Transcription of the plasmid-encoded toxin gene from Enteroaggregative Escherichia coli is regulated by a novel co-activation mechanism involving CRP and Fis

Molecular Microbiology

Volumn 81, Issue 1, 2011, Pages 179-191

  Rossiter, Amanda E ^a   Browning, Douglas F ^a   Leyton, Denisse L ^a   Johnson, Matthew D ^a   Godfrey, Rita E ^a   Wardius, Catherine A ^a   Desvaux, Mickael ^a   Cunningham, Adam F ^a   Ruiz Perez, Fernando ^b   Nataro, James P ^b   Busby, Stephen J W ^a   Henderson, Ian R ^a  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP BINDING PROTEIN; FACTOR FOR INVERSION STIMULATION;

ARTICLE; BACTERIAL GENE; CONTROLLED STUDY; ENTEROAGGREGATIVE ESCHERICHIA COLI; MUTATIONAL ANALYSIS; NONHUMAN; PET GENE; PRIORITY JOURNAL; PROMOTER REGION; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; TRANSPOSON;

BACTERIAL TOXINS; BASE SEQUENCE; CYCLIC AMP RECEPTOR PROTEIN; DNA TRANSPOSABLE ELEMENTS; ENTEROTOXINS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; FACTOR FOR INVERSION STIMULATION PROTEIN; GENE EXPRESSION REGULATION, BACTERIAL; MOLECULAR SEQUENCE DATA; MUTAGENESIS, INSERTIONAL; PLASMIDS; SERINE ENDOPEPTIDASES; TRANSCRIPTION, GENETIC;

ESCHERICHIA COLI;

EID: 79959563147     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2011.07685.x     Document Type: Article

References (53)

1. Akhter, Y., Yellaboina, S., Farhana, A., Ranjan, A., Ahmed, N., and Hasnain, S.E. (2008) Genome scale portrait of cAMP-receptor protein (CRP) regulons in mycobacteria points to their role in pathogenesis. Gene 407: 148-158.
2. Al-Hasani, K., Navarro-Garcia, F., Huerta, J., Sakellaris, H., and Adler, B. (2009) The immunogenic SigA enterotoxin of Shigella flexneri 2a binds to HEp-2 cells and induces fodrin redistribution in intoxicated epithelial cells. PLoS ONE 4: e8223.
3. Baba, T., Ara, T., Hasegawa, M., Takai, Y., Okumura, Y., Baba, M., etal. (2006) Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol 2: 20060008.
4. Bell, A., Gaston, K., Williams, R., Chapman, K., Kolb, A., Buc, H., etal. (1990) Mutations that alter the ability of the Escherichia coli cyclic AMP receptor protein to activate transcription. Nucleic Acids Res 18: 7243-7250.
5. Belyaeva, T.A., Rhodius, V.A., Webster, C.L., and Busby, S.J. (1998) Transcription activation at promoters carrying tandem DNA sites for the Escherichia coli cyclic AMP receptor protein: organisation of the RNA polymerase alpha subunits. J Mol Biol 277: 789-804.
6. Betancourt-Sanchez, M., and Navarro-Garcia, F. (2009) Pet secretion, internalization and induction of cell death during infection of epithelial cells by enteroaggregative Escherichia coli. Microbiology 155: 2895-2906.
7. Browning, D., Savery, N., Kolb, A., and Busby, S. (2009) Assays for transcription factor activity. Methods Mol Biol 543: 369-387.
8. Browning, D.F., and Busby, S.J. (2004) The regulation of bacterial transcription initiation. Nat Rev Microbiol 2: 57-65.
9. Browning, D.F., Lee, D.J., Wolfe, A.J., Cole, J.A., and Busby, S.J. (2006) The Escherichia coli K-12 NarL and NarP proteins insulate the nrf promoter from the effects of integration host factor. J Bacteriol 188: 7449-7456.
10. Chaudhuri, R.R., Sebaihia, M., Hobman, J.L., Webber, M.A., Leyton, D.L., Goldberg, M.D., etal. (2010) Complete genome sequence and comparative metabolic profiling of the prototypical enteroaggregative Escherichia coli strain 042. PLoS ONE 5: e8801.
11. Desvaux, M., Parham, N.J., and Henderson, I.R. (2004a) The autotransporter secretion system. Res Microbiol 155: 53-60.
12. Desvaux, M., Parham, N.J., and Henderson, I.R. (2004b) Type V protein secretion: simplicity gone awry? Curr Issues Mol Biol 6: 111-124.
13. Desvaux, M., Khan, A., Beatson, S.A., Scott-Tucker, A., and Henderson, I.R. (2005) Protein secretion systems in Fusobacterium nucleatum: genomic identification of Type 4 piliation and complete Type V pathways brings new insight into mechanisms of pathogenesis. Biochim Biophys Acta 1713: 92-112.
14. Desvaux, M., Cooper, L.M., Filenko, N.A., Scott-Tucker, A., Turner, S.M., Cole, J.A., and Henderson, I.R. (2006) The unusual extended signal peptide region of the type V secretion system is phylogenetically restricted. FEMS Microbiol Lett 264: 22-30.
15. Dorman, C.J. (1995) 1995 Flemming Lecture. DNA topology and the global control of bacterial gene expression: implications for the regulation of virulence gene expression. Microbiology 141: 71-1280.
16. Ebright, R.H., Ebright, Y.W., and Gunasekera, A. (1989) Consensus DNA site for the Escherichia coli catabolite gene activator protein (CAP): CAP exhibits a 450-fold higher affinity for the consensus DNA site than for the E. coli lac DNA site. Nucleic Acids Res 17: 10295-10305.
17. Emmer, M., deCrombrugghe, B., Pastan, I., and Perlman, R. (1970) Cyclic AMP receptor protein of E. coli: its role in the synthesis of inducible enzymes. Proc Natl Acad Sci USA 66: 480-487.
18. Eslava, C., Navarro-Garcia, F., Czeczulin, J.R., Henderson, I.R., Cravioto, A., and Nataro, J.P. (1998) Pet, an autotransporter enterotoxin from enteroaggregative Escherichia coli. Infect Immun 66: 3155-3163.
19. Gaston, K., Bell, A., Kolb, A., Buc, H., and Busby, S. (1990) Stringent spacing requirements for transcription activation by CRP. Cell 62: 733-743.
20. Grainger, D.C., and Busby, S.J. (2008) Global regulators of transcription in Escherichia coli: mechanisms of action and methods for study. Adv Appl Microbiol 65: 93-113.
21. Guyer, D.M., Henderson, I.R., Nataro, J.P., and Mobley, H.L. (2000) Identification of sat, an autotransporter toxin produced by uropathogenic Escherichia coli. Mol Microbiol 38: 53-66.
22. Harrington, S.M., Dudley, E.G., and Nataro, J.P. (2006) Pathogenesis of enteroaggregative Escherichia coli infection. FEMS Microbiol Lett 254: 12-18.
23. Henderson, I.R., and Lam, A.C. (2001) Polymorphic proteins of Chlamydia spp.-autotransporters beyond the Proteobacteria. Trends Microbiol 9: 573-578.
24. Henderson, I.R., Hicks, S., Navarro-Garcia, F., Elias, W.P., Philips, A.D., and Nataro, J.P. (1999) Involvement of the enteroaggregative Escherichia coli plasmid-encoded toxin in causing human intestinal damage. Infect Immun 67: 5338-5344.
25. Henderson, I.R., Navarro-Garcia, F., Desvaux, M., Fernandez, R.C., and Ala'Aldeen, D. (2004) Type V protein secretion pathway: the autotransporter story. Microbiol Mol Biol Rev 68: 692-744.
26. Jayaraman, P.S., Peakman, T.C., Busby, S.J., Quincey, R.V., and Cole, J.A. (1987) Location and sequence of the promoter of the gene for the NADH-dependent nitrite reductase of Escherichia coli and its regulation by oxygen, the Fnr protein and nitrite. J Mol Biol 196: 781-788.
27. Koch, C., and Kahmann, R. (1986) Purification and properties of the Escherichia coli host factor required for inversion of the G segment in bacteriophage Mu. J Biol Chem 261: 15673-15678.
28. Kolb, A., Kotlarz, D., Kusano, S., and Ishihama, A. (1995) Selectivity of the Escherichia coli RNA polymerase E sigma 38 for overlapping promoters and ability to support CRP activation. Nucleic Acids Res 23: 819-826.
29. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
30. Lodge, J., Fear, J., Busby, S., Gunasekaran, P., and Kamini, N.R. (1992) Broad host range plasmids carrying the Escherichia coli lactose and galactose operons. FEMS Microbiol Lett 74: 271-276.
31. McLeod, S.M., Xu, J., and Johnson, R.C. (2000) Coactivation of the RpoS-dependent proP P2 promoter by fis and cyclic AMP receptor protein. J Bacteriol 182: 4180-4187.
32. Mallik, P., Paul, B.J., Rutherford, S.T., Gourse, R.L., and Osuna, R. (2006) DksA is required for growth phase-dependent regulation, growth rate-dependent control, and stringent control of fis expression in Escherichia coli. J Bacteriol 188: 5775-5782.
33. Marteyn, B., West, N.P., Browning, D.F., Cole, J.A., Shaw, J.G., Palm, F., etal. (2010) Modulation of Shigella virulence in response to available oxygen in vivo. Nature 465: 355-358.
34. Miller, J. (1972) Experiments in Molecular Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
35. Morin, N., Tirling, C., Ivison, S.M., Kaur, A.P., Nataro, J.P., and Steiner, T.S. (2010) Autoactivation of the AggR regulator of enteroaggregative Escherichia coli in vitro and in vivo. FEMS Immunol Med Microbiol 58: 344-355.
36. Muller, C.M., Aberg, A., Straseviciene, J., Emody, L., Uhlin, B.E., and Balsalobre, C. (2009) Type 1 fimbriae, a colonization factor of uropathogenic Escherichia coli, are controlled by the metabolic sensor CRP-cAMP. PLoS Pathog 5: e1000303.
37. Nataro, J.P., Deng, Y., Cookson, S., Cravioto, A., Savarino, S.J., Guers, L.D., etal. (1995) Heterogeneity of enteroaggregative Escherichia coli virulence demonstrated in volunteers. J Infect Dis 171: 465-468.
38. O'Croinin, T., Carroll, R.K., Kelly, A., and Dorman, C.J. (2006) Roles for DNA supercoiling and the Fis protein in modulating expression of virulence genes during intracellular growth of Salmonella enterica serovar Typhimurium. Mol Microbiol 62: 869-882.
39. Parham, N.J., Pollard, S.J., Desvaux, M., Scott-Tucker, A., Liu, C., Fivian, A., and Henderson, I.R. (2005) Distribution of the serine protease autotransporters of the Enterobacteriaceae among extraintestinal clinical isolates of Escherichia coli. J Clin Microbiol 43: 4076-4082.
40. Pul, U., Lux, B., Wurm, R., and Wagner, R. (2008) Effect of upstream curvature and transcription factors H-NS and LRP on the efficiency of Escherichia coli rRNA promoters P1 and P2 - a phasing analysis. Microbiology 154: 2546-2558.
41. Rhen, M., and Dorman, C.J. (2005) Hierarchical gene regulators adapt Salmonella enterica to its host milieus. Int J Med Microbiol 294: 487-502.
42. Rhodius, V.A., West, D.M., Webster, C.L., Busby, S.J., and Savery, N.J. (1997) Transcription activation at class II CRP-dependent promoters: the role of different activating regions. Nucleic Acids Res 25: 326-332.
43. Ruiz-Perez, F., Henderson, I.R., Leyton, D.L., Rossiter, A.E., Zhang, Y., and Nataro, J.P. (2009) Roles of periplasmic chaperone proteins in the biogenesis of serine protease autotransporters of Enterobacteriaceae. J Bacteriol 191: 6571-6583.
44. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
45. Sarkar, G., and Sommer, S.S. (1990) The 'megaprimer' method of site-directed mutagenesis. Biotechniques 8: 404-407.
46. Sasse-Dwight, S., and Gralla, J.D. (1988) Probing co-operative DNA-binding in vivo. The lac O1:O3 interaction. J Mol Biol 202: 107-119.
47. Sheikh, J., Hicks, S., Dall'Agnol, M., Phillips, A.D., and Nataro, J.P. (2001) Roles for Fis and YafK in biofilm formation by enteroaggregative Escherichia coli. Mol Microbiol 41: 983-997.
48. Steen, J.A., Harrison, P., Seemann, T., Wilkie, I., Harper, M., Adler, B., and Boyce, J.D. (2010) Fis is essential for capsule production in Pasteurella multocida and regulates expression of other important virulence factors. PLoS Pathog 6: e1000750.
49. Travers, A., Schneider, R., and Muskhelishvili, G. (2001) DNA supercoiling and transcription in Escherichia coli: the FIS connection. Biochimie 83: 213-217.
50. Ushida, C., and Aiba, H. (1990) Helical phase dependent action of CRP: effect of the distance between the CRP site and the -35 region on promoter activity. Nucleic Acids Res 18: 6325-6330.
51. West, D., Williams, R., Rhodius, V., Bell, A., Sharma, N., Zou, C., etal. (1993) Interactions between the Escherichia coli cyclic AMP receptor protein and RNA polymerase at class II promoters. Mol Microbiol 10: 789-797.
52. Won, H.S., Lee, Y.S., Lee, S.H., and Lee, B.J. (2009) Structural overview on the allosteric activation of cyclic AMP receptor protein. Biochim Biophys Acta 1794: 1299-1308.
53. Zubay, G., Schwartz, D., and Beckwith, J. (1970) Mechanism of activation of catabolite-sensitive genes: a positive control system. Proc Natl Acad Sci USA 66: 104-110.