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Organotypic slice cultures from rat brain tissue: a new approach for Naegleria fowleri CNS infection in vitro

Published online by Cambridge University Press:  13 September 2005

C. GIANINAZZI ,
M. SCHILD ,
N. MÜLLER ,
S. L. LEIB ,
F. SIMON ,
S. NUÑEZ ,
P. JOSS  and
B. GOTTSTEIN
C. GIANINAZZI
Affiliation:
Institute of Parasitology, University of Bern, Länggass-Strasse 122, CH-3001 Bern, Switzerland
M. SCHILD
Affiliation:
Institute of Parasitology, University of Bern, Länggass-Strasse 122, CH-3001 Bern, Switzerland
N. MÜLLER
Affiliation:
Institute of Parasitology, University of Bern, Länggass-Strasse 122, CH-3001 Bern, Switzerland
S. L. LEIB
Affiliation:
Institute for Infectious Diseases, University of Bern, Friedbühlstrasse 51, CH-3010 Bern, Switzerland
F. SIMON
Affiliation:
Institute for Infectious Diseases, University of Bern, Friedbühlstrasse 51, CH-3010 Bern, Switzerland
S. NUÑEZ
Affiliation:
Institute of Parasitology, University of Bern, Länggass-Strasse 122, CH-3001 Bern, Switzerland
P. JOSS
Affiliation:
Institute for Infectious Diseases, University of Bern, Friedbühlstrasse 51, CH-3010 Bern, Switzerland
B. GOTTSTEIN
Affiliation:
Institute of Parasitology, University of Bern, Länggass-Strasse 122, CH-3001 Bern, Switzerland
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Abstract

The free-living amoeba Naegleria fowleri is the aetiological agent of primary amoebic meningoencephalitis (PAM), a disease leading to death in the vast majority of cases. In patients suffering from PAM, and in corresponding animal models, the brain undergoes a massive inflammatory response, followed by haemorrhage and severe tissue necrosis. Both, in vivo and in vitro models are currently being used to study PAM infection. However, animal models may pose ethical issues, are dependent upon availability of specific infrastructural facilities, and are time-consuming and costly. Conversely, cell cultures lack the complex organ-specific morphology found in vivo, and thus, findings obtained in vitro do not necessarily reflect the situation in vivo. The present study reports infection of organotypic slice cultures from rat brain with N. fowleri and compares the findings in this culture system with in vivo infection in a rat model of PAM, that proved complementary to that of mice. We found that brain morphology, as present in vivo, is well retained in organotypic slice cultures, and that infection time-course including tissue damage parallels the observations in vivo in the rat. Therefore, organotypic slice cultures from rat brain offer a new in vitro approach to study N. fowleri infection in the context of PAM.

Keywords

Naegleria fowleriorganotypic slice culturesprimary amoebic meningoencephalitis (PAM)rat
Type
Research Article
Information
Parasitology , Volume 132 , Issue 6 , June 2006 , pp. 797 - 804
Copyright
2005 Cambridge University Press

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References

REFERENCES

Barnett, N. D., Kaplan, A. M., Hopkin, R. J., Saubolle, M. A. and Rudinsky, M. F. ( 1996). Primary amoebic meningoencephalitis with Naegleria fowleri: clinical review. Pediatric Neurology 15, 230–234.CrossRefGoogle Scholar
Becker, A. J., Gillardon, F., Blumcke, I., Langendorfer, D., Beck, H. and Wiestler, O. D. ( 1999). Differential regulation of apoptosis-related genes in resistant and vulnerable subfields of the rat epileptic hippocampus. Molecular Brain Research 67, 172–176.CrossRefGoogle Scholar
Bifrare, Y. D., Gianinazzi, C., Imboden, H., Leib, S. L. and Täuber, M. G. ( 2003). Bacterial meningitis causes two distinct forms of cellular damage in the hippocampal dentate gyrus in infant rats. Hippocampus 13, 481–488.CrossRefGoogle Scholar
Bradley, S. G., Toney, D., Zhang, M. Y. and Marciano-Cabral, F. ( 1996). Dependence of growth, metabolic expression, and pathogenicity of Naegleria fowleri on exogenous porphyrins. Journal of Parasitology 82, 763–768.CrossRefGoogle Scholar
Chen, Z. L. and Strickland, S. ( 1997). Neuronal death in the hippocampus is promoted by plasmin-catalyzed degradation of laminin. Cell 91, 917–925.CrossRefGoogle Scholar
Cho, M. S., Jung, S. Y., Park, S., Kim, K. H., Kim, H. I., Sohn, S., Kim, H. J., Im, K. I. and Shin, H. J. ( 2003). Immunological characterizations of a cloned 13.1-kilodalton protein from pathogenic Naegleria fowleri. Clinical and Diagnostic Laboratory Immunology 10, 954–549.Google Scholar
Fulford, D. E. and Marciano-Cabral, F. ( 1986). Cytolytic activity of Naegleria fowleri cell-free extract. Journal of Protozoology 33, 498–502.CrossRefGoogle Scholar
Gianinazzi, C., Grandgirard, D., Simon, F., Imboden, H., Joss, P., Täuber, M. G. and Leib, S. L. ( 2004 a). Apoptosis of hippocampal neurons in organotypic slice culture models: direct effect of bacteria revisited. Journal of Neuropathology and Experimental Neurology 63, 610–617.Google Scholar
Gianinazzi, C., Grandgirard, D., Imboden, H., Egger, L., Meli, D. N., Bifrare, Y. D., Joss, P. C., Täuber, M. G., Borner, C. and Leib, S. L. ( 2004 b). Caspase-3 mediates hippocampal apoptosis in pneumococcal meningitis. Acta Neuropathologica (Berlin) 105, 499–507.Google Scholar
Herbst, R., Ott, C., Jacobs, T., Marti, T., Marciano-Cabral, F. and Lippe, M. ( 2002). Pore-forming polypeptides of the pathogenic protozoon Naegleria fowleri. Journal of Biological Chemistry 277, 22353–22360.CrossRefGoogle Scholar
Im, K. I. and Lee, K. T. ( 1985). Failure of immunization with Naegleria fowleri in mice born to immune mothers. Kisaengchunghak Chapchi 23, 151–155.CrossRefGoogle Scholar
Jarolim, K. L., McCosh, J. K., Howard, M. J. and John, D. T. ( 2000). A light microscopy study of the migration of Naegleria fowleri from the nasal submucosa to the central nervous system during the early stage of primary amebic meningoencephalitis in mice. Journal of Parasitology 86, 50–55.CrossRefGoogle Scholar
Jarolim, K. L., McCosh, J. K. and Howard, M. J. ( 2002). The role of blood vessels and lungs in the dissemination of Naegleria fowleri following intranasal inoculation in mice. Folia Parasitologica (Praha) 49, 183–188.CrossRefGoogle Scholar
John, D. T. and Hoppe, K. L. ( 1990). Susceptibility of wild mammals to infection with Naegleria fowleri. Journal of Parasitology 76, 865–868.CrossRefGoogle Scholar
John, D. T. and Howard, M. J. ( 1993). Virulence of Naegleria fowleri affected by axenic cultivation and passage in mice. Folia Parasitologica (Praha) 40, 187–191.Google Scholar
John, D. T. and John, R. A. ( 1994). Enhancement of virulence of Naegleria fowleri by growth in Vero-cell cultures. Journal of Parasitology 80, 149–151.CrossRefGoogle Scholar
Kuroki, T., Yagita, K., Sugiyama, H., Yamai, S., Fukuma, T., Katsube, Y. and Endo, T. ( 1998). Experimental infection of Naegleria fowleri in mice. Kansenshogaku Zasshi 72, 1064–1069.CrossRefGoogle Scholar
Leib, S. L., Clements, J. M., Lindberg, R. L., Heimgartner, C., Loeffler, J. M., Pfister, L. A., Täuber, M. G. and Leppert, D. ( 2001). Inhibition of matrix metalloproteinases and tumour necrosis factor alpha converting enzyme as adjuvant therapy in pneumococcal meningitis. Brain 124, 1734–1742.CrossRefGoogle Scholar
Martinez, A. J. and Visvesvara, G. S. ( 1997). Free-living, amphizoic and opportunistic amebas. Brain Pathology 7, 583–598.CrossRefGoogle Scholar
May, R. G. and John, D. T. ( 1982). Intravenous infection of mice with Naegleria fowleri. Folia Parasitologica (Praha) 29, 201–210.Google Scholar
McLaughlin, G. L., Vodkin, M. H. and Huizinga, H. W. ( 1991). Amplification of repetitive DNA for the specific detection of Naegleria fowleri. Journal of Clinical Microbiology 29, 227–230.Google Scholar
Meli, D. N., Christen, S. and Leib, S. L. ( 2003). Matrix metalloproteinase-9 in pneumococcal meningitis: activation via an oxidative pathway. Journal of Infectious Diseases 187, 1411–1415.CrossRefGoogle Scholar
Müller, N., Vonlaufen, N., Gianinazzi, C., Leib, S. L. and Hemphill, A. ( 2002). Application of real-time fluorescent PCR for quantitative assessment of Neospora caninum infections in organotypic slice cultures of rat central nervous system tissue. Journal of Clinical Microbiology 40, 252–255.CrossRefGoogle Scholar
Nitatori, T., Sato, N., Waguri, S., Karasawa, Y., Araki, H., Shibanai, K., Kominami, E. and Uchiyama, Y. ( 1995). Delayed neuronal death in the CA1 pyramidal cell layer of the gerbil hippocampus following transient ischemia is apoptosis. Journal of Neuroscience 15, 1001–1011.CrossRefGoogle Scholar
Okuda, D. T. and Coons, S. ( 2003). Naegleria fowleri meningoencephalitis. Neurology 61, E1.CrossRefGoogle Scholar
Rojas-Hernandez, S., Jarillo-Luna, A., Rodriguez-Monroy, M., Moreno-Fierros, L. and Campos-Rodriguez, R. ( 2004). Immunohistochemical characterization of the initial stages of Naegleria fowleri meningoencephalitis in mice. Parasitology Research 94, 31–36.Google Scholar
Ryu, J. S., Soh, C. T. and Im, K. I. ( 1984). Ultrastructural observation of Naegleria fowleri trophozoite in mouse brain and axenic culture. Kisaengchunghak Chapchi 22, 259–266.CrossRefGoogle Scholar
Scheidegger, A., Vonlaufen, N., Naguleswaran, A., Gianinazzi, C., Müller, N., Leib, S. L. and Hemphill, A. ( 2005). Differential effects of IFN-gamma and TNF-alpha on Toxoplasma gondii proliferation in organotypic rat brain slice cultures. Journal of Parasitology 91, 307–315.CrossRefGoogle Scholar
Stephany, J. D., Pearl, G. S. and Gonzalez, O. R. ( 2004). Pathologic quiz case: headache in an 8-year-old child. Primary amebic meningoencephalitis due to Naegleria fowleri. Archives of Pathology and Laboratory Medicine 128, 33–34.Google Scholar
Stoppini, L., Buchs, P. A. and Müller, D. ( 1991). A simple method for organotypic cultures of nervous tissue. Journal of Neuroscience Methods 37, 173–182.CrossRefGoogle Scholar
Stoppini, L., Buchs, P. A., Brun, R., Müller, D., Duport, S., Parisi, L. and Seebeck, T. ( 2000). Infection of organotypic slice cultures from rat central nervous tissue with Trypanosoma brucei brucei. International Journal of Medical Microbiology 290, 105–113.CrossRefGoogle Scholar
Strasser, U. and Fischer, G. ( 1995). Quantitative measurement of neuronal degeneration in organotypic hippocampal cultures after combined oxygen/glucose deprivation. Journal of Neuroscience Methods 57, 177–186.CrossRefGoogle Scholar
Toney, D. and Marciano-Cabral, M. F. ( 1994). Modulation of complement resistance and virulence of Naegleria fowleri amoebae by alterations in growth media. Journal of Eukaryotic Microbiology 41, 337–343.CrossRefGoogle Scholar
Tsvetkova, N., Schild, M., Panaiotov, S., Kurdova-Mintcheva, R., Gottstein, B., Walochnik, J., Aspock, H., Lucas, M. S. and Müller, N. ( 2004). The identification of free-living environmental isolates of amoebae from Bulgaria. Parasitology Research 92, 405–413.CrossRefGoogle Scholar
Vonlaufen, N., Gianinazzi, C., Müller, N., Simon, F., Björkman, C., Jungi, T. W., Leib, S. L. and Hemphill, A. ( 2002). Infection of organotypic slice cultures from rat central nervous tissue with Neospora caninum: an alternative approach to study host-parasite interactions. International Journal for Parasitology 32, 533–542.CrossRefGoogle Scholar