Identification of substrates and chaperone from the Yersinia enterocolitica 1B Ysa type III secretion system

Infection and Immunity

Volumn 71, Issue 1, 2003, Pages 242-253

  Foultier, Boris ^a   Troisfontaines, Paul ^b   Vertommen, Didier ^a   Marenne, Marie Noëlle ^a   Rider, Mark ^a   Parsot, Claude ^c   Cornelis, Guy R ^a,b  

^a DE DUVE INSTITUTE   (Belgium)

^b UNIVERSITY OF BASEL   (Switzerland)

^c INSTITUT PASTEUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CHAPERONE; PROTEIN SYCB; PROTEIN YSA; PROTEIN YSPA; PROTEIN YSPB; PROTEIN YSPC; PROTEIN YSPD; UNCLASSIFIED DRUG; YERSINIA OUTER PROTEIN E;

AMINO ACID SEQUENCE; ARTICLE; HELA CELL; HUMAN; HUMAN CELL; LOW TEMPERATURE; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PLASMID; PRIORITY JOURNAL; PROMOTER REGION; SALMONELLA ENTERICA; SEQUENCE ANALYSIS; SHIGELLA FLEXNERI; YERSINIA ENTEROCOLITICA;

ANIMALS; BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL PROTEINS; BIOLOGICAL TRANSPORT; CELL LINE; CHROMOSOMES, BACTERIAL; GENE EXPRESSION REGULATION, BACTERIAL; HELA CELLS; HUMANS; MACROPHAGES; MICE; MOLECULAR CHAPERONES; MOLECULAR SEQUENCE DATA; SEQUENCE ANALYSIS, DNA; SUBSTRATE SPECIFICITY; YERSINIA ENTEROCOLITICA;

EID: 0037218166     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.71.1.242-253.2003     Document Type: Article

References (65)

1. Bernardini, M. L., J. Mounier, H. d'Hauteville, M. Coquis-Rondon, and P. J. Sansonetti. 1989. Identification of icsA, a plasmid locus of Shigella flexneri that governs bacterial intra- and intercellular spread through interaction with F-actin. Proc. Natl. Acad. Sci. USA 86:3867-3871.
2. Boland, A., and G. R. Cornelis. 1998. Role of YopP in suppression of tumor necrosis factor alpha release by macrophages during Yersinia infection. Infect. Immun. 66:1878-1884.
3. Buchrieser, C., P. Glaser, C. Rusniok, H. Nedjari, H. D'Hauteville, F. Kunst, P. Sansonetti, and C. Parsot. 2000. The virulence plasmid pWR100 and the repertoire of proteins secreted by the type III secretion apparatus of Shigella flexneri. Mol. Microbiol. 38:760-771.
4. Carniel, E., I. Guilvout, and M. Prentice. 1996. Characterization of a large chromosomal "high-pathogenicity island" in biotype 1B Yersinia enterocolitica. J. Bacteriol. 178:6743-6751.
5. Chen, Y., M. R. Smith, K. Thirumalai, and A. Zychlinsky. 1996. A bacterial invasin induces macrophage apoptosis by binding directly to ICE. EMBO J. 15:3853-3860.
6. Clauser, K. R., P. Baker, and A. L. Burlingame. 1999. Role of accurate mass measurement (± 10 ppm) in protein identification strategies employing MS or MS/MS and database searching. Anal. Chem. 71:2871-2882.
7. Cornelis, G., Y. Laroche, G. Balligand, M. P. Sory, and G. Wauters. 1987. Yersinia enterocolitica, a primary model for bacterial invasiveness. Rev. Infect. Dis. 9:64-87.
8. Cornelis, G. R., and H. Wolf-Watz. 1997. The Yersinia Yop virulon: A bacterial system for subverting eukaryotic cells. Mol. Microbiol. 23:861-867.
9. Cover, T. L., and R. C. Aber. 1989. Yersinia enterocolitica. N. Engl. J. Med. 321:16-24.
10. Demers, B., P. J. Sansonetti, and C. Parsot. 1998. Induction of type III secretion in Shigella flexneri is associated with differential control of transcription of genes encoding secreted proteins. EMBO J. 17:2894-2903.
11. Foultier, B., P. Troisfontaines, S. Müller, F. R. Opperdoes, and G. R. Cornelis. 2002. Characterization of the ysa pathogenicity locus in the chromosome of Yersinia enterocolitica and phylogeny analysis of type III secretion systems. J. Mol. Evol. 55:37-51.
12. Frithz-Lindsten, E., A. Holmstrom, L Jacobsson, M. Soltani, J. Olsson, R. Rosqvist, and A. Forsberg. 1998. Functional conservation of the effector protein translocators PopB/YopB and PopD/YopD of Pseudomonas aeruginosa and Yersinia pseudotuberculosis. Mol. Microbiol. 29:1155-1165.
13. Grutzkau, A., C. Hanski, H. Hahn, and E. O. Riecken. 1990. Involvement of M cells in the bacterial invasion of Peyer's patches: A common mechanism shared by Yersinia enterocolitica and other enteroinvasive bacteria. Gut 31: 1011-1015.
14. Haller, J. C., S. Carlson, K. J. Pederson, and D. E. Pierson. 2000. A chromosomally encoded type III secretion pathway in Yersinia enterocolitica is important in virulence. Mol. Microbiol. 36:1436-1446.
15. Hanski, C., U. Kutschka, H. P. Schmoranzer, M. Naumann, A. Stallmach, H. Hahn, H. Menge, and E. O. Riecken. 1989. Immunohistochemical and electron microscopic study of interaction of Yersinia enterocolitica serotype 08 with intestinal mucosa during experimental enteritis. Infect. Immun. 57:673-678.
16. Hermant, D., R. Menard, N. Arricau, C. Parsot, and M. Y. Popoff. 1995. Functional conservation of the Salmonella and Shigella effectors of entry into epithelial cells. Mol. Microbiol. 17:781-789.
17. High, N., J. Mounier, M. C. Prevost, and P. J. Sansonetti. 1992. IpaB of Shigella flexneri causes entry into epithelial cells and escape from the phagocytic vacuole. EMBO J. 11:1991-1999.
18. Ichinohe, H., M. Yoshioka, H. Fukushima, S. Kaneko, and T. Maruyama. 1991. First isolation of Yersinia enterocolitica serotype O:8 in Japan. J. Clin. Microbiol. 29:846-847.
19. Iriarte, M., and G. R. Cornelis. 1998. YopT, a new Yersinia Yop effector protein, affects the cytoskeleton of host cells. Mol. Microbiol. 29:915-929.
20. Isberg, R. R., and S. Falkow. 1985. A single genetic locus encoded by Yersinia pseudotuberculosis permits invasion of cultured animal cells by Escherichia coli K-12. Nature 317:262-264.
21. Issartel, J. P., V. Koronakis, and C. Hughes. 1991. Activation of Escherichia coli prohaemolysin to the mature toxin by acyl carrier protein-dependent fatty acylation. Nature 351:759-761.
22. Kaneko, S., and T. Maruyama. 1987. Pathogenicity of Yersinia enterocolitica serotype O3 biotype 3 strains. J. Clin. Microbiol. 25:454-455.
23. Kaniga, K., I. Delor, and G. R. Cornelis. 1991. A wide-host-range suicide vector for improving reverse genetics in gram-negative bacteria: Inactivation of the blaA gene of Yersinia enterocolitica. Gene 109:137-141.
24. Kaniga, K., S. Tucker, D. Trollinger, and J. E. Galan. 1995. Homologs of the Shigella IpaB and IpaC invasins are required for Salmonella typhimurium entry into cultured epithelial cells. J. Bacteriol. 177:3965-3971.
25. Lafleur, L., O. Hammerberg, G. Delage, and C. H. Pai. 1979. Yersinia enterocolitica infection in children: 4 Years experience in the Montreal urban community. Contrib. Microbiol. Immunol. 5:298-303.
26. Makino, S., C. Sasakawa, K. Kamata, T. Kurata, and M. Yoshikawa. 1986. A genetic determinant required for continuous reinfection of adjacent cells on large plasmid in S. flexneri 2a. Cell 46:551-555.
27. Marjai, E., M. Kalman, I. Kajary, A. Belteky, and M. Rodler. 1987. Isolation from food and characterization by virulence tests of Yersinia enterocolitica associated with an outbreak. Acta Microbiol. Hung. 34:97-109.
28. Mavris, M., A. L. Page, R. Tournebize, B. Demers, P. Sansonetti, and C. Parsot. 2002. Regulation of transcription by the activity of the Shigella flexneri type III secretion apparatus. Mol. Microbiol. 43:1543-1553.
29. Menard, R., M. C. Prevost, P. Gounon, P. Sansonetti, and C. Dehio. 1996. The secreted Ipa complex of Shigella flexneri promotes entry into mammalian cells. Proc. Natl. Acad. Sci. USA 93:1254-1258.
30. Menard, R., P. Sansonetti, and C. Parsot. 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.
31. Menard, R., P. Sansonetti, C. Parsot, and T. Vasselon. 1994. Extracellular association and cytoplasmic partitioning of the IpaB and IpaC invasins of S. flexneri. Cell 79:515-525.
32. Menard, R., P. J. Sansonetti, and C. Parsot. 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.
33. Miao, E. A., C. A. Scherer, R. M. Tsolis, R. A. Kingsley, L. G. Adams, A. J. Baumler, and S. L. Miller. 1999. Salmonella typhimurium leucine-rich repeat proteins are targeted to the SPI1 and SPI2 type III secretion systems. Mol. Microbiol. 34:850-864.
34. Michiels, T., P. Wattiau, R. Brasseur, J. M. Ruysschaert, and G. Cornelis. 1990. Secretion of Yop proteins by yersiniae. Infect. Immun. 58:2840-2849.
35. Mills, S. D., A. Boland, M. P. Sory, P. van der Smissen, C. Kerbourch, B. B. Finlay, and G. R. Cornelis. 1997. Yersinia enterocolitica induces apoptosis in macrophages by a process requiring functional type III secretion and translocation mechanisms and involving YopP, presumably acting as an effector protein. Proc. Natl. Acad. Sci. USA 94:12638-12643.
36. Mirold, S., W. Rabsch, M. Rohde, S. Stender, H. Tschape, H. Russmann, E. Igwe, and W. D. Hardt. 1999. Isolation of a temperate bacteriophage encoding the type III effector protein SopE from an epidemic Salmonella typhimurium strain. Proc. Natl. Acad. Sci. USA 96:9845-9850.
37. Neyt, C., and G. Cornelis. 1999. 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. 33:971-981.
38. Neyt, C., and G. R, Cornelis. 1999. Role of SycD, the chaperone of the Yersinia Yop translocators YopB and YopD. Mol. Microbiol. 31:143-156.
39. Nhieu, G. T., and P. J. Sansonetti. 1999. Mechanism of Shigella entry into epithelial cells. Curr. Opin. Microbiol. 2:51-55.
40. Page, A. L., H. Ohayon, P. J. Sansonetti, and C. Parsot. 1999. The secreted IpaB and IpaC invasins and their cytoplasmic chaperone IpgC are required for intercellular dissemination of Shigella flexneri. Cell. Microbiol. 1:183-193.
41. Page, A. L., P. Sansonetti, and C. Parsot. 2002. Spa15 of Shigella flexneri, a third type of chaperone in the type III secretion pathway. Mol. Microbiol. 43:1533-1542.
42. Parsot, C., R. Menard, P. Gounon, and P. J. Sansonetti. 1995. Enhanced secretion through the Shigella flexneri Mxi-Spa translocon leads to assembly of extracellular proteins into macromolecular structures. Mol. Microbiol. 16:291-300.
43. Portnoy, D. A., S. L. Moseley, and S. Falkow. 1981. Characterization of plasmids and plasmid-associated determinants of Yersinia enterocolitica pathogenesis. Infect. Immun. 31:775-782.
44. Rakin, A., C. Noelting, S. Schubert, and J. Heesemann. 1999. Common and specific characteristics of the high-pathogenicity island of Yersinia enterocolitica. Infect. Immun. 67:5265-5274.
45. Rosqvist, R., I. Bolin, and H. Wolf-Watz. 1988. Inhibition of phagocytosis in Yersinia pseudotuberculosis: A virulence plasmid-encoded ability involving the Yop2b protein. Infect. Immun. 56:2139-2143.
46. Sansonetti, P. J., J. Arondel, J. R. Cantey, M. C. Prevost, and M. Huerre, 1996. Infection of rabbit Peyer's patches by Shigella flexneri: Effect of adhesive or invasive bacterial phenotypes on follicle-associated epithelium. Infect. Immun. 64:2752-2764.
47. Sansonetti, P. J., D. J. Kopecko, and S. B. Formal. 1982. Involvement of a plasmid in the invasive ability of Shigella flexneri. Infect. Immun. 35:852-860.
48. Sansonetti, P. J., A. Ryter, P. Clerc, A. T. Maurelli, and J. Mounier. 1986. Multiplication of Shigella flexneri within HeLa cells: Lysis of the phagocytic vacuole and plasmid-mediated contact hemolysis. Infect. Immun. 51:461-469.
49. Sarker, M. R., C. Neyt, I. Stainier, and G. R. Cornelis. 1998. The Yersinia Yop virulon: LcrV is required for extrusion of the translocators YopB and YopD. J. Bacteriol. 180:1207-1214.
50. Sasakawa, C., B. Adler, T. Tobe, N. Okada, S. Nagai, K. Komatsu, and M. Yoshikawa. 1989. Functional organization and nucleotide sequence of virulence Region-2 on the large virulence plasmid in Sizigella flexneri 2a. Mol. Microbiol. 3:1191-1201.
51. Sasakawa, C., K. Kamata, T. Sakai, S. Makino, M. Yamada, N. Okada, and M. Yoshikawa. 1988. Virulence-associated genetic regions comprising 31 kilobases of the 230-kilobase plasmid in Shigella flexneri 2a. J. Bacteriol. 170:2480-2484.
52. Sory, M. P., A. Boland, I. Lambermont, and G. R. Cornelis. 1995. 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 92:11998-12002.
53. Sory, M. P., and G. R. Cornelis. 1994. Translocation of a hybrid YopEadenylate cyclase from Yersinia enterocolitica into HeLa cells. Mol. Microbiol. 14:583-594.
54. Stanley, P., L. C. Packman, V. Koronakis, and C. Hughes. 1994. Fatty acylation of two internal lysine residues required for the toxic activity of Escherichia coli hemolysin. Science 266:1992-1996.
55. Stebbins, C. E., and J. E. Galan. 2001. Maintenance of an unfolded polypeptide by a cognate chaperone in bacterial type III secretion. Nature 414:77-81.
56. Tacket, C. O., J. Ballard, N. Harris, J. Allard, C. Nolan, T. Quan, and M. L. Cohen. 1985. An outbreak of Yersinia enterocolitica infections caused by contaminated tofu (soybean curd). Am. J. Epidemiol. 121:705-711.
57. Tilney, L. G., and D. A. Portnoy. 1989. Actin filaments and the growth, movement, and spread of the intracellular bacterial parasite, Listeria monocytogenes. J. Cell Biol. 109:1597-1608.
58. Venkatesan, M. M., J. M. Buysse, and D. J. Kopecko. 1988. Characterization of invasion plasmid antigen genes (ipaBCD) from Shigella flexneri. Proc. Natl. Acad. Sci. USA 85:9317-9321.
59. Wassef, J. S., D. F. Keren, and J. L. Mailloux. 1989. Role of M cells in initial antigen uptake and in ulcer formation in the rabbit intestinal loop model of shigellosis. Infect. Immun. 57:858-863.
60. Wauters, G., K. Kandolo, and M. Janssens. 1987. Revised biogrouping scheme of Yersinia enterocolitica. Contrib. Microbiol. Immunol. 9:14-21.
61. Wilm, M., and M. Mann. 1996. Analytical properties of the nanoelectrospray ion source. Anal. Chem. 68:1-8.
62. Young, B. M., and G. M. Young. 2002. Evidence for targeting of Yop effectors by the chromosomally encoded Ysa type III secretion system of Yersinia enterocolitica. J. Bacteriol. 184:5563-5571.
63. Young, B. M., and G. M. Young. 2002. YP1A is exported by the Ysc, Ysa, and flagellar type III secretion systems of Yersinia enterocolitica. J. Bacteriol. 184:1324-1334.
64. Zychlinsky, A., B. Kenny, R. Menard, M. C. Prevost, I. B. Holland, and P. J. Sansonetti. 1994. IpaB mediates macrophage apoptosis induced by Shigella flexneri. Mol. Microbiol. 11:619-627.
65. Zychlinsky, A., M. C. Prevost, and P. J. Sansonetti. 1992. Shigella flexneri induces apoptosis in infected macrophages. Nature 358:167-169.