Skip to main content

Advertisement

Log in

Toxoplasma gondii invasion and replication in astrocyte primary cultures and astrocytoma cell lines: systematic review of the literature

  • Review
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

Toxoplasma gondii is a cosmopolitan protozoan which infects all homoeothermic species, including humans. This parasite may cause severe neurological problems in congenitally infected newborns or immunocompromised individuals, but it also provokes psychiatric and neurological disorders as well as behavioural and sensory deficit. There is controversy regarding the effect of T. gondii upon astrocytes, which may serve as parasite proliferation recipients or protective immune response activators within the central nervous system. This apparent contradiction could partially be due to the infection degree obtained in the different experiments reported. Thus, we decided to systematically review the in vitro models used to study these phenomena. Fifteen articles from which direct invasion and replication data could be gathered were found. Very heterogeneous results emerged, mainly due to diversity of models in relation to parasite strain (virulence), host species, parasite dose and evaluation times after infection. Also, the results were measured in diverse ways, i.e. some reported percent infected cells, while others informed parasites per vacuole or cell, or parasitic vacuoles per cell. Very few conclusions could be drawn, among them that human astrocytoma cell lines and mouse astrocytes seem more susceptible to infection and less resistant to tachyzoite proliferation than human primary culture astrocytes. The present study supports the need to reanalyse T. gondii astrocyte invasion and replication processes, especially with the use of actual technology, which allows detailed mechanistic studies.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Berdoy M, Webster J, Macdonald D (2000) Fatal attraction in rats infected with Toxoplasma gondii. Proc Biol Sci 267:1591–1594

    Article  PubMed  CAS  Google Scholar 

  • Boyle JP, Radke JR (2009) A history of studies that examine the interactions of Toxoplasma with its host cell emphasis on in vitro models. Int J Parasitol 39:903–914

    Article  PubMed  Google Scholar 

  • Brenier-Pinchart MP, Blanc-Gonnet E, Marche PN, Berger F, Durand F, Ambroise-Thomas P, Pelloux H (2004) Infection of human astrocytes and glioblastoma cells with Toxoplasma gondii: monocyte chemotactic protein 1 secretion and chemokine expression in vitro. Acta Neuropathol 107:245–249

    Article  PubMed  CAS  Google Scholar 

  • Carruthers VB, Suzuki Y (2007) Effects of Toxoplasma gondii infection on the brain. Schizophr Bull 33:745–751

    Article  PubMed  Google Scholar 

  • Creuzet C, Robert F, Roisin MP, Van Tan H, Benes C, Dupouy-Camet FR (1998) Neurons in primary culture are less efficiently infected by Toxoplasma gondii than glial cells. Parasitol Res 84:25–30

    Article  PubMed  CAS  Google Scholar 

  • Däubener W, Pilz K, Seghrouchni-Zennati S, Bilzer T, Fischer HG, Hadding U (1993) Induction of toxoplasmostasis in a human glioblastoma by interferon gamma. J Neuroimmunol 43:31–38

    Article  PubMed  Google Scholar 

  • Däubener W, Remscheid C, Nockemann S, Pilz K, Seghrouchni S, Mackenzie C, Seghrouchni S, Hadding U (1996) Anti-parasitic effector mechanisms in human brain tumor cells: role of interferon-gamma and tumor necrosis factor-alpha. Eur J Immunol 26:487–492

    Article  PubMed  Google Scholar 

  • el-Sagaff S, Salem HS, Nichols W, Tonkel AK, Abo-Zenadah NY (2005) Cell death pattern in cerebellum neurons infected with Toxoplasma gondii. J Egypt Soc Parasitol 35:809–818

    PubMed  Google Scholar 

  • Estran C, Brenier-Pinchart MP, Pelletier L, Cesbron-Delauw MF, Pelloux H (2006) Toxoplasma gondii in human astrocytes in vitro: interleukin (IL)-12 and IL-10 do not influence cystogenesis. J Parasitol 92:1108–1110

    Article  PubMed  CAS  Google Scholar 

  • Fagard R, Van Tan H, Creuzet C, Pelloux H (1999) Differential development of Toxoplasma gondii in neural cells. Parasitol Today 15:504–507

    Article  PubMed  CAS  Google Scholar 

  • Fischer HG, Nitzgen B, Reichmann G, Gross U, Hadding U (1997a) Cytokine responses induced by Toxoplasma gondii in astrocytes and microglial cells. Eur J Immunol 27:1539–1548

    Article  PubMed  CAS  Google Scholar 

  • Fischer HG, Nitzgen B, Reichmann G, Gross U, Hadding U (1997b) Host cells of Toxoplasma gondii encystation in infected primary culture from mouse brain. Parasitol Res 83:637–641

    Article  PubMed  CAS  Google Scholar 

  • Flegr J, Kodym P, Tolarova V (2000) Correlation of duration of latent Toxoplasma gondii infection with personality changes in women. Biol Psychol 53:57–68

    Article  PubMed  CAS  Google Scholar 

  • Giaume C, Kirchhoff F, Matute C, Reichenbach A, Verkhratsky A (2007) Glia: the fulcrum of brain diseases. Cell Death Differ 14:1324–1335

    Article  PubMed  CAS  Google Scholar 

  • Gulinello M, Acquarone M, Kim JH, Spray DC, Barbosa HS, Sellers R, Tanowitz HB, Weiss LM (2010) Acquired infection with Toxoplasma gondii in adult mice results in sensorimotor deficits but normal cognitive behavior despite widespread brain pathology. Microbes Infect 12:528–537

    Article  PubMed  CAS  Google Scholar 

  • Halonen SK, Weiss LM (2000) Investigation into the mechanism of gamma interferon-mediated inhibition of Toxoplasma gondii in murine astrocytes. Infect Immun 68:3426–3430

    Article  PubMed  CAS  Google Scholar 

  • Halonen SK, Lyman WD, Chiu FC (1996) Growth and development of Toxoplasma gondii in human neurons and astrocytes. J Neuropathol Exp Neurol 55:1150–1156

    Article  PubMed  CAS  Google Scholar 

  • Halonen SK, Chiu F, Weiss LM (1998) Effect of cytokines on growth of Toxoplasma gondii in murine astrocytes. Infect Immun 66:4989–4993

    PubMed  CAS  Google Scholar 

  • Hamidinejat H, Ghorbanpoor M, Hosseini H, Alavi SM, Nabavi L, Jalali MH, Borojeni MP, Jafari H, Mohammadaligol S (2010) Toxoplasma gondii infection in first-episode and patient individuals with schizophrenia. Int J Infect Dis 14:978–981

    Article  Google Scholar 

  • Jones J, Lopez A, Wilson M (2003) Congenital toxoplasmosis. Am Fam Physician 67:2131–2138

    PubMed  Google Scholar 

  • Lüder CGK, Giraldo-Velásquez M, Sendtner M, Gross U (1999) Toxoplasma gondii in primary rat CNS cells: differential contribution of neurons, astrocytes, and microglial cells for the intracerebral development and stage differentiation. Exp Parasitol 93:23–32

    Article  PubMed  Google Scholar 

  • Martens S, Parvanova I, Zerrahn J, Griffiths G, Schell G, Reichmann G, Howard JC (2005) Disruption of Toxoplasma gondii parasitophorous vacuoles by the mouse p47 resistance GTPases. PLoS Pathog 1:24–30

    Article  Google Scholar 

  • Melzer T, Duffy A, Weiss LM, Halonen SK (2008) The gamma interferon (IFN-gamma) inducible GTP-binding protein IGTP is necessary for toxoplasma vacuolar disruption and induces parasite egression in IFN-gamma-stimulated astrocytes. Infect Immun 76:4883–4894

    Article  PubMed  CAS  Google Scholar 

  • Montoya JG, Liesenfeld O (2004) Toxoplasmosis. Lancet 363:1965–1976

    Article  PubMed  CAS  Google Scholar 

  • Pelloux H, Ricard J, Nissou MF, Renversez JC, Vuillez JP, Meunier A, Ambroise-Thomas P (1994) Infection with Toxoplasma gondii does not alter TNF-α and IL-6 secretion by a human astrocytoma cell line. Mediators Inflamm 3:291–295

    Article  PubMed  CAS  Google Scholar 

  • Pelloux H, Pernod G, Polack B, Coursange E, Ricard J, Verna JM, Ambroise-Thomas P (1996) Influence of cytokines on Toxoplasma gondii growth in human astrocytoma-derived cells. Parasitol Res 82:598–603

    Article  PubMed  CAS  Google Scholar 

  • Peterson PK, Gekker G, Hu S, Chao C (1993) Intracellular survival and multiplication of Toxoplasma gondii in astrocytes. J Infect Dis 168:1472–1478

    Article  PubMed  CAS  Google Scholar 

  • Peterson PK, Gekker G, Hu S, Chao CC (1995) Human astrocytes inhibit intracellular multiplication of Toxoplasma gondii by a nitric oxide-mediated mechanism. J Infect Dis 171:516–518

    Article  PubMed  CAS  Google Scholar 

  • Shen DF, Matteson DM, Tuaillon N, Suedekum BK, Buggage RR, Chan CC (2001) Involvement of apoptosis and interferon-gamma in murine toxoplasmosis. Invest Ophthalmol Vis Sci 42:2031–2036

    PubMed  CAS  Google Scholar 

  • Skallová A, Kodym P, Frynta D, Flegr J (2006) The role of dopamine in Toxoplasma-induced behavioural alterations in mice: an ethological and ethopharmacological study. Parasitology 133:525–535

    Article  PubMed  Google Scholar 

  • Strack A, Asensio VC, Campbell IL, Schlüter D, Deckert M (2002) Chemokines are differentially expressed by astrocytes, microglia and inflammatory leukocytes in Toxoplasma encephalitis and critically regulated by interferon-gamma. Acta Neuropathol 103:458–468

    Article  PubMed  CAS  Google Scholar 

  • Takahashi J, Fukuda T, Tanaka J, Minamitani M, Onouchi K, Makioka A (2001) Bax-induced apoptosis not demonstrated in the congenital toxoplasmosis in mice. Brain Dev 23:50–53

    Article  PubMed  CAS  Google Scholar 

  • Troyo A, Chinchilla M (2003) In vitro multiplication of Toxoplasma gondii and Trypanosoma cruzi in mouse, rat and hamster astrocytes. Rev Biol Trop 51:639–645

    PubMed  Google Scholar 

  • Volterra A, Meldolesi J (2005) Astrocytes, from brain glue to communication elements: the revolution continues. Nat Rev Neurosci 6:626–640

    Article  PubMed  CAS  Google Scholar 

  • Vyas A, Kim SK, Giacomini N, Boothroyd JC, Sapolsky RM (2007) Behavioral changes induced by Toxoplasma infection of rodents are highly specific to aversion of cat odors. Proc Natl Acad Sci U S A 104:6442–6447

    Article  PubMed  CAS  Google Scholar 

  • Webster JP, McConkey GA (2010) Toxoplasma gondii-altered host behaviour: clues as to mechanism of action. Folia Parasitol (Praha) 57:95–104

    Google Scholar 

  • Wilson EH, Hunter CA (2004) The role of astrocytes in the immunopathogenesis toxoplasmic encephalitis. Int J Parasitol 34:543–548

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Dolores Correa.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Contreras-Ochoa, C.O., Lagunas-Martínez, A., Belkind-Gerson, J. et al. Toxoplasma gondii invasion and replication in astrocyte primary cultures and astrocytoma cell lines: systematic review of the literature. Parasitol Res 110, 2089–2094 (2012). https://doi.org/10.1007/s00436-012-2836-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-012-2836-7

Keywords

Navigation