Characterization of the highly regulated antigen BBA05 in the enzootic cycle of Borrelia burgdorferi

Infection and Immunity

Volumn 78, Issue 1, 2010, Pages 100-107

  Xu, Haijun ^a   He, Ming ^a   Pang, Xiujuan ^b   Xu, Zao C ^a   Piesman, Joseph ^c   Yang, X Frank ^a  

^a INDIANA UNIVERSITY   (United States)

^b SHENYANG PHARMACEUTICAL UNIVERSITY   (China)

^c NATIONAL CENTER FOR EMERGING AND ZOONOTIC INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN BBA05; BACTERIAL ANTIGEN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL STRAIN; BACTERIAL TRANSMISSION; BORRELIA BURGDORFERI; CONTROLLED STUDY; FEEDING; GENE EXPRESSION REGULATION; MOLTING; MOUSE; MUTANT; NONHUMAN; NYMPHAEA; PRIORITY JOURNAL; SPIROCHAETA; TICK;

ANIMALS; ANTIGENS, BACTERIAL; BACTERIAL PROTEINS; BORRELIA BURGDORFERI; GENE EXPRESSION REGULATION, BACTERIAL; MICE; MICE, INBRED C3H; MUTATION; PROTEIN TRANSPORT;

EID: 73449103589     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01008-09     Document Type: Article

References (71)

1. Barbour, A. G., A. Jasinskas, M. A. Kayala, D. H. Davies, A. C. Steere, P. Baldi, and P. L. Felgner. 2008. A genome-wide proteome array reveals a limited set of immunogens in natural infections of humans and white-footed mice with Borrelia burgdorferi. Infect. Immun. 76:3374-3389.
2. Blevins, J., K. E. Hagman, and M. V. Norgard. 2008. Assessment of decorinbinding protein A to the infectivity of Borrelia burgdorferi in the murine models of needle and tick infection. BMC Microbiol. 8:82.
3. Boardman, B. K., M. He, Z. Ouyang, H. Xu, X. Pang, and X. F. Yang. 2008. Essential role of the response regulator Rrp2 in the infectious cycle of Borrelia burgdorferi. Infect. Immun. 76:3844-3853.
4. 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.
5. Brooks, C. S., S. R. Vuppala, A. M. Jett, and D. R. Akins. 2006. Identification of Borrelia burgdorferi outer surface proteins. Infect. Immun. 74:296-304.
6. Burtnick, M. N., J. S. Downey, P. J. Brett, J. A. Boylan, J. G. Frye, T. R. Hoover, and F. C. Gherardini. 2007. Insights into the complex regulation of rpoS in Borrelia burgdorferi. Mol. Microbiol. 65:277-293.
7. Caimano, M. J., C. H. Eggers, K. R. O. Hazlett, and J. D. Radolf. 2004. RpoS is not central to the general stress response in Borrelia burgdorferi but does control expression of one or more essential virulence determinants. Infect. Immun. 72:6433-6445.
8. Caimano, M. J., R. Iyer, C. H. Eggers, C. Gonzalez, E. A. Morton, M. A. Gilbert, I. Schwartz, and J. D. Radolf. 2007. Analysis of the RpoS regulon in Borrelia burgdorferi in response to mammalian host signals provides insight into RpoS function during the enzootic cycle. Mol. Microbiol. 65:1193-1217.
9. 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.
10. Clifton, D. R., C. L. Nolder, J. L. Hughes, A. J. Nowalk, and J. A. Carroll. 2006. Regulation and expression of bba66 encoding an immunogenic infection-associated lipoprotein in Borrelia burgdorferi. Mol. Microbiol. 61:243-258.
11. Coleman, A. S., X. Yang, M. Kumar, X. Zhang, K. Promnares, D. Shroder, M. R. Kenedy, J. F. Anderson, D. R. Akins, and U. Pal. 2008. Borrelia burgdorferi complement regulator-acquiring surface protein 2 does not contribute to complement resistance or host infectivity. PLoS One 3:3010e.
12. de Silva, A. M., S. R. Telford, L. R. Brunet, S. W. Barthold, and E. Fikrig. 1996. Borrelia burgdorferi OspA is an arthropod-specific transmission-blocking Lyme disease vaccine. J. Exp. Med. 183:271-275.
13. Elias, A. F., P. E. Stewart, D. Grimm, M. J. Caimano, C. H. Eggers, K. Tilly, J. L. Bono, D. R. Akins, J. D. Radolf, T. G. Schwan, and P. Rosa. 2002. Clonal polymorphism of Borrelia burgdorferi strain B31 MI: implications for mutagenesis in an infectious strain background. Infect. Immun. 70:2139-2150.
14. Feng, S., S. W. Barthold, S. R. Telford III, and E. Fikrig. 1996. P55, an immunogenic but nonprotective 55-kilodalton Borrelia burgdorferi protein in murine Lyme disease. Infect. Immun. 64:363-365.
15. Feng, S., S. Das, T. Lam, R. A. Flavell, and E. Fikrig. 1995. A 55-kilodalton antigen encoded by a gene on a Borrelia burgdorferi 49-kilobase plasmid is recognized by antibodies in sera from patients with Lyme disease. Infect. Immun. 63:3459-3466.
16. Fingerle, V., G. Goettner, L. Gern, B. Wilske, and U. Schulte-Spechtel. 2007. Complementation of a Borrelia afzelii OspC mutant highlights the crucial role of OspC for dissemination of Borrelia afzelii in Ixodes ricinus. Int. J. Med. Microbiol. 297:97-107.
17. 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 Ixodes ricinus nymphs. J. Clin. Microbiol. 40:1456-1463.
18. Fischer, J. R., K. T. LeBlanc, and J. M. Leong. 2006. Fibronectin binding protein BBK32 of the Lyme disease spirochete promotes bacterial attachment to glycosaminoglycans. Infect. Immun. 74:435-441.
19. 54 is required for mammalian infection and vector transmission but not for tick colonization. Proc. Natl. Acad. Sci. U.S.A. 102:5162-5167.
20. Frank, K. L., S. F. Bundle, M. E. Kresge, C. H. Eggers, and D. S. Samuels. 2003. aadA confers streptomycin resistance in Borrelia burgdorferi. J. Bacteriol. 185:6723-6727.
21. 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.
22. Gautam, A., M. Hathaway, N. McClain, G. Ramesh, and R. Ramamoorthy. 2008. Analysis of the determinants of bba64 (P35) gene expression in Borrelia burgdorferi using a gfp reporter. Microbiology 154:275-285.
23. Gilbert, M. A., E. A. Morton, S. F. Bundle, and D. S. Samuels. 2007. Artificial regulation of ospC expression in Borrelia burgdorferi. Mol. Microbiol. 63: 1259-1273.
24. Gilmore, R. D., and J. Piesman. 2000. Inhibition of Borrelia burgdorferi migration from the midgut to the salivary glands following feeding by ticks on OspC-immunized mice. Infect. Immun. 68:411-414.
25. Gilmore, R. D., Jr., R. R. Howison, V. L. Schmit, A. J. Nowalk, D. R. Clifton, C. Nolder, J. L. Hughes, and J. A. Carroll. 2007. Temporal expression analysis of the Borrelia burgdorferi paralogous gene family 54 genes BBA64, BBA65, and BBA66 during persistent infection in mice. Infect. Immun. 75:2753-2764.
26. Grimm, D., K. Tilly, R. Byram, P. E. Stewart, J. G. Krum, D. M. Bueschel, T. G. Schwan, P. F. Policastro, A. F. Elias, and P. A. Rosa. 2004. Outersurface protein C of the Lyme disease spirochete: a protein induced in ticks for infection of mammals. Proc. Natl. Acad. Sci. U.S.A. 101:3142-3147.
27. 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.
28. He, M., B. K. Boardman, D. Yan, and X. F. Yang. 2007. Regulation of expression of the fibronectin-binding protein BBK32 in Borrelia burgdorferi. J. Bacteriol. 189:8377-8380.
29. Hübner, 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. U.S.A. 98:12724-12729.
30. Kawabata, H., S. J. Norris, and H. Watanabe. 2004. BBE02 disruption mutants of Borrelia burgdorferi B31 have a highly transformable, infectious phenotype. Infect. Immun. 72:7147-7154.
31. 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.
32. Li, X., X. Liu, D. S. Beck, F. S. Kantor, and E. Fikrig. 2006. Borrelia burgdorferi lacking BBK32, a fibronectin-binding protein, retains full pathogenicity. Infect. Immun. 74:3305-3313.
33. Li, X., G. Neelakanta, X. Liu, D. S. Beck, F. S. Kantor, D. Fish, J. F. Anderson, and E. Fikrig. 2007. Role of outer surface protein D in the Borrelia burgdorferi life cycle. Infect. Immun. 75:4237-4244.
34. 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.
35. 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.
36. Lybecker, M. C., and D. S. Samuels. 2007. Temperature-induced regulation of RpoS by a small RNA in Borrelia burgdorferi. Mol. Microbiol. 64:1075-1089.
37. Maruskova, M., M. D. Esteve-Gassent, V. L. Sexton, and J. Seshu. 2008. Role of the BBA64 locus of Borrelia burgdorferi in early stages of infectivity in a murine model of Lyme disease. Infect. Immun. 76:391-402.
38. Maruskova, M., and J. Seshu. 2008. Deletion of BBA64, BBA65, and BBA66 loci does not alter the infectivity of Borrelia burgdorferi in the murine model of Lyme disease. Infect. Immun. 76:5274-5284.
39. McDowell, J. V., S. Y. Sung, M. Labandeira-Rey, J. T. Skare, and R. T. Marconi. 2001. Analysis of mechanisms associated with loss of infectivity of clonal populations of Borrelia burgdorferi B31MI. Infect. Immun. 69:3670-3677.
40. Medrano, M. S., Y. Ding, X. G. Wang, P. Lu, J. Coburn, and L. T. Hu. 2007. Regulators of expression of the oligopeptide permease A proteins of Borrelia burgdorferi. J. Bacteriol. 189:2653-2659.
41. Montgomery, R. R., S. E. Malawista, K. J. M. Feen, and L. K. Bockenstedt. 1996. Direct demonstration of antigenic substitution of Borrelia burgdorferi ex vivo: exploration of the paradox of the early immune response to outer surface proteins A and C in Lyme disease. J. Exp. Med. 183:261-269.
42. 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. U.S.A. 98:670-675.
43. 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.
44. Ouyang, Z., J. S. Blevins, and M. V. Norgard. 2008. Transcriptional interplay among the regulators Rrp2, RpoN, and RpoS in Borrelia burgdorferi. Microbiology 154:2641-2658.
45. Pal, U., J. Dai, X. Li, G. Neelakanta, P. Luo, M. Kumar, P. Wang, X. Yang, J. Anderson, and E. Fikrig. 2008. A differential role for BB0365 in the persistence of Borrelia burgdorferi in mice and ticks. J. Infect. Dis. 197:148-155.
46. Pal, U., and E. Fikrig. 2003. Adaptation of Borrelia burgdorferi in the vector and vertebrate host. Microbes Infect. 5:659-666.
47. Pal, U., X. Li, T. Wang, R. R. Montgomery, N. Ramamoorthi, A. M. deSilva, F. Bao, X. Yang, M. Pypaert, and D. Pradhan. 2004. TROSPA, an Ixodes scapularis receptor for Borrelia burgdorferi. Cell 119:457-468.
48. Pal, U., X. Yang, M. Chen, L. K. Bockenstedt, J. F. Anderson, R. A. Flavell, M. V. Norgard, and E. Fikrig. 2004. OspC facilitates Borrelia burgdorferi invasion of Ixodes scapularis salivary glands. J. Clin. Invest. 113:220-230.
49. 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.
50. Radolf, J. D., and M. J. Caimano. 2008. The long strange trip of Borrelia burgdorferi outer-surface protein C. Mol. Microbiol. 69:1-4.
51. Ramamoorthi, N., S. Narasimhan, U. Pal, F. Bao, X. F. Yang, D. Fish, J. Anguita, M. V. Norgard, F. S. Kantor, J. F. Anderson, R. A. Koski, and E. Fikrig. 2005. The Lyme disease agent exploits a tick protein to infect the mammalian host. Nature 436:573-577.
52. 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. U.S.A. 99:1562-1567.
53. Samuels, D. S. 1995. Electrotransformation of the spirochete Borrelia burgdorferi, p. 253-259. In J. A. Nickoloff (ed.), Methods in molecular biology. Humana Press, Totowa, NJ.
54. Schwan, T. G. 2003. Temporal regulation of outer surface proteins of the Lyme-disease spirochete Borrelia burgdorferi. Biochem. Soc. Trans. 31:108-112.
55. 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.
56. 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. U.S.A. 92:2909-2913.
57. Seshu, J., M. D. Esteve-Gassent, M. Labandeira-Rey, J. H. Kim, J. P. Trzeciakowski, M. Hook, and J. T. Skare. 2006. Inactivation of the fibronectin-binding adhesin gene bbk32 significantly attenuates the infectivity potential of Borrelia burgdorferi. Mol. Microbiol. 59:1591-1601.
58. Shi, Y., Q. Xu, K. McShan, and F. T. Liang. 2008. Both decorin-binding proteins A and B are critical for the overall virulence of Borrelia burgdorferi. Infect. Immun. 76:1239-1246.
59. Singh, S. K., and H. J. Girschick. 2004. Molecular survival strategies of the Lyme disease spirochete Borrelia burgdorferi. Lancet Infect. Dis. 4:575-583.
60. N). J. Bacteriol. 189:2139-2144.
61. Stewart, P. E., A. Bestor, J. N. Cullen, and P. A. Rosa. 2008. A tightly regulated surface protein of Borrelia burgdorferi is not essential to the mousetick infectious cycle. Infect. Immun. 76:1970-1978.
62. Stewart, P. E., X. Wang, D. M. Bueschel, D. R. Clifton, D. Grimm, K. Tilly, J. A. Carroll, J. J. Weis, and P. A. Rosa. 2006. Delineating the requirement for the Borrelia burgdorferi virulence factor OspC in the mammalian host. Infect. Immun. 74:3547-3553.
63. Tilly, K., J. G. Krum, A. Bestor, M. W. Jewett, D. Grimm, D. Bueschel, R. Byram, D. Dorward, M. J. VanRaden, P. Stewart, and P. Rosa. 2006. Borrelia burgdorferi OspC protein required exclusively in a crucial early stage of mammalian infection. Infect. Immun. 74:3554-3564.
64. 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.
65. Xu, Q., K. McShan, and F. T. Liang. 2007. Identification of an ospC operator critical for immune evasion of Borrelia burgdorferi. Mol. Microbiol. 64:220-231.
66. Xu, Q., K. McShan, and F. T. Liang. 2008. Verification and dissection of the ospC operator by using flaB promoter as a reporter in Borrelia burgdorferi. Microb. Pathog. 45:70-78.
67. 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.
68. Yang, X., T. G. Popova, K. E. Hagman, S. K. Wikel, G. B. Schoeler, M. J. Caimano, J. D. Radolf, and M. V. Norgard. 1999. Identification, characterization, and expression of three new members of the Borrelia burgdorferi Mlp (2.9) lipoprotein gene family. Infect. Immun. 67:6008-6018.
69. 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. U.S.A. 100:11001- 11006.
70. Yang, X. F., U. Pal, S. M. Alani, E. Fikrig, and M. V. Norgard. 2004. Essential role for OspA/B in the life cycle of the Lyme disease spirochete. J. Exp. Med. 199:641-648.
71. Yang, X., A. S. Coleman, J. Anguita, and U. Pal. 2009. A chromosomally encoded virulence factor protects the Lyme disease pathogen against hostadaptive immunity. PLoS Pathog. 5:e1000326.