A tightly regulated surface protein of Borrelia burgdorferi is not essential to the mouse-tick infectious cycle

Infection and Immunity

Volumn 76, Issue 5, 2008, Pages 1970-1978

  Stewart, Philip E ^a   Bestor, Aaron ^a   Cullen, Jonah N ^a   Rosa, Patricia A ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN; OUTER SURFACE PROTEIN D; BACTERIAL RNA; BACTERIUM ANTIBODY; BORDETELLA VIRULENCE FACTOR; MESSENGER RNA; OUTER MEMBRANE PROTEIN; OUTER SURFACE PROTEIN D, BORRELIA BURGDORFERI;

ANIMAL EXPERIMENT; ARTICLE; BACTERIAL INFECTION; BACTERIAL STRAIN; BACTERIAL SURVIVAL; BORRELIA BURGDORFERI; CELL DENSITY; CORRELATION ANALYSIS; DIGESTION; FEEDING; GENE DELETION; GENETIC ENGINEERING; MEAL; MOLTING; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; REGULATORY MECHANISM; TICK; ANIMAL; ANKLE; BIOSYNTHESIS; BLADDER; BLOOD; EAR; GASTROINTESTINAL TRACT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; LYME DISEASE; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PHYSIOLOGY; TIME; WESTERN BLOTTING;

ANIMALS; ANKLE JOINT; ANTIBODIES, BACTERIAL; BACTERIAL OUTER MEMBRANE PROTEINS; BLOTTING, WESTERN; BORRELIA BURGDORFERI; EAR; GASTROINTESTINAL TRACT; GENE DELETION; GENE EXPRESSION PROFILING; LYME DISEASE; MICE; MUTAGENESIS, INSERTIONAL; RNA, BACTERIAL; RNA, MESSENGER; TICKS; TIME FACTORS; URINARY BLADDER; VIRULENCE FACTORS, BORDETELLA;

EID: 42949083309     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.00714-07     Document Type: Article

References (62)

1. Anderson, J. F., R. C. Johnson, L. A. Magnarelli, and F. W. Hyde. 1986. Involvement of birds in the epidemiology of the Lyme disease agent Borrelia burgdorferi. Infect. Immun. 51:394-396.
2. Anderson, J. F., and L. A. Magnarelli. 1984. Avian and mammalian hosts for spirochete-infected ticks and insects in a Lyme disease focus in Connecticut. Yale J. Biol. Med. 57:627-641.
3. Blevins, J. S., A. T. Revel, M. J. Caimano, X. F. Yang, J. A. Richardson, K. E. Hagman, and M. V. Norgard. 2004. The luxS gene is not required for Borrelia burgdorferi tick colonization, transmission to a mammalian host, or induction of disease. Infect. Immun. 72:4864-4867.
4. Bono, J. L., A. F. Elias, J. J. Kupko III, B. Stevenson, K. Tilly, and P. Rosa. 2000. Efficient targeted mutagenesis in Borrelia burgdorferi. J. Bacteriol. 182:2445-2452.
5. Brooks, C. S., P. S. Hefty, S. E. Jolliff, and D. R. Akins. 2003. Global analysis of Borrelia burgdorferi genes regulated by mammalian host-specific signals. Infect. Immun. 71:3371-3383.
6. Burgdorfer, W., A. G. Barbour, S. F. Hayes, J. L. Benach, E. Grunwaldt, and J. P. Davis. 1982. Lyme disease: a tick-borne spirochetosis? Science 216:1317-1319.
7. Casjens, S., N. Palmer, R. van Vugt, W. M. Huang, B. Stevenson, P. Rosa, R. Lathigra, G. Sutton, J. Peterson, R. J. Dodson, D. Haft, E. Hickey, M. Gwinn, O. White, and C. 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.
8. Clark, K., A. Hendricks, and D. Burge. 2005. Molecular identification and analysis of Borrelia burgdorferi sensu lato in lizards in the southeastern United States. Appl. Environ. Microbiol. 71:2616-2625.
9. 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.
10. Elias, A. F., J. L. Bono, J. J. Kupko III, 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.
11. 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.
12. 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. Weidmann, 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.
13. Grimm, D., A. F. Elias, K. Tilly, and P. A. Rosa. 2003. Plasmid stability during in vitro propagation of Borrelia burgdorferi assessed at a clonal level. Infect. Immun. 71:3138-3145.
14. Grimm, D., K. Tilly, D. M. Bueschel, M. A. Fisher, P. F. Policastro, F. C. Gherardini, T. G. Schwan, and P. A. Rosa. 2005. Defining plasmids required by Borrelia burgdorferi for colonization of tick vector Ixodes scapularis (Acari: Ixodidae). J. Med. Entomol. 42:676-684.
15. 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.
16. Hellwage, J., T. Meri, T. Heikkilä, A. Alitalo, J. Panelius, P. Lahdenne, J. T. Seppälä, and S. Meri. 2001. The complement regulator factor H binds to the surface protein OspE of Borrelia burgdorferi. J. Biol. Chem. 276:8427-8435.
17. 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.
18. Hübner, A., A. T. Revel, D. M. Nolen, K. E. Hagman, and M. V. Norgard. 2003. Expression of a luxS gene is not required for Borrelia burgdorferi infection of mice via needle inoculation. Infect. Immun. 71:2892-2896.
19. Indest, K. J., J. K. Howell, M. B. Jacobs, D. Scholl-Meeker, S. J. Norris, and M. T. Philipp. 2001. Analysis of Borrelia burgdorferi vlsE gene expression and recombination in the tick vector. Infect. Immun. 69:7083-7090.
20. Iyer, R., O. Kalu, J. Purser, S. Norris, B. Stevenson, and I. Schwartz. 2003. Linear and circular plasmid content in Borrelia burgdorferi clinical isolates. Infect. Immun. 71:3699-3706.
21. Iyer, R., D. Livens, A. Adams, J. Nowakowski, D. McKenna, S. Bittker, D. Cooper, G. P. Wormser, and I. Schwartz. 2001. Characterization of Borrelia burgdorferi isolated from erythema migrans lesions: interrelationship of three molecular typing methods. J. Clin. Microbiol. 39:2954-2957.
22. - mutant of Borrelia burgdorferi, the Lyme disease spirochete, via ticks. Infect. Immun. 74:3678-3681.
23. Jewett, M. W., K. Lawrence, A. C. Bestor, K. Tilly, D. Grimm, P. Shaw, M. Vanraden, F. Gherardini, and P. A. Rosa. 2007. The critical role of the linear plasmid lp36 in the infectious cycle of Borrelia burgdorferi. Mol. Microbiol. 64:1358-1374.
24. Kawabata, H., S. J. Norris, and H. Watanabe. 2004. BBE02 disruption mutants of Borrelia burgdorferi B31 have a highly transformable, infectious phenotype. Infect. Immun. 72:7147-7154.
25. Kraiczy, P., C. Skerka, M. Kirschlink, V. Brade, and P. F. Zipfel. 2001. Immune evasion of Borrelia burgdorferi by acquisition of human complement regulators FHL-1/reconectin and factor H. Eur. J. Immunol. 31:1674-1684.
26. 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. 70:44798-44804.
27. 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.
28. 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.
29. 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.
30. Marconi, R. T., D. S. Samuels, R. K. Landry, and C. F. Garon. 1994. Analysis of the distribution and molecular heterogeneity of the ospD gene among the Lyme disease spirochetes: evidence for lateral gene exchange. J. Bacteriol. 176:4572-4582.
31. Miller, J. C., K. von Lackum, K. Babb, J. D. McAlister, and B. Stevenson. 2003. Temporal analysis of Borrelia burgdorferi Erp protein expression throughout the mammal-tick infectious cycle. Infect. Immun. 71:6943-6952.
32. Narasimhan, S., M. J. Caimano, F. T. Liang, F. Santiago, M. Laskowski, M. T. Philipp, A. R. Pachner, J. D. Radolf, and E. Fikrig. 2003. Borrelia burgdorferi transcriptome in the central nervous system of non-human primates. Proc. Natl. Acad. Sci. USA 100:15953-15958.
33. 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.
34. 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.
35. Nosbisch, L. K., and A. M. de Silva. 2007. Lack of detectable variation at Borrelia burgdorferi vlsE locus in ticks. J. Med. Entomol. 44:168-170.
36. 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.
37. Ohnishi, J., B. Schneider, W. B. Messer, J. Piesman, and A. M. de Silva. 2003. Genetic variation at the vlsE locus of Borrelia burgdorferi within ticks and mice over the course of a single transmission cycle. J. Bacteriol. 185: 4432-4441.
38. Ojaimi, C., C. Brooks, S. Casjens, P. Rosa, A. Elias, A. G. Barbour, A. Jasinskas, J. Benach, L. Katona, J. Radolf, M. Caimano, J. Skare, K. Swingle, D. Akins, and I. Schwartz. 2003. Profiling temperature-induced changes in Borrelia burgdorferi gene expression using whole genome arrays. Infect. Immun. 71:1689-1705.
39. 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.
40. Palmer, N., C. Fraser, and S. Casjens. 2000. Distribution of twelve linear extrachromosomal DNAs in natural isolates of Lyme disease spirochetes. J. Bacteriol. 182:2476-2480.
41. Piesman, J., J. R. Oliver, and R. J. Sinsky. 1990. Growth kinetics of the Lyme disease spirochete (Borrelia burgdorferi) in vector ticks (Ixodes dammini). Am. J. Trop. Med. Hyg. 42:352-357.
42. 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.
43. Probert, W. S., and R. B. LeFebvre. 1994. Protection of C3H/HeN mice from challenge with Borrelia burgdorferi through active immunization with OspA, OspB, or OspC, but not with OspD or the 83-kilodalton antigen. Infect. Immun. 62:1920-1926.
44. Purser, J. E., M. B. Lawrenz, M. J. Caimano, 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.
45. Purser, J. E., and S. J. Norris. 2000. Correlation between plasmid content and infectivity in Borrelia burgdorferi. Proc. Natl. Acad. Sci. USA 97:13865-13870.
46. Ramamoorthi, N., S. Narasimhan, U. Pal, F. Bao, X. F. Yang, D. Fish, J. Anguita, M. V. Norgard, F. S. Kantor, J. F. Anderson, R. A. Koski, and E. Fikrig. 2005. The Lyme disease agent exploits a tick protein to infect the mammalian host. Nature 436:573-577.
47. Revel, A. T., J. S. Blevins, C. Almazan, L. Neil, K. M. Kocan, J. de la Fuente, K. E. Hagman, and M. V. Norgard. 2005. bptA (bbe16) is essential for the persistence of the Lyme disease spirochete, Borrelia burgdorferi, in its natural tick vector. Proc. Natl. Acad. Sci. USA 102:6972-6977.
48. Ribeiro, J. M. C. 1988. The midgut hemolysin of Ixodes dammini (Acari: Ixodidae). J. Parasitol. 74:532-537.
49. 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.
50. Schwan, T. G., W. Burgdorfer, M. E. Schrumpf, and R. H. Karstens. 1988. The urinary bladder, a consistent source of Borrelia burgdorferi in experimentally infected white-footed mice (Peromyscus leucopus). J. Clin. Microbiol. 26:893-895.
51. 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.
52. 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.
53. Simpson, W. J., W. Burgdorfer, M. E. Schrumpf, R. H. Karstens, and T. G. Schwan. 1991. Antibody to a 39-kilodalton Borrelia burgdorferi antigen (P39) as a marker for infection in experimentally and naturally inoculated animals. J. Clin. Microbiol. 29:236-243.
54. Stevenson, B., and K. Babb. 2002. LuxS-mediated quorum sensing in Borrelia burgdorferi, the Lyme disease spirochete. Infect. Immun. 70:4099-4105.
55. Stevenson, B., N. El-Hage, M. A. Hines, J. C. Miller, and K. Babb. 2002. Differential binding of host complement inhibitor factor H by Borrelia burgdorferi Erp surface proteins: a possible mechanism underlying the expansive host range of Lyme disease spirochetes. Infect. Immun. 70:491-497.
56. 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.
57. Terekhova, D., R. Iyer, G. P. Wormser, and I. Schwartz. 2006. Comparative genome hybridization reveals substantial variation among clinical isolates of Borrelia burgdorferi sensu stricto with different pathogenic properties. J. Bacteriol. 188:6124-6134.
58. Tilly, K., J. G. Krum, A. Bestor, M. W. Jewett, D. Grimm, D. Bueschel, R. Byram, D. Dorward, 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.
59. Tokarz, R., J. M. Anderton, L. I. Katona, and J. L. Benach. 2004. Combined effects of blood and temperature shift on Borrelia burgdorferi gene expression as determined by whole genome DNA array. Infect. Immun. 72:5419-5432.
60. von Lackum, K., J. C. Miller, T. Bykowski, S. P. Riley, M. E. Woodman, V. Brade, P. Kraiczy, B. Stevenson, and R. Wallich. 2005. Borrelia burgdorferi regulates expression of complement regulator-acquiring surface protein 1 during the mammal-tick infection cycle. Infect. Immun. 73:7398-7405.
61. 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.
62. Zhang, J.-R., and S. J. Norris. 1998. Kinetics and in vivo induction of genetic variation of vlsE in Borrelia burgdorferi. Infect. Immun. 66:3689-3697.