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Research Paper

Transmembrane domains of type III-secreted proteins affect bacterial-host interactions in enteropathogenic E. coli

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Pages 902-917 | Received 21 Sep 2020, Accepted 01 Mar 2021, Published online: 17 Mar 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;76:262–310.
  • Cornelis GR. The type III secretion injectisome. Nat Rev Microbiol. 2006;4(11):811–825.
  • Deng W, Marshall NC, Rowland JL, et al. Assembly, structure, function and regulation of type III secretion systems. Nat Rev Microbiol. 2017;15(6):323–337.
  • Marlovits TC, Kubori T, Sukhan A, et al. Structural insights into the assembly of the type III secretion needle complex. Science. 2004;306(5698):1040–1042.
  • Moraes TF, Spreter T, Strynadka NC. Piecing together the type III injectisome of bacterial pathogens. Curr Opin Struct Biol. 2008;18(2):258–266.
  • Wagner S, Grin I, Malmsheimer S, 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(19):365.
  • Luo W, Donnenberg MS. Analysis of the function of enteropathogenic Escherichia coli EspB by random mutagenesis. Infect Immun. 2006;74(2):810–820.
  • Luo W, Donnenberg MS. Interactions and predicted host membrane topology of the enteropathogenic Escherichia coli translocator protein EspB. J Bacteriol. 2011;193(12):2972–2980.
  • Mattei PJ, Faudry E, Job V, et al. Membrane targeting and pore formation by the type III secretion system translocon. Febs J. 2011;278(3):414–426.
  • Diepold A, Wagner S. Assembly of the bacterial type III secretion machinery. FEMS Microbiol Rev. 2014;38(4):802–822.
  • Notti RQ, Stebbins CE, Structure T. Function of Type III Secretion Systems. Microbiol Spectr. 2016;1:4. DOI:10.1128/microbiolspec.VMBF-0004-2015
  • Dey S, Chakravarty A, Guha Biswas P, et al. The Type III Secretion System Needle, Tip and Translocon. Protein Sci. 2019. DOI:10.1002/pro.3682
  • Epler CR, Dickenson NE, Olive AJ, et al. Liposomes recruit IpaC to the Shigella flexneri type III secretion apparatus needle as a final step in secretion induction. Infect Immun. 2009;77(7):2754–2761.
  • Espina M, Olive AJ, Kenjale R, et al. IpaD localizes to the tip of the type III secretion system needle of Shigella flexneri. Infect Immun. 2006;74(8):4391–4400. .
  • Collazo CM, Galan JE. The invasion-associated type III system of Salmonella typhimurium directs the translocation of Sip proteins into the host cell. Mol Microbiol. 1997;24(4):747–756.
  • Deng W, Puente JL, Gruenheid S, et al. Dissecting virulence: systematic and functional analyses of a pathogenicity island. Proc Natl Acad Sci USA. 2004;101(10):3597–3602.
  • Kresse AU, Rohde M, Guzman CA. The EspD Protein of EnterohemorrhagicEscherichia coli Is Required for the Formation of Bacterial Surface Appendages and Is Incorporated in the Cytoplasmic Membranes of Target Cells. Infect Immun. 1999;67(9):4834–4842.
  • Lai LC, Wainwright LA, Stone KD, et al. A third secreted protein that is encoded by the enteropathogenic Escherichia coli pathogenicity island is required for transduction of signals and for attaching and effacing activities in host cells. Infect Immun. 1997;65(6):2211–2217.
  • Barzu S, Benjelloun-Touimi Z, Phalipon A, et al. Functional analysis of the Shigella flexneri IpaC invasin by insertional mutagenesis. Infect Immun. 1997;65(5):1599–1605.
  • Hakansson S, Schesser K, Persson C, et al. The YopB protein of Yersinia pseudotuberculosis is essential for the translocation of Yop effector proteins across the target cell plasma membrane and displays a contact-dependent membrane disrupting activity. Embo J. 1996;15(21):5812–5823.
  • Barta ML, Tachiyama S, Muthuramalingam M, et al. Using disruptive insertional mutagenesis to identify the in situ structure-function landscape of the Shigella translocator protein IpaB. Protein Sci. 2018;27(8):1392–1406.
  • Romano FB, Tang Y, Rossi KC, et al. Type 3 Secretion Translocators Spontaneously Assemble a Hexadecameric Transmembrane Complex. J Biol Chem. 2016;291(12):6304–6315.
  • Tang Y, Romano FB, Brena M, et al. The Pseudomonas aeruginosa type III secretion translocator PopB assists the insertion of the PopD translocator into host cell membranes. J Biol Chem. 2018;293(23):8982–8993.
  • Faudry E, Job V, Dessen A, et al. Type III secretion system translocator has a molten globule conformation both in its free and chaperone-bound forms. Febs J. 2007;274(14):3601–3610.
  • Ide T, Laarmann S, Greune L, et al. Characterization of translocation pores inserted into plasma membranes by type III-secreted Esp proteins of enteropathogenic Escherichia coli. Cell Microbiol. 2001;3(10):669–679.
  • Romano FB, Rossi KC, Savva CG, et al. Efficient Isolation of Pseudomonas aeruginosa Type III Secretion Translocators and Assembly of Heteromeric Transmembrane Pores in Model Membranes. Biochemistry. 2011;50(33):7117–7131.
  • Schoehn G, Di Guilmi AM, Lemaire D, et al. Oligomerization of type III secretion proteins PopB and PopD precedes pore formation in Pseudomonas. Embo J. 2003;22(19):4957–4967.
  • Job V, Mattei PJ, Lemaire D, et al. Structural basis of chaperone recognition of type III secretion system minor translocator proteins. J Biol Chem. 2010;285(30):23224–23232.
  • Menard R, Sansonetti P, Parsot C. The secretion of the Shigella flexneri Ipa invasins is activated by epithelial cells and controlled by IpaB and IpaD. Embo J. 1994;13(22):5293–5302.
  • Menard R, Sansonetti P, Parsot C, et al. Extracellular association and cytoplaSmic partitioning of the IpaB and IpaC invasins of S. flexneri. flexneri Cell. 1994;79(3):515–525.
  • Miki T, Shibagaki Y, Danbara H, et al. Functional characterization of SsaE, a novel chaperone protein of the type III secretion system encoded by Salmonella pathogenicity island 2. J Bacteriol. 2009;191(22):6843–6854.
  • Neyt C, Cornelis GR. Role of SycD, the chaperone of the Yersinia Yop translocators YopB and YopD. Mol Microbiol. 1999;31(1):143–156.
  • Wainwright LA, Kaper JB. EspB and EspD require a specific chaperone for proper secretion from enteropathogenic Escherichia coli. Mol Microbiol. 1998;27(6):1247–1260.
  • Akeda Y, Galan JE. Chaperone release and unfolding of substrates in type III secretion. Nature. 2005;437(7060):911–915.
  • Burkinshaw BJ, Strynadka NC. Assembly and structure of the T3SS. Biochim Biophys Acta. 2014;1843(8):1649–1663.
  • Lunelli M, Lokareddy RK, Zychlinsky A, et al. IpaB-IpgC interaction defines binding motif for type III secretion translocator. Proc Natl Acad Sci USA. 2009;106(24):9661–9666.
  • Akopian D, Shen K, Zhang X, et al. Signal recognition particle: an essential protein-targeting machine. Annu Rev Biochem. 2013;82(1):693–721.
  • Elvekrog MM, Walter P. Dynamics of co-translational protein targeting. Curr Opin Chem Biol. 2015;29:79–86.
  • Saraogi I, Shan SO. Co-translational protein targeting to the bacterial membrane. Biochim Biophys Acta. 2014;1843(8):1433–1441.
  • Deng W, Yu HB, Li Y, et al. SepD/SepL-dependent secretion signals of the type III secretion system translocator proteins in enteropathogenic Escherichia coli. J Bacteriol. 2015;197(7):1263–1275.
  • Hueck CJ. Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol Mol Biol Rev. 1998;62:379–433.
  • McDermott JE, Corrigan A, Peterson E, et al. Computational prediction of type III and IV secreted effectors in gram-negative bacteria. Infect Immun. 2011;79(1):23–32. .
  • Tomalka AG, Stopford CM, Lee PC, et al. A translocator-specific export signal establishes the translocator-effector secretion hierarchy that is important for type III secretion system function. Mol Microbiol. 2012;86(6):1464–1481.
  • Arnold R, Brandmaier S, Kleine F, et al. Sequence-based prediction of type III secreted proteins. PLoS Pathog. 2009;5(4):e1000376. .
  • 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(4):e1000375.
  • Krampen L, Malmsheimer S, Grin I, et al. Revealing the mechanisms of membrane protein export by virulence-associated bacterial secretion systems. Nat Commun. 2018;9(1):3467. .
  • Croxen MA, Law RJ, Scholz R, et al. Recent advances in understanding enteric pathogenic Escherichia coli. Clin Microbiol Rev. 2013;26:822–880.
  • Daniell SJ, Kocsis E, Morris E, et al. 3D structure of EspA filaments from enteropathogenic Escherichia coli. Mol Microbiol. 2003;49(2):301–308.
  • Knutton S, Rosenshine I, Pallen MJ, et al. A novel EspA-associated surface organelle of enteropathogenic Escherichia coli involved in protein translocation into epithelial cells. Embo J. 1998;17(8):2166–2176. .
  • Gaytan MO, Martinez-Santos VI, Soto E, et al. Secretion System in Attaching and Effacing Pathogens. Front Cell Infect Microbiol. 2016;6:129.
  • Yerushalmi G, Litvak Y, Gur-Arie L, et al. Dynamics of expression and maturation of the type III secretion system of enteropathogenic Escherichia coli. J Bacteriol. 2014;196(15):2798–2806.
  • 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.
  • Tseytin I, Madar A, Mitrovic B, et al. The Third Transmembrane Domain of EscR Is Critical for Function of the Enteropathogenic Escherichia coli Type III Secretion System. mSphere. 2018;4:3. DOI:10.1128/mSphere.00162-18
  • White SH, Wimley WC. Hydrophobic interactions of peptides with membrane interfaces. Biochim Biophys Acta. 1998;1376(3):339–352.
  • White SH, Wimley WC. Membrane protein folding and stability: physical principles. Annu Rev Biophys Biomol Struct. 1999;28(1):319–365.
  • Letzelter M, Sorg I, Mota LJ, et al. The discovery of SycO highlights a new function for type III secretion effector chaperones. Embo J. 2006;25(13):3223–3233. .
  • Woestyn S, Sory MP, Boland A, et al. The cytosolic SycE and SycH chaperones of Yersinia protect the region of YopE and YopH involved in translocation across eukaryotic cell membranes. Mol Microbiol. 1996;20(6):1261–1271.
  • Nguyen VS, Jobichen C, Tan KW, 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(11):2022–2031. .
  • Kenny B, DeVinney R, Stein M, et al. Enteropathogenic E. coli (EPEC) transfers its receptor for intimate adherence into mammalian cells. Cell. 1997;91:(4):511–520.
  • Mills E, Baruch K, Aviv G, et al. Dynamics of the type III secretion system activity of enteropathogenic Escherichia coli. MBio. 2013;4(4):4.
  • Mills E, Baruch K, Charpentier X, et al. Real-time analysis of effector translocation by the type III secretion system of enteropathogenic Escherichia coli. Cell Host Microbe. 2008;3(2):104–113.
  • Luo Y, Frey EA, Pfuetzner RA, et al. Crystal structure of enteropathogenic Escherichia coli intimin–receptor complex. Nature. 2000;405(6790):1073–1077.
  • Hessa T, Meindl-Beinker NM, Bernsel A, et al. Molecular code for transmembrane-helix recognition by the Sec61 translocon. Nature. 2007;450(7172):1026–1030.
  • Baruch K, Gur-Arie L, Nadler C, et al. Metalloprotease type III effectors that specifically cleave JNK and NF-kappaB. Embo J. 2011;30(1):221–231.
  • Goure J, Pastor A, Faudry E, et al. The V antigen of Pseudomonas aeruginosa is required for assembly of the functional PopB/PopD translocation pore in host cell membranes. Infect Immun. 2004;72(8):4741–4750.
  • Myeni SK, Wang L, Zhou D. SipB-SipC complex is essential for translocon formation. PLoS One. 2013;8(3):e60499.
  • Jayasinghe S, Hristova K, White SH. Energetics, stability, and prediction of transmembrane helices. J Mol Biol. 2001;312(5):927–934.
  • Gasteiger E, Gattiker A, Hoogland C, et al. ExPASy: the proteomics server for in-depth protein knowledge and analysis. Nucleic Acids Res. 2003;31(13):3784–3788.
  • Wilkins MR, Gasteiger E, Bairoch A, et al. Protein identification and analysis tools in the ExPASy server. Methods Mol Biol. 1999;112:531–552.
  • Abe A, Heczko U, Hegele RG, et al. Two enteropathogenic Escherichia coli type III secreted proteins, EspA and EspB, are virulence factors. J Exp Med. 1998;188(10):1907–1916.
  • Tacket CO, Sztein MB, Losonsky G, et al. Role of EspB in Experimental Human EnteropathogenicEscherichia coli Infection. Infect Immun. 2000;68(6):3689–3695.
  • Wachter C, Beinke C, Mattes M, et al. Insertion of EspD into epithelial target cell membranes by infecting enteropathogenic Escherichia coli. Mol Microbiol. 2002;31(6):1695–1707.
  • Iguchi A, Thomson NR, Ogura Y, 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.
  • Gauthier A, Puente JL, Finlay BB. 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.
  • Gibson DG, Benders GA, Andrews-Pfannkoch C, et al. Complete chemical synthesis, assembly, and cloning of a Mycoplasma genitalium genome. Science. 2008;319(5867):1215–1220.
  • Gibson DG, Young L, Chuang RY, et al. Enzymatic assembly of DNA molecules up to several hundred kilobases. Nat Methods. 2009;6(5):343–345.
  • Rose RE. The nucleotide sequence of pACYC184. Nucleic Acids Res. 1988;16(1):355.
  • Creasey EA, Friedberg D, Shaw RK, et al. CesAB is an enteropathogenic Escherichia coli chaperone for the type-III translocator proteins EspA and EspB. Microbiology. 2003;149(12):3639–3647.