Molecular characterization of a 6.6-kilodalton Borrelia burgdorferi outer membrane-associated lipoprotein (lp6.6) which appears to be downregulated during mammalian infection

Infection and Immunity

Volumn 65, Issue 2, 1997, Pages 412-421

  Lahdenne, Pekka ^a,b   Porcella, Stephen F ^a   Hagman, Kayla E ^a   Akins, Darrin R ^a   Popova, Taissia G ^a   Cox, David L ^c   Katona, Laura I ^d   Radolf, Justin D ^a   Norgard, Michael V ^a,e  

^a UNIVERSITY OF TEXAS AT DALLAS   (United States)

^b UNIVERSITY OF HELSINKI   (Finland)

^c CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

^d STONY BROOK UNIVERSITY   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

LIPOPROTEIN; OUTER MEMBRANE PROTEIN; SIGNAL PEPTIDE;

ACYLATION; AMINO ACID SEQUENCE; ARTICLE; BORRELIA BURGDORFERI; CONSENSUS SEQUENCE; DNA SEQUENCE; GENE EXPRESSION REGULATION; IMMUNOBLOTTING; INFECTION; NONHUMAN; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN PROCESSING;

EID: 0031020230     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/iai.65.2.412-421.1997     Document Type: Article

References (63)

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. Internal 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 84:6470-6974.
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 are targeted by antibody-dependent, complement-mediated killing in the rhesus monkey. Infect. Immun. 62:4929-1937.
7. Barbour, A. G. 1984. Isolation and cultivation of Lyme disease spirochetes. Yale J. Biol. Med. 57:521-525.
8. Barbour, A. G., W. Burgdorfer, E. Grunwaldt, and A. C. Steere. 1983. Antibodies of patients with Lyme disease to components of the Ixodes dammini spirochete. J. Clin. Invest. 72:504-515.
9. Barbour, A. G., and C. F. Garon. 1987. Linear plasmids of the bacterium Borrelia burgdorferi have covalently closed ends. Science 237:409-411.
10. 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.
11. Barthold, S. W., and L. K. Bockenstedt. 1993. Passive immunizing activity of sera from mice infected with Borrelia burgdorferi. Infect. Immun. 61:4696-4702.
12. 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.
13. 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.
14. 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.
15. 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.
16. Bledsoe, H. A., J. A. Carroll, T. R. Whelchel, M. A. Farmer, D. W. Dorward, and F. C. Gherardini. 1994. Isolation and partial characterization at Borrelia burgdorferi inner and outer membranes by using isopycnic centrifugation. J. Bacteriol. 176:7447-7455.
17. 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.
18. Brusca, J. S., and J. D. Radolf. 1994. Isolation of integral membrane proteins hv phase partitioning with Triton X-114. Methods Enzymol. 228:182-193.
19. Burgdorfer, W. 1989. Vector/host relationships of the Lyme disease spirochete. Borrelia burgdorferi. Rheum. Dis. Clin. N. Am. 15:775-787.
20. Centers for Disease Control and Prevention. 1996. Lyme disease - United States, 1995. Morbid. Mortal. Weekly Rep. 46:481-484.
21. Champion, C. I., D. 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. 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.
23. Cox, D. L., D. R. Akins, S. F. Porcella, M. V. Norgard, and J. D. Radolf. 1995. Treponema pallidum in gel microdroplets: a novel strategy for investigation of treponemal molecular architecture. Mol. Microbiol. 15:1151-1164.
24. Craft, J. E., D. K. Fischer, G. T. Shimamoto, and A. C. Steere. 1986. Antigens of Borrelia burgdorferi recognized during Lyme disease. Appearance of a new immunoglobulin M response and expansion of the immunoglobulin G response late in the illness. J. Clin. Invest. 78:934-939.
25. 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.
26. Devereux, J., P. Haeberli, and O. Smithies. 1984. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 12:387-395.
27. Dressler, F., J. A. Whalen, B. N. Reinhardt, and A. C. Steere. 1993. Western blotting in the serodiagnosis of Lyme disease. J. Infect. Dis. 167:392-400.
28. Engstrom, S. M., E. Shoop, and R. C. Johnson. 1995. Immunoblot interpretation criteria for serodiagnosis of early Lyme disease. J. Clin. Microbiol. 33:419-427.
29. 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.
30. 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.
31. Hayashi, S., and H. C. Wu. 1990. Lipoproteins in bacteria. J. Bioenerg. Biomembr. 22:451-471.
32. Jones, J. D., K. W. Bourell, M. V. Norgard, and J. D. Radolf. 1995. Membrane topology of Borrelia burgdorferi and Treponema pallidum lipoproteins. Infect. Immun. 63:2424-2434.
33. 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.
34. Katona, L. I., G. Beck, and G. S. Habicht. 1992. Purification and immunological characterization of a major low-molecular-weight lipoprotein from Borrelia burgdorferi. Infect. Immun. 60:4995-5003.
35. Katona, L. I., and G. S. Habicht. 1996. Unpublished observations.
36. Kyte, J., and R. F. Doolittle. 1982. A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157:105-132.
37. 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.
38. Levine, J. F., M. L. Wilson, and A. Spielman. 1985. Mice as reservoirs of the Lyme disease spirochete. Am. J. Trop. Med. Hyg. 34:355-360.
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. Matsudaira, P. 1987. Sequence from picomole quantities of proteins electroblotted onto polyvinylidene difluoride membranes. J. Biol. Chem. 262: 10035-10038.
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. Philipp, M. T., K. Aydintug, R. P. Bohm, F. B. Cogswell, V. A. Dennis, H. N. Lanners, R. C. Lowrie, E. D. Roberts, M. D. Conway, M. Karacorlu, G. A. Peyman, D. J. Gubler, B. J. B. Johnson, J. Piesman, and Y. Gu. 1993. Early and early disseminated phases of Lyme disease in the rhesus monkey: a model for infection in humans. Infect. Immun. 61:3047-3059.
43. Platt, T. 1986. Transcription termination and the regulation of gene expression. Annu. Rev. Biochem. 55:339-372.
44. 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.
45. Pugsley, A. P. 1993. The complete general secretory pathway in gram-negative bacteria. Microbiol. Rev. 57:50-108.
46. Radolf, J. D., K. W. Bourell, D. R. Akins, J. S. Brusca, and M. V. Norgard. 1994. Analysis of Borrelia burgdorferi membrane architecture by freeze-fracture electron microscopy. J. Bacteriol. 176:21-31.
47. 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.
48. Roberts, E. D., R. P. Bohm, F. B. Cogswell, H. N. Lanners, R. C. Lowrie, L. Povinelli, J. Piesman, and M. T. Philipp. 1995. Chronic Lyme disease in the rhesus monkey. Lab. Invest. 72:146-160.
49. 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.
50. 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.
51. 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.
52. Sambri, V., A. Moroni, F. Massaria, E. Brocchi, F. De Simone, and R. Cevenini. 1991. Immunological characterization of a low molecular mass polypeptidic antigen of Borrelia burgdorferi. FEMS Microbiol. Immunol. 76:345-350.
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. 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.
55. Schwartz, J. J., A. Gazumyan, and I. Schwartz. 1992. rRNA gene organization in the Lyme disease spirochete, Borrelia burgdorferi. J. Bacteriol. 174: 3757-3765.
56. Sinsky, R. J., and J. Piesman. 1989. Ear punch biopsy method for detection and isolation of Borrelia burgdorferi from rodents. J. Clin. Microbiol. 27: 1723-1727.
57. 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.
58. Stevenson, B., K. Tilly, and P. A. Rosa. 1996. A family of gene located on four separate 32-kilobase circular plasmids in Borrelia burgdorferi B31. J. Bacteriol. 178:3508-3516.
59. Szczepanski, A., and J. L. Benach. 1991. Lyme borreliosis: host responses to Borrelia burgdorferi. Microbiol. Rev. 55:21-34.
60. von Heijne, G. 1984. Analysis of the distribution of charged residues in the N-terminal region of signal sequences: implications for protein export in prokaryotic and eukaryotic cells. EMBO J. 3:2315-2318.
61. 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.
62. Wallich, R., M. M. Simon, H. Hofmann, S. E. Moter, U. E. Schaible, and M. D. Kramer. 1993. Molecular and immunological characterization of a novel polymorphic lipoprotein of Borrelia burgdorferi. Infect. Immun. 61: 4158-4166.
63. Yuen, S., M. W. Hunkapiller, K. J. Wilson, and P. M. Yuan. 1986. SDS-PAGE electroblotting. Applied Biosystems User Bull. 25:1-15.