Conversion of PtdIns(4, 5)P2 into PtdIns(5)P by the S.flexneri effector IpgD reorganizes host cell morphology

EMBO Journal

Volumn 21, Issue 19, 2002, Pages 5069-5078

  Niebuhr, Kirsten ^a   Giuriato, Sylvie ^a   Pedron, Thierry ^a   Philpott, Dana J ^a   Gaits, Frédérique ^a   Sable, Julia ^a   Sheetz, Michael P ^a   Parsot, Claude ^a   Sansonetti, Philippe J ^a   Payrastre, Bernard ^a  

^a CHU PURPAN   (France)

Author keywords

Bacterial entry; IpgD; Phosphoinositides; S.flexneri

Indexed keywords

INOSITOL 4 PHOSPHATASE; INOSITOL DERIVATIVE; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; PHOSPHATIDYLINOSITOL 5 MONOPHOSPHATE; PHOSPHOINOSITIDE PHOSPHATASE; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

ACTIN FILAMENT; ARTICLE; BACTERIAL INFECTION; BACTERIAL VIRULENCE; CELL MEMBRANE; CELL STRUCTURE; CHROMOSOME TRANSLOCATION; CONTROLLED STUDY; DEPHOSPHORYLATION; EPITHELIUM CELL; EUKARYOTIC CELL; FEMALE; GENETIC TRANSFECTION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HOST CELL; HUMAN; HUMAN CELL; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; SHIGELLA FLEXNERI;

1-PHOSPHATIDYLINOSITOL 3-KINASE; 3T3 CELLS; ANIMALS; BACTERIAL PROTEINS; CELL ADHESION; ENZYME ACTIVATION; HELA CELLS; HUMANS; KINETICS; MICE; MUTAGENESIS, SITE-DIRECTED; PHOSPHATIDYLINOSITOL 4,5-DIPHOSPHATE; PHOSPHATIDYLINOSITOL PHOSPHATES; PHOSPHORIC MONOESTER HYDROLASES; POLYMERASE CHAIN REACTION; RECOMBINANT FUSION PROTEINS; SHIGELLA FLEXNERI; TRANSFECTION;

BACTERIA (MICROORGANISMS); EUKARYOTA; NEGIBACTERIA; SHIGELLA; SHIGELLA FLEXNERI;

EID: 18644379244     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/cdf522     Document Type: Article

References (40)

1. Adam, T., Arpin, M., Prévost, M.-C., Gounon, P. and Sansonetti, P.J. (1995) Cytoskeletal rearrangements and the functional role for T-plastin during entry of Shigella flexneri into HeLa cells. J. Cell Biol., 129, 367-381.
2. Allaoui, A., Ménard, R., Sansonetti, P.J. and Parsot, C. (1993) Characterization of the Shigella flexneri ipgD and ipgF genes, which are located in the proximal part of the mxi locus. Infect. Immun., 61, 1707-1714.
3. Azuma, T., Witke, W., Stossel, T.P., Hartwig J.H. and Kwiatkowski, D.J. (1998) Gelsolin is a downstream effector of rac for fibroblast motility. EMBO J., 17, 1362-1370.
4. Bligh, E.G. and Dyer, W.J. (1959) A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol., 37, 911-919.
5. Blondeau, F., Laporte, J., Bodin, S., Superti-Furga, G., Payrastre, B. and Mandel, J.L. (2000) Myotubularin, a phosphatase deficient in myotubular myopathy, acts on phosphatidylinositol 3-kinase and phosphatidylinositol 3-phosphate pathway. Hum. Mol. Genet., 9, 2223-2229.
6. Choquet, D., Felsenfeld, D.P. and Sheetz, M.P. (1997) Extracellular matrix rigidity causes strengthening of integrin-cytoskeleton linkages. Cell, 88, 39-48.
7. Clerc, P. and Sansonetti, P.J. (1987) Entry of Shigella flexneri into HeLa cells: evidence for directed phagocytosis involving actin polymerization and myosin accumulation. Infect. Immun., 55, 2681-2688.
8. Czech, M.P. (2000) PIP2 and PIP3: complex roles at the cell surface. Cell, 100, 603-606.
9. Dai, J. and Sheetz, M.P. (1995) Mechanical properties of neuronal growth cone membranes studied by tether formation with laser optical tweezers. Biophys. J., 68, 988-996.
10. Eckmann, L. et al. (1997) D-Myo-inositol 1, 4, 5, 6-tetrakisphosphate produced in human intestinal epithelial cells in response to Salmonella invasion inhibits phosphoinositide 3-kinase signaling pathways. Proc. Natl Acad. Sci. USA, 94, 14456-14460.
11. Erneux, C., Lemos, M., Verjans, B., Vanderhaeghen, P., Delvaux, A. and Dumont, J.E. (1989) Soluble and particulate Ins(1, 4, 5)P3/Ins(1, 3, 4, 5)P4 5-phosphatase in bovine brain. Eur. J. Biochem., 181, 317-322.
12. Finlay, B.B. and Falkow, S. (1990) Salmonella interactions with polarized human intestinal Caco-2 epithelial cells. J. Infect. Dis., 162, 1096-1106.
13. Francis, C.L., Ryan, T.A., Jones, B.D., Smith, S.J. and Falkow, S. (1993) Ruffles induced by Salmonella and other stimuli direct macropinocytosis of bacteria. Nature, 364, 639-642.
14. Galan, J.E. and Bliska, J.B. (1996) Cross talks between bacterial pathogens and their host cells. Annu. Rev. Cell. Dev. Biol., 12, 221-255.
15. Galyov, E.E., Wood, M.W., Rosquist, R., Mullan, P.B., Watson, P.R., Hedges, S. and Wallis, T.S. (1997) A secreted effector protein of Salmonella dublin is translocated into eukaryotic cells and mediates inflammation and fluid secretion in infected ileal mucosa. Mol. Microbiol., 25, 903-912.
16. Garcia, M.I., Labigne, A. and Le Bouguenec, C. (1994) Nucleotide sequence of the afimbrial-adhesin-encoding afa-3 gene cluster and its translocation via flanking IS1 insertion sequences. J. Bacteriol., 176, 7601-7613.
17. Hinchliffe, K.A. (2000) Intracellular signalling: is PIP2 a messenger too? Curr. Biol., 10, R104-R105.
18. Hinchliffe, K.A., Ciruela, A. and Irvine, R.F. (1998) PIPkins, their substrates and their products: new functions for old enzymes. Biochim. Biophys. Acta, 1436, 87-104.
19. Hong, K.H. and Miller, V.L. (1998) Identification of a novel Salmonella invasion locus homologous to Shigella ipgDE. J. Bacteriol., 180, 1793-1802.
20. Ireton, K., Payrastre, B., Chap, H., Ogawa, W., Sakaue, H., Kasuga, M. and Cossart, P. (1996) A role for phosphoinositide 3-kinase in bacterial invasion. Science, 274, 780-782.
21. Kozma, R., Ahmed, S., Best, A. and Lim, L. (1995) The Ras-related protein Cdc42Hs and bradykinin promote formation of peripheral actin microspikes and filopodia in Swiss 3T3 fibroblasts. Mol. Cell. Biol., 15, 1942-1952.
22. Kuo, S.C. and Sheetz, M.P. (1993) Force of single kinesin molecules measured with optical tweezers. Science, 260, 232-234.
23. Marcus, S.L., Wenk, M.R., Steele-Mortimer, O. and Finlay, B.B. (2001) A synaptogamin-homologous region of Salmonella typhimurium SigD is essential for inositol phosphatase activity and Akt activation. FEBS Lett., 494, 201-207.
24. Mengaud, J., Ohayon, H., Gounon, P., Mège, R.-M. and Cossart, P. (1996) E-cadherin is the receptor for internalin, a surface protein required for entry of Listeria monocytogenes into epithelial cells. Cell, 84, 923-932.
25. Morris, J.B., Hinchliffe, K.A., Ciruela, A., Letcher, A.J. and Irvine, R.F. (2000) Thrombin stimulation of platelets causes an increase in phosphatidylinositol 5-phosphate revealed by mass assay. FEBS Lett., 475, 57-60.
26. Mounier, J., Laurent, V., Hall, A., Fort, P., Carlier, F., Sansonetti, P.J. and Egile, C. (1999) Rho family GTPases control entry of Shigellaflexneri into epithelial cells but not intracellular motility. J. Cell Sci., 112, 2069-2080.
27. Niebuhr, K., Jouihri, N., Allaoui, A., Gounon, P., Sansonetti, P. and Parsot, C. (2000) IpgD, a protein secreted by the type III secretion machinery of Shigella flexneri, is chaperoned by IpgE and implicated in entry focus formation. Mol. Microbiol., 38, 8-19.
28. Norris, F.A., Atkin R.C. and Majerus, P.W. (1997) The cDNA cloning and characterization of inositol polyphosphate 4-phosphatase type II. Evidence for conserved alternative splicing in the 4-phosphatase family. J. Biol. Chem., 272, 23859-23864.
29. Norris, F.A., Wilson, M.P., Wallis, T.S., Galyov, E.E. and Majerus, P.W. (1998) SopB, a protein required for virulence of Salmonella dublin, is an inositol phosphate phosphatase. Proc. Natl Acad. Sci. USA, 95, 14057-14059.
30. Odorizzi, G., Babst, M. and Emr, S.D. (2000) Phosphoinositide signaling and the regulation of membrane trafficking in yeast. Trends Biochem. Sci., 25, 229-235.
31. Payrastre, B., Gironcel, D., Plantavid, M., Mauco, G., Breton, M. and Chap, H. (1994) Phosphoinositide 3-phosphatase segregates from phosphatidylinositol 3-kinase in EGF-stimulated A431 cells and fails to in vitro hydrolyze phosphatidylinositol (3, 4, 5)trisphosphate. FEBS Lett., 341, 113-118.
32. Payrastre, B., Missy, K., Giuriato, S., Bodin, S., Plantavid, M. and Gratacap, M.P. (2001) Phosphoinositides: key players in cell signalling, in time and space. Cell Signal., 13, 377-387.
33. Rameh, L.E., Tolias, K.F., Duckworth, B.C. and Cantley, L.C. (1997) A new pathway for synthesis of phosphatidylinositol-4, 5-bisphosphate. Nature, 390, 192-196.
34. Raucher, D., Stauffer, T., Chen, W., Shen, K., Guo, S., York, J.D., Sheetz, M.P. and Meyer, T. (2000) Phosphatidylinositol 4, 5-bisphosphate functions as a second messenger that regulates cytoskeleton-plasma membrane adhesion. Cell, 100, 221-228.
35. Sbrissa, D., Ikonomov, O.C. and Shisheva, A. (1999) PIKfyve, a mammalian ortholog of yeast Fab1p lipid kinase, synthesizes 5- phosphoinositides. J. Biol. Chem., 274, 21589-21597.
36. Sechi, A.S. and Wehland, J. (2000) The actin cytoskeleton and plasma membrane connection: PtdIns(4, 5)P2 influences cytoskeletal protein activity at the plasma membrane. J. Cell Sci., 113, 3685-3695.
37. Toker, A. (1998) The synthesis and cellular roles of phosphatidylinositol 4, 5-bisphosphate. Curr. Opin. Cell Biol., 10, 254-261.
38. Tolias, K.F., Rameh, L.E., Ishihara, H., Shibasaki, Y., Chen, J., Prestwich, G.D., Cantley, L.C. and Carpenter, C.L. (1998) Type I phosphatidylinositol-4-phosphate 5-kinases synthesize the novel lipids phosphatidylinositol 3, 5-bisphosphate and phosphatidylinositol 5-phosphate. J. Biol. Chem., 273, 18040-18046.
39. Tran Van Nhieu, G., Caron, E., Hall, A. and Sansonetti, P.J. (1999) IpaC induces actin polymerization and filopodia formation during Shigella entry into epithelial cells. EMBO J., 18, 3249-3262.
40. Van Gijsegem, F., Genin, S. and Boucher, C. (1993) Conservation of secretion pathways for pathogenicity determinants of plant and animal bacteria. Trends Microbiol., 1, 175-180.