Salmonella typhimurium leucine-rich repeat proteins are targeted to the SPl1 and SPl2 type III secretion systems

Molecular Microbiology

Volumn 34, Issue 4, 1999, Pages 850-864

  Miao, Edward A ^a   Scherer, Christina A ^a   Tsolis, Renée M ^b   Kingsley, Robert A ^c   Adams, L Garry ^b   Bäumler, Andreas J ^c   Miller, Samuel I ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b TEXAS A AND M UNIVERSITY   (United States)

^c TEXAS A AND M UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CYCLIC AMP; HYBRID PROTEIN; VIRULENCE FACTOR;

ARTICLE; CONTROLLED STUDY; GENE NUMBER; NONHUMAN; PRIORITY JOURNAL; PROTEIN SECRETION; PROTEIN TARGETING; SALMONELLA TYPHIMURIUM; SALMONELLOSIS; TRANSCRIPTION REGULATION;

ANIMALIA; BACTERIA (MICROORGANISMS); EUKARYOTA; NEGIBACTERIA; PROKARYOTA; SALMONELLA TYPHIMURIUM; SHIGELLA FLEXNERI; TYPHIMURIUM; YERSINIA;

EID: 0032701087     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.1999.01651.x     Document Type: Article

References (62)

1. Alpuche-Aranda, C.M., Berthiaume, E.P., Mock, B., Swanson, J.A., and Miller, S.I. (1995) Spacious phagosome formation within mouse macrophages correlates with Salmonella serotype pathogenicity and host susceptibility. Infect Immun 63:4456-4462.
2. Bajaj, V., Hwang, C., and Lee, C.A. (1995) hilA is a novel ompR/toxR family member that activates the expression of Salmonella typhimurium invasion genes. Mol Microbiol 18: 715-727.
3. Bajaj, V., Lucas, R.L., Hwang, C., and Lee, C.A. (1996) Coordinate regulation of Salmonella typhimurium invasion genes by environmental and regulatory factors is mediated by control of hilA expression. Mol Microbiol 22: 703-714.
4. Benson, N.R., and Goldman, B.S. (1992) Rapid mapping in Salmonella typhimurium with Mud-P22 prophages. J Bacteriol 174: 1673-1681.
5. Boland, A., Sory, M.P., Iriarte, M., Kerbourch, C., Wattiau, P., and Cornelis, G.R. (1996) 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: 5191-5201.
6. Buchanan, S.G., and Gay, N.J. (1996) Structural and functional diversity in the leucine-rich repeat family of proteins. Prog Biophys Mol Biol 65: 1-44.
7. Buysse, J.M., Hartman, A.B., Strockbine, N., and Venkatesan, M. (1995) Genetic polymorphism of the ipaH multicopy antigen gene in Shigella spps. & enteroinvasive Escherichia coil. Microb Pathog 19: 335-349.
8. Chen, L.M., Kaniga, K., and Galán, J.E. (1996) Salmonella spp. are cytotoxic for cultured macrophages. Mol Microbiol 21: 1101-1115.
9. Cirillo, D.M., Valdivia, R.H., Monack, D.M., and Falkow, S. (1998) Macrophage-dependent induction of the Salmonella pathogenicity island 2 type III secretion system and its role in intracellular survival. Mol Microblol 30: 175-188.
10. Davis, R.W., Botstein, D., and Roth, J.R. (1980) Advanced Bacterial Genetics: A Manual for Genetic Engineering. Cold Spring Harbor, NY: Cold Spring, Harbor Laboratory Press.
11. Deiwick, J., Nikolaus, T., Shea, J.E., Gleeson, C., Holden, D.W., and Hensel, M. (1998) Mutations in Salmonella pathogenicity island 2 (SPI2) genes affecting transcription of SPI1 genes and resistance to antimicrobial agents. J Bacteriol 180: 4775-4780.
12. Deiwick, J., Nikolaus, T., Erdogan, S., and Hensel, M. (1999) Environmental regulation of Salmonella pathogenicity island 2 gene expression. Mol Microbiol 31: 1759-1773.
13. Demers, B., Sansonetti, P.J., and Parsot, C. (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.
14. Francis, C.L., Ryan, T.A., Jones, B.D., Smith, S.J., and Falkow, S. (1993) Ruffles induced by Salmonella and other stimuli direct macropinocytosis of bacteria. Nature 364: 639-642.
15. Freiberg, C., Fellay, R., Bairoch, A., Broughton, W.J., Rosenthal, A., and Perret, X. (1997) Molecular basis of symbiosis between Rhizobium and legumes. Nature 387: 394-401.
16. Fu, Y., and Galán, J.E. (1998) The Salmonella typhimurium tyrosine phosphatase SptP is translocated into host cells and disrupts the actin cytoskeleton. Mol Microbiol 27: 359-368.
17. Galyov, E.E., Wood, M.W., Rosqvist, R., Mullan, P.B., Watson, P.R., Hedges, S., and Wallis, T.S. (1997) A secreted effector protein of Salmonella dublin is translocated into eukaryotic cells and mediates inflammation and fluid secretion in infected ileal mucosa. Mol Microbiol 25: 903-912.
18. Gunn, J.S., and Miller, S.I. (1996) PhoP-PhoQ activates transcription of pmrAB, encoding a two-component regulatory system involved in Salmonella typhimurium antimicrobial peptide resistance. J Bacteriol 178: 6857-6864.
19. Gunn, J.S., Belden, W.J., and Miller, S.I. (1998) Identification of PhoP-PhoQ activated genes within a duplicated region of the Salmonella typhimurium chromosome. Microb Pathog 25: 77-90.
20. BAD promoter. J Bacteriol 177: 4121-4130.
21. Hardt, W.D., Urlaub, H., and Galán, J.E. (1998a) A substrate of the centisome 63 type III protein secretion system of Salmonella typhimurium is encoded by a cryptic bacteriophage. Proc Natl Acad Sci USA 95: 2574-2579.
22. Hardt, W.D., Chen, L.M., Schuebel, K.E., Bustelo, X.R., and Galán, J.E. (1998b) S. typhimurium encodes an activator of Rho GTPases that induces membrane ruffling and nuclear responses in host cells. Cell 93: 815-826.
23. Hensel, M., Shea, J.E., Gleeson, C., Jones, M.D., Dalton, E., and Holden, D.W. (1995) Simultaneous identification of bacterial virulence genes by negative selection. Science 269: 400-403.
24. Hensel, M., Shea, J.E., Raupach, B., Monack, D., Falkow, S., Gleeson, C., Kubo, T., and Holden, D.W. (1997) Functional analysis of ssaJ and the ssaK/U operon, 13 genes encoding components of the type III secretion apparatus of Salmonella pathogenicity island 2. Mol Microbiol 24: 155-167.
25. Hensel, M., Shea, J.E., Waterman, S.R., Mundy, R., Nikolaus, T., Banks, G., et al. (1998) Genes encoding putative effector proteins of the type III secretion system of Salmonella pathogenicity island 2 are required for bacterial virulence and proliferation in macrophages. Mol Microbiol 30: 163-174.
26. Hobble, S., Chen, L.M., Davis, R.J., and Galán, J.E. (1997) Involvement of mitogen-activated protein kinase pathways in the nuclear responses and cytokine production induced by Salmonella typhimurium in cultured intestinal epithelial cells. J Immunol 159: 5550-5559.
27. Hoiseth, S.K., and Stocker, B.A. (1981) Aromatic-dependent Salmonella typhimurium are non-virulent and effective as live vaccines. Nature 291: 238-239.
28. Hong, K.H., and Miller, V.L. (1998) Identification of a novel Salmonella invasion locus homologous to Shigella ipgDE. J Bacteriol 180: 1793-1802.
29. Hueck, C.J. (1998) Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol Mol Biol Rev 62: 379-433.
30. Hueck, C.J., Hantman, M.J., Bajaj, V., Johnston, C., Lee, C.A., and Miller, S.I. (1995) Salmonella typhimurium secreted invasion determinants are homologous to Shigella Ipa proteins. Mol Microbiol 18: 479-490.
31. Johnston, C., Pegues, D.A., Hueck, C.J., Lee, A., and Miller, S.I. (1996) Transcriptional activation of Salmonella typhimurium invasion genes by a member of the phosphorylated response-regulator superfamily. Mol Microbiol 22: 715-727.
32. Jones, M.A., Wood, M.W., Mullan, P.B., Watson, P.R., Wallis, T.S., and Galyov, E.E. (1998) Secreted effector proteins of Salmonella dublin act in concert to induce enteritis. Infect Immun 66: 5799-5804.
33. Kaniga, K., Uralil, J., Bliska, J.B., and Galán, J.E. (1996) A secreted protein tyrosine phosphatase with modular effector domains in the bacterial pathogen Salmonella typhimurium. Mol Microbiol 21: 633-641.
34. Leckie, F., Mattei, B., Capodicasa, C., Hemmings, A., Nuss, L., De Aracri, B., etal. (1999) The specificity of polygalacturonase-inhibiting protein (PGIP): A single amino acid substitution in the solvent-exposed β-strand/β-turn region of the leucinerich repeats (LRRs) confers a new recognition capability. Embo J 18: 2352-2363.
35. Leung, K.Y., Reisner, B.S., and Straley, S.C. (1990) YopM inhibits platelet aggregation and is necessary for virulence of Yersinia pestis in mice. Infect Immun 58: 3262-3271.
36. McCormick, B.A., Colgan, S.P., Delp-Archer, C., Miller, S.I., and Madara, J.L. (1993) Salmonella typhimurium attachment to human intestinal epithelial monolayers: Transcellular signalling to subepithelial neutrophils. J Cell Biol 123: 895-907.
37. Miller, S.I., and Mekalanos, J.J. (1990) Constitutive expression of the phoP regulon attenuates Salmonella virulence and survival within macrophages. J Bacteriol 172: 2485-2490.
38. Miller, S.I., Kukral, A.M., and Mekalanos, J.J. (1989) A two-component regulatory system (phoP/phoQ) controls Salmonella typhimurium virulence. Proc Natl Acad Sci USA 86: 5054-5058.
39. Miller, S.I., Hohmann, E.L., and Pegues, D.A. (1995) Salmonella (Including Salmonella typhi). New York, NY: Churchill Livingston.
40. Monack, D.M., Raupach, B., Hromockyj, A.E., and Falkow, S. (1996) Salmonella typhimurium invasion induces apoptosis in infected macrophages. Proc Natl Acad Sci USA 93: 9833-9838.
41. Norris, F.A., Wilson, M.P., Wallis, T.S., Galyov, E.E., and Majerus, P.W. (1998) SopB, a protein required for virulence of Salmonella dublin, is an inositol phosphate phosphatase. Proc Natl Acad Sci USA 95: 14057-14059.
42. Ochman, H., Soncini, F.C., Solomon, F., and Groisman, E.A. (1996) Identification of a pathogenicity island required for Salmonella survival in host cells. Proc Natl Acad Sci USA 93: 7800-7804.
43. Pegues, D.A., Hantman, M.J., Behlau, I., and Miller, S.I. (1995) PhoP/PhoQ transcriptional repression of Salmonella typhimurium invasion genes: Evidence for a role in protein secretion. Mol Microbiol 17: 169-181.
44. 2+-response plasmid pCD1 of Yersinia pestis KIM5. Infect Immun 66: 4611-4623.
45. Rakeman, J.L., Bonifield, H.R., and Miller, S.I. (1999) A HilA-independent pathway to Salmonella typhimurium invasion gene transcription. J Bacteriol 181: 3096-3104.
46. Schesser, K., Frithz-Lindsten, E., and Wolf-Watz, H. (1996) Delineation and mutational analysis of the Yersinia pseudotuberculosis YopE domains which mediate translocation across bacterial and eukaryotic cellular membranes. J Bacteriol 178: 7227-7233.
47. Sebo, P., Glaser, P., Sakamoto, H., and Ullmann, A. (1991) High-level synthesis of active adenylate cyclase toxin of Bordetella pertussis in a reconstructed Escherichia coli system. Gene 104:19-24.
48. Shea, J.E., Beuzon, C.R., Gleeson, C., Mundy, R., and Holden, D.W. (1999) Influence of the Salmonella typhimurium pathogenicity island 2 type III secretion system on bacterial growth In the mouse. Infect Immun 67: 213-219.
49. Skorupski, K., and Taylor, R.K. (1996) Positive selection vectors for allelic exchange. Gene 169: 47-52.
50. Skrzypek, E., Cowan, C., and Straley, S.C. (1998) Targeting of the Yersinia pestis YopM protein into HeLa cells and intracellular trafficking to the nucleus. Mol Microbiol 30: 1051-1065.
51. Sory, M.P., and Cornelis, G.R. (1994) Translocation of a hybrid YopE-adenylate cyclase from Yersinia enterocolitica into HeLa cells. Mol Microbiol 14: 583-594.
52. Sory, M.P., Boland, A., Lambermont, I., and Cornelis, G.R. (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. Stojiljkovic, I., Bäumler, A.J., and Heffron, F. (1995) Ethanolamine utilization in Salmonella typhimurium: Nucleotide sequence, protein expression, and mutational analysis of the cchA cchB eutE eutJ eutG eutH gene cluster. J Bacteriol 177: 1357-1366.
54. Tang, W.-J.Y. (1993) Blot-affinity purification of antibodies. In Antibodies in Cell Biology. Asai, D.J. (eds), San Diego, CA: Academic Press, pp. 95-100.
55. Tsolis, R.M., Adams, L.G., Ficht, T.A., and Bäumler, A.J. (1999a) Contribution of Salmonella typhimurium virulence factors to diarrheal disease in calves. Infect Immun 67: 4879-4885.
56. Tsolis, R.M., Townsend, S.M., Miao, E.A., Miller, S.I., Ficht, T.A., Adams, L.G., and Bäumler, A.J. (1999b) Identification of a putative Salmonella typhimurium host range factor with homology to IpaH and YopM by signature-tagged mutagenesis. Infect Immun 67: (in press).
57. Valdivia, R.H., and Falkow, S. (1997) Fluorescence-based isolation of bacterial genes expressed within host cells. Science 277: 2007-2011.
58. Venkatesan, M.M., Buysse, J.M., and Hartman, A.B. (1991) Sequence variation in two ipaH genes of Shigella flexneri 5 and homology to the LRG-like family of proteins. Mol Microbiol 5: 2435-2445.
59. Wang, R.F., and Kushner, S.R. (1991) Construction of versatile low-copy-number vectors for cloning, sequencing and gene expression in Escherichia coll. Gene 100: 195-199.
60. Wolff, C., Nisan, I., Hanski, E., Frankel, G., and Rosenshine, I. (1998) Protein translocation into host epithelial cells by infecting enteropathogenic Escherichia coli. Mol Microbiol 28: 143-155.
61. Wood, M.W., Rosqvist, R., Mullan, P.B., Edwards, M.H., and Galyov, E.E. (1996) SopE, a secreted protein of Salmonella dublin, is translocated into the target eukaryotic cell via a sip-dependent mechanism and promotes bacterial entry. Mol Microbiol 22: 327-338.
62. Zhou, D., Mooseker, M.S., and Galán, J.E. (1999) Role of the S. typhimurium actin-binding protein SipA in bacterial internalization. Science 283: 2092-2095.