The Shigella T3SS needle transmits a signal for MxiC release, which controls secretion of effectors

Molecular Microbiology

Volumn 78, Issue 6, 2010, Pages 1365-1378

  Martinez Argudo, Isabel ^a   Blocker, Ariel J ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN MXIC; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ARTICLE; BACTERIUM MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN SECRETION; SHIGELLA; SIGNAL TRANSDUCTION; TYPE III SECRETION SYSTEM;

BACTERIAL PROTEINS; BACTERIAL SECRETION SYSTEMS; DYSENTERY, BACILLARY; GENE EXPRESSION REGULATION, BACTERIAL; HOST-PATHOGEN INTERACTIONS; HUMANS; PROTEIN TRANSPORT; SHIGELLA FLEXNERI;

ANIMALIA; BACTERIA (MICROORGANISMS); EUKARYOTA; NEGIBACTERIA; SHIGELLA;

EID: 78449271872     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2010.07413.x     Document Type: Article

References (57)

1. Allaoui, A., Sansonetti, P.J., Menard, R., Barzu, S., Mounier, J., Phalipon, A., and Parsot, C. (1995) MxiG, a membrane protein required for secretion of Shigella spp. Ipa invasins: involvement in entry into epithelial cells and in intercellular dissemination. Mol Microbiol 17: 461-470.
2. Bahrani, F.K., Sansonetti, P.J., and Parsot, C. (1997) Secretion of Ipa proteins by Shigella flexneri: inducer molecules and kinetics of activation. Infect Immun 65: 4005-4010.
3. Blocker, A., Gounon, P., Larquet, E., Niebuhr, K., Cabiaux, V., Parsot, C., and Sansonetti, P. (1999) The tripartite type III secreton of Shigella flexneri inserts IpaB and IpaC into host membranes. J Cell Biol 147: 683-693.
4. Blocker, A., Jouihri, N., Larquet, E., Gounon, P., Ebel, F., Parsot, C., et al. (2001) Structure and composition of the Shigella flexneri 'needle complex', a part of its type III secreton. Mol Microbiol 39: 652-663.
5. Blocker, A.J., Deane, J.E., Veenendaal, A.K., Roversi, P., Hodgkinson, J.L., Johnson, S., and Lea, S.M. (2008) What's the point of the type III secretion system needle? Proc Natl Acad Sci USA 105: 6507-6513.
6. Botteaux, A., Sory, M.P., Biskri, L., Parsot, C., and Allaoui, A. (2009) MxiC is secreted by and controls the substrate specificity of the Shigella flexneri type III secretion apparatus. Mol Microbiol 71: 449-460.
7. Cisz, M., Lee, P.C., and Rietsch, A. (2008) ExoS controls the cell contact-mediated switch to effector secretion in Pseudomonas aeruginosa. J Bacteriol 190: 2726-2738.
8. Coombes, B.K., Brown, N.F., Valdez, Y., Brumell, J.H., and Finlay, B.B. (2004) Expression and secretion of Salmonella pathogenicity island-2 virulence genes in response to acidification exhibit differential requirements of a functional type III secretion apparatus and SsaL. J Biol Chem 279: 49804-49815.
9. Cordes, F.S., Daniell, S., Kenjale, R., Saurya, S., Picking, W.L., Picking, W.D., et al. (2005) Helical packing of needles from functionally altered Shigella type III secretion systems. J Mol Biol 354: 206-211.
10. Cornelis, G.R. (2006) The type III secretion injectisome. Nat Rev Microbiol 4: 811-825.
11. Datsenko, K.A., and Wanner, B.L. (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97: 6640-6645.
12. Davis, A.J., and Mecsas, J. (2007) Mutations in the Yersinia pseudotuberculosis type III secretion system needle protein, YscF, that specifically abrogate effector translocation into host cells. J Bacteriol 189: 83-97.
13. Day, J.B., Ferracci, F., and Plano, G.V. (2003) Translocation of YopE and YopN into eukaryotic cells by Yersinia pestis yopN, tyeA, sycN, yscB and lcrG deletion mutants measured using a phosphorylatable peptide tag and phosphospecific antibodies. Mol Microbiol 47: 807-823.
14. Deane, J.E., Roversi, P., King, C., Johnson, S., and Lea, S.M. (2008) Structures of the Shigella flexneri type 3 secretion system protein MxiC reveal conformational variability amongst homologues. J Mol Biol 377: 985-992.
15. Deane, J.E., Abrusci, P., Johnson, S., and Lea, S.M. (2009) Timing is everything: the regulation of type III secretion. Cell Mol Life Sci 67: 1065-1075.
16. Deng, W., Puente, J.L., Gruenheid, S., Li, Y., Vallance, B.A., Vazquez, A., et al. (2004) Dissecting virulence: systematic and functional analyses of a pathogenicity island. Proc Natl Acad Sci USA 101: 3597-3602.
17. Deng, W., Li, Y., Hardwidge, P.R., Frey, E.A., Pfuetzner, R.A., Lee, S., et al. (2005) Regulation of type III secretion hierarchy of translocators and effectors in attaching and effacing bacterial pathogens. Infect Immun 73: 2135-2146.
18. Du, Z., Tan, Y., Yang, H., Qiu, J., Qin, L., Wang, T., et al. (2009) Gene expression profiling of Yersinia pestis with deletion of lcrG, a known negative regulator for Yop secretion of type III secretion system. Int J Med Microbiol 299: 355-366.
19. Dykxhoorn, D.M., St Pierre, R., and Linn, T. (1996) A set of compatible tac promoter expression vectors. Gene 177: 133-136.
20. Epler, C.R., Dickenson, N.E., Olive, A.J., Picking, W.L., and Picking, W.D. (2009) Liposomes recruit IpaC to the Shigella flexneri type III secretion apparatus needle as a final step in secretion induction. Infect Immun 77: 2754-2761.
21. Espina, M., Olive, A.J., Kenjale, R., Moore, D.S., Ausar, S.F., Kaminski, R.W., et al. (2006) IpaD localizes to the tip of the type III secretion system needle of Shigella flexneri. Infect Immun 74: 4391-4400.
22. Ferracci, F., Schubot, F.D., Waugh, D.S., and Plano, G.V. (2005) Selection and characterization of Yersinia pestis YopN mutants that constitutively block Yop secretion. Mol Microbiol 57: 970-987.
23. Forsberg, A., Viitanen, A.M., Skurnik, M., and Wolf-Watz, H. (1991) The surface-located YopN protein is involved in calcium signal transduction in Yersinia pseudotuberculosis. Mol Microbiol 5: 977-986.
24. Frye, J., Karlinsey, J.E., Felise, H.R., Marzolf, B., Dowidar, N., McClelland, M., and Hughes, K.T. (2006) Identification of new flagellar genes of Salmonella enterica serovar Typhimurium. J Bacteriol 188: 2233-2243.
25. Galan, J.E., and Wolf-Watz, H. (2006) Protein delivery into eukaryotic cells by type III secretion machines. Nature 444: 567-573.
26. Iriarte, M., Sory, M.P., Boland, A., Boyd, A.P., Mills, S.D., Lambermont, I., and Cornelis, G.R. (1998) TyeA, a protein involved in control of Yop release and in translocation of Yersinia Yop effectors. EMBO J 17: 1907-1918.
27. Johnson, S., and Blocker, A. (2008) Characterization of soluble complexes of the Shigella flexneri type III secretion system ATPase. FEMS Microbiol Lett 286: 274-278.
28. Johnson, S., Roversi, P., Espina, M., Olive, A., Deane, J.E., Birket, S., et al. (2007) Self-chaperoning of the type III secretion system needle tip proteins IpaD and BipD. J Biol Chem 282: 4035-4044.
29. Jouihri, N., Sory, M.P., Page, A.L., Gounon, P., Parsot, C., and Allaoui, A. (2003) MxiK and MxiN interact with the Spa47 ATPase and are required for transit of the needle components MxiH and MxiI, but not of Ipa proteins, through the type III secretion apparatus of Shigella flexneri. Mol Microbiol 49: 755-767.
30. Kenjale, R., Wilson, J., Zenk, S.F., Saurya, S., Picking, W.L., Picking, W.D., and Blocker, A. (2005) The needle component of the type III secreton of Shigella regulates the activity of the secretion apparatus. J Biol Chem 280: 42929-42937.
31. Kresse, A.U., Beltrametti, F., Muller, A., Ebel, F., and Guzman, C.A. (2000) Characterization of SepL of enterohemorrhagic Escherichia coli. J Bacteriol 182: 6490-6498.
32. Kubori, T., and Galan, J.E. (2002) Salmonella type III secretion-associated protein InvE controls translocation of effector proteins into host cells. J Bacteriol 184: 4699-4708.
33. Kubori, T., Matsushima, Y., Nakamura, D., Uralil, J., Lara-Tejero, M., Sukhan, A., et al. (1998) Supramolecular structure of the Salmonella typhimurium type III protein secretion system. Science 280: 602-605.
34. Le Gall, T., Mavris, M., Martino, M.C., Bernardini, M.L., Denamur, E., and Parsot, C. (2005) Analysis of virulence plasmid gene expression defines three classes of effectors in the type III secretion system of Shigella flexneri. Microbiology 151: 951-962.
35. Lee, P.C., Stopford, C.M., Svenson, A.G., and Rietsch, A. (2010) Control of effector export by the Pseudomonas aeruginosa type III secretion proteins PcrG and PcrV. Mol Microbiol 75: 924-941.
36. Magdalena, J., Hachani, A., Chamekh, M., Jouihri, N., Gounon, P., Blocker, A., and Allaoui, A. (2002) Spa32 regulates a switch in substrate specificity of the type III secreton of Shigella flexneri from needle components to Ipa proteins. J Bacteriol 184: 3433-3441.
37. Matson, J.S., and Nilles, M.L. (2001) LcrG-LcrV interaction is required for control of Yops secretion in Yersinia pestis. J Bacteriol 183: 5082-5091.
38. Mavris, M., Page, A.L., Tournebize, R., Demers, B., Sansonetti, P., and Parsot, C. (2002) Regulation of transcription by the activity of the Shigella flexneri type III secretion apparatus. Mol Microbiol 43: 1543-1553.
39. Menard, R., Sansonetti, P.J., and Parsot, C. (1993) Nonpolar mutagenesis of the ipa genes defines IpaB, IpaC, and IpaD as effectors of Shigella flexneri entry into epithelial cells. J Bacteriol 175: 5899-5906.
40. Menard, R., Sansonetti, P., and Parsot, C. (1994) The secretion of the Shigella flexneri Ipa invasins is activated by epithelial cells and controlled by IpaB and IpaD. EMBO J 13: 5293-5302.
41. Morita-Ishihara, T., Ogawa, M., Sagara, H., Yoshida, M., Katayama, E., and Sasakawa, C. (2006) Shigella Spa33 is an essential C-ring component of type III secretion machinery. J Biol Chem 281: 599-607.
42. Nilles, M.L., Williams, A.W., Skrzypek, E., and Straley, S.C. (1997) Yersinia pestis LcrV forms a stable complex with LcrG and may have a secretion-related regulatory role in the low-Ca2+ response. J Bacteriol 179: 1307-1316.
43. O'Connell, C.B., Creasey, E.A., Knutton, S., Elliott, S., Crowther, L.J., Luo, W., et al. (2004) SepL, a protein required for enteropathogenic Escherichia coli type III translocation, interacts with secretion component SepD. Mol Microbiol 52: 1613-1625.
44. Olive, A.J., Kenjale, R., Espina, M., Moore, D.S., Picking, W.L., and Picking, W.D. (2007) Bile salts stimulate recruitment of IpaB to the Shigella flexneri surface, where it colocalizes with IpaD at the tip of the type III secretion needle. Infect Immun 75: 2626-2629.
45. Pallen, M.J., Beatson, S.A., and Bailey, C.M. (2005) Bioinformatics analysis of the locus for enterocyte effacement provides novel insights into type-III secretion. BMC Microbiol 5: 9.
46. Parsot, C. (1994) Shigella flexneri: genetics of entry and intercellular dissemination in epithelial cells. Curr Top Microbiol Immunol 192: 217-241.
47. Parsot, C., Menard, R., Gounon, P., and Sansonetti, P.J. (1995) Enhanced secretion through the Shigella flexneri Mxi-Spa translocon leads to assembly of extracellular proteins into macromolecular structures. Mol Microbiol 16: 291-300.
48. Parsot, C., Ageron, E., Penno, C., Mavris, M., Jamoussi, K., D'Hauteville, H., et al. (2005) A secreted anti-activator, OspD1, and its chaperone, Spa15, are involved in the control of transcription by the type III secretion apparatus activity in Shigella flexneri. Mol Microbiol 56: 1627-1635.
49. Picking, W.L., Nishioka, H., Hearn, P.D., Baxter, M.A., Harrington, A.T., Blocker, A., and Picking, W.D. (2005) 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 73: 1432-1440.
50. Roehrich, A.D., Martinez-Argudo, I., Johnson, S., Blocker, A.J., and Veenendaal, A.K. (2010) The extreme C terminus of Shigella flexneri IpaB is required for regulation of type III secretion, needle tip composition, and binding. Infect Immun 78: 1682-1691.
51. Sansonetti, P.J., Kopecko, D.J., and Formal, S.B. (1982) Involvement of a plasmid in the invasive ability of Shigella flexneri. Infect Immun 35: 852-860.
52. Schroeder, G.N., and Hilbi, H. (2008) Molecular pathogenesis of Shigella spp.: controlling host cell signaling, invasion, and death by type III secretion. Clin Microbiol Rev 21: 134-156.
53. Torruellas, J., Jackson, M.W., Pennock, J.W., and Plano, G.V. (2005) The Yersinia pestis type III secretion needle plays a role in the regulation of Yop secretion. Mol Microbiol 57: 1719-1733.
54. Veenendaal, A.K., Hodgkinson, J.L., Schwarzer, L., Stabat, D., Zenk, S.F., and Blocker, A.J. (2007) The type III secretion system needle tip complex mediates host cell sensing and translocon insertion. Mol Microbiol 63: 1719-1730.
55. Wang, D., Roe, A.J., McAteer, S., Shipston, M.J., and Gally, D.L. (2008) Hierarchal type III secretion of translocators and effectors from Escherichia coli O157: H7 requires the carboxy terminus of SepL that binds to Tir. Mol Microbiol 69: 1499-1512.
56. Yu, X.J., McGourty, K., Liu, M., Unsworth, K.E., and Holden, D.W. (2010) pH sensing by intracellular Salmonella induces effector translocation. Science 328: 1040-1043.
57. Zenk, S.F., Stabat, D., Hodgkinson, J.L., Veenendaal, A.K., Johnson, S., and Blocker, A.J. (2007) Identification of minor inner-membrane components of the Shigella type III secretion system 'needle complex. Microbiology 153: 2405-2415.