Skip to main content
Log in

Murine leukocytes stimulation by Toxoplasma gondii antigens induces high level of IFN-γ production

  • Original Article
  • Published:
Comparative Clinical Pathology Aims and scope Submit manuscript

Abstract

Toxoplasma gondii (T. gondii) is an obligate intracellular parasitic protozoan, infecting a wide range of warm-blooded vertebrates. It is important for T. gondii to balance the response between cellular and humoral immune system for various aspects of its own survival. The aim of this study was to determine the level of IFN-γ and IL-4 production by murine peritoneal leukocytes stimulated with T. gondii lysate antigens (TLAs), excretory/secretory antigens (ESAs), and a combination of them (TLAs:ESAs). TLAs, ESAs, and TLA + ESA, considered as the experimental groups, were prepared and used to stimulate murine peritoneal leukocytes. The level of the IFN-γ and IL-4 secreted by the stimulated leukocytes was measured. In addition, untreated and phytohemagglutinin-treated groups were considered as negative and positive controls, respectively. As compared to the negative control, the level of IL-4 was lower in each of the experimental groups (P < 0.05); however, no statistically significant difference was observed between the positive control and each of the experimental groups (P > 0.05). Moreover, there was a significant difference for the level of IFN-γ between each of the experimental groups and both negative and positive controls (P < 0.05). The findings showed that the antigens of T. gondii were able to increase the IFN-γ production and decrease the level of IL-4 production.

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.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Andrew SM, Titus JA, Zumstein L (2002) Dialysis and concentration of protein solutions. Curr Protoc Toxicol appendix 3:a.3h.:1–5. https://doi.org/10.1002/0471140856.txa03hs10

  • Chaves AC, Ceravolo IP, Gomes JA, Zani CL, Romanha AJ, Gazzinelli RT (2001) IL-4 and IL-13 regulate the induction of indoleamine 2,3-dioxygenase activity and the control of toxoplasma gondii replication in human fibroblasts activated with IFN-gamma. Eur J Immunol 31:333–344. https://doi.org/10.1002/1521-4141(200102)31:2&#60;333::aid-immu333&#62;3.0.co;2-x

  • Coombes JL, Hunter CA (2015) Immunity to toxoplasma gondii--into the 21st century. Parasite Immunol 37:105–107. https://doi.org/10.1111/pim.12177

    Article  PubMed  CAS  Google Scholar 

  • Costa-Silva T, Meira C, Ferreira I, Hiramoto R, Pereira-Chioccola V (2008) Evaluation of immunization with tachyzoite excreted-secreted proteins in a novel susceptible mouse model (A/Sn) for Toxoplasma gondii. Exp Parasitol 120:227

    Article  CAS  Google Scholar 

  • Costa-Silva TA, Borges MM, Galhardo CS, Pereira-Chioccola VL (2012) Immunization with excreted/secreted proteins in AS/n mice activating cellular and humoral response against Toxoplasma gondii infection. Acta Trop 124:203–209. https://doi.org/10.1016/j.actatropica.2012.08.013

    Article  PubMed  CAS  Google Scholar 

  • Daryani A et al (2014a) Determination of parasitic load in different tissues of murine toxoplasmosis after immunization by excretory-secretory antigens using Real time QPCR. Exp Parasitol 143:55

    Article  CAS  Google Scholar 

  • Daryani A, Sharif M, Kalani H, Rafiei A, Kalani F, Ahmadpour E (2014b) Electrophoretic Patterns of Toxoplasma gondii Excreted/Secreted Antigens and Their Role in Induction of the Humoral Immune Response. Jundishapur J Microbiol 7:e9525–e9525. https://doi.org/10.5812/jjm.9525

    Article  PubMed  PubMed Central  Google Scholar 

  • Dogruman-Al F, Fidan I, Celebi B, Yesilyurt E, Erdal B, Babur C, Kustimur S (2011) Cytokine profile in murine toxoplasmosis. Asian Pac J Trop Med 4:16–19. https://doi.org/10.1016/s1995-7645(11)60024-2

    Article  PubMed  CAS  Google Scholar 

  • Faridnia R, Daryani A, Sarvi S, Sharif M, Kalani H (2018) Vaccination against Toxoplasma gondii using rhoptry antigens: a systematic review. Comp Immunol Microbiol Infect Dis 59:32–40. https://doi.org/10.1016/j.cimid.2018.09.005

    Article  PubMed  Google Scholar 

  • Gazzinelli RT et al (1994) Parasite-induced IL-12 stimulates early IFN-gamma synthesis and resistance during acute infection with toxoplasma gondii. J Immunol (Baltimore, md : 1950) 153:2533–2543

    CAS  Google Scholar 

  • Gazzinelli RT et al (1996) In the absence of endogenous IL-10, mice acutely infected with toxoplasma gondii succumb to a lethal immune response dependent on CD4+ T cells and accompanied by overproduction of IL-12, IFN-gamma and TNF-alpha. J Immunol (Baltimore, md : 1950) 157:798–805

    CAS  Google Scholar 

  • Halonen SK, Weiss LM (2013) Toxoplasmosis. Handb Clin Neurol 114:125–145. https://doi.org/10.1016/B978-0-444-53490-3.00008-X

    Article  PubMed  PubMed Central  Google Scholar 

  • Hehl AB et al (2015) Asexual expansion of toxoplasma gondii merozoites is distinct from tachyzoites and entails expression of non-overlapping gene families to attach, invade, and replicate within feline enterocytes. BMC Genomics 16:66. https://doi.org/10.1186/s12864-015-1225-x

    Article  PubMed  PubMed Central  Google Scholar 

  • Kalani H et al (2016a) Comparison of eight cell-free media for maintenance of Toxoplasma gondii tachyzoites. Iran J Parasitol 11:104–109

    PubMed  PubMed Central  Google Scholar 

  • Kalani H, Khanahmad Shahreza H, Daryani A, Yousefi HA, Pestechian N, Mansouri V (2016b) The gene expression level of IFN-gammaR1 and IFN-gammaR2 in a murine model treated with Toxoplasma gondii and its products. Gastroenterol Hepatol Bed Bench 9:124–131

    PubMed  PubMed Central  Google Scholar 

  • Kalani H, Khanahmad Shahreza H, Daryani A, Yousefi HA, Pestechian N, Mansouri V (2016c) The gene expression level of IFN-γR1 and IFN-γR2 in a murine model treated with toxoplasma gondii and its products. Gastroenterols Hepatol Bed Bench 9:124–131

    Google Scholar 

  • Khan IA, Schwartzman JD, Matsuura T, Kasper LH (1997) A dichotomous role for nitric oxide during acute Toxoplasma gondii infection in mice. Proc Natl Acad Sci U S A 94:13955–13960

    Article  CAS  Google Scholar 

  • Kruger NJ (1994) The Bradford method for protein quantitation. Methods Mol Biol (Clifton, NJ) 32:9–15. https://doi.org/10.1385/0-89603-268-x:9

    Article  CAS  Google Scholar 

  • Nguyen TD et al (2003) Virulent Toxoplasma gondii strain RH promotes T-cell-independent overproduction of proinflammatory cytokines IL12 and gamma-interferon. J Med Microbiol 52:869–876. https://doi.org/10.1099/jmm.0.04860-0

    Article  PubMed  CAS  Google Scholar 

  • Pestechian N, Khanahmad Shahreza H, Faridnia R, Kalani H (2016) Manipulation of IL-10 gene expression by toxoplasma gondii and its products. Med J Islam Repub Iran 30:410

    PubMed  PubMed Central  Google Scholar 

  • Roberts CW, Ferguson DJ, Jebbari H, Satoskar A, Bluethmann H, Alexander J (1996) Different roles for interleukin-4 during the course of toxoplasma gondii infection. Infect Immun 64:897–904

    Article  CAS  Google Scholar 

  • Suzuki Y (2002) Host resistance in the brain against Toxoplasma gondii. J Infect Dis 185(Suppl 1):S58–S65. https://doi.org/10.1086/337999

    Article  PubMed  CAS  Google Scholar 

  • Swierczynski B, Bessieres MH, Cassaing S, Guy S, Oswald I, Seguela JP, Pipy B (2000) Inhibitory activity of anti-interleukin-4 and anti-interleukin-10 antibodies on toxoplasma gondii proliferation in mouse peritoneal macrophages cocultured with splenocytes from infected mice. Parasitol Res 86:151–157

    Article  CAS  Google Scholar 

  • Wagner A et al (2015) Prime-boost vaccination with toxoplasma lysate antigen, but not with a mixture of recombinant protein antigens, leads to reduction of brain cyst formation in BALB/c mice. PloS one 10:e0126334. https://doi.org/10.1371/journal.pone.0126334

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhao Y, Wilson D, Matthews S, Yap GS (2007) Rapid elimination of toxoplasma gondii by gamma interferon-primed mouse macrophages is independent of CD40 signaling. Infect Immun 75:4799–4803. https://doi.org/10.1128/iai.00738-07

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Acknowledgments

The authors are thankful to Mrs. Mahin Ghafourzadeh for their kind assistance at the laboratory.

Funding

The Vice Chancellor of Research and Technology, Shahid Sadoughi University of Medical Sciences and Health Services provided funding for this study (grant no: 795).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Hamed Kalani.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fattahi-Bafghi, A., Mirzaei, F., Mirjalili, A. et al. Murine leukocytes stimulation by Toxoplasma gondii antigens induces high level of IFN-γ production. Comp Clin Pathol 29, 533–537 (2020). https://doi.org/10.1007/s00580-020-03091-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00580-020-03091-2

Keywords

Navigation