Analysis of promoter elements involved in the transcriptional initiation of RpoS-dependent Borrelia burgdorferi genes

Journal of Bacteriology

Volumn 186, Issue 21, 2004, Pages 7390-7402

  Eggers, Christian H ^a   Caimano, Melissa J ^a   Radolf, Justin D ^a  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; GREEN FLUORESCENT PROTEIN; LIPOPROTEIN; NUCLEOTIDE; SIGMA FACTOR; SIGMA FACTOR RPOS; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENE; BORRELIA BURGDORFERI; CATALYSIS; CONTROLLED STUDY; DBPBA GENE; ESCHERICHIA COLI; FLAB GENE; GENE EXPRESSION; GENETIC ANALYSIS; GENETIC COMPLEMENTATION; LYME DISEASE; MOLECULAR RECOGNITION; NONHUMAN; NUCLEOTIDE SEQUENCE; ORTHOLOGY; OSPC GENE; OSPE GENE; PRIORITY JOURNAL; PROMOTER REGION; REPORTER GENE; RPOS GENE; TEMPERATURE; TRANSCRIPTION INITIATION;

ANTIGENS, BACTERIAL; BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL PROTEINS; BASE SEQUENCE; BORRELIA BURGDORFERI; GENE EXPRESSION REGULATION, BACTERIAL; MOLECULAR SEQUENCE DATA; MUTATION; PROMOTER REGIONS (GENETICS); SIGMA FACTOR; TEMPERATURE; TRANSCRIPTION, GENETIC;

BACTERIA (MICROORGANISMS); BORRELIA; BORRELIA BURGDORFERI; ESCHERICHIA COLI; SPIROCHAETALES;

EID: 6044267456     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.186.21.7390-7402.2004     Document Type: Article

References (92)

1. Akins, D. R., K. W. Bourell, M. J. Caimano, M. V. Norgard, and J. D. Radolf. 1998. A new animal model for studying Lyme disease spirochetes in a mammalian host-adapted state. J. Clin. Investig. 101:2240-2250.
2. Akins, D. R., M. J. Caimano, X. Yang, F. Cerna, M. V. Norgard, and J. D. Radolf. 1999. Molecular and evolutionary analysis of Borrelia burgdorfen 297 circular plasmid-encoded lipoproteins with OspE- and OspF-like leader peptides. Infect. Immun. 67:1526-1532.
3. Akins, D. R., S. F. Porcella, T. G. Popova, D. Shevchenko, S. I. Baker, M. Li, M. V. Norgard, and J. D. Radolf. 1995. Evidence for in vivo but not in vitro expression of a Borrelia burgdorfen outer surface protein F (OspF) homolog. Mol. Microbiol. 18:507-520.
4. Alitalo, A., T. Meri, H. Lankinen, L Seppala, P. Lahdenne, P. S. Hefty, D. Akins, and S. Meri. 2002. Complement inhibitor factor H binding to Lyme disease spirochetes is mediated by inducible expression of multiple plasmid-encoded outer surface protein E paralogs. J. Immunol. 169:3847-3853.
5. Alverson, J., S. F. Bundle, C. D. Sohaskey, M. C. Lybecker, and D. S. Samuels. 2003. Transcriptional regulation of the ospAB and ospC promoters from Borrelia burgdorfen. Mol. Microbiol. 48:1665-1677.
6. Anguita, J., S. Samanta, B. Revilla, K. Suk, S. Das, S. W. Barthold, and E. Fikrig. 2000. Borrelia burgdorferi gene expression in vivo and spirochete pathogenicity. Infect. Immun. 68:1222-1230.
7. 70 subunit is responsible for the recognition of the 'extended-10' motif at promoters. EMBO J. 16:4034-4040.
8. s. Mol. Microbiol. 39:1153-1165.
9. Blattner, F. R. 1997. The complete genome sequence of Escherichia coli K12. Science 277:1453-1474.
10. Bohannon, D. E., N. Connell, J. Keener, A. Tormo, M. Espinosa-Urgel, M. M. Zambrano, and R. Kolter. 1991. Stationary-phase-inducible "gearbox" promoters: differential effects of katF mutations and role of sigma 70. J. Bacteriol. 173:4482-4492.
11. Boylan, J. A., J. E. Posey, and F. C. Gherardini. 2003. Borrelia oxidative stress response regulator, BosR: a distinctive Zn-dependent transcriptional activator. Proc. Natl. Acad. Sci. USA 100:11684-11689.
12. Caimano, M. J. C. H. Eggers, K. R. O. Hazlett, and J. D. Radolf. RpoS is not central to the general stress response in Borrelia burgdorferi but does control expression of one or more central virulence determinants. Infect. Immun., in press.
13. Caimano, M. J., X. Yang, T. G. Popova, M. L. Clawson, D. R. Akins, M. V. Norgard, and J. D. Radolf. 2000. Molecular and evolutionary characterization of the cp32/18 family of supercoiled plasmids in Borrelia burgdorferi 297. Infect. Immun. 68:1574-1586.
14. Campbell, E. A., O. Muzzin, M. Chlenov, J. L. Sun, C. A. Olson, O. Weinman, M. L. Trester-Zedlitz, and S. A. Darst. 2002. Structure of the bacterial RNA polymerase promoter specificity σ subunit. Mol. Cell 9:527-539.
15. Carroll, J. A., P. E. Stewart, P. Rosa, A. F. Elias, and C. F. Garon. 2003. An enhanced GFP reporter system to monitor gene expression in Borrelia burgdorferi. Microbiology 149:1819-1828.
16. Casjens, S., N. Palmer, R. van Vugt, W. M. Huang, B. Stevenson, P. Rosa, R. Lathigra, G. Sutton, J. Peterson, R. J. Dodson, D. Haft, E. Hickey, M. Gwinn, O. White, and C. M. Fraser. 2000. A bacterial genome in flux: the twelve linear and nine circular extrachromosomal DNAs in an infectious isolate of the Lyme disease spirochete Borrelia burgdorferi. Mol. Microbiol. 35:490-516.
17. Casjens, S., R. van Vugt, K. Tilly, P. A. Rosa, and B. Stevenson. 1997. Homology throughout the multiple 32-kilobase circular plasmids present in Lyme disease spirochetes. J. Bacteriol. 179:217-227.
18. Connell, N., Z. Ban, F. Moreno, and R. Kolter. 1987. An E. coli promoter induced by the cessation of growth. Mol. Microbiol. 1:195-201.
19. Dobrikova, E. Y., J. Bugrysheva, and F. C. Cabello. 2001. Two independent transcriptional units control the complex and simultaneous expression of the bmp paralogous chromosomal gene family in Borrelia burgdorferi. Mol. Microbiol. 39:370-378.
20. Eggers, C. H., M. J. Caimano, M. L. Clawson, W. G. Miller, D. S. Samuels, and J. D. Radolf. 2002. Identification of loci critical for replication and compatibility of a Borrelia burgdorferi cp32 plasmid and use of a cp32-based shuttle vector for the expression of fluorescent reporters in the Lyme disease spirochaete. Mol. Microbiol. 43:281-295.
21. Espinosa-Urgel, M., C. Chamizo, and A. Tormo. 1996. A consensus structure for sigma S-dependent promoters. Mol. Microbiol. 21:657-659.
22. Fingerle, V., S. Rauser, B. Hammer, O. Kahl, C. Heimerl, U. Schulte-Spechtel, L. Gern, and B. Wilske. 2002. Dynamics of dissemination and outer surface protein expression of different European Borrelia burgdorferi sensu lato strains in artificially infected bodes ricinus nymphs. J. Clin. Microbiol. 40:1456-1463.
23. Fraser, C. M., S. Casjens, W. M. Huang, G. G. Sutton, R. Clayton, R. Lathigra, O. White, K. A. Ketchum, R. Dodson, E. K. Hickey, M. Gwinn, B. Dougherty, J. F. Tomb, R. D. Fleischmann, D. Richardson, J. Peterson, A. R. Kerlavage, J. Quackenbush, S. Salzberg, M. Hanson, R. van Vugt, N. Palmer, M. D. Adams, J. Gocayne, J. Weidman, T. Utterback, L. Watthey, L. McDonald, P. Artiach, C. Bowman, S. Garland, C. Fujii, M. D. Cotton, K. Horst, K. Roberts, B. Hatch, H. O. Smith, and J. C. Venter. 1997. Genomic sequence of a Lyme disease spirochaete, Borrelia burgdorferi. Nature 390:580-586.
24. s RNA polymerase. Mol. Microbiol. 42:939-954.
25. Gattiker, A., E. Gasteiger, and A. Bairoch. 2002. ScanProsite: a reference implementation of a PROSITE scanning tool. Appl. Bioinformatics 1:107-108.
26. 70- like promoter. Microbiology 143:1681-1690.
27. 70 promoter. J. Bacteriol. 179:2289-2299.
28. Guzman, L. M., D. Belin, M. J. Carson, and J. Beckwith. 1995. Tight regulation, modulation, and high-level expression by vectors containing the arabinose pBAD promoter. J. Bacteriol. 177:4121-4130.
29. Hagman, K. E., P. Lahdenne, T. G. Popova, S. F. Porcella, D. R. Akins, J. D. Radolf, and M. V. Norgard. 1998. Decorin-binding protein of Borrelia burgdorferi is encoded within a two-gene operon and is protective in the murine model of Lyme borreliosis. Infect. Immun. 66:2674-2683.
30. Hales, L. M., and H. A. Shuman. 1999. The Legionella pneumophila rpoS gene is required for growth within Acanthamoeba castellanii. J. Bacteriol. 181:4879-4889.
31. Hawley, D. K., and W. R. McClure. 1983. Compilation and analysis of Escherichia coli promoter DNA sequences. Nucleic Acids Res. 11:2237-2255.
32. Hefty, P. S., S. E. Jolliff, M. J. Caimano, S. K. Wikel, and D. R. Akins. 2002. Changes in temporal and spatial patterns of outer surface lipoprotein expression generate population heterogeneity and antigenic diversity in the Lyme disease spirochete, Borrelia burgdorferi. Infect. Immun. 70:3468-3478.
33. Hefty, P. S., S. E. Jolliff, M. J. Caimano, S. K. Wikel, J. D. Radolf, and D. R. Akins. 2001. Regulation of OspE-related, OspF-related, and Elp lipoproteins of Borrelia burgdorferi strain 297 by mammalian host-specific signals. Infect. Immun. 69:3618-3627.
34. Hellwage, J., T. Meri, T. Heikkila, A. Alitalo, J. Panelius, P. Lahdenne, I. J. Seppala, and S. Meri. 2001. The complement regulator factor H binds to the surface protein OspE of Borrelia burgdorferi. J. Biol. Chem. 276:8427-8435.
35. Hengge-Aronis, R. 2000. The general stress response in Escherichia coli, p. 161-178. In G. Storz and R. Hengge-Aronis (ed.), Bacterial stress responses. ASM Press, Washington, D.C.
36. Hengge-Aronis, R. 2002. Recent insights into the general stress response regulatory network in Escherichia coli. J. Mol. Microbiol. Biotechnol. 4:341-346.
37. s-selective? Curr. Opin. Microbiol. 5:591-595.
38. Hengge-Aronis, R. 2003. Regulation of gene expression during entry into stationary phase, p. 1497-1512. In E. M. Neidhardt, R. Curtiss III, J. L. Ingraham, E. C. C. Lin, K. B. Low, B. Magasanik, W. S. Reznikoff, M. Riley, M. Schaechter, and H. E. Umbarger (ed.), Escherichia coli and Salmonella: cellular and molecular biology. ASM Press, Washington, D.C.
39. Hubner, A., X. Yang, D. M. Nolen, T. G. Popova, F. C. Cabello, and M. V. Norgard. 2001. Expression of Borrelia burgdorferi OspC and DbpA is controlled by a RpoN-RpoS regulatory pathway. Proc. Natl. Acad. Sci. USA 98:12724-12729.
40. Indest, K. J., R. Ramamoorthy, and M. T. Philipp. 2000. Transcriptional regulation in spirochetes. J. Mol. Microbiol. Biotechnol. 2:473-481.
41. Ishihama, A. 2000. Functional modulation of Escherichia coli RNA polymerase. Annu. Rev. Microbiol. 54:499-518.
42. Knight, S. W., and D. S. Samuels. 1999. Natural synthesis of a DNA-binding protein from the C-terminal domain of DNA gyrase A in Borrelia burgdorferi. EMBO J. 18:4875-4881.
43. Kobryn, K., D. Z. Naigamwalla, and G. Chaconas. 2000. Site-specific DNA binding and bending by the Borrelia burgdorferi Hbb protein. Mol. Microbiol. 37:145-155.
44. Kraiczy, P., C. Skerka, M. Kirschfink, V. Brade, and P. F. Zipfel. 2001. Immune evasion of Borrelia burgdorferi by acquisition of human complement regulators FHL-1/reconectin and Factor H. Eur. J. Immunol. 31:1674-1684.
45. s-RNA polymerase. J. Biol. Chem. 278:37160-37168.
46. Lane, R. S., J. Piesman, and W. Burgdorfer. 1991. Lyme borreliosis: relation of its causative agent to its vectors and hosts in North America and Europe. Annu. Rev. Entomol. 36:587-609.
47. Lange, R., M. Barth, and R. Hengge-Aronis. 1993. Complex transcriptional control of the sigma s-dependent stationary-phase-induced and osmotically regulated osmY (csi-5) gene suggests novel roles for Lrp, cyclic AMP (cAMP) receptor protein-cAMP complex, and integration host factor in the stationary-phase response of Escherichia coli. J. Bacteriol. 175:7910-7917.
48. 38 (rpoS) RNA polymerase promoter engagement via -10 region nucleotides. J. Biol. Chem. 276:30064-30071.
49. 38 (rpoS) RNA polymerase: amino acid clusters for DNA binding and isomerization. J. Biol. Chem. 277:47420-47427.
50. Lin, B., S. A. Short, M. Eskildsen, M. S. Klempner, and L. T. Hu. 2001. Functional testing of putative oligopeptide permease (Opp) proteins of Borrelia burgdorferi: a complementation model in opp(-) Escherichia coli. Biochim. Biophys. Acta 1499:222-231.
51. Liveris, D., V. Mulay, and I. Schwartz. 2004. Functional Properties of Borrelia burgdorferi recA. J. Bacteriol. 186:2275-2280.
52. Loewen, P. C. B. Hu, J. Strutinsky, and R. Sparling. 1998. Regulation in the rpoS regulon of Escherichia coli. Can. J. Microbiol. 44:707-717.
53. Lonetto, M., M. Gribskov, and C. A. Gross. 1992. The sigma 70 family: sequence conservation and evolutionary relationships. J. Bacteriol. 174:3843-3849.
54. Makinoshima, H., A. Nishimura, and A. Ishihama. 2002. Fractionation of Escherichia coli cell populations at different stages during growth transition to stationary phase. Mol. Microbiol. 43:269-279.
55. Marconi, R. T., D. S. Samuels, and C. F. Garon. 1993. Transcriptional analyses and mapping of the ospC gene in Lyme disease spirochetes. J. Bacteriol. 175:926-932.
56. Marconi, R. T., S. Y. Sung, C. A. Norton Hughes, and J. A. Carlyon. 1996. Molecular and evolutionary analyses of a variable series of genes in Borrelia burgdorferi that are related to ospE and ospF, constitute a gene family, and share a common upstream homology box. J. Bacteriol. 178:5615-5626.
57. McDowell, J. V., J. Wolfgang, E. Tran, M. S. Metts, D. Hamilton, and R. T. Marconi. 2003. Comprehensive analysis of the factor H binding capabilities of Borrelia species associated with Lyme disease: delineation of two distinct classes of factor H binding proteins. Infect. Immun. 71:3597-3602.
58. Metis, M. S., J. V. McDowell, M. Theisen, P. R. Hansen, and R. T. Marconi. 2003. Analysis of the OspE determinants involved in binding of factor H and OspE-targeting antibodies elicited during Borrelia burgdorferi infection in mice. Infect. Immun. 71:3587-3596.
59. Miller, J. H. 1992. A short course in bacterial genetics. A laboratory manual and handbook for Escherichia coli and related bacteria, p. 72-74. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
60. Miller, W. G., A. H. Bates, S. T. Horn, M. T. Brandie, M. R. Wachtel, and R. E. Mandrell. 2000. Detection on surfaces and in Caco-2 cells of Campylobacter jejuni cells transformed with new gfp, yfp, and cfp marker plasmids. Appl. Environ. Microbiol. 66:5426-5436.
61. Miller, W. G., and S. E. Lindow. 1997. An improved GFP cloning cassette designed for prokaryotic transcriptional fusions. Gene 191:149-153.
62. Morrissey, J. H. 1981. Silver stain for proteins in polyacrylamide gels: a modified procedure with enhanced uniform sensitivity. Analyt. Biochem. 117:307-310.
63. Ohnishi, J., J. Piesman, and A. M. Desilva. 2001. Antigenic and genetic heterogeneity of Borrelia burgdorferi populations transmitted by ticks. Proc. Natl. Acad. Sci. USA 98:670-675.
64. Pal, U., and E. Fikrig. 2003. Adaptation of Borrelia burgdorferi in the vector and vertebrate host. Microbes Infect. 5:659-666.
65. Porcella, S. F., C. A. Fitzpatrick, and J. L. Bono. 2000. Expression and immunological analysis of the plasmid-borne mlp genes of Borrelia burgdorferi B31. Infect. Immun. 68:4992-5001.
66. Putteet-Driver, A. D., J. Zhong, and A. G. Barbour. 2004. Transgenic expression of RecA of the spirochetes Borrelia burgdorferi and Borrelia hermsii in Escherichia coli revealed differences in DNA repair and recombination phenotypes. J. Bacteriol. 186:2266-2274.
67. Ramos-Gonzalez, M. I., and S. Molin. 1998. Cloning, sequencing, and phenotypic characterization of the rpoS gene from Pseudomonasputida KT2440. J. Bacteriol. 180:3421-3431.
68. Roberts, D. M., M. Caimano, J. McDowell, M. Theisen, A. Holm, E. Orff, D. Nelson, S. Wikel, J. Radolf, and R. T. Marconi. 2002. Environmental regulation and differential production of members of the Bdr protein family of Borrelia burgdorferi. Infect. Immun. 70:7033-7041.
69. Samuels, D. S. 1995. Electrotransformation of the spirochete Borrelia burgdorferi. Electrotransformation protocols for microorganisms. Methods Mol. Biol. 47:253-259.
70. Schellhorn, H. E., J. P. Audia, L. I. Wei, and L. Chang. 1998. Identification of conserved, RpoS-dependent stationary-phase genes of Escherichia coli. J. Bacteriol. 180:6283-6291.
71. Schwan, T. G. 2003. Temporal regulation of outer surface proteins of the Lyme-disease spirochaete Borrelia burgdorferi. Biochem. Soc. Trans. 31:108-112.
72. Schwan, T. G., J. Piesman, W. T. Golde, M. C. Dolan, and P. A. Rosa. 1995. Induction of an outer surface protein on Borrelia burgdorferi during tick feeding. Proc. Natl. Acad. Sci. USA 92:2909-2913.
73. Seshadri, R., and J. E. Samuel. 2001. Characterization of a stress-induced alternate sigma factor, RpoS, of Coxiella burnetii and its expression during the development cycle. Infect. Immun. 69:4874-4883.
74. Seshu, J., and J. T. Skare. 2000. The many faces of Borrelia burgdorferi. J. Mol. Microbiol. Biotechnol. 2:463-472.
75. Silhavy, T. J., M. L. Berman, and L. W. Enquist. 1984. Experiments with gene fusions, p. 107-112. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
76. Sohaskey, C. D., C. Arnold, and A. G. Barbour. 1997. Analysis of promoters in Borrelia burgdorferi by use of a transiently expressed reporter gene. J. Bacteriol. 179:6837-6842.
77. Sohaskey, C. D., W. R. Zuckert, and A. G. Barbour. 1999. The extended promoters for two outer membrane lipoprotein genes of Borrelia spp. uniquely include a T-rich region. Mol. Microbiol. 33:41-51.
78. Steere, A. C. 2001. Lyme disease. N. Engl. J. Med. 345:115-125.
79. Stevenson, B., J. L. Bono, T. G. Schwan, and P. A. Rosa. 1998. Borrelia burgdorferi Erp proteins are immunogenic in mammals infected by tick bite, and their synthesis is inducible in cultured bacteria. Infect. Immun. 66:2648-2654.
80. Stevenson, B., T. G. Schwan, and P. A. Rosa. 1995. Temperature-related differential expression of antigens in the Lyme disease spirochete, Borrelia burgdorferi. Infect. Immun. 63:4535-4539.
81. Stevenson, B., K. Tilly, and P. A. Rosa. 1996. A family of genes located on four separate 32-kilobase circular plasmids in Borrelia burgdorferi. J. Bacteriol. 178:3508-3516.
82. Tanaka, K., S. Kusano, N. Fujita, A. Ishihama, and H. Takahashi. 1995. Promoter determinants for Escherichia coli RNA polymerase holoenzyme containing sigma 38 (the rpoS gene product). Nucleic Acids Res. 23:827-834.
83. Tilly, K., S. Casjens, B. Stevenson, J. L. Bono, D. S. Samuels, D. Hogan, and P. A. Rosa. 1997. The Borrelia burgdorferi circular plasmid cp26: conservation of plasmid structure and targeted inactivation of the ospC gene. Mol. Microbiol. 25:361-373.
84. Tilly, K., J. Fuhrman, J. Campbell, and D. S. Samuels. 1996. Isolation of Borrelia burgdoreri genes encoding homologues of DNA-binding protein HU and ribosomal protein S20. Microbiology 142:2471-2479.
85. Volkert, M. R., L. I. Hajec, Z. Matyasevic, F. C. Fang, and R. Prince. 1994. Induction of the Escherichia coli aidB gene under oxygen-limiting conditions requires a functional rpoS (katF) gene. J. Bacteriol. 176:7638-7645.
86. Waldburger, C., T. Gardella, R. Wong, and M. M. Susskind. 1990. Changes in conserved region 2 of Escherichia coli sigma 70 affecting promoter recognition. J. Mol. Biol. 215:267-276.
87. Wang, X. G., J. M. Kidder, J. P. Scagliotti, M. S. Klempner, R. Noring, and L. T. Hu. 2004. Analysis of differences in the functional properties of the substrate binding proteins of the Borrelia burgdorferi oligopeptide permease (Opp) operon. J. Bacteriol. 186:51-60.
88. Wang, X. G., B. Lin, J. M. Kidder, S. Telford, and L. T. Hu. 2002. Effects of environmental changes on expression of the oligopeptide permease (opp) genes of Borrelia burgdorferi. J. Bacteriol. 184:6198-6206.
89. Yang, X., M. S. Goldberg, T. G. Popova, G. B. Scheeler, S. K. Wikel, K. E. Hagman, and M. V. Norgard. 2000. Interdependence of environmental factors influencing reciprocal patterns of gene expression in virulent Borrelia burgdorferi. Mol. Microbiol. 37:1470-1479.
90. Yang, X. F., S. M. Alani, and M. V. Norgard. 2003. The response regulator Rrp2 is essential for the expression of major membrane lipoproteins in Borrelia burgdorferi. Proc. Natl. Acad. Sci. USA 100:1100-1106.
91. Yang, X. F., A. Hubner, T. G. Popova, K. E. Hagman, and M. V. Norgard. 2003. Regulation of expression of the paralogous Mlp family in Borrelia burgdorferi. Infect. Immun. 71:5012-5020.
92. Yim, H. H., R. L. Brems, and M. Villarejo. 1994. Molecular characterization of the promoter of osmY, an RpoS-dependent gene. J. Bacteriol. 176:100-107.