Vascular binding of a pathogen under shear force through mechanistically distinct sequential interactions with host macromolecules

Molecular Microbiology

Volumn 86, Issue 5, 2012, Pages 1116-1131

  Moriarty, Tara J ^a,b   Shi, Meiqing ^b,e   Lin, Yi Pin ^c   Ebady, Rhodaba ^a   Zhou, Hong ^b,f   Odisho, Tanya ^a   Hardy, Pierre Olivier ^b   Salman Dilgimen, Aydan ^b   Wu, Jing ^d,g   Weening, Eric H ^d,h   Skare, Jon T ^d   Kubes, Paul ^b   Leong, John ^c   Chaconas, George ^b  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF CALGARY   (Canada)

^c TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d TEXAS A AND M UNIVERSITY   (United States)

^e UNIVERSITY OF MARYLAND   (United States)

^f NANJING MEDICAL UNIVERSITY   (China)

^g TEXAS A AND M UNIVERSITY   (United States)

^h UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; FIBRONECTIN; GLYCOSAMINOGLYCAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL TRANSLOCATION; BACTERIUM ADHERENCE; BLOOD FLOW; BLOOD VESSEL; BORRELIA BURGDORFERI; CONTROLLED STUDY; HOST PATHOGEN INTERACTION; IN VIVO STUDY; MALE; MICROSCOPY; MOLECULAR MECHANICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; SHEAR STRESS; SPIROCHETE;

ANIMALS; BACTERIAL ADHESION; BACTERIAL PROTEINS; BORRELIA BURGDORFERI; ENDOTHELIUM, VASCULAR; FIBRONECTINS; GLYCOSAMINOGLYCANS; HOST-PATHOGEN INTERACTIONS; LYME DISEASE; MICE; PROTEIN BINDING;

BACTERIA (MICROORGANISMS); BORRELIA BURGDORFERI; MUS; SPIROCHAETA;

EID: 84870254664     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12045     Document Type: Article

References (61)

1. Andruski, B., McCafferty, D.M., Ignacy, T., Millen, B., and McDougall, J.J. (2008) Leukocyte trafficking and pain behavioral responses to a hydrogen sulfide donor in acute monoarthritis. Am J Physiol Regul Integr Comp Physiol 295: R814-R820.
2. Antonara, S., Ristow, L., and Coburn, J. (2011) Adhesion mechanisms of Borrelia burgdorferi. Adv Exp Med Biol 715: 35-49.
3. Bankhead, T., and Chaconas, G. (2007) The role of VlsE antigenic variation in the Lyme disease spirochete: persistence through a mechanism that differs from other pathogens. Mol Microbiol 65: 1547-1558.
4. Barbour, A.G. (1984) Isolation and cultivation of Lyme disease spirochetes. Yale J Biol Med 57: 521-525.
5. Benoit, V.M., Fischer, J.R., Lin, Y., Parveen, N., and Leong, J.M. (2011) Allelic variation of the Lyme disease spirochete adhesin DbpA influences spirochetal binding to decorin, dermatan sulfate, and mammalian cells. Infect Immun 79: 3501-3509.
6. Bentley, K.L., Klebe, R.J., Hurst, R.E., and Horowitz, P.M. (1985) Heparin binding is necessary, but not sufficient, for fibronectin aggregation. A fluorescence polarization study. J Biol Chem 260: 7250-7256.
7. Brissette, C.A., Bykowski, T., Cooley, A.E., Bowman, A., and Stevenson, B. (2009) Borrelia burgdorferi RevA antigen binds host fibronectin. Infect Immun 77: 2802-2812.
8. Carroll, J.A., El-Hage, N., Miller, J.C., Babb, K., and Stevenson, B. (2001) Borrelia burgdorferi RevA antigen is a surface-exposed outer membrane protein whose expression is regulated in response to environmental temperature and pH. Infect Immun 69: 5286-5293.
9. Casjens, S., Palmer, N., van Vugt, R., Huang, W.H., Stevenson, B., Rosa, P., etal. (2000) A bacterial genome in flux: the twelve linear and nine circular extrachromosomal DNAs in an infectious isolate of the Lyme disease spirochete Borrelia burgdorferi. Mol Microbiol 35: 490-516.
10. Christner, M., Franke, G.C., Schommer, N.N., Wendt, U., Wegert, K., Pehle, P., etal. (2010) The giant extracellular matrix-binding protein of Staphylococcus epidermidis mediates biofilm accumulation and attachment to fibronectin. Mol Microbiol 75: 187-207.
11. Drake, S.L., Varnum, J., Mayo, K.H., Letourneau, P.C., Furcht, L.T., and McCarthy, J.B. (1993) Structural features of fibronectin synthetic peptide FN-C/H II, responsible for cell adhesion, neurite extension, and heparan sulfate binding. J Biol Chem 268: 15859-15867.
12. Dunham-Ems, S.M., Caimano, M.J., Pal, U., Wolgemuth, C.W., Eggers, C.H., Balic, A., and Radolf, J.D. (2009) Live imaging reveals a biphasic mode of dissemination of Borrelia burgdorferi within ticks. J Clin Invest 119: 3652-3665.
13. Dunham-Ems, S.M., Caimano, M.J., Eggers, C.H., and Radolf, J.D. (2012) Borrelia burgdorferi requires the alternative sigma factor RpoS for dissemination within the vector during tick-to-mammal transmission. PLoS Pathog 8: e1002532.
14. Eggers, C.H., Caimano, M.J., Clawson, M.L., Miller, W.G., Samuels, D.S., and Radolf, J.D. (2002) Identification of loci critical for replication and compatibility of a Borrelia burgdorferi cp32-based shuttle vector for the expression of fluorescent reporters in the Lyme disease spirochete. Mol Microbiol 43: 281-295.
15. Fink, D.L., Green, B.A., and St Geme, J.W., 3rd (2002) The Haemophilus influenzae Hap autotransporter binds to fibronectin, laminin, and collagen IV. Infect Immun 70: 4902-4907.
16. Fischer, J.R., Leblanc, K.T., and Leong, J.M. (2006) Fibronectin binding protein BBK32 of the Lyme disease spirochete promotes bacterial attachment to glycosaminoglycans. Infect Immun 74: 435-441.
17. Fraser, C.M., Casjens, S., Huang, W.M., Sutton, G.G., Clayton, R., Lathigra, R., etal. (1997) Genomic sequence of a Lyme disease spirochaete, Borrelia burgdorferi. Nature 390: 580-586.
18. Hallstrom, 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.
19. Harman, M.W., Dunham-Ems, S.M., Caimano, M.J., Belperron, A.A., Bockenstedt, L.K., Fu, H.C., etal. (2012) The heterogeneous motility of the Lyme disease spirochete in gelatin mimics dissemination through tissue. Proc Natl Acad Sci USA 109: 3059-3064.
20. Heilmann, C., Hartleib, J., Hussain, M.S., and Peters, G. (2005) The multifunctional Staphylococcus aureus autolysin aaa mediates adherence to immobilized fibrinogen and fibronectin. Infect Immun 73: 4793-4802.
21. Henderson, B., Nair, S., Pallas, J., and Williams, M.A. (2011) Fibronectin: a multidomain host adhesin targeted by bacterial fibronectin-binding proteins. FEMS Microbiol Rev 35: 147-200.
22. Hyde, J.A., Weening, E.H., Chang, M., Trzeciakowski, J.P., Hook, M., Cirillo, J.D., and Skare, J.T. (2011) Bioluminescent imaging of Borrelia burgdorferi in vivo demonstrates that the fibronectin-binding protein BBK32 is required for optimal infectivity. Mol Microbiol 82: 99-113.
23. Ingham, K.C., Brew, S.A., and Atha, D.H. (1990) Interaction of heparin with fibronectin and isolated fibronectin domains. Biochem J 272: 605-611.
24. Kim, J.H., Singvall, J., Schwarz-Linek, U., Johnson, B.J., Potts, J.R., and Hook, M. (2004) BBK32, a fibronectin binding MSCRAMM from Borrelia burgdorferi, contains a disordered region that undergoes a conformational change on ligand binding. J Biol Chem 279: 41706-41714.
25. Klopocki, A.G., Yago, T., Mehta, P., Yang, J., Wu, T., Leppanen, A., etal. (2008) Replacing a lectin-domain residue in L-selectin enhances binding to P-selectin glycoprotein ligand-1 but not to 6-sulfo-sialyl Lewis x. J Biol Chem 283: 11493-11500.
26. Labandeira-Rey, M., and Skare, J.T. (2001) Decreased infectivity in Borrelia burgdorferi strain B31 is associated with loss of linear plasmid 25 or 28-1. Infect Immun 69: 446-455.
27. Lee, W.Y., Moriarty, T.J., Wong, C.H., Zhou, H., Strieter, R.M., van Rooijen, N., etal. (2010) An intravascular immune response to Borrelia burgdorferi involves Kupffer cells and iNKT cells. Nat Immunol 11: 295-302.
28. Ley, K., Laudanna, C., Cybulsky, M.I., and Nourshargh, S. (2007) Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat Rev Immunol 7: 678-689.
29. Li, X., Liu, X., Beck, D.S., Kantor, F.S., and Fikrig, E. (2006) Borrelia burgdorferi lacking BBK32, a fibronectin-binding protein, retains full pathogenicity. Infect Immun 74: 3305-3313.
30. Lyon, M., Rushton, G., Askari, J.A., Humphries, M.J., and Gallagher, J.T. (2000) Elucidation of the structural features of heparan sulfate important for interaction with the Hep-2 domain of fibronectin. J Biol Chem 275: 4599-4606.
31. Meenan, N.A., Visai, L., Valtulina, V., Schwarz-Linek, U., Norris, N.C., Gurusiddappa, S., etal. (2007) The tandem beta-zipper model defines high affinity fibronectin-binding repeats within Staphylococcus aureus FnBPA. J Biol Chem 282: 25893-25902.
32. Moriarty, T.J., and Chaconas, G. (2009) Identification of the determinant conferring permissive substrate usage in the telomere resolvase, ResT. J Biol Chem 284: 23293-23301.
33. Moriarty, T.J., Norman, M.U., Colarusso, P., Bankhead, T., Kubes, P., and Chaconas, G. (2008) Real-time high resolution 3D imaging of the lyme disease spirochete adhering to and escaping from the vasculature of a living host. PLoS Pathog 4: e1000090.
34. Norman, M.U., Moriarty, T.J., Dresser, A.R., Millen, B., Kubes, P., and Chaconas, G. (2008) Molecular mechanisms involved in vascular interactions of the Lyme disease pathogen in a living host. PLoS Pathog 4: e1000169.
35. Norris, N.C., Bingham, R.J., Harris, G., Speakman, A., Jones, R.P., Leech, A., etal. (2011) Structural and functional analysis of the tandem beta-zipper interaction of a Streptococcal protein with human fibronectin. J Biol Chem 286: 38311-38320.
36. Norris, S.J., Coburn, J., Leong, J.M., Hu, L.T., and Hook, M. (2010) Pathobiology of Lyme disease Borrelia. In Borrelia: Molecular Biology, Host Interaction and Pathogenesis D. Samuels, S., and Radolf, J.D. (eds). Norwich: Horizon Scientific Press, pp. 293-325.
37. Pankov, R., and Yamada, K.M. (2002) Fibronectin at a glance. J Cell Sci 115: 3861-3863.
38. Parveen, N., and Leong, J.M. (2000) Identification of a candidate glycosaminoglycan-binding adhesin of the Lyme disease spirochete Borrelia burgdorferi. Mol Microbiol 35: 1220-1234.
39. Parveen, N., Caimano, M., Radolf, J.D., and Leong, J.M. (2003) Adaptation of the Lyme disease spirochaete to the mammalian host environment results in enhanced glycosaminoglycan and host cell binding. Mol Microbiol 47: 1433-1444.
40. Parveen, N., Cornell, K.A., Bono, J.L., Chamberland, C., Rosa, P., and Leong, J.M. (2006) Bgp, a secreted glycosaminoglycan-binding protein of Borrelia burgdorferi strain N40, displays nucleosidase activity and is not essential for infection of immunodeficient mice. Infect Immun 74: 3016-3020.
41. Prabhakaran, S., Liang, X., Skare, J.T., Potts, J.R., and Hook, M. (2009) A novel fibronectin binding motif in MSCRAMMs targets F3 modules. PLoS ONE 4: e5412.
42. Probert, W.S., and Johnson, B.J. (1998) Identification of a 47kDa fibronectin-binding protein expressed by Borrelia burgdorferi isolate B31. Mol Microbiol 30: 1003-1015.
43. Probert, W.S., Kim, J.H., Hook, M., and Johnson, B.J. (2001) Mapping the ligand-binding region of Borrelia burgdorferi fibronectin-binding protein BBK32. Infect Immun 69: 4129-4133.
44. Raibaud, S., Schwarz-Linek, U., Kim, J.H., Jenkins, H.T., Baines, E.R., Gurusiddappa, S., etal. (2005) Borrelia burgdorferi binds fibronectin through a tandem beta-zipper, a common mechanism of fibronectin binding in Staphylococci, Streptococci, and spirochetes. J Biol Chem 280: 18803-18809.
45. Samuels, D.S. (1995) Electrotransformation of the spirochete Borrelia burgdorferi. Methods Mol Biol 47: 253-259.
46. Schmid, G. (1989) Epidemiology and clinical similarities of human spirochetal diseases. Rev Infect Dis 11: S1460-S1469.
47. Schmit, V.L., Patton, T.G., and Gilmore, R.D., Jr. (2011) Analysis of Borrelia burgdorferi surface proteins as determinants in establishing host cell interactions. Front Microbiol 2 (141): 1-8.
48. Schwarz-Linek, U., Hook, M., and Potts, J.R. (2004) The molecular basis of fibronectin-mediated bacterial adherence to host cells. Mol Microbiol 52: 631-641.
49. Seshu, J., Esteve-Gassent, M.D., Labandeira-Rey, M., Kim, J.H., Trzeciakowski, J.P., Hook, M., and Skare, J.T. (2006) Inactivation of the fibronectin-binding adhesin gene bbk32 significantly attenuates the infectivity potential of Borrelia burgdorferi. Mol Microbiol 59: 1591-1601.
50. Sharma, A., Askari, J.A., Humphries, M.J., Jones, E.Y., and Stuart, D.I. (1999) Crystal structure of a heparin- and integrin-binding segment of human fibronectin. EMBO J 18: 1468-1479.
51. Stanek, G., Wormser, G.P., Gray, J., and Strle, F. (2012) Lyme borreliosis. Lancet 379: 461-473.
52. Steere, A.C., Coburn, J., and Glickstein, L. (2004) The emergence of Lyme disease. J Clin Invest 113: 1093-1101.
53. Tamura, G.S., Hull, J.R., Oberg, M.D., and Castner, D.G. (2006) High-affinity interaction between fibronectin and the group B streptococcal C5a peptidase is unaffected by a naturally occurring four-amino-acid deletion that eliminates peptidase activity. Infect Immun 74: 5739-5746.
54. Thomas, W.E. (2009) Mechanochemistry of receptor-ligand bonds. Curr Opin Struct Biol 19: 50-55.
55. Tourand, Y., Bankhead, T., Wilson, S.L., Putteet-Driver, A.D., Barbour, A.G., Byram, R., etal. (2006) Differential telomere processing by Borrelia telomere resolvases in vitro but not in vivo. J Bacteriol 188: 7378-7386.
56. Wang, L., Fuster, M., Sriramarao, P., and Esko, J.D. (2005) Endothelial heparan sulfate deficiency impairs L-selectin- and chemokine-mediated neutrophil trafficking during inflammatory responses. Nat Immunol 6: 902-910.
57. Wilske, B. (2005) Epidemiology and diagnosis of Lyme borreliosis. Ann Med 37: 568-579.
58. Wu, J., Weening, E.H., Faske, J.B., Hook, M., and Skare, J.T. (2011) Invasion of eukaryotic cells by Borrelia burgdorferi requires β1 integrins and Src kinase activity. Infect Immun 79: 1338-1348.
59. Yang, X.F., Pal, U., Alani, S.M., Fikrig, E., and Norgard, M.V. (2004) Essential role for OspA/B in the life cycle of the Lyme disease spirochete. J Exp Med 199: 641-648.
60. Zeghouf, M., Li, J., Butland, G., Borkowska, A., Canadien, V., Richards, D., etal. (2004) Sequential Peptide Affinity (SPA) system for the identification of mammalian and bacterial protein complexes. J Proteome Res 3: 463-468.
61. Zipfel, P.F., Wurzner, R., and Skerka, C. (2007) Complement evasion of pathogens: common strategies are shared by diverse organisms. Mol Immunol 44: 3850-3857.