Behavioral alterations induced by Toxoplasma gondii during different stages of infection in mice | ||||
| Journal of Applied Veterinary Sciences | ||||
| Article 1, Volume 1, Issue 1, October 2016, Page 1-6 PDF (381.92 K) | ||||
| Document Type: Original Article | ||||
| DOI: 10.21608/javs.2016.61815 | ||||
 View on SCiNiTO | ||||
| Authors | ||||
Motamed Elsayed Mahmoud  1; Yoshifumi Nishikawa2
| ||||
| 1Department of Animal Behavior and Husbandry, Faculty of Veterinary Medicine, Sohag University, Sohag, 82524, Egypt | ||||
| 2National Research Center for Protozoan Diseases, Host Defense Research Unit, Obihiro University of Agriculture and Veterinary Medicine, Inada-cho, Obihiro, Hokkaido 080-8555, Japan | ||||
| Abstract | ||||
| Acute, chronic and reactivation of Toxoplasma gondii (T. gondii) infections are approximately found in 30-60% of population world-wide. T. gondii is a pathogen relevant to psychiatric disorders. We have recently found that reactivation of chronic T. gondii induced depressive-like behaviors in mice. In the present study, we aimed to illustrate the behavioral alterations in mice during acute, chronic and after reactivation of chronic T. gondii. Behavioral battery included sucrose preference and forced swim, and fear conditioning tests, and measurement of locomotor activity following T. gondii infection in mice. First, we prepared an ethogram and confirmed that specific pathogen free-BALB/c mice exhibited sickness-like behaviors during acute infection. In addition, reduced sucrose preference and increased immobility in forced swim test (putative indicators to anhedonic and despair-like behaviors, respectively) were exhibited in acute phase. While in chronic stage such symptoms were not exhibited at all. In turn, relapse of depressive- and some of sickness-like symptoms noticed after reactivation of chronic T. gondii infection. Interestingly, increased freezing time in fear conditioning was displayed during acute and reactivated T. gondii but not during chronic infection. Further, despite the well-known contribution of neurotransmitters; serotonin and dopamine in major depressive disorder, low levels of these neurotransmitters were observed in the brain not only in acute but also during chronic infection. Without interpolation of these symptoms to human psychiatric disorders, collectively, our results demonstrated the crucial changes induced by acute and reactivated T. gondii in modifying the behavior of mice. | ||||
| Keywords | ||||
| Depressive-and sickness-like behaviors; Mice; Toxoplasma gondii infection | ||||
| References | ||||
|
BORSINI, F., VOLTERRA, G., MELI. A. 1986. Does the behavioral "despair" test measure "despair"? Physiology and Behavior 38: 385–386.
BARLOW, D.H., DURAND, V.M. 2005. Abnormal Psychology: An Integrative Approach , 5th edition, Belmont, CA, USA: Thomson Wadsworth, pp. 248.
BERDOY, M., WEBSTER, J.P., MACDONALD, D.W. 2000. Fatal attraction in rats infected with Toxoplasma gondii. Proceding, Biological Sciences/The royal Society 267:1591–1594.
BROWN, C.R., HUNTER, C.A., ESTES, R.G., BECKMANN, E., FORMAN, J., DAVID, C., REMINGTON, J.S., MCLEOD, R. 1995. Definitive identification of a gene that confers resistance against Toxoplasma cyst burden and encephalitis. Immunology 85: 419–428.
CARRUTHERS, V.B., SUZUKI, Y. 2007. Effects of Toxoplasma gondii infection on the brain.Schizophrenia Bulletin 33:745–751.
DUPONT, C.D., CHRISTIAN, D.A., HUNTER, C.A. 2012. "Immune response and immunopathology during toxoplasmosis". Seminal Immunopathology 34: 793.
DÄUBENER, W., WANAGAT, N., PILZ K., SEGHROUCHNI, S., FISCHER, H.G., HADDING, U. 1994. A new, simple, bioassay for human IFN-gamma. Journal of Immunological Methods 168: 39–47.
FUJIGAKI, S., SAITO, K., TAKEMURA, M., MAEKAWA, N., YAMADA, Y., WADA, H., SEISHIMA, M. 2002. L-Tryptophan-l-Kynurenine Pathway Metabolism Accelerated by Toxoplasma gondii Infection Is Abolished in Gamma Interferon-Gene-Deficient Mice: Cross-Regulation between Inducible Nitric Oxide Synthase and Indoleamine-2, 3-Dioxygenase. Infection and Immunity 70: 779–786.
FUKUI,S., SCHWARCZ, R., RAPOPORT, S.I., TAKADA, Y., SMITH, Q.R.1991. Blood-brain barrier transport of kynurenines: implications for brain synthesis and metabolism. Journal of Neurochemistry. 56: 2007–2017.
KIM, H., CHEN, L., LIM, G., SUNG, B., WANG, S., MCCABE, M.F., RUSANESCU, G., YANG, L., TIAN, Y., MAO, J. 2012. Brain indoleamine 2, 3-dioxygenase contributes to the comorbidity of pain and depression. Journal of Clinical Investigation. 122: 2940–2954.
LESTAGE, J., VERRIER, D., PALIN, K., DANTZER, R. 2002. The enzyme indoleamine 2, 3-dioxygenase is induced in the mouse brain in response to peripheral administration of lipopolysaccharide and superantigen. Brain, Behavior and Immunity 16: 596–601.
LING, V, J., LESTER, D., MORTENSEN, P.B., LANGENBERG, P.W., POSTOLACHE, T.T. 2011."Toxoplasma gondii Seropositivity and Suicide rates in Women". Journal of Nervous and Mental Disorders 199: 440–444
LYONS, R. E., MCLEOD, R., ROBERTS, C.W. 2002 Toxoplasma gondii tachyzoite- bradyzoite interconversion. Trends in Parasitology. 18:198–201.
MAHMOUD, M.E., Ihara, F., Fereig, R.M., NISHIMURA, M., Y. NISHIKAWA. 2016. Induction of depression-related behaviors by reactivation of chronic Toxoplasma gondii infection in mice. Behavioral Brain Research 298: 125–133.
MAHMOUD, M.E., F., SALMAN, D., NISHIMURA, Y.NISHIKAWA, M. 2015. Mechanisms of interferon-beta-induced inhibition of T. gondii growth in murine macrophages and embryonic fibroblasts: role of immunity-related GTPaseM1.Cellular Microbiol.17:1069.
MONTOYA, J.G., LIESENFELD, O. 2004. "Toxoplasmosis". Lancet 363: 1965–1976.
MÜLLER, N. 1997. Role of the cytokine network in the CNS and psychiatric disorders. Der Nervenarzt 68:11.
NIELSEN, C.K., ARNT, J., SÁNCHEZ, C. 2000. Intracranial self-stimulation and sucrose intake differ as hedonic measures following chronic mild stress interstrain and interindividual differences. Behavioral Brain Research 107: 21–33.
O'CONNOR, J., C., ANDRÉ, C., WANG, Y., LAWSON, M.A., SZEGEDI, LESTAGE, S.S, J. 2009a. Interferon-gamma and tumor necrosis factor-alpha mediate the upregulation of indoleamine 2, 3-dioxygenase and the induction of depressive-like behavior in mice response to bacillus Calmette–Guérin. Journal of Neuroscience. 29: 4200–4209.
O'CONNOR, J.C, ANDRÉ, C., WANG, Y., LAWSON, M.A., SZEGEDI, S.S., LESTAGE, J., CASTANON N, KELLEY, K.W., DANTZER, R. 2009b. Lipopolysaccharide-induced depressive-like behavior is mediated by indoleamine 2, 3-dioxygenase activation in mice. Molecular Psychiatry 14: 511–522.
OXENKRUG, G. 2013. Serotonin-kynurenine hypothesis of depression: historical overview and recent developments. Current Drug Targets.14: 514–521.
PEARCE, B.D., KRUSZON-MORAN, D., . JONES, J.L. 2012. The relationship between Toxoplasma gondii infection and mood disorders in the third National Health and Nutrition Survey. Biological Psychiatry 72: 290–295
PEDERSEN, M.G., MORTENSEN, P.B., NORGAARD-PEDERSEN, B., POSTOLACHE, T.T. 2012. "Toxoplasma gondii infection and self-directed violence in mothers". Archive of General Psychiatry 69: 1123.
RUSSO, S., KEMA, I.P., FOKKEMA, M.R., BOON, J.C., WILLEMSE, P.H., DE, VRIES E.G., DEN BOER, J.A., KORF, J. 2003. Tryptophan as a link between psychopathology and somatic states. Psychosomatic Medicine 65: 665–671.
STREKALOVA, T., SPANAGEL, R., BARTSCH, D., HENN, F.A., GASS, P. 2002..Stress-induced anhedonia in mice is associated with deficits in forced swimming and exploration. Neuropsycho-pharmacology. 29:2007–2017.
SUZUKI, Y., KANG, H., PARMLEY, S., LIM, S., PARK, D. 2000. Induction of tumor necrosis factor-alpha and inducible nitric oxide synthase fails to prevent toxoplasmic encephalitis in the absence of interferon-gamma in genetically resistant BALB/c mice. Microbes and Infection 2: 455–462.
SUZUKI, Y., YANG, Q., REMINGTON, J.S. 1995.Genetic resistance against acute toxoplasmosis depends on the strain of T. gondii. Journal of Parasitology 81: 1032.
WICHERS, M.C., KOEK, G.H., ROBAEYS, G., VERKERK, R., SCHARPÉ, S., MAESM. 2005. IDO and interferon-alpha-induced depressive symptoms: a shift in hypothesis from tryptophan depletion to neurotoxicity. Molecular Psychiatry. 10: 538–544.
ZHANG, Y., TRÄSKMAN-BENDZ, L., JANELIDZE, S., LANGENBERG, P., SALEH, A., CONSTANTINE, N. 2012. Toxoplasma gondii immunoglobulin G antibodies and nonfatal suicidal self-directed violence. Journal of Clinical Psychiatry. 73:1069–1076. | ||||
|
Statistics Article View: 295 PDF Download: 385 |
||||
