Skip to main content
Log in

Improvement of Heart Redox States Contributes to the Beneficial Effects of Selenium Against Penconazole-Induced Cardiotoxicity in Adult Rats

  • Published:
Biological Trace Element Research Aims and scope Submit manuscript

Abstract

The present study was performed to evaluate the protective effect of selenium (Se) against penconazole (PEN)-induced oxidative stress in the cardiac tissue of adult rats. Male Wistar rats were divided into four groups of six each. The first group represented the controls. For the second group (PEN), no treatment was performed during the first 6 days, and then, the rats received intraperitoneally 67 mg/kg body weight (bw) of PEN every 2 days from day 7 until day 15, the sacrifice day. For the third group (Se + PEN), Se was administered daily through the diet at a dose of 0.5 mg/kg of diet for 15 days. Rats of this group received also every 2 days PEN (67 mg/kg bw) from day 7 until day 15. The fourth group (Se) received daily, through the diet, Se (0.5 mg/Kg of diet) during 15 days. Our results showed that Se reduced significantly the elevated cardiac levels of malondialdehyde and protein carbonyl following PEN treatment, and attenuated DNA fragmentation induced by this fungicide. In addition, Se modulated the alterations of antioxidant status: enzymatic (superoxide dismutase, glutathione peroxidase, and catalase) and nonenzymatic (glutathione and vitamin C) antioxidants in the heart of PEN-treated rats. This trace element was also able to alleviate perturbations of lipid profile. The protective effect of selenium was further evident through the histopathological changes produced by PEN in the heart tissue. Taken together, our results indicated that Se might be beneficial against PEN-induced cardiac oxidative damage in rats.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

AChE:

Acetylcholinesterase

AI:

Atherogenic index

Bw:

Body weight

CAT:

Catalase

DTNB:

5,5′-dithiobis-2-nitrobenzoic acid

GPx:

Glutathione peroxidase

GSH:

Reduced glutathione

HDL-C:

High-density lipoprotein cholesterol

LDL-C:

Low-density lipoprotein cholesterol

MDA:

Malondialdehyde

MRL:

Maximum residue limits

Na2SeO3 :

Sodium selenite

PCO:

Protein carbonyl

PEN:

Penconazole

ROS:

Reactive oxygen species

Se:

Selenium

SOD:

Superoxide dismutase

TBA:

Thiobarbituric acid

TC:

Total cholesterol

TG:

Triglyceride

References

  1. Tinggi U (2008) Selenium: its role as antioxidant in human health. Environ Health Prev Med 13:102–108

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  2. El-Demerdash FM, Nasr HM (2014) Antioxidant effect of selenium on lipid peroxidation, hyperlipidemia and biochemical parameters in rats exposed to diazinon. J Trace Elem Med Biol 28:89–93

    Article  PubMed  CAS  Google Scholar 

  3. Tinggi U, Reilly C, Patterson CM (1992) Determination of selenium in foodstuffs using spectrofluorometry and hydride generation atomic absorption spectrometry. J Food Comp Anal 5:269–280

    Article  CAS  Google Scholar 

  4. Rayman M (2012) Selenium and human health. Lancet 379:1256–1268

    Article  PubMed  CAS  Google Scholar 

  5. Brigelius-Flohe R, Banning A, Schnurr K (2003) Selenium-dependent enzymes in endothelial cell function. Antioxid Redox Signal 5:205–215

    Article  PubMed  CAS  Google Scholar 

  6. Zhong GG, Jiang Y, Li ZB, Zhang BG, Zhang WJ, Yue G (1990) Protective action of selenium and manganese on xanthine and xanthine oxidase induced oxidative damage to cultured heart cells. Chinese Med J Peking 103:735–742

    CAS  Google Scholar 

  7. Danesi F, Malaguti M, Nunzio MD, Maranesi M, Biagi PL, Bordoni A (2006) Counteraction of adriamycin-induced oxidative damage in rat heart by selenium dietary supplementation. J Agric Food Chem 54:1203–1208

    Article  PubMed  CAS  Google Scholar 

  8. Sohal RS, Weindruch R (1996) Oxidative stress, caloric restriction and aging. Science 273:59–63

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  9. Heistad DD (2006) Oxidative stress and vascular disease: 2005 Duff lecture. Arterioscler Thromb Vasc Biol 26:689–695

    Article  PubMed  CAS  Google Scholar 

  10. Jaiswal SK, Nj S, Sharma B (2013) Carbofuran induced oxidative stress in rat heart: ameliorative effect of vitamin C. ISRN Oxid Med ID 824102

  11. Wang P, Jiang S, Liu D, Wang PI, Zhou Z (2005) Direct enantiomeric resolutions of chiral triazole pesticides by high-performance liquid chromatography. J Biochem Biophys Methods 62:219–230

    Article  PubMed  CAS  Google Scholar 

  12. Buchenauer H (1987) Mechanism of action of triazol fungicides and related compounds. In: Lyr H (ed) Modern selective fungicides: properties, applications, mechanisms of action. Longman Scientific and Technical, Co-published in the United States with John Wiley and Sons, Inc, New York, pp. 205–232

    Google Scholar 

  13. Kenyon DM, Dixon GR, Helfer S (1997) The repression and stimulation of growth of Erysiphe sp. on Rhododendron by fungicidal compounds. Plant Pathol 46:425–431

    Article  CAS  Google Scholar 

  14. Percival GC, Boyle S (2005) Evaluation of microcapsule trunk injections for the control of apple scab and powdery mildew. Ann Appl Biol 147:119–127

    Article  Google Scholar 

  15. Kim IS, Beaudette LA, Shim JH, Trevors JT, Suh YT (2002) Environmental fate of the triazole fungicide propiconazole in a rice-paddy-soil lysimeter. Plant Soil 239:321–331

    Article  CAS  Google Scholar 

  16. Singh N (2005) Mobility of four triazole fungicides in two Indian soils. Pest Manag Sci 61:191–196

    Article  PubMed  CAS  Google Scholar 

  17. Güdücü HE, İnam R, Aboul-Enein HY (2011) Determination of organophosphorus and triazole pesticides by gas chromatography and application to vegetable and commercial samples. J Liq Chrom Rel Technol 34:2473–2483

    Article  CAS  Google Scholar 

  18. El-Sharkawy EE, El-Nisr NA (2013) Testicular dysfunction induced by penconazole fungicide on male albino rats. Comp Clin Path 22:475–480

    Article  CAS  Google Scholar 

  19. Perdichizzi S, Mascolo MG, Silingardi P, Morandi E, Rotondo F, Guerrini A, Prete L, Vaccari M, Colacci A (2014) Cancer-related genes transcriptionally induced by the fungicide penconazole. Toxicol in Vitro 28:125–130

    Article  PubMed  CAS  Google Scholar 

  20. Council of European Communities (1986) Council instructions about the protection of living animals used in scientific investigations. Off J Eur Commun (JO 86/609/CEE) L358: 1–18

  21. Ben Amara I, Fetoui H, Guermazi F, Zeghal N (2009) Dietary selenium addition improves cerebrum and cerebellum impairments induced by methimazole in suckling rats. Int J Dev Neurosci 27:719–726

    Article  PubMed  CAS  Google Scholar 

  22. Hotz CS, Fitzpatrick DW, Trick KD, L’Abbe MR (1997) Dietary iodine and selenium interact to affect thyroid hormone metabolism of rats. J Nutr 127:1214–1218

    PubMed  CAS  Google Scholar 

  23. Lowry OH, Rosebrugh NJ, Farr AL, Randall RJ (1951) Protein measurement with the folin phenol reagent. J Biol Chem 193:265–275

    PubMed  CAS  Google Scholar 

  24. Draper HH, Hadley M (1990) Malondialdehyde determination as index of lipid peroxidation. Methods Enzymol 186:421–431

    Article  PubMed  CAS  Google Scholar 

  25. Reznick AZ, Packer L (1994) Oxidative damage to proteins: spectrophotometric method for carbonyl. Method Enzymol. Academic Press, New York, p. 357

    Google Scholar 

  26. Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126

    Article  PubMed  CAS  Google Scholar 

  27. Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287

    Article  PubMed  CAS  Google Scholar 

  28. Flohe L, Gunzler WA (1984) Assays of glutathione peroxidase. Methods Enzymol 105:114–121

    Article  PubMed  CAS  Google Scholar 

  29. Ellman GL (1959) Tissue sulfhydryl groups. Arch Biochem Biophys 82:70–77

    Article  PubMed  CAS  Google Scholar 

  30. Jacques-Silva MC, Nogueira CW, Broch LC, Flores EMM, Rocha JBT (2001) Diphenyl diselenide and ascorbic acid changes deposition of selenium and ascorbic acid in liver and brain of mice. J Pharmacol Toxicol 88:119–125

    Article  CAS  Google Scholar 

  31. Friedewald WT (1972) Estimation of concentration of low-density lipoprotein cholesterol in plasma without use of the preparative ultracentrifuge. Clin Chem 18:499–502

    PubMed  CAS  Google Scholar 

  32. Ellman GL, Courtney KD, Andres V, Featherstone R (1961) A new and rapid colorimetric determination of acetyl cholinesterase activity. Biochem Pharmacol 7:88–95

    Article  PubMed  CAS  Google Scholar 

  33. Hester SD, Nesnow S (2008) Transcriptional responses in thyroid tissues from rats treated with a tumorigenic and a non-tumorigenic triazole conazole fungicide. Toxicol Appl Pharm 227:357–369

    Article  CAS  Google Scholar 

  34. Ross JA, Moore T, Leavitt SA (2009) In vivo mutagenicity of conazole fungicides correlates with tumorigenicity. Mutagenesis 24:149–152

    Article  PubMed  CAS  Google Scholar 

  35. Moser VC, Barone S, Smialowicz RJ, Harris MW, Davis BJ, Overstreet D, Mauney M, Chapin RE (2001) The effects of perinatal tebuconazole exposure on adult neurological, immunological, and reproductive function in rats. J Toxicol Sci 62:339–352

    Article  CAS  Google Scholar 

  36. Georgopapadakou NH, Walsh TJ (1996) Antifungal agents: chemotherapeutic targets and immunologic strategies. Antimicrob Agents CH 40:279–291

    CAS  Google Scholar 

  37. Peffer RC, Moggs JG, Pastoor T, Currie RA, Wright J, Milburn G, Waechter F, Rusyn I (2007) Mouse liver effects of cyproconazole, a triazole fungicide: role of the constitutive androstane receptor. J Toxicol Sci 99:315–325

    Article  CAS  Google Scholar 

  38. Papaefthimiou C, Theophilidis G (2001) The cardiotoxic action of the pyrethroid insecticide deltamethrin, the azole fungicide prochloraz, and their synergy on the semi-isolated heart of the bee Apis mellifera macedonica. Pestic Biochem Phys 69:77–91

    Article  CAS  Google Scholar 

  39. Won KJ, Lin HY, Jung S, Cho SM, Shin HC, Bae YM, Lee SH, Kim HJ, Jeon BH, Kim B (2012) Antifungal miconazole induces cardiotoxicity via inhibition of APE/Ref-1-related pathway in rat neonatal cardiomyocytes. J Toxicol Sci 126:298–305

    Article  CAS  Google Scholar 

  40. Farber JL, Kyle ME, Coleman JB (1990) Biology of disease: mechanisms of cell injury by activated oxygen species. La Inves 62:670–679

    CAS  Google Scholar 

  41. Radhiga T, Rajamanickam C, Senthil S, Pugalendi KV (2012) Effect of ursolic acid on cardiac marker enzymes, lipid profile and macrosco. Food Chem Toxicol 50:3971–3977

    Article  PubMed  CAS  Google Scholar 

  42. Ogutcu A, Uzunhisarcikli M, Kalender S, Durak D, Bayrakdar F, Kalender Y (2006) The effects of organophosphate insecticide diazinon on malondialdehyde levels and myocardial cells in rat heart tissue and protective role of vitamin E. Pestic Biochem Phys 86:93–98

    Article  CAS  Google Scholar 

  43. Gan L, Liu Q, Xu HB, Zhu YS, Yang XL (2002) Effects of selenium overexposure on glutathione peroxidase and thioredoxin reductase gene expressions and activities. Biol Trace Elem Res 89:165–175

    Article  PubMed  CAS  Google Scholar 

  44. Halliwell B, Gutteridge JMC (2001) Oxidative stress: adaptation, damage, repair and death. In: Halliwell B, Gutteridge JMC (eds), Free Radic Biol Med. 3rd Ed. Oxford, UK: Oxford University Press, Oxford, pp 246–350.

  45. Jawalekar SL, Kulkarni UJ, Surve VT, Deshmukh YA (2010) Status of lipid profile, MDA and protein carbonyl in patients with cardiovascular diseases. Arch Appl Sci Res 2:8–14

    CAS  Google Scholar 

  46. Ben Amara I, Soudani N, Hakim A, Troudi A, Zeghal KH, Boudawara T, Zeghal N (2011) Protective effects of vitamin E and selenium against dimethoate-induced cardiotoxicity in vivo: biochemical and histological studies. Environ Toxicol. doi:10.1002/tox.20759

    Google Scholar 

  47. Yuan X, Tang C (1999) Lead effect on DNA and albumin in chicken blood and the protection of selenium nutrition. J Environ Sci Health 34:1875–1887

    Article  Google Scholar 

  48. Scott D, Galloway SM, Marshall RR, et al (1991) International commission for protection against environment mutagens and carcinogens. Genotoxicity under extreme culture conditions. A report from ICPEMC task Group 9. Mutat Res 257:147–204

    Article  PubMed  CAS  Google Scholar 

  49. Jawich D, Lteif R, Pfohl-Leszkowicz A, Strehaiano P (2006) Effects of penconazole on two yeast strains: growth kinetics and molecular studies. Mol Nutr Food Res 50:552–556

    Article  PubMed  CAS  Google Scholar 

  50. Cavalcantea DGSM, Martinez CBR, Sofiaa SH (2008) Genotoxic effects of Roundup® on the fish Prochilodus lineatus. Mutat Res 655:41–46

    Article  CAS  Google Scholar 

  51. Eder E, Wacker M, Lutz U, Nair J, Fang X, Bartsch H, Beland F, Schlatter J, Lutz W (2006) Oxidative stress related DNA adducts in the liver of female rats fed with sunflower-, rapeseed-, olive-or coconut oil supplemented diets. Chem Biol Interact 159:81–89

    Article  PubMed  CAS  Google Scholar 

  52. Soloneski S, González M, Piaggio E, Reigosa MA, Larramendy ML (2002) Effect of dithiocarbamate pesticide zineb and its commercial formulation azzurro. III. Genotoxic evaluation on Chinese hamster ovary (CHO) cells. Mutat Res 514:201–212

    Article  PubMed  CAS  Google Scholar 

  53. El-Bayoumy K (2001) The protective role of selenium on genetic damage and on cancer. Mutat Res 475:123–139

    Article  PubMed  CAS  Google Scholar 

  54. Kara H, Cevik A, Konar V, Dayangac A, Yilmaz M (2007) Protective effects of antioxidants against cadmium-induced oxidative damage in rat testes. Biol Trace Elem Res 120:205–211

    Article  PubMed  CAS  Google Scholar 

  55. Ananya R, Subeena S, Kumar DA, Kumar DT, Kumar MS (2005) Oxidative stress and histopathological changes in the heart following oral lindane (gamma hexachlorohexane) administration in rats. Med Sci Monit 11:325–329

    Google Scholar 

  56. Townsend DM, Tew KD, Tapiero H (2003) The importance of glutathione in human disease. Biomed Pharmacother 57:144–155

    Article  CAS  Google Scholar 

  57. Priscilla DH, Prince PSM (2009) Cardioprotective effect of gallic acid on cardiac troponin-T, cardiac marker enzymes, lipid peroxidation products and antioxidants in experimentally induced myocardial infarction in Wistar rats. Chem Biol Interact 179:118–124

    Article  PubMed  CAS  Google Scholar 

  58. May JM (2000) How does ascorbic acid prevent endothelial dysfunction? Free Radic Biol Med 28:1421–1429

    Article  PubMed  CAS  Google Scholar 

  59. Hill MF, Singal PK (1997) Right and left myocardial antioxidant responses during heart failure subsequent to myocardial infarction. Circulation 96:2414–2420

    Article  PubMed  CAS  Google Scholar 

  60. Li S, Li X, Rozanski GJ (2003) Regulation of glutathione in cardiac myocytes. J Mol Cell Cardiol 35:1145–1152

    Article  PubMed  CAS  Google Scholar 

  61. Chen Z, Young TE, Ling J, Chang SC, Gallie DR (2003) Increasing vitamin C content of plants through enhanced ascorbate recycling. Proc Natl Acad Sci U S A 100:3525–3530

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  62. Rotruck JT, Pope AL, Ganther HE, Swanson AB, Hafeman DG, Hoekstra WG (1973) Selenium: biochemical role as a component of glutathione peroxidase. Science 179:588–590

    Article  PubMed  CAS  Google Scholar 

  63. Said L, Banni M, Kerkeni A, Said K, Messaoudi I (2010) Influence of combined treatment with zinc and selenium on cadmium induced testicular pathophysiology in rat. Food Chem Toxicol 48:2759–2765

    Article  PubMed  CAS  Google Scholar 

  64. Hoover DB, Ganote CE, Ferguson SM, Blakely RD, Parsons RL (2004) Localization of cholinergic innervation in guinea pig heart by immunohistochemistry for high-affinity choline transporters. Cardiovasc Res 62:112–121

    Article  PubMed  CAS  Google Scholar 

  65. Lefkowitz RJ, Hoffman BB, Taylor P (1996) Neurotransmission: the autonomic and somatic motor nervous systems. In: Hardman JG, Limbird LL, Molinoff PB, Ruddon RW, Gilman AG (eds) Goodman and Gilman’s the pharmacological basis of therapeutics, 9th edn. McGraw-Hill, New York, pp. 105–139

    Google Scholar 

  66. Tsakiris S, Angelogianni P, Schulpis KH, Stavridis C (2000) Protective effect of L-phenylalanine on rat brain acetylcholinesterase inhibition induced by free radicals. Clin Biochem 33:103–106

    Article  PubMed  CAS  Google Scholar 

  67. Kolesárová V, Šinko G, Šiviková K, Dianovský J (2013) In vitro inhibition of blood cholinesterase activities from cattle by triazole fungicides. Int J Cytol Cytosystematics Cytogenet 66:346–350

    Google Scholar 

  68. Sies H (1993) Strategies of antioxidant defense. Eur J Biochem 215:213–219

    Article  PubMed  CAS  Google Scholar 

  69. Bas H, Kalender Y (2011) Chlorpyrifos induced cardiotoxicity in rats and the protective role of quercetin and catechin. Gazi Univ J Sci 24:387–395

    Google Scholar 

  70. Hsu YT, Wolter KG, Youle RJ (1997) Cytosol-to-membrane redistribution of Bax and Bcl-X(L) during apoptosis. Proc Natl Acad Sci U S A 94:3668–3672

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the Ministry of Higher Education and Scientific Research [UR/11ES-70], Tunisia. The authors are thankful to Mr. Chedli Tmar for the maintenance of the laboratory animals and to Mrs. Raoudha Ben Amar Abdennadher for her skillful technical assistance.

Conflict of Interest

The authors declare that they have no competing interests.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Najiba Zeghal.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chaâbane, M., Tir, M., Hamdi, S. et al. Improvement of Heart Redox States Contributes to the Beneficial Effects of Selenium Against Penconazole-Induced Cardiotoxicity in Adult Rats. Biol Trace Elem Res 169, 261–270 (2016). https://doi.org/10.1007/s12011-015-0426-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12011-015-0426-0

Keywords

Navigation