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Research Paper

Interactions and substrate selectivity within the SctRST complex of the type III secretion system of enteropathogenic Escherichia coli

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Article: 2013763 | Received 25 Jul 2021, Accepted 05 Nov 2021, Published online: 29 Dec 2021

References

  • Buttner D. Protein export according to schedule: architecture, assembly, and regulation of type III secretion systems from plant- and animal-pathogenic bacteria. Microbiol Mol Biol Rev. 2012;76:262–20. doi:10.1128/MMBR.05017-11.
  • Bhavsar AP, Guttman JA, Finlay BB. Manipulation of host-cell pathways by bacterial pathogens. Nature. 2007;449:827–834. doi:10.1038/nature06247.
  • Deng W, Marshall NC, Rowland JL, McCoy JM, Worrall LJ, Santos AS, Strynadka NCJ, Finlay BB. Assembly, structure, function and regulation of type III secretion systems. Nat Rev Microbiol. 2017;15:323–337. doi:10.1038/nrmicro.2017.20.
  • Wagner S, Grin I, Malmsheimer S, Singh N, Torres-Vargas CE, Westerhausen S. Bacterial type III secretion systems: a complex device for the delivery of bacterial effector proteins into eukaryotic host cells. FEMS Microbiol Lett. 2018;365(19). doi:10.1093/femsle/fny201.
  • Diepold A, Wagner S. Assembly of the bacterial type III secretion machinery. FEMS Microbiol Rev. 2014;38:802–822. doi:10.1111/1574-6976.12061.
  • Hu B, Lara-Tejero M, Kong Q, Galan JE, Liu J. In situ molecular architecture of the salmonella type III secretion machine. Cell. 2017;168(6):1065–74 e10. doi:10.1016/j.cell.2017.02.022.
  • Hu J, Worrall LJ, Vuckovic M, Hong C, Deng W, Atkinson CE, Finlay BB, Yu Z, Strynadka NCJ. T3S injectisome needle complex structures in four distinct states reveal the basis of membrane coupling and assembly. Nat Microbiol. 2019;4(11):2010–2019. doi:10.1038/s41564-019-0545-z.
  • Kuhlen L, Abrusci P, Johnson S, Gault J, Deme J, Caesar J, Dietsche T, Mebrhatu MT, Ganief T, Macek B, et al. Structure of the core of the type III secretion system export apparatus. Nat Struct Mol Biol. 2018;25(7):583–590. doi:10.1038/s41594-018-0086-9.
  • Miletic S, Fahrenkamp D, Goessweiner-Mohr N, Wald J, Pantel M, Vesper O, Kotov V, Marlovits TC. Substrate-engaged type III secretion system structures reveal gating mechanism for unfolded protein translocation. Nat Commun. 2021;12(1):1546. doi:10.1038/s41467-021-21143-1.
  • Deng W, Puente JL, Gruenheid S, Li Y, Vallance BA, Vazquez A, Barba J, Ibarra JA, O’Donnell P, Metalnikov P, et al. Dissecting virulence: systematic and functional analyses of a pathogenicity island. Proc Natl Acad Sci USA. 2004;101(10):3597–3602. doi:10.1073/pnas.0400326101.
  • Tseytin I, Madar A, Mitrovic B, Deng W, Finlay BB, Sal-Man N. The third transmembrane domain of EscR Is critical for function of the enteropathogenic Escherichia coli. mSphere. 3(4);2018:e00162–18.
  • Wagner S, Konigsmaier L, Lara-Tejero M, Lefebre M, Marlovits TC, Galan JE. Organization and coordinated assembly of the type III secretion export apparatus. Proc Natl Acad Sci U S A. 2010;107(41):17745–17750. doi:10.1073/pnas.1008053107.
  • Fabiani FD, Renault TT, Peters B, Dietsche T, Galvez EJC, Guse A, Freier K, Charpentier E, Strowig T, Franz-Wachtel M, et al. A flagellum-specific chaperone facilitates assembly of the core type III export apparatus of the bacterial flagellum. PLoS Biol. 2017;15(8):e2002267. doi:10.1371/journal.pbio.2002267.
  • Fukumura T, Makino F, Dietsche T, Kinoshita M, Kato T, Wagner S, Namba K, Imada K, Minamino T . Assembly and stoichiometry of the core structure of the bacterial flagellar type III export gate complex. PLoS Biol. 2017;15(8):e2002281. doi:10.1371/journal.pbio.2002281.
  • Ward E, Renault TT, Kim EA, Erhardt M, Hughes KT, Blair DF. Type-III secretion pore formed by flagellar protein FliP. Mol Microbiol. 2018;107(1):94–103. doi:10.1111/mmi.13870.
  • Singh N, Kronenberger T, Eipper A, Weichel F, Franz-Wachtel M, Macek B, Wagner S. Conserved salt bridges facilitate assembly of the helical core export apparatus of a salmonella enterica type III secretion system. J Mol Biol. 2021;433(19):167175. doi:10.1016/j.jmb.2021.167175.
  • Gaytán MO, Martínez-Santos VI, Soto E, Gonzalez-Pedrajo, B. Type three secretion system in attaching and effacing pathogens. Front Cell Infect Microbiol. 2016;6:129.
  • Tseytin I, Mitrovic B, David N, Langenfeld K, Zarivach R, Diepold A, Sal-Man N. The role of the small export apparatus protein, SctS, in the activity of the type III Secretion system. Front Microbiol. 2019;10:2551. doi:10.3389/fmicb.2019.02551.
  • Fink A, Sal-Man N, Gerber D, Shai Y. Transmembrane domains interactions within the membrane milieu: principles, advances and challenges. Biochim Biophys Acta. 2012;1818(4):974–983. doi:10.1016/j.bbamem.2011.11.029.
  • Russ WP, Engelman DM. The GxxxG motif: a framework for transmembrane helix-helix association. J Mol Biol. 2000;296(3):911–919. doi:10.1006/jmbi.1999.3489.
  • Sal-Man N, Gerber D, Bloch I, Shai Y. Specificity in transmembrane helix-helix interactions mediated by aromatic residues. J Biol Chem. 2007;282(27):19753–19761. doi:10.1074/jbc.M610368200.
  • Sal-Man N, Gerber D, Shai Y. The identification of a minimal dimerization motif QXXS that enables homo- and hetero-association of transmembrane helices in vivo. J Biol Chem. 2005;280(29):27449–27457. doi:10.1074/jbc.M503095200.
  • Sal-Man N, Gerber D, Shai Y. Proline localized to the interaction interface can mediate self-association of transmembrane domains. Biochim Biophys Acta. 2014;1838(9):2313–2318. doi:10.1016/j.bbamem.2014.05.006.
  • Sal-Man N, Shai Y. Arginine mutations within a transmembrane domain of Tar, an Escherichia coli aspartate receptor, can drive homodimer dissociation and heterodimer association in vivo. Biochem J. 2005;385(1):29–36. doi:10.1042/BJ20041022.
  • Dietsche T, Tesfazgi Mebrhatu M, Brunner MJ, Abrusci P, Yan J, Franz-Wachtel M, Schärfe C, Zilkenat S, Grin I, Galán JE, et al. Structural and functional characterization of the bacterial type III secretion export apparatus. PLoS Pathog. 2016;12(12):e1006071. doi:10.1371/journal.ppat.1006071.
  • Zilkenat S, Franz-Wachtel M, Stierhof YD, Galan JE, Macek B, Wagner S. Determination of the stoichiometry of the complete bacterial type III secretion needle complex using a combined quantitative proteomic approach. Mol Cell Proteomics. 2016;15(5):1598–1609. doi:10.1074/mcp.M115.056598.
  • Hüsing S, Halte , M, van Look U, Guse A, Gálvez EJC, Charpentier E, Blair, DF, Erhardt, M, Renault, TT, et al. Controlling membrane barrier during bacterial type-III protein secretion. 2020:2020.11.25.397760.
  • Baruch K, Gur-Arie L, Nadler C, Koby S, Yerushalmi G, Ben-Neriah Y, Yogev, O, Shaulian, E, Guttman, C, Zarivach, R, Rosenshine, I . Metalloprotease type III effectors that specifically cleave JNK and NF-kappaB. EMBO J. 2011;30(1):221–231. doi:10.1038/emboj.2010.297.
  • Erhardt M, Wheatley P, Kim EA, Hirano T, Zhang Y, Sarkar MK, Hughes KT, Blair DF. Mechanism of type-III protein secretion: regulation of FlhA conformation by a functionally critical charged-residue cluster. Mol Microbiol. 2017;104(2):234–249. doi:10.1111/mmi.13623.
  • 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 10(3) . 2019;e00818-19.
  • Diaz-Guerrero M, Gaytan MO, Soto E, Espinosa N, Garcia-Gomez E, Marcos-Vilchis A, Andrade A, González-Pedrajo B. CesL regulates type III secretion substrate specificity of the enteropathogenic E. coli Injectisome. Microorganisms. 2021;9(5):1047. doi:10.3390/microorganisms9051047.
  • Inoue Y, Morimoto YV, Namba K, Minamino T. Novel insights into the mechanism of well-ordered assembly of bacterial flagellar proteins in Salmonella. Sci Rep. 2018;8(1):1787. doi:10.1038/s41598-018-20209-3.
  • Lara-Tejero M. The type III secretion system sorting platform. Curr Top Microbiol Immunol. 2020;427:133–142. doi:10.1007/82_2019_167.
  • Minamino T. Arginine mutations within a transmembrane domain of Tar, an Escherichia coli aspartate receptor, can drive homodimer dissociation and heterodimer association in vivo. FEMS Microbiol Lett. 2018;365(12). doi:10.1093/femsle/fny117.
  • Portaliou AG, Tsolis KC, Loos MS, Balabanidou V, Rayo J, Tsirigotaki A, Crepin, VF, Frankel, G, Kalodimos, CG, Karamanou, S, Economou, A, 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(23):3517–3531. doi:10.15252/embj.201797515.
  • Soto E, Espinosa N, Diaz-Guerrero M, Gaytan MO, Puente JL, Gonzalez-Pedrajo B. Functional characterization of EscK (Orf4), a sorting platform component of the enteropathogenic Escherichia coli Injectisome. J Bacteriol. 2017;199.
  • Deng W, Li Y, Hardwidge PR, Frey EA, Pfuetzner RA, Lee S, Gruenheid, S, Strynakda, NCJ, Puente, JL, Finlay, BB, et al. Regulation of type III secretion hierarchy of translocators and effectors in attaching and effacing bacterial pathogens. Infect Immun. 2005;73(4):2135–2146. doi:10.1128/IAI.73.4.2135-2146.2005.
  • Ho O, Rogne P, Edgren T, Wolf-Watz H, Login FH, Wolf-Watz M. Characterization of the ruler protein interaction interface on the substrate specificity switch protein in the Yersinia Type III Secretion System. J Biol Chem. 2017;292(8):3299–3311. doi:10.1074/jbc.M116.770255.
  • Shaulov L, Gershberg J, Deng W, Finlay BB, Sal-Man N. The ruler protein escp of the enteropathogenic Escherichia coli type III secretion system is involved in calcium sensing and secretion hierarchy regulation by interacting with the gatekeeper protein SepL. mBio. 2017;8.
  • Thomassin JL, Thomas NA HX, Thomas NA. Role of EscU auto-cleavage in promoting type III effector translocation into host cells by enteropathogenic Escherichia coli. BMC Microbiol. 2011;11(1):205. doi:10.1186/1471-2180-11-205.
  • Iguchi A, Thomson NR, Ogura Y, Saunders D, Ooka T, Henderson IR, Harris D, Asadulghani M, Kurokawa K, Dean P, et al. Complete genome sequence and comparative genome analysis of enteropathogenic Escherichia coli O127:H6 Strain E2348/69. J Bacteriol. 2009;191(1):347–354. doi:10.1128/JB.01238-08.
  • Gauthier A, Puente JL, Finlay BB, , , , , , et al. Secretin of the Enteropathogenic Escherichia coli Type III secretion system requires components of the type III apparatus for assembly and localization. Infect Immun. 2003;71(6):3310–3319. doi:10.1128/IAI.71.6.3310-3319.2003.
  • Durfee T, Nelson R, Baldwin S, Plunkett G 3rd, Burland V, Mau B, Petrosino JF, Qin X, Muzny DM, Ayele M, et al. The Complete Genome Sequence of Escherichia coli DH10B: insights into the Biology of a Laboratory Workhorse. J Bacteriol. 2008;190(7):2597–2606. doi:10.1128/JB.01695-07.
  • Gibson DG, Benders GA, Andrews-Pfannkoch C, Denisova EA, Baden-Tillson H, Zaveri J, Stockwell TB, Brownley A, Thomas DW, Algire MA, et al. Complete chemical synthesis, assembly, and cloning of a mycoplasma genitalium genome. Science. 2008;319(5867):1215–1220. doi:10.1126/science.1151721.
  • Gibson DG, Young L, Chuang RY, Venter JC, Hutchison CA 3rd, Smith HO. Smith HO Enzymatic assembly of DNA molecules up to several hundred kilobases. Nat Methods. 2009;6:343–345. doi:10.1038/nmeth.1318.
  • Zilkenat S, Dietsche T, Monjaras Feria JV, Torres-Vargas CE, Mebrhatu MT, Wagner S. Blue native PAGE analysis of bacterial secretion complexes. Methods Mol Biol. 2017;1615:321–351.