Locus of enterocyte effacement-encoded regulator (Ler) of pathogenic Escherichia coli competes off histone-like nucleoid-structuring protein (H-NS) through noncooperative DNA binding

Journal of Biological Chemistry

Volumn 289, Issue 20, 2014, Pages 13739-13750

  Winardhi, Ricksen S ^a,b,c   Gulvady, Ranjit ^b,c   Mellies, Jay L ^d   Yan, Jie ^b,c,e  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^d REED COLLEGE   (United States)

^e NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING ENERGY; ESCHERICHIA COLI; GENES; PROTEINS; TRANSCRIPTION;

BINDING MODES; DNA FOLDING; ENTEROHEMORRHAGIC ESCHERICHIA COLI; MAGNESIUM CONCENTRATIONS; MAGNETIC TWEEZERS; PATHOGENIC ESCHERICHIA COLI; PROTEIN CONCENTRATIONS; VIRULENCE GENE;

DNA;

BACTERIAL PROTEIN; HISTONE LIKE NUCLEOID STRUCTURING PROTEIN; LOCUS OF ENTEROCYTE EFFACEMENT ENCODED REGULATOR; MAGNESIUM CHLORIDE; POTASSIUM CHLORIDE; UNCLASSIFIED DRUG; BACTERIAL DNA; DNA BINDING PROTEIN; ESCHERICHIA COLI PROTEIN; H-NS PROTEIN, BACTERIA; LER PROTEIN, E COLI; PROTEIN BINDING; TRANSACTIVATOR PROTEIN;

ARTICLE; ATOMIC FORCE MICROSCOPY; BINDING AFFINITY; BINDING COMPETITION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ESCHERICHIA COLI; MAGNETIC TWEEZER; MAGNETISM; NONHUMAN; PATHOGENICITY ISLAND; PH; PRIORITY JOURNAL; PROTEIN DNA BINDING; TEMPERATURE; CHEMISTRY; CONFORMATION; DOSE RESPONSE; DRUG EFFECTS; ENTEROHEMORRHAGIC ESCHERICHIA COLI; ENTEROPATHOGENIC ESCHERICHIA COLI; ENZYME SPECIFICITY; GENETICS; METABOLISM;

BACTERIAL PROTEINS; BINDING, COMPETITIVE; DNA, BACTERIAL; DNA-BINDING PROTEINS; DOSE-RESPONSE RELATIONSHIP, DRUG; ENTEROHEMORRHAGIC ESCHERICHIA COLI; ENTEROPATHOGENIC ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; HYDROGEN-ION CONCENTRATION; MAGNESIUM CHLORIDE; NUCLEIC ACID CONFORMATION; POTASSIUM CHLORIDE; PROTEIN BINDING; SUBSTRATE SPECIFICITY; TEMPERATURE; TRANS-ACTIVATORS;

EID: 84901036070     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.545954     Document Type: Article

References (45)

1. Lucchini, S., Rowley, G., Goldberg, M. D., Hurd, D., Harrison, M., and Hinton, J. C. (2006) H-NS mediates the silencing of laterally acquired genes in bacteria. PLoS Pathog. 2, e81
2. Dorman, C. (2004) H-NS: a universal regulator for a dynamic genome. Nat. Rev. Microbiol. 2, 391-400
3. Fang, F. C., and Rimsky, S. (2008) New insights into transcriptional regulation by H-NS. Curr. Opin. Microbiol. 11, 113-120
4. Ali, S. S., Xia, B., Liu, J., and Navarre, W. W. (2012) Silencing of foreign DNA in bacteria. Curr. Opin. Microbiol. 15, 175-181
5. Torres, A. G., López-Sánchez, G. N., Milflores-Flores, L., Patel, S. D., Rojas- López, M., Martínez de la Peña, C. F., Arenas-Hernández, M. M., and Martínez-Laguna, Y. (2007) Ler and H-NS, regulators controlling expression of the long polar fimbriae of Escherichia coli O157:H7. J. Bacteriol. 189, 5916-5928
6. Berdichevsky, T., Friedberg, D., Nadler, C., Rokney, A., Oppenheim, A., and Rosenshine, I. (2005) Ler is a negative autoregulator of the LEE1 operon in enteropathogenic Escherichia coli. J. Bacteriol. 187, 349-357
7. Smyth, C. P., Lundbäck, T., Renzoni, D., Siligardi, G., Beavil, R., Layton, M., Sidebotham, J. M., Hinton, J. C., Driscoll, P. C., Higgins, C. F., and Ladbury, J. E. (2000) Oligomerization of the chromatin-structuring protein H-NS. Mol. Microbiol. 36, 962-972
8. Esposito, D., Petrovic, A., Harris, R., Ono, S., Eccleston, J. F., Mbabaali, A., Haq, I., Higgins, C. F., Hinton, J. C., Driscoll, P. C., and Ladbury, J. E. (2002) H-NS oligomerization domain structure reveals the mechanism for high order self-association of the intact protein. J. Mol. Biol. 324, 841-850
9. Ceschini, S., Lupidi, G., Coletta, M., Pon, C. L., Fioretti, E., and Angeletti, M. (2000) Multimeric self-assembly equilibria involving the histone-like protein H-NS. A thermodynamic study. J. Biol. Chem. 275, 729-734
10. Ueguchi, C., Seto, C., Suzuki, T., and Mizuno, T. (1997) Clarification of the dimerization domain and its functional significance for the Escherichia coli nucleoid protein H-NS. J. Mol. Biol. 274, 145-151
11. Amit, R., Oppenheim, A. B., and Stavans, J. (2003) Increased bending rigidity of single DNA molecules by H-NS, a temperature and osmolarity sensor. Biophys. J. 84, 2467-2473
12. Liu, Y., Chen, H., Kenney, L. J., and Yan, J. (2010) A divalent switch drives H-NS/DNA-binding conformations between stiffening and bridging modes. Genes Dev. 24, 339-344
13. Dame, R. T., Wyman, C., and Goosen, N. (2000) H-NS mediated compaction of DNA visualised by atomic force microscopy. Nucleic Acids Res. 28, 3504-3510
14. Winardhi, R. S., Fu, W., Castang, S., Li, Y., Dove, S. L., and Yan, J. (2012) Higher order oligomerization is required for H-NS family member MvaT to form gene-silencing nucleoprotein filament. Nucleic Acids Res. 40, 8942-8952
15. Lim, C. J., Whang, Y. R., Kenney, L. J., and Yan, J. (2012) Gene silencing H-NS paralogue StpA forms a rigid protein filament along DNA that blocks DNA accessibility. Nucleic Acids Res. 40, 3316-3328
16. Qu, Y., Lim, C. J., Whang, Y. R., Liu, J., and Yan, J. (2013) Mechanism of DNA organization by Mycobacterium tuberculosis protein Lsr2. Nucleic Acids Res. 41, 5263-5272
17. Lim, C. J., Lee, S. Y., Kenney, L. J., and Yan, J. (2012) Nucleoprotein filament formation is the structural basis for bacterial protein H-NS gene silencing. Sci. Rep. 2, 509
18. Walthers, D., Li, Y., Liu, Y., Anand, G., Yan, J., and Kenney, L. J. (2011) Salmonella enterica response regulator SsrB relieves H-NS silencing by displacing H-NS bound in polymerization mode and directly activates transcription. J. Biol. Chem. 286, 1895-1902
19. Sperandio, V., Mellies, J. L., Delahay, R. M., Frankel, G., Crawford, J. A., Nguyen, W., and Kaper, J. B. (2000) Activation of enteropathogenic Escherichia coli (EPEC) LEE2 and LEE3 operons by Ler. Mol. Microbiol. 38, 781-793
20. Mellies, J. L., Benison, G., McNitt, W., Mavor, D., Boniface, C., and Larabee, F. J. (2011) Ler of pathogenic Escherichia coli forms toroidal protein-DNA complexes. Microbiology 157, 1123-1133
21. Bustamante, V. H., Santana, F. J., Calva, E., and Puente, J. L. (2001) Transcriptional regulation of type III secretion genes in enteropathogenic Escherichia coli: Ler antagonizes H-NS-dependent repression. Mol. Microbiol. 39, 664-678
22. Dorman, C. J., Hinton, J. C., and Free, A. (1999) Domain organization and oligomerization among H-NS-like nucleoid-associated proteins in bacteria. Trends Microbiol. 7, 124-128
23. Cordeiro, T. N., Schmidt, H., Madrid, C., Juárez, A., Bernadó, P., Griesinger, C., García, J., and Pons, M. (2011) Indirect DNA readout by an H-NS related protein: structure of the DNA complex of the C-terminal domain of Ler. PLoS Pathog. 7, e1002380
24. Elliott, S. J., Sperandio, V., Girón, J. A., Shin, S., Mellies, J. L., Wainwright, L., Hutcheson, S. W., McDaniel, T. K., and Kaper, J. B. (2000) The locus of enterocyte effacement (LEE)-encoded regulator controls expression of both LEE- and non-LEE-encoded virulence factors in enteropathogenic and enterohemorrhagic Escherichia coli. Infect. Immun. 68, 6115-6126
25. Yerushalmi, G., Nadler, C., Berdichevski, T., and Rosenshine, I. (2008) Mutational analysis of the locus of enterocyte effacement-encoded regulator (Ler) of enteropathogenic Escherichia coli. J. Bacteriol. 190, 7808-7818
26. Umanski, T., Rosenshine, I., and Friedberg, D. (2002) Thermoregulated expression of virulence genes in enteropathogenic Escherichia coli. Microbiology 148, 2735-2744
27. Wang, H., Bash, R., Yodh, J. G., Hager, G. L., Lohr, D., and Lindsay, S. M. (2002) Glutaraldehyde modified mica: a new surface for atomic force microscopy of chromatin. Biophys. J. 83, 3619-3625
28. Fu, H., Freedman, B. S., Lim, C. T., Heald, R., and Yan, J. (2011) Atomic force microscope imaging of chromatin assembled in Xenopus laevis egg extract. Chromosoma 120, 245-254
29. García, J., Cordeiro, T. N., Prieto, M. J., and Pons, M. (2012) Oligomerization and DNA binding of Ler, a master regulator of pathogenicity of enterohemorrhagic and enteropathogenic Escherichia coli. Nucleic Acids Res. 40, 10254-10262
30. Toro, E., and Shapiro, L. (2010) Bacterial chromosome organization and segregation. Cold Spring Harbor Perspect. Biol. 2, a000349
31. Wang, M. D., Schnitzer, M. J., Yin, H., Landick, R., Gelles, J., and Block, S. M. (1998) Force and velocity measured for single molecules of RNA polymerase. Science 282, 902-907
32. Yan, J., and Marko, J. (2003) Effects of DNA-distorting proteins on DNA elastic response. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 68, 011905
33. Bustamante, C., Marko, J. F., Siggia, E. D., and Smith, S. (1994) Entropic elasticity of λ-phage DNA. Science 265, 1599-1600
34. Marko, J., and Siggia, E. (1995) Stretching DNA. Macromolecules 28, 8759-8770
35. Smith, S. B., Finzi, L., and Bustamante, C. (1992) Direct mechanical measurements of the elasticity of single DNA molecules by using magnetic beads. Science 258, 1122-1126
36. Hill, A. V. (1910) The possible effects of the aggregation of the molecules of hæmoglobin on its dissociation curves. J. Physiol. 40, iv-vii
37. Steinmann, R., and Dersch, P. (2013) Thermosensing to adjust bacterial virulence in a fluctuating environment. Future Microbiol. 8, 85-105
38. Christian, J. H., and Waltho, J. A. (1961) The sodium and potassium content of non-halophilic bacteria in relation to salt tolerance. J. Gen. Microbiol. 25, 97-102
39. Lusk, J. E., Williams, R. J., and Kennedy, E. P. (1968) Magnesium and the growth of Escherichia coli. J. Biol. Chem. 243, 2618-2624
40. Martin-Orozco, N., Touret, N., Zaharik, M. L., Park, E., Kopelman, R., Miller, S., Finlay, B. B., Gros, P., and Grinstein, S. (2006) Visualization of vacuolar acidification-induced transcription of genes of pathogens inside macrophages. Mol. Biol. Cell 17, 498-510
41. Holbrook, J. A., Tsodikov, O. V., Saecker, R. M., and Record, M. T. (2001) Specific and non-specific interactions of integration host factor with DNA: thermodynamic evidence for disruption of multiple IHF surface salt-bridges coupled to DNA binding. J. Mol. Biol. 310, 379-401
42. Lin, J., Chen, H., Dröge, P., and Yan, J. (2012) Physical organization of DNA by multiple non-specific DNA-binding modes of integration host factor (IHF). PLoS One 7, e49885
43. Fu, H., Le, S., Chen, H., Muniyappa, K., and Yan, J. (2013) Force and ATP hydrolysis dependent regulation of RecA nucleoprotein filament by single-stranded DNA binding protein. Nucleic Acids Res. 41, 924-932
44. Record, M. T., Jr., Lohman, M. L., and De Haseth, P. (1976) Ion effects on ligand-nucleic acid interactions. J. Mol. Biol. 107, 145-158
45. Stoebel, D. M., Free, A., and Dorman, C. J. (2008) Anti-silencing: overcoming H-NS-mediated repression of transcription in Gram-negative enteric bacteria. Microbiology 154, 2533-2545