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Diphenyl diselenide reduces inflammation in the mouse model of pleurisy induced by carrageenan: reduction of pro-inflammatory markers and reactive species levels

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Abstract

Objective

We reported the anti-inflammatory action of diphenyl diselenide [(PhSe)2] in an acute inflammation model induced by carrageenan.

Materials

Male adult Swiss mice.

Methods

Mice were treated with (PhSe)2 (50 mg/kg) or vehicle (10 ml/kg) per oral route. After 30 min, animals received saline (0.1 ml) or saline containing 1 % carrageenan (0.1 ml) into the pleural cavity. Total and differential leukocyte counts, myeloperoxidase (MPO) activity, pro-inflammatory cytokines, tumor necrosis factor (TNF)-α, interleukin (IL)-1β, IL-6 and interferon (INF)-γ] and reactive species (RS) were determined in pleural fluids. Pleural exudate accumulation was determined by Evans blue assay. Statistical analysis was performed by using a two-way ANOVA followed by the Duncan’s test.

Results

(PhSe)2 treatment was effective against the increase in total and differential leukocyte counts, MPO activity, RS levels and pleural exudate caused by carrageenan. (PhSe)2 partially protected against the increase in TNF-α, IL-1β, IL-6 and INF-γ levels induced by carrageenan. (PhSe)2 had a similar anti-inflammatory profile to that of dexamethasone.

Conclusion

The anti-inflammatory property of (PhSe)2 was demonstrated in the mouse model of pleurisy induced by carrageenan. The antioxidant property of (PhSe)2 is related, at least in part, to the anti-inflammatory action of this compound.

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References

  1. Lunardelli A, Leite CE, Pires MGS, Oliveira JR. Extract of the bristles of Dirphia sp. increases nitric oxide in a rat pleurisy model. Inflamm Res. 2006;55:129–35.

    Article  PubMed  CAS  Google Scholar 

  2. Lentsch AB, Ward PA. Regulation of experimental lung inflammation. Resp Physiol. 2001;128:17–21.

    Article  CAS  Google Scholar 

  3. Saleh TSF, Calixto JB, Medeiros YS. Effects of antiinflammatory drugs upon nitrate and myeloperoxidase levels in the mouse pleurisy induced by carrageenan. Peptides. 1999;20:949–56.

    Article  PubMed  CAS  Google Scholar 

  4. Vinegar R, Truax JF, Selph JL, Voelker FA. Pathway of onset, development, and decay of carrageenan pleurisy in the rat. Fed Proc. 1982;41(9):2588–95.

    PubMed  CAS  Google Scholar 

  5. Costa R, Fernandes ES, Menezes-de-Lima O, Campos MM, Calixto JB. Effect of novel selective non-peptide kinin B1 receptor antagonists on mouse pleurisy induced by carrageenan. Peptides. 2006;27:2967–75.

    Article  PubMed  CAS  Google Scholar 

  6. Froede TS, Buss ZS, dos Reis GO, Medeiros YS. Evidence of anti-inflammatory effects of Pioglitazone in the murine pleurisy model induced by carrageenan. Int Immunopharmacol. 2009;9:1394–400.

    Article  CAS  Google Scholar 

  7. Nogueira CW, Zeni G, Rocha JBT. Organoselenium and organotellurium compounds: toxicology and pharmacology. Chem Rev. 2004;104:6255–86.

    Article  PubMed  CAS  Google Scholar 

  8. Nogueira CW, Rocha JBT. Diphenyl diselenide a Janus-faced molecule. J Braz Chem Soc. 2010;21:2055–71.

    Article  CAS  Google Scholar 

  9. Savegnago L, Trevisan M, Alves D, Rocha JBT, Nogueira CW, Zeni G. Antisecretory and antiulcer effects of diphenyl diselenide. Environ Toxicol Pharmacol. 2006;21:86–92.

    Article  PubMed  CAS  Google Scholar 

  10. Savegnago L, Pinto LG, Jesse CR, Rocha JBT, Nogueira CW, Zeni G. Spinal mechanisms of antinociceptive action caused by diphenyl diselenide. Brain Res. 2007;1162:32–7.

    Article  PubMed  CAS  Google Scholar 

  11. Rosa RM, Roesler R, Braga AL, Saffi J, Henriques JAP. Pharmacology and toxicology of diphenyl diselenide in several biological models. Braz J Med Biol Res. 2007;40:1287–304.

    Article  PubMed  CAS  Google Scholar 

  12. Luchese C, Nogueira CW. Diphenyl diselenide in its selenol form has dehydroascorbate reductase and glutathione S-transferase-like activity dependent on the glutathione content. J Pharm Pharmacol. 2010;62:1146–51.

    Article  PubMed  CAS  Google Scholar 

  13. Nogueira CW, Quinhones EB, Jung EAC, Zeni G, Rocha JBT. Anti-inflammatory and antinociceptive activity of diphenyl diselenide. Inflamm Res. 2003;52:56–63.

    Article  PubMed  CAS  Google Scholar 

  14. Savegnago L, Pinto LG, Jesse CR, Alves D, Rocha JBT, Nogueira CW, Zeni G. Antinociceptive properties of diphenyl diselenide: evidences for the mechanism of action. Eur J Pharmacol. 2007;555:129–38.

    Article  PubMed  CAS  Google Scholar 

  15. Prigol M, Schumacher RF, Nogueira CW, Zeni G. Convulsant effect of diphenyl diselenide in rats and mice and its relationship to plasma levels. Toxicol Lett. 2009;189:35–9.

    Article  PubMed  CAS  Google Scholar 

  16. Maciel EN, Flores EMM, Rocha JBT, Folmer V. Comparative deposition of diphenyl diselenide in liver, kidney, and brain of mice. Bull Environ Contam Toxicol. 2003;70:470–6.

    Article  PubMed  CAS  Google Scholar 

  17. Savegnago L, Jesse CR, Santos ARS, Rocha JBT, Nogueira CW. Mechanisms involved in the antinociceptive effect caused by diphenyl diselenide in the formalin test. J Pharm Pharmacol. 2008;60:1679–86.

    Article  PubMed  CAS  Google Scholar 

  18. Paulmier C. Selenium reagents and intermediates. In: Organic Synthesis. Pergamon, Oxford; 1986.

  19. Henriques MG, Rae GA, Cordeiro RS, Williams TJ. Endothelin-1 inhibits PAF-induced paw oedema and pleurisy in the mouse. Br J Pharmacol. 1992;106:579–82.

    Article  PubMed  CAS  Google Scholar 

  20. Suzuki K, Ota H, Sasagawa S, Sakatani T, Fujikura T. Assay method for myeloperoxidase in human polymorphonuclear leukocytes. Anal Biochem. 1983;132:345–52.

    Article  PubMed  CAS  Google Scholar 

  21. Loetchutinat C, Kothan S, Dechsupa S, Meesungnoen J, Jay-Gerin J, Mankhetkorn S. Spectrofluorometric determination of intracellular levels of reactive oxygen species in drug-sensitive and drug-resistant cancer cells using the 2′,7′-dichlorofluorescein diacetate assay. Radiat Phys Chem. 2005;72:323–31.

    Article  CAS  Google Scholar 

  22. Vianna RMJ, Calixto JB. Characterization of the receptor and the mechanisms underlying the inflammatory response induced by des-Arg9-BK in mouse pleurisy. Br J Pharmacol. 1998;123:281–91.

    Article  PubMed  CAS  Google Scholar 

  23. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principles of protein-dye binding. Anal Biochem. 1976;72:248–54.

    Article  PubMed  CAS  Google Scholar 

  24. Paul EL, Lunardelli A, Caberlon E, Oliveira CB, Santos RCV, Biolchi V, Bastos CMA, Moreira KB, Nunes FB, Gosmann G, Oliveira JR. Anti-inflammatory and immunomodulatory effects of Baccharis trimera aqueous extract on induced pleurisy in rats and lymphoproliferation in vitro. Inflammation. 2009;32:419–25.

    Article  PubMed  CAS  Google Scholar 

  25. Froede TS, Medeiros YS. Myeloperoxidase and adenosine-deaminase levels in the pleural fluid leakage induced by carraggenan in the mouse model of pleurisy. Med Inflamm. 2001;10:223–7.

    Google Scholar 

  26. Zhao L, Tao JY, Zhang SL, Pang R, Jin F, Dong JH, Guo YJ. Inner anti-inflammatory mechanisms of petroleum ether extract from Melilotus suaveolens Ledeb. Inflammation. 2007;30:213–23.

    Article  PubMed  Google Scholar 

  27. Cuzzocrea S, Mazzon E, Calabro G, Dugo L, Sarro A, Loo FAJV, Achille PC. Inducible nitric oxide synthase—knockout mice exhibit resistance to pleurisy and lung injury caused by carrageenan. Am J Respir Crit Care Med. 2000;162:1859–66.

    PubMed  CAS  Google Scholar 

  28. Bradley JR. TNF-mediated inflammatory disease. J Pathol. 2008;214:149–60.

    Article  PubMed  CAS  Google Scholar 

  29. Oliveira SHP, Canetti C, Ribeiro RA, Cunha FQ. Neutrophil migration induced by IL-1b depends upon LTB4 released by macrophages and upon TNF-a and IL-1b released by mast cells. Inflammation. 2008;31:36–46.

    Article  PubMed  CAS  Google Scholar 

  30. Utsunomiya I, Nagai S, Oh-ishi S. Sequential appearance of IL-1 and IL-6 activities in rat carrageenan-induced pleurisy. J Immunol. 1991;147:1803–9.

    PubMed  CAS  Google Scholar 

  31. Romano M, Sironi M, Toniatti C, Polentarutti N, Fruscella P, Ghezzi P, Faggioni R, Luini W, Van Hinsbergh V, Sozzani S, Bussolino F, Poli V, Ciliberto G, Mantovani A. Role of IL-6 and its soluble receptor in induction of chemokines and leukocyte recruitment. Immunity. 1997;6:315–25.

    Article  PubMed  CAS  Google Scholar 

  32. Alonzi T, Fattori E, Cappelletti M, Ciliberto G, Poli V. Impaired stat3 activation following localized inflammatory stimulus in IL-6 deficient mice. Cytokine. 1998;10:13–8.

    Article  PubMed  CAS  Google Scholar 

  33. Borish LC, Steinke JW. Cytokines and chemokines. J Allergy Clin Immunol. 2003;111:460–75.

    Article  Google Scholar 

  34. Morioka N, Inoue A, Hanada T, Kumagai K, Takeda K, Ikoma K, Hide I, Tamura Y, Shiomi H, Dohi T, Nakata Y. Nitric oxide synergistically potentiates interleukin-1 beta-induced increase of cyclooxigenase-2 mRNA levels, resulting in the facilitation of substance P release from primary afferent neurons: involvement of cGMP-independent mechanisms. Neuropharmacology. 2002;43:868–76.

    Article  PubMed  CAS  Google Scholar 

  35. O’Shaughnessy MC, Vetsika EK, Inglis JJ, Carleson J, Haigh R, Kidd BL, Winyard PG. The effect of substance P on nitric oxide release in a rheumatoid arthritis model. Inflamm Res. 2006;55:236–40.

    Article  PubMed  Google Scholar 

  36. Menegazzi M, Di Paola R, Mazzon E, Genovese T, Crisafulli C. Glycyrrhizin attenuates the development of carrageenan-induced lung injury in mice. Pharmacol Res. 2008;58:22–31.

    Article  PubMed  CAS  Google Scholar 

  37. Hort MA, Straliotto MR, Netto PM, Rocha JBT, de Bem AF, Ribeiro-do-Valle RM. Diphenyl diselenide effectively reduces atherosclerotic lesions in LDLr−/− mice by attenuation of oxidative stress and inflammation. J Cardiovasc Pharmacol. 2011;58:91–101.

    Article  PubMed  CAS  Google Scholar 

  38. Meotti FC, Stangherlin EC, Zeni G, Nogueira CW, Rocha JBT. Protective role of aryl and alkyl diselenides on lipid peroxidation. Environ Res. 2004;94:276–82.

    Article  PubMed  CAS  Google Scholar 

  39. Kade IJ, Paixao MW, Rodrigues OED, Barbosa NBV, Braga AL, Avila DS, Nogueira CW, Rocha JBT. Comparative studies on dicholesteroyl diselenide and diphenyl diselenide as antioxidant agents and their effect on the activities of Na+/K+ ATPase and delta-aminolevulinic acid dehydratase in the rat brain. Neurochem Res. 2008;33:167–78.

    Article  PubMed  CAS  Google Scholar 

  40. de Bem AF, Protella RD, Farina M, Perottoni J, Paixao MW, Nogueira CW, Rocha JBT. Low toxicity of diphenyl diselenide in rabbits: a long-term study. Basic Clin Pharmacol Toxicol. 2007;101:47–55.

    Article  PubMed  Google Scholar 

  41. Prigol M, Bruning CA, Nogueira CW, Zeni G. The role of the glutathione system in seizures induced by diphenyl diselenide in rat pups. Chem Biol Interact. 2011;193:65–70.

    Article  PubMed  CAS  Google Scholar 

  42. Cuzzocrea S, Crisafulli C, Mazzon E, Esposito E, Muià C, Abdelrahman M, Di Paola R, Thiemermann C. Inhibition of glycogen synthase kinase-3 beta attenuates the development of carrageenan-induced lung injury in mice. Br J Pharmacol. 2006;149:687–702.

    Article  PubMed  CAS  Google Scholar 

  43. Chen CC, Chow MP, Huang WC, Lin YC, Chang YJ. Flavonoids inhibit tumor necrosis factor-alpha-induced up-regulation of intercellular adhesion molecule-1 (ICAM-1) in respiratory epithelial cells through activator protein-1 and nuclear factor-kappaB: structure-activity relationships. Mol Pharmacol. 2004;66:683–93.

    Article  PubMed  CAS  Google Scholar 

  44. Impellizzeri D, Esposito E, Mazzon E, Paterniti I, Di Paola R, Bramanti P, Morittu VM, Procopio A, Britti D, Cuzzocrea S. The effects of oleuropein aglycone, an olive oil compound, in a mouse model. Clin Nutr. 2011;30:533–40.

    Article  PubMed  CAS  Google Scholar 

  45. Shin KM, Shen L, Park SJ, Jeong JH, Lee KT. Bis-(3-hydroxyphenyl) diselenide inhibits LPS-stimulated iNOS and COX-2 expression in RAW 264.7 macrophage cells through the NF-kappaB inactivation. J Pharm Pharmacol. 2009;61(4):479–86.

    PubMed  CAS  Google Scholar 

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Acknowledgments

The financial support by FAPERGS, CAPES and CNPq is gratefully acknowledged. M.P. is recipient of CAPES (PNPD) fellowship.

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Authors and Affiliations

  1. Mestrado em Nanociências, Centro de Ciências Tecnológicas, Centro Universitário Franciscano, Santa Maria, RS, CEP 97010-032, Brazil

    Cristiane Luchese

  2. Departamento de Química, Centro de Ciências Naturais e Exatas, Universidade Federal de Santa Maria, Santa Maria, RS, CEP 97105-900, Brazil

    Marina Prigol, Marta M. M. F. Duarte & Cristina W. Nogueira

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  1. Cristiane Luchese
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  2. Marina Prigol
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  3. Marta M. M. F. Duarte
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  4. Cristina W. Nogueira
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Correspondence to Cristina W. Nogueira.

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Responsible Editor: Michael Parnham.

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Luchese, C., Prigol, M., Duarte, M.M.M.F. et al. Diphenyl diselenide reduces inflammation in the mouse model of pleurisy induced by carrageenan: reduction of pro-inflammatory markers and reactive species levels. Inflamm. Res. 61, 1117–1124 (2012). https://doi.org/10.1007/s00011-012-0504-0

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  • DOI: https://doi.org/10.1007/s00011-012-0504-0

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