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Molecular Organization and Assembly of the Export Apparatus of Flagellar Type III Secretion Systems

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Bacterial Type III Protein Secretion Systems

Part of the book series: Current Topics in Microbiology and Immunology ((CT MICROBIOLOGY,volume 427))

Abstract

The bacterial flagellum is a supramolecular motility machine consisting of the basal body, the hook, and the filament. For construction of the flagellum beyond the cellular membranes, a type III protein export apparatus uses ATP and proton-motive force (PMF) across the cytoplasmic membrane as the energy sources to transport flagellar component proteins from the cytoplasm to the distal end of the growing flagellar structure. The protein export apparatus consists of a PMF-driven transmembrane export gate complex and a cytoplasmic ATPase complex. In addition, the basal body C ring acts as a sorting platform for the cytoplasmic ATPase complex that efficiently brings export substrates and type III export chaperone–substrate complexes from the cytoplasm to the export gate complex. In this book chapter, we will summarize our current understanding of molecular organization and assembly of the flagellar type III protein export apparatus.

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References

  • Abrusci P, Vergara-Irigaray M, Johnson S, Beeby MD, Hendrixson DR, Roversi P, Friede ME, Deane JE, Jensen GJ, Tang CM, Lea SM (2013) Architecture of the major component of the type III secretion system export apparatus. Nat Struct Mol Biol 20:99–104

    CAS  PubMed  Google Scholar 

  • Bai F, Morimoto YV, Yoshimura SDJ, Hara N, Kami-ike N, Namba K, Minamino T (2014) Assembly dynamics and the roles of FliI ATPase of the bacterial flagellar export apparatus. Sci Rep 4:6528

    CAS  PubMed  PubMed Central  Google Scholar 

  • Baker MA, Hynson RM, Ganuelas LA, Mohammadi NS, Liew CW, Rey AA, Duff AP, Whitten AE, Jeffries CM, Delalez NJ, Morimoto YV, Stock D, Armitage JP, Turberfield AJ, Namba K, Berry RM, Lee LK (2016) Domain-swap polymerization drives the self-assembly of the bacterial flagellar motor. Nat Struct Mol Biol 23:197–203

    CAS  PubMed  Google Scholar 

  • Bange G, KĂĽmmerer 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. Proc Natl Acad Sci USA 107:11295–11300

    CAS  PubMed  Google Scholar 

  • Barker CS, Samatey FA (2012) Cross-complementation study of the flagellar type III export apparatus membrane protein FlhB. PLoS ONE 7:e44030

    CAS  PubMed  PubMed Central  Google Scholar 

  • Barker CS, Meshcheryakova IV, Kostyukova AS, Samatey FA (2010) FliO regulation of FliP in the formation of the Salmonella enterica flagellum. PLoS Genet 6:e1001143

    PubMed  PubMed Central  Google Scholar 

  • Berg HC (2003) The rotary motor of bacterial flagella. Ann Rev Biochem 72:19–54

    CAS  PubMed  Google Scholar 

  • Chen S, Beeby M, Murphy GE, Leadbetter JR, Hendrixson DR, Briegel A, Li Z, Shi J, Tocheva EI, MĂĽller A, Dobro MJ, Jensen GJ (2011) Structural diversity of bacterial flagellar motors. EMBO J 30:2972–2981

    CAS  PubMed  PubMed Central  Google Scholar 

  • Claret L, Susannah CR, Higgins M, Hughes C (2003) Oligomerization and activation of the FliI ATPase central to bacterial flagellum assembly. Mol Microbiol 48:1349–1355

    CAS  PubMed  PubMed Central  Google Scholar 

  • Diepold A, Wiesand U, Cornelis GR (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. Mol Microbiol 82:502–514

    PubMed  Google Scholar 

  • Diepold A, Kudryashev M, Delalez NJ, Berry RM, Armitage JP (2015) Composition, formation, and regulation of the cytosolic C-ring, a dynamic component of the type III secretion injectisome. PLoS Biol 13(1):e1002039

    PubMed  PubMed Central  Google Scholar 

  • Diepold A, Sezgin E, Huseyin M, Mortimer T, Eggeling C, Armitage JP (2017) A dynamic and adaptive network of cytosolic interactions governs protein export by the T3SS injectisome. Nat Commun 8:15940

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dietsche T, Tesfazgi Mebrhatu M, Brunner MJ, Abrusci P, Yan J, Franz-Wachtel M, Schärfe C, Zilkenat S, Grin I, Galán JE, Kohlbacher O, Lea S, Macek B, Marlovits TC, Robinson CV, Wagner S (2016) Structural and functional characterization of the bacterial type III secretion export apparatus. PLoS Pathog 12:e1006071

    PubMed  PubMed Central  Google Scholar 

  • Erhardt M, Wheatley P, Kim EA, Hirano T, Zhang Y, Sarkar MK, Hughes KT, Blair DF (2017) Mechanism of type-III protein secretion: regulation of FlhA conformation by a functionally critical charged-residue cluster. Mol Microbiol 104:234–249

    CAS  PubMed  PubMed Central  Google Scholar 

  • Evans LD, Poulter S, Terentjev EM, Hughes C, Fraser GM (2013) A chain mechanism for flagellum growth. Nature 504:287–290

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fabiani FD, Renault TT, Peters B, Dietsche T, Gálvez EJC, Guse A, Freier K, Charpentier E, Strowig T, Franz-Wachtel M, Macek B, Wagner S, Hensel M, Erhardt M (2017) A flagellum-specific chaperone facilitates assembly of the core type III export apparatus of the bacterial flagellum. PLoS Biol 15:e2002267

    PubMed  PubMed Central  Google Scholar 

  • Fan F, Macnab RM (1996) Enzymatic characterization of FliI: an ATPase involved in flagellar assembly in Salmonella typhimurium. J Biol Chem 271:31981–31988

    CAS  PubMed  Google Scholar 

  • Ferris HU, Furukawa Y, Minamino T, Kroetz MB, Kihara M, Namba K, Macnab RM (2005) FlhB regulates ordered export of flagellar components via autocleavage mechanism. J Biol Chem 280:41236–41242

    CAS  PubMed  Google Scholar 

  • Fraser GM, Hirano T, Ferris HU, Devgan LL, Kihara M, Macnab RM (2003) Substrate specificity of type III flagellar protein export in Salmonella is controlled by subdomain interactions in FlhB. Mol Microbiol 48:1043–1057

    CAS  PubMed  Google Scholar 

  • Fukumura T, Makino F, Dietsche T, Kinoshita M, Kato T, Wagner S, Namba K, Imada K, Minamino T (2017) Assembly and stoichiometry of the core structure of the bacterial flagellar type III export gate complex. PLoS Biol 15:e2002281

    PubMed  PubMed Central  Google Scholar 

  • Furukawa Y, Inoue Y, Sakaguchi A, Mori Y, Fukumura T, Miyata T, Namba K, Minamino T (2016) Structural stability of flagellin subunits affects the rate of flagellin export in the absence of FliS chaperone. Mol Microbiol 102:405–416

    CAS  PubMed  Google Scholar 

  • Galán JE, Lara-Tejero M, Marlovits TC, Wagner S (2014) Bacterial type III secretion systems: specialized nanomachines for protein delivery into target cells. Annu Rev Microbiol 68:415–438

    PubMed  PubMed Central  Google Scholar 

  • González-Pedrajo B, Fraser GM, Minamino T, Macnab RM (2002) Molecular dissection of Salmonella FliH, a regulator of the ATPase FliI and the type III flagellar protein export pathway. Mol Microbiol 45:967–982

    PubMed  Google Scholar 

  • González-Pedrajo B, Minamino T, Kihara M, Namba K (2006) Interactions between C ring proteins and export apparatus components: a possible mechanism for facilitating type III protein export. Mol Microbiol 60:984–998

    PubMed  Google Scholar 

  • Hara N, Namba K, Minamino T (2011) Genetic characterization of conserved charged residues in the bacterial flagellar type III export protein FlhA. PLoS ONE 6:e22417

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hara N, Morimoto YV, Kawamoto A, Namba K, Minamino T (2012) Interaction of the extreme N-terminal region of FliH with FlhA is required for efficient bacterial flagellar protein export. J Bacteriol 194:5353–5360

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hu B, Morado DR, Margolin W, Rohde JR, Arizmendi O, Picking WL, Picking WD, Liu J (2015) Visualization of the type III secretion sorting platform of Shigella flexneri. Proc Natl Acad Sci USA 112:1047–1052

    CAS  PubMed  Google Scholar 

  • Hu B, Lara-Tejero M, Kong Q, Galán JE, Liu J (2017) In situ molecular architecture of the Salmonella type III secretion machine. Cell 168:1065–1074

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ibuki T, Imada K, Minamino T, Kato T, Miyata T, Namba K (2011) Common architecture between the flagellar protein export apparatus and F- and V-ATPases. Nat Struct Mol Biol 18:277–282

    CAS  PubMed  Google Scholar 

  • Ibuki T, Uchida Y, Hironaka Y, Namba K, Imada K, Minamino T (2013) Interaction between FliJ and FlhA, components of the bacterial flagellar type III export apparatus. J Bacteriol 195:466–473

    CAS  PubMed  PubMed Central  Google Scholar 

  • Imada K, Minamino T, Tahara A, Namba K (2007) Structural similarity between the flagellar type III ATPase FliI and F1-ATPase subunits. Proc Natl Acad Sci USA 104:485–490

    CAS  PubMed  Google Scholar 

  • Imada K, Minamino T, Kinoshita M, Furukawa Y, Namba K (2010) Structural insight into the regulatory mechanisms of interactions of the flagellar type III chaperone FliT with its binding partners. Proc Natl Acad Sci USA 107:8812–8817

    CAS  PubMed  Google Scholar 

  • Imada K, Minamino T, Uchida Y, Kinoshita M, Namba K (2016) Insight into the flagella type III export revealed by the complex structure of the type III ATPase and its regulator. Proc Natl Acad Sci USA 113:3633–3638

    CAS  PubMed  Google Scholar 

  • Inoue Y, Morimoto YV, Namba K, Minamino T (2018) Novel insights into the mechanism of well-ordered assembly of bacterial flagellar proteins in Salmonella. Sci Rep 8:1787

    PubMed  PubMed Central  Google Scholar 

  • Kawamoto A, Morimoto YV, Miyata T, Minamino T, Hughes KT, Kato T, Namba K (2013) Common and distinct structural features of Salmonella injectisome and flagellar basal body. Sci Rep 3:3369

    PubMed  PubMed Central  Google Scholar 

  • Kazetani K, Minamino T, Miyata T, Kato T, Namba K (2009) ATP-induced FliI hexamerization facilitates bacterial flagellar protein export. Biochem Biophys Res Commun 388:323–327

    CAS  PubMed  Google Scholar 

  • Kihara M, Miller GU, Macnab RM (2000) Deletion analysis of the flagellar switch protein FliG of Salmonella. J Bacteriol 182:3022–3028

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kihara M, Minamino T, Yamaguchi S, Macnab RM (2001) Intergenic suppression between the flagellar MS ring protein FliF of Salmonella and FlhA, a membrane component of its export apparatus. J Bacteriol 183:1655–1662

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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. Mol Microbiol 90:1249–1261

    CAS  PubMed  Google Scholar 

  • Kinoshita M, Nakanishi Y, Furukawa Y, Namba K, Imada K, Minamino T (2016) Rearrangements of α-helical structures of FlgN chaperone control the binding affinity for its cognate substrates during flagellar type III export. Mol Microbiol 101:656–670

    CAS  PubMed  Google Scholar 

  • Kinoshita M, Aizawa S, Inoue Y, Namba K, Minamino T (2017) The role of intrinsically disordered C-terminal region of FliK in substrate specificity switching of the bacterial flagellar type III export. Mol Microbiol 105:572–588

    CAS  PubMed  Google Scholar 

  • Kinoshita M, Furukawa Y, Uchiyama S, Imada K, Namba K, Minamino T (2018a) Insight into adaptive remodeling of the rotor ring complex of the bacterial flagellar motor. Biochem Biophys Res Commun 496:12–17

    CAS  PubMed  Google Scholar 

  • Kinoshita M, Namba K, Minamino T. (2018) Effect of a clockwise-locked deletion in FliG on the FliG ring structure of the bacterial flagellar motor. Genes Cells 23:241–247 (2018)

    Google Scholar 

  • Kubori T, Shimamoto N, Yamaguchi S, Namba K, Aizawa S (1992) Morphological pathway of flagellar assembly in Salmonella typhimurium. J Mol Biol 226:433–446

    CAS  PubMed  Google Scholar 

  • Kuhlen L, Abrusci P, Johnson S, Gault J, Deme J, Caesar J, Dietsche T, Mebrhatu MT, Ganief T, Macek B, Wagner S, Robinson CV, Lea SM (2018) Structure of the core of the type III secretion system export apparatus. Nat Struct Mol Biol 25:583–590

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kutsukake K, Minamino T, Yokoseki T (1994) Isolation and characterization of FliK-independent flagellation mutants from Salmonella typhimurium. J Bacteriol 176:7625–7629

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lara-Tejero M, Kato J, Wagner S, Liu X, Galán JE (2011) A sorting platform determines the order of protein secretion in bacterial type III systems. Science 331:1188–1191

    CAS  PubMed  Google Scholar 

  • Lee KL, Ginsburg MA, Crovace C, Donohoe M, Stock D (2010) Structure of the torque ring of the flagellar motor and the molecular basis for rotational switching. Nature 466:996–1000

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lee PC, Zmina SE, Stopford CM, Toska J, Rietsch A (2014) Control of type III secretion activity and substrate specificity by the cytoplasmic regulator PcrG. Proc Natl Acad Sci USA 111:2027–2036

    Google Scholar 

  • Li H, Sourjik V (2011) Assembly and stability of flagellar motor in Escherichia coli. Mol Microbiol 80:886–899

    CAS  PubMed  Google Scholar 

  • Lynch MJ, Levenson R, Kim EA, Sircar R, Blair DF, Dahlquist FW, Crane BR (2017) Co-folding of a FliF-FliG split domain forms the basis of the MS: C ring interface within the bacterial flagellar motor. Structure 25:317–328

    CAS  PubMed  PubMed Central  Google Scholar 

  • Macnab RM (2004) Type III flagellar protein export and flagellar assembly. Biochim Biophys Acta 1694:207–217

    CAS  PubMed  Google Scholar 

  • Makino F, Shen D, Kajimura N, Kawamoto A, Pissaridou P, Oswin H, Pain M, Murillo I, Namba K, Blocker AJ (2016) The architecture of the cytoplasmic region of type III secretion systems. Sci Rep 6:33341

    CAS  PubMed  PubMed Central  Google Scholar 

  • McDowell MA, Marcoux J, McVicker G, Johnson S, Fong YH, Stevens R, Bowman LA, Degiacomi MT, Yan J, Wise A, Friede ME, Benesch JL, Deane JE, Tang CM, Robinson CV, Lea SM (2016) Characterisation of Shigella Spa33 and Thermotoga FliM/N reveals a new model for C-ring assembly in T3SS. Mol Microbiol 99:749–766

    CAS  PubMed  Google Scholar 

  • McMurry JL, Murphy JW, González-Pedrajo B (2006) The FliN-FliH interaction mediates localization of flagellar export ATPase FliI to the C ring complex. Biochemistry 45:11790–11798

    CAS  PubMed  Google Scholar 

  • Meshcheryakov VA, Kitao A, Matsunami H, Samatey FA (2013) Inhibition of a type III secretion system by the deletion of a short loop in one of its membrane proteins. Acta Crystallogr D Biol Crystallogr 69:812–820

    CAS  PubMed  PubMed Central  Google Scholar 

  • Minamino T (2014) Protein export through the bacterial flagellar type III export pathway. Biochim Biophys Acta 1843:1642–1648

    CAS  PubMed  Google Scholar 

  • Minamino T (2018) Hierarchical protein export mechanism of the bacterial flagellar type III protein export apparatus. FEMS Microbiol Lett 365:fny117

    Google Scholar 

  • Minamino T, Macnab RM (1999) Components of the Salmonella flagellar export apparatus and classification of export substrates. J Bacteriol 181:1388–1394

    CAS  PubMed  PubMed Central  Google Scholar 

  • Minamino T, Macnab RM (2000a) Domain structure of Salmonella FlhB, a flagellar export component responsible for substrate specificity switching. J Bacteriol 182:4906–4919

    CAS  PubMed  PubMed Central  Google Scholar 

  • Minamino T, Macnab RM (2000b) FliH, a soluble component of the type III flagellar export apparatus of Salmonella, forms a complex with FliI and inhibits its ATPase activity. Mol Microbiol 37:1494–1503

    CAS  PubMed  Google Scholar 

  • Minamino T, Macnab RM (2000c) Interactions among components of the Salmonella flagellar export apparatus and its substrates. Mol Microbiol 35:1052–1064

    CAS  PubMed  Google Scholar 

  • Minamino T, Namba K (2008) Distinct roles of the FliI ATPase and proton motive force in bacterial flagellar protein export. Nature 451:485–488

    CAS  PubMed  Google Scholar 

  • Minamino T, Iino T, Kutuskake K (1994) Molecular characterization of the Salmonella typhimurium flhB operon and its protein products. J Bacteriol 176:7630–7637

    CAS  PubMed  PubMed Central  Google Scholar 

  • Minamino T, Tame JRH, Namba K, Macnab RM (2001) Proteolytic analysis of the FliH/FliI complex, the ATPase component of the type III flagellar export apparatus of Salmonella. J Mol Biol 312:1027–1036

    CAS  PubMed  Google Scholar 

  • Minamino T, González-Pedrajo B, Oosawa K, Namba K, Macnab RM (2002) Structural properties of FliH, an ATPase regulatory component of the Salmonella type III flagellar export apparatus. J Mol Biol 322:281–290

    CAS  PubMed  Google Scholar 

  • Minamino T, Imada K, Namba K (2008) Mechanisms of type III protein export for bacterial flagellar assembly. Mol BioSyst 4:1105–1111

    CAS  PubMed  Google Scholar 

  • Minamino T, Yoshimura SDJ, Morimoto YV, González-Pedrajo B, Kami-ike N, Namba K (2009) Roles of the extreme N-terminal region of FliH for efficient localization of the FliH-FliI complex to the bacterial flagellar type III export apparatus. Mol Microbiol 74:1471–1483

    CAS  PubMed  Google Scholar 

  • Minamino T, Morimoto YV, Hara N, Namba K (2011) An energy transduction mechanism used in bacterial type III protein export. Nat Commun 2:475

    PubMed  PubMed Central  Google Scholar 

  • Minamino T, Kinoshita M, Hara N, Takeuchi S, Hida A, Koya S, Glenwright H, Imada K, Aldridge PD, Namba K (2012a) Interaction of a bacterial flagellar chaperone FlgN with FlhA is required for efficient export of its cognate substrates. Mol Microbiol 83:775–788

    CAS  PubMed  Google Scholar 

  • Minamino T, Kinoshita M, Imada K, Namba K (2012b) Interaction between FliI ATPase and a flagellar chaperone FliT during bacterial flagellar export. Mol Microbiol 83:168–178

    CAS  PubMed  Google Scholar 

  • Minamino T, Morimoto YV, Kinoshita M, Aldridge PD, Namba K (2014) The bacterial flagellar protein export apparatus processively transports flagellar proteins even with extremely infrequent ATP hydrolysis. Sci Rep 4:7579

    CAS  PubMed  PubMed Central  Google Scholar 

  • Minamino T, Morimoto YV, Hara N, Aldridge PD, Namba K (2016) The Bacterial flagellar type III export gate complex is a dual fuel engine that can use both H+ and Na+ for flagellar protein export. PLoS Pathog 12:e1005495

    PubMed  PubMed Central  Google Scholar 

  • Moore SA, Jia Y (2010) Structure of the cytoplasmic domain of the flagellar secretion apparatus component FlhA from Helicobacter pylori. J Biol Chem 285:21060–21069

    CAS  PubMed  PubMed Central  Google Scholar 

  • Morimoto YV, Minamino T (2014) Structure and function of the bi-directional bacterial flagellar motor. Biomolecules 4:217–234

    PubMed  PubMed Central  Google Scholar 

  • Morimoto YV, Ito M, Hiraoka KD, Che Y-S, Bai F, Kami-ike N, Namba K, Minamino T (2014) Assembly and stoichiometry of FliF and FlhA in Salmonella flagellar basal body. Mol Microbiol 91:1214–1226

    CAS  PubMed  Google Scholar 

  • Morimoto YV, Kami-ike N, Miyata T, Kawamoto A, Kato T, Namba K, Minamino T (2016) High-resolution pH imaging of living bacterial cell to detect local pH differences. mBio 7:e01911-16

    Google Scholar 

  • Notti RQ, Bhattacharya S, Lilic M, Stebbins CE (2015) A common assembly module in injectisome and flagellar type III secretion sorting platforms. Nat Commun 6:7125

    PubMed  PubMed Central  Google Scholar 

  • Ohnishi K, Fan F, Schoenhals GJ, Kihara M, Macnab RM (1997) The FliO, FliP, FliQ, and FliR proteins of Salmonella typhimurium: putative components for flagellar assembly. J Bacteriol 179:6092–6099

    CAS  PubMed  PubMed Central  Google Scholar 

  • Okabe M, Minamino T, Imada K, Namba K, Kihara M (2009) Role of the N-terminal domain of FliI ATPase in bacterial flagellar protein export. FEBS Lett 583:743–748

    CAS  PubMed  Google Scholar 

  • Park SY, Lowder B, Bilwes AM, Blair DF, Crane BR (2006) Structure of FliM provides insight into assembly of the switch complex in the bacterial flagella motor. Proc Natl Acad Sci USA 103:11886–11891

    CAS  PubMed  Google Scholar 

  • Paul K, Harmon JG, Blair DF (2006) Mutational analysis of the flagellar rotor protein FliN: identification of surfaces important for flagellar assembly and switching. J Bacteriol 188:5240–5248

    CAS  PubMed  PubMed Central  Google Scholar 

  • Paul K, Erhardt M, Hirano T, Blair DF, Hughes KT (2008) Energy source of the flagellar type III secretion. Nature 451:489–492

    CAS  PubMed  Google Scholar 

  • Paul K, Gonzalez-Bonet G, Bilwes AM, Crane BR, Blair D (2011) Architecture of the flagellar rotor. EMBO J 30:2962–2971

    CAS  PubMed  PubMed Central  Google Scholar 

  • Saijo-Hamano Y, Imada K, Minamino T, Kihara M, Shimada M, Kitao A, Namba K (2010) Structure of the cytoplasmic domain of FlhA and implication for flagellar type III protein export. Mol Microbiol 76:260–268

    CAS  PubMed  Google Scholar 

  • Terahara N, Inoue Y, Kodera N, Morimoto YV, Uchihashi T, Imada K, Ando T, Namba K, Minamino T (2018) Insight into structural remodeling of the FlhA ring responsible for bacterial flagellar type III protein export. Sci Adv 4:eaao7054

    Google Scholar 

  • Terashima H, Kawamoto A, Tastumi C, Namba K, Minamino T, Imada K (2018) In vitro reconstitution of functional type III protein export and insights into flagellar assembly. mBio 9:e00988-18

    Google Scholar 

  • Thomas DR, Morgan DG, DeRosier DJ (1999) Rotational symmetry of the C ring and a mechanism for the flagellar rotary motor. Proc Natl Acad Sci USA 96:10134–10139

    CAS  PubMed  Google Scholar 

  • Thomas J, Stafford GP, Hughes C (2004) Docking of cytosolic chaperone-substrate complexes at the membrane ATPase during flagellar type III protein export. Proc Natl Acad Sci USA 101:3945–3950

    CAS  PubMed  Google Scholar 

  • Ueno T, Oosawa K, Aizawa S (1992) M ring, S ring and proximal rod of the flagellar basal body of Salmonella typhimurium are composed of subunits of a single protein, FliF. J Mol Biol 227:672–677

    CAS  PubMed  Google Scholar 

  • Vartanian AS, Paz A, Fortgang EA, Abramson J, Dahlquist FW (2012) Structure of flagellar motor proteins in complex allows for insights into motor structure and switching. J Biol Chem 287:35779–35783

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wagner S, Königsmaier L, Lara-Tejero M, Lefebre M, Marlovits TC, Galán JE (2010) Organization and coordinated assembly of the type III secretion export apparatus. Proc Natl Acad Sci USA 107:17745–17750

    CAS  PubMed  Google Scholar 

  • Wagner S, Grin I, Grin I, Malmsheimer S, Singh N, Torres-Vargas CE, Westerhausen S (2018) Bacterial type III secretion systems: a complex device for the delivery of bacterial effector proteins into eukaryotic host cells. FEMS Microbiol Lett 365:fny201

    Google Scholar 

  • Worrall LJ, Vuckovic M, Strynadka NCJ (2010) Crystal structure of the C-terminal domain of the Salmonella type III secretion system export apparatus protein InvA. Protein Sci 19:1091–1096

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xing Q, Shi K, Portaliou A, Rossi P, Economou A, Kalodimos CG (2018) Structure of chaperone-substrate complexes docked onto the export gate in a type III secretion system. Nat Commun 9:1773

    PubMed  PubMed Central  Google Scholar 

  • Xue C, Lam KH, Zhang H, Sun K, Lee SH, Chen X, Au SWN (2018) Crystal structure of the FliF-FliG complex from Helicobacter pylori yields insight into the assembly the motor MS–C ring in the bacterial flagellum. J Biol Chem 293:2066–2078

    CAS  PubMed  Google Scholar 

  • Zarivach R, Deng W, Vuckovic M, Felise HB, Nguyen HV, Miller SI, Finlay BB, Strynadka NC (2008) Structural analysis of the essential self-cleaving type III secretion proteins EscU and SpaS. Nature 453:124–127

    CAS  PubMed  Google Scholar 

  • Zilkenat S, Franz-Wachtel M, Stierhof YD, Galán JE, Macek B, Wagner S (2016) Determination of the stoichiometry of the complete bacterial type III secretion needle complex using a combined quantitative proteomic approach. Mol Cell Proteomics 15:1598–1609

    CAS  PubMed  PubMed Central  Google Scholar 

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Authors and Affiliations

  1. Graduate School of Frontier Biosciences, Osaka University, 1-3 Yamadaoka, Suita, Osaka, 565-0871, Japan

    Tohru Minamino, Akihiro Kawamoto, Miki Kinoshita & Keiichi Namba

  2. Institute for Protein Research, Osaka University, 3-2 Yamadaoka, Suita, Osaka, 565-0871, Japan

    Akihiro Kawamoto

  3. Center for Biosystems Dynamics Research & SPring-8 Center, RIKEN, 1-3 Yamadaoka, Suita, Osaka, 565-0871, Japan

    Keiichi Namba

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  1. Tohru Minamino
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  2. Akihiro Kawamoto
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  3. Miki Kinoshita
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  4. Keiichi Namba
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Correspondence to Tohru Minamino .

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Editors and Affiliations

  1. Institute of Microbiology and Infection Medicine, University of TĂĽbingen, TĂĽbingen, Germany

    Samuel Wagner

  2. Boyer Center for Molecular Medicine, Yale University School of Medicine, New Haven, CT, USA

    Jorge E. Galan

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Minamino, T., Kawamoto, A., Kinoshita, M., Namba, K. (2019). Molecular Organization and Assembly of the Export Apparatus of Flagellar Type III Secretion Systems. In: Wagner, S., Galan, J. (eds) Bacterial Type III Protein Secretion Systems. Current Topics in Microbiology and Immunology, vol 427. Springer, Cham. https://doi.org/10.1007/82_2019_170

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