Adhesins of Leptospira interrogans Mediate the Interaction to Fibrinogen and Inhibit Fibrin Clot Formation In Vitro

PLoS Neglected Tropical Diseases

Volumn 7, Issue 8, 2013, Pages

  Oliveira, Rosane ^a,b   Domingos, Renan F ^a,b   Siqueira, Gabriela H ^a,b   Fernandes, Luis G ^a,b   Souza, Natalie M ^a,b   Vieira, Monica L ^a   de Morais, Zenaide M ^b   Vasconcellos, Silvio A ^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

ADHESIN; BACTERIAL PROTEIN; FIBRINOGEN; MEMBRANE PROTEIN; PLASMIN; RECOMBINANT PROTEIN;

ARTICLE; BINDING ASSAY; BIOINFORMATICS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FIBRIN CLOT; GENE SEQUENCE; HUMAN; IMMUNOFLUORESCENCE TEST; LEPTOSPIRA INTERROGANS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; WESTERN BLOTTING;

EID: 84883401353     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0002396     Document Type: Article

References (60)

1. Faine S, Adler B, Bolin C, Perolat P (1999) Leptospira and Leptospirosis. Melbourne, Australia: MediSci Press.
2. Bharti AR, Nally JE, Ricaldi JN, Matthias MA, Diaz MM, et al. (2003) Leptospirosis: a zoonotic disease of global importance. Lancet Infect Dis 3: 757-771.
3. Levett PN, (2001) Leptospirosis. Clin Microbiol Rev 14: 296-326.
4. Plank R, Dean D, (2000) Overview of the epidemiology, microbiology, and pathogenesis of Leptospira spp. in humans. Microbes Infect 2: 1265-1276.
5. McBride AJ, Athanazio DA, Reis MG, Ko AI, (2005) Leptospirosis. Curr Opin Infect Dis 18: 376-386.
6. Marotto PC, Ko AI, Murta-Nascimento C, Seguro AC, Prado RR, et al. (2010) Early identification of leptospirosis-associated pulmonary hemorrhage syndrome by use of a validated prediction model. J Infect 60: 218-223.
7. Zhang YX, Geng Y, Bi B, He JY, Wu CF, et al. (2005) Identification and classification of all potential hemolysin encoding genes and their products from Leptospira interrogans serogroup Icterohae-morrhagiae serovar Lai. Acta Pharmacol Sin 26: 453-461.
8. Hauk P, Negrotto S, Romero EC, Vasconcellos SA, Genovez ME, et al. (2005) Expression and characterization of HlyX hemolysin from Leptospira interrogans serovar Copenhageni: potentiation of hemolytic activity by LipL32. Biochem Biophys Res Commun 333: 1341-1347.
9. Carvalho E, Barbosa AS, Gomez RM, Cianciarullo AM, Hauk P, et al. (2009) Leptospiral TlyC is an extracellular matrix-binding protein and does not present hemolysin activity. FEBS Lett 17: 1381-5.
10. Degen JL, Bugge TH, Goguen JD, (2007) Fibrin and fibrinolysis in infection and host defense. J Thromb Haemost 5 Suppl 1: 24-31.
11. Lahteenmaki K, Kuusela P, Korhonen TK, (2001) Bacterial plasminogen activators and receptors. FEMS Microbiol Rev 25: 531-552.
12. Vieira ML, Vasconcellos SA, Goncales AP, de Morais ZM, Nascimento AL, (2009) Plasminogen acquisition and activation at the surface of leptospira species lead to fibronectin degradation. Infect Immun 77: 4092-4101.
13. Vieira ML, de Morais ZM, Vasconcellos SA, Romero EC, Nascimento AL, (2011) In vitro evidence for immune evasion activity by human plasmin associated to pathogenic Leptospira interrogans. Microb Pathog 51: 360-365.
14. Choy HA, Kelley MM, Chen TL, Moller AK, Matsunaga J, et al. (2007) Physiological osmotic induction of Leptospira interrogans adhesion: LigA and LigB bind extracellular matrix proteins and fibrinogen. Infect Immun 75: 2441-2450.
15. Pinne M, Choy HA, Haake DA, (2010) The OmpL37 surface-exposed protein is expressed by pathogenic Leptospira during infection and binds skin and vascular elastin. PLoS Negl Trop Dis 4: e815.
16. Choy HA, Kelley MM, Croda J, Matsunaga J, Babbitt JT, et al. (2011) The multifunctional LigB adhesin binds homeostatic proteins with potential roles in cutaneous infection by pathogenic Leptospira interrogans. PLoS One 6: e16879.
17. Lin YP, McDonough SP, Sharma Y, Chang YF, (2011) Leptospira immunoglobulin-like protein B (LigB) binding to the C-terminal fibrinogen alphaC domain inhibits fibrin clot formation, platelet adhesion and aggregation. Mol Microbiol 79: 1063-1076.
18. Vieira ML, Atzingen MV, Oliveira TR, Oliveira R, Andrade DM, et al. (2010) In vitro identification of novel plasminogen-binding receptors of the pathogen Leptospira interrogans. PLoS One 5: e11259.
19. Domingos RF, Vieira ML, Romero EC, Goncales AP, de Morais ZM, et al. (2012) Features of two proteins of Leptospira interrogans with potential role in host-pathogen interactions. BMC Microbiol 12: 50.
20. Souza NM, Vieira ML, Alves IJ, de Morais ZM, Vasconcellos SA, et al. (2012) Lsa30, a novel adhesin of Leptospira interrogans binds human plasminogen and the complement regulator C4bp. Microb Pathog 53: 125-134.
21. Fernandes LG, Vieira ML, Kirchgatter K, Alves IJ, de Morais ZM, et al. (2012) OmpL1 Is an Extracellular Matrix- and Plasminogen-Interacting Protein of Leptospira spp. Infect Immun 80: 3679-3692.
22. Siqueira GH, Atzingen MV, Alves IJ, Morais ZM, Vasconcellos SA, Nascimento ALTO, (2013) Characterization of three novel adhesins of Leptospira interrogans. Am J Trop Med Hyg [In press].
23. Turner LH, (1970) Leptospirosis. 3. Maintenance, isolation and demonstration of leptospires. Trans R Soc Trop Med Hyg 64: 623-646.
24. Nakai K, Kanehisa M, (1991) Expert system for predicting protein localization sites in gram-negative bacteria. Proteins 11: 95-110.
25. Nakai K, Horton P, (1999) PSORT: a program for detecting sorting signals in proteins and predicting their subcellular localization. Trends Biochem Sci 24: 34-36.
26. Schultz J, Milpetz F, Bork P, Ponting CP, (1998) SMART, a simple modular architecture research tool: identification of signaling domains. Proc Natl Acad Sci U S A 95: 5857-5864.
27. Letunic I, Copley RR, Pils B, Pinkert S, Schultz J, et al. (2006) SMART 5: domains in the context of genomes and networks. Nucleic Acids Res 34: D257-260.
28. Finn RD, Mistry J, Schuster-Bockler B, Griffiths-Jones S, Hollich V, et al. (2006) Pfam: clans, web tools and services. Nucleic Acids Res 34: D247-251.
29. Juncker AS, Willenbrock H, Von Heijne G, Brunak S, Nielsen H, et al. (2003) Prediction of lipoprotein signal peptides in Gram-negative bacteria. Protein Sci 12: 1652-1662.
30. Ramos CR, Abreu PA, Nascimento AL, Ho PL, (2004) A high-copy T7 Escherichia coli expression vector for the production of recombinant proteins with a minimal N-terminal His-tagged fusion peptide. Braz J Med Biol Res 37: 1103-1109.
31. Forster KM, Hartwig DD, Seixas FK, Bacelo KL, Amaral M, et al. (2013) A conserved region of leptospiral immunoglobulin-like A and B proteins as a DNA vaccine elicits a prophylactic immune response against leptospirosis. Clin Vaccine Immunol 20: 725-731.
32. Goulart C, Darrieux M, Rodriguez D, Pimenta FC, Brandileone MC, et al. (2011) Selection of family 1 PspA molecules capable of inducing broad-ranging cross-reactivity by complement deposition and opsonophagocytosis by murine peritoneal cells. Vaccine 29: 1634-1642.
33. Lin YP, Lee DW, McDonough SP, Nicholson LK, Sharma Y, et al. (2009) Repeated domains of leptospira immunoglobulin-like proteins interact with elastin and tropoelastin. J Biol Chem 284: 19380-19391.
34. Malmstrom J, Beck M, Schmidt A, Lange V, Deutsch EW, et al. (2009) Proteome-wide cellular protein concentrations of the human pathogen Leptospira interrogans. Nature 460: 762-765.
35. Atzingen MV, Barbosa AS, De Brito T, Vasconcellos SA, de Morais ZM, et al. (2008) Lsa21, a novel leptospiral protein binding adhesive matrix molecules and present during human infection. BMC Microbiol 8: 70.
36. Oliveira R, de Morais ZM, Goncales AP, Romero EC, Vasconcellos SA, et al. (2011) Characterization of novel OmpA-like protein of Leptospira interrogans that binds extracellular matrix molecules and plasminogen. PLoS One 6: e21962.
37. Weisel JW, (2005) Fibrinogen and fibrin. Adv Protein Chem 70: 247-299.
38. Sun H, (2006) The interaction between pathogens and the host coagulation system. Physiology (Bethesda) 21: 281-288.
39. Flick MJ, Du X, Prasad JM, Raghu H, Palumbo JS, et al. (2013) Genetic elimination of the binding motif on fibrinogen for the S. aureus virulence factor ClfA improves host survival in septicemia. Blood 121: 1783-1794.
40. Dramsi S, Morello E, Poyart C, Trieu-Cuot P, (2012) Epidemiologically and clinically relevant Group B Streptococcus isolates do not bind collagen but display enhanced binding to human fibrinogen. Microbes Infect 14: 1044-1048.
41. Collins J, van Pijkeren JP, Svensson L, Claesson MJ, Sturme M, et al. (2012) Fibrinogen-binding and platelet-aggregation activities of a Lactobacillus salivarius septicaemia isolate are mediated by a novel fibrinogen-binding protein. Mol Microbiol 85: 862-877.
42. Houston S, Hof R, Francescutti T, Hawkes A, Boulanger MJ, et al. (2011) Bifunctional role of the Treponema pallidum extracellular matrix binding adhesin Tp0751. Infect Immun 79: 1386-1398.
43. Haapasalo M, Muller KH, Uitto VJ, Leung WK, McBride BC, (1992) Characterization, cloning, and binding properties of the major 53-kilodalton Treponema denticola surface antigen. Infect Immun 60: 2058-2065.
44. Edwards AM, Jenkinson HF, Woodward MJ, Dymock D, (2005) Binding properties and adhesion-mediating regions of the major sheath protein of Treponema denticola ATCC 35405. Infect Immun 73: 2891-2898.
45. Bamford CV, Fenno JC, Jenkinson HF, Dymock D, (2007) The chymotrypsin-like protease complex of Treponema denticola ATCC 35405 mediates fibrinogen adherence and degradation. Infect Immun 75: 4364-4372.
46. Rivera J, Vannakambadi G, Hook M, Speziale P, (2007) Fibrinogen-binding proteins of Gram-positive bacteria. Thromb Haemost 98: 503-511.
47. Davis SL, Gurusiddappa S, McCrea KW, Perkins S, Hook M, (2001) SdrG, a fibrinogen-binding bacterial adhesin of the microbial surface components recognizing adhesive matrix molecules subfamily from Staphylococcus epidermidis, targets the thrombin cleavage site in the Bbeta chain. J Biol Chem 276: 27799-27805.
48. Liu CZ, Shih MH, Tsai PJ, (2005) ClfA(221-550), a fibrinogen-binding segment of Staphylococcus aureus clumping factor A, disrupts fibrinogen function. Thromb Haemost 94: 286-294.
49. Verma A, Brissette CA, Bowman AA, Shah ST, Zipfel PF, et al. (2010) Leptospiral endostatin-like protein A is a bacterial cell surface receptor for human plasminogen. Infect Immun 78: 2053-2059.
50. Mendes RS, Von Atzingen M, de Morais ZM, Goncales AP, Serrano SM, et al. (2011) The novel leptospiral surface adhesin Lsa20 binds laminin and human plasminogen and is probably expressed during infection. Infect Immun 79: 4657-4667.
51. Wagenaar JF, Goris MG, Sakundarno MS, Gasem MH, Mairuhu AT, et al. (2007) What role do coagulation disorders play in the pathogenesis of leptospirosis? Trop Med Int Health 12: 111-122.
52. Wagenaar JF, Goris MG, Partiningrum DL, Isbandrio B, Hartskeerl RA, et al. (2010) Coagulation disorders in patients with severe leptospirosis are associated with severe bleeding and mortality. Trop Med Int Health 15: 152-159.
53. De Francesco Daher E, Oliveira Neto FH, Ramirez SM, (2002) Evaluation of hemostasis disorders and anticardiolipin antibody in patients with severe leptospirosis. Rev Inst Med Trop Sao Paulo 44: 85-90.
54. Chierakul W, Tientadakul P, Suputtamongkol Y, Wuthiekanun V, Phimda K, et al. (2008) Activation of the coagulation cascade in patients with leptospirosis. Clin Infect Dis 46: 254-260.
55. Higgins R, Cousineau G, (1977) The pathogenesis of leptospirosis I. Hemorrhages in experimental leptospirosis in guinea pigs. Can J Comp Med 41: 174-181.
56. Ren SX, Fu G, Jiang XG, Zeng R, Miao YG, et al. (2003) Unique physiological and pathogenic features of Leptospira interrogans revealed by whole-genome sequencing. Nature 422: 888-893.
57. Bulach DM, Zuerner RL, Wilson P, Seemann T, McGrath A, et al. (2006) Genome reduction in Leptospira borgpetersenii reflects limited transmission potential. Proc Natl Acad Sci U S A 103: 14560-14565.
58. Picardeau M, Bulach DM, Bouchier C, Zuerner RL, Zidane N, et al. (2008) Genome sequence of the saprophyte Leptospira biflexa provides insights into the evolution of Leptospira and the pathogenesis of leptospirosis. PLoS One 3: e1607.
59. Ricaldi JN, Fouts DE, Selengut JD, Harkins DM, Patra KP, et al. (2012) Whole genome analysis of Leptospira licerasiae provides insight into leptospiral evolution and pathogenicity. PLoS Negl Trop Dis 6: e1853.
60. Chou LF, Chen YT, Lu CW, Ko YC, Tang CY, et al. (2012) Sequence of Leptospira santarosai serovar Shermani genome and prediction of virulence-associated genes. Gene 511: 364-370.