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Diphenyl diselenide and sodium selenite associated with chemotherapy in experimental toxoplasmosis: influence on oxidant/antioxidant biomarkers and cytokine modulation

Published online by Cambridge University Press:  08 August 2014

CLEBER F. BARBOSA ,
ALEXANDRE A. TONIN ,
ALEKSANDRO S. DA SILVA ,
MARIA I. DE AZEVEDO ,
DANIELI U. MONTEIRO ,
EMILY P. WACZUK ,
THIAGO DUARTE ,
CARINE HERMES ,
GIOVANA CAMILLO  and
FERNANDA F. VOGEL
...Show all authors
CLEBER F. BARBOSA
Affiliation:
Department of Microbiology and Parasitology, Universidade Federal de Santa Maria, Brazil
ALEXANDRE A. TONIN*
Affiliation:
Department of Small Animal Clinical, Universidade Federal de Santa Maria, Brazil
ALEKSANDRO S. DA SILVA
Affiliation:
Department of Animal Science, Universidade do Estado de Santa Catarina, Brazil
MARIA I. DE AZEVEDO
Affiliation:
Department of Microbiology and Parasitology, Universidade Federal de Santa Maria, Brazil
DANIELI U. MONTEIRO
Affiliation:
Department of Microbiology and Parasitology, Universidade Federal de Santa Maria, Brazil
EMILY P. WACZUK
Affiliation:
Department of Chemistry, Universidade Federal de Santa Maria, Brazil
THIAGO DUARTE
Affiliation:
Department of Physiology and Pharmacology, Universidade Federal de Santa Maria, Brazil
CARINE HERMES
Affiliation:
Department of Clinical and Toxicological Analysis, Universidade Federal de Santa Maria, Brazil
GIOVANA CAMILLO
Affiliation:
Universidade do Extremo Sul Catarinense, UNESC, Brazil
FERNANDA F. VOGEL
Affiliation:
Universidade do Extremo Sul Catarinense, UNESC, Brazil
LUCIANA FACCIO
Affiliation:
Department of Microbiology and Parasitology, Universidade Federal de Santa Maria, Brazil
PAULA T. TONIN
Affiliation:
Universidade do Extremo Sul Catarinense, UNESC, Brazil
PATRICIA WOLKMER
Affiliation:
Department of Chemistry, Universidade Federal de Santa Maria, Brazil
MARTA R. LEAL
Affiliation:
Department of Preventive Veterinary Medicine, Universidade Federal de Santa Maria, Brazil
MARTA M. M. F. DUARTE
Affiliation:
Universidade Luterana do Brasil, ULBRA, Brazil
RAFAEL N. MORESCO
Affiliation:
Department of Clinical and Toxicological Analysis, Universidade Federal de Santa Maria, Brazil
SONIA T. A. LOPES
Affiliation:
Department of Small Animal Clinical, Universidade Federal de Santa Maria, Brazil
MARIO L. DE LA RUE
Affiliation:
Department of Microbiology and Parasitology, Universidade Federal de Santa Maria, Brazil
*
* Corresponding author: Departamento de Clínica de Pequenos animais/LacVet – Laboratório de Análises Clínicas Veterinária – Hospital Veterinário UFSM Sala 108, Universidade Federal de Santa Maria (UFSM), Campus Universitário, CEP 97105-900, Santa Maria, RS, Brazil. E-mail: tonin.aat@gmail.com
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Summary

The aim of this study was to assess the effect of sulfamethoxazole/trimethoprim (ST) supplemented with diphenyl diselenide and sodium selenite in experimental toxoplasmosis, on oxidant/antioxidant biomarkers and cytokine levels. Eighty-four BALB/c mice were divided in seven groups: group A (negative control), and groups B to G (infected). Blood and liver samples were collected on days 4 and 20 post infection (p.i.). Levels of thiobarbituric acid (TBA) reactive substances and advanced oxidation protein products (AOPP) were assessed in liver samples. Both biomarkers were significantly increased in infected groups on day 4 p.i., while they were reduced on day 20 p.i., compared with group A. Glutathione reductase (GR) activity significantly (P<0·01) increased on day 4 p.i., in group G, compared with group A. INF-γ was significantly increased (P<0·001) in both periods, day 4 (groups B, C, F and G) and 20 p.i. (groups C, F and G). IL-10 significantly reduced (P<0·001) on day 4 p.i. in group B; however, in the same period, it was increased (P<0·001) in groups C and G, compared with group A. On day 20 p.i., IL-10 increased (P<0·001) in groups F and G. Therefore, our results highlighted that these forms of selenium, associated with the chemotherapy, were able to reduce lipid peroxidation and protein oxidation, providing a beneficial immunological balance between the production of pro- and anti-inflammatory cytokines.

Keywords

Toxoplasmosisselenium compoundslipid peroxidationprotein oxidationcytokines
Type
Research Article
Information
Parasitology , Volume 141 , Issue 13 , November 2014 , pp. 1761 - 1768
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Copyright
Copyright © Cambridge University Press 2014 

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References

REFERENCES

Arababadi, M. K., Mosavi, R., Khorramdelazad, H., Yaghini, N., Zarandi, E. R., Araste, M., Pourali, R., Nekhei, Z. and Kennedy, D. (2010). Cytokine patterns after therapy with Avonex®, Rebif®, Betaferon® and CinnoVex® in relapsing-remitting multiple sclerosis in Iranian patients. Biomarkers in Medicine 4, 755–759.CrossRefGoogle ScholarPubMed
Aspinall, T. V., Joynson, D. H., Guy, E., Hyde, J. E. and Sims, P. F. (2002). The molecular basis of sulfonamide resistance in Toxoplasma gondii and implications for the clinical management of toxoplasmosis. Journal of Infectious Diseases 185, 1637–1643.CrossRefGoogle ScholarPubMed
Baatz, H., Mirshahi, A., Puchta, J., Gumbel, H. and Hattenbach, L. O. (2006). Reactivation of Toxoplasma retinochoroiditis under atovaquone therapy in an immunocompetent patient. Ocular Immunology and Inflammation 14, 185–187.Google Scholar
Boosalis, M. G. (2008). The role of selenium in chronic disease. Nutrition in Clinical Practice 23, 152–160.CrossRefGoogle ScholarPubMed
Brenneisen, P., Steinbrenner, H. and Sies, H. (2005). Selenium, oxidative stress, and health aspects. Molecular Aspects of Medicine 26, 256–267.Google Scholar
Butura, A., Nilsson, K., Morgan, K., Morgan, T. R., French, S. W., Johansson, I., Schuppe-Koistinen, I. and Ingelman-Sundberg, M. (2009). The impact of CYP2E1 on the development of alcoholic liver disease as studied in a transgenic mouse model. Journal of Hepatology 50, 572–583.Google Scholar
Carr, A., Tindall, B., Brew, B. J., Marriott, D. J., Harkness, J. L., Penny, R. and Cooper, D. A. (1992). Low-dose trimethoprim-sulphamethoxazole prophylaxis for toxoplasmic encephalitis in patients with AIDS. Annals of Internal Medicine 117, 106–111.CrossRefGoogle ScholarPubMed
Cooper, D. Y., Levin, S., Narasimhulu, S. and Rosenthal, O. (1965). Photochemical action spectrum of the terminal oxidase of mixed function oxidase systems. Science 147, 400–402.Google Scholar
Dalle-Donne, I., Giustarini, D., Colombo, R., Rossi, R. and Milzani, A. (2003). Protein carbonylation in human diseases. Trends in Molecular Medicine 9, 169–176.Google Scholar
Dannemann, B., McCutchan, J. A., Israelski, D., Antoniskis, D., Leport, C., Luft, B., Nussbaum, J., Clumeck, N., Morlat, P., Chiu, J., Vilde, J. L., Orellana, M., Feigal, D., Bartok, A., Heseltine, P., Leedom, J. and Remington, J. (1992). The California Collaborative Treatment Group. Treatment of toxoplasmic encephalitis in patients with AIDS. A randomized trial comparing pyrimethamine plus clindamycin to pyrimethamine plus sulfadiazine. Annals of Internal Medicine 116, 33–43.CrossRefGoogle ScholarPubMed
Davies, K. J. (1987). Protein damage and degradation by oxygen radicals. I. General aspects. Journal of Biological Chemistry 262, 9895–9901.CrossRefGoogle ScholarPubMed
Davidson-York, D., Galey, F. D., Blanchard, P. and Gardner, I. A. (1999). Selenium elimination in pigs after an outbreak of selenium toxicosis. Journal of Veterinary Diagnostic Investigation 11, 352–357.Google Scholar
Davies, K. J. and Goldberg, A. L. (1987). Oxygen radicals stimulate intracellular proteolysis and lipid peroxidation by independent mechanisms in erythrocytes. Journal of Chemical Biology 262, 8220–8226.Google Scholar
Dean, R. T., Fu, S., Stocker, R. and Davies, J. M. (1997). Biochemistry and pathology of radical-mediated protein oxidation. Biochemical Journal 324, 1–18.CrossRefGoogle ScholarPubMed
Denkers, E. Y. and Gazzinelli, R. T. (1998). Regulation and function of T-cell mediated immunity during Toxoplasma gondii infection. Clinical Microbiology Reviews 11, 569–588.Google Scholar
Derouin, F. and Chastany, C. (1989). In vitro effects of folate inhibitors on Toxoplasma gondii . Antimicrobial Agents and Chemotherapy 33, 1753–1759.Google Scholar
Dubey, J. P. (2010). Toxoplasmosis of Animals and Humans, 2nd Edn. p. 313. CRC Press, Boca Raton, FL, USA.Google Scholar
Fleming, J., Ghose, A. and Harrison, P. R. (2001). Molecular mechanisms of cancer prevention by selenium compounds. Nutrition and Cancer 40, 42–49.Google Scholar
Gatkowska, J., Wieczorek, M., Dziadek, B., Dzitko, K. and Dlugonska, H. (2012). Behavioral changes in mice caused by Toxoplasma gondii invasion of brain. Parasitology Research 111, 53–58.CrossRefGoogle ScholarPubMed
Gazzinelli, R. T., Hakim, F. T., Hieny, S., Shearer, G. M. and Sher, A. (1991). Opportunistic infections and retrovirus-induced immunodeficiency: studies of acute and chronic infections with Toxoplasma gondii in mice infected with LP-BM5 murine leukemia viruses. Infection and Immunity 60, 4394–4401.Google Scholar
Gazzinelli, R., Xu, Y., Hieny, S., Cheever, A. and Sher, A. (1992). Simultaneous depletion of CD41 and CD81T lymphocytes is required to reactivate chronic infection with Toxoplasma gondii . Journal of Immunology 149, 175–180.Google Scholar
Gazzinelli, R. T., Wysocka, M., Hayashi, S., Denkers, E. Y., Hieny, S., Caspar, P., Trinchieri, G. and Sher, A. (1994). Parasite-induced IL-12 stimulates early IFN-γ synthesis and resistance during acute infection with Toxoplasma gondii . Journal of Immunology 153, 2533–2543.Google Scholar
Gazzinelli, R. T., Wysocka, M., Hieny, S., Scharton-Kersten, T., Cheever, A., Kuhn, R., Muller, W., Trinchieri, G. and Sher, A. (1996). In the absence of endogenous IL-10, mice acutely infected with Toxoplasma gondii succumb to a lethal immune response dependent upon CD41T cells and accompanied by overproduction of IL-12, IFN-γ, and TNF-α . Journal of Immunology 157, 798–805.Google Scholar
Grossman, P. L. and Remington, J. S. (1979). The effect of trimethoprim and sulphamethoxazole on Toxoplasma gondii in vitro and in vivo . American Journal of Tropical Medicine and Hygiene 28, 445–455.Google Scholar
Guengerich, F. P. (2008). Cytochrome p450 and chemical toxicology. Chemical Research in Toxicology 21, 70–83.Google Scholar
Heinecke, J. W., Li, W., Daehnke, H. L. and Goldstein, J. A. (1993). Dityrosine, a specific marker of oxidation, is synthesized by the myeloperoxidase-hydrogen peroxide system of human neutrophils and macrophages. Journal of Biological Chemistry 268, 4069–4077.CrossRefGoogle ScholarPubMed
Hermes, C. L., Hausen, B. S., Sangoi, M. B., Almeida, T. C., Carvalho, J. A. M., Gomes, P. and Moresco, R. N. (2013). An automated technique for the measurement of the plasma glutathione reductase activity and determination of reference limits for a healthy population. Clinical Chemistry and Laboratory Medicine 5, 31–33.CrossRefGoogle Scholar
Hoffmann, P. R. and Berry, M. J. (2008). The influence of selenium on immune responses. Molecular Nutrition and Food Research 52, 1273–1280.Google Scholar
Johnson, L. L. (1992). A protective role for endogenous tumor necrosis factor in Toxoplasma gondii infection. Infection and Immunity 60, 1979–1985.CrossRefGoogle ScholarPubMed
Kamerbeek, N. M., van Zwieten, R., de Boer, M., Morren, G., Vuil, H., Bannink, N., Lincke, C., Dolman, K. M., Becker, K., Schirmer, R. H., Gromer, S. and Roos, D. (2007). Molecular basis of glutathione reductase deficiency in human blood cells. Blood 109, 3560–3566.CrossRefGoogle ScholarPubMed
Li, S., Cui, L., Zhao, J., Dai, P., Zong, S., Zuo, W., Chen, C., Jin, H., Gao, H. and Liu, Q. (2011). Seroprevalence of Toxoplasma gondii infection in female sterility patients in China. Journal of Parasitology 97, 529–530.Google Scholar
Lu, J. and Jiang, C. (2005). Selenium and cancer chemoprevention: hypotheses integrating the actions of selenoproteins and selenium metabolites in epithelial and non-epithelial target cells. Antioxidants and Redox Signaling 7, 1715–1727.CrossRefGoogle ScholarPubMed
Lu, D., Ma, Y., Zhang, W., Bao, D., Dong, W., Lian, H., Huang, L. and Zhang, L. (2012). Knockdown of cytochrome P450 2E1 inhibits oxidative stress and apoptosis in the cTnT(R141W) dilated cardiomyopathy transgenic mice. Hypertension 60, 81–89.Google Scholar
Luft, B. J., Brooks, R. G., Conley, F. G., McCabe, R. E. and Remington, J. S. (1984). Toxoplasmic encephalitis in patients with acquired immune deficiency syndrome. Journal of the American Medical Association 252, 913–917.Google Scholar
Mahan, D. C., Cline, T. R. and Richert, B. (1999). Effects of dietary levels of selenium enriched yeast and sodium selenite as selenium sources fed to growing-finishing pigs on performance, tissue selenium, serum glutathione peroxidase activity, carcass characteristics and loin quality. Journal of Animal Science 77, 2172–2179.Google Scholar
Mahmoud, K. Z. and Edens, F. W. (2003). Influence of selenium sources on age related and mild heat stress-related changes of blood and liver glutathione redox cycle in broiler chickens (Gallus domesticus). Comparative Biochemistry and Physiology-Part B. Biochemistry and Molecular Biology 136, 921–934.CrossRefGoogle ScholarPubMed
Mannervik, B. and Carlberg, I. (1985). Glutathione reductase. Methods in Enzymology 113, 484–490.Google Scholar
Meotti, F. C., Borges, V. C., Zeni, G., Rocha, J. B. and Nogueira, C. W. (2003). Potential renal and hepatic toxicity of diphenyl diselenide, diphenyl ditelluride and Ebselen for rats and mice. Toxicology Letters 143, 9–16.Google Scholar
Mordue, D. G., Monroy, F., La Regina, M., Dinarello, C. A. and Sibley, L. D. (2001). Acute toxoplasmosis leads to lethal overproduction of Th1 cytokines. Immunology 167, 4574–4584.Google ScholarPubMed
Mugesh, G., du Mont, W. W. and Sies, H. (2001). Chemistry of biologically important synthetic organoselenium compounds. Chemical Reviews 101, 2125–2179.Google Scholar
Naithani, R. (2008). Organoselenium compounds in cancer chemoprevention. Mini-Reviews in Medicinal Chemistry 8, 657–668.Google Scholar
Nebert, D. W. and Dalton, T. P. (2006). The role of cytochrome P450 enzymes in endogenous signalling pathways and environmental carcinogenesis. Nature Reviews Cancer 6, 947–960.Google Scholar
Nogueira, C. W., Meotti, F. C., Curte, E., Pilissao, C., Zeni, G. and Rocha, J. B. (2003). Investigations into the potential neurotoxicity induced by diselenides in mice and rats. Toxicology 183, 29–37.CrossRefGoogle ScholarPubMed
Ohkawa, H., Ohishi, N. and Yagi, K. (1979). Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Analytical Biochemistry 95, 351–358.Google Scholar
Petersen, D. R. and Doorn, J. A. (2004). Reactions of 4-hydroxynonenal with proteins and cellular targets. Free Radical Biology and Medicine 37, 937–945.CrossRefGoogle ScholarPubMed
Prigol, M., Schumacher, R. F., Nogueira, C. W. and Zeni, G. (2009). Convulsant effect of diphenyl diselenide in rats and mice and its relationship to plasma levels. Toxicology Letters 189, 35–39.Google Scholar
Rayman, M. P. (2005). Selenium in cancer prevention: a review of the evidence and mechanism of action. Proceedings of the Nutrition Society 64, 527–542.Google Scholar
Rayman, M. P. (2008). Food-chain selenium and human health: emphasis on intake. British Journal of Nutrition 100, 254–268.Google Scholar
Rossato, J. I., Ketzer, L. A., Centuriao, F. B., Silva, S. J., Ludtke, D. S., Zeni, G., Braga, A. L., Rubin, M. A. and Rocha, J. B. (2002). Antioxidant properties of new chalcogenides against lipid peroxidation in rat brain. Neurochemical Research 27, 297–303.Google Scholar
Scharton-Kersten, T. M., Wynn, T. A., Denkers, E. Y., Bala, S., Showe, L., Grunvald, E., Hieny, S., Gazzinelli, R. T. and Sher, A. (1996). In the absence of endogenous IFN-γ mice develop unimpaired IL-12 responses to Toxoplasma gondii while failing to control acute infection. Journal of Immunology 157, 4045–4054.CrossRefGoogle ScholarPubMed
Schattenberg, J. M., Wang, Y., Rigoli, R. M., Koop, D. R. and Czaja, M. J. (2004). CYP2E1 overexpression alters hepatocyte death from menadione and fatty acids by activation of ERK1/2 signaling. Hepatology 39, 444–455.Google Scholar
Smit, A. J. and Lutgers, H. L. (2004). The clinical relevance of advanced glycation endproducts (AGE) and recent developments in pharmaceutics to reduce AGE accumulation. Current Medicinal Chemistry 11, 2767–2784.Google Scholar
Suzuki, Y., Conley, F. K. and Remington, J. S. (1989). Importance of endogenous IFN-γ for the prevention of toxoplasmic encephalitis in mice. Journal of Immunology 143, 2045–2050.Google Scholar
Tenter, A. M., Heckeroth, A. R. and Weiss, L. M. (2000). Toxoplasma gondii: from animals to humans. International Journal for Parasitology 30, 1217–1258.Google Scholar
Thomas, H. V., Thomas, D. R., Salmon, R. L., Lewis, G. and Smith, A. P. (2004). Toxoplasma and coxiella infection and psychiatric morbidity: a retrospective cohort analysis. BMC Psychiatry 4, 32.Google Scholar
Thum, T. and Borlak, J. (2002). Testosterone, cytochrome P450, and cardiac hypertrophy. FASEB Journal 16, 1537–1549.Google Scholar
van Gisbergen, K. P., Geijtenbeek, T. B. and van Kooyk, Y. (2005). Close encounters of neutrophils and DCs. Trends in Immunology 26, 626–631.Google Scholar
Vermeulen, A. N. (1998). Progress in recombinant vaccine development against coccidiosis. A review and prospects into the next millennium. International Journal for Parasitology 28, 1121–1130.CrossRefGoogle ScholarPubMed
Wen, X., Wang, J. S., Backman, J. T., Laitila, J. and Neuvonen, P. J. (2002). Trimethoprim and sulfamethoxazole are selective inhibitors of CYP2C8 and CYP2C9, respectively. Drug Metabolism and Disposition 30, 631–635.Google Scholar
Witko-Sarsat, V., Friedlander, M., Nguyen Khoa, T., Capeillere-Blandin, C., Nguyen, A. T., Canteloup, S., Dayer, J. M., Jungers, P., Drueke, T. and Descamps-Latscha, B. (1998). Advanced oxidation protein products as novel mediators of inflammation and monocyte activation in a chronic renal failure. Journal of Immunology 161, 2524–2532.Google Scholar
Wong, S. and Remington, J. S. (1994). Toxoplasmosis in pregnancy. Clinical Infectious Diseases 18, 853–861.Google Scholar
Wu, D. and Cederbaum, A. I. (2001). Removal of glutathione produces apoptosis and necrosis in HepG2 cells overexpressing CYP2E1. Alcoholism: Clinical and Experimental Research 25, 619–628.Google Scholar
Yuan, Z., Gao, S., Liu, Q., Xia, X., Liu, X., Liu, B. and Hu, R. (2007). Toxoplasma gondii antibodies in cancer patients. Cancer Letters 254, 71–74.Google Scholar