Neurological impairment caused by Schistosoma mansoni systemic infection exhibits early features of idiopathic neurodegenerative disease

Article


Gasparotto, Juciano, Senger, Mario Roberto, de Sa Moreira, Emilio Telles, Brum, Pedro Ozorio, Kessler, Flavio Gabriel Carazza, Peixoto, Daniel Oppermann, Panzenhagen, Alana Castro, Ong, Lin Kooi, Soares, Marlene Campos, Reis, Patricia Alves, Schirato, Giuliana Viegas, Valente, Walter Cesar Goes, Montoya, Bogar Omar Araujo, Silva, Floriano P., Moreira, Jose Claudio Fonseca, Dal-Pizzol, Felipe, Castro-Faria-Neto, Hugo C. and Gelain, Daniel Pens. 2021. "Neurological impairment caused by Schistosoma mansoni systemic infection exhibits early features of idiopathic neurodegenerative disease." Journal of Biological Chemistry. 297 (2), pp. 1-17. https://doi.org/10.1016/j.jbc.2021.100979
Article Title

Neurological impairment caused by Schistosoma mansoni systemic infection exhibits early features of idiopathic neurodegenerative disease

ERA Journal ID2230
Article CategoryArticle
AuthorsGasparotto, Juciano (Author), Senger, Mario Roberto (Author), de Sa Moreira, Emilio Telles (Author), Brum, Pedro Ozorio (Author), Kessler, Flavio Gabriel Carazza (Author), Peixoto, Daniel Oppermann (Author), Panzenhagen, Alana Castro (Author), Ong, Lin Kooi (Author), Soares, Marlene Campos (Author), Reis, Patricia Alves (Author), Schirato, Giuliana Viegas (Author), Valente, Walter Cesar Goes (Author), Montoya, Bogar Omar Araujo (Author), Silva, Floriano P. (Author), Moreira, Jose Claudio Fonseca (Author), Dal-Pizzol, Felipe (Author), Castro-Faria-Neto, Hugo C. (Author) and Gelain, Daniel Pens (Author)
Journal TitleJournal of Biological Chemistry
Journal Citation297 (2), pp. 1-17
Article Number100979
Number of Pages17
Year2021
Place of PublicationUnited States
ISSN0021-9258
1083-351X
Digital Object Identifier (DOI)https://doi.org/10.1016/j.jbc.2021.100979
Web Address (URL)https://www.sciencedirect.com/science/article/pii/S002192582100781X
Abstract

Schistosomiasis, a neglected tropical disease caused by trematodes of the Schistosoma genus, affects over 250 million people around the world. This disease has been associated with learning and memory deficits in children, whereas reduced attention levels, impaired work capacity, and cognitive deficits have been observed in adults. Strongly correlated with poverty and lack of basic sanitary conditions, this chronic endemic infection is common in Africa, South America, and parts of Asia and contributes to inhibition of social development and low quality of life in affected areas. Nonetheless, studies on the mechanisms involved in the neurological impairment caused by schistosomiasis are scarce. Here, we used a murine model of infection with Schistosoma mansoni in which parasites do not invade the central nervous system to evaluate the consequences of systemic infection on neurologic function. We observed that systemic infection with S. mansoni led to astrocyte and microglia activation, expression of oxidative stress-induced transcription factor Nrf2, oxidative damage, Tau phosphorylation, and amyloid-β peptide accumulation in the prefrontal cortex of infected animals. We also found impairment in spatial learning and memory as evaluated by the Morris water maze task. Administration of anthelmintic (praziquantel) and antioxidant (N-acetylcysteine plus deferoxamine) treatments was effective in inhibiting most of these phenotypes, and the combination of both treatments had a synergistic effect to prevent such changes. These data demonstrate new perspectives toward the understanding of the pathology and possible therapeutic approaches to counteract long-term effects of systemic schistosomiasis on brain function.

KeywordsAmyloid-beta peptides; Central nervous systems; Learning and memory; Neglected tropical disease; Neurologic function; Schistosoma mansoni; Social development; Synergistic effect
ANZSRC Field of Research 2020320499. Immunology not elsewhere classified
321405. Pharmaceutical sciences
320902. Cellular nervous system
Institution of OriginUniversity of Southern Queensland
Byline AffiliationsFederal University of Rio Grande do Sul, Brazil
Oswaldo Cruz Foundation (Fiocruz), Brazil
Monash University
University of the Extreme South of Santa Catarina, Brazil
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Tyrosine Hydroxylase Phosphorylation in Catecholaminergic Brain Regions: A Marker of Activation following Acute Hypotension and Glucoprivation
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The Sustained Phase of Tyrosine Hydroxylase Activation In vivo
Ong, Lin Kooi, Sominsky, Luba, Dickson, Phillip W., Hodgson, Deborah M. and Dunkley, Peter R.. 2012. "The Sustained Phase of Tyrosine Hydroxylase Activation In vivo." Neurochemical Research. 37 (9), pp. 1938-1943. https://doi.org/10.1007/s11064-012-0812-3
Increased microglial activation in the rat brain following neonatal exposure to a bacterial mimetic
Sominsky, L., Walker, A. K., Ong, L. K., Tynan, R. J., Walker, F. R. and Hodgson, D. M.. 2012. "Increased microglial activation in the rat brain following neonatal exposure to a bacterial mimetic." Behavioural Brain Research. 226 (1), pp. 351-356. https://doi.org/10.1016/j.bbr.2011.08.038
The effects of footshock and immobilization stress on tyrosine hydroxylase phosphorylation in the rat locus coeruleus and adrenal gland
Ong, L. K., Guan, L., Stutz, B., Dickson, P. W., Dunkley, P. R. and Bobrovskaya, L.. 2011. "The effects of footshock and immobilization stress on tyrosine hydroxylase phosphorylation in the rat locus coeruleus and adrenal gland." Neuroscience. 192, pp. 20-27. https://doi.org/10.1016/j.neuroscience.2011.06.087
Epigenetic Inheritance of Anxiety-Like Behaviour in Rats - Role of Early Life Exposure to a Bacterial Mimetic
Sominsky, L., Walker, A. K., Ong, L., Tynan, R. J., Walker, F. R. and Hodgson, D. M.. 2011. "Epigenetic Inheritance of Anxiety-Like Behaviour in Rats - Role of Early Life Exposure to a Bacterial Mimetic." Journal of Developmental Origins of Health and Disease. 2, pp. S109-S109.
Neonatal respiratory infection and adult re-infection: Effect on glucocorticoid and mineralocorticoid receptors in the hippocampus in BALB/c mice
Wynne, O., Horvat, J. C., Kim, R. Y., Ong, L. K., Smith, R., Hansbro, P. M., Clifton, V. L. and Hodgson, D. M.. 2011. "Neonatal respiratory infection and adult re-infection: Effect on glucocorticoid and mineralocorticoid receptors in the hippocampus in BALB/c mice." Brain, Behavior, and Immunity. 25 (6), pp. 1214-1222. https://doi.org/10.1016/j.bbi.2011.03.014
Sustained Phosphorylation of Tyrosine Hydroxylase at Serine 40 in VIVO
Ong, L. K., Sominsky, L., Walker, A. K., Hodgson, D. M., Goodchild, A. K., Bobrovskaya, L., Dickson, P. W. and Dunkley, P. R.. 2011. "Sustained Phosphorylation of Tyrosine Hydroxylase at Serine 40 in VIVO." 23rd Biennial Meeting of the International Society for Neurochemistry (2011). Athen, Greece 28 Aug - 01 Sep 2011 United Kingdom.
The Effect of Social Defeat on Tyrosine Hydroxylase Phosphorylation in the Rat Brain and Adrenal Gland
Ong, Lin Kooi, Bobrovskaya, Larisa, Walker, Frederick R., Day, Trevor A., Dickson, Phillip W. and Dunkley, Peter R.. 2011. "The Effect of Social Defeat on Tyrosine Hydroxylase Phosphorylation in the Rat Brain and Adrenal Gland." Neurochemical Research. 36 (1), pp. 27-33. https://doi.org/10.1007/s11064-010-0255-7
Tyrosine hydroxylase phosphorylation in response to footshock and restraint stress
Ong, L., Guan, L., Stutz, B., Dickson, P., Dunkley, P. and Bobrovskaya, L.. 2010. "Tyrosine hydroxylase phosphorylation in response to footshock and restraint stress." Journal of Neurochemistry. 115, pp. 77-77.
Signal transduction pathways and tyrosine hydroxylase regulation in the adrenal medulla following glucoprivation: An in vivo analysis
Bobrovskaya, Larisa, Damanhuri, Hanafi A., Ong, Lin Kooi, Schneider, Jennifer J., Dickson, Phillip W., Dunkley, Peter R. and Goodchild, Ann K.. 2010. "Signal transduction pathways and tyrosine hydroxylase regulation in the adrenal medulla following glucoprivation: An in vivo analysis." Neurochemistry International: the journal for the publication of cellular and molecular aspects of neurochemistry. 57 (2), pp. 162-167. https://doi.org/10.1016/j.neuint.2010.05.009
The effect of social conflict on tyrosine hydroxylase phosphorylation in catecholamine-producing cells from sprague-dawley rats
Ong, L., Bobrovskaya, L., Walker, F., Day, Trevor, Dickson, P. and Dunkley, P.. 2009. "The effect of social conflict on tyrosine hydroxylase phosphorylation in catecholamine-producing cells from sprague-dawley rats." 22nd Biennial Meeting of the International Society for Neurochemistry & Asian Pacific Society for Neurochemistry (2009). South Korea 23 - 29 Aug 2009 United Kingdom.
Cross-neutralisation of Australian brown and tiger snake venoms with commercial antivenoms: Cross-reactivity or antivenom mixtures?
O’Leary, Margaret A., Schneider, Jennifer J., Prakash Krishnan, Brian, Lavis, Christopher, McKendry, Amy, Ong, Lin Kooi and Isbister, Geoffrey K.. 2007. "Cross-neutralisation of Australian brown and tiger snake venoms with commercial antivenoms: Cross-reactivity or antivenom mixtures?" Toxicon. 50 (2), pp. 206-213. https://doi.org/10.1016/j.toxicon.2007.03.014