H-NS-like nucleoid-associated proteins, mobile genetic elements and horizontal gene transfer in bacteria

Plasmid

Volumn 75, Issue , 2014, Pages 1-11

  Dorman, Charles J ^a  

^a TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

H NS; Horizontal gene transfer; IncHI plasmids; Nucleoid associated proteins; StpA; Thermoregulation

Indexed keywords

HISTONE LIKE NUCLEOID STRUCTURING PROTEIN; BACTERIAL PROTEIN; CHAPERONE; NUCLEOID ASSOCIATED PROTEINS; SIGMA FACTOR RPOS; STPA PROTEIN; UNCLASSIFIED DRUG; BACTERIAL DNA;

AMINO ACID SEQUENCE; BACTERIAL GENE; BACTERIAL GENETICS; BACTERIUM CONJUGATION; CHROMOSOME; DNA SEQUENCE; DNA TRANSFER; ESCHERICHIA COLI; GENE EXPRESSION; GENE SILENCING; GENETIC TRAIT; GENETIC TRANSCRIPTION; GENOMIC ISLAND; HORIZONTAL GENE TRANSFER; MOBILE GENETIC ELEMENT; NONHUMAN; PHENOTYPE; PLASMID; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN INTERACTION; REVIEW; SEQUENCE ALIGNMENT; THERMOREGULATION; BINDING SITE; CONSENSUS SEQUENCE; OLIGOMERIZATION; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; BACTERIAL CHROMOSOME; BACTERIUM; GENE EXPRESSION REGULATION; GENETICS; INTERSPERSED REPEAT; MOLECULAR EVOLUTION; MOLECULAR GENETICS;

AMINO ACID SEQUENCE; BACTERIA; BACTERIAL PROTEINS; CHROMOSOMES, BACTERIAL; DNA, BACTERIAL; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION, BACTERIAL; GENE TRANSFER, HORIZONTAL; INTERSPERSED REPETITIVE SEQUENCES; MOLECULAR SEQUENCE DATA; PLASMIDS;

EID: 84904903516     PISSN: 0147619X     EISSN: 10959890     Source Type: Journal    
DOI: 10.1016/j.plasmid.2014.06.004     Document Type: Review

References (150)

1. Abe H., et al. Global regulation by horizontally transferred regulators establishes the pathogenicity of Escherichia coli. DNA Res. 2008, 15:25-38.
2. Ali S.S., et al. Structural insights into the regulation of foreign genes in Salmonella by the Hha/H-NS complex. J. Biol. Chem. 2013, 288:13356-13369.
3. Arold S.T., et al. H-NS forms a superhelical protein scaffold for DNA condensation. Proc. Natl. Acad. Sci. USA 2010, 107:15728-15732.
4. Atlung T., Ingmer H. H-NS: a modulator of environmentally regulated gene expression. Mol. Microbiol. 1997, 24:7-17.
5. Azam T.A., Ishihama A. Twelve species of the nucleoid-associated protein from Escherichia coli. Sequence recognition specificity and DNA binding affinity. J. Biol. Chem. 1999, 274:33105-33113.
6. Aznar S., et al. The Hha protein facilitates incorporation of horizontally acquired DNA in enteric bacteria. Microbiology 2013, 159:545-554.
7. Bae S.-H., et al. Structure of the nucleoid-associated protein Cnu reveals common binding sites for H-NS in Cnu and Hha. Biochemistry 2008, 47:1993-2001.
8. Bahl M.I., et al. Persistence mechanisms of conjugative plasmids. Methods Mol. Biol. 2009, 532:73-102.
9. Baños R.C., et al. Differential regulation of horizontally acquired and core genome genes by the bacterial modulator H-NS. PLoS Genet. 2009, 5:e1000513.
10. Baños R.C., et al. Differential functional properties of chromosomal- and plasmid-encoded H-NS proteins. Res. Microbiol. 2011, 162:382-385.
11. Battesti A., et al. H-NS regulation of IraD and IraM antiadaptors for control of RpoS degradation. J. Bacteriol. 2012, 194:2470-2478.
12. 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. 2003, 47:825-838.
13. Beloin C., et al. Shigella flexneri 2a strain 2457T expresses three members of the H-NS-like protein family: characterization of the Sfh protein. Mol. Genet. Genomics 2003, 270:66-77.
14. Beltrametti F., et al. Transcriptional regulation of the esp genes of enterohemorrhagic Escherichia coli. J. Bacteriol. 1999, 181:3409-3418.
15. Bingle L.E., et al. Microarray analysis of the Ler regulon in enteropathogenic and enterohaemorrhagic Escherichia coli strains. PLoS One 2014, 9:e80160.
16. Bouffartigues E., et al. H-NS cooperative binding to high-affinity sites in a regulatory element results in transcriptional silencing. Nat. Struct. Mol. Biol. 2007, 14:441-448.
17. Boyd E.F., et al. Mosaic structure of plasmids from natural populations of Escherichia coli. Genetics 1996, 143:1091-1100.
18. Browning D.F., et al. Effects of nucleoid-associated proteins on bacterial chromosome structure and gene expression. Curr. Opin. Microbiol. 2010, 13:773-780.
19. Cameron A.D., Dorman C.J. A fundamental regulatory mechanism operating through OmpR and DNA topology controls expression of Salmonella pathogenicity islands SPI-1 and SPI-2. PLoS Genet. 2012, 8:e1002615.
20. Corbett D., et al. SlyA and H-NS regulate transcription of the Escherichia coli K5 capsule gene cluster, and expression of slyA in Escherichia coli is temperature-dependent, positively autoregulated, and independent of H-NS. J. Biol. Chem. 2007, 282:33326-33335.
21. Cordeiro T.N., et al. Indirect DNA readout by an H-NS related protein: structure of the DNA complex of the C-terminal domain of Ler. PLoS Pathog. 2011, 7:e1002380.
22. Costechareyre D., et al. Cyt toxin expression reveals an inverse regulation of insect and plant virulence factors of Dickeya dadantii. Environ. Microbiol. 2010, 12:3290-3301.
23. Dagberg B., Uhlin B.E. Regulation of virulence-associated plasmid genes in enteroinvasive Escherichia coli. J. Bacteriol. 1992, 174:7606-7612.
24. Dame R.T. The role of nucleoid-associated proteins in the organization and compaction of bacterial chromatin. Mol. Microbiol. 2005, 56:858-870.
25. Dame R.T., et al. Bacterial chromatin organization by H-NS protein unraveled using dual DNA manipulation. Nature 2006, 444:387-390.
26. Deighan P., et al. A role for the Escherichia coli H-NS-like protein StpA in OmpF porin expression through modulation of micF RNA stability. Mol. Microbiol. 2000, 38:126-139.
27. Deighan P., et al. Three-way interactions among the Sfh, StpA and H-NS nucleoid-structuring proteins of Shigella flexneri 2a strain 2457T. Mol. Microbiol. 2003, 48:1401-1416.
28. Dersch P., et al. The nucleoid-associated DNA-binding protein H-NS is required for the efficient adaptation of Escherichia coli K-12 to a cold environment. Mol. Gen. Genet. 1994, 245:255-259.
29. Dillon S.C., Dorman C.J. Bacterial nucleoid-associated proteins, nucleoid structure and gene expression. Nat. Rev. Microbiol. 2010, 8:185-195.
30. Dillon S.C., et al. Genome-wide analysis of the H-NS and Sfh regulatory networks in Salmonella Typhimurium identifies a plasmid-encoded transcription silencing mechanism. Mol. Microbiol. 2010, 76:1250-1265.
31. Dobrindt U., et al. Genome dynamics and its impact on evolution of Escherichia coli. Med. Microbiol. Immunol. 2010, 199:145-154.
32. Doetsch, M., et al., 2011. Transient RNA-protein interactions in RNA folding. FEBS J. 278, 1634-1642.
33. Domingues S., et al. Natural transformation facilitates transfer of transposons, integrons and gene cassettes between bacterial species. PLoS Pathog. 2012, 8:e1002837.
34. Dorman C.J. H-NS: a universal regulator for a dynamic genome. Nat. Rev. Microbiol. 2004, 2:391-400.
35. Dorman C.J. H-NS, the genome sentinel. Nat. Rev. Microbiol. 2007, 5:157-161.
36. Dorman C.J. Regulatory integration of horizontally transferred genes in bacteria. Front. Biosci. 2009, 14:4103-4112.
37. Dorman C.J. Nucleoid-associated proteins and bacterial physiology. Adv. Appl. Microbiol. 2009, 67:47-64.
38. Dorman C.J. Horizontally acquired homologues of the nucleoid-associated protein H-NS: implications for gene regulation. Mol. Microbiol. 2010, 75:264-267.
39. Dorman C.J. Regulation of transcription by DNA supercoiling in Mycoplasma genitalium: global control in the smallest known self-replicating genome. Mol. Microbiol. 2011, 81:302-304.
40. Dorman C.J. Genome architecture and global gene regulation in bacteria: making progress towards a unified model?. Nat. Rev. Microbiol. 2013, 11:349-355.
41. Dorman C.J., Ní Bhriain N. Thermal regulation of fimA, the Escherichia coli gene coding for the type 1 fimbrial subunit protein. FEMS Microbiol. Lett. 1992, 78:125-130.
42. Dorman C.J., et al. DNA supercoiling and environmental regulation of virulence gene expression in Shigella flexneri. Nature 1990, 344:789-792.
43. Dorman C.J., et al. Domain organization and oligomerization among H-NS-like nucleoid-associated proteins in bacteria. Trends Microbiol. 1999, 7:124-128.
44. Doyle M., Dorman C.J. Reciprocal transcriptional and posttranscriptional growth-phase-dependent expression of sfh, a gene that encodes a paralogue of the nucleoid-associated protein H-NS. J. Bacteriol. 2006, 188:7581-7591.
45. Doyle M., et al. An H-NS-like stealth protein aids horizontal DNA transmission in bacteria. Science 2007, 315:251-252.
46. Duong N., et al. Thermosensing coordinates a cis-regulatory module for transcriptional activation of the intracellular virulence system in Salmonella enterica serovar Typhimurium. J. Biol. Chem. 2007, 282:34077-34084.
47. Ebersbach G., Gerdes K. Plasmid segregation mechanisms. Annu. Rev. Genet. 2005, 39:453-479.
48. Falconi M., et al. 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. 1998, 17:7033-7043.
49. Fang F.C., Rimsky S. New insights into transcriptional regulation by H-NS. Curr. Opin. Microbiol. 2008, 11:113-120.
50. Fernandez-de-Alba C., et al. On the origin of the selectivity of plasmidic H-NS towards horizontally acquired DNA: linking H-NS oligomerization and cooperative DNA binding. J. Mol. Biol. 2013, 425:2347-2358.
51. Forns N., et al. Temperature-dependent conjugative transfer of R27: role of chromosome- and plasmid-encoded Hha and H-NS proteins. J. Bacteriol. 2005, 187:3950-3959.
52. Fortier L.-C., Sekulovic O. Importance of prophages to evolution and virulence of bacterial pathogens. Virulence 2013, 4:354-365.
53. Free A., Dorman C.J. Coupling of Escherichia coli hns mRNA levels to DNA synthesis by autoregulation: implications for growth phase control. Mol. Microbiol. 1995, 18:101-113.
54. 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. 1997, 179:909-918.
55. Free A., et al. The StpA protein functions as a molecular adapter to mediate repression of the bgl operon by truncated H-NS in Escherichia coli. J. Bacteriol. 1998, 180:994-997.
56. Free A., et al. 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. 2001, 42:903-917.
57. Gally D.L., et al. Environmental regulation of the fim switch controlling type 1 fimbrial phase variation in Escherichia coli K-12: effects of temperature and media. J. Bacteriol. 1993, 175:6186-6193.
58. García J., et al. Oligomerization and DNA binding of Ler, a master regulator of pathogenicity of enterohemorrhagic and enteropathogenic Escherichia coli. Nucleic Acids Res. 2012, 40:10254-10262.
59. Garcillán-Barcia M.P., et al. The diversity of conjugative relaxases and its application in plasmid classification. FEMS Microbiol. Rev. 2009, 33:657-687.
60. Gerdes K., et al. Pushing and pulling in prokaryotic DNA segregation. Cell 2010, 141:927-942.
61. Ghosh S.K., et al. Mechanisms for chromosome and plasmid segregation. Annu. Rev. Biochem. 2006, 75:211-241.
62. Giangrossi M., et al. Mutagenesis of the downstream region of the Escherichia coli hns promoter. Biochimie 2001, 83:251-259.
63. Gilmour M.W., et al. Cellular location and temperature-dependent assembly of IncHI1 plasmid R27-encoded TrhC-associated conjugative transfer protein complexes. Mol. Microbiol. 2001, 42:705-715.
64. Giuliodori A.M., et al. The cspA mRNA is a thermosensor that modulates translation of the cold-shock protein CspA. Mol. Cell 2010, 37:21-33.
65. Göransson M., et al. Transcriptional silencing and thermoregulation of gene expression in Escherichia coli. Nature 1990, 344:682-685.
66. Hayes F., Barillà D. The bacterial segrosome: a dynamic nucleoprotein machine for DNA trafficking and segregation. Nat. Rev. Microbiol. 2006, 4:133-143.
67. Heroven A.K., et al. RovA is autoregulated and antagonizes H-NS-mediated silencing of invasin and rovA expression in Yersinia pseudotuberculosis. Mol. Microbiol. 2004, 53:871-888.
68. Tyr). Mol. Microbiol. 1992, 6:2113-2124.
69. James V., Hugouvieux-Cotte-Pattat N. Regulatory systems modulating the transcription of the pectinase genes of Erwinia chrysanthemi are conserved in Escherichia coli. Microbiology 1996, 142:2613-2619.
70. 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 1999, 96:10776-10781.
71. Johansson J., et al. Heteromeric interactions among nucleoid-associated bacterial proteins: localization of StpA-stabilizing regions in H-NS of Escherichia coli. J. Bacteriol. 2001, 183:2343-2347.
72. Johnson T.J., et al. Plasmid replicon typing of commensal and pathogenic Escherichia coli isolates. Appl. Environ. Microbiol. 2007, 73:1976-1983.
73. Jordi B.J., et al. The positive regulator CfaD overcomes the repression mediated by histone-like protein H-NS (H1) in the CFA/I fimbrial operon of Escherichia coli. EMBO J. 1992, 11:2627-2632.
74. Kane K.A., Dorman C.J. Rational design of an artificial genetic switch: Co-option of the H-NS-repressed proU operon by the VirB virulence master regulator. J. Bacteriol. 2011, 193:5950-5960.
75. Kawula T.H., Orndorff P.E. Rapid site-specific DNA inversion in Escherichia coli mutants lacking the histonelike protein H-NS. J. Bacteriol. 1991, 173:4116-4123.
76. Lang B., et al. High-affinity DNA binding sites for H-NS provide a molecular basis for selective silencing within proteobacterial genomes. Nucleic Acids Res. 2007, 35:6330-6337.
77. 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 1991, 88:10907-10911.
78. Levine J.A., et al. H-NST induces LEE expression and the formation of attaching and effacing lesions in enterohemorrhagic Escherichia coli. PLoS One 2014, 9:e86618.
79. Lim C.J., et al. Gene silencing H-NS paralogue StpA forms a rigid protein filament along DNA that blocks DNA accessibility. Nucleic Acids Res. 2012, 40:3316-3328.
80. Lithgow J.K., et al. Alternate SlyA and H-NS nucleoprotein complexes control hlyE expression in Escherichia coli K-12. Mol. Microbiol. 2007, 66:685-698.
81. Liu Y., et al. A divalent switch drives H-NS/DNA-binding conformations between stiffening and bridging modes. Genes Dev. 2010, 24:339-344.
82. Lucchini S., et al. H-NS mediates the silencing of laterally acquired genes in bacteria. PLoS Pathog. 2006, 2:e81.
83. Lucchini S., et al. The H-NS-like protein StpA represses the RpoS (sigma 38) regulon during exponential growth of Salmonella Typhimurium. Mol. Microbiol. 2009, 74:1169-1186.
84. Madrid C., et al. Temperature- and H-NS-dependent regulation of a plasmid-encoded virulence operon expressing Escherichia coli hemolysin. J. Bacteriol. 2002, 184:5058-5066.
85. Madrid C., et al. The novel Hha/YmoA family of nucleoid-associated proteins: use of structural mimicry to modulate the activity of the H-NS family of proteins. Mol. Microbiol. 2007, 63:7-14.
86. Maher D., Taylor D.E. Host range and transfer efficiency of incompatibility group HI plasmid. Can. J. Microbiol. 1993, 39:581-587.
87. Martínez-Santos V.I., et al. Transcriptional regulation of the ecp operon by EcpR, IHF, and H-NS in attaching and effacing Escherichia coli. J. Bacteriol. 2012, 194:5020-5033.
88. Maurer S., et al. A systematic in vitro study of nucleoprotein complexes formed by bacterial nucleoid-associated proteins revealing novel types of DNA organization. J. Mol. Biol. 2009, 387:1261-1276.
89. Mayer O., et al. RNA chaperone activity and RNA-binding properties of the E. coli protein StpA. Nucleic Acids Res. 2007, 35:1257-1269.
90. Mcginty S.É., Rankin D.J. The evolution of conflict resolution between plasmids and their bacterial hosts. Evolution 2012, 66:1662-1670.
91. Müller C.M., et al. Differential effects and interactions of endogenous and horizontally acquired H-NS-like proteins in pathogenic Escherichia coli. Mol. Microbiol. 2010, 75:280-293.
92. Navarre W.W., et al. Selective silencing of foreign DNA with low GC content by the H-NS protein in Salmonella. Science 2006, 313:236-238.
93. Navarre W.W., et al. Silencing of xenogeneic DNA by H-NS-facilitation of lateral gene transfer in bacteria by a defense system that recognizes foreign DNA. Genes Dev. 2007, 21:1456-1471.
94. Ono S., et al. H-NS is a part of a thermally controlled mechanism for bacterial gene regulation. Biochem. J. 2005, 391:203-213.
95. Ohta T., et al. RpoS function is essential for bgl silencing caused by C-terminally truncated H-NS in Escherichia coli. J. Bacteriol. 1999, 181:6278-6283.
96. Olsén A., et al. The RpoS sigma factor relieves H-NS-mediated transcriptional repression of csgA, the subunit gene of fibronectin-binding curli in Escherichia coli. Mol. Microbiol. 1993, 7:523-536.
97. Oshima T., et al. Escherichia coli histone-like protein H-NS preferentially binds to horizontally acquired DNA in association with RNA polymerase. DNA Res. 2006, 13:141-153.
98. Park H.S., et al. Novel role for a bacterial nucleoid protein in translation of mRNAs with suboptimal ribosome-binding sites. Genes Dev. 2010, 24:1345-1350.
99. Paytubi S., et al. YdgT, the Hha paralogue in Escherichia coli, forms heteromeric complexes with H-NS and StpA. Mol. Microbiol. 2004, 54:251-263.
100. Paytubi S., et al. Role of plasmid- and chromosomally encoded Hha proteins in modulation of gene expression in E. coli O157:H7. Plasmid 2013, 70:52-60.
101. Paytubi S., et al. A novel role for antibiotic resistance plasmids in facilitating Salmonella adaptation to non-host environments. Environ. Microbiol. 2014, 16:950-962.
102. Phadtare S., Severinov K. RNA remodeling and gene regulation by cold shock proteins. RNA Biol. 2010, 7:788-795.
103. Pinto U.M., et al. The ABCs of plasmid replication and segregation. Nat. Rev. Microbiol. 2012, 10:755-765.
104. Poore C.A., Mobley H.L. Differential regulation of the Proteus mirabilis urease gene cluster by UreR and H-NS. Microbiology 2003, 149:3383-3394.
105. Porter M.E., Dorman C.J. A role for H-NS in the thermo-osmotic regulation of virulence gene expression in Shigella flexneri. J. Bacteriol. 1994, 176:4187-4191.
106. Prosseda G., et al. The virF promoter in Shigella: more than just a curved DNA stretch. Mol. Microbiol. 2004, 51:523-537.
107. Rajkowitsch L., Schroeder R. Dissecting RNA chaperone activity. RNA 2007, 13:2053-2060.
108. Reisner A., et al. Synergistic effects in mixed Escherichia coli biofilms: conjugative plasmid transfer drives biofilm expansion. J. Bacteriol. 2006, 188:3582-3588.
109. Reyes-Lamothe R., et al. High-copy bacterial plasmids diffuse in the nucleoid-free space, replicate stochastically and are randomly partitioned at cell division. Nucleic Acids Res. 2014, 42:1042-1051.
110. Rimsky S., Travers A. Pervasive regulation of nucleoid structure and function by nucleoid-associated proteins. Curr. Opin. Microbiol. 2011, 14:136-141.
111. Rimsky S., et al. A molecular mechanism for the repression of transcription by the H-NS protein. Mol. Microbiol. 2001, 42:1311-1323.
112. Rowe S., et al. Regulation of the Escherichia coli K5 capsule gene cluster: evidence for the roles of H-NS, BipA, and integration host factor in regulation of group 2 capsule gene clusters in pathogenic E. coli. J. Bacteriol. 2000, 182:2741-2745.
113. Schumacher M.A. Bacterial plasmid partition machinery: a minimalist approach to survival. Curr. Opin. Struct. Biol. 2012, 22:72-79.
114. Schuster C.F., Bertram R. Toxin-antitoxin systems are ubiquitous and versatile modulators of prokaryotic cell fate. FEMS Microbiol. Lett. 2013, 340:73-85.
115. Serna A., et al. Regulation of bacterial conjugation in microaerobiosis by host encoded functions ArcAB and SdhABCD. Genetics 2010, 184:947-958.
116. Sherburne C.K., et al. The complete DNA sequence and analysis of R27, a large IncHI plasmid from Salmonella typhi that is temperature sensitive for transfer. Nucleic Acids Res. 2000, 28:2177-21786.
117. Smillie C., et al. Mobility of plasmids. Microbiol. Mol. Biol. Rev. 2010, 74:434-452.
118. 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. 1996, 15:4970-4980.
119. Sonnenfield J.M., et al. 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 2001, 83:243-249.
120. Stella S., et al. Environmental control of the in vivo oligomerization of nucleoid protein H-NS. J. Mol. Biol. 2006, 355:169-174.
121. Stoebel D.M., et al. Anti-silencing: overcoming H-NS-mediated repression of transcription in Gram-negative enteric bacteria. Microbiology 2008, 154:2533-2545.
122. Strohmaier H., et al. Signal transduction and bacterial conjugation: characterization of the role of ArcA in regulating conjugative transfer of the resistance plasmid R1. J. Mol. Biol. 1998, 277:309-316.
123. Takeda, T., et al., 2011. Distribution of genes encoding nucleoid-associated protein homologs in plasmids. Int. J. Evol. Biol. doi:10.4061/2011/685015.
124. Teramoto J., et al. A novel nucleoid protein of Escherichia coli induced under anaerobiotic growth conditions. Nucleic Acids Res. 2010, 38:3605-3618.
125. Trachman J.D., Maas W.K. Temperature regulation of heat-labile enterotoxin (LT) synthesis in Escherichia coli is mediated by an interaction of H-NS protein with the LT A-subunit DNA. J. Bacteriol. 1998, 180:3715-3718.
126. Trachman J.D., Yasmin M. Thermo-osmoregulation of heat-labile enterotoxin expression by Escherichia coli. Curr. Microbiol. 2004, 49:353-360.
127. Tran C.N., et al. A multifactor regulatory circuit involving H-NS, VirF and an antisense RNA modulates transcription of the virulence gene icsA of Shigella flexneri. Nucleic Acids Res. 2011, 39:8122-8134.
128. Turner E.C., Dorman C.J. H-NS antagonism in Shigella flexneri by VirB, a virulence gene transcription regulator that is closely related to plasmid partition factors. J. Bacteriol. 2007, 189:3403-3413.
129. Ueda T., et al. Functions of the Hha and YdgT proteins in transcriptional silencing by the nucleoid proteins, H-NS and StpA, in Escherichia coli. DNA Res. 2013, 20:263-271.
130. Uliczka F., et al. Unique cell adhesion and invasion properties of Yersinia enterocolitica O:3, the most frequent cause of human Yersiniosis. PLoS Pathog. 2011, 7:e1002117.
131. Umanski T., et al. Thermoregulated expression of virulence genes in enteropathogenic Escherichia coli. Microbiology 2002, 148:2735-2744.
132. Unterholzner S.J., et al. Toxin-antitoxin systems: Biology, identification, and application. Mob. Genet. Elem. 2013, 3:e26219.
133. Uyar E., et al. Differential binding profiles of StpA in wild-type and h-ns mutant cells: a comparative analysis of cooperative partners by chromatin immunoprecipitation-microarray analysis. J. Bacteriol. 2009, 191:2388-2391.
134. Wagner M.A., et al. Silencing and activating type IV secretion genes of the F-like conjugative resistance plasmid R1. Microbiology 2013, 159:2481-2491.
135. Walthers D., et al. The response regulator SsrB activates expression of diverse Salmonella pathogenicity island 2 promoters and counters silencing by the nucleoid-associated protein H-NS. Mol. Microbiol. 2007, 65:477-493.
136. 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. J. Biol. Chem. 2011, 286:1895-1902.
137. Wang W., et al. Chromosome organization by a nucleoid-associated protein in live bacteria. Science 2011, 333:1445-1449.
138. White-Ziegler C.A., Davis T.R. Genome-wide identification of H-NS-controlled, temperature-regulated genes in Escherichia coli K-12. J. Bacteriol. 2009, 191:1106-1110.
139. White-Ziegler C.A., et al. Thermoregulation of Escherichia coli pap transcription: H-NS is a temperature-dependent DNA methylation blocking factor. Mol. Microbiol. 1998, 28:1121-1137.
140. White-Ziegler C.A., et al. H-NS controls pap and daa fimbrial transcription in Escherichia coli in response to multiple environmental cues. J. Bacteriol. 2000, 182:6391-6400.
141. Will W.R., Frost L.S. Characterization of the opposing roles of H-NS and TraJ in transcriptional regulation of the F-plasmid tra operon. J. Bacteriol. 2006, 188:507-514.
142. Will W.R., et al. The role of H-NS in silencing F transfer gene expression during entry into stationary phase. Mol. Microbiol. 2004, 54:769-782.
143. Williams R.M., et al. Probing the structure, function, and interactions of the Escherichia coli H-NS and StpA proteins by using dominant negative derivatives. J. Bacteriol. 1996, 178:4335-4343.
144. Williamson H.S., Free A. A truncated H-NS-like protein from enteropathogenic Escherichia coli acts as an H-NS antagonist. Mol. Microbiol. 2005, 55:808-827.
145. Winardhi R.S., et al. Locus of enterocyte effacement-encoded regulator (Ler) of pathogenic Escherichia coli competes off nucleoid structuring protein H-NS through non-cooperative DNA binding. J. Biol. Chem. 2014, 289:13739-13750.
146. Wozniak R.A., Waldor M.K. Integrative and conjugative elements: mosaic mobile genetic elements enabling dynamic lateral gene flow. Nat. Rev. Microbiol. 2010, 8:552-563.
147. Zhang A., Belfort M. Nucleotide sequence of a newly-identified Escherichia coli gene, stpA, encoding an H-NS-like protein. Nucleic Acids Res. 1992, 20:6735.
148. Zhang A., et al. Escherichia coli protein StpA stimulates self-splicing by promoting RNA assembly in vitro. RNA 1995, 1:783-793.
149. Zhang A., et al. Escherichia coli protein analogs StpA and H-NS: regulatory loops, similar and disparate effects on nucleic acid dynamics. EMBO J. 1996, 15:1340-1349.
150. Zhang W., Baseman J.B. Transcriptional regulation of MG_149, an osmoinducible lipoprotein gene from Mycoplasma genitalium. Mol. Microbiol. 2011, 81:327-339.