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Volume 169, Issue 6

Virulence-associated type III secretion systems in Gram-negative bacteria Open Access

This article is part of the Bacterial Cell Envelopes collection.

Abstract

Virulence-associated bacterial type III secretion systems are multiprotein molecular machines that promote the pathogenicity of bacteria towards eukaryotic host cells. These machines form needle-like structures, named injectisomes, that span both bacterial and host membranes, forming a direct conduit for the delivery of bacterial proteins into host cells. Once within the host, these bacterial effector proteins are capable of manipulating a multitude of host cell functions. In recent years, the knowledge of assembly, structure and function of these machines has grown substantially and is presented and discussed in this review.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): bacterial pathogenicity and type III secretion systems
Funding
This study was supported by the:
  • Deutsches Zentrum für Infektionsforschung (Award TTU 06 819)
    • Principle Award Recipient: SamuelWagner
  • Deutsche Forschungsgemeinschaft (Award WA3299/5-1, EXC2124)
    • Principle Award Recipient: SamuelWagner
© 2023 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
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2023-06-13
2024-04-28
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References

  1. Abby SS, Rocha EPC. The non-flagellar type III secretion system evolved from the bacterial flagellum and diversified into host-cell adapted systems. PLoS Genet 2012; 8:e1002983 [View Article] [PubMed]
     [Google Scholar]
  2. Zilkenat S, Franz-Wachtel M, Stierhof Y-D, Galán JE, Macek B et al. Determination of the stoichiometry of the complete bacterial type III secretion needle complex using a combined quantitative proteomic approach. Mol Cell Proteomics 2016; 15:1598–1609 [View Article] [PubMed]
     [Google Scholar]
  3. Troisfontaines P, Cornelis GR. Type III secretion: more systems than you think. Physiology 2005; 20:326–339 [View Article] [PubMed]
     [Google Scholar]
  4. Heuck AP, Brovedan MA. Evolutionary conservation, variability, and adaptation of Type III secretion systems. J Membr Biol 2022; 255:599–612 [View Article] [PubMed]
     [Google Scholar]
  5. Kuhlen L, Abrusci P, Johnson S, Gault J, Deme J et al. Author correction: structure of the core of the type III secretion system export apparatus. Nat Struct Mol Biol 2018; 25:743 [View Article] [PubMed]
     [Google Scholar]
  6. Kuhlen L, Johnson S, Zeitler A, Bäurle S, Deme JC et al. The substrate specificity switch FlhB assembles onto the export gate to regulate type three secretion. Nat Commun 2020; 11:1296 [View Article] [PubMed]
     [Google Scholar]
  7. Dietsche T, Tesfazgi Mebrhatu M, Brunner MJ, Abrusci P, Yan J et al. Structural and functional characterization of the bacterial Type III secretion export apparatus. PLoS Pathog 2016; 12:e1006071 [View Article] [PubMed]
     [Google Scholar]
  8. Johnson S, Kuhlen L, Deme JC, Abrusci P, Lea SM. The structure of an injectisome export gate demonstrates conservation of architecture in the core export gate between flagellar and virulence type III secretion systems. mBio 2019; 10:e00818-19 [View Article] [PubMed]
     [Google Scholar]
  9. Butan C, Lara-Tejero M, Li W, Liu J, Galán JE. High-resolution view of the type III secretion export apparatus in situ reveals membrane remodeling and a secretion pathway. Proc Natl Acad Sci 2019; 116:24786–24795 [View Article] [PubMed]
     [Google Scholar]
  10. Hu J, Worrall LJ, Vuckovic M, Hong C, Deng W et al. T3S injectisome needle complex structures in four distinct states reveal the basis of membrane coupling and assembly. Nat Microbiol 2019; 4:2010–2019 [View Article] [PubMed]
     [Google Scholar]
  11. Hüsing S, Halte M, van Look U, Guse A, Gálvez EJC et al. Control of membrane barrier during bacterial type-III protein secretion. Nat Commun 2021; 12:3999 [View Article] [PubMed]
     [Google Scholar]
  12. Miletic S, Fahrenkamp D, Goessweiner-Mohr N, Wald J, Pantel M et al. Substrate-engaged type III secretion system structures reveal gating mechanism for unfolded protein translocation. Nat Commun 2021; 12:1546 [View Article] [PubMed]
     [Google Scholar]
  13. Singh N, Kronenberger T, Eipper A, Weichel F, Franz-Wachtel M et al. Conserved salt bridges facilitate assembly of the helical core export apparatus of a Salmonella enterica Type III secretion system. J Mol Biol 2021; 433:167175 [View Article] [PubMed]
     [Google Scholar]
  14. Ferris HU, Furukawa Y, Minamino T, Kroetz MB, Kihara M et al. FlhB regulates ordered export of flagellar components via autocleavage mechanism. J Biol Chem 2005; 280:41236–41242 [View Article] [PubMed]
     [Google Scholar]
  15. Minamino T, Macnab RM. Domain structure of Salmonella FlhB, a flagellar export component responsible for substrate specificity switching. J Bacteriol 2000; 182:4906–4914 [View Article] [PubMed]
     [Google Scholar]
  16. Zarivach R, Deng W, Vuckovic M, Felise HB, Nguyen HV et al. Structural analysis of the essential self-cleaving type III secretion proteins EscU and SpaS. Nature 2008; 453:124–127 [View Article] [PubMed]
     [Google Scholar]
  17. Björnfot A-C, Lavander M, Forsberg A, Wolf-Watz H. Autoproteolysis of YscU of Yersinia pseudotuberculosis is important for regulation of expression and secretion of Yop proteins. J Bacteriol 2009; 191:4259–4267 [View Article] [PubMed]
     [Google Scholar]
  18. Edqvist PJ, Olsson J, Lavander M, Sundberg L, Forsberg A et al. YscP and YscU regulate substrate specificity of the Yersinia type III secretion system. J Bacteriol 2003; 185:2259–2266 [View Article] [PubMed]
     [Google Scholar]
  19. Monjarás Feria JV, Lefebre MD, Stierhof Y-D, Galán JE, Wagner S. Role of autocleavage in the function of a type III secretion specificity switch protein in Salmonella enterica serovar Typhimurium. mBio 2015; 6:e01459–15 [View Article] [PubMed]
     [Google Scholar]
  20. Abrusci P, Vergara-Irigaray M, Johnson S, Beeby MD, Hendrixson DR et al. Architecture of the major component of the type III secretion system export apparatus. Nat Struct Mol Biol 2013; 20:99–104 [View Article] [PubMed]
     [Google Scholar]
  21. Inoue Y, Kinoshita M, Namba K, Minamino T. Mutational analysis of the C-terminal cytoplasmic domain of FlhB, a transmembrane component of the flagellar type III protein export apparatus in Salmonella. Genes Cells 2019; 24:408–421 [View Article] [PubMed]
     [Google Scholar]
  22. Worrall LJ, Vuckovic M, Strynadka NCJ. Crystal structure of the C-terminal domain of the Salmonella type III secretion system export apparatus protein InvA. Protein Sci 2010; 19:1091–1096 [View Article] [PubMed]
     [Google Scholar]
  23. Minamino T, Kinoshita M, Inoue Y, Kitao A, Namba K. Conserved GYXLI Motif of FlhA Is Involved in dynamic domain motions of FlhA required for flagellar protein export. Microbiol Spectr 2022; 10:e0111022 [View Article] [PubMed]
     [Google Scholar]
  24. Yuan B, Portaliou AG, Parakra R, Smit JH, Wald J et al. Structural dynamics of the functional nonameric Type III translocase export gate. J Mol Biol 2021; 433:167188 [View Article] [PubMed]
     [Google Scholar]
  25. Schraidt O, Lefebre MD, Brunner MJ, Schmied WH, Schmidt A et al. Topology and organization of the Salmonella typhimurium type III secretion needle complex components. PLoS Pathog 2010; 6:e1000824 [View Article] [PubMed]
     [Google Scholar]
  26. Schraidt O, Marlovits TC. Three-dimensional model of Salmonella’s needle complex at subnanometer resolution. Science 2011; 331:1192–1195 [View Article] [PubMed]
     [Google Scholar]
  27. Spreter T, Yip CK, Sanowar S, André I, Kimbrough TG et al. A conserved structural motif mediates formation of the periplasmic rings in the type III secretion system. Nat Struct Mol Biol 2009; 16:468–476 [View Article] [PubMed]
     [Google Scholar]
  28. Yip CK, Kimbrough TG, Felise HB, Vuckovic M, Thomas NA et al. Structural characterization of the molecular platform for type III secretion system assembly. Nature 2005; 435:702–707 [View Article] [PubMed]
     [Google Scholar]
  29. Worrall LJ, Hong C, Vuckovic M, Deng W, Bergeron JRC et al. Near-atomic-resolution cryo-EM analysis of the Salmonella T3S injectisome basal body. Nature 2016; 540:597–601 [View Article] [PubMed]
     [Google Scholar]
  30. Hu J, Worrall LJ, Hong C, Vuckovic M, Atkinson CE et al. Cryo-EM analysis of the T3S injectisome reveals the structure of the needle and open secretin. Nat Commun 2018; 9:3840 [View Article] [PubMed]
     [Google Scholar]
  31. Majewski DD, Okon M, Heinkel F, Robb CS, Vuckovic M et al. Characterization of the pilotin-secretin complex from the Salmonella enterica Type III secretion system using hybrid structural methods. Structure 2021; 29:125–138 [View Article] [PubMed]
     [Google Scholar]
  32. Burghout P, Beckers F, de Wit E, van Boxtel R, Cornelis GR et al. Role of the pilot protein YscW in the biogenesis of the YscC secretin in Yersinia enterocolitica. J Bacteriol 2004; 186:5366–5375 [View Article] [PubMed]
     [Google Scholar]
  33. Lunelli M, Kamprad A, Bürger J, Mielke T, Spahn CMT et al. Cryo-EM structure of the Shigella type III needle complex. PLoS Pathog 2020; 16:e1008263 [View Article] [PubMed]
     [Google Scholar]
  34. Goessweiner-Mohr N, Kotov V, Brunner MJ, Mayr J, Wald J et al. Structural control for the coordinated assembly into functional pathogenic type-3 secretion systems. Mol Biol 2019714097 [View Article]
     [Google Scholar]
  35. Hu B, Lara-Tejero M, Kong Q, Galán JE, Liu J. In situ molecular architecture of the Salmonella Type III secretion machine. Cell 2017; 168:1065–1074 [View Article] [PubMed]
     [Google Scholar]
  36. Ibuki T, Imada K, Minamino T, Kato T, Miyata T et al. Common architecture of the flagellar type III protein export apparatus and F- and V-type ATPases. Nat Struct Mol Biol 2011; 18:277–282 [View Article] [PubMed]
     [Google Scholar]
  37. Soto JE, Galán JE, Lara-Tejero M. Assembly and architecture of the type III secretion sorting platform. Proc Natl Acad Sci U S A 2022; 119:e2218010119 [View Article] [PubMed]
     [Google Scholar]
  38. Muthuramalingam M, Whittier SK, Lovell S, Battaile KP, Tachiyama S et al. The structures of SctK and SctD from Pseudomonas aeruginosa reveal the interface of the type III secretion system basal body and sorting platform. J Mol Biol 2020; 432:166693 [View Article] [PubMed]
     [Google Scholar]
  39. Diepold A, Sezgin E, Huseyin M, Mortimer T, Eggeling C et al. A dynamic and adaptive network of cytosolic interactions governs protein export by the T3SS injectisome. Nat Commun 2017; 8:15940 [View Article] [PubMed]
     [Google Scholar]
  40. Lara-Tejero M, Kato J, Wagner S, Liu X, Galán JE. A sorting platform determines the order of protein secretion in bacterial type III systems. Science 2011; 331:1188–1191 [View Article] [PubMed]
     [Google Scholar]
  41. Johnson S, Blocker A. Characterization of soluble complexes of the Shigella flexneri type III secretion system ATPase. FEMS Microbiol Lett 2008; 286:274–278 [View Article] [PubMed]
     [Google Scholar]
  42. Bzymek KP, Hamaoka BY, Ghosh P. Two translation products of Yersinia yscQ assemble to form a complex essential to type III secretion. Biochemistry 2012; 51:1669–1677 [View Article] [PubMed]
     [Google Scholar]
  43. McDowell MA, Marcoux J, McVicker G, Johnson S, Fong YH et al. Characterisation of Shigella Spa33 and Thermotoga FliM/N reveals a new model for C-ring assembly in T3SS. Mol Microbiol 2016; 99:749–766 [View Article] [PubMed]
     [Google Scholar]
  44. Diepold A, Kudryashev M, Delalez NJ, Berry RM, Armitage JP. Composition, formation, and regulation of the cytosolic C-ring, a dynamic component of the type III secretion injectisome. PLoS Biol 2015; 13:e1002039 [View Article] [PubMed]
     [Google Scholar]
  45. Bernal I, Börnicke J, Heidemann J, Svergun D, Horstmann JA et al. Molecular organization of soluble type III secretion system sorting platform complexes. J Mol Biol 2019; 431:3787–3803 [View Article] [PubMed]
     [Google Scholar]
  46. Yu X-J, Liu M, Matthews S, Holden DW. Tandem translation generates a chaperone for the Salmonella type III secretion system protein SsaQ. J Biol Chem 2011; 286:36098–36107 [View Article] [PubMed]
     [Google Scholar]
  47. Lara-Tejero M, Qin Z, Hu B, Butan C, Liu J et al. Role of SpaO in the assembly of the sorting platform of a Salmonella type III secretion system. PLoS Pathog 2019; 15:e1007565 [View Article] [PubMed]
     [Google Scholar]
  48. Notti RQ, Bhattacharya S, Lilic M, Stebbins CE. A common assembly module in injectisome and flagellar type III secretion sorting platforms. Nat Commun 2015; 6:7125 [View Article] [PubMed]
     [Google Scholar]
  49. Majewski DD, Worrall LJ, Hong C, Atkinson CE, Vuckovic M et al. Cryo-EM structure of the homohexameric T3SS ATPase-central stalk complex reveals rotary ATPase-like asymmetry. Nat Commun 2019; 10:626 [View Article] [PubMed]
     [Google Scholar]
  50. Akeda Y, Galán JE. Chaperone release and unfolding of substrates in type III secretion. Nature 2005; 437:911–915 [View Article] [PubMed]
     [Google Scholar]
  51. Jensen JL, Yamini S, Rietsch A, Spiller BW. The structure of the Type III secretion system export gate with CdsO, an ATPase lever arm. PLoS Pathog 2020; 16:e1008923 [View Article] [PubMed]
     [Google Scholar]
  52. Romo-Castillo M, Andrade A, Espinosa N, Monjarás Feria J, Soto E et al. EscO, a functional and structural analog of the flagellar FliJ protein, is a positive regulator of EscN ATPase activity of the enteropathogenic Escherichia coli injectisome. J Bacteriol 2014; 196:2227–2241 [View Article] [PubMed]
     [Google Scholar]
  53. Lorenzini E, Singer A, Singh B, Lam R, Skarina T et al. Structure and protein-protein interaction studies on Chlamydia trachomatis protein CT670 (YscO Homolog). J Bacteriol 2010; 192:2746–2756 [View Article] [PubMed]
     [Google Scholar]
  54. Xing Q, Shi K, Portaliou A, Rossi P, Economou A et al. Structures of chaperone-substrate complexes docked onto the export gate in a type III secretion system. Nat Commun 2018; 9:1773 [View Article] [PubMed]
     [Google Scholar]
  55. Torres-Vargas CE, Kronenberger T, Roos N, Dietsche T, Poso A et al. The inner rod of virulence-associated type III secretion systems constitutes a needle adapter of one helical turn that is deeply integrated into the system’s export apparatus. Mol Microbiol 2019; 112:918–931 [View Article] [PubMed]
     [Google Scholar]
  56. Loquet A, Sgourakis NG, Gupta R, Giller K, Riedel D et al. Atomic model of the type III secretion system needle. Nature 2012; 486:276–279 [View Article] [PubMed]
     [Google Scholar]
  57. Guo EZ, Desrosiers DC, Zalesak J, Tolchard J, Berbon M et al. A polymorphic helix of A Salmonella needle protein relays signals defining distinct steps in type III secretion. PLoS Biol 2019; 17:e3000351 [View Article] [PubMed]
     [Google Scholar]
  58. Park D, Lara-Tejero M, Waxham MN, Li W, Hu B et al. Visualization of the type III secretion mediated Salmonella-host cell interface using cryo-electron tomography. Elife 2018; 7:e39514 [View Article] [PubMed]
     [Google Scholar]
  59. Journet L, Agrain C, Broz P, Cornelis GR. The needle length of bacterial injectisomes is determined by a molecular ruler. Science 2003; 302:1757–1760 [View Article] [PubMed]
     [Google Scholar]
  60. Tamano K, Aizawa S, Katayama E, Nonaka T, Imajoh-Ohmi S et al. Supramolecular structure of the Shigella type III secretion machinery: the needle part is changeable in length and essential for delivery of effectors. EMBO J 2000; 19:3876–3887 [View Article] [PubMed]
     [Google Scholar]
  61. Rathinavelan T, Lara-Tejero M, Lefebre M, Chatterjee S, McShan AC et al. NMR model of PrgI-SipD interaction and its implications in the needle-tip assembly of the Salmonella type III secretion system. J Mol Biol 2014; 426:2958–2969 [View Article] [PubMed]
     [Google Scholar]
  62. Guo EZ, Galán JE. Cryo-EM structure of the needle filament tip complex of the Salmonella type III secretion injectisome. Proc Natl Acad Sci 2021; 118:e2114552118 [View Article] [PubMed]
     [Google Scholar]
  63. Broz P, Mueller CA, Müller SA, Philippsen A, Sorg I et al. Function and molecular architecture of the Yersinia injectisome tip complex. Mol Microbiol 2007; 65:1311–1320 [View Article] [PubMed]
     [Google Scholar]
  64. Johnson S, Roversi P, Espina M, Olive A, Deane JE et al. Self-chaperoning of the type III secretion system needle tip proteins IpaD and BipD. J Biol Chem 2007; 282:4035–4044 [View Article] [PubMed]
     [Google Scholar]
  65. Chatterjee S, Zhong D, Nordhues BA, Battaile KP, Lovell S et al. The crystal structures of the Salmonella type III secretion system tip protein SipD in complex with deoxycholate and chenodeoxycholate. Protein Sci 2011; 20:75–86 [View Article] [PubMed]
     [Google Scholar]
  66. Erskine PT, Knight MJ, Ruaux A, Mikolajek H, Wong Fat Sang N et al. High resolution structure of BipD: an invasion protein associated with the type III secretion system of Burkholderia pseudomallei. J Mol Biol 2006; 363:125–136 [View Article] [PubMed]
     [Google Scholar]
  67. Chaudhury S, Battaile KP, Lovell S, Plano GV, De Guzman RN. Structure of the Yersinia pestis tip protein LcrV refined to 1.65 Å resolution.. Acta Crystallogr Sect F Struct Biol Cryst Commun 2013477–481 [View Article]
     [Google Scholar]
  68. Gébus C, Faudry E, Bohn Y-ST, Elsen S, Attree I. Oligomerization of PcrV and LcrV, protective antigens of Pseudomonas aeruginosa and Yersinia pestis. J Biol Chem 2008; 283:23940–23949 [View Article] [PubMed]
     [Google Scholar]
  69. Lee P-C, Stopford CM, Svenson AG, Rietsch A. Control of effector export by the Pseudomonas aeruginosa type III secretion proteins PcrG and PcrV. Mol Microbiol 2010; 75:924–941 [View Article] [PubMed]
     [Google Scholar]
  70. Matson JS, Nilles ML. LcrG-LcrV interaction is required for control of Yops secretion in Yersinia pestis. J Bacteriol 2001; 183:5082–5091 [View Article] [PubMed]
     [Google Scholar]
  71. Matson JS, Nilles ML. Interaction of the Yersinia pestis type III regulatory proteins LcrG and LcrV occurs at a hydrophobic interface. BMC Microbiol 2002; 2:16 [View Article] [PubMed]
     [Google Scholar]
  72. Sekiya K, Ohishi M, Ogino T, Tamano K, Sasakawa C 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 U S A 2001; 98:11638–11643 [View Article] [PubMed]
     [Google Scholar]
  73. Wang YA, Yu X, Yip C, Strynadka NC, Egelman EH. Structural polymorphism in bacterial EspA filaments revealed by cryo-EM and an improved approach to helical reconstruction. Structure 2006; 14:1189–1196 [View Article] [PubMed]
     [Google Scholar]
  74. Daniell SJ, Kocsis E, Morris E, Knutton S, Booy FP et al. 3D structure of EspA filaments from enteropathogenic Escherichia coli. Mol Microbiol 2003; 49:301–308 [View Article] [PubMed]
     [Google Scholar]
  75. Lyons BJE, Atkinson CE, Deng W, Serapio-Palacios A, Finlay BB et al. Cryo-EM structure of the EspA filament from enteropathogenic Escherichia coli: revealing the mechanism of effector translocation in the T3SS. Structure 2021; 29:479–487 [View Article] [PubMed]
     [Google Scholar]
  76. Zheng W, Peña A, Ilangovan A, Baghshomali YN, Frankel G et al. Cryoelectron-microscopy structure of the enteropathogenic Escherichia coli type III secretion system EspA filament. Proc Natl Acad Sci U S A 2021; 118:e2022826118 [View Article] [PubMed]
     [Google Scholar]
  77. Creasey EA, Friedberg D, Shaw RK, Umanski T, Knutton S et al. CesAB is an enteropathogenic Escherichia coli chaperone for the type-III translocator proteins EspA and EspB. Microbiology 2003; 149:3639–3647 [View Article] [PubMed]
     [Google Scholar]
  78. Nguyen VS, Jobichen C, Tan KW, Tan YW, Chan SL et al. Structure of AcrH-AopB chaperone-translocator complex reveals a role for membrane hairpins in Type III secretion system translocon assembly. Structure 2015; 23:2022–2031 [View Article] [PubMed]
     [Google Scholar]
  79. Schreiner M, Niemann HH. Crystal structure of the Yersinia enterocolitica type III secretion chaperone SycD in complex with a peptide of the minor translocator YopD. BMC Struct Biol 2012; 12:13 [View Article] [PubMed]
     [Google Scholar]
  80. Lara-Tejero M, Galán JE. Salmonella enterica serovar typhimurium pathogenicity island 1-encoded type III secretion system translocases mediate intimate attachment to nonphagocytic cells. Infect Immun 2009; 77:2635–2642 [View Article] [PubMed]
     [Google Scholar]
  81. Kundracik E, Trichka J, Díaz Aponte J, Roistacher A, Rietsch A. PopB-PcrV interactions are essential for pore formation in the Pseudomonas aeruginosa Type III secretion system translocon. mBio 2022; 13:e0238122 [View Article] [PubMed]
     [Google Scholar]
  82. Ide T, Laarmann S, Greune L, Schillers H, Oberleithner H et al. Characterization of translocation pores inserted into plasma membranes by type III-secreted Esp proteins of enteropathogenic Escherichia coli. Cell Microbiol 2001; 3:669–679 [View Article] [PubMed]
     [Google Scholar]
  83. Srikanth CV, Mercado-Lubo R, Hallstrom K, McCormick BA. Salmonella effector proteins and host-cell responses. Cell Mol Life Sci 2011; 68:3687–3697 [View Article] [PubMed]
     [Google Scholar]
  84. Volk M, Vollmer I, Heroven AK, Dersch P. Transcriptional and post-transcriptional regulatory mechanisms controlling type III secretion. Curr Top Microbiol Immunol 2020; 427:11–33 [View Article] [PubMed]
     [Google Scholar]
  85. Westerhausen S, Nowak M, Torres-Vargas CE, Bilitewski U, Bohn E et al. A NanoLuc luciferase-based assay enabling the real-time analysis of protein secretion and injection by bacterial type III secretion systems. Mol Microbiol 2020; 113:1240–1254 [View Article] [PubMed]
     [Google Scholar]
  86. Wagner S, Königsmaier L, Lara-Tejero M, Lefebre M, Marlovits TC et al. Organization and coordinated assembly of the type III secretion export apparatus. Proc Natl Acad Sci 2010; 107:17745–17750 [View Article] [PubMed]
     [Google Scholar]
  87. Diepold A, Amstutz M, Abel S, Sorg I, Jenal U et al. Deciphering the assembly of the Yersinia type III secretion injectisome. EMBO J 2010; 29:1928–1940 [View Article] [PubMed]
     [Google Scholar]
  88. Sukhan A, Kubori T, Wilson J, Galán JE. Genetic analysis of assembly of the Salmonella enterica serovar Typhimurium type III secretion-associated needle complex. J Bacteriol 2001; 183:1159–1167 [View Article] [PubMed]
     [Google Scholar]
  89. Tseytin I, Dagan A, Oren S, Sal-Man N. The role of EscD in supporting EscC polymerization in the type III secretion system of enteropathogenic Escherichia coli. Biochim Biophys Acta Biomembr 2018; 1860:384–395 [View Article] [PubMed]
     [Google Scholar]
  90. Tachiyama S, Chang Y, Muthuramalingam M, Hu B, Barta ML et al. The cytoplasmic domain of MxiG interacts with MxiK and directs assembly of the sorting platform in the Shigella type III secretion system. J Biol Chem 2019; 294:19184–19196 [View Article] [PubMed]
     [Google Scholar]
  91. Diepold A, Wiesand U, Amstutz M, Cornelis GR. Assembly of the Yersinia injectisome: the missing pieces. Mol Microbiol 2012; 85:878–892 [View Article] [PubMed]
     [Google Scholar]
  92. Kato J, Dey S, Soto JE, Butan C, Wilkinson MC et al. A protein secreted by the Salmonella type III secretion system controls needle filament assembly. Elife 2018; 7:e35886 [View Article] [PubMed]
     [Google Scholar]
  93. Monlezun L, Liebl D, Fenel D, Grandjean T, Berry A et al. PscI is a type III secretion needle anchoring protein with in vitro polymerization capacities. Mol Microbiol 2015; 96:419–436 [View Article] [PubMed]
     [Google Scholar]
  94. Burkinshaw BJ, Deng W, Lameignère E, Wasney GA, Zhu H et al. Structural analysis of a specialized type III secretion system peptidoglycan-cleaving enzyme. J Biol Chem 2015; 290:10406–10417 [View Article] [PubMed]
     [Google Scholar]
  95. Poyraz O, Schmidt H, Seidel K, Delissen F, Ader C et al. Protein refolding is required for assembly of the type three secretion needle. Nat Struct Mol Biol 2010; 17:788–792 [View Article] [PubMed]
     [Google Scholar]
  96. Galán JE, Lara-Tejero M, Marlovits TC, Wagner S. Bacterial type III secretion systems: specialized nanomachines for protein delivery into target cells. Annu Rev Microbiol 2014; 68:415–438 [View Article] [PubMed]
     [Google Scholar]
  97. Wood SE, Jin J, Lloyd SA. YscP and YscU switch the substrate specificity of the Yersinia type III secretion system by regulating export of the inner rod protein YscI. J Bacteriol 2008; 190:4252–4262 [View Article] [PubMed]
     [Google Scholar]
  98. Sukhan A, Kubori T, Galán JE. Synthesis and localization of the Salmonella SPI-1 type III secretion needle complex proteins PrgI and PrgJ. J Bacteriol 2003; 185:3480–3483 [View Article] [PubMed]
     [Google Scholar]
  99. Monjarás Feria J, García-Gómez E, Espinosa N, Minamino T, Namba K et al. Role of EscP (Orf16) in injectisome biogenesis and regulation of type III protein secretion in enteropathogenic Escherichia coli. J Bacteriol 2012; 194:6029–6045 [View Article] [PubMed]
     [Google Scholar]
  100. Agrain C, Sorg I, Paroz C, Cornelis GR. Secretion of YscP from Yersinia enterocolitica is essential to control the length of the injectisome needle but not to change the type III secretion substrate specificity. Mol Microbiol 2005; 57:1415–1427 [View Article]
     [Google Scholar]
  101. Bergeron JRC, Fernández L, Wasney GA, Vuckovic M, Reffuveille F et al. The structure of a type 3 secretion system (T3SS) ruler protein suggests a molecular mechanism for needle length sensing. J Biol Chem 2016; 291:1676–1691 [View Article] [PubMed]
     [Google Scholar]
  102. Wagner S, Grin I, Malmsheimer S, Singh N, Torres-Vargas CE et al. Bacterial type III secretion systems: a complex device for the delivery of bacterial effector proteins into eukaryotic host cells. FEMS Microbiol Lett 2018; 365:fny201 [View Article] [PubMed]
     [Google Scholar]
  103. Erhardt M, Singer HM, Wee DH, Keener JP, Hughes KT. An infrequent molecular ruler controls flagellar hook length in Salmonella enterica. EMBO J 2011; 30:2948–2961 [View Article] [PubMed]
     [Google Scholar]
  104. Cheung M, Shen D-K, Makino F, Kato T, Roehrich AD et al. Three-dimensional electron microscopy reconstruction and cysteine-mediated crosslinking provide a model of the type III secretion system needle tip complex. Mol Microbiol 2015; 95:31–50 [View Article] [PubMed]
     [Google Scholar]
  105. Sory MP, Boland A, Lambermont I, Cornelis GR. Identification of the YopE and YopH domains required for secretion and internalization into the cytosol of macrophages, using the cyaA gene fusion approach. Proc Natl Acad Sci 1995; 92:11998–12002 [View Article] [PubMed]
     [Google Scholar]
  106. Lloyd SA, Norman M, Rosqvist R, Wolf-Watz H. Yersinia YopE is targeted for type III secretion by N-terminal, not mRNA, signals. Mol Microbiol 2001; 39:520–531 [View Article] [PubMed]
     [Google Scholar]
  107. Rüssmann H, Kubori T, Sauer J, Galán JE. Molecular and functional analysis of the type III secretion signal of the Salmonella enterica InvJ protein. Mol Microbiol 2002; 46:769–779 [View Article] [PubMed]
     [Google Scholar]
  108. Rosqvist R, Håkansson S, Forsberg A, Wolf-Watz H. Functional conservation of the secretion and translocation machinery for virulence proteins of Yersiniae, Salmonellae and Shigellae. EMBO J 1995; 14:4187–4195 [View Article] [PubMed]
     [Google Scholar]
  109. Frithz-Lindsten E, Holmström A, Jacobsson L, Soltani M, Olsson J et al. Functional conservation of the effector protein translocators PopB/YopB and PopD/YopD of Pseudomonas aeruginosa and Yersinia pseudotuberculosis. Mol Microbiol 1998; 29:1155–1165 [View Article] [PubMed]
     [Google Scholar]
  110. Anderson DM, Fouts DE, Collmer A, Schneewind O. Reciprocal secretion of proteins by the bacterial type III machines of plant and animal pathogens suggests universal recognition of mRNA targeting signals. Proc Natl Acad Sci 1999; 96:12839–12843 [View Article] [PubMed]
     [Google Scholar]
  111. Subtil A, Parsot C, Dautry-Varsat A. Secretion of predicted Inc proteins of Chlamydia pneumoniae by a heterologous type III machinery. Mol Microbiol 2001; 39:792–800 [View Article] [PubMed]
     [Google Scholar]
  112. Samudrala R, Heffron F, McDermott JE. Accurate prediction of secreted substrates and identification of a conserved putative secretion signal for type III secretion systems. PLoS Pathog 2009; 5:e1000375 [View Article] [PubMed]
     [Google Scholar]
  113. Wang Y, Zhang Q, Sun M-A, Guo D. High-accuracy prediction of bacterial type III secreted effectors based on position-specific amino acid composition profiles. Bioinformatics 2011; 27:777–784 [View Article] [PubMed]
     [Google Scholar]
  114. Allen-Vercoe E, Toh MCW, Waddell B, Ho H, DeVinney R. A carboxy-terminal domain of Tir from enterohemorrhagic Escherichia coli O157:H7 (EHEC O157:H7) required for efficient type III secretion. FEMS Microbiol Lett 2005; 243:355–364 [View Article] [PubMed]
     [Google Scholar]
  115. Kim BH, Kim HG, Kim JS, Jang JI, Park YK. Analysis of functional domains present in the N-terminus of the SipB protein. Microbiology 2007; 153:2998–3008 [View Article] [PubMed]
     [Google Scholar]
  116. Tomalka AG, Stopford CM, Lee PC, Rietsch A. A translocator-specific export signal establishes the translocator-effector secretion hierarchy that is important for type III secretion system function. Mol Microbiol 2012; 86:1464–1481 [View Article] [PubMed]
     [Google Scholar]
  117. Ramamurthi KS, Schneewind O. Yersinia yopQ mRNA encodes a bipartite type III secretion signal in the first 15 codons. Mol Microbiol 2003; 50:1189–1198 [View Article]
     [Google Scholar]
  118. Cheng LW, Anderson DM, Schneewind O. Two independent type III secretion mechanisms for YopE in Yersinia enterocolitica. Mol Microbiol 1997; 24:757–765 [View Article] [PubMed]
     [Google Scholar]
  119. Stebbins CE, Galán JE. Maintenance of an unfolded polypeptide by a cognate chaperone in bacterial type III secretion. Nature 2001; 414:77–81 [View Article] [PubMed]
     [Google Scholar]
  120. Tucker SC, Galán JE. Complex function for SicA, a Salmonella enterica serovar typhimurium type III secretion-associated chaperone. J Bacteriol 2000; 182:2262–2268 [View Article] [PubMed]
     [Google Scholar]
  121. Krampen L, Malmsheimer S, Grin I, Trunk T, Lührmann A et al. Revealing the mechanisms of membrane protein export by virulence-associated bacterial secretion systems. Nat Commun 2018; 9:3467 [View Article] [PubMed]
     [Google Scholar]
  122. Letzelter M, Sorg I, Mota LJ, Meyer S, Stalder J et al. The discovery of SycO highlights a new function for type III secretion effector chaperones. EMBO J 2006; 25:3223–3233 [View Article] [PubMed]
     [Google Scholar]
  123. Portaliou AG, Tsolis KC, Loos MS, Balabanidou V, Rayo J et al. Hierarchical protein targeting and secretion is controlled by an affinity switch in the type III secretion system of enteropathogenic Escherichia coli. EMBO J 2017; 36:3517–3531 [View Article] [PubMed]
     [Google Scholar]
  124. Ernst NH, Reeves AZ, Ramseyer JE, Lesser CF. High-throughput screening of Type III secretion determinants reveals a major chaperone-independent pathway. mBio 2018; 9:e01050-18 [View Article] [PubMed]
     [Google Scholar]
  125. Parsot C, Hamiaux C, Page A-L. The various and varying roles of specific chaperones in type III secretion systems. Curr Opin Microbiol 2003; 6:7–14 [View Article] [PubMed]
     [Google Scholar]
  126. Sun P, Tropea JE, Austin BP, Cherry S, Waugh DS. Structural characterization of the Yersinia pestis type III secretion system needle protein YscF in complex with its heterodimeric chaperone YscE/YscG. J Mol Biol 2008; 377:819–830 [View Article] [PubMed]
     [Google Scholar]
  127. Quinaud M, Chabert J, Faudry E, Neumann E, Lemaire D et al. The PscE-PscF-PscG complex controls type III secretion needle biogenesis in Pseudomonas aeruginosa. J Biol Chem 2005; 280:36293–36300 [View Article] [PubMed]
     [Google Scholar]
  128. Evdokimov AG, Phan J, Tropea JE, Routzahn KM, Peters HK et al. Similar modes of polypeptide recognition by export chaperones in flagellar biosynthesis and type III secretion. Nat Struct Biol 2003; 10:789–793 [View Article] [PubMed]
     [Google Scholar]
  129. Muskotál A, Király R, Sebestyén A, Gugolya Z, Végh BM et al. Interaction of FliS flagellar chaperone with flagellin. FEBS Lett 2006; 580:3916–3920 [View Article] [PubMed]
     [Google Scholar]
  130. Yip CK, Finlay BB, Strynadka NCJ. Structural characterization of a type III secretion system filament protein in complex with its chaperone. Nat Struct Mol Biol 2005; 12:75–81 [View Article] [PubMed]
     [Google Scholar]
  131. Souza C de A, Richards KL, Park Y, Schwartz M, Torruellas Garcia J et al. The YscE/YscG chaperone and YscF N-terminal sequences target YscF to the Yersinia pestis type III secretion apparatus. Microbiology 2018; 164:338–348 [View Article] [PubMed]
     [Google Scholar]
  132. Lee VT, Schneewind O. Yop fusions to tightly folded protein domains and their effects on Yersinia enterocolitica type III secretion. J Bacteriol 2002; 184:3740–3745 [View Article] [PubMed]
     [Google Scholar]
  133. Feldman MF, Müller S, Wüest E, Cornelis GR. SycE allows secretion of YopE-DHFR hybrids by the Yersinia enterocolitica type III Ysc system. Mol Microbiol 2002; 46:1183–1197 [View Article] [PubMed]
     [Google Scholar]
  134. Radics J, Königsmaier L, Marlovits TC. Structure of a pathogenic type 3 secretion system in action. Nat Struct Mol Biol 2014; 21:82–87 [View Article] [PubMed]
     [Google Scholar]
  135. LeBlanc MA, Fink MR, Perkins TT, Sousa MC. Type III secretion system effector proteins are mechanically labile. Proc Natl Acad Sci 2021; 118:12 [View Article] [PubMed]
     [Google Scholar]
  136. Zhang Y, Lara-Tejero M, Bewersdorf J, Galán JE. Visualization and characterization of individual type III protein secretion machines in live bacteria. Proc Natl Acad Sci U S A 2017; 114:6098–6103 [View Article] [PubMed]
     [Google Scholar]
  137. Schlumberger MC, Müller AJ, Ehrbar K, Winnen B, Duss I et al. Real-time imaging of type III secretion: Salmonella SipA injection into host cells. Proc Natl Acad Sci U S A 2005; 102:12548–12553 [View Article] [PubMed]
     [Google Scholar]
  138. Portaliou AG, Tsolis KC, Loos MS, Balabanidou V, Rayo J et al. Hierarchical protein targeting and secretion is controlled by an affinity switch in the type III secretion system of enteropathogenic Escherichia coli. EMBO J 2017; 36:3517–3531 [View Article] [PubMed]
     [Google Scholar]
  139. Gilzer D, Schreiner M, Niemann HH. Direct interaction of a chaperone-bound type III secretion substrate with the export gate. Nat Commun 2022; 13:2858 [View Article] [PubMed]
     [Google Scholar]
  140. Yu X-J, Grabe GJ, Liu M, Mota LJ, Holden DW. SsaV interacts with SsaL to control the translocon-to-effector switch in the Salmonella SPI-2 Type three secretion system. mBio 2018; 9:e01149-18 [View Article] [PubMed]
     [Google Scholar]
  141. Shen D-K, Blocker AJ. MxiA, MxiC and IpaD regulate substrate selection and secretion mode in the T3SS of Shigella flexneri. PLoS One 2016; 11:e0155141 [View Article] [PubMed]
     [Google Scholar]
  142. Gaytán MO, Monjarás Feria J, Soto E, Espinosa N, Benítez JM et al. Novel insights into the mechanism of SepL-mediated control of effector secretion in enteropathogenic Escherichia coli. MicrobiologyOpen 2018; 7:e00571 [View Article] [PubMed]
     [Google Scholar]
  143. Kubori T, Galán JE. Salmonella type III secretion-associated protein InvE controls translocation of effector proteins into host cells. J Bacteriol 2002; 184:4699–4708 [View Article] [PubMed]
     [Google Scholar]
  144. Botteaux A, Sory MP, Biskri L, Parsot C, Allaoui A. MxiC is secreted by and controls the substrate specificity of the Shigella flexneri type III secretion apparatus. Mol Microbiol 2009; 71:449–460 [View Article] [PubMed]
     [Google Scholar]
  145. Pienkoß S, Javadi S, Chaoprasid P, Nolte T, Twittenhoff C et al. The gatekeeper of Yersinia type III secretion is under RNA thermometer control. PLoS Pathog 2021; 17:e1009650 [View Article] [PubMed]
     [Google Scholar]
  146. Ngo T-D, Perdu C, Jneid B, Ragno M, Novion Ducassou J et al. The PopN gate-keeper complex acts on the ATPase PscN to regulate the T3SS secretion switch from early to middle substrates in Pseudomonas aeruginosa. J Mol Biol 2020; 432:166690 [View Article] [PubMed]
     [Google Scholar]
  147. Erhardt M, Wheatley P, Kim EA, Hirano T, Zhang Y et al. Mechanism of type-III protein secretion: Regulation of FlhA conformation by a functionally critical charged-residue cluster. Mol Microbiol 2017; 104:234–249 [View Article] [PubMed]
     [Google Scholar]
  148. Minamino T, Morimoto YV, Hara N, Namba K. An energy transduction mechanism used in bacterial flagellar type III protein export. Nat Commun 2011; 2:475 [View Article] [PubMed]
     [Google Scholar]
  149. Minamino T, Namba K. Distinct roles of the FliI ATPase and proton motive force in bacterial flagellar protein export. Nature 2008; 451:485–488 [View Article] [PubMed]
     [Google Scholar]
  150. Erhardt M, Mertens ME, Fabiani FD, Hughes KT. ATPase-independent type-III protein secretion in Salmonella enterica. PLoS Genet 2014; 10:e1004800 [View Article] [PubMed]
     [Google Scholar]
  151. Paul K, Erhardt M, Hirano T, Blair DF, Hughes KT. Energy source of flagellar type III secretion. Nature 2008; 451:489–492 [View Article] [PubMed]
     [Google Scholar]
  152. Renault TT, Abraham AO, Bergmiller T, Paradis G, Rainville S et al. Bacterial flagella grow through an injection-diffusion mechanism. Elife 2017; 6:e23136 [View Article] [PubMed]
     [Google Scholar]
  153. Jumper J, Evans R, Pritzel A, Green T, Figurnov M et al. Highly accurate protein structure prediction with AlphaFold. Nature 2021; 596:583–589 [View Article] [PubMed]
     [Google Scholar]
  154. Bryant P, Pozzati G, Elofsson A. Improved prediction of protein-protein interactions using AlphaFold2. Nat Commun 2022; 13:1265 [View Article] [PubMed]
     [Google Scholar]
  155. Wagner S, Diepold A. A unified nomenclature for injectisome-type type III secretion systems. Curr Top Microbiol Immunol 2020; 427:1–10 [View Article] [PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.001328
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Virulence-associated type III secretion systems in Gram-negative bacteria
Microbiology 169, 001328 (2023); https://doi.org/10.1099/mic.0.001328
/content/journal/micro/10.1099/mic.0.001328
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