Borrelia burgdorferi EbfC defines a newly-identified, widespread family of bacterial DNA-binding proteins

Nucleic Acids Research

Volumn 37, Issue 6, 2009, Pages 1973-1983

  Riley, Sean P ^a,d   Bykowski, Tomasz ^a,e   Cooley, Anne E ^a,f   Burns, Logan H ^a   Babb, Kelly ^a,g   Brissette, Catherine A ^a   Bowman, Amy ^a   Rotondi, Matthew ^b,h   Miller, Clarke M ^b,i   Demoll, Edward ^b   Lim, Kap ^c   Fried, Michael G ^a   Stevenson, Brian ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

^c UNIVERSITY OF MARYLAND BIOTECHNOLOGY INSTITUTE   (United States)

^d UNIVERSITY OF CHICAGO   (United States)

^e Center for Post Graduate Medical Education   (Poland)

^f NORTHWESTERN UNIVERSITY   (United States)

^g BioVitesse   (United States)

^h WEILL CORNELL MEDICAL COLLEGE   (United States)

ⁱ UNIVERSITY OF LOUISVILLE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; BACTERIAL PROTEIN; DNA BINDING PROTEIN; EBFC PROTEIN; OUTER MEMBRANE PROTEIN; PROTEIN ERP; UNCLASSIFIED DRUG;

ALPHA HELIX; ARTICLE; BACTERIAL GENOME; BINDING AFFINITY; BORRELIA BURGDORFERI; CONTROLLED STUDY; DNA CONFORMATION; DNA SEQUENCE; DNA TRANSCRIPTION; GENE LOCATION; NONHUMAN; NUCLEOTIDE BINDING SITE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DNA BINDING; SITE DIRECTED MUTAGENESIS; AMINO ACID SEQUENCE; BINDING SITE; CHEMISTRY; CLASSIFICATION; CONFORMATION; GENETICS; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; OPERATOR GENE; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN TERTIARY STRUCTURE;

BACTERIA (MICROORGANISMS); BORRELIA BURGDORFERI;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BASE SEQUENCE; BINDING SITES; BORRELIA BURGDORFERI; CONSERVED SEQUENCE; DNA, BACTERIAL; DNA-BINDING PROTEINS; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; OPERATOR REGIONS, GENETIC; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY;

EID: 64549106854     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkp027     Document Type: Article

References (56)

1. Stevenson,B., Bykowski,T., Cooley,A.E., Babb,K., Miller,J.C., Woodman,M.E., von Lackum,K. and Riley,S.P. (2006) The Lyme disease spirochete Erp protein family: Structure, function and regulation of expression. In: Cabello,F.C., Godfrey,H.P. and Hulinska,D. (eds), Molecular Biology of Spirochetes., IOS Press, Amsterdam, pp. 354-372.
2. Alitalo,A., Meri,T., Lankinen,H., Seppälä,I., Lahdenne,P., Hefty,P.S., Akins,D. and Meri,S. (2002) Complement inhibitor factor H binding to Lyme disease spirochetes is mediated by inducible expression of multiple plasmid-encoded outer surface protein E paralogs. J. Immunol., 169, 3847-3853.
3. Brissette,C.A., Cooley,A.E., Burns,L.H., Riley,S.P., Verma,A., Woodman,M.E., Bykowski,T. and Stevenson,B. (2008) Lyme borreliosis spirochete Erp proteins, their known host ligands, and potential roles in mammalian infection. Int. J. Med. Microbiol., 298(Suppl. 1) 257-267.
4. Brissette,C.A., Haupt,K., Barthel,D., Cooley,A.E., Bowman,A., Skerka,C., Wallich,R., Zipfel,P.F., Kraiczy,P. and Stevenson,B. (2009) The Borrelia burgdorferi infection-associated surface proteins ErpP, ErpA, and ErpC bind human plasminogen. Infect. Immun., 77, 300-306.
5. Brissette,C.A., Verma,A., Bowman,A., Cooley,A.E. and Stevenson,B. (2009) The Borrelia burgdorferi outer-surface protein ErpX binds mammalian laminin. Microbiology, in press.
6. Haupt,K., Kraiczy,P., Wallich,R., Brade,V., Skerka,C. and Zipfel,P.F. (2008) FHR-1, an additional human plasma protein, binds to complement regulator-acquiring surface proteins of Borrelia burgdorferi. Int. J. Med. Microbiol., 298(Suppl. 1), 287-291.
7. Hellwage,J., Meri,T., Heikkilä,T., Alitalo,A., Panelius,J., Lahdenne,P., Seppälä,I.J.T. and Meri,S. (2001) The complement regulatory factor H binds to the surface protein OspE of Borrelia burgdorferi. J. Biol. Chem., 276, 8427-8435.
8. Kraiczy,P., Hellwage,J., Skerka,C., Kirschfink,M., Brade,V., Zipfel,P.F. and Wallich,R. (2003) Immune evasion of Borrelia burgdorferi: mapping of a complement inhibitor factor H-binding site of BbCRASP-3, a novel member of the Erp protein family. Eur. J. Immunol., 33 697-707.
9. Metts,M.S., McDowell,J.V., Theisen,M., Hansen,P.R. and Marconi,R.T. (2003) Analysis of the OspE determinants involved in binding of factor H and OspE-targeting antibodies elicited during Borrelia burgdorferi infection. Infect. Immun., 71, 3587-3596.
10. Stevenson,B., El-Hage,N., Hines,M.A., Miller,J.C. and Babb,K. (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.
11. Casjens,S., van Vugt,R., Tilly,K., Rosa,P.A. and Stevenson,B. (1997) Homology throughout the multiple 32-kilobase circular plasmids present in Lyme disease spirochetes. J. Bacteriol., 179, 217-227.
12. Eggers,C.H. and Samuels,D.S. (1999) Molecular evidence for a new bacteriophage of Borrelia burgdorferi. J. Bacteriol., 181, 7308-7313.
13. Stevenson,B., Tilly,K. and Rosa,P.A. (1996) A family of genes located on four separate 32-kilobase circular plasmids in Borrelia burgdorferi B31. J. Bacteriol., 178, 3508-3516.
14. Stevenson,B., Zückert,W.R. and Akins,D.R. (2001) Repetition, conservation, and variation: The multiple cp32 plasmids of Borrelia species. In: Saier,M.H. and García-Lara,J. (eds), The Spirochetes: Molecular and Cellular Biology, Horizon Press, Oxford, pp. 87-100.
15. Casjens,S., Palmer,N., van Vugt,R., Huang,W.M., Stevenson,B., Rosa,P., Lathigra,R., Sutton,G., Peterson,J., Dodson,R.J. et al. (2000) A bacterial genome in flux: The twelve linear and nine circular extrachromosomal DNAs of an infectious isolate of the Lyme disease spirochete Borrelia burgdorferi. Mol. Microbiol., 35, 490-516.
16. Babb,K., McAlister,J.D., Miller,J.C. and Stevenson,B. (2004) Molecular characterization of Borrelia burgdorferi erp promoter/operator elements. J. Bacteriol., 186, 2745-2756.
17. Babb,K., Bykowski,T., Riley,S.P., Miller,M.C., DeMoll,E. and Stevenson,B. (2006) Borrelia burgdorferi EbfC, a novel, chromosomally-encoded protein, binds specific DNA sequences adjacent to erp loci on the spirochete's resident cp32 prophages. J. Bacteriol. 188, 4331-4339.
18. Lim,K., Tempczyk,A., Parsons,J.F., Bonander,N., Toedt,J., Kelman,Z., Howard,A., Eisenstein,E. and Herzberg,O. (2003) Crystal structure of YbaB from Haemophilus influenzae (HI0442), a protein of unknown function coexpressed with the recombinational DNA repair protein RecR. Proteins, 50, 375-379.
19. Marchler-Bauer,A., Anderson,J.B., Cherukuri,P.F., DeWeese-Scott,C., Geer,L.Y., Gwadz,M., He,S., Hurwitz,D.I., Jackson,J.D., Ke,Z. et al. (2005) CDD: A conserved domain database for protein classification. Nucleic Acids Res., 33, D192-D196.
20. Ho,S.N., Hunt,H.D., Horton,R.M., Pullen,J.K. and Pease,L.R. (1989) Site-directed mutagensis by overlap extension using polymerase chain reaction. Gene, 77, 51-59.
21. Adams,C.A. and Fried,M.G. (2007) Analysis of protein-DNA equilibria by native gel electrophoresis. In: Schuck,P. (ed.), Protein Interactions: Biophysical Approaches for the Study of Complex Reversible Systems. Springer, New York, pp. 417-446.
22. Abramoff,M.D., Magelhaes,P.J. and Ram,S.J. (2004) Image processing with ImageJ. Biophotonics International, 11, 36-42.
23. Fried,M.G. and Crothers,D.M. (1981) Equilibria and kinetics of Lac repressor-operator interactions by polyacrylamide gel electrophoresis. Nucleic Acids Res., 9, 6505-6525.
24. Fried,M.G., Kanugula,S., Bromberg,J.L. and Pegg,A.E. (1996) DNA binding mechanism of O6-alkylguanine-DNA alkyltransferase: Stoichiometry and effects of DNA base composition and secondary structure on complex stability. Biochemistry, 35, 15295-15301.
25. Munteanu,M.G., Vlahovicek,K., Parthasaraty,S., Simon,I. and Pongor,S. (1998) Rod models of DNA: Sequence-dependent anisotropic elastic modelling of local bending phenomena. Trends Biochem. Sci., 23 341-346.
26. Jones,T.A. (2004) Interactive electron-density map interpretation: From INTER to O. Acta Crystallogr. D Biol. Crystallogr., 60, 2115-2125.
27. Brunger,A.T., Adams,P.D., Clore,G.M., DeLano,W.L., Gros,P., Grosse-Kunstleve,R.W., Jiang,J.S., Kuszewski,J., Nilges,M., Pannu,N.S. et al. (1998) Crystallography & NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr., 54, 905-921.
28. Kraulis,P. (1991) MOLSCRIPT: A program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr., 24, 946-950.
29. Bacon,D.J. and Anderson,W.F. (1988) A fast algorithm for rendering space-filling molecule pictures. J. Mol. Graph., 6, 219-220.
30. Merritt,E.A. and Bacon,D.J. (1997) Raster3D photorealistic molecular graphics. Methods Enzymol., 277, 505-524.
31. Tourand,Y., Korbryn,K. and Chaconas,G. (2003) Sequence-specific recognition but position-dependent cleavage of two distinct telomeres by the Borrelia burgdorferi telomere resolvase, ResT. Mol. Microbiol., 48, 901-911.
32. Fried,M.G., Kanugula,S., Bromberg,J.L. and Pegg,A.E. (1996) DNA binding mechanism of O6-alkylguanine-DNA alkyltransferase: Stoichiometry and effects of DNA base composition and secondary structure on complex stability. Biochemistry, 35, 15295-15301.
33. Fraser,C.M., Casjens,S., Huang,W.M., Sutton,G.G., Clayton,R., Lathigra,R., White,O., Ketchum,K.A., Dodson,R., Hickey,E.K. et al. (1997) Genomic sequence of a Lyme disease spirochaete, Borrelia burgdorferi. Nature, 390, 580-586.
34. Mandelkern,M., Elias,J.G., Eden,D. and Crothers,D.M. (1981) The dimensions of DNA in solution. J. Mol. Biol., 152, 153-161.
35. Anthonissen,F.M., De Kesel,M., Hoet,P.P. and Bigaignon,G.H. (1994) Evidence for the involvement of different genospecies of Borrelia in the clinical outcome of Lyme disease in Belgium. Res. Microbiol. 145, 327-331.
36. Balmelli,T. and Piffaretti,J.C. (1995) Association between different clinical manifestations of Lyme disease and different species of Borrelia burgdorferi sensu lato. Res. Microbiol., 146, 329-340.
37. van Dam,A.P., Kuiper,H., Vos,K., Widjojokusumo,A., de Jongh,B.M., Spanjaard,L., Ramselaar,A.C.P., Kramer,M.D. and Dankert,J. (1993) Different genospecies of Borrelia burgdorferi are associated with distinct clinical manifestations of Lyme borreliosis. Clin. Infect. Dis., 17, 708-717.
38. Drlica,K. and Rouviére-Yaniv,J. (1987) Histonelike proteins of bacteria. Microbiol. Rev., 51, 301-319.
39. Stavans,J. and Oppenheim,A. (2006) DNA-protein interactions and bacterial chromosome architecture. Phys. Biol., 3, R1-R10.
40. Miller,J.C., Bono,J.L., Babb,K., El-Hage,N., Casjens,S. and Stevenson,B. (2000) A second allele of eppA in Borrelia burgdorferi strain B31 is located on the previously undetected circular plasmid cp9-2. J. Bacteriol., 182, 6254-6258.
41. Hinnebusch,B.J. and Bendich,A.J. (1997) The bacterial nucleoid visualized by fluorescence microscopy of cells lysed within agarose: comparison of Escherichia coli and spirochetes of the genus Borrelia. J. Bacteriol., 179, 2228-2237.
42. Luijsterburg,M.S., Noom,M.C., Wuite,G.J.L. and Dame,R.T. (2006) The architectural role of nucleoid-associated proteins in the organization of bacterial chromatin: A molecular perspective. J. Struct. Biol., 156, 262-272.
43. Travers,A. and Muskhelishvili,G. (1998) DNA microloops and microdomains: a general mechanism for transcription activation by torsional transmission. J. Mol. Biol., 279, 1027-1043.
44. Goosen,N. and van de Putte,P. (1995) The regulation of transcription initiation by integration host factor. Mol. Microbiol., 16, 1-7.
45. Ishihama,A. (1999) Modulation of the nucleoid, the transcription apparatus, and the translation machinery in bacteria for stationary phase survival. Genes Cells, 4, 135-143.
46. Jaffar Ali,B.M., Amit,R., Braslavsky,I., Oppenheim,A.B., Gileadi,O. and Stavans,J. (2001) Compaction of single DNA molecules induced by binding of integration host factor (IHF). Proc. Natl Acad. Sci. USA, 98 10658-10663.
47. Dame,R.T., Luijsterburg,M.S., Krin,E., Bertin,P.N., Wagner,R. and Wuite,G.J. (2005) DNA bridging: A property shared among H-NS-like proteins. J. Bacteriol., 187, 1845-1848.
48. Luijsterburg,M.S., Noom,M.C., Wuite,G.J. and Dame,R.T. (2006) The architectural role of nucleoid-associated proteins in the organization of bacterial chromatin: A molecular perspective. J. Struct. Biol., 156, 262-272.
49. Mouw,K.W. and Rice,P.A. (2007) Shaping the Borrelia burgdorferi genome: Crystal structure and binding properties of the DNA-bending protein Hbb. Mol. Microbiol., 63, 1319-1330.
50. Kobryn,K., Naigamwalla,D.Z. and Chaconas,G. (2000) Site-specific DNA binding and bending by the Borrelia burgdorferi Hbb protein. Mol. Microbiol., 37, 145-155.
51. Tilly,K., Fuhrman,J., Campbell,J. and Samuels,D.S. (1996) Isolation of Borrelia burgdorferi genes encoding homologues of DNA-binding protein HU and ribosomal protein S20. Microbiology, 142, 2471-2479.
52. Knight,S.W. and Samuels,D.S. (1999) Natural synthesis of a DNA-binding protein from the C-terminal domain of DNA gyrase A in Borrelia burgdorferi. EMBO J., 18, 4875-4881.
53. Freundlich,M., Ramani,N., Mathew,E., Sirko,A. and Tsui,P. (1992) The role of integration host factor in gene expression in Escherichia coli. Mol. Microbiol., 6, 2557-2563.
54. Dorman,C.J. and Deighan,P. (2003) Regulation of gene expression by histone-like proteins in bacteria. Curr. Opin. Genet. Dev., 13 179-184.
55. von Lackum,K., Ollison,K.M., Bykowski,T., Nowalk,A.J., Hughes,J.L., Carroll,J.A., Zückert,W.R. and Stevenson,B. (2007) Regulated synthesis of the Borrelia burgdorferi inner-membrane lipoprotein IpLA7 (P22, P22-A) during the Lyme disease spirochaete's mammal-tick infectious cycle. Microbiology, 153, 1361-1371.
56. Medrano,M.S., Ding,Y., Wang,X.G., Lu,P., Coburn,J. and Hu,L.T. (2007) Regulators of expression of the oligopeptide permease A proteins of Borrelia burgdorferi. J. Bacteriol., 189, 2653-2659.