Increasing the interaction of Borrelia burgdorferi with decorin significantly reduces the 50 percent infectious dose and severely impairs dissemination

Infection and Immunity

Volumn 75, Issue 9, 2007, Pages 4272-4281

  Xu, Qilong ^a   Seemanaplli, Sunita V ^a   McShan, Kristy ^a   Fang, Ting Liang ^a  

^a LOUISIANA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; BINDING PROTEIN; DECORIN; DECORIN BINDING PROTEIN A; PROTEIN ANTIBODY; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTHRITIS; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GROWTH; BACTERIAL INFECTION; BACTERIAL REPRODUCTION; BACTERIAL VIRULENCE; BACTERICIDAL ACTIVITY; BORRELIA BURGDORFERI; CONTROLLED STUDY; DISEASE MODEL; GROWTH INHIBITION; LYME DISEASE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SCID MOUSE;

ADHESINS, BACTERIAL; ANIMALS; ANTI-BACTERIAL AGENTS; ANTIBODIES, BACTERIAL; BACTERIAL OUTER MEMBRANE PROTEINS; BORRELIA BURGDORFERI; BORRELIA INFECTIONS; EXTRACELLULAR MATRIX PROTEINS; MICE; MICE, INBRED BALB C; MICE, SCID; MICROBIAL SENSITIVITY TESTS; PROTEOGLYCANS;

EID: 34548499147     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.00560-07     Document Type: Article

References (50)

1. Barthold, S. W. 1991. Infectivity of Borrelia burgdorferi relative to route of inoculation and genotype in laboratory mice. J. Infect. Dis. 163:419-420.
2. 1. J. Immunol. 177:657-664.
3. Brown, E. L., B. P. Guo, P. O'Neal, and M. Hook. 1999. Adherence of Borrelia burgdorferi. Identification of critical lysine residues in DbpA required for decorin binding. J. Biol. Chem. 274:26272-26278.
4. Brown, E. L., R. M. Wooten, B. J. Johnson, R. V. Iozzo, A. Smith, M. C. Dolan, B. P. Guo, J. J. Weis, and M. Hook. 2001. Resistance to Lyme disease in decorin-deficient mice. J. Clin. Investig. 107:845-852.
5. 3-chain integrin ligand identified using a phage display library. Mol. Microbiol. 34:926-940.
6. Coburn, J., J. R. Fischer, and J. M. Leong. 2005. Solving a sticky problem: new genetic approaches to host cell adhesion by the Lyme disease spirochete. Mol. Microbiol. 57:1182-1195.
7. 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.
8. Crother, T. R., C. I. Champion, X. Y. 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.
9. 3 recognition. Infect. Immun. 69:3455-3459.
10. de Silva, A. M., D. Fish, T. R. Burkot, Y. Zhang, and E. Fikrig. 1997. OspA antibodies inhibit the acquisition of Borrelia burgdorferi by Ixodes ticks. Infect. Immun. 65:3146-3150.
11. de Silva, A. M., S. R. Telford III, 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.
12. 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.
13. 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.
14. Fischer, J. R., N. Parveen, L. Magoun, and J. M. Leong. 2003. Decorin-binding proteins A and B confer distinct mammalian cell type-specific attachment by Borrelia burgdorferi, the Lyme disease spirochete. Proc. Natl. Acad. Sci. USA 100:7307-7312.
15. Fung, B. P., G. L. McHugh, J. M. Leong, and A. C. Steere. 1994. Humoral immune response to outer surface protein C of Borrelia burgdorferi in Lyme disease: role of the immunoglobulin M response in the serodiagnosis of early infection. Infect. Immun. 62:3213-3221.
16. 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.
17. Gilmore, R. D., Jr., 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.
18. 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.
19. Guo, B. P., E. L. Brown, D. W. Dorward, L. C. Rosenberg, and M. Hook. 1998. Decorin-binding adhesins from Borrelia burgdorferi. Mol. Microbiol. 30:711-723.
20. Hagman, K. E., P. Lahdenne, T. G. Popova, S. F. Porcella, D. R. Akins, J. D. Radolf, and M. V. Norgard. 1998. Decorin-binding protein of Borrelia burgdorferi is encoded within a two-gene operon and is protective in the murine model of Lyme borreliosis. Infect. Immun. 66:2674-2683.
21. 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.
22. Lawrenz, M. B., H. Kawabata, J. E. Purser, and S. J. Norris. 2002. Decreased electroporation efficiency in Borrelia burgdorferi containing linear plasmids lp25 and lp56: impact on transformation of infectious B. burgdorferi. Infect. Immun. 70:4798-4804.
23. Liang, F. T., E. L. Brown, T. Wang, R. V. Iozzo, and E. Fikrig. 2004. Protective niche for Borrelia burgdorferi to evade humoral immunity. Am. J. Pathol. 165:977-985.
24. 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.
25. 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.
26. 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.
27. 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.
28. 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.
29. 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. Investig. 113:220-230.
30. Parveen, N., and J. M. Leong. 2000. Identification of a candidate glycosaminoglycan-binding adhesin of the Lyme disease spirochete Borrelia burgdorferi. Mol. Microbiol. 35:1220-1234.
31. Parveen, N., D. Robbins, and J. M. Leong. 1999. Strain variation in glycosaminoglycan recognition influences cell-type-specific binding by Lyme disease spirochetes. Infect. Immun. 67:1743-1749.
32. Probert, W. S., and B. J. Johnson. 1998. Identification of a 47 kDa fibronectin-binding protein expressed by Borrelia burgdorferi isolate B31. Mol. Microbiol. 30:1003-1015.
33. Probert, W. S., J. H. Kim, M. Hook, and B. J. Johnson. 2001. Mapping the ligand-binding region of Borrelia burgdorferi fibronectin-binding protein BBK32. Infect. Immun. 69:4129-4133.
34. Purser, J. E., M. B. Lawrenz, M. J. Caimano, J. K. Howell, J. D. Radolf, and S. J. Norris. 2003. A plasmid-encoded nicotinamidase (PncA) is essential for infectivity of Borrelia burgdorferi in a mammalian host. Mol. Microbiol. 48:753-764.
35. Reed, L. J., and H. Mueneh. 1938. A simple method of estimating fifty per cent endpoint. Am. J. Hygiene 27:493-497.
36. 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.
37. 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.
38. Seiler, K. P., and J. J. Weis. 1996. Immunity to Lyme disease: protection, pathology and persistence. Curr. Opin. Immunol. 8:503-509.
39. 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.
40. Shi, Y., Q. Xu, S. V. Seemanapalli, K. McShan, and F. T. Liang. 2006. The dbpBA locus of Borrelia burgdorferi is not essential for infection of mice. Infect. Immun. 74:6509-6512.
41. Steere, A. C. 2001. Lyme disease. N. Engl. J. Med. 345:115-125.
42. 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.
43. Strother, K. O., E. Hodzic, S. W. Barthold, and A. M. de Silva. 2007. Infection of mice with Lyme disease spirochetes constitutively producing outer surface proteins A and B. Infect. Immun. 75:2786-2794.
44. 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.
45. Tsao, J., A. G. Barbour, C. J. Luke, E. Fikrig, and D. Fish. 2001. OspA immunization decreases transmission of Borrelia burgdorferi spirochetes from infected Peromyscus leucopus mice to larval Ixodes scapularis ticks. Vector Borne Zoonotic Dis. 1:65-74.
46. Tsao, J. I., J. T. Wootton, J. Bunikis, M. G. Luna, D. Fish, and A. G. Barbour. 2004. An ecological approach to preventing human infection: vaccinating wild mouse reservoirs intervenes in the Lyme disease cycle. Proc. Natl. Acad. Sci. USA 101:18159-18164.
47. 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.
48. Xu, Q., S. V. Seemanapalli, L. Lomax, K. McShan, X. Li, E. Fikrig, and F. T. Liang. 2005. Association of linear plasmid 28-1 with an arthritic phenotype of Borrelia burgdorferi. Infect. Immun. 73:7208-7215.
49. Xu, Q., S. V. Seemanapalli, K. McShan, and F. T. Uang. 2006. Constitutive expression of outer surface protein C diminishes the ability of Borrelia burgdorferi to evade specific humoral immunity. Infect. Immun. 74:5177-5184.
50. 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.