodimos, C.G. (2018) Structures of chaperone-substrate complexes docked onto the export gate in a type III secretion system. Nature Communications, 9, 1773.
Yin, M., Yan, Z. & Li, X. (2018) Structural insight into the assembly of the type II secretion system pilotin-secretin complex from enterotoxigenic Escherichia coli. Nature Microbiology, 3, 581-587.
Zhang, Y., Lara-Tejero, M., Bewersdorf, J. & Galán, J.E. (2017) Visualization and characterization of individual type III protein secretion machines in live bacteria. Proceedings of the National Academy of Sciences of the United States of America, 114, 6098-6103.
Zhou, X., Teper, D., Andrade, M.O., Zhang, T., Chen, S., Song, W.Y. et al. (2018) A phosphorylation switch on lon protease regulates bacterial type III secretion system in host. MBio, 9, e02146-17.