Interaction of Yersinia with Host Cells

  • Anne Boland
  • Guy R. Cornelis
Part of the Subcellular Biochemistry book series (SCBI, volume 33)

Abstract

The Yersinia genus contains three species that are pathogenic for humans: Y. pestis, the agent of plague, and two enteropathogens, Y. pseudotuberculosis and Y. enterocolitica, that are generally acquired by ingestion of contaminated food. While Y. pseudotuberculosis is mainly a rodent pathogen, Y. enterocolitica is a frequent cause of disease in humans and provokes gastrointestinal syndromes of variable severity. After infection, secondary manifestations such as erythema nodosum and reactive arthritis can occur (for review, see Cover and Aber, 1989). Although these three pathogens have different entry routes and cause different diseases, they share a remarkable tropism for the lymphoid tissues of their host, where they are able to resist the non-specific immune defense mechanisms.

Keywords

Eukaryotic Cell Focal Adhesion Kinase Protein Tyrosine Phosphatase Yersinia Enterocolitica Yersinia Pestis 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Allaoui, A., Woestyn, S., Sluiters, C., and Cornelis, G.R., 1994, YscU, a Yersinia enterocolitica inner membrane protein involved in Yop secretion, J. Bacteriol. 176: 4534–4542.PubMedGoogle Scholar
  2. Allaoui, A., Scheen, R., Lambert de Rouvroit, C.L., and Cornelis, G.R., 1995a, VirG, a Yersinia enterocolitica lipoprotein involved in Cat’ dependency, is related to ExsB of Pseudomonas aeruginosa, J. Bacteriol. 177: 4230–4237.PubMedGoogle Scholar
  3. Allaoui, A., Schulte, R., and Cornelis, G.R., 1995b, Mutational analysis of the Yersinia enterocoliticia virC operon: characterization of yscE, F, G I, J, K required for Yop secretion and yscH encoding YopR, Mol. Microbiol. 18: 343–355.PubMedGoogle Scholar
  4. Anderson, D.M., and Schneewind, O., 1997, A mRNA signal for the type III secretion of. Yop proteins by Yersinia enterocolitica, Science 278: 1140–1143.PubMedGoogle Scholar
  5. Andersson, K., Carballeira, N., Magnusson, K.E., Persson, C., Stendahl, O., Wolf-Watz, H., and Hillman, M., 1996, YopH of Yersinia pseudotuberculosis interrupts early phosphotyrosine signalling associated with phagocytosis, Mol. Microbiol. 20: 1057–1069.PubMedGoogle Scholar
  6. Autenrieth, I.B., and Firsching, R., 1996, Penetration of M cells and destruction of Peyer’s patches by Yersinia enterocolitica: an ultrastructural and histological study, J. Med. Microbiol. 44: 285–294.PubMedGoogle Scholar
  7. Autenrieth, I.B., and Heesemann, J., 1992, In vivo neutralization of tumor necrosis factor-alpha and interferon-gamma abrogates resistance to Yersinia enterocolitica infection in mice, Med. Microbiol. Immunol. Berl. 181: 333–338.Google Scholar
  8. Balligand, G., Laroche, Y., and Cornelis, G., 1985, Genetic analysis of virulence plasmid from a serogroup 9 Yersinia enterocolitica strain: role of outer membrane protein P1 in resistance to human serum and autoagglutination, Infect. Immun. 48: 78 2786.Google Scholar
  9. Bergman, T., Erickson, K., Galyov, E.E., Persson, C., and Wolf-Watz, H., 1994, The lcrB (yscN/U) gene cluster of Yersinia pseudotuberculosis is involved in Yop secretion and shows high homology to the spa gene clusters of Shigella flexneri and Salmonella typhimurium, J. Bacteriol. 176: 2619–2626.PubMedGoogle Scholar
  10. Beuscher, H.U., Rodel, E, Forsberg, A., and Rollinghoff, M., 1995, Bacterial evasion of host immune defense: Yersinia enterocolitica encodes a suppressor for tumor necrosis factor alpha expression, Infect. Immun. 63: 1270–1277.PubMedGoogle Scholar
  11. Black, D.S., and Bliska, J.B., 1997, Identification of p130cB’ 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.PubMedGoogle Scholar
  12. Bliska, J.B., 1995, Crystal structure of the Yersinia tyrosine phosphatase, Trends. Microbiol. 3: 125–127.PubMedGoogle Scholar
  13. Bliska, J.B., and Black, D.S., 1995, Inhibition of the Fc receptor-mediated oxidative burst in macrophages by the Yersinia pseudotuberculosis tyrosine phosphatase, Infect. Immun. 63: 681–685.PubMedGoogle Scholar
  14. Bliska, J.B., and Falkow, S., 1992, Bacterial resistance to complement killing mediated by the Ail protein of Yersinia enterocolitica, Proc. Natl. Acad. Sci. USA 89: 3561–3565.PubMedGoogle Scholar
  15. Bliska, J.B., Guan, K.L., Dixon, J.E., and Falkow, S., 1991, A mechanism of bacterial pathogenesis: Tyrosine phosphate hydrolysis of host proteins by an essential Yersinia virulence determinant, Proc. Natl. Acad. Sci. USA 88: 1187–1191.PubMedGoogle Scholar
  16. Bliska, J.B., Clemens, J.C., Dixon, J.E., and Falkow, S., 1992, The Yersinia tyrosine phosphatase: specificity of a bacterial virulence determinant for phosphoproteins in the J774A.1 macrophage. J. Exp. Med. 176: 1625–1630.PubMedGoogle Scholar
  17. Bliska, J.B., Copass, M.C., and Falkow, S., 1993, The Yersinia pseudotuberculosis adhesin YadA mediates intimate bacterial attachment to and entry into HEp-2 cells, Infect. Immun. 61: 3914–3921.PubMedGoogle Scholar
  18. Boland, A., and Cornelis, G.R., 1998, Role of YopP in suppression of tumor necrosis factor alpha release by macrophages during Yersinia infection, Infect. Immun. 66: 1878 1884.Google Scholar
  19. Boland, A., Sory, M.-P., Iriarte, M., Kerbourch, C., Wattiau, P., and Cornelis, G.R., 1996, Status of YopM and YopN in the Yersinia Yop virulon: YopM of Y. enterocolitica is internalized inside the cytosol of PU5–1.8 macrophages by the YopB, D, N delivery apparatus, EMBO J. 15: 5191–5201.PubMedGoogle Scholar
  20. Bölin, I., and Wolf-Watz, H., 1988, The plasmid encoded Yop2b protein of Yersinia pseudotuberculosis is a virulence determinant regulated by calcium and temperature at the level of transcription, Mol. MicrobioL 2: 237–245.PubMedGoogle Scholar
  21. Bölin, I., Norlander, L., and Wolf-Watz, H., 1982, Temperature-inducible outer membrane protein of Yersinia pseudotuberculosis and Yersinia enterocolitica is associated with the virulence plasmid, Infect. Immun. 37: 506–512.PubMedGoogle Scholar
  22. Boyd, A.P., Sory, M.-P., Iriarte, M., and Cornelis, G.R., 1998, Heparin interferes with translocation of Yop proteins into HeLa cells and binds to LcrG, a regulatory component of the Yersinia Yop apparatus, Mol. MicrobioL 27: 425–436.PubMedGoogle Scholar
  23. Caron, E., Gross, A., Liautard, J: P., and Dornand, J., 1996, Brucella species release a specific, protease-sensitive, inhibitor of TNF-a expression, active on human macrophage-like cells, J. ImmunoL 156: 2885–2893.Google Scholar
  24. Cavanaugh, D.C., and Randall, R., 1959, The role of multiplication of Pasteurella pestis in mononuclear phagocytes in the pathogenesis of flea-borne plague. J. Immunol. 83: 348–363.PubMedGoogle Scholar
  25. Charnetzky, W.T., and Shuford, W.W., 1985, Survival and growth of Yersinia pestis within macrophages and an effect of the loss of the 47-megadalton plasmid on growth in macrophages, Infect. Immun. 47: 234–241.PubMedGoogle Scholar
  26. Cheng, L.W., Anderson, D.M., and Schneewind, 0., 1997, Two independent type III secretion mechanisms for YopE in Yersinia enterocolitica, Mol. Microbiol. 24: 757–765.PubMedGoogle Scholar
  27. China, B., Michiels, T., and Cornelis, G.R., 1990, The pYV plasmid of Yersinia encodes a lipoprotein, YIpA, related to TraT, MoL Microbiol. 4: 1585–1593.PubMedGoogle Scholar
  28. China, B., Sory, M.-P., N’Guyen, B.T., de Bruyere, M., and Comelis, G.R., 1993, Role of the YadA protein in prevention of opsonization of Yersinia enterocolitica by C3b molecules, Infect. Immun. 61: 3129–3136.PubMedGoogle Scholar
  29. China, B., N’Guyen, B.T., de Bruyere, M., and Cornelis, G.R., 1994, Role of YadA in resistance of Yersinia enterocolitica to phagocytosis by human polymorphonuclear leukocytes, Infect. Immun. 62: 1275–1281.PubMedGoogle Scholar
  30. Clark, M.A., Hirst, B.H., and Jepson, M.A., 1998, M-cell surface 01 integrin expression and invasin-mediated targeting of Yersinia pseudotuberculosis to mouse Peyer’s patch M cells, Infect. Immun. 66: 1237–1243.PubMedGoogle Scholar
  31. Cole, S.P., Guiney, D.G., and Corbeil, L.B., 1993, Molecular analysis of a gene encoding a serumresistance-associated 76kDa surface antigen of Haemophilus somnus. J. Gen. Microbiol. 139: 2135–2143.Google Scholar
  32. Collazo, C.M., and Galan, J.E., 1997, The invasion-associated type III system of Salmonella typhimurium directs the translocation of Sip proteins into the host cell, Mol. Microbiol. 24: 747–756.PubMedGoogle Scholar
  33. Cornelis, G.R., Slithers, C., Delor, I., Geib, D., Kaniga, K., Lambert de Rouvroit, C.L., Sory, M.-P., Vanooteghem, J.-C., and Michiels, T., 1991, ymoA, a Yersinia enterocolitica chromosomal gene modulating the expression of virulence functions, Mol. Microbiol. 5: 1023–1034.Google Scholar
  34. Cornelis, G.R., Iriarte, M., and Sory, M.-P, 1995, Environmental control of virulence functions and signal transduction in Yersinia enterocolitica, in: Signal transduction and bacterial virulence ( R. Rappuoli, V. Scartato, and B. Arico, eds.), R.G. Landes company, Austin. pp. 95–110.Google Scholar
  35. Cornelis, G.R., Boland, A., Boyd, A.P., Geuijen, C., Iriarte, M., Neyt, C., Sory, M.-P., and Stainier, I., 1998, The virulence plasmid of Yersinia, an antihost genome, Micro. Mol. BioL Rev.,in press.Google Scholar
  36. Cover, T.L., and Aber, R.C., 1989, Yersinia enterocolitica, N. Engl. J. Med. 321: 16–24.Google Scholar
  37. De Marco, L., Mazzucato, M., Masotti, A., and Ruggeri, Z.M., 1994, Localization and charac-terization of an a-thrombin-binding site on platelet glycoprotein lba, J. Biol. Chem. 269: 6478–6484.PubMedGoogle Scholar
  38. Deibel, C., Krämer, S., Chakraborty, T., and Ebel, E, 1998, EspE, a novel secreted protein of attaching and effacing bacteria, is directly translocated into infected host cells, where it appears as a tyrosine-phosphorylated 90kDa protein, Mol. Microbiol. 28: 463–474.PubMedGoogle Scholar
  39. Delor, I., and Cornelis, G.R., 1992, Role of Yersinia enterocolitica Yst toxin in experimental infection of young rabbits, Infect. Immun. 60: 4269–4277.PubMedGoogle Scholar
  40. Demuth, A., Goebel, W., Beuscher, H.U., and Kuhn, M., 1996, Differential regulation of cytokine and cytokine receptor mRNA expression upon infection of bone marrow-derived macrophages with Listeria monocytogenes, Infect. Immun. 64: 3475–3483.PubMedGoogle Scholar
  41. Dunlevy, J.R., and Couchman, J.R., 1993, Controlled induction of focal adhesion disassembly and migration in primary fibroblasts, J. Cell Sci. 105: 489–500.PubMedGoogle Scholar
  42. Emödy, L., Heesemann, J., Wolf-Watz, H., Skurnik, M., Kapperud, G., O’Toole, P., and Wadstrom, T., 1989, Binding to collagen by Yersinia enterocolitica and Yersinia pseudotuberculosis: evidence for yopA-mediated and chromosomally encoded mechanisms, J. Bacteriol. 171: 6674–6679.PubMedGoogle Scholar
  43. Fällman, M., Andersson, K., Häkansson, S., Magnusson, K.E., Stendahl, O., and Wolf-Watz, H., 1995, Yersinia pseudotuberculosis inhibits Fc receptor-mediated phagocytosis in J774 cells, Infect. Immun. 63: 3117–3124.Google Scholar
  44. Fällman, M., Persson, C., and Wolf-Watz, H., 1997, Yersinia proteins that target host cell signaling pathways, J. Clin. Invest. 99: 1153–1157.PubMedGoogle Scholar
  45. Fields, K.A., Plano, G.V., and Straley, S.C., 1994, A low-Ca’ response (LCR) secretion (ysc) locus lies within the lcrB region of the LCR plasmid in Yersinia pestis, J. Bacteriol. 176: 569–579.PubMedGoogle Scholar
  46. Forsberg, A., and Wolf-Watz, H., 1988, The virulence protein YopS of Yersinia pseudotuberculosis is regulated at transcriptional level by plasmid-plB1-encoded trans-acting elements controlled by temperature and calcium, Mol. Microbiol. 2: 121–133.PubMedGoogle Scholar
  47. Forsberg, A., Viitanen, A.M., Skurnik, M., and Wolf-Watz, H., 1991, The surface-located YopN protein is involved in calcium signal transduction in Yersinia pseudotuberculosis, Mol. Microbiol. 5: 977–986.PubMedGoogle Scholar
  48. Foster, R., Thorner, J., and Martin, G.S., 1989, Nucleotidylation, not phosphorylation, is the major source of the phosphotyrosine detected in enteric bacteria, J. Bacteriol. 171: 272–279.PubMedGoogle Scholar
  49. Frithz-Lindsten, E., Du, Y., Rosqvist, R., and Forsberg, A., 1997, Intracellular targeting of exoenzyme S of Pseudomonas aeruginosa via type III-dependent translocation induces phagocytosis resistance, cytotoxicity and disruption of actin microfilaments, Mol. Microbiol. 25: 1125–1139.PubMedGoogle Scholar
  50. Fu, Y., and Galan, J.E., 1998, The Salmonella typhimurium tyrosine phosphatase SptP is translocated into host cells and disrupts the actin cytoskeleton, Mol. Microbiol. 27: 359–368.PubMedGoogle Scholar
  51. Galyov, E.E., Hdkansson, S., Forsberg, A., and Wolf-Watz, H., 1993, A secreted protein kinase of Yersinia pseudotuberculosis is an indispensable virulence determinant, Nature 361: 730–732.PubMedGoogle Scholar
  52. Galyov, E.E., HAkansson, S., and Wolf-Watz, H., 1994, Characterization of the operon encoding the YpkA Ser/Thr protein kinase and the YopJ protein of Yersinia pseudotuberculosis, J. Bacteriol. 176: 4543–4548.PubMedGoogle Scholar
  53. Gemski, P., Lazere, J.R., and Casey, T., 1980a, Plasmid associated with pathogenicity and calcium dependency of Yersinia enterocolitica, Infect. Immun. 27: 682–685.PubMedGoogle Scholar
  54. Gemski, P., Lazere, J.R., Casey, T., and Wohlhieter, J.A.,1980b, Presence of a virulence-associated plasmid in Yersinia pseudotuberculosis, Infect. Immun. 28: 1044–1047.Google Scholar
  55. Goguen, J.D., Walker, W.S., Hatch, T.P., and Yother, J., 1986, Plasmid-determined cytotoxicity in Yersinia pestis and Yersinia pseudotuberculosis, Infect. Immun. 51: 788–794.PubMedGoogle Scholar
  56. Gralnick, H.R., Williams, S., McKeown, L.P., Hansmann, K., Fenton II, J.W., and Krutzsch, H., 1994, High-affinity a-thrombin binding to platelet glycoprotein Iba: identification of two binding domains, Proc. Natl. Acad. Sci. USA 91: 6334–6338.Google Scholar
  57. Green, S.P., Hartland, E.L., Robins Browne, R.M., and Phillips, W.A., 1995, Role of YopH in the suppression of tyrosine phosphorylation and respiratory burst activity in murine macrophages infected with Yersinia enterocolitica, J. Leukoc. Biol. 57: 972–977.PubMedGoogle Scholar
  58. Grützkau, A., Hanski, C., Hahn, H., and Riecken, E.O., 1990, Involvement of M cells in the bacterial invasion of Peyer’s patches: a common mechanism shared by Yersinia enterocolitica and other enteroinvasive bacteria, GUT 31: 1011–1015.PubMedGoogle Scholar
  59. Guan, K.L., and Dixon, J.E., 1990, Protein tyrosine phosphatase activity of an essential virulence determinant in Yersinia, Science 249: 553–556.PubMedGoogle Scholar
  60. Guan, K.L., and Dixon, J.E., 1991, Evidence for protein-tyrosine-phosphatase catalysis proceeding via a cysteine-phosphate intermediate, J. Biol. Chem. 266: 17026–17030.PubMedGoogle Scholar
  61. Haimovich, B., Regan, C., DiFazio, L., Ginalis, E., Ji, P., Purohit, U., Rowley, R.B., Bolen, J., and Greco, R., 1996, The FcyRII receptor triggers pp125F^K phosphorylation in platelets, J. Biol. Chem. 271: 16332–16337.PubMedGoogle Scholar
  62. Hâkansson, S., Bergman, T., Vanooteghem, J.-C., Cornelis, G., and Wolf-Watz, H., 1993, YopB and YopD constitute a novel class of Yersinia Yop proteins, Infect. Immun. 61: 71–80.PubMedGoogle Scholar
  63. Hâkansson, S., Galyov, E.E., Rosqvist, R., and Wolf-Watz, H., 1996a, The Yersinia YpkA Ser/Thr kinase is translocated and subsequently targeted to the inner surface of the HeLa cell plasma membrane, Mol. Microbiol. 20: 593–603.PubMedGoogle Scholar
  64. Hâkansson, S., Schesser, K., Persson, C., Galyov, E.E., Rosqvist, R., Homble, E, and Wolf-Watz, H., 1996b, The YopB protein of Yersinia pseudotuberculosis is essential for the translocation of Yop effector proteins across the target cell plasma membrane and displays a contact dependent membrane disrupting activity, EMBO J. 15: 5812–5823.PubMedGoogle Scholar
  65. Han, Y.W., and Miller, V.L., 1997, Reevaluation of the virulence phenotype of the inv yadA double mutants of Yersinia pseudotuberculosis, Infect. Immun. 65: 327–330.PubMedGoogle Scholar
  66. Hanski, C., Kutschka, U., Schmoranzer, H.P., Naumann, M., Stallmach, A., Hahn, H., Menge, H., and Riecken, E.O., 1989, Immunohistochemical and electron microscopic study of interaction of Yersinia enterocolitica serotype 0:8 with intestinal mucosa during experimental enteritis, Infect. Immun. 57: 673–678.Google Scholar
  67. Hartland, E.L., Green, S.P., Phillips, W.A., and Robins Browne, R.M., 1994, Essential role of YopD in inhibition of the respiratory burst of macrophages by Yersinia enterocolitica, Infect. Immun. 62: 4445–4453.PubMedGoogle Scholar
  68. Heesemann, J., and Grater, L., 1987, Genetic evidence that the outer membrane protein Yopl of Yersinia enterocolitica mediates adherence and phagocytosis resistance to human epithelial cells, FEMS Microbiol. Letts. 40: 37–41.Google Scholar
  69. Holmström, A., Pettersson, J., Rosqvist, R., Hâkansson, S., Tafazoli, E, Fällman, M., Magnusson, K.E., Wolf-Watz, H., and Forsberg, A., 1997, YopK of Yersinia pseudotuberculosis controls translocation of Yop effectors across the eukaryotic cell membrane, Mol. Microbiol. 24: 73–91.PubMedGoogle Scholar
  70. Iriarte, M., and Cornelis, G.R., 1995, MyfF, an element of the network regulating the synthesis of fibrillae in Yersinia enterocolitica, J. Bacteriol. 177: 738–744.PubMedGoogle Scholar
  71. Iriarte, M., and Cornelis, G.R., 1998, YopT, a new Yersinia Yop effector protein, affects the cytoskeleton of host cells. Mol. Microbiol. in press.Google Scholar
  72. Iriarte, M., Vanooteghem, J.-C., Delor, I., Diaz, R., Knutton, S., and Cornelis, G.R., 1993, The Myf fibrillae of Yersinia enterocolitica, Mol. Microbiol. 9: 507–520.PubMedGoogle Scholar
  73. Iriarte, M., Sory, M.-P, Boland, A., Boyd, A.P., Mills, S.D., Lambermont, I., and Cornelis, G.R., 1998, TyeA, a protein involved in control of Yop release and in translocation of Yersinia Yop effectors, EMBO J. 17: 1907–1918.PubMedGoogle Scholar
  74. Isberg, R.R., and Falkow, S., 1985, A single genetic locus encoded by Yersinia pseudotuberculosis permits invasion of cultured animal cells by Escherichia coli K-12. Nature 317: 262–264.PubMedGoogle Scholar
  75. Isberg, R.R., and Leong, J.M., 1990, Multiple ß, chain integrins are receptors for invasin, a protein that promotes bacterial penetration into mammalian cells, Cell 60: 861–871.PubMedGoogle Scholar
  76. Isberg, R.R., and Tran Van Nhieu, G., 1995, The mechanism of phagocytic uptake promoted by invasin-integrin interaction, Trends Cell Biol. 5: 120–124.PubMedGoogle Scholar
  77. 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.PubMedGoogle Scholar
  78. Isberg, R.R., Swain, A., and Falkow, S., 1988, Analysis of expression and thermoregulation of the Yersinia pseudotuberculosis inv gene with hybrid proteins, Infect. Immun. 56: 2133–2138.PubMedGoogle Scholar
  79. Kapperud, G., Namork, E., and Skarpeid, H.J., 1985, Temperature-inducible surface fibrillae associated with the virulence plasmid of Yersinia entercolitica and Yersinia pseudotuberculosis, Infect. Immun. 47: 561–566.PubMedGoogle Scholar
  80. Kobe, B., and Deisenhofer, J., 1994, The leucine-rich repeat: a versatile binding motif, Trends Biochem. Sci. 19: 415–420.PubMedGoogle Scholar
  81. Koster, M., Bitter, W., de Cock, H., Allaoui, A., Cornelis, G.R., and Tommassen, J., 1997, The outer membrane component, YscC, of the Yop secretion machinery of Yersinia enterocolitica forms a ring-shaped multimeric complex, Mol. Microbiol. 26: 789–798.PubMedGoogle Scholar
  82. Lachica, R.V., Zink, D.L., and Ferris, W.R., 1984, Association of fibril structure formation with cell surface properties of Yersinia enterocolitica, Infect. Immun. 46: 272–275.PubMedGoogle Scholar
  83. Lambert de Rouvroit, C.L., Sluiters, C., and Cornelis, G.R., 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.Google Scholar
  84. Lee, C., 1997, Type III secretion systems: machines to deliver bacterial proteins into eukaryotic cells? Trends Microbiol. 5: 148–155.PubMedGoogle Scholar
  85. Lee, V.T., Anderson, D.M., and Schneewind, 0., 1998, Targeting of Yersinia Yop proteins into the cytosol of HeLa cells: one-step translocation of YopE across bacterial and eukaryotic membranes is dependent on SycE chaperone, Mol. Microbiol. 28: 593–601.PubMedGoogle Scholar
  86. Leong, J.M., Fournier, R.S., and Isberg, R.R., 1990, Identification of the integrin binding domain of the Yersinia pseudotuberculosis invasin protein, EMBO J. 9: 1979–1989.PubMedGoogle Scholar
  87. Leong, J.M., Morrissey, P.E., and Isberg, R.R., 1993, A 76-amino acid disulfide loop in the Yersinia pseudotuberculosis invasin protein is required for integrin receptor recognition, J. Biol. Chem. 268: 20524–20532.PubMedGoogle Scholar
  88. Leong, J.M., Morrissey, P.E.; Marra, A., and Isberg, R.R., 1995, An aspartate residue of the Yersinia pseudotuberculosis invasin protein that is critical for integrin binding, EMBO J. 14: 422–431.PubMedGoogle Scholar
  89. Leung, K.Y., and Straley, S.C., 1989, The yopM gene of Yersinia pestis encodes a released protein having homology with the human platelet surface protein GPIba, J. Bacteriol. 171: 4623–4632.PubMedGoogle Scholar
  90. Leung, K.Y., Reisner, B.S., and Straley, S.C., 1990, YopM inhibits platelet aggregation and is necessary for virulence of Yersinia pestis in mice, Infect. Immun. 58: 3262–3271.PubMedGoogle Scholar
  91. Lian, C.J., and Pai, C.H., 1985, Inhibition of human neutrophil chemiluminescence by plasmid-mediated outer membrane proteins of Yersinia enterocolitica, Infect. Immun. 49: 145–151.PubMedGoogle Scholar
  92. Lian, C.J., Hwang, W.S., and Pai, C.H., 1987, Plasmid-mediated resistance to phagocytosis in Yersinia enterocolitica, Infect. Immun. 55: 1176–1183.PubMedGoogle Scholar
  93. 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.Google Scholar
  94. Mantle,M., Basaraba, L., Peacock, S.C., and Gall, D.G., 1989, Binding of Yersinia enterocolitica to rabbit intestinal brush border membranes, mucus, and mucin, Infect. Immun. 57:3292–3299.Google Scholar
  95. Marra, A., and Isberg, R.R., 1997, Invasin-dependent and invasin-independent pathways for translocation of Yersinia pseudotuberculosis across the Peyer’s patch intestinal epithelium, Infect. Immun. 65: 3412–3421.PubMedGoogle Scholar
  96. Michiels, T., and Cornelis, G., 1988, Nucleotide sequence and transcription analysis of yop51 from Yersinia enterocolitica W22703, Microb. Pathog. 5: 449–459.PubMedGoogle Scholar
  97. Michiels, T., and Cornelis, G.R., 1991, Secretion of hybrid proteins by the Yersinia Yop export system, J. Bacteriol. 173: 1677–1685.PubMedGoogle Scholar
  98. Michiels, T., Wattiau, P., Brasseur, R., Ruysschaert, J.M., and Cornelis, G., 1990, Secretion of Yop proteins by Yersiniae, Infect. Immun. 58: 2840–2849.PubMedGoogle Scholar
  99. Michiels, T., Vanooteghem, J.-C., Lambert de Rouvroit, C.L., China, B., Gustin, A., Boudry, P., and Cornelis, G.R., 1991, Analysis of virC, an operon involved in the secretion of Yop proteins by Yersinia enterocolitica, J. Bacteriol. 173: 4994–5009.PubMedGoogle Scholar
  100. Miller, V.L., and Falkow, S., 1988, Evidence for two genetic loci in Yersinia enterocolitica that can promote invasion of epithelial cells, Infect. Immun. 56: 1242–1248.PubMedGoogle Scholar
  101. Mills, S.D., Boland, A., Sory, M.-P., Van der Smissen, P., Kerbourch, C., Finlay, B.B., and Cornelis, G.R., 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.Google Scholar
  102. Mittler, R., and Lam, E., 1996, Sacrifice in the face of foes: pathogen-induced programmed cell death in plants, Trends. MicrobioL 4: 10–15.PubMedGoogle Scholar
  103. Monack, D.M., Mecsas, J., Ghori, N., and Falkow, S., 1997, Yersinia signals macrophages to undergo apoptosis and YopJ is necessary for this cell death, Proc. Natl. Acad. Sci. USA 94: 10385–10390.PubMedGoogle Scholar
  104. Nakajima, R., and Brubaker, R.R., 1993, Association between virulence of Yersinia pestis and suppression of gamma interferon and tumor necrosis factor alpha, Infect. Immun. 61: 23–31.PubMedGoogle Scholar
  105. Nakajima, R., Motin, V.L., and Brubaker, R.R., 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.PubMedGoogle Scholar
  106. Nilles, M.L., Williams, A.W., Skrzypek, E., and Straley, S.C., 1997, Yersinia pestis LcrV forms a stable complex with LcrG and may have a secretion-related regulatory role in the lowCa2 response, J. Bacteriol. 179: 1307–1316.Google Scholar
  107. Palmer, L.E., Hobbie, S., Galan, J.E., and Bliska, J.B., 1998, YopJ of Yersinia pseudotuberculosis is required for the inhibition of macrophage TNFtx production and downregulation of the MAP kinases p38 and JNK, Mol. MicrobioL 27: 953–965.PubMedGoogle Scholar
  108. Pepe, J.C., and Miller, V.L., 1993, Yersinia enterocolitica invasin: a primary role in the initiation of infection, Proc. Natl. Acad. Sci. USA 90: 6473–6477.Google Scholar
  109. Pepe, J.C., Badger, J.L., and Miller, V.L., 1994, Growth phase and low pH affect the thermal regulation of the Yersinia enterocolitica inv gene, Mol. Microbiol. 11: 123–135.PubMedGoogle Scholar
  110. Pepe, J.C., Wachtel, M.R., Wagar, E., and Miller, V.L., 1995, Pathogenesis of defined invasion mutants of Yersinia enterocolitica in a BALB/c mouse model of infection, Infect. Immun. 63: 4837–4848.PubMedGoogle Scholar
  111. Perona, R., Montaner, S., Saniger, L., Sanchez Perez, I., Bravo, R., and Lacal, J.C., 1997, Activation of the nuclear factor-kB by Rho, CDC42, and Rac-1 proteins, Genes. Dev. 11: 463–475.PubMedGoogle Scholar
  112. Perry, R.D., and Brubaker, R.R., 1983, Vwa+ phenotype of Yersinia enterocolitica, Infect. Immun. 40: 166–171.PubMedGoogle Scholar
  113. Persson, C., Nordfelth, R., Holmström, A., Häkansson, S., Rosqvist, R., and Wolf-Watz, H., 1995, Cell-surface-bound Yersinia translocate the protein tyrosine phosphatase YopH by a polarized mechanism into the target cell, Mol. Microbiol. 18: 135–150.PubMedGoogle Scholar
  114. Persson, C., Carballeira, N., Wolf-Watz, H., and Fällman, M., 1997, The PTPase YopH inhibits uptake of Yersinia, tyrosine phosphorylation of p130ce5 and FAK, and the associated accumulation of these proteins in peripheral focal adhesions, EMBO J. 16: 2307–2318.PubMedGoogle Scholar
  115. Petruzzelli, L., Takami, M., and Herrera, R., 1996, Adhesion through the interaction of lymphocyte function-associated antigen-1 with intracellular adhesion molecule-1 induces tyrosine phosphorylation of p130`°s and its association with c-CrkII, J. Biol. Chem. 271: 7796–7801.PubMedGoogle Scholar
  116. Pettersson, J., Nordfelth, R., Dubinina, E., Bergman, T., Gustafsson, M., Magnusson, K.E., and Wolf-Watz, H., 1996, Modulation of virulence factor expression by pathogen target cell contact, Science 273: 1231–1233.PubMedGoogle Scholar
  117. Plano, G.V., and Straley, S.C., 1993, Multiple effects of lcrD mutations in Yersinia pestis, J. Bacteriol. 175: 3536–3545.PubMedGoogle Scholar
  118. Plano, G.V., and Straley, S.C., 1995, Mutations in yscC, yscD, and yscG prevent high-level expression and secretion of V antigen and Yops in Yersinia pestis, J. Bacteriol. 177: 3843–3854.PubMedGoogle Scholar
  119. Plano, G.V., Barve, S.S., and Straley, S.C., 1991, LcrD, a membrane-bound regulator of the Yersinia pestis low-calcium response, J. Bacteriol. 173: 7293–7303.PubMedGoogle Scholar
  120. Portnoy, D.A., and Falkow, S., 1981, Virulence-associated plasmids from Yersinia enterocolitica and Yersinia pestis, J. Bacteriol. 148: 877–883.PubMedGoogle Scholar
  121. Reisner, B.S., and Straley, S.C., 1992, Yersinia pestis YopM: thrombin binding and overexpression, Infect. Immun. 60: 5242–5252.Google Scholar
  122. Roggenkamp, A., Neuberger, H.R., Flugel, A., Schmoll, T., and Heesemann, J., 1995, Substitution of two histidine residues in YadA protein of Yersinia enterocolitica abrogates collagen binding, cell adherence and mouse virulence, Mol. Microbiol. 16: 1207–1219.PubMedGoogle Scholar
  123. Roggenkamp, A., Ruckdeschel, K., Leitritz, L., Schmitt, R., and Heesemann, J., 1996, Deletion of amino acids 29 to 81 in adhesion protein YadA of Yersinia enterocolitica serotype 0:8 results in selective abrogation of adherence to neutrophils, Infect. Immun. 64: 2506–2514.PubMedGoogle Scholar
  124. Rosenshine, I., Duronio, V., and Finlay, B.B., 1992, Tyrosine protein kinase inhibitors block invasin-promoted bacterial uptake by epithelial cells, Infect. Immun. 60: 2211–2217.PubMedGoogle Scholar
  125. Rosqvist, R., Bölin, I., and Wolf-Watz, H., 1988, Inhibition of phagocytosis in Yersinia pseudo-tuberculosis: a virulence plasmid-encoded ability involving the Yop2b protein, Infect. Immun. 56: 2139–2143.PubMedGoogle Scholar
  126. Rosqvist, R., Forsberg, A., Rimpilainen, M., Bergman, T., and Wolf-Watz, H., 1990, The cytotoxic protein YopE of Yersinia obstructs the primary host defence, Mol. Microbiol. 4: 657–667.PubMedGoogle Scholar
  127. Rosqvist, R., Forsberg, A., and Wolf-Watz, H., 1991, Intracellular targeting of the Yersinia YopE cytotoxin in mammalian cells induces actin microfilament disruption, Infect. Immun. 59: 4562–4569.PubMedGoogle Scholar
  128. Rosqvist, R., Magnusson, K.E., and Wolf-Watz, H., 1994, Target cell contact triggers expression and polarized transfer of Yersinia YopE cytotoxin into mammalian cells, EMBO J. 13: 964–972.PubMedGoogle Scholar
  129. Ruckdeschel, K., Roggenkamp, A., Schubert, S., and Heesemann, J., 1996, Differential contribution of Yersinia enterocolitica virulence factors to evasion of microbicidal action of neutrophils, Infect. Immun. 64: 724–733.PubMedGoogle Scholar
  130. Ruckdeschel, K., Machold, J., Roggenkamp, A., Schubert, S., Pierre, J., Zumbihl, R., Liautard, J.-P., Heesemann, J., and Rouot, B., 1997a, Yersinia enterocolitica promotes deactivation of macrophage mitogen-activated protein kinases extracellular signal-regulated kinase-1/2, p38, and c-Jun NH2-terminal kinase, J. Biol. Chem. 272: 15920–15927.Google Scholar
  131. Ruckdeschel, K., Roggenkamp, A., Lafont, V., Mangeat, P., Heesemann, J., and Rouot, B., 1997b, Interaction of Yersinia enterocolitica with macrophages leads to macrophage cell death through apoptosis, Infect. Immun. 65: 4813–4821.PubMedGoogle Scholar
  132. Ruckdeschel, K., Harb, S., Roggenkamp, A., Hornef, M., Zumbihl, R., Köhler, S., Heesemann, J., and Rouot, B., 1998, Yersinia enterocolitica impairs activation of transcription factor NF-KB: involvement in the induction of programmed cell death and in the suppression of the macrophage tumor necrosis factor a production, J. Exp. Med. 187: 1069–1079.Google Scholar
  133. Salmond, G.P., and Reeves, P.J., 1993, Membrane traffic ‘wardens and protein secretion in gram-negative bacteria, Trends Biochem. Sci. 18: 7–12.Google Scholar
  134. Saltman, L.H., Lu, Y., Zaharias, E.M., and Isberg, R.R., 1996, A region of the Yersinia pseudo-tuberculosis invasin protein that contributes to high affinity binding to integrin receptors, J. Biol. Chem. 271: 23438–23444.PubMedGoogle Scholar
  135. Sarker, M.R., Neyt, C., Stainier, I., and Cornelis, G.R., 1998a, The Yersinia Yop virulon: LcrV is required for extrusion of the translocators YopB and YopD, J. Bacteriol. 180: 1207–1214.PubMedGoogle Scholar
  136. Sarker, M.R., Sory, M.-P., Boyd, A.P., Iriarte, M., and Cornelis, G.R., 1998b, LcrG is required for efficient internalization of Yersinia Yop effector proteins into eukaryotic cells, Infect. Immun. 66: 2976–2979.PubMedGoogle Scholar
  137. Schesser, K., Frithz-Lindsten, E., and Wolf-Watz, H., 1996, Delineation and mutational analysis of the Yersinia pseudotuberculosis YopE domains which mediate translocation across bacterial and eukaryotic cellular membranes, J. Bacteriol. 178: 7227–7233.PubMedGoogle Scholar
  138. Schesser, K., Spiik, A.-K., Dukuzumuremyi, J.-M., Neurath, M.F., Pettersson, S., and Wolf-Watz, H., 1998, The yopJ locus is required for Yersinia-mediated inhibition of NF-KB activation and cytokine expression: YopJ contains a eukaryotic SH2-like domain that is essential for its repressive activity, Mol. Microbiol. 28: 1067–1079.PubMedGoogle Scholar
  139. Schulze-Koops, H., Burkhardt, H., Heesemann, J., von der Mark, K., and Emmrich, F, 1992, Plasmid-encoded outer membrane protein YadA mediates specific binding of enteropathogenic Yersiniae to various types of collagen, Infect. Immun. 60: 2153–2159.PubMedGoogle Scholar
  140. Schulze-Koops, H., Burkhardt, H., Heesemann, J., Kirsch, T., Swoboda, B., Bull, C., Goodman, S., and Emmrich, F, 1993, Outer membrane protein YadA of enteropathogenic Yersiniae mediates specific binding to cellular but not plasma fibronectin, Infect. Immun. 61: 2513–2519.PubMedGoogle Scholar
  141. Shi, L., Mai, S., Israels, S., Browne, K., Trapani, J.A., and Greenberg, A.H., 1997, Granzyme B (GraB) autonomously crosses the cell membrane and perforin initiates apoptosis and GraB nuclear localization, J. Exp. Med. 185: 855–866.PubMedGoogle Scholar
  142. Siebers, A., and Finlay, B.B., 1996, M cells and the pathogenesis of mucosal and systemic infections, Trends. Microbiol. 4: 22–29.PubMedGoogle Scholar
  143. Simonet, M., Richard, S., and Berche, P., 1990, Electron microscopic evidence for in vivo extra-cellular localization of Yersinia pseudotuberculosis harboring the pYV plasmid, Infect. Immun. 58: 841–845.PubMedGoogle Scholar
  144. Simonet, M., Riot, B., Fortineau, N., and Berche, P., 1996, Invasin production by Yersinia pestis is abolished by insertion of an IS200-like element within the inv gene, Infect. Immun. 64: 375–379.PubMedGoogle Scholar
  145. Skrzypek, E., and Straley, S.C., 1993, LcrG, a secreted protein involved in negative regulation of the low-calcium response in Yersinia pestis, J. Bacteriol. 175: 3520–3528.Google Scholar
  146. Skurnik, M., and Wolf-Watz, H., 1989, Analysis of the yopA gene encoding the Yopl virulence determinants of Yersinia spp, Mol. Microbiol. 3: 517–529.Google Scholar
  147. Skurnik, M., Bölin, I., Heikkinen, H., Piha, S., and Wolf-Watz, H., 1984, Virulence plasmid-associated autoagglutination in Yersinia spp, J. Bacteriol. 158: 1033–1036.PubMedGoogle Scholar
  148. Skurnik, M., el Tahir, Y., Saarinen, M., Jalkanen, S., and Toivanen, P., 1994, YadA mediates specific binding of enteropathogenic Yersinia enterocolitica to human intestinal submucosa. Infect. Immun. 62: 1252–1261.PubMedGoogle Scholar
  149. Smith, G.L., 1994, Virus strategies for evasion of the host response to infection, Trends Microbiol. 2: 81–88.PubMedGoogle Scholar
  150. Sory, M.-P., and Cornelis, G.R., 1994, Translocation of a hybrid YopE-adenylate cyclase from Yersinia enterocolitica into HeLa cells, Mol. Microbio!. 14: 583–594.Google Scholar
  151. Sory, M.-P, Boland, A., Lambermont, I., and Cornelis, G.R., 1995, Identification of the YopE and YopH domains required for secretion and internalization into the cytosol of macrophages, using the cyaA gene fusion approach, Proc. Natl. Acad. Sci. USA 92: 11998–12002.PubMedGoogle Scholar
  152. Stainier, I., Iriarte, M., and Cornelis, G.R., 1997, YscMl and YscM2, two Yersinia enterocolit- ica proteins causing down regulation of yop transcription, Mol. Microbiol. 26: 833–843.PubMedGoogle Scholar
  153. Straley, S.C., and Bowmer, W.S.,1986, Virulence genes regulated at the transcriptional level by Cat+ in Yersinia pestis include structural genes for outer membrane proteins, Infect. Immun. 51: 445–454.Google Scholar
  154. Symons, M., 1996, Rho family GTPases: the cytoskeleton and beyond, Trends. Biochem. Sci. 21: 178–181.PubMedGoogle Scholar
  155. Tamm, A., Tarkkanen, A.M., Korhonen, T.K., Kuusela, P., Toivanen, P., and Skurnik, M., 1993, Hydrophobic domains affect the collagen-binding specificity and surface polymerization as well as the virulence potential of the YadA protein of Yersinia enterocolitica, Mol. Microbiol. 10: 995–1011.PubMedGoogle Scholar
  156. Tang, X., Frederick, R.D., Zhou, J., Halterman, D.A., Jia, Y., and Martin, G.B., 1996, Initiation of plant disease resistance by physical interaction of AvrPto and Pto kinase, Science 274: 2060–2063.PubMedGoogle Scholar
  157. Tertti, R., Skurnik, M., Vartio, T., and Kuusela, P., 1992, Adhesion protein YadA of Yersinia species mediates binding of bacteria to fibronectin, Infect. Immun. 60: 3021–3024.PubMedGoogle Scholar
  158. Van Antwerp, D.J., Martin, S.J., Verma, I.M., and Green, D.R., 1998, Inhibition of TNF-a induced apoptosis by NF-KB, Trends Cell Biol. 8: 107–111.PubMedGoogle Scholar
  159. Van den Ackerveken, G., Marois, E., and Bonas, U., 1996, Recognition of the bacterial avirulence protein AvrBs3 occurs inside the host plant cell, Cell 87: 1307–1316.PubMedGoogle Scholar
  160. Vassalli, P., 1992, The pathophysiology of tumor necrosis factors, Annu. Rev. Immunol. 10: 411–452.PubMedGoogle Scholar
  161. Visser, L.G., Annema, A., and van Furth, R., 1995, Role of Yops in inhibition of phagocytosis and killing of opsonized Yersinia enterocolitica by human granulocytes, Infect. Immun. 63: 2570–2575.PubMedGoogle Scholar
  162. Wachtel, M.R., and Miller, V.L., 1995, In vitro and in vivo characterization of an ail mutant of Yersinia enterocolitica, Infect. Immun. 63: 2541–2548.Google Scholar
  163. Wattiau, P., and Cornelis, G.R., 1993, SycE, a chaperone-like protein of Yersinia enterocolitica involved in the secretion of YopE, Mol. Microbial. 8: 123–131.Google Scholar
  164. Wattiau, P., Bernier, B., Deslee, P., Michiels, T., and Cornelis, G.R., 1994, Individual chaperones required for Yop secretion by Yersinia, Proc. Natl. Acad. Sci. USA 91: 10493–10497.PubMedGoogle Scholar
  165. Woestyn, S., Allaoui, A., Wattiau, P., and Cornelis, G.R., 1994, YscN, the putative energizer of the Yersinia Yop secretion machinery, J. Bacteriol. 176: 1561–1569.PubMedGoogle Scholar
  166. Woestyn, S., Sory, M.-P., Boland, A., Lequenne, O., and Cornelis, G.R., 1996, The cytosolic SycE and SycH chaperones of Yersinia protect the region of YopE and YopH involved in translocation across eukaryotic cell membranes, Mol. Microbiol. 20: 1261–1271.PubMedGoogle Scholar
  167. Wolff, C., Nisan, I., Hanski, E., Frankel, G., and Rosenshine, I., 1998, Protein translocation into host epithelial cells by infecting enteropathogenic Escherichia coli, Mol. Microbiol. 28: 143–155.PubMedGoogle Scholar
  168. Yang, Y., and Isberg, R.R., 1997, Transcriptional regulation of the Yersinia pseudotuberculosis pH6 antigen adhesin by two envelope-associated components, Mol. Microbiol. 24: 499–510.PubMedGoogle Scholar
  169. 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.PubMedGoogle Scholar
  170. Young, V.B., Falkow, S., and Schoolnik, G.K., 1992, The invasin protein of Yersinia enterocolitica: internalization of invasin-bearing bacteria by eukaryotic cells is associated with reorganization of the cytoskeleton, J. Cell Biol. 116: 197–207.Google Scholar
  171. Young, V.B., Miller, V.L., Falkow, S., and Schoolnik, G.K., 1990, Sequence, localization and func- tion of the invasin protein of Yersinia enterocolitica, Mol. Microbiol. 4: 1119–1128.Google Scholar
  172. Zaleska, M., Lounatmaa, K., Nurminen, M., Wahlstrom, E., and Makela, P.H., 1985, A novel virulence-associated cell surface structure composed of 47 kDa protein subunits in Yersinia enterocolitica, EMBO J. 4: 1013–1018.PubMedGoogle Scholar
  173. Zhang, Z.Y., Clemens, J.C., Schubert, H.L., Stuckey, J.A., Fischer, M.W.F., Hume, D.M., Saper, M.A., and Dixon, J.E., 1992, Expression, purification, and physicochemical characterization of a recombinant Yersinia protein tyrosine phosphatase, J. Biol. Chem. 267: 23759–23766.PubMedGoogle Scholar
  174. Zychlinsky, A., and Sansonetti, P., 1997, Apoptosis in bacterial pathogenesis, J. Clin. Invest. 100: 493–496.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2000

Authors and Affiliations

  • Anne Boland
    • 1
  • Guy R. Cornelis
    • 1
  1. 1.Microbial Pathogenesis Unit, Christian de Duve Institute of Cellular PathologyUniversité Catholique de Louvain, Facutté de MedecíneBrusselsBelgium

Personalised recommendations