Yersinia pestis: Mechanisms of entry into and resistance to the host cell

Frontiers in Cellular and Infection Microbiology

Volumn 3, Issue DEC, 2013, Pages

  Ke, Yuehua ^a   Chen, Zeliang ^a   Yang, Ruifu ^a  

^a BEIJING INSTITUTE OF MICROBIOLOGY AND EPIDEMIOLOGY   (China)

Author keywords

Anti phagocytosis; Intracellular survival; Invasion; T3SS

Indexed keywords

AIL PROTEIN; BACTERIAL PROTEIN; CELL SURFACE PROTEIN; COMPLEMENT RECEPTOR; FRACTION 1 ANTIGEN; IMMUNOGLOBULIN RECEPTOR; LIPOPOLYSACCHARIDE; OMPX PROTEIN; PLASMINOGEN ACTIVATOR; PSA PROTEIN; SCAVENGER RECEPTOR A; UNCLASSIFIED DRUG; YADBC PROTEIN; YERSINIA OUTER PROTEIN E; YERSINIA OUTER PROTEIN H; YERSINIA OUTER PROTEIN O; YERSINIA OUTER PROTEIN T;

BACTERIAL SURVIVAL; CELL INVASION; CELL PHAGOCYTOSIS; CYTOSKELETON; DENDRITIC CELL; ESCHERICHIA COLI; FIBROBLAST; HOST CELL; HOST PATHOGEN INTERACTION; HUMAN; LIFE CYCLE; MACROPHAGE; MICROENVIRONMENT; NEUTROPHIL; NONHUMAN; PLAGUE; REVIEW; TEMPERATURE; YERSINIA PESTIS; ANIMAL; ANTI-PHAGOCYTOSIS; ENDOCYTOSIS; GENE EXPRESSION REGULATION; IMMUNE EVASION; IMMUNOLOGY; INTRACELLULAR SURVIVAL; INVASION; PATHOGENICITY; PHYSIOLOGY; TYPE III SECRETION SYSTEM;

ANTI-PHAGOCYTOSIS; INTRACELLULAR SURVIVAL; INVASION; T3SS;

ANIMALS; ENDOCYTOSIS; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; IMMUNE EVASION; YERSINIA PESTIS;

EID: 84897927940     PISSN: None     EISSN: 22352988     Source Type: Journal    
DOI: 10.3389/fcimb.2013.00106     Document Type: Review

References (112)

1. Aepfelbacher, M. (2004). Modulation of Rho GTPases by type III secretion system translocated effectors of yersinia. Ergebnisse Physiol. Biol. Chem. Exp. Pharmakol. 152, 65-77. doi: 10.1007/s10254-004-0035-3.
2. Aili, M., Isaksson, E. L., Hallberg, B., Wolf-Watz, H., and Rosqvist, R. (2006). Functional analysis of the YopE GTPase-activating protein (GAP) activity of Yersinia pseudotuberculosis. Cell Microbiol. 8, 1020-1033. doi: 10.1111/j.1462-5822.2005.00684.x.
3. Anisimov, A. P., Bakhteeva, I. V., Panfertsev, E. A., Tat'yana, E. S., Tat'yana, B. K., Platonov, M. E., et al. (2009). The subcutaneous inoculation of pH 6 antigen mutants of Yersinia pestis does not affect virulence and immune response in mice. J. Med. Microbiol. 58, 26-36. doi: 10.1099/jmm.0.005678-0.
4. Areschoug, T., and Gordon, S. (2008). Pattern recognition receptors and their role in innate immunity: focus on microbial protein ligands. Contrib. Microbiol. 15, 45-60. doi: 10.1159/000135685.
5. Areschoug, T., and Gordon, S. (2009). Scavenger receptors: role in innate immunity and microbial pathogenesis. Cell Microbiol. 11, 1160-1169. doi: 10.1111/j.1462-5822.2009.01326.x.
6. Bahta, M., and Burke, T. R. (2012). Yersinia pestis and approaches to targeting its outer protein H protein-tyrosine phosphatase (YopH). Curr. Med. Chem. 19, 5726-5734. doi: 10.2174/092986712803988866.
7. Bartra, S. S., Styer, K. L., O'Bryant, D. M., Nilles, M. L., Hinnebusch, B. J., Aballay, A., et al. (2008). Resistance of Yersinia pestis to complement-dependent killing is mediated by the Ail outer membrane protein. Infect. Immun. 76, 612-622. doi: 10.1128/IAI.01125-07.
8. Barz, C., Abahji, T. N., Trülzsch, K., and Heesemann, J. (2000). The Yersinia Ser/Thr protein kinase YpkA/YopO directly interacts with the small GTPases RhoA and Rac-1. FEBS Lett. 482, 139-143. doi: 10.1016/S0014-5793(00)02045-7.
9. Bearden, S. W., Fetherston, J. D., and Perry, R. D. (1997). Genetic organization of the yersiniabactin biosynthetic region and construction of avirulent mutants in Yersinia pestis. Infect. Immun. 65, 1659-1668.
10. Beer, K., and Miller, V. (1992). Amino acid substitutions in naturally occurring variants of ail result in altered invasion activity. J. Bacteriol. 174, 1360-1369.
11. Benedek, O., Nagy, G., and Emody, L. (2004). Intracellular signalling and cytoskeletal rearrangement involved in Yersinia pestis plasminogen activator (Pla) mediated HeLa cell invasion. Microb. Pathog. 37, 47-54. doi: 10.1016/j.micpath.2004.04.001.
12. Bichowsky-Slomnicki, L., and Ben-Efraim, S. (1963). Biological activities in extracts of Pasteurella pestis and their relation to the "pH 6 antigen". J. Bacteriol. 86, 101-111.
13. Black, D. S., and Bliska, J. B. (2002). The RhoGAP activity of the Yersinia pseudotuberculosis cytotoxin YopE is required for antiphagocytic function and virulence. Mol. Microbiol. 37, 515-527. doi: 10.1046/j.1365-2958.2000.02021.x.
14. Cambi, A., and Figdor, C. G. (2003). Dual function of C-type lectin-like receptors in the immune system. Curr. Opin. Cell Biol. 15, 539-546. doi: 10.1016/j.ceb.2003.08.004.
15. Cannon, G. J., and Swanson, J. A. (1992). The macrophage capacity for phagocytosis. J. Cell Sci. 101, 907-913.
16. Cathelyn, J. S., Crosby, S. D., Lathem, W. W., Goldman, W. E., and Miller, V. L. (2006). RovA, a global regulator of Yersinia pestis, specifically required for bubonic plague. Proc. Natl. Acad. Sci. U.S.A. 103, 13514-13519. doi: 10.1073/pnas.0603456103.
17. Chain, P. S., Hu, P., Malfatti, S. A., Radnedge, L., Larimer, F., Vergez, L. M., et al. (2006). Complete genome sequence of Yersinia pestis strains antiqua and Nepal516: evidence of gene reduction in an emerging pathogen. J. Bacteriol. 188, 4453-4463. doi: 10.1128/JB.00124-06.
18. Cossart, P., and Sansonetti, P. J. (2004). Bacterial invasion: the paradigms of enteroinvasive pathogens. Science 304, 242-248. doi: 10.1126/science.1090124.
19. Cowan, C., Jones, H. A., Kaya, Y. H., Perry, R. D., and Straley, S. C. (2000). Invasion of epithelial cells by Yersinia pestis: evidence for a Y. pestis-specific invasin. Infect. Immun. 68, 4523-4530. doi: 10.1128/IAI.68.8.4523-4530.2000.
20. Davis, K. J., Fritz, D. L., Pitt, M. L., Welkos, S. L., Worsham, P. L., and Friedlander, A. M. (1996). Pathology of experimental pneumonic plague produced by fraction 1-positive and fraction 1-negative Yersinia pestis in African green monkeys (Cercopithecus aethiops). Arch. Pathol. Lab. Med. 120, 156-163.
21. Degen, J., Bugge, T., and Goguen, J. (2007). Fibrin and fibrinolysis in infection and host defense. J. Thromb. Haemost. 5, 24-31. doi: 10.1111/j.1538-7836.2007.02519.x.
22. Deleuil, F., Mogemark, L., Francis, M. S., Wolf-Watz, H., and Fällman, M. (2003). Interaction between the Yersinia protein tyrosine phosphatase YopH and eukaryotic Cas/Fyb is an important virulence mechanism. Cell. Microbiol. 5, 53-64. doi: 10.1046/j.1462-5822.2003.00236.x.
23. Du, Y., Rosqvist, R., and Forsberg, Å. (2002). Role of fraction 1 antigen of Yersinia pestis in inhibition of phagocytosis. Infect. Immun. 70, 1453-1460. doi: 10.1128/IAI.70.3.1453-1460.2002.
24. Dukuzumuremyi, J.-M., Rosqvist, R., Hallberg, B., Åkerström, B., Wolf-Watz, H., and Schesser, K. (2000). The Yersinia protein kinase A is a host factor inducible RhoA/Rac-binding virulence factor. J. Biol. Chem. 275, 35281-35290. doi: 10.1074/jbc.M003009200.
25. East, L., and Isacke, C. M. (2002). The mannose receptor family. Biochim. Biophys. Acta 1572, 364-386. doi: 10.1016/S0304-4165(02)00319-7.
26. Ezekowitz, R. A., Williams, D. J., Koziel, H., Armstrong, M. Y., Warner, A., Richards, F. F., et al. (1991). Uptake of pneumocystis carinii mediated by the macrophage mannose receptor. Nature 351, 155-158. doi: 10.1038/351155a0.
27. Felek, S., and Krukonis, E. S. (2009). The Yersinia pestis ail protein mediates binding and Yop delivery to host cells required for plague virulence. Infect. Immun. 77, 825-836. doi: 10.1128/IAI.00913-08.
28. Felek, S., Tsang, T. M., and Krukonis, E. S. (2010). Three Yersinia pestis adhesins facilitate Yop delivery to eukaryotic cells and contribute to plague virulence. Infect. Immun. 78, 4134-4150. doi: 10.1128/IAI.00167-10.
29. Forman, S., Wulff, C. R., Myers-Morales, T., Cowan, C., Perry, R. D., and Straley, S. C. (2008). yadBC of Yersinia pestis, a new virulence determinant for bubonic plague. Infect. Immun. 76, 578-587. doi: 10.1128/IAI.00219-07.
30. Friedrich, N., Hagedorn, M., Soldati-Favre, D., and Soldati, T. (2012). Prison break: pathogens' strategies to egress from host cells. Microbiol. Mol. Biol. Rev. 76, 707-720. doi: 10.1128/MMBR.00024-12.
31. Fukuto, H. S., Svetlanov, A., Palmer, L. E., Karzai, A. W., and Bliska, J. B. (2010). Global gene expression profiling of Yersinia pestis replicating inside macrophages reveals the roles of a putative stress-induced operon in regulating type III secretion and intracellular cell division. Infect. Immun. 78, 3700-3715. doi: 10.1128/IAI.00062-10.
32. Galvan, E. M., Chen, H., and Schifferli, D. M. (2007). The Psa fimbriae of Yersinia pestis interact with phosphatidylcholine on alveolar epithelial cells and pulmonary surfactant. Infect. Immun. 75, 1272-1279. doi: 10.1128/IAI.01153-06.
33. Grabenstein, J. P., Fukuto, H. S., Palmer, L. E., and Bliska, J. B. (2006). Characterization of phagosome trafficking and identification of PhoP-regulated genes important for survival of Yersinia pestis in macrophages. Infect. Immun. 74, 3727-3741. doi: 10.1128/IAI.00255-06.
34. Greenberg, S. (1999). Modular components of phagocytosis. J. Leukoc. Biol. 66, 712-717.
35. Groves, E., Dart, A. E., Covarelli, V., and Caron, E. (2008). Molecular mechanisms of phagocytic uptake in mammalian cells. Cell. Mol. Life Sci. 65, 1957-1976. doi: 10.1007/s00018-008-7578-4.
36. Groves, E., Rittinger, K., Amstutz, M., Berry, S., Holden, D. W., Cornelis, G. R., et al. (2010). Sequestering of rac by the Yersinia effector YopO blocks Fcγ receptor-mediated phagocytosis. J. Biol. Chem. 285, 4087-4098. doi: 10.1074/jbc.M109.071035.
37. Hamid, N., Gustavsson, A., Andersson, K., McGee, K., Persson, C., Rudd, C. E., et al. (1999). YopH dephosphorylates cas and Fyn-binding protein in macrophages. Microb. Pathog. 27, 231. doi: 10.1006/mpat.1999.0301.
38. Huang, X. Z., and Lindler, L. E. (2004). The pH 6 antigen is an antiphagocytic factor produced by Yersinia pestis independent of Yersinia outer proteins and capsule antigen. Infect. Immun. 72, 7212-7219. doi: 10.1128/IAI.72.12.7212-7219.2004.
39. Huang, Z. Y., Hunter, S., Chien, P., Kim, M. K., Han-Kim, T. H., Indik, Z. K., et al. (2011). Interaction of two phagocytic host defense systems: fcgamma receptors and complement receptor 3. J. Biol. Chem. 286, 160-168. doi: 10.1074/jbc.M110.163030.
40. Iriarte, M., and Cornelis, G. R. (1998). YopT, a new Yersinia Yop effector protein, affects the cytoskeleton of host cells. Mol. Microbiol. 29, 915-929. doi: 10.1046/j.1365-2958.1998.00992.x.
41. 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. doi: 10.1016/0092-8674(87)90335-7.
42. Jaumouille, V., and Grinstein, S. (2011). Receptor mobility, the cytoskeleton, and particle binding during phagocytosis. Curr. Opin. Cell Biol. 23, 22-29. doi: 10.1016/j.ceb.2010.10.006.
43. Juris, S. J., Rudolph, A. E., Huddler, D., Orth, K., and Dixon, J. E. (2000). A distinctive role for the Yersinia protein kinase: actin binding, kinase activation, and cytoskeleton disruption. Proc. Natl. Acad. Sci.U.S.A. 97, 9431-9436. doi: 10.1073/pnas.170281997.
44. Kerschen, E. J., Cohen, D. A., Kaplan, A. M., and Straley, S. C. (2004). The plague virulence protein YopM targets the innate immune response by causing a global depletion of NK cells. Infect. Immun. 72, 4589-4602. doi: 10.1128/IAI.72.8.4589-4602.2004.
45. Khandelwal, P., Keliikuli, K., Smith, C. L., Saper, M. A., and Zuiderweg, E. R. (2002). Solution structure and phosphopeptide binding to the N-terminal domain of Yersinia YopH: comparison with a crystal structure. Biochemistry 41, 11425-11437. doi: 10.1021/bi026333l.
46. Kim, M., Ashida, H., Ogawa, M., Yoshikawa, Y., Mimuro, H., and Sasakawa, C. (2010). Bacterial interactions with the host epithelium. Cell Host Microbe 8, 20-35. doi: 10.1016/j.chom.2010.06.006.
47. Kirjavainen, V., Jarva, H., Biedzka-Sarek, M., Blom, A. M., Skurnik, M., and Meri, S. (2008). Yersinia enterocolitica serum resistance proteins YadA and Ail bind the complement regulator C4b-binding protein. PLoS Pathog. 4:e1000140. doi: 10.1371/journal.ppat.1000140.
48. Kolodziejek, A. M., Schnider, D. R., Rohde, H. N., Wojtowicz, A. J., Bohach, G. A., Minnich, S. A., et al. (2010). Outer membrane protein X (Ail) contributes to Yersinia pestis virulence in pneumonic plague and its activity is dependent on the lipopolysaccharide core length. Infect. Immun. 78, 5233-5243. doi: 10.1128/IAI.00783-10.
49. Kolodziejek, A. M., Sinclair, D. J., Seo, K. S., Schnider, D. R., Deobald, C. F., Rohde, H. N., et al. (2007). Phenotypic characterization of OmpX, an Ail homologue of Yersinia pestis KIM. Microbiology 153, 2941-2951. doi: 10.1099/mic.0.2006/005694-0.
50. Kukkonen, M., and Korhonen, T. K. (2004). The omptin family of enterobacterial surface proteases/adhesins: from housekeeping in escherichia coli to systemic spread of Yersinia pestis. Int. J. Med. Microbiol. 294, 7-14. doi: 10.1016/j.ijmm.2004.01.003.
51. Kukkonen, M., Suomalainen, M., Kyllönen, P., Lähteenmäki, K., Lång, H., Virkola, R., et al. (2004). Lack of O-antigen is essential for plasminogen activation by Yersinia pestis and salmonella enterica. Mol. Microbiol. 51, 215-225. doi: 10.1046/j.1365-2958.2003.03817.x.
52. Lahteenmaki, K., Kukkonen, M., and Korhonen, T. K. (2001). The pla surface protease/adhesin of Yersinia pestis mediates bacterial invasion into human endothelial cells. FEBS Lett. 504, 69-72. doi: 10.1016/S0014-5793(01)02775-2.
53. Lathem, W. W., Price, P. A., Miller, V. L., and Goldman, W. E. (2007). A plasminogen-activating protease specifically controls the development of primary pneumonic plague. Science 315, 509-513. doi: 10.1126/science.1137195.
54. Lawson, J. N., Lyons, C. R., and Johnston, S. A. (2006). Expression profiling of Yersinia pestis during mouse pulmonary infection. DNA Cell Biol. 25, 608-616. doi: 10.1089/dna.2006.25.608.
55. Leigh, S. A., Forman, S., Perry, R. D., and Straley, S. C. (2005). Unexpected results from the application of signature-tagged mutagenesis to identify Yersinia pestis genes required for adherence and invasion. Microb. Pathog. 38, 259-266. doi: 10.1016/j.micpath.2005.02.004.
56. Lindler, L. E., Klempner, M. S., and Straley, S. C. (1990). Yersinia pestis pH 6 antigen: genetic, biochemical, and virulence characterization of a protein involved in the pathogenesis of bubonic plague. Infect. Immun. 58, 2569-2577.
57. Lindler, L. E., and Tall, B. D. (1993). Yersinia pestis pH 6 antigen forms fimbriae and is induced by intracellular association with macrophages. Mol. Microbiol. 8, 311-324. doi: 10.1111/j.1365-2958.1993.tb01575.x.
58. Liu, F., Chen, H., Galvan, E. M., Lasaro, M. A., and Schifferli, D. M. (2006). Effects of psa and F1 on the adhesive and invasive interactions of Yersinia pestis with human respiratory tract epithelial cells. Infect. Immun. 74, 5636-5644. doi: 10.1128/IAI.00612-06.
59. Lobo, L. A. (2006). Adhesive properties of the purified plasminogen activator pla of Yersinia pestis. FEMS Microbiol. Lett. 262, 158-162. doi: 10.1111/j.1574-6968.2006.00382.x.
60. Lowry, M. B., Duchemin, A. M., Robinson, J. M., and Anderson, C. L. (1998). Functional separation of pseudopod extension and particle internalization during Fc gamma receptor-mediated phagocytosis. J. Exp. Med. 187, 161-176. doi: 10.1084/jem.187.2.161.
61. Lukaszewski, R. A., Kenny, D. J., Taylor, R., Rees, D. G., Hartley, M. G., and Oyston, P. C. (2005). Pathogenesis of Yersinia pestis infection in BALB/c mice: effects on host macrophages and neutrophils. Infect. Immun. 73, 7142-7150. doi: 10.1128/IAI.73.11.7142-7150.2005.
62. Makoveichuk, E., Cherepanov, P., Lundberg, S., Forsberg, Å., and Olivecrona, G. (2003). pH6 antigen of Yersinia pestis interacts with plasma lipoproteins and cell membranes. J. Lipid Res. 44, 320-330. doi: 10.1194/jlr.M200182-JLR200.
63. May, R. C., and Machesky, L. M. (2001). Phagocytosis and the actin cytoskeleton. J. Cell Sci. 114, 1061-1077.
64. McGreal, E. P., Miller, J. L., and Gordon, S. (2005). Ligand recognition by antigen-presenting cell C-type lectin receptors. Curr. Opin. Immunol. 17, 18-24. doi: 10.1016/j.coi.2004.12.001.
65. Méresse, S., Steele-Mortimer, O., Moreno, E., Desjardins, M., Finlay, B., and Gorvel, J.-P. (1999). Controlling the maturation of pathogen-containing vacuoles: a matter of life and death. Nat. Cell Biol. 1, E183-E188. doi: 10.1038/15620.
66. Miller, V., Bliska, J., and Falkow, S. (1990). Nucleotide sequence of the Yersinia enterocolitica ail gene and characterization of the Ail protein product. J. Bacteriol. 172, 1062-1069.
67. Miller, V., and Falkow, S. (1988). Evidence for two genetic loci in Yersinia enterocolitica that can promote invasion of epithelial cells. Infect. Immun. 56, 1242-1248.
68. Miller, V. L., Beer, K. B., Heusipp, G., Young, B. M., and Wachtel, M. R. (2001). Identification of regions of Ail required for the invasion and serum resistance phenotypes. Mol. Microbiol. 41, 1053-1062. doi: 10.1046/j.1365-2958.2001.02575.x.
69. Mohammadi, S., and Isberg, R. R. (2009). Yersinia pseudotuberculosis virulence determinants invasin, YopE, and YopT modulate RhoG activity and localization. Infect. Immun. 77, 4771-4782. doi: 10.1128/IAI.00850-09.
70. Navarro, L., Koller, A., Nordfelth, R., Wolf-Watz, H., Taylor, S., and Dixon, J. E. (2007). Identification of a molecular target for the Yersinia protein kinase a. Mol. Cell 26, 465-477. doi: 10.1016/j.molcel.2007.04.025.
71. Nimmerjahn, F., and Ravetch, J. V. (2008). Fcgamma receptors as regulators of immune responses. Nat. Rev. Immunol. 8, 34-47. doi: 10.1038/nri2206.
72. Odin, J. A., Edberg, J. C., Painter, C. J., Kimberly, R. P., and Unkeless, J. C. (1991). Regulation of phagocytosis and [Ca2+]i flux by distinct regions of an Fc receptor. Science 254, 1785-1788. doi: 10.1126/science.1837175.
73. Paerregaard, A., Espersen, F., and Skurnik, M. (1991). Role of the Yersinia outer membrane protein YadA in adhesion to rabbit intestinal tissue and rabbit intestinal brush border membrane vesicles. APMIS 99, 226-232. doi: 10.1111/j.1699-0463.1991.tb05143.x.
74. Parkhill, J., Wren, B. W., Thomson, N. R., Titball, R. W., Holden, M. T., Prentice, M. B., et al. (2001). Genome sequence of Yersinia pestis, the causative agent of plague. Nature 413, 523-527. doi: 10.1038/35097083.
75. Pawel-Rammingen, V., Telepnev, M. V., Schmidt, G., Aktories, K., Wolf-Watz, H., and Rosqvist, R. (2002). 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. doi: 10.1046/j.1365-2958.2000.01898.x.
76. Payne, D., Tatham, D., Williamson, E. D., and Titball, R. W. (1998). The pH 6 antigen of Yersinia pestis binds to β1-linked galactosyl residues in glycosphingolipids. Infect. Immun. 66, 4545-4548.
77. Peiser, L., Mukhopadhyay, S., and Gordon, S. (2002). Scavenger receptors in innate immunity. Curr. Opin. Immunol. 14, 123-128. doi: 10.1016/S0952-7915(01)00307-7.
78. Perry, R. D., and Fetherston, J. D. (1997). Yersinia pestis-etiologic agent of plague. Clin. Microbiol. Rev. 10, 35-66.
79. Phan, J., Lee, K., Cherry, S., Tropea, J. E., Burke, T. R. Jr., and Waugh, D. S. (2003). High-resolution structure of the Yersinia pestis protein tyrosine phosphatase YopH in complex with a phosphotyrosyl mimetic-containing hexapeptide. Biochemistry 42, 13113-13121. doi: 10.1021/bi030156m.
80. Pizarro-Cerda, J., and Cossart, P. (2006). Bacterial adhesion and entry into host cells. Cell 124, 715-727. doi: 10.1016/j.cell.2006.02.012.
81. Pluddemann, A., Mukhopadhyay, S., and Gordon, S. (2006). The interaction of macrophage receptors with bacterial ligands. Expert Rev. Mol. Med. 8, 1-25. doi: 10.1017/S1462399406000159.
82. Prehna, G., Ivanov, M. I., Bliska, J. B., and Stebbins, C. (2006). Yersinia virulence depends on mimicry of host rho-family nucleotide dissociation inhibitors. Cell 126, 869-880. doi: 10.1016/j.cell.2006.06.056.
83. Pujol, C., Klein, K. A., Romanov, G. A., Palmer, L. E., Cirota, C., Zhao, Z., et al. (2009). Yersinia pestis can reside in autophagosomes and avoid xenophagy in murine macrophages by preventing vacuole acidification. Infect. Immun. 77, 2251-2261. doi: 10.1128/IAI.00068-09.
84. Roppenser, B., Röder, A., Hentschke, M., Ruckdeschel, K., and Aepfelbacher, M. (2009). Yersinia enterocolitica differentially modulates RhoG activity in host cells. J. Cell Sci. 122, 696-705. doi: 10.1242/jcs.040345.
85. Rosqvist, R., Forsberg, Å., Rimpiläinen, M., Bergman, T., and Wolf-Watz, H. (1990). The cytotoxic protein YopE of Yersinia obstructs the primary host defence. Mol. Microbiol. 4, 657-667. doi: 10.1111/j.1365-2958.1990.tb00635.x.
86. Schmidt, G. (2011). Yersinia enterocolitica outer protein T (YopT). Eur. J. Cell Biol. 90, 955-958. doi: 10.1016/j.ejcb.2010.12.005.
87. Schraven, B., and Reth, M. (2007). Immunoreceptors and integrins. Immunol. Rev. 218, 5-8. doi: 10.1111/j.1600-065X.2007.00549.x.
88. Sebbane, F., Jarrett, C. O., Gardner, D., Long, D., and Hinnebusch, B. J. (2006). Role of the Yersinia pestis plasminogen activator in the incidence of distinct septicemic and bubonic forms of flea-borne plague. Proc. Natl. Acad. Sci.U.S.A. 103, 5526-5530. doi: 10.1073/pnas.0509544103.
89. Shao, F. (2008). Biochemical functions of Yersinia type III effectors. Curr. Opin. Microbiol. 11, 21-29. doi: 10.1016/j.mib.2008.01.005.
90. Shao, F., Vacratsis, P. O., Bao, Z., Bowers, K. E., Fierke, C. A., and Dixon, J. E. (2003). Biochemical characterization of the Yersinia YopT protease: cleavage site and recognition elements in Rho GTPases. Proc. Natl. Acad. Sci.U.S.A. 100, 904-909. doi: 10.1073/pnas.252770599.
91. Sodeinde, O. A., Subrahmanyam, Y., Stark, K., Quan, T., Bao, Y., and Goguen, J. D. (1992). A surface protease and the invasive character of plague. Science 258, 1004-1007. doi: 10.1126/science.1439793.
92. Song, Y., Tong, Z., Wang, J., Wang, L., Guo, Z., Han, Y., et al. (2004). Complete genome sequence of Yersinia pestis strain 91001, an isolate avirulent to humans. DNA Res. 11, 179-197. doi: 10.1093/dnares/11.3.179.
93. Songsungthong, W., Higgins, M. C., Rolán, H. G., Murphy, J. L., and Mecsas, J. (2010). ROS-inhibitory activity of YopE is required for full virulence of Yersinia in mice. Cell. Microbiol. 12, 988-1001. doi: 10.1111/j.1462-5822.2010.01448.x.
94. Sorg, I., Hoffmann, C., Dumbach, J., Aktories, K., and Schmidt, G. (2003). The C terminus of YopT is crucial for activity and the N terminus is crucial for substrate binding. Infect. Immun. 71, 4623-4632. doi: 10.1128/IAI.71.8.4623-4632.2003.
95. Sousa, S., Lecuit, M., and Cossart, P. (2005). Microbial strategies to target, cross or disrupt epithelia. Curr. Opin. Cell Biol. 17, 489-498. doi: 10.1016/j.ceb.2005.08.013.
96. Swanson, J. A., and Baer, S. C. (1995). Phagocytosis by zippers and triggers. Trends Cell Biol. 5, 89-93. doi: 10.1016/S0962-8924(00)88956-4.
97. Taylor, P. R., Martinez-Pomares, L., Stacey, M., Lin, H. H., Brown, G. D., and Gordon, S. (2005). Macrophage receptors and immune recognition. Annu. Rev. Immunol. 23, 901-944. doi: 10.1146/annurev.immunol.23.021704.115816.
98. Trasak, C., Zenner, G., Vogel, A., Yüksekdag, G., Rost, R., Haase, I., et al. (2007). Yersinia protein kinase YopO is activated by a novel G-actin binding process. J. Biol. Chem. 282, 2268-2277. doi: 10.1074/jbc.M610071200.
99. Trülzsch, K., Sporleder, T., Igwe, E. I., Rüssmann, H., and Heesemann, J. (2004). Contribution of the major secreted yops of Yersinia enterocolitica, O: 8 to pathogenicity in the mouse infection model. Infect. Immun. 72, 5227-5234. doi: 10.1128/IAI.72.9.5227-5234.2004.
100. Tsang, T. M., Felek, S., and Krukonis, E. S. (2010). Ail binding to fibronectin facilitates Yersinia pestis binding to host cells and Yop delivery. Infect. Immun. 78, 3358-3368. doi: 10.1128/IAI.00238-10.
101. Vachon, E., Martin, R., Plumb, J., Kwok, V., Vandivier, R. W., Glogauer, M., et al. (2006). CD44 is a phagocytic receptor. Blood 107, 4149-4158. doi: 10.1182/blood-2005-09-3808.
102. van Zon, J. S., Tzircotis, G., Caron, E., and Howard, M. (2009). A mechanical bottleneck explains the variation in cup growth during FcgammaR phagocytosis. Mol. Syst. Biol. 5, 298. doi: 10.1038/msb.2009.59.
103. Viboud, G. I., Mejía, E., and Bliska, J. B. (2006). Comparison of YopE and YopT activities in counteracting host signalling responses to Yersinia pseudotuberculosis infection. Cell. Microbiol. 8, 1504-1515. doi: 10.1111/j.1462-5822.2006.00729.x.
104. Welkos, S., Friedlander, A., and Davis, K. (1997). Studies on the role of plasminogen activator in systemic infection by virulent Yersinia pestis strain C092. Microb. Pathog. 23, 211-223. doi: 10.1006/mpat.1997.0154.
105. Wiley, D. J., Nordfeldth, R., Rosenzweig, J., DaFonseca, C. J., Gustin, R., Wolf-Watz, H., et al. (2006). The Ser/Thr kinase activity of the Yersinia protein kinase A (YpkA) is necessary for full virulence in the mouse, mollifying phagocytes, and disrupting the eukaryotic cytoskeleton. Microb. Pathog. 40, 234-243. doi: 10.1016/j.micpath.2006.02.001.
106. Wright, S. D., Ramos, R. A., Tobias, P. S., Ulevitch, R. J., and Mathison, J. C. (1990). CD14, a receptor for complexes of lipopolysaccharide (LPS) and LPS binding protein. Science 249, 1431-1433. doi: 10.1126/science.1698311.
107. Yang, Y., Merriam, J. J., Mueller, J. P., and Isberg, R. R. (1996). The psa locus is responsible for thermoinducible binding of Yersinia pseudotuberculosis to cultured cells. Infect. Immun. 64, 2483-2489.
108. Zavialov, A. V., Berglund, J., Pudney, A. F., Fooks, L. J., Ibrahim, T. M., MacIntyre, S., et al. (2003). Structure and biogenesis of the capsular f1 antigen from Yersinia pestis: preserved folding energy drives fiber formation. Cell 113, 587-596. doi: 10.1016/S0092-8674(03)00351-9.
109. Zhang, S., Park, C. G., Zhang, P., Bartra, S. S., Plano, G. V., Klena, J. D., et al. (2008). Plasminogen activator Pla of Yersinia pestis utilizes murine DEC-205 (CD205) as a receptor to promote dissemination. J. Biol. Chem. 283, 31511. doi: 10.1074/jbc.M804646200.
110. Zhang, Z. Y., Clemens, J., Schubert, H., Stuckey, J., Fischer, M., Hume, D., et al. (1992). Expression, purification, and physicochemical characterization of a recombinant Yersinia protein tyrosine phosphatase. J. Biol. Chem. 267, 23759-23766.
111. Zhou, D., Qin, L., Han, Y., Qiu, J., Chen, Z., Li, B., et al. (2006). Global analysis of iron assimilation and fur regulation in Yersinia pestis. FEMS Microbiol. Lett. 258, 9-17. doi: 10.1111/j.1574-6968.2006.00208.x.
112. Zumbihl, R., Aepfelbacher, M., Andor, A., Jacobi, C. A., Ruckdeschel, K., Rouot, B., et al. (1999). The cytotoxin YopT of Yersinia enterocolitica induces modification and cellular redistribution of the small GTP-binding protein RhoA. J. Biol. Chem. 274, 29289-29293. doi: 10.1074/jbc.274.41.29289.