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

Journal of Bacteriology

Volumn 187, Issue 23, 2005, Pages 7985-7995

  Zhang, Hongming ^a   Marconi, Richard T ^a,b  

^a VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENT FACTOR H; METHYLNITRONITROSOGUANIDINE; OUTER MEMBRANE PROTEIN; PROTEIN OSPE; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL GENOME; BACTERIOPHAGE; BORRELIA BURGDORFERI; BORRELIA INFECTION; CONTROLLED STUDY; DNA ISOLATION; IMMUNOBLOTTING; MOUSE; NONHUMAN; OPEN READING FRAME; OPERON; PLASMID; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROMOTER REGION; PROPHAGE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ISOLATION; SEQUENCE HOMOLOGY; TRANSCRIPTION INITIATION SITE;

ANIMALS; BACTERIOPHAGES; BASE SEQUENCE; BORRELIA BURGDORFERI; GENOME, BACTERIAL; LYME DISEASE; METHYLNITRONITROSOGUANIDINE; MICE; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; OPERON; PLASMIDS; PROMOTER REGIONS (GENETICS); TRANSCRIPTION, GENETIC; UP-REGULATION; VIRAL PROTEINS; VIRULENCE;

ANIMALIA; BACTERIA (MICROORGANISMS); BORRELIA; BORRELIA BURGDORFERI;

EID: 28044434613     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.187.23.7985-7995.2005     Document Type: Article

References (56)

1. Acheson, D. W., J. Reidl, X. Zhang, G. T. Keusch, J. J. Mekalanos, and M. K. Waldor. 1998. In vivo transduction with Shiga toxin 1-encoding phage. Infect. Immun. 66:4496-4498.
2. Akins, D. R., K. W. Bourell, M. J. Caimano, M. V. Norgard, and J. R. Radolf. 1998. A new animal model for studying Lyme disease spirochetes in a mammalian host-adapted state. J. Clin. Investig. 101:2240-2250.
3. Alitalo, A., T. Men, L. Rämö, T. S. Jokiranta, T. Heikkilä, I. J. T. Seppälä, J. Oksi, M. Viljanen, and S. Meri. 2001. Complement evasion by Borrelia burgdoiferi: serum-resistant strains promote C3b inactivation. Infect. Immun. 69:3685-3691.
4. Alitalo, A., M. T., H. Lankinen, I. Seppälä, 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. Anderton, J., R. Tokarz, C. Thill, C. Kuhlow, C. Brooks, D. Akins, L. Katona, and J. Benach. 2004. Whole-genome DNA array analysis of the response of Borrelia burgdorferi to a bactericidal monoclonal antibody. Infect. Immun. 72:2035-2044.
6. Harbour, A. G., and C. F. Garon. 1987. Linear plasmids of the bacterium Borrelia burgdorferi have covalently closed ends. Science 237:409-411.
7. Barbour, A. G., and S. F. Hayes. 1986. Biology of Borrelia species. Microbiol. Rev. 50:381-400.
8. Bazinet, C., J. Benbasat, J. King, J. M. Carazo, and J. L. Carrascosa. 1988. Purification and organization of the gene 1 portal protein required for phage P22 DNA packaging. Biochemistry 27:1849-1856.
9. Brooks, C. S., P. S. Hefty, S. E. Joliff, and D. R. Akins. 2003. Global analysis of Borrelia burgdorferi genes regulated by mammalian host-specific signals. Infect. Immun. 71:3371-3383.
10. Bruggemann, H., S. Baumer, W. F. Fricke, A. Wiezer, H. Liesegang, I. Decker, C. Herzberg, R. Martinez-Arias, R. Merkl, A. Henne, and G. Gottschalk. 2003. The genome sequence of Clostridium tetani, the causative agent of tetanus disease. Proc. Natl. Acad. Sci. USA 100:1316-1321.
11. Brussow, H., C. Canchaya, and W.-D. Hardt. 2004. Phages and the evolution of bacterial pathogens: from genomic rearrangements to lysogenic conversion. Microbiol. Mol. Biol. Rev. 68:560-602.
12. 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.
13. Canchaya, C, G. Fournous, and H. Brussow. 2004. The impact of prophages on bacterial chromosomes. Mol. Microbiol. 53:9-18.
14. Carlyon, J. A., C. LaVoie, S. Y. Sung, and R. T. Marconi. 1998. Analysis of the organization of multi-copy linear and circular plasmid carried open reading frames in Borrelia burgdorferi sensu lato isolates. Infect. Immun. 66:1149-1158.
15. 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.
16. Casjens, S., R. van Vugt, K. Tilly, P. A. Rosa, and B. Stevenson. 1997. Homology throughout the multiple 32-kilobase circular plasmids in Lyme Disease spirochetes. J. Bacteriol. 179:217-227.
17. Damman, C. J., C. H. Eggers, D. S. Samuels, and D. B. Oliver. 2000. Characterization of Borrelia burgdorferi BlyA and BlyB proteins: a prophage-encoded holin-like system. J. Bacteriol. 182:6791-6797.
18. Earnhart, C. G., E. L. Buckles, J. S. Dumler, and R. T. Marconi. 2005. Demonstration of OspC type diversity in invasive human Lyme disease isolates and identification of previously uncharacterized epitopes that define the specificity of the OspC antibody response. Infect. Immun. 73:7869-7877.
19. Eggers, C., and D. S. Samuels. 1999. Molecular evidence for a new bacteriophage of Borrelia burgdorferi. J. Bacteriol. 181:7308-7313.
20. Eggers, C. H., S. Casjens, S. F. Hayes, C. F. Garon, C. J. Damman, D. B. Oliver, and D. S. Samuels. 2000. Bacteriophages of spirochetes. J. Mol. Microbiol. Biotechnol. 4:365-373.
21. Eggers, C. H., B. J. Kimmel, J. L. Bono, A. F. Elias, P. Rosa, and D. S. Samuels. 2001. Transduction by phiBB-1, a bacteriophage of Borrelia burgdorferi. J. Bacteriol. 183:4771-4778.
22. Ferdows, M. S., and A. G. Barbour. 1989. Megabase-sized linear DNA in the bacterium Borrelia burgdorferi, the Lyme disease agent. Proc. Natl. Acad. Sci. USA 86:5969-5973.
23. Frackman, S., D. A. Siegele, and M. Feiss. 1985. A functional domain of bacteriophage lambda terminase for prohead binding. J. Mol. Biol. 180:283-300.
24. Fraser, C., 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. Fleischman, D. Richardson, J. Peterson, A. R. Kerlavage, J. Quackenbush, S. Salzberg, M. Hanson, R. 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.
25. Grundling, A., M. Manson, and R. Young. 2001. Holins kill without warning. Proc. Natl. Acad. Sci. USA 98:9348-9352.
26. Hayes, S. F., W. Burgdorfer, and A. G. Barbour. 1983. Bacteriophage in the Ixodes dammini spirochete, etiological agent of Lyme disease. J. Bacteriol. 154:1436-1439.
27. Hefty, P. S., C. S. Brooks, A. M. Jett, G. L. White, S. K. Wikel, R. C. Kennedy, and D. R. Akins. 2002. OspE-related, OspF-related and ELp lipoproteins are immunogenic in baboons experimentally infected with Borrelia burgdorferi and in human Lyme disease patients. J. Clin. Microbiol. 40:4256-4265.
28. Hefty, P. S., S. E. Jolliff, M. J. Caimano, S. K. Wikel, J. D. Radolf, and D. R. Akins. 2001. Regulation of the OspE-related, OspF-related, and Elp lipoproteins of Borrelia burgdoiferi strain 297 by mammalian host-specific signals. Infect. Immun. 69:3618-3627.
29. Hellwage, J., T. Meri, T. Heikkila, A. Alitalo, J. Panelius, P. Landenne, I. J. T. 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.
30. Hovis, K., J. V. McDowell, L. Griffin, and R. T. Marconi. 2004. Identification and characterization of a linear plasmid encoded factor H-binding protein (FhbA) of the relapsing fever spirochete, Borrelia hermsii. J. Bacteriol. 186:2612-2618.
31. Humphrey, S. B., T. B. Stanton, and N. S. Jense. 1995. Mitomycin C induction of bacteriophages from Serpulina hyodysenteriae and Serpulina innocens. FEMS Microbiol. Lett. 134:97-101.
32. Humphrey, S. B., T. B. Stanton, N. S. Jensen, and R. L. Zuerner. 1997. Purification and characterization of VSH-1, a generalized transducing bacteriophage of Serpulina hyodysenteriae. J. Bacteriol. 179:323-329.
33. 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. European J. Immunol. 31:1674-1684.
34. Kraiczy, P., C. Skerka, and P. F. Zipfel. 2001. Further characterization of complement regulator-acquiring surface proteins of Borrelia burgdorferi. Infect. Immun. 69:7800-7809.
35. Lam, T. T., T.-P. K. Nguyen, R. R. Montgomery, F. S. Kantor, E. Fikrig, and R. A. Flavell. 1994. Outer surface protein E and F of Borrelia burgdorferi, the agent of Lyme disease. Infect. Immun. 62:290-298.
36. 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.
37. Marconi, R. T., D. S. Samuels, T. G. Schwan, and C. F. Garon. 1993. Identification of a protein in several Borrelia species which is related to OspC of the Lyme disease spirochetes. J. Clin. Microbiol. 31:2577-2583.
38. Marconi, R. T., S. Y. Sung, C. N. 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.
39. McDowell, J. V., J. Wolfgang, E. Tran, M. S. Metis, 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.
40. Metis, S., J. V. McDowell, M. Theisen, P. R. Hansen, and R. T. Marconi. 2003. Analysis of the OspE determinants involved in the binding of factor H and OspE targeting antibodies elicited during infection in mice. Infect. Immun. 71:3587-3596.
41. Miller, E. S., J. F. Heidelberg, J. A. Eisen, W. C. Nelson, A. S. Durkin, A. Ciecko, T. V. Feldblyum, O. White, I. T. Paulsen, W. C. Nierman, J. Lee, B. Szczypinski, and C. M. Fraser. 2003. Complete genome sequence of the broad-host-range vibriophage KVP40: comparative genomics of a T4-related bacteriophage. J. Bacteriol. 185:5220-5233.
42. Ojaimi, C., C. Brooks, S. Casjens, P. Rosa, A. Elias, A. G. Harbour, A. Jasinskas, J. Benach, L. Katona, J. Radolf, M. Caimano, J. Skare, K. Swingle, D. Akins, and I. Schwarte. 2003. Profiling of temperature-induced changes in Borrelia burgdorferi gene expression by using whole genome arrays. Infect. Immun. 71:1689-1705.
43. Porcella, S. F., T. G. Popova, D. R. Akins, M. Li, J. R. Radolf, and M. V. Norgard. 1996. Borrelia burgdorferi supercoiled plasmids encode multicopy open reading frames and a lipoprotein gene family. J. Bacteriol. 178:3293-3307.
44. Roberts, D., M. Caimano, J. McDowell, M. Theisen, A. Holm, E. Orff, D. Nelson, S. Wikel, J. Radolf, and R. Marconi. 2002. Environmental regulation and differential expression of members of the Bdr protein family of Borrelia burgdorferi. Infect. Immun. 70:7033-7041.
45. Roberts, D. M., M. Theisen, and R. T. Marconi. 2000. Analysis of the cellular localization of Bdr paralogs in Borrelia burgdorferi, a causative agent of Lyme disease: evidence for functional diversity. J. Bacteriol. 182:4222-4226.
46. Sadziene, A., B. Wilske, M. S. Ferdows, and A. G. Harbour. 1993. The cryptic ospC gene of Borrelia burgdorferi B31 is located on a circular plasmid. Infect. Immun. 61:2192-2195.
47. Steere, A. C. 2001. Lyme disease. N. Engl. J. Med. 345:115-125.
48. Stevenson, B., S. Casjens, R. van Vugt, S. F. Porcella, K. Tilly, J. L. Bono, and P. Rosa. 1997. Characterization of cp18, a naturally truncated member of the cp32 family of Borrelia burgdorferi plasmids. J. Bacteriol. 179:4285-4291.
49. Stevenson, B., K. Tilly, and P. A. Rosa. 1996. A family of genes located on four separate 32-kilobase circular plasmids in Borrelia burgdorferi B31. J. Bacteriol. 178:3508-3516.
50. Stromdahl, E. Y., P. C. Williamson, T. M. Kollars, Jr., S. R. Evans, R. K. Barry, M. A. Vince, and N. A. Dobbs. 2003. Evidence of Borrelia lonestari DNA in Amblyomma americanum (Acari: Ixodidae) removed from humans. J. Clin. Microbiol. 41:5557-5562.
51. Sung, S. Y., J. McDowell, J. A. Carlyon, and R. T. Marconi. 2000. Mutation and recombination in the upstream homology box flanked ospE related genes of the Lyme disease spirochetes results in the development of new antigenic variants during infection. Infect. Immun. 68:1319-1327.
52. Tokarz, R., J. Anderton, L. Katona, and J. Benach. 2004. Combined effects of blood and temperature shift on Borrelia burgdorferi gene expression as determined by whole genome DNA array. Infect. Immun. 72:5419-5432.
53. Varela, A. S., M. P. Luttrell, E. W. Howerth, V. A. Moore, W. R. Davidson, D. E. Stallknecht, and S. E. Little. 2004. First culture isolation of Borrelia lonestari, putative agent of southern tick-associated rash illness. J. Clin. Microbiol. 42:1163-1169.
54. Zhang, H., A. Raji, M. Theisen, P. R. Hansen, and R. T. Marconi. 2005. bdrF2 of the Lyme disease spirochetes is coexpressed with a series of cytoplasmic proteins and is produced specifically during early infection. J. Bacteriol. 187:175-184.
55. Zipfel, P. F., C. Skerka, J. Hellwage, S. T. Jokiranta, S. Meri, V. Brade, P. Kraiczy, M. Noris, and G. Remuzzi. 2002. Structure-function studies of the complement system. Biochem. Soc. Trans. 30:971-978.
56. Zuckert, W. R., and J. Meyer. 1996. Circular and linear plasmids of Lyme Disease spirochetes have extensive homology: characterization of a repeated DNA element. J. Bacteriol. 178:2287-2298.