Comparative transcriptional profiling of Borrelia burgdorferi clinical isolates differing in capacities for hematogenous dissemination

Infection and Immunity

Volumn 73, Issue 10, 2005, Pages 6791-6802

  Ojaimi, Caroline ^a   Mulay, Vishwaroop ^a   Liveris, Dionysios ^a   Iyer, Radha ^a   Schwartz, Ira ^a  

^a NEW YORK MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BBA74 PROTEIN; KANAMYCIN; PORIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIUM ISOLATE; BB0329 GENE; BB0330 GENE; BB0603 GENE; BBA74 GENE; BBB29 GENE; BORRELIA BURGDORFERI; CELL SURFACE; GENE; GENE EXPRESSION; GENE LOCATION; GENETIC TRANSCRIPTION; GENOTYPE; GROWTH RATE; LYME DISEASE; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PATHOGENESIS; PRIORITY JOURNAL;

ALLELES; BACTERIAL OUTER MEMBRANE PROTEINS; BORRELIA BURGDORFERI; ERYTHEMA CHRONICUM MIGRANS; GENE EXPRESSION PROFILING; GENES, BACTERIAL; HUMANS; LYME DISEASE; MUTATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OPERON; PLASMIDS; TRANSCRIPTION, GENETIC;

EID: 25444464870     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.73.10.6791-6802.2005     Document Type: Article

References (83)

1. Achouak, W., T. Heulin, and J. M. Pages. 2001. Multiple facets of bacterial porins. FEMS Microbiol. Lett. 199:1-7.
2. 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 burgdorferi outer surface protein F (OspF) homologue. Mol. Microbiol. 18:507-520.
3. Anderton, J. M., R. Tokarz, C. D. Thill, C. J. Kuhlow, C. S. Brooks, D. R. Akins, L. I. Katona, and J. L. Benach. 2004. Whole-genome DNA array analysis of the response of Borrelia burgdorferi to a bactericidal monoclonal antibody. Infect. Immun. 72:2035-2044.
4. Anguita, J., M. N. Hedrick, and E. Fikrig. 2003. Adaptation of Borrelia burgdorferi in the tick and the mammalian host. FEMS Microbiol. Rev. 27:493-504.
5. Benach, J. L., E. M. Bosler, J. P. Hanrahan, J. L. Coleman, G. S. Habicht, T. F. Bast, D. J. Cameron, J. L. Ziegler, A. G. Barbour, W. Burgdorfer, R. Edelman, and R. A. Kaslow. 1983. Spirochetes isolated from the blood of two patients with Lyme disease. N. Engl. J. Med. 308:740-742.
6. Benjamini, Y., and Y. Hochberg. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B 57:289-300.
7. 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.
8. Boucher, J. C., H. Yu, M. H. Mudd, and V. Deretic. 1997. Mucoid Pseudomonas aeruginosa in cystic fibrosis: characterization of muc mutations in clinical isolates and analysis of clearance in a mouse model of respiratory infection. Infect. Immun. 65:3838-3846.
9. Boyce, J. D., P. A. Cullen, and B. Adler. 2004. Genomic-scale analysis of bacterial gene and protein expression in the host. Emerg. Infect. Dis. 10:1357-1362.
10. Brooks, C. S., P. S. Hefty, S. E. Jolliff, and D. R. Akins. 2003. Global analysis of Borrelia burgdorferi genes regulated by mammalian host-specific signals. Infect. Immun. 71:3371-3383.
11. Bunikis, J., L. Noppa, and S. Bergstrom. 1995. Molecular analysis of a 66-kDa protein associated with the outer membrane of Lyme disease Borrelia. FEMS Microbiol. Lett. 131:139-145.
12. Bunikis, J., L. Noppa, Y. Ostberg, A. G. Barbour, and S. Bergstrom. 1996. Surface exposure and species specificity of an immunoreactive domain of a 66-kilodalton outer membrane protein (P66) of the Borrelia spp. that cause Lyme disease. Infect. Immun. 64:5111-5116.
13. 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.
14. Chen, T., Y. Hosogi, K. Nishikawa, K. Abbey, R. D. Fleischmann, J. Walling, and M. J. Duncan. 2004. Comparative whole-genome analysis of virulent and avirulent strains of Porphyromonas gingivalis. J. Bacteriol. 186:5473-5479.
15. Coburn, J., W. Chege, L. Magoun, S. C. Bodary, and J. M. Leong. 1999. Characterization of a candidate Borrelia burgdorferi beta3-chain integrin ligand identified using a phage display library. Mol. Microbiol. 34:926-940.
16. Coburn, J., and C. Cugini. 2003. Targeted mutation of the outer membrane protein P66 disrupts attachment of the Lyme disease agent, Borrelia burgdorferi, to integrin alphavbeta3. Proc. Natl. Acad. Sci. USA 100:7301-7306.
17. Conway, T., and G. K. Schoolnik. 2003. Microarray expression profiling: capturing a genome-wide portrait of the transcriptome. Mol. Microbiol. 47:879-889.
18. Cummings, C. A., and D. A. Relman. 2000. Using DNA microarrays to study host-microbe interactions. Emerg. Infect. Dis. 6:513-525.
19. Cundell, D. R., B. J. Pearce, J. Sandros, A. M. Naughton, and H. R. Masure. 1995. Peptide permeases from Streptococcus pneumonias affect adherence to eucaiyotic cells. Infect. Immun. 63:2493-2498.
20. Dunny, G. M., B. A. Leonard, and P. J. Hedberg. 1995. Pheromone-inducible conjugation in Enterococcus faecalis: interbacterial and host-parasite chemical communication. J. Bacteriol. 177:871-876.
21. Feinberg, A. P., and B. Vogelstein. 1983. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal. Biochem. 132:6-13.
22. Fikrig, E., S. W. Barthold, W. Sun, W. Feng, S. R. Telford III, and R. A. Flavell. 1997. Borrelia burgdorferi P35 and P37 proteins, expressed in vivo, elicit protective immunity. Immunity 6:531-539.
23. Foretz, M., D. Postic, and G. Baranton. 1997. Phylogenetic analysis of Borrelia burgdorferi sensu stricto by arbitrarily primed PCR and pulsed-field gel electrophoresis. Int. J. Syst. Bacteriol. 47:11-18.
24. 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. Fuji, 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. Gilmore, R. D., Jr., M. L. Mbow, and B. Stevenson. 2001. Analysis of Borrelia burgdorferi gene expression during life cycle phases of the tick vector Ixodes scapularis. Microbes Infect. 3:799-808.
26. Grimm, D., C. H. Eggers, M. J. Caimano, K. Tilly, P. E. Stewart, A. F. Elias, J. D. Radolf, and P. A. Rosa. 2004. Experimental assessment of the roles of linear plasmids Ip25 and Ip28-1 of Borrelia burgdorferi throughout the infectious cycle. Infect. Immun. 72:5938-5946.
27. Hubner, A., A. T. Revel, D. M. Nolen, K. E. Hagman, and M. V. Norgard. 2003. Expression of a luxS gene is not required for Borrelia burgdorferi infection of mice via needle inoculation. Infect. Immun. 71:2892-2896.
28. Iyer, R., O. Kalu, J. Purser, S. Norris, B. Stevenson, and I. Schwartz. 2003. Linear and circular plasmid content in Borrelia burgdorferi clinical isolates. Infect. Immun. 71:3699-3706.
29. Iyer, R., D. Liveris, A. Adams, J. Nowakowski, D. McKenna, S. Bittker, D. Cooper, G. P. Wormser, and I. Schwartz. 2001. Characterization of Borrelia burgdorferi isolated from erythema migrans lesions: interrelationship of three molecular typing methods. J. Clin. Microbiol. 39:2954-2957.
30. Janeway, C. A., Jr., and R. Medzhitov. 2002. Innate immune recognition. Annu. Rev. Immunol. 20:197-216.
31. Koide, T., P. A. Zaini, L. M. Moreira, R. Z. Vencio, A. Y. Matsukuma, A. M. Durham, D. C. Teixeira, H. El Dorry, P. B. Monteiro, A. C. da Silva, S. Verjovski-Almeida, A. M. da Silva, and S. L. Gomes. 2004. DNA microarray-based genome comparison of a pathogenic and a nonpathogenic strain of Xylella fastidiosa delineates genes important for bacterial virulence. J. Bacteriol. 186:5442-5449.
32. Labandeira-Rey, M., and J. T. Skare. 2001. Decreased infectivity in Borrelia burgdorferi strain B31 is associated with loss of linear plasmid 25 or 28-1. Infect. Immun. 69:446-455.
33. Leonard, B. A., A. Podbielski, P. J. Hedberg, and G. M. Dunny. 1996. Enterococcus faecalis pheromone binding protein, PrgZ, recruits a chromosomal oligopeptide permease system to import sex pheromone cCF10 for induction of conjugation. Proc. Natl. Acad. Sci. USA 93:260-264.
34. Liang, F. T., M. B. Jacobs, L. C. Bowers, and M. T. Philipp. 2002. An immune evasion mechanism for spirochetal persistence in Lyme borreliosis. J. Exp. Med. 195:415-422.
35. 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.
36. Livak, K. J., and T. D. Schmittgen. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(- delta delta C(T)) method. Methods 25:402-408.
37. Liveris, D., A. Gazumyan, and I. Schwartz. 1995. Molecular typing of Borrelia burgdorferi sensu lato by PCR-restriction fragment length polymorphism analysis. J. Clin. Microbiol. 33:589-595.
38. Liveris, D., S. Varde, R. Iyer, S. Koenig, S. Bittker, D. Cooper, D. McKenna, J. Nowakowski, R. B. Nadelman, G. P. Wormser, and I. Schwartz. 1999. Genetic diversity of Borrelia burgdorferi in Lyme disease patients as determined by culture versus direct PCR with clinical specimens. J. Clin. Microbiol. 37:565-569.
39. Liveris, D., G. P. Wormser, J. Nowakowski, R. Nadelman, S. Bittker, D. Cooper, S. Varde, F. H. Moy, G. Forseter, C. S. Pavia, and I. Schwartz. 1996. Molecular typing of Borrelia burgdorferi from Lyme disease patients by PCR-restriction fragment length polymorphism analysis. J. Clin. Microbiol. 34:1306-1309.
40. Mathiesen, D. A., J. H. Oliver, Jr., C. P. Kolbert, E. D. Tullson, B. J. Johnson, G. L. Campbell, P. D. Mitchell, K. D. Reed, S. R. Telford III, J. F. Anderson, R. S. Lane, and D. H. Persing. 1997. Genetic heterogeneity of Borrelia burgdorferi in the United States. J. Infect. Dis. 175:98-107.
41. Maurelli, A. T., R. E. Fernandez, C. A. Bloch, C. K. Rode, and A. Fasano. 1998. "Black holes" and bacterial pathogenicity: a large genomic deletion that enhances the virulence of Shigella spp. and enteroinvasive Escherichia coli. Proc. Natl. Acad. Sci. USA 95:3943-3948.
42. Medzhitov, R. and C. Janeway, Jr. 2000. Innate immunity. N. Engl. J. Med. 343:338-344.
43. Moore, R. A., S. Reckseidler-Zenteno, H. Kim, W. Nierman, Y. Yu, A. Tuanyok, J. Warawa, D. DeShazer, and D. E. Woods. 2004. Contribution of gene loss to the pathogenic evolution of Burkholderia pseudomallei and Burkholderia mallei. Infect. Immun. 72:4172-4187.
44. Narasimhan, S., M. J. Caimano, F. T. Liang, F. Santiago, M. Laskowski, M. T. Philipp, A. R. Pachner, J. D. Radolf, E. Fikrig, and M. J. Camaino. 2003. Borrelia burgdorferi transcriptome in the central nervous system of non-human primates. Proc. Natl. Acad. Sci. USA 100:15953-15958.
45. Narasimhan, S., F. Santiago, R. A. Koski, B. Brei, J. F. Anderson, D. Fish, and E. Fikrig. 2002. Examination of the Borrelia burgdorferi transcriptome in Ixodes scapularis during feeding. J. Bacteriol. 184:3122-3125.
46. Ojaimi, C., C. Brooks, D. Akins, S. Casjens, P. Rosa, A. Elias, A. Barbour, A. Jasinskas, J. Benach, L. Katonah, J. Radolf, M. Caimano, J. Skare, K. Swingle, S. Sims, and I. Schwartz. 2002. Borrelia burgdorferi gene expression profiling with membrane-based arrays. Methods Enzymol. 358:165-177.
47. Ojaimi, C., C. Brooks, S. Casjens, P. Rosa, A. Elias, A. Barbour, A. Jasinskas, J. Benach, L. Katona, J. Radolf, M. Caimano, J. Skare, K. Swingle, D. Akins, and I. Schwartz. 2003. Profiling of temperature-induced changes in Borrelia burgdorferi gene expression by using whole genome arrays. Infect. Immun. 71:1689-1705.
48. Ostberg, Y., J. A. Carroll, M. Pinne, J. G. Krum, P. Rosa, and S. Bergstrom. 2004. Pleiotropic effects of inactivating a carboxyl-terminal protease, CtpA in Borrelia burgdorferi. J. Bacteriol. 186:2074-2084.
49. Ostberg, Y., M. Pinne, R. Benz, P. Rosa, and S. Bergstrom. 2002. Elimination of channel-forming activity by insertional inactivation of the p13 gene in Borrelia burgdorferi. J. Bacteriol. 184:6811-6819.
50. Parra-Lopez, C., M. T. Baer, and E. A. Groisman. 1993. Molecular genetic analysis of a locus required for resistance to antimicrobial peptides in Salmonella typhimurium. EMBO J. 12:4053-4062.
51. Perego, M., C. F. Higgins, S. R. Pearce, M. P. Gallagher, and J. A. Hoch. 1991. The oligopeptide transport system of Bacillus subtilis plays a role in the initiation of sporulation. Mol. Microbiol. 5:173-185.
52. Porcella, S. F., and T. G. Schwan. 2001. Borrelia burgdorferi and Treponema pallidum: a comparison of functional genomics, environmental adaptations, and pathogenic mechanisms. J. Clin. Investig. 107:651-656.
53. Probert, W. S., and B. J. Johnson. 1998. Identification of a 47 kDa fibronectin-binding protein expressed by Borrelia burgdorferi isolate B31. Mol. Microbiol. 30:1003-1015.
54. Purser, J. E., M. B. Lawrenz, M. J. Caimano, J. K. Howell, J. D. Radolf, and S. J. Norris. 2003. A plasmid-encoded nicotinamidase (PncA) is essential for infectivity of Borrelia burgdorferi in a mammalian host. Mol. Microbiol. 48:753-764.
55. Purser, J. E., and S. J. Norris. 2000. Correlation between plasmid content and infectivity in Borrelia burgdorferi. Proc. Natl. Acad. Sci. USA 97:13865-13870.
56. 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.
57. Rudner, D. Z., J. R. LeDeaux, K. Ireton, and A. D. Grossman. 1991. The spo0K locus of Bacillus subtilis is homologous to the oligopeptide permease locus and is required for sporulation and competence. J. Bacteriol. 173:1388-1398.
58. Salama, N., K. Guillemin, T. K. McDaniel, G. Sherlock, L. Tompkins, and S. Falkow. 2000. A whole-genome microarray reveals genetic diversity among Helicobacter pylori strains. Proc. Natl. Acad. Sci. USA 97:14668-14673.
59. Samuels, D. S. 1995. Electrotransformation of the spirochete Borrelia burgdorferi. Methods Mol. Biol. 47:253-259.
60. Schoolnik, G. K. 2002. Functional and comparative genomics of pathogenic bacteria. Curr. Opin. Microbiol. 5:20-26.
61. Schoolnik, G. K. 2002. Microarray analysis of bacterial pathogenicity. Adv. Microb. Physiol. 46:1-45.
62. Schwan, T. G., and J. Piesman. 2000. Temporal changes in outer surface proteins A and C of the Lyme disease-associated spirochete, Borrelia burgdorferi, during the chain of infection in ticks and mice. J. Clin. Microbiol. 38:382-388.
63. 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.
64. Schwartz, I., G. P. Wormser, J. J. Schwartz, D. Cooper, P. Weissensee, A. Gazumyan, E. Zimmermann, N. S. Goldberg, S. Bittker, and G. L. Campbell. 1992. Diagnosis of early Lyme disease by polymerase chain reaction amplification and culture of skin biopsies from erythema migrans lesions. J. Clin. Microbiol. 30:3082-3088.
65. Shevchuk, N. A., A. V. Bryksin, Y. A. Nusinovich, F. C. Cabello, M. Sutherland, and S. Ladisch. 2004. Construction of long DNA molecules using long PCR-based fusion of several fragments simultaneously. Nucleic Acids Res. 32:e19.
66. Skare, J. T., C. I. Champion, T. A. Mirzabekov, E. S. Shang, D. R. Blanco, H. Erdjument-Bromage, P. Tempst, B. L. Kagan, J. N. Miller, and M. A. Lovett. 1996. Porin activity of the native and recombinant outer membrane protein Oms28 of Borrelia burgdorferi. J. Bacteriol. 178:4909-4918.
67. Skare, J. T., T. A. Mirzabekov, E. S. Shang, D. R. Blanco, H. Erdjument-Bromage, J. Bunikis, S. Bergstrom, P. Tempst, B. L. Kagan, J. N. Miller, and M. A. Lovett. 1997. The Oms66 (p66) protein is a Borrelia burgdorferi porin. Infect. Immun. 65:3654-3661.
68. Sokurenko, E. V., D. L. Hasty, and D. E. Dykhuizen. 1999. Pathoadaptive mutations: gene loss and variation in bacterial pathogens. Trends Microbiol. 7:191-195.
69. Spach, D. H., W. C. Liles, G. L. Campbell, R. E. Quick, D. E. Anderson, Jr., and T. R. Pritsche. 1993. Tick-borne diseases in the United States. N. Engl. J. Med. 329:936-947.
70. Steere, A. C. 2001. Lyme disease. N. Engl. J. Med. 345:115-125.
71. Steere, A. C., R. L. Grodzicki, A. N. Kornblatt, J. E. Craft, A. G. Barbour, W. Burgdorfer, G. P. Schmid, E. Johnson, and S. E. Malawista. 1983. The spirochetal etiology of Lyme disease. N. Engl. J. Med. 308:733-740.
72. 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.
73. Suk, K., S. Das, W. Sun, B. Jwang, S. W. Barthold, R. A. Flavell, and E. Fikrig. 1995. Borrelia burgdorferi genes selectively expressed in the infected host. Proc. Natl. Acad. Sci. USA 92:4269-4273.
74. Tokarz, R., J. M. Anderton, L. I. Katona, and J. L. 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.
75. Wang, G., C. Ojaimi, R. Iyer, V. Saksenberg, S. A. McClain, G. P. Wormser, and I. Schwartz. 2001. Impact of genotypic variation of Borrelia burgdorferi sensu stricto on kinetics of dissemination and severity of disease in C3H/HeJ mice. Infect. Immun. 69:4303-4312.
76. Wang, G., C. Ojaimi, H. Wu, V. Saksenberg, R. Iyer, D. Liveris, S. A. McClain, G. P. Wormser, and I. Schwartz. 2002. Disease severity in a murine model of Lyme borreliosis is associated with the genotype of the infecting Borrelia burgdorferi sensu stricto strain. J. Infect. Dis. 186:782-791.
77. Wang, G., A. P. van Dam, I. Schwartz, and J. Dankert. 1999. Molecular typing of Borrelia burgdorferi sensu lato: taxonomic, epidemiological, and clinical implications. Clin. Microbiol. Rev. 12:633-653.
78. 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.
79. Wormser, G. P., S. Bittker, D. Cooper, J. Nowakowski, R. B. Nadelman, and C. Pavia. 2000. Comparison of the yields of blood cultures using serum or plasma from patients with early Lyme disease. J. Clin. Microbiol. 38:1648-1650.
80. Wormser, G. P., D. Liveris, J. Nowakowski, R. B. Nadelman, L. F. Cavaliere, D. McKenna, D. Holmgren, and I. Schwartz. 1999. Association of specific subtypes of Borrelia burgdorferi with hematogenous dissemination in early Lyme disease. J. Infect. Dis. 180:720-725.
81. Yang, X., M. S. Goldberg, T. G. Popova, G. B. Schoeler, 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.
82. Zhang, J. R., J. M. Hardham, A. G. Barbour, and S. J. Norris. 1997. Antigenic variation in Lyme disease borreliae by promiscuous recombination of VMP-like sequence cassettes. Cell 89:275-285.
83. Zhong, J., and A. G. Barbour. 2004. Cross-species hybridization of a Borrelia burgdorferi DNA array reveals infection- and culture-associated genes of the unsequenced genome of the relapsing fever agent Borrelia hermsii. Mol. Microbiol. 51:729-748.