Yersinia-induced apoptosis in vivo aids in the establishment of a systemic infection of mice

Journal of Experimental Medicine

Volumn 188, Issue 11, 1998, Pages 2127-2137

  Monack, Denise M ^a   Mecsas, Joan ^a   Bouley, Donna ^a   Falkow, Stanley ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Mac 1 antibody; Macrophages; TUNEL reactions; Virulence; YopJ

Indexed keywords

BACTERIAL PROTEIN; CYTOKINE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; VIRULENCE FACTOR; YOPJ PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL INFECTION; BACTERIAL VIRULENCE; BACTERIUM MUTANT; CONTROLLED STUDY; CYTOKINE PRODUCTION; FEMALE; INFLAMMATION; MOUSE; NONHUMAN; PLASMID; PRIORITY JOURNAL; YERSINIA PSEUDOTUBERCULOSIS;

ANIMALS; APOPTOSIS; FEMALE; LYMPHOID TISSUE; MICE; MICE, INBRED BALB C; MUTATION; VIRULENCE; YERSINIA; YERSINIA INFECTIONS;

EID: 0031744367     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.188.11.2127     Document Type: Article

References (55)

1. Carter, P.B. 1975. Animal model of human disease. Yersinia enteritis. Animal model: oral Yersinia enterocolitica infection of mice. Am. J. Pathol. 81:703-706.
2. Cornelis, G., Y. Laroche, G. Balligand, M.P. Sory, and G. Wauters. 1987. Yersinia enterocolitica, a primary model for bacterial invasiveness. Rev. Infect. Dis. 9:64-87.
3. Bottone, E.J. 1977. Yersinia enterocolitica: a panoramic view of a charismatic microorganism. CRC Crit. Rev. Microbiol. 5:211-241.
4. Ahvonen, P., K. Sievers, and K. Aho. 1969. Arthritis associated with Yersinia enterocolitica infection. Acta Rheumatol. Scand. 15:232-253.
5. Bouza, E., A. Dominguez, M. Meseguer, L. Buzon, D. Boixeda, M.J. Revillo, L. de Rafael, and J. Martinez-Beltran. 1980. Yersinia enterocolitica Septicemia. Am. J. Clin. Pathol. 74: 404-409.
6. Grützkau, A., C. Hanski, H. Hahn, and E.O. Riecken. 1990. Involvement of M cells in the bacterial invasion ot Peyer's patches: a common mechanism shared by Yersinia enterocolitica and other enteroinvasive bacteria. Gut. 31:1011-1015.
7. Pepe, J.C., M.R. Wachtel, E. Wagar, and V.L. Miller. 1995. Pathogenesis of defined invasion mutants of Yersinia enterocolitica in a BALB/c mouse model of infection. Infect. Immun. 63:4837-4848.
8. Bliska, J.B., and S. Falkow. 1992. Bacterial resistance to complement killing mediated by the Ail protein of Yersinia enterocolitica. Proc. Natl. Acad. Sci. USA. 89:3561-3565.
9. China, B., M.P. Sory, B.T. N'Guyen, M. De Bruyere, and G.R. Cornelis. 1993. Role of the YadA protein in prevention of opsonization of Yersinia enterocolitica by C3b molecules. Infect. Immun. 61:3129-3136.
10. Pilz, D., T. Vocke, J. Heesemann, and V. Brade. 1992. Mechanism of YadA-mediated serum resistance of Yersinia enterocolitica serotype O3. Infect. Immun. 60:189-195.
11. Hanski, C., M. Naumann, A. Grützkau, G. Pluschke, B. Friedrich, H. Hahn, and E.O. Riecken. 1991. Humoral and cellular defense against intestinal murine infection with Yersinia enterocolitica. Infect. Immun. 59:1106-1111.
12. Cornelis, G.R., and H. Wolf-Watz. 1997. The Yersinia Yop virulon: a bacterial system for subverting eukaryotic cells. Mol. Microbiol. 23:861-867.
13. Brubaker, R.R. 1991. Factors promoting acute and chronic diseases caused by yersiniae. Clin. Microbiol. Rep. 4:309-324.
14. Bliska, J.B., K.L. 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.
15. Rosqvist, R., I. Bolin, and H. Wolf-Watz. 1988. Inhibition of phagocytosis in Yersinia pseudotuberculosis: a virulence plasmid-encoded ability involving the Yop2b protein. Infect. Immun. 56:2139-2143.
16. Black, D.S., and J.B. Bliska. 1997. Identification of p130Cas as a substrate of Yersinia YopH (Yop51), a bacterial protein tyrosine phosphatase that translocates into mammalian cells and targets focal adhesions. EMBO (Eur. Mol. Biol. Organ.) J. 16:2730-2744.
17. Rosqvist, R., A. Forsberg, M. Rimpilainen, T. Bergman, and H. Wolf-Watz. 1990. The cytotoxic protein YopE of Yersinia obstructs the primary host defence. Mol. Microbiol. 4:657-667.
18. Fallman, M., K. Andersson, S. Hakansson, K.E. Magnusson, O. Stendahl, and H. Wolf-Watz. 1995. Yersinia pseudotuberculosis inhibits Fc receptor-mediated phagocytosis in J774 cells. Infect. Immun. 63:3117-3124.
19. Leung, K.Y., and S.C. Straley. 1989. The yopM gene of Yersinia pestis encodes a released protein having homology with the human platelet surface protein GPIb alpha. J. Bacteriol. 171:4623-4632.
20. 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.
21. Boland, A., M.P. Sory, M. Iriarte, C. Kerbourch, P. Wattiau, and G.R. Cornelis. 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 (Eur. Mol. Biol. Organ.) J. 15: 5191-5201.
22. Galyov, E.E., S. Hakansson, A. Forsberg, and H. Wolf-Watz. 1993. A secreted protein kinase of Yersinia pseudotuberculosis is an indispensable virulence determinant. Nature. 361:730-732.
23. Hakansson, S., E.E. Galyov, R. Rosqvist, and H. Wolf-Watz. 1996. 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.
24. Guzman, C.A., E. Domann, M. Rohde, D. Bruder, A. Darji, S. Weiss, J. Wehland, T. Chakraborty, and K.N. Timmis. 1996. Apoptosis of mouse dendritic cells is triggered by listeriolysin, the major virulence determinant of Listeria monocytogenes. Mol. Microbiol. 20:119-126.
25. Chen, L.M., K. Kaniga, and J.E. Galan. 1996. Salmonella spp. are cytotoxic for cultured macrophages. Mol. Microbiol. 21:1101-1115.
26. Monack, D.M., B. Raupach, A.E. Hromockyj, and S. Falkow. 1996. Salmonella typhimurium invasion induces apoptosis in infected macrophages. Proc. Natl. Acad. Sci. USA. 93:9833-9838.
27. Chen, Y., and A. Zychlinsky. 1994. Apoptosis induced by bacterial pathogens. Microb. Pathog. 17:203-212.
28. Zychlinsky, A., and P. Sansonetti. 1997. Perspectives series: host/pathogen interactions. Apoptosis in bacterial pathogenesis.J. Clin. Invest. 100:493-495.
29. Zychlinsky, A., B. Kenny, R. Menard, M.C. Prevost, I.B. Holland, and P.J. Sansonetti. 1994. IpaB mediates macrophage apoptosis induced by Shigella flexneri. Mol. Microbiol. 11:619-627.
30. Ruckdeschel, K., A. Roggenkamp, V. Lafont, P. Mangeat, J. Heesemann, and B. Rouot. 1997. Interaction of Yersinia enterocolitica with macrophages leads to macrophage cell death through apoptosis. Infect. Immun. 65:4813-4821.
31. 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.
32. Mills, S.D., 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.
33. Palmer, L.E., S. Hobbie, J.E. Galan, and J.B. Bliska. 1998. YopJ of Yersinia pseudotuberculosis is required for the inhibition of macrophage TNF-alpha production and downregulation of the MAP kinases p38 and JNK. Mol. Microbiol. 27:953-965.
34. Boland, A., and G.R. Cornelis. 1998. Role of YopP in suppression of tumor necrosis factor alpha release by macrophages during Yersinia infection. Infect. Immun. 66:1878-1884.
35. Schesser, K., A. Splik, J. Dukuzumuremyi, M. Neurath, S. Petterson, 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.
36. 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.
37. Autenrieth, I.B., and J. Heesemann. 1992. In vivo neutralization of tumor necrosis factor-alpha and interferon-gamma abrogates resistance to Yersinia enterocolitica infection in mice. Med. Microbiol. Immunol. 181:333-338.
38. Ruckdeschel, K., S. Harb, A. Roggenkamp, M. Hornef, R. Zumbihl, S. Köhler, 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 a production. J. Exp. Med. 187:1069-1079.
39. Donnenberg, M.S., and J.B. Kaper. 1991. Construction of an eae deletion mutant of enteropathogenic Escherichia coli by using a positive-selection suicide vector. Infect. Immun. 59: 4310-4317.
40. Springer, T., G. Galfre, D.S. Secher, and C. Milstein. 1979. Mac-1: a macrophage differentiation antigen identified by monoclonal antibody. Eur. J. Immunol. 9:301-306.
41. Reed, L.J., and H. Muench. 1938. A simple method of estimating fifty percent endpoints. Am. J. Hyg. 27:493-497.
42. Lagasse, E., and I.L. Weissman. 1996. Flow cytometric identification of murine neutrophils and monocytes. J. Immunol. Methods. 197:139-150.
43. Shapiro, H.M. Practical Flow Cytometry. Third ed. 1995. John Wiley & Sons, Inc., New York. 542 pp.
44. 2+ in Yersinia pestis include structural genes for outer membrane proteins. Infect. Immun. 51:445-454.
45. Galyov, E.E., S. Hakansson, and H. Wolf-Watz. 1994. Characterization of the operon encoding the YpkA Ser/Thr protein kinase and the YopJ protein of Yersinia pseudotuberculosis. J Bacteriol. 176:4543-4548.
46. Heesemann, J., K. Gaede, and I.B. Autenrieth. 1993. Experimental Yersinia enterocolitica infection in rodents: a model for human yersiniosis. APMIS. 101:417-429.
47. Bohn, E., and I.B. Autenrieth. 1996. IL-12 is essential for resistance against Yersinia enterocolitica by triggering IFN-gamma production in NK cells and CD4+ T cells. J. Immunol. 156: 1458-1468.
48. Bohn, E., E. Schmitt, C. Bielfeldt, A. Noll, R. Schulte, and I.B. Autenrieth. 1998. Ambiguous role of interleukin-12 in Yersinia enterocolitica infection in susceptible and resistant mouse strains. Infect. Immun. 66:2213-2220.
49. Autenrieth, I.B., A. Tingle, A. Reske-Kunz, and J. Heesemann. 1992. T lymphocytes mediate protection against Yersinia enterocolitica in mice: characterization of murine T-cell clones specific for Y. enterocolitica. Infect. Immun. 60:1140-1149.
50. Autenrieth, I.B., M. Beer, E. Bohn, S.H. Kaufmann, and J. Heesemann 1994. Immune responses to Yersinia enterocolitica in susceptible BALB/c and resistant C57BL/6 mice: an essential role for gamma interferon. Infect. Immun. 62:2590-2599.
51. Autenrieth, I.B., V. Kempf, T. Sprinz, S. Preger, and A. Schnell. 1996. Defense mechanisms in Peyer's patches and mesentenc lymph nodes against Yersinia enterocolitica involve integrins and cytokines. Infect. Immun. 64:1357-1368.
52. Nagata, S. 1997. Apoptosis by death factor. Cell. 88:355-365.
53. Zychlinsky, A., and P.J. Sansonetti. 1997. Apoptosis as a proinflammatory event: what can we learn from bacteria-induced cell death? Trends Microbiol. 5:201-204.
54. Zychlinsky, A., C. Fitting, J.M. Cavaillon, and P.J. Sansonetti. 1994. Interleukin 1 is released by murine macrophages during apoptosis induced by Shigella flexneri. J. Clin. Invest. 94:1328-1332.
55. Perdomo, O.J., J.M. Cavaillon, M. Huerre, H. Ohayon, P. Gounon, and P.J. Sansonetti. 1994. Acute inflammation causes epithelial invasion and mucosal destruction in experimental shigellosis. J. Exp. Med. 180:1307-1319.