Time-resolved assembly of a nucleoprotein complex between Shigella flexneri virF promoter and its transcriptional repressor H-NS

Nucleic Acids Research

Volumn 42, Issue 21, 2014, Pages 13039-13050

  Ulissi, Ulisse ^a,c   Fabbretti, Attilio ^a   Sette, Marco ^b   Giuliodori, Anna Maria ^a   Spurio, Roberto ^a  

^a UNIVERSITY OF CAMERINO   (Italy)

^b UNIVERSITY OF ROME TOR VERGATA   (Italy)

^c UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; BACTERIAL PROTEIN; DNA BINDING PROTEIN; H-NS PROTEIN, BACTERIA; REPRESSOR PROTEIN; VIRULENCE FACTOR;

BINDING SITE; CHEMISTRY; DNA FOOTPRINTING; GENETICS; METABOLISM; PATHOGENICITY; PROMOTER REGION; SHIGELLA FLEXNERI;

BACTERIAL PROTEINS; BINDING SITES; DNA FOOTPRINTING; DNA, BACTERIAL; DNA-BINDING PROTEINS; PROMOTER REGIONS, GENETIC; REPRESSOR PROTEINS; SHIGELLA FLEXNERI; VIRULENCE FACTORS;

EID: 84945207881     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku1052     Document Type: Article

References (45)

1. Spassky, A., Rimsky, S., Garreau, H. And Buc, H. (1984) Hla, an E. coli DNA-binding protein which accumulates in stationary phase, strongly compacts DNA in vitro. Nucleic Acids Res., 12, 5321-5340.
2. Dame, R. T., Wyman, C. And Goosen, N. (2001) Structural basis for preferential binding of H-NS to curved DNA. Biochimie, 83, 231-234.
3. Dorman, C. J. (2004) H-NS: A universal regulator for a dynamic genome. Nat. Rev. Microbiol., 2, 391-400.
4. Pon, C. L., Stella, S. And Gualerzi, C. O. (2005) Repression of transcription by curved DNA and nucleoid protein H-NS: A mode of bacterial gene regulation. In: Ohyama, T (ed). DNA Conformation and Transcription. Landes Bioscience, Georgetown, TX, pp. 52-65.
5. Navarre, W. W. (2010) H-NS as a defence system. In: Dame, RT and Dorman, CJ (eds). Bacterial Chromatin. Springer Science+Business Media, NY, pp. 251-322.
6. Atlung, T. And Ingmer, H. (1997) H-NS: A modulator of environmentally regulated gene expression. Mol. Microbiol., 24, 7-17.
7. Prosseda, G., Falconi, M., Nicoletti, M., Casalino, M., Micheli, G. And Colonna, B. (2002) Histone-like proteins and the Shigella invasivity regulon. Res. Microbiol., 153, 461-468.
8. Goransson, M., Sonden, B., Nilsson, P., Dagberg, B., Forsman, K., Emanuelsson, K. And Uhlin, B. E. (1990) Transcriptional silencing and thermoregulation of gene expression in Escherichia coli. Nature, 344, 682-685.
9. Falconi, M., Higgins, N. P., Spurio, R., Pon, C. L. And Gualerzi, C. O. (1993) Expression of the gene encoding the major bacterial nucleotide protein H-NS is subject to transcriptional auto-repression. Mol. Microbiol., 10, 273-282.
10. Falconi, M., Brandi, A., La Teana, A., Gualerzi, C. O. And Pon, C. L. (1996) Antagonistic involvement of FIS and H-NS proteins in the transcriptional control of hns expression. Mol. Microbiol., 19, 965-975.
11. Dame, R. T., Wyman, C., Wurm, R., Wagner, R. And Goosen, N. (2002) Structural basis for H-NS mediated trapping of RNA polymerase in the open initiation complex at the rrnB P1. J. Biol. Chem., 277, 2146-2150.
12. Schroder, O. And Wagner, R. (2002) The bacterial regulatory protein H-NS-a versatile modulator of nucleic acid structures. Biol. Chem., 383, 945-960.
13. Tobe, T., Yoshikawa, M. And Sasakawa, C. (1995) Thermoregulation of virB transcription in Shigella flexneri by sensing of changes in local DNA superhelicity. J. Bacteriol., 177, 1094-1097.
14. Falconi, M., Colonna, B., Prosseda, G., Micheli, G. And Gualerzi, C. O. (1998) Thermoregulation of Shigella and Escherichia coli EIEC pathogenicity. A temperature-dependent structural transition of DNA modulates accessibility of virF promoter to transcriptional repressor H-NS. EMBO J., 17, 7033-7043.
15. Spurio, R., Durrenberger, M., Falconi, M., La Teana, A., Pon, C. L. And Gualerzi, C. O. (1992) Lethal overproduction of the Escherichia coli nucleoid protein H-NS: ultramicroscopic and molecular autopsy. Mol. Gen. Genet., 23, 201-211.
16. Sette, M., Spurio, R., Trotta, E., Brandizi, C., Brandi, A., Pon, C. L., Barbato, G., Boelens, R. And Gualerzi, C. O. (2009) Sequence-specific recognition of DNA by the C-terminal domain of nucleoidassociated protein H-NS. J. Bio. l Chem., 284, 30453-30462.
17. Falconi, M., Prosseda, G., Giangrossi, M., Beghetto, E. And Colonna, B. (2001) Involvement of FIS in the H-NS-mediated regulation of virF gene of Shigella and enteroinvasive Escherichia coli. Mol. Microbiol., 42, 439-452.
18. Sambrook, J., Fritsch, E. F. And Maniatis, T. (2001) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
19. Shcherbakova, I., Mitra, S., Beer, H. R. And Brenowitz, M. (2006) Fast Fenton footprinting: A laboratory-based method for the time-resolved analysis of DNA, RNA and proteins. Nucleic Acids Res., 34, e48.
20. Fabbretti, A., Milon, P., Giuliodori, A. M., Gualerzi, C. O. And Pon, C. L. (2007) Real-time dynamics of ribosome-ligand interaction by time-resolved chemical probing methods. Methods Enzymol., 430, 45-58.
21. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J. And Bax, A. (1995) NMRPipe: A multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR, 6, 277-293.
22. Lang, B., Blot, N., Bouffartigues, E., Buckle, M., Geertz, M., Gualerzi, C. O., Mavathur, R., Muskhelishvili, G., Pon, C. L., Rimsky, S. et al. (2007) High-affinity DNA binding sites for H-NS provide a molecular basis for selective silencing within proteobacterial genomes. Nucleic Acids Res., 35, 6330-6337.
23. Hu, Z., Frith, M., Niu, T. And Weng, Z. (2003) SeqVISTA: A graphical tool for sequence feature visualization and comparison. BMC Bioinformat., 4, 1-8.
24. Hsieh, M. And Brenowitz, M. (1996) Quantitative kinetics footprinting of protein-DNA association reactions. Methods Enzymol., 274, 478-492.
25. Pogozelski, W. K., McNeese, T. J. And Tullius, T. D. (1995) What species is responsible for strand scission in the reaction of [FeIIEDTA]2-and H2O2 with DNA? J. Am. Chem. Soc., 117, 6428-6433.
26. Haber, F. AndWeiss, J. (1934) The catalytic decomposition of hydrogen peroxide by iron salts. Proc. R. Soc. Lond., 147, 332-351.
27. Latham, J. A. And Chek, T. (1989) Defining the inside and outside of a catalytic RNA molecule. Science, 245, 276-282.
28. Dame, R. T. (2005) The role of nucleoid-associated proteins in the organization and compaction of bacterial chromatin. Mol. Microbiol., 56, 858-870.
29. Bertin, P., Hommais, F., Krin, E., Soutourina, O., Tendeng, C., Derzelle, S. And Danchin, A. (2001) H-NS and H-NS-like proteins in Gram-negative bacteria and their multiple role in the regulation of bacterial metabolism. Biochimie, 83, 235-241.
30. Hommais, F., Krin, E., Laurent-Winter, C., Soutourina, O., Malpertuy, A., Le Caer, J. P., Danchin, A. And Bertin, P. (2001) Large-scale monitoring of pleiotropic regulation of gene expression by the prokaryotic nucleoid-associated protein, H-NS. Mol. Microbiol., 40, 20-36.
31. Castang, S., McManus, H. R., Turner, K. H. And Dove, S. L. (2008) H-NS family members function co-ordinately in an opportunistic pathogen. Proc. Natl. Acad. Sci. U. S. A., 105, 18947-18952.
32. Navarre, W. W., McClelland, M., Libby, S. J. And Fang, F. C. (2007) Silencing of xenogeneic DNA by H-NS-facilitation of lateral gene transfer in bacteria by a defense system that recognizes foreign DNA. Genes Dev., 21, 1456-1471.
33. Bracco, L., Kotlarz, D., Kolb, A., Diekmann, S. And Buc, H. (1989) Synthetic curved DNA sequences can act as transcriptional activators in Escherichia coli. EMBO J., 8, 4289-4296.
34. Yamada, H., Yoshida, T., Tanaka, K., Sasakawa, C. And Mizuno, T. (1991) Molecular analysis of the Escherichia coli hns gene encoding a DNA-binding protein, which preferentially recognizes curved DNA sequences. Mol. Gen. Genet., 230, 332-336.
35. Zuber, F., Kotlarz, D., Rimsky, S. And Buc, H. (1994) Modulated expression of promoters containing upstream curved DNA sequences by the Escherichia coli nucleoid protein H-NS. Mol. Microbiol., 12, 231-240.
36. Spurio, R., Falconi, M., Brandi, A., Pon, C. L. And Gualerzi, C. O. (1997) The oligomeric structure of nucleoid protein H-NS is necessary for recognition of intrinsically curved DNA and for DNA bending. EMBO J., 16, 1795-1805.
37. Rimsky, S. And Spassky, A. (1990) Sequence determinants for H1 binding on Escherichia coli lac and gal promoters. Biochemistry, 29, 3765-3571.
38. Stella, S., Spurio, R., Falconi, M., Pon, C. L. And Gualerzi, C. O. (2005) Nature and mechanism of the in vivo oligomerization of nucleoid protein H-NS. EMBO J., 24, 2896-2905.
39. Bouffartigues, E., Buckle, M., Badaut, C., Travers, A. And Rimsky, S. (2007) H-NS cooperative binding to high-affinity sites in a regulatory element results in transcriptional silencing. Nat. Struct. Mol. Biol., 14, 441-448.
40. Maurelli, A. T. And Sansonetti, P. J. (1988) Identification of a chromosomal gene controlling temperature regulated expression of Shigella virulence. Proc. Natl. Acad. Sci. U. S. A., 85, 2820-2824.
41. Prosseda, G., Falconi, M., Giangrossi, M., Gualerzi, C. O., Micheli, G. And Colonna, B. (2004) The virF promoter in Shigella: more than just a curved DNA stretch. Mol. Microbiol., 51, 523-537.
42. Dorman, C. J. And Porter, M. E. (1998) The Shigella virulence gene regulatory cascade: A paradigm of bacterial gene control mechanisms. Mol. Microbiol., 29, 677-684.
43. Durand, J. M. B., Dagberg, B., Uhlin, B. E. And Bjork, R. (2000) Transfer RNA modification, temperature and DNA superhelicity have a common target in the regulatory network of the virulence of Shigella flexneri: The expression of the virF gene. Mol. Microbiol., 35, 924-935.
44. Gordon, B. R., Li, Y., Cote, A., Weirauch, M. T., Ding, P., Hughes, T. R., Navarre, W. W., Xia, B. And Liu, J. (2011) Structural basis for recognition of AT-rich DNA by unrelated xenogeneic silencing proteins. Proc. Natl. Acad. Sci. U. S. A., 108, 10690-10695.
45. Rohs, R., Jin, X., West, S. M., Joshi, R., Honig, B. And Mann, R. S. (2010) Origins of specificity in protein-DNA recognition. Ann. Rev. Biochem., 79, 233-269.