Characterization of unique regions of Borrelia burgdorferi surface-located membrane protein

Infection and Immunity

Volumn 78, Issue 11, 2010, Pages 4477-4487

  Yang, Xiuli ^a,b   Lenhart, Tiffany R ^c   Kariu, Toru ^a,b   Anguita, Juan ^d   Akins, Darrin R ^c   Pal, Utpal ^a,b  

^a UNIVERSITY OF MARYLAND   (United States)

^b VIRGINIA MARYLAND REGIONAL COLLEGE OF VETERINARY MEDICINE   (United States)

^c UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

^d UNIVERSITY OF MASSACHUSETTS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; LOCATED MEMBRANE PROTEIN 1; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL SURVIVAL; BACTERICIDAL ACTIVITY; BORRELIA BURGDORFERI; BORRELIA INFECTION; CARBOXY TERMINAL SEQUENCE; CARDITIS; CONTROLLED STUDY; ENZYME RECONSTITUTION; GENE DELETION; IMMUNIZATION; MOUSE; MUTANT; NONHUMAN; PLANT GROWTH; PRIORITY JOURNAL; PROTEIN FUNCTION;

ANIMALS; ANTIBODIES, BACTERIAL; BACTERIAL OUTER MEMBRANE PROTEINS; BORRELIA BURGDORFERI; HEART; HOST-PATHOGEN INTERACTIONS; IMMUNE SERA; JOINTS; LYME DISEASE; MEMBRANE PROTEINS; MICE; MICE, INBRED C3H; MYOCARDITIS; ORGAN SPECIFICITY; URINARY BLADDER;

EID: 78049419952     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00501-10     Document Type: Article

References (53)

1. Alag, R., N. Bharatham, A. Dong, T. Hills, A. Harikishore, A. A. Widjaja, S. G. Shochat, R. Hui, and H. S. Yoon. 2009. Crystallographic structure of the tetratricopeptide repeat domain of Plasmodium falciparum FKBP35 and its molecular interaction with Hsp90 C-terminal pentapeptide. Protein Sci. 18: 2115-2124.
2. Anderson, J. F. 1989. Epizootiology of Borrelia in Ixodes tick vectors and reservoir hosts. Rev. Infect. Dis. 11(Suppl. 6):S1451-S1459.
3. Antonara, S., R. M. Chafel, M. LaFrance, and J. Coburn. 2007. Borrelia burgdorferi adhesins identified using in vivo phage display. Mol. Microbiol. 66:262-276.
4. Arnold, K., L. Bordoli, J. Kopp, and T. Schwede. 2006. The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22:195-201. (Pubitemid 43205406)
5. Barthold, S. W., M. S. deSouza, J. L. Janotka, A. L. Smith, and D. H. Persing. 1993. Chronic Lyme borreliosis in the laboratory mouse. Am. J. Pathol. 143:959-971.
6. Barthold, S. W., M. DeSouza, E. Fikrig, and D. H. Persing. 1992. Lyme borreliosis in the laboratory mouse, p. 223-242. In S. E. Schuster (ed.), Lyme disease. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
7. Barthold, S. W., E. Hodzic, S. Tunev, and S. Feng. 2006. Antibody-mediated disease remission in the mouse model of Lyme borreliosis. Infect. Immun. 74:4817-4825.
8. Barthold, S. W., D. H. Persing, A. L. Armstrong, and R. A. Peeples. 1991. Kinetics of Borrelia burgdorferi: dissemination and evolution of disease following intradermal inoculation of mice. Am. J. Pathol. 163:263-273.
9. 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.
10. Bockenstedt, L. K., I. Kang, C. Chang, D. Persing, A. Hayday, and S. W. Barthold. 2001. CD4 T helper 1 cells facilitate regression of murine Lyme carditis. Infect. Immun. 69:5264-5269.
11. 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.
12. Brooks, C. S., S. R. Vuppala, A. M. Jett, and D. R. Akins. 2006. Identification of Borrelia burgdorferi outer surface proteins. Infect. Immun. 74:296-304.
13. Bubeck-Martinez, S. 2005. Immune evasion of the Lyme disease spirochetes. Front. Biosci. 10:873-878.
14. Carroll, J. A., C. F. Garon, and T. G. Schwan. 1999. Effects of environmental pH on membrane proteins in Borrelia burgdorferi. Infect. Immun. 67:3181-3187.
15. Coleman, A. S., X. Yang, M. Kumar, X. Zhang, K. Promnares, D. Shroder, M. R. Kenedy, J. F. Anderson, D. R. Akins, and U. Pal. 2008. Borrelia burgdorferi complement regulator-acquiring surface protein 2 does not contribute to complement resistance or host infectivity. PLoS One 3:3010e.
16. Connolly, S. E., and J. L. Benach. 2005. The versatile roles of antibodies in Borrelia infections. Nat. Rev. Microbiol. 3:411-420.
17. Cortajarena, A. L., J. Wang, and L. Regan. 2010. Crystal structure of a designed tetratricopeptide repeat module in complex with its peptide ligand. FEBS J. 277:1058-1066.
18. 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.
19. Feng, S., E. Hodzic, and S. W. Barthold. 2000. Lyme arthritis resolution with antiserum to a 37-kilodalton Borrelia burgdorferi protein. Infect. Immun. 68:4169-4173.
20. Frank, K. L., S. F. Bundle, M. E. Kresge, C. E. Eggers, and D. S. Samuels. 2003. aadA confers streptomycin resistance in Borrelia burgdorferi. J. Bacteriol. 185:6723-6727.
21. Gilbert, M. A., E. A. Morton, S. F. Bundle, and D. S. Samuels. 2007. Artificial regulation of ospC expression in Borrelia burgdorferi. Mol. Microbiol. 63:1259-1273.
22. Goebl, M., and M. Yanagida. 1991. The TPR snap helix: a novel protein repeat motif from mitosis to transcription. Trends Biochem. Sci. 16:173-177.
23. 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. U. S. A. 101:3142-3147.
24. Hu, L. T., and M. S. Klempner. 1997. Host-pathogen interactions in the immunopathogenesis of Lyme disease. J. Clin. Immunol. 17:354-365.
25. 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.
26. Kumar, M., X. Yang, A. S. Coleman, and U. Pal. 2010. BBA52 facilitates Borrelia burgdorferi transmission from feeding ticks to murine hosts. J. Infect. Dis. 201:1084-1095.
27. Lenhart, T. R., and D. R. Akins. 2010. Borrelia burgdorferi locus BB0795 encodes a BamA orthologue required for growth and efficient localization of outer membrane proteins. Mol. Microbiol. 75:692-709.
28. Li, X., U. Pal, N. Ramamoorthi, X. Liu, D. C. Desrosiers, C. H. Eggers, J. F. Anderson, J. D. Radolf, and E. Fikrig. 2007. The Lyme disease agent Borrelia burgdorferi requires BB0690, a Dps homologue, to persist within ticks. Mol. Microbiol. 63:694-710.
29. 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.
30. Mulay, V., M. J. Caimano, D. Liveris, D. C. Desrosiers, J. D. Radolf, and I. Schwartz. 2007. Borrelia burgdorferi BBA74, a periplasmic protein associated with the outer membrane, lacks porin-like properties. J. Bacteriol. 189:2063-2068.
31. Nadelman, R. B., and G. P. Wormser. 1998. Lyme borreliosis. Lancet 352: 557-565.
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. U. S. A. 100:15953-15958.
33. Narasimhan, S., F. Santiago, R. A. Koski, B. Brei, J. F. Anderson, D. Fish, and E. Fikrig. 2002. Examination of the Borrelia burgdorferi transcriptome in Ixodes scapularis during feeding. J. Bacteriol. 184:3122-3125.
34. Ojaimi, C., C. Brooks, S. Casjens, P. Rosa, A. Elias, A. Barbour, A. Jasinskas, J. Benach, L. Katona, J. Radolf, M. Caimano, J. Skare, K. Swingle, D. Akins, and I. Schwartz. 2003. Profiling of temperature-induced changes in Borrelia burgdorferi gene expression by using whole genome arrays. Infect. Immun. 71:1689-1705.
35. Pal, U., R. R. Montgomery, D. Lusitani, P. Voet, V. Weynants, S. E. Malawista, Y. Lobet, and E. Fikrig. 2001. Inhibition of Borrelia burgdorferitick interactions in vivo by outer surface protein A antibody. J. Immunol. 166:7398-7403.
36. Pal, U., P. Wang, F. Bao, X. Yang, S. Samanta, R. Schoen, G. P. Wormser, I. Schwartz, and E. Fikrig. 2008. Borrelia burgdorferi basic membrane proteins A and B participate in the genesis of Lyme arthritis. J. Exp. Med. 205:133-141.
37. 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.
38. Promnares, K., M. Kumar, D. Y. Shroder, X. Zhang, J. F. Anderson, and U. Pal. 2009. Borrelia burgdorferi small lipoprotein Lp6.6 is a member of multiple protein complexes in the outer membrane and facilitates pathogen transmission from ticks to mice. Mol. Microbiol. 74:112-125.
39. 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.
40. 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. U. S. A. 102:6972-6977.
41. Revel, A. T., A. M. Talaat, and M. V. Norgard. 2002. DNA microarray analysis of differential gene expression in Borrelia burgdorferi, the Lyme disease spirochete. Proc. Natl. Acad. Sci. U. S. A. 99:1562-1567.
42. Scheufler, C., A. Brinker, G. Bourenkov, S. Pegoraro, L. Moroder, H. Bartunik, F. U. Hartl, and I. Moarefi. 2000. Structure of TPR domain-peptide complexes: critical elements in the assembly of the Hsp70-Hsp90 multichaperone machine. Cell 101:199-210.
43. 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. U. S. A. 92:2909-2913.
44. Seiler, K. P., and J. J. Weis. 1996. Immunity to Lyme disease: protection, pathology and persistence. Curr. Opin. Immunol. 8:503-509.
45. 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 fi- bronectin-binding adhesin gene bbk32 significantly attenuates the infectivity potential of Borrelia burgdorferi. Mol. Microbiol. 59:1591-1601.
46. Shen, A., H. D. Kamp, A. Grundling, and D. E. Higgins. 2006. A bifunctional O-GlcNAc transferase governs flagellar motility through anti-repression. Genes Dev. 20:3283-3295.
47. Shi, Y., Q. Xu, K. McShan, and F. T. Liang. 2008. Both decorin-binding proteins A and B are critical for the overall virulence of Borrelia burgdorferi. Infect. Immun. 76:1239-1246.
48. Steere, A. C., J. Coburn, and L. Glickstein. 2004. The emergence of Lyme disease. J. Clin. Invest. 113:1093-1101.
49. 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.
50. Yamamoto, H., K. Fukui, H. Takahashi, S. Kitamura, T. Shiota, K. Terao, M. Uchida, M. Esaki, S. Nishikawa, T. Yoshihisa, K. Yamano, and T. Endo. 2009. Roles of Tom70 in import of presequence-containing mitochondrial proteins. J. Biol. Chem. 284:31635-31646.
51. Yang, X., A. S. Coleman, J. Anguita, and U. Pal. 2009. A chromosomally encoded virulence factor protects the Lyme disease pathogen against host-adaptive immunity. PLoS Pathog. 5:e1000326.
52. 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.
53. Zhang, X., X. Yang, M. Kumar, and U. Pal. 2009. BB0323 function is essential for Borrelia burgdorferi virulence and persistence through tick-rodent transmission cycle. J. Infect. Dis. 200:1318-1330.