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Published in: Acta Neuropathologica 3/2004

01-03-2004 | Regular Paper

Infection of human astrocytes and glioblastoma cells with Toxoplasma gondii: monocyte chemotactic protein-1 secretion and chemokine expression in vitro

Authors: Marie-Pierre Brenier-Pinchart, Emmanuelle Blanc-Gonnet, Patrice N. Marche, François Berger, François Durand, Pierre Ambroise-Thomas, Hervé Pelloux

Published in: Acta Neuropathologica | Issue 3/2004

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Abstract

In immunocompromised hosts, disruption of toxoplasmic cysts and conversion from bradyzoites to tachyzoites occur in brain. In these areas, infiltrates of mononuclear cells are observed. In the murine toxoplasmosis model, recent data suggest that chemokines may play a role in leukocyte recruitment in the central nervous system (CNS). This study analyzed the monocyte chemotactic protein-1 (MCP-1) secretion and chemokine expression after Toxoplasma gondii infection of human astrocytes, glioblastoma cells (U373) and fibroblasts (MRC5) in vitro. T. gondii infection of these CNS cells, astrocytes and glioblastoma cells significantly increased MCP-1 secretion, particularly for astrocytes. In our cellular models, the pattern of chemokine gene expression is dominated by MCP-1 expression. MCP-1 mRNAs were also quantified by real-time-PCR (LightCycler). The behavior of cells studied after T. gondii infection was different (invasion and growth) and the cell mechanisms of chemokine regulation could be dependent on the type of cells infected, while MCP-1 may contribute to the cell recruitment during human cerebral reactivation of T. gondii.
Literature
1.
go back to reference Adams DH, Lloyd AR (1997) Chemokines: leucocytes recruitment and activation cytokines. Lancet 349:490–495CrossRefPubMed Adams DH, Lloyd AR (1997) Chemokines: leucocytes recruitment and activation cytokines. Lancet 349:490–495CrossRefPubMed
2.
go back to reference Bajetto A, Bonavia R, Barbero S, Florio T, Schettini G (2001) Chemokines and their receptors in the central nervous system. Front Neuroendocrin 22:147–184CrossRef Bajetto A, Bonavia R, Barbero S, Florio T, Schettini G (2001) Chemokines and their receptors in the central nervous system. Front Neuroendocrin 22:147–184CrossRef
3.
go back to reference Bonhomme A, Bouchot A, Pezzella N, Gomez J, Le Moal H, Pinon JM (1999) Signaling during the invasion of host cells by Toxoplasma gondii. FEMS Microbiol Rev 23:551–561CrossRefPubMed Bonhomme A, Bouchot A, Pezzella N, Gomez J, Le Moal H, Pinon JM (1999) Signaling during the invasion of host cells by Toxoplasma gondii. FEMS Microbiol Rev 23:551–561CrossRefPubMed
4.
go back to reference Brenier-Pinchart MP, Pelloux H, Simon J, Ricard J, Bosson JL, Ambroise-Thomas P (2000) Toxoplasma gondii induces the secretion of monocyte chemotactic protein-1 in human fibroblasts, in vitro. Mol Cell Biochem 209:79–87CrossRefPubMed Brenier-Pinchart MP, Pelloux H, Simon J, Ricard J, Bosson JL, Ambroise-Thomas P (2000) Toxoplasma gondii induces the secretion of monocyte chemotactic protein-1 in human fibroblasts, in vitro. Mol Cell Biochem 209:79–87CrossRefPubMed
5.
go back to reference Brenier-Pinchart MP, Pelloux H, Derouich-Guergour D, Ambroise-Thomas P (2001) Chemokines in host-protozoan-parasite interactions. Trends Parasitol 17:292–296CrossRefPubMed Brenier-Pinchart MP, Pelloux H, Derouich-Guergour D, Ambroise-Thomas P (2001) Chemokines in host-protozoan-parasite interactions. Trends Parasitol 17:292–296CrossRefPubMed
6.
go back to reference Brenier-Pinchart MP, Vigan I, Jouvin-Marche E, Marche PN, Pelet E, Gross U, Ambroise-Thomas P, Pelloux H (2002) Monocyte chemotactic protein-1 secretion and expression after Toxoplasma gondii infection in vitro depend on the stage of the parasite. FEMS Microbiol Lett 214:45–49CrossRefPubMed Brenier-Pinchart MP, Vigan I, Jouvin-Marche E, Marche PN, Pelet E, Gross U, Ambroise-Thomas P, Pelloux H (2002) Monocyte chemotactic protein-1 secretion and expression after Toxoplasma gondii infection in vitro depend on the stage of the parasite. FEMS Microbiol Lett 214:45–49CrossRefPubMed
7.
go back to reference Däubener W, Pilz K, Zennati SS, Bilzer T, Fisher HG, Hadding U (1993) Induction of toxoplasmostasis in a human glioblastoma by interferon γ. J Neuroimmunol 43:31–38CrossRefPubMed Däubener W, Pilz K, Zennati SS, Bilzer T, Fisher HG, Hadding U (1993) Induction of toxoplasmostasis in a human glioblastoma by interferon γ. J Neuroimmunol 43:31–38CrossRefPubMed
8.
go back to reference Denney CF, Eckmann L, Reed SL (1999) Chemokine secretion of human cells in response to Toxoplasma gondii infection. Infect Immun 67:1547–1552PubMed Denney CF, Eckmann L, Reed SL (1999) Chemokine secretion of human cells in response to Toxoplasma gondii infection. Infect Immun 67:1547–1552PubMed
9.
go back to reference Fagard R, Van Tan H, Creuzet C, Pelloux H (1999) Differential development of Toxoplasma gondii in neuronal cells. Parasitol Today 15:504–507CrossRefPubMed Fagard R, Van Tan H, Creuzet C, Pelloux H (1999) Differential development of Toxoplasma gondii in neuronal cells. Parasitol Today 15:504–507CrossRefPubMed
10.
go back to reference Frenkel JK (1988) Pathophysiology of toxoplasmosis. Parasitol Today 4:273–278CrossRef Frenkel JK (1988) Pathophysiology of toxoplasmosis. Parasitol Today 4:273–278CrossRef
11.
go back to reference Halonen SK, Lyman WD, Chiu FC (1996) Growth and development of Toxoplasma gondii in human neurons and astrocytes. J Neuropathol Exp Neur 55:1150–1156 Halonen SK, Lyman WD, Chiu FC (1996) Growth and development of Toxoplasma gondii in human neurons and astrocytes. J Neuropathol Exp Neur 55:1150–1156
12.
go back to reference Hunter CA, Remington JS (1994) Immunopathogenesis of toxoplasmosis encephalitis. J Infect Dis 170:1057–1067PubMed Hunter CA, Remington JS (1994) Immunopathogenesis of toxoplasmosis encephalitis. J Infect Dis 170:1057–1067PubMed
13.
go back to reference Kim JM, Oh YK, Kim YJ, Cho SJ, Ahn MH, Cho YJ (2001) Nuclear factor-kappa B plays a major role in the regulation of chemokine expression of HeLa cells in response to Toxoplasma gondii. Parasitol Res 87:758–763CrossRefPubMed Kim JM, Oh YK, Kim YJ, Cho SJ, Ahn MH, Cho YJ (2001) Nuclear factor-kappa B plays a major role in the regulation of chemokine expression of HeLa cells in response to Toxoplasma gondii. Parasitol Res 87:758–763CrossRefPubMed
14.
go back to reference Luther AS, Cyster JG (2001) Chemokines as regulators of T cell differentiation. Nat Immunol 2:102–107CrossRefPubMed Luther AS, Cyster JG (2001) Chemokines as regulators of T cell differentiation. Nat Immunol 2:102–107CrossRefPubMed
15.
go back to reference Peterson PK, Gekker G, Hu S, Chao CC (1993) Intracellular survival and multiplication of Toxoplasma gondii in astrocytes. J Infect Dis 168:1472–1478PubMed Peterson PK, Gekker G, Hu S, Chao CC (1993) Intracellular survival and multiplication of Toxoplasma gondii in astrocytes. J Infect Dis 168:1472–1478PubMed
16.
go back to reference Reiter-Owona I, Seitz H, Gross U, Sahm M, Rockstroh JK, Seitz HM (2000) Is stage conversion the initiating event for reactivation of Toxoplasma gondii in brain of AIDS patients? J Parasitol 86:531–536PubMed Reiter-Owona I, Seitz H, Gross U, Sahm M, Rockstroh JK, Seitz HM (2000) Is stage conversion the initiating event for reactivation of Toxoplasma gondii in brain of AIDS patients? J Parasitol 86:531–536PubMed
17.
go back to reference Schlüter D, Deckert M, Hof H, Frei K (2001) Toxoplasma gondii infection of neurons induces neuronal cytokine and chemokine production, but gamma interferon and tumor necrosis factor-stimulated neurones fail to inhibit the invasion and growth of T. gondii. Infect Immun 69:7889–7893CrossRefPubMed Schlüter D, Deckert M, Hof H, Frei K (2001) Toxoplasma gondii infection of neurons induces neuronal cytokine and chemokine production, but gamma interferon and tumor necrosis factor-stimulated neurones fail to inhibit the invasion and growth of T. gondii. Infect Immun 69:7889–7893CrossRefPubMed
18.
go back to reference Senger DL, Tudan C, Guiot MC, Mazzoni IE, Molenkamp G, LeBlanc R, Antel J, Olivier A, Snipes GJ, Kaplan DR (2002) Suppression of Rac activity induces apoptosis of human glioma cells but not normal human astrocytes. Cancer Res 62:2131–2140PubMed Senger DL, Tudan C, Guiot MC, Mazzoni IE, Molenkamp G, LeBlanc R, Antel J, Olivier A, Snipes GJ, Kaplan DR (2002) Suppression of Rac activity induces apoptosis of human glioma cells but not normal human astrocytes. Cancer Res 62:2131–2140PubMed
19.
go back to reference Sharafeldin A, Eltayeb R, Pashenkov M, Bakhiet M (2000) Chemokines are produced in the brain early during the course of experimental African trypanosomiasis. J Neuroimmunol 103:165–170CrossRefPubMed Sharafeldin A, Eltayeb R, Pashenkov M, Bakhiet M (2000) Chemokines are produced in the brain early during the course of experimental African trypanosomiasis. J Neuroimmunol 103:165–170CrossRefPubMed
20.
go back to reference Strack A, Asensio VC, Campbell IL, Schlülter D, Deckert M (2002) Chemokines are differentially expressed by astrocytes, microglia and inflammatory leukocytes in Toxoplasma encephalitis and critically regulated by interferon-γ. Acta Neuropathol 103:454–468CrossRef Strack A, Asensio VC, Campbell IL, Schlülter D, Deckert M (2002) Chemokines are differentially expressed by astrocytes, microglia and inflammatory leukocytes in Toxoplasma encephalitis and critically regulated by interferon-γ. Acta Neuropathol 103:454–468CrossRef
21.
go back to reference Strack A, Schlüter D, Asension VC, Capbell IL, Deckert M (2002) Regulation of the kinetics of intracerebral chemokine gene expression in murine Toxoplasma encephalitis: impact of host genetic factors. Glia 40:372–377CrossRefPubMed Strack A, Schlüter D, Asension VC, Capbell IL, Deckert M (2002) Regulation of the kinetics of intracerebral chemokine gene expression in murine Toxoplasma encephalitis: impact of host genetic factors. Glia 40:372–377CrossRefPubMed
22.
go back to reference Suzuki Y (2002) Host resistance in the brain against Toxoplasma gondii. J Infect Dis 185:58–65CrossRef Suzuki Y (2002) Host resistance in the brain against Toxoplasma gondii. J Infect Dis 185:58–65CrossRef
23.
go back to reference Takeshima H, Kuratsu JI, Takeya M, Yoshimura T, Ushio Y (1994) Expression and localization of messenger RNA and protein for monocyte chemoattractant protein-1 in human malignant glioma. J Neurosurg 8:1056–1062 Takeshima H, Kuratsu JI, Takeya M, Yoshimura T, Ushio Y (1994) Expression and localization of messenger RNA and protein for monocyte chemoattractant protein-1 in human malignant glioma. J Neurosurg 8:1056–1062
Metadata
Title
Infection of human astrocytes and glioblastoma cells with Toxoplasma gondii: monocyte chemotactic protein-1 secretion and chemokine expression in vitro
Authors
Marie-Pierre Brenier-Pinchart
Emmanuelle Blanc-Gonnet
Patrice N. Marche
François Berger
François Durand
Pierre Ambroise-Thomas
Hervé Pelloux
Publication date
01-03-2004
Publisher
Springer-Verlag
Published in
Acta Neuropathologica / Issue 3/2004
Print ISSN: 0001-6322
Electronic ISSN: 1432-0533
DOI
https://doi.org/10.1007/s00401-003-0804-0

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