Biological Trace Element Research

, Volume 150, Issue 1–3, pp 328–336 | Cite as

Evaluating the Potential Role of Pomegranate Peel in Aluminum-Induced Oxidative Stress and Histopathological Alterations in Brain of Female Rats

Article

Abstract

Studies have shown that pomegranate, Punica granatum Linn. (Lythraceae), has remarkable biological and medicinal properties. However, the effects of pomegranate peel methanolic extract (PPME) on the aluminum-induced oxidative stress and histopathological change have not been reported yet. To determine the effect of PPME (200 mg/kg bwt) on the aluminum chloride (AlCl3; 34 mg/kg bwt)-induced neurotoxicity, aluminum accumulation in brain and oxidant/antioxidant status were determined. The change of brain structure was investigated with hematoxylin and eosin, and anti-apoptosis effects of PPME were analyzed by immunohistochemistry. The present study showed an indication of carcinogenicity in the AlCl3-treated group representing an increase in tissue tumor markers such as tumor necrosis factor-α and angiogenin and inflammation by inducing an increase in prostaglandin E2 and prostaglandin F2α. PPME protected brain through decreasing the aluminum accumulation and stimulating antioxidant activities and anti-apoptotic proteins namely Bcl-2. Therefore, these results indicated that pomegranate peel methanolic extract could inhibit aluminum-induced oxidative stress and histopathological alternations in brain of female rats, and these effects may be related to anti-apoptotic and antioxidants activities.

Keywords

Aluminum chloride Pomegranate peel Oxidant/antioxidant status Anti-apoptosis Brain Rats 

References

  1. 1.
    Verstraeten SV, Aimo L, Oteiza PI (2008) Aluminium and lead: molecular mechanisms of brain toxicity. Arch Toxicol 82(11):789–802PubMedCrossRefGoogle Scholar
  2. 2.
    Kumar V, Gill KD (2009) Aluminium neurotoxicity: neurobehavioural and oxidative aspects. Arch Toxicol 83(11):965–978PubMedCrossRefGoogle Scholar
  3. 3.
    Ribes D, Colomina MT, Vicens P, Domingo JL (2008) Effects of oral aluminum exposure on behavior and neurogenesis in a transgenic mouse model of Alzheimer’s disease. Exp Neurol 214(2):293–300PubMedCrossRefGoogle Scholar
  4. 4.
    Shati AA, Elsaid FG, Hafez EE (2011) Biochemical and molecular aspects of aluminium chloride-induced neurotoxicity in mice and the protective role of Crocus sativus L. extraction and honey syrup. Neuroscience 175:66–74PubMedCrossRefGoogle Scholar
  5. 5.
    Saiyed SM, Yokel RA (2005) Aluminium content of some foods and food products in the USA, with aluminium food additives. Food Addit Contam 22(3):234–244PubMedCrossRefGoogle Scholar
  6. 6.
    Turkez H, Yousef MI, Geyikoglu F (2010) Propolis prevents aluminium-induced genetic and hepatic damages in rat liver. Food Chem Toxicol 48(10):2741–2746PubMedCrossRefGoogle Scholar
  7. 7.
    Sanchez-Iglesias S, Soto-Otero R, Iglesias-Gonzalez J, Barciela-Alonso MC, Bermejo-Barrera P, Mendez-Alvarez E (2007) Analysis of brain regional distribution of aluminium in rats via oral and intraperitoneal administration. J Trace Elem Med Biol 21(Suppl 1):31–34PubMedCrossRefGoogle Scholar
  8. 8.
    Bhadauria M (2012) Combined treatment of HEDTA and propolis prevents aluminum induced toxicity in rats. Food Chem Toxicol 50(7):2487–2495PubMedCrossRefGoogle Scholar
  9. 9.
    Nehru B, Bhalla P (2006) Reversal of an aluminium induced alteration in redox status in different regions of rat brain by administration of centrophenoxine. Mol Cell Biochem 290(1–2):185–191PubMedCrossRefGoogle Scholar
  10. 10.
    Sharma D, Sethi P, Hussain E, Singh R (2009) Curcumin counteracts the aluminium-induced ageing-related alterations in oxidative stress, Na+, K + ATPase and protein kinase C in adult and old rat brain regions. Biogerontology 10(4):489–502PubMedCrossRefGoogle Scholar
  11. 11.
    González M, Bernal C, Mahieu S, Carrillo M (2009) The interactions between the chronic exposure to aluminum and liver regeneration on bile flow and organic anion transport in rats. Biol Trace Elem Res 127(2):164–176PubMedCrossRefGoogle Scholar
  12. 12.
    El-Sayed WM, Al-Kahtani MA, Abdel-Moneim AM (2011) Prophylactic and therapeutic effects of taurine against aluminum-induced acute hepatotoxicity in mice. J Hazard Mater 192(2):880–886PubMedCrossRefGoogle Scholar
  13. 13.
    Abdel Moneim AE, Dkhil MA, Al-Quraishy S (2011) Effects of flaxseed oil on lead acetate-induced neurotoxicity in rats. Biol Trace Elem Res 144(1–3):904–913PubMedCrossRefGoogle Scholar
  14. 14.
    de Nigris F, Balestrieri ML, Williams-Ignarro S, D’Armiento FP, Fiorito C, Ignarro LJ, Napoli C (2007) The influence of pomegranate fruit extract in comparison to regular pomegranate juice and seed oil on nitric oxide and arterial function in obese Zucker rats. Nitric Oxide 17(1):50–54PubMedCrossRefGoogle Scholar
  15. 15.
    Ricci D, Giamperi L, Bucchini A, Fraternale D (2006) Antioxidant activity of Punica granatum fruits. Fitoterapia 77(4):310–312PubMedCrossRefGoogle Scholar
  16. 16.
    Faria A, Calhau C, de Freitas V, Mateus N (2006) Procyanidins as antioxidants and tumor cell growth modulators. J Agric Food Chem 54(6):2392–2397PubMedCrossRefGoogle Scholar
  17. 17.
    Abdel Moneim A (2012) Antioxidant activities of Punica granatum (pomegranate) peel extract on brain of rats. J Med Plants Res 6(2):195–199Google Scholar
  18. 18.
    Yousef MI, Salama AF (2009) Propolis protection from reproductive toxicity caused by aluminium chloride in male rats. Food Chem Toxicol 47(6):1168–1175PubMedCrossRefGoogle Scholar
  19. 19.
    Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95(2):351–358PubMedCrossRefGoogle Scholar
  20. 20.
    Berkels R, Purol-Schnabel S, Roesen R (2004) Measurement of nitric oxide by reconversion of nitrate/nitrite to NO. Methods Mol Biol 279:1–8PubMedGoogle Scholar
  21. 21.
    Ellman GL (1959) Tissue sulfhydryl groups. Arch Biochem Biophys 82(1):70–77PubMedCrossRefGoogle Scholar
  22. 22.
    Nishikimi M, Appaji N, Yagi K (1972) The occurrence of superoxide anion in the reaction of reduced phenazine methosulfate and molecular oxygen. Biochem Biophys Res Commun 46(2):849–854PubMedCrossRefGoogle Scholar
  23. 23.
    Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126PubMedCrossRefGoogle Scholar
  24. 24.
    Paglia DE, Valentine WN (1967) Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med 70(1):158–169PubMedGoogle Scholar
  25. 25.
    Factor VM, Kiss A, Woitach JT, Wirth PJ, Thorgeirsson SS (1998) Disruption of redox homeostasis in the transforming growth factor-alpha/c-myc transgenic mouse model of accelerated hepatocarcinogenesis. J Biol Chem 273(25):15846–15853PubMedCrossRefGoogle Scholar
  26. 26.
    Jamshidzadeh A, Baghban M, Azarpira N, Mohammadi Bardbori A, Niknahad H (2008) Effects of tomato extract on oxidative stress induced toxicity in different organs of rats. Food Chem Toxicol 46(12):3612–3615PubMedCrossRefGoogle Scholar
  27. 27.
    Ishak K, Baptista A, Bianchi L, Callea F, De Groote J, Gudat F, Denk H, Desmet V, Korb G, MacSween RN et al (1995) Histological grading and staging of chronic hepatitis. J Hepatol 22(6):696–699PubMedCrossRefGoogle Scholar
  28. 28.
    Ohyashiki T, Karino T, Suzuki S, Matsui K (1996) Effect of aluminum ion on Fe(2+)-induced lipid peroxidation in phospholipid liposomes under acidic conditions. J Biochem 120(5):895–900PubMedCrossRefGoogle Scholar
  29. 29.
    Yousef MI (2004) Aluminium-induced changes in hemato-biochemical parameters, lipid peroxidation and enzyme activities of male rabbits: protective role of ascorbic acid. Toxicology 199(1):47–57PubMedCrossRefGoogle Scholar
  30. 30.
    Yousef MI, El-Morsy AM, Hassan MS (2005) Aluminium-induced deterioration in reproductive performance and seminal plasma biochemistry of male rabbits: protective role of ascorbic acid. Toxicology 215(1–2):97–107PubMedCrossRefGoogle Scholar
  31. 31.
    Flora SJ, Mehta A, Satsangi K, Kannan GM, Gupta M (2003) Aluminum-induced oxidative stress in rat brain: response to combined administration of citric acid and HEDTA. Comp Biochem Physiol C Toxicol Pharmacol 134(3):319–328PubMedCrossRefGoogle Scholar
  32. 32.
    Abdel Moneim AE, Dkhil M, Al-Quraishy S (2011) The redox status in rats treated with flaxseed oil and lead-induced hepatotoxicity. Biol Trace Elem Res 143(1):457–467PubMedCrossRefGoogle Scholar
  33. 33.
    Nehru B, Anand P (2005) Oxidative damage following chronic aluminium exposure in adult and pup rat brains. J Trace Elem Med Biol 19(2–3):203–208PubMedCrossRefGoogle Scholar
  34. 34.
    Negi PS, Jayaprakasha GK, Jena BS (2003) Antioxidant and antimutagenic activities of pomegranate peel extracts. Food Chem 80(3):393–397CrossRefGoogle Scholar
  35. 35.
    Singh RP, Chidambara Murthy KN, Jayaprakasha GK (2001) Studies on the antioxidant activity of pomegranate (Punica granatum) peel and seed extracts using in vitro models. J Agric Food Chem 50(1):81–86CrossRefGoogle Scholar
  36. 36.
    Yokel RA (2002) Aluminum chelation principles and recent advances. Coord Chem Rev 228(2):97–113CrossRefGoogle Scholar
  37. 37.
    Mahieu S, Contini Mdel C, Gonzalez M, Millen N (2009) Melatonin reduces oxidative damage induced by aluminium in rat kidney. Toxicol Lett 190(1):9–15PubMedCrossRefGoogle Scholar
  38. 38.
    Becaria A, Bondy SC, Campbell A (2003) Aluminum and copper interact in the promotion of oxidative but not inflammatory events: implications for Alzheimer’s disease. J Alzheimers Dis 5(1):31–38PubMedGoogle Scholar
  39. 39.
    Ghribi O, DeWitt DA, Forbes MS, Herman MM, Savory J (2001) Co-involvement of mitochondria and endoplasmic reticulum in regulation of apoptosis: changes in cytochrome c, Bcl-2 and Bax in the hippocampus of aluminum-treated rabbits. Brain Res 903(1–2):66–73PubMedCrossRefGoogle Scholar
  40. 40.
    Colak S, Geyikoglu F, Keles ON, Turkez H, Topal A, Unal B (2011) The neuroprotective role of boric acid on aluminum chloride-induced neurotoxicity. Toxicol Ind Health 27(8):700–710PubMedCrossRefGoogle Scholar
  41. 41.
    Morgan MJ, Kim Y-S, Z-g L (2008) TNF[alpha] and reactive oxygen species in necrotic cell death. Cell Res 18(3):343–349PubMedCrossRefGoogle Scholar
  42. 42.
    Consilvio C, Vincent AM, Feldman EL (2004) Neuroinflammation, COX-2, and ALS–a dual role? Exp Neurol 187(1):1–10PubMedCrossRefGoogle Scholar
  43. 43.
    Takadera T, Yumoto H, Tozuka Y, Ohyashiki T (2002) Prostaglandin E(2) induces caspase-dependent apoptosis in rat cortical cells. Neurosci Lett 317(2):61–64PubMedCrossRefGoogle Scholar
  44. 44.
    Weiner HL, Weiner LH, Swain JL (1987) Tissue distribution and developmental expression of the messenger RNA encoding angiogenin. Science 237(4812):280–282PubMedCrossRefGoogle Scholar
  45. 45.
    Maihofner C, Charalambous MP, Bhambra U, Lightfoot T, Geisslinger G, Gooderham NJ (2003) Expression of cyclooxygenase-2 parallels expression of interleukin-1beta, interleukin-6 and NF-kappaB in human colorectal cancer. Carcinogenesis 24(4):665–671PubMedCrossRefGoogle Scholar
  46. 46.
    Adams LS, Seeram NP, Aggarwal BB, Takada Y, Sand D, Heber D (2006) Pomegranate juice, total pomegranate ellagitannins, and punicalagin suppress inflammatory cell signaling in colon cancer cells. J Agric Food Chem 54(3):980–985PubMedCrossRefGoogle Scholar
  47. 47.
    Aslam MN, Lansky EP, Varani J (2006) Pomegranate as a cosmeceutical source: pomegranate fractions promote proliferation and procollagen synthesis and inhibit matrix metalloproteinase-1 production in human skin cells. J Ethnopharmacol 103(3):311–318PubMedCrossRefGoogle Scholar
  48. 48.
    Rasheed Z, Akhtar N, Anbazhagan AN, Ramamurthy S, Shukla M, Haqqi TM (2009) Polyphenol-rich pomegranate fruit extract (POMx) suppresses PMACI-induced expression of pro-inflammatory cytokines by inhibiting the activation of MAP Kinases and NF-kappaB in human KU812 cells. J Inflamm (Lond) 6:1CrossRefGoogle Scholar
  49. 49.
    Larrosa M, Gonzalez-Sarrias A, Yanez-Gascon MJ, Selma MV, Azorin-Ortuno M, Toti S, Tomas-Barberan F, Dolara P, Espin JC (2010) Anti-inflammatory properties of a pomegranate extract and its metabolite urolithin-A in a colitis rat model and the effect of colon inflammation on phenolic metabolism. J Nutr Biochem 21(8):717–725PubMedCrossRefGoogle Scholar
  50. 50.
    Faria A, Calhau C (2011) The bioactivity of pomegranate: impact on health and disease. Crit Rev Food Sci 51(7):626–634CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  1. 1.Biomedical Research Center, Health Sciences Technology ParkUniversity of GranadaGranadaSpain
  2. 2.Department of Zoology and Entomology, Faculty of ScienceHelwan UniversityCairoEgypt

Personalised recommendations