MtrR Control of a Transcriptional Regulatory Pathway in Neisseria meningitidis That Influences Expression of a Gene (nadA) Encoding a Vaccine Candidate

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  Cloward, Jason M ^a,b,c   Shafer, William M ^a,b  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b ATLANTA VA MEDICAL CENTER   (United States)

^c NATIONAL CENTER FOR IMMUNIZATION AND RESPIRATORY DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; ADHESIN NADA; BACTERIAL PROTEIN; PROTEIN FARR; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR MTRR; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL STRAIN; COMPLEX FORMATION; CONTROLLED STUDY; DNA BINDING; DNA DETERMINATION; DNA SEQUENCE; FARR GENE; GENE CONTROL; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE INTERACTION; GENE OVEREXPRESSION; GENE TARGETING; MOLECULAR STABILITY; MTRR GENE; NADA GENE; NEISSERIA MENINGITIDIS; NONHUMAN; PROMOTER REGION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; TRANSCRIPTION REGULATION;

ADHESINS, BACTERIAL; BACTERIAL PROTEINS; BACTERIAL VACCINES; BASE SEQUENCE; DEOXYRIBONUCLEASE I; DNA, BACTERIAL; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; MOLECULAR SEQUENCE DATA; NEISSERIA MENINGITIDIS; REPRESSOR PROTEINS; SPECIES SPECIFICITY; TRANSCRIPTION, GENETIC;

EID: 84873669252     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0056097     Document Type: Article

References (42)

1. Cartwright KA, Stuart JM, Jones DM, Noah ND, (1987) The Stonehouse survey: nasopharyngeal carriage of meningococci and Neisseria lactamica. Epidemiol Infect 99: 591-601.
2. Stephens DS, Greenwood B, Brandtzaeg P, (2007) Epidemic meningitis, meningococcaemia, and Neisseria meningitidis. Lancet 369: 2196-2210.
3. Sharip A, Sorvillo F, Redelings MD, Mascola L, Wise M, et al. (2006) Population-based analysis of meningococcal disease mortality in the United States: 1990-2002. Pediatr Infect Dis J 25: 191-194.
4. Cartwright KA (1995) Meningococcal Carriage and Disease. In: Cartwright KA, editor. Meningococcal Disease. Chichester: John Wiley & Sons. pp. 115-146.
5. Virji M, (2009) Pathogenic neisseriae: surface modulation, pathogenesis and infection control. Nat Rev Microbiol 7: 274-286.
6. Nassif X, Beretti JL, Lowy J, Stenberg P, O'Gaora P, et al. (1994) Roles of pilin and PilC in adhesion of Neisseria meningitidis to human epithelial and endothelial cells. Proc Natl Acad Sci U S A 91: 3769-3773.
7. Scheuerpflug I, Rudel T, Ryll R, Pandit J, Meyer TF, (1999) Roles of PilC and PilE proteins in pilus-mediated adherence of Neisseria gonorrhoeae and Neisseria meningitidis to human erythrocytes and endothelial and epithelial cells. Infect Immun 67: 834-843.
8. Virji M, Kayhty H, Ferguson DJ, Alexandrescu C, Heckels JE, et al. (1991) The role of pili in the interactions of pathogenic Neisseria with cultured human endothelial cells. Mol Microbiol 5: 1831-1841.
9. Simon D, Rest RF, (1992) Escherichia coli expressing a Neisseria gonorrhoeae opacity-associated outer membrane protein invade human cervical and endometrial epithelial cell lines. Proc Natl Acad Sci U S A 89: 5512-5516.
10. Virji M, Saunders JR, Sims G, Makepeace K, Maskell D, et al. (1993) Pilus-facilitated adherence of Neisseria meningitidis to human epithelial and endothelial cells: modulation of adherence phenotype occurs concurrently with changes in primary amino acid sequence and the glycosylation status of pilin. Mol Microbiol 10: 1013-1028.
11. Comanducci M, Bambini S, Brunelli B, Adu-Bobie J, Arico B, et al. (2002) NadA, a novel vaccine candidate of Neisseria meningitidis. J Exp Med 195: 1445-1454.
12. Capecchi B, Adu-Bobie J, Di Marcello F, Ciucchi L, Masignani V, et al. (2005) Neisseria meningitidis NadA is a new invasin which promotes bacterial adhesion to and penetration into human epithelial cells. Mol Microbiol 55: 687-698.
13. Martin P, Makepeace K, Hill SA, Hood DW, Moxon ER, (2005) Microsatellite instability regulates transcription factor binding and gene expression. Proc Natl Acad Sci U S A 102: 3800-3804.
14. Metruccio MM, Pigozzi E, Roncarati D, Berlanda Scorza F, Norais N, et al. (2009) A novel phase variation mechanism in the meningococcus driven by a ligand-responsive repressor and differential spacing of distal promoter elements. PLoS Pathog 5: e1000710.
15. Martin P, van de Ven T, Mouchel N, Jeffries AC, Hood DW, et al. (2003) Experimentally revised repertoire of putative contingency loci in Neisseria meningitidis strain MC58: evidence for a novel mechanism of phase variation. Mol Microbiol 50: 245-257.
16. Murphy GL, Connell TD, Barritt DS, Koomey M, Cannon JG, (1989) Phase variation of gonococcal protein II: regulation of gene expression by slipped-strand mispairing of a repetitive DNA sequence. Cell 56: 539-547.
17. Schielke S, Huebner C, Spatz C, Nagele V, Ackermann N, et al. (2009) Expression of the meningococcal adhesin NadA is controlled by a transcriptional regulator of the MarR family. Mol Microbiol 72: 1054-1067.
18. Lee EH, Rouquette-Loughlin C, Folster JP, Shafer WM, (2003) FarR regulates the farAB-encoded efflux pump of Neisseria gonorrhoeae via an MtrR regulatory mechanism. J Bacteriol 185: 7145-7152.
19. Schielke S, Schmitt C, Spatz C, Frosch M, Schubert-Unkmeir A, et al. (2010) The transcriptional repressor FarR is not involved in meningococcal fatty acid resistance mediated by the FarAB efflux pump and dependent on lipopolysaccharide structure. Appl Environ Microbiol 76: 3160-3169.
20. Fagnocchi L, Pigozzi E, Scarlato V, Delany I, (2012) In the NadR regulon, adhesins and diverse meningococcal functions are regulated in response to signals in human saliva. J Bacteriol 194: 460-474.
21. Takahama U, Oniki T, Murata H, (2002) The presence of 4-hydroxyphenylacetic acid in human saliva and the possibility of its nitration by salivary nitrite in the stomach. FEBS Lett 518: 116-118.
22. Johnson PJ, Stringer VA, Shafer WM, (2011) Off-target gene regulation mediated by transcriptional repressors of antimicrobial efflux pump genes in Neisseria gonorrhoeae. Antimicrob Agents Chemother 55: 2559-2565.
23. Silver LE, Clark VL, (1995) Construction of a translational lacZ fusion system to study gene regulation in Neisseria gonorrhoeae. Gene 166: 101-104.
24. Stephens DS, Swartley JS, Kathariou S, Morse SA, (1991) Insertion of Tn916 in Neisseria meningitidis resulting in loss of group B capsular polysaccharide. Infect Immun 59: 4097-4102.
25. Schielke S, Spatz C, Schwarz RF, Joseph B, Schoen C, et al. (2011) Characterization of FarR as a highly specialized, growth phase-dependent transcriptional regulator in Neisseria meningitidis. Int J Med Microbiol 301: 325-333.
26. Hagman KE, Pan W, Spratt BG, Balthazar JT, Judd RC, et al. (1995) Resistance of Neisseria gonorrhoeae to antimicrobial hydrophobic agents is modulated by the mtrRCDE efflux system. Microbiology 141 (Pt 3) (): 611-622.
27. Lucas CE, Balthazar JT, Hagman KE, Shafer WM, (1997) The MtrR repressor binds the DNA sequence between the mtrR and mtrC genes of Neisseria gonorrhoeae. J Bacteriol 179: 4123-4128.
28. Zalucki YM, Mercante AD, Cloward JM, Ohneck EA, Kandler J, et al. (2011) Function and regulation of Neisseria gonorrhoeae efflux pumps. Microbial Efflux Pumps: Current Research: Horizon Scientific and Caister Academic Press.
29. Lee EH, Shafer WM, (1999) The farAB-encoded efflux pump mediates resistance of gonococci to long-chained antibacterial fatty acids. Mol Microbiol 33: 839-845.
30. Hagman KE, Shafer WM, (1995) Transcriptional control of the mtr efflux system of Neisseria gonorrhoeae. J Bacteriol 177: 4162-4165.
31. Ohneck EA, Zalucki YM, Johnson PJ, Dhulipala V, Golparian D, et al. (2011) A novel mechanism of high-level, broad-spectrum antibiotic resistance caused by a single base pair change in Neisseria gonorrhoeae. MBio 2.
32. Rouquette-Loughlin CE, Balthazar JT, Hill SA, Shafer WM, (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.
33. Shafer WM, Balthazar JT, Hagman KE, Morse SA, (1995) Missense mutations that alter the DNA-binding domain of the MtrR protein occur frequently in rectal isolates of Neisseria gonorrhoeae that are resistant to faecal lipids. Microbiology 141 (Pt 4) (): 907-911.
34. Enriquez R, Abad R, Chanto G, Corso A, Cruces R, et al. (2010) Deletion of the Correia element in the mtr gene complex of Neisseria meningitidis. J Med Microbiol 59: 1055-1060.
35. Shafer WM, Guymon LF, Lind I, Sparling PF, (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.
36. Menard R, Sansonetti PJ, Parsot C, (1993) Nonpolar mutagenesis of the ipa genes defines IpaB, IpaC, and IpaD as effectors of Shigella flexneri entry into epithelial cells. J Bacteriol 175: 5899-5906.
37. Skaar EP, Lazio MP, Seifert HS, (2002) Roles of the recJ and recN genes in homologous recombination and DNA repair pathways of Neisseria gonorrhoeae. J Bacteriol 184: 919-927.
38. Laemmli UK, (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
39. Folster JP, Dhulipala V, Nicholas RA, Shafer WM, (2007) Differential regulation of ponA and pilMNOPQ expression by the MtrR transcriptional regulatory protein in Neisseria gonorrhoeae. J Bacteriol 189: 4569-4577.
40. Folster JP, Johnson PJ, Jackson L, Dhulipali V, Dyer DW, et al. (2009) MtrR modulates rpoH expression and levels of antimicrobial resistance in Neisseria gonorrhoeae. J Bacteriol 191: 287-297.
41. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Laboratory Press.
42. Prentki P, Krisch HM, (1984) In vitro insertional mutagenesis with a selectable DNA fragment. Gene 29: 303-313.