Adaptation to the host environment: regulation of the SPI1 type III secretion system in Salmonella enterica serovar Typhimurium

Current Opinion in Microbiology

Volumn 10, Issue 1, 2007, Pages 24-29

  Ellermeier, Jeremy R ^a   Slauch, James M ^a,b  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b UNIVERSITY OF ILLINOIS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

OUTER MEMBRANE PROTEIN REGULATOR;

EVOLUTIONARY ADAPTATION; GENE EXPRESSION; GENETIC TRANSCRIPTION; HOST; NONHUMAN; PATHOGENICITY ISLAND; REVIEW; SALMONELLA TYPHIMURIUM;

ADAPTATION, PHYSIOLOGICAL; BACTERIAL PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; GENOMIC ISLANDS; PROTEIN TRANSPORT; SALMONELLA TYPHIMURIUM; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; VIRULENCE;

SALMONELLA; SALMONELLA ENTERICA; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM;

EID: 33846842428     PISSN: 13695274     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mib.2006.12.002     Document Type: Review

References (53)

1. Zhou D., and Galan J. Salmonella entry into host cells: the work in concert of type III secreted effector proteins. Microbes Infect 3 (2001) 1293-1298
2. Wallis T.S., and Galyov E.E. Molecular basis of Salmonella-induced enteritis. Mol Microbiol 36 (2000) 997-1005
3. Tsolis R.M., Adams L.G., Hantman M.J., Scherer C.A., Kimbrough T., Kingsley R.A., Ficht T.A., Miller S.I., and Baumler A.J. SspA is required for lethal Salmonella enterica serovar Typhimurium infections in calves but is not essential for diarrhea. Infect Immun 68 (2000) 3158-3163
4. Zhang S., Santos R.L., Tsolis R.M., Stender S., Hardt W.D., Baumler A.J., and Adams L.G. The Salmonella enterica serotype Typhimurium effector proteins SipA, SopA, SopB, SopD, and SopE2 act in concert to induce diarrhea in calves. Infect Immun 70 (2002) 3843-3855
5. Baumler A.J., Tsolis R.M., Ficht T.A., and Adams L.G. Evolution of host adaptation in Salmonella enterica. Infect Immun 66 (1998) 4579-4587
6. Porwollik S., Wong R.M., and McClelland M. Evolutionary genomics of Salmonella: gene acquisitions revealed by microarray analysis. Proc Natl Acad Sci USA 99 (2002) 8956-8961
7. Gallois A., Klein J.R., Allen L.A., Jones B.D., and Nauseef W.M. Salmonella pathogenicity island 2-encoded type III secretion system mediates exclusion of NADPH oxidase assembly from the phagosomal membrane. J Immunol 166 (2001) 5741-5748
8. Vazquez-Torres A., and Fang F.C. Salmonella evasion of the NADPH phagocyte oxidase. Microbes Infect 3 (2001) 1313-1320
9. Marlovits T.C., Kubori T., Sukhan A., Thomas D.R., Galan J.E., and Unger V.M. Structural insights into the assembly of the type III secretion needle complex. Science 306 (2004) 1040-1042
10. Marlovits T.C., Kubori T., Lara-Tejero M., Thomas D., Unger V.M., and Galan J.E. Assembly of the inner rod determines needle length in the type III secretion injectisome. Nature 441 (2006) 637-640
11. Akeda Y., and Galan J.E. Chaperone release and unfolding of substrates in type III secretion. Nature 437 (2005) 911-915
12. Yip C.K., Kimbrough T.G., Felise H.B., Vuckovic M., Thomas N.A., Pfuetzner R.A., Frey E.A., Finlay B.B., Miller S.I., and Strynadka N.C. Structural characterization of the molecular platform for type III secretion system assembly. Nature 435 (2005) 702-707
13. Lostroh C.P., and Lee C.A. The Salmonella pathogenicity island-1 type III secretion system. Microbes Infect 3 (2001) 1281-1291
14. Lee C.A., Jones B.D., and Falkow S. Identification of a Salmonella typhimurium invasion locus by selection for hyperinvasive mutants. Proc Natl Acad Sci USA 89 (1992) 1847-1851
15. Darwin K.H., and Miller V.L. InvF is required for expression of genes encoding proteins secreted by the SPI1 type III secretion apparatus in Salmonella typhimurium. J Bacteriol 181 (1999) 4949-4954
16. Eichelberg K., and Galan J.E. Differential regulation of Salmonella typhimurium type III secreted proteins by pathogenicity island 1 (SPI-1)-encoded transcriptional activators InvF and HilA. Infect Immun 67 (1999) 4099-4105
17. Bajaj V., Hwang C., and Lee C.A. hilA is a novel ompR/toxR family member that activates the expression of Salmonella typhimurium invasion genes. Mol Microbiol 18 (1995) 715-727
18. Ahmer B.M., van Reeuwijk J., Watson P.R., Wallis T.S., and Heffron F. Salmonella SirA is a global regulator of genes mediating enteropathogenesis. Mol Microbiol 31 (1999) 971-982
19. Ellermeier C.D., Ellermeier J.R., and Slauch J.M. HilD, HilC and RtsA constitute a feed forward loop that controls expression of the SPI1 type three secretion system regulator hilA in Salmonella enterica serovar Typhimurium. Mol Microbiol 57 (2005) 691-705. This work demonstrates the regulation of rtsA, hilC, hilD, and hilA by HilC, HilD and RtsA, and that each regulator has a role in the host during infection. It also demonstrates BarA/SirA and EnvZ/OmpR control of hilA through HilD. These data form the basis of our current model of SPI1 regulation.
20. Martin R.G., and Rosner J.L. The AraC transcriptional activators. Curr Opin Microbiol 4 (2001) 132-137
21. Darwin K.H., and Miller V.L. The putative invasion protein chaperone SicA acts together with InvF to activate the expression of Salmonella typhimurium virulence genes. Mol Microbiol 35 (2000) 949-960
22. Darwin K.H., and Miller V.L. Type III secretion chaperone-dependent regulation: activation of virulence genes by SicA and InvF in Salmonella typhimurium. EMBO J 20 (2001) 1850-1862
23. Schechter L.M., and Lee C.A. AraC/XylS family members, HilC and HilD, directly bind and derepress the Salmonella typhimurium hilA promoter. Mol Microbiol 40 (2001) 1289-1299
24. Olekhnovich I.N., and Kadner R.J. DNA-binding activities of the HilC and HilD virulence regulatory proteins of Salmonella enterica serovar Typhimurium. J Bacteriol 184 (2002) 4148-4160
25. Ellermeier C.D., and Slauch J.M. RtsA and RtsB coordinately regulate expression of the invasion and flagellar genes in Salmonella enterica serovar Typhimurium. J Bacteriol 185 (2003) 5096-5108
26. De Keersmaecker S.C., Marchal K., Verhoeven T.L., Engelen K., Vanderleyden J., and Detweiler C.S. Microarray analysis and motif detection reveal new targets of the Salmonella enterica serovar Typhimurium HilA regulatory protein, including hilA itself. J Bacteriol 187 (2005) 4381-4391
27. Lostroh C.P., and Lee C.A. The HilA box and sequences outside it determine the magnitude of HilA-dependent activation of P(prgH) from Salmonella pathogenicity island 1. J Bacteriol 183 (2001) 4876-4885
28. Ellermeier C.D., and Slauch J.M. RtsA coordinately regulates DsbA and the Salmonella pathogenicity island 1 type III secretion system. J Bacteriol 186 (2004) 68-79
29. Tsolis R.M., Townsend S.M., Miao E.A., Miller S.I., Ficht T.A., Adams L.G., and Baumler A.J. Identification of a putative Salmonella enterica serotype Typhimurium host range factor with homology to IpaH and YopM by signature-tagged mutagenesis. Infect Immun 67 (1999) 6385-6393
30. Olekhnovich I.N., and Kadner R.J. Crucial roles of both flanking sequences in silencing of the hilA promoter in Salmonella enterica. J Mol Biol 357 (2006) 373-386
31. Schechter L.M., Jain S., Akbar S., and Lee C.A. The small nucleoid-binding proteins H-NS, HU, and Fis affect hilA expression in Salmonella enterica serovar Typhimurium. Infect Immun 71 (2003) 5432-5435
32. AltierC: Genetic and environmental control of Salmonella invasion. J Microbiol 2005, 43 Spec No:85-92.
33. Pratt L.A., Hsing W., Gibson K.E., and Silhavy T.J. From acids to osmZ: multiple factors influence synthesis of the OmpF and OmpC porins in Escherichia coli. Mol Microbiol 20 (1996) 911-917
34. Feng X., Walthers D., Oropeza R., and Kenney L.J. The response regulator SsrB activates transcription and binds to a region overlapping OmpR binding sites at Salmonella pathogenicity island 2. Mol Microbiol 54 (2004) 823-835
35. Lucas R.L., and Lee C.A. Roles of hilC and hilD in regulation of hilA expression in Salmonella enterica serovar Typhimurium. J Bacteriol 183 (2001) 2733-2745
36. Romeo T. Global regulation by the small RNA-binding protein CsrA and the non-coding RNA molecule CsrB. Mol Microbiol 29 (1998) 1321-1330
37. Johnston C., Pegues D.A., Hueck C.J., Lee A., and Miller S.I. Transcriptional activation of Salmonella typhimurium invasion genes by a member of the phosphorylated response-regulator superfamily. Mol Microbiol 22 (1996) 715-727
38. Rakeman J.L., Bonifield H.R., and Miller S.I. A HilA-independent pathway to Salmonella typhimurium invasion gene transcription. J Bacteriol 181 (1999) 3096-3104
39. Lawhon S.D., Frye J.G., Suyemoto M., Porwollik S., McClelland M., and Altier C. Global regulation by CsrA in Salmonella typhimurium. Mol Microbiol 48 (2003) 1633-1645
40. Prouty A.M., and Gunn J.S. Salmonella enterica serovar Typhimurium invasion is repressed in the presence of bile. Infect Immun 68 (2000) 6763-6769
41. Suzuki K., Wang X., Weilbacher T., Pernestig A.K., Melefors O., Georgellis D., Babitzke P., and Romeo T. Regulatory circuitry of the CsrA/CsrB and BarA/UvrY systems of Escherichia coli. J Bacteriol 184 (2002) 5130-5140
42. Weilbacher T., Suzuki K., Dubey A.K., Wang X., Gudapaty S., Morozov I., Baker C.S., Georgellis D., Babitzke P., and Romeo T. A novel sRNA component of the carbon storage regulatory system of Escherichia coli. Mol Microbiol 48 (2003) 657-670
43. Fortune D.R., Suyemoto M., and Altier C. Identification of CsrC and characterization of its role in epithelial cell invasion in Salmonella enterica serovar Typhimurium. Infect Immun 74 (2006) 331-339. This work demonstrates the effects of the CsrA-antagonistic small RNAs CsrB and CsrC, which alter the levels of SPI1 gene expression and Salmonella invasion. In addition, the authors demonstrate that deletions of both csrB and csrC combine to give an invasion defect similar to that of a sirA deletion, suggesting SirA-mediated SPI1 regulation occurs entirely through the csr system.
44. Teplitski M., Goodier R.I., and Ahmer B.M. Pathways leading from BarA/SirA to motility and virulence gene expression in Salmonella. J Bacteriol 185 (2003) 7257-7265
45. Masse E., and Gottesman S. A small RNA regulates the expression of genes involved in iron metabolism in Escherichia coli. Proc Natl Acad Sci USA 99 (2002) 4620-4625
46. Vecerek B., Moll I., Afonyushkin T., Kaberdin V., and Blasi U. Interaction of the RNA chaperone Hfq with mRNAs: direct and indirect roles of Hfq in iron metabolism of Escherichia coli. Mol Microbiol 50 (2003) 897-909
47. Geissmann T.A., and Touati D. Hfq, a new chaperoning role: binding to messenger RNA determines access for small RNA regulator. EMBO J 23 (2004) 396-405
48. Masse E., Vanderpool C.K., and Gottesman S. Effect of RyhB small RNA on global iron use in Escherichia coli. J Bacteriol 187 (2005) 6962-6971
49. Baxter M.A., Fahlen T.F., Wilson R.L., and Jones B.D. HilE interacts with HilD and negatively regulates hilA transcription and expression of the Salmonella enterica serovar Typhimurium invasive phenotype. Infect Immun 71 (2003) 1295-1305
50. Yeh K.S., Tinker J.K., and Clegg S. FimZ binds the Salmonella typhimurium fimA promoter region and may regulate its own expression with FimY. Microbiol Immunol 46 (2002) 1-10
51. Baxter M.A., and Jones B.D. The fimYZ genes regulate Salmonella enterica serovar Typhimurium invasion in addition to type 1 fimbrial expression and bacterial motility. Infect Immun 73 (2005) 1377-1385
52. Jones BD: Salmonella invasion gene regulation: a story of environmental awareness. J Microbiol 2005, 43 Spec No:110-117.
53. Baxter M, Jones BD: Identification of regulatory pathways that translate environmental signals into changes in expression of Salmonella motility, adherence, and invasion [abstract]. 103rd General Meeting of the American Society for Microbiology 2003, abstr. D-110.