IpaD of Shigella flexneri is independently required for regulation of Ipa protein secretion and efficient insertion of IpaB and IpaC into host membranes

Infection and Immunity

Volumn 73, Issue 3, 2005, Pages 1432-1440

  Picking, Wendy L ^a   Nishioka, Hiroaki ^b   Hearn, Patricia D ^a   Baxter, M Aaron ^a   Harrington, Amanda T ^a   Blocker, Ariel ^b   Picking, William D ^a  

^a UNIVERSITY OF KANSAS   (United States)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; PROTEIN IPAB; PROTEIN IPAC; PROTEIN IPAD; UNCLASSIFIED DRUG; BACTERIAL ANTIGEN; IPAB PROTEIN, SHIGELLA; IPAC PROTEIN, SHIGELLA; IPAD PROTEIN, SHIGELLA FLEXNERI;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL GENE; BACTERIAL VIRULENCE; CELL INVASION; CELL MEMBRANE; CELL VACUOLE; COLON MUCOSA; CONTROLLED STUDY; EMBRYO; GENE DELETION; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; INTESTINE CELL; MEMBRANE DAMAGE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN SECRETION; SHIGELLA FLEXNERI; TARGET CELL; TYPE III SECRETION SYSTEM; ANIMAL; CELL LINE; CYTOLOGY; ERYTHROCYTE MEMBRANE; GENE EXPRESSION REGULATION; GENETICS; HEMOLYSIS; INTESTINE; METABOLISM; MICROBIOLOGY; PATHOGENICITY;

ANIMALS; ANTIGENS, BACTERIAL; BACTERIAL PROTEINS; CELL LINE; CELL MEMBRANE; ERYTHROCYTE MEMBRANE; GENE DELETION; GENE EXPRESSION REGULATION, BACTERIAL; HEMOLYSIS; HUMANS; INTESTINES; SHIGELLA FLEXNERI;

EID: 15544376398     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.73.3.1432-1440.2005     Document Type: Article

References (39)

1. Allaoui, A., P. J. Sansonetti, and C. Parsot. 1993. MxiD, an outer membrane protein necessary for the secretion of the Shigella flexneri Ipa invasins. Mol. Microbiol. 7:59-68.
2. Bennett, J. C. Q., and C. Hughes. 2000. From flagellum assembly to virulence: the extended family of type III export chaperones. Trends Microbiol. 8:202-204.
3. Blocker, A., P. Gounon, E. Larquet, K. Niebuhr, V. Cabiaux, C. Parsot, and P. Sansonetti. 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., K. Komoriya, and S-I. Aizawa. 2003. Type III secretion systems and bacterial flagella: insights into their function from structural similarities. Proc. Natl. Acad. Sci. USA 100:3027-3030.
5. Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 7:248-254.
6. 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.
7. Davis, R., M. E. Marquart, D. Lucius, and W. D. Picking. 1998. Protein-protein interactions in the assembly of Shigella flexneri invasion plasmid antigens IpaB and IpaC into protein complexes. Biochim. Biophys. Acta 1429:45-56.
8. 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.
9. 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.
10. Goure, J., A. Pastor, E. Faudry, J. Chabert, A. Dessen, and I. Attree. 2004. The V antigen of Pseudomonas aeruginosa is required for assembly of the functional PopB/PopD translocation pore in host cell membranes. Infect. Immun. 72:4741-4750.
11. Hale, T. L. 1991. Genetic basis of virulence in Shigella species. Microbiol. Rev. 55:206-224.
12. Harrington, A. T., P. D. Hearn, W. L. Picking, J. R. Barker, A. Wessel, and W. D. Picking. 2003. Structural characterization of the N terminus of IpaC from Shigella flexneri. Infect. Immun. 71:1255-1264.
13. Holmstrom, A., J. Olsson, P. Cherepanov, E. Maier, R. Nordfelth, J. Pettersson, R. Benz, H. Wolf-Watz, and A. Forsberg. 2001. LcrV is a channel size-determining component of the Yop effector translocon of Yersinia. Mol. Microbiol. 39:620-632.
14. Hueck, C. J. 1998. Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol. Mol. Biol. Rev. 62:379-433.
15. Kaniga, K., D. Trollinger, and J. E. Galan. 1995. Identification of two targets of the type III protein secretion system encoded by the inv and spa loci of Salmonella typhimurium that have homology to the Shigella IpaD and IpaA proteins. J. Bacteriol. 177:7078-7085.
16. Kuwae, A., S. Yoshida, K. Tamano, H. Mimuro, T. Suzuki, and C. Sasakawa. 2001. Shigella invasion of macrophage requires the insertion of IpaC into the host plasma membrane: functional analysis of IpaC. J. Biol. Chem. 276:32230-32239.
17. Marquart, M. E., W. L. Picking, and W. D. Picking. 1995. Structural analysis of invasion plasmid antigen D (IpaD) from Shigella ftexneri. Biochem. Biophys. Res. Commun. 214:963-970.
18. Marquart, M. E., W. L. Picking, and W. D. Picking. 1996. Soluble invasion plasmid antigen C (IpaC) from Shigella flexneri elicits epithelial cell responses related to pathogen invasion. Infect. Immun. 64:4182-4187.
19. 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.
20. 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.
21. 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.
22. 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.
23. 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.
24. Nilles, M. L., K. A., Fields, and S. C. Straley. 1998. The V antigen of Yersinia pestis regulates Yop vectorial targeting as well as Yop secretion through effects on YopB and LcrG. J. Bacteriol. 180:3410-3420.
25. 2+ response. J. Bacteriol. 179:1307-1316.
26. Oaks, E. V., M. E. Wingfield, and S. B. Formal. 1985. Plaque formation by virulent Shigella flexneri. Infect. Immun. 48:124-129.
27. Osiecki, J. C., J. Barker, W. L. Picking, A. B. Serfis, E. Berring, S. Shah, A. Harrington, and W. D. Picking. 2001. IpaC from Shigella and SipC from Salmonella possess similar biochemical properties but are functionally distinct. Mol. Microbiol. 42:469-481.
28. Penheiter, K. L., N. Mathur, D. Giles, T. Fahlen, and B. D. Jones. 1997. Non-invasive Salmonella typhimurium mutants are avirulent because of an inability to enter and destroy M cells of ileal Peyer's patches. Mol. Microbiol. 24:697-709.
29. Pettersson, J., A. Holmstrom, J. Hill, S. Leary, E. Frithz-Lindsten, A. von Euler-Matell, E. Carlsson, R. Titball, A. 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.
30. Picking, W. L., L. Coye, J. C. Osiecki, A. Barnoski Serfis, E. Schaper, and W. D. Picking. 2001. Identification of functional regions within invasion plasmid antigen C (IpaC) of Shigella flexneri. Mol. Microbiol. 39:100-111.
31. 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.
32. Sarker, M. R., C. Neyt, I. Stainier, and G. R. Cornells. 1998. The Yersinia Yop virulon: LcrV is required for extrusion of the translocators YopB and YopD. J. Bacteriol. 180:1207-1214.
33. Schuch, R., and A. T. Maurelli. 2001. MxiM and MxiJ, base elements of the Mxi-Spa type III secretion system of Shigella, interact with and stabilize the MxiD secretin in the cell envelope. J. Bacteriol. 183:6991-6998.
34. Terajima, J., E. Moriishi, T. Kurata, and H. Watanabe. 1999. Preincubation of recombinant Ipa proteins of Shigella sonnei promotes entry of non-invasive Escherichia coli into HeLa cells. Microb. Pathog. 27:223-230.
35. Tran Van Nhieu, G., R. Bourdet-Sicard, G. Dumenil, A. Blocker, and P. J. Sansonetti. 2000. Bacterial signals and cell responses during Shigella entry into epithelial cells. Cell. Microbiol. 2:187-193.
36. Tran Van Nhieu, G., E. Caron, A. Hall, and P. J. Sansonetti. 1999. IpaC induces actin polymerization and filopodia formation during Shigella entry into epithelial cells. EMBO J. 18:3249-3262.
37. Turbyfill, K. R., S. W. Joseph, and E. V. Oaks. 1995. Recognition of three epitopic regions on invasion plasmid antigen C by immune sera of rhesus monkeys infected with Shigella flexneri 2a. Infect. Immun. 63:3927-3935.
38. Turbyfill, K. R., J. A. Mertz, C. P. Mallett, and E. V. Oaks. 1998. Identification of epitope and surface-exposed domains of Shigella flexneri invasion plasmid antigen D (IpaD). Infect. Immun. 66:1999-2006.
39. 1 integrin promotes entry of the bacteria into mammalian cells. J. Exp. Med. 183:991-999.