The Treponema denticola AtcR LytTR domain-containing response regulator interacts with three architecturally distinct promoter elements: Implications for understanding the molecular signaling mechanisms that drive the progression of periodontal disease

Molecular Oral Microbiology

Volumn 29, Issue 5, 2014, Pages 219-232

  Miller, D P ^a   Frederick, J R ^a   Sarkar, J ^a   Marconi, R T ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Denticola; LytTR; Periodontal disease; Spirochete; Treponema

Indexed keywords

ATCR PROTEIN; BACTERIAL DNA; BACTERIAL PROTEIN; DNA BINDING PROTEIN; LYTTR1 PROTEIN; LYTTR2 PROTEIN; LYTTR3 PROTEIN; RECOMBINANT PROTEIN; REGULATOR PROTEIN; UNCLASSIFIED DRUG; SIGMA FACTOR; TRANSCRIPTION FACTOR;

ARTICLE; BACTERIAL GENOME; BIOINFORMATICS; CONTROLLED STUDY; DISEASE COURSE; DNA BINDING; DNA STRUCTURE; GEL MOBILITY SHIFT ASSAY; IMMOBILIZED METAL AFFINITY CHROMATOGRAPHY; MOLECULAR INTERACTION; MOLECULAR RECOGNITION; NONHUMAN; OPEN READING FRAME; PERIODONTAL DISEASE; PROMOTER REGION; PROTEIN MOTIF; RECEPTOR AFFINITY; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION SITE; TREPONEMA DENTICOLA; ADAPTATION; BIOLOGY; DNA SEQUENCE; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; HUMAN; MICROBIOLOGICAL EXAMINATION; MICROBIOLOGY; NUCLEOTIDE MOTIF; REGULATORY SEQUENCE; REGULON;

ADAPTATION, PHYSIOLOGICAL; BACTERIAL PROTEINS; BACTERIOLOGICAL TECHNIQUES; COMPUTATIONAL BIOLOGY; DISEASE PROGRESSION; ELECTROPHORETIC MOBILITY SHIFT ASSAY; GENE EXPRESSION REGULATION, BACTERIAL; GENOME, BACTERIAL; HUMANS; NUCLEOTIDE MOTIFS; PERIODONTAL DISEASES; PROMOTER REGIONS, GENETIC; REGULATORY SEQUENCES, NUCLEIC ACID; REGULON; SEQUENCE ANALYSIS, DNA; SIGMA FACTOR; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TREPONEMA DENTICOLA;

EID: 84908354604     PISSN: 20411006     EISSN: 20411014     Source Type: Journal    
DOI: 10.1111/omi.12059     Document Type: Article

References (54)

1. Abdelnour, A., Arvidson, S., Bremell, T., Ryden, C. and Tarkowski, A. (1993) The accessory gene regulator (agr) controls Staphylococcus aureus virulence in a murine arthritis model. Infect Immun 61: 3879-3885.
2. Arthur, D.C., Edwards, R.A., Tsutakawa, S., Tainer, J.A., Frost, L.S. and Glover, J.N. (2011) Mapping interactions between the RNA chaperone FinO and its RNA targets. Nucleic Acids Res 39: 4450-4463.
3. Bailey, T.L. and Elkan, C. (1994) Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc Int Conf Intell Syst Mol Biol 2: 28-36.
4. Ba-Thein, W., Lyristis, M., Ohtani, K. et al. (1996) The virR/virS locus regulates the transcription of genes encoding extracellular toxin production in Clostridium perfringens. J Bacteriol 178: 2514-2520.
5. Belete, B., Lu, H. and Wozniak, D.J. (2008) Pseudomonas aeruginosa AlgR regulates type IV pilus biosynthesis by activating transcription of the fimU-pilVWXY1Y2E operon. J Bacteriol 190: 2023-2030.
6. Bian, J., Liu, X., Cheng, Y.Q. and Li, C. (2013) Inactivation of cyclic Di-GMP binding protein TDE0214 affects the motility, biofilm formation, and virulence of Treponema denticola. J Bacteriol 195: 3897-3905.
7. Burns, L.H., Adams, C.A., Riley, S.P. et al. (2010) BpaB, a novel protein encoded by the Lyme disease spirochete's cp32 prophages, binds to erp operator 2 DNA. Nucleic Acids Res 38: 5443-5455.
8. Dasgupta, N., Wolfgang, M.C., Goodman, A.L. et al. (2003) A four-tiered transcriptional regulatory circuit controls flagellar biogenesis in Pseudomonas aeruginosa. Mol Microbiol 50: 809-824.
9. Dewhirst, F.E., Chen, T., Izard, J. et al. (2010) The human oral microbiome. J Bacteriol 192: 5002-5017.
10. Ellen, R.P. and Galimanas, V.B. (2005) Spirochetes at the forefront of periodontal infections. Periodontol 2000 38: 13-32.
11. Feng, J., Goss, T.J., Bender, R.A. and Ninfa, A.J. (1995) Repression of the Klebsiella aerogenes nac promoter. J Bacteriol 177: 5535-5538.
12. Frederick, J.R., Rogers, E.A. and Marconi, R.T. (2008) Analysis of a growth-phase-regulated two-component regulatory system in the periodontal pathogen Treponema denticola. J Bacteriol 190: 6162-6169.
13. Frederick, J.R., Sarkar, J., McDowell, J.V. and Marconi, R.T. (2011) Molecular signaling mechanisms of the periopathogen, Treponema denticola. J Dent Res 90: 1155-1163.
14. Galperin, M.Y. (2004) Bacterial signal transduction network in a genomic perspective. Environ Microbiol 6: 552-567.
15. Galperin, M.Y. (2006) Structural classification of bacterial response regulators: diversity of output domains and domain combinations. J Bacteriol 188: 4169-4182.
16. Galperin, M.Y. (2008) Telling bacteria: do not LytTR. Structure 16: 657-659.
17. Gao, R., Mack, T.R. and Stock, A.M. (2007) Bacterial response regulators: versatile regulatory strategies from common domains. Trends Biochem Sci 32: 225-234.
18. Garcia, B., Latasa, C., Solano, C., Garcia-del Portillo, F., Gamazo, C. and Lasa, I. (2004) Role of the GGDEF protein family in Salmonella cellulose biosynthesis and biofilm formation. Mol Microbiol 54: 264-277.
19. Garmyn, D., Augagneur, Y., Gal, L., Vivant, A.L. and Piveteau, P. (2012) Listeria monocytogenes differential transcriptome analysis reveals temperature-dependent Agr regulation and suggests overlaps with other regulons. PLoS ONE 7: e43154.
20. Gilles-Gonzalez, M.A. and Gonzalez, G. (2004) Signal transduction by heme-containing PAS-domain proteins. J Appl Physiol 96: 774-783.
21. Grant, C.E., Bailey, T.L. and Noble, W.S. (2011) FIMO: scanning for occurrences of a given motif. Bioinformatics 27: 1017-1018.
22. Guex, N. and Peitsch, M.C. (1997) SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 18: 2714-2723.
23. Hengge, R. (2009) Principles of c-di-GMP signalling in bacteria. Nat Rev Microbiol 7: 263-273.
24. Holm, L. and Rosenstrom, P. (2010) Dali server: conservation mapping in 3D. Nucleic Acids Res 38: W545-W549.
25. Irie, Y., Starkey, M., Edwards, A.N., Wozniak, D.J., Romeo, T. and Parsek, M.R. (2010) Pseudomonas aeruginosa biofilm matrix polysaccharide Psl is regulated transcriptionally by RpoS and post-transcriptionally by RsmA. Mol Microbiol 78: 158-172.
26. Kiupakis, A.K. and Reitzer, L. (2002) ArgR-independent induction and ArgR-dependent superinduction of the astCADBE operon in Escherichia coli. J Bacteriol 184: 2940-2950.
27. Koenig, R.L., Ray, J.L., Maleki, S.J., Smeltzer, M.S. and Hurlburt, B.K. (2004) Staphylococcus aureus AgrA binding to the RNAIII-agr regulatory region. J Bacteriol 186: 7549-7555.
28. Kostick, J.L., Szkotnicki, L.T., Rogers, E.A., Bocci, P., Raffaelli, N. and Marconi, R.T. (2011) The diguanylate cyclase, Rrp1, regulates critical steps in the enzootic cycle of the Lyme disease spirochetes. Mol Microbiol 81: 219-231.
29. Lang, B., Blot, N., Bouffartigues, E. et al. (2007) High-affinity DNA binding sites for H-NS provide a molecular basis for selective silencing within proteobacterial genomes. Nucleic Acids Res 35: 6330-6337.
30. Leech, A.J., Sprinkle, A., Wood, L., Wozniak, D.J. and Ohman, D.E. (2008) The NtrC family regulator AlgB, which controls alginate biosynthesis in mucoid Pseudomonas aeruginosa, binds directly to the algD promoter 10.1128/JB.01307-07. J Bacteriol 190: 581-589.
31. Lizewski, S.E., Schurr, J.R., Jackson, D.W., Frisk, A., Carterson, A.J. and Schurr, M.J. (2004) Identification of AlgR-regulated genes in Pseudomonas aeruginosa by use of microarray analysis. J Bacteriol 186: 5672-5684.
32. Lyristis, M., Bryant, A.E., Sloan, J. et al. (1994) Identification and molecular analysis of a locus that regulates extracellular toxin production in Clostridium perfringens. Mol Microbiol 12: 761-777.
33. Martin, M.J., Clare, S., Goulding, D. et al. (2013) The agr locus regulates virulence and colonization genes in Clostridium difficile 027. J Bacteriol 195: 3672-3681.
34. McDowell, J.V., Frederick, J., Stamm, L. and Marconi, R.T. (2007) Identification of the gene encoding the FhbB protein of Treponema denticola, a highly unique factor H-like protein 1 binding protein. Infect Immun 75: 1050-1054.
35. McDowell, J.V., Frederick, J., Miller, D.P. et al. (2011) Identification of the primary mechanism of complement evasion by the periodontal pathogen, Treponema denticola. Mol Oral Microbiol 26: 140-149.
36. Miller, D.P., Bell, J.K., McDowell, J.V. et al. (2012) Structure of factor H binding protein B (FhbB) of the periopathogen, Treponema denticola: insights into the progression of periodontal disease. J Biol Chem 287: 12715-12722.
37. Moglich, A., Ayers, R.A. and Moffat, K. (2009) Structure and signaling mechanism of Per-ARNT-Sim domains. Structure 17: 1282-1294.
38. Munch, R., Hiller, K., Grote, A. et al. (2005) Virtual Footprint and PRODORIC: an integrative framework for regulon prediction in prokaryotes. Bioinformatics 21: 4187-4189.
39. Nikolskaya, A.N. and Galperin, M.Y. (2002) A novel type of conserved DNA-binding domain in the transcriptional regulators of the AlgR/AgrA/LytR family. Nucleic Acids Res 30: 2453-2459.
40. Penaloza-Vazquez, A., Fakhr, M.K., Bailey, A.M. and Bender, C.L. (2004) AlgR functions in algC expression and virulence in Pseudomonas syringae pv. syringae. Microbiology 150: 2727-2737.
41. Porrua, O., Garcia-Gonzalez, V., Santero, E., Shingler, V. and Govantes, F. (2009) Activation and repression of a sigmaN-dependent promoter naturally lacking upstream activation sequences. Mol Microbiol 73: 419-433.
42. Ringner, M. and Krogh, M. (2005) Folding free energies of 5′-UTRs impact post-transcriptional regulation on a genomic scale in yeast. PLoS Comput Biol 1: e72.
43. Risoen, P.A., Havarstein, L.S., Diep, D.B. and Nes, I.F. (1998) Identification of the DNA-binding sites for two response regulators involved in control of bacteriocin synthesis in Lactobacillus plantarum C11. Mol Gen Genet 259: 224-232.
44. Rode, T.M., Langsrud, S., Holck, A. and Moretro, T. (2007) Different patterns of biofilm formation in Staphylococcus aureus under food-related stress conditions. Int J Food Microbiol 116: 372-383.
45. Samuels, D.S. (2011) Gene regulation in Borrelia burgdorferi. Annu Rev Microbiol 65: 479-499.
46. Sarkar, J., Frederick, J. and Marconi, R.T. (2010) The Hpk2-Rrp2 two-component regulatory system of Treponema denticola: a potential regulator of environmental and adaptive responses. Mol Oral Microbiol 25: 241-251.
47. Schuck, A., Diwa, A. and Belasco, J.G. (2009) RNase E autoregulates its synthesis in Escherichia coli by binding directly to a stem-loop in the rne 5′ untranslated region. Mol Microbiol 72: 470-478.
48. Seshadri, R., Myers, G.S.A., Tettelin, H. et al. (2004) Comparison of the genome of the oral pathogen Treponema denticola with other spirochete genomes. Proc Natl Acad Sci USA 101: 5646-5651.
49. Sidote, D.J., Barbieri, C.M., Wu, T. and Stock, A.M. (2008) Structure of the Staphylococcus aureus AgrA LytTR domain bound to DNA reveals a beta fold with an unusual mode of binding. Structure 16: 727-735.
50. Socransky, S., Haffajee, A., Cugini, M., Smith, C. and Kent, R.J. (1998) Microbial complexes in subgingival plaque. J Clin Periodontol 25: 134-144.
51. Sun, F., Li, C., Jeong, D., Sohn, C., He, C. and Bae, T. (2010) In the Staphylococcus aureus two-component system sae, the response regulator SaeR binds to a direct repeat sequence and DNA binding requires phosphorylation by the sensor kinase SaeS. J Bacteriol 192: 2111-2127.
52. Traber, K. and Novick, R. (2006) A slipped-mispairing mutation in AgrA of laboratory strains and clinical isolates results in delayed activation of agr and failure to translate delta- and alpha-haemolysins. Mol Microbiol 59: 1519-1530.
53. Zhang, H. and Marconi, R.T. (2005) Demonstration of cotranscription and 1-methyl-3-nitroso-nitroguanidine induction of a 30-gene operon of Borrelia burgdorferi: evidence that the 32-kilobase circular plasmids are prophages. J Bacteriol 187: 7985-7995.
54. Zuker, M. (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31: 3406-3415.