Hostname: page-component-cd9895bd7-fscjk Total loading time: 0 Render date: 2024-12-24T03:10:16.621Z Has data issue: false hasContentIssue false

Nerolidol-loaded nanospheres prevent hepatic oxidative stress of mice infected by Trypanosoma evansi

Published online by Cambridge University Press:  17 October 2016

MATHEUS D. BALDISSERA*
Affiliation:
Department of Microbiology and Parasitology, Universidade Federal de Santa Maria (UFSM), Santa Maria, RS, Brazil
CARINE F. SOUZA
Affiliation:
Department of Microbiology and Parasitology, Universidade Federal de Santa Maria (UFSM), Santa Maria, RS, Brazil
THIRSSA H. GRANDO
Affiliation:
Department of Microbiology and Parasitology, Universidade Federal de Santa Maria (UFSM), Santa Maria, RS, Brazil
GEISA S. DOLCI
Affiliation:
Department of Physiology and Pharmacology, Universidade Federal de Santa Maria (UFSM), Santa Maria, RS, Brazil
LUCIANA F. COSSETIN
Affiliation:
Department of Microbiology and Parasitology, Universidade Federal de Santa Maria (UFSM), Santa Maria, RS, Brazil
KAREN L. S. MOREIRA
Affiliation:
Department of Morphology, Universidade Federal de Santa Maria (UFSM), Santa Maria, RS, Brazil
MARCELO L. DA VEIGA
Affiliation:
Department of Morphology, Universidade Federal de Santa Maria (UFSM), Santa Maria, RS, Brazil
MARIA IZABEL U. M. DA ROCHA
Affiliation:
Department of Morphology, Universidade Federal de Santa Maria (UFSM), Santa Maria, RS, Brazil
ALINE A. BOLIGON
Affiliation:
Laboratory of Phytochemistry, Universidade Federal de Santa Maria (UFSM), Santa Maria, RS, Brazil
MARLI M. A. DE CAMPOS
Affiliation:
Laboratory of Phytochemistry, Universidade Federal de Santa Maria (UFSM), Santa Maria, RS, Brazil
LENITA M. STEFANI
Affiliation:
Department of Animal Science, Universidade do Estado de Santa Catarina (UDESC), Chapecó, SC, Brazil
ALEKSANDRO S. DA SILVA
Affiliation:
Department of Animal Science, Universidade do Estado de Santa Catarina (UDESC), Chapecó, SC, Brazil
SILVIA G. MONTEIRO*
Affiliation:
Department of Microbiology and Parasitology, Universidade Federal de Santa Maria (UFSM), Santa Maria, RS, Brazil
*
*Corresponding author: Department of Microbiology and Parasitology, Universidade Federal de Santa Maria (UFSM), Santa Maria, RS, Brazil. E-mail: [email protected] and [email protected]
*Corresponding author: Department of Microbiology and Parasitology, Universidade Federal de Santa Maria (UFSM), Santa Maria, RS, Brazil. E-mail: [email protected] and [email protected]

Summary

The aim of this study was to evaluate the effect of nerolidol free (N-F) and nerolidol-loaded in nanospheres (N-NS) on the hepatic antioxidant/oxidant status of mice experimentally infected by Trypanosoma evansi. In the liver it was measured: reactive oxygen species (ROS), thiobarbituric reactive acid substances (TBARS) and non-protein thiols (NPSH), catalase (CAT), superoxide dismutase (SOD) and glutathione-S-transferase (GST) and performed histopathological examination. In addition, seric levels of aspartate aminotransferase (AST) and alanine aminotransferase (ALT) were measured. Liver samples from mice infected by T. evansi showed increased (P < 0·05) ROS, TBARS, AST and ALT levels and SOD activity, and decreased NPSH levels and CAT activity (P < 0·05) compared with uninfected animals. N-NS treatment prevented (P < 0·05) ROS and TBARS increase, and increased NPSH levels, and ameliorate CAT and SOD activities on liver of infected mice. Moreover, N-NS treatment reduced (P < 0·05) AST and ALT levels, and prevented histopathological changes caused by the parasite. N-NS protected the liver from the oxidative stress caused by T. evansi, which might be due to its antioxidant properties. Nerolidol might be considered a promising therapeutic agent against oxidative stress, and nanotechnology is an encouraging approach to be explored.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2016 

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

Aebi, H. (1984). Catalase in vitro . Methods in Enzymology 105, 121126.Google Scholar
Anschau, V., Dafré, A. L., Perin, A. P., Iagher, F., Tizatoo, M. V. and Miletti, L. C. (2013) Glutathione and iron at the crossroad of redox metabolism in rats infected by Trypanosoma evansi . Parasitology Research 112, 23612366.Google Scholar
Arruda, D. C., D'Alexandri, F. L., Katzin, A. M. and Uliana, S. R. (2005). Antileishmanial activity of the terpene nerolidol. Antimicrobial Agents and Chemotherapy 49, 16791687.Google Scholar
Baldissera, M. D., Oliveira, C. B., Rech, V. C., Rezer, J. F. P., Sagrillo, M. R., Alves, M. P., da Silva, A. P. T., Leal, D. B. R., Boligon, A. A., Athayde, M. L., Da Silva, A. S., Mendes, R. E. and Monteiro, S. G. (2014). Treatment with essential oil of Achyrocline satureioides in rats infected with Trypanosoma evansi : relationship between protective effect and tissue damage. Pathology-Research and Practice 210, 10681074.CrossRefGoogle ScholarPubMed
Baldissera, M. D., Rech, V. C., Gring, M., Kolling, J., Da Silva, A. S., Gressler, L. T., Souza, C. F., Vaucher, R. A., Schwertz, C. I., Mendes, R. E., Leipnitz, G., Wyse, A. T. S., Stefani, L. M. and Monteiro, S. G. (2015). Relationship between pathological findings and enzymes of the energy metabolism in liver of rats infected by Trypanosoma evansi . Parasitology International 64, 547552.Google Scholar
Baldissera, M. D., Grando, T. H., Souza, C. F., Cossetin, L. F., Sagrillo, M. R., Nascimento, K., da Silva, A. P. T., Dalla Lana, D. F., da Silva, A. S., Stefani, L. M. and Monteiro, S. G. (2016). Nerolidol nanospheres increases its trypanocidal efficacy against Trypanosoma evansi: new approach against diminazene aceturate resistance and toxicity. Experimental Parasitology 166, 144149.Google Scholar
Biswas, D., Choudhury, A. and Misra, K. K. (2001). Histopathology of Trypanosoma (Trypanozoon) evansi infection in bandicoot rat. I. Visceral Organs. Experimental Parasitology 99, 148159.Google Scholar
Boligon, A. A., Piana, M., Kubiça, T. F., Mario, D. N., Dalmolin, T. V., Bonez, P. C., Weiblen, R., Lovato, L., Alves, S. H., Campos, M. M. A. and Athayde, M. L. (2015). HPLC analysis and antimicrobial, antimycobacterial and antiviral activities of Tabernaemontana catharinensis A. DC. Journal of Applied Biomedicine 13, 718.CrossRefGoogle Scholar
Bradford, M. M. (1976). A rapid sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein – dye binding. Analytical Biochemistry 72, 248254.Google Scholar
Calleja, M. A., Vieites, J. M., Montero-Meterdez, T., Torres, M. I., Faus, M. J., Gil, A. and Suárez, A. (2013). The antioxidant effect of β-caryophyllene protects rat liver from carbon tetrachloride-induced fribosis by inhibiting hepatic stellate cell activation. British Journal of Nutrition 109, 394401.Google Scholar
Chaudhuri, S., Varshney, J. P. and Patra, R. C. (2008). Erythrocytic antioxidant defense, lipid peroxides level and blood iron, zinc and cooper concentrations in dogs naturally infected with Babesia gibsoni . Research in Veterinary Science 85, 120124.CrossRefGoogle Scholar
Colpo, C. B., Monteiro, S. G., Stainki, D. R., Colpo, E. T. B. and Henriques, G. B. (2005). Natural infection by Trypanosoma evansi in dogs. Ciência Rural 35, 717719.Google Scholar
Da Silva, A. S., Doyle, R. L. and Monteiro, S. G. (2006). Métodos de contenção e confecção de esfregaço sanguíneo para pesquisa de hemoparasitas em ratos e camundongos. Revista da FZVA 13, 153157.Google Scholar
De Franceschi, I. D., Rieger, E., Vargas, A. P., Rojas, D. B., Campos, A. G., Rech, V. C., Feksa, L. R. and Wannmacher, C. M. D. (2013). Effect of leucine administration to female rats during pregnancy and lactation on oxidative stress and enzymes activities of phosphoryl transfer network in cerebral cortex and hippocampus of the offspring. Neurochemical Research 38, 632643.Google Scholar
Desquenes, M., Dargantes, A., Lai, D. H., Lun, Z. R., Holzmuller, P. and Jittapalapong, S. (2013). Trypanosoma evansi and surra: a review and perspectives on transmission, epidemiology and control, impact, and zoonotic aspects. BioMed Research International 2013, 321237.Google Scholar
El-Deeb, W. M. and Elmoslemany, A. M. (2015). Cardiac and oxidative stress biomarkers in Trypanosoma evansi infected camels: diagnostic and prognostic prominence. Parasitology 142, 767772.Google Scholar
Ellman, G. L. (1959). Tissue sulfhydryl groups. Archives of Biochemistry and Biophysics 82, 7077.Google Scholar
Fessi, H., Puiseux, J., Devissaguet, N., Ammoury, N. and Benita, S. (1989). Nanocapsule formation by interfacial polymer deposition following solvent displacement. International Journal of Pharmaceutics 55, 14.CrossRefGoogle Scholar
Fontana, M. C., Coradini, K., Guterres, S. S., Pohlmann, A. R. and Beck, R. C. (2009). Nanoencapsulation as a way to control the release and to increase the photostability of clobetasol propionate: influence of the nanostructured system. Journal of Biomedical Nanotechnology 5, 254263.Google Scholar
Gruber, J. W., Kittipongpatana, N., Bloxton, J. D.; Der Marderosian, A., Schaefer, F. T. and Gibbs, R. (2004). High-performance liquid chromatography and thin-layer chromatography assays for devil's club (Oplopanax horridus). Journal of Chromatographic Science 42, 196199.Google Scholar
Habig, W. H., Pabst, M. J. and Jakoby, W. B. (1974). Glutathione S-transferase. The first enzymatic step in mercapturic acid formation. Journal of Biological Chemistry 249, 71307139.Google Scholar
Halliwell, B. and Gutteridge, J. M. C. (2005). Free Radicals in Biology and Medicine, 4th Edn. Oxford University Press, New York.Google Scholar
Halliwell, B. and Whiteman, M. (2004). Measuring reactive oxygen species and oxidative damage in vivo and in cell culture: how should you do it and what do the results mean? British Journal of Pharmacology 142, 231255.Google Scholar
Herrera, H. M., Dávila, A. M., Norek, A., Abreu, U. G. and Souza, S. S. (2004). Enzootiology of Trypanosoma evansi in Pantanal, Brazil. Veterinary Parasitology 125, 263275.Google Scholar
Huang, G. J., Deng, J. S., Huang, S. S., Shao, Y. Y., Chen, C. C. and Kuo, Y. H. (2012). Protective effect of antrosterol from Antrodia camphorata submerged whole broth against carbon tetrachloride-induced acute liver injury in mice. Food Chemistry 132, 709716.CrossRefGoogle Scholar
Lang, G. and Buchbauer, G. (2012). A review on recent research results (2008–2010) on essential oils as antimicrobials and antifungals. A review. Flavour and Fragrance Journal 27, 1339.Google Scholar
Lawler, J. M., Song, W. and Demaree, S. R. (2003). Hind limb unloading increases oxidative stress and disrupts antioxidant capacity in skeletal muscle. Free Radical Biology and Medicine 35, 916.Google Scholar
Marchiori, M. L., Lubini, G., Dalla Nora, G., Friedrich, R. B., Fontana, M. C., Ourique, A. F., Bastos, M. O., Rigo, L. A., Silva, C. B., Tedesco, S. B. and Beck, R. C. (2010). Hydrogel containing dexamethasone-loaded nanocapsules for cutaneous administration: preparation, characterization, and in vitro drug release study. Drug Development and Industrial Pharmacy 36, 962971.Google Scholar
Marques, A. M., Barreto, A. L., Batista, E. M., Curvelo, J. A., Velozo, L. S., Moreira, L., Guimarães, E. F., Soares, R. M. and Kaplan, M. A. (2010). Chemistry and biological activity of essential oils from Piper claussenianum (Piperaceae). Natural Product Communications 5, 18371840.Google Scholar
Meister, A. (1983). Selective modification of glutathiones metabolism. Science 220, 472477.Google Scholar
Misra, H. P. and Fridovich, I. (1972). The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. Journal of Biological Chemistry 25, 31703175.Google Scholar
Mohd-Shukri, H. B. and Zainal-Abidin, B. A. H. (2011). The effects of nerolidol, allicin and berenil on the morphology of Trypanosoma evansi in mice: a comparative study using light and electron microscopic approaches. Malaysian Applied Biology Journal 40, 2532.Google Scholar
Nogueira Neto, J. D., de Almeida, A. A. C., Oliveira, J. S., dos Santos, P. S., de Souza, D. P. and de Freitas, R. M. (2013). Antioxidant effects of nerolidol in mice hippocampus after open field test. Neurochemical Research 38, 18611870.CrossRefGoogle ScholarPubMed
Ohkawa, H., Ohishi, N. and Yagi, K. (1979). Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Analytical Biochemistry 95, 351358.CrossRefGoogle ScholarPubMed
Ranjithkumar, M., Kamili, N. M., Saxena, A., Dan, A., Dey, S. and Raut, S. S. (2011). Disturbance of oxidant/antioxidant equilibrium in horses naturally infected with Trypanosoma evansi . Veterinary Parasitology 180, 349353.CrossRefGoogle ScholarPubMed
Rezaei, S. A. and Dalir-Naghadeh, B. (2006). Evaluation of antioxidant status and oxidative stress in cattle naturally infected with Theileria annulata . Veterinary Parasitology 142, 179186.Google Scholar
Robbins and Contran (2008). Patologia- Bases Patológicas das Doenças, 8ª edição. Elsevier, Philadelphia, 2012.Google Scholar
Rocha, N. F. M., de Oliveira, G. V., de Araújo, F. Y. R., Rios, E. R. V., Carvalho, A. M. R., Vasconcelos, L. F., Macêdo, D. S., Soares, P. M. G., De Sousa, D. P. and de Sousa, F. C. F. (2011). (-)-α-Bisabolol-induced gastroprotection is associated with reduction in lipid peroxidation, superoxide dismutase activity and neutrophil migration. European Journal of Pharmaceutical Sciences 44, 455461.Google Scholar
Rodrigues, A., Fighera, R. A., Souza, T. M., Schild, A. L. and Soares, M. P. (2005). Surtos de tripanossomíase por Trypanosoma evansi em equinos no Rio Grande do Sul: aspectos epidemiológicos, clínicos, hematológicos e patológicos. Pesquisa Veterinária Brasileira 25, 239249.CrossRefGoogle Scholar
Sabir, S. M. and Rocha, J. B. T. (2008). Water-extractable phytochemicals from Phyllanthus niruni exhibit distinct in vitro antioxidant and in vivo hepatoprotective activity against paracetamol-induced liver damage in mice. Food Chemistry 111, 845851.Google Scholar
Saleh, M. A., Al-Salahy, M. B. and Sanousi, S. A. (2009). Oxidative stress in blood of camels (Camelus dromedaries) naturally infected with Trypanosoma evansi . Veterinary Parasitology 162, 192199.Google Scholar
Sena, L. A. and Chandel, N. S. (2012). Physiological roles of mitochondrial reactive oxygen species. Molecular Cell 48, 158167.Google Scholar
Shao, B., Zhu, L., Dong, M., Wang, J., Xie, H., Zhang, Q., Du, Z. and Zhu, S. (2012). DNA damage and oxidative stress induced by endosulfan exposure in zebrafish (Danio rerio). Ecotoxicology 21, 15331540.Google Scholar
Silva, M. P. N., Oliveira, G. L. S., de Carvalho, R. B. F., de Sousa, D. P., Freitas, R. M., Pinto, P. L. S. and de Moraes, J. (2014). Antischistosomal activity of the terpene nerolidol. Molecules 19, 37933803.Google Scholar
Soppimath, K. S., Aminabhavi, T. M., Kulkarni, A. R. and Rudzinski, W. E. (2001). Biodegradable polymeric nanoparticles as drug delivery devices. Journal of Controlled Release 70, 120.Google Scholar
Sureda, A., Box, A., Enseñat, M., Alou, E., Tauler, P., Deudero, S. and Pons, A. (2006). Enzymatic antioxidant response of a labrid fish (Coris julis) liver to environmental caulerpenyne. Comparative Biochemistry and Physiology, Part C 144, 191196.Google Scholar
Winterbourn, C. C. (2015). Are free radicals involved in thiol-based redox signaling? Free Radical Biology and Medicine 80, 164170.Google Scholar