Leptospira interrogans Binds to Cadherins

PLoS Neglected Tropical Diseases

Volumn 8, Issue 1, 2014, Pages 15-

  Evangelista, Karen ^a   Franco, Ricardo ^a   Schwab, Andrew ^a   Coburn, Jenifer ^a  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CADHERIN; LEUKOCYTE ANTIGEN; VASCULAR ENDOTHELIAL CADHERIN;

ANIMAL CELL; ARTICLE; BACTERIUM ADHERENCE; CELL ADHESION; CONTROLLED STUDY; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; IMMUNOBLOTTING; LEPTOSPIRA INTERROGANS; LEPTOSPIROSIS; LIQUID CHROMATOGRAPHY; NONHUMAN; PROTEIN ANALYSIS; PROTEIN MICROARRAY; TANDEM MASS SPECTROMETRY; CELL LINE; METABOLISM; PHYSIOLOGY;

ANTIGENS, CD; BACTERIAL ADHESION; CADHERINS; CELL LINE; HUMANS; LEPTOSPIRA INTERROGANS;

EID: 84893799614     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0002672     Document Type: Article

References (69)

1. Adler B, de la Pena Moctezuma A, (2010) Leptospira and leptospirosis. Vetrinary Microbiology 140: 287-296.
2. Ballard SA, Williamson M, Adler B, Vinh T, Faine S, (1986) Interactions of virulent and avirulent leptospires with primary cultures of renal epithelial cells. J Med Microbiol 21: 59-67.
3. Ito T, Yanagawa R, (1987) Leptospiral attachment to extracellular matrix of mouse fibroblast (L929) cells. Vet Microbiol 15: 89-96.
4. Merien F, Baranton G, Perolat P, (1997) Invasion of Vero cells and induction of apoptosis in macrophages by pathogenic Leptospira interrogans are correlated with virulence. Infect Immun 65: 729-738.
5. Merien F, Truccolo J, Rougier Y, Baranton G, Perolat P, (1998) In vivo apoptosis of hepatocytes in guinea pigs infected with Leptospira interrogans serovar icterohaemorrhagiae. FEMS Microbiol Lett 169: 95-102.
6. Thomas DD, Higbie LM, (1990) In vitro association of leptospires with host cells. Infect Immun 58: 581-585.
7. Tsuchimoto M, Niikura M, Ono E, Kida H, Yanagawa R, (1984) Leptospiral attachment to cultured cells. Zentralbl Bakteriol Mikrobiol Hyg A 258: 268-274.
8. Vinh T, Faine S, Adler B, (1984) Adhesion of leptospires to mouse fibroblasts (L929) and its enhancement by specific antibody. J Med Microbiol 18: 73-85.
9. Breiner DD, Fahey M, Salvador R, Novakova J, Coburn J, (2009) Leptospira interrogans binds to human cell surface receptors including proteoglycans. Infect Immun 77: 5528-5536.
10. Kefford B, Marshall KC, (1984) Adhesion of Leptospira at a solid-liquid interface: a model. Arch Microbiol 138: 84-88.
11. Martinez-Lopez DG, Fahey M, Coburn J, (2010) Responses of human endothelial cells to pathogenic and non-pathogenic Leptospira species. PLoS Negl Trop Dis 4: e918.
12. 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.
13. 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.
14. Barbosa AS, Abreu PA, Neves FO, Atzingen MV, Watanabe MM, et al. (2006) A newly identified leptospiral adhesin mediates attachment to laminin. Infect Immun 74: 6356-6364.
15. 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.
16. Pinne M, Matsunaga J, Haake DA, (2012) A novel approach to identification of host ligand-binding proteins: leptospiral outer-membrane protein microarray. J Bacteriol 194: 6074-87.
17. Atzingen MV, Gomez RM, Schattner M, Pretre G, Goncales AP, 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.
18. 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 583: 1381-1385.
19. Castiblanco-Valencia MM, Fraga TR, Silva LB, Monaris D, Abreu PA, 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.
20. Ching AT, Favaro RD, Lima SS, Chaves AD, de Lima MA, et al. (2012) Lepstospira interrogans shotgun phage display identified LigB as a heparin-binding protein. Biochem Biophys Res Commun 427: 774-9.
21. Chirathaworn C, Patarakul K, Saksit V, Poovorawan Y, (2007) Binding of Leptospira to extracellular matrix proteins. J Med Assoc Thai 90: 2136-2142.
22. Choy HA, (2012) Multiple activities of LigB potentiate virulence of Leptospira interrogans: inhibition of alternative and classical pathways of complement. PLoS ONE 7: e41566.
23. 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.
24. 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: 3679-92.
25. Figueira CP, Croda J, Choy HA, Haake DA, Reis MG, et al. (2011) Heterologous expression of pathogen-specific genes LigA and LigB in the saprophyte Leptospira biflexa confers enhanced adhesion to cultured cells and fibronectin. BMC Microbiol 11: 129.
26. 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.
27. Ito T, Yanagawa R, (1987) Leptospiral attachment to four structural components of extracellular matrix. Nippon Juigaku Zasshi 49: 875-882.
28. 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.
29. Lin YP, McDonough SP, Sharma Y, Chang YF, (2010) The terminal immunoglobulin-like repeats of LigA and LigB of Leptospira enhance their binding to gelatin binding domain of fibronectin and host cells. PLoS ONE 5: e11301.
30. Longhi MT, Oliveira TR, Romero EC, Goncales AP, de Morais ZM, et al. (2009) A newly identified protein of Leptospira interrogans mediates binding to laminin. J Med Microbiol 58: 1275-1282.
31. Matsunaga J, Medeiros MA, Sanchez Y, Werneid KF, Ko AI, (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.
32. 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.
33. Oliveira TR, Longhi MT, Goncales AP, de Morais ZM, Vasconcellos SA, et al. (2010) LipL53, a temperature regulated protein from Leptospira interrogans that binds to extracellular matrix molecules. Microbes Infect 12: 207-217.
34. 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.
35. Stevenson B, Choy HA, Pinne M, Rotondi ML, Miller MC, et al. (2007) Leptospira interrogans endostatin-like outer membrane proteins bind host fibronectin, laminin and regulators of complement. PLoS ONE 2: e1188.
36. 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.
37. 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.
38. 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.
39. Coburn J, Leong J, Erban J, (1993) Integrin αIIbβ3 mediates binding of the Lyme disease agent, Borrelia burgdorferi, to human platelets. Proc Natl Acad Sci USA 90: 7058-7063.
40. Faine S, Adler B., Bolin C., and Perolat P. (1999) Leptospira and Leptospirosis. Melbourne, Australia: MedSci.
41. Matsunaga J, Barocchi MA, Croda J, Young TA, Sanchez Y, et al. (2003) Pathogenic Leptospira species express surface-exposed proteins belonging to the bacterial immunoglobulin superfamily. Mol Microbiol 49: 929-945.
42. Silva EF, Santos CS, Athanazio DA, Seyffert N, Seixas FK, et al. (2008) Characterization of virulence of Leptospira isolates in a hamster model. Vaccine 26: 3892-3896.
43. Nascimento AL, Ko AI, Martins EA, Monteiro-Vitorello CB, Ho PL, et al. (2004) Comparative genomics of two Leptospira interrogans serovars reveals novel insights into physiology and pathogenesis. J Bacteriol 186: 2164-2172.
44. Edgell CJ, McDonald CC, Graham JB, (1983) Permanent cell line expressing human factor VIII-related antigen established by hybridization. Proceedings of the National Academy of Sciences of the United States of America 80: 3734-3737.
45. Ades EW, Candal FJ, Swerlick RA, George VG, Summers S, et al. (1992) HMEC-1: establishment of an immortalized human microvascular endothelial cell line. J Invest Dermatol 99: 683-690.
46. Laemmli UK, (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
47. Behera AK, Durand E, Cugini C, Antonara S, Bourassa L, et al. (2008) Borrelia burgdorferi BBB07 interaction with integrin α3β1 stimulates production of pro-inflammatory mediators in primary human chondrocytes. Cell Microbiol 10: 320-331.
48. Coburn J, Barthold SW, Leong JM, (1994) Diverse Lyme disease spirochetes bind integrin αIIbβ3 on human platelets. Infect Immunity 62: 5559-5567.
49. Coburn J, Magoun L, Bodary SC, Leong JM, (1998) Integrins αvβ3 and α5β1 mediate attachment of lyme disease spirochetes to human cells. Infect Immun 66: 1946-1952.
50. Ito T, Yanagawa R, (1987) Attachment of antigenic variants of Leptospira to mouse fibroblasts resisting inhibitory effect of anti-parent antiserum. Jpn J Vet Res 35: 251-261.
51. Bonazzi M, Lecuit M, Cossart P, (2009) Listeria monocytogenes internalin and E-cadherin: from bench to bedside. Cold Spring Harb Perspect Biol 1: a003087.
52. Boyle EC, Finlay BB, (2003) Bacterial pathogenesis: exploiting cellular adherence. Curr Opin Cell Biol 15: 633-639.
53. Hauck CR, (2002) Cell adhesion receptors- signaling capacity and exploitation by bacterial pathogens. Med Microbiol Immunol 191: 55-62.
54. Juliano RL, (2002) Signal transduction by cell adhesion receptors and the cytoskeleton: functions of integrins, cadherins, selectins, and immunoglobulin-superfamily members. Annu Rev Pharmacol Toxicol 42: 283-323.
55. Hyafil F, Babinet C, Jacob F, (1981) Cell-cell interactions in early embryogenesis: a molecular approach to the role of calcium. Cell 26: 447-454.
56. Niessen CM, Leckband D, Yap AS, (2011) Tissue organization by cadherin adhesion molecules: dynamic molecular and cellular mechanisms of morphogenetic regulation. Physiol Rev 91: 691-731.
57. Lecuit M, Ohayon H, Braun L, Mengaud J, Cossart P, (1997) Internalin of Listeria monocytogenes with an intact leucine-rich repeat region is sufficient to promote internalization. Infect Immun 65: 5309-5319.
58. Mengaud J, Ohayon H, Gounon P, Mege RM, Cossart P, (1996) E-cadherin is the receptor for internalin, a surface protein required for entry of L. monocytogenes into epithelial cells. Cell 84: 923-932.
59. Fardini Y, Wang X, Temoin S, Nithianantham S, Lee D, et al. (2011) Fusobacterium nucleatum adhesin FadA binds vascular endothelial cadherin and alters endothelial integrity. Mol Microbiol 82: 1468-1480.
60. Staunton DE, Dustin ML, Springer TA, (1989) Functional cloning of ICAM-2, a cell adhesion ligand for LFA-1 homologous to ICAM-1. Nature 339: 61-64.
61. Del Carlo Bernardi F, Ctenas B, da Silva LF, Nicodemo AC, Saldiva PH, et al. (2012) Immune receptors and adhesion molecules in human pulmonary leptospirosis. Hum Pathol 43: 1601-1610.
62. Kerr JR, (1999) Cell adhesion molecules in the pathogenesis of and host defence against microbial infection. Mol Pathol 52: 220-230.
63. Medeiros Fda R, Spichler A, Athanazio DA, (2010) Leptospirosis-associated disturbances of blood vessels, lungs and hemostasis. Acta Trop 115: 155-162.
64. Dejana E, Orsenigo F, Lampugnani MG, (2008) The role of adherens junctions and VE-cadherin in the control of vascular permeability. J Cell Sci 121: 2115-2122.
65. Vestweber D, (2008) VE-cadherin: the major endothelial adhesion molecule controlling cellular junctions and blood vessel formation. Arterioscler Thromb Vasc Biol 28: 223-232.
66. Mengaud J, Lecuit M, Lebrun M, Nato F, Mazie JC, et al. (1996) Antibodies to the leucine-rich repeat region of internalin block entry of Listeria monocytogenes into cells expressing E-cadherin. Infect Immun 64: 5430-5433.
67. Kefford B, Marshall KC, (1986) The role of bacterial surface and substratum hydrophobicity in adhesion of Leptospira biflexa serovar Patoc 1 to inert surfaces. Microb Ecol 12: 315-322.
68. Navarro P, Ruco L, Dejana E, (1998) Differential localization of VE- and N-cadherins in human endothelial cells: VE-cadherin competes with N-cadherin for junctional localization. J Cell Biol 140: 1475-1484.
69. Prozialeck WC, Lamar PC, Appelt DM, (2004) Differential expression of E-cadherin, N-cadherin and beta-catenin in proximal and distal segments of the rat nephron. BMC Physiol 4: 10.