Ompl1 is an extracellular matrix- and plasminogen-interacting protein of Leptospira spp

Infection and Immunity

Volumn 80, Issue 10, 2012, Pages 3679-3692

  Fernandes, Luis G V ^a,b   Vieira, Monica L ^a,b   Kirchgatter, Karin ^b   Alves, Ivy J ^a   de Morais, Zenaide M ^b   Vasconcellos, Silvio A ^b   Romero, Eliete C ^c   Nascimento, Ana L T O ^a,b  

^a INSTITUTO BUTANTAN   (Brazil)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

^c INSTITUTO ADOLFO LUTZ   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

FIBRONECTIN; LAMININ; OUTER MEMBRANE PROTEIN; OUTER MEMBRANE PROTEIN L1; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANTIBODY TITER; ARTICLE; CELLULAR IMMUNITY; CIRCULAR DICHROISM; CONTROLLED STUDY; ESCHERICHIA COLI; FEMALE; HUMAN; IMMUNOGENICITY; LEPTOSPIRA; LEPTOSPIROSIS; LYMPHOCYTE PROLIFERATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECONDARY STRUCTURE;

ANIMALS; BACTERIAL ADHESION; BACTERIAL OUTER MEMBRANE PROTEINS; BINDING SITES; CLONING, MOLECULAR; CRICETINAE; ESCHERICHIA COLI; FIBRINOLYSIN; FIBRONECTINS; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; LAMININ; LEPTOSPIRA; LEPTOSPIROSIS; MALE; MESOCRICETUS; MICE; MICE, INBRED BALB C; PHYLOGENY; PLASMINOGEN; PROTEIN BINDING; PROTEIN CONFORMATION; RECOMBINANT PROTEINS;

EID: 84867615409     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00474-12     Document Type: Article

References (81)

1. Adler B, de la Pena Moctezuma A. 2009. Leptospira and leptospirosis. Vet. Microbiol. 140:287-296.
2. Atzingen MV, et al. 2008. Lsa21, a novel leptospiral protein binding adhesive matrix molecules and present during human infection. BMC Microbiol. 8:70. doi:10.1186/1471-2180-8-70.
3. Atzingen MV, et al. 2009. Lp95, a novel leptospiral protein that binds extracellular matrix components and activates e-selectin on endothelial cells. J. Infect. 59:264-276.
4. Barbosa AS, et al. 2006. A newly identified leptospiral adhesin mediates attachment to laminin. Infect. Immun. 74:6356-6364.
5. Barbosa AS, et al. 2010. Functional characterization of LcpA, a surfaceexposed protein of Leptospira spp. that binds the human complement regulator C4BP. Infect. Immun. 78:3207-3216.
6. Barnett JK, et al. 1999. Expression and distribution of leptospiral outer membrane components during renal infection of hamsters. Infect. Immun. 67:853-861.
7. Barocchi MA, Ko AI, Reis MG, McDonald KL, Riley LW. 2002. Rapid translocation of polarized MDCK cell monolayers by Leptospira interrogans, an invasive but nonintracellular pathogen. Infect. Immun. 70:6926-6932.
8. Bharti AR, et al. 2003. Leptospirosis: a zoonotic disease of global importance. Lancet Infect. Dis. 3:757-771.
9. Branger C, et al. 2005. Protection against Leptospira interrogans sensu lato challenge by DNA immunization with the gene encoding hemolysinassociated protein 1. Infect. Immun. 73:4062-4069.
10. Carvalho E, et al. 2009. Leptospiral TlyC is an extracellular matrixbinding protein and does not present hemolysin activity. FEBS Lett. 583: 1381-1385.
11. Castiblanco-Valencia MM, et al. 2012. Leptospiral immunoglobulin-like proteins interact with human complement regulators factor H, FHL-1, FHR-1, and C4BP. J. Infect. Dis. 205:995-1004.
12. Choy HA, et al. 2007. Physiological osmotic induction of Leptospira interrogans adhesion: LigA and LigB bind extracellular matrix proteins and fibrinogen. Infect. Immun. 75:2441-2450.
13. Coleman JL, Benach JL. 1999. Use of the plasminogen activation system by microorganisms. J. Lab. Clin. Med. 134:567-576.
14. de la Pena-Moctezuma A, Bulach DM, Kalambaheti T, Adler B. 1999. Comparative analysis of the LPS biosynthetic loci of the genetic subtypes of serovar Hardjo: Leptospira interrogans subtype Hardjoprajitno and Leptospira borgpetersenii subtype Hardjobovis. FEMS Microbiol. Lett. 177:319-326.
15. Dennehy M, Williamson AL. 2005. Factors influencing the immune response to foreign antigen expressed in recombinant BCG vaccines. Vaccine 23:1209-1224.
16. Domingos RF, et al. 2012. Features of two proteins of Leptospira interrogans with potential role in host-pathogen interactions. BMC Microbiol. 12:50. doi:10.1186/1471-2180-12-50.
17. Dong H, et al. 2008. Characterization of the ompL1 gene of pathogenic Leptospira species in China and cross-immunogenicity of the OmpL1 protein. BMC Microbiol. 8:223. doi:10.1186/1471-2180-8-223.
18. Faine S, Adler B, Bolin C, Perolat P. 1999. Leptospira and leptospirosis, 2nd ed. MediSci, Melbourne, Australia.
19. Faisal SM, et al. 2008. Evaluation of protective immunity of Leptospira immunoglobulin like protein A (LigA) DNA vaccine against challenge in hamsters. Vaccine 26:277-287.
20. Flannery B, et al. 2001. Evaluation of recombinant Leptospira antigenbased enzyme-linked immunosorbent assays for the serodiagnosis of leptospirosis. J. Clin. Microbiol. 39:3303-3310.
21. Galen RS, Gambino SR. 1975. Beyond normality: the predictive value and efficiency of medical diagnosis. John Wiley & Sons, Inc, New York, NY.
22. Gruber A, Zingales B. 1995. Alternative method to remove antibacterial antibodies from antisera used for screening of expression libraries. Biotechniques 19:28, 30.
23. Haake DA, et al. 1993. Molecular cloning and sequence analysis of the gene encoding OmpL1, a transmembrane outer membrane protein of pathogenic Leptospira spp. J. Bacteriol. 175:4225-4234.
24. Haake DA, et al. 2000. The leptospiral major outer membrane protein LipL32 is a lipoprotein expressed during mammalian infection. Infect. Immun. 68:2276-2285.
25. Haake DA, et al. 1999. Leptospiral outer membrane proteins OmpL1 and LipL41 exhibit synergistic immunoprotection. Infect. Immun. 67:6572-6582.
26. Haake DA, et al. 2004. Molecular evolution and mosaicism of leptospiral outer membrane proteins involves horizontal DNA transfer. J. Bacteriol. 186:2818-2828.
27. Hauk P, et al. 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.
28. Hoke DE, Egan S, Cullen PA, Adler B. 2008. LipL32 is an extracellular matrix-interacting protein of Leptospira spp. and Pseudoalteromonas tunicata. Infect. Immun. 76:2063-2069.
29. Iwamoto E, et al. 2009. Nationwide survey of Leptospira antibodies in dogs in Japan: results from microscopic agglutination test and enzymelinked immunosorbent assay. J. Vet. Med. Sci. 71:1191-1199.
30. Ko AI, Galvao Reis M, Ribeiro Dourado CM, Johnson WD, Jr, Riley LW. 1999. Urban epidemic of severe leptospirosis in Brazil. Salvador Leptospirosis Study Group. Lancet 354:820-825.
31. Koizumi N, Watanabe H. 2005. Leptospirosis vaccines: past, present, and future. J. Postgrad. Med. 51:210-214.
32. Lahteenmaki K, Kuusela P, Korhonen TK. 2001. Bacterial plasminogen activators and receptors. FEMS Microbiol. Rev. 25:531-552.
33. Larkin MA, et al. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23:2947-2948.
34. Levett PN. 2001. Leptospirosis. Clin. Microbiol. Rev. 14:296-326.
35. Lin X, Sun A, Ruan P, Zhang Z, Yan J. 2011. Characterization of conserved combined T and B cell epitopes in Leptospira interrogans major outer membrane proteins OmpL1 and LipL41. BMC Microbiol. 11:21. doi:10.1186/1471-2180-11-21.
36. Lin YP, Chang YF. 2007. A domain of the Leptospira LigB contributes to high affinity binding of fibronectin. Biochem. Biophys. Res. Commun. 362:443-448.
37. Lin YP, et al. 2009. Repeated domains of Leptospira immunoglobulinlike proteins interact with elastin and tropoelastin. J. Biol. Chem. 284: 19380-19391.
38. Longhi MT, et al. 2009. A newly identified protein of Leptospira interrogans mediates binding to laminin. J. Med. Microbiol. 58:1275-1282.
39. Lucas DS, et al. 2011. Recombinant LipL32 and LigA from Leptospira are unable to stimulate protective immunity against leptospirosis in the hamster model. Vaccine 29:3413-3418.
40. Malmstrom J, et al. 2009. Proteome-wide cellular protein concentrations of the human pathogen Leptospira interrogans. Nature 460:762-765.
41. Maneewatch S, et al. 2007. OmpL1 DNA vaccine cross-protects against heterologous Leptospira spp. challenge. Asian Pac. J. Allergy Immunol. 25:75-82.
42. Marrack P, McKee AS, Munks MW. 2009. Towards an understanding of the adjuvant action of aluminium. Nat. Rev. 9:287-293.
43. Matthias MA, et al. 2008. Human leptospirosis caused by a new, antigenically unique Leptospira associated with a Rattus species reservoir in the Peruvian Amazon. PLoS Negl. Trop. Dis. 2:e213. doi:10.1371/journal.pntd.0000213.
44. Mendes RS, 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.
45. Merien F, Truccolo J, Baranton G, Perolat P. 2000. Identification of a 36-kDa fibronectin-binding protein expressed by a virulent variant of Leptospira interrogans serovar Icterohaemorrhagiae. FEMS Microbiol. Lett. 185:17-22.
46. Nally JE, et al. 2005. Purification and proteomic analysis of outer membrane vesicles from a clinical isolate of Leptospira interrogans serovar Copenhageni. Proteomics 5:144-152.
47. Natarajaseenivasan K, et al. 2008. Serodiagnosis of severe leptospirosis: evaluation of ELISA based on the recombinant OmpL1 or LipL41 antigens of Leptospira interrogans serovar Autumnalis. Ann. Trop. Med. Parasitol. 102:699-708.
48. Okuda M, et al. 2005. Enzyme-linked immunosorbent assay for the detection of canine Leptospira antibodies using recombinant OmpL1 protein. J. Vet. Med. Sci. 67:249-254.
49. Oliveira R, et al. 2011. Characterization of novel OmpA-like protein of Leptospira interrogans that binds extracellular matrix molecules and plasminogen. PLoS One 6:e21962. doi:10.1371/journal.pone.0021962.
50. Oliveira TR, et al. 2008. Evaluation of leptospiral recombinant antigens MPL17 and MPL21 for serological diagnosis of leptospirosis by enzymelinked immunosorbent assays. Clin. Vaccine Immunol. 15:1715-1722.
51. Oliveira TR, et al. 2010. LipL53, a temperature regulated protein from Leptospira interrogans that binds to extracellular matrix molecules. Microbes Infect. 12:207-217.
52. Perez-Iratxeta C, Andrade-Navarro MA. 2008. K2D2: estimation of protein secondary structure from circular dichroism spectra. BMC Struct. Biol. 8:25. doi:10.1186/1472-6807-8-25.
53. 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. doi:10.1371/journal.pntd.0000815.
54. Pinne M, Haake DA. 2009. A comprehensive approach to identification of surface-exposed, outer membrane-spanning proteins of Leptospira interrogans. PLoS One 4:e6071. doi:10.1371/journal.pone.0006071.
55. Plank R, Dean D. 2000. Overview of the epidemiology, microbiology, and pathogenesis of Leptospira spp. in humans. Microbes Infect. 2:1265-1276.
56. Qiu XF, Xu HF, Guo ZQ, Wang J, Yan J. 2008. Establishment and application of ELISAs based on rLipL32/1-LipL21-OmpL1/2 fusion antigen of Leptospira interrogans. Zhejiang Da Xue Xue Bao 37:592-598. (In Chinese.)
57. 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.
58. Reed SG, Bertholet S, Coler RN, Friede M. 2009. New horizons in adjuvants for vaccine development. Trends Immunol. 30:23-32.
59. Rost B, Yachdav G, Liu J. 2004. The PredictProtein server. Nucleic Acids Res. 32:W321-W326. doi:10.1093/nar/gkh377.
60. Salonen EM, Zitting A, Vaheri A. 1984. Laminin interacts with plasminogen and its tissue-type activator. FEBS Lett. 172:29-32.
61. Schmidt A, et al. 2011. Absolute quantification of microbial proteomes at different states by directed mass spectrometry. Mol. Syst. Biol. 7:510. doi: 10.1038/msb.2011.37.
62. Seixas FK, et al. 2007. Recombinant Mycobacterium bovis BCG expressing the LipL32 antigen of Leptospira interrogans protects hamsters from challenge. Vaccine 26:88-95.
63. Shang ES, et al. 1995. The rare outer membrane protein, OmpL1, of pathogenic Leptospira species is a heat-modifiable porin. Infect. Immun. 63:3174-3181.
64. Stevenson B, et al. 2007. Leptospira interrogans endostatin-like outer membrane proteins bind host fibronectin, laminin and regulators of complement. PLoS One 2:e1188. doi:10.1371/journal.pone.0001188.
65. Storni T, Kundig TM, Senti G, Johansen P. 2005. Immunity in response to particulate antigen-delivery systems. Adv. Drug Deliv. Rev. 57:333-355.
66. Studier FW. 1991. Use of bacteriophage T7 lysozyme to improve an inducible T7 expression system. J. Mol. Biol. 219:37-44.
67. Sun A, Wang Y, Du P, Wu S, Yan J. 2011. A sensitive and specific IgM-ELISA for the serological diagnosis of human leptospirosis using a rLipL32/1-LipL21-OmpL1/2 fusion protein. Biomed. Environ. Sci. 24: 291-299.
68. Sun H. 2006. The interaction between pathogens and the host coagulation system. Physiology (Bethesda) 21:281-288.
69. Turner LH. 1970. Leptospirosis. 3. Maintenance, isolation and demonstration of leptospires. Trans. R. Soc. Trop. Med. Hyg. 64:623-646.
70. Verma A, et al. 2010. Leptospiral endostatin-like protein A is a bacterial cell surface receptor for human plasminogen. Infect. Immun. 78:2053-2059.
71. Verma A, et al. 2006. LfhA, a novel factor H-binding protein of Leptospira interrogans. Infect. Immun. 74:2659-2666.
72. Vernel-Pauillac F, Merien F. 2006. Proinflammatory and immunomodulatory cytokine mRNA time course profiles in hamsters infected with a virulent variant of Leptospira interrogans. Infect. Immun. 74:4172-4179.
73. Vieira ML, et al. 2010. In vitro identification of novel plasminogenbinding receptors of the pathogen Leptospira interrogans. PLoS One 5:e11259. doi:10.1371/journal.pone.0011259.
74. Vieira ML, et al. 2010. Lsa63, a newly identified surface protein of Leptospira interrogans binds laminin and collagen IV. J. Infect. 60:52-64.
75. 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.
76. Vieira ML, Pimenta DC, de Morais ZM, Vasconcellos SA, Nascimento AL. 2009. Proteome analysis of Leptospira interrogans virulent strain. Open Microbiol. J. 3:69-74.
77. 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.
78. Vieira ML, Atzingen MV, Oliveira R, Mendes RS, Domingos RF, Vasconcellos SA, Nascimento ALTO. Plasminogen binding proteins and plasmin generation on the surface of Leptospira spp. - the contribution to the bacteria-host interactions. J. Biomed. Biotechnol., in press.
79. Vieira ML, Atzingen MV, Oliveira R, Mendes RS, Domingos RF, Vasconcellos SA, Nascimento ALTO. Plasminogen binding proteins and plasmin generation on the surface of Leptospira spp. - the contribution to the bacteria-host interactions. J. Biomed. Biotechnol., in press.
80. Zhang XY, et al. 2005. Expression and comparative analysis of genes encoding outer membrane proteins LipL21, LipL32 and OmpL1 in epidemic leptospires. Acta Biochim. Biophys. Sin. 37:649-656.
81. Zuerner R, Haake D, Adler B, Segers R. 2000. Technological advances in the molecular biology of Leptospira. J. Mol. Microbiol. Biotechnol. 2:455-462.