Modulation of horizontally acquired genes by the Hha-YdgT proteins in Salmonella enterica serovar typhimurium

Journal of Bacteriology

Volumn 190, Issue 3, 2008, Pages 1152-1156

  Vivero, Aitziber ^a   Baños, Rosa C ^a   Mariscotti, Javier F ^b   Oliveros, Juan Carlos ^b   García Del Portillo, Francisco ^b   Juárez, Antonio ^a   Madrid, Cristina ^a  

^a UNIVERSITY OF BARCELONA   (Spain)

^b CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTIC AGENT; BACTERIAL DNA; BACTERIAL PROTEIN; CHLORAMPHENICOL; HHA PROTEIN; HISTONE LIKE NUCLEOID STRUCTURING PROTEIN; UNCLASSIFIED DRUG; VIRULENCE FACTOR; YDGT PROTEIN; YMOA PROTEIN;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL VIRULENCE; BACTERIUM MUTANT; DNA SEQUENCE; GENE EXPRESSION; GENOMIC ISLAND; HHA GENE; HORIZONTAL GENE TRANSFER; NONHUMAN; OPEN READING FRAME; PRIORITY JOURNAL; SALMONELLA ENTERICA; SALMONELLA TYPHIMURIUM; STRAIN IDENTIFICATION; YDGT GENE;

ANIMALS; BACTERIAL PROTEINS; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; GENE TRANSFER, HORIZONTAL; MICE; MICE, INBRED BALB C; PROTEOME; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SALMONELLA INFECTIONS, ANIMAL; SALMONELLA TYPHIMURIUM; TRANSCRIPTION, GENETIC; VIRULENCE;

SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM;

EID: 38649136298     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.01206-07     Document Type: Article

References (40)

1. Bertin, P., E. H. Lee, P. Lejeune, C. Colson, A. Danchin, and E. Collatz. 1994. The H-NS protein is involved in the biogenesis of flagella in Escherichia coli. J. Bacteriol. 176:5537-5540.
2. Beuzón, C. R., and D. W. Holden. 2001. Use of mixed infections with Salmonella strains to study virulence genes and their interactions in vivo. Microbes Infect. 3:1345-1352.
3. Camacho, E., and J. Casadesús. 2005. Regulation of traJ transcription in the Salmonella virulence plasmid by strand-specific DNA adenine hemimethylation. Mol. Microbiol. 57:1700-1718.
4. Camacho, E. M., and J. Casadesús. 2002. Conjugal transfer of the virulence plasmid of Salmonella enterica is regulated by a leucine-responsive regulatory protein and DNA adenine methylation. Mol. Microbiol. 44:1589-1598.
5. r cassetes with the option of Flp-catalyzed excision of the antibiotic resistance determinant. Gene 158:2-14.
6. Coombes, B. K., M. E. Wickham, M. J. Lowden, N. F. Brown, and B. B. Finlay. 2005. Negative regulation of Salmonella pathogenicity island 2 is required for contectual control of virulence during typhoid. Proc. Natl. Acad. Sci. USA 102:17460-17465.
7. Cornelis, G., C. Sluiters, I. Delor, D. Gelb, K. Kaniga, C. Lambert de Rouvroit, M. P. Sory, J. C. Vanooteghem, and T. Michiels. 1991. ymoA, a Yersinia enterocolitica chromosomal gene modulating the expression of virulence functions. Mol. Microbiol. 5:1023-1034.
8. Cunningham, T. P., R. C. Montelaro, and E. P. Greenberg. 1993. Lentivirus envelope sequences and proviral genomes are stabilized in Escherichia coli when cloned in low-copy-number plasmid vector. Gene 9:93-98.
9. Datsenko, K. A., and B. L. Wanner. 2000. One-step inactivation of chromosomal genes in Escherichia coli K12. Proc. Natl. Acad. Sci. USA 97:6640-6645.
10. Dole, S., V. Nagarajavel, and K. Schnetz. 2004. The histone-like nucleoid structuring protein H-NS represses the Escherichia coli bgl operon downstream of the promoter. Mol. Microbiol. 52:589-600.
11. Dorman, C. J. 2004. H-NS: a universal regulator for a dynamic genome. Nat. Rev. Microbiol. 2:391-400.
12. Dorman, C. J. 2007. H-NS, the genome sentinel. Nat. Rev. Microbiol. 5:157-161.
13. Ellison, D. W., and V. L. Miller. 2006. H-NS represses inv transcription in Yersinia enterocolitica through competition with RovA and interaction with YmoA. J. Bacteriol. 188:5101-5112.
14. Fahlen, T. F., R. L. Wilson, J. D. Boddicker, and B. D. Jones. 2001. Hha is a negative modulator of transcription of hilA, the Salmonella enterica serovar Typhimurium invasion gene transcriptional activator. J. Bacteriol. 183:6620-6629.
15. Forns, N., R. C. Baños, C. Balsalobre, A. Juárez, and C. Madrid. 2005. Temperature-dependent conjugative transfer of R27: role of chromosome-and plasmid-encoded Hha and H-NS proteins. J. Bacteriol. 187:3950-3959.
16. Garcia, J., T. N. Cordeiro, J. M. Nieto, I. Pons, A. Juárez, and M. Pons. 2005. Interaction between the bacterial nucleoid-associated proteins Hha and H-NS involves a conformational change of Hha. Biochem. J. 388:755-762.
17. Garcia, J., C. Madrid, A. Juárez, and M. Pons. 2006. New roles for key residues in helices H1 and H2 of the Escherichia coli H-NS N-terminal domain: H-NS dimer stabilization and Hha binding. J. Mol. Biol. 359:679-689.
18. Gillen, K. L., and K. T. Hughes. 1991. Negative regulatory loci coupling flagellar synthesis to flagellar assembly in Salmonella typhimurium. J. Bacteriol. 173:2301-2310.
19. Hoiseth, S. K., and B. A. Stocker. 1981. Aromatic-dependent Salmonella enterica are non-virulent and effective as live vaccines. Nature 291:238-239.
20. Jones, B. D. 2005. Salmonella invasion gene regulation: a story of environmental awareness. J. Microbiol. 43:110-117.
21. Jordi, B. J., and C. F. Higgins. 2000. The downstream regulatory element of the proU operon of Salmonella typhimurium inhibits open complex formation by RNA polymerase at a distance. J. Biol. Chem. 275:12123-12128.
22. Lucchini, S., G. Rowley, M. D. Goldberg, D. Hurd, M. Harrison, and J. C. Hinton. 2006. H-NS mediates the silencing of laterally acquired genes in bacteria. PLoS Pathog. 2:e81.
23. Madrid, C., C. Balsalobre, J. García, and A. Juárez. 2007. 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. 63:7-14.
24. Madrid, C., J. García, M. Pons, and A. Júarez. 2007. Molecular evolution of the H-NS protein: interaction with Hha-like proteins is restricted to Enterobacteriaceae. J. Bacteriol. 189:265-268.
25. Madrid, C., J. M. Nieto, S. Paytubí, F. Falconi, C. O. Gualerzi, and A. Juárez. 2002. Temperature- and H-NS-dependent regulation of a plasmid-encoded virulence operon expressing Escherichia coli hemolysin. J. Bacteriol. 184:5058-5066.
26. McClelland, M., K. E. Sanderson, J. Spieth, S. W. Clifton, P. Latreille, L. Courtney, S. Porwollik, J. Ali, M. Dante, F. Du, S. Hou, D. Layman, S. Leonard, C. Nguyen, K. Scott, A. Holmes, N. Grewal, E. Mulvaney, E. Ryan, H. Sun, L. Florea, W. Miller, T. Stoneking, M. Nhan, R. Waterston, and R. K. Wilson. 2001. Complete genome sequence of Salmonella enterica serovar Typhimurium LT2, Nature 413:852-856.
27. Mikulskis, A. V., and G. Cornelis. 1994. A new class of proteins regulating gene expression in enterobacteria. Mol. Microbiol. 11:77-86.
28. Navarre, W. W., S. Porwollik, Y. Wang, M. McClelland, H. Rosen, S. J. Libby, and F. C. Fang. 2006. Selective silencing of foreign DNA with low GC content by the H-NS protein in Salmonella. Science 313:236-238.
29. Nieto, J. M., M. Carmona, S. Bolland, Y. Jubete, F. de la Cruz, and A. Juarez. 1991. The hha gene modulates hemolysin expression in Escherichia coli. Mol. Microbiol. 5:1285-1293.
30. Nieto, J. M., C. Madrid, E. Miquelay, J. L. Parra, S. Rodríguez, and A. Juárez. 2002. Evidence for direct protein-protein interaction between members of the enterobacterial Hha/YmoA and H-NS families of proteins. J. Bacteriol. 184:629-635.
31. Nieto, J. M., C. Madrid, A. Prenafeta, E. Miquelay, C. Balsalobre, M. Carrascal, and A. Juárez. 2000. Expression of the hemolysin 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.
32. Olekhnovich, I. N., and R. J. Kadner. 2006. Crucial roles of both flanking sequences in silencing of the hilA promoter in Salmonella enterica. J. Mol. Biol. 357:373-386.
33. Paytubi, S., C. Madrid, N. Forns, J. M. Nieto, C. Balsalobre, B. E. Uhlin, and A. Juárez. 2004. YdgT, the Hha paralogue in Escherichia coli, forms heteromeric complexes with H-NS and StpA. Mol. Microbiol. 54:251-263.
34. Pflum, M. K. 2006. H-NS gives invading DNA the silent treatment. Nat. Chem. Biol. 2:400-401.
35. Rimsky, S. 2004. Structure of the histone-like protein H-NS and its role in regulation and genome superstructure. Curr. Opin. Microbiol. 7:109-114.
36. Sharma, V. K., and R. L. J. Zuerner. 2004. Role of hha and ler in transcriptional regulation of the esp operon of enterohemorrhagic Escherichia coli O157:H7. J. Bacteriol. 186:7290-7301.
37. Silphaduang, U., M. Mascarenhas, M. Karmali, and B. K. Coombes. 2007. Repression of intracellular virulence factors in Salmonella by the Hha and YdgT nucleoid-associated proteins. J. Bacteriol. 189:3669-3673.
38. Tatusov, R. L., D. A. Natale, I. V. Garkavtsev, T. A. Tatusova, U. T. Shankavaram, B. S. Rao, B. Kiryutin, M. Y. Galperin, N. D. Fedorova, and E. V. Koonina. 2001. The COG database: new developments in phylogenetic classification of proteins from complete genomes. Nucleic Acids Res. 29:22-28.
39. Torreblanca, J., S. Marqués, and J. Casadesús. 1999. Synthesis of finP RNA by plasmids F and pSLT is regulated by DNA adenine methylation. Genetics 152:31-45.
40. Walthers, D., R. K. Carroll, W. W. Navarre, S. J. Libby, F. C. Fang, and L. J. Kenney. 2007. 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. 65:477-493.