Bacterial Pili exploit integrin machinery to promote immune activation and efficient blood-brain barrier penetration

Nature Communications

Volumn 2, Issue 1, 2011, Pages

  Banerjee, Anirban ^a   Kim, Brandon J ^a   Carmona, Ellese M ^a   Cutting, Andrew S ^a   Gurney, Michael A ^a   Carlos, Chris ^a   Feuer, Ralph ^a   Prasadarao, Nemani V ^b   Doran, Kelly S ^a,c  

^a SAN DIEGO STATE UNIVERSITY   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; CHEMOKINE; PROTEIN PILA; UNCLASSIFIED DRUG; VERY LATE ACTIVATION ANTIGEN 2; FOCAL ADHESION KINASE; INTERLEUKIN 8;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL MENINGITIS; BACTERIAL VIRULENCE; BACTERIUM PILUS; BLOOD BRAIN BARRIER; BLOOD VESSEL PERMEABILITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; GENE EXPRESSION PROFILING; HUMAN; HUMAN CELL; IMMUNE RESPONSE; MALE; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; STREPTOCOCCUS AGALACTIAE; ANIMAL; BACTERIUM ADHERENCE; FIMBRIA; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; NEUTROPHIL; PHYSIOLOGY; SECRETION; SIGNAL TRANSDUCTION;

BACTERIA (MICROORGANISMS); MUS; PILA; STREPTOCOCCUS SP. 'GROUP B';

ANIMALS; BACTERIAL ADHESION; BLOOD-BRAIN BARRIER; CHEMOKINES; CHEMOTAXIS, LEUKOCYTE; FIMBRIAE, BACTERIAL; FOCAL ADHESION PROTEIN-TYROSINE KINASES; INTEGRIN ALPHA2BETA1; INTERLEUKIN-8; MENINGITIS, BACTERIAL; MICE; NEUTROPHILS; SIGNAL TRANSDUCTION; STREPTOCOCCUS AGALACTIAE;

EID: 80052634774     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms1474     Document Type: Article

References (59)

1. Edwards, M. S. & Baker, C. J. Group B Streptococcal Infections (Saunders, 2005).
2. Doran, K. S. & Nizet, V. Molecular pathogenesis of neonatal group B streptococcal infection: No longer in its infancy. Mol. Microbiol. 54, 23-31 (2004).
3. Doran, K. S., Liu, G. Y. & Nizet, V. Group B streptococcal beta-hemolysin/cytolysin activates neutrophil signaling pathways in brain endothelium and contributes to development of meningitis. J. Clin. Invest. 112, 736-744 (2003).
4. Lauer, P. et al. Genome analysis reveals pili in Group B Streptococcus. Science 309, 105 (2005).
5. Barocchi, M. A. et al. A pneumococcal pilus influences virulence and host inflammatory responses. Proc. Natl Acad. Sci. USA 103, 2857-2862 (2006).
6. Mora, M. et al. Group A Streptococcus produce pilus-like structures containing protective antigens and Lancefield T antigens. Proc. Natl Acad. Sci. USA 102, 15641-15646 (2005).
7. Kline, K. A., Dodson, K. W., Caparon, M. G. & Hultgren, S. J. A tale of two pili: Assembly and function of pili in bacteria. Trends Microbiol. 18, 224-232 (2010).
8. Maisey, H. C., Hensler, M., Nizet, V. & Doran, K. S. Group B streptococcal pilus proteins contribute to adherence to and invasion of brain microvascular endothelial cells. J. Bacteriol. 189, 1464-1467 (2007).
9. Mandlik, A., Swierczynski, A., Das, A. & Ton-That, H. Corynebacterium diphtheriae employs specific minor pilins to target human pharyngeal epithelial cells. Mol. Microbiol. 64, 111-124 (2007).
10. Nelson, A. L. et al. RrgA is a pilus-associated adhesin in Streptococcus pneumoniae. Mol. Microbiol. 66, 329-340 (2007).
11. Rosini, R. et al. Identification of novel genomic islands coding for antigenic pilus-like structures in Streptococcus agalactiae. Mol. Microbiol. 61, 126-141 (2006).
12. Nobbs, A. H. et al. Sortase A utilizes an ancillary protein anchor for efficient cell wall anchoring of pili in Streptococcus agalactiae. Infect. Immun. 76, 3550-3560 (2008).
13. Margarit, I. et al. Preventing bacterial infections with pilus-based vaccines: The group B streptococcus paradigm. J. Infect. Dis. 199, 108-115 (2009).
14. Lembo, A. et al. Regulation of CovR expression in Group B Streptococcus impacts blood-brain barrier penetration. Mol. Microbiol. 77, 431-443 (2010).
15. Banerjee, A. et al. Activation of brain endothelium by pneumococcal neuraminidase NanA promotes bacterial internalization. Cell. Microbiol. 12, 1576-1588 (2010).
16. Bradley, P. P., Priebat, D. A., Christensen, R. D. & Rothstein, G. Measurement of cutaneous inflammation: Estimation of neutrophil content with an enzyme marker. J. Invest. Dermatol. 78, 206-209 (1982).
17. Izore, T. et al. Structural basis of host cell recognition by the pilus adhesin from Streptococcus pneumoniae. Structure 18, 106-115 (2010).
18. Deivanayagam, C. C. S. et al. Novel fold and assembly of the repetitive B region of the Staphylococcus aureus collagen-binding surface protein. Structure 8, 67-78 (2000).
19. Cruz, M. A., Yuan, H., Lee, J. R., Wise, R. J. & Handin, R. I. Interaction of the von Willebrand factor (vWF) with collagen. J. Biol. Chem. 270, 10822-10827 (1995).
20. Konto-Ghiorghi, Y. et al. Dual role for pilus in adherence to epithelial cells and biofilm formation in Streptococcus agalactiae. PLoS Pathog. 5, e1000422 (2009).
21. Parsons, J. T. Focal adhesion kinase: The first ten years. J. Cell. Sci. 116, 1409-1416 (2003).
22. Mercurio, A. M. Lessons from the alpha2 integrin knockout mouse. Am. J. Pathol. 161, 3-6 (2002).
23. Pilorget, A. et al. Lebectin, a Macrovipera lebetina venom-derived C-type lectin, inhibits angiogenesis both in vitro and in vivo. J. Cell. Physiol. 211, 307-315 (2007).
24. Shin, S., Paul-Satyaseela, M., Lee, J. S., Romer, L. H. & Kim, K. S. Focal adhesion kinase is involved in type III group B streptococcal invasion of human brain microvascular endothelial cells. Microb. Pathog. 41, 168-173 (2006).
25. Reddy, M. A., Wass, C. A., Kim, K. S., Schlaepfer, D. D. & Prasadarao, N. V. Involvement of focal adhesion kinase in Escherichia coli invasion of human brain microvascular endothelial cells. Infect. Immun. 68, 6423-6430 (2000).
26. van Sorge, N. M. et al. The group B streptococcal serine-rich repeat 1 glycoprotein mediates penetration of the blood-brain barrier. J. Infect. Dis. 199, 1479-1487 (2009).
27. Daley, J. M., Thomay, A. A., Connolly, M. D., Reichner, J. S. & Albina, J. E. Use of Ly6G-specific monoclonal antibody to deplete neutrophils in mice. J. Leukoc. Biol. 83, 64-70 (2008).
28. Kaya, M. et al. Effects of lipopolysaccharide on the radiation-induced changes in the blood-brain barrier and the astrocytes. Brain Res. 1019, 105-112 (2004).
29. Stamatovic, S. M. et al. Monocyte chemoattractant protein-1 regulation of blood-brain barrier permeability. J. Cereb. Blood Flow Metab. 25, 593-606 (2005).
30. Betz, A. L. An overview of the multiple functions of the Blood Brain Barrier. NIDA Res. Monogr. 120, 54-72 (1992).
31. Doran, K. S. et al. Blood-brain barrier invasion by group B Streptococcus depends upon proper cell-surface anchoring of lipoteichoic acid. J. Clin. Invest. 115, 2499-2507 (2005).
32. Gutekunst, H., Eikmanns, B. J. & Reinscheid, D. J. The novel fibrinogen-binding protein FbsB promotes Streptococcus agalactiae invasion into epithelial cells. Infect. Immun. 72, 3495-3504 (2004).
33. Tenenbaum, T. et al. Streptococcus agalactiae invasion of human brain microvascular endothelial cells is promoted by the laminin-binding protein Lmb. Microbes Infect. 9, 714-720 (2007).
34. Tazi, A. et al. The surface protein HvgA mediates group B streptococcus hypervirulence and meningeal tropism in neonates. J. Exp. Med. 207, 2313-2322 (2010).
35. Godaly, G., Otto, G., Burdick, M. D., Strieter, R. M. & Svanborg, C. Fimbrial lectins influence the chemokine repertoire in the urinary tract mucosa. Kidney Int. 71, 778-786 (2007).
36. Hilleringmann, M. et al. Pneumococcal pili are composed of protofilaments exposing adhesive clusters of Rrg A. PLoS Pathog. 4, e1000026 (2008).
37. Kreikemeyer, B. et al. Streptococcus pyogenes collagen type I-binding Cpa surface protein. Expression profile, binding characteristics, biological function, and potential clinical impact. J. Biol. Chem. 280, 33228-33239 (2005).
38. Dehio, M., Gomez-Duarte, O. G., Dehio, C. & Meyer, T. F. Vitronectin-dependent invasion of epithelial cells by Neisseria gonorrhoeae involves alpha(v) integrin receptors. FEBS Lett. 424, 84-88 (1998).
39. Agerer, F., Michel, A., Ohlsen, K. & Hauck, C. R. Integrin-mediated invasion of Staphylococcus aureus into human cells requires Src family protein-tyrosine kinases. J. Biol. Chem. 278, 42524-42531 (2003).
40. Al-Okla, S., Chatenay-Rivauday, C., Klein, J. P. & Wachsmann, D. Involvement of alpha5beta1 integrins in interleukin 8 production induced by oral viridans streptococcal protein I/IIf in cultured endothelial cells. Cell. Microbiol. 1, 157-168 (1999).
41. Eitel, J., Heise, T., Thiesen, U. & Dersch, P. Cell invasion and IL-8 production pathways initiated by YadA of Yersinia pseudotuberculosis require common signalling molecules (FAK, c-Src, Ras) and distinct cell factors. Cell. Microbiol. 7, 63-77 (2005).
42. Unkmeir, A. et al. Fibronectin mediates Opc-dependent internalization of Neisseria meningitidis in human brain microvascular endothelial cells. Mol. Microbiol. 46, 933-946 (2002).
43. Sokolova, O. et al. Interaction of Neisseria meningitidis with human brain microvascular endothelial cells: Role of MAP-and tyrosine kinases in invasion and inflammatory cytokine release. Cell. Microbiol. 6, 1153-1166 (2004).
44. Bosman, F. T. Integrins: Cell adhesives and modulators of cell function. Histochem. J. 25, 469-477 (1993).
45. Tan, S., Tompkins, L. S. & Amieva, M. R. Helicobacter pylori usurps cell polarity to turn the cell surface into a replicative niche. PLoS Pathog. 5, e1000407 (2009).
46. Soriani, M. et al. Group B Streptococcus crosses human epithelial cells by a paracellular route. J. Infect. Dis. 193, 241-250 (2006).
47. Easton, A., Haque, A., Chu, K., Lukaszewski, R. & Bancroft, G. J. A critical role for neutrophils in resistance to experimental infection with Burkholderia pseudomallei. J. Infect. Dis. 195, 99-107 (2007).
48. Leendertse, M. et al. Neutrophils are essential for rapid clearance of Enterococcus faecium in mice. Infect. Immun. 77, 485-491 (2009).
49. de Bont, E. S. et al. Tumor necrosis factor-alpha, interleukin-1 beta, and interleukin-6 plasma levels in neonatal sepsis. Pediatr. Res. 33, 380-383 (1993).
50. van Faassen, H. et al. Neutrophils play an important role in host resistance to respiratory infection with Acinetobacter baumannii in mice. Infect. Immun. 75, 5597-5608 (2007).
51. Marks, M. et al. Influence of neutropenia on the course of serotype 8 pneumococcal pneumonia in mice. Infect. Immun. 75, 1586-1597 (2007).
52. Gresham, H. D. et al. Survival of Staphylococcus aureus inside neutrophils contributes to infection. J. Immunol. 164, 3713-3722 (2000).
53. Mednick, A. J., Feldmesser, M., Rivera, J. & Casadevall, A. Neutropenia alters lung cytokine production in mice and reduces their susceptibility to pulmonary cryptococcosis. Eur. J. Immunol. 33, 1744-1753 (2003).
54. Maione, D. et al. Identification of a universal Group B streptococcus vaccine by multiple genome screen. Science 309, 148-150 (2005).
55. van Sorge, N. M. et al. Anthrax toxins inhibit neutrophil signaling pathways in brain endothelium and contribute to the pathogenesis of meningitis. PLoS One 3, e2964 (2008).
56. Sasik, R., Calvo, E. & Corbeil, J. Statistical analysis of high-density oligonucleotide arrays: A multiplicative noise model. Bioinformatics 18, 1633-1640 (2002).
57. Vesterlund, S., Paltta, J., Karp, M. & Ouwehand, A. C. Measurement of bacterial adhesion-in vitro evaluation of different methods. J. Microbiol. Methods 60, 225-233 (2005).
58. Kwok, T. et al. Helicobacter exploits integrin for type IV secretion and kinase activation. Nature 449, 862-866 (2007).
59. Feuer, R. et al. Coxsackievirus B3 and the neonatal CNS: The roles of stem cells, developing neurons, and apoptosis in infection, viral dissemination, and disease. Am. J. Pathol. 163, 1379-1393 (2003).