Pathogenic trickery: Deception of host cell processes

Nature Reviews Molecular Cell Biology

Volumn 2, Issue 8, 2001, Pages 578-588

  Knodler, Leigh A ^a   Celli, Jean ^a   Brett Finlay, B ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA (MICROORGANISMS);

BACTERIAL PROTEIN; CELL SURFACE RECEPTOR; GUANOSINE TRIPHOSPHATASE; LIGAND;

ANIMAL; BACTERIAL INFECTION; BACTERIAL PHENOMENA AND FUNCTIONS; BACTERIUM; BACTERIUM ADHERENCE; CELL VACUOLE; CHEMISTRY; CYTOSKELETON; EUKARYOTIC CELL; GENETICS; HUMAN; MAMMAL; MICROBIOLOGY; MOLECULAR MIMICRY; PATHOLOGY; PHAGOCYTOSIS; PHYSIOLOGY; REVIEW; SIGNAL TRANSDUCTION; ULTRASTRUCTURE; VIRULENCE;

ANIMALS; BACTERIA; BACTERIAL ADHESION; BACTERIAL INFECTIONS; BACTERIAL PHYSIOLOGY; BACTERIAL PROTEINS; CYTOSKELETON; EUKARYOTIC CELLS; GTP PHOSPHOHYDROLASES; HUMANS; LIGANDS; MAMMALS; MOLECULAR MIMICRY; PHAGOCYTOSIS; RECEPTORS, CELL SURFACE; SIGNAL TRANSDUCTION; VACUOLES; VIRULENCE;

EID: 0035432063     PISSN: 14710072     EISSN: None     Source Type: Journal    
DOI: 10.1038/35085062     Document Type: Review

References (125)

1. Uings, I. J. & Farrow, S. N. Cell receptors and cell signalling. Mol. Pathol. 53, 295-299 (2000).
2. Virji, M. Microbial utilization of human signalling molecules. Microbiology 142, 3319-3336 (1996).
3. Boudreau, N. J. & Jones, P. L. Extracellular matrix and integrin signalling: the shape of things to come. Biochem. J. 339, 481-488 (1999).
4. Lebrun, M., Mengaud, J., Ohayon, H., Nato, F. & Cossart, P. Internalin must be on the bacterial surface to mediate entry of Listeria monocytogenes into epithelial cells. Mol. Microbiol. 21, 579-592 (1996).
5. Dramsi, S., Dehoux, P. & Cossart, P. Common features of Gram-positive bacterial proteins involved in cell recognition. Mol. Microbiol. 9, 1119-1121 (1993).
6. 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). These authors used affinity chromatography to isolate the mammalian receptor for Listeria internalin.
7. Lecuit, M., Ohayon, H., Braun, L., Mengaud, J. & Cossart, P. Internalin of Listeria monocytogenes with an intact leucine-rich repeat region is sufficient to promote internalization. Infect. Immun. 65, 5309-5319 (1997).
8. Lecuit, M. et al. A single amino acid in E-cadherin responsible for host specificity towards the human pathogen Listeria monocytogenes. EMBO J. 18, 3956-3963 (1999).
9. Lecuit, M. et al. A transgenic model for listeriosis: role of internalin in crossing the intestinal barrier. Science 292, 1722-1725 (2001). This paper is the culmination of many in vitro studies on Listeria interaction with host cells. It shows that the internalin-E-cadherin interaction is crucial for the establishment of infection in vivo.
10. Gaillard, J. L., Berche, P., Mounier, J., Richard, S. & Sansonetti, P. In vitro model of penetration and intracellular growth of Listeria monocytogenes in the human enterocyte-like cell line Caco-2. Infect. Immun. 55, 2822-2829 (1987).
11. Braun, L. et al. InIB: an invasion protein of Listeria monocytogenes with a novel type of surface association. Mol. Microbiol. 25, 285-294 (1997).
12. Marino, M., Braun, L., Cossart, P. & Ghosh, P. Structure of the InIB leucine-rich repeats, a domain that triggers host cell invasion by the bacterial pathogen L. monocytogenes. Mol. Cell 4, 1063-1072 (1999).
13. Braun, L., Ghebrehiwet, B. & Cossart, P. gC1q-R/p32, a C1q-binding protein, is a receptor for the InIB invasion protein of Listeria monocytogenes. EMBO J. 19, 1458-1466 (2000).
14. 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). References 13 and 14 identified the elusive mammalian receptor for the Listeria surface protein, InIB.
15. Ghebrehiwet, B. & Peerschke, E. I. Structure and function of gC1q-R: a multiligand binding cellular protein. Immunobiology 199, 225-238 (1998).
16. Birchmeier, C. & Gherardi, E. Developmental roles of HGF/SF and its receptor, the c-Met tyrosine kinase. Trends Cell Biol. 8, 404-410 (1998).
17. Corvera, S. & Czech, M. P. Direct targets of phosphoinositide 3-kinase products in membrane traffic and signal transduction. Trends Cell Biol. 8, 442-446 (1998).
18. 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).
19. Leong, J. M., Fournier, R. S. & Isberg, R. R. Identification of the integrin binding domain of the Yersinia pseudotuberculosis invasin protein. EMBO J. 9, 1979-1989 (1990). The first reported example of bacterial ligand mimicry.
20. 1 integrin receptor. J. Biol. Chem. 266, 24367-24375 (1991).
21. 1 chain integrins is determined by ligand affinity and receptor density. EMBO J. 12, 1887-1895 (1993).
22. 1 chain indicate a role for endocytosis factors in bacterial internalization. J. Biol. Chem. 271, 7665-7672 (1996).
23. Isberg, R. R., Hamburger, Z. & Dersch, P. Signaling and invasin-promoted uptake via integrin receptors. Microbes Infect. 2, 793-801 (2000).
24. Weidow, C. L., Black, D. S., Bliska, J. B. & Bouton, A. H. CAS/Crk signalling mediates uptake of Yersinia into human epithelial cells. Cell Microbiol. 2, 549-560 (2000).
25. Hoessli, D. C. et al. Signaling through sphingolipid microdomains of the plasma membrane: the concept of signaling platform. Glycoconj. J. 17, 191-197 (2000).
26. Rosenberger, C. M., Brumell, J. H. & Finlay, B. B. Microbial pathogenesis: lipid rafts as pathogen portals. Curr. Biol. 10, R823-R825 (2000).
27. Baorto, D. M. et al. Survival of fimH-expressing enterobacteria in macrophages relies on glycolipid traffic. Nature 389, 636-639 (1997).
28. Peyron, P., Bordier, C., N'Diaye, E. N. & Maridonneau-Parini, I. Nonopsonic phagocytosis of Mycobacterium kansasii by human neutrophils depends on cholesterol and is mediated by CR3 associated with glycosylphosphatidylinositol-anchored proteins. J. Immunol. 165, 5186-5191 (2000).
29. Gatfield, J. & Pieters, J. Essential role for cholesterol in entry of mycobacteria into macrophages. Science 288, 1647-1650 (2000).
30. 1 integrin recognition and subsequent internalization through a pathway involving caveolae and dynamic unstable microtubules. Infect. Immun. 69, 1856-1868 (2001).
31. Wooldridge, K. G., Williams, P. H. & Ketley, J. M. Host signal transduction and endocytosis of Campylobacter jejuni. Microb. Pathog. 21, 299-305 (1996).
32. Mordue, D. G., Desai, N., Dustin, M. & Sibley, L. D. invasion by Toxoplasma gondii establishes a moving junction that selectively excludes host cell plasma membrane proteins on the basis of their membrane anchoring. J. Exp. Med. 190, 1783-1792 (1999).
33. Lauer, S. et al. Vacuolar uptake of host components, and a role for cholesterol and sphingomyelin in malarial infection. EMBO J. 19, 3556-3564 (2000).
34. Hueck, C. J. Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol. Mol. Biol. Rev. 62, 379-433 (1998). An excellent overview of type III secretion systems and their secreted proteins.
35. Schmitz, A. A., Govek, E. E., Bottner, B. & Van Aelst, L. Rho GTPases: signaling, migration, and invasion. Exp. Cell Res. 261, 1-12 (2000).
36. Aderem, A. & Underhill D. M. Mechanisms of phagocytosis in macrophages. Annu. Rev. Immunol. 17, 593-623 (1999).
37. Caron, E. & Hall, A. Identification of two distinct mechanisms of phagocytosis controlled by different Rho GTPases. Science 282, 1717-1721 (1998).
38. Rosqvist, R., Bolin, I. & Wolf-Watz, H. Inhibition of phagocytosis in Yersinia pseudotuberculosis: a virulence plasmid-encoded ability involving the Yop2b protein. Infect. Immun. 56, 2139-2143 (1988).
39. Ramarao, N., Gray-Owen, S. D., Backert, S. & Meyer, T. F. Helicobacter pylori inhibits phagocytosis by professional phagocytes involving type IV secretion components. Mol. Microbiol. 37, 1389-1404 (2000).
40. Goosney, D. L., Celli, J., Kenny, B. & Finlay, B. B. Enteropathogenic Escherichia coli inhibits phagocytosis. Infect. Immun. 67, 490-495 (1999).
41. Persson, C. et al. Localization of the Yersinia PTPase to focal complexes is an important virulence mechanism. Mol. Microbiol. 33, 828-838 (1999).
42. Montagna, L. G., Ivanov, M. I. & Bliska, J. B. Identification of residues in the N-terminal domain of the Yersinia tyrosine phosphatase that are critical for substrate recognition. J. Biol. Chem. 276, 5005-5011 (2001).
43. Evdokimov, A. G., Tropea, J. E., Routzahn, K. M., Copeland, T. D. & Waugh, D. S. Structure of the N-terminal domain of Yersinia pestis YopH at 2.0 Å resolution. Acta Crystallogr. D Biol. Crystallogr. 57, 793-799 (2001).
44. Persson, C., Carballeira, N., Wolf-Watz, H. & Fallman, M. The PTPase YopH inhibits uptake of Yersinia, tyrosine phosphorylation of p130Cas and FAK, and the associated accumulation of these proteins in peripheral focal adhesions. EMBO J. 16, 2307-2318 (1997).
45. Black, D. S. & Bliska, J. B. Identification of p130Cas 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 (1997). References 44 and 45 identify the host cell targets of the Yersinia effector YopH as components of focal adhesions.
46. Hamid, N. et al. YopH dephosphorylates Cas and Fyn-binding protein in macrophages. Microb. Pathog. 27, 231-242 (1999).
47. Black, D. S., Marie-Cardine, A., Schraven, B. & Bliska, J. B. The Yersinia tyrosine phosphatase YopH targets a novel adhesion-regulated signalling complex in macrophages. Cell. Microbiol. 2, 401-414 (2000).
48. Fallman, M. et al. Yersinia pseudotuberculosis inhibits Fc receptor-mediated phagocytosis in J774 cells. Infect. Immun. 63, 3117-3124 (1995).
49. Von Pawel-Rammingen, U. et al. GAP activity of the Yersinia YopE cytotoxin specifically targets the Rho pathway: a mechanism for disruption of actin microfilament structure. Mol. Microbiol. 36, 737-748 (2000).
50. Zumbihl, R. et al. The cytotoxin YopT of Yersinia enterocolitica induces modification and cellular redistribution of the small GTP-binding protein RhoA. J. Biol. Chem. 274, 29289-29293 (1999).
51. Goehring, U. M., Schmidt, G., Pederson, K. J., Aktories, K. & Barbieri, J. T. The N-terminal domain of Pseudomonas aeruginosa exoenzyme S is a GTPase-activating protein for Rho GTPases. J. Biol. Chem. 274, 36369-36372 (1999).
52. Cowell, B. A., Chen, D. Y., Frank, D. W., Vallis, A. J. & Fleiszig, S. M. ExoT of cytotoxic Pseudomonas aeruginosa prevents uptake by corneal epithelial cells. Infect. Immun. 68, 403-406 (2000).
53. 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).
54. Allen, L. A., Schlesinger, L. S. & Kang, B. Virulent strains of Helicobacter pylori demonstrate delayed phagocytosis and stimulate homotypic phagosome fusion in macrophages. J. Exp. Med. 191, 115-128 (2000).
55. Sansonetti, P. J. Rupture, invasion and inflammatory destruction of the intestinal barrier by Shigella, making sense of prokaryote-eukaryote cross-talks. FEMS Microbiol. Rev. 25, 3-14 (2001).
56. Sansonetti, P. J., Kopecko, D. J. & Formal, S. B. Involvement of a plasmid in the invasive ability of Shigella flexneri. Infect. Immun. 35, 852-860 (1982).
57. 1 integrin promotes entry of the bacteria into mammalian cells. J. Exp. Med. 183, 991-999 (1996).
58. Skoudy, A. et al. CD44 binds to the Shigella IpaB protein and participates in bacterial invasion of epithelial cells. Cell Microbiol. 2, 19-33 (2000). References 57 and 58 show the direct interaction of Shigella Ipa proteins with mammalian receptors.
59. Menard, R., Prevost, M. C., Gounon, P., Sansonetti, P. & Dehio, C. The secreted Ipa complex of Shigella flexneri promotes entry into mammalian cells. Proc. Natl Acad. Sci. USA 93, 1254-1258 (1996).
60. Blocker, A. et al. The tripartite type III secreton of Shigella flexneri inserts IpaB and IpaC into host membranes. J. Cell Biol. 147, 683-693 (1999).
61. Tran Van Nhieu, G., Bourdet-Sicard, R., Dumenil, G., Blocker, A. & Sansonetti, P. J. Bacterial signals and cell responses during Shigella entry into epithelial cells. Cell Microbiol. 2, 187-193 (2000).
62. 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). Together with reference 65, these authors demonstrate the manipulation of the host cell cytoskeleton by two Shigella effectors, IpA and IpaC, to promote bacterial entry.
63. Bourdet-Sicard, R., Egile, C., Sansonetti, P. J. & Tran Van Nhieu, G. Diversion of cytoskeletal processes by Shigella during invasion of epithelial cells. Microbes Infect. 2, 813-819 (2000).
64. Mounier, J. et al. Rho family GTPases control entry of Shigella flexneri into epithelial cells but not intracellular motility. J. Cell Sci. 112, 2069-2080 (1999).
65. Bourdet-Sicard, R. et al. Binding of the Shigella protein IpaA to vinculin induces F-actin depolymerization. EMBO J. 18, 5853-5862 (1999).
66. Niebuhr, K. et al. 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 (2000).
67. Hardt, W. D., Chen, L. M., Schuebel, K. E., Bustelo, X. R. & Galan, J. E. S. typhimurium encodes an activator of Rho GTPases that induces membrane ruffling and nuclear responses in host cells. Cell 93, 815-826 (1998). This paper, along with reference 77, shows the coordinate regulation of Rho GTPases by the Salmonella effectors SopE and SptP during invasion, to induce and then dampen membrane raffling.
68. Criss, A. K., Ahlgren, D. M., Jou, T. S., McCormick, B. A. & Casanova, J. E. The GTPase Rac1 selectively regulates Salmonella invasion at the apical plasma membrane of polarized epithelial cells. J. Cell Sci. 114, 1331-1341 (2001).
69. Rudolph, M. G. et al. Biochemical analysis of SopE from Salmonella typhimurium, a highly efficient guanosine nucleotide exchange factor for RhoGTPases. J. Biol. Chem. 274, 30501-30509 (1999).
70. 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).
71. Zhou, D., Mooseker, M. S. & Galan, J. E. Role of the S. typhimurium actin-binding protein SipA in bacterial internalization. Science 283, 2092-2095 (1999).
72. Zhou, D., Mooseker M. S. & Galan, J. E. An invasion-associated Salmonella protein modulates the actin-bundling activity of plastin. Proc. Natl Acad. Sci. USA 96, 10176-10181 (1999).
73. Scherer, C. A., Cooper, E. & Miller, S. I. The Salmonella type III secretion translocon protein SspC is inserted into the epithelial cell plasma membrane upon infection. Mol. Microbiol. 37, 1133-1145 (2000).
74. Hayward, R. D. & Koronakis, V. Direct nucleation and bundling of actin by the SipC protein of invasive Salmonella. EMBO J. 18, 4926-4934 (1999).
75. McGhie, E. J., Hayward, R. D. & Koronakis, V. Cooperation between actin-binding proteins of invasive Salmonella: SipA potentiates SipC nucleation and bundling of actin. EMBO J. 20, 2131-2139 (2001).
76. Fu, Y. & Galan, J. E. The Salmonella typhimurium tyrosine phosphatase SptP is translocated into host cells and disrupts the actin cytoskeleton. Mol. Microbiol. 27, 359-368 (1998).
77. Fu, Y. & Galan, J. E. A Salmonella protein antagonizes Rac-1 and Cdc42 to mediate host-cell recovery after bacterial invasion. Nature 401, 293-297 (1999).
78. Stebbins, C. E. & Galan, J. E. Modulation of host signaling by a bacterial mimic: structure of the Salmonella effector SptP bound to Rac1. Mol. Cell 6, 1449-1460 (2000).
79. Goebel, W. & Kuhn, M. Bacterial replication in the host cell cytosol. Curr. Opin. Microbiol. 3, 49-53 (2000).
80. Frischknecht, F. & Way, M. Surfing pathogens and the lessons learned for actin polymerization. Trends Cell Biol. 11, 30-38 (2001).
81. Meresse, S. et al. Controlling the maturation of pathogen-containing vacuoles: a matter of life and death. Nature Cell Biol. 1, E183-E188 (1999).
82. Comerci, D. J., Martinez-Lorenzo, M. J., Sieira, R., Gorvel, J. P. & Ugalde, R. A. Essential role of the VirB machinery in the maturation of the Brucella abortus-containing vacuole. Cell. Microbiol. 3, 159-168 (2001).
83. Vogel, J. P. & Isberg, R. R. Cell biology of Legionella pneumophila. Curr. Opin. Microbiol. 2, 30-34 (1999).
84. Subtil, A., Parsot, C. & Dautry-Varsat, A. Secretion of predicted Inc proteins of Chlamydia pneumoniae by a heterologous type III machinery. Mol. Microbiol. 39, 792-800 (2001).
85. Duclos, S. & Desjardins, M. Subversion of a young phagosome: the survival strategies of intracellular pathogens. Cell. Microbiol. 2, 365-377 (2000).
86. Heinzen, R. A., Hackstadt, T. & Samuel, J. E. Developmental biology of Coxiella burnettii. Trends Microbiol. 7, 149-154 (1999).
87. Sinai, A. P. & Joiner, K. A. Safe haven: the cell biology of nonfusogenic pathogen vacuoles. Annu. Rev. Microbiol. 51, 415-462 (1997).
88. Meresse, S., Steele-Mortimer, O., Finlay, B. B. & Gorvel, J. P. The rab7 GTPase controls the maturation of Salmonella typhimurium-containing vacuoles in HeLa cells. EMBO J. 18, 4394-4403 (1999). This paper shows that the GTPase Rab7 regulates the maturation of the Salmonella-containing vacuole.
89. Beuzon, C. R. et al. Salmonella maintains the integrity of its intracellular vacuole through the action of SifA. EMBO J. 19, 3235-3249 (2000).
90. Brumell, J. H., Rosenberger, C. M., Gotto, G. T., Marcus, S. L. & Finlay, B. B. SifA permits survival and replication of Salmonella typhimurium in murine macrophages. Cell. Microbiol. 3, 75-84 (2001).
91. Stein, M. A., Leung, K. Y., Zwick, M., Garcia-del Portillo, F. & Finlay, B. B. Identification of a Salmonella virulence gene required for formation of filamentous structures containing lysosomal membrane glycoproteins within epithelial cells. Mol. Microbiol. 20, 151-164 (1996).
92. Uchiya, K. et al. A Salmonella virulence protein that inhibits cellular trafficking. EMBO J. 18, 3924-3933 (1999).
93. Horwitz, M. A. Phagocytosis of the Legionnaires' disease bacterium (Legionella pneumophila) occurs by a novel mechanism: engulfment within a pseudopod coil. Cell 36, 27-33 (1984).
94. Rathman, M., Barker, L. P. & Falkow, S. The unique trafficking pattern of Salmonella typhimurium-containing phagosomes in murine macrophages is independent of the mechanism of bacterial entry. Infect. Immun. 65, 1475-1485 (1997).
95. Mordue, D. G. & Sibley, L. D. Intracellular fate of vacuoles containing Toxoplasma gondii is determined at the time of formation and depends on the mechanism of entry. J. Immunol. 159, 4452-4459 (1997).
96. Da Silva, R. P., Hall, B. F., Joiner, K. A. & Sacks, D. L. CR1, the C3b receptor, mediates binding of infective Leishmania major metacyclic promastigotes to human macrophages. J. Immunol. 143, 617-622 (1989).
97. Alvarez-Dominguez, C., Vazquez-Boland, J. A., Carrasco-Marin, E., Lopez-Mato, P. & Leyva-Cobian, F. Host cell heparan sulfate proteoglycans mediate attachment and entry of Listeria monocytogenes, and the listerial surface protein ActA is involved in heparan sulfate receptor recognition. Infect. Immun. 65, 78-88 (1997).
98. Isberg, R. R. & Leong, J. M. Multiple β. chain integrins are receptors for invasin, a protein that promotes bacterial penetration into mammalian cells. Cell 60, 861-871 (1990).
99. Flugel, A. et al. Interaction of enteropathogenic Yersinia enterocolitica with complex basement membranes and the extracellular matrix proteins collagen type IV, laminin-1 and-2, and nidogen/entactin. J. Biol. Chem. 269, 29732-29738 (1994).
100. van Putten, J. P. & Paul, S. M. Binding of syndecan-like cell surface proteoglycan receptors is required for Neisseria gonorrhoeae entry into human mucosal cells. EMBO J. 14, 2144-2154 (1995).
101. - gonococci into HEp-2 cells requires concerted action of glycosaminoglycans, fibronectin and integrin receptors. Mol. Microbiol. 29, 369-379 (1998).
102. Gray-Owen, S. D., Dehio, C., Haude, A., Grunert, F. & Meyer, T. F. CD66 carcinoembryonic antigens mediate interactions between Opa-expressing Neisseria gonorrhoeae and human polymorphonuclear phagocytes. EMBO J. 16, 3435-3445 (1997).
103. Chen, T., Grunert, F., Medina-Marino, A. & Gotschlich, E. C. Several carcinoembryonic antigens (CD66) serve as receptors for gonococcal opacity proteins. J. Exp. Med. 185, 1557-1564 (1997).
104. Virji, M., Makepeace, K. & Moxon, E. R. Distinct mechanisms of interactions of Opc-expressing meningococci at apical and basolateral surfaces of human endothelial cells; the role of integrins in apical interactions. Mol. Microbiol. 14, 173-184 (1994).
105. de Vries, F. P., Cole, R., Dankert, J., Frosch, M. & van Putten, J. P. Neisseria meningitidis producing the Opc adhesin binds epithelial cell proteoglycan receptors. Mol. Microbiol. 27, 1203-1212 (1998).
106. Abraham, S. N., Sun, D., Dale, J. B. & Beachey, E. H. Conservation of the D-mannose-adhesion protein among type 1 fimbriated members of the family Enterobacteriaceae. Nature 336, 682-684 (1988).
107. Striker, R., Nilsson, U., Stonecipher, A., Magnusson, G. & Huttgren, S. J. Structural requirements for the glycolipid receptor of human uropathogenic Escherichia coli. Mol. Microbiol. 16, 1021-1029 (1995).
108. Ryu, H., Kim, Y. S., Grange, P. A. & Cassels, F. J. Escherichia coli strain RDEC-1 AF/R1 endogenous fimbrial glycoconjugate receptor molecules in rabbit small intestine. Infect. Immun. 69, 640-649 (2001).
109. 2 integrin on the surface of human target cells. J. Biol. Chem. 272, 30463-30469 (1997).
110. Russell, D. G. & Wright, S. D. Complement receptor type 3 (CR3) binds to an Arg-Gly-Asp-containing region of the major surface glycoprotein, gp63, of Leishmania promastigotes. J. Exp. Med. 168, 279-292 (1988).
111. 1. Cell. Microbiol. 1, 101-117 (1999).
112. Ozeri, V., Rosenshine, I., Mosher, D. F., Fassier, R. & Hanski, E. Roles of integrins and fibronectin in the entry of Streptococcus pyogenes into cells via protein F1. Mol. Microbiol. 30, 625-637 (1998).
113. 2 integrin (CD11b/CD18). J. Exp. Med. 193, 1035-1044 (2001).
114. 2 integrins on bovine leukocytes. FEMS Microbiol. Lett. 179, 161-167 (1999).
115. Sturgill-Koszycki, S. et al. Lack of acidification in Mycobacterium phagosomes produced by exclusion of the vesicular proton-ATPase. Science 263, 678-681 (1994).
116. Deretic, V. & Fratti, R. A. Mycobacterium tuberculosis phagosome. Mol. Microbiol. 31, 1603-1609 (1999).
117. 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).
118. Roy, C. R., Berger, K. H. & Isberg, R. R. Legionella pneumophila DotA protein is required for early phagosome trafficking decisions that occur within minutes of bacterial uptake. Mol. Microbiol. 28, 663-674 (1996).
119. 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).
120. Joshi, A. D., Sturgill-Koszycki, S. & Swanson, M. S. Evidence that Dot-dependent and-independent factors isolate the Legionella pneumophila phagosome from the endocytic network in mouse macrophages. Cell. Microbiol. 3, 99-114 (2001).
121. Pizarro-Cerda, J. et al. Brucella abortus transits through the autophagic pathway and replicates in the endoplasmic reticulum of nonprofessional phagocytes. Infect. Immun. 66, 5711-5724 (1998).
122. Heinzen, R. A., Scidmore, M. A., Rockey, D. D. & Hackstadt, T. Differential interaction with endocytic and exocytic pathways distinguish parasitophorous vacuoles of Coxiella burnetii and Chlamydia trachomatis. Infect. Immun. 64, 796-809 (1996).
123. Hackstadt, T. Redirection of host vesicle trafficking pathways by intracellular parasites. Traffic 1, 93-99 (2000).
124. Hakansson, S., Charron, A. J. & Sibley, L. D. Toxoplasma evacuoles: a two-step process of secretion and fusion forms the parasitophorous vacuole. EMBO J. 20, 3132-3144 (2001). In an elegant study, the authors uncouple Toxoplasma secretion from invasion to show that the Toxoptasma parasitophorous vacuole is formed in a two-step process.
125. Scianimanico, S. et al. Impaired recruitment of the small GTPase rab7 correlates with the inhibition of phagosome maturation by Leishmania donovani promastigotes. Cell. Microbiol. 1, 19-32 (1999).