Lyme borreliosis spirochete Erp proteins, their known host ligands, and potential roles in mammalian infection

International Journal of Medical Microbiology

Volumn 298, Issue SUPPL. 1, 2008, Pages 257-267

  Brissette, Catherine A ^a   Cooley, Anne E ^a   Burns, Logan H ^a   Riley, Sean P ^a   Verma, Ashutosh ^a   Woodman, Michael E ^a   Bykowski, Tomasz ^a   Stevenson, Brian ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

Author keywords

Adhesin; Borrelia burgdorferi; Complement; Factor H; Laminin; Outer surface protein

Indexed keywords

ADHESIN; BACTERIAL PROTEIN; COMPLEMENT FACTOR H; LAMININ; PROTEIN ERP;

BACTERIAL COLONIZATION; BORRELIA BURGDORFERI; EXTRACELLULAR MATRIX; GENE LOCUS; LYME DISEASE; NONHUMAN; PARASITE VECTOR; PROTEIN BINDING; PROTEIN FUNCTION; SHORT SURVEY; TICK;

ANIMALS; BACTERIAL OUTER MEMBRANE PROTEINS; BORRELIA BURGDORFERI; COMPLEMENT FACTOR H; HOST-PATHOGEN INTERACTIONS; HUMANS; LAMININ; LIGANDS; LIPOPROTEINS; LYME DISEASE;

EID: 48349147505     PISSN: 14384221     EISSN: 16180607     Source Type: Journal    
DOI: 10.1016/j.ijmm.2007.09.004     Document Type: Short Survey

References (117)

1. Akins D.R., Porcella S.F., Popova T.G., Shevchenko D., Baker S.I., Li M., Norgard M.V., and Radolf J.D. Evidence for in vivo but not in vitro expression of a Borrelia burgdorferi outer surface protein F (OspF) homologue. Mol. Microbiol. 18 (1995) 507-520
2. Akins D.R., Caimano M.J., Yang X., Cerna F., Norgard M.V., and Radolf J.D. Molecular and evolutionary analysis of Borrelia burgdorferi 297 circular plasmid-encoded lipoproteins with OspE- and OspF-like leader peptides. Infect. Immun. 67 (1999) 1526-1532
3. Alitalo A., Meri T., Rämö L., Jokiranta T.S., Heikkilä T., Seppälä I.J.T., Oksi J., Viljanen M., and Meri S. Complement evasion by Borrelia burgdorferi: serum-resistant strains promote C3b inactivation. Infect. Immun. 69 (2001) 3685-3691
4. Alitalo A., Meri T., Lankinen H., Seppälä I., Lahdenne P., Hefty P.S., Akins D., and Meri S. 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
5. Alitalo A., Meri T., Chen T., Lankinen H., Cheng Z.-Z., Jokiranta T.S., Seppälä I.J.T., Lahdenne P., Hefty P.S., Akins D.R., and Meri S. 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
6. Aslam M., and Perkins S.J. Folded-back solution structure of monomeric factor H of human complement by synchrotron X-ray and neutron scattering, analytical ultracentrifugation and constrained molecular modeling. J. Mol. Biol. 309 (2001) 1117-1138
7. Avery V.M., and Gordon D.L. Characterization of factor H binding to polymorphonuclear leukocytes. J. Immunol. 151 (1993) 5545-5553
8. Babb K., McAlister J.D., Miller J.C., and Stevenson B. Molecular characterization of Borrelia burgdorferi erp promoter/operator elements. J. Bacteriol. 186 (2004) 2745-2756
9. Babb K., Bykowski T., Riley S.P., Miller M.C., DeMoll E., and Stevenson B. 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 (2006) 4331-4339
10. Barbosa A.S., Abreu P.A.E., Neves F.O., Atzingen M.V., Watanabe M.M., Vieira M.L., Morais Z.M., Vasconcellos S.A., and Nascimentao A.L.T.O. A newly identified leptospiral adhesin mediates attachment to laminin. Infect. Immun. 74 (2006) 6356-6364
11. Barthold S.W. Infectivity of Borrelia burgdorferi relative to route of inoculation and genotype in laboratory mice. J. Infect. Dis. 163 (1991) 419-420
12. Brade V., Kleber I., and Acker G. Differences of two Borrelia burgdorferi strains in complement activation and serum resistance. Immunobiology 185 (1992) 453-465
13. Breitner-Ruddock S., Würzner R., Schulze J., and Brade V. Heterogeneity in the complement-dependent bacteriolysis within the species of Borrelia burgdorferi. Med. Microbiol. Immunol. 185 (1997) 253-260
14. Brooks C.S., Vuppala S.R., Jett A.M., Alitalo A., Meri S., and Akins D.R. Complement regulator-acquiring surface protein 1 imparts resistance to human serum in Borrelia burgdorferi. J. Immunol. 175 (2005) 3299-3308
15. Caimano M.J., Yang X., Popova T.G., Clawson M.L., Akins D.R., Norgard M.V., and Radolf J.D. Molecular and evolutionary characterization of the cp32/18 family of supercoiled plasmids in Borrelia burgdorferi 297. Infect. Immun. 68 (2000) 1574-1586
16. Casjens S., van Vugt R., Tilly K., Rosa P.A., and Stevenson B. Homology throughout the multiple 32-kilobase circular plasmids present in Lyme disease spirochetes. J. Bacteriol. 179 (1997) 217-227
17. Casjens S., Palmer N., van Vugt R., Huang W.M., Stevenson B., Rosa P., Lathigra R., Sutton G., Peterson J., Dodson R.J., Haft D., Hickey E., Gwinn M., White O., and Fraser C. 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 (2000) 490-516
18. Casjens S.R., Huang W.M., Gilcrease E.B., Qiu W., McCaig W.D., Luft B.J., Schutzer S.E., and Fraser C.M. Comparative genomics of Borrelia burgdorferi. In: Cabello F.C., Hulinska D., and Godfrey H.P. (Eds). Molecular Biology of Spirochetes (2006), IOS Press, Amsterdam 79-95
19. Cassatt D.R., Patel N.K., Ulbrandt N.D., and Hanson M.S. DbpA, but not OspA, is expressed by Borrelia burgdorferi during spirochetemia and is a target for protective antibodies. Infect. Immun. 66 (1998) 5379-5387
20. Cheng Z.Z., Hellwage J., Seeberger H., Zipfel P.F., Meri S., and Jokiranta T.S. Comparison of surface recognition and C3b binding properties of mouse and human complement factor H. Mol. Immunol. 43 (2006) 972-979
21. Colognato H., and Yurchenco P.D. Form and function: the laminin family of heterotrimers. Dev. Dyn. 218 (2000) 213-234
22. Damman C.J., Eggers C.H., Samuels D.S., and Oliver D.B. Characterization of Borrelia burgdorferi BlyA and BlyB proteins: a prophage-encoded holin-like system. J. Bacteriol. 182 (2000) 6791-6797
23. Das S., Barthold S.W., Stocker Giles S., Montgomery R.R., Telford S.R., and Fikrig E. Temporal pattern of Borrelia burgdorferi p21 expression in ticks and the mammalian host. J. Clin. Invest. 99 (1997) 987-995
24. De Koning J., Bosma R.B., and Hoogkamp-Korstanje J.A. Demonstration of spirochaetes in patients with Lyme disease with a modified silver stain. J. Med. Microbiol. 23 (1987) 261-267
25. 2 (CD11b/CD18). J. Immunol. 160 (1998) 4057-4066
26. Eggers C.H., and Samuels D.S. Molecular evidence for a new bacteriophage of Borrelia burgdorferi. J. Bacteriol. 181 (1999) 7308-7313
27. Eggers C.H., Kimmel B.J., Bono J.L., Elias A.F., Rosa P., and Samuels D.S. Transduction by ØBB-1, a bacteriophage of Borrelia burgdorferi. J. Bacteriol. 183 (2001) 4771-4778
28. Eggers C.H., Caimano M.J., and Radolf J.D. Analysis of promoter elements involved in the transcription initiation of RpoS-dependent Borrelia burgdorferi genes. J. Bacteriol. 186 (2004) 7390-7402
29. Eggers C.H., Caimano M.J., and Radolf J.D. Sigma factor selectivity in Borrelia burgdorferi: RpoS recognition of the ospE/ospF/elp promoters is dependent on the sequence of the -10 region. Mol. Microbiol. 59 (2006) 1859-1875
30. El-Hage N., Babb K., Carroll J.A., Lindstrom N., Fischer E.R., Miller J.C., Gilmore Jr. R.D., Mbow M.L., and Stevenson B. Surface exposure and protease insensitivity of Borrelia burgdorferi Erp (OspEF-related) lipoproteins. Microbiology 147 (2001) 821-830
31. El-Hage N., and Stevenson B. Simultaneous coexpression of Borrelia burgdorferi Erp proteins occurs through a specific, erp locus-directed regulatory mechanism. J. Bacteriol. 184 (2002) 4536-4543
32. Feng S., Hodzic E., Stevenson B., and Barthold S.W. Humoral immunity to Borrelia burgdorferi N40 decorin binding proteins during infection of laboratory mice. Infect. Immun. 66 (1998) 2827-2835
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., Gwinn M., Dougherty B., Tomb J.-F., Fleischmann R.D., Richardson D., Peterson J., Kerlavage A.R., Quackenbush J., Salzberg S., Hanson M., van Vugt R., Palmer N., Adams M.D., Gocayne J., Weidmann J., Utterback T., Watthey L., McDonald L., Artiach P., Bowman C., Garland S., Fujii C., Cotton M.D., Horst K., Roberts K., Hatch B., Smith H.O., and Venter J.C. Genomic sequence of a Lyme disease spirochaete, Borrelia burgdorferi. Nature 390 (1997) 580-586
34. Friese M.A., Hellwage J., Jokiranta T.S., Meri S., Peter H.H., Eibel H., and Zipfel P.F. FHL-1/reconectin and factor H: two human complement regulators which are encoded by the same gene are differently expressed and regulated. Mol. Immunol. 36 (1999) 809-818
35. Gilmore Jr. R.D., Mbow M.L., and Stevenson B. Analysis of Borrelia burgdorferi gene expression during life cycle phases of the tick vector Ixodes scapularis. Microbes Infect. 3 (2001) 799-808
36. Grab D.J., Givens C., and Kennedy R. Fibronectin-binding activity in Borrelia burgdorferi. Biochim. Biophys. Acta 1407 (1998) 135-145
37. Guo B.P., Norris S.J., Rosenberg L.C., and Höök M. Adherence of Borrelia burgdorferi to the proteoglycan decorin. Infect. Immun. 63 (1995) 3467-3472
38. Hagman K.E., Lahdenne P., Popova T.G., Porcella S.F., Akins D.R., Radolf J.D., and Norgard M.V. Decorin-binding protein of Borrelia burgdorferi is encoded within a two-gene operon and is protective in the murine model of Lyme borreliosis. Infect. Immun. 66 (1998) 2674-2683
39. Hammerschmidt S., Agarwal V., Kunert A., Haelbich H., Skerka C., and Zipfel P.F. The host immune regulator factor H interacts via two contact sites with the PspC protein of Streptococcus pneumoniae and mediates adhesion to host epithelial cells. J. Immunol. 178 (2007) 5848-5858
40. Hartmann K., Corvey C., Skerka C., Kirschfink M., Karas M., Brade V., Miller J.C., Stevenson B., Wallich R., Zipfel P.F., and Kraiczy P. 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
41. Häupl T., Hahn G., Rittig M., Krause A., Schoerner C., Schönherr U., Kalden J.R., and Burmester G.R. Persistence of Borrelia burgdorferi in ligamentous tissue from a patient with chronic Lyme borreliosis. Arthritis. Rheum. 36 (1993) 1621-1626
42. Haupt K., Wallich R., Kraiczy P., Brade V., Skerka C., and Zipfel P.F. Binding of human FHR-1 to serum resistant Borrelia burgdorferi is mediated by borrelial complement regulator-acquiring surface proteins. J. Infect. Dis. 196 (2007) 124-133
43. Hefty P.S., Jolliff S.E., Caimano M.J., Wikel S.K., Radolf J.D., and Akins D.R. Regulation of OspE-related, OspF-related, and Elp lipoproteins of Borrelia burgdorferi strain 297 by mammalian host-specific signals. Infect. Immun. 69 (2001) 3618-3627
44. Hefty P.S., Jolliff S.E., Caimano M.J., Wikel S.K., and Akins D.R. Changes in the temporal and spatial patterns of outer surface lipoprotein expression generate population heterogeneity and antigenic diversity in the Lyme disease spirochete, Borrelia burgdorferi. Infect. Immun. 70 (2002) 3468-3478
45. Hellwage J., Kühn S., and Zipfel P.F. The human complement regulatory factor-H-like protein 1, which represents a truncated form of factor H, displays cell-attachment activity. Biochem. J. 326 (1997) 321-327
46. Hellwage J., Jokiranta T.S., Koistinen V., Vaarala O., Meri S., and Zipfel P.F. Functional properties of complement factor H-related proteins FHR-3 and FHR-4: binding to the C3d region of C3b and differential regulation by heparin. FEBS Lett. 462 (1999) 345-352
47. Hellwage J., Meri T., Heikkilä T., Alitalo A., Panelius J., Lahdenne P., Seppälä I.J.T., and Meri S. The complement regulatory factor H binds to the surface protein OspE of Borrelia burgdorferi. J. Biol. Chem. 276 (2001) 8427-8435
48. Hellwage J., Jokiranta T.S., Friese M.A., Wolk T.U., Kampen E., Zipfel P.F., and Meri S. Complement C3b/C3d and cell surface polyanions are recognized by overlapping binding sites on the most carboxy-terminal domain of complement factor H. J. Immunol. 169 (2002) 6935-6944
49. Hellwage J., Eberle F., Babuke T., Seeberger H., Richter H., Kunert A., Hartl A., Zipfel P.F., Jokiranta T.S., and Jozsi M. Two factor H-related proteins from the mouse: expression, analysis and functional characterization. Immunogenetics 58 (2006) 883-893
50. Hovis K.M., Tran E., Sundy C.M., Buckles E., McDowell J.V., and Marconi R.T. Selective binding of Borrelia burgdorfer OspE paralogs to factor H and serum proteins from diverse animals: possible expansion of the role of OspE in Lyme disease pathogenesis. Infect. Immun. 74 (2006) 1967-1972
51. Iyer R., Kalu O., Purser J., Norris S., Stevenson B., and Schwartz I. Linear and circular plasmid content in Borrelia burgdorferi clinical isolates. Infect. Immun. 71 (2003) 3699-3706
52. Jokiranta T.S., Cheng Z.Z., Seeberger H., Józsi M., Heinen S., Noris M., Remuzzi G., Ormsby R., Gordon D.L., Meri S., Hellwage J., and Zipfel P.F. Binding of complement factor H to endothelial cells is mediated by the carboxy-terminal glycosaminoglycan binding site. Am. J. Pathol. 167 (2005) 1173-1181
53. Jószi M., Oppermann M., Lambris J.D., and Zipfel P.F. The C-terminus of complement factor H is essential for host cell protection. Mol. Immunol. 44 (2007) 2697-2706
54. Kochi S.K., Johnson R.C., and Dalmasso A.P. Complement-mediated killing of the Lyme disease spirochete Borrelia burgdorferi: role of antibody in formation of an effective membrane attack complex. J. Immunol. 146 (1991) 3964-3970
55. Kraiczy P., Hunfeld K.-P., Breiner-Ruddock S., Würzner R., Acker G., and Brade V. Comparison of two laboratory methods for the determination of serum resistance in Borrelia burgdorferi isolates. Immunobiology 201 (2000) 406-419
56. Kraiczy P., Skerka C., Brade V., and Zipfel P.F. Further characterization of complement regulator-acquiring surface proteins of Borrelia burgdorferi. Infect. Immun. 69 (2001) 7800-7809
57. Kraiczy P., Skerka C., Kirschfink M., Brade V., and Zipfel P.F. Immune evasion of Borrelia burgdorferi by acquisition of human complement regulators FHL-1/reconectin and factor H. Eur. J. Immunol. 31 (2001) 1674-1684
58. Kraiczy P., Skerka C., Kirschfink M., Zipfel P.F., and Brade V. Immune evasion of Borrelia burgdorferi: insufficient killing of the pathogens by complement and antibody. Int. J. Med. Microbiol. 291 Suppl. 33 (2002) 141-146
59. Kraiczy P., Skerka C., Zipfel P.F., and Brade V. Complement regulator-acquiring surface proteins of Borrelia burgdorferi: a new protein family involved in complement resistance. Wien. Klin. Wochenschr. 114 (2002) 568-573
60. Kraiczy P., Hellwage J., Skerka C., Kirschfink M., Brade V., Zipfel P.F., and Wallich R. 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
61. Kraiczy P., Hartmann K., Hellwage J., Skerka C., Brade V., Zipfel P.F., Wallich R., and Stevenson B. 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
62. Kraiczy P., Hellwage J., Skerka C., Becker H., Kirschfink M., Simon M.M., Brade V., Zipfel P.F., and Wallich R. 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
63. Kraiczy P., Rossmann E., Brade V., Simon M.M., Skerka C., Zipfel P.F., and Wallich R. Binding of human complement regulators FHL-1 and factor H to CRASP-1 orthologs of Borrelia burgdorferi. Wien. Klin. Wochenschr. 118 (2006) 669-676
64. Kurtenbach K., Sewell H.-S., Ogden N.H., Randolph S.E., and Nuttall P.A. Serum complement sensitivity as a key factor in Lyme disease ecology. Infect. Immun. 66 (1998) 1248-1251
65. Kurtenbach K., DeMichelis S., Etti S., Schäfer S.M., Sewell H.-S., Brade V., and Kraiczy P. Host association of Borrelia burgdorferi sensu lato - the key role of host complement. Trends Microbiol. 10 (2002) 74-79
66. Lam T.T., Nguyen T.-P.K., Montgomery R.R., Kantor F.S., Fikrig E., and Flavell R.A. Outer surface proteins E and F of Borrelia burgdorferi, the agent of Lyme disease. Infect. Immun. 62 (1994) 290-298
67. Liang F.T., Nelson F.K., and Fikrig E. Molecular adaptation of Borrelia burgdorferi in the murine host. J. Exp. Med. 196 (2002) 275-280
68. Malhotra R., Ward M., Sim R.B., and Bird M.I. Identification of human complement factor H as a ligand for L-selectin. Biochem. J. 341 (1999) 61-69
69. Marconi R.T., Sung S.Y., Hughes C.A.N., and Carlyon J.A. Molecular and evolutionary analyses of a variable series of genes in Borrelia burgdorferi that are related to ospE and ospF, constitute a gene family, and share a common upstream homology box. J. Bacteriol. 178 (1996) 5615-5626
70. McDowell J.V., Sung S.Y., Price G., and Marconi R.T. Demonstration of the genetic stability and temporal expression of select members of the Lyme disease spirochete OspF protein family during infection in mice. Infect. Immun. 69 (2001) 4831-4838
71. McDowell J.V., Wolfgang J., Tran E., Metts M.S., Hamilton D., and Marconi R.T. Comprehensive analysis of the factor H binding capabilities of Borrelia species associated with Lyme disease: delineation of two distinct classes of factor H binding proteins. Infect. Immun. 71 (2003) 3597-3602
72. McDowell J.V., Wolfgang J., Senty L., Sundy C.M., Noto M.J., and Marconi R.T. Demonstration of the involvement of outer surface protein E coiled coil structural domains and higher order structural elements in the binding of infection-induced antibody and the complement-regulatory protein, factor H. J. Immunol. 173 (2004) 7471-7480
73. McDowell J.V., Hovis K.M., Zhang H., Tran E., Lankford J., and Marconi R.T. Evidence that BBA68 protein (BbCRASP-1) of the Lyme disease spirochetes does not contribute to factor H-mediated immune evasion in humans and other animals. Infect. Immun. 74 (2006) 3030-3034
74. McRae J.L., Duthy T.G., Griggs K.M., Ormsby R.J., Cowan P.J., Cromer B.A., McKinstry W.J., Parker M.W., Murphy B.F., and Gordon D.L. Human factor H-related protein 5 has cofactor activity, inhibits C3 convertase activity, binds heparin and C-reactive protein, and associates with lipoprotein. J. Immunol. 174 (2005) 6250-6256
75. Metts M.S., McDowell J.V., Theisen M., Hansen P.R., and Marconi R.T. Analysis of the OspE determinants involved in binding of factor H and OspE-targeting antibodies elicited during Borrelia burgdorferi infection. Infect. Immun. 71 (2003) 3587-3596
76. Miller J.C., Bono J.L., Babb K., El-Hage N., Casjens S., and Stevenson B. A second allele of eppA in Borrelia burgdorferi strain B31 is located on the previously undetected circular plasmid cp9-2. J. Bacteriol. 182 (2000) 6254-6258
77. Miller J.C., von Lackum K., Babb K., McAlister J.D., and Stevenson B. Temporal analysis of Borrelia burgdorferi Erp protein expression throughout the mammal-tick infectious cycle. Infect. Immun. 71 (2003) 6943-6952
78. Miller J.C., Narayan K., Stevenson B., and Pachner A.R. Expression of Borrelia burgdorferi erp genes during infection of non-human primates. Microb. Pathog. 39 (2005) 27-33
79. Miller J.C., and Stevenson B. Borrelia burgdorferi erp genes are expressed at different levels within tissues of chronically infected mammalian hosts. Int. J. Med. Microbiol. 296 Suppl. 1 (2006) 185-194
80. Miller J.C., von Lackum K., Woodman M.E., and Stevenson B. Detection of Borrelia burgdorferi gene expression during mammalian infection using transcriptional fusions that produce green fluorescent protein. Microb. Pathog. 41 (2006) 43-47
81. Misasi R., Huemer H.P., Schwaeble W., Solder E., Larcher C., and Dierich M.P. Human complement factor H: an additional gene product of 43 kDa isolated from human plasma shows cofactor activity for the cleavage of the third component of complement. Eur. J. Immunol. 19 (1989) 1765-1768
82. Oppermann M., Manuelian T., Józsi M., Brandt E., Jokiranta T.S., Heinen S., Meri S., Skerka C., Götze O., and Zipfel P.F. The C-terminus of complement regulator factor H mediates target recognition: evidence for a compact conformation of the native protein. Clin. Exp. Immunol. 144 (2006) 342-352
83. Pachner A.R., Basta J., Delaney E., and Hulinska D. Localization of Borrelia burgdorferi in murine Lyme borreliosis by electron microscopy. Am. J. Trop. Med. Hyg. 52 (1995) 128-133
84. Park C.T., and Wright S.D. Plasma lipopolysaccharide-binding protein is found associated with a particle containing apolipoprotein A-I, phospholipid, and factor H-related proteins. J. Biol. Chem. 271 (1996) 18054-18060
85. Park C.T., and Wright S.D. Fibrinogen is a component of a novel lipoprotein particle: factor H-related protein (FHRP)-associated lipoprotein particle (FALP). Blood 95 (2000) 198-204
86. Patarakul K., Cole M.F., and Hughes C.A.N. Complement resistance in Borrelia burgdorferi strain 297: outer membrane proteins prevent MAC formation at lysis susceptible sites. Microb. Pathog. 27 (1999) 25-41
87. Pausa M., Pellis V., Cinco M., Giulianini P.G., Presani G., Perticarari S., Murgia R., and Tedesco F. Serum-resistant strains of Borrelia burgdorferi evade complement-mediated killing by expressing a CD59-like complement inhibitory molecule. J. Immunol. 170 (2003) 3214-3222
88. Perkins S.J., and Goodship T.H. Molecular modelling of the C-terminal domains of factor H of human complement: a correlation between haemolytic uraemic syndrome and a predicted heparin binding site. J. Mol. Biol. 316 (2002) 217-224
89. Porcella S.F., Popova T.G., Akins D.R., Li M., Radolf J.D., and Norgard M.V. Borrelia burgdorferi supercoiled plasmids encode multi-copy tandem open reading frames and a lipoprotein gene family. J. Bacteriol. 178 (1996) 3293-3307
90. Probert W.S., and Johnson B.J.B. Identification of a 47 kDA fibronectin-binding protein expressed by Borrelia burgdorferi isolate B31. Mol. Microbiol. 30 (1998) 1003-1015
91. Prodinger W.M., Hellwage J., Spruth M., Deirich M.P., and Zipfel P.F. The C-terminus of factor H: monoclonal antibodies inhibit heparin binding and identify epitopes common to factor H and factor H-related proteins. Biochem. J. 331 (1998) 41-47
92. Simpson W.J., Garon C.F., and Schwan T.G. Borrelia burgdorferi contains repeated DNA sequences that are species specific and plasmid associated. Infect. Immun. 58 (1990) 847-853
93. Stanek G., and Strle F. Lyme borreliosis. Lancet 362 (2003) 1639-1647
94. Stevenson B., Schwan T.G., and Rosa P.A. Temperature-related differential expression of antigens in the Lyme disease spirochete, Borrelia burgdorferi. Infect. Immun. 63 (1995) 4535-4539
95. Stevenson B., Tilly K., and Rosa P.A. A family of genes located on four separate 32-kilobase circular plasmids in Borrelia burgdorferi B31. J. Bacteriol. 178 (1996) 3508-3516
96. Stevenson B., Casjens S., van Vugt R., Porcella S.F., Tilly K., Bono J.L., and Rosa P. Characterization of cp18, a naturally truncated member of the cp32 family of Borrelia burgdorferi plasmids. J. Bacteriol. 179 (1997) 4285-4291
97. Stevenson B., Bono J.L., Schwan T.G., and Rosa P. Borrelia burgdorferi Erp proteins are immunogenic in mammals infected by tick bite, and their synthesis is inducible in cultured bacteria. Infect. Immun. 66 (1998) 2648-2654
98. Stevenson B., Casjens S., and Rosa P. Evidence of past recombination events among the genes encoding the Erp antigens of Borrelia burgdorferi. Microbiology 144 (1998) 1869-1879
99. Stevenson B., Porcella S.F., Oie K.L., Fitzpatrick C.A., Raffel S.J., Lubke L., Schrumpf M.E., and Schwan T.G. The relapsing fever spirochete Borrelia hermsii contains multiple, antigen-encoding circular plasmids that are homologous to the cp32 plasmids of Lyme disease spirochetes. Infect. Immun. 68 (2000) 3900-3908
100. Stevenson B., Zückert W.R., and Akins D.R. 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 (2001), Horizon Press, Oxford 87-100
101. Stevenson B., El-Hage N., Hines M.A., Miller J.C., and Babb K. 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 (2002) 491-497
102. Stevenson B., and Miller J.C. Intra- and interbacterial genetic exchange of Lyme disease spirochete erp genes generates sequence identity amidst diversity. J. Mol. Evol. 57 (2003) 309-324
103. Stevenson B., Bykowski T., Cooley A.E., Babb K., Miller J.C., Woodman M.E., von Lackum K., and Riley S.P. The Lyme disease spirochete Erp lipoprotein family: structure, function and regulation of expression. In: Cabello F.C., Godfrey H.P., and Hulinska D. (Eds). Molecular Biology of Spirochetes (2006), IOS Press, Amsterdam 354-372
104. Stevenson, B., Choy, H.A., Pinne, M., Rotondi, M.L., Miller, M.C., DeMoll, E., Kraiczy, P., Cooley, A.E., Creamer, T.P., Suchard, M.A., Brissette, C.A. Verma, A., Haake, D.A., 2007. Leptospira interrogans endostatin-like outer membrane proteins bind host fibronectin, laminin and regulators of complement. PLoS ONE 2, e1188
105. Suk K., Das S., Sun W., Jwang B., Barthold S.W., Flavell R.A., and Fikrig E. Borrelia burgdorferi genes selectively expressed in the infected host. Proc. Natl. Acad. Sci. USA 92 (1995) 4269-4273
106. Swofford D.L. PAUP*, Phylogenetic Analysis using Parsimony (*and Other Methods), Version 4 (2000), Sinauer Associates, Sunderland, MA
107. van Dam A.P., Oei A., Jaspars R., Fijen C., Wilske B., Spanjaard L., and Dankert J. Complement-mediated serum sensitivity among spirochetes that cause Lyme disease. Infect. Immun. 65 (1997) 1228-1236
108. Vaziri-Sani F., Hellwage J., Zipfel P.F., Sjöholm A.G., Iancu R., and Karpman D. Factor H binds to washed human platelets. J. Thromb. Haemostasis 3 (2005) 154-162
109. Verma A., Hellwage J., Artiushin S., Zipfel P.F., Kraiczy P., Timoney J.F., and Stevenson B. LfhA, a novel factor H-binding protein of Leptospira interrogans. Infect. Immun. 74 (2006) 2659-2666
110. Wallich R., Pattathu J., Kitiratschky V., Brenner C., Zipfel P.F., Brade V., Simon M.M., and Kraiczy P. Identification and functional characterization of complement regulator-acquiring surface protein 1 of the Lyme disease spirochetes Borrelia afzelii and Borrelia garinii. Infect. Immun. 73 (2005) 2351-2359
111. Woodman M.E., Cooley A.E., Miller J.C., Lazarus J.J., Tucker K., Bykowski T., Botto M., Hellwage J., Wooten R.M., and Stevenson B. Borrelia burgdorferi binding of host complement regulator factor H is not required for efficient mammalian infection. Infect. Immun. 75 (2007) 3131-3139
112. Wormser G.P. Hematogenous dissemination in early Lyme disease. Wien. Klin. Wochenschr. 118 (2006) 634-637
113. Zhang H., and Marconi R.T. Demonstration of cotranscription and 1-methyl-3-nitroso-nitroguanidine induction of a 30-gene operon of Borrelia burgdorferi: evidence that the 32-kilobase circular plasmids are prophages. J. Bacteriol. 187 (2005) 7985-7995
114. Zipfel P.F., and Skerka C. FHL-1/reconectin: a human complement and immune regulator with cell-adhesive function. Immunol. Today 20 (1999) 135-140
115. Zipfel P.F., Skerka C., Hellwage J., Jokiranta S.T., Meri S., Brade V., Kraiczy P., Noris M., and Remuzzi G. Factor H family proteins: on complement, microbes and human diseases. Biochem. Soc. Trans. 30 (2002) 971-978
116. Zipfel P.F., Edey M., Heinen S., Jozzi M., Richter H., Misselwitz J., Hoppe B., Routledge D., Strain L., Hughes A.E., Goodship J.A., Licht C., Goodship T.H.J., and Skerka C. Deletion of complement factor H-related genes CFHR1 and CFHR3 is associated with atypical hemolytic uremic syndrome. PLoS Genet. 3 (2007) e41
117. Zückert W.R., and Meyer J. Circular and linear plasmids of Lyme disease spirochetes have extensive homology: characterization of a repeated DNA element. J. Bacteriol. 178 (1996) 2287-2298