OspC is potent plasminogen receptor on surface of borrelia burgdorferi

Journal of Biological Chemistry

Volumn 287, Issue 20, 2012, Pages 16860-16868

  Önder, Özlem ^a   Humphrey, Parris T ^a,b   McOmber, Brian ^a   Korobova, Farida ^a   Francella, Nicholas ^a   Greenbaum, Doron C ^a   Brisson, Dustin ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b The University of Arizona   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACKGROUND LEVEL; BORRELIA BURGDORFERI; COLOCALIZATION; LYME DISEASE; MOLECULAR MECHANISM; OUTER MEMBRANE; OUTER SURFACE; STAINING ASSAYS; SURFACE PROTEINS; WILD-TYPE BACTERIA;

TISSUE;

BACTERIA;

BACTERIAL PROTEIN; OUTER SURFACE PROTEIN C; PLASMIN; PLASMINOGEN; PLASMINOGEN RECEPTOR; PROTEIN ANTIBODY; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; BORRELIA BURGDORFERI; CONTROLLED STUDY; IMMUNOFLUORESCENCE; MASS SPECTROMETRY; MOLECULAR MECHANICS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN IMMOBILIZATION; PROTEIN LOCALIZATION; WILD TYPE;

ANTIGENS, BACTERIAL; BACTERIAL OUTER MEMBRANE PROTEINS; BORRELIA BURGDORFERI; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; LYME DISEASE; PLASMINOGEN;

BACTERIA (MICROORGANISMS); BORRELIA BURGDORFERI; IXODIDA; VERTEBRATA;

EID: 84860847495     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.290775     Document Type: Article

References (65)

1. Travis, J., Potempa, J., and Maeda, H. (1995) Are bacterial proteinases pathogenic factors? Trends Microbiol. 3, 405-407
2. Goguen, J. D., Hoe, N. P., and Subrahmanyam, Y. V. (1995) Proteases and bacterial virulence. A view from the trenches. Infect. Agents Dis. 4, 47-54
3. Lähteenmäki, K., Kuusela, P., and Korhonen, T. K. (2001) Bacterial plasminogen activators and receptors. FEMS Microbiol. Rev. 25, 531-552 (Pubitemid 34019193)
4. Lähteenmäki, K., Edelman, S., and Korhonen, T. K. (2005) Bacterial metastasis. The host plasminogen system in bacterial invasion. Trends Microbiol. 13, 79-85 (Pubitemid 40174867)
5. Coleman, J. L., and Benach, J. L. (1999) Use of the plasminogen activation system by microorganisms. J. Lab. Clin. Med. 134, 567-576
6. Grab, D. J., Perides, G., Dumler, J. S., Kim, K. J., Park, J., Kim, Y. V., Nikolskaia, O., Choi, K. S., Stins, M. F., and Kim, K. S. (2005) Borrelia burgdorferi, host-derived proteases, and the blood-brain barrier. Infect. Immun. 73, 1014-1022 (Pubitemid 40165762)
7. Coleman, J. L., Gebbia, J. A., Piesman, J., Degen, J. L., Bugge, T. H., and Benach, J. L. (1997) Plasminogen is required for efficient dissemination of B. burgdorferi in ticks and for enhancement of spirochetemia in mice. Cell 89, 1111-1119 (Pubitemid 127678744)
8. Coleman, J. L., Sellati, T. J., Testa, J. E., Kew, R. R., Furie, M. B., and Benach, J. L. (1995) Borrelia burgdorferi binds plasminogen, resulting in enhanced penetration of endothelial monolayers. Infect. Immun. 63, 2478-2484
9. Mignatti, P., and Rifkin, D. B. (1993) Biology and biochemistry of proteinases in tumor invasion. Physiol. Rev. 73, 161-195 (Pubitemid 23065437)
10. Plow, E. F., Herren, T., Redlitz, A., Miles, L. A., and Hoover-Plow, J. L. (1995) The cell biology of the plasminogen system. FASEB J. 9, 939-945
11. Plow, E. F., Ploplis, V. A., Carmeliet, P., and Collen, D. (1999) Plasminogen and cell migration in vivo. Fibrinolysis & Proteolysis 13, 49-53 (Pubitemid 29274403)
12. Sun, H., Ringdahl, U., Homeister, J. W., Fay, W. P., Engleberg, N. C., Yang, A. Y., Rozek, L. S., Wang, X., Sjöbring, U., and Ginsburg, D. (2004) Plasminogen is a critical host pathogenicity factor for group A streptococcal infection. Science 305, 1283-1286 (Pubitemid 39129231)
13. Klempner, M. S., Noring, R., Epstein, M. P., McCloud, B., Hu, R., Limentani, S. A., and Rogers, R. A. (1995) Binding of human plasminogen and urokinase-type plasminogen activator to the Lyme disease spirochete, Borrelia burgdorferi. J. Infect. Dis. 171, 1258-1265
14. Gebbia, J. A., Monco, J. C., Degen, J. L., Bugge, T. H., and Benach, J. L. (1999) The plasminogen activation system enhances brain and heart invasion in murine relapsing fever borreliosis. J. Clin. Invest. 103, 81-87 (Pubitemid 29031166)
15. Coleman, J. L., Roemer, E. J., and Benach, J. L. (1999) Plasmin-coated Borrelia burgdorferi degrades soluble and insoluble components of the mammalian extracellular matrix. Infect. Immun. 67, 3929-3936 (Pubitemid 29357012)
16. Hu, L. T., Perides, G., Noring, R., and Klempner, M. S. (1995) Binding of human plasminogen to Borrelia burgdorferi. Infect. Immun. 63, 3491-3496
17. Klempner, M. S., Noring, R., Epstein, M. P., McCloud, B., and Rogers, R. A. (1996) Binding of human urokinase type plasminogen activator and plasminogen to Borrelia species. J. Infect. Dis. 174, 97-104 (Pubitemid 26255560)
18. Nordstrand, A., Shamaei-Tousi, A., Ny, A., and Bergström, S. (2001) Delayed invasion of the kidney and brain by Borrelia crocidurae in plasminogen- deficient mice. Infect. Immun. 69, 5832-5839 (Pubitemid 32786523)
19. Blevins, J. S., Revel, A. T., Smith, A. H., Bachlani, G. N., and Norgard, M. V. (2007) Adaptation of a luciferase gene reporter and lac expression system to Borrelia burgdorferi. Appl. Environ. Microbiol. 73, 1501-1513 (Pubitemid 46417875)
20. Hallström, T., Haupt, K., Kraiczy, P., Hortschansky, P., Wallich, R., Skerka, C., and Zipfel, P. F. (2010) 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. 202, 490-498
21. Fuchs, H., Wallich, R., Simon, M. M., and Kramer, M. D. (1994) The outer surface protein A of the spirochete Borrelia burgdorferi is a plasmin(ogen) receptor. Proc. Natl. Acad. Sci. U.S.A. 91, 12594-12598
22. 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) Borrelia burgdorferi infection-associated proteins ErpP, ErpA, and ErpC bind human plasminogen. Infect. Immun. 77, 300-306
23. Lagal, V., Portnoï, D., Faure, G., Postic, D., and Baranton, G. (2006) Borrelia burgdorferi sensu stricto invasiveness is correlated with OspC-plasminogen affinity. Microbes Infect. 8, 645-652
24. Hu, L. T., Pratt, S. D., Perides, G., Katz, L., Rogers, R. A., and Klempner, M. S. (1997) Isolation, cloning, and expression of a 70-kilodalton plasminogen binding protein of Borrelia burgdorferi. Infect. Immun. 65, 4989-4995 (Pubitemid 27513541)
25. Inaba, K. (2009) Disulfide bond formation system in Escherichia coli. J. Biochem. 146, 591-597
26. Demain, A. L., and Vaishnav, P. (2009) Production of recombinant proteins by microbes and higher organisms. Biotechnol. Adv. 27, 297-306
27. Fuchs, R., Jauris, S., Lottspeich, F., Preac-Mursic, V., Wilske, B., and Soutschek, E. (1992) Molecular analysis and expression of a Borrelia burgdorferi gene encoding a 22-kDa protein (pC) in Escherichia coli. Mol. Microbiol. 6, 503-509
28. Schwan, T. G., Piesman, J., Golde, W. T., Dolan, M. C., and Rosa, P. A. (1995) Induction of an outer surface protein on Borrelia burgdorferi during tick feeding. Proc. Natl. Acad. Sci. U.S.A. 92, 2909-2913
29. Masuzawa, T., Kurita, T., Kawabata, H., and Yanagihara, Y. (1994) Relationship between infectivity and OspC expression in Lyme disease Borrelia. FEMS Microbiol. Lett. 123, 319-324 (Pubitemid 24323018)
30. Fingerle, V., Hauser, U., Liegl, G., Petko, B., Preac-Mursic, V., and Wilske, B. (1995) Expression of outer surface proteins A and C of Borrelia burgdorferi in Ixodes ricinus. J. Clin. Microbiol. 33, 1867-1869
31. Schwan, T. G., and Piesman, J. (2000) 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. 38, 382-388 (Pubitemid 30043321)
32. Gilmore, R. D., Jr., and Piesman, J. (2000) Inhibition of Borrelia burgdorferi migration from the midgut to the salivary glands following feeding by ticks on OspC-immunized mice. Infect. Immun. 68, 411-414
33. Grimm, D., Tilly, K., Byram, R., Stewart, P. E., Krum, J. G., Bueschel, D. M., Schwan, T. G., Policastro, P. F., Elias, A. F., and Rosa, P. A. (2004) Outer surface protein C of the Lyme disease spirochete. A protein induced in ticks for infection of mammals. Proc. Natl. Acad. Sci. U.S.A. 101, 3142-3147 (Pubitemid 38327748)
34. Pal, U., Yang, X., Chen, M., Bockenstedt, L. K., Anderson, J. F., Flavell, R. A., Norgard, M. V., and Fikrig, E. (2004) OspC facilitates Borrelia burgdorferi invasion of Ixodes scapularis salivary glands. J. Clin. Invest. 113, 220-230 (Pubitemid 38544207)
35. Tilly, K., Krum, J. G., Bestor, A., Jewett, M. W., Grimm, D., Bueschel, D., Byram, R., Dorward, D., Vanraden, M. J., Stewart, P., and Rosa, P. (2006) Borrelia burgdorferi OspC protein required exclusively in a crucial early stage of mammalian infection. Infect. Immun. 74, 3554-3564 (Pubitemid 43794547)
36. Fingerle, V., Goettner, G., Gern, L., Wilske, B., and Schulte-Spechtel, U. (2007) Complementation of a Borrelia afzelii OspC mutant highlights the crucial role of OspC for dissemination of Borrelia afzelii in Ixodes ricinus. Int. J. Med. Microbiol. 297, 97-107 (Pubitemid 46386489)
37. Radolf, J. D., and Caimano, M. J. (2008) The long strange trip of Borrelia burgdorferi outer-surface protein C. Mol. Microbiol. 69, 1-4 (Pubitemid 351832750)
38. Zuckert, W. R. (2007) Laboratory maintenance of Borrelia burgdorferi. Curr. Protoc. Microbiol. Chapter 12, Unit 12C.1
39. Alverson, J., Bundle, S. F., Sohaskey, C. D., Lybecker, M. C., and Samuels, D. S. (2003) Transcriptional regulation of the ospAB and ospC promoters from Borrelia burgdorferi. Mol. Microbiol. 48, 1665-1677 (Pubitemid 36751069)
40. Carroll, J. A., Garon, C. F., and Schwan, T. G. (1999) Effects of environmental pH on membrane proteins in Borrelia burgdorferi. Infect. Immun. 67, 3181-3187 (Pubitemid 29291478)
41. El-Hage, N., and Stevenson, B. (2002) Simultaneous coexpression of Borrelia burgdorferi Erp proteins occurs through a specific, erp locus-directed regulatory mechanism. J. Bacteriol. 184, 4536-4543 (Pubitemid 34832582)
42. Kumru, O. S., Bunikis, I., Sorokina, I., Bergström, S., and Zückert, W. R. (2011) Specificity and role of the Borrelia burgdorferi CtpA protease in outer membrane protein processing. J. Bacteriol. 193, 5759-5765
43. Sarkar, A., Hayes, B. M., Dulebohn, D. P., and Rosa, P. A. (2011) Regulation of the virulence determinant OspC by bbd18 on linear plasmid lp17 of Borrelia burgdorferi. J. Bacteriol. 193, 5365-5373
44. Elias, A. F., Stewart, P. E., Grimm, D., Caimano, M. J., Eggers, C. H., Tilly, K., Bono, J. L., Akins, D. R., Radolf, J. D., Schwan, T. G., and Rosa, P. (2002) Clonal polymorphism of Borrelia burgdorferi strain B31 MI. Implications for mutagenesis in an infectious strain background. Infect. Immun. 70, 2139-2150 (Pubitemid 34242216)
45. Onder, O., Turkarslan, S., Sun, D., and Daldal, F. (2008) Overproduction or absence of the periplasmic protease DegP severely compromises bacterial growth in the absence of the dithiol:disulfide oxidoreductase DsbA. Mol. Cell. Proteomics 7, 875-890 (Pubitemid 351737089)
46. Wiener, M. C., Sachs, J. R., Deyanova, E. G., and Yates, N. A. (2004) Differential mass spectrometry. A label-free LC-MS method for finding significant differences in complex peptide and protein mixtures. Anal. Chem. 76, 6085-6096 (Pubitemid 39382956)
47. Xie, F., Liu, T., Qian, W. J., Petyuk, V. A., and Smith, R. D. (2011) Liquid chromatography-mass spectrometry-based quantitative proteomics. J. Biol. Chem. 286, 25443-25449
48. Cederholm-Williams, S. A. (1981) Concentration of plasminogen and antiplasmin in plasma and serum. J. Clin. Pathol. 34, 979-981
49. Burgdorfer, W., Barbour, A. G., Hayes, S. F., Benach, J. L., Grunwaldt, E., and Davis, J. P. (1982) Lyme disease. A tick-borne spirochetosis? Science 216, 1317-1319
50. Rooijakkers, S. H., van Wamel, W. J., Ruyken, M., van Kessel, K. P., and van Strijp, J. A. (2005) Anti-opsonic properties of staphylokinase. Microbes Infect. 7, 476-484 (Pubitemid 40603446)
51. Xu, Q., McShan, K., and Liang, F. (2008) Essential protective role attributed to the surface lipoproteins of Borrelia burgdorferi against innate defences. Mol. Microbiol. 69, 15-29 (Pubitemid 351832757)
52. Earnhart, C. G., Leblanc, D. V., Alix, K. E., Desrosiers, D. C., Radolf, J. D., and Marconi, R. T. (2010) Identification of residues within ligand-binding domain 1 (LBD1) of the Borrelia burgdorferi OspC protein required for function in the mammalian environment. Mol. Microbiol. 76, 393- 408
53. Seemanapalli, S. V., Xu, Q., McShan, K., and Liang, F. T. (2010) Outer surface proteinC is a dissemination-facilitating factor of Borrelia burgdorferi during mammalian infection. PLoS ONE 5, e15830
54. 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 (Pubitemid 38525929)
55. Burns, L. H., Adams, C. A., Riley, S. P., Jutras, B. L., Bowman, A., Chenail, A. M., Cooley, A. E., Haselhorst, L. A., Moore, A. M., Babb, K., Fried, M. G., and Stevenson, B. (2010) BpaB, a novel protein encoded by the Lyme disease spirochete's cp32 prophages, binds to erp Operator 2 DNA. Nucleic Acids Res. 38, 5443-5455
56. Narasimhan, S., Santiago, F., Koski, R. A., Brei, B., Anderson, J. F., Fish, D., and Fikrig, E. (2002) Examination of the Borrelia burgdorferi transcriptome in Ixodes scapularis during feeding. J. Bacteriol. 184, 3122-3125 (Pubitemid 34517837)
57. Tokarz, R., Anderton, J. M., Katona, L. I., and Benach, J. L. (2004) Combined effects of blood and temperature shift on Borrelia burgdorferi gene expression as determined by whole genome DNA array. Infect. Immun. 72, 5419-5432 (Pubitemid 39223430)
58. Wormser, G. P., Brisson, D., Liveris, D., Hanincová, K., Sandigursky, S., Nowakowski, J., Nadelman, R. B., Ludin, S., and Schwartz, I. (2008) Borrelia burgdorferi genotype predicts the capacity for hematogenous dissemination during early Lyme disease. J. Infect. Dis. 198, 1358-1364
59. Dykhuizen, D. E., Brisson, D., Sandigursky, S., Wormser, G. P., Nowakowski, J., Nadelman, R. B., and Schwartz, I. (2008) The propensity of different Borrelia burgdorferi sensu stricto genotypes to cause disseminated infections in humans. Am. J. Trop. Med. Hyg. 78, 806-810 (Pubitemid 351845140)
60. Seinost, G., Dykhuizen, D. E., Dattwyler, R. J., Golde, W. T., Dunn, J. J., Wang, I. N., Wormser, G. P., Schriefer, M. E., and Luft, B. J. (1999) Four clones of Borrelia burgdorferi sensu stricto cause invasive infection in humans. Infect. Immun. 67, 3518-3524 (Pubitemid 29291524)
61. Eicken, C., Sharma, V., Klabunde, T., Owens, R. T., Pikas, D. S., Höök, M., and Sacchettini, J. C. (2001) Crystal structure of Lyme disease antigen outer surface protein C from Borrelia burgdorferi. J. Biol. Chem. 276, 10010-10015
62. Kumaran, D., Eswaramoorthy, S., Luft, B. J., Koide, S., Dunn, J. J., Lawson, C. L., and Swaminathan, S. (2001) Crystal structure of outer surface protein C (OspC) from the Lyme disease spirochete, Borrelia burgdorferi. EMBO J. 20, 971-978 (Pubitemid 32186788)
63. Barbour, A. G., Tessier, S. L., and Todd, W. J. (1983) Lyme disease spirochetes and ixodid tick spirochetes share a common surface antigenic determinant defined by a monoclonal antibody. Infect. Immun. 41, 795- 804
64. Moriarty, T. J., Norman, M. U., Colarusso, P., Bankhead, T., Kubes, P., and Chaconas, G. (2008) Real time high resolution three-dimensional imaging of the lyme disease spirochete adhering to and escaping from the vasculature of a living host. PLoS Pathog. 4, e1000090
65. Boyle, M. D., and Lottenberg, R. (1997) Plasminogen activation by invasive human pathogens. Thromb. Haemost. 77, 1-10 (Pubitemid 27064959)