Subversion of phosphoinositide metabolism by intracellular bacterial pathogens

Nature Cell Biology

Volumn 6, Issue 11, 2004, Pages 1026-1033

  Pizarro Cerdá, Javier ^a   Cossart, Pascale ^a  

^a INSTITUT PASTEUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHATIDYLINOSITIDE;

BACTERIAL INFECTION; BACTERIAL VIRULENCE; CELL MATURATION; CELL MEMBRANE; CELL METABOLISM; CELL MOTILITY; CELL PROLIFERATION; CELL TRANSPORT; CELLULAR DISTRIBUTION; ESCHERICHIA COLI; HOST CELL; HUMAN; LEGIONELLA PNEUMOPHILA; LIPOGENESIS; METABOLIC ACTIVATION; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PHOSPHOINOSITIDE METABOLISM; PRIORITY JOURNAL; REVIEW; YERSINIA;

1-PHOSPHATIDYLINOSITOL 4-KINASE; BACTERIA; BACTERIAL PHYSIOLOGY; PHAGOCYTOSIS; PHOSPHATIDYLINOSITOLS; PHOSPHORIC MONOESTER HYDROLASES; SIGNAL TRANSDUCTION;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; LEGIONELLA; LEGIONELLA PNEUMOPHILA; MYCOBACTERIUM; MYCOBACTERIUM TUBERCULOSIS; YERSINIA;

EID: 7944228843     PISSN: 14657392     EISSN: None     Source Type: Journal    
DOI: 10.1038/ncb1104-1026     Document Type: Review

References (79)

1. Cossart, P. & Sansonetti, P. J. Bacterial invasion: the paradigms of enteroinvasive pathogens. Science 304, 242-248 (2004).
2. Meresse, S. et al. Controlling the maturation of pathogen-containing vacuoles: a matter of life and death. Nature Cell Biol. 1, 183-188 (1999).
3. Brumell, J. H. & Grinstein, S. Role of lipid-mediated signal transduction in bacterial internalization. Cell. Microbiol. 5, 287-297 (2003).
4. Botelho, R. J., Scott, C. C. & Grinstein, S. Phosphoinositide involvement in phagocytosis and phagosome maturation. Curr. Top. Microbiol. Immunol. 282, 1-30 (2004).
5. Payrastre, B. et al. Phosphoinositides: key players in cell signalling, in time and space. Cell. Signal. 13, 377-387 (2001).
6. 2+-independent F-actin assembly and disassembly during Fc receptor-mediated phagocytosis in mouse macrophages. J. Cell Biol. 113, 757-767 (1991).
7. Yin, H. L. & Janmey, P. A. Phosphoinositide regulation of the actin cytoskeleton. Annu. Rev. Physiol. 65, 761-789 (2003).
8. Defacque, H. et al. Phosphoinositides regulate membrane-dependent actin assembly by latex bead phagosomes. Mol. Biol. Cell 13, 1190-1202 (2002).
9. Lemmon, M. A. Phosphoinositide recognition domains. Traffic 4, 201-213 (2003).
10. Botelho, R. J. et al. Localized biphasic changes in phosphatidylinositol-4,5-bisphosphate at sites of phagocytosis. J. Cell Biol. 151, 1353-1368 (2000).
11. Coppolino, M. G. et al. Inhibition of phosphatidylinositol-4-phosphate 5-kinase lα impairs localized actin remodeling and suppresses phagocytosis. J. Biol. Chem. 277, 43849-43857 (2002).
12. Cox, D. & Greenberg, S. Phagocytic signaling strategies: Fcγ-receptor-mediated phagocytosis as a model system. Semin. Immunol. 13, 339-345 (2001).
13. Vieira, O. V. et al. Distinct roles of class I and class III phosphatidylinositol 3-kinases in phagosome formation and maturation. J. Cell Biol. 155, 19-25 (2001).
14. Marshall, J. G. et al. Restricted accumulation of phosphatidylinositol 3-kinase products in a plasmalemal subdomain during Fc γ receptor-mediated phagocytosis. J. Cell Biol. 153, 1369-1380 (2001).
15. Cox, D., Tseng, C. C., Bjekic, G. & Greenberg S. A requirement for phosphatidylinositol 3-kinase in pseudopod extension. J. Biol. Chem. 274, 1240-1247 (1999).
16. 3. Curr. Top. Microbiol. Immunol. 282, 117-163 (2004).
17. Cox, D., Dale, B. M., Kashiwada, M., Helgason, C. D. & Greenberg, S. A regulatory role for Src homology 2 domain-containing inositol 5′-phosphatase (SHIP) in phagocytosis mediated by Fc γ receptors and complement receptor 3 ((αMβ2; CD11b /CD18). J. Exp. Med. 193, 61-71 (2001).
18. Cao, X. et al. The inositol 3-phosphatase PTEN negatively regulates Fc γ receptor signaling, but supports Toll-like receptor 4 signaling in murine peritoneal macrophages. J. Immunol. 172, 4851-4857 (2004).
19. Ellson, C. D. et al. Phosphatidylinositol 3-phosphate is generated in phagosomal membranes. Curr. Biol. 11, 1631-1635 (2001).
20. Simonsen, A. et al. EEA1 links PI(3)K function to Rab5 regulation of endosome fusion. Nature 394, 494-498 (1998).
21. Raiborg, C. et al. Hrs sorts ubiquitinated proteins into clathrin-coated microdomains of early endosomes. Nature Cell Biol. 4, 394-398 (2002).
22. Zhan, Y., Virbasius, J. V., Song, X., Pomerleau, D. P. & Zhou GW. The p40phox and p47phox PX domains of NADPH oxidase target cell membranes via direct and indirect recruitment by phosphoinositides. J. Biol. Chem. 8, 4512-4518 (2002).
23. Worby, C. A. & Dixon, J. E. Sorting out the cellular functions of sorting nexins. Nature Rev. Mol. Cell Biol. 3, 919-931 (2002).
24. Cozier, G. E. et al. The phox homology (PX) domain-dependent, 3-phosphoinositide-mediated association of sorting nexin-1 with an early sorting endosomal compartment is required for its ability to regulate epidermal growth factor receptor degradation. J. Biol. Chem. 277, 48730-48736 (2002).
25. Henry, R. M., Hoppe, A. D., Joshi, N. & Swanson, J. A. The uniformity of phagosome maturation in macrophages. J. Cell Biol. 164, 185-189 (2004).
26. Putzker, M., Sauer, H. & Sobe, D. Plague and other human infections caused by Yersinia species. Clin. Lab. 47, 453-466 (2001).
27. Isberg, R. R. & Leong, J. M. Multiple β 1 chain integrins are receptors for invasin, a protein that promotes bacterial penetration into mammalian cells. Cell 60, 861-871 (1990).
28. Alrutz, M. A. et al. 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 (2001).
29. Wong, K. W. & Isberg, R. R. Arf6 and phosphoinositol-4-phosphate-5-kinase activities permit bypass of the Rac1 requirement for β1 integrin-mediated bacterial uptake. J. Exp. Med. 198, 603-614 (2003).
30. Brown, F. D., Rozelle, A. L., Yin, H. L., Balla, T. & Donaldson, J. G. Phosphatidylinositol 4,5-bisphosphate and Arf6-regulated membrane traffic. J. Cell Biol. 154, 1007-1017 (2001).
31. Derrien, V. et al. A conserved C-terminal domain of EFA6-family ARF6-guanine nucleotide exchange factors induces lengthening of microvilli-like membrane protrusions. J. Cell Sci. 115, 2867-2879 (2002).
32. Niedergang, F., Colucci-Guyon, E., Dubois, T., Raposo, G. & Chavrier, P. ADP ribosylation factor 6 is activated and controls membrane delivery during phagocytosis in macrophages. J. Cell Biol. 161, 1143-1150 (2003).
33. Dussurget, O., Pizarro-Cerdá, J. & Cossart, P. Molecular determinants of Listeria monocytogenes virulence. Annu. Rev. Microbiol. 58, 587-610 (2004).
34. Mengaud, J., Ohayon, H., Gounon, P., Mege, R.-M. & Cossart P. E-cadherin is the receptor for internalin, a surface protein required for entry of L. monocytogenes into epithelial cells. Cell 84, 923-932 (1996).
35. Shen, Y., Naujokas, M., Park, M. & Ireton K. InIB-dependent internalization of Listeria is mediated by the Met receptor tyrosine kinase. Cell 103, 501-510 (2000).
36. Ireton, K. et al. A role for phosphoinositide 3-kinase in bacterial invasion. Science 274, 780-782 (1996).
37. Ireton, K., Payrastre, B. & Cossart, P. The Listeria monocytogenes protein InIB is an agonist of mammalian phosphoinositide 3-kinase. J. Biol. Chem. 274, 17025-17032 (1999).
38. Maulik, G. et al. Activated c-Met signals through PI3K with dramatic effects on cytoskeletal functions in small cell lung cancer. J. Cell. Mol. Med. 6, 539-553 (2002).
39. Banerjee, M. et al. GW domains of the Listeria monocytogenes invasion protein InIB are required for potentiation of Met activation. Mol. Microbiol. 52, 257-2571 (2004).
40. Berne, H. et al. A role for cofilin and LIM kinase in Listeria-induced phagocytosis. J. Cell Biol. 155, 101-112 (2001).
41. Seveau, S., Bierne, H., Giroux, S., Prevost, M. C. & Cossart, P. Role of lipid rafts in E cadherin- and HGF-R/Met-mediated entry of Listeria monocytogenes into host cells. J. Cell Biol. 166, 743-753 (2004).
42. Bierne, H. et al. The invasion protein InIB from Listeria monocytogenes activates PLC-γ1 downstream from PI 3-kinase. Cell. Microbiol. 2, 465-476 (2000).
43. Alvarez-Dominguez, C., Barbieri, A. M., Beron, W., Wandinger-Ness, A. & Stahl, P. D. Phagocytosed live Listeria monocytogenes influences Rab5-regulated in vitro phagosome-endosome fusion. J. Biol. Chem. 271, 13834-13843 (1996).
44. Mansell, A., Khelef, N., Cossart, P. & O'Neill, L. A. Internalin B activates nuclear factor-kappa B via Ras, phosphoinositide 3-kinase, and Akt. J. Biol. Chem. 276, 43597-43603 (2001).
45. Martinez, J. J., Mulvey, M. A., Schilling, J. D., Pinkner, J. S. & Hultgren, S. J. Type 1 pilus-mediated bacterial invasion of bladder epithelial cells. EMBO J. 19, 2803-2812 (2000).
46. Min, G. et al. Localization of uroplakin la, the urothelial receptor for bacterial adhesin FimH, on the six inner domains of the 16 nm urothelial plaque particle. J. Mol. Biol. 317, 697-706 (2002).
47. Duncan, M. J., Li, G., Shin, J. S., Carson, J. L. & Abraham, S. N. Bacterial penetration of bladder epithelium through lipid rafts. J. Biol. Chem. 279, 18944-18951 (2004).
48. Philpott, D. J., Edgeworth, J. D. & Sansonetti P. J. The pathogenesis of Shigella flexneri infection: lessons from in vitro and in vivo studies. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 355, 575-586 (2000).
49. Hueck, C. J. Type III protein secretion systems in bacterial pathogens of animals and-plants. Microbiol. Mol. Biol. Rev. 62, 379-433 (1998).
50. Tran Van Nhieu, G., Caron, E., Hall, A. & Sansonetti, P. J. IpaC induces actin polymerization and filopodia formation during Shigella entry into epithelial cells. EMBO J. 18, 3249-3262 (1999).
51. Kuwae, A. et al. Shigella invasion of macrophage requires the insertion of IpaC into the host plasma membrane. Functional analysis of IpaC. J. Biol. Chem. 276, 32230-32239 (2001).
52. Niebuhr, K. et al. Conversion of PtdIns(4,5)P(2) into PtdIns(5)P by the S. flexneri effector IpgD reorganizes host cell morphology. EMBO J. 21, 5069-5078 (2002).
53. Rameh, L. E., Tolias, K. F., Duckworth, B. C. & Cantley, L. C. A new pathway for synthesis of phosphatidylinositol-4,5-bisphosphate. Nature 390, 192-196 (1997).
54. Raucher, D. et al. Phosphatidylinositol 4,5-bisphosphate functions as a second messenger that regulates cytoskeleton-plasma membrane adhesion. Cell 100, 221-228 (2000).
55. House, D., Bishop, A., Parry, C., Dougan, G. & Wain, J. Typhoid fever: pathogenesis and disease. Curr. Opin. Infect. Dis. 14, 573-578 (2001).
56. Norris, F. A., Wilson, M. P., Wallis, T. S., Galyov, E. E., & Majerus, P. W. SopB, a protein required for virulence of Salmonella dublin, is an inositol phosphate phosphatase. Proc. Natl Acad. Sci. USA 95, 14057-14059 (1998).
57. Zhou, D., Chen, L. M., Hernandez, L., Shears, S. B. & Galan, J. E. A Salmonella inositol polyphosphatase acts in conjunction with other bacterial effectors to promote host cell actin cytoskeleton rearrangements and bacterial internalization. Mol. Microbiol. 39, 248-259 (2001).
58. 2 by bacterial SigD promotes membrane fission during invasion by Salmonella. Nature Cell Biol. 4, 766-773 (2002).
59. Pattni, K., Jepson, M., Stenmark, H. & Banting G. A PtdIns(3)P-specific probe cycles on and off host cell membranes during Salmonella invasion of mammalian cells. Curr. Biol. 11, 1636-1642 (2001).
60. Scott, C. C., Cuellar-Mata, P., Matsuo, T., Davidson, H. W. & Grinstein, S. Role of 3-phosphoinositides in the maturation of Salmonella-containing vacuoles within host cells. J. Biol. Chem. 277, 12770-12776 (2002).
61. Chua, J. & Deretic, V. Mycobacterium tuberculosis reprograms waves of phosphatidylinositol 3-phosphate on phagosomal organelles. J. Biol. Chem. 279, 36982-36989 (2004).
62. Hernandez, L. D., Hueffer, K., Wenk, M. R. & Galan, J. E. Salmonella modulates vesicular traffic by altering phosphoinositide metabolism. Science 304, 1805-1807 (2004).
63. Steele-Mortimer, O., Meresse, S., Gorvel, J. P., Toh, B. H. & Finlay, B. B. Biogenesis of Salmonella typhimurium-containing vacuoles in epithelial cells involves interactions with the early endocytic pathway. Cell. Microbiol. 1, 33-49 (1999).
64. Steele-Mortimer, O. et al. Activation of Akt/protein kinase B in epithelial cells by the Salmonella typhimurium effector sigD. J. Biol. Chem. 275, 37718-37724 (2000).
65. Marcus, S. L., Wenk, M. R., Steele-Mortimer, O. & Finlay, B. B. A synaptojanin-homologous region of Salmonella typhimurium SigD is essential for inositol phosphatase activity and Akt activation. FEBS Lett. 494, 201-207 (2001).
66. Clarke, S. C., Haigh, R. D., Freestone, P. P. & Williams, P.H Virulence of enteropathogenic Escherichia coli, a global pathogen. Clin. Microbiol. Rev. 16, 365-378 (2003).
67. Rosenshine, I. et al. A pathogenic bacterium triggers epithelial signals to form a functional bacterial receptor that mediates actin pseudopod formation. EMBO J. 15, 2613-2624 (1996).
68. Celli, J., Olivier, M. & Finlay, B. B. Enteropathogenic Escherichia coli mediates antiphagocytosis through the inhibition of PI 3-kinase-dependent pathways. EMBO J. 20, 1245-1258 (2001).
69. Smith, I. Mycobacterium tuberculosis pathogenesis and molecular determinants of virulence. Clin. Microbiol. Rev. 16, 463-496 (2003).
70. Sturgill-Koszycki, S. et al. Lack of acidification in Mycobacterium phagosomes produced by exclusion of the vesicular proton-ATPase. Science 263, 678-681 (1994).
71. Clemens, D. L. & Horwitz, M. A. Characterization of the Mycobacterium tuberculosis phagosome and evidence that phagosomal maturation is inhibited. J. Exp. Med. 181, 257-270 (1995).
72. 2+/calmodulin-P13K hVPS34 cascade. J. Exp. Med. 198, 653-659 (2003).
73. Fratti, R. A., Chua, J., Vergne, I. & Deretic, V. Mycobacterium tuberculosis glycosylated phosphatidylinositol causes phagosome maturation arrest. Proc. Natl Acad. Sci. USA 100, 5437-5442 (2003).
74. Viera, O. V. et al. Acquisition of Hrs, an essential component of phagosomal maturation, is impaired by mycobacteria. Mol. Cell. Biol. 24, 4593-4604 (2004).
75. Vergne, I. et al. Mycobacterium tuberculosis phagosome maturation arrest: mycobacterial phosphatidylinositol analog phosphatidylinostol mannoside stimulates early endosomal fusion. Mol. Biol. Cell 15, 751-760 (2004).
76. Anes, E. et al. Selected lipids activate phagosome actin assembly and maturation resulting in killing of pathogenic mycobacteria. Nature Cell Biol. 5, 793-802 (2003).
77. Du, G. et al. Regulation of phospholipase D1 subcellular cycling through coordination of multiple membrane association motifs. J. Cell Biol. 162, 305-315 (2003).
78. Gozani, O. et al. The PHD finger of the chromatin-associated protein ING2 functions as a nuclear phosphoinositide receptor. Cell 114, 99-111 (2003).
79. Clarke, J. H. Lipid signalling: picking out the PIPs. Curr. Biol. 13, R815-R817 (2003).