The Bartonella henselae VirB/Bep system interferes with vascular endothelial growth factor (VEGF) signalling in human vascular endothelial cells

Cellular Microbiology

Volumn 13, Issue 3, 2011, Pages 419-431

  Scheidegger, Florine ^a   Quebatte, Maxime ^a   Mistl, Claudia ^a   Dehio, Christoph ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PERVANADATE; PHOSPHATASE; PHOSPHOLIPASE C GAMMA; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 2; VIRB PROTEIN;

ARTICLE; BACTERIAL STRAIN; CALCIUM TRANSPORT; CAT SCRATCH DISEASE; CELL PROLIFERATION; CELL SURFACE; ENDOTHELIUM CELL; ENZYME ACTIVATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; TYPE IV SECRETION SYSTEM; WOUND CLOSURE;

BACTERIAL PROTEINS; BARTONELLA HENSELAE; BLOTTING, WESTERN; CALCIUM; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ENDOTHELIAL CELLS; HUMANS; IMMUNOBLOTTING; MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHOLIPASE C GAMMA; PHOSPHORYLATION; POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; VANADATES; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

BACTERIA (MICROORGANISMS); BARTONELLA HENSELAE;

EID: 79951486650     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2010.01545.x     Document Type: Article

References (48)

1. Augustin, H. (2004) Methods in Endothelial Cell Biology. Berlin: Springer.
2. 2+ and von Willebrand factor release in human endothelial cells. Am J Pathol 138: 213-221.
3. Carmeliet, P., Ferreira, V., Breier, G., Pollefeyt, S., Kieckens, L., Gertsenstein, M., etal. (1996) Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 380: 435-439.
4. Carpenter, A.E., Jones, T.R., Lamprecht, M.R., Clarke, C., Kang, I.H., Friman, O., etal. (2006) CellProfiler: image analysis software for identifying and quantifying cell phenotypes. Genome Biol 7: R100.
5. Chian, C.A., Arrese, J.E., and Pierard, G.E. (2002) Skin manifestations of Bartonella infections. Int J Dermatol 41: 461-466.
6. Clapham, D.E. (2007) Calcium signaling. Cell 131: 1047-1058.
7. Conley, T., Slater, L., and Hamilton, K. (1994) Rochalimaea species stimulate human endothelial cell proliferation and migration in vitro. J Lab Clin Med 124: 521-528.
8. Dehio, C. (2005) Bartonella-host-cell interactions and vascular tumour formation. Nat Rev Microbiol 3: 621-631.
9. Dehio, C. (2008) Infection-associated type IV secretion systems of Bartonella and their diverse roles in host cell interaction. Cell Microbiol 10: 1591-1598.
10. Dehio, C., Meyer, M., Berger, J., Schwarz, H., and Lanz, C. (1997) Interaction of Bartonella henselae with endothelial cells results in bacterial aggregation on the cell surface and the subsequent engulfment and internalisation of the bacterial aggregate by a unique structure, the invasome. J Cell Sci 110: 2141-2154.
11. Dhillon, A.S., and Kolch, W. (2002) Untying the regulation of the Raf-1 kinase. Arch Biochem Biophys 404: 3-9.
12. Drancourt, M., Birtles, R., Chaumentin, G., Vandenesch, F., Etienne, J., and Raoult, D. (1996) New serotype of Bartonella henselae in endocarditis and cat-scratch disease. Lancet 347: 441-443.
13. Florin, T.A., Zaoutis, T.E., and Zaoutis, L.B. (2008) Beyond cat scratch disease: widening spectrum of Bartonella henselae infection. Pediatrics 121: e1413-e1425.
14. Fong, G.H., Zhang, L., Bryce, D.M., and Peng, J. (1999) Increased hemangioblast commitment, not vascular disorganization, is the primary defect in flt-1 knock-out mice. Development 126: 3015-3025.
15. Fuhrmann, O., Arvand, M., Gohler, A., Schmid, M., Krull, M., Hippenstiel, S., etal. (2001) Bartonella henselae induces NF-kappaB-dependent upregulation of adhesion molecules in cultured human endothelial cells: possible role of outer membrane proteins as pathogenic factors. Infect Immun 69: 5088-5097.
16. Garcia, F.U., Wojta, J., Broadley, K.N., Davidson, J.M., and Hoover, R.L. (1990) Bartonella bacilliformis stimulates endothelial cells in vitro and is angiogenic in vivo. Am J Pathol 136: 1125-1135.
17. Hiratsuka, S., Minowa, O., Kuno, J., Noda, T., and Shibuya, M. (1998) Flt-1 lacking the tyrosine kinase domain is sufficient for normal development and angiogenesis in mice. Proc Natl Acad Sci USA 95: 9349-9354.
18. Holmes, K., Roberts, O.L., Thomas, A.M., and Cross, M.J. (2007) Vascular endothelial growth factor receptor-2: structure, function, intracellular signalling and therapeutic inhibition. Cell Signal 19: 2003-2012.
19. Hunter, T. (1995) Protein kinases and phosphatases: the yin and yang of protein phosphorylation and signaling. Cell 80: 225-236.
20. Kempf, V.A., Volkmann, B., Schaller, M., Sander, C.A., Alitalo, K., Riess, T., and Autenrieth, I.B. (2001) Evidence of a leading role for VEGF in Bartonella henselae-induced endothelial cell proliferations. Cell Microbiol 3: 623-632.
21. Kirby, J.E., and Nekorchuk, D.M. (2002) Bartonella-associated endothelial proliferation depends on inhibition of apoptosis. Proc Natl Acad Sci USA 99: 4656-4661.
22. Koehler, J.E., and Tappero, J.W. (1993) Bacillary angiomatosis and bacillary peliosis in patients infected with human immunodeficiency virus. Clin Infect Dis 17: 612-624.
23. Korff, T., and Augustin, H.G. (1998) Integration of endothelial cells in multicellular spheroids prevents apoptosis and induces differentiation. J Cell Biol 143: 1341-1352.
24. Korff, T., and Augustin, H.G. (1999) Tensional forces in fibrillar extracellular matrices control directional capillary sprouting. J Cell Sci 112: 3249-3258.
25. Lawson, N.D., Mugford, J.W., Diamond, B.A., and Weinstein, B.M. (2003) Phospholipase C gamma-1 is required downstream of vascular endothelial growth factor during arterial development. Genes Dev 17: 1346-1351.
26. Olsson, A.K., Dimberg, A., Kreuger, J., and Claesson-Welsh, L. (2006) VEGF receptor signalling - in control of vascular function. Nat Rev Mol Cell Biol 7: 359-371.
27. Pulliainen, A.T., and Dehio, C. (2008) Bartonella henselae: suvbersion of vascular endothelial cell functions by translocated bacterial effector proteins. Int J Biochem Cell Biol 41: 507-510.
28. Quebatte, M., Dehio, M., Tropel, D., Basler, A., Toller, I., Raddatz, G., etal. (2010) The BatR/BatS two-component regulatory system controls the adaptive response of Bartonella henselae during human endothelial cell infection. J Bacteriol 192: 3352-3367.
29. Regnery, R.L., Anderson, B.E., Clarridge, J.E., 3rd, Rodriguez-Barradas, M.C., Jones, D.C., and Carr, J.H. (1992) Characterization of a novel Rochalimaea species, R. henselae sp. nov., isolated from blood of a febrile, human immunodeficiency virus-positive patient. J Clin Microbiol 30: 265-274.
30. Resto-Ruiz, S.I., Schmiederer, M., Sweger, D., Newton, C., Klein, T.W., Friedman, H., and Anderson, B.E. (2002) Induction of a potential paracrine angiogenic loop between human THP-1 macrophages and human microvascular endothelial cells during Bartonella henselae infection. Infect Immun 70: 4564-4570.
31. Riess, T., Andersson, S.G., Lupas, A., Schaller, M., Schafer, A., Kyme, P., etal. (2004) Bartonella adhesin a mediates a proangiogenic host cell response. J Exp Med 200: 1267-1278.
32. Riess, T., Raddatz, G., Linke, D., Schafer, A., and Kempf, V.A. (2007) Analysis of Bartonella adhesin A expression reveals differences between various B. henselae strains. Infect Immun 75: 35-43.
33. Saenz, H.L., Engel, P., Stoeckli, M.C., Lanz, C., Raddatz, G., Vayssier-Taussat, M., etal. (2007) Genomic analysis of Bartonella identifies type IV secretion systems as host adaptability factors. Nat Genet 39: 1469-1476.
34. Sakurai, Y., Ohgimoto, K., Kataoka, Y., Yoshida, N., and Shibuya, M. (2005) Essential role of Flk-1 (VEGF receptor 2) tyrosine residue 1173 in vasculogenesis in mice. Proc Natl Acad Sci USA 102: 1076-1081.
35. Scheidegger, F., Ellner, Y., Guye, P., Rhomberg, T.A., Weber, H., Augustin, H.G., and Dehio, C. (2009) Distinct activities of Bartonella henselae type IV secretion effector proteins modulate capillary-like sprout formation. Cell Microbiol 11: 1088-1101.
36. Schmid, M.C., Schulein, R., Dehio, M., Denecker, G., Carena, I., and Dehio, C. (2004) The VirB type IV secretion system of Bartonella henselae mediates invasion, proinflammatory activation and antiapoptotic protection of endothelial cells. Mol Microbiol 52: 81-92.
37. Schmid, M.C., Scheidegger, F., Dehio, M., Balmelle-Devaux, N., Schulein, R., Guye, P., etal. (2006) A translocated bacterial protein protects vascular endothelial cells from apoptosis. PLoS Pathog 2: e115.
38. Schulein, R., Guye, P., Rhomberg, T.A., Schmid, M.C., Schroder, G., Vergunst, A.C., etal. (2005) A bipartite signal mediates the transfer of type IV secretion substrates of Bartonella henselae into human cells. Proc Natl Acad Sci USA 102: 856-861.
39. Shalaby, F., Rossant, J., Yamaguchi, T.P., Gertsenstein, M., Wu, X.F., Breitman, M.L., and Schuh, A.C. (1995) Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice. Nature 376: 62-66.
40. Shibuya, M. (2006) Differential roles of vascular endothelial growth factor receptor-1 and receptor-2 in angiogenesis. J Biochem Mol Biol 39: 469-478.
41. Sobke, A.C., Selimovic, D., Orlova, V., Hassan, M., Chavakis, T., Athanasopoulos, A.N., etal. (2006) The extracellular adherence protein from Staphylococcus aureus abrogates angiogenic responses of endothelial cells by blocking Ras activation. FASEB J 20: 2621-2623.
42. Takahashi, H., and Shibuya, M. (2005) The vascular endothelial growth factor (VEGF)/VEGF receptor system and its role under physiological and pathological conditions. Clin Sci (Lond) 109: 227-241.
43. Takahashi, T., Ueno, H., and Shibuya, M. (1999) VEGF activates protein kinase C-dependent, but Ras-independent Raf-MEK-MAP kinase pathway for DNA synthesis in primary endothelial cells. Oncogene 18: 2221-2230.
44. Takahashi, T., Yamaguchi, S., Chida, K., and Shibuya, M. (2001) A single autophosphorylation site on KDR/Flk-1 is essential for VEGF-A-dependent activation of PLC-gamma and DNA synthesis in vascular endothelial cells. EMBO J 20: 2768-2778.
45. Waltenberger, J., Claesson-Welsh, L., Siegbahn, A., Shibuya, M., and Heldin, C.H. (1994) Different signal transduction properties of KDR and Flt1, two receptors for vascular endothelial growth factor. J Biol Chem 269: 26988-26995.
46. Weber, H., Claffey, J., Hogan, M., Pampillon, C., and Tacke, M. (2008) Analyses of Titanocenes in the spheroid-based cellular angiogenesis assay. Toxicol In Vitro 22: 531-534.
47. Yashima, R., Abe, M., Tanaka, K., Ueno, H., Shitara, K., Takenoshita, S., and Sato, Y. (2001) Heterogeneity of the signal transduction pathways for VEGF-induced MAPKs activation in human vascular endothelial cells. J Cell Physiol 188: 201-210.
48. Zeng, H., Sanyal, S., and Mukhopadhyay, D. (2001) Tyrosine residues 951 and 1059 of vascular endothelial growth factor receptor-2 (KDR) are essential for vascular permeability factor/vascular endothelial growth factor-induced endothelium migration and proliferation, respectively. J Biol Chem 276: 32714-32719.