Intravenous infection of virulent shigellae causes fulminant hepatitis in mice

Cellular Microbiology

Volumn 7, Issue 1, 2005, Pages 115-127

  Martino, Maria Celeste ^a   Rossi, Giacomo ^b   Tattoli, Ivan ^a   Martini, Irene ^a   Chiavolini, Damiana ^c   Cortese, Giancarlo ^d   Pozzi, Gianni ^c   Bernardini, Maria Lina ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b UNIVERSITY OF CAMERINO   (Italy)

^c UNIVERSITY OF SIENA   (Italy)

^d REGINA ELENA NATIONAL CANCER INSTITUTE   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

AMINOTRANSFERASE; GAMMA INTERFERON; INTERLEUKIN 12; INTERLEUKIN 18; INTERLEUKIN 1BETA; INTERLEUKIN 6; MESSENGER RNA;

AMINOTRANSFERASE BLOOD LEVEL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BACTERIAL VIRULENCE; BACTERIUM MUTANT; CONTROLLED STUDY; FEMALE; GRAM NEGATIVE SEPSIS; IMMUNE RESPONSE; INFECTIOUS HEPATITIS; INTRAVENOUS ADMINISTRATION; LIVER GRANULOMA; MORTALITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; SHIGELLA; SURVIVAL;

ANIMALS; APOPTOSIS; COLONY COUNT, MICROBIAL; DISEASE MODELS, ANIMAL; DYSENTERY, BACILLARY; FEMALE; GRANULOMA; HEPATITIS; HEPATOCYTES; INTERFERON TYPE II; INTERLEUKIN-1; INTERLEUKIN-12; INTERLEUKIN-18; INTERLEUKIN-1BETA; INTERLEUKIN-6; LIVER; MICE; MICE, INBRED BALB C; PEPTIDE FRAGMENTS; RNA, MESSENGER; SHIGELLA; TRANSAMINASES; VIRULENCE;

ANIMALIA; MURINAE; RODENTIA; SHIGELLA;

EID: 12444254017     PISSN: 14625814     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2004.00441.x     Document Type: Article

References (49)

1. Allaoui, A., Mounier, J., Prevost, C., Sansonetti, P.J., and Parsot, C. (1992) icsB: a Shigella flexneri virulence gene necessary for the lysis of protrusions during intercellular spread. Mol Microbiol 6: 1605-1616.
2. Bernardini, M.L., Arondel, J., Martini, I., Aidara, A., and Sansonetti, P.J. (2001) Parameters underlying successful protection with live attenuated mutants in experimental shigellosis. Infect Immun 69: 1072-1083.
3. Buchrieser, C., Glaser, P., Rusniok, C., Nedjari, H., D'Hauteville, H., Kunst, F., et al. (2000) The virulence plasmid pWR100 and the repertoire of proteins secreted by the type III secretion apparatus of Shigella flexneri. Mol Microbiol 38: 760-771.
4. Buttner, D., and Bonas, U. (2002) Port of entry: the type III secretion translocon. Trends Microbiol 10: 186-192.
5. Chen, Y., Smith, M.R., Thirumalai, K., and Zychlinsky, A. (1996) A bacterial invasin induces macrophage apoptosis by binding directly to ICE. EMBO J 15: 3853-3860.
6. Co, D.O., Hogan, L.H., II-Kim, S., and Sandor, M. (2004) T cell contributions to the different phases of granuloma formation. Immunol Lett 92: 135-142.
7. Dilworth, D.D., and McCarrey, J.R. (1992) Single step elimination of contaminating DNA prior to reverse transcriptase PCR. PCR Meth Appl 1: 279-282.
8. Edgeworth, J.D., Spencer, J., Phalipon, A., Griffin, G.E., and Sansonetti, P.J. (2002) Cytotoxicity and interleukin-1beta processing following Shigella flexneri infection of human monocyte-derived dendritic cells. Eur J Immunol 32: 1464-1471.
9. Etheridge, M.E., Hoque, A.T., and Sack, D.A. (1996) Pathologic study of a rabbit model for shigellosis. Lab Anim Sci 46: 61-66.
10. Ferluga, J., and Allison, A.C. (1978) Role of mononuclear infiltrating cells in pathogenesis of hepatitis. Lancet ii: 610-611.
11. Fernandez, M.I., Thuizat, A., Pedron, T., Neutra, M., Phalipon, A., and Sansonetti, P.J. (2003) A newborn mouse model for the study of intestinal pathogenesis of shigellosis. Cell Microbiol 5: 481-491.
12. Formal, S.B., Kundel, D., Schneider, H., Kunev, N., and Sprinz, H. (1961) Studies with Vibrio cholerae in the ligated loop of the rabbit intestine. J Exp Pathol 42: 504-510.
13. Fratazzi, C., Arbeit, R.D., Carini, C., and Remold, H.G. (1997) Programmed cell death of Mycobacterium avium serovar 4-infected human macrophages prevents the mycobacteria from spreading and induces mycobacterial growth inhibition by freshly added, uninfected macrophages. J Immunol 158: 4320-4327.
14. Girardin, S.E., Boneca, I.G., Carneiro, L.A., Antignac, A., Jehanno, M., Viala, J., et al. (2003) Nod1 detects a unique muropeptide from Gram negative bacterial peptidoglycan. Science 300: 1584-1587.
15. Hathaway, L.J., Griffin, G.E., Sansonetti, P.J., and Edgeworth, J.D. (2002) Human monocytes kill Shigella flexneri but then die by apoptosis associated with suppression of proinflammatory cytokine production. Infect Immun 70: 3833-3842.
16. Hilbi, H., Moss, J.E., Hersh, D., Chen, Y., Arondel, J., Banerjee, S., et al. (1998) Shigella-induced apoptosis is dependent on caspase-1 which binds to IpaB. J Biol Chem 273: 32895-32900.
17. Keane, J., Balcewicz-Sablinska, M., Remold, H., Chupp, G.L., Meek, B.B., Fenton, M.J., and Kornfeld, H. (1997) Infection by Mycobacterium tubercolosis promotes human alveolar macrophage apoptosis. Infect Immun 65: 298-304.
18. Kotloff, K.L., Winickoff, J.P., Ivanoff, B., Clemens, J.D., Swerdlow, D.L., Sansonetti, P.J., et al. (1999) Global burden of Shigella infections: implication for vaccine development and implementation. WHO Bull 77: 651-666.
19. Levine, V.D., Overtruf, G.D., and Mathies, A.W. (1974) Shigella dysenteriae type 1: severe dysentery and sepsis with hematologic, hepatic and renal complications. Western J Med 121 501-504.
20. Mandic-Mulec, I., Weiss, J., and Zychlinsky, A. (1997) Shigella flexneri is trapped in polymorphonuclear leukocyte vacuoles and efficiently killed. Infect Immun 65: 110-115.
21. Matsunaga, K., and Ito, M. (2000) Quantitative analysis of apoptotic cell death in granulomatous inflammation induced by intravenous challenge with Cryptococcus neoformans and bacillus Calmette-Guérin vaccine. Pathol Int 50: 206-218.
22. Maurelli, A.T., Blackmon, B., and Curtiss, R., III (1984) Temperature-dependent expression of virulence genes in Shigella species. Infect Immun 43: 195-201.
23. Menard, R., Sansonetti, P.J., and Parsot, C. (1993) Nonpolar mutagenesis of the ipa genes defines IpaB, IpaC: and IpaD as effectors of Shigella flexneri entry into epithelial cells. J Bacteriol 175: 5899-5906.
24. Miller, J.H. (1992) A Short Course in Bacterial Genetics Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
25. Mizoguchi, Y., Sakagami, Y., Kuboi, H., Kobayashi, K., and Yano, I. (1988) Effects of the polysaccharide in an experimental massive hepatic cells necrosis model. Biochem Biophys Res Commun 155: 1305-1310.
26. Modlin, R.L., Pirmez, C., Hofman, F.M., Torigian, V., Uyemura, K., Rea, T.H., et al. (1989) Lymphocytes bearing antigen-specific gamma delta T-cell receptors accumulate in human infectious disease lesions. Nature 339: 544-548.
27. Molloy, A., Laochumroonvorapong, P., and Kaplan, G. (1994) Apoptosis, but not necrosis, of infected monocytes is coupled with killing of intracellular bacillus Calmette-Guerin. J Exp Med 180 1499-1509.
28. Moss, J.E., Aliprantis, A.O., and Zychlinsky, A. (1999) The regulation of apoptosis by microbial pathogens. Int Rev Cytol 187: 203-259.
29. Nagakawa, J., Hishinuma, I., Hirota, K., Miyamoto, K., Yamanaka, T., Tsukidate, K., et al. (1990) Involvement of tumor necrosis factor-alfa in the pathogenesis of activated-macrophage-mediated hepatitis in mice. Gastroenterology 99: 758-765.
30. Naito, M., and Takahashi, K. (1991) The role of Kupffer cells in glucan induced granuloma formation in the liver of mice depleted of blood monocytes by administration of strontium-89. Lab Invest 64 664-674.
31. Nofech-Mozes, Y., Yuhas, Y., Kaminsky, E., Weizman, A., and Ashkenazi, S. (2000) Induction of mRNA for tumor necrosis factor-alfa and interleukin-1 beta in mice brain, spleen and liver in an animal model of Shigella-related seizures. Isr Med Assoc J 2: 86-90.
32. Perdomo, O.J., Cavaillon, J.M., Huerre, M., Ohayon, H., Gounon, P., and Sansonetti, P.J. (1994) Acute inflammation causes epithelial invasion and mucosal destruction in experimental shigellosis. J Exp Med 180: 1307-1319.
33. Phalipon, A., Kaufmann, M., Michetti, P., Cavaillon, J.M., Huerre, M., Sansonetti, P.J., and Kraehembuhl, J. P. (1995) Monoclonal immunoglobulin A antibody directed against serotype-specific epitope of Shigella flexneri lipopolysaccharide protects against murine experimental shgellosis. J Exp Med 182: 769-778.
34. Philpott, D.J., Yamaoka, S., Israel, A., and Sansonetti, P.J. (2000) Invasive Shigella flexneri activates NF-kappa B through a lipopolysaccharide-dependent innate intracellular response and leads to IL-8 expression in epithelial cells. J Immunol 165: 903-914.
35. Salgame, P., Abrams, J.S., Clayberger, C., Goldstein, H., Convit, J., Modlin, R.L., and Bloom, B.R. (1991) Differing lymphokine profiles of functional subsets of human CD4 and CD8 T cell clones. Science 254: 279-282.
36. Sansonetti, P.J., Kopecko, D.J., and Formal, S.B. (1982) Involvement of a plasmid in the invasive ability of Shigella flexneri. Infect Immun 35: 852-860.
37. Sansonetti, P.J., Arondel, J., Fontaine, A., d'Hauteville, H., and Bernardini, M.L. (1991) ompB (osmo-regulation) and icsA (cell-to-cell spread) mutants of Shigella flexneri: vaccine candidates and probes to study the pathogenesis of shigellosis. Vaccine 9: 416-422.
38. Sansonetti, P.J., Arondel, J., Huerre, M., Harada, A., and Matsushima, K. (1999) Interleukin-8 controls bacterial transepithelial translocation at the cost of epithelial destruction in experimental shigellosis. Infect Immun 67: 1471-1480.
39. Sansonetti, P.J., Phalipon, A., Arondel, J., Thirumalai, K., Banerjee, S., Akira, S., et al. (2000) Caspase-1 activation of IL-1beta and IL-18 are essential for Shigella flexneri-induced inflammation. Immunity 12: 581-590.
40. Sereny, B. (1957) Experimental Shigella conjunctivitis. Acta Microbiol Hung 2: 293-296.
41. Stern, M.K., and Gitnik, G.L. (1976) Shigella hepatitis. JAMA 235: 26-28.
42. Takahashi, K., Naito, M., Umeda, S., and Shultz, L.D. (1994) The role of macrophage colony-stimulating factor in hepatic glucan-induced granuloma formation in the osteopetrosis mutant mouse defective in the production of macrophages colony-stimulating factor. Am J Pathol 144: 1381-1392.
43. Takeuchi, A., Jervis, H.R., and Formal, S.B. (1975) Animal model of human disease. Bacillary dysentery, shigellosis, Shigella dysentery. Animal model: monkey shigellosis or dysentery. Am J Pathol 81: 251-254.
44. Voino-Yasenetsky, M.V., and Voino-Yasenetskaya, M.K. (1962) Experimental pneumonia caused by bacteria of Shigella group. Acta Microbiol Acad Sci Hung 11: 439-454.
45. Weinrauch, Y., Drujan, D., Shapiro, S.D., Weiss, J., and Zychlinsky, A. (2002) Neutrophil elastase targets virulence factors of enterobacteria. Nature 417: 91-94.
46. Wyke, R.J., Canalese, J.C., Gimson, A.E., and Williams, R. (1982) Bacteraemia in patients with fulminant hepatic failure. Liver 2: 45-52.
47. Yamaoka, H., Sakaguchi, N., Sano, K., and Ito, M. (1996) Intravascular granuloma induced by intravenous inoculation of Cryptococcus neoformans. Mycopathologia 133: 149-158.
48. Zychlinsky, A., Prevost, M.C., and Sansonetti, P.J. (1992) Shigella flexneri induces apoptosis in infected macrophages. Nature 358: 167-169.
49. Yychlinsky, A., Fitting, C., Cavaillon, J.M., and Sansonetti, P.J. (1994) Interleukin 1 is released by murine macrophages during apoptosis induced by Shigella flexneri. J Clin Invest 94: 1328-1332.