Expression of the bmpB Gene of Borrelia burgdorferi is modulated by two distinct transcription termination events

Journal of Bacteriology

Volumn 187, Issue 8, 2005, Pages 2592-2600

  Ramamoorthy, Ramesh ^a,b   McClain, Natalie A ^a   Gautam, Aarti ^a   Scholl Meeker, Dorothy ^a  

^a TULANE NATIONAL PRIMATE RESEARCH CENTER   (United States)

^b Div of Bacteriol and Parasitology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENE PRODUCT; MESSENGER RNA; PROTEIN BMPA; PROTEIN BMPB; RHO FACTOR; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENE; BMPA GENE; BMPB GENE; BMPC GENE; BMPD GENE; BORRELIA BURGDORFERI; GENE; GENE EXPRESSION REGULATION; GENE LOCATION; LYME DISEASE; NONHUMAN; NORTHERN BLOTTING; OPERON; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; RNA ANALYSIS; TRANSCRIPTION TERMINATION;

BACTERIAL PROTEINS; BORRELIA BURGDORFERI GROUP; GENE EXPRESSION REGULATION, BACTERIAL; LIPOPROTEINS; PROMOTER REGIONS (GENETICS); RHO FACTOR; TRANSCRIPTION, GENETIC;

BORRELIA; BORRELIA BURGDORFERI;

EID: 16844366655     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.187.8.2592-2600.2005     Document Type: Article

References (47)

1. Akin, E., G. L. McHugh, R. A. Flavell, E. Fikrig, and A. C. Steere. 1999. The immunoglobulin (IgG) antibody response to OspA and OspB correlates with severe and prolonged Lyme arthritis and the IgG response to P35 correlates with mild and brief arthritis. Infect. Immun. 67:173-181.
2. Aron, L., M. Alekshun, L. Perlee, I. Schwartz, H. P. Godfrey, and F. C. Cabello. 1994. Cloning and DNA sequence analysis of bmpC, a gene encoding a potential membrane lipoprotein of Borrelia burgdorferi. FEMS Microbiol. Lett. 123:75-82.
3. Barthold, S. W., S. A. Levy, E. Fikrig, L. K. Bockenstedt, and A. L. Smith. 1995. Serologic responses of dogs naturally exposed to or vaccinated against Borrelia burgdorferi infection. J. Am. Vet. Med. Assoc. 207:1435-1440.
4. Bono, J. L., K. Tilly, B. Stevenson, D. Hogan, and P. Rosa. 1998. Oligopeptide permease in Borrelia burgdorferi: putative peptide-binding components encoded by both chromosomal and plasmid loci. Microbiology 144:1033-1044.
5. Brooks, C. S., P. S. Hefty, S. E. Jolliff, S., and D. R. Akins. 2003. Global analysis of Borrelia burgdorferi genes regulated by mammalian host-specific signals. Infect. Immun. 71:3371-3383.
6. Bundoc, V. G., and A. G. Barbour. 1989. Clonal polymorphisms of outer membrane protein OspB of Borrelia burgdorferi. Infect. Immun. 57:2733-2741.
7. 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.
8. Condon, C., C. Squires, and C. L. Squires. 1995. Control of rRNA transcription in Escherichia coli. Microbiol. Rev. 59:623-645.
9. Das, A. 1992. How the phage lambda N gene product suppresses transcription termination: communication of RNA polymerase with regulatory proteins mediated by signals in nascent RNA. J. Bacteriol. 174:6711-6716.
10. Das, A. 1993. Control of transcription termination by RNA-binding proteins. Annu. Rev. Biochem. 62:893-930.
11. 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.
12. Dressler, F., J. A. Whalen, B. N. Reinhardt, and A. C. Steere. 1993. Western blotting in the serodiagnosis of Lyme disease. J. Infect. Dis. 167:392-400.
13. Engstrom, S. M., E. Shoop, and R. C. Johnson. 1995. Immunoblot interpretation criteria for the serodiagnosis of early Lyme disease. J. Clin. Microbiol. 33:419-427.
14. Fawcett, P. T., C. Rose, K. M. Gibney, C. A. Chase, B. Kiehl, and R. A. Doughty. 1993. Detection of antibodies to the recombinant P39 protein of Borrelia burgdorferi using enzyme immunoassay and immunoblotting. J. Rheumatol. 20:734-738.
15. 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. Whattey, 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. Genome sequence of a Lyme disease spirochaete, Borrelia burgdorferi. Nature 390:580-586.
16. Gorbacheva, V. Y., H. P. Godfrey, and F. C. Cabello. 2000. Analysis of the bmp gene family in Borrelia burgdorferi sensu lato. J. Bacteriol. 182:2037-2042.
17. Hagman, K. E., P. Lahdenne, T. G. Popova, S. F. Porcella, D. R. Akins, J. D. Radolf, and M. V. Norgard. 1998. Decorin-binding proteins 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.
18. Hauser, U., G. Lehnert, R. Lobentanzer, and B. Wilske. 1997. Interpretation criteria for standardized Western blots for three European species of Borrelia burgdorferi sensu lato. J. Clin. Microbiol. 35:1433-1444.
19. Howe, T. R., F. W. LaQuier, and A. G. Barbour. 1986. Organization of genes encoding two outer membrane proteins of the Lyme disease agent Borrelia burgdorferi within a single transcriptional unit. Infect. Immun. 54:207-212.
20. 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 pathway. Proc. Natl. Acad. Sci. USA 98:12724-12729.
21. Liang, F. T., F. K. Nelson, and E. Fikrig. 2002. Molecular adaptation of Borrelia burgdorferi in the murine host. J. Exp. Med. 196:275-280.
22. Liang, F. T., M. J. Caimano, J. D. Radolf, and E. Fikrig. 2004. Borrelia burgdorferi outer surface protein (osp) B expression independent of ospA. Microb. Pathog. 37:35-40.
23. Magnarelli, L. A., J. W. Ijdo, S. J. Padula, R. A. Flavell, and E. Fikrig. 2000. Serologic diagnosis of Lyme borreliosis by using enzyme-linked immunosorbent assays with recombinant antigens. J. Clin. Microbiol. 38:1735-1739.
24. Magnarelli, L. A., J. W. Ijdo, A. E. Van Andel, C. Wu, S. J. Padula, and E. Fikrig. 2000. Serologic confirmation of Ehrlichia equi and Borrelia burgdorferi infections in horses from the northeastern United States. J. Am. Vet. Med. Assoc. 217:1045-1050.
25. Magnarelli, L. A., S. A. Levy, J. W. Ijdo, C. Wu, S. J. Padula, E., and Fikrig. 2001. Reactivity of dog sera to whole-cell or recombinant antigens of Borrelia burgdorferi by ELISA and immunoblot analysis. J. Med. Microbiol. 50:889-895.
26. Nichols, T. L., C. A. Whitehouse, and F. E. Austin. 2000. Transcriptional analysis of a superoxide dismutase gene of Borrelia burgdorferi. FEMS Microbiol. Lett. 183:37-42.
27. Nudler, E., and M. E. Gottesman. 2002. Transcription termination and antitermination in E. coli. Genes Cells 7:755-768.
28. Oh, S. H., Y. H. Song, D. H. Yoo, S. Y. Kim, and H. Lee. 1993. Distribution of Borrelia burgdorferi specific antibody among patients with juvenile rheumatoid arthritis in Korea. J. Korean Med. Sci. 8:405-412.
29. Oksi, J., J. Uksila, M. Marjamaki, J. Nikoskelainen, and M. K. Viljanen. 1995. Antibodies against whole sonicated Borrelia burgdorferi spirochetes, 41-kilodalton flagellin, and P39 protein in patients with PCR- or culture-proven late Lyme borreliosis. J. Clin. Microbiol. 33:2260-2264.
30. Pachner, A. R., D. Dail, L. Li, L. Gurey, S. Feng, E. Hodzic, and S. Barthold. 2002. Humoral immune response associated with Lyme borreliosis in non-human primates: analysis by immunoblotting and enzyme-linked immunosorbent assay with sonicates or recombinant proteins. Clin. Diagn. Lab. Immunol. 9:1348-1355.
31. Piesman, J., T. N. Mather, R. Sinsky, and A. Spielman. 1987. Duration of tick attachment and Borrelia burgdorferi transmission. J. Clin. Microbiol. 25:557-558.
32. Pollack, R. J., S. R. Telford III, and A. Spielman. 1993. Standardization of medium for culturing Lyme disease spirochetes. J. Clin. Microbiol. 31:1251-1255.
33. Ramamoorthy, R., L. Povinelli, and M. T. Philipp. 1996. Molecular characterization, genomic arrangement, and expression of bmpD, a new member of the bmp class of genes encoding membrane proteins of Borrelia burgdorferi. Infect. Immun. 64:1259-1264.
34. Ramamoorthy, R., and M. T. Philipp. 1998. Differential expression of Borrelia burgdorferi proteins during growth in vitro. Infect. Immun. 66:5119-5124.
35. Revel, A. T., A. M. Talaat, and M. V. Norgard. 2002. DNA microarray analysis of differential gene expression in Borrelia burgdorferi, the Lyme disease spirochete. Proc. Natl. Acad. Sci. USA 99:1562-1567.
36. Roberts, J. W. 1993. RNA and protein elements of E. coli and lambda transcription antitermination complexes. Cell 72:653-655.
37. Roessler, D., U. Hauser, and B. Wilske. 1997. Heterogeneity of BmpA (P39) among European isolates of Borrelia burgdorferi sensu lato and the influence of interspecies variability on serodiagnosis. J. Clin. Microbiol. 35:2752-2758.
38. Samuels, D. S. 1995. Electrotransformation of the spirochete Borrelia burgdorferi. Methods Mol. Biol. 47:253-259.
39. Sanger, F., S. Nicklen, and A. R. Coulson. 1977. DNA sequencing with chain-terminating inhibitors. Proc. Natl. Sci. Acad. USA 74:5463-5467.
40. Sarkatova, M., E. Dobrikova, and F. C. Cabello. 2000. Development of an extrachromosomal cloning vector system for use in Borrelia burgdorferi. Proc. Natl. Acad. Sci. USA 97:4850-4855.
41. Schouls, L. M., H. G. J. van der Heide, and J. D. A. van Embden. 1991. Characterization of the 35-kilodalton Treponema pallidum subsp. pallidum recombinant lipoprotein TmpC and antibody response to lipidated and non-lipidated T. pallidum antigens. Infect. Immun. 59:3536-3546.
42. Simpson, W. J., M. E. Schrumpf, and T. G. Schwan. 1990. Reactivity of human Lyme borreliosis sera with a 39-kilodalton antigen specific to Borrelia burgdorferi. J. Clin. Microbiol. 28:1329-1337.
43. Simpson, W. J., W. Cieplak, M. E. Schrumpf, A. G. Barbour, and T. G. Schwan. 1994. Nucleotide sequence and analysis of the gene in Borrelia burgdorferi encoding the immunogenic P39 antigen. FEMS Microbiol. Lett. 119:381-388.
44. Stewart, P. E., R. Thalken, J. L. Bono, and P. Rosa. 2001. Isolation of circular plasmid region sufficient for autonomous replication and transformation of infectious Borrelia burgdorferi. Mol. Microbiol. 39:714-721.
45. Torres, M., C. Condon, J.-M, Balada, C. Squires, and C. L. Squires. 2001. Ribosomal protein S4 is a transcription factor with properties remarkably similar to NusA, a protein involved in both non-ribosomal and ribosomal RNA antitermination. EMBO J. 20:3811-3820.
46. Wilske, B., C. Habermann, V. Fingerle, B. Hillenbrand, S. Jauris-Heipke, G. Lehnert, I. Pradel, D. Rossler, and U. Schulte-Spechtel. 1999. An improved recombinant IgG immunoblot for serodiagnosis of Lyme borreliosis. Med. Microbiol. Immunol. 188:139-144.
47. Zuker, M., and P. Stiegler. 1981. Optimal computer folding of large RNA sequences using thermodynamics and auxiliary information. Nucleic Acids Res. 9:133-148.