The failure of immune response evasion by linear plasmid 28-1-deficient Borrelia burgdorferi is attributable to persistent expression of an outer surface protein

Infection and Immunity

Volumn 76, Issue 9, 2008, Pages 3984-3991

  Embers, Monica E ^a   Alvarez, Xavier ^a   Ooms, Tara ^a   Philipp, Mario T ^a  

^a TULANE NATIONAL PRIMATE RESEARCH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; MESSENGER RNA; OUTER SURFACE PROTEIN C; OUTER SURFACE PROTEIN C ANTIBODY; PROTEIN ANTIBODY; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL INFECTION; BORRELIA BURGDORFERI; CONTROLLED STUDY; DIALYSIS MEMBRANE; DOWN REGULATION; GENE; HOST; IMMUNE RESPONSE; MOUSE; NONHUMAN; PERITONEAL CAVITY; PLASMID; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT;

ANIMALS; ANTIBODIES, BACTERIAL; ANTIGENS, BACTERIAL; BACTERIAL OUTER MEMBRANE PROTEINS; BORRELIA BURGDORFERI; DOWN-REGULATION; GENE EXPRESSION REGULATION, BACTERIAL; LIPOPROTEINS; MICE; MICE, SCID; PLASMIDS;

EID: 51949109424     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.00387-08     Document Type: Article

References (45)

1. Akins, D. R., K. W. Bourell, M. J. Caimano, M. V. Norgard, and J. D. Radolf. 1998. A new animal model for studying Lyme disease spirochetes in a mammalian host-adapted state. J. Clin. Investig. 101:2240-2250.
2. Bankhead, T., and G. Chaconas. 2007. The role of VlsE antigenic variation in the Lyme disease spirochete: persistence through a mechanism that differs from other pathogens. Mol. Microbiol. 65:1547-1558.
3. Barbour, A. G., S. F. Hayes, R. A. Heiland, M. E. Scnrumpf, aad S. L. Tessier. 1986. A Bomefia-specific monoclonal antibody binds to a flagellar epitope. Infect. Immun. 52:549-554.
4. 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.
5. Casjens, S., N. Palmer, R. van Vugt, W. M. Huang, B. Stevenson, P. Rosa, R. Lathigra, G. Sutton, J. Peterson, R. J. Dodson, D. Hall, 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.
6. Crother, T. R., C. I. Champion, J. P. Whitelegge, R. Aguilera, X.-Y. Wu, D. R. Blanco, J. N. Miller, and M. A. Lovett. 2004. Temporal analysis of the antigenic composition of Borrelia burgdorferi during infection in rabbit skin. Infect. Immun. 72:5063-5072.
7. Crother, T. R., C. I. Champion, X.-V. 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.
8. Embers, M. E., R. Ramamoorthy, and M. T. Philipp. 2004. Survival strategies of Borrelia burgdorferi, the etiologic agent of Lyme disease. Microbes Infect. 6:312-316.
9. Feng, S., E. Hodzic, and S. W. Barthold. 2000. Lyme arthritis resolution with antiserum to a 37-kilodalton Borrelia burgdorferi protein. Infect. Immun. 68:4169-4173.
10. Fraser, C. M., S. Casjens, W. M. Huang, G. G. Sutton, R. Clayton, R. Lathigra, O. White, K. A. Ketchum, R. Dodson, E. K. Hkkey, M. Gwinn, B. Dougherty, J.-F. Tomb, R. D. Fleischmann, D. Richardson, J. Peterson, A. R. Keriavage, 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 390:380-586.
11. 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.
12. 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. Outer-surface protein C of the Lyme disease spirochete: a protein induced in ticks for infection of mammals. Proc. Natl. Acad. Sci. USA 101:3142-3147.
13. Hefty, P. S, S. E. Jollif, M. J. Caimano, S. K. Wikel, and D. R. Akins. 2002. Changes in temporal and spatial patterns of outer surface lipoprotein expression generate population heterogeneity and antigenic diversity in the Lyme disease spirochete, Borrelia burgdorferi. Infect. Immun. 70:3468-3478.
14. 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.
15. 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.
16. 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.
17. 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.
18. 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.
19. Lawrenz, M. B., R. M. Wooten, and S. J. Norris. 2004. Effects of vlsE complementation on the infectivity of Borrelia burgdorferi lacking the linear plasmid lp28-l. Infect. Immun. 72:6577-6585.
20. 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.
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., 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.
23. Mbow, M. L., R. D. Gilmore, Jr., and R. G. Titus. 1999. An OspC-specific monoclonal antibody passively protects mice from tick-transmitted infection by Borrelia burgdorferi B31. Infect. Immun. 67:5470-5472.
24. National Research Council. 1996. Guide for the care and use of laboratory animals. National Academy Press, Washington, DC.
25. Norton, J. J., and A. C. Steere. 1995. Lyme disease. Adv. Intern. Med. 40:69-117.
26. Pfaffl, M. W. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29:e45.
27. Pfaffl, M. W., G. W. Horgan, and L. Dempfle. 2002. Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res. 30:e36.
28. 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.
29. Ramamoorthy, R., and M. T. Philipp. 1998. Differential expression of Borrelia burgdorferi proteins during growth in vitro. Infect. Immun. 66:5119-5124.
30. 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.
31. 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.
32. Seiler, K. P., and J. J. Weis. 1996. Immunity to Lyme disease: protection, pathology and persistence. Curr. Opin. Immunol. 8:503-509.
33. Sigal, L. H. 1997. Lyme diseases review of aspects of its immunology and immunopathogenesis. Annu. Rev. Immunol. 15:63-92.
34. Steere, A. C, and L. Giickstein. 2004. Elucidation of Lyme arthritis. Nat. Rev. Immunol. 4:143-152.
35. Stevenson, B., T. G. Scbwan, and P. A. Rosa. 1995. Temperature-related differential expression of antigens in the Lyme disease spirochete, Borrelia burgdorferi. Infect. Immun. 63:4535-4539.
36. Stewart, P. E., R. Byram, D. Grimm, K. Tilly, and P. A. Rosa. 2005. The plasmids of Borrelia burgdorferi: essential genetic elements of a pathogen. Plasmid 53:1-13.
37. Thomas, V., J. Anguita, S. Samanta, P. A. Rosa, P. Stewart, S. W. Barthold, and E. Fikrig. 2001. Dissociation of infectivity and pathogenicity in Borrelia burgdorferi. Infect. Immun. 69:3507-3509.
38. Tilly, K., A. Bestor, M. W. Jewett, and P. Rosa. 2007. Rapid clearance of Lyme disease spirochetes lacking OspC from skin. Infect. Immun. 75:1517-1519.
39. 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.
40. Xu, Q., S. V. Seemanapalli, K. McShan, and F. T. Liang. 2006. Constitutive expression of outer surface protein C diminishes the ability of Borrelia burgdorferi to evade specific humoral immunity. Infect. Immun. 74:5177-5184.
41. 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.
42. 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.
43. (Erratum, 96:447, 1999.)
44. 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.
45. (Erratum, 67 :468, 1999.)