Integration Host Factor is required for FarR repression of the farAB-encoded efflux pump of Neisseria gonorrhoeae

Molecular Microbiology

Volumn 60, Issue 6, 2006, Pages 1381-1400

  Lee, Eun Hee ^a   Hill, Stuart A ^b   Napier, Ruth ^a   Shafer, William M ^a,c  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NORTHERN ILLINOIS UNIVERSITY   (United States)

^c ATLANTA VA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEOXYRIBONUCLEASE; HOST FACTOR 1; INTEGRATION HOST FACTOR;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; DNA BINDING; DNA FLANKING REGION; DNA FOOTPRINTING; DNA SEQUENCE; EFFUSION; GENE DELETION; GENE REPRESSION; GENE TARGETING; GENETIC ANALYSIS; IN VITRO STUDY; MOLECULAR MECHANICS; NEISSERIA GONORRHOEAE; NONHUMAN; OPERON; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FUNCTION; TRANSCRIPTION INITIATION;

BASE PAIRING; BINDING SITES; DNA, BACTERIAL; DRUG RESISTANCE, BACTERIAL; FATTY ACIDS; GENE EXPRESSION REGULATION, BACTERIAL; INTEGRATION HOST FACTORS; MOLECULAR SEQUENCE DATA; NEISSERIA GONORRHOEAE; OPERON; PROMOTER REGIONS (GENETICS); PROTEIN FOOTPRINTING; REPRESSOR PROTEINS; SEQUENCE DELETION;

ANIMALIA; NEISSERIA GONORRHOEAE;

EID: 33744469583     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2006.05185.x     Document Type: Article

References (58)

1. Alazard R. Bétermier M. Chandler M. 1992 Escherichia coli integration host factor stabilizes bacteriophage Mu repressor interactions with operator DNA in vitro. Mol Microbiol 6: 1707 1714.
2. Alekshun M.N. Levy S.B. 1999 The mar regulon: multiple resistance to antibiotics and other toxic chemicals. Trends Microbiol 7: 410 413.
3. Alekshun M.N. Levy S.B. Mealy T.R. Seaton B.A. Head J.F. 2001 The crystal structure of MarR, a regulator or multiple antibiotic resistance, at 2.3 Å resolution. Nature 9: 710 714.
4. Baker R.F. Yanofsky C.F. 1968 The periodicity of RNA polymerase initiations: a new regulatory feature of transcription. Proc Natl Acad Sci USA 60: 313 320.
5. Bétermier M. Rousseau P. Alazard R. Chandler M. 1995 Mutual stabilisation of bacteriophage Mu repressor and histone-like proteins in a nucleoprotein structure. J Mol Biol 479: 332 341.
6. Chatterjee A. Chaudhuri S. Saha G. Gupta S. Chowdhury R. 2004 Effect of bile on the cell surface permeability barrier and efflux system of Vibrio cholerae. J Bacteriol 186: 6809 6814.
7. Choy H.E. Adhya S. 1992 Control of gal transcription through DNA looping; inhibition of the initial transcribing complex. Proc Natl Acad Sci USA 89: 11264 11268.
8. Craig N. Nash H.A. 1984 E. coli integration host factor binds to specific sites in DNA. Cell 39: 707 716.
9. Delahay R.M. Robertson B.D. Balthazar J.T. Shafer W.M. Ison C.A. 1997 Involvement of the gonococcal MtrE protein in the resistance of Neisseria gonorrhoeae to toxic hydrophobic compounds. Microbiology 143: 2127 2133.
10. Evans K. Adewoye L. Poole K. 2001 MexR repressor of the mexAB-oprM multidrug efflux operon of Pseudomonas aeruginosa: identification of MexR binding sites in the mexA-mexR intergenic binding sites in the mexA-mexR intergenic region. J Bacteriol 183: 807 812.
11. Filutowicz M. Inman R. 1991 A compact nucleoprotein structure is produced by binding of Escherichia coli integration host factor (IHF) to the replication origin of plasmid R6K. J Biol Chem 266: 47077 47083.
12. Flamm E.L. Weisberg R.A. 1985 Primary structure of the hip gene of Escherichia coli and of its product, the beta subunit of integration host factor. J Mol Biol 25: 117 128.
13. Freundlich M. Ramani N. Mathew E. Sirko A. Tsui P. 1992 The role of integration host factor in gene expression in Escherichia coli. Mol Microbiol 6: 2557 2563.
14. Friedman D.I. 1988 Integration host factor: a protein for all reasons. Cell 55: 545 554.
15. Fyfe J.A. Davies J.K. 1998 An AT-rich tract containing an integration host factor-binding domain and two UP-like elements enhances transcription from the pilEp1 promoter of Neisseria gonorrhoeae. J Bacteriol 180: 2152 2159.
16. Gama M.-J. Toussaint A. Higgins N.P. 1992 Stabilization of bacteriophage Mu repressor-operator complexes by the Escherichia coli integration host factor protein. Mol Microbiol 6: 1715 1722.
17. Griffo G. Oppenheim A.B. Gottesman M.E. 1989 Repression of the 1 pcin promoter by integrative host factor. J Mol Biol 209: 55 64.
18. Gunn J.S. Stein D.C. 1996 Use of a non-selective transformation technique to construct a multiply restriction/modification-deficient mutant of Neisseria gonorrhoeae. Mol Gen Genet 251: 509 527.
19. Guymon L.F. Sparling P.F. 1975 Altered crystal violet permeability and lytic behavior in antibiotic-resistant and -sensitive strains of Neisseria gonorrhoeae. J Bacteriol 124: 757 763.
20. Hagman K.E. Shafer W.M. 1995 Transcriptional control of the mtr efflux system of Neisseria gonorrhoeae. J Bacteriol 177: 4162 4165.
21. Hagman K.E. Pan W. Spratt B.G. Balthazar J.T. Judd R.C. Shafer W.M. 1995 Resistance of Neisseria gonorrhoeae to antimicrobial hydrophobic agents is modulated by the mtrCDE efflux system. Microbiology 141: 611 622.
22. Haluzi H. Goitein D. Koby S. Mendelson I. Teff D. Mengeritsky G., et al. 1991 Genes coding for integration host factor are conserved in gram negative bacteria. J Bacteriol 173: 6297 6299.
23. Hill S.A. Samuels D.S. Carlson J.H. Wilson J. Hogan D. Lubke L. Belland R.J. 1997 Integration host factor is a transcriptional cofactor of pilF in Neisseria gonorrhoeae. Mol Microbiol 23: 649 656.
24. Huang L. Tsui P. Freundlich M. 1990 Integration host factor is a negative effector of the in vivo and in vitro expression of ompC in Escherichia coli. J Bacteriol 172: 5293 5298.
25. Jerse A.E. Sharma N.D. Simms A.N. Crow E.T. Snyder L.A. Shafer W.M. 2003 A gonococcal efflux pump system enhances bacterial survival in a female mouse model of genital tract infection. Infect Immun 71: 5576 5582.
26. Kim J. Zwieb C. Wu C. Adhya S. 1989 Bending of DNA by gene-regulatory proteins: construction and use of a DNA bending vector. Gene 85: 15 23.
27. Krause H.M. Higgins N.P. 1986 Positive and negative regulation of a Mu operator by Mu repressor and E. coli integration host factor. J Biol Chem 261: 3744 3752.
28. Kur J. Hasam N. Szybalski W. 1989 Physical and biological consequences of interactions between integration host factor (IHF) and coliphage lambda late p'R promoter and its mutants. Gene 81: 1 15.
29. Lee E.-H. Shafer W.M. 1999 The farAB-encoded efflux pump mediates resistance of gonococci to long-chained antibacterial fatty acids. Mol Microbiol 33: 839 845.
30. Lee E.-H. Rouquette-Loughlin C. Folster J.P. Shafer W.M. 2003 FarR regulates the farAB-encoded efflux pump of Neisseria gonorrhoeae via an MtrR regulatory mechanism. J Bacteriol 185: 7145 7152.
31. Lewis. D.E.A. 2003 Identification of promoters of Escherichia coli and phage in transcription section plasmid pSA850. Methods Enzymol 370: 618 645.
32. Lim D. Poole K. Strynadka N.C. 2002 Crystal structure of the MexR repressor of the mexRAB-oprM multidrug efflux operon of Pseudomonas aeruginosa. J Biol Chem 277: 29253 29259.
33. Lucas C.E. Balthazar J.T. Hagman K.E. Shafer W.M. 1997 The MtrR repressor binds the DNA sequence between the mtrR and mtrC genes of Neisseria gonorrhoeae. J Bacteriol 179: 4123 4128.
34. McFarland L. Mietzner T. Knapp J.S. Sandstrom E. Homes K.K. Morse S.A. 1983 Gonococcal susceptibility to fecal lipids can be mediated by an mtr-independent mechanism. J Clin Microbiol 18: 121 127.
35. Martin R.G. Rosner J.L. 1995 Binding of purified multiple antibiotic-resistance repressor protein (MarR) to mar operator sequences. Proc Natl Acad Sci USA 92: 5456 5460.
36. Miller H.I. 1984 Primary structure of the himA gene of E. coli homology with DNA binding protein HU and association with the phenylalany tRNA synthetase operon. Cold Spring Harb Symp Quant Biol 49: 691 698.
37. Miller P.F. Sulavik M.C. 1996 Overlaps and parallels in the regulation of intrinsic multiple-antibiotic resistance in Escherichia coli. Mol Microbiol 21: 441 448.
38. Moitoso de Vargas L. Kim S. Landy A. 1989 DNA looping generated by DNA bending protein IHF and the two domains of lambda integrase. Science 474: 1457 1461.
39. Nash H.A. Robertson C.A. 1981 Purification and properties of the Escherichia coli protein factor required for lambda integrative recombination. J Biol Chem 256: 9476 9453.
40. Pan W. Spratt B.G. 1994 Regulation of the permeability of the gonococcal cell envelope by the mtr system. Mol Microbiol 11: 769 775.
41. Peacock S. Weissbach H. Nash H.A. 1984 In vitro regulation of phage lambda cII gene expression by Escherichia coli integration host factor. Proc Natl Acad Sci USA 81: 6009 6013.
42. Pérez-Martín. J. Rojo F. De Lorenzo V. 1994 Promoters responsive to DNA bending: a common theme in prokaryotic gene expression. Microbiol Rev 58: 268 290.
43. Ramani N. Huang L. Freundlich M. 1992 In vitro integration host factor with the ompF promoter-regulatory region of Escherichia coli. Mol Gen Genet 231: 478 255.
44. Robertson C.A. Nash H.A. 1988 Bending of the bacteriophage lambda attachment site by Escherichia coli integration host factor. J Biol Chem 263: 3554 3557.
45. Rosenberg E.Y. Bertenthal D. Nilles M.L. Bertrand K.P. Nikaido H. 2003 Bile salts and fatty acids induce the expression of Escherichia coli AcrAB multidrug efflux pump through their interaction with Rob regulatory protein. Mol Microbiol 48: 1609 1619.
46. Rouquette-Loughlin C. Balthazar J.T. Hill S.A. Shafer W.M. 2004 Modulation of the mtrCDE-encoded efflux pump gene complex of Neisseria meningitidis due to a Correia element insertion sequence. Mol Microbiol 54: 731 741.
47. Saier M.H., Jr, Paulsen I.T. Matin A. 1997 A bacterial model system for understanding multi-drug resistance. Microb Drug Resist 3: 289 295.
48. Shafer W.M. Guymon L.F. Lind I. Sparling P.F. 1984 Identification of an envelope mutation (env-10) resulting in increased antibiotic susceptibility and pyocin resistance in a clinical isolate of Neisseria gonorrhoeae. Antimicrob Agents Chemother 25: 767 769.
49. Shafer W.M. Veal W.L. Lee E.-H. Zarantonelli L. Balthazar J.T. Rouquette C. 2001 Genetic organization and regulation of antimicrobial efflux systems possessed by Neisseria gonorrhoeae and Neisseria meningitidis. J Mol Microbiol Biotech 3: 219 477.
50. Silver L.E. Clark V.L. 1995 Construction of a translational lacZ fusion system to study gene regulation in Neisseria gonorrhoeae. Gene 166: 101 104.
51. Stenzel T.T. Patel P. Bastia D. 1987 The integration host factor of Escherichia coli binds to bent DNA at the origin of replication of the plasmid pSC101. Cell 49: 709 717.
52. Thanassi D.G. Cheng L.W. Nikaido H. 1997 Active efflux of bile salts by Escherichia coli. J Bacteriol 179: 2512 2518.
53. Tomizawa J. Itoh T. Selzer G. Som T. 1981 Inhibition of ColE1 RNA primer formation by a plasmid-specified small RNA. Proc Natl Acad Sci USA 78: 1421 1425.
54. Tsui P. Huang L. Freundlich M. 1991 Integration host factor binds specifically to multiple sites in the ompB promoter of Escherichia coli and inhibits transcription. J Bacteriol 173: 5800 5807.
55. Veal W.L. Nicholas R.A. Shafer W.M. 2002 Overexpression of the MtrC-MtrD-MtrE efflux pump due to an mtrR mutation is required for chromosomally mediated penicillin resistance in Neisseria gonorrhoeae. J Bacteriol 184: 5619 5647.
56. Wang R.F. Kushner S.R. 1991 Construction of versatile low-copy-number vectors for cloning, sequencing, gene expression in Escherichia coli. Gene 100: 195 199.
57. Wu H.M. Crothers D.M. 1984 The locus of sequence-directed and protein-induced DNA bending. Nature 308: 509 513.
58. Zarantonelli L. Borthagary G. Lee E.-H. Shafer W.M. 2001 Decreased susceptibility to azithromycin and erthyromycin mediated by a novel mtrR promoter mutation in Neisseria gonorrhoeae. J Antimicrob Chemother 47: 651 654.