Decorin-binding protein of Borrelia burgdorferi is encoded within a two- gene operon and is protective in the murine model of Lyme borreliosis

Infection and Immunity

Volumn 66, Issue 6, 1998, Pages 2674-2683

  Hagman, Kayla E ^a   Lahdenne, Pekka ^b   Popova, Taissla G ^a   Porcella, Stephen F ^a,d   Akins, Darrin R ^a   Radolf, Justin D ^a   Norgard, Michael V ^a,c  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b UNIVERSITY OF HELSINKI   (Finland)

^c UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^d NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; DECORIN;

AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIUM ISOLATION; BORRELIA BURGDORFERI; CONTROLLED STUDY; GENETIC CODE; IMMUNOREACTIVITY; LYME DISEASE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; OPERON; OUTER MEMBRANE; PRIORITY JOURNAL; PROTEIN MODIFICATION;

BORRELIA BURGDORFERI;

EID: 0031812736     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/iai.66.6.2674-2683.1998     Document Type: Article

References (66)

1. Aebersold, R. H., B. T. David, L. E. Hood, and S. B. H. Kent. 1986. Electroblotting onto activated glass. J. Biol. Chem. 261:4229-4238.
2. Aebersold, R. H., J. Leavitt, R. A. Saavedra, L. E. Hood, and S. B. H. Kent. 1987. Internel amino acid sequence analysis of proteins separated by one- or two-dimensional gel electrophoresis by in situ protease digestion on nitrocellulose. Proc. Natl. Acad. Sci. USA 84:6970-6974.
3. Akins, D. R., S. F. Porcella, T. G. Popova, D. Shevchenko, 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.
4. Altschul, S. F., W. Gish, W. Miller, E. W. Myers, and D. J. Lipman. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.
5. Andrews, P. C., and J. E. Dixon. 1987. A procedure for in situ alkylation of cysteine residues on glass fiber prior to protein microsequence analysis. Anal. Biochem. 161:524-528.
6. Aydintug, M. K., Y. Gu, and M. T. Philipp. 1994. Borrelia burgdorferi antigens that arc targeted by antibody-dependent, complement-mediated killing in the rhesus monkey. Infect. Immun. 62:4929-4937.
7. Barbour, A. G. 1984. Isolation and cultivation of Lyme disease spirochetes. Yale J. Biol. Med. 57:521-525.
8. Barbour, A. G., and C. F. Garon. 1987. Linear plasmids of the bacterium Borrelia burgdorferi have covalently closed ends. Science 237:409-411.
9. Barbour, A. G., S. L. Tessier, and W. J. Todd. 1983. Lyme disease spirochetes and ixodid tick spirochetes share a common surface antigenic determinant defined by a monoclonal antibody. Infect. Immun. 41:795-804.
10. Barthold, S. W., and L. K. Bockenstedt. 1993. Passive immunizing activity of sera from mice infected with Borrelia burgdorferi. Infect. Immun. 61:4696-4702.
11. Barthold, S. W., M. S. deSouza, J. L. Janotka, A. L. Smith, and D. H. Persing. 1993. Chronic Lyme borreliosis in the laboratory mouse. Am. J. Pathol. 143:959-971.
12. Barthold, S. W., E. Fikrig, L. K. Bockenstedt, and D. H. Persing. 1995. Circumvention of outer surface protein A immunity by host-adapted Borrelia burgdorferi. Infect. Immun. 63:2255-2261.
13. Barthold, S. W., D. H. Persing, A. L. Armstrong, and R. A. Peeples. 1991. Kinetics of Borrelia burgdorferi dissemination and evolution of disease after intradermal inoculation of mice. Am. J. Pathol. 139:263-273.
14. Belisle, J. T., M. E. Brandt, J. D. Radolf, and M. V. Norgard. 1994. Fatty acids of Treponema pallidum and Borrelia burgdorferi lipoproteins. J. Bacteriol. 176:2151-2157.
15. Bledsoe, H. A., J. A. Carroll, T. R. Whelchel, M. A. Farmer, D. W. Dorward, and F. C. Gherardini. 1994. Isolation and partial characterization of Borrelia burgdorferi inner and outer membranes by using isopycnic centrifugation. J. Bacteriol. 176:7447-7455.
16. Brusca, J. S., A. W. McDowall, M. V. Norgard, and J. D. Radolf. 1991. Localization of outer surface proteins A and B in both the outer membrane and intracellular compartments of Borrelia burgdorferi. J. Bacteriol. 173: 8004-8008.
17. Brusca, J. S., and J. D. Radolf. 1994. Isolation of integral membrane proteins by phase partitioning with Triton X-114. Methods Enzymol. 228:182-193.
18. Bundoc, V. G., and A. G. Barbour. 1989. Clonal polymorphisms of outer membrane protein OspB of Borrelia burgdorferi. Infect. Immun. 57:2733-2741.
19. 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.
20. Caporale, D. A., and T. D. Kocher. 1994. Sequence variation in the outer-surface-protein genes of Borrelia burgdorferi. Mol. Biol. Evol. 11:51-64.
21. Champion, C. I., C. R. Blanco, J. T. Skare, D. A. Haake, M. Giladi, D. Foley, J. N. Miller, and M. A. Lovett. 1994. A 9.0-kilobase-pair circular plasmid of Borrelia burgdorferi encodes an exported protein: evidence for expression only during infection. Infect. Immun. 62:2653-2661.
22. Coleman, J. L., R. C. Rogers, and J. L. Benach. 1992. Selection of an escape variant of Borrelia burgdorferi by use of bactericidal monoclonal antibodies to OspB. Infect. Immun. 60:3098-3104.
23. Cox, D. L., D. R. Akins, K. W. Bourell, P. Lahdenne, M. V. Norgard, and J. D. Radolf. 1996. Limited surface exposure of Borrelia burgdorferi outer surface lipoproteins. Proc. Natl. Acad. Sci. USA 93:7973-7978.
24. deSilva, 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.
25. Devereux, J., P. Haeberli, and O. Smithies. 1984. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 12:387-395.
26. 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.
27. Fikrig, E., S. W. Barthold, F. S. Kantor, and R. A. Flavell. 1990. Protection of mice against the Lyme disease agent by immunizing with recombinant OspA. Science 250:553-556.
28. 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.
29. Guo, B. P., S. J. Norris, L. C. Rosenberg, and M. Höök. 1995. Adherence of Borrelia burgdorferi to the proteoglycan decorin. Infect. Immun. 63:3467-3472.
30. Hagman, K. E., P. Lahdenne, T. G. Popova, K. Bourell, D. R. Akins, J. D. Radolf, and M. V. Norgard. Unpublished observations.
31. Hayashi, S., and H. C. Wu. 1990. Lipoproteins in bacteria. J. Bioenerg. Biomembr. 22:451-471.
32. Hinnebusch, J., and A. G. Barbour. 1992. Linear and circular plasmid copy numbers in Borrelia burgdorferi. J. Bacteriol. 174:5251-5257.
33. Johnson, R. C., C. Kodner, and M. Russell. 1986. Passive immunization of hamsters against experimental infection with the Lyme disease spirochete. Infect. Immun. 53:713-714.
34. Jonsson, M., and S. Bergstrom. 1995. Transcriptional and translational regulation of the expression of the major outer surface proteins in Lyme disease Borrelia strains. Microbiology 141:1321-1329.
35. Kochi, S. K., and R. C. Johnson. 1988. Role of immunoglobulin G in killing of Borrelia burgdorferi by the classical complement pathway. Infect. Immun. 56:314-321.
36. Kochi, S. K., R. C. Johnson, and A. P. Dalmasso. 1991. Complement-mediated killing of the Lyme disease spirochete Borrelia burgdorferi: role of antibody in formation of an effective membrane attack complex. J. Immunol. 146:3964-3970.
37. Lahdenne, P., S. F. Porcella, K. E. Hagman, D. R. Akins, T. G. Popova, D. L. Cox, L. I. Katona, J. U. Radolf, and M. V. Norgard. 1997. Molecular characterization of a 6.6-kilodalton Borrelia burgdorferi outer membrane-associated lipoprotein (Ip6.6) which appears to be downregulated during mammalian infection. Infect. Immun. 65:412-421.
38. Lam, T. T., T.-P. K. Nguyen, R. R. Montgomery, F. S. Kantor, E. Fikrig, and R. A. Flavell. 1994. Outer surface proteins E and F of Borrelia burgdorferi, the agent of Lyme disease. Infect. Immun. 62:290-298.
39. Ma, J., and R. T. Coughlin. 1993. A simple, colorimetric microtiter assay for borreliacidal activity of antisera. J. Microbiol. Methods 17:145-153.
40. Mathiesen, D. A., J. H. Oliver, C. P. Kolbert, E. D. Tullson, B. J. B. Johnson, G. L. Campbell, P. D. Mitchell, K. D. Reed, S. R. Telford, 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. Matsudaira, P. 1987. Sequence from picomole quantities of proteins electroblotted onto polyvinylidene difluoride membranes. J. Biol. Chem. 262: 10035-10038.
42. 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.
43. Morbidity and Mortality Weekly Report. 1997. Lyme disease - United States, 1996. Morbid. Mortal. Weekly Rep. 46:531-535.
44. Norris, S. J., C. J. Carter, J. K. Howell, and A. G. Barbour. 1992. Low-passage-associated proteins of Borrelia burgdorferi B31: characterization and molecular cloning of OspD, a surface-exposed, plasmid-encoded lipoprotein. Infect. Immun. 60:4662-4672.
45. Padilla, M. L., S. M. Callister, R. F. Schell, G. L. Bryant, D. A. Jobe, S. D. Lovrich, B. K, DuChateau, and J. R. Jensen. 1996. Characterization of the protective borreliacidal antibody response in humans and hamsters after vaccination with Borrelia burgdorferi outer surface protein A vaccine. J. Infect. Dis. 174:739-746.
46. Platt, T. 1986. Transcription termination and the regulation of gene expression. Annu. Rev. Biochem. 55:339-372.
47. Porcella, S. F., T. G. Popova, D. R. Akins, M. Li, J. D. Radolf, and M. V. Norgard. 1996. Borrelia burgdorferi supercoiled plasmids encode multicopy tandem open reading frames and a lipoprotein gene family. J. Bacteriol. 178:3293-3307.
48. Probert, W. S., K. M. Allsup, and R. B. LeFebvre. 1995. Identification and characterization of a surface-exposed, 66-kilodalton protein from Borrelia burgdorferi. Infect. Immun. 63:1933-1939.
49. Radolf, J. D., M. S. Goldberg, K. Bourell, S. I. Baker, J. D. Jones, and M. V. Norgard. 1995. Characterization of outer membranes isolated from Borrelia burgdorferi, the Lyme disease spirochete. Infect. Immun. 63:2154-2163.
50. Roehrig, J. T., J. Piesman, A. R. Hunt, M. G. Keen, C. M. Happ, and B. J. B. Johnson. 1992. The hamster immune response to tick-transmitted Borrelia burgdorferi differs from the response to needle-inoculated, cultured organisms. J. Immunol. 149:3648-3653.
51. Sadziene, A., P. A. Thompson, and A. G. Barbour. 1993. In vitro inhibition of Borrelia burgdorferi growth by antibodies. J. Infect. Dis. 167:165-172.
52. Sadziene, A., B. Wilske, M. S. Ferdows, and A. G. Barbour. 1993. The cryptic ospC gene of Borrelia burgdorferi B31 is located on a circular plasmid. Infect. Immun. 61:2192-2195.
53. Schaible, U. E., L. Gern, R. Wallich, M. D. Kramer, M. Prester, and M. M. Simon. 1993. Distinct patterns of protective antibodies are generated against Borrelia burgdorferi in mice experimentally inoculated with high and low doses of antigen. Immunol. Lett. 36:219-226.
54. Schoen, R. T., F. Meurice, C. M. Brunet, S. Cretella, D. S. Krause, J. E. Craft, and E. Fikrig. 1995. Safety and immunogenicity of an outer surface protein A vaccine in subjects with previous Lyme disease. J. Infect. Dis. 172:1324-1329.
55. 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.
56. Schwartz, J. J., A. Gazumyan, and I. Schwartz. 1992. rRNA gene organization in the Lyme disease spirochete, Borrelia burgdorferi. J. Bacteriol. 174: 3757-3765.
57. Simon, M. M., U. E. Schaible, M. D. Kramer, C. Eckerskorn, C. Museteanu, H. K. Muller-Hermelink, and R. Wallich. 1991. Recombinant outer surface protein A from Borrelia burgdorferi induces antibodies protective against spirochetal infection in mice. J. Infect. Dis. 164:123-132.
58. Simpson, W. J., W. Cieplak, M. E. Schrumpf, A. G. Barbour, and T. G. Schwan. 1994. Nucleotide sequence and analysis of the gene in Borrelia burgdorferi encoding the immunogenic P39 antigen. FEMS Microbiol. Lett. 119:381-388.
59. Sinsky, R. J., and j. Piesman. 1989. Ear punch biopsy method for detection and isolation of Borrelia burgdorferi from rodents. J. Clin. Microhiol. 27: 1723-1727.
60. Skare, J. T., E. S. Shang, D. M. Foley, D. R. Blanco, C. I. Champion, T. Mirzabekov, Y. Sokolov, B. L. Kagan, J. N. Miller, and M. A. Lovett. 1995. Virulent strain associated outer membrane proteins of Borrelia burgdorferi. J. Clin. Invest. 96:2380-2392.
61. Steere, A. C. 1995. Borrelia burgdorferi (Lyme disease, Lyme borreliosis), p. 2143-2155. In G. L. Mandell, J. E. Bennett, and R. Dolin (ed.), Principles and practice of infectious diseases. Churchill Livingstone, New York, N.Y.
62. 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.
63. Van Hoecke, C., M. Comberbach, D. De Grave, P. Desmons, D. Fu, P. Hauser, E. Lebacq, Y. Lobet, and P. Voet. 1996. Evaluation of the safety, reactogenicity and immunogenicity of three recombinant outer surface protein (OspA) Lyme vaccines in healthy adults. Vaccine 14:1620-1626.
64. Wallich, R., C. Brenner, M. D. Kramer, and M. M. Simon. 1995. Molecular cloning and immunological characterization of a novel linear-plasmid-encoded gene, pG, of Borrelia burgdorferi expressed only in vivo. Infect. Immun. 63:3327-3335.
65. Wilske, B., V. Preac-Mursic, S. Jauris, A. Hofmann, I. Pradel, E. Soutschek, E. Schwab, G. Will, and G. Wanner. 1993. Immunological and molecular polymorphisms of OspC. an immunodominant major outer surface protein of Borrelia burgdorferi. Infect. Immun. 61:2182-2191.
66. Yuen, S., M. W. Hunkapiller, K. J. Wilson, and P. M. Yuan. 1986. SDS-PAGE electroblotting. Applied Biosystems User Bull. 25:1-15.