H-NS: A universal regulator for a dynamic genome

Nature Reviews Microbiology

Volumn 2, Issue 5, 2004, Pages 391-400

  Dorman, Charles J ^a  

^a TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

CURVED DNA; HISTONE LIKE NUCLEOID STRUCTURING PROTEIN; BACTERIAL PROTEIN; CHAPERONE; DNA BINDING PROTEIN; ESCHERICHIA COLI PROTEIN; FACTOR FOR INVERSION STIMULATION; H NS PROTEIN, BACTERIA; H-NS PROTEIN, BACTERIA; REPRESSOR PROTEIN; STPA PROTEIN, E COLI;

BACTERIAL GENOME; ESCHERICHIA COLI; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENETIC CODE; GENETIC REGULATION; HAEMOPHILUS INFLUENZAE; HORIZONTAL GENE TRANSFER; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW; SALMONELLA; SHIGELLA FLEXNERI; THERMOSTABILITY; TRANSCRIPTION REGULATION; GENE EXPRESSION REGULATION; GENETICS; PHYSIOLOGY;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; HAEMOPHILUS; HAEMOPHILUS INFLUENZAE; SALMONELLA; SHIGELLA; SHIGELLA FLEXNERI;

BACTERIAL PROTEINS; DNA-BINDING PROTEINS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; FACTOR FOR INVERSION STIMULATION PROTEIN; GENE EXPRESSION REGULATION, BACTERIAL; GENOME, BACTERIAL; MOLECULAR CHAPERONES; REPRESSOR PROTEINS;

EID: 2442560235     PISSN: 17401526     EISSN: None     Source Type: Journal    
DOI: 10.1038/nrmicro883     Document Type: Review

References (110)

1. Ali Azam, T. & Ishihama, A. Twelve species of the nucleoid-associated protein from Escherichia coli: sequence recognition specificity and DNA binding affinity. J. Biol. Chem. 274, 33105-33113 (1999).
2. Ali Azam, T., Iwata, A., Nishimura, A., Ueda, S. & Ishihama, A. Growth phase-dependent variation in protein composition of the Escherichia coli nucleoid. J. Bacteriol. 181, 6361-6370 (1999).
3. Brunetti, R., Prosseda, G., Beghetto, E., Colonna, B. & Micheli, G. The looped domain organization of the nucleoid in histone-like protein defective Escherichia coli strains. Biochimie 83, 873-882 (2001).
4. Pedersen, A. G., Jensen, L. J., Brunak, S., Staerfeldt, H. H. & Ussery, D. W. A DNA structural atlas for Escherichia coli. J. Mol. Biol. 299, 907-930 (2000).
5. Dorman, C. J. & Deighan, P. Regulation of gene expression by histone-like proteins in bacteria. Curr. Opin. Genet. Dev. 13 179-184 (2003).
6. Dersch, P., Schmidt, K. & Bremer, E. Synthesis of the Escherichia coli K-12 nucleoid-associated DNA-binding protein H-NS is subjected to growth-phase control and autoregulation. Mol. Microbiol. 8, 875-889 (1993).
7. Falconi, M., Brandi, A., La Teana, A., Gualerzi, C. O. & Pon, C. L. Antagonistic involvement of Fis and H-NS proteins in the transcriptional control of hns expression. Mol. Microbiol. 19, 965-975 (1996).
8. Free, A. & Dorman, C. J. Coupling of Escherichia coli hns mRNA levels to DNA synthesis by autoregulation: implications for growth phase control. Mol. Microbiol. 18, 101-113 (1995).
9. Hinton, J. C. D. et al. Expression and mutational analysis of the nucleoid-associated protein H-NS of Salmonella typhimurium. Mol. Microbiol. 6, 2327-2337 (1992).
10. Ueguchi, C., Kakeda, M. & Mizuno, T. Autoregulatory expression of the Escherichia coli hns gene encoding a nucleoid protein: H-NS functions as a repressor of its own transcription. Mol. Gen. Genet. 236, 171-178 (1993).
11. Sondén, B. & Uhlin, B. E. Coordinated and differential expression of histone-like proteins in Escherichia coli: regulation and function of the H-NS analog StpA. EMBO J. 15, 4970-4980 (1996).
12. Free, A. & Dorman, C. J. The Escherichia coli stpA gene is transiently expressed during growth in rich medium and is induced in minimal medium and by stress conditions. J. Bacteriol. 179, 909-918 (1997).
13. Deighan, P., Beloin, C. & Dorman, C. J. Three-way interactions among the Sfh, StpA and H-NS nucleoid-associated proteins of Shigella flexneri 2a strain 2457T. Mol. Microbiol. 48, 1401-1416 (2003).
14. Falconi, M., Higgins, N. P., Spurio, R., Pon, C. L. & Gualerzi, C. O. Expression of the gene encoding the major bacterial nucleoid protein H-NS is subject to transcriptional auto-repression. Mol. Microbiol. 10, 273-282 (1993).
15. Zhang, A., Rimsky, S., Reaban, M. E., Buc, H. & Belfort, M. Escherichia coli protein analogs StpA and H-NS: regulatory loops, similar and disparate effects on nucleic acid dynamics. EMBO J. 15, 1340-1349 (1996).
16. Dorman, C. J., Hinton, J. C. D. & Free, A. Domain organization and oligomerization among H-NS-like nucleoid-associated proteins in bacteria. Trends Microbiol. 7, 124-128 (1999).
17. Schröder, O. & Wagner, R. The bacterial regulatory protein H-NS - a versatile modulator of nucleic acid structures. Biol. Chem. 383, 945-960 (2002).
18. Tendeng, C. & Bertin, P. H-NS in Gram-negative bacteria: a family of multifaceted proteins. Trends Microbiol. 11, 511-518 (2003).
19. Tupper, A. E. et al. The chromatin associated protein H-NS alters DNA topology in vitro. EMBO J. 13, 258-268 (1994).
20. Sonnenfield, J. M., Burns, C. M., Higgins, C. F. & Hinton, J. C. D. The nucleoid-associated protein StpA binds curved DNA, has a greater DNA-binding affinity than H-NS and is present in significant levels in hns mutants. Biochimie 83, 1-7 (2001).
21. Deighan, P., Free, A. & Dorman, C. J. A role for the Escherichia coli H-NS-like protein StpA in OmpF porin expression through modulation of micF RNA stability. Mol. Microbiol. 38, 126-139 (2000).
22. Zhang, A., Derbyshire, V., Salvo, J. L. & Belfort, M. Escherichia coli protein StpA stimulates self-splicing by promoting RNA assembly in vitro. RNA 1, 783-793 (1995).
23. Hommais, F. et al. Large-scale monitoring of pleiotropic regulation of gene expression by the prokaryotic nucleoid-associated protein, H-NS. Mol. Microbiol. 40, 20-36 (2001).
24. Kawula, T. H. & Orndorff, P. E. Rapid site-specific DNA inversion in Escherichia coli mutants lacking the histonelike protein H-NS. J. Bacteriol. 173, 4116-4123 (1991).
25. O'Gara, J. P. & Dorman, C. J. Effects of local transcription and H-NS on inversion of the fim switch of Escherichia coli. Mol. Microbiol. 36, 457-466 (2000).
26. Starcic-Erjavec, M. et al. H-NS and Lrp serve as positive modulators of traJ expression from the Escherichia coli plasmid pRK100. Mol. Gen. Genomics 270, 94-102 (2003).
27. Nasser, W. & Reverchon, S. H-NS-dependent activation of pectate lyases synthesis in the phytopathogenic bacterium Erwinia chrysanthemi is mediated by the PeCT repressor. Mol. Microbiol. 43, 733-748 (2002).
28. Bertin, P. et al. The H-NS protein is involved in the biogenesis of flagella in Escherichia coli. J. Bacteriol. 176 5537-5540 (1994).
29. Ko, M. & Park, C. H-NS-dependent regulation of flagellar synthesis is mediated by a LysR-like family protein. J. Bacteriol. 182, 4670-4672 (2000).
30. Soutourina, O. et al. Multiple control of flagellum biosynthesis in Escherichia coli: role of H-NS protein and the cyclic AMP-catabolite activator protein complex in transcription of the fihDC master operon. J. Bacteriol. 181, 7500-7508 (1999).
31. Donato, G. M. & Kawula, T. H. Enhanced binding of altered H-NS protein to flagellar rotor protein FliG causes increased flagellar rotational speed and hypermotility in Escherichia coli. J. Biol. Chem. 273, 24030-24036 (1998).
32. Yamada, H., Muramatsu, S. & Mizuno, T. An Escherichia coli protein that preferentially binds to sharply curved DNA. J. Biochem. 108, 420-425 (1990).
33. Yamada, H., Yoshida, T., Tanaka, K., Sasakawa, C. & Mizuno, T. 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 (1991).
34. Bracco, L., Kotlarz, D., Kolb, A., Diekmann, S. & Buc, H. Synthetic curved DNA sequences can act as transcriptional activators in Escherichia coli. EMBO J. 8, 4289-4296 (1989).
35. Jauregui, R., Abreu-Goodger, C., Moreno-Hagelsieb, G., Collado-Vides, J. & Merino, E. Conservation of DNA curvature signals in regulatory regions of prokaryotic genes. Nucleic Acids Res. 31 6770-6777 (2003).
36. Barbic, A., Zimmer, D. P. & Crothers, D. M. Structural origins of adenine-tract bending. Proc. Natl Acad. Sci. USA 100 2369-2373 (2003).
37. La Teana, A. et al. Identification of a cold shock transcriptional enhancer of the Escherichia coli gene encoding nucleoid protein H-NS. Proc. Natl Acad. Sci. USA 88, 10907-10911 (1991).
38. Lease, R. A. & Belfort, M. Riboregulation by DsrA RNA: trans-actions for global economy. Mol. Microbiol. 38, 667-672 (2000).
39. Brescia, C. C., Mikulecky, P. J., Feig, A. L. & Sledjeski, D. D. Identification of the Hfq-binding site on DsrA RNA: Hfq binds without altering DsrA secondary structure. RNA 9, 33-43 (2003).
40. Welch, T. J., Farewell, A., Neidhardt, F. C. & Bartlett, D. H. Stress response of Escherichia coli to elevated hydrostatic pressure. J. Bacteriol. 175, 7170-7177 (1993).
41. Johansson, J. & Uhlin, B. E. Differential protease-mediated turnover of H-NS and StpA revealed by a mutation altering protein stability and stationary phase survival of Escherichia coli. Proc. Natl Acad. Sci. USA 96, 10776-10781 (1999).
42. Reusch, R. N. et al. Posttranslational modification of E. coli histone-like protein H-NS and bovine histones by short-chain poly-(R)-3-hydroxybutyrate (cPHB). FEBS Lett. 527 319-322 (2002).
43. Schneider, D. A., Ross, W. & Gourse, R. L. Control of rRNA expression in Escherichia coli. Curr. Opin. Microbiol. 6, 151-156 (2003).
44. Dame, R. T., Wyman, C., Wurm, R., Wagner, R. & Goosen, N. 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 (2002).
45. Beloin, C. & Dorman, C. J. An extended role for the nucleoid structuring protein H-NS in the virulence gene regulatory cascade of Shigella flexneri. Mol. Microbiol. 47, 825-838 (2003).
46. Caramel, A. & Schnetz, K. Lac and lambda repressors relieve silencing of the Escherichia coli bgl promoter. Activation by alteration of a repressing nucleoprotein complex. J. Mol. Biol. 284, 875-883 (1998).
47. Falconi, M., Prosseda, G., Giangrossi, M., Beghetto, E. & Colonna, B. Involvement of Fis in the H-NS-mediated regulation of virF gene of Shigella and enteroinvasive Escherichia coli. Mol. Microbiol. 42, 439-452 (2001).
48. Haack, K. R., Robinson, C. L., Miller, K. J., Fowlkes, J. W. & Mellies, J. L. Interaction of Ler at the LEE5 (tir) operon of enteropathogenic Escherichia coli. Infect. Immun. 71, 384-392 (2003).
49. Jordi, B. J. A. M. et al. The positive regulator CfaD overcomes the repression mediated by the histone-like protein H-NS (H1) in the CFA/I fimbrial operon of Escherichia coli. EMBO J. 11, 2627-2632 (1992).
50. Tobe, T., Yoshikawa, M., Mizuno, T. & Sasakawa, C. Transcriptional control of the invasion regulatory gene virB of Shigella flexneri: activation by VirF and repression by H-NS. J. Bacteriol. 175, 6142-6149 (1993).
51. Westermark, M., Oscarsson, J., Mizunoe, Y., Urbonaviciene, J. & Uhlin, B. E. Sending and activation of ClyA cytotoxin expression in Escherichia coli. J. Bacteriol. 182, 6347-6357 (2000).
52. Yu, R. R. & DiRita, V. Regulation of gene expression in Vibrio cholerae by ToxT involves both antirepression and RNA polymerase stimulation. Mol. Microbiol. 43, 119-134 (2002).
53. Schnetz, K. & Wang, J. C. Silencing of the Escherichia coli bgl promoter: effects of template supercoiling and cell extracts on promoter activity in vitro. Nucleic Acids Res. 24, 2422-2428 (1996).
54. Mukerji, M. & Mahadevan, S. Characterization of the negative elements involved in silencing the bgl operon of Escherichia coli: possible roles for DNA gyrase, H-NS, and CRP-cAMP in regulation. Mol. Microbiol. 24, 617-627 (1997).
55. 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, 2467-2473 (2003).
56. Badaut, C. et al. The degree of oligomerization of the H-NS nucleoid structuring protein is related to specific binding to DNA. J. Biol. Chem. 277, 41657-41666 (2002).
57. s-dependent genes in Escherichia coli. J. Bacteriol. 177, 3455-3464 (1995).
58. Fletcher, S.A. & Csonka, L. N. Fine-structure deletion analysis of the transcriptional silencer of the proU operon of Salmonella typhimurium. J. Bacteriol. 177, 4508-4513 (1995 ).
59. Nieto, J. M. et al. Expression of the haemolysin operon in Escherichia coli is modulated by a nucleoid-protein complex that includes the proteins Hha and H-NS. Mol. Gen. Genet. 263, 349-358 (2000).
60. Nieto, J. M. et al. Evidence for direct protein-protein interaction between members of the Enterobacterial Hha/YmoA and H-NS families of proteins. J. Bacteriol. 184, 629-635 (2002).
61. Porter, M. E. & Dorman, C. J. A role for H-NS in the thermo-osmotic regulation of virulence-gene expression in Shigela flexneri. J. Bacteriol. 176, 4187-4191 (1994).
62. 70-directed transcription in vitro from osmotically regulated P1 and P2 promoters of proU in Escherichia coli. J. Bacteriol. 178, 4176-4181 (1996).
63. Gowrishankar, J. & Manna, D. How is osmotic regulation of transcription of the Escherichia coli proU operon achieved? A review and a model. Genetica 97, 363-378.
64. Falconi, M., Colonna, B., Prosseda, G., Micheli, G. & Gualerzi, C. O. 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 (1998).
65. Rohde, J. R., Luan, X. S., Rohde, H., Fox, J. M. & Minnich, S. A. The Yersinia enterocolitica pYV virulence plasmid contains multiple intrinsic DNA bends which melt at 37°C. J. Bacteriol. 181, 4198-4204 (1999).
66. Ussery, D. W., Higgins, C. F. & Bolshoy, A. Environmental influences on DNA curvature. J. Biomol. Struct. Dyn. 16, 811-823 (1999).
67. Sinden R. R., Pearson, C. E., Potaman, V. N. & Ussery, D. W. DNNA: structure and function. Adv. Gen. Biol. 5A, 1-141 (1998).
68. Ceschini, S. et al. Multimeric self-assembly equilibria involving the histone-like protein H-NS. A thermodynamic study. J. Biol. Chem. 275, 729-734 (2000).
69. Bloch, V. et al. The H-NS dimerization domain defines a new fold contributing to DNA recognition. Nature Struct. Biol. 10, 212-218 (2003).
70. Esposito, D. et al. H-NS oligomerization domain structure reveals the mechanism for high order self-association of the intact protein. J. Mol. Biol. 324, 841-850 (2002).
71. Cusick, M. E. & Belfort, M. E. Domain structure and RNA annealing activity of the Escherichia coli regulatory protein StpA. Mol. Microbiol. 28, 847-857 (1998).
72. Ueguchi, C., Seto, C., Suzuki, T. & Mizuno, T. Clarification of the dimerization domain and its functional significance for the Escherichia coli nucleoid protein H-NS. J. Mol. Biol. 274, 145-151 (1997).
73. 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. J. Mol. Biol. 263, 149-162 (1996).
74. Shindo, H. et al. Solution structure of the DNA binding domain of a nucleoid-associated protein, H-NS, from Escherichia coli. FEBS Lett. 360, 125-131 (1995).
75. Shindo, H. et al. Identification of the DNA binding surface of H-NS protein from Escherichia coli by heteronuclear NMR spectroscopy. FEBS Lett. 455, 63-69 (1999).
76. Smyth, C. P. et al. Oligomerization of the chromatin-structuring protein HNS. Mol. Microbiol. 36, 962-972 (2000).
77. Tippner, D. & Wagner, R. Fluorescence analysis of the Escherichia coli transcription regulator H-NS reveals two distinguishable complexes dependent on binding to specific or non-specific DNA sites. J. Biol. Chem. 270, 22243-22247 (1995).
78. 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 J. 16, 1795-1805 (1995).
79. Dame, R. T., Wyman, C. & Goosen, N. H-NS mediated compaction of DNA visualized by atomic force microscopy. Nucleic Acids Res. 28, 3504-3510 (2000).
80. Spurio, R. et al. Lethal overproduction of the Escherichia coli nucleoid protein H-NS: ultramicroscopic and molecular autopsy. Mol. Gen. Genet. 231, 201-211 (1992).
81. Rimsky, S., Zuber, F., Buckle, M. & Buc, H. A molecular mechanism for the repression of transcription by the H-NS protein. Mol. Microbiol. 42, 1311-1323 (2001).
82. Dame, R. T. & Goosen, N. HU: promoting or counteracting DNA compaction? FEBS Lett. 529, 151-156 (2002).
83. Free, A., Williams, R. M. & Dorman, C. J. The StpA protein functions as a molecular adapter to mediate repression of the bgl operon by truncated H-NS in Escherichia coli. J. Bacteriol. 180 994-997 (1998).
84. Free, A., Porter, M. E., Deighan, P. & Dorman, C. J. Requirement for the molecular adapter function of StpA at the Escherichia coli bgl promoter depends upon the level of truncated H-NS protein. Mol. Microbiol. 42, 903-918 (2001).
85. Johansson, J., Eriksson, S., Sondén, B., Wai, S. N. & Uhlin, B. E. Heteromeric interactions among nucleoid-associated bacterial proteins: localization of StpA-stabilizing regions in H-NS of Escherichia coli. J. Bacteriol. 183, 2343-2347 (2001).
86. Williams, R. M., Rimsky S. & Buc, H. Probing the structure, function, and interactions of the Escherichia coli H-NS and StpA proteins using dominant negative derivatives. J. Bacteriol. 178 4335-4343 (1996).
87. Claret, L. & Rouvière-Yaniv, J. Variation in HU composition during growth of Escherichia coli: the heterodimer is required for long term survival. J. Mol. Biol. 273, 93-104 (1997).
88. Claret, L. & Rouvière-Yaniv, J. Regulation of HU α and HU β by CRP and FIS in Escherichia coli. J. Mol. Biol. 263, 126-139 (1996).
89. Tanaka, H. et al. Role of HU proteins in forming and constraining supercoils of chromosomal DNA in Escherichia coli. Mol. Gen. Genet. 248, 518-526 (1995).
90. Oberto, J. & Rouvière-Yaniv, J. Serratia marcescens contains a heterodimeric HU protein like Escherichia coli and Salmonella typhimurium. J Bacteriol. 178, 293-297 (1996).
91. Cases, I. & de Lorenzo, V. The genomes of Pseudomonas encode a third HU protein. Microbiol. 148, 1243-1245 (2002 ).
92. Fleischmann, R. D. et al. Whole-genome random sequencing of Haemophilus influenzae Rd. Science 269, 496-512 (1995).
93. B. Nucleic Acids Res. 19, 1063-1066 (1991).
94. B RNA replication, is essential for rpoS translation in Escherichia coli. Genes Dev. 10, 1143-1151 (1996).
95. Nogueira, T. & Springer, M. Post-transcriptional control by global regulators of gene expression in bacteria. Curr. Opin. Microbiol. 3, 154-158 (2000).
96. Nieto, J. M. et al. The hha gene modulates haemolysin expression in Escherichia coli. Mol. Microbiol. 5, 1285-1293 (1991).
97. Robertson, C. A. & Nash, H. A. Bending of the bacteriophage λ attachment site by Escherichia coli integration host factor. J. Biol. Chem. 263, 3554-3557 (1988).
98. Ball, C. A. & Johnson, R. C. Multiple effects of Fis on integration and the control of lysogeny in phage λ. J. Bacteriol. 173, 4032-4038 (1991).
99. Liu, Q. & Richardson, C. C. Gene 5. 5 protein of bacteriophage T7 inhibits the nucleoid protein H-NS of Escherichia coli. Proc. Natl Acad. Sci. USA 90, 1761-1765 (1993).
100. Buchrieser, C. et al. The virulence plasmid pWR 100 and the repertoire of proteins secreted by the type III secretion apparatus of Shigella flexneri. Mol. Microbiol. 38, 760-771 (2000).
101. Wilson, R. L. et al. Fis, a DNA nucleoid-associated protein, is involved in Salmonella typhimurium SPI-1 invasion gene expression. Mol. Microbiol. 39, 79-88 (2001).
102. Schechter, L. M., Jain, S., Akbar, S. & Lee, C. A. The small nucleoid-binding proteins H-NS, HU, and Fis affect hilA expression in Salmonella enterica serovar Typhimurium. Infect. Immun. 71, 5432-5435 (2003).
103. Nye, M. B. & Taylor, R. K. Vibrio cholerae H-NS domain structure and function with respect to transcriptional repression of ToxR regulon genes reveals differences among H-NS family members. Mol. Microbiol. 50, 427-444 (2003).
104. Cerdan, R. et al. Crystal structure of the N-terminal dimerization domain of VicH, the H-NS-like protein of Vibrio cholerae. J. Mol. Biol. 334, 179-185 (2003).
105. Bustamante, V. H., Santana, F. J., Calve, E. & Puente, J. L. Transcriptional regulation of type III secretion genes in enteropathogenic Escherichia coli: Ler antagonizes H-NS-dependent repression. Mol. Microbiol. 39, 664-678 (2001).
106. Beloin, C., Deighan, P., Doyle, M. & Dorman, C. J. Shigella flexneri 2a strain 2457T expresses three members of the H-NS-like protein family: characterization of the Sfh protein. Mol. Gen. Genomics 270, 66-77 (2003).
107. Prosseda, G. et al. The virF promoter in Shigella: more than just a curved DNA stretch. Mol. Microbiol. 51, 523-537 (2004).
108. Afflerbach, H., Schröder, O. & Wagner, R. Conformational changes of the upstream DNA mediated by H-NS and Fis regulate E. coli rrnB promoter activity. J. Mol. Biol. 286, 339-353 (1999).
109. Afflerbach, H., Schröder, O. & Wagner, R. Effects of the Escherichia coli DNA-binding protein H-NS on rRNA synthesis in vivo. Mol. Microbiol. 28, 641-653 (1998).
110. Rimsky, S. Structure of the histone-like protein H-NS and its role in regulation and genome superstructure. Curr. Opin. Microbiol. 7, 1-6 (2004).