Genetic analysis of the formation of the Ysc-Yop translocation pore in macrophages by Yersinia enterocolitica: Role of LcrV, YscF and YopN

Microbial Pathogenesis

Volumn 35, Issue 6, 2003, Pages 243-258

  Marenne, Marie Noëlle ^a   Journet, Laure ^b   Mota, Luis Jaime ^b   Cornelis, Guy R ^a,b  

^a DE DUVE INSTITUTE   (Belgium)

^b UNIVERSITY OF BASEL   (Switzerland)

Author keywords

LcrV; Needle; Traffic; Translocation pore; Type III secretion

Indexed keywords

BACTERIAL PROTEIN; CARRIER PROTEIN; FLUORESCENT DYE; LACTATE DEHYDROGENASE; PROTEIN LCRV; PROTEIN YOPN; PROTEIN YSCF; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BACTERIAL GENETICS; BACTERIUM MUTANT; CHANNEL GATING; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME RELEASE; GENE FUNCTION; GENE TRANSLOCATION; GENETIC ANALYSIS; LYSIS; MACROPHAGE; MOLECULAR BIOLOGY; MOLECULAR WEIGHT; MOUSE; NONHUMAN; OSMOSIS; PRIORITY JOURNAL; PROTEIN SYNTHESIS; YERSINIA ENTEROCOLITICA;

BACTERIA (MICROORGANISMS); EUKARYOTA; YERSINIA; YERSINIA ENTEROCOLITICA;

EID: 0242321266     PISSN: 08824010     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0882-4010(03)00154-2     Document Type: Article

References (67)

1. Sory M.P., Cornelis G.R. Translocation of a hybrid YopE-adenylate cyclase from Yersinia enterocolitica into HeLa cells. Mol Microbiol. 14:1994;583-594.
2. Rosqvist R., Magnusson K.E., Wolf-Watz H. Target cell contact triggers expression and polarized transfer of Yersinia YopE cytotoxin into mammalian cells. EMBO J. 13:1994;964-972.
3. Cornelis G.R. The Yersinia Ysc-Yop Type III weaponry. Nat Rev Mol Cell Biol. 3:2002;742-752.
4. Forsberg A., Viitanen A.M., Skurnik M., Wolf-Watz H. The surface-located YopN protein is involved in calcium signal transduction in Yersinia pseudotuberculosis. Mol Microbiol. 5:1991;977-986.
5. Boland A., Sory M.P., Iriarte M., Kerbourch C., Wattiau P., Cornelis G.R. Status of YopM and YopN in the Yersinia Yop virulon: YopM of Y. enterocolitica is internalized inside the cytosol of PU5-1.8 macrophages by the YopB, D, N delivery apparatus. EMBO J. 15:1996;5191-5201.
6. Cheng L., Schneewind O. Yersinia enterocolitica TyeA, an intracellular regulator of the type III machinery, is required for specific targeting of YopE, YopH, YopM, and YopN into the cytosol of eukaryotic cells. J Bacteriol. 182:2000;3183-3190.
7. Iriarte M., Sory M.P., Boland A., Boyd A.P., Mills S.D., Lambermont I., Cornelis G.R. TyeA, a protein involved in control of Yop release and in translocation of Yersinia Yop effectors. Embo J. 17:1998;1907-1918.
8. Sarker M.R., Sory M.P., Boyd A.P., Iriarte M., Cornelis G.R. LcrG is required for efficient translocation of Yersinia Yop effector proteins into eukaryotic cells. Infect Immun. 66:1998;2976-2979.
9. Skryzpek E., Straley S.C. LcrG, a secreted protein involved in negative regulation of the low-calcium response in Yersinia pestis. J Bacteriol. 175:1993;3520-3528.
10. Persson C., Nordfelth R., Holmström A., Hakansson S., Rosqvist R., Wolf-Watz H. Cell-surface-bound Yersinia translocate the protein tyrosine phosphatase YopH by a polarized mechanism into the target cell. Mol Microbiol. 18:1995;135-150.
11. Hakansson S., Bergman T., Vanooteghem J.C., Cornelis G., Wolf-Watz H. YopB and YopD constitute a novel class of Yersinia Yop proteins. Infect Immun. 61:1993;71-80.
12. Welch R.A. Pore-forming cytolysins of gram-negative bacteria. Mol Microbiol. 5:1991;521-528.
13. Viboud G., So S., Ryndak M., Bliska J. Proinflammatory signalling stimulated by the type III translocation factor YopB is counteracted by multiple effectors in epithelial cells infected with Yersinia pseudotuberculosis. Mol Microbiol. 47:2003;1305-1315.
14. Wattiau P., Bernier B., Deslee P., Michiels T., Cornelis G.R. Individual chaperones required for Yop secretion by Yersinia. Proc Natl Acad Sci USA. 91:1994;10493-10497.
15. Neyt C., Cornelis G.R. Role of SycD, the chaperone of the Yersinia Yop translocators YopB and YopD. Mol Microbiol. 31:1999;143-156.
16. Price S.B., Leung K.Y., Barve S.S., Straley S.C. Molecular analysis of lcrGVH, the V antigen operon of Yersinia pestis. J Bacteriol. 171:1989;5646-5653.
17. Bergman T., Hakansson S., Forsberg A., Norlander L., Macellaro A., Backman A., Bolin I., Wolf-Watz H. Analysis of the V antigen lcrGVH-yopBD operon of Yersinia pseudotuberculosis: evidence for a regulatory role of LcrH and LcrV. J Bacteriol. 173:1991;1607-1616.
18. Francis M.S., Wolf-Watz H., Forsberg A. Regulation of type III secretion systems. Curr Opin Microbiol. 5:2002;166-172.
19. Francis M.S., Lloyd S.A., Wolf-Watz H. The type III secretion chaperone LcrH co-operates with YopD to establish a negative, regulatory loop for control of Yop synthesis in Yersinia pseudotuberculosis. Mol Microbiol. 42:2001;1075-1093.
20. 2+ response. J Bacteriol. 179:1997;1307-1316.
21. Sarker M.R., Neyt C., Stainier I., Cornelis G.R. The Yersinia Yop virulon: LcrV is required for extrusion of the translocators YopB and YopD. J Bacteriol. 180:1998;1207-1214.
22. Lee V.T., Tam C., Schneewind O. LcrV, a substrate for Yersinia enterocolitica type III secretion, is required for toxin targeting into the cytosol of HeLa cells. J Biol Chem. 275:2000;36869-36875.
23. 2+ response, and virulence of Yersinia pestis. J Bacteriol. 177:1995;2530-2542.
24. Nilles M.L., Fields K.A., Straley S.C. The V antigen of Yersinia pestis regulates Yop vectorial targeting as well as Yop secretion through effects on YopB and LcrG. J Bacteriol. 180:1998;3410-3420.
25. Matson J.S., Nilles M.L. LcrG-LcrV interaction is required for control of Yops secretion in Yersinia pestis. J Bacteriol. 183:2001;5082-5091.
26. Cheng L.W., Kay O., Schneewind O. Regulated secretion of YopN by the type III machinery of Yersinia enterocolitica. J Bacteriol. 183:2001;5293-5301.
27. Matson J.S., Nilles M.L. Interaction of the Yersinia pestis type III regulatory proteins LcrG and LcrV occurs at a hydrophobic interface. BMC Microbiol. 2:2002;16-25.
28. Lawton D.G., Longstaff C., Wallace B.A., Hill J., Leary S.E., Titball R.W., Brown K.A. Interactions of the type III secretion pathway proteins LcrV and LcrG from Yersinia pestis are mediated by coiled-coil domains. J Biol Chem. 277:2002;38714-38722.
29. Hakansson S., Schesser K., Persson C., Galyov E.E., Rosqvist R., Homble F., Wolf-Watz H. 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. 15:1996;5812-5823.
30. Neyt C., Cornelis G.R. Insertion of a Yop translocation pore into the macrophage plasma membrane by Yersinia enterocolitica: requirement for translocators YopB and YopD, but not LcrG. Mol Microbiol. 33:1999;971-981.
31. Viboud G.I., Bliska J.B. A bacterial type III secretion system inhibits actin polymerization to prevent pore formation in host cell membranes. EMBO J. 20:2001;5373-5382.
32. Holmström A., Olsson J., Cherepanov P., Maier E., Nordfelth R., Pettersson J., Benz R., Wolf-Watz H., Forsberg A. LcrV is a channel size-determining component of the Yop effector translocon of Yersinia. Mol Microbiol. 39:2001;620-632.
33. Fields K.A., Nilles M.L., Cowan C., Straley S.C. Virulence role of V antigen of Yersinia pestis at the bacterial surface. Infect Immun. 67:1999;5395-5408.
34. Pettersson J., Holmström A., Hill J., Leary S., Frithz-Lindsten E., von Euler-Matell A., Carlsson E., Titball R., Forsberg A., Wolf-Watz H. The V-antigen of Yersinia is surface exposed before target cell contact and involved in virulence protein translocation. Mol Microbiol. 32:1999;961-976.
35. Hoiczyk E., Blobel G. Polymerization of a single protein of the pathogen Yersinia enterocolitica into needles punctures eukaryotic cells. Proc Natl Acad Sci USA. 98:2001;4669-4674.
36. Bhakdi S., Greulich S., Muhly M., Eberspacher B., Becker H., Thiele A., Hugo F. Potent leukocidal action of Escherichia coli hemolysin mediated by permeabilization of target cell membranes. J Exp Med. 169:1989;737-754.
37. Kirby J.E., Vogel J.P., Andrews H.L., Isberg R.R. Evidence for pore-forming ability by Legionella pneumophila. Mol Microbiol. 27:1998;323-336.
38. Stainier I., Iriarte M., Cornelis G.R. YscM1 and YscM2, two Yersinia enterocolitica proteins causing downregulation of yop transcription. Mol Microbiol. 26:1997;833-843.
39. Holmström A., Petterson J., Rosqvist R., Hakansson S., Tafazoli F., Fallman M., Magnusson K.E., Wolf-Watz H., Forsberg A. YopK of Yersinia pseudotuberculosis controls translocation of Yop effectors across the eukaryotic cell membrane. Mol Microbiol. 24:1997;73-91.
40. Boyd A.P., Grosdent N., Totemeyer S., Geuijen C., Bleves S., Iriarte M., Lambermont I., Octave J.N., Cornelis G.R. Yersinia enterocolitica can deliver Yop proteins into a wide range of cell types: development of a delivery system for heterologous proteins. Eur J Cell Biol. 79:2000;659-671.
41. Sory M.P., Boland A., Lambermont I., Cornelis G.R. Identification of the YopE and YopH domains required for secretion and internalization into the cytosol of macrophages, using the cyaA gene fusion approach. Proc Natl Acad Sci USA. 92:1995;11998-12002.
42. Day J.B., Ferracci F., Plano G.V. 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. 47:2003;807-823.
43. Nakajima R., Brubaker R.R. Association between virulence of Yersinia pestis and suppression of gamma interferon and tumor necrosis factor alpha. Infect Immun. 61:1993;23-31.
44. Motin V.L., Nakajima R., Smirnov G.B., Brubaker R.R. Passive immunity to Yersiniae mediated by anti-recombinant V antigen and protein A-V antigen fusion peptide. Infect Immun. 62:1994;4192-4201.
45. Nakajima R., Motin V.L., Brubaker R.R. Suppression of cytokines in mice by protein A-V antigen fusion peptide and restoration of synthesis by active immunization. Infect Immun. 63:1995;3021-3029.
46. Roggenkamp A., Geiger A.M., Leitritz L., Kessler A., Heesemann J. Passive immunity to infection with Yersinia spp. mediated by anti-recombinant V antigen is dependent on polymorphism of V antigen. Infect Immun. 65:1997;446-451.
47. Sing A., Roggenkamp A., Geiger A.M., Heesemann J. Yersinia enterocolitica evasion of the host innate immune response by V antigen-induced IL-10 production of macrophages is abrogated in IL-10-deficient mice. J Immunol. 168:2002;1315-1321.
48. Cornelis G. The Yersinia deadly kiss. J Bacteriol. 180:1998;5495-5504.
49. Wilson R.K., Shaw R.K., Daniell S., Knutton S., Franke I.G. Role of EscF, a putative needle complex protein, in the type III protein translocation system of enteropathogenic Escherichia coli. Cell Microbiol. 3:2001;753-762.
50. Knutton S., Rosenshine I., Pallen M.J., Nisan I., Neves B.C., Bain C., Wolff C., Dougan G., Frankel G. A novel EspA-associated surface organelle of enteropathogenic Escherichia coli involved in protein translocation into epithelial cells. EMBO J. 15:1998;2166-2176.
51. Sekiya K., Ohishi M., Ogino T., Tamano K., Sasakawa C., Abe A. Supermolecular structure of the enteropathogenic Escherichia coli type III secretion system and its direct interaction with the EspA-sheath-like structure. Proc Natl Acad Sci USA. 98:2001;11638-11643.
52. Ide T., Laarmann S., Greune L., Schillers H., Oberleithner H., Schmidt M.A. Characterization of translocation pores inserted into plasma membranes by type III-secreted Esp proteins of enteropathogenic Escherichia coli. Cell Microbiol. 3:2001;669-679.
53. Hartland E.L., Daniell S.J., Delahay R.M., Neves B.C., Wallis T., Shaw R.W., Hale C., Knutton S., Frankel G. The type III protein translocation system of enteropathogenic Escherichia coli involves EspA-EspB protein interactions. Mol Microbiol. 35:2000;1483-1492.
54. Francis M.S., 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. 29:1998;799-813.
55. Miller V.L., Mekalanos J.J. A novel suicide vector and its use in construction of insertion mutations: osmoregulation of outer membrane proteins and virulence determinants in Vibrio cholerae requires toxR. J Bacteriol. 170:1988;2575-2583.
56. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227:1970;680-685.
57. Towbin H., Staehelin H.T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci USA. 76:1979;4350-4354.
58. Bodeus M., Sory M.P., Fang J.C., Janssens M., Delferriere N., Cornelis G., Wauters G., Burtomboy G. Production of rat hybridomas directed against Yersinia enterocolitica. Bazin H. Rat hybridoma and rat monoclonal antibodies. 1990;335-338 CRC Press, Boca Raton, FL.
59. Kaniga K., Delor I., Cornelis G.R. A wide-host-range suicide vector for improving reverse genetics in gram-negative bacteria: inactivation of the blaA gene of Yersinia enterocolitica. Gene. 109:1991;137-141.
60. Neyt C., Iriarte M., Thi V.H., Cornelis G.R. Virulence and arsenic resistance in Yersiniae. J Bacteriol. 179:1997;612-619.
61. Boland A., Cornelis G.R. Role of YopP in suppression of tumor necrosis factor alpha release by macrophages during Yersinia infection. Infect Immun. 66:1998;1878-1884.
62. Schulte R., Wattiau P., Hartland E., Robins-Browne R., Cornelis G. Differential secretion of interleukin-8 by human epithelial cell lines upon entry of virulent or nonvirulent Yersinia enterocolitica. Infect Immun. 64:1996;2106-2113.
63. Kovach M.E., Elzer P.H., Hill D.S., Robertson G.T., Farris M.A., Roop R.M., Peterson K.M. Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene. 166:1995;175-176.
64. Kunkel T., Roberts J., Zakour R. Rapid and efficient site-specific mutagenesis without phenotypic selection. Meth Enzymol. 154:1987;367-382.
65. Grosdent N., Maridonneau-Parini I., Sory M.P., Cornelis G.R. Role of Yops and adhesins in resistance of Yersinia enterocolitica to phagocytosis. Infect Immun. 70:2002;4165-4176.
66. Iriarte M., Cornelis G.R. YopT, a new Yersinia Yop effector protein, affects the cytoskeleton of host cells. Mol Microbiol. 29:1998;915-929.
67. China B., Michiels T., Cornelis G.R. The pYV plasmid of Yersinia encodes a lipoprotein, YlpA, related to TraT. Mol Microbiol. 4:1990;1585-1593.