Interleukin-10 and inhibition of innate immunity to Yersiniae: Roles of Yops and LcrV (V antigen)

Infection and Immunity

Volumn 71, Issue 7, 2003, Pages 3673-3681

  Brubaker, Robert R ^a  

^a Michigan State University ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CD14 ANTIGEN; GAMMA INTERFERON; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 10; LCR V ANTIGEN; TOLL LIKE RECEPTOR 2; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; YOPS ANTIGEN;

ANTIGEN BINDING; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERICIDAL ACTIVITY; BACTERIOSTASIS; BINDING AFFINITY; CALCIUM BINDING; CALCIUM SIGNALING; CELL SURVIVAL; CELLULAR IMMUNITY; CYTOKINE PRODUCTION; DOWN REGULATION; ENZYME RELEASE; GENE ACTIVITY; GENE AMPLIFICATION; GENE CONTROL; GENE FUNCTION; GENE MUTATION; GENETIC CODE; HOMEOSTASIS; INFLAMMATION; MUTATIONAL ANALYSIS; NONHUMAN; PASSIVE IMMUNIZATION; PATHOGENICITY; PHAGOCYTE; PHAGOCYTOSIS; PLAGUE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; RECEPTOR BINDING; SHORT SURVEY; TRANSCRIPTION INITIATION; UPREGULATION; YERSINIA; YERSINIA PESTIS; YERSINIA PSEUDOTUBERCULOSIS;

ANIMALS; ANTIGENS, BACTERIAL; BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL PROTEINS; CALCIUM; HUMANS; IMMUNITY, NATURAL; INFLAMMATION; INTERFERON TYPE II; INTERLEUKIN-10; MICE; PORE FORMING CYTOTOXIC PROTEINS; TUMOR NECROSIS FACTOR-ALPHA; YERSINIA; YERSINIA INFECTIONS;

EID: 0037973623     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.71.7.3673-3681.2003     Document Type: Short Survey

References (112)

1. Achtman, M., K. Zurth, G. Morelli, G. Torrea, A. Guiyoule, and E. Carniel. 1999. Yersinia pestis, the cause of plague, is a recently emerged clone of Yersinia pseudotuberculosis. Proc. Natl. Acad. Sci. USA 96:14043-14048.
2. Andersson, K., K.-E. Magnussen, M. Majeed, O. Stendahl, and M. Fällman. 1999. Yersinia pseudotuberculosis-induced calcium signaling in neutrophils is blocked by the virulence effector YopH. Infect. Immun. 67:2567-2574.
3. Bergman, T., S. Håkansson, Å. Forsberg, L. Norlander, A. Macellaro, A. Bäckman, I. Bölin, and H. Wolf-Watz. 1991. Analysis of the V antigen lcrGVH-yopBD operon of Yersinia pseudotuberculosis: evidence for a regulatory role of LcrH and LcrV. J. Bacteriol. 173:1607-1616.
4. Black, D. S., A. Marie-Cardine, B. Schraven, and J. B. Bliska. 2000. The Yersinia tyrosine phosphatase YopH targets a novel adhesion-regulated signalling complex in macrophages. Cell Microbiol. 2:401-414.
5. Bliska, J. B., and D. S. Black. 1995. Inhibition of the Fc receptor-mediated oxidative burst in macrophages by the Yersinia pseudotuberculosis tyrosine phosphatase. Infect. Immun. 63:681-685.
6. Bliska, J. B., K. Guan, J. E. Dixon, and S. Falkow. 1991. Tyrosine phosphate hydrolysis of host proteins by an essential Yersinia virulence determinant. Proc. Natl. Acad. Sci. USA 88:1187-1191.
7. Boland, A., and G. R. Cornelis. 1998. Role of YopP in supression of tumor necrosis factor alpha release by macrophages during Yersinia infection. Infect. Immun. 66:1878-1884.
8. Brubaker, R. R. 1991. Factors promoting acute and chronic diseases caused by yersiniae. Clin. Microbiol. Rev. 4:309-324.
9. Brubaker, R. R. 2000. Yersinia pestis and bubonic plague. In M. Dworkin, S. Falkow, E. Rosenberg, K.-H. Schleifer, and E. Stackelbrandt (ed.), The prokaryotes, an evolving electronic resource for the microbiological community. Springer-Verlag. [Online.] http://www.link.springer.de. Accessed: 8 September 2000.
10. Brubaker, R. R. 1972. Yersinia: biochemistry and genetics of virulence. Curr. Top. Microbiol. Immunol. 57:111-158.
11. Brubaker, R. R., E. D. Beesley, and M. J. Surgalla. 1965. Pasteurella pestis: role of pesticin I and iron in experimental plague. Science 149:422-424.
12. Brubaker, R. R., A. K. Sample, D.-Z. Yu, R. J. Zahorchak, P. C. Hu, and J. M. Fowler. 1987. Proteolysis of V antigen from Yersinia pestis. Microb. Pathog. 2:49-62.
13. Brubaker, R. R., and M. J. Surgalla. 1964. The effect of Ca++ and Mg++ on lysis, growth, and production of virulence antigens by Pasteurella pestis. J. Infect. Dis. 114:13-25.
14. Burrows, T. W. 1956. An antigen determining virulence in Pasteurella pestis. Nature 177:426-427.
15. Burrows, T. W. 1960. Biochemical properties of virulent and avirulent strains of bacteria: Salmonella typhosa and Pasteurella pestis. Ann. N. Y. Acad. Sci. 88:1125-1135.
16. Burrows, T. W. 1963. Virulence of Pasteurella pestis and immunity to plague. Ergeb. Mikrobiol. 37:59-113.
17. Burrows, T. W., and G. A. Bacon. 1958. The effects of loss of different virulence determinants on the virulence and immunogenicity of strains of Pasteurella pestis. Br. J. Exp. Pathol. 39:278-291.
18. Burrows, T. W., and G. W. Bacon. 1954. The basis of virulence in Pasteurella pestis: comparative behavior of virulent and avirulent strains in vivo. Br. J. Exp. Pathol. 35:134-143.
19. Butler, T. 1983. Plague and other Yersinia infections. Plenum Press, New York, N.Y.
20. Büttner, D., and U. Bonas. 2002. Port of entry - the type III secretion translocon. Trends Microbiol. 10:186-192.
21. Cambronne, E. D., and O. Schneewind. 2002. Yersinia enterocolitica type III secretion: yscM1 and yscM2 regulate yop gene expression by a posttranscriptional mechanism that targets the 5′ untranslated region of yop mRNA. J. Bacteriol. 184:5880-5893.
22. Cavanaugh, D. C., and R. Randall. 1959. The role of multiplication of Pasteurella pestis in mononuclear phagocytes in the pathogenesis of fleaborne plague. J. Immunol. 85:348-363.
23. Collmer, A., M. Lindeberg, T. Petniki-Ocwieja, D. J. Schneider, and J. R. Alfano. 2002. Genomic mining type III secretion system effectors in Pseudomonas syringae yields new picks for all TTSS prospectors. Trends Microbiol. 10:462-469.
24. Cornelis, G. R. 2000. Molecular and cell biology aspects of plague. Proc. Natl. Acad. Sci. USA 97:8778-8783.
25. Cornelis, G. R. 1998. The Yersinia deadly kiss. J. Bacteriol. 180:5495-5504.
26. Cornelis, G. R. 1994. Yersinia pathogenicity factors. Curr. Top. Microbiol. Immunol. 192:243-263.
27. Cornelis, G. R. 2002. Yersinia type III secretion: send in the effectors. J. Cell Biol. 158:401-408.
28. Cornelis, G. R. 2002. The Yersinia Ysc-Yop 'type III' weaponry. Nat. Rev. Mol. Cell Biol. 3:742-752.
29. Cornelis, G. R. 2002. The Yersinia Ysc-Yop virulence apparatus. Int. J. Med. Microbiol. 291:455-462.
30. Cornelis, G. R. 1992. Yersiniae, finely tuned pathogens. SGM Symp. 49:231-265.
31. Cornelis, G. R., A. Boland, A. P. Boyd, C. Geuijen, M. Iriarte, C. Neyt, M.-P. Sory, and I. Stainier. 1998. The virulence plasmid of Yersinia, an antihost genome. Microbiol. Mol. Biol. Rev. 62:1315-1352.
32. Cornelis, G. R., and F. Van Gijsegem. 2000. Assembly and function of type III secretory systems. Annu. Rev. Microbiol. 54:735-774.
33. Cornelis, G. R., and H. Wolf-Watz. 1997. The Yersinia Yop virulon: a bacterial system for subverting eukaryotic cells. Mol. Microbiol. 23:861-867.
34. Denecker, G., W. Declercq, C. A. Geuijen, R. Benabdillah, M. van Gurp, M. Sory, P. Vandenabeele, and G. R. Cornelis. 2001. Yersinia enterocolitica YopP-induced apoptosis of macrophages involves the apoptotic signaling cascade upstream of Bid. J. Biol. Chem. 276:19706-19714.
35. Denecker, G., S. Tötemeyer, L. J. Mota, P. Troisfontaines, I. Lambermont, C. Youta, I. Stainier, M. Ackermann, and G. R. Cornelis. 2002. Effect of low- and high-virulence Yersinia enterocolitica strains on the inflammatory response of human umbilical vein endothelial cells. Infect. Immun. 70:3510-3520.
36. Deng, W., V. Burland, G. Plunkett III, A. Boutin, G. F. Mayhew, P. Liss, N. T. Perna, D. J. Rose, B. Mau, S. Zhou, D. C. Schwartz, J. D. Fetherston, L. E. Lindler, R. R. Brubaker, G. V. Plano, S. C. Straley, K. A. McDonough, M. L. Nilles, J. S. Matson, F. R. Blattner, and R. D. Perry. 2002. Genome sequence of Yersinia pestis KIM. J. Bacteriol. 184:4601-4611.
37. Dreyfus, L. A., and R. R. Brubaker. 1978. Consequences of aspartase deficiency in Yersinia pestis. J. Bacteriol. 136:757-764.
38. Fearon, D. T., and R. M. Locksley. 1996. The instructive role of innate immunity in the acquired immune response. Science 272:50-53.
39. Fields, K. A., M. L. Nilles, C. Cowan, and S. C. Straley. 1999. Virulence role of V antigen of Yersinia pestis at the bacterial surface. Infect. Immun. 67:5395-5408.
40. Finlay, R. B., and S. Falkow. 1997. Common themes in microbial pathogenicity revisited. Microbiol. Mol. Biol. Rev. 61:136-169.
41. Galán, J. E., and A. Collemer. 1999. Type III secretion machines: bacterial devices for protein delivery into host cells. Science 284:1322-1328.
42. Ghosh, S., and M. Karin. 2002. Missing pieces in the NF-κB puzzle. Cell 109(Suppl.):S81-S96.
43. Grosdent, N., I. Maridonneau-Parini, M. P. Sory, and G. R. Cornelis. 2002. Role of Yops and adhesins in resistance of Yersinia enterocolitica to phagocytosis. Infect. Immun. 70:4165-4167.
44. Guan, K., and J. E. Dixon. 1990. Protein tyrosine phosphatase activity of an essential virulence determinant in Yersinia. Science 249:553-556.
45. Hamid, N., A. Gustavsson, K. Andersson, K. McGee, C. Persson, C. E. Rudd, and M. Fallman. 1999. YopH dephosphorylates Cas and Fyn-binding protein in macrophages. Microb. Pathog. 27:231-242.
46. Hinnebusch, J., P. Cherepanov, Y. Du, A. Rudolph, J. D. Dixon, T. Schwan, and Å. Forsberg. 1999. Murine toxin of Yersinia pestis shows phospholipase D activity but is not required for virulence in mice. Int. J. Med. Microbiol. 290:483-487.
47. Hueck, C. J. 1998. Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol. Mol. Biol. Rev. 62:379-433.
48. Janssen, W. A., G. W. Fukui, and M. J. Surgalla. 1958. A study of the fare of Pasteurella pestis following intracardial injection into guinea pigs. J. Infect. Dis. 103:183-187.
49. Janssen, W. A., and M. J. Surgalla. 1969. Plague bacillus: survival within host phagocytes. Science 163:950-952.
50. Kirschning, C. J., H. Wesche, T. Merrill Ayres, and M. Rothe. 1998. Human Toll-like receptor 2 confers responsiveness to bacterial lipopolysaccharide. J. Exp. Med. 188:2091-2097.
51. Kobayashi, K., K. Kaneda, and T. Kasama. 2001. Immunopathogenesis of delayed-type hypersensitivity. Microsc. Res. Tech. 52:241-245.
52. Lähteenmäki, K., R. Virkola, A. Sarén, L. Emödy, and T. K. Korhonen. 1998. Expression of plasminogen activator Pla of Yersinia pestis enhances bacterial attachment to the mammalian extracellular matrix. Infect. Immun. 66:5755-5762.
53. Lambert de Rouvroit, C., C. Sluiters, and G. R. Cornelis. 1992. Role of the transcriptional activator, VirF, and temperature in the expression of the pYV plasmid genes of Yersinia enterocolitica. Mol. Microbiol. 6:395-409.
54. Lawton, W. D., R. L. Erdman, and M. J. Surgalla. 1963. Biosynthesis and purification of V and W antigen in Pasteurella pestis. J. Immunol. 91:179-184.
55. Lee, V. T., and O. Schneewind. 2002. Protein secretion and the pathogenesis of bacterial infections. Genes Dev. 15:1725-1752.
56. Lory, S. 1998. Secretion of proteins and assembly of bacterial surface organelles: shared pathways of extracellular protein targeting. Curr. Opin. Microbiol. 1:27-35.
57. Medzhitov, R., and C. A. Janeway, Jr. 1997. Innate immunity: the virtues of a nonclonal system of recognition. Cell 91:295-298.
58. Medzhitov, R., P. Preston-Hurlbert, E. Kopp, A. Stadlen, C. Chen, S. Ghosh, and C. A. Janeway, Jr. 1998. MyD88 is an adapter protein in the hToll/IL-1 receptor family signaling pathways. Mol. Cell 2:253-258.
59. Mehigh, R. J., and R. R. Brubaker. 1993. Major stable peptides of Yersinia pestis synthesized during the low-calcium response. Infect. Immun. 61:13-22.
60. Mills, D. S., A. Boland, M.-P. Sory, P. Van der Smissen, C. Kerbourch, B. B. Finlay, and G. R. Cornelis. 1997. Yersinia enterocolitica induces apoptosis in macrophages by a process requiring functional type III secretion and translocation mechanisms and involving YopP, presumably acting as an effector protein. Proc. Natl. Acad. Sci. USA 94:12638-12643.
61. Monack, D. M., J. Mecsas, N. Ghori, and S. Falkow. 1997. Yersinia signals macrophages to undergo apoptosis and YopJ is necessary for this cell death. Proc. Natl. Acad. Sci. USA 94:10385-10390.
62. Moore, K. W., R. de Waal Malefyt, R. L. Coffman, and A. O'Garra. 2001. Interleukin-10 and the interleukin-10 receptor. Annu. Rev. Immunol. 19:683-765.
63. Mortlock, R. P., and R. R. Brubaker. 1962. Glucose-6-phosphate dehydrogenase and 6-phosphogluconate dehydrogenase activities of Pasteurella pestis and Pasteurella pseudotuberculosis. J. Bacteriol. 84:1122-1123.
64. Motin, V. L., R. Nakajima, G. B. Smirvnov, and R. R. Brubaker. 1994. Passive immunity to yersiniae mediated by anti-recombinant V antigen and protein A-V antigen fusion peptide. Infect. Immun. 62:4192-4201.
65. Motin, V. L., Y. A. Nedialkov, and R. R. Brubaker. 1996. V antigen-polyhistidine fusion peptide: binding to LcrH and active immunity against plague. Infect. Immun. 64:4313-4318.
66. Muzio, M., S. Natoli, S. Saccani, M. Levrero, and A. Mantovani. 1998. The human Toll signaling pathway: divergence of nuclear factor κB and JNK/SAPK activation upstream of tumor necrosis factor receptor-associated factor 6 (TRAF6). J. Exp. Med. 187:2097-2101.
67. Nakajima, R., and R. R. Brubaker. 1993. Association between virulence of Yersinia pestis and suppression of gamma interferon and tumor necrosis factor alpha. Infect. Immun. 61:23-31.
68. Nakajima, R., V. L. Motin, and R. R. Brubaker. 1995. Suppression of cytokines in mice by protein A-V antigen fusion peptide and restoration of synthesis by active immunization. Infect. Immun. 63:3021-3029.
69. Nedialkov, Y. A., V. L. Motin, and R. R. Brubaker. 1997. Resistance to lipopolysaccharide mediated by the Yersinia pestis V antigen-polyhistidine fusion peptide: amplification of interleukin-10. Infect. Immun. 65:1196-1203.
70. Orth, K., Z. Xu, M. B. Mudgett, Z. Q. Bao, L. E. Palmer, J. B. Bliska, W. F. Mangel, B. Staskawicz, and J. E. Dixon. 2000. Disruption of signaling by Yersinia effector YopJ, a ubiquitin-like protease. Science 290:1594-1597.
71. Orth, K., L. E. Palmer, Z. Q. Bao, S. Stewart, A. E. Rudolph, J. B. Bliska, and J. E. Dixon. 1999. Inhibition of the mitogen-activated protein kinase kinase superfamily by a Yersinia effector. Science 285:1920-1923.
72. Palmer, L. E., S. Hobbie, J. E. Galán, and J. B. Bliska. 1998. YopJ of Yersinia pseudotuberculosis is required for the inhibition of macrophage TNF-α production and downstream regulation of the MAP kinase p38 and JNK. Mol. Microbiol. 27:953-965.
73. Palmer, L. E., A. R. Pancetti, S. Greenberg, and J. B. Bliska. 1999. YopJ of Yersinia spp. is sufficient to cause downregulation of multiple mitogen-activated protein kinases in eukaryotic cells. Infect. Immun. 67:708-716.
74. Parkhill, J., B. W. Wren, N. R. Thomson, R. W. Titball, M. T. G. Holden, M. B. Prentice, M. Sebaihia, K. D. James, C. Chercher, K. L. Mungall, S. Baker, D. Basham, S. D. Bentley, K. Brooks, A. M. Cerdeño-Tárraga, T. Chillingworth, A. Cronin, R. M. Davies, P. Davis, G. Dougan, T. Feltwell, N. Hamlin, S. Holroyd, K. Jagels, A. V. Karlyshev, S. Leather, S. Moule, P. C. F. Oyston, M. Quail, K. Rutherford, M. Simmonds, J. Skelton, K. Stevens, S. Whitehead, and B. G. Barrell. 2001. Genome sequence of Yersinia pestis, the causative agent of plague. Nature 413:523-527.
75. Perry, R. D., and J. D. Fetherston. 1997. Yersinia pestis - etiologic agent of plague. Clin. Microbiol. Rev. 10:35-66.
76. 2+ response operon encodes the V antigen of Yersinia pestis. Infect. Immun. 54:428-434.
77. Persson, C., R. Nordfelth, K. Andersson, Å. Forsberg, H. Wolf-Watz, and M. Fallman. 1999. Localization of the Yersinia PTPase to focal complexes is an important virulence mechanism. Mol. Microbiol. 33:828-838.
78. Pettersson, J., A. Holmstrom, J. Hill, S. Leary, E. Frithz-Lindsten, A. von-Euler-Matell, E. Carlsson, R. Titball, Å. Forsberg, and H. Wolf-Watz. 1999. The V antigen of Yersinia is surface exposed before target cell contact and involved in virulence protein translocation. Mol. Microbiol. 32:961-976.
79. Pettersson, J., R. Nordfeith, E. Dubinina, T. Bergman, M. Gustafsson, K. E. Magnusson, and H. Wolf-Watz. 1996. Modulation of virulence factor expression by pathogen target cell contact. Science 273:1231-1233.
80. 2+ response virulence genes. J. Bacteriol. 173:2649-2657.
81. Rohde, J. R., X.-S. Luan, H. Rohde, J. M. Fox, and S. A. Minnich. 1999. The Yersinia enterocolitica pYV virulence plasmid contains multiple intrinsic DNA bends which melt at 37°C. J. Bacteriol. 181:4198-4204.
82. Rosqvist, R., K. E. Magnusson, and H. Wolf-Watz. 1994. Target cell contact triggers expression and polarized transfer of Yersinia YopE cytotoxin into mammalian cells. EMBO J. 13:964-972.
83. Ruckdeschel, K., S. Harb, A. Roggenkamp, M. Hornef, R. Zumbihl, S. Kohler, J. Heesemann, and B. Rouot. 1998. Yersinia enterocolitica impairs activation of transcription factor NF-κB: involvement in the induction of programmed cell death and in the suppression of the macrophage tumor necrosis factor alpha production. J. Exp. Med. 187:1069-1079.
84. Ruckdeschel, K., A. Roggenkamp, S. Schubert, and J. Heesemann. 1996. Differential contribution of Yersinia enterocolitica virulence factors to evasion of microbicidal action of neutrophils. Infect. Immun. 64:724-733.
85. Sample, A. K., and R. R. Brubaker. 1987. Post-translational regulation of Lcr plasmid-mediated peptides in pesticinogenic Yersinia pestis. Microb. Pathog. 3:239-248.
86. Sarker, M. R., C. Neyt, E. Stainier, and G. R. Cornelis. 1998. The Yersinia Yop virulon: LcrV is required for extrusion of the translocators YopB and YopD. J. Bacteriol. 180:1207-1214.
87. Sauvonnet, N., I. Lambermont, P. Van der Bruggen, and G. R. Cornelis. 1997. YopH prevents monocyte chemoattractant protein 1 expression in macrophages and T cell proliferation through fractionation of the phosphatidylinositol 3-kinase pathway. Mol. Microbiol. 45:805-815.
88. Sauvonnet, N., B. Predet-Balede, J. A. Garcia-Sanz, and G. R. Cornelis. 2002. Regulation of mRNA expression in macrophages following Yersinia enterocolitica infection: role of different Yop effectors. J. Biol. Chem. 277:25133-25142.
89. Sawa, T., T. L. Yahr, M. Ohara, K. Kurahashi, M. A. Gropper, J. P. Wiener-Kronish, and D. W. Frank. 1999. Active and passive immunization with the Pseudomonas V antigen protects against type III intoxication and lung injury. Nat. Med. 5:392-398.
90. Schesser, K., A. K. Spiik, J. M. Dukuzumuremyl, M. F. Neurath, S. Pettersson, and H. Wolf-Watz. 1998. The YopJ locus is required for Yersinia-mediated inhibition of NF-κB activation and cytokine expression: YopJ contains a eukaryotic SH2-like domain that is essential for its repressive activity. Mol. Microbiol. 28:1067-1079.
91. Sing, A., A. Roggenkamp, A. M. Geiger, and J. Heesemann. 2002. Yersinia enterocolitica evasion of the host immune response by V antigen-induced IL-10 production of macrophages is abrogated in IL-10-deficient mice. J. Immunol. 168:1315-1321.
92. Sing, A., D. Rost, N. Tvardovaskaia, A. Roggenkamp, A. Wiedemann, C. J. Kirschning, M. Aepfelbacher, and J. Heesemann. 2002. Yersinia V-antigen exploits Toll-like receptor 2 and CD14 for interleukin 10-mediated immunosuppression. J. Exp. Med. 196:1017-1024.
93. Smith, H., J. Keppie, E. C. Cocking, and K. Witt. 1960. The chemical basis of the virulence of Pasteurella pestis. I. The isolation and the aggressive properties of Past. pestis and its products from infected guinea pigs. Br. J. Exp. Pathol. 41:452-459.
94. Smith, T. 1934. Parasitism and disease. Princeton University Press, Princeton, N.J.
95. Sodeinde, O. A., A. K. Sample, R. R. Brubaker, and J. D. Goguen. 1988. Plasminogen activator/coagulase gene of Yersinia pestis is responsible for degradation of plasmid-encoded outer membrane proteins. Infect. Immun. 56:2749-2752.
96. Sodeinde, O. A., Y. V. B. K. Subrahmanyam, K. Stark, T. Quan, Y. Bao, and J. D. Goguen. 1992. A surface protease and the invasive character of plague. Science 258:1004-1007.
97. 2+ in Yersinia pestis include structural genes for outer membrane proteins. Infect. Immun. 51:445-454.
98. Straley, S. C., and R. R. Brubaker. 1981. Cytoplasmic and membrane proteins of yersiniae cultivated under conditions simulating mammalian intracellular environment. Proc. Natl. Acad. Sci. USA 78:1224-1228.
99. Straley, S. C., and P. A. Harmon. 1984. Growth in mouse peritoneal macrophages of Yersinia pestis lacking established virulence determinants. Infect. Immun. 45:649-654.
100. Takeuchi, O., K. Hoshino, T. Kawai, H. Sanjo, H. Takada, T. Ogawa, K. Takeda, and S. Akira. 1999. Differential roles of TLR2 and TLR4 in recognition of gram-negative and gram-positive bacterial cell wall components. Immunity 11:443-451.
101. Tato, C. M., and C. A. Hunter. 2002. Host-pathogen interactions: subversion and utilization of the NF-κB pathway during infection. Infect. Immun. 70:3311-3317.
102. Une, T., and R. R. Brubaker. 1984. Roles of V antigen in promoting virulence and immunity in yersiniae. J. Immunol. 133:2226-2230.
103. Une, T., R. Nakajima, and R. R. Brubaker. 1986. Roles of V antigen in promoting virulence in Yersinia. Contrib. Microbiol. Immunol. 9:179-185.
104. Vasselon, T., and P. A. Detmers. 2002. Toll receptors: a central element in innate immune responses. Infect. Immun. 70:1033-1041.
105. Wang, P., P. Wu, M. I. Siegel, R. W. Egan, and M. M. Billah. 1995. Interleukin (IL)-10 inhibits nuclear factor kappa B (NF kappa B) activation in human monocytes. IL-10 and IL-4 suppress cytokine synthesis by different mechanisms. J. Biol. Chem. 270:9558-9563.
106. Wang, Q., R. Dziarski, C. J. Kirschning, M. Muzio, and D. Gupta. 2001. Micrococci and peptidoglycan activate TLR2→MyD88→IRAK→TRAF→ NIK→IKK→NF-κB signal transduction pathway that induces transcription of interleukin-8. Infect. Immun. 69:2270-2276.
107. Yahr, T. L., L. M. Mende-Mueller, M. B. Friese, and D. W. Frank. 1997. Identification of type III secreted products of the Pseudomonas aeruginosa exoenzyme S regulon. J. Bacteriol. 179:7165-7168.
108. Yamamoto, K., S. Sato, H. Hemmi, H. Sanjo, S. Uematsu, T. Kaisho, K. Hoshino, O. Takeuchi, M. Kobayashi, T. Fujita, K. Takeda, and S. Akira. 2002. Essential role for TIRAP in activation of the signalling cascade shared by TLR2 and TLR4. Nature 420:324-328.
109. Yang, R. B., G. R. Mark, A. Gray, A. Huang, M. H. Xie, M. Zhang, A. Goddard, W. I. Wood, A. L. Gurney, and P. J. Godowksi. 1998. Toll-like receptor-2 mediates lipopolysaccharide-induced cellular signalling. Nature 395:284-288.
110. Yao, T., J. Mecsas, J. I. Healy, S. Falkow, and Y. Chein. 1999. Suppression of T and B lymphocyte activation by a Yersinia pseudotuberculosis virulence factor, YopH. J. Exp. Med. 190:1343-1350.
111. Yoon, S., Z. Liu, Y. Eyobo, and K. Orth. 2003. Yersinia effector YopJ inhibits yeast MAPK signaling pathways by an evolutionarily conserved mechanism. J. Biol. Chem. 278:2131-2135.
112. Zhang, Z. Y., J. C. Clemens, H. L. Schubert, J. A. Stuckey, M. W. Fischer, D. M. Hume, M. A. Saper, and J. E. Dixon. 1992. Expression, purification, and physicochemical characterization of a recombinant Yersinia protein tyrosine phosphatase. J. Biol. Chem. 267:23759-23766.