Yersinia pseudotuberculosis-induced calcium signaling in neutrophils is blocked by the virulence effector YopH

Infection and Immunity

Volumn 67, Issue 5, 1999, Pages 2567-2574

  Andersson, Kerstin ^a   Magnusson, Karl Eric ^a   Majeed, Meytham ^a,c   Stendahl, Olle ^a   Fällman, Maria ^b  

^a LINKÖPING UNIVERSITY   (Sweden)

^b UMEÅ UNIVERSITY   (Sweden)

^c UNIVERSITY OF VERONA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; FORMYLMETHIONYLLEUCYLPHENYLALANINE; FURA 2 ACETOXYMETHYL ESTER; GUANINE NUCLEOTIDE BINDING PROTEIN; INTEGRIN; INVASIN; PROTEIN TYROSINE PHOSPHATASE; UNCLASSIFIED DRUG; VIRULENCE FACTOR; VIRULENCE FACTOR YOPH;

ARTICLE; BACTERIAL INFECTION; BACTERIAL VIRULENCE; BACTERIUM ADHERENCE; CALCIUM CELL LEVEL; CELL SURFACE; CONTROLLED STUDY; HUMAN; HUMAN CELL; NEUTROPHIL; PHAGOCYTOSIS; PRIORITY JOURNAL; YERSINIA PSEUDOTUBERCULOSIS;

EID: 0032959552     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/iai.67.5.2567-2574.1999     Document Type: Article

References (66)

1. Andersson, K., N. Carballeira, K.-E. Magnusson, C. Persson, O. Stendahl, H. Wolf-Watz, and M. Fällman. 1996. YopH of Yersinia pseudotuberculosis interrupts early phosphotyrosine signalling associated with phagocytosis. Mol. Microbiol. 20:1057-1069.
2. Aplin, A., A. Howe, S. Alahari, and R. Juliano. 1998. Signal transduction and signal modulation by cell adhesion receptors: the role of integrins, cadherins, immunoglobulin-cell adhesion molecules, and selectins. Pharmacol. Rev. 50: 197-263.
3. 2+ regulates the respiratory burst of human neutrophils. Biochim. Biophys. Acta 1404:475-483.
4. Cas as a substrate of Yersinia YopH (Yop51), a bacterial protein tyrosine phosphatase that translocates into mammalian cells and targets focal adhesions. EMBO J. 16: 2730-2744.
5. Bliska, J. B., and D. S. Black. 1995. Inhibition of the Fc receptor-mediated oxidative burst in macrophages by the Yersinia pseudotuberculosis tyrosine phosphatase. Infect. Immun. 63:681-685.
6. Bohnsack, J., and X. Zhou. 1992. Divalent cation substitution reveals CD18- and very late antigen-dependent pathways that mediate human neutrophil adherence to fibronectin. J. Immunol. 149:1340-1347.
7. Bölin, I., L. Norlander, and H. Wolf-Watz. 1982. Temperature-inducible outer membrane protein of Yersinia pseudotuberculosis and Yersinia enterocolitica is associated with the virulence plasmid. Infect. Immun. 37:506-512.
8. Bölin, I., and H. Wolf-Watz. 1984. Molecular cloning of the temperature-inducible outer membrane protein 1 of Yersinia pseudotuberculosis. Infect. Immun. 43:72-78.
9. Bölin, I., and H. Wolf-Watz. 1988. The plasmid-encoded Yop2b protein of Yersinia pseudotuberculosis is a virulence determinant regulated by calcium and temperature at the level of transcription. Mol. Microbiol. 2:237-245.
10. Böyum, A. 1968. Isolation of mononuclear cells and granulocytes from human blood. Isolation of mononuclear cells by one centrifugation, and of granulocytes by combining centrifugation and sedimentation at 1 g. Scand. J. Clin. Lab. Invest. Suppl. 97:77-89.
11. Clark, E. A., and J. S. Brugge. 1995. Integrins and signal transduction pathways: the road taken. Science 268:233-239.
12. Cornelis, G. R., and H. Wolf-Watz. 1997. The Yersinia Yop virulon: a bacterial system for subverting eukaryotic cells. Mol. Microbiol. 23:861-867.
13. Denu, J. M., J. A. Stuckey, M. A. Saper, and J. E. Dixon. 1996. Form and function in protein dephosphorylation. Cell 87:361-364.
14. Fällman, M., K. Andersson, S. Håkansson, K.-E. Magnusson, O. Stendahl, and H. Wolf-Watz. 1995. Yersinia pseudotuberculosis inhibits Fc receptor-mediated phagocytosis in J774 cells. Infect. Immun. 63:3117-3124.
15. Fällman, M., C. Persson, and H. Wolf-Watz. 1997. Yersinia proteins that target host cell signaling pathways. J. Clin. Invest. 99:1153-1157.
16. Francis, M. S., and H. Wolf-Watz. 1998. YopD of Yersinia pseudotuberculosis is translocated into the cytosol of HeLa epithelial cells: evidence of a structural domain necessary for translocation. Mol. Microbiol. 29:799-813.
17. 2+ indicators with greatly improved fluorescence properties. J. Biol. Chem. 260: 3440-3450.
18. Guan, K. L., and J. E. Dixon. 1990. Protein tyrosine phosphatase activity of an essential virulence determinant in Yersinia. Science 249:553-556.
19. Gustafson, M., and K. Magnusson. 1992. A novel principle for quantitation of fast intracellular calcium changes using Fura-2 and a modified image processing system-applications in studies of neutrophil motility and phagocytosis. Cell Calcium 13:473-486.
20. Hamid, N., A. Gustavsson, K. Andersson, K. McGee, C. Persson, C. Rudd, and M. Fällman. Unpublished data.
21. Hartland, E. L., S. P. Green, W. A. Phillips, and R. M. Robins-Browne. 1994. Essential role of YopD in inhibition of the respiratory burst of macrophages by Yersinia enterocolitica. Infect. Immun. 62:4445-4453.
22. 3. Biochem. J. 317:403-409.
23. Huttenlocher, A., S. Palecek, Q. Lu, W. Zhang, R. Meilgren, D. Lauffenburger, M. Ginsberg, and A. Horwitz. 1997. Regulation of cell migration by the calcium-dependent protease calpain. J. Biol. Chem. 272:32719-32722.
24. Hynes, R. O. 1992. Integrins: versatility, modulation, and signaling in cell adhesion. Cell 69:11-25.
25. Håkansson, S., K. Schesser, C. Persson, E. E. Galyov, R. Rosqvist, F. Homble, and H. Wolf-Watz. 1996. The YopB protein of Yersinia pseudotuberculosis is essential for the translocation of Yop effector proteins across the target cell plasma membrane and displays a contact-dependent membrane disrupting activity. EMBO J. 15:5812-5823.
26. 1 chain integrins are receptors for invasin, a protein that promotes bacterial penetration into mammalian cells. Cell 60:861-871.
27. Jaconi, M., D. Lew, J. Carpentier, K. Magnusson, M. Sjögren, and O. Stendahl. 1990. Cytosolic free calcium elevation mediates the phagosome-lysosome fusion during phagocytosis in human neutrophils. J. Cell Biol. 110: 1555-1564.
28. 2+ in human neutrophils: initiation by adherence receptors of the integrin family. J. Cell Biol. 112:1249-1257.
29. Jockusch, B. M., P. Bubeck, K. Giehl, M. Kroemker, J. Moschner, M. Rothkegel, M. Rudiger, K. Schluter, G. Stanke, and J. Winkler. 1995. The molecular architecture of focal adhesions. Annu. Rev. Cell Dev. Biol. 11:379-416.
30. Kanner, S. 1996. Focal adhesion kinase-related fakB is regulated by the integrin LFA-1 and interacts with the SH3 domain of phospholipase C gamma 1. Cell. Immunol. 171:164-169.
31. 2+- and calcineurin-dependent recycling of an integrin to the front of migrating neutrophils. Nature 377:75-79.
32. 3-mediated endothelial cell migration is triggered through distinct signaling mechanisms. J. Cell Biol. 121:163-170.
33. 2+-independent phagocytosis in human neutrophils. Nature 315:509-511.
34. Marks, P., and F. Maxfield. 1990. Local and global changes in cytosolic free calcium in neutrophils during chemotaxis and phagocytosis. Cell Calcium 11: 181-190.
35. γ in rat embryo fibroblasts. Proc. Natl. Acad. Sci. USA 88: 7111-7115.
36. Miyamoto, S., H. Teramoto, O. A. Coso, J. S. Gutkind, P. D. Burbelo, S. K. Akiyama, and K. M. Yamada. 1995a. Integrin function: molecular hierarchies of cytoskeletal and signaling molecules. J. Cell Biol. 131:791-605.
37. 2+-induced exocytosis in individual human neutrophils: high- and low-affinity granule populations and submaximal responses. EMBO J. 17:1279-1288.
38. Persson, C., K. Andersson, R. Nordfelth, Ä. Forsberg, H. Wolf-Watz, and M. Fällman. Unpublished data.
39. Cas and FAK, and the associated accumulation of these proteins in peripheral focal adhesions. EMBO J. 16:2307-2318.
40. Persson, C., R. Nordfelth, A. Holmström, S. Håkansson, R. Rosqvist, and H. Wolf-Watz. 1995. Cell-surface-bound Yersinia translocate the protein tyrosine phosphatase YopH by a polarized mechanism into the target cell. Mol. Micrcbiol. 18:135-150.
41. 2+ from intracellular stores in neutrophils. Immunology 80:157-159.
42. Pettersson, J., R. Nordfelth, E. Dubinina, T. Bergman, M. Gustafsson, K.-E. Magnusson, and H. Wolf-Watz. 1996. Modulation of virulence factor expression by pathogen target cell contact. Science 273:1231-1233.
43. 2+ release and influx in human neutrophils using a novel confocal laser scanning mode. Biochem. Biophys. Res. Commun. 229:109-113.
44. 1 heterodimer. J. Leukoc. Biol. 53:576-582.
45. Rosqvist, R., I. Bölin, and H. Wolf-Watz. 1988. Inhibition of phagocytosis in Yersinia pseudotuberculosis: a virulence plasmid-encoded ability involving the Yop2b protein. Infect. Immun. 56:2139-2143.
46. Rosqvist, R., A. Forsberg, M. Rimpilainen, T. Bergman, and H. Wolf-Watz. 1990. The cytotoxic protein YopE of Yersinia obstructs the primary host defence. Mol. Microbiol. 4:657-667.
47. Rosqvist, R., A. Forsberg, and H. Wolf-Watz. 1991. Intracellular targeting of the Yersinia YopE cytotoxin in mammalian cells induces actin microfilament disruption. Infect. Immun. 59:4562-4569.
48. Rosqvist, R., K.-E. Magnusson, and H. Wolf-Watz. 1994. Target cell contact triggers expression and polarized transfer of Yersinia YopE cytotoxin into mammalian cells. EMBO J. 13:964-972.
49. Rosqvist, R., M. Skurnik, and H. Wolf-Watz. 1988. Increased virulence of Yersinia pseudotuberculosis by two independent mutations. Nature 334:522-525.
50. Ruckdeschel, K., A. Roggenkamp, S. Schubert, and J. Heesemann. 1996. Differential contribution of Yersinia enterocolitica virulence factors to evasion of microbicidal action of neutrophils. Infect. Immun. 64:724-733.
51. Salmond, G. P., and P. J. Reeves. 1993. Membrane traffic wardens and protein secretion in gram-negative bacteria. Trends Biochem. Sci. 18:7-12.
52. Schesser, K., A.-K. Spiik, J.-M. Dukuzumuremyi, M. F. Neurath, S. Pettersson, and H. Wolf-Watz. 1998. The yopJ locus is required for Yersinia-mediated inhibition of Nκ-KB activation and cytokine expression: YopJ contains a eucaryotic SH2-like domain that is essential for its repressive activity. Mol. Microbiol. 28:1067-1079.
53. Schwartz, M. 1993. Signaling by integrins: implications for tumorigenesis. Cancer Res. 53:1503-1506.
54. v integrins mediate the rise in intracellular calcium in endothelial cells on fibronectin even though they play a minor role in adhesion. J. Biol. Chem. 269:11133-11137.
55. Schwartz, M. A., M. D. Schaller, and M. H. Ginsberg. 1995. Integrins: emerging paradigms of signal transduction. Annu. Rev. Cell Dev. Biol. 11: 549-599.
56. Sengeløv, H., P. Follin, L. Kjeldsen, K. Lollike, C. Dahlgren, and N. Borregaard. 1995. Mobilization of granules and secretory vesicles during in vivo exudation of human neutrophils. J. Immunol. 154:4157-4165.
57. Sengeløv, H., L. Kjeldsen, and N. Borregaard. 1993. Control of exocytosis in early neutrophil activation. J. Immunol. 150:1535-1543.
58. Simonet, M., S. Richard, and P. Berche. 1990. Electron microscopic evidence for in vivo extracellular localization of Yersinia pseudotuberculosis harboring the pYV plasmid. Infect. Immun. 58:841-845.
59. Sjaastad, M., and W. Nelson. 1997. Integrin-mediated calcium signaling and regulation of cell adhesion by intracellular calcium. Bioessays 19:47-55.
60. 2+ stores during phagocytosis in human neutrophils. Science 265:1439-1441.
61. 2+ stores. Blood 85:2194-2201.
62. Tonks, N. K., and B. G. Neel. 1996. From form to function: signaling by protein tyrosine phosphatases. Cell 87:365-368.
63. 1 chain integrins is determined by ligand affinity and receptor density. EMBO J. 12:1887-1895.
64. 2+ signaling in Jurkat T lymphocytes. J. Immunol. 158:1618-1627.
65. Visser, L. G., A. Annema, and R. van Furth. 1995. Role of Yops in inhibition of phagocytosis and killing of opsonized Yersinia enterocolitica by human granulocytes. Infect. Immun. 63:2570-2575.
66. Zhang, Z. Y., J. C. Clemens, H. L. Schubert, J. A. Stuckey, M. W. Fischer, D. M. Hume, M. A. Saper, and J. E. Dixon. 1992. Expression, purification, and physicochemical characterization of a recombinant Yersinia protein tyrosine phosphatase. J. Biol. Chem. 267:23759-23766.