Plasminogen acquisition and activation at the surface of Leptospira species lead to fibronectin degradation

Infection and Immunity

Volumn 77, Issue 9, 2009, Pages 4092-4101

  Vieira, Monica L ^a,b   Vasconcellos, Silvio A ^b   Gonçales, Amane P ^b   De Morais, Zenaide M ^b   Nascimento, Ana L T O ^a,b  

^a INSTITUTO BUTANTAN   (Brazil)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

3,4,5,6 TETRAHYDRO 1 MORPHOLINOMETHYL 2(1H) PYRIMIDINONE; 4 NITROANILIDE DIHYDROCHLORIDEIN; 6 AMINOCAPROIC CID; FIBRONECTIN; LYSINE; OUTER MEMBRANE PROTEIN; PLASMIN; PLASMINOGEN; UNCLASSIFIED DRUG; UROKINASE;

ARTICLE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CELL CULTURE; CELL GROWTH; CHEMICAL LABELING; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENVIRONMENTAL FACTOR; ENZYME ACTIVITY; EXTRACELLULAR MATRIX; IMMUNOFLUORESCENCE; LEPTOSPIRA INTERROGANS; NONHUMAN; OSMOLARITY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; SURFACE PROPERTY; TEMPERATURE SENSITIVITY;

6-AMINOCAPROIC ACID; ANIMALS; BACTERIAL OUTER MEMBRANE PROTEINS; CRICETINAE; FIBRONECTINS; HUMANS; LEPTOSPIRA INTERROGANS; PLASMIN; PLASMINOGEN; PROTEIN BINDING; VIRULENCE;

EID: 69049111014     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00353-09     Document Type: Article

References (79)

1. Anda, P., J. A. Gebbia, P. B. Backenson, J. L. Coleman, and J. L. Benach. 1996. A glyceraldehyde-3-phosphate dehydrogenase homolog in Borrelia burgdorferi and Borrelia hermsii. Infect. Immun. 64:262-268.
2. Attali, C., C. Durmort, T. Vernet, and A. M. Di Guilmi. 2008. The interaction of Streptococcus pneumoniae with plasmin mediates transmigration across endothelial and epithelial monolayers by intercellular junction cleavage. Infect. Immun. 76:5350-5356.
3. Atzingen, M. V., A. S. Barbosa, T. De Brito, S. A. Vasconcellos, Z. M. de Morais, D. M. Lima, P. A. Abreu, and A. L. Nascimento. 2008. Lsa21, a novel leptospiral protein binding adhesive matrix molecules and present during human infection. BMC Microbiol. 8:70.
4. Barbosa, A. S., P. A. E. Abreu, F. O. Neves, M. V. Atzingen, M. M. Watanabe, M. L. Vieira, Z. M. Morais, S. A. Vasconcellos, and A. L. T. O. Nascimento. 2006. A newly identified leptospiral adhesin mediates attachment to laminin. Infect. Immun. 74:6356-6364.
5. Barocchi, M. A., A. I. Ko, M. G. Reis, K. L. McDonald, and L. W. Riley. 2002. Rapid translocation of polarized MDCK cell monolayers by Leptospira interrogans, an invasive but nonintracellular pathogen. Infect. Immun. 70:6926-6932.
6. Bergmann, S., and S. Hammerschmidt. 2007. Fibrinolysis and host response in bacterial infections. Thromb. Haemos. 98:512-520.
7. Bharti, A. R., J. E. Nally, J. N. Ricaldi, M. A. Matthias, M. M. Diaz, M. A. Lovett, P. N. Levett, R. H. Gilman, M. R. Willig, E. Gotuzzo, and J. M. Vinetz. 2003. Leptospirosis: a zoonotic disease of global importance. Lancet Infect. Dis. 3:757-771.
8. Border, W. A., S. Okuda, T. Nakamura, L. R. Languino, and E. Ruoslahti. 1991. Role of TGF-beta 1 in experimental glomerulonephritis. Ciba Found. Symp. 157:178-193.
9. Bulach, D. M., R. L. Zuerner, P. Wilson, T. Seemann, A. McGrath, P. A. Cullen, J. Davis, M. Johnson, E. Kuczek, D. P. Alt, B. Peterson-Burch, R. L. Coppel, J. I. Rood, J. K. Davies, and B. Adler. 2006. Genome reduction in Leptospira borgpetersenii reflects limited transmission potential. Proc. Natl. Acad. Sci. USA 103:14560-14565.
10. Candela, M., G. Miccoli, S. Bergmann, S. Turroni, B. Vitali, S. Hammerschmidt, and P. Brigidi. 2008. Plasminogen-dependent proteolytic activity in Bifidobacterium lactis. Microbiology 154:2457-2462.
11. Choy, H. A., M. M. Kelley, T. L. Chen, A. K. Møller, J. Matsunaga, and D. A. Haake. 2007. Physiological osmotic induction of Leptospira interrogans adhesion: LigA and LigB bind extracellular matrix proteins and fibrinogen. Infect. Immun. 75:2441-2450.
12. Coleman, J. L., and J. L. Benach. 2000. The generation of enzymatically active plasmin on the surface of spirochetes. Methods 21:133-141.
13. Coleman, J. L., and J. L. Benach. 1999. Use of the plasminogen activation system by microorganisms. J. Lab. Clin. Med. 134:567-576.
14. Coleman, J. L., J. A. Gebbia, J. Piesman, J. L. Degen, T. H. Bugge, and J. L. Benach. 1997. Plasminogen is required for efficient dissemination of B. burgdorferi in ticks and for enhancement of spirochetemia in mice. Cell 89:1111-1119.
15. Coleman, J. L., E. J. Roemer, and J. L. Benach. 1999. Plasmin-coated Borrelia burgdorferi degrades soluble and insoluble components of the mammalian extracellular matrix. Infect. Immun. 67:3929-3936.
16. Coleman, J. L., T. J. Sellati, J. E. Testa, R. R. Kew, M. B. Furie, and J. L. Benach. 1995. Borrelia burgdorferi binds plasminogen, resulting in enhanced penetration of endothelial monolayers. Infect. Immun. 63:2478-2484.
17. Collen, D., G. Tytgat, H. Claeys, M. Verstraete, and P. Wallen. 1972. Metabolism of plasminogen in healthy subjects: effect of tranexamic acid. J. Clin. Investig. 51:1310-1318.
18. Cullen, P. A., D. A. Haake, and B. Adler. 2004. Outer membrane proteins of pathogenic spirochetes. FEMS Microbiol. Rev. 28:291-318.
19. Degen, J. L., T. H. Bugge, and J. D. Goguen. 2007. Fibrin and fibrinolysis in infection and host defense. J. Thromb. Haemost. 5(Suppl 1):24-31.
20. Faine, S., B. Adler, C. Bolin, and P. Perolat. 1999. Leptospira and leptospirosis, 2nd ed, p. 259. MediSci, Melbourne, Australia.
21. Fenno, J. C., M. Tamura, P. M. Hannam, G. W. K. Wong, R. A. Chan, and B. C. McBride. 2000. Identification of a Treponema denticola OppA homologue that binds host proteins present in the subgingival environment. Infect. Immun. 68:1884-1892.
22. Goto, H., and Y. Kawaoka. 1998. A novel mechanism for the acquisition of virulence by a human influenza A virus. Proc. Natl. Acad. Sci. USA 95:10224-10228.
23. Guo, Y., J. Li, E. Hagstrom, and T. Ny. 2008. Protective effects of plasmin-(ogen) in a mouse model of Staphylococcus aureus-induced arthritis. Arthritis Rheum. 58:764-772.
24. Haake, D. A., G. Chao, R. L. Zuerner, J. K. Barnett, D. Barnett, M. Mazel, J. Matsunaga, P. N. Levett, and C. A. Bolin. 2000. The leptospiral major outer membrane protein LipL32 is a lipoprotein expressed during mammalian infection. Infect. Immun. 68:2276-2285.
25. Haake, D. A., M. Dundoo, R. Cader, B. M. Kubak, R. A. Hartskeerl, J. J. Sejvar, and D. A. Ashford. 2002. Leptospirosis, water sports, and chemoprophylaxis. Clin. Infect. Dis. 34:e40-e43.
26. Haake, D. A., and J. Matsunaga. 2002. Characterization of the leptospiral outer membrane and description of three novel leptospiral membrane proteins. Infect. Immun. 70:4936-4945.
27. Haake, D. A., E. M. Walker, D. R. Blanco, C. A. Bolin, M. N. Miller, and M. A. Lovett. 1991. Changes in the surface of Leptospira interrogans serovar grippotyphosa during in vitro cultivation. Infect. Immun. 59:1131-1140.
28. Haile, W. B., J. L. Coleman, and J. L. Benach. 2006. Reciprocal upregulation of urokinase plasminogen activator and its inhibitor, PAI-2, by Borrelia burgdorferi affects bacterial penetration and host-inflammatory response. Cell. Microbiol. 8:1349-1360.
29. Hauk, P., F. Macedo, E. C. Romero, S. A. Vasconcellos, Z. M. de Morais, A. S. Barbosa, and P. L. Ho. 2008. In LipL32, the major leptospiral lipoprotein, the C terminus is the primary immunogenic domain and mediates interaction with collagen IV and plasma fibronectin. Infect. Immun. 76:2642-2650.
30. Hoke, D. E., S. Egan, P. A. Cullen, and B. Adler. 2008. LipL32 is an extracellular matrix-interacting protein of Leptospira spp. and Pseudoalteromonas tunicata. Infect. Immun. 76:2063-2069.
31. Hu, L. T., G. Perides, R. Noring, and M. S. Klempner. 1995. Binding of human plasminogen to Borrelia burgdorferi. Infect. Immun. 63:3491-3496.
32. Jobin, M. C., J. Brassard, S. Quessy, M. Gottschalk, and D. Grenier. 2004. Acquisition of host plasmin activity by the swine pathogen Streptococcus suis serotype 2. Infect. Immun. 72:606-610.
33. Kinnby, B., N. A. Booth, and G. Svensater. 2008. Plasminogen binding by oral streptococci from dental plaque and inflammatory lesions. Microbiology 154:924-931.
34. Klempner, M. S., R. Noring, M. P. Epstein, B. McCloud, R. Hu, S. A. Limentani, and R. A. Rogers. 1995. Binding of human plasminogen and urokinase-type plasminogen activator to the Lyme disease spirochete, Borrelia burgdorferi. J. Infect. Dis. 171:1258-1265.
35. Klempner, M. S., R. Noring, M. P. Epstein, B. McCloud, and R. A. Rogers. 1996. Binding of human urokinase type plasminogen activator and plasminogen to Borrelia species. J. Infect. Dis. 174:97-104.
36. Ko, A. I., M. Galvao Reis, C. M. Ribeiro Dourado, W. D. Johnson, Jr., L. W. Riley, et al. 1999. Urban epidemic of severe leptospirosis in Brazil. Lancet 354:820-825.
37. Lahteenmaki, K., P. Kuusela, and T. K. Korhonen. 2001. Bacterial plasminogen activators and receptors. FEMS Microbiol. Rev. 25:531-552.
38. LeBouder, F., E. Morello, G. F. Rimmelzwaan, F. Bosse, C. Péchoux, B. Delmas, and B. Riteau. 2008. Annexin II incorporated into influenza virus particles supports virus replication by converting plasminogen into plasmin. J. Virol. 82:6820-6828.
39. Levett, P. N. 2001. Leptospirosis. Clin. Microbiol. Rev. 14:296-326.
40. Leytus, S. P., L. K. Bowles, J. Konisky, and W. F. Mangel. 1981. Activation of plasminogen to plasmin by a protease associated with the outer membrane of Escherichia coli. Proc. Natl. Acad. Sci. USA 78:1485-1489.
41. Li, Z., V. A. Ploplis, E. L. French, and M. D. Boyle. 1999. Interaction between group A streptococci and the plasmin(ogen) system promotes virulence in a mouse skin infection model. J. Infect. Dis. 179:907-914.
42. Lijnen, H. R., F. De Cock, B. Van Hoef, B. Schlott, and D. Collen. 1994. Characterization of the interaction between plasminogen and staphylokinase. Eur. J. Biochem. 224:143-149.
43. Lo, M., D. M. Bulach, D. R. Powell, D. A. Haake, J. Matsunaga, M. L. Paustian, R. L. Zuerner, and B. Adler. 2006. Effects of temperature on gene expression patterns in Leptospira interrogans serovar Lai as assessed by whole-genome microarrays. Infect. Immun. 74:5848-5859.
44. Lottenberg, R., C. C. Broder, and M. D. P. Boyle. 1987. Identification of a specific receptor for plasmin on a group A streptococcus. Infect. Immun. 55:1914-1918.
45. Lottenberg, R., C. C. Broder, M. D. P. Boyle, S. J. Kain, B. L. Schroeder, and R. Curtiss III. 1992. Cloning, sequence analysis, and expression in Escherichia coli of a streptococcal plasmin receptor. J. Bacteriol. 174:5204-5210.
46. Magalhaes, V., I. Veiga-Malta, M. R. Almeida, M. Baptista, A. Ribeiro, P. Trieu-Cuot, and P. Ferreira. 2007. Interaction with human plasminogen system turns on proteolytic activity in Streptococcus agalactiae and enhances its virulence in a mouse model. Microbes Infect. 9:1276-1284.
47. Maldonado, J., C. Marina, J. Puig, Z. Maizo, and L. Avilan. 2006. A study of cutaneous lesions caused by Leishmania mexicana in plasminogen-deficient mice. Exp. Mol. Pathol. 80:289-294.
48. Matsunaga, J., M. A. Barocchi, J. Croda, T. A. Young, Y. Sanchez, I. Siqueira, C. A. Bolin, M. G. Reis, L. W. Riley, D. A. Haake, and A. I. Ko. 2003. Pathogenic Leptospira species express surface-exposed proteins belonging to the bacterial immunoglobulin superfamily. Mol. Microbiol. 49:929-945.
49. Matsunaga, J., M. Lo, D. M. Bulach, R. L. Zuerner, B. Adler, and D. A. Haake. 2007. Response of Leptospira interrogans to physiologic osmolarity: relevance in signaling the environment-to-host transition. Infect. Immun. 75:2864-2874.
50. Matsunaga, J., M. A. Medeiros, Y. Sanchez, K. F. Werneid, and A. I. Ko. 2007. Osmotic regulation of expression of two extracellular matrix-binding proteins and a haemolysin of Leptospira interrogans: differential effects on LigA and Sph2 extracellular release. Microbiology 153:3390-3398.
51. Matsunaga, J., Y. Sanchez, X. Xu, and D. A. Haake. 2005. Osmolarity, a key environmental signal controlling expression of leptospiral proteins LigA and LigB and the extracellular release of LigA. Infect. Immun. 73:70-78.
52. McCoy, H. E., C. C. Broder, and R. Lottenberg. 1991. Streptokinases produced by pathogenic group C streptococci demonstrate species-specific plasminogen activation. J. Infect. Dis. 164:515-521.
53. Mekalanos, J. J. 1992. Environmental signals controlling expression of virulence determinants in bacteria. J. Bacteriol. 174:1-7.
54. Nakai, K., and M. Kanehisa. 1991. Expert system for predicting protein localization sites in gram-negative bacteria. Proteins 11:95-110.
55. Nally, J. E., J. F. Timoney, and B. Stevenson. 2001. Temperature-regulated protein synthesis by Leptospira interrogans. Infect. Immun. 69:400-404.
56. Nally, J. E., J. P. Whitelegge, S. Bassilian, D. R. Blanco, and M. A. Lovett. 2007. Characterization of the outer membrane proteome of Leptospira interrogans expressed during acute lethal infection. Infect. Immun. 75:766-773.
57. Nascimento, A. L., S. Verjovski-Almeida, M. A. Van Sluys, C. B. Monteiro-Vitorello, L. E. Camargo, L. A. Digiampietri, R. A. Harstkeerl, P. L. Ho, M. V. Marques, M. C. Oliveira, J. C. Setubal, D. A. Haake, and E. A. Martins. 2004. Genome features of Leptospira interrogans serovar Copenhageni. Braz. J. Med. Biol. Res. 37:459-477.
58. Nordstrand, A., A. Shamaei-Tousi, A. Ny, and S. Bergstrom. 2001. Delayed invasion of the kidney and brain by Borrelia crocidurae in plasminogen-deficient mice. Infect. Immun. 69:5832-5839.
59. Okada, K., S. Ueshima, T. Takaishi, H. Yuasa, H. Fukao, and O. Matsuo. 1996. Effects of fibrin and alpha2-antiplasmin on plasminogen activation by staphylokinase. Am. J. Hematol. 53:151-157.
60. Okumura, Y., M. Yano, M. Murakami, S. Mori, T. Towatari, and H. Kido. 1999. The extracellular processing of HIV-1 envelope glycoprotein gp160 by human plasmin. FEBS Lett. 442:39-42.
61. Oliveira, T. R., M. T. Longhi, Z. M. de Morais, E. C. Romero, R. M. Blanco, K. Kirchgatter, S. A. Vasconcellos, and A. L. Nascimento. 2008. Evaluation of leptospiral recombinant antigens MPL17 and MPL21 for serological diagnosis of leptospirosis by enzyme-linked immunosorbent assays. Clin. Vaccine Immunol. 15:1715-1722.
62. Pancholi, V., and V. A. Fischetti. 1992. A major surface protein on group A streptococci is a glyceraldehyde-3-phosphate-dehydrogenase with multiple binding activity. J. Exp. Med. 176:415-426.
63. Pantzar, M., A° . Ljungh, and T. Wadström. 1998. Plasminogen binding and activation at the surface of Helicobacter pylori CCUG 17874. Infect. Immun. 66:4976-4980.
64. Picardeau, M., D. M. Bulach, C. Bouchier, R. L. Zuerner, N. Zidane, P. J. Wilson, S. Creno, E. S. Kuczek, S. Bommezzadri, J. C. Davis, A. McGrath, M. J. Johnson, C. Boursaux-Eude, T. Seemann, Z. Rouy, R. L. Coppel, J. I. Rood, A. Lajus, J. K. Davies, C. Medigue, and B. Adler. 2008. Genome sequence of the saprophyte Leptospira biflexa provides insights into the evolution of Leptospira and the pathogenesis of leptospirosis. PLoS ONE 3:e1607.
65. Plank, R., and D. Dean. 2000. Overview of the epidemiology, microbiology, and pathogenesis of Leptospira spp. in humans. Microbes Infect. 2:1265-1276.
66. Ren, S. X., G. Fu, X. G. Jiang, R. Zeng, Y. G. Miao, H. Xu, Y. X. Zhang, H. Xiong, G. Lu, L. F. Lu, H. Q. Jiang, J. Jia, Y. F. Tu, J. X. Jiang, W. Y. Gu, Y. Q. Zhang, Z. Cai, H. H. Sheng, H. F. Yin, Y. Zhang, G. F. Zhu, M. Wan, H. L. Huang, Z. Qian, S. Y. Wang, W. Ma, Z. J. Yao, Y. Shen, B. Q. Qiang, Q. C. Xia, X. K. Guo, A. Danchin, I. Saint Girons, R. L. Somerville, Y. M. Wen, M. H. Shi, Z. Chen, J. G. Xu, and G. P. Zhao. 2003. Unique physiological and pathogenic features of Leptospira interrogans revealed by whole-genome sequencing. Nature 422:888-893.
67. Ristow, P., P. Bourhy, F. W. da Cruz McBride, C. P. Figueira, M. Huerre, P. Ave, I. S. Girons, A. I. Ko, and M. Picardeau. 2007. The OmpA-like protein Loa22 is essential for leptospiral virulence. PLoS Pathog. 3:e97.
68. Rojas, M., I. Labrador, J. L. Concepcion, E. Aldana, and L. Avilan. 2008. Characteristics of plasminogen binding to Trypanosoma cruzi epimastigotes. Acta Trop. 107:54-58.
69. Sanderson-Smith, M. L., K. Dinkla, J. N. Cole, A. J. Cork, P. G. Maamary, J. D. McArthur, G. S. Chhatwal, and M. J. Walker. 2008. M protein-mediated plasminogen binding is essential for the virulence of an invasive Streptococcus pyogenes isolate. FASEB J. 22:2715-2722.
70. Schlott, B., K. H. Guhrs, M. Hartmann, A. Rocker, and D. Collen. 1998. NH2-terminal structural motifs in staphylokinase required for plasminogen activation. J. Biol. Chem. 273:22346-22350.
71. Sodeinde, O. A., Y. V. Subrahmanyam, K. Stark, T. Quan, Y. Bao, and J. D. Goguen. 1992. A surface protease and the invasive character of plague. Science 258:1004-1007.
72. Stevenson, B., H. A. Choy, M. Pinne, M. L. Rotondi, M. C. Miller, E. Demoll, P. Kraiczy, A. E. Cooley, T. P. Creamer, M. A. Suchard, C. A. Brissette, A. Verma, and D. A. Haake. 2007. Leptospira interrogans endostatin-like outer membrane proteins bind host fibronectin, laminin and regulators of complement. PLoS ONE 2:e1188.
73. Sun, H. 2006. The interaction between pathogens and the host coagulation system. Physiology 21:281-288.
74. Svensson, M. D., U. Sjobring, F. Luo, and D. E. Bessen. 2002. Roles of the plasminogen activator streptokinase and the plasminogen-associated M protein in an experimental model for streptococcal impetigo. Microbiology 148:3933-3945.
75. Verma, A., J. Hellwage, S. Artiushin, P. F. Zipfel, P. Kraiczy, J. F. Timoney, and B. Stevenson. 2006. LfhA, a novel factor H-binding protein of Leptospira interrogans. Infect. Immun. 74:2659-2666.
76. Vinetz, J. M. 2001. Leptospirosis. Curr. Opin. Infect. Dis. 14:527-538.
77. Xolalpa, W., A. J. Vallecillo, M. Lara, G. Mendoza-Hernandez, M. Comini, R. Spallek, M. Singh, and C. Espitia. 2007. Identification of novel bacterial plasminogen-binding proteins in the human pathogen Mycobacterium tuberculosis. Proteomics 7:3332-3341.
78. Yavlovich, A., A. A.-R. Higazi, and S. Rottem. 2001. Plasminogen binding and activation by Mycoplasma fermentans. Infect. Immun. 69:1977-1982.
79. Young, K. C., G. Y. Shi, D. H. Wu, L. C. Chang, B. I. Chang, C. P. Ou, and H. L. Wu. 1998. Plasminogen activation by streptokinase via a unique mechanism. J. Biol. Chem. 273:3110-3116.