Transcriptional regulation of the Borrelia burgdorferi antigenically variable VlsE surface protein

Journal of Bacteriology

Volumn 188, Issue 13, 2006, Pages 4879-4889

  Bykowski, Tomasz ^a   Babb, Kelly ^a,c   Von Lackum, Kate ^a   Riley, Sean P ^a   Morris, Steven J ^b   Stevenson, Brian ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

^b UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^c PURDUE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOPLASM PROTEIN; DNA BINDING PROTEIN; MEMBRANE PROTEIN; PROTEIN VLSE; UNCLASSIFIED DRUG;

ANTIGENIC VARIATION; ARTICLE; BACTERIAL CELL; BACTERIAL COLONIZATION; BORRELIA BURGDORFERI; DNA PROTEIN COMPLEX; GEL MOBILITY SHIFT ASSAY; GENE CASSETTE; GENE CONTROL; GENE EXPRESSION; GENETIC RECOMBINATION; IMMUNE RESPONSE; LYME DISEASE; MAMMAL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN SYNTHESIS; SILENT GENE; SPIROCHETE; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION;

5' UNTRANSLATED REGIONS; ANIMALS; ANTIGENS, BACTERIAL; ARACHNID VECTORS; BACTERIAL PROTEINS; BORRELIA BURGDORFERI; FEMALE; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; HYDROGEN-ION CONCENTRATION; IXODES; LARVA; LIFE CYCLE STAGES; LIPOPROTEINS; LYME DISEASE; MICE; MICE, INBRED BALB C; MOLECULAR SEQUENCE DATA; NYMPH; TEMPERATURE; TRANSCRIPTION INITIATION SITE; TRANSCRIPTION, GENETIC; VIRULENCE;

ACARI; ANIMALIA; BORRELIA BURGDORFERI; MAMMALIA; SPIROCHAETALES;

EID: 33745442559     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00229-06     Document Type: Article

References (59)

1. Babb, K., J. D. McAlister, J. C. Miller, and B. Stevenson. 2004. Molecular characterization of Borrelia burgdorferi erp promoter/operator elements, J. Bacteriol. 186:2745-2756,
2. Babb, K., K. von Lackum, R. L. Wattier, S. P. Riley, and B. Stevenson. 2005. Synthesis of autoinducer 2 by the Lyme disease spirochete, Borrelia burgdorferi. J. Bacteriol. 187:3079-3087.
3. Barbour, A. G. 1990. Antigenic variation of a relapsing fever Borrelia species. Annu. Rev. Microbiol. 44:155-171.
4. Barbour, A. G. 1984. Isolation and cultivation of Lyme disease spirochetes. Yale J. Biol. Med. 57:521-525.
5. Barbour, A. G., S. F. Hayes, R. A. Heiland, M. E. Schrumpf, and S. L. Tessier. 1986. A Borrelia-specific monoclonal antibody binds to a flagellar epitope. Infect. Immun. 52:549-554.
6. Barbour, A. G., and B. I. Restrepo. 2000. Antigenic variation in vector-borne pathogens. Emerg. Infect. Dis. 6:449-457.
7. Bowman, A. S., J. R. Sauer, K. Zhu, and J. W. Dillwith. 1995. Biosynthesis of salivary prostaglandins in the lone star tick, Amblyomma americanum. Insect Biochem. Mol. Biol. 25:735-741.
8. Browning, D. F., and S. J. Busby. 2004. The regulation of bacterial transcription initiation. Nat. Rev. Microbiol. 2:57-65.
9. Carroll, J. A., R. M. Cordova, and C. F. Garon. 2000. Identification of eleven pH-regulated genes in Borrelia burgdorferi localized to linear plasmids. Infect. Immun. 68:6677-6684.
10. Carroll, J. A., N. El-Hage, J. C. Miller, K. Babb, and B. Stevenson. 2001. Borrelia burgdorferi RevA antigen is a surface-exposed outer membrane protein whose expression is regulated in response to environmental temperature and pH. Infect. Immun. 69:5286-5293.
11. Carroll, J. A., C. F. Garon, and T. G. Schwan. 1999. Effects of environmental pH on membrane proteins in Borrelia burgdorferi. Infect. Immun. 67:3181-3187.
12. Cassatt, D. R., N. K. Patel, N. D. Ulbrandt, and M. S. Hanson. 1998. DbpA, but not OspA, is expressed by Borrelia burgdorferi during spirochetemia and is a target for protective antibodies. Infect. Immun. 66:5379-5387.
13. Chatterji, D., and A. K. Ojha. 2001. Revisiting the stringent response, ppGpp and starvation signalling. Curr. Opin. Microbiol. 4:160-165.
14. Crother, T. R., C. I. Champion, X.-Y. Wu, D. R. Blanco, J. N. Miller, and M. A. Lovett. 2003. Antigenic composition of Borrelia burgdorferi during infection of SCID mice. Infect. Immun. 71:3419-3428.
15. Donelson, J. E. 2003. Antigenic variation and the African trypanosome genome. Acta Trop. 85:391-404.
16. 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.
17. Graham, S. V., B. Wymer, and J. D. Barry. 1998. Activity of a trypanosome metacyclic variant surface glycoprotein gene promoter is dependent upon life cycle stage and chromosomal context. Mol. Cell. Biol. 18:1137-1146.
18. Grimm, D., K. Tilly, D. M. Bueschel, M. A. Fisher, P. F. Policastro, F. C. Gherardini, T. G. Schwan, and P. A. Rosa. 2005. Defining plasmids required by Borrelia burgdorferi for colonization of tick vector Ixodes scapularis (Acari: Ixodidae). J. Med. Entomol. 42:676-684.
19. Hagman, K. E., X. Yang, S. K. Wikel, G. B. Schoeler, M. J. Caimano, J. D. Radolf, and M. V. Norgard. 2000. Decorin-binding protein A (DbpA) of Borrelia burgdorferi is not protective when immunized mice are challenged via tick infestation and correlates with the lack of DbpA expression by B. burgdorferi in ticks. Infect. Immun. 68:4759-4764.
20. Hodzic, E., S. Feng, K. J. Freet, and S. W. Barthold. 2003. Borrelia burgdorferi population dynamics and prototype gene expression during infection of immunocompetent and immunodeficient mice. Infect. Immun. 71:5042-5055.
21. Hodzic, E., S. Feng, K. J. Freet, D. L. Borjesson, and S. W. Barthold. 2002. Borrelia burgdorferi population kinetics and selected gene expression at the host-vector interface. Infect. Immun. 70:3382-3388.
22. Hudson, C. R., J. G. Frye, F. D. Quinn, and F. C. Gherardini. 2001. Increased expression of Borrelia burgdorferi vlsE in response to human endothelial cell membranes. Mol. Microbiol. 41:229-239.
23. Indest, K. J., J. K. Howell, M. B. Jacobs, D. Scholl-Meeker, S. J. Norris, and M. T. Philipp. 2001. Analysis of Borrelia burgdorferi vlsE gene expression and recombination in the tick vector. Infect. Immun. 69:7083-7090.
24. Iyer, R., J. M. Hardham, G. P. Wormser, I. Schwartz, and S. J. Norris. 2000. Conservation and heterogeneity of vlsE among human and tick isolates of Borrelia burgdorferi. Infect. Immun. 68:1714-1718.
25. Kawabata, H., F. Myouga, Y. Inagaki, N. Murai, and H. Watanabe. 1998. Genetic and immunological analyses of Vls (VMP-like sequences) of Borrelia urgdorferi. Microb. Pathog. 24:155-166.
26. Konkel, M. E., and K. Tilly. 2000. Temperature-regulated expression of bacterial virulence genes. Microbes Infect. 2:157-166.
27. Labandeira-Rey, M., J. Seshu, and J. T. Skare. 2003. The absence of linear plasmid 25 or 28-1 of Borrelia burgdorferi dramatically alters the kinetics of experimental infection via distinct mechanisms. Infect. Immun. 71:4608-4613.
28. 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.
29. Lawrenz, M. B., J. M. Hardham, R. T. Owens, J. Nowakowski, A. C. Steere, G. P. Wormser, and S. J. Norris. 1999. Human antibody responses to VlsE antigenic variation protein of Borrelia burgdorferi. J. Clin. Microbiol. 37:3997-4004.
30. Ledin, K. E., N. S. Zeidner, J. M. Ribeiro, B. J. Biggerstaff, M. C. Dolan, G. Dietrich, L. Vredevoe, and J. Piesman. 2005. Borreliacidal activity of saliva of the tick Amblyomma americanum. Med. Vet. Entomol. 19:90-95.
31. Liang, F. T., J. M. Nowling, and M. T. Philipp. 2000. Cryptic and exposed invariable regions of VlsE, the variable surface antigen of Borrelia burgdorferi s1. J. Bacteriol. 182:3597-3601.
32. Liang, F. T., and M. T. Philipp. 1999. Analysis of antibody response to invariable regions of VlsE, the variable surface antigen of Borrelia burgdorferi. Infect. Immun. 67:6702-6706.
33. Liang, F. T., J. Yan, M. L. Mbow, S. L. Sviat, R. D. Gilmore, M. Mamula, and E. Fikrig. 2004. Borrelia burgdorferi changes its surface antigenic expression in response to host immune responses. Infect. Immun. 72:5759-5767.
34. Martinez-Antonio, A., and J. Collado-Vides. 2003. Identifying global regulators in transcriptional regulatory networks in bacteria. Curr. Opin. Microbiol. 6:482-489.
35. McDowell, J. V., S.-Y. Sung, L. T. Hu, and R. T. Marconi. 2002. Evidence that the variable regions of the central domain of VLsE are antigenic during infection with Lyme disease spirochetes. Infect. Immun. 70:4196-4203.
36. Miller, J. C. 2005. Example of real-time quantitative reverse transcription-PCR (Q-RT-PCR) analysis of bacterial gene expression during mammalian infection: Borrelia burgdorferi in mouse tissues, p. 1D.3. In R. Coico, T. Kowalik, J. Quarles, B. Stevenson, and R. Taylor (ed.), Current protocols in microbiology. Wiley, Hoboken, NJ.
37. Miller, J. C., and B. Stevenson. 2004. Increased expression of Borrelia burgdorferi factor h-binding surface proteins during transmission from ticks to mice. Int. J. Med. Microbiol. 293 S. 37:120-125.
38. Miller, J. C., K. von Lackum, K. Babb, J. D. McAlister, and B. Stevenson. 2003. Temporal analysis of Borrelia burgdorferi Erp protein expression throughout the mammal-tick infectious cycle. Infect. Immun. 71:6943-6952.
39. Ohnishi, J., J. Piesman, and A. M. de Silva. 2001. Antigenic and genetic heterogeneity of Borrelia burgdorferi populations transmitted by ticks. Proc. Natl. Acad. SCi. USA 98:670-675.
40. Ohnishi, J., B. Schneider, W. B. Messer, J. Piesman, and A. M. deSilva. 2003. Genetic variation at the vlsE locus of Borrelia burgdorferi within ticks and mice over the course of a single transmission cycle. J. Bacteriol. 185:4432-4441.
41. PÉrez-Rueda, E., and J. Collado-Vides. 2000. The repertoire of DNA-binding transcriptional regulators in Escherichia coli. Nucleic Acids Res. 28:1838-1847.
42. Piesman, J., B. S. Schneider, and N. S. Zeidner. 2001. Use of quantitative PCR to measure density of Borrelia burgdorferi in the midgut and salivary glands of feeding tick vectors. J. Clin. Microbiol. 39:4145-4148.
43. 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.
44. Ramamoorthy, R., and D. Scholl-Meeker. 2001. Borrelia burgdorferi proteins whose expression is similarly affected by culture temperature and pH. Infect. Immun. 69:2739-2742.
45. Rurangirwa, F. R., D. Stiller, D. M. French, and G. H. Palmer. 1999. Restriction of major surface protein 2 (MSP2) variants during tick transmission of the ehrlichia Anaplasma marginale. Proc. Natl. Acad. Sci. USA 96:3171-3176.
46. Samuels, D. S., K. E. Mach, and C. F. Garon. 1994. Genetic transformation of the Lyme disease agent Borrelia burgdorferi with coumarin-resistant gyrB. J. Bacteriol. 176:6045-6049.
47. Schwan, T. G., and B. J. Hinnebusch. 1998. Bloodstream- versus tick-associated variants of a relapsing fever bacterium. Science 280:1938-1940.
48. 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.
49. Seshu, J., J. A. Boylan, F. C. Gherardini, and J. T. Skare. 2004. Dissolved oxygen levels alter gene expression and antigen profiles in Borrelia burgdorferi. Infect. Immun. 72:1580-1586.
50. Stevenson, B., J. L. Bono, T. G. Schwan, and P. 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.
51. 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.
52. Stevenson, B., K. von Lackum, S. P. Riley, A. E. Cooley, M. E. Woodman, and T. Bykowski. Evolving models of Lyme disease spirochete gene regulation. Wien. Klin. Wochenschr., in press.
53. Stroether, K. O., A. Broadwater, and A. M. DeSilva. 2005. Plasmid requirements for infection of ticks by Borrelia burgdorferi. Vector-Borne Zoonot. Dis. 5:237-245.
54. von Lackum, K., J. C. Miller, T. Bykowski, S. P. Riley, M. E. Woodman, V. Brade, P. Kraiczy, B. Stevenson, and R. Wallich. 2005. Borrelia burgdorferi regulates expression of complement regulator-acquiring surface protein 1 during the mammal-tick infection cycle. Infect. Immun. 73:7398-7405.
55. Wang, D., D. J. Botkin, and S. J. Norris. 2003. Characterization of the vis antigenic variation loci of the Lyme disease spirochaetes Borrelia garinii Ip90 and Borrelia afzelii ACA1. Mol. Microbiol. 47:1407-1417.
56. 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.
57. 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 89:1-20.
58. Zhang, J.-R., and S. J. Norris. 1998. Genetic variation of the Borrelia burgdorferi gene vlsE involves cassette-specific, segmental gene conversion. Infect. Immun. 66:3698-3704.
59. Zhang, J.-R., and S. J. Norris. 1998. Kinetics and in vivo induction of genetic variation of vlsE in Borrelia burgdorferi. Infect. Immun. 66:3689-3697.