Passage through Ixodes scapularis ticks enhances the virulence of a weakly pathogenic isolate of Borrelia burgdorferi

Infection and Immunity

Volumn 78, Issue 1, 2010, Pages 138-144

  Adusumilli, Sarojini ^a   Booth, Carmen J ^a   Anguita, Juan ^b   Fikrig, Erol ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MASSACHUSETTS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATTENUATION; BACTERIAL GENE; BACTERIAL VIRULENCE; BACTERIUM ISOLATION; BORRELIA BURGDORFERI; CONTROLLED STUDY; GENE EXPRESSION REGULATION; INOCULATION; IXODE SCAPULARIS; IXODES; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; PATHOGENESIS; PATHOGENICITY; PRIORITY JOURNAL; SPIROCHETE; SYRINGE;

ANIMALS; ARACHNID VECTORS; BORRELIA BURGDORFERI; IXODES; LYME DISEASE; MICE; MICE, INBRED C3H; NYMPH; VIRULENCE;

EID: 73449129730     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00470-09     Document Type: Article

References (37)

1. Anguita, J., S. Samanta, B. Revilla, K. Suk, S. Das, S. W. Barthold, and E. Fikrig. 2000. Borrelia burgdorferi gene expression in vivo and spirochete pathogenicity. Infect. Immun. 68:1222-1230.
2. Anguita, J., V. Thomas, S. Samanta, R. Persinski, C. Hernanz, S. W. Barthold, and E. Fikrig. 2001. Borrelia burgdorferi-induced inflammation facilitates spirochete adaptation and variable major protein-like sequence locus recombination. J. Immunol. 167:3383-3390.
3. Barthold, S. W., S. Feng, L. K. Bockenstedt, E. Fikrig, and K. Feen. 1997. Protective and arthritis-resolving activity in sera of mice infected with Borrelia burgdorferi. Clin. Infect. Dis. 25(Suppl. 1):S9-S17.
4. Blevins, J. S., K. E. Hagman, and M. V. Norgard. 2008. Assessment of decorin-binding protein A to the infectivity of Borrelia burgdorferi in the murine models of needle and tick infection. BMC Microbiol. 8:82.
5. Exner, M. M., X. Wu, D. R. Blanco, J. N. Miller, and M. A. Lovett. 2000. Protection elicited by native outer membrane protein Oms66 (p66) against host-adapted Borrelia burgdorferi: conformational nature of bactericidal epitopes. Infect. Immun. 68:2647-2654.
6. Feder, H. M., Jr., B. J. Johnson, S. O'Connell, E. D. Shapiro, A. C. Steere, G. P. Wormser, W. A. Agger, H. Artsob, P. Auwaerter, J. S. Dumler, J. S. Bakken, L. K. Bockenstedt, J. Green, R. J. Dattwyler, J. Munoz, R. B. Nadelman, I. Schwartz, T. Draper, E. McSweegan, J. J. Halperin, M. S. Klempner, P. J. Krause, P. Mead, M. Morshed, R. Porwancher, J. D. Radolf, R. P. Smith, Jr., S. Sood, A. Weinstein, S. J. Wong, and L. Zemel. 2007. A critical appraisal of "chronic Lyme disease." N. Engl. J. Med. 357:1422-1430.
7. Fikrig, E., W. Feng, S. W. Barthold, S. R. Telford III, and R. A. Flavell. 2000. Arthropod- and host-specific Borrelia burgdorferi bbk32 expression and the inhibition of spirochete transmission. J. Immunol. 164:5344-5351.
8. 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.
9. Gilmore, R. D., Jr., R. R. Howison, V. L. Schmit, and J. A. Carroll. 2008. Borrelia burgdorferi expression of the bba64, bba65, bba66, and bba73 genes in tissues during persistent infection in mice. Microb. Pathog. 45:355-360.
10. 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.
11. 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. U. S. A. 101:3142-3147.
12. Hengge, U. R., A. Tannapfel, S. K. Tyring, R. Erbel, G. Arendt, and T. Ruzicka. 2003. Lyme borreliosis. Lancet Infect. Dis. 3:489-500.
13. Hodzic, E., S. Feng, K. J. Freet, and S. W. Barthold. 2003. Borrelia burgdorferi population dynamics and prototype gene expression during infection of immunocompetent and immunodeficient mice. Infect. Immun. 71:5042-5055.
14. Hodzic, E., S. Feng, K. J. Freet, D. L. Borjesson, and S. W. Barthold. 2002. Borrelia burgdorferi population kinetics and selected gene expression at the host-vector interface. Infect. Immun. 70:3382-3388.
15. Hovius, J. W., A. P. van Dam, and E. Fikrig. 2007. Tick-host-pathogen interactions in Lyme borreliosis. Trends Parasitol. 23:434-438.
16. Hughes, J. L., C. L. Nolder, A. J. Nowalk, D. R. Clifton, R. R. Howison, V. L. Schmit, R. D. Gilmore, Jr., and J. A. Carroll. 2008. Borrelia burgdorferi surface-localized proteins expressed during persistent murine infection are conserved among diverse Borrelia spp. Infect. Immun. 76:2498-2511.
17. Kuss, S. K., C. A. Etheredge, and J. K. Pfeiffer. 2008. Multiple host barriers restrict poliovirus trafficking in mice. PLoS Pathog. 4:e1000082.
18. Li, X., X. Liu, D. S. Beck, F. S. Kantor, and E. Fikrig. 2006. Borrelia burgdorferi lacking BBK32, a fibronectin-binding protein, retains full pathogenicity. Infect. Immun. 74:3305-3313.
19. Li, X., G. Neelakanta, X. Liu, D. S. Beck, F. S. Kantor, D. Fish, J. F. Anderson, and E. Fikrig. 2007. Role of outer surface protein D in the Borrelia burgdorferi life cycle. Infect. Immun. 75:4237-4244.
20. Liang, F. T., F. K. Nelson, and E. Fikrig. 2002. DNA microarray assessment of putative Borrelia burgdorferi lipoprotein genes. Infect. Immun. 70:3300-3303.
21. McDowell, J. V., S. Y. Sung, L. T. Hu, and R. T. Marconi. 2002. Evidence that the variable regions of the central domain of VlsE are antigenic during infection with Lyme disease spirochetes. Infect. Immun. 70:4196-4203.
22. Munderloh, U. G., and T. J. Kurtti. 1995. Cellular and molecular interrelationships between ticks and prokaryotic tick-borne pathogens. Annu. Rev. Entomol. 40:221-243.
23. 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.
24. Norman, M. U., T. J. Moriarty, A. R. Dresser, B. Millen, P. Kubes, and G. Chaconas. 2008. Molecular mechanisms involved in vascular interactions of the Lyme disease pathogen in a living host. PLoS Pathog. 4:e1000169.
25. Ojaimi, C., V. Mulay, D. Liveris, R. Iyer, and I. Schwartz. 2005. Comparative transcriptional profiling of Borrelia burgdorferi clinical isolates differing in capacities for hematogenous dissemination. Infect. Immun. 73:6791-6802.
26. Ouyang, Z., J. S. Blevins, and M. V. Norgard. 2008. Transcriptional interplay among the regulators Rrp2, RpoN and RpoS in Borrelia burgdorferi. Microbiology 154:2641-2658.
27. Pal, U., J. Dai, X. Li, G. Neelakanta, P. Luo, M. Kumar, P. Wang, X. Yang, J. F. Anderson, and E. Fikrig. 2008. A differential role for BB0365 in the persistence of Borrelia burgdorferi in mice and ticks. J. Infect. Dis. 197:148-155.
28. 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. Invest. 113:220-230.
29. Parveen, N., K. A. Cornell, J. L. Bono, C. Chamberland, P. Rosa, and J. M. Leong. 2006. Bgp, a secreted glycosaminoglycan-binding protein of Borrelia burgdorferi strain N40, displays nucleosidase activity and is not essential for infection of immunodeficient mice. Infect. Immun. 74:3016-3020.
30. Pfeiffer, J. K., and K. Kirkegaard. 2005. Increased fidelity reduces poliovirus fitness and virulence under selective pressure in mice. PLoS Pathog. 1:e11.
31. Rosa, P. A., K. Tilly, and P. E. Stewart. 2005. The burgeoning molecular genetics of the Lyme disease spirochaete. Nat. Rev. Microbiol. 3:129-143.
32. 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.
33. Scully, L. R., and M. J. Bidochka. 2006. The host acts as a genetic bottleneck during serial infections: an insect-fungal model system. Curr. Genet. 50:335-345.
34. Singh, S. K., and H. J. Girschick. 2004. Molecular survival strategies of the Lyme disease spirochete Borrelia burgdorferi. Lancet Infect. Dis. 4:575-583.
35. Stewart, P. E., A. Bestor, J. N. Cullen, and P. A. Rosa. 2008. A tightly regulated surface protein of Borrelia burgdorferi is not essential to the mouse-tick infectious cycle. Infect. Immun. 76:1970-1978.
36. 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.
37. Yang, X. F., S. M. Alani, and M. V. Norgard. 2003. The response regulator Rrp2 is essential for the expression of major membrane lipoproteins in Borrelia burgdorferi. Proc. Natl. Acad. Sci. U. S. A. 100:11001-11006.