Cell invasion of Yersinia pseudotuberculosis by invasin and YadA requires protein kinase C, phospholipase C-γ1 and Akt kinase

Cellular Microbiology

Volumn 11, Issue 12, 2009, Pages 1782-1801

  Uliczka, Frank ^a,b   Kornprobst, Tina ^a   Eitel, Julia ^c   Schneider, Daniela ^d   Dersch, Petra ^a,b  

^a TECHNICAL UNIVERSITY OF BRAUNSCHWEIG   (Germany)

^b HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

^c CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^d Bundesministerium für Risikobewertung ^*  (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BETA1 INTEGRIN; INTERLEUKIN 8; INVASIN; MITOGEN ACTIVATED PROTEIN KINASE; OUTER MEMBRANE PROTEIN; PHOSPHOLIPASE C GAMMA1; PROTEIN KINASE B; PROTEIN KINASE B BETA; PROTEIN KINASE C; PROTEIN KINASE C ALPHA; PROTEIN KINASE C BETA; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; YADA PROTEIN;

ARTICLE; BACTERIUM ADHERENCE; CELL INVASION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; EPITHELIUM CELL; HUMAN; HUMAN CELL; INTERNALIZATION; LISTERIA MONOCYTOGENES; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; RNA INTERFERENCE; SALMONELLA TYPHIMURIUM; SIGNAL TRANSDUCTION; YERSINIA PSEUDOTUBERCULOSIS;

ADHESINS, BACTERIAL; CELL LINE; ENZYME INHIBITORS; HOST-PATHOGEN INTERACTIONS; HUMANS; INTERLEUKIN-8; ONCOGENE PROTEIN V-AKT; PHAGOCYTOSIS; PHOSPHOLIPASE C GAMMA; PROTEIN KINASE C; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; YERSINIA PSEUDOTUBERCULOSIS; YERSINIA PSEUDOTUBERCULOSIS INFECTIONS;

MAMMALIA; YERSINIA PSEUDOTUBERCULOSIS;

EID: 72749110360     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2009.01371.x     Document Type: Article

References (82)

1. Alrutz, M.A., and Isberg, R.R. (1998) Involvement of focal adhesion kinase in invasin-mediated uptake. Proc Natl Acad Sci USA 95: 13658-13663.
2. Alrutz, M.A., Srivastava, A., Wong, K.W., D'Souza-Schorey, C., Tang, M., Ch'ng, L.E., et al. (2001) Efficient uptake of Yersinia pseudotuberculosis via integrin receptors involves a Rac1-Arp 2/3 pathway that bypasses N-WASP function. Mol Microbiol 42: 689-703.
3. Anilkumar, N., Parsons, M., Monk, R., Ng, T., and Adams, J.C. (2003) Interaction of fascin and protein kinase Calpha: a novel intersection in cell adhesion and motility. EMBO J 22: 5390-5402.
4. Bae, Y.S., Cantley, L.G., Chen, C.S., Kim, S.R., Kwon, K.S., and Rhee, S.G. (1998) Activation of phospholipase C-gamma by phosphatidylinositol 3,4,5-trisphosphate. J Biol Chem 273: 4465-4469.
5. Banan, A., Zhang, L.J., Farhadi, A., Fields, J.Z., Shaikh, M., and Keshavarzian, A. (2004) PKC-beta1 isoform activation is required for EGF-induced NF-kappaB inactivation and IkappaBalpha stabilization and protection of F-actin assembly and barrier function in enterocyte monolayers. Am J Physiol Cell Physiol 286: 723-738.
6. Barbieri, M.A., Kohn, A.D., Roth, R.A., and Stahl, P.D. (1998) Protein kinase B/akt and rab5 mediate Ras activation of endocytosis. J Biol Chem 273: 19367-19370.
7. Barnett, S.F., Bilodeau, M.T., and Lindsley, C.W. (2005) The Akt/PKB family of protein kinases: a review of small molecule inhibitors and progress towards target validation. Curr Top Med Chem 5: 109-125.
8. Bergmann, S., Lang, A., Rohde, M., Agarwal, V., Rennemeier, C., Grashoff, C., et al. (2009) Integrin-linked kinase is required for vitronectin-mediated internalization of Strep-tococcus pneumoniae by host cells. J Cell Sci 122: 256- 267.
9. Bierne, H., and Cossart, P. (2002) InlB, a surface protein of Listeria monocytogenes that behaves as an invasin and a growth factor. J Cell Sci 115: 3357-3367.
10. Bierne, H., Dramsi, S., Gratacap, M.P., Randriamampita, C., Carpenter, G., Payrastre, B., and Cossart, P. (2000) The invasion protein InlB from Listeria monocytogenes activates PLC-g1 downstream from I 3-kinase. Cell Microbiol 2: 465-476.
11. Brazil, D.P., and Hemmings, B.A. (2001) Ten years of protein kinase B signalling: a hard Akt to follow. Trends Biochem Sci 26: 657-664.
12. Brazil, D.P., Yang, Z.Z., and Hemmings, B.A. (2004) Advances in protein kinase B signalling: AKTion on multiple fronts. Trends Biochem Sci 29: 233-242.
13. Bruce-Staskal, P.J., Weidow, C.L., Gibson, J.J., and Bouton, A.H. (2002) Cas, Fak and Pyk2 function in diverse signaling cascades to promote Yersinia uptake. J Cell Sci 115: 2689-2700.
14. Burnham, C.A., Shokoples, S.E., and Tyrrell, G.J. (2007) Invasion of HeLa cells by group B streptococcus requires the phosphoinositide-3-kinase signalling pathway and modulates phosphorylation of host-cell Akt and glycogen synthase kinase-3. Microbiology 153: 4240-4252.
15. Cardone, M.H., Roy, N., Stennicke, H.R., Salvesen, G.S., Franke, T.F., Stanbridge, E., et al. (1998) Regulation of cell death protease caspase-9 by phosphorylation. Science 282: 1318-1321.
16. Cenni, V., Sirri, A., Riccio, M., Lattanzi, G., Santi, S., de Pol, A., et al. (2003) Targeting of the Akt/PKB kinase to the actin skeleton. Cell Mol Life Sci 60: 2710-2720.
17. Choi, J.H., Yang, Y.R., Lee, S.K., Kim, I.S., Ha, S.H., Kim, E.K., et al. (2007) Phospholipase C-gamma1 potentiates integrin-dependent cell spreading and migration through Pyk2/paxillin activation. Cell Signal 19: 1784-1796.
18. Coombes, B.K., and Mahony, J.B. (2002) Identification of MEK- and phosphoinositide 3-kinase-dependent signalling as essential events during Chlamydia pneumoniae invasion of HEp2 cells. Cell Microbiol 4: 447-460.
19. Coxon, P.Y., Summersgill, J.T., Ramirez, J.A., and Miller, R.D. (1998) Signal transduction during Legionella pneumophila entry into human monocytes. Infect Immun 66: 2905- 2913.
20. Datta, S.R., Brunet, A., and Greenberg, M.E. (1999) Cellular survival: a play in three Akts. Genes Dev 13: 2905-2927. Dehio, M., Gomez-Duarte, O.G., Dehio, C., and Meyer, T.F. (1998) Vitronectin-dependent invasion of epithelial cells by Neisseria gonorrhoeae involves alpha (v) integrin receptors. FEBS Lett 424: 84-88.
21. Dehio, M., Gomez-Duarte, O.G., Dehio, C., and Meyer, T.F. (1998) Vitronectin-dependent invasion of epithelial cells by Neisseria gonorrhoeae involves alpha (v) integrin recep- tors. FEBS Lett 424: 84-88.
22. Dempsey, E.C., Newton, A.C., Mochly-Rosen, D., Fields, A.P., Reyland, M.E., Insel, P.A., and Messing, R.O. (2000) Protein kinase C isozymes and the regulation of diverse cell responses. Am J Physiol Lung Cell Mol Physiol 279: L429-L438.
23. Dersch, P., and Isberg, R.R. (1999) A region of the Yersinia pseudotuberculosis invasin protein enhances integrin- mediated uptake into mammalian cells and promotes self association. EMBO J 18: 1199-1213.
24. Eitel, J., and Dersch, P. (2002) The YadA protein of Yersinia pseudotuberculosis mediates high-efficiency uptake into human cells under environmental conditions in which invasin is repressed. Infect Immun 70: 4880-4891.
25. Eitel, J., Heise, T., Thiesen, U., and Dersch, P. (2005) 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.
26. Etienne-Manneville, S., and Hall, A. (2002) Rho GTPases in cell biology. Nature 420: 629-635.
27. Falasca, M., Logan, S.K., Lehto, V.P., Baccante, G., Lemmon, M.A., and Schlessinger, J. (1998) Activation of phospholipase C gamma by PI 3-kinase-induced PH domain-mediated membrane targeting. EMBO J 17: 414- 422.
28. Farhadi, A., Keshavarzian, A., Ranjbarab, Z., Fields, J.Z., and Banan, A. (2006) The role of protein kinase C isoforms in modulating injury and repair of the intestinal barrier. J Pharmacol Exp Ther 316: 1-7.
29. Freissler, E., Meyer auf der Heyde, A., David, G., Meyer, T.F., and Dehio, C. (2000) Syndecan-1 and syndecan-4 can mediate the invasion of OpaHSPG-expressing Neisseria gonorrhoeae into epithelial cells. Cell Microbiol 2: 69-82.
30. Gratacap, M.P., Payrastre, B., Viala, C., Mauco, G., Plantavid, M., and Chap, H. (1998) Phosphatidylinositol 3,4,5- trisphosphate-dependent stimulation of phospholipase C-gamma2 is an early key event in FcgammaRIIA- mediated activation of human platelets. J Biol Chem 273: 24314-24321.
31. Grutzkau, A., Hanski, C., Hahn, H., and Riecken, E.O. (1990) Involvement of M cells in the bacterial invasion of Peyer's patches: a common mechanism shared by Yersinia enterocolitica and other enteroinvasive bacteria. Gut 31: 1011- 1015.
32. Heise, T., and Dersch, P. (2006) Identification of a domain in Yersinia virulence factor YadA that is crucial for extracellular matrix-specific cell adhesion and uptake. Proc Natl Acad Sci USA 103: 3375-3380.
33. Hilpela, P., Vartiainen, M.K., and Lappalainen, P. (2004) Regulation of the actin cytoskeleton by PI(4,5),P2 and PI(3,4,5), P3. Curr Top Microbiol Immunol 282: 117- 163.
34. Huang, F.C., Li, Q., and Cherayil, B.J. (2005) A phosphatidyl- inositol-3-kinase-dependent anti-inflammatory pathway activated by Salmonella in epithelial cells. FEMS Microbiol Lett 243: 265-270.
35. Hudson, K.J., Bliska, J.B., and Bouton, A.H. (2005) Distinct mechanisms of integrin binding by Yersinia pseudotuber- culosis adhesins determine the phagocytic response of host macrophages. Cell Microbiol 7: 1474-1489.
36. Iden, S., and Collard, J.G. (2008) Crosstalk between small GTPases and polarity proteins in cell polarization. Nat Rev Mol Cell Biol 9: 846-859.
37. Isberg, R.R., Voorhis, D.L., and Falkow, S. (1987) Identification of invasin: a protein that allows enteric bacteria to penetrate cultured mammalian cells. Cell 50: 769-778.
38. Isberg, R.R., Hamburger, Z., and Dersch, P. (2000) Signaling and invasin-promoted uptake via integrin receptors. Microbes Infect 2: 793-801.
39. Jones, N.P., and Katan, M. (2007) Role of phospholipase Cgamma1 in cell spreading requires association with a beta-Pix/GIT1-containing complex, leading to activation of Cdc42 and Rac1. Mol Cell Biol 27: 5790-5805
40. Katan, M. (2005) New insights into the families of PLC enzymes: looking back and going forward. Biochem J 391: e7-e9.
41. Kenny, B., and Finlay, B.B. (1997) Intimin-dependent binding of enteropathogenic Escherichia coli to host cells triggers novel signaling events, including tyrosine phosphorylation of phospholipase C-gamma1. Infect Immun 65: 2528- 2536.
42. Kierbel, A., Gassama-Diagne, A., Mostov, K., and Engel, J.N. (2005) The phosphoinositol-3-kinase-protein kinase B/Akt pathway is critical for Pseudomonas aeruginosa strain PAK internalization. Mol Biol Cell 16: 2577-2585.
43. Knodler, L.A., Finlay, B.B., and Steele-Mortimer, O. (2005) The Salmonella effector protein SopB protects epithelial cells from apoptosis by sustained activation of Akt. J Biol Chem 280: 9058-9064.
44. Lee, S.B., and Rhee, S.G. (1995) Significance of PIP2 hydrolysis and regulation of phospholipase C isozymes. Curr Opin Cell Biol 7: 183-189.
45. Logie, L., Ruiz-Alcaraz, A.J., Keane, M., Woods, Y.L., Bain, J., Marquez, R., et al. (2007) Characterization of a protein kinase B inhibitor in vitro and in insulin-treated liver cells. Diabetes 56: 2218-2227.
46. Luo, B.H., Carman, C.V., and Springer, T.A. (2007) Structural basis of integrin regulation and signaling. Annu Rev Immunol 25: 619-647.
47. Lutz, R., and Bujard, H. (1997) Independent and tight regulation of transcriptional units in Escherichia coli via the LacR/O, the TetR/O and AraC/I1-I2 regulatory elements. Nucleic Acids Res 25: 1203-1210.
48. McGee, K., Zettl, M., Way, M., and Fallman, M. (2001) A role for N-WASP in invasin-promoted internalisation. FEBS Lett 509: 59-65.
49. Maina, C.V., Riggs, P.D., Grandea, A.G., III, Slatko, B.E., Moran, L.S., Tagliamonte, J.A., et al. (1988) An Escherichia coli vector to express and purify foreign proteins by fusion to and separation from maltose-binding protein. Gene 74: 365-373.
50. Manning, B.D., and Cantley, L.C. (2007) AKT/PKB signaling: navigating downstream. Mansell, A., Khelef, N., Cossart, P., and O'Neill, L.A. (2001) Internalin B activates nuclear factor-kappa B via Ras, phosphoinositide 3-kinase, and Akt. J Biol Chem 276: 43597-43603.
51. Marra, A., and Isberg, R.R. (1996) Analysis of the role of invasin during Yersinia pseudotuberculosis infection of mice. Ann N Y Acad Sci 797: 290-292.
52. Mellor, H., and Parker, P.J. (1998) The extended protein kinase C superfamily. Biochem J 332 (2): 281-292.
53. Ng, T., Parsons, M., Hughes, W.E., Monypenny, J., Zicha, D., Gautreau, A., et al. (2001) Ezrin is a downstream effector of trafficking PKC-integrin complexes involved in the control of cell motility. EMBO J 20: 2723-2741.
54. Owen, K.A., Thomas, K.S., and Bouton, A.H. (2007) The differential expression of adhesins determines the requirement for FAK and/or Pyk2 during bacterial phagocytosis by macrophages. Cell Microbiol 9: 596-609.
55. Parsons, J.T. (2003) Focal adhesion kinase: the first ten years. J 1800
56. Pendaries, C., Tronchere, H., Arbibe, L., Mounier, J., Gozani, O., Cantley, L., et al. (2006) PtdIns5P activates the host cell PI3-kinase/Akt pathway during Shigella flexneri infection. EMBO J 25: 1024-1034.
57. Prasadarao, N.V., Srivastava, P.K., Rudrabhatla, R.S., Kim, K.S., Huang, S.H., and Sukumaran, S.K. (2003) Cloning and expression of the Escherichia coli K1 outer membrane protein A receptor, a gp96 homologue. Infect Immun 71: 1680-1688.
58. Rameh, L.E., Rhee, S.G., Spokes, K., Kazlauskas, A., Cantley, L.C., and Cantley, L.G. (1998) Phosphoinositide 3-kinase regulates phospholipase Cgamma-mediated calcium signaling. J Biol Chem 273: 23750-23757.
59. Rebecchi, M.J., and Pentyala, S.N. (2000) Structure, function, and control of phosphoinositide-specific phospholipase C. Physiol Rev 80: 1291-1335.
60. Rhee, S.G. (2001) Regulation of phosphoinositide-specific phospholipase C. Annu Rev Biochem 70: 281-312.
61. Ridley, A.J. (2006) Rho GTPases and actin dynamics in membrane protrusions and vesicle trafficking. Trends Cell Biol 16: 522-529.
62. Rottner, K., Stradal, T.E., and Wehland, J. (2005) Bacteriahost-cell interactions at the plasma membrane: stories on actin cytoskeleton subversion. Dev Cell 9: 3-17.
63. Rubsamen-Waigmann, H., Pfutzner, A., and Biesert, L. (1993) [Effect of antiviral agents]. Immun Infekt 21: 106- 110.
64. Scharenberg, A.M., and Kinet, J.P. (1998) PtdIns-3,4,5-P3: a regulatory nexus between tyrosine kinases and sustained calcium signals. Cell 94: 5-8.
65. Schulte, R., Kerneis, S., Klinke, S., Bartels, H., Preger, S., Kraehenbuhl, J.P., et al. (2000) Translocation of Yersinia enterocolitica across reconstituted intestinal epithelial monolayers is triggered by Yersinia invasin binding to beta1 integrins apically expressed on M-like cells. Cell Microbiol 2: 173-185.
66. Sidhu, G., Li, W., Laryngakis, N., Bishai, E., Balla, T., and Southwick, F. (2005) Phosphoinositide 3-kinase is required for intracellular Listeria monocytogenes actin-based motility and filopod formation. J Biol Chem 280: 11379- 11386.
67. Singer, W.D., Brown, H.A., and Sternweis, P.C. (1997) Regulation of eukaryotic phosphatidylinositol-specific phospholipase C and phospholipase D. Annu Rev Biochem 66: 475-509.
68. Steele-Mortimer, O., Knodler, L.A., Marcus, S.L., Scheid, M.P., Goh, B., Pfeifer, C.G., et al. (2000) Activation of Akt/protein kinase B in epithelial cells by the Salmonella typhimurium effector sigD. J Biol Chem 275: 37718- 37724.
69. Strauch, E., Voigt, I., Broll, H., and Appel, B. (2000) Use of a plasmid of a Yersinia enterocolitica biogroup 1A strain for the construction of cloning vectors. J Biotechnol 79: 63- 72.
70. Sukumaran, S.K., and Prasadarao, N.V. (2002) Regulation of protein kinase C in Escherichia coli K1 invasion of human brain microvascular endothelial cells. J Biol Chem 277: 12253-12262.
71. Sukumaran, S.K., McNamara, G., and Prasadarao, N.V. (2003) Escherichia coli K-1 interaction with human brain micro-vascular endothelial cells triggers phospholipase C-gamma1 activation downstream of phosphatidylinositol 3-kinase. J Biol Chem 278: 45753-45762.
72. Takenawa, T., and Itoh, T. (2001) Phosphoinositides, key molecules for regulation of actin cytoskeletal organization and membrane traffic from the plasma membrane. Biochim Biophys Acta 1533: 190-206.
73. Tolias, K.F., Hartwig, J.H., Ishihara, H., Shibasaki, Y., Cantley, L.C., and Carpenter, C.L. (2000) Type Ialpha phosphatidylinositol-4-phosphate 5-kinase mediates Racdependent actin assembly. Curr Biol 10: 153-156.
74. Tran Van Nhieu, G., and Isberg, R.R. (1993) Bacterial internalization mediated by beta 1 chain integrins is determined by ligand affinity and receptor density. EMBO J 12: 1887- 1895.
75. Tvorogov, D., Wang, X.J., Zent, R., and Carpenter, G. (2005) Integrin-dependent PLC-gamma1 phosphorylation mediates fibronectin-dependent adhesion. J Cell Sci 118: 601- 610.
76. Vanhaesebroeck, B., and Alessi, D.R. (2000) The PI3K-PDK1 connection: more than just a road to PKB. Biochem J 346 (Part 3): 561-576.
77. Wang, B., Yurecko, R.S., Dedhar, S., and Cleary, P.P. (2006) Integrin-linked kinase is an essential link between integrins and uptake of bacterial pathogens by epithelial cells. Cell Microbiol 8: 257-266.
78. Weidow, C.L., Black, D.S., Bliska, J.B., and Bouton, A.H. (2000) CAS/Crk signalling mediates uptake of Yersinia into human epithelial cells. Cell Microbiol 2: 549-560.
79. Wong, K.W., and Isberg, R.R. (2003) Arf6 and phosphoinositol-4-phosphate-5-kinase activities permit bypass of the Rac1 requirement for beta1 integrinmediated bacterial uptake. J Exp Med 198: 603-614.
80. Wong, K.W., and Isberg, R.R. (2005) Yersinia pseudotuberculosis spatially controls activation and misregulation of host cell Rac1. PLoS Pathog 1: e16.
81. Wong, K.W., Mohammadi, S., and Isberg, R.R. (2008) The polybasic region of rac1 modulates bacterial uptake independently of self association and membrane targeting. J Biol Chem 283: 35954-35965.
82. Yu, H., Fukami, K., Itoh, T., and Takenawa, T. (1998) Phosphorylation of phospholipase Cgamma1 on tyrosine residue 783 by platelet-derived growth factor regulates reorganization of the cytoskeleton. Exp Cell Res 243: 113-122