Crystal structures of the Erp protein family members ErpP and ErpC from Borrelia burgdorferi reveal the reason for different affinities for complement regulator factor H

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1854, Issue 5, 2015, Pages 349-355

  Brangulis, Kalvis ^a,b,c   Petrovskis, Ivars ^b   Kazaks, Andris ^b   Akopjana, Inara ^b   Tars, Kaspars ^b,d  

^a LATVIAN INSTITUTE OF ORGANIC SYNTHESIS   (Latvia)

^b LATVIAN BIOMEDICAL RESEARCH AND STUDY CENTRE   (Latvia)

^c RIGA STRADINS UNIVERSITY   (Latvia)

^d UNIVERSITY OF LATVIA   (Latvia)

Author keywords

Borrelia Ixodes; Complement; Lyme borreliosis; Lyme disease therapy; Outer surface proteins; Spirochetes

Indexed keywords

BACTERIAL PROTEIN; COMPLEMENT FACTOR H; ERPC PROTEIN; ERPP PROTEIN; OUTER MEMBRANE PROTEIN; UNCLASSIFIED DRUG; BACTERIAL OUTER MEMBRANE PROTEINS; ERPC PROTEIN, BORRELIA BURGDORFERI; ERPP PROTEIN, BORRELIA BURGDORFERI; PROTEIN BINDING; RECEPTORS, CELL SURFACE;

ARTICLE; BACTERIAL STRAIN; BINDING AFFINITY; BINDING SITE; BORRELIA BURGDORFERI; COMPLEX FORMATION; CRYSTAL STRUCTURE; LYME DISEASE; MOLECULAR CLONING; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN PURIFICATION; AMINO ACID SEQUENCE; BINDING SITES; CHEMISTRY; COMPARATIVE STUDY; CRYSTALLOGRAPHY, X-RAY; METABOLISM; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SEQUENCE HOMOLOGY, AMINO ACID; SUBSTRATE SPECIFICITY;

BORRELIA; BORRELIA BURGDORFERI; IXODES; IXODIDA;

AMINO ACID SEQUENCE; BACTERIAL OUTER MEMBRANE PROTEINS; BINDING SITES; COMPLEMENT FACTOR H; CRYSTALLOGRAPHY, X-RAY; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, CELL SURFACE; SEQUENCE HOMOLOGY, AMINO ACID; SUBSTRATE SPECIFICITY;

EID: 84922287220     PISSN: 15709639     EISSN: 18781454     Source Type: Journal    
DOI: 10.1016/j.bbapap.2014.12.025     Document Type: Article

References (43)

1. A.G. Barbour, and D. Fish The biological and social phenomenon of Lyme disease Science 260 1993 1610 1616
2. A.C. Steere, J. Coburn, and L. Glickstein The emergence of Lyme disease J. Clin. Invest. 113 2004 1093 1101
3. P. Kraiczy, C. Skerka, M. Kirschfink, V. Brade, and P.F. Zipfel Immune evasion of Borrelia burgdorferi by acquisition of human complement regulators FHL-1/reconectin and Factor H Eur. J. Immunol. 31 2001 1674 1684
4. C. Siegel, T. Hallstrom, C. Skerka, H. Eberhardt, B. Uzonyi, T. Beckhaus, M. Karas, R. Wallich, B. Stevenson, P.F. Zipfel, and P. Kraiczy Complement factor H-related proteins CFHR2 and CFHR5 represent novel ligands for the infection-associated CRASP proteins of Borrelia burgdorferi PLoS ONE 5 2010 e13519
5. C. Hammerschmidt, T. Hallstrom, C. Skerka, R. Wallich, B. Stevenson, P.F. Zipfel, and P. Kraiczy Contribution of the infection-associated complement regulator-acquiring surface protein 4 (ErpC) to complement resistance of Borrelia burgdorferi Clin. Dev. Immunol. 2012 2012 349657
6. P.F. Zipfel, T. Hallstrom, and K. Riesbeck Human complement control and complement evasion by pathogenic microbes-tipping the balance Mol. Immunol. 56 2013 152 160
7. E.R. Podack, and J. Tschopp Membrane attack by complement Mol. Immunol. 21 1984 589 603
8. P.F. Zipfel, T.S. Jokiranta, J. Hellwage, V. Koistinen, and S. Meri The factor H protein family Immunopharmacology 42 1999 53 60
9. J. Ripoche, A.J. Day, T.J. Harris, and R.B. Sim The complete amino acid sequence of human complement factor H Biochem. J. 249 1988 593 602
10. C. Estaller, W. Schwaeble, M. Dierich, and E.H. Weiss Human complement factor H: two factor H proteins are derived from alternatively spliced transcripts Eur. J. Immunol. 21 1991 799 802
11. S. Kuhn, and P.F. Zipfel Mapping of the domains required for decay acceleration activity of the human factor H-like protein 1 and factor H Eur. J. Immunol. 26 1996 2383 2387
12. C. Skerka, Q. Chen, V. Fremeaux-Bacchi, and L.T. Roumenina Complement factor H related proteins (CFHRs) Mol. Immunol. 56 2013 170 180
13. C. Skerka, C. Timmann, R.D. Horstmann, and P.F. Zipfel Two additional human serum proteins structurally related to complement factor H. Evidence for a family of factor H-related genes J. Immunol. 148 1992 3313 3318
14. E. Goicoechea de Jorge, J.J. Caesar, T.H. Malik, M. Patel, M. Colledge, S. Johnson, S. Hakobyan, B.P. Morgan, C.L. Harris, M.C. Pickering, and S.M. Lea Dimerization of complement factor H-related proteins modulates complement activation in vivo Proc. Natl. Acad. Sci. U. S. A. 110 2013 4685 4690
15. S. Kuhn, C. Skerka, and P.F. Zipfel Mapping of the complement regulatory domains in the human factor H-like protein 1 and in factor H1 J. Immunol. 155 1995 5663 5670
16. M.C. Schneider, B.E. Prosser, J.J. Caesar, E. Kugelberg, S. Li, Q. Zhang, S. Quoraishi, J.E. Lovett, J.E. Deane, R.B. Sim, P. Roversi, S. Johnson, C.M. Tang, and S.M. Lea Neisseria meningitidis recruits factor H using protein mimicry of host carbohydrates Nature 458 2009 890 893
17. P. Kraiczy, C. Skerka, V. Brade, and P.F. Zipfel Further characterization of complement regulator-acquiring surface proteins of Borrelia burgdorferi Infect. Immun. 69 2001 7800 7809
18. P. Kraiczy, and B. Stevenson Complement regulator-acquiring surface proteins of Borrelia burgdorferi: structure, function and regulation of gene expression Ticks Tick Borne Dis. 4 2013 26 34
19. J. Hellwage, T. Meri, T. Heikkila, A. Alitalo, J. Panelius, P. Lahdenne, I.J. Seppala, and S. Meri The complement regulator factor H binds to the surface protein OspE of Borrelia burgdorferi J. Biol. Chem. 276 2001 8427 8435
20. K. Haupt, P. Kraiczy, R. Wallich, V. Brade, C. Skerka, and P.F. Zipfel Binding of human factor H-related protein 1 to serum-resistant Borrelia burgdorferi is mediated by borrelial complement regulator-acquiring surface proteins J. Infect. Dis. 196 2007 124 133
21. P. Kraiczy, J. Hellwage, C. Skerka, H. Becker, M. Kirschfink, M.M. Simon, V. Brade, P.F. Zipfel, and R. Wallich Complement resistance of Borrelia burgdorferi correlates with the expression of BbCRASP-1, a novel linear plasmid-encoded surface protein that interacts with human factor H and FHL-1 and is unrelated to Erp proteins J. Biol. Chem. 279 2004 2421 2429
22. F.S. Cordes, P. Roversi, P. Kraiczy, M.M. Simon, V. Brade, O. Jahraus, R. Wallis, C. Skerka, P.F. Zipfel, R. Wallich, and S.M. Lea A novel fold for the factor H-binding protein BbCRASP-1 of Borrelia burgdorferi Nat. Struct. Mol. Biol. 12 2005 276 277
23. J.J. Caesar, R. Wallich, P. Kraiczy, P.F. Zipfel, and S.M. Lea Further structural insights into the binding of complement factor H by complement regulator-acquiring surface protein 1 (CspA) of Borrelia burgdorferi Acta Crystallogr. Sect. F: Struct. Biol. Cryst. Commun. 69 2013 629 633
24. K. Hartmann, C. Corvey, C. Skerka, M. Kirschfink, M. Karas, V. Brade, J.C. Miller, B. Stevenson, R. Wallich, P.F. Zipfel, and P. Kraiczy Functional characterization of BbCRASP-2, a distinct outer membrane protein of Borrelia burgdorferi that binds host complement regulators factor H and FHL-1 Mol. Microbiol. 61 2006 1220 1236
25. E.A. Rogers, and R.T. Marconi Delineation of species-specific binding properties of the CspZ protein (BBH06) of Lyme disease spirochetes: evidence for new contributions to the pathogenesis of Borrelia spp Infect. Immun. 75 2007 5272 5281
26. K. Brangulis, I. Petrovskis, A. Kazaks, J. Bogans, M. Otikovs, K. Jaudzems, R. Ranka, and K. Tars Structural characterization of CspZ, a complement regulator factor H and FHL-1 binding protein from Borrelia burgdorferi FEBS J. 281 2014 2613 2622
27. P. Kraiczy, K. Hartmann, J. Hellwage, C. Skerka, M. Kirschfink, V. Brade, P.F. Zipfel, R. Wallich, and B. Stevenson Immunological characterization of the complement regulator factor H-binding CRASP and Erp proteins of Borrelia burgdorferi Int. J. Med. Microbiol. 293 Suppl. 37 2004 152 157
28. P. Kraiczy, J. Hellwage, C. Skerka, M. Kirschfink, V. Brade, P.F. Zipfel, and R. Wallich 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 2003 697 707
29. A. Bhattacharjee, J.S. Oeemig, R. Kolodziejczyk, T. Meri, T. Kajander, M.J. Lehtinen, H. Iwai, T.S. Jokiranta, and A. Goldman Structural basis for complement evasion by Lyme disease pathogen Borrelia burgdorferi J. Biol. Chem. 288 2013 18685 18695
30. B. Stevenson, K. Tilly, and P.A. Rosa A family of genes located on four separate 32-kilobase circular plasmids in Borrelia burgdorferi B31 J. Bacteriol. 178 1996 3508 3516
31. J.J. Caesar, S. Johnson, P. Kraiczy, and S.M. Lea ErpC, a member of the complement regulator-acquiring family of surface proteins from Borrelia burgdorferi, possesses an architecture previously unseen in this protein family Acta Crystallogr. Sect. F: Struct. Biol. Cryst. Commun. 69 2013 624 628
32. A. Seling, C. Siegel, V. Fingerle, B.L. Jutras, C.A. Brissette, C. Skerka, R. Wallich, P.F. Zipfel, B. Stevenson, and P. Kraiczy Functional characterization of Borrelia spielmanii outer surface proteins that interact with distinct members of the human factor H protein family and with plasminogen Infect. Immun. 78 2010 39 48
33. A.G. Leslie The integration of macromolecular diffraction data Acta Crystallogr. D Biol. Crystallogr. 62 2006 48 57
34. P. Evans Scaling and assessment of data quality Acta Crystallogr. D Biol. Crystallogr. 62 2006 72 82
35. M.D. Winn, C.C. Ballard, K.D. Cowtan, E.J. Dodson, P. Emsley, P.R. Evans, R.M. Keegan, E.B. Krissinel, A.G. Leslie, A. McCoy, S.J. McNicholas, G.N. Murshudov, N.S. Pannu, E.A. Potterton, H.R. Powell, R.J. Read, A. Vagin, and K.S. Wilson Overview of the CCP4 suite and current developments Acta Crystallogr. D Biol. Crystallogr. 67 2011 235 242
36. A.J. McCoy, R.W. Grosse-Kunstleve, P.D. Adams, M.D. Winn, L.C. Storoni, and R.J. Read Phaser crystallographic software J. Appl. Crystallogr. 40 2007 658 674
37. K. Cowtan The Buccaneer software for automated model building. 1. Tracing protein chains Acta Crystallogr. D Biol. Crystallogr. 62 2006 1002 1011
38. P. Emsley, and K. Cowtan Coot: model-building tools for molecular graphics Acta Crystallogr. D Biol. Crystallogr. 60 2004 2126 2132
39. G.N. Murshudov, A.A. Vagin, and E.J. Dodson Refinement of macromolecular structures by the maximum-likelihood method Acta Crystallogr. D Biol. Crystallogr. 53 1997 240 255
40. A. Alitalo, T. Meri, H. Lankinen, I. Seppala, P. Lahdenne, P.S. Hefty, D. Akins, and S. Meri 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 2002 3847 3853
41. M.S. Metts, J.V. McDowell, M. Theisen, P.R. Hansen, and R.T. Marconi Analysis of the OspE determinants involved in binding of factor H and OspE-targeting antibodies elicited during Borrelia burgdorferi infection in mice Infect. Immun. 71 2003 3587 3596
42. A. Alitalo, T. Meri, T. Chen, H. Lankinen, Z.Z. Cheng, T.S. Jokiranta, I.J. Seppala, P. Lahdenne, P.S. Hefty, D.R. Akins, and S. Meri Lysine-dependent multipoint binding of the Borrelia burgdorferi virulence factor outer surface protein E to the C terminus of factor H J. Immunol. 172 2004 6195 6201
43. A. Bhattacharjee, J.S. Oeemig, R. Kolodziejczyk, T. Meri, T. Kajander, M.J. Lehtinen, H. Iwai, T.S. Jokiranta, and A. Goldman Structural basis for complement evasion by Lyme disease pathogen Borrelia burgdorferi J. Biol. Chem. 288 2013 18685 18695