Intranasal inoculation of mice with Yersinia pseudotuberculosis causes a lethal lung infection that is dependent on Yersinia outer proteins and PhoP

Infection and Immunity

Volumn 75, Issue 1, 2007, Pages 429-442

  Fisher, Michael L ^a   Castillo, Cynthia ^a   Mecsas, Joan ^a  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PHOP PROTEIN; UNCLASSIFIED DRUG; YERSINIA OUTER PROTEIN B; YERSINIA OUTER PROTEIN E; YERSINIA OUTER PROTEIN H;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL GROWTH; BACTERIAL VIRULENCE; BIRD DISEASE; COLONY FORMING UNIT; CONTROLLED STUDY; DISEASE MODEL; EFFECTOR CELL; HISTOPATHOLOGY; INOCULATION; LETHAL GENE; LUNG INFECTION; MAMMAL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; RISK FACTOR; STRAIN IDENTIFICATION; YERSINIA PSEUDOTUBERCULOSIS;

ADMINISTRATION, INTRANASAL; ANIMALS; BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL PROTEINS; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; MICE; MICE, INBRED BALB C; RESPIRATORY TRACT INFECTIONS; TRANSLOCATION, GENETIC; VIRULENCE; YERSINIA PSEUDOTUBERCULOSIS; YERSINIA PSEUDOTUBERCULOSIS INFECTIONS;

EID: 33846029503     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.01287-06     Document Type: Article

References (90)

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. Angelichio, M. J., D. S. Merrell, and A. Camilli. 2004. Spatiotemporal analysis of acid adaptation-mediated Vibrio cholerae hyperinfectivity. Infect. Immun. 72:2405-2407.
3. Anisimov, A. P., S. V. Dentovskaya, G. M. Titareva, I. V. Bakhteeva, R. Z. Shaikhutdinova, S. V. Balakhonov, B. Lindner, N. A. Kocharova, S. y. N. Senchenkova, O. Holst, G. B. Pier, and Y. A. Knirel. 2005. Intraspecies and temperature-dependent variations in susceptibility of Yersinia pestis to the bactericidal action of serum and to polymyxin B. Infect. Immun. 73:7324-7331.
4. Balada, J. M., and J. Mecsas. 2006. Yersinia has a tropism for B and T cell zones of lymph node that is independent of the type III secretion system. PLOS Pathog, in press.
5. Barz, C., T. N. Abahji, K. Trulzsch, and J. Heesemann. 2000. The Yersinia Ser/Thr protein kinase YpkA/YopO directly interacts with the small GTPases RhoA and Rac-1. FEBS Lett. 482:139-143.
6. Bengoechea, J., B. Lindner, U. Seydel, R. Diaz, and I. Moriyon. 1998. Yersinia pseudotuberculosis and Yersinia pestis are more resistant to bactericidal cationic peptides than Yersinia enterocolitica. Microbiology 144:1509-1515.
7. Bigler, R. D., R. R. Atkins, and E. J. Wing. 1981. Yersinia enterocolitica lung infection. Arch. Intern. Med. 141:1529-1530.
8. Black, D. S., and J. B. Bliska. 2000. The RhoGAP activity of the Yersinia pseudotuberculosis cytotoxin YopE is required for antiphagocytic function and virulence. Mol. Microbiol. 37:515-527.
9. Bliska, J., K. Guan, J. 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.
10. Bolin, I., L. Norlander, and H. Wolf-Watz. 1982. Temperature-inducible outer membrane protein of Yersinia pseudotuberculosis and Yersinia enterocolitica is associated with the virulence plasmid. Infect. Immun. 37:506-512.
11. Bottone, E. J. 1997. Yersinia enterocolitica: the charisma continues. Clin. Microbiol. Rev. 10:257-276.
12. Bresnahan, J. F., U. G. Whitworth, Y. Hayes, E. Summers, and J. Pollock. 1984. Yersinia enterocolitica infection in breeding colonies of ruffed lemurs. J. Am. Vet. Med. Assoc. 185:1354-1356.
13. Butler, S. M., and A. Camilli. 2004. Both chemotaxis and net motility greatly influence the infectivity of Vibrio cholerae. Proc. Natl. Acad. Sci. USA 101: 5018-5023.
14. Carnoy, C., C. Mullet, H. Muller-Alouf, E. Leteurtre, and M. Simonet. 2000. Superantigen YPMa exacerbates the virulence of Yersinia pseudotuberculosis in mice. Infect. Immun. 68:2553-2559.
15. 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. 83:348-363.
16. Chen, T. H., and S. S. Elberg. 1977. Scanning electron microscopic study of virulent Yersinia pestis and Yersinia pseudotuberculosis type 1. Infect. Immun. 15:972-977.
17. Chiavolini, D., G. Memmi, T. Maggi, F. Iannelli, G. Pozzi, and M. Oggioni. 2003. The three extra-cellular zinc metalloproteinases of Streptococcus pneumoniae have a different impact on virulence in mice. BMC Microbiol. 3:14.
18. Cornelis, G., J.-C. Vanootegem, and C. Sluiters. 1987. Transcription of the yop regulon from Y. enterocolitica requires trans acting pYV and chromosomal genes. Microb. Pathog. 2:367-379.
19. Cornelis, G. R. 2000. Molecular and cell biology aspects of plague. Proc. Natl. Acad. Sci. USA 97:8778-8783.
20. Di Genaro, M. S., M. E. Escudero, C. Aguilera, L. Scardapane, and A. M. de Guzman. 1998, Intranasal immunization with Yersinia enterocolitica O:8 cellular extract protects against local challenge infection. Microbiol. Immunol. 42:781-788.
21. Doll, J. M., P. S. Zeitz, P. Ettestad, A. L. Bucholtz, T. Davis, and K. Gage. 1994. Cat-transmitted fatal pneumonic plague in a person who traveled from Colorado to Arizona. Am. J. Trop. Med. Hyg. 51:109-114.
22. Eskay, R. L., M. Grino, and H. T. Chen. 1990. Interleukins, signal transduction, and the immune system-mediated stress response. Adv. Exp. Med. Biol. 274:331-343.
23. Fingold, J. M. 1969. Pneumonic plague in monkeys. An electron microscopic study. Am. J. Pathol. 54:167-183.
24. Fullner, K. J., J. C. Boucher, M. A. Hanes, G. K. Haines, III, B. M. Meehan, C. Walchle, P. J. Sansonetti, and J. J. Mekalanos. 2002. The contribution of accessory toxins of Vibrio cholerae O1 El Tor to the proinflammatory response in a murine pulmonary cholera model. J. Exp. Med. 195:1455-1462. doi:10.1084/jem.20020318.
25. George, S. E., M. J. Kohan, M. I. Gilmour, M. S. Taylor, H. G. Brooks, J. P. Creason, and L. D. Claxton. 1993. Pulmonary clearance and inflammatory response in C3H/HeJ mice after intranasal exposure to Pseudomonas spp. Appl. Environ. Microbiol. 59:3585-3591.
26. George, S. E., M. J. Kohan, D. A. Whitehouse, J. P. Creason, C. Y. Kawanishi, R. L. Sherwood, and L. D. Claxton. 1991. Distribution, clearance, and mortality of environmental pseudomonads in mice upon intranasal exposure. Appl. Environ. Microbiol. 57:2420-2425.
27. Grabenstein, Jens, P., M. Marceau, C. Pujol, M. Simonet, and J. B. Bliska. 2004. The response regulator PhoP of Yersinia pseudotuberculosis is important for replication in macrophages and for virulence. Infect. Immun. 72: 4973-4984.
28. Grabenstein, Jens P., H. S. Fukuto, L. E. Palmer, and J. B. Bliska. 2006. Characterization of phagosome trafficking and identification of PhoP-regulated genes important for survival of Yersinia pestis in macrophages. Infect. Immun. 74:3727-3741.
29. Groisman, E. A. 2001. The pleiotropic two-component regulatory system PhoP-PhoQ. J. Bacteriol. 183:1835-1842.
30. 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. 70:4165-4176.
31. Guarner, J., W. Shieh, P. Greer, J. Gabastou, M. Chu, E. Hayes, K. Nolte, and S. Zaki. 2002. Immunohistochemical detection of Yersinia pestis in formalin-fixed, paraffin-embedded tissue. Anat. Pathol. 117:205-209.
32. Guirado, E., S. Gordillo, O. Gil, J. Diaz, G. Tapia, C. Vilaplana, V. Ausina, and P.-J. Cardona. 2006. Intragranulomatous necrosis in pulmonary granulomas is not related to resistance against Mycobacterium tuberculosis infection in experimental murine models induced by aerosol. Int. J. Exp. Pathol. 87:139-149.
33. Hagiwara, S., Y. Ishii, Y. Sugiyama, and S. Kitamura. 1995. Hypersensitivity pneumonitis caused by a home humidifier. Nihon Kyobu Shikkan Gakkai Zasshi 33:1024-1029. [In Japanese.]
34. Han, Y., and V. Miller. 1997. Reevaluation of the virulence phenotype of the inv yadA double mutants of Yersinia pseudotuberculosis. Infect. Immun. 65: 327-330.
35. Hava, D. L., and A. Camilli. 2002. Large-scale identification of serotype 4 Streptococcus pneumoniae virulence factors. Mol. Microbiol. 45:1389-1406.
36. Honko, A. N., N. Sriranganathan, C. J. Lees, and S. B. Mizel. 2006. Flagellin is an effective adjuvant for immunization against lethal respiratory challenge with Yersinia pestis. Infect. Immun. 74:1113-1120.
37. Hubbert, W. T., C. W. Petenyi, L. A. Glasgow, C. T. Uyeda, and S. A. Creighton. 1971. Yersinia pseudotuberculosis infection in the United States. Septicemia, appendicitis, and mesenteric lymphadenitis. Am. J. Trop. Med. Hyg. 20:679-684.
38. Irvin, C. G., and J. H. Bates. 15 May 2003. Measuring the lung function in the mouse: the challenge of size. Respir. Res. 4:4. [Epub ahead of print.]
39. Isberg, R. R., and J. M. Leong. 1990. Multiple beta 1 chain integrins are receptors for invasin, a protein that promotes bacterial penetration into mammalian cells. Cell 60:861-871.
40. Isberg, R. R., A. Swain, and S. Falkow. 1988. Analysis of expression and thermoregulation of the Yersinia pseudotuberculosis inv gene with hybrid proteins. Infect. Immun. 56:2133-2138.
41. Ivanov, M. I., J. A. Stuckey, H. L. Schubert, M. A. Saper, and J. B. Bliska. 2005. Two substrate-targeting sites in the Yersinia protein tyrosine phosphatase co-operate to promote bacterial virulence. Mol. Microbiol. 55:1346-1356.
42. Jones, T., J. J. Adamovicz, S. L. Cyr, C. R. Bolt, N. Bellerose, L. M. Pitt, G. H. Lowell, and D. S. Burt. 2006. Intranasal protollin (TM)/F1-V vaccine elicits respiratory and serum antibody responses and protects mice against lethal aerosolized plague infection. Vaccine 24:1625-1632.
43. Kapperud, G., E. Namork, and H. J. Skarpeid. 1985. Temperature-inducible surface fibrillae associated with the virulence plasmid of Yersinia enterocolitica and Yersinia pseudotuberculosis. Infect. Immun. 47:561-566.
44. Kawahara, K., H. Tsukano, H. Watanabe, B. Lindner, and M. Matsuura. 2002. Modification of the structure and activity of lipid A in Yersinia pestis lipopolysaccharide by growth temperature. Infect. Immun. 70:4092-4098.
45. Kerschen, E. J., D. A. Cohen, A. M. Kaplan, and S. C. Straley. 2004. The plague virulence protein YopM targets the innate immune response by causing a global depletion of NK cells. Infect. Immun. 72:4589-4602.
46. 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.
47. Lathem, W. W, S. D. Crosby, V. L. Miller, and W. E. Goldman. 2005. Progression of primary pneumonic plague: a mouse model of infection, pathology, and bacterial transcriptional activity. Proc. Natl. Acad. Sci. USA 102:17786-17791.
48. Leung, K. Y., B. S. Reisner, and S. C. Straley. 1990. YopM inhibits platelet aggregation and is necessary for virulence of Yersinia pestis in mice. Infect. Immun. 58:3262-3271.
49. Logsdon, L. K., and J. Mecsas. 2003. Requirement of the Yersinia pseudotuberculosis effectors YopH and YopE in colonization and persistence in intestinal and lymph tissues. Infect. Immun. 71:4595-4607.
50. Mair, N. S., and G. S. Ziffo. 1974. Isolation of Y. pseudotuberculosis from a foal. Vet. Rec. 94:152-153.
51. Mallett, C. P., T. L. Hale, R. W. Kaminski, T. Larsen, N. Orr, D. Cohen, and G. H. Lowell. 1995. Intransal or intragastric immunization with proteosome-Shigella lipopolysaccharide vaccines protects against lethal pneumonia in a murine model of Shigella infection. Infect. Immun. 63:2382-2386.
52. Marceau, M., F. Sebbane, F. Ewann, F. Collyn, B. Lindner, M. A. Campos, J.-A. Bengoechea, and M. Simonet. 2004. The pmrF polymyxin-resistance operon of Yersinia pseudotuberculosis is upregulated by the PhoP-PhoQ two-component system but not by PmrA-PmrB, and is not required for virulence. Microbiology 150:3947-3957.
53. Marketon, M. M., R. W. DePaolo, K. L. DeBord, B. Jabri, and O. Schneewind. 2005. Plague bacteria target immune cells during infection. Science 309: 1739-1741.
54. McDonald, C., P. O. Vacratsis, J. B. Bliska, and J. E. Dixon. 2003. The Yersinia virulence factor YopM forms a novel protein complex with two cellular kinases. J. Biol. Chem. 278:18514-18523.
55. Mecsas, J., I. Bills, and S. Falkow. 2001. Identification of attenuated Yersinia pseudotuberculosis strains and characterization of an orogastric infection in BALB/c mice on day 5 postinfection by signature-tagged mutagenesis. Infect. Immun. 69:2779-2787.
56. Monack, D. M., J. Mecsas, D. Bouley, and S. Falkow. 1998. Yersinia-induced apoptosis in vivo aids in the establishment of a systemic infection of mice. J. Exp. Med. 188:2127-2137.
57. 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.
58. Montagna, L. G., M. I. Ivanov, and J. B. Bliska. 2001. 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.
59. Najdenski, H., A. Vesselinova, E. Golkocheva, S. Garbom, and H. Wolf-Watz. 2003. Experimental infections with wild and mutant Yersinia pseudotuberculosis strains in rabbits. J. Vet. Med. Series B 50:280-288.
60. Nikolova, S., Y. Tzvetkov, H. Najdenski, and A. Vesselinova. 2001. Isolation of pathogenic yersiniae from wild animals in Bulgaria. J. Vet. Med. Series B 48:203-209.
61. Obwolo, M. J., and T. J. Gruffydd-Jones. 1977. Yersinia pseudotuberculosis in the cat. Vet. Rec. 100:424-425.
62. Orth, K. 2002. Function of the Yersinia effector YopJ. Curr. Opin. Microbiol. 5:38-43.
63. 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 protein protease. Science 290:1594-1597.
64. Oyston, P. C. F., N. Dorrell, K. Williams, S.-R. Li, M. Green, R. W. Titball, and B. W. Wren. 2000. The response regulator PhoP is important for survival under conditions of macrophage-induced stress and virulence in Yersinia pestis. Infect. Immun. 68:3419-3425.
65. Paff, J. R., D. A. Triplett, and T. N. Saari. 1976. Clinical and laboratory aspects of Yersinia pseudotuberculosis infections, with a report of two cases. Am. J. Clin. Pathol. 66:101-110.
66. Parkhill, J., B. W. Wren, N. R. Thomson, R. W. Titball, M. T. G. Holden, M. B. Prentice, M. Sebaihia, K. D. James, C. Churcher, K. L. Mungall, S. Baker, D. Basham, S. D. Bentley, K. Brooks, A. M. Cerdeno-Tarraga, 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.
67. Perry, R. D., and J. D. Fetherston. 1997. Yersinia pestis-etiologic agent of plague. Clin. Microbiol. Rev. 10:35-66.
68. Persson, C., R. Nordfelth, K. Andersson, A. 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.
69. Phalipon, A., M. Kaufmann, P. Michetti, J. Cavaillon, M. Huerre, P. Sansonetti, and J. Kraehenbuhl. 1995. Monoclonal immunoglobulin A antibody directed against serotype-specific epitope of Shigella flexneri lipopolysaccharide protects against murine experimental shigellosis. J. Exp. Med. 182:769-778.
70. Rebeil, R., R. K. Ernst, B. B. Gowen, S. I. Miller, and B. J. Hinnebusch. 2004. Variation in lipid A structure in the pathogenic yersiniae. Mol. Microbiol. 52:1363-1373.
71. Reed, D. S., and M. J. Martinez. 2006. Respiratory immunity is an important component of protection elicited by subunit vaccination against pneumonic plague. Vaccine 24:2283-2289.
72. Reed, L. J., and H. A. Muench. 1938. A simple method for estimating fifty percent end points. Am. J. Hyg. 27:493-497.
73. Sansonetti, P. J., A. Phalipon, J. Arondel, K. Thirumalai, S. Banerjee, S. Akira, K. Takeda, and A. Zychlinsky. 2000. Caspase-1 activation of IL-1β and IL-18 are essential for Shigella flexneri-induced inflammation. Immunity 12:581-590.
74. Sauvonnet, N., I. Lambermont, P. v. d. Bruggen, and G. R. Cornelis. 2002. YopH prevents monocyte chemoattractant protein 1 expression in macrophages and T-cell proliferation through inactivation of the phosphatidylinositol 3-kinase pathway. Mol. Microbiol. 45:805-815.
75. Simonet, M., B. Riot, N. Fortineau, and P. Berche. 1996. Invasin production by Yersinia pestis is abolished by insertion of an IS200-like element within the inv gene. Infect. Immun. 64:375-379.
76. Skurnik, M., and H. Wolf-Watz. 1989. Analysis of the yopA gene encoding the Yop1 virulence determinants of Yersinia spp. Mol. Microbiol. 3:517-529.
77. - Yersinia pestis in BALB/c mice. Infect. Immun. 57:1200-1210.
78. Titball, R. W., J. Hill, D. G. Lawton, and K. A. Brown. 2003. Yersinia pestis and plague. Biochem. Soc. Trans. 31:104-107.
79. Trulzsch, K., T. Sporleder, E. I. Igwe, H. Russmann, and J. Heesemann. 2004. Contribution of the major secreted Yops of Yersinia enterocolitica O:8 to pathogenicity in the mouse infection model. Infect. Immun. 72:5227-5234.
80. - or Pstr phenotypes of yersiniae. Infect. Immun. 43:895-900.
81. van Zonneveld, M., J. M. Droogh, M. W. J. A. Fieren, I. C. Gyssens, T. van Gelder, and W. Weimar. 2002. Yersinia pseudotuberculosis bacteraemia in a kidney transplant patient. Nephrol. Dial. Transplant. 17:2252-2254.
82. Velianov, D., S. Nikolova, K. Naidenski, T. Raducheva, and V. Kusovski. 1993. Studies on aerosol Yersinia pseudotuberculosis infection of guinea-pigs. Acta Microbiol. Bulg. 30:3-10.
83. Viboud, G. I., and J. B. Bliska. 2001. A bacterial type III secretion system inhibits actin polymerization to prevent pore formation in host cell membranes. EMBO J. 20:5373-5382.
84. Viboud, G. I., and J. B. Bliska. 2005. Yersinia outer proteins: role in modulation of host cell signalling responses and pathogenesis. Annu. Rev. Microbiol. 59:69-39.
85. Visser L. G., A. Annema, and R. van Furth. 1995. Role of Yops in inhibition of phagocytosis and killing of opsonized Yersinia enterocolitica by human granulocytes. Infect. Immun. 63:2570-2575.
86. Wang, S., D. Heilman, F. Liu, T. Giehl, S. Joshi, X. Huang, T.-h. Chou, J. Goguen, and S. Lu. 2004. A DNA vaccine producing LcrV antigen in oligomers is effective in protecting mice from lethal mucosal challenge of plague. Vaccine 22:3348-3357.
87. Watson, R. P., T. W. Blanchard, M. G. Mense, and P. W. Gasper. 2001. Histopathology of experimental plague in cats. Vet. Pathol. 38:165-172.
88. Winfield, M. D., T. Latifi, and E. A. Groisman. 2005. Transcriptional regulation of the 4-amino-4-deoxy-L-arabinose biosynthetic genes in Yersinia pestis. J. Biol. Chem. 280:14765-14772.
89. Zhang, Z. Y., Y. Wang, L. Wu, E. B. Fauman, J. A. Stuckey, H. L. Schubert, M. A. Saper, and J. E. Dixon. 1994. The Cys(X)5Arg catalytic motif in phosphoester hydrolysis. Biochemistry 33:15266-15270.
90. +- responsive PhoP regulator in Yersinia pestis. FEMS Microbiol. Lett. 250:85-95.