Diminished LcrV secretion attenuates Yersinia pseudotuberculosis virulence

Journal of Bacteriology

Volumn 189, Issue 23, 2007, Pages 8417-8429

  Bröms, Jeanette E ^a,b,c   Francis, Matthew S ^a   Forsberg, Åke ^a,b  

^a UMEÅ UNIVERSITY   (Sweden)

^b SWEDISH DEFENCE RESEARCH AGENCY   (Sweden)

^c UMEÅ UNIVERSITY HOSPITAL   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEIN; PROTEIN LCRV; REGULATOR PROTEIN; TOLL LIKE RECEPTOR 2; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL VIRULENCE; CELL MEMBRANE; CONTROLLED STUDY; GENE MUTATION; GENE TRANSLOCATION; GENETIC VARIABILITY; HOST CELL; HUMAN; HUMAN CELL; IMMUNOMODULATION; IN VITRO STUDY; MOUSE; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN SECRETION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; TARGET CELL; YERSINIA PSEUDOTUBERCULOSIS;

ANIMALS; ANTIGENS, BACTERIAL; BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL PROTEINS; FEMALE; HELA CELLS; HUMANS; MICE; MICE, INBRED C57BL; MUTATION; NUCLEIC ACID CONFORMATION; PORE FORMING CYTOTOXIC PROTEINS; RNA, BACTERIAL; VIRULENCE; YERSINIA PSEUDOTUBERCULOSIS; YERSINIA PSEUDOTUBERCULOSIS INFECTIONS;

BACTERIA (MICROORGANISMS); MURINAE; NEGIBACTERIA; YERSINIA PSEUDOTUBERCULOSIS;

EID: 36749036576     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00936-07     Document Type: Article

References (64)

1. Anderson, D. M., and O. Schneewind. 1997. A mRNA signal for the type III secretion of Yop proteins by Yersinia enterocolitica. Science 278:1140-1143.
2. Anderson, D. M., and O. Schneewind. 1999. Yersinia enterocolitica type III secretion: an mRNA signal that couples translation and secretion of YopQ. Mol. Microbiol. 31:1139-1148.
3. Auerbuch, V., and R. R. Isberg. 2007. Growth of Yersinia pseudotuberculosis in mice occurs independently of Toll-like receptor 2 expression and induction of interleukin-10. Infect. Immun. 75:3561-3570.
4. Bölin, I., L. Norlander, and H. Wolf-Watz. 1982. Temperature-inducible outer membrane protein of Yersinia pseudotuberculosis and Yersinia enterocolitica is associated with the virulence plasmid. Infect. Immun. 37:506-512.
5. Bölin, I., and H. Wolf-Watz. 1984. Molecular cloning of the temperature-inducible outer membrane protein 1 of Yersinia pseudotuberculosis. Infect. Immun. 43:72-78.
6. Bröms, J. E., C. Sundin, M. S. Francis, and Å. Forsberg. 2003. Comparative analysis of type III effector translocation by Yersinia pseudotuberculosis expressing native LcrV or PcrV from Pseudomonas aeruginosa. J. Infect. Dis. 188:239-249.
7. Cornelis, G. R., A. Boland, A. P. Boyd, C. Geuijen, M. Iriarte, C. Neyt, M. P. Sory, and I. Stainier. 1998. The virulence plasmid of Yersinia, an antihost genome. Microbiol. Mol. Biol. Rev. 62:1315-1352.
8. Cowan, C., A. V. Philipovskiy, C. R. Wulff-Strobel, Z. Ye, and S. C. Straley. 2005. Anti-LcrV antibody inhibits delivery of Yops by Yersinia pestis KIM5 by directly promoting phagocytosis. Infect. Immun. 73:6127-6137.
9. DeBord, K. L., V. T. Lee, and O. Schneewind. 2001. Roles of LcrG and LcrV during type III targeting of effector Yops by Yersinia enterocolitica. J. Bacteriol. 183:4588-1598.
10. Derewenda, U., A. Mateja, Y. Devedjiev, K. M. Routzahn, A. G. Evdokimov, Z. S. Derewenda, and D. S. Waugh. 2004. The structure of Yersinia pestis V-antigen, an essential virulence factor and mediator of immunity against plague. Structure (Cambridge) 12:301-306.
11. Fields, K. A., M. L. Nilles, C. Cowan, and S. C. Straley. 1999. Virulence role of V antigen of Yersinia pestis at the bacterial surface. Infect. Immun. 67: 5395-5408.
12. Francis, M. S., S. A. Lloyd, and H. Wolf-Watz. 2001. 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. 42:1075-1093.
13. Francis, M. S., and H. Wolf-Watz. 1998. YopD of Yersinia pseudotuberculosis is translocated into the cytosol of HeLa epithelial cells: evidence of a structural domain necessary for translocation. Mol. Microbiol. 29:799-813.
14. Ghosh, P. 2004. Process of protein transport by the type III secretion system. Microbiol. Mol. Biol. Rev. 68:771-795.
15. Goure, J., P. Broz, O. Attree, G. R. Cornelis, and I. Attree. 2005. Protective anti-V antibodies inhibit Pseudomonas and Yersinia translocon assembly within host membranes. J. Infect. Dis. 192:218-225.
16. Håkansson, S., K. Schesser, C. Persson, E. E. Galyov, R. Rosqvist, F. Homble, and H. Wolf-Watz. 1996. 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. 15:5812-5823.
17. 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 O8 with intestinal mucosa during experimental enteritis. Infect. Immun. 57:673-678.
18. Hill, J., S. E. Leary, K. F. Griffin, E. D. Williamson, and R. W. Titball. 1997. Regions of Yersinia pestis V antigen that contribute to protection against plague identified by passive and active immunization. Infect. Immun. 65: 4476-4482.
19. Holmström, A., J. Olsson, P. Cherepanov, E. Maier, R. Nordfelth, J. Pettersson, R. Benz, H. Wolf-Watz, and Å. Forsberg. 2001. LcrV is a channel size-determining component of the Yop effector translocon of Yersinia. Mol. Microbiol. 39:620-632.
20. Horton, R. M., and L. R. Pease. 1991. Recombination and mutagenesis of DNA sequences using PCR, p. 217-247. In M. J. McPherson (ed.), Directed mutagenesis: a practical approach. Oxford University Press, New York, NY.
21. Karavolos, M. H., A. J. Roe, M. Wilson, J. Henderson, J. J. Lee, D. L. Gally, and C. M. Khan. 2005. Type III secretion of the Salmonella effector protein SopE is mediated via an N-terminal amino acid signal and not an mRNA sequence. J. Bacteriol. 187:1559-1567.
22. Lawton, D. G., C. Longstaff, B. A. Wallace, J. Hill, S. E. Leary, R. W. Titball, and K. A. Brown. 2002. Interactions of the type III secretion pathway proteins LcrV and LcrG from Yersinia pestis are mediated by coiled-coil domains. J. Biol. Chem. 277:38714-38722.
23. Lee, V. T., C. Tam, and O. Schneewind. 2000. LcrV, a substrate for Yersinia enterocolitica type III secretion, is required for toxin targeting into the cytosol of HeLa cells. J. Biol. Chem. 275:36869-36875.
24. Lian, C. J., W. S. Hwang, and C. H. Pai. 1987. Plasmid-mediated resistance to phagocytosis in Yersinia enterocolitica. Infect. Immun. 55:1176-1183.
25. Lloyd, S. A., Å. Forsberg, H. Wolf-Watz, and M. S. Francis. 2001. Targeting exported substrates to the Yersinia TTSS: different functions for different signals? Trends Microbiol. 9:367-371.
26. Lloyd, S. A., M. Norman, R. Rosqvist, and H. Wolf-Watz. 2001. Yersinia YopE is targeted for type III secretion by N-terminal, not mRNA, signals. Mol. Microbiol. 39:520-531.
27. Marenne, M. N., L. Journet, L. J. Mota, and G. R. Cornells. 2003. Genetic analysis of the formation of the Ysc-Yop translocation pore in macrophages by Yersinia enterocolitica: role of LcrV, YscF and YopN. Microb. Pathog. 35:243-258.
28. Marketon, M. M., R. W. DePaolo, K. L. DeBord, B. Jabri, and O. Schneewind. 2005. Plague bacteria target immune cells during infection. Science 309:1739-1741.
29. Mathews, D. H., J. Sabina, M. Zuker, and D. H. Turner. 1999. Expanded sequence dependence of thermodynamic parameters improves prediction of RNA secondary structure. J. Mol. Biol. 288:911-940.
30. Matson, J. S., and M. L. Nilles. 2001. LcrG-LcrV interaction is required for control of Yops secretion in Yersinia pestis. J. Bacteriol. 183:5082-5091.
31. Milton, D. L., R. O'Toole, P. Horstedt, and H. Wolf-Watz. 1996. Flagellin A is essential for the virulence of Vibrio anguillarum. J. Bacteriol. 178:1310-1319.
32. Motin, V. L., R. Nakajima, G. B. Smirnov, and R. R. Brubaker. 1994. Passive immunity to yersiniae mediated by anti-recombinant V antigen and protein A-V antigen fusion peptide. Infect. Immun. 62:4192-4201.
33. Mueller, C. A., P. Broz, S. A. Muller, P. Ringler, F. Erne-Brand, I. Sorg, M. Kuhn, A. Engel, and G. R. Cornelis. 2005. The V-antigen of Yersinia forms a distinct structure at the tip of injectisome needles. Science 310:674-676.
34. Nakajima, R., V. L. Motin, and R. R. Brubaker. 1995. Suppression of cytokines in mice by protein A-V antigen fusion peptide and restoration of synthesis by active immunization. Infect. Immun. 63:3021-3029.
35. Neyt, C., and G. R. 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.
36. 2+ response. J. Bacteriol. 179:1307-1316.
37. Olsson, J., P. J. Edqvist, J. E. Bröms, Å. Forsberg, H. Wolf-Watz, and M. S. Francis. 2004. The YopD translocator of Yersinia pseudotuberculosis is a multifunctional protein comprised of discrete domains. J. Bacteriol. 186: 4110-4123.
38. Pallen, M. J., S. A. Beatson, and C. M. Bailey. 2005. Bioinformatics, genomics and evolution of non-flagellar type-III secretion systems: a Darwinian perspective. FEMS Microbiol. Rev. 29:201-229.
39. Pettersson, J., A. Holmström, J. Hill, S. Leary, E. Frithz-Lindsten, A. von Euler-Matell, E. Carlsson, R. Titball, Å. Forsberg, and H. Wolf-Watz. 1999. The V-antigen of Yersinia is surface exposed before target cell contact and involved in virulence protein translocation. Mol. Microbiol. 32:961-976.
40. Pettersson, J., R. Nordfelth, E. Dubinina, T. Bergman, M. Gustafsson, K. E. Magnusson, and H. Wolf-Watz. 1996. Modulation of virulence factor expression by pathogen target cell contact. Science 273:1231-1233.
41. Pouliot, K., N. Pan, S. Wang, S. Lu, E. Lien, and J. D. Goguen. 2007. Evaluation of the role of LcrV-Toll-like receptor 2-mediated immunomodulation in the virulence of Yersinia pestis. Infect. Immun. 75:3571-3580.
42. 2+ response virulence genes. J. Bacteriol. 173:2649-2657.
43. Ramamurthi, K. S., and O. Schneewind. 2003. Substrate recognition by the Yersinia type III protein secretion machinery. Mol. Microbiol. 50: 1095-1102.
44. Ramamurthi, K. S., and O. Schneewind. 2003. Yersinia yopQ mRNA encodes a bipartite type III secretion signal in the first 15 codons. Mol. Microbiol. 50:1189-1198.
45. Rimpiläinen, M., Å. Forsberg, and H. Wolf-Watz. 1992. A novel protein, LcrQ, involved in the low-calcium response of Yersinia pseudotuberculosis shows extensive homology to YopH. J. Bacteriol. 174:3355-3363.
46. Rosqvist, R., Å. Forsberg, and H. Wolf-Watz. 1991. Intracellular targeting of the Yersinia YopE cytotoxin in mammalian cells induces actin microfilament disruption. Infect. Immun. 59:4562-4569.
47. Rosqvist, R., C. Persson, S. Håkansson, R. Nordfeldt, and H. Wolf-Watz. 1995. Translocation of the Yersinia YopE and YopH virulence proteins into target cells is mediated by YopB and YopD. Contrib. Microbiol. Immunol. 13:230-234.
48. Simon, R., U. Priefer, and A. Pühler. 1983. A broad host range mobilisation system for in vivo genetic engineering: transposon mutagenesis in gram negative bacteria. Biotechnology 1:787-796.
49. Simonet, M., S. Richard, and P. Berche. 1990. Electron microscopic evidence for in vivo extracellular localization of Yersinia pseudotuberculosis harboring the pYV plasmid. Infect. Immun. 58:841-845.
50. Sing, A., D. Reithmeier-Rost, K. Granfors, J. Hill, A. Roggenkamp, and J. Heesemann. 2005. A hypervariable N-terminal region of Yersinia LcrV determines Toll-like receptor 2-mediated IL-10 induction and mouse virulence. Proc. Natl. Acad. Sci. USA 102:16049-16054.
51. Sing, A., A. Roggenkamp, A. M. Geiger, and J. Heesemann. 2002. 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. 168:1315-1321.
52. Sing, A., D. Rost, N. Tvardovskaia, A. Roggenkamp, A. Wiedemann, C. J. Kirschning, M. Aepfelbacher, and J. Heesemann. 2002. Yersinia V-antigen exploits Toll-like receptor 2 and CD14 for interleukin 10-mediated immunosuppression. J. Exp. Med. 196:1017-1024.
53. 2+ response, and virulence of Yersinia pestis. J. Bacteriol. 177:2530-2542.
54. Sorg, J. A., N. C. Miller, and O. Schneewind. 2005. Substrate recognition of type III secretion machines - testing the RNA signal hypothesis. Cell. Microbiol. 7:1217-1225.
55. Sory, M. P., and G. R. Cornelis. 1994. Translocation of a hybrid YopE-adenylate cyclase from Yersinia enterocolitica into HeLa cells. Mol. Microbiol. 14:583-594.
56. Stainier, I., M. Iriarte, and G. R. Cornelis. 1997. YscM1 and YscM2, two Yersinia enterocolitica proteins causing downregulation of yop transcription. Mol. Microbiol. 26:833-843.
57. 2+ in Yersinia pestis include structural genes for outer membrane proteins. Infect. Immun. 51:445-454.
58. Tardy, F., F. Homble, C. Neyt, R. Wattiez, G. R. Cornelis, J. M. Ruysschaert, and V. Cabiaux. 1999. Yersinia enterocolitica type III secretion-translocation system: channel formation by secreted Yops. EMBO J. 18:6793-6799.
59. Titball, R. W., and E. D. Williamson. 2001. Vaccination against bubonic and pneumonic plague. Vaccine 19:4175-4184.
60. Viboud, G. I., and J. B. Bliska. 2005. Yersinia outer proteins: role in modulation of host cell signaling responses and pathogenesis. Annu. Rev. Microbiol. 59:69-89.
61. Warren, S. M., and G. M. Young. 2005. An amino-terminal secretion signal is required for Yp1A export by the Ysa, Ysc, and flagellar type III secretion systems of Yersinia enterocolitica biovar 1B. J. Bacteriol. 187:6075-6083.
62. Weeks, S., J. Hill, A. Friedlander, and S. Welkos. 2002. Anti-V antigen antibody protects macrophages from Yersinia pestis-induced cell death and promotes phagocytosis. Microb. Pathog. 32:227-237.
63. Wulff-Strobel, C. R., A. W. Williams, and S. C. Straley. 2002. LcrQ and SycH function together at the Ysc type III secretion system in Yersinia pestis to impose a hierarchy of secretion. Mol. Microbiol. 43:411-423.
64. Zuker, M. 2003. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 31:3406-3415.