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Abstract
The Apicomplexa protozoan Toxoplasma gondii is a mandatory intracellular parasite and the causative agent of toxoplasmosis. This illness is of medical importance due to its high prevalence worldwide and may cause neurological alterations in immunocompromised persons. In chronically infected immunocompetent individuals, this parasite forms tissue cysts mainly in the brain. In addition, T. gondii infection has been related to mental illnesses such as schizophrenia, bipolar disorder, depression, obsessive-compulsive disorder, as well as mood, personality, and other behavioral changes. In the present study, we evaluated the kinetics of behavioral alterations in a model of chronic infection, assessing anxiety, depression and exploratory behavior, and their relationship with neuroinflammation and parasite cysts in brain tissue areas, blood-brain-barrier (BBB) integrity, and cytokine status in the brain and serum. Adult female C57BL/6 mice were infected by gavage with 5 cysts of the ME-49 type II T. gondii strain, and analyzed as independent groups at 30, 60 and 90 days postinfection (dpi). Anxiety, depressive-like behavior, and hyperactivity were detected in the early (30 dpi) and long-term (60 and 90 dpi) chronic T. gondii infection, in a direct association with the presence of parasite cysts and neuroinflammation, independently of the brain tissue areas, and linked to BBB disruption. These behavioral alterations paralleled the upregulation of expression of tumor necrosis factor (TNF) and CC-chemokines (CCL2/MCP-1, CCL3/MIP-1α, CCL4/MIP-1β and CCL5/RANTES) in the brain tissue. In addition, increased levels of interferon-gamma (IFNγ), TNF and CCL2/MCP-1 were detected in the peripheral blood, at 30 and 60 dpi. Our data suggest that the persistence of parasite cysts induces sustained neuroinflammation, and BBB disruption, thus allowing leakage of cytokines of circulating plasma into the brain tissue. Therefore, all these factors may contribute to behavioral changes (anxiety, depressive-like behavior, and hyperactivity) in chronic T. gondii infection.
Highlights
The protozoan parasite Toxoplasma gondii is the etiologic agent of toxoplasmosis [1, 2]
The acute phase of T. gondii infection is characterized by presence of tachyzoite forms and the chronic phase is defined by the presence of encysted bradyzoite forms, called tissue cysts [7]
Female C57BL/6 mice were infected with 5 cysts of the ME-49 T. gondii strain
Summary
The protozoan parasite Toxoplasma gondii is the etiologic agent of toxoplasmosis [1, 2] This infection afflicts a third of the world population, with a seroprevalence ranging from 0.8 to 92%, depending on the region and habits of the populations [3, 4]. Among the reported behavioral changes are loss of predator fear [17, 18], decreased anxiety [10], increased exploratory behavior [19, 20] and impairment of long-term memory during chronic infection [21] All these findings contributed to the hypothesis of host manipulation by the parasite, contributing to exposition to definitive host predator and T. gondii cycle maintenance
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