Synergistic effects of resveratrol (free and inclusion complex) and sulfamethoxazole-trimetropim treatment on pathology, oxidant/antioxidant status and behavior of mice infected with Toxoplasma gondii

Microbial Pathogenesis

Volumn 95, Issue , 2016, Pages 166-174

  Bottari, Nathieli B ^a   Baldissera, Matheus D ^b   Tonin, Alexandre A ^a   Rech, Virginia C ^b   Alves, Catiane B ^b   D'Avila, Fernanda ^b   Thomé, Gustavo R ^a   Guarda, Naiara S ^a   Moresco, Rafael N ^a   Camillo, Giovana ^a   Vogel, Fernanda F ^a   Luchese, Cristiane ^c   Schetinger, Maria Rosa C ^a   Morsch, Vera M ^a   Tochetto, Camila ^a   Fighera, Rafael ^a   Nishihira, Vivian S K ^b   Da Silva, Aleksandro S ^a,d  

^a FEDERAL UNIVERSITY OF SANTA MARIA   (Brazil)

^b CENTRO UNIVERSITÁRIO FRANCISCANO   (Brazil)

^c FEDERAL UNIVERSITY OF PELOTAS   (Brazil)

^d SANTA CATARINA STATE UNIVERSITY   (Brazil)

Author keywords

Behavior; Nanotecnology; Oxidants antioxidants; Resveratrol; Toxoplasma gondii

Indexed keywords

COTRIMOXAZOLE; NANOPARTICLE; RESVERATROL; ANTIINFECTIVE AGENT; ANTIOXIDANT; NONSTEROID ANTIINFLAMMATORY AGENT; OXIDIZING AGENT; STILBENE DERIVATIVE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ANTIOXIDANT ASSAY; ANXIETY; ARTICLE; BRAIN CYST; CHRONIC DISEASE; CONTROLLED STUDY; DISEASE COURSE; DRUG POTENTIATION; ELEVATED PLUS MAZE TEST; HISTOPATHOLOGY; INFECTION; LATENT PERIOD; LOCOMOTION; LONG TERM MEMORY; MEMORY; MOUSE; NONHUMAN; OPEN FIELD TEST; PASSIVE AVOIDANCE TEST; PRIORITY JOURNAL; TACHYZOITE; TOXOPLASMA GONDII; TOXOPLASMOSIS; ANIMAL; ANTAGONISTS AND INHIBITORS; BRAIN; COMBINATION DRUG THERAPY; DISEASE MODEL; LIVER; OXIDATIVE STRESS; PATHOLOGY; TOXOPLASMOSIS, ANIMAL; TREATMENT OUTCOME;

ANIMALS; ANTI-INFECTIVE AGENTS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; ANTIOXIDANTS; BEHAVIOR, ANIMAL; BRAIN; DISEASE MODELS, ANIMAL; DRUG SYNERGISM; DRUG THERAPY, COMBINATION; LIVER; MICE; OXIDANTS; OXIDATIVE STRESS; STILBENES; TOXOPLASMOSIS, ANIMAL; TREATMENT OUTCOME; TRIMETHOPRIM, SULFAMETHOXAZOLE DRUG COMBINATION;

EID: 84962787219     PISSN: 08824010     EISSN: 10961208     Source Type: Journal    
DOI: 10.1016/j.micpath.2016.04.002     Document Type: Article

References (43)

1. Black M.W., Boothroyd J.C. Lytic cycle of Toxoplasma gondii. Microbiol. Mol. Biol. Rev. 2000, 64:607-623.
2. Dubey J.P. Toxoplasmosis of Animals and Humans 2012, CRC Press, Boca Raton. second ed.
3. Tender A.M., Heckeroth A.R., Weiss L.M. Toxoplasma gondii: from animals to humans. Int. J. Parasitol. 2000, 30:1217-1258.
4. Dubey J.P., Shen S.K., Kwok O.C., Frenkel J.K. Infection and immunity with the RH strain of Toxoplasma gondii in rats and mice. J. Parasitol. 1999, 85:657-662.
5. Carr A., Brett Tindall B., Brew B.J., Marriott D.J., Harkness J.L., Penny R., Cooper D.A. Low-dose trimethoprim-sulfamethoxazole prophylaxis for toxoplasmic encephalitis in patients with AIDS. Ann. Intern. Med. 1992, 117:106-111.
6. De Souza W., Duarte E.S.M., Urbina J.A., Vommaro R.C. Antiproliferative activities of two novel quinuclidine inhibitors against Toxoplasma gondii tachyzoites in vitro. J. Antimicrob. Chemother. 2006, 58:59-65.
7. Lopes F.M.R., Gonçalves D.D., Mitsuka-Breganó R., Freire R.L., Navarro I.T. Toxoplasma gondii infection in pregnancy. Braz. J. Infect. Dis. 2007, 11:5.
8. Schultz T.L., Hencken C.P., Woodard L.E., Posner G.H., Yolken R.H., Jones-Brando L., Carruthers V.B. A thiazole derivative of artemisinin moderately reduces toxoplasma gondii cyst burden in infected mice. J. Parasitol. 2014, 100:516-521.
9. Barbosa C., Tonin A.A., Faccio L., Da Silva A.S., Vogel F., Rue M. Diphenyl diselenide and sodium selenite associated with chemotherapy in experimental toxoplasmosis: influence on oxidant/antioxidant biomarkers and cytokine modulation. Parasitol 2014, 141:1761-1768.
10. Imamura G., Bertelli A.A., Bertelli A., Otani H., Maulik N., Das D.K. Pharmacological preconditioning with resveratrol: an insight with iNOS knockout mice. Am. J. Physiol. Heart Circ. Physiol. 2002, 282:1996-2003.
11. Frémon L. Biological effects of resveratrol. Life Sci. 2000, 66:663-673.
12. De la Lastra C.A., Villegas I. Resveratrol as an antioxidant and pro-oxidant agent: mechanisms and clinical implications. Biochem. Soc. Trans. 2007, 35:1156-1160.
13. Watal G., Watal A., Rai P.K., Rai D.K., Sharma G., Sharma B. Biomedical applications of nano-antioxidant. Methods Mol. Biol. 2013, 1028:147-151.
14. Musyanovych A., Landfester K. Polymer micro- and nanocapsules as biological carriers with multifunctional properties. Macromol. Biosci. 2014, 14:458-477.
15. Pellow P., Chopin S.E., File M., Brile Y. Validation of open: closed arm entries in an elevated plus maze as a measure of anxiety in the rat. J. Neurosci. Methods 1982, 14:149-167.
16. Clénet F., Bouyon E., Hascoet M., Bourin M. Light/dark cycle manipulation influences mice behavior in the elevated plus maze. Behav. Brain Res. 2006, 166:140-149.
17. Sakaguchi M., Koseki M., Wakamatsu M., Matsumura E. Effects of systemic administration of beta-casomorphin-5 on learning and memory in mice. Eur. J. Pharmacol. 2006, 530:81-87.
18. Walsh R.N., Cummins R.A. The open-field test: a critical review. Psychol. Bull. 1976, 83:482-504.
19. Dumas J.L., et al. Evaluation of the efficacy of prolonged administration of azithromycin in a murine model of chronic toxoplasmosis. J. Antimicrob. Chemother. 1994, 34:111-118.
20. Hanasand M., Omdal R., Norheim K.B., Goransson L.G., Brede C. Improved detection of advanced oxidation protein products in plasma. Clin. Chim. Acta 2012, 413:901-906.
21. Erel O. A new automated colorimetric method for measuring total oxidant status. Clin. Biochem. 2005, 38:1103-1111.
22. Erel O. A novel automated direct measurement method for total antioxidant capacity using a new generation, more stable ABTS radical cation. Clin. Biochem. 2005, 37:277-285.
23. Benzie I.F.F., Strain J.J. Ferric reducing ability of plasma (FRAP) as a measure of antioxidant power: the FRAP assay. Anal. Biochem. 1996, 239:70-76.
24. Durary R.A.B., Willington E.A. Carelton's Histological Techniques 1976, Oxford University Press, London.
25. Correa G., Da Silva C.M., Moreira-Souza A.C.A., Vommaro R.C., Coutinho-Silva R. Activation of the P2X7 receptor triggers the elimination of Toxoplasma gondii tachyzoites from infected macrophages. Microb. Infect. 2010, 12:497-504.
26. Flegr J., Preiss M., Klose J., Hávlicek J., Vitakova M., Kodym P. Decreased level of psychobiological factor novelty seeking and lower intelligence in men latently infected with the protozoan parasite Toxoplasma gondii dopamine, a missing link between schizophrenia and toxoplasmosis?. Biol. Psychol. 2003, 63:253-268.
27. Webster J.P., Brunton C.F.A., MacDonald D.W. Effect of Toxoplasma gondii upon neophobic behavior in wild brown rats, Rattus norvegicus. Parasitology 1993, 109:37-43.
28. Queiroz M.L., Viel T.A., Papa C.H.G., Lescano S.A.Z., Chieff P.P. Behavioral changes in Rattus norvegicus coinfected by Toxocara canis and Toxoplasma gondii. Rev. Inst. Med. Trop. Sao Paulo 2013, 55:51-53.
29. Berenreiterová M., Flegr J., Kuběna A.A., Němec P. The distribution of Toxoplasma gondii cysts in the brain of a mouse with latent toxoplasmosis: implications for the behavioral manipulation hypothesis. Plos One 2011, 6:e28925.
30. Frozza R.L., Bernardi A., Hoppe J.B., Meneghetti A.B., Battastini A.M., Pohlmann A.R., Guterres S.S., Salbego C. Lipid-core nanocapsules improve the effects of resveratrol against Abeta-induced neuroinflammation. J. Biomed. Nanotechnol. 2013, 9:2086-2104.
31. Yarovisky F., Zhang D., Andersen J.F., Bannenberg G.L., Serhan C.N., Hayden M.S., Hieny S., Sutterwalla F.S., Flavell R.A., Ghosh S., Sher A. TLR11 activation of dendritic cells by a protozoan profilin-like protein. Science 2005, 308:1626-1629.
32. Cooper D.Y., Levin S., Narasimhulu S., Rosenthal O. Photochemical action spectrum of the terminal oxidase of mixed function oxidase systems. Science 1965, 147:400-402.
33. Guengerich F.P. Cytochrome p450 and chemical toxicology. Chem. Res. Toxicol. 2008, 21:70-83.
34. Wu D., Cederbaum A.I. Removal of glutathione produces apoptosis and necrosis in HepG2 cells overexpressing CYP2E1. Alcohol. Clin. Exp. Res. 2001, 25:619-628.
35. Csiszár A., Csiszar A., Pinto J.T., Gautam T., Kleusch C., Hoffmann B., Tucsek Z., Toth P., Sonntag W.E., Ungvari Z. Resveratrol encapsulated in novel fusogenic liposomes activates Nrf2 and attenuates oxidative stress in cerebromicrovascular endothelial cells from aged rats. J. Gerontol. Biol. Sci. Med. Sci. 2014, 69. 10.1093/gerona/glu029.
36. Kwok L.Y., Schlüter D., Clayton C., Soldati D. The antioxidant systems in Toxoplasma gondii and the role of cytosolic catalase in defence against oxidative injury. Mol. Microbiol. 2014, 51:47-61.
37. Kwok L.Y., Schlüter D., Clayton C., Soldati D. The antioxidant systems in Toxoplasma gondii and the role of cytosolic catalase in defence against oxidative injury. Mol. Microbiol. 2014, 51:47-61.
38. Ding M., Kwok L.Y., Schlüter D., Clayton C., Soldati D. The antioxidant systems in Toxoplasma gondii and the role of cytosolic catalase in defence against oxidative injury. Mol. Microbiol. 2004, 51:47-61.
39. Bottari N.B., Baldissera M.D., Tonin A.A., Rech V.C., Nishihira V.S.K., Thomé G.R., Schetinger M.R.C., Morsch V.M., Camillo G., Vogel F.F., Tochetto C., Fighera R., Machado G., Stefani L.M., Da Silva A.S. Sulfamethoxazole-trimethoprim associated with resveratrol for the treatment of toxoplasmosis in mice: influence on the activity of enzymes involved in brain neurotransmission. Microb. Pathog. 2015, 79:17-23.
40. Bottari N.B., Baldissera M.D., Tonin A.A., Rech V.C., Nishihira V.S.K., Thomé G., Schetinger M.R.C., Morsch V.M., Camillo G., Voguel F.F., Tochetto C., Fighera R., Machado G., Da Silva A.S. Effects of sulfamethoxazole-trimethoprim associated to resveratrol on its free form and complexed with 2-hydroxypropyl-β-cyclodextrin on cytokines levels of mice infected by Toxoplasma gondii. Microb. Pathog. 2015, 87:40-44.
41. Bereswill S., Muñoz M., Fischer A., Plickert R., Haag L.M., Otto B., Kuhl A.A., Loddenkemper J., Gobel U.B., Heimesaat M.M. Anti-Inflammatory effects of resveratrol, curcumin and simvastatin in acute small intestinal inflammation. PLoS One 2010, 5:e15099.
42. Martins-Duarte E.S., De Souza W., Vommaro R.C. Toxoplasma gondii: the effect of fluconazole combined with sulfadiazine and pyrimethamine against acute toxoplasmosis in murine model. Exp. Parasitol. 2013, 133:294-299.
43. Remington J.S. Trimethoprim-sulfamethoxazole in murine toxoplasmosis. Antimicrob. Agents Chemother. 1976, 9:222-223.