BosR (BB0647) controls the RpoN-RpoS regulatory pathway and virulence expression in Borrelia burgdorferi by a novel DNA-binding mechanism

PLoS Pathogens

Volumn 7, Issue 2, 2011, Pages

  Ouyang, Zhiming ^a   Deka, Ranjit K ^a   Norgard, Michael V ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; BOSR PROTEIN; FERRIC UPTAKE REGULATOR; LIPOPROTEIN; RECOMBINANT PROTEIN; REGULATOR PROTEIN; SIGMA FACTOR RPON; SIGMA FACTOR RPOS; UNCLASSIFIED DRUG; BACTERIAL DNA; DNA BINDING PROTEIN; PEROXIDE REPRESSOR PROTEINS; REPRESSOR PROTEIN; SIGMA FACTOR; SIGMA FACTOR KATF PROTEIN, BACTERIA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL GENE; BACTERIAL MUTATION; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BORRELIA BURGDORFERI; CONTROLLED STUDY; GENE CONTROL; IN VITRO STUDY; MOUSE; NONHUMAN; NUCLEOTIDE BINDING SITE; NUCLEOTIDE SEQUENCE; PROTEIN DNA BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM; ANIMAL; CHEMISTRY; GENE EXPRESSION REGULATION; GENETICS; ISOLATION AND PURIFICATION; LYME DISEASE; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; PATHOGENICITY; PATHOLOGY; PHYSIOLOGY; PROTEIN BINDING; REGULATOR GENE; SIGNAL TRANSDUCTION; TRANSGENIC ORGANISM; VIRULENCE;

BORRELIA BURGDORFERI; MAMMALIA;

ANIMALS; BACTERIAL PROTEINS; BASE SEQUENCE; BORRELIA BURGDORFERI; DNA, BACTERIAL; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; GENES, REGULATOR; LYME DISEASE; MICE; MOLECULAR SEQUENCE DATA; ORGANISMS, GENETICALLY MODIFIED; PROTEIN BINDING; RECOMBINANT PROTEINS; REPRESSOR PROTEINS; RNA POLYMERASE SIGMA 54; SIGMA FACTOR; SIGNAL TRANSDUCTION; VIRULENCE;

EID: 79952237303     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1001272     Document Type: Article

References (68)

1. Gruber TM, Gross CA, (2003) Multiple sigma subunits and the partitioning of bacterial transcription space. Annu Rev Microbiol 57: 441-466.
2. Ghosh T, Bose D, Zhang X, (2010) Mechanisms for activating bacterial RNA polymerase. FEMS Microbiol Rev 34: 611-627.
3. Rappas M, Bose D, Zhang X, (2007) Bacterial enhancer-binding proteins: unlocking sigma54-dependent gene transcription. Curr Opin Struct Biol 17: 110-116.
4. Wigneshweraraj S, Bose D, Burrows PC, Joly N, Schumacher J, et al. (2008) Modus operandi of the bacterial RNA polymerase containing the sigma54 promoter-specificity factor. Mol Microbiol 68: 538-546.
5. Burgdorfer W, Barbour AG, Hayes SF, Benach JL, Grunwaldt E, et al. (1982) Lyme disease-a tick-borne spirochetosis? Science 216: 1317-1319.
6. Steere AC, Grodzicki RL, Kornblatt AN, Craft JE, Barbour AG, et al. (1983) The spirochetal etiology of Lyme disease. N Engl J Med 308: 733-740.
7. Fraser CM, Casjens S, Huang WM, Sutton GG, Clayton R, et al. (1997) Genomic sequence of a Lyme disease spirochaete, Borrelia burgdorferi. Nature 390: 580-586.
8. Burtnick MN, Downey JS, Brett PJ, Boylan JA, Frye JG, et al. (2007) Insights into the complex regulation of rpoS in Borrelia burgdorferi. Mol Microbiol 65: 277-293.
9. Hubner A, Yang X, Nolen DM, Popova TG, Cabello FC, et al. (2001) Expression of Borrelia burgdorferi OspC and DbpA is controlled by a RpoN-RpoS regulatory pathway. Proc Natl Acad Sci U S A 98: 12724-12729.
10. Ouyang Z, Blevins JS, Norgard MV, (2008) Transcriptional interplay among the regulators Rrp2, RpoN and RpoS in Borrelia burgdorferi. Microbiology 154: 2641-2658.
11. Smith AH, Blevins JS, Bachlani GN, Yang XF, Norgard MV, (2007) Evidence that RpoS (sigmaS) in Borrelia burgdorferi is controlled directly by RpoN (sigma54/sigmaN). J Bacteriol 189: 2139-2144.
12. Brooks CS, Hefty PS, Jolliff SE, Akins DR, (2003) Global analysis of Borrelia burgdorferi genes regulated by mammalian host-specific signals. Infect Immun 71: 3371-3383.
13. Caimano MJ, Iyer R, Eggers CH, Gonzalez C, Morton EA, et al. (2007) Analysis of the RpoS regulon in Borrelia burgdorferi in response to mammalian host signals provides insight into RpoS function during the enzootic cycle. Mol Microbiol 65: 1193-1217.
14. Schwan TG, Piesman J, Golde WT, Dolan MC, Rosa PA, (1995) Induction of an outer surface protein on Borrelia burgdorferi during tick feeding. Proc Natl Acad Sci U S A 92: 2909-2913.
15. Yang X, Goldberg MS, Popova TG, Schoeler GB, Wikel SK, et al. (2000) Interdependence of environmental factors influencing reciprocal patterns of gene expression in virulent Borrelia burgdorferi. Mol Microbiol 37: 1470-1479.
16. Fisher MA, Grimm D, Henion AK, Elias AF, Stewart PE, et al. (2005) Borrelia burgdorferi sigma54 is required for mammalian infection and vector transmission but not for tick colonization. Proc Natl Acad Sci U S A 102: 5162-5167.
17. Yang XF, Alani SM, Norgard MV, (2003) The response regulator Rrp2 is essential for the expression of major membrane lipoproteins in Borrelia burgdorferi. Proc Natl Acad Sci U S A 100: 11001-11006.
18. Xu H, Caimano MJ, Lin T, He M, Radolf JD, et al. (2010) Role of acetyl-phosphate in activation of the Rrp2-RpoN-RpoS pathway in Borrelia burgdorferi. PLoS Pathog 6 (9): e1001104.
19. Grimm D, Tilly K, Byram R, Stewart PE, Krum JG, et al. (2004) Outer-surface protein C of the Lyme disease spirochete: a protein induced in ticks for infection of mammals. Proc Natl Acad Sci U S A 101: 3142-3147.
20. Pal U, Yang X, Chen M, Bockenstedt LK, Anderson JF, et al. (2004) OspC facilitates Borrelia burgdorferi invasion of Ixodes scapularis salivary glands. J Clin Invest 113: 220-230.
21. Blevins JS, Hagman KE, Norgard MV, (2008) Assessment of decorin-binding protein A to the infectivity of Borrelia burgdorferi in the murine models of needle and tick infection. BMC Microbiol 8: 82.
22. Shi Y, Xu Q, McShan K, Liang FT, (2008) Both decorin-binding proteins A and B are critical for overall virulence of Borrelia burgdorferi. Infect Immun 76: 1239-1246.
23. Weening EH, Parveen N, Trzeciakowski JP, Leong JM, Hook M, et al. (2008) Borrelia burgdorferi lacking DbpBA exhibits an early survival defect during experimental infection. Infect Immun 76: 5694-5705.
24. Blevins JS, Xu H, He M, Norgard MV, Reitzer L, et al. (2009) Rrp2, a sigma54-dependent transcriptional activator of Borrelia burgdorferi, activates rpoS in an enhancer-independent manner. J Bacteriol 191: 2902-2905.
25. Lybecker MC, Samuels DS, (2007) Temperature-induced regulation of RpoS by a small RNA in Borrelia burgdorferi. Mol Microbiol 64: 1075-1089.
26. Lybecker MC, Abel CA, Feig AL, Samuels DS, (2010) Identification and function of the RNA chaperone Hfq in the Lyme disease spirochete Borrelia burgdorferi. Mol Microbiol 78: 622-635.
27. Ouyang Z, He M, Oman T, Yang XF, Norgard MV, (2009) A manganese transporter, BB0219 (BmtA), is required for virulence by the Lyme disease spirochete, Borrelia burgdorferi. Proc Natl Acad Sci U S A 106: 3449-3454.
28. Katona LI, Tokarz R, Kuhlow CJ, Benach J, Benach JL, (2004) The fur homologue in Borrelia burgdorferi. J Bacteriol 186: 6443-6456.
29. Boylan JA, Posey JE, Gherardini FC, (2003) Borrelia oxidative stress response regulator, BosR: a distinctive Zn-dependent transcriptional activator. Proc Natl Acad Sci U S A 100: 11684-11689.
30. Carpenter BM, Whitmire JM, Merrell DS, (2009) This is not your mother's repressor: the complex role of fur in pathogenesis. Infect Immun 77: 2590-2601.
31. Posey JE, Gherardini FC, (2000) Lack of a role for iron in the Lyme disease pathogen. Science 288: 1651-1653.
32. Hyde JA, Shaw DK, Smith R Iii, Trzeciakowski JP, Skare JT, (2009) The BosR regulatory protein of Borrelia burgdorferi interfaces with the RpoS regulatory pathway and modulates both the oxidative stress response and pathogenic properties of the Lyme disease spirochete. Mol Microbiol 74: 1344-1355.
33. Hyde JA, Shaw DK, Smith R 3rd, Trzeciakowski JP, Skare JT, (2010) Characterization of a conditional bosR mutant in Borrelia burgdorferi. Infect Immun 78: 265-274.
34. Ouyang Z, Kumar M, Kariu T, Haq S, Goldberg M, et al. (2009) BosR (BB0647) governs virulence expression in Borrelia burgdorferi. Mol Microbiol 74: 1331-1343.
35. Samuels DS, Radolf JD, (2009) Who is the BosR around here anyway? Mol Microbiol 74: 1295-1299.
36. Dmitriev AV, McDowell EJ, Chaussee MS, (2008) Inter- and intraserotypic variation in the Streptococcus pyogenes Rgg regulon. FEMS Microbiol Lett 284: 43-51.
37. Luo F, Lizano S, Bessen DE, (2008) Heterogeneity in the polarity of Nra regulatory effects on streptococcal pilus gene transcription and virulence. Infect Immun 76: 2490-2497.
38. Ribardo DA, McIver KS, (2006) Defining the Mga regulon: Comparative transcriptome analysis reveals both direct and indirect regulation by Mga in the group A streptococcus. Mol Microbiol 62: 491-508.
39. Ojaimi C, Mulay V, Liveris D, Iyer R, Schwartz I, (2005) Comparative transcriptional profiling of Borrelia burgdorferi clinical isolates differing in capacities for hematogenous dissemination. Infect Immun 73: 6791-6802.
40. Wang G, van Dam AP, Schwartz I, Dankert J, (1999) Molecular typing of Borrelia burgdorferi sensu lato: taxonomic, epidemiological, and clinical implications. Clin Microbiol Rev 12: 633-653.
41. Labandeira-Rey M, Skare JT, (2001) Decreased infectivity in Borrelia burgdorferi strain B31 is associated with loss of linear plasmid 25 or 28-1. Infect Immun 69: 446-455.
42. Purser JE, Norris SJ, (2000) Correlation between plasmid content and infectivity in Borrelia burgdorferi. Proc Natl Acad Sci U S A 97: 13865-13870.
43. Akins DR, Bourell KW, Caimano MJ, Norgard MV, Radolf JD, (1998) A new animal model for studying Lyme disease spirochetes in a mammalian host-adapted state. J Clin Invest 101: 2240-2250.
44. Barthold SW, de Souza MS, Janotka JL, Smith AL, Persing DH, (1993) Chronic Lyme borreliosis in the laboratory mouse. Am J Pathol 143: 959-971.
45. Blevins JS, Revel AT, Smith AH, Bachlani GN, Norgard MV, (2007) Adaptation of a luciferase gene reporter and lac expression system to Borrelia burgdorferi. Appl Environ Microbiol 73: 1501-1513.
46. Eggers CH, Caimano MJ, Radolf JD, (2004) Analysis of promoter elements involved in the transcriptional initiation of RpoS-dependent Borrelia burgdorferi genes. J Bacteriol 186: 7390-7402.
47. Ouyang Z, Haq S, Norgard MV, (2010) Analysis of the dbpBA upstream regulatory region controlled by RpoS in Borrelia burgdorferi. J Bacteriol 192: 1965-1974.
48. Yang XF, Lybecker MC, Pal U, Alani SM, Blevins J, et al. (2005) Analysis of the ospC regulatory element controlled by the RpoN-RpoS regulatory pathway in Borrelia burgdorferi. J Bacteriol 187: 4822-4829.
49. Desrosiers DC, Sun YC, Zaidi AA, Eggers CH, Cox DL, et al. (2007) The general transition metal (Tro) and Zn2+ (Znu) transporters in Treponema pallidum: analysis of metal specificities and expression profiles. Mol Microbiol 65: 137-152.
50. Althaus EW, Outten CE, Olson KE, Cao H, O'Halloran TV, (1999) The ferric uptake regulation (Fur) repressor is a zinc metalloprotein. Biochemistry 38: 6559-6569.
51. Traore DA, El Ghazouani A, Ilango S, Dupuy J, Jacquamet L, et al. (2006) Crystal structure of the apo-PerR-Zn protein from Bacillus subtilis. Mol Microbiol 61: 1211-1219.
52. Sheikh MA, Taylor GL, (2009) Crystal structure of the Vibrio cholerae ferric uptake regulator (Fur) reveals insights into metal co-ordination. Mol Microbiol 72: 1208-1220.
53. Escolar L, Perez-Martin J, de Lorenzo V, (1999) Opening the iron box: transcriptional metalloregulation by the Fur protein. J Bacteriol 181: 6223-6229.
54. Joslin SN, Hendrixson DR, (2008) Analysis of the Campylobacter jejuni FlgR response regulator suggests integration of diverse mechanisms to activate an NtrC-like protein. J Bacteriol 190: 2422-2433.
55. Li X, Pal U, Ramamoorthi N, Liu X, Desrosiers DC, et al. (2007) The Lyme disease agent Borrelia burgdorferi requires BB0690, a Dps homologue, to persist within ticks. Mol Microbiol 63: 694-710.
56. Mitra R, Das HK, Dixit A, (2005) Identification of a positive transcription regulatory element within the coding region of the nifLA operon in Azotobacter vinelandii. Appl Environ Microbiol 71: 3716-3724.
57. Shimada T, Ishihama A, Busby SJ, Grainger DC, (2008) The Escherichia coli RutR transcription factor binds at targets within genes as well as intergenic regions. Nucleic Acids Res 36: 3950-3955.
58. Baichoo N, Helmann JD, (2002) Recognition of DNA by Fur: a reinterpretation of the Fur box consensus sequence. J Bacteriol 184: 5826-5832.
59. Friedman YE, O'Brian MR, (2003) A novel DNA-binding site for the ferric uptake regulator (Fur) protein from Bradyrhizobium japonicum. J Biol Chem 278: 38395-38401.
60. Lee JW, Helmann JD, (2007) Functional specialization within the Fur family of metalloregulators. Biometals 20: 485-499.
61. Goosen N, van de Putte P, (1995) The regulation of transcription initiation by integration host factor. Mol Microbiol 16: 1-7.
62. Kiupakis AK, Reitzer L, (2002) ArgR-independent induction and ArgR-dependent superinduction of the astCADBE operon in Escherichia coli. J Bacteriol 184: 2940-2950.
63. Lu CD, Abdelal AT, (1999) Role of ArgR in activation of the ast operon, encoding enzymes of the arginine succinyltransferase pathway in Salmonella typhimurium. J Bacteriol 181: 1934-1938.
64. Gao M, D'Haeze W, De Rycke R, Holsters M, (2001) Dual control of the nodA operon of Azorhizobium caulinodans ORS571 by a nod box and a NifA-sigma54-type promoter. Mol Genet Genomics 265: 1050-1059.
65. Hughes CA, Kodner CB, Johnson RC, (1992) DNA analysis of Borrelia burgdorferi NCH-1, the first northcentral U.S. human Lyme disease isolate. J Clin Microbiol 30: 698-703.
66. Pollack RJ, Telford SR 3rd, Spielman A, (1993) Standardization of medium for culturing Lyme disease spirochetes. J Clin Microbiol 31: 1251-1255.
67. Samuels DS, (1995) Electrotransformation of the spirochete Borrelia burgdorferi. Methods Mol Biol 47: 253-259.
68. Revel AT, Blevins JS, Almazan C, Neil L, Kocan KM, et al. (2005) bptA (bbe16) is essential for the persistence of the Lyme disease spirochete, Borrelia burgdorferi, in its natural tick vector. Proc Natl Acad Sci U S A 102: 6972-6977.