Nucleoprotein filament formation is the structural basis for bacterial protein H-NS gene silencing

Scientific Reports

Volumn 2, Issue , 2012, Pages

  Lim, Ci Ji ^a,b,c   Lee, Sin Yi ^b,d   Kenney, Linda J ^b,d,e   Yan, Jie ^a,b,c,d  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^d NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^e UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; BACTERIAL PROTEIN; DNA BINDING PROTEIN; H NS PROTEIN, BACTERIA; H-NS PROTEIN, BACTERIA; NUCLEOPROTEIN;

ARTICLE; ATOMIC FORCE MICROSCOPY; BIOLOGICAL MODEL; CHEMISTRY; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; MACROMOLECULE; METABOLISM; MUTATION; ULTRASTRUCTURE;

BACTERIAL PROTEINS; DNA, BACTERIAL; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; GENE SILENCING; MACROMOLECULAR SUBSTANCES; MICROSCOPY, ATOMIC FORCE; MODELS, BIOLOGICAL; MUTATION; NUCLEOPROTEINS;

EID: 84864150307     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep00509     Document Type: Article

References (35)

1. Azam, T. A., Iwata, A., Nishimura, A., Ueda, S. & Ishihama, A. Growth phasedependent variation in protein composition of the Escherichia coli nucleoid. Journal of Bacteriology 181, 6361-6370 (1999). (Pubitemid 29512946)
2. Azam, T. A., Hiraga, S. & Ishihama, A. Two types of localization of the DNAbinding proteins within the Escherichia coli nucleoid. Genes to Cells 5, 613-626 (2000). (Pubitemid 30641954)
3. Browning, D. F., Grainger, D. C. & Busby, S. J. Effects of nucleoid-associated proteins on bacterial chromosome structure and gene expression. Curr Opin Microbiol 13, 773-80 (2010).
4. Dorman, C. J. H-NS, the genome sentinel. Nat Rev Microbiol 5, 157-61 (2007). (Pubitemid 46151874)
5. McGovern, V., Higgins, N. P., Chiz, R. S. & Jaworski, A. H-NS over-expression induces an artificial stationary phase by silencing global transcription. Biochimie 76, 1019-29 (1994).
6. Hommais, F. et al. Large-scale monitoring of pleiotropic regulation of gene expression by the prokaryotic nucleoid-associated protein, H-NS. Molecular Microbiology 40, 20-36 (2001). (Pubitemid 32322859)
7. Lucchini, S. et al. H-NS mediates the silencing of laterally acquired genes in bacteria. PLoS Pathog 2, e81 (2006).
8. Niki, H., Yamaichi, Y. & Hiraga, S. Dynamic organization of chromosomal DNA in Escherichia coli. Genes Dev 14, 212-23 (2000). (Pubitemid 30070986)
9. Tupper, A. E. et al. The chromatin-associated protein H-NS alters DNA topology in vitro. Embo Journal 13, 258-68 (1994).
10. Hulton, C. S. et al. Histone-like protein H1 (H-NS), DNA supercoiling, and gene expression in bacteria. Cell 63, 631-42 (1990).
11. Ueguchi, C. & Mizuno, T. The Escherichia coli nucleoid protein H-NS functions directly as a transcriptional repressor. Embo Journal 12, 1039-46 (1993). (Pubitemid 23095853)
12. Amit, R.,Oppenheim, A. B. & Stavans, J. Increased bending rigidity of single DNA molecules by H-NS, a temperature and osmolarity sensor. Biophys J 84, 2467-73 (2003). (Pubitemid 36373568)
13. Dame, R. T., Wyman, C. & Goosen, N. H-NS mediated compaction of DNA visualised by atomic force microscopy. Nucleic Acids Research 28, 3504-10 (2000).
14. Dame, R. T., Noom,M. C. & Wuite, G. J. Bacterial chromatin organization by HNS protein unravelled using dualDNA manipulation. Nature 444, 387-90 (2006). (Pubitemid 44764116)
15. Liu, Y., Chen, H., Kenney, L. J. & Yan, J. A divalent switch drives H-NS/DNAbinding conformations between stiffening and bridging modes. Genes Dev 24, 339-44 (2010).
16. Atlung, T. & Ingmer, H. H-NS: a modulator of environmentally regulated gene expression. Molecular Microbiology 24, 7-17 (1997). (Pubitemid 27160834)
17. Ono, S. et al.H-NS is a part of a thermally controlled mechanism for bacterial gene regulation. Biochemical Journal 391, 203-13 (2005). (Pubitemid 41532416)
18. Walthers, D. et al. Salmonella enterica Response Regulator SsrB Relieves H-NS Silencing by Displacing H-NS Bound in Polymerization Mode and Directly Activates Transcription. Journal of Biological Chemistry 286, 1895-1902 (2011).
19. Lim, C. J., Whang, Y. R., Kenney, L. J. & Yan, J. Gene silencing H-NS paralogue StpA forms a rigid protein filament along DNA that blocks DNA accessibility. Nucleic Acids Research 40, 3316-3328 (2011).
20. Ueguchi, C., Suzuki, T., Yoshida, T., Tanaka, K. & Mizuno, T. Systematic mutational analysis revealing the functional domain organization of Escherichia coli nucleoid protein H-NS. Journal of Molecular Biology 263, 149-62 (1996). (Pubitemid 26363079)
21. Ueguchi, C., Seto, C., Suzuki, T. & Mizuno, T. Clarification of the dimerization domain and its functional significance for the Escherichia coli nucleoid protein HNS. Journal of Molecular Biology 274, 145-51 (1997). (Pubitemid 27520601)
22. Spurio, R., Falconi, M., Brandi, A., Pon, C. L. & Gualerzi, C. O. The oligomeric structure of nucleoid protein H-NS is necessary for recognition of intrinsically curved DNA and for DNA bending. Embo Journal 16, 1795-805 (1997). (Pubitemid 27151972)
23. Williams, R. M., Rimsky, S. & Buc, H. Probing the structure, function, and interactions of the Escherichia coli H-NS and StpA proteins by using dominant negative derivatives. Journal of Bacteriology 178, 4335-4343 (1996). (Pubitemid 26262218)
24. Yan, J. & Marko, J. F. Effects of DNA-distorting proteins on DNAelastic response. Phys Rev E Stat Nonlin Soft Matter Phys 68, 011905 (2003).
25. Yan, J., Skoko, D. & Marko, J. F. Near-field-magnetic-tweezer manipulation of singleDNAmolecules. Phys Rev E Stat Nonlin Soft Matter Phys 70, 011905 (2004).
26. Marko, J. F. & Siggia, E. D. Stretching DNA. Macromolecules 28, 8759-8770 (1995).
27. Wiggins, P. A., Dame, R. T., Noom, M. C. & Wuite, G. J. L. Protein-Mediated Molecular Bridging: A Key Mechanism in Biopolymer Organization. Biophysical Journal 97, 1997-2003 (2009).
28. Arold S. T., Leonard, P. G., Parkinson, G. N. & Ladbury, J. E. H-NS forms a superhelical protein scaffold forDNAcondensation. Proc Natl Acad SciUS A107, 15728-32 2010
29. Bouffartigues, E., Buckle, M., Badaut, C., Travers, A. & Rimsky, S. H-NS cooperative binding to high-affinity sites in a regulatory element results in transcriptional silencing. Nat Struct Mol Biol 14, 441-8 (2007). (Pubitemid 46685883)
30. Lang, B. et al.High-affinity DNA binding sites for H-NS provide a molecular basis for selective silencing within proteobacterial genomes. Nucleic Acids Research 35, 6330-7 (2007). (Pubitemid 350018593)
31. Rimsky, S., Zuber, F., Buckle, M. & Buc, H. A molecular mechanism for the repression of transcription by the H-NS protein. Molecular Microbiology 42, 1311-1323 (2001). (Pubitemid 34209091)
32. Chen, C. C., Chou, M. Y., Huang, C. H., Majumder, A. & Wu, H. Y. A cisspreading nucleoprotein filament is responsible for the gene silencing activity found in the promoter relay mechanism. Journal of Biological Chemistry 280, 5101-5112 (2005). (Pubitemid 40288686)
33. Castang, S., McManus, H. R., Turner, K. H. & Dove, S. L. H-NS family members function coordinately in an opportunistic pathogen. Proc Natl Acad Sci U S A 105, 18947-52 (2008).
34. Gordon, B. R., Imperial, R., Wang, L., Navarre, W. W. & Liu, J. Lsr2 of Mycobacterium represents a novel class of H-NS-like proteins. Journal of Bacteriology 190, 7052-9 (2008).
35. Wang, H. D. et al. Glutaraldehyde modified mica: A new surface for atomic force microscopy of chromatin. Biophysical Journal 83, 3619-3625 (2002).