Outer surface proteins of borrelia: Peerless immune evasion tools

Current Protein and Peptide Science

Volumn 15, Issue 1, 2014, Pages 75-88

  Pulzova, Lucia ^a,b   Bhide, Mangesh ^a,b  

^a UNIVERSITY OF VETERINARY MEDICINE   (Slovakia)

^b INSTITUTE OF NEUROIMMUNOLOGY   (Slovakia)

Author keywords

Borrelia; Immune evasion; Lyme disease; Protein; Protein interactions; Surface proteins; Ticks

Indexed keywords

ADRENALIN; ATROPINE; BACTERIAL PROTEIN; CHEMOKINE RECEPTOR CCR5; COMPLEMENT REGULATOR ACQUIRING SURFACE PROTEIN; CXCL1 CHEMOKINE; CXCL9 CHEMOKINE; DECORIN; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INTEGRIN; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 12P40; INTERLEUKIN 18; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; LIPOPROTEIN; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; MEMBRANE PROTEIN; MONOCYTE CHEMOTACTIC PROTEIN 1; NORADRENALIN; OUTER SURFACE PROTEIN A; OUTER SURFACE PROTEIN B; PROTEIN P66; TOLL LIKE RECEPTOR 1; TOLL LIKE RECEPTOR 2; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; UNINDEXED DRUG;

BACTERIAL COLONIZATION; BACTERIAL TRANSLOCATION; BACTERIAL TRANSMISSION; BORRELIA; BORRELIA INFECTION; CELL CONTACT; EXTRACELLULAR MATRIX; HUMAN; HUMORAL IMMUNITY; IMMUNE EVASION; LYME DISEASE; NONHUMAN; PATHOGENESIS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION; SURVIVAL RATE; UPREGULATION; VASCULAR ENDOTHELIUM;

ANIMALS; BACTERIAL PROTEINS; BORRELIA BURGDORFERI; GENE EXPRESSION REGULATION, BACTERIAL; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNE EVASION; LYME DISEASE; MEMBRANE PROTEINS; PROTEIN BINDING; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; TICKS;

EID: 84897477890     PISSN: 13892037     EISSN: 18755550     Source Type: Journal    
DOI: 10.2174/1389203715666140221124213     Document Type: Review

References (159)

1. Huppertz, H.I.; Bohme, M.; Standaert, S.M.; Karch, H.; Plotkin, S.A. Incidence of Lyme borreliosis in the Wurzburg region of Germany. Eur. J. Clin. Microbiol. Infect. Dis., 1999, 18, 697-703.
2. Herman-Giddens, M.E. RE: Endemic tickborne infectious diseases in Louisiana and the Gulf south. J. La. State Med. Soc., 2009; 161(6): 325-339. J. La. State Med. Soc., 2010, 162, 64; author reply 64-65.
3. Fell, E. An update on Lyme disease and other tick-borne illnesses. Nurse Pract., 2000, 25, 38-40, 43-34, 47-38 passim; quiz 56-37.
4. Wilske, B.; Fingerle, V.; Schulte-Spechtel, U. Microbiological and serological diagnosis of Lyme borreliosis. FEMS Immunol. Med. Microbiol., 2007, 49, 13-21.
5. Margos, G.; Gatewood, A.G.; Aanensen, D.M.; Hanincova, K.; Terekhova, D.; Vollmer, S.A.; Cornet, M.; Piesman, J.; Donaghy, M.; Bormane, A.; Hurn, M.A.; Feil, E.J.; Fish, D.; Casjens, S.; Wormser, G.P.; Schwartz, I.; Kurtenbach, K. MLST of housekeeping genes captures geographic population structure and suggests a European origin of Borrelia burgdorferi. Proc. Natl. Acad. Sci. USA, 2008, 105, 8730-8735.
6. Takayama, K.; Rothenberg, R.J.; Barbour, A.G. Absence of lipopolysaccharide in the Lyme disease spirochete, Borrelia burgdorferi. Infect. Immun., 1987, 55, 2311-2313.
7. Benhnia, M.R.; Wroblewski, D.; Akhtar, M.N.; Patel, R.A.; Lavezzi, W.; Gangloff, S.C.; Goyert, S.M.; Caimano, M.J.; Radolf, J.D.; Sellati, T.J. Signaling through CD14 attenuates the inflammatory response to Borrelia burgdorferi, the agent of Lyme disease. J. Immunol., 2005, 174, 1539-1548.
8. Mehra, R.; Londono, D.; Sondey, M.; Lawson, C.; Cadavid, D. Structure-function investigation of vsp serotypes of the spirochete Borrelia hermsii. PLoS One, 2009, 4, e7597.
9. Liang, F.T.; Yan, J.; Mbow, M.L.; Sviat, S.L.; Gilmore, R.D.; Mamula, M.; Fikrig, E. Borrelia burgdorferi changes its surface antigenic expression in response to host immune responses. Infect. Immun., 2004, 72, 5759-5767.
10. Stevenson, B.; Miller, J.C. Intra-and interbacterial genetic exchange of Lyme disease spirochete erp genes generates sequence identity amidst diversity. J. Mol. Evol., 2003, 57, 309-324.
11. Barbour, A.G.; Travinsky, B. Evolution and distribution of the ospC Gene, a transferable serotype determinant of Borrelia burgdorferi. MBio., 2010, 1(4), pii: e00153-10.
12. Qiu, W.G.; Schutzer, S.E.; Bruno, J.F.; Attie, O.; Xu, Y.; Dunn, J.J.; Fraser, C.M.; Casjens, S.R.; Luft, B.J. Genetic exchange and plasmid transfers in Borrelia burgdorferi sensu stricto revealed by three-way genome comparisons and multilocus sequence typing. Proc. Natl. Acad. Sci. USA, 2004, 101, 14150-14155.
13. 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.; Fraser, C.M. 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., 2000, 35, 490-516.
14. Schwan, T.G.; Piesman, J. Temporal changes in outer surface proteins A and C of the lyme disease-associated spirochete, Borrelia burgdorferi, during the chain of infection in ticks and mice. J. Clin. Microbiol., 2000, 38, 382-388.
15. Dunham-Ems, S.M.; Caimano, M.J.; Pal, U.; Wolgemuth, C.W.; Eggers, C.H.; Balic, A.; Radolf, J.D. Live imaging reveals a biphasic mode of dissemination of Borrelia burgdorferi within ticks. J. Clin. Invest., 2009, 119, 3652-3665.
16. Xu, H.; He, M.; He, J.J.; Yang, X.F. Role of the surface lipoprotein BBA07 in the enzootic cycle of Borrelia burgdorferi. Infect. Immun., 2010, 78, 2910-2918.
17. Cugini, C.; Medrano, M.; Schwan, T.G.; Coburn, J. Regulation of expression of the Borrelia burgdorferi beta(3)-chain integrin ligand, P66, in ticks and in culture. Infect. Immun., 2003, 71, 1001-1007.
18. Liang, F.T.; Xu, Q.; Sikdar, R.; Xiao, Y.; Cox, J.S.; Doerrler, W.T. BB0250 of Borrelia burgdorferi is a conserved and essential inner membrane protein required for cell division. J. Bacteriol., 2010, 192, 6105-6115.
19. Pal, U.; de Silva, A.M.; Montgomery, R.R.; Fish, D.; Anguita, J.; Anderson, J.F.; Lobet, Y.; Fikrig, E. Attachment of Borrelia burgdorferi within Ixodes scapularis mediated by outer surface protein A. J. Clin. Invest., 2000, 106, 561-569.
20. Revel, A.T.; Blevins, J.S.; Almazan, C.; Neil, L.; Kocan, K.M.; de la Fuente, J.; Hagman, K.E. Norgard, M.V. bptA (bbe16) is essential for the persistence of the Lyme disease spirochete, Borrelia burgdorferi, in its natural tick vector. Proc. Natl. Acad. Sci., USA, 2005, 102, 6972-6977.
21. Li, X.; Pal, U.; Ramamoorthi, N.; Liu, X.; Desrosiers, D.C.; Eggers, C.H.; Anderson, J.F.; Radolf, J.D.; Fikrig, E. The Lyme disease agent Borrelia burgdorferi requires BB0690, a Dps homologue, to persist within ticks. Mol. Microbiol., 2007, 63, 694-710.
22. Zhang, L.; Zhang, Y.; Adusumilli, S.; Liu, L.; Narasimhan, S.; Dai, J.; Zhao, Y.O.; Fikrig, E. Molecular interactions that enable movement of the Lyme disease agent from the tick gut into the hemolymph. PLoS Pathog., 2011, 7, e1002079.
23. Kumar, M.; Kaur, S.; Kariu, T.; Yang, X.; Bossis, I.; Anderson, J.F.; Pal, U. Borrelia burgdorferi BBA52 is a potential target for transmission blocking Lyme disease vaccine. Vaccine 2011, 29, 9012-9019.
24. Patton, T.G.; Dietrich, G.; Dolan, M.C.; Piesman, J.; Carroll, J.A.; Gilmore, R.D. Jr. Functional analysis of the Borrelia burgdorferi bba64 gene product in murine infection via tick infestation. PLoS One, 2011, 6, e19536.
25. Pal, U.; Yang, X.; Chen, M.; Bockenstedt, L.K.; Anderson, J.F.; Flavell, R.A.; Norgard, M.V.; Fikrig, E. OspC facilitates Borrelia burgdorferi invasion of Ixodes scapularis salivary glands. J. Clin. Invest.; 2004, 113, 220-230.
26. Ramamoorthi, N.; Narasimhan, S.; Pal, U.; Bao, F.; Yang, X.F.; Fish, D.; Anguita, J.; Norgard, M.V.; Kantor, F.S.; Anderson, J.F.; Koski, R.A.; Fikrig, E. The Lyme disease agent exploits a tick protein to infect the mammalian host. Nature, 2005, 436, 573-577.
27. Gilmore, R.D.; Jr.; Howison, R.R.; Schmit, V.L.; Carroll, J.A. Borrelia burgdorferi expression of the bba64, bba65, bba66, and bba73 genes in tissues during persistent infection in mice. Microb. Pathog., 2008, 45, 355-360.
28. Gilmore, R.D.; Jr.; Howison, R.R.; Schmit, V.L.; Nowalk, A.J.; Clifton, D.R.; Nolder, C.; Hughes, J.L.; Carroll, J.A. Temporal expression analysis of the Borrelia burgdorferi paralogous gene family 54 genes BBA64, BBA65, and BBA66 during persistent infection in mice. Infect. Immun., 2007, 75, 2753-2764.
29. Morrison, T.B.; Weis, J.H.; Weis, J.J. Borrelia burgdorferi outer surface protein A (OspA) activates and primes human neutrophils. J. Immunol., 1997, 158, 4838-4845.
30. Hsieh, Y.F.; Liu, H.W.; Hsu, T.C.; Wei, J.C.; Shih, C.M.; Krause, P.J.; Tsay, G.J. Serum reactivity against Borrelia burgdorferi OspA in patients with rheumatoid arthritis. Clin. Vaccine Immunol., 2007, 14, 1437-1441.
31. Guo, X.; Booth, C.J.; Paley, M.A.; Wang, X.; DePonte, K.; Fikrig, E.; Narasimhan, S.; Montgomery, R.R. Inhibition of neutrophil function by two tick salivary proteins. Infect. Immun., 2009, 77, 2320-2329.
32. Tyson, K.; Elkins, C.; Patterson, H.; Fikrig, E.; de Silva, A. Biochemical and functional characterization of Salp20, an Ixodes scapularis tick salivary protein that inhibits the complement pathway. Insect. Mol. Biol., 2007, 16, 469-479.
33. Marchal, C.M.; Luft, B.J.; Yang, X.; Sibilia, J.; Jaulhac, B.; Boulanger, N.M. Defensin is suppressed by tick salivary gland extract during the in vitro interaction of resident skin cells with Borrelia burgdorferi. J. Invest. Dermatol., 2009, 129, 2515-2517.
34. Horka, H.; Cerna-Kyckova, K.; Skallova, A.; Kopecky, J. Tick saliva affects both proliferation and distribution of Borrelia burgdorferi spirochetes in mouse organs and increases transmission of spirochetes to ticks. Int. J. Med. Microbiol., 2009, 299, 373-380.
35. Hirschfeld, M.; Kirschning, C.J.; Schwandner, R.; Wesche, H.; Weis, J.H.; Wooten, R.M.; Weis, J.J. Cutting edge: inflammatory signaling by Borrelia burgdorferi lipoproteins is mediated by tolllike receptor 2. J. Immunol., 1999, 163, 2382-2386.
36. Ebnet, K.; Brown, K.D.; Siebenlist, U.K.; Simon, M.M.; Shaw, S. Borrelia burgdorferi activates nuclear factor-kappa B and is a potent inducer of chemokine and adhesion molecule gene expression in endothelial cells and fibroblasts. J. Immunol., 1997, 158, 3285-3292.
37. Singh, S.K.; Girschick, H.J., Toll-like receptors in Borrelia burgdorferi-induced inflammation. Clin. Microbiol. Infect.,2006, 12, 705-717.
38. Suhonen, J.; Komi, J.; Soukka, J.; Lassila, O.; Viljanen, M.K. Interaction between Borrelia burgdorferi and immature human dendritic cells. Scand. J. Immunol., 2003, 58, 67-75.
39. Szczepanski, A.; Benach, J.L. Lyme borreliosis: host responses to Borrelia burgdorferi. Microbiol. Rev., 1991, 55, 21-34.
40. Salazar, J.C.; Pope, C.D.; Sellati, T.J.; Feder, H.M.; Jr.; Kiely, T.G.; Dardick, K.R.; Buckman, R.L.; Moore, M.W.; Caimano, M.J.; Pope, J.G.; Krause, P.J.; Radolf, J.D. Coevolution of markers of innate and adaptive immunity in skin and peripheral blood of patients with erythema migrans. J. Immunol., 2003, 171, 2660-2670.
41. Sellati, T.J.; Waldrop, S.L.; Salazar, J.C.; Bergstresser, P.R.; Picker, L.J.; Radolf, J. D. The cutaneous response in humans to Treponema pallidum lipoprotein analogues involves cellular elements of both innate and adaptive immunity. J. Immunol., 2001, 166, 4131-4140.
42. Sellati, T.J.; Wilkinson, D.A.; Sheffield, J.S.; Koup, R.A.; Radolf, J.D.; Norgard, M.V. Virulent Treponema pallidum, lipoprotein, and synthetic lipopeptides induce CCR5 on human monocytes and enhance their susceptibility to infection by human immunodeficiency virus type 1. J. Infect. Dis., 2000, 181, 283-293.
43. Mullegger, R.R.; Means, T.K.; Shin, J.J.; Lee, M.; Jones, K.L.; Glickstein, L.J.; Luster, A.D.; Steere, A.C. Chemokine signatures in the skin disorders of Lyme borreliosis in Europe: predominance of CXCL9 and CXCL10 in erythema migrans and acrodermatitis and CXCL13 in lymphocytoma. Infect. Immun., 2007, 75, 4621-4628.
44. Sjowall, J.; Carlsson, A.; Vaarala, O.; Bergstrom, S.; Ernerudh, J.; Forsberg, P.; Ekerfelt, C. Innate immune responses in Lyme borreliosis: enhanced tumour necrosis factor-alpha and interleukin-12 in asymptomatic individuals in response to live spirochetes. Clin. Exp. Immunol., 2005, 141, 89-98.
45. Dennis, V.A.; Jefferson, A.; Singh, S.R.; Ganapamo, F.; Philipp, M.T. Interleukin-10 anti-inflammatory response to Borrelia burgdorferi, the agent of Lyme disease: a possible role for suppressors of cytokine signaling 1 and 3. Infect. Immun., 2006, 74, 5780-5789.
46. Scheckelhoff, M.R.; Telford, S.R.; Wesley, M.; Hu, L.T. Borrelia burgdorferi intercepts host hormonal signals to regulate expression of outer surface protein A. Proc. Natl. Acad. Sci. USA, 2007, 104, 7247-7252.
47. Steere, A.C.; Glickstein, L. Elucidation of Lyme arthritis. Nat. Rev. Immunol., 2004, 4, 143-152.
48. rd.; Spielman, A. Delayed dissemination of Lyme disease spirochetes from the site of deposition in the skin of mice. J. Infect. Dis., 1992, 166, 827-831.
49. Hyde, J.A.; Weening, E.H.; Chang, M.; Trzeciakowski, J.P.; Hook, M.; Cirillo, J.D.; Skare, J.T. Bioluminescent imaging of Borrelia burgdorferi in vivo demonstrates that the fibronectin-binding protein BBK32 is required for optimal infectivity. Mol. Microbiol., 2011, 82, 99-113.
50. Parveen, N.; Cornell, K.A.; Bono, J.L.; Chamberland, C.; Rosa, P.; Leong, J.M. Bgp, a secreted glycosaminoglycan-binding protein of Borrelia burgdorferi strain N40, displays nucleosidase activity and is not essential for infection of immunodeficient mice. Infect. Immun., 2006, 74, 3016-3020.
51. Salo, J.; Loimaranta, V.; Lahdenne, P.; Viljanen, M.K.; Hytonen, J. Decorin binding by DbpA and B of Borrelia garinii, Borrelia afzelii, and Borrelia burgdorferi sensu Stricto. J. Infect. Dis., 2011, 204, 65-73.
52. Fischer, J.R.; Parveen, N.; Magoun, L.; Leong, J.M., Decorinbinding proteins A and B confer distinct mammalian cell typespecific attachment by Borrelia burgdorferi, the Lyme disease spirochete. Proc. Natl. Acad. Sci. USA, 2003, 100, 7307-7312.
53. Guo, B.P.; Norris, S.J.; Rosenberg, L.C.; Hook, M. Adherence of Borrelia burgdorferi to the proteoglycan decorin. Infect. Immun., 1995, 63, 3467-3472.
54. Zambrano, M.C.; Beklemisheva, A.A.; Bryksin, A.V.; Newman, S.A.; Cabello, F.C. Borrelia burgdorferi binds to, invades, and colonizes native type I collagen lattices. Infect. Immun., 2004, 72, 3138-3146.
55. Skare, J.T.; Mirzabekov, T.A.; Shang, E.S.; Blanco, D.R.; Erdjument-Bromage, H.; Bunikis, J.; Bergstrom, S.; Tempst, P.; Kagan, B.L.; Miller, J.N.; Lovett, M.A. The Oms66 (p66) protein is a Borrelia burgdorferi porin. Infect. Immun., 1997, 65, 3654-3661.
56. LaFrance, M.E.; Pierce, J.V.; Antonara, S.; Coburn, J. The Borrelia burgdorferi integrin ligand P66 affects gene expression by human cells in culture. Infect. Immun., 2011, 79, 3249-3261.
57. Dressler, F.; Whalen, J.A.; Reinhardt, B.N.; Steere, A.C. Western blotting in the serodiagnosis of Lyme disease. J. Infect. Dis., 1993, 167, 392-400.
58. Fikrig, E.; Feng, W.; Barthold, S.W.; Telford, S.R.; 3rd; Flavell, R.A. Arthropod-and host-specific Borrelia burgdorferi bbk32 expression and the inhibition of spirochete transmission. J. Immunol., 2000, 164, 5344-5351.
59. Brissette, C.A.; Bykowski, T.; Cooley, A.E.; Bowman, A.; Stevenson, B. Borrelia burgdorferi RevA antigen binds host fibronectin. Infect. Immun., 2009, 77, 2802-2812.
60. Brissette, C.A.; Rossmann, E.; Bowman, A.; Cooley, A.E.; Riley, S.P.; Hunfeld, K.P.; Bechtel, M.; Kraiczy, P.; Stevenson, B. The borrelial fibronectin-binding protein RevA is an early antigen of human Lyme disease. Clin. Vaccine Immunol., 2010, 17, 274-280.
61. Verma, A.; Brissette, C.A.; Bowman, A.; Stevenson, B. Borrelia burgdorferi BmpA is a laminin-binding protein. Infect. Immun., 2009, 77, 4940-4946.
62. Brissette, C.A.; Verma, A.; Bowman, A.; Cooley, A.E.; Stevenson, B. The Borrelia burgdorferi outer-surface protein ErpX binds mammalian laminin. Microbiology, 2009, 155, 863-872.
63. Pal, U.; Wang, P.; Bao, F.; Yang, X.; Samanta, S.; Schoen, R.; Wormser, G.P.; Schwartz, I.; Fikrig, E. Borrelia burgdorferi basic membrane proteins A and B participate in the genesis of Lyme arthritis. J. Exp. Med., 2008, 205, 133-141.
64. Pulzova, L.; Kovac, A.; Mucha, R.; Mlynarcik, P.; Bencurova, E.; Madar, M.; Novak, M.; Bhide, M. OspA-CD40 dyad: ligandreceptor interaction in the translocation of neuroinvasive Borrelia across the blood-brain barrier. Sci. Rep., 2011, 1, 86.
65. Trollmo, C.; Meyer, A.L.; Steere, A.C.; Hafler, D.A.; Huber, B.T. Molecular mimicry in Lyme arthritis demonstrated at the single cell level: LFA-1 alpha L is a partial agonist for outer surface protein A-reactive T cells. J. Immunol., 2001, 166, 5286-5291.
66. Floden, A.M.; Watt, J.A.; Brissette, C.A. Borrelia burgdorferi enolase is a surface-exposed plasminogen binding protein. PLoS One, 2011, 6, e27502.
67. Moriarty, T.J.; Norman, M.U.; Colarusso, P.; Bankhead, T.; Kubes, P.; Chaconas, G. Real-time high resolution 3D imaging of the lyme disease spirochete adhering to and escaping from the vasculature of a living host. PLoS Pathog., 2008, 4, e1000090.
68. Coleman, J.L.; Benach, J.L. The urokinase receptor can be induced by Borrelia burgdorferi through receptors of the innate immune system. Infect. Immun., 2003, 71, 5556-5564.
69. Hu, L.T.; Perides, G.; Noring, R.; Klempner, M.S. Binding of human plasminogen to Borrelia burgdorferi. Infect. Immun., 1995, 63, 3491-3496.
70. Zhao, Z.; Fleming, R.; McCloud, B.; Klempner, M.S. CD14 mediates cross talk between mononuclear cells and fibroblasts for upregulation of matrix metalloproteinase 9 by Borrelia burgdorferi. Infect. Immun., 2007, 75, 3062-3069.
71. Norgard, M.V.; Arndt, L.L.; Akins, D.R.; Curetty, L.L.; Harrich, D.A.; Radolf, J.D. Activation of human monocytic cells by Treponema pallidum and Borrelia burgdorferi lipoproteins and synthetic lipopeptides proceeds via a pathway distinct from that of lipopolysaccharide but involves the transcriptional activator NFkappa B. Infect. Immun., 1996, 64, 3845-3852.
72. Klempner, M.S.; Noring, R.; Epstein, M.P.; McCloud, B.; Hu, R.; Limentani, S.A.; Rogers, R.A. Binding of human plasminogen and urokinase-type plasminogen activator to the Lyme disease spirochete, Borrelia burgdorferi. J. Infect. Dis.; 1995, 171, 1258-1265.
73. Fuchs, H.; Wallich, R.; Simon, M.M.; Kramer, M.D. The outer surface protein A of the spirochete Borrelia burgdorferi is a plasmin(ogen) receptor. Proc. Natl. Acad. Sci. USA, 1994, 91, 12594-12598.
74. Lagal, V.; Portnoi, D.; Faure, G.; Postic, D.; Baranton, G. Borrelia burgdorferi sensu stricto invasiveness is correlated with OspCplasminogen affinity. Microbes Infect., 2006, 8, 645-652.
75. Brissette, C.A.; Haupt, K.; Barthel, D.; Cooley, A.E.; Bowman, A.; Skerka, C.; Wallich, R.; Zipfel, P.F.; Kraiczy, P.; Stevenson, B. Borrelia burgdorferi infection-associated surface proteins ErpP, ErpA, and ErpC bind human plasminogen. Infect. Immun., 2009, 77, 300-306.
76. Hu, L.T.; Pratt, S.D.; Perides, G.; Katz, L.; Rogers, R.A.; Klempner, M.S. Isolation, cloning, and expression of a 70-kilodalton plasminogen binding protein of Borrelia burgdorferi. Infect. Immun., 1997, 65, 4989-4995.
77. Hallstrom, T.; Haupt, K.; Kraiczy, P.; Hortschansky, P.; Wallich, R.; Skerka, C.; Zipfel, P.F. Complement regulator-acquiring surface protein 1 of Borrelia burgdorferi binds to human bone morphogenic protein 2, several extracellular matrix proteins, and plasminogen. J. Infect. Dis., 2010, 202, 490-498.
78. Schwan, T.G.; Piesman, J.; Golde, W.T.; Dolan, M.C.; Rosa, P.A. Induction of an outer surface protein on Borrelia burgdorferi during tick feeding. Proc. Natl. Acad. Sci. USA, 1995, 92, 2909-2913.
79. Crowley, H.; Huber, B.T., Host-adapted Borrelia burgdorferi in mice expresses OspA during inflammation. Infect. Immun., 2003, 71, 4003-4010.
80. Perides, G.; Noring, R.; Klempner, M.S. Inhibition of Borrelia burgdorferi-bound fibrinolytic enzymes by alpha2-antiplasmin, PAI-1 and PAI-2. Biochem. Biophys. Res. Commun., 1996, 219, 690-695.
81. Coleman, J.L.; Sellati, T.J.; Testa, J.E.; Kew, R.R.; Furie, M.B.; Benach, J.L. Borrelia burgdorferi binds plasminogen, resulting in enhanced penetration of endothelial monolayers. Infect. Immun., 1995, 63, 2478-2484.
82. Gebbia, J.A.; Coleman, J.L.; Benach, J.L. Borrelia spirochetes upregulate release and activation of matrix metalloproteinase gelatinase B (MMP-9) and collagenase 1 (MMP-1) in human cells. Infect. Immun., 2001, 69, 456-462.
83. Coleman, J.L.; Gebbia, J.A.; Benach, J.L., Borrelia burgdorferi and other bacterial products induce expression and release of the urokinase receptor (CD87). J. Immunol., 2001, 166, 473-480.
84. Coleman, J.L.; Roemer, E.J.; Benach, J.L. Plasmin-coated borrelia Burgdorferi degrades soluble and insoluble components of the mammalian extracellular matrix. Infect. Immun., 1999, 67, 3929-3936.
85. Gebbia, J.A.; Coleman, J.L.; Benach, J.L. Selective induction of matrix metalloproteinases by Borrelia burgdorferi via toll-like receptor 2 in monocytes. J. Infect. Dis., 2004, 189, 113-119.
86. Nowalk, A.J.; Nolder, C.; Clifton, D.R.; Carroll, J.A. Comparative proteome analysis of subcellular fractions from Borrelia burgdorferi by NEPHGE and IPG. Proteomics 2006, 6, 2121-2134.
87. Barbour, A.G.; Jasinskas, A.; Kayala, M.A.; Davies, D.H.; Steere, A.C.; Baldi, P.; Felgner, P.L. A genome-wide proteome array reveals a limited set of immunogens in natural infections of humans and white-footed mice with Borrelia burgdorferi. Infect. Immun., 2008, 76, 3374-3389.
88. Liang, F.T.; Brown, E.L.; Wang, T.; Iozzo, R.V.; Fikrig, E. Protective niche for Borrelia burgdorferi to evade humoral immunity. Am. J. Pathol., 2004, 165, 977-985.
89. Behera, A.K.; Durand, E.; Cugini, C.; Antonara, S.; Bourassa, L.; Hildebrand, E.; Hu, L.T.; Coburn, J. Borrelia burgdorferi BBB07 interaction with integrin alpha3beta1 stimulates production of proinflammatory mediators in primary human chondrocytes. Cell Microbiol., 2008, 10, 320-331.
90. Dechanet, J.; Grosset, C.; Taupin, J.L.; Merville, P.; Banchereau, J.; Ripoche, J.; Moreau, J.F. CD40 ligand stimulates proinflammatory cytokine production by human endothelial cells. J. Immunol., 1997, 159, 5640-5647.
91. Hollenbaugh, D.; Mischel-Petty, N.; Edwards, C.P.; Simon, J.C.; Denfeld, R.W.; Kiener, P.A.; Aruffo, A. Expression of functional CD40 by vascular endothelial cells. J. Exp. Med., 1995, 182, 33-40.
92. Karmann, K.; Hughes, C.C.; Schechner, J.; Fanslow, W.C.; Pober, J.S. CD40 on human endothelial cells: inducibility by cytokines and functional regulation of adhesion molecule expression. Proc. Natl. Acad. Sci., USA, 1995, 92, 4342-4346.
93. Kurtenbach, K.; De Michelis, S.; Etti, S.; Schafer, S.M.; Sewell, H.S.; Brade, V.; Kraiczy, P. Host association of Borrelia burgdorferi sensu lato--the key role of host complement. Trends Microbiol., 2002, 10, 74-79.
94. Alitalo, A.; Meri, T.; Lankinen, H.; Seppala, I.; Lahdenne, P.; Hefty, P.S.; Akins, D.; 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., 2002, 169, 3847-3853.
95. Kraiczy, P.; Skerka, C.; Kirschfink, M.; Zipfel, P.F.; Brade, V. Mechanism of complement resistance of pathogenic Borrelia burgdorferi isolates. Int. Immunopharmacol., 2001, 1, 393-401.
96. Kraiczy, P.; Skerka, C.; Kirschfink, M.; Brade, V.; Zipfel, P.F. Immune evasion of Borrelia burgdorferi by acquisition of human complement regulators FHL-1/reconectin and Factor H. Eur. J. Immunol., 2001, 31, 1674-1684.
97. Bhide, M.R.; Escudero, R.; Camafeita, E.; Gil, H.; Jado, I.; Anda, P. Complement factor H binding by different Lyme disease and relapsing fever Borrelia in animals and human. BMC Res. Notes, 2009, 2, 134.
98. Kraiczy, P.; Hellwage, J.; Skerka, C.; Becker, H.; Kirschfink, M.; Simon, M.M.; Brade, V.; Zipfel, P.F.; 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., 2004, 279, 2421-2429.
99. Kraiczy, P.; Seling, A.; Brissette, C.A.; Rossmann, E.; Hunfeld, K.P.; Bykowski, T.; Burns, L.H.; Troese, M.J.; Cooley, A.E.; Miller, J.C.; Brade, V.; Wallich, R.; Casjens, S.; Stevenson, B. Borrelia burgdorferi complement regulator-acquiring surface protein 2 (CspZ) as a serological marker of human Lyme disease. Clin. Vaccine Immunol., 2008, 15, 484-491.
100. Kraiczy, P.; Skerka, C.; Brade, V.; Zipfel, P.F. Further characterization of complement regulator-acquiring surface proteins of Borrelia burgdorferi. Infect. Immun., 2001, 69, 7800-7809.
101. McDowell, J.V.; Wolfgang, J.; Tran, E.; Metts, M.S.; Hamilton, D.; 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., 2003, 71, 3597-3602.
102. Rossmann, E.; Kitiratschky, V.; Hofmann, H.; Kraiczy, P.; Simon, M.M.; Wallich, R. Borrelia burgdorferi complement regulatoracquiring surface protein 1 of the Lyme disease spirochetes is expressed in humans and induces antibody responses restricted to nondenatured structural determinants. Infect. Immun., 2006, 74, 7024-7028.
103. Rossmann, E.; Kraiczy, P.; Herzberger, P.; Skerka, C.; Kirschfink, M.; Simon, M.M.; Zipfel, P.F.; Wallich, R. Dual binding specificity of a Borrelia hermsii-associated complement regulator-acquiring surface protein for factor H and plasminogen discloses a putative virulence factor of relapsing fever spirochetes. J. Immunol., 2007, 178, 7292-7301.
104. Hartmann, K.; Corvey, C.; Skerka, C.; Kirschfink, M.; Karas, M.; Brade, V.; Miller, J.C.; Stevenson, B.; Wallich, R.; Zipfel, P.F.; 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., 2006, 61, 1220-1236.
105. Kraiczy, P.; Hanssen-Hubner, C.; Kitiratschky, V.; Brenner, C.; Besier, S.; Brade, V.; Simon, M.M.; Skerka, C.; Roversi, P.; Lea, S.M.; Stevenson, B.; Wallich, R.; Zipfel, P.F., Mutational analyses of the BbCRASP-1 protein of Borrelia burgdorferi identify residues relevant for the architecture and binding of host complement regulators FHL-1 and factor H. Int. J. Med. Microbiol., 2009, 299, 255-268.
106. Kraiczy, P.; Hellwage, J.; Skerka, C.; Kirschfink, M.; Brade, V.; Zipfel, P.F.; 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., 2003, 33, 697-707.
107. Wallich, R.; Pattathu, J.; Kitiratschky, V.; Brenner, C.; Zipfel, P.F.; Brade, V.; Simon, M.M.; 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., 2005, 73, 2351-2359.
108. Miller, J.C.; von Lackum, K.; Babb, K.; McAlister, J.D.; Stevenson, B. Temporal analysis of Borrelia burgdorferi Erp protein expression throughout the mammal-tick infectious cycle. Infect. Immun., 2003, 71, 6943-6952.
109. Miller, J.C.; von Lackum, K.; Woodman, M.E.; Stevenson, B. Detection of Borrelia burgdorferi gene expression during mammalian infection using transcriptional fusions that produce green fluorescent protein. Microb. Pathog., 2006, 41, 43-47.
110. Miller, J.C.; Stevenson, B. Borrelia burgdorferi erp genes are expressed at different levels within tissues of chronically infected mammalian hosts. Int. J. Med. Microbiol., 2006, 296 Suppl 40, 185-194.
111. Bhide, M.R.; Travnicek, M.; Levkutova, M.; Curlik, J.; Revajova, V.; Levkut, M. Sensitivity of Borrelia genospecies to serum complement from different animals and human: a host-pathogen relationship. FEMS Immunol. Med. Microbiol., 2005, 43, 165-172.
112. Ishii, N.; Isogai, E.; Isogai, H.; Kimura, K.; Nishikawa, T.; Fujii, N.; Nakajima, H. T cell response to Borrelia garinii, Borrelia afzelii, and Borrelia japonica in various congenic mouse strains. Microbiol. Immunol., 1995, 39, 929-935.
113. Ishiguro, F.; Takada, N.; Yano, Y.; Harada, M.; Masuzawa, T.; Iida, H. Prevalence of antibodies to Borrelia spirochetes among wild small rodents in central and western Japan. Microbiol. Immunol., 1995, 39, 419-424.
114. Bhide, M.; Bhide, K.; Pulzova, L.; Madar, M.; Mlynarcik, P.; Bencurova, E.; Hresko, S.; Mucha, R. Variable regions in the sushi domains 6-7 and 19-20 of factor H in animals and human lead to change in the affinity to factor H binding protein of Borrelia. J. Proteomics, 2012, 75, 4520-4528.
115. Kisova-Vargova, L.; Cernanska, D.; Bhide, M. Comparative study of binding of ovine complement factor H with different Borrelia genospecies. Folia Microbiol. (Praha), 2012, 57, 123-128.
116. Hovis, K.M.; McDowell, J.V.; Griffin, L.; Marconi, R.T. Identification and characterization of a linear-plasmid-encoded factor Hbinding protein (FhbA) of the relapsing fever spirochete Borrelia hermsii. J. Bacteriol., 2004, 186, 2612-2618.
117. McDowell, J.V.; Wolfgang, J.; Senty, L.; Sundy, C.M.; Noto, M.J.; 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., 2004, 173, 7471-7480.
118. Ripoche, J.; Day, A.J.; Harris, T.J.; Sim, R.B. The complete amino acid sequence of human complement factor H. Biochem. J., 1988, 249, 593-602.
119. Zipfel, P.F.; Skerka, C.; Hellwage, J.; Jokiranta, S.T.; Meri, S.; Brade, V.; Kraiczy, P.; Noris, M.; Remuzzi, G. Factor H family proteins: on complement, microbes and human diseases. Biochem. Soc. Trans., 2002, 30, 971-978.
120. Rodriguez de Cordoba, S.; Esparza-Gordillo, J.; Goicoechea de Jorge, E.; Lopez-Trascasa, M.; Sanchez-Corral, P. The human complement factor H: functional roles, genetic variations and disease associations. Mol. Immunol., 2004, 41, 355-367.
121. Hellwage, J.; Meri, T.; Heikkila, T.; Alitalo, A.; Panelius, J.; Lahdenne, P.; Seppala, I. J.; Meri, S. The complement regulator factor H binds to the surface protein OspE of Borrelia burgdorferi. J. Biol. Chem., 2001, 276, 8427-8435.
122. Hammerschmidt, C.; Hallstrom, T.; Skerka, C.; Wallich, R.; Stevenson, B.; Zipfel, P.F.; Kraiczy, P. Contribution of the infectionassociated complement regulator-acquiring surface protein 4 (ErpC) to complement resistance of Borrelia burgdorferi. Clin. Dev. Immunol., 2012, 2012, 349657.
123. Pietikainen, J.; Meri, T.; Blom, A.M.; Meri, S. Binding of the complement inhibitor C4b-binding protein to Lyme disease Borreliae. Mol. Immunol., 2010, 47, 1299-1305.
124. Carlsson, F.; Berggard, K.; Stalhammar-Carlemalm, M.; Lindahl, G. Evasion of phagocytosis through cooperation between two ligand-binding regions in Streptococcus pyogenes M protein. J. Exp. Med., 2003, 198, 1057-1068.
125. Grosskinsky, S.; Schott, M.; Brenner, C.; Cutler, S.J.; Simon, M.M.; Wallich, R. Human complement regulators C4b-binding protein and C1 esterase inhibitor interact with a novel outer surface protein of Borrelia recurrentis. PLoS Negl. Trop. Dis., 2010, 4, e698.
126. Pausa, M.; Pellis, V.; Cinco, M.; Giulianini, P.G.; Presani, G.; Perticarari, S.; Murgia, R.; Tedesco, F. Serum-resistant strains of Borrelia burgdorferi evade complement-mediated killing by expressing a CD59-like complement inhibitory molecule. J. Immunol., 2003, 170, 3214-3222.
127. Comstock, L.E.; Fikrig, E.; Shoberg, R.J.; Flavell, R.A.; Thomas, D.D. A monoclonal antibody to OspA inhibits association of Borrelia burgdorferi with human endothelial cells. Infect. Immun., 1993, 61, 423-431.
128. Szczepanski, A.; Furie, M.B.; Benach, J.L.; Lane, B.P.; Fleit, H.B., Interaction between Borrelia burgdorferi and endothelium in vitro. J. Clin. Invest., 1990, 85, 1637-1647.
129. Norman, M.U.; Moriarty, T.J.; Dresser, A.R.; Millen, B.; Kubes, P.; Chaconas, G. Molecular mechanisms involved in vascular interactions of the Lyme disease pathogen in a living host. PLoS Pathog., 2008, 4, e1000169.
130. Pulzova, L.; Bhide, M.R.; Andrej, K. Pathogen translocation across the bloodâ€"brain barrier. FEMS Immunol. Med. Mic., 2009, 57, 203-213.
131. Moriarty, T.J.; Shi, M.; Lin, Y.P.; Ebady, R.; Zhou, H.; Odisho, T.; Hardy, P.O.; Salman-Dilgimen, A.; Wu, J.; Weening, E.H.; Skare, J.T.; Kubes, P.; Leong, J.; Chaconas, G. Vascular binding of a pathogen under shear force through mechanistically distinct sequential interactions with host macromolecules. Mol. Microbiol., 2012, 86, 1116-1131.
132. Livengood, J.A.; Gilmore, R.D.; Jr., Invasion of human neuronal and glial cells by an infectious strain of Borrelia burgdorferi. Microbes Infect., 2006, 8, 2832-2840.
133. Dotevall, L.; Rosengren, L. E.; Hagberg, L. Increased cerebrospinal fluid levels of glial fibrillary acidic protein (GFAp) in Lyme neuroborreliosis. Infection, 1996, 24, 125-129.
134. Widhe, M.; Grusell, M.; Ekerfelt, C.; Vrethem, M.; Forsberg, P.; Ernerudh, J. Cytokines in Lyme borreliosis: lack of early tumour necrosis factor-alpha and transforming growth factor-beta1 responses are associated with chronic neuroborreliosis. Immunology, 2002, 107, 46-55.
135. Ramesh, G.; Alvarez, A.L.; Roberts, E.D.; Dennis, V.A.; Lasater, B.L.; Alvarez, X.; Philipp, M.T. Pathogenesis of Lyme neuroborreliosis: Borrelia burgdorferi lipoproteins induce both proliferation and apoptosis in rhesus monkey astrocytes. Eur. J. Immunol., 2003, 33, 2539-2550.
136. Thomas, W.; Forero, M.; Yakovenko, O.; Nilsson, L.; Vicini, P.; Sokurenko, E.; Vogel, V. Catch-bond model derived from allostery explains force-activated bacterial adhesion. Biophys. J., 2006, 90, 753-764.
137. Schutzer, S.E.; Coyle, P.K.; Krupp, L.B.; Deng, Z.; Belman, A.L.; Dattwyler, R.; Luft, B.J. Simultaneous expression of Borrelia OspA and OspC and IgM response in cerebrospinal fluid in early neurologic Lyme disease. J. Clin. Invest., 1997, 100, 763-767.
138. Rupprecht, T.A.; Koedel, U.; Heimerl, C.; Fingerle, V.; Paul, R.; Wilske, B.; Pfister, H.W. Adhesion of Borrelia garinii to neuronal cells is mediated by the interaction of OspA with proteoglycans. J. Neuroimmunol., 2006, 175, 5-11.
139. Londono, D.; Cadavid, D. Bacterial lipoproteins can disseminate from the periphery to inflame the brain. Am. J. Pathol., 2010, 176, 2848-2857.
140. Zabriskie, J.B. Rheumatic fever: a model for the pathological consequences of microbial-host mimicry. Clin. Exp. Rheumatol., 1986, 4, 65-73.
141. Raveche, E.S.; Schutzer, S.E.; Fernandes, H.; Bateman, H.; McCarthy, B.A.; Nickell, S.P.; Cunningham, M.W. Evidence of Borrelia autoimmunity-induced component of Lyme carditis and arthritis. J. Clin. Microbiol., 2005, 43, 850-856.
142. Weigelt, W.; Schneider, T.; Lange, R. Sequence homology between spirochaete flagellin and human myelin basic protein. Immunol. Today, 1992, 13, 279-280.
143. Fritzsche, M. Geographical and seasonal correlation of multiple sclerosis to sporadic schizophrenia. Int. J. Health Geogr., 2002, 1, 5.
144. Fritzsche, M. Seasonal correlation of sporadic schizophrenia to Ixodes ticks and Lyme borreliosis. Int. J. Health Geogr., 2002, 1, 2.
145. Miller, L.C.; Lynch, E.A.; Isa, S.; Logan, J.W.; Dinarello, C.A.; Steere, A.C. Balance of synovial fluid IL-1 beta and IL-1 receptor antagonist and recovery from Lyme arthritis. Lancet, 1993, 341, 146-148.
146. Porat, R.; Poutsiaka, D.D.; Miller, L.C.; Granowitz, E.V.; Dinarello, C.A. Interleukin-1 (IL-1) receptor blockade reduces endotoxin and Borrelia burgdorferi-stimulated IL-8 synthesis in human mononuclear cells. FASEB J., 1992, 6, 2482-2486.
147. Pal, U.; Li, X.; Wang, T.; Montgomery, R.R.; Ramamoorthi, N.; Desilva, A.M.; Bao, F.; Yang, X.; Pypaert, M.; Pradhan, D.; Kantor, F.S.; Telford, S.; Anderson, J.F.; Fikrig, E. TROSPA, an Ixodes scapularis receptor for Borrelia burgdorferi. Cell, 2004, 119, 457-468.
148. Fikrig, E.; Pal, U.; Chen, M.; Anderson, J.F.; Flavell, R.A. OspB antibody prevents Borrelia burgdorferi colonization of Ixodes scapularis. Infect. Immun., 2004, 72, 1755-1759.
149. Purser, J.E.; Lawrenz, M.B.; Caimano, M.J.; Howell, J.K.; Radolf, J.D.; Norris, S.J. A plasmid-encoded nicotinamidase (PncA) is essential for infectivity of Borrelia burgdorferi in a mammalian host. Mol. Microbiol., 2003, 48, 753-764.
150. Hughes, J.L.; Nolder, C.L.; Nowalk, A.J.; Clifton, D.R.; Howison, R.R.; Schmit, V.L.; Gilmore, R.D.; Jr.; Carroll, J.A. Borrelia burgdorferi surface-localized proteins expressed during persistent murine infection are conserved among diverse Borrelia spp. Infect. Immun., 2008, 76, 2498-2511.
151. Bestor, A.; Rego, R.O.; Tilly, K.; Rosa, P.A. Competitive advantage of Borrelia burgdorferi with outer surface protein BBA03 during tick-mediated infection of the mammalian host. Infect. Immun., 2012, 80, 3501-3511.
152. Li, C.; Xu, H.; Zhang, K.; Liang, F.T. Inactivation of a putative flagellar motor switch protein FliG1 prevents Borrelia burgdorferi from swimming in highly viscous media and blocks its infectivity. Mol. Microbiol., 2010, 75, 1563-1576.
153. Mulay, V.B.; Caimano, M.J.; Iyer, R.; Dunham-Ems, S.; Liveris, D.; Petzke, M.M.; Schwartz, I.; Radolf, J.D. Borrelia burgdorferi bba74 is expressed exclusively during tick feeding and is regulated by both arthropod-and mammalian host-specific signals. J. Bacteriol., 2009, 191, 2783-2794.
154. Mulay, V.; Caimano, M.J.; Liveris, D.; Desrosiers, D.C.; Radolf, J.D.; Schwartz, I. Borrelia burgdorferi BBA74, a periplasmic protein associated with the outer membrane, lacks porin-like properties. J. Bacteriol., 2007, 189, 2063-2068.
155. Bykowski, T.; Woodman, M.E.; Cooley, A.E.; Brissette, C. A.; Wallich, R.; Brade, V.; Kraiczy, P.; Stevenson, B. Borrelia burgdorferi complement regulator-acquiring surface proteins (BbCRASPs): Expression patterns during the mammal-tick infection cycle. Int. J. Med. Microbiol., 2008, 298 Suppl 1, 249-256.
156. Haupt, K.; Kraiczy, P.; Wallich, R.; Brade, V.; Skerka, C.; Zipfel, P.F. 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., 2007, 196, 124-133.
157. Schwab, J.; Hammerschmidt, C.; Richter, D.; Skerka, C.; Matuschka, F.R.; Wallich, R.; Zipfel, P. F.; Kraiczy, P., Borrelia valaisiana resist complement-mediated killing independently of the recruitment of immune regulators and inactivation of complement components. PLoS One, 2013, 8, e53659.
158. Siegel, C.; Hallstrom, T.; Skerka, C.; Eberhardt, H.; Uzonyi, B.; Beckhaus, T.; Karas, M.; Wallich, R.; Stevenson, B.; Zipfel, P. F.; Kraiczy, P. Complement factor H-related proteins CFHR2 and CFHR5 represent novel ligands for the infection-associated CRASP proteins of Borrelia burgdorferi. PLoS One, 2010, 5, e13519.
159. Cluss, R.G.; Silverman, D.A.; Stafford, T.R., Extracellular secretion of the Borrelia burgdorferi Oms28 porin and Bgp, a glycosaminoglycan binding protein. Infect Immun., 2004, 72, 6279-6286.