Outer surface protein A protects lyme disease spirochetes from acquired host immunity in the tick vector

Infection and Immunity

Volumn 76, Issue 11, 2008, Pages 5228-5237

  Battisti, James M ^a,b   Bono, James L ^a,c   Rosa, Patricia A ^a   Schrumpf, Merry E ^a   Schwan, Tom G ^a   Policastro, Paul F ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b UNIVERSITY OF MONTANA   (United States)

^c U S MEAT ANIMAL RESEARCH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

OUTER SURFACE PROTEIN A;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; B LYMPHOCYTE; BACTERIAL COLONIZATION; BACTERIAL STRAIN; BACTERIAL SURVIVAL; BORRELIA BURGDORFERI; CONTROLLED STUDY; IMMUNE RESPONSE; IMMUNOCOMPETENCE; IN VITRO STUDY; LARVAL STAGE; LYME DISEASE; MOLECULAR CLONING; MOUSE; NONHUMAN; PARASITE VECTOR; PRIORITY JOURNAL; PROTEIN FUNCTION; SPIROCHETE; TICK;

ANIMALS; ANTIBODIES, BACTERIAL; ANTIGENS, BACTERIAL; ANTIGENS, SURFACE; ARACHNID VECTORS; BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL VACCINES; BLOTTING, WESTERN; BORRELIA BURGDORFERI; ELECTROPHORESIS, POLYACRYLAMIDE GEL; LIPOPROTEINS; LYME DISEASE; MICE; TICKS;

EID: 55849126646     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.00410-08     Document Type: Article

References (69)

1. Anderson, J. F., R. C. Johnson, L. A. Magnarelli, and F. W. Hyde. 1985. Identification of endemic foci of Lyme disease: isolation of Borrelia burgdorferi from feral rodents and ticks (Dermacentor variabilis). J. Clin. Microbiol. 22:36-38.
2. Barbour, A. G. 1984. Isolation and cultivation of Lyme disease spirochetes. Yale J. Biol. Med. 57:521-525.
3. Barbour, A. G., and C. F. Garon. 1987. Linear plasmids of the bacterium Borrelia burgdorferi have covalently closed ends. Science 237:409-411.
4. Barbour, A. G., S. L. Tessier, and S. F. Hayes. 1984. Variation in a major surface protein of Lyme disease spirochetes. Infect. Immun. 45:94-100.
5. 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.
6. 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.
7. Becker, M., J. Bunikis, B. D. Lade, J. J. Dunn, A. G. Barbour, and C. L. Lawson. 2005. Structural investigation of Borrelia burgdorferi OspB, a bactericidal Fab target. J. Biol. Chem. 280:17363-17370.
8. Belperron, A. A., and L. K. Bockenstedt. 2001. Natural antibody affects survival of the spirochete Borrelia burgdorferi within feeding ticks. Infect. Immun. 69:6456-6462.
9. Bergström, S., V. G. Bundoc, and A. G. Barbour. 1989. Molecular analysis of linear plasmid-encoded major surface proteins, OspA and OspB, of the Lyme disease spirochete Borrelia burgdorferi. Mol. Microbiol. 3:479-486.
10. Bono, J. L., A. F. Elias, J. J. Kupko, B. Stevenson, K. Tilly, and P. Rosa. 2000. Efficient targeted mutagenesis in Borrelia burgdorferi. J. Bacteriol. 182:2445-2452.
11. Brunet, L. R., C. Sellitto, A. Spielman, and S. R. Telford III. 1995. Antibody response of the mouse reservoir of Borrelia burgdorferi in nature. Infect. Immun. 63:3030-3036.
12. Bunikis, J., and A. G. Barbour. 1999. Access of antibody or trypsin to an integral outer membrane protein (P66) of Borrelia burgdorferi is hindered by Osp lipoproteins. Infect. Immun. 67:2874-2883.
13. Bunikis, J., J. Tsao, C. J. Luke, M. G. Luna, D. Fish, and A. G. Barbour. 2004. Borrelia burgdorferi infection in a natural population of Peromyscus leucopus mice: a longitudinal study in an area where Lyme borreliosis is highly endemic. J. Infect. Dis. 189:1515-1523.
14. Casjens, S., N. Palmer, R. Van Vugt, W. Mun 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.
15. Casjens, S., R. van Vugt, K. Tilly, P. A. Rosa, and B. Stevenson. 1997. Homology throughout the multiple 32-kilobase circular plasmids present in Lyme disease spirochetes. J. Bacteriol. 179:217-227.
16. Coleman, J. L., J. A. Gebbia, J. Piesman, J. L. Degen, T. H. Bugge, and J. L. Benach. 1997. Plasminogen is required for efficient dissemination of B. burgdorferi in ticks and for enhancement of spirochetemia in mice. Cell 89:1111-1119.
17. de Silva, A. M., and E. Fikrig. 1995. Growth and migration of Borrelia burgdorferi in Ixodes ticks during blood feeding. Am. J. Trop. Med. Hyg. 53:397-404.
18. de Silva, A. M., E. Fikrig, E. Hodzic, F. S. Kantor, S. R. Telford, and S. W. Barthold. 1998. Immune evasion by tickborne and host-adapted Borrelia burgdorferi. J. Infect. Dis. 177:395-400.
19. 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.
20. de Silva, A. M., N. S. Zeidner, Y. Zhang, M. C. Dolan, J. Piesman, and E. Fikrig. 1999. Influence of outer surface protein A antibody on Borrelia burgdorferi within feeding ticks. Infect. Immun. 67:30-35.
21. Donahue, J. G., J. Piesman, and A. Spielman. 1987. Reservoir competence of white-footed mice for Lyme disease spirochetes. Am. J. Trop. Med. Hyg. 36:92-96.
22. Elias, A. F., J. L. Bono, J. J. Kupko, P. E. Stewart, J. G. Krum, and P. A. Rosa. 2003. New antibiotic resistance cassettes suitable for genetic studies in Borrelia burgdorferi. J. Mol. Microbiol. Biotechnol. 6:29-40.
23. 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.
24. Fikrig, E., S. R. Telford, S. W. Barthold, F. S. Kantor, A. Spielman, and R. A. Flavell. 1992. Elimination of Borrelia burgdorferi from vector ticks feeding on OspA immunized mice. Proc. Natl. Acad. Sci. USA 89:5418-5421.
25. Finlay, B. B., and S. Falkow. 1997. Common themes in microbial pathogenicity revisited. Microbiol. Mol. Biol. Rev. 61:136-169.
26. Fisher, M. A., D. Grimm, A. K. Henion, A. F. Elias, P. E. Stewart, P. A. Rosa, and F. C. Gherardini. 2005. Borrelia burgdorferi sigma(54) is required for mammalian infection and vector transmission but not for tick colonization. Proc. Natl. Acad. Sci. USA 102:5162-5167.
27. 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. F. 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. Gerland, 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.
28. Fuchs, H., R. Wallich, M. M. Simon, and M. D. Kramer. 1994. The outer surface protein A of the spirochete Borrelia burgdorferi is a plasmin(ogen) receptor. Proc. Natl. Acad. Sci. USA 91:12594-12598.
29. 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. USA 101:3142-3147.
30. Hanson, M. S., D. R. Cassatt, B. P. Guo, N. K. Patel, M. P. McCarthy, D. W. Dorward, and M. Hook. 1998. Active and passive immunity against Borrelia burgdorferi decorin binding protein A (DbpA) protects against infection. Infect. Immun. 66:2143-2153.
31. Howe, T. R., F. W. LaQuier, and A. G. Barbour. 1986. Organization of genes encoding two outer membrane proteins of the Lyme disease agent Borrelia burgdorferi within a single transcriptional unit. Infect. Immun. 54:207-212.
32. Howe, T. R., L. W. Mayer, A. G. Barbour, S. L. Tessier, and W. J. Todd. 1985. A single recombinant plasmid expressing two major outer surface proteins of the Lyme disease spirochete. Science 227:645-646.
33. Kelly, R. 1971. Cultivation of Borrelia hermsii. Science 173:443-444.
34. Kitamura, D., J. Roes, R. Kuhn, and K. Rajewsky. 1991. A B cell-deficient mouse by targeted disruption of the membrane exon of the immunoglobulin mu chain gene. Nature 350:423-426.
35. Knülle, W. 1966. Equilibrium humidities and survival of some tick larvae. J. Med. Entomol. 2:335-338.
36. Kramer, M. D., R. Wallich, and M. M. Simon. 1996. The outer surface protein A (OspA) of Borrelia burgdorferi: a vaccine candidate and bioactive mediator. Infection 24:190-194.
37. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
38. Lane, R. S., J. Piesman, and W. Burgdorfer. 1991. Lyme borreliosis: relation of its causative agent to its vectors and hosts in North America and Europe. Annu. Rev. Entomol. 36:587-609.
39. Li, H., J. J. Dunn, B. J. Luft, and C. L. Lawson. 1997. 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. Proc. Natl. Acad. Sci. USA 94:3584-3589.
40. Magnarelli, L. A., J. F. Anderson, K. E. Hyland, D. Fish, and J. B. McAninch. 1988. Serologic analyses of Peromyscus leucopus, a rodent reservoir for Borrelia burgdorferi, in northeastern United States. J. Clin. Microbiol. 26:1138-1141.
41. Moody, K. D., R. L. Adams, and S. W. Barthold. 1994. Effectiveness of antimicrobial treatment against Borrelia burgdorferi infection in mice. Antimicrob. Agents Chemother. 38:1567-1572.
42. Neelakanta, G., X. Li, U. Pal, X. Liu, D. S. Beck, K. Deponte, D. Fish, F. S. Kantor, and E. Fikrig. 2007. Outer surface protein B is critical for Borrelia burgdorferi adherence and survival within Ixodes ticks. PLoS Pathog. 3:e33.
43. Noppa, L., Y. Östberg, M. Lavrinovicha, and S. Bergström. 2001. P13, an integral membrane protein of Borrelia burgdorferi, is C-terminally processed and contains surface-exposed domains. Infect. Immun. 69:3323-3334.
44. 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.
45. Pal, U., A. M. de Silva, R. R. Montgomery, D. Fish, J. Anguita, J. F. Anderson, Y. Lobet, and E. Fikrig. 2000. Attachment of Borrelia burgdorferi within Ixodes scapularis mediated by outer surface protein A. J. Clin. Investig. 106:561-569.
46. Pal, U., X. Li, T. Wang, R. R. Montgomery, N. Ramamoorthi, A. M. De Silva, F. Bao, X. Yang, M. Pypaert, D. Pradhan, F. S. Kantor, S. Telford, J. F. Anderson, and E. Fikrig. 2004. TROSPA, an Ixodes scapularis receptor for Borrelia burgdorferi. Cell 119:457-468.
47. Pal, U., R. R. Montgomery, D. Lusitani, P. Voet, V. Weynants, S. E. Malawista, Y. Lobet, and E. Fikrig. 2001. Inhibition of Borrelia burgdorferi-tick interactions in vivo by outer surface protein A antibody. J. Immunol. 166:7398-7403.
48. Pavia, C., M. A. Inchiosa, and G. P. Wormser. 2002. Efficacy of short-course ceftriaxone therapy for Borrelia burgdorferi infection in C3H mice. Antimicrob. Agents Chemother. 46:132-134.
49. Piesman, J., N. S. Zeidner, and B. S. Schneider. 2003. Dynamic changes in Borrelia burgdorferi populations in Ixodes scapularis (Acari:Ixodidae) during transmission: studies at the mRNA level. Vector Borne Zoonotic Dis. 3:125-132.
50. Policastro, P. F., and T. G. Schwan. 2003. Experimental infection of Ixodes scapularis larvae (Acari:Ixodidae) by immersion in low passage cultures of Borrelia burgdorferi. J. Med. Entomol. 40:364-370.
51. Pollack, R. J., S. R. Telford, and A. Spielman. 1991. Rectal infusion and aspiration of material through the guts of ixodid ticks (Acari:Ixodidae). J. Med. Entomol. 28:809-815.
52. Ribeiro, J. M., T. N. Mather, J. Piesman, and A. Spielman. 1987. Dissemination and salivary delivery of Lyme disease spirochetes in vector ticks (Acari:Ixodidae). J. Med. Entomol. 24:201-205.
53. Rosa, P., D. S. Samuels, D. Hogan, B. Stevenson, S. Casjens, and K. Tilly. 1996. Directed insertion of a selectable marker into a circular plasmid of Borrelia burgdorferi. J. Bacteriol. 178:5946-5953.
54. Rosa, P. A., T. Schwan, and D. Hogan. 1992. Recombination between genes encoding major outer surface proteins A and B of Borrelia burgdorferi. Mol. Microbiol. 6:3031-3040.
55. Rudolph, D., and W. Knulle. 1974. Site and mechanism of water vapour uptake from the atmosphere in ixodid ticks. Nature 249:84-85.
56. Sadziene, A., D. D. Thomas, and A. G. Barbour. 1995. Borrelia burgdorferi mutant lacking Osp: biological and immunological characterization. Infect. Immun. 63:1573-1580.
57. 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.
58. Schwan, T. G., K. K. Kime, M. E. Schrumpf, J. E. Coe, and W. J. Simpson. 1989. Antibody response in white-footed mice (Peromyscus leucopus) experimentally infected with the Lyme disease spirochete (Borrelia burgdorferi). Infect. Immun. 57:3445-3451.
59. 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.
60. 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 28:2909-2913.
61. Steere, A. C., V. K. Sikand, F. Meurice, D. L. Parenti, E. Fikrig, R. T. Schoen, J. Nowakowski, C. H. Schmid, S. Laukamp, C. Buscarino, and D. S. Krause for the Lyme Disease Vaccine Study Group. 1998. Vaccination against Lyme disease with recombinant Borrelia burgdorferi outer surface lipoprotein A with adjuvant. N. Engl. J. Med. 339:209-215.
62. Stoenner, H. G., T. Dodd, and C. Larsen. 1982. Antigenic variation of Borrelia hermsii. J. Exp. Med. 156:1297-1311.
63. Thanassi, W. T., and R. T. Schoen. 2000. The Lyme disease vaccine: conception, development, and implementation. Ann. Intern. Med. 132:661-668.
64. Towbin, H., T. Staehelin, and J. Gordon. 1979. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. USA 76:4350-4354.
65. Valenzuela, J. G., R. Charlab, T. N. Mather, and J. M. Ribeiro. 2000. Purification, cloning, and expression of a novel salivary anticomplement protein from the tick, Ixodes scapularis. J. Biol. Chem. 275:18717-18723.
66. Van Hoecke, C., D. Fu, D. De Grave, P. Voet, and E. Lebacq. 1998. Clinical and immunological assessment of a candidate Lyme disease vaccine in healthy adults: antibody persistence and effect of a booster dose at month 12. Vaccine 16:1688-1692.
67. Vieira, J., and J. Messing. 1991. New pUC-derived cloning vectors with different selectable markers and DNA replication origins. Gene 100:189-194.
68. Winston, P. W., and D. H. Bates. 1960. Saturated solutions for the control of humidity in biological research. Ecology 41:232-237.
69. Yang, X. F. 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.