The Type III Secretion Translocation Pore Senses Host Cell Contact

PLoS Pathogens

Volumn 12, Issue 3, 2016, Pages

  Armentrout, Erin I ^a   Rietsch, Arne ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; PCRV PROTEIN; TRANSLOCATOR POPB; TRANSLOCATOR POPD; UNCLASSIFIED DRUG; TYPE III SECRETION SYSTEM;

ARTICLE; BACTERIAL STRAIN; BACTERIAL TRANSLOCATION; CELL CONTACT; CONTROLLED STUDY; CROSS LINKING; CYTOTOXICITY; GENETIC PROCEDURES; HEMOLYSIS; HOST CELL; HUMAN; HUMAN CELL; NONHUMAN; PROTEIN PROTEIN INTERACTION; PSEUDOMONAS AERUGINOSA; TYPE III SECRETION SYSTEM; WESTERN BLOTTING; YERSINIA PSEUDOTUBERCULOSIS; AMINO ACID SEQUENCE; CELL SURVIVAL; DRUG EFFECTS; GENETICS; HOST PATHOGEN INTERACTION; METABOLISM; MOLECULAR GENETICS; MOLECULAR MODEL; PROTEIN TRANSPORT; SEQUENCE ALIGNMENT;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CELL SURVIVAL; HOST-PATHOGEN INTERACTIONS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN TRANSPORT; SEQUENCE ALIGNMENT; TYPE III SECRETION SYSTEMS;

EID: 84962460177     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1005530     Document Type: Article

References (51)

1. Diepold A, Armitage JP, Type III secretion systems: the bacterial flagellum and the injectisome. Philos Trans R Soc Lond B Biol Sci. 2015;370(1679). doi: 10.1098/rstb.2015.002026370933.
2. Galan 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;68:415–38. doi: 10.1146/annurev-micro-092412-15572525002086.
3. Rosqvist R, Magnusson KE, Wolf-Watz H, Target cell contact triggers expression and polarized transfer of Yersinia YopE cytotoxin into mammalian cells. EMBO J. 1994;13(4):964–72. Epub 1994/02/15. 8112310; PubMed Central PMCID: PMC394898.
4. Sory MP, Cornelis GR, Translocation of a hybrid YopE-adenylate cyclase from Yersinia enterocolitica into HeLa cells. Mol Microbiol. 1994;14(3):583–94. Epub 1994/11/01. 7885236.
5. Kaniga K, Tucker S, Trollinger D, Galan JE, Homologs of the Shigella IpaB and IpaC invasins are required for Salmonella typhimurium entry into cultured epithelial cells. J Bacteriol. 1995;177(14):3965–71. Epub 1995/07/01. 7608068; PubMed Central PMCID: PMC177125.
6. Parsot C, Menard R, Gounon P, Sansonetti PJ, Enhanced secretion through the Shigella flexneri Mxi-Spa translocon leads to assembly of extracellular proteins into macromolecular structures. Mol Microbiol. 1995;16(2):291–300. Epub 1995/04/01. 7565091.
7. Blocker A, Gounon P, Larquet E, Niebuhr K, Cabiaux V, Parsot C, et al. The tripartite type III secreton of Shigella flexneri inserts IpaB and IpaC into host membranes. J Cell Biol. 1999;147(3):683–93. 10545510.
8. Mueller CA, Broz P, Cornelis GR, The type III secretion system tip complex and translocon. Mol Microbiol. 2008;68(5):1085–95. Epub 2008/04/24. MMI6237 [pii] doi: 10.1111/j.1365-2958.2008.06237.x18430138.
9. Goure J, Pastor A, Faudry E, Chabert J, Dessen A, Attree I, 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):4741–50. 15271936.
10. Goure J, Broz P, Attree O, Cornelis GR, Attree I, Protective anti-V antibodies inhibit Pseudomonas and Yersinia translocon assembly within host membranes. J Infect Dis. 2005;192(2):218–25. 15962216.
11. Picking WL, Nishioka H, Hearn PD, Baxter MA, Harrington AT, Blocker A, et al. IpaD of Shigella flexneri is independently required for regulation of Ipa protein secretion and efficient insertion of IpaB and IpaC into host membranes. Infect Immun. 2005;73(3):1432–40. 15731041.
12. Frithz-Lindsten E, Holmstrom A, Jacobsson L, Soltani M, Olsson J, Rosqvist R, et al. Functional conservation of the effector protein translocators PopB/YopB and PopD/YopD of Pseudomonas aeruginosa and Yersinia pseudotuberculosis. Mol Microbiol. 1998;29(5):1155–65. Epub 1998/10/10. 9767584.
13. Dacheux D, Goure J, Chabert J, Usson Y, Attree I, Pore-forming activity of type III system-secreted proteins leads to oncosis of Pseudomonas aeruginosa-infected macrophages. Mol Microbiol. 2001;40(1):76–85. 11298277.
14. Marenne MN, Journet L, Mota LJ, Cornelis GR, Genetic analysis of the formation of the Ysc-Yop translocation pore in macrophages by Yersinia enterocolitica: role of LcrV, YscF and YopN. Microb Pathog. 2003;35(6):243–58. 14580388.
15. Lara-Tejero M, Galan JE, Salmonella enterica serovar typhimurium pathogenicity island 1-encoded type III secretion system translocases mediate intimate attachment to nonphagocytic cells. Infect Immun. 2009;77(7):2635–42. Epub 2009/04/15. IAI.00077-09 [pii] doi: 10.1128/IAI.00077-0919364837; PubMed Central PMCID: PMC2708559.
16. Ide T, Laarmann S, Greune L, Schillers H, Oberleithner H, Schmidt MA, Characterization of translocation pores inserted into plasma membranes by type III-secreted Esp proteins of enteropathogenic Escherichia coli. Cell Microbiol. 2001;3(10):669–79. Epub 2001/10/03. 146 [pii]. 11580752.
17. Cisz M, Lee PC, Rietsch A, ExoS controls the cell contact-mediated switch to effector secretion in Pseudomonas aeruginosa. J Bacteriol. 2008;190(8):2726–38.
18. Schoehn G, Di Guilmi AM, Lemaire D, Attree I, Weissenhorn W, Dessen A, Oligomerization of type III secretion proteins PopB and PopD precedes pore formation in Pseudomonas. Embo J. 2003;22(19):4957–67. 14517235.
19. Faudry E, Vernier G, Neumann E, Forge V, Attree I, Synergistic pore formation by type III toxin translocators of Pseudomonas aeruginosa. Biochemistry. 2006;45(26):8117–23. 16800636.
20. De Geyter C, Wattiez R, Sansonetti P, Falmagne P, Ruysschaert JM, Parsot C, et al. Characterization of the interaction of IpaB and IpaD, proteins required for entry of Shigella flexneri into epithelial cells, with a lipid membrane. Eur J Biochem. 2000;267(18):5769–76. 10971588.
21. Allmond LR, Karaca TJ, Nguyen VN, Nguyen T, Wiener-Kronish JP, Sawa T, Protein binding between PcrG-PcrV and PcrH-PopB/PopD encoded by the pcrGVH-popBD operon of the Pseudomonas aeruginosa type III secretion system. Infect Immun. 2003;71(4):2230–3. Epub 2003/03/26. 12654846; PubMed Central PMCID: PMC152033.
22. Yu XJ, McGourty K, Liu M, Unsworth KE, Holden DW, pH sensing by intracellular Salmonella induces effector translocation. Science. 2010;328(5981):1040–3. Epub 2010/04/17. doi: 10.1126/science.118900020395475.
23. Lee VT, Mazmanian SK, Schneewind O, A program of Yersinia enterocolitica type III secretion reactions is activated by specific signals. J Bacteriol. 2001;183(17):4970–8. 11489848.
24. Broms JE, Forslund AL, Forsberg A, Francis MS, Dissection of homologous translocon operons reveals a distinct role for YopD in type III secretion by Yersinia pseudotuberculosis. Microbiology. 2003;149(Pt 9):2615–26. Epub 2003/09/02. 12949185.
25. Mueller CA, Broz P, Muller SA, Ringler P, Erne-Brand F, Sorg I, et al. The V-antigen of Yersinia forms a distinct structure at the tip of injectisome needles. Science. 2005;310(5748):674–6. 16254184.
26. Osiecki JC, Barker J, Picking WL, Serfis AB, Berring E, Shah S, et al. IpaC from Shigella and SipC from Salmonella possess similar biochemical properties but are functionally distinct. Mol Microbiol. 2001;42(2):469–81. Epub 2001/11/13. 2654 [pii]. 11703668.
27. Broz P, Mueller CA, Muller SA, Philippsen A, Sorg I, Engel A, et al. Function and molecular architecture of the Yersinia injectisome tip complex. Mol Microbiol. 2007;65(5):1311–20. 17697254.
28. Chaudhury S, Battaile KP, Lovell S, Plano GV, De Guzman RN, Structure of the Yersinia pestis tip protein LcrV refined to 1.65 A resolution. Acta Crystallogr Sect F Struct Biol Cryst Commun. 2013;69(Pt 5):477–81. doi: 10.1107/S174430911300857923695558; PubMed Central PMCID: PMCPMC3660882.
29. Kelley LA, Sternberg MJ, Protein structure prediction on the Web: a case study using the Phyre server. Nat Protoc. 2009;4(3):363–71. Epub 2009/02/28. doi: 10.1038/nprot.2009.219247286.
30. Sundin C, Thelaus J, Broms JE, Forsberg A, Polarisation of type III translocation by Pseudomonas aeruginosa requires PcrG, PcrV and PopN. Microb Pathog. 2004;37(6):313–22. Epub 2004/12/28. doi: 10.1016/j.micpath.2004.10.00515619427.
31. Lee PC, Zmina SE, Stopford CM, Toska J, Rietsch A, Control of type III secretion activity and substrate specificity by the cytoplasmic regulator PcrG. Proc Natl Acad Sci U S A. 2014;111(19):E2027–36. doi: 10.1073/pnas.140265811124778208; PubMed Central PMCID: PMC4024851.
32. 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(6):1464–81. Epub 2012/11/06. doi: 10.1111/mmi.1206923121689; PubMed Central PMCID: PMC3524397.
33. Yang H, Shan Z, Kim J, Wu W, Lian W, Zeng L, et al. Regulatory role of PopN and its interacting partners in type III secretion of Pseudomonas aeruginosa. J Bacteriol. 2007;189(7):2599–609. Epub 2007/01/24. doi: 10.1128/JB.01680-0617237176; PubMed Central PMCID: PMC1855783.
34. Kuwae A, Yoshida S, Tamano K, Mimuro H, Suzuki T, Sasakawa C, Shigella invasion of macrophage requires the insertion of IpaC into the host plasma membrane. Functional analysis of IpaC. J Biol Chem. 2001;276(34):32230–9.
35. Moraes TF, Spreter T, Strynadka NC, Piecing together the type III injectisome of bacterial pathogens. Curr Opin Struct Biol. 2008;18(2):258–66. Epub 2008/02/09. S0959-440X(07)00211-4 [pii] doi: 10.1016/j.sbi.2007.12.01118258424.
36. Mounier J, Popoff MR, Enninga J, Frame MC, Sansonetti PJ, Van Nhieu GT, The IpaC carboxyterminal effector domain mediates Src-dependent actin polymerization during Shigella invasion of epithelial cells. PLoS Pathog. 2009;5(1):e1000271. Epub 2009/01/24. doi: 10.1371/journal.ppat.100027119165331; PubMed Central PMCID: PMC2621354.
37. Discola KF, Forster A, Boulay F, Simorre JP, Attree I, Dessen A, et al. Membrane and chaperone recognition by the major translocator protein PopB of the type III secretion system of Pseudomonas aeruginosa. J Biol Chem. 2014;289(6):3591–601. doi: 10.1074/jbc.M113.51792024297169; PubMed Central PMCID: PMCPMC3916559.
38. Mattei PJ, Faudry E, Job V, Izore T, Attree I, Dessen A, Membrane targeting and pore formation by the type III secretion system translocon. FEBS J. 2011;278(3):414–26.
39. Veenendaal AK, Hodgkinson JL, Schwarzer L, Stabat D, Zenk SF, Blocker AJ, The type III secretion system needle tip complex mediates host cell sensing and translocon insertion. Mol Microbiol. 2007;63(6):1719–30. Epub 2007/03/21. doi: 10.1111/j.1365-2958.2007.05620.x17367391.
40. Francis MS, Wolf-Watz H, YopD of Yersinia pseudotuberculosis is translocated into the cytosol of HeLa epithelial cells: evidence of a structural domain necessary for translocation. Mol Microbiol. 1998;29(3):799–813. 9723919.
41. Olsson J, Edqvist PJ, Broms JE, Forsberg A, Wolf-Watz H, Francis MS, The YopD translocator of Yersinia pseudotuberculosis is a multifunctional protein comprised of discrete domains. J Bacteriol. 2004;186(13):4110–23.
42. Costa TR, Edqvist PJ, Broms JE, Ahlund MK, Forsberg A, Francis MS, YopD self-assembly and binding to LcrV facilitate type III secretion activity by Yersinia pseudotuberculosis. The Journal of biological chemistry. 2010;285(33):25269–84. Epub 2010/06/08. doi: 10.1074/jbc.M110.14431120525687; PubMed Central PMCID: PMC2919090.
43. Sato H, Hunt ML, Weiner JJ, Hansen AT, Frank DW, Modified needle-tip PcrV proteins reveal distinct phenotypes relevant to the control of type III secretion and intoxication by Pseudomonas aeruginosa. PLoS One. 2011;6(3):e18356. Epub 2011/04/12. doi: 10.1371/journal.pone.001835621479247; PubMed Central PMCID: PMC3066235.
44. Lee PC, 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(4):924–41.
45. Roehrich AD, Martinez-Argudo I, Johnson S, Blocker AJ, Veenendaal AK, The extreme C terminus of Shigella flexneri IpaB is required for regulation of type III secretion, needle tip composition, and binding. Infect Immun. 2010;78(4):1682–91. Epub 2010/01/21. IAI.00645-09 [pii] doi: 10.1128/IAI.00645-0920086081; PubMed Central PMCID: PMC2849396.
46. Kenjale R, Wilson J, Zenk SF, Saurya S, Picking WL, Picking WD, et al. The needle component of the type III secreton of Shigella regulates the activity of the secretion apparatus. J Biol Chem. 2005;280(52):42929–37. 16227202.
47. Martinez-Argudo I, Blocker AJ, The Shigella T3SS needle transmits a signal for MxiC release, which controls secretion of effectors. Mol Microbiol. 2010;78(6):1365–78. Epub 2010/12/15. doi: 10.1111/j.1365-2958.2010.07413.x21143311; PubMed Central PMCID: PMC3020320.
48. Torruellas J, Jackson MW, Pennock JW, Plano GV, The Yersinia pestis type III secretion needle plays a role in the regulation of Yop secretion. Mol Microbiol. 2005;57(6):1719–33. 16135236.
49. Ross JA, Plano GV, A C-terminal region of Yersinia pestis YscD binds the outer membrane secretin YscC. J Bacteriol. 2011;193(9):2276–89. doi: 10.1128/JB.01137-1021357482; PubMed Central PMCID: PMCPMC3133092.
50. Rietsch A, Mekalanos JJ, Metabolic regulation of type III secretion gene expression in Pseudomonas aeruginosa. Mol Microbiol. 2006;59(3):807–20. 16420353; PubMed Central PMCID: PMCPMC2654213.
51. Rietsch A, Vallet-Gely I, Dove SL, Mekalanos JJ, ExsE, a secreted regulator of type III secretion genes in Pseudomonas aeruginosa. Proc Natl Acad Sci U S A. 2005;102(22):8006–11. Epub 2005/05/25. doi: 10.1073/pnas.050300510215911752; PubMed Central PMCID: PMC1142391.