Hostname: page-component-586b7cd67f-dlnhk Total loading time: 0 Render date: 2024-11-22T14:00:08.559Z Has data issue: false hasContentIssue false

Trypanosoma evansi infection impairs memory, increases anxiety behaviour and alters neurochemical parameters in rats

Published online by Cambridge University Press:  21 August 2013

PATRÍCIA WOLKMER*
Affiliation:
Department of Chemistry, Universidade Federal de Santa Maria, Brazil Department of Small Animals, Universidade Federal de Santa Maria, Brazil
FRANCINE C. PAIM
Affiliation:
Department of Small Animals, Universidade Federal de Santa Maria, Brazil
CÁSSIA B. DA SILVA
Affiliation:
Department of Small Animals, Universidade Federal de Santa Maria, Brazil
BIBIANA M. GAI
Affiliation:
Department of Chemistry, Universidade Federal de Santa Maria, Brazil
FABIANO B. CARVALHO
Affiliation:
Department of Chemistry, Universidade Federal de Santa Maria, Brazil
ANA CRISTINA G. DA SOUZA
Affiliation:
Department of Chemistry, Universidade Federal de Santa Maria, Brazil
MICHELLE M. DA ROSA
Affiliation:
Department of Chemistry, Universidade Federal de Santa Maria, Brazil
ALEKSANDRO S. DA SILVA
Affiliation:
Department of Microbiology and Parasitology, Universidade Federal de Santa Maria, Brazil
PAULA R. PEREIRA
Affiliation:
Department of Small Animals, Universidade Federal de Santa Maria, Brazil
SONIA T. A. LOPES
Affiliation:
Department of Small Animals, Universidade Federal de Santa Maria, Brazil
CRISTINA W. NOGUEIRA
Affiliation:
Department of Chemistry, Universidade Federal de Santa Maria, Brazil
MARIBEL A. RUBIN
Affiliation:
Department of Chemistry, Universidade Federal de Santa Maria, Brazil
SILVIA G. MONTEIRO
Affiliation:
Department of Microbiology and Parasitology, Universidade Federal de Santa Maria, Brazil
CINTHIA M. MAZZANTI
Affiliation:
Department of Chemistry, Universidade Federal de Santa Maria, Brazil Department of Small Animals, Universidade Federal de Santa Maria, Brazil
*
*Corresponding author: Departamento de Pequenos Animais da UFSM, Universidade Federal de Santa Maria, Av Roraima, Campus Universitário, 97105-900, Hospital Veterinário, Sala 103, Santa Maria – RS, Brasil. E-mail: [email protected]

Summary

The aim of this study was to investigate neurochemical and enzymatic changes in rats infected with Trypanosoma evansi, and their interference in the cognitive parameters. Behavioural assessment (assessment of cognitive performance), evaluation of cerebral L-[3H]glutamate uptake, acetylcholinesterase (AChE) activity and Ca+2 and Na+, K+-ATPase activity were evaluated at 5 and 30 days post infection (dpi). This study demonstrates a cognitive impairment in rats infected with T. evansi. At 5 dpi memory deficit was demonstrated by an inhibitory avoidance test. With the chronicity of the disease (30 dpi) animals showed anxiety symptoms. It is possible the inhibition of cerebral Na+, K+-ATPase activity, AChE and synaptosomal glutamate uptake are involved in cognitive impairment in infected rats by T. evansi. The understanding of cerebral host–parasite relationship may shed some light on the cryptic symptoms of animals and possibly human infection where patients often present with other central nervous system (CNS) disorders.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2013 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Abril, C., Engels, M., Liman, A., Hilbe, M., Albini, S., Franchini, M., Suter, M. and Ackermann, M. (2004). Both viral and host factors contribute to neurovirulence of bovine herpesviruses 1 and 5 in interferon receptor-deficient mice. Journal of Virology 78, 36443653.CrossRefGoogle ScholarPubMed
Agresti, C., Meomartini, M. E., Amadio, S., Ambrosini, E., Volonte, C., Aloisi, F. and Visentin, S. (2005). ATP regulates oligodendrocyte progenitor migration, proliferation, and differentiation: involvement of metabotropic P2 receptors. Brain Research. Brain Research Reviews 48, 157165.CrossRefGoogle ScholarPubMed
Al-Qarawi, A. A., Abdel-Rahman, H. and Elmougy, S. A. (2001). Impairment in the pituitary-thyroid axis of the Camelus dromedarius infected with Trypanosoma evansi. Deutsche Tierarztliche Wochenschrift 108, 172174.Google ScholarPubMed
Beal, M. F. (1992 a). Mechanisms of excitotoxicity in neurologic diseases. FASEB Journal 6, 33383344.CrossRefGoogle ScholarPubMed
Beal, M. F. (1992 b). Role of excitotoxicity in human neurological disease. Current Opinion in Neurobiology 2, 657662.CrossRefGoogle ScholarPubMed
Berlin, D., Loeb, E. and Baneth, G. (2009). Disseminated central nervous system disease caused by Trypanosoma evansi in a horse. Veterinary Parasitology 161, 316319.CrossRefGoogle ScholarPubMed
Boldyrev, A., Bulygina, E., Carpenter, D. and Schoner, W. (2003). Glutamate receptors communicate with Na+/K+-ATPase in rat cerebellum granule cells: demonstration of differences in the action of several metabotropic and ionotropic glutamate agonists on intracellular reactive oxygen species and the sodium pump. Journal of Molecular Neuroscience 21, 213222.CrossRefGoogle ScholarPubMed
Boldyrev, A., Bulygina, E., Gerassimova, O., Lyapina, L. and Schoner, W. (2004). Functional relationship between Na/K-ATPase and NMDA-receptors in rat cerebellum granule cells. Biochemistry. Biokhimiia 69, 429434.CrossRefGoogle ScholarPubMed
Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248254.CrossRefGoogle ScholarPubMed
Brun, R., Hecker, H. and Lun, Z. R. (1998). Trypanosoma evansi and T. equiperdum: distribution, biology, treatment and phylogenetic relationship (a review). Veterinary Parasitology 79, 95107.CrossRefGoogle Scholar
Brunelli, M., Garcia-Gil, M., Mozzachiodi, R., Scuri, R. and Zaccardi, M. L. (1997). Neurobiological principles of learning and memory. Archives Italiennes de Biologie 135, 1536.Google ScholarPubMed
Cahill, L., Brioni, J. and Izquierdo, I. (1986). Retrograde memory enhancement by diazepam: its relation to anterograde amnesia, and some clinical implications. Psychopharmacology (Berlin) 90, 554556.CrossRefGoogle ScholarPubMed
Carvalho, F. B., Mello, C. F., Marisco, P. C., Tonello, R., Girardi, B. A., Ferreira, J., Oliveira, M. S. and Rubin, M. A. (2012). Spermidine decreases Na(+),K(+)-ATPase activity through NMDA receptor and protein kinase G activation in the hippocampus of rats. European Journal of Pharmacology 684, 7986.CrossRefGoogle Scholar
Choi, D. W. (1988). Glutamate neurotoxicity and diseases of the nervous system. Neuron 1, 623634.CrossRefGoogle ScholarPubMed
Collingridge, G. L. and Lester, R. A. (1989). Excitatory amino acid receptors in the vertebrate central nervous system. Pharmacological Reviews 41, 143210.Google ScholarPubMed
Danbolt, N. C. (2001). Glutamate uptake. Progress in Neurobiology 65, 1105.CrossRefGoogle ScholarPubMed
Dargie, J. D., Murray, P. K., Murray, M., Grimshaw, W. R. and Mcintyre, W. I. (1979). Bovine trypanosomiasis: the red cell kinetics of ndama and Zebu cattle infected with Trypanosoma congolense. Parasitology 78, 271286.CrossRefGoogle ScholarPubMed
Das, A., Dikshit, M. and Nath, C. (2005 a). Role of molecular isoforms of acetylcholinesterase in learning and memory functions. Pharmacology, Biochemistry, and Behavior 81, 8999.CrossRefGoogle ScholarPubMed
Das, A., Rai, D., Dikshit, M., Palit, G. and Nath, C. (2005 b). Nature of stress: differential effects on brain acetylcholinesterase activity and memory in rats. Life Science 77, 22992311.CrossRefGoogle ScholarPubMed
Da Silva, A. S., Costa, M. M., Wolkmer, P., Zanette, R. A., Faccio, L., Gressler, L. T., Dorneles, T. E., Santurio, J. M., Lopes, S. T. and Monteiro, S. G. (2009 a). Trypanosoma evansi: hematologic changes in experimentally infected cats. Experimental Parasitology 123, 3134.CrossRefGoogle ScholarPubMed
Da Silva, A. S., Hoehne, L., Tonin, A. A., Zanette, R. A., Wolkmer, P., Costa, M. M., Moraes, D. P., Flores, E. M., Santurio, J. M., Lopes, S. T. and Monteiro, S. G. (2009 b). Trypanosoma evansi: levels of copper, iron and zinc in the bloodstream of infected cats. Experimental Parasitology 123, 3538.CrossRefGoogle ScholarPubMed
Da Silva, A. S., Wolkmer, P., Machado Costa, M., Paim, F., Belmonte Oliveira, C., Adriel Zanette, R., Morais Santurio, J., Dos Anjos Lopes, S. T. and Gonzalez Monteiro, S. (2009 c). Lipid peroxidation in cats experimentally infected with Trypanosoma evansi. Parasitology Research 106, 157161.CrossRefGoogle ScholarPubMed
Da Silva, A. S., Pierezan, F., Wolkmer, P., Costa, M. M., Oliveiro, C. B., Tonin, A. A., Santurio, J. M., Lopes, S. T. and Monteiro, S. G. (2010 a). Pathological findings associated with experimental infection by Trypanosoma evansi in cats. Journal of Comparative Pathology 142, 170176.CrossRefGoogle ScholarPubMed
Da Silva, A. S., Spanevello, R., Stefanello, N., Wolkmer, P., Costa, M. M., Zanette, R. A., Lopes, S. T., Santurio, J. M., Schetinger, M. R. and Monteiro, S. G. (2010 b). Influence of Trypanosoma evansi in blood, plasma, and brain cholinesterase of experimentally infected cats. Research in Veterinary Science 88, 281284.CrossRefGoogle ScholarPubMed
Da Silva, A. S., Belle, L. P., Bitencourt, P. E., Perez, H. A., Thome, G. R., Costa, M. M., Oliveira, C. B., Teixeira, M. M., Moretto, M. B., Mazzanti, C. M., Lopes, S. T. and Monteiro, S. G. (2011 a). Trypanosoma evansi: adenosine deaminase activity in the brain of infected rats. Experimental Parasitology 127, 173177.CrossRefGoogle ScholarPubMed
Da Silva, A. S., Monteiro, S. G., Goncalves, J. F., Spanevello, R., Oliveira, C. B., Costa, M. M., Jaques, J. A., Morsch, V. M., Schetinger, M. R., Mazzanti, C. M. and Lopes, S. T. (2011 b). Acetylcholinesterase activity and lipid peroxidation in the brain and spinal cord of rats infected with Trypanosoma evansi. Veterinary Parasitology 175, 237244.CrossRefGoogle ScholarPubMed
Da Silva, A. S., Pimentel, V. C., Jaques, J. A., Wolkmer, P., Tavares, K. C., Lazzarotto, C. R., Miletti, L. C., Schetinger, M. R., Mazzanti, C. M., Lopes, S. T. and Monteiro, S. G. (2011 c). Biochemical detection of adenosine deaminase in Trypanosoma evansi. Experimental Parasitology 128, 298300.CrossRefGoogle ScholarPubMed
Da Silva, A. S., Oliveira, C. B., Bertoncheli, C. M., Santos, R. P., Beckmann, D. V., Wolkmer, P., Gressler, L. T., Tonin, A. A., Graca, D. L., Mazzanti, A., Lopes, S. T. and Monteiro, S. G. (2012 a). Clinical signs and histopathology of brain, spinal cord and muscle of the pelvic limb of rats experimentally infected with Trypanosoma evansi. Pathology, Research and Practice 208, 3944.CrossRefGoogle ScholarPubMed
Da Silva, A. S., Oliveira, C. B., Rosa, L. D., Leal, C. A., Da Cruz, R. C., Thome, G. R., Athayde, M. L., Schetinger, M. R., Monteiro, S. G. and Lopes, S. T. (2012 b). Influence of Trypanosoma evansi in adenine nucleotides and nucleoside concentration in serum and cerebral cortex of infected rats. Experimental Parasitology 131, 8084.CrossRefGoogle ScholarPubMed
Dos Reis, E. A., De Oliveira, L. S., Lamers, M. L., Netto, C. A. and Wyse, A. T. (2002). Arginine administration inhibits hippocampal Na(+),K(+)-ATPase activity and impairs retention of an inhibitory avoidance task in rats. Brain Research 951, 151157.CrossRefGoogle Scholar
Edwards, F. A., Gibb, A. J. and Colquhoun, D. (1992). ATP receptor-mediated synaptic currents in the central nervous system. Nature 359, 144147.CrossRefGoogle ScholarPubMed
Ellman, G. L., Courtney, K. D., Andres, V. Jr. and Feather-Stone, R. M. (1961). A new and rapid colorimetric determination of acetylcholinesterase activity. Biochemical Pharmacology 7, 8895.CrossRefGoogle ScholarPubMed
Erecinska, M. and Silver, I. A. (1994). Ions and energy in mammalian brain. Progress in Neurobiology 43, 3771.CrossRefGoogle ScholarPubMed
Fiske, C. H. and Subbarow, Y. (1927). The nature of the “inorganic phosphate” in voluntary muscle. Science 65, 401403.CrossRefGoogle Scholar
Fonnum, F. (1984). Glutamate: a neurotransmitter in mammalian brain. Journal of Neurochemistry 42, 111.CrossRefGoogle ScholarPubMed
Franca, R. T., Da Silva, A. S., Wolkmer, P., Oliveira, V. A., Pereira, M. E., Leal, M. L., Silva, C. B., Nunes, M. A., Dressler, V. L., Mazzanti, C. M., Monteiro, S. G. and Lopes, S. T. (2011). Delta-aminolevulinate dehydratase activity in red blood cells of rats infected with Trypanosoma evansi. Parasitology 138, 12721277.CrossRefGoogle ScholarPubMed
Frevert, U., Movila, A., Nikolskaia, O. V., Raper, J., Mackey, Z. B., Abdulla, M., McKerrow, J. and Grab, D. J. (2012). Early invasion of brain parenchyma by African trypanosomes. PLoS ONE 7, e43913.CrossRefGoogle ScholarPubMed
Frussa-Filho, R., Barbosa-Junior, H., Silva, R. H., Da Cunha, C. and Mello, C. F. (1999). Naltrexone potentiates the anxiolytic effects of chlordiazepoxide in rats exposed to novel environments. Psychopharmacology (Berlin) 147, 168173.CrossRefGoogle ScholarPubMed
Gandhi, C. R. and Ross, D. H. (1988). Characterization of a high-affinity Mg2+-independent Ca2+-ATPase from rat brain synaptosomal membranes. Journal of Neurochemistry 50, 248256.CrossRefGoogle ScholarPubMed
Genn, R. F., Tucci, S. A., Thomas, A., Edwards, J. E. and File, S. E. (2003). Age-associated sex differences in response to food deprivation in two animal tests of anxiety. Neuroscience and Biobehavioral Reviews 27, 155161.CrossRefGoogle ScholarPubMed
Glushchenko, T. S. and Izvarina, N. L. (1997). Na+,K(+)-ATPase activity in neurons and glial cells of the olfactory cortex of the rat brain during the development of long-term potentiation. Neuroscience and Behavioral Physiology 27, 4952.CrossRefGoogle ScholarPubMed
Greenamyre, J. T. and Porter, R. H. (1994). Anatomy and physiology of glutamate in the CNS. Neurology 44, S713.Google ScholarPubMed
Guerra, G. P., Mello, C. F., Sauzem, P. D., Berlese, D. B., Furian, A. F., Tabarelli, Z. and Rubin, M. A. (2006). Nitric oxide is involved in the memory facilitation induced by spermidine in rats. Psychopharmacology (Berlin) 186, 150158.CrossRefGoogle ScholarPubMed
Gutierrez, C., Corbera, J. A., Juste, M. C., Doreste, F. and Morales, I. (2006). Clinical, hematological, and biochemical findings in an outbreak of abortion and neonatal mortality associated with Trypanosoma evansi infection in dromedary camels. Annals of the New York Academy of Sciences 1081, 325327.CrossRefGoogle Scholar
Habila, N., Inuwa, M. H., Aimola, I. A., Udeh, M. U. and Haruna, E. (2012). Pathogenic mechanisms of Trypanosoma evansi infections. Research in Veterinary Science 93, 1317.CrossRefGoogle ScholarPubMed
Hanahisa, Y. and Yamaguchi, M. (1998). Increase of Ca2+-ATPase activity in the brain microsomes of rats with increasing ages: involvement of protein kinase C. Brain Research Bulletin 46, 329332.CrossRefGoogle ScholarPubMed
Hartmann, H., Eckert, A. and Muller, W. E. (1994). Disturbances of the neuronal calcium homeostasis in the aging nervous system. Life Science 55, 20112018.CrossRefGoogle ScholarPubMed
Headley, P. M. and Grillner, S. (1990). Excitatory amino acids and synaptic transmission: the evidence for a physiological function. Trends in Pharmacological Sciences 11, 205211.CrossRefGoogle ScholarPubMed
Herrera, H. M., Davila, A. M., Norek, A., Abreu, U. G., Souza, S. S., D'andrea, P. S. and Jansen, A. M. (2004). Enzootiology of Trypanosoma evansi in Pantanal, Brazil. Veterinary Parasitology 125, 263275.CrossRefGoogle Scholar
Joshi, P. P., Shegokar, V. R., Powar, R. M., Herder, S., Katti, R., Salkar, H. R., Dani, V. S., Bhargava, A., Jannin, J. and Truc, P. (2005). Human trypanosomiasis caused by Trypanosoma evansi in India: the first case report. American Journal of Tropical Medicine and Hygiene 73, 491495.CrossRefGoogle ScholarPubMed
Kraus-Friedmann, N. (1990). Calcium sequestration in the liver. Cell Calcium 11, 625640.CrossRefGoogle ScholarPubMed
Lalonde, R., Kim, H. D. and Fukuchi, K. (2004). Exploratory activity, anxiety, and motor coordination in bigenic APPswe + PS1/DeltaE9 mice. Neuroscience Letters 369, 156161.CrossRefGoogle ScholarPubMed
Lapiz-Bluhm, M. D., Bondi, C. O., Doyen, J., Rodriguez, G. A., Bedard-Arana, T. and Morilak, D. A. (2008). Behavioural assays to model cognitive and affective dimensions of depression and anxiety in rats. Journal of Neuroendocrinology 20, 11151137.CrossRefGoogle ScholarPubMed
Lotti, M. (1995). Cholinesterase inhibition: complexities in interpretation. Clinical Chemistry 41, 18141818.CrossRefGoogle ScholarPubMed
Magnoni, M. S., Govoni, S., Battaini, F. and Trabucchi, M. (1991). The aging brain: protein phosphorylation as a target of changes in neuronal function. Life Science 48, 373385.CrossRefGoogle ScholarPubMed
Moseley, A. E., Williams, M. T., Schaefer, T. L., Bohanan, C. S., Neumann, J. C., Behbehani, M. M., Vorhees, C. V. and Lingrel, J. B. (2007). Deficiency in Na,K-ATPase alpha isoform genes alters spatial learning, motor activity, and anxiety in mice. Journal of Neuroscience 27, 616626.CrossRefGoogle Scholar
Oliveira, C. B., Spanevello, R., Da Silva, A. S., Souza, V. C., Pimentel, V. C., Thome, G. R., Schetinger, M. R., Lopes, S. T., Leal, D. B. and Monteiro, S. G. (2011). Trypanosoma evansi: activities of adenine nucleotide degradation enzymes in cerebral cortex of infected rats. Experimental Parasitology 128, 225229.CrossRefGoogle ScholarPubMed
Paim, F. C., Da Silva, A. S., Wolkmer, P., Costa, M. M., Da Silva, C. B., Paim, C. B., Oliveira, M. S., Silva, L. F., Mello, C. F., Monteiro, S. G., Mazzanti, C. M. and Lopes, S. T. (2011 a). Trypanosoma evansi: concentration of 3-nitrotyrosine in the brain of infected rats. Experimental Parasitology 129, 2730.CrossRefGoogle ScholarPubMed
Paim, F. C., Duarte, M. M., Costa, M. M., Da Silva, A. S., Wolkmer, P., Silva, C. B., Paim, C. B., Franca, R. T., Mazzanti, C. M., Monteiro, S. G., Krause, A. and Lopes, S. T. (2011 b). Cytokines in rats experimentally infected with Trypanosoma evansi. Experimental Parasitology 128, 365370.CrossRefGoogle ScholarPubMed
Prast, H. and Philippu, A. (2001). Nitric oxide as modulator of neuronal function. Progress in Neurobiology 64, 5168.CrossRefGoogle ScholarPubMed
Rakonczay, Z. (2003). Potencies and selectivities of inhibitors of acetylcholinesterase and its molecular forms in normal and Alzheimer's disease brain. Acta biologica Hungarica 54, 183189.CrossRefGoogle ScholarPubMed
Rodrigues, A., Fighera, R. A., Souza, T. M., Schild, A. L. and Barros, C. S. (2009). Neuropathology of naturally occurring Trypanosoma evansi infection of horses. Veterinary Pathology 46, 251258.CrossRefGoogle ScholarPubMed
Rohn, T. T., Hinds, T. R. and Vincenzi, F. F. (1993). Ion transport ATPases as targets for free radical damage. Protection by an aminosteroid of the Ca2+ pump ATPase and Na+/K+ pump ATPase of human red blood cell membranes. Biochemical Pharmacology 46, 525534.CrossRefGoogle ScholarPubMed
Rothman, S. M. and Olney, J. W. (1995). Excitotoxicity and the NMDA receptor – still lethal after eight years. Trends in Neurosciences 18, 5758.Google ScholarPubMed
Rubin, M. A., Berlese, D. B., Stiegemeier, J. A., Volkweis, M. A., Oliveira, D. M., Dos Santos, T. L., Fenili, A. C. and Mello, C. F. (2004). Intra-amygdala administration of polyamines modulates fear conditioning in rats. Journal of Neuroscience 24, 23282334.CrossRefGoogle ScholarPubMed
Sattler, R., Xiong, Z., Lu, W. Y., Hafner, M., Macdonald, J. F. and Tymianski, M. (1999). Specific coupling of NMDA receptor activation to nitric oxide neurotoxicity by PSD-95 protein. Science 284, 18451848.CrossRefGoogle ScholarPubMed
Schweigert, I. D., De Oliveira, D. L., Scheibel, F., Da Costa, F., Wofchuk, S. T., Souza, D. O. and Perry, M. L. (2005). Gestational and postnatal malnutrition affects sensitivity of young rats to picrotoxin and quinolinic acid and uptake of GABA by cortical and hippocampal slices. Brain Research. Developmental Brain Research 154, 177185.CrossRefGoogle ScholarPubMed
Scuri, R., Lombardo, P., Cataldo, E., Ristori, C. and Brunelli, M. (2007). Inhibition of Na+/K+ ATPase potentiates synaptic transmission in tactile sensory neurons of the leech. European Journal of Neuroscience 25, 159167.CrossRefGoogle ScholarPubMed
Silman, I. and Sussman, J. L. (2005). Acetylcholinesterase: ‘classical’ and ‘non-classical’ functions and pharmacology. Current Opinion in Pharmacology 5, 293302.CrossRefGoogle ScholarPubMed
Smith, S. J., MacDermott, A. B. and Weight, F. F. (1983). Detection of intracellular Ca2+ transients in sympathetic neurones using arsenazo III. Nature 304, 350352.CrossRefGoogle ScholarPubMed
Soreq, H. and Seidman, S. (2001). Acetylcholinesterase – new roles for an old actor. Nature Reviews. Neuroscience 2, 294302.CrossRefGoogle ScholarPubMed
Trevisan, G., Maldaner, G., Velloso, N. A., Sant'anna Gda, S., Ilha, V., Velho Gewehr Cde, C., Rubin, M. A., Morel, A. F. and Ferreira, J. (2009). Antinociceptive effects of 14-membered cyclopeptide alkaloids. Journal of Natural Products 72, 608612.CrossRefGoogle ScholarPubMed
Tuntasuvan, D., Sarataphan, N. and Nishikawa, H. (1997). Cerebral trypanosomiasis in native cattle. Veterinary Parasitology 73, 357363.CrossRefGoogle ScholarPubMed
Tuntasuvan, D., Mimapan, S., Sarataphan, N., Trongwongsa, L., Intraraksa, R. and Luckins, A. G. (2000). Detection of Trypanosoma evansi in brains of the naturally infected hog deer by streptavidine-biotin immunohistochemistry. Veterinary Parasitology 87, 223230.CrossRefGoogle ScholarPubMed
Wolkmer, P., Da Silva, A. S., Cargnelutti, J. F., Costa, M. M., Traesel, C. K., Lopes, S. T. D. A. and Monteiro, S. G. (2007). Erithropoietic response in Trypanosoma evansi infected rats with different parasitaemia intensity. Ciencia Rural 37, 16821687.CrossRefGoogle Scholar
Wolkmer, P., Da Silva, A. S., Traesel, C. K., Paim, F. C., Cargnelutti, J. F., Pagnoncelli, M., Picada, M. E., Monteiro, S. G. and Lopes, S. T. (2009). Lipid peroxidation associated with anemia in rats experimentally infected with Trypanosoma evansi. Veterinary Parasitology 165, 4146.CrossRefGoogle ScholarPubMed
Wolkmer, P., Lopes, S. T., Franciscato, C., Da Silva, A. S., Traesel, C. K., Siqueira, L. C., Pereira, M. E., Monteiro, S. G. and Mazzanti, C. M. (2010). Trypanosoma evansi: cholinesterase activity in acutely infected Wistar rats. Experimental Parasitology 125, 251255.CrossRefGoogle ScholarPubMed
Wolkmer, P., Da Silva, C. B., Paim, F. C., Da Silva, A. S., Tavares, K. C., Lazzarotto, C. R., Palma, H. E., Thome, G. R., Miletti, L. C., Schetinger, M. R., Lopes, S. T. and Mazzanti, C. M. (2012). Biochemistry detection of acetylcholinesterase activity in Trypanosoma evansi and possible functional correlations. Experimental Parasitology 132, 546549.CrossRefGoogle ScholarPubMed
Wolkmer, P., Da Silva, C. B., Paim, F. C., Duarte, M. M., Castro, V., Palma, H. E., Franca, R. T., Felin, D. V., Siqueira, L. C., Lopes, S. T., Schetinger, M. R., Monteiro, S. G. and Mazzanti, C. M. (2013). Pre-treatment with curcumin modulates acetylcholinesterase activity and proinflammatory cytokines in rats infected with Trypanosoma evansi. Parasitology International 62, 144149.CrossRefGoogle ScholarPubMed
Wyse, A. T., Streck, E. L., Barros, S. V., Brusque, A. M., Zugno, A. I. and Wajner, M. (2000). Methylmalonate administration decreases Na+,K+-ATPase activity in cerebral cortex of rats. Neuroreport 11, 23312334.CrossRefGoogle ScholarPubMed
Wyse, A. T., Bavaresco, C. S., Reis, E. A., Zugno, A. I., Tagliari, B., Calcagnotto, T. and Netto, C. A. (2004). Training in inhibitory avoidance causes a reduction of Na+,K+-ATPase activity in rat hippocampus. Physiology and Behavior 80, 475479.CrossRefGoogle ScholarPubMed