Lipoprotein succession in Borrelia burgdorferi: Similar but distinct roles for OspC and VlsE at different stages of mammalian infection

Molecular Microbiology

Volumn 89, Issue 2, 2013, Pages 216-227

  Tilly, Kit ^a   Bestor, Aaron ^a   Rosa, Patricia A ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LIPOPROTEIN; OUTER SURFACE PROTEIN A; OUTER SURFACE PROTEIN C; OUTER SURFACE PROTEIN VLSE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGENIC VARIATION; ARTICLE; BACTERIAL VIRULENCE; BACTERIUM MUTANT; BORRELIA BURGDORFERI; CONTROLLED STUDY; DISEASE COURSE; GENE PRODUCT; LIPID ANALYSIS; LYME DISEASE; MOUSE; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN SYNTHESIS; SCID MOUSE; VLSE GENE;

ANIMALS; ANTIGENIC VARIATION; ANTIGENS, BACTERIAL; ANTIGENS, SURFACE; BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL PROTEINS; BACTERIAL VACCINES; BORRELIA BURGDORFERI; LIPOPROTEINS; LYME DISEASE; MICE; MICE, INBRED C3H; MICE, SCID; MUTATION;

BORRELIA BURGDORFERI; IXODIDA; MAMMALIA;

EID: 84880135672     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12271     Document Type: Article

References (68)

1. Akins, D.K., Bourell, K.W., Caimano, M.J., Norgard, M.V., and Radolf, J.D. (1998) A new animal model for studying Lyme disease spirochetes in a mammalian host-adapted state. J Clin Invest 101: 2240-2250.
2. Bankhead, T., and Chaconas, G. (2007) The role of VlsE antigenic variation in the Lyme disease spirochete: persistence through a mechanism that differs from other pathogens. Mol Microbiol 65: 1547-1558.
3. Barbour, A.G., Tessier, S.L., and Todd, W.J. (1983) Lyme disease spirochetes and ixodid tick spirochetes share a common surface antigenic determinant defined by a monoclonal antibody. Infect Immun 41: 795-804.
4. Barbour, A.G., Hayes, S.F., Heiland, R.A., Schrumpf, M.E., and Tessier, S.L. (1986) A Borrelia-specific monoclonal antibody binds to a flagellar epitope. Infect Immun 52: 549-554.
5. Battisti, J.M., Bono, J.L., Rosa, P.A., Schrumpf, M.E., Schwan, T.G., and Policastro, P.F. (2008) Outer surface protein A protects Lyme disease spirochetes from acquired host immunity in the tick vector. Infect Immun 76: 5228-5237.
6. Bestor, A., Rego, R.O., Tilly, K., and Rosa, P.A. (2012) Competitive advantage of Borrelia burgdorferi with outer surface protein BBA03 during tick-mediated infection of the mammalian host. Infect Immun 80: 3501-3511.
7. Brisson, D., and Dykhuizen, D.E. (2004) ospC diversity in Borrelia burgdorferi: different hosts are different niches. Genetics 168: 713-722.
8. Bykowski, T., Babb, K., von Lackum, K., Riley, S., Norris, S.J., and Stevenson, B. (2006) Transcriptional regulation of the Borrelia burgdorferi antigenically variable VlsE surface protein. J Bacteriol 188: 4879-4889.
9. Byram, R., Stewart, P.E., and Rosa, P.A. (2004) The essential nature of the ubiquitous 26kb circular replicon of Borrelia burgdorferi. J Bacteriol 186: 3561-3569.
10. Casjens, S., Palmer, N., van Vugt, R., Huang, W.M., Stevenson, B., Rosa, P., etal. (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.
11. Casjens, S.R., Mongodin, E.F., Qiu, W.G., Luft, B.J., Schutzer, S.E., Gilcrease, E.B., etal. (2012) Genome stability of lyme disease spirochetes: comparative genomics of Borrelia burgdorferi plasmids. PLoS ONE 7: e33280.
12. Coutte, L., Botkin, D.J., Gao, L., and Norris, S.J. (2009) Detailed analysis of sequence changes occurring during vlsE antigenic variation in the mouse model of Borrelia burgdorferi infection. PLoS Pathog 5: e1000293.
13. Crother, C.R., Champion, C.I., Wu, X.Y., Blanco, D.R., Miller, J.N., and Lovett, M.A. (2003) Antigenic composition of Borrelia burgdorferi during infection of SCID mice. Infect Immun 71: 3419-3428.
14. Crother, T.R., Champion, C.I., Whitelegge, J., Aguilera, R., Wu, X.-Y., Blanco, D.R., etal. (2004) Temporal analysis of the antigenic composition of Borrelia burgdorferi during infection in rabbit skin. Infect Immun 72: 5063-5072.
15. Dulebohn, D.P., Bestor, A., Rego, R.O., Stewart, P.E., and Rosa, P.A. (2011) The Borrelia burgdorferi linear plasmid lp38 is dispensable for completion of the mouse-tick infectious cycle. Infect Immun 79: 3510-3517.
16. Dunham-Ems, S.M., Caimano, M.J., Eggers, C.H., and Radolf, J.D. (2012) Borrelia burgdorferi requires the alternative sigma factor RpoS for dissemination within the vector during tick-to-mammal transmission. PLoS Pathog 8: e1002532.
17. Earnhart, C.G., Leblanc, D.V., Alix, K.E., Desrosiers, D.C., Radolf, J.D., and Marconi, R.T. (2010) Identification of residues within ligand-binding domain 1 (LBD1) of the Borrelia burgdorferi OspC protein required for function in the mammalian environment. Mol Microbiol 76: 393-408.
18. Eicken, C., Sharma, V., Klabunde, T., Owens, R.T., Pikas, D.S., Höök, M., and Sacchettini, J.C. (2001) Crystal structure of Lyme disease antigen outer surface protein C from Borrelia burgdorferi. J Biol Chem 276: 10010-10015.
19. Eicken, C., Sharma, V., Klabunde, T., Lawrenz, M.B., Hardham, J.M., Norris, S.J., and Sacchettini, J.C. (2002) Crystal structure of Lyme disease variable surface antigen VlsE of Borrelia burgdorferi. J Biol Chem 277: 21691-21696.
20. Elias, A.F., Stewart, P.E., Grimm, D., Caimano, M.J., Eggers, C.H., Tilly, K., etal. (2002) Clonal polymorphism of Borrelia burgdorferi strain B31 MI: implications for mutagenesis in an infectious strain background. Infect Immun 70: 2139-2150.
21. Elias, A.F., Bono, J.L., Kupko, J.J., Stewart, P.E., Krum, J.G., and Rosa, P.A. (2003) New antibiotic resistance cassettes suitable for genetic studies in Borrelia burgdorferi. J Mol Microbiol Biotechnol 6: 29-40.
22. Embers, M.E., Alvarez, X., Ooms, T., and Philipp, M.T. (2008) The failure of immune response evasion by linear plasmid 28-1-deficient Borrelia burgdorferi is attributable to persistent expression of an outer surface protein. Infect Immun 76: 3984-3991.
23. Fingerle, V., Hauser, U., Liegl, G., Petko, B., Preac-Mursic, V., and Wilske, B. (1995) Expression of outer surface proteins A and C of Borrelia burgdorferi in Ixodes ricinus. J Clin Microbiol 33: 1867-1869.
24. Frank, K.L., Bundle, S.F., Kresge, M.E., Eggers, C.H., and Samuels, D.S. (2003) aadA confers streptomycin resistance in Borrelia burgdorferi. J Bacteriol 185: 6723-6727.
25. Fraser, C.M., Casjens, S., Huang, W.M., Sutton, G.G., Clayton, R., Lathigra, R., etal. (1997) Genomic sequence of a Lyme disease spirochaete, Borrelia burgdorferi. Nature 390: 580-586.
26. Grimm, D., Tilly, K., Byram, R., Stewart, P.E., Krum, J.G., Bueschel, D.M., etal. (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.
27. Grimm, D., Tilly, K., Bueschel, D.M., Fisher, M.A., Policastro, P.F., Gherardini, F.C., etal. (2005) Defining plasmids required by Borrelia burgdorferi for colonization of tick vector Ixodes scapularis (Acari: Ixodidae). J Med Entomol 42: 676-684.
28. Hodzic, E., Feng, S., Freet, K.J., Borjesson, D.L., and Barthold, S.W. (2002) Borrelia burgdorferi population kinetics and selected gene expression at the host-vector interface. Infect Immun 70: 3382-3388.
29. Hodzic, E., Feng, S., Freet, K.J., and Barthold, S.W. (2003) Borrelia burgdorferi population dynamics and prototype gene expression during infection of immunocompetent and immunodeficient mice. Infect Immun 71: 5042-5055.
30. Indest, K.J., Howell, J.K., Jacobs, M.B., Scholl-Meeker, D., Norris, S.J., and Philipp, M.T. (2001) Analysis of Borrelia burgdorferi vlsE gene expression and recombination in the tick vector. Infect Immun 69: 7083-7090.
31. Jewett, M.W., Byram, R., Bestor, A., Tilly, K., Lawrence, K., Burtnick, M.N., etal. (2007a) Genetic basis for retention of a critical virulence plasmid of Borrelia burgdorferi. Mol Microbiol 66: 975-990.
32. Jewett, M.W., Lawrence, K., Bestor, A.C., Tilly, K., Grimm, D., Shaw, P., etal. (2007b) The critical role of the linear plasmid lp36 in the infectious cycle of Borrelia burgdorferi. Mol Microbiol 64: 1358-1374.
33. Jewett, M.W., Lawrence, K.A., Bestor, A., Byram, R., Gherardini, F., and Rosa, P.A. (2009) GuaA and GuaB are essential for Borrelia burgdorferi survival in the tick-mouse infectious cycle. J Bacteriol 191: 6231-6241.
34. Kumaran, D., Eswaramoorthy, S., Luft, B.J., Koide, S., Dunn, J.J., Lawson, C.L., and Swaminathan, S. (2001) Crystal structure of outer surface protein C (OspC) from the Lyme disease spirochete, Borrelia burgdorferi. EMBO J 20: 971-978.
35. Labandeira-Rey, M., and Skare, J.T. (2001) Decreased infectivity in Borrelia burgdorferi strain B31 is associated with loss of linear plasmid 25 or 28-1. Infect Immun 69: 446-455.
36. Labandeira-Rey, M., Seshu, J., and Skare, J.T. (2003) The absence of linear plasmid 25 or 28-1 of Borrelia burgdorferi dramatically alters the kinetics of experimental infection via distinct mechanisms. Infect Immun 71: 4608-4613.
37. Lagal, V., Portnoi, D., Faure, G., Postic, D., and Baranton, G. (2006) Borrelia burgdorferi sensu stricto invasiveness is correlated with OspC-plasminogen affinity. Microbes Infect 8: 645-652.
38. LaRocca, T.J., Crowley, J.T., Cusack, B.J., Pathak, P., Benach, J., London, E., etal. (2010) Cholesterol lipids of Borrelia burgdorferi form lipid rafts and are required for the bactericidal activity of a complement-independent antibody. Cell Host Microbe 8: 331-342.
39. Lawrenz, M.B., Wooten, R.M., and Norris, S.J. (2004) Effects of vlsE complementation on the infectivity of Borrelia burgdorferi lacking the linear plasmid lp28-1. Infect Immun 72: 6577-6585.
40. Liang, F.T., Jacobs, M.B., Bowers, L.C., and Philipp, M.T. (2002a) An immune evasion mechanism for spirochetal persistence in Lyme borreliosis. J Exp Med 195: 415-422.
41. Liang, F.T., Nelson, F.K., and Fikrig, E. (2002b) Molecular adaptation of Borrelia burgdorferi in the murine host. J Exp Med 196: 275-280.
42. Liang, F.T., Yan, J., Mbow, M.L., Sviat, S.L., Gilmore, R.D., Mamula, M., and Fikrig, E. (2004) Borrelia burgdorferi changes its surface antigenic expression in response to host immune responses. Infect Immun 72: 5759-5767.
43. Ohnishi, J., Piesman, J., and de Silva, A.M. (2001) Antigenic and genetic heterogeneity of Borrelia burgdorferi populations transmitted by ticks. Proc Natl Acad Sci USA 98: 670-675.
44. Onder, O., Humphrey, P.T., McOmber, B., Korobova, F., Francella, N., Greenbaum, D.C., and Brisson, D. (2012) OspC is potent plasminogen receptor on surface of Borrelia burgdorferi. J Biol Chem 287: 16860-16868.
45. Pal, U., and Fikrig, E. (2003) Adaptation of Borrelia burgdorferi in the vector and vertebrate host. Microbes Infect 5: 659-666.
46. Pal, U., de Silva, A.M., Montgomery, R.R., Fish, D., Anguita, J., Anderson, J.F., etal. (2000) Attachment of Borrelia burgdorferi within Ixodes scapularis mediated by outer surface protein A. J Clin Invest 106: 561-569.
47. Pal, U., Yang, X., Chen, M., Bockenstedt, L.K., Anderson, J.F., Flavell, R.A., etal. (2004) OspC facilitates Borrelia burgdorferi invasion of Ixodes scapularis salivary glands. J Clin Invest 113: 220-230.
48. Purser, J.E., and Norris, S.J. (2000) Correlation between plasmid content and infectivity in Borrelia burgdorferi. Proc Natl Acad Sci USA 97: 13865-13870.
49. Purser, J.E., Lawrenz, M.B., Caimano, M.J., Radolf, J.D., and Norris, S.J. (2003) A plasmid-encoded nicotinamidase (PncA) is essential for infectivity of Borrelia burgdorferi in a mammalian host. Mol Microbiol 48: 753-764.
50. Radolf, J.D., Caimano, M.J., Stevenson, B., and Hu, L.T. (2012) Of ticks, mice and men: understanding the dual-host lifestyle of Lyme disease spirochaetes. Nat Rev Microbiol 10: 87-99.
51. Rego, R.O., Bestor, A., and Rosa, P.A. (2011) Defining the plasmid-encoded restriction-modification systems of the Lyme disease spirochete Borrelia burgdorferi. J Bacteriol 193: 1161-1171.
52. Sadziene, A., Wilske, B., Ferdows, M.S., and Barbour, A.G. (1993) The cryptic ospC gene of Borrelia burgdorferi B31 is located on a circular plasmid. Infect Immun 61: 2192-2195.
53. Samuels, D.S. (1995) Electrotransformation of the spirochete Borrelia burgdorferi. In Methods in Molecular Biology. Nickoloff, J.A. (ed.). Totowa, NJ: Humana Press, Inc, pp. 253-259.
54. Schwan, T.G., Piesman, J., Golde, W.T., Dolan, M.C., and Rosa, P.A. (1995) Induction of an outer surface protein on Borrelia burgdorferi during tick feeding. Proc Natl Acad Sci USA 92: 2909-2913.
55. Seemanapalli, S.V., Xu, Q., McShan, K., and Liang, F.T. (2010) Outer surface protein C is a dissemination-facilitating factor of Borrelia burgdorferi during mammalian infection. PLoS ONE 5: e15830.
56. Stewart, P.E., Wang, X., Bueschel, D.M., Clifton, D.R., Grimm, D., Tilly, K., etal. (2006) Delineating the requirement for the Borrelia burgdorferi virulence factor OspC in the mammalian host. Infect Immun 74: 3547-3553.
57. Tilly, K., Krum, J.G., Bestor, A., Jewett, M.W., Grimm, D., Bueschel, D., etal. (2006) Borrelia burgdorferi OspC protein required exclusively in a crucial early stage of mammalian infection. Infect Immun 74: 3554-3564.
58. Tilly, K., Bestor, A., Jewett, M.W., and Rosa, P. (2007) Rapid clearance of Lyme disease spirochetes lacking OspC from skin. Infect Immun 75: 1517-1519.
59. Tilly, K., Bestor, A., Dulebohn, D.P., and Rosa, P.A. (2009) OspC-independent infection and dissemination by host-adapted Borrelia burgdorferi. Infect Immun 77: 2672-2682.
60. Tokarz, R., Anderton, J.M., Katona, L.I., and Benach, J.L. (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.
61. Wilske, B., Preac-Mursic, V., Schierz, G., and Busch, K.V. (1986) Immunochemical and immunological analysis of European Borrelia burgdorferi strains. Zentralbl Bakteriol Mikrobiol Hyg A 263: 92-102.
62. Wilske, B., Preac-Mursic, V., Schierz, G., Kuhbeck, R., Barbour, A.G., and Kramer, M. (1988) Antigenic variability of Borrelia burgdorferi. In Lyme Disease and Related Disorders. Benach, J.L., and Bosler, E.M. (eds). New York: New York Academy of Sciences, pp. 126-143.
63. Wormser, G.P., Liveris, D., Hanincova, K., Brisson, D., Ludin, S., Stracuzzi, V.J., etal. (2008) Effect of Borrelia burgdorferi genotype on the sensitivity of C6 and 2-tier testing in North American patients with culture-confirmed Lyme disease. Clin Infect Dis 47: 910-914.
64. Xu, Q., McShan, K., and Liang, F.T. (2008a) Essential protective role attributed to the surface lipoproteins of Borrelia burgdorferi against innate defenses. Mol Microbiol 69: 15-29.
65. Xu, Q., McShan, K., and Liang, F.T. (2008b) Modification of Borrelia burgdorferi to overproduce OspA or VlsE alters its infectious behaviour. Microbiology 154: 3420-3429.
66. Yang, X.F., Pal, U., Alani, S.M., Fikrig, E., and Norgard, M.V. (2004) Essential role for OspA/B in the life cycle of the Lyme disease spirochete. J Exp Med 199: 641-648.
67. Zhang, J.R., and Norris, S.J. (1998) Kinetics and in vivo induction of genetic variation of vlsE in Borrelia burgdorferi. Infect Immun 66: 3689-3697.
68. Zhang, J.R., Hardham, J.M., Barbour, A.G., and Norris, S.J. (1997) Antigenic variation in Lyme disease borreliae by promiscuous recombination of VMP-like sequence cassettes. Cell 89: 275-285.