Punica granatum L. protects mice against hexavalent chromiuminduced genotoxicity

Brazilian Journal of Pharmaceutical Sciences

Volumn 49, Issue 4, 2013, Pages 689-697

  Ávila, Renato Ivan de ^a   Guerra, Meirielle Teixeira ^a   Borges, Kamilla de Almeida Souza ^a   Vieira, Marcelo de Sousa ^a   Oliveira Junior, Luiz Marcos de ^a   Furtado, Humberto ^a   Mota, Mariana Flavia da ^a   Arruda, Andréa Fernandes ^a   Valadares, Marize Campos ^a  

^a FEDERAL UNIVERSITY OF GOIÁS   (Brazil)

Author keywords

Chemoprevention; Hexavalent chromium induced genotoxicity; Oxidative damage; Pomegranate chemoprotective effects; Punica granatum chemoprotective effects; Punica granatum pharmacognosy; Punicaceae chemoprotective effects; Punicaceae pharmacognosy

Indexed keywords

ALCOHOL; CHROMIUM; HEXAVALENT CHROMIUM; POMEGRANATE EXTRACT; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW; CHEMOPROPHYLAXIS; CHROMIUM BLOOD LEVEL; CHROMIUM POISONING; CONTROLLED STUDY; ERYTHROCYTE; ERYTHROCYTE COUNT; EXPOSURE; FRUIT; GENOTOXICITY; HEAVY METAL POISONING; KIDNEY LEVEL; LIVER LEVEL; MALE; MICRONUCLEATED POLYCHROMATIC ERYTHROCYTE; MOUSE; NONHUMAN; POMEGRANATE; SURVIVAL; TISSUE LEVEL; TREATMENT DURATION;

EID: 84897422552     PISSN: 19848250     EISSN: 21759790     Source Type: Journal    
DOI: 10.1590/S1984-82502013000400008     Document Type: Article

References (64)

1. ACHARYA, U.R.; MISHRA, M.; TRIPATHY, R.R.; MISHRA, I. Testicular dysfunction and antioxidative defense system of Swiss mice after chromic acid exposure. Reprod. Toxicol., v.22, n.1, p.87-91, 2006.
2. ANDRADE, R.G.; DALVI, L.T.; SILVA, J.M.C.; LOPES, G.K.B.; ALONSO, A.; Hermes-Lima, M. The antioxidant effect of tannic acid on the in vitro copper-mediated formation of free radicals. Arch. Biochem. Biophys., v.437, n.1, p.1-9, 2005.
3. AMAROWICZ, R.; TROSZYNSKA, A.; SHAHIDI, F. Antioxidant activity of almond seed extract and its fractions. J. Food Lipids, v.12, n.4, p.344-358, 2005.
4. AQUIL, F.; AHMAD, I. Antibacterial properties of traditionally used Indian medicinal plants. Methods Find. Exp. Clin. Pharmacol., v.29, n.2, p.79-92, 2007.
5. Arreola-Mendoza, L.; REYES, J.L.; MELENDEZ, E.; MARTÍN, D.; NAMORADO, M.C.; SANCHEZ, E.; DEL RAZO, L.M. Alpha-tocopherol protects against the renal damage caused by potassium dichromate. Toxicology, v.21, n.2-3, p.237-246, 2006.
6. ASSOCIATION OF OFFICIAL ANALYTICAL CHEMISTS. Official methods of analysis of the Association Analitical Chemists. 14.ed. Washington: AOAC, 1990. 1298 p.
7. BALANSKY, R.M.; D'agostini, F.D.; Izzotti, A.; DE Flora, S. Less than additive interaction between cigarette smoke and chromium (VI) in inducing clastogenic damage in rodents. Carcinogenesis, v.21, n.9, p.1677-1682, 2000.
8. BARCELOUX, D.G. Chromium. Clin. Toxicol., v.37, n.2, p.173-194, 1999.
9. BISHAYEE, A.; BHATIA, D.; THOPPIL, R.J.; DARVESH, A.S.; NEVO, E.; LANSKY, E.P. Pomegranate-mediated chemoprevention of experimental hepatocarcinogenesis involves Nrf2-regulated antioxidant mechanisms. Carcinogenesis, v.32, n.6, p.888-896, 2011.
10. BRAGA, L.C.; LEITE, A.A.; XAVIER, K.G.; TAKAHASHI, J.A.; BEMQUERER, M.P.; Chartone-Souza, E.; Nascimento, A.M. Synergic interaction between pomegranate extract and antibiotics against Staphylococcus aureus. Can. J. Microbiol., v.51, n.7, p.541-547, 2005.
11. FARMACOPEIA BRASILEIRA. 3.ed. São Paulo: Organização Andrei, 1977. 1213 p.
12. CAYIR, K.; KARADENIZ, A.; Simşek, N.; Yildirim, S.; Karakuş, E.; Kara, A.; Akkoyun, H.T.; Sengül, E. Pomegranate seed extract attenuates chemotherapy-induced acute nephrotoxicity and hepatotoxicity in rats. J. Med. Food, v.14, n.10, p.1254-1262, 2011.
13. CERDA, B.; LLORACH, R.; CERON, J.J.; ESPIN, J.C.; Tomas-Barberan, F.A. Evaluation of the bioavailability and metabolism in the rat of punicalagin, an antioxidant polyphenol from pomegranate juice. Eur. J. Nutr., v.42, n.1, p.18-28, 2003.
14. CHANG, H.; TSAO, D.; TSENG, W. Hexavalent chromium inhibited the expression of RKIP of heart in vivo and in vitro. Toxicol. In Vitro, v.25, n.1, p.1-6, 2011.
15. CHIDAMBARA, M.K.N.; JAYAPRAKASHA, G.K.; SINGH, R.P. Studies on the antioxidant activity of pomegranate (Punica granatum) peel and seed extracts using in vivo models. J. Agric. Food. Chem., v.50, n.1, p.4791-4795, 2002.
16. CHIN, L.; LEUNG, D.W.M.; TAYLOR, H.H. Lead chelation to immobilised Symphytum officinale L. (comfrey) root tannins. Chemosphere, v.76, n.5, p.711-715, 2009.
17. CHOW, C.K. Antioxidant nutrients and environmental health: introduction. Toxicology, v.180, n.1, p.1-3, 2002.
18. COLLINS, B.J.; STOUT, M.D.; LEVINE, K.E.; KISSLING, G.E.; MELNICK, R.L.; FENNELL, T.R.; WALDEN, R.; ABDO, K.; PRITCHARD, J.B.; FERNANDO, R.A.; BURKA, L.T.; HOOTH, M.J. Exposure to hexavalent chromium resulted in significantly higher tissue chromium burden compared with trivalent chromium following similar oral doses to male F344/N rats and female B6C3F1 mice. Toxicol. Sci., v.118, n.2, p.368-379, 2010.
19. DASSPRAKASH, M.V.; ARUN, R.; ABRAHAM, S.K.; PREMKUMAR, K. In vitro and in vivo evaluation of antioxidant and antigenotoxic potential of Punica granatum leaf extract. Pharm. Biol., v.50, n.12, p.1523-1530, 2012.
20. DEB, D.D.; PARIMALA, G.; DEVI, S.S.; CHAKRABARTI, T. Role of Carum copticum seeds in modulating chromium-induced toxicity on human bronchial epithelial cells and human peripheral blood lymphocytes. Exp. Toxicol. Pathol., v.64, n.7-8, p.889-897, 2012.
21. FEN, W.; SUN, H.; KLUZ, T.; CLANCY, H.; KIOK, K.; COSTA, M. Epigallocatechin-3-gallate (EGCG) protects against chromate-induced toxicity in vitro. Toxicol. Appl. Pharmacol., v.258, n.2, p.166-175, 2012.
22. GUHA, G.; RAJKUMAR, V.; KUMAR, R.A.; MATHEW, L. Aqueous extract of Phyllanthus amarus inhibits chromium(VI)-induced toxicity in MDA-MB-435S cells. Food Chem. Toxicol., v.48, n.1, p.396-401, 2010.
23. JOHANNINGSMEIER, D.; HARRIS, G. Pomegranate as a functional food and nutraceutical source. Annu. Rev. Food. Sci. Technol., v.2, p.181-201, 2011.
24. KALAYARASAN, S.; SRIRAM, N.; SURESHKUMAR, A.; SUDHANDIRAN, G. Chromium (VI)-induced oxidative stress and apoptosis is reduced by garlic and its derivative S-allylcysteine through the activation of Nrf2 in the hepatocytes of Wistar rats. J. Appl. Toxicol., v.28, n.7, p.908-919, 2008.
25. KARAMAC, M. Chelation of Cu(II), Zn(II), and Fe(II) by tannin constituents of selected edible nuts. Int. J. Mol. Sci., v.10, n.12, p.5485-5497, 2009a.
26. KARAMAC, M. In vitro study on efficacy of tannin fractions of edible nuts as antioxidants. Eur. J. Lipids Sci. Technol., v.111, n.11, p.1063-1071, 2009b.
27. KHAN, M.R.; SIDDIQUI, S.; PARVEEN, K.; JAVED, S.; DIWAKAR, S.; SIDDIQUI, W.A. Nephroprotective action of tocotrienol-rich fraction (TRF) from palm oil against potassium dichromate (K2Cr2O7)-induced acute renal injury in rats. Chem. Biol. Interact., v.186, n.2, p.228-238, 2010.
28. LANSKY, E.P.; NEWMAN, R.A. Punica granatum (pomegranate) and its potential for prevention and treatment of inflammation and cancer. J. Ethnopharmacol., v.109, n.2, p.177-206, 2007.
29. LIU, G.; CHEN, X. Regulation of the p53 transcriptional activity. J. Cell. Biochem., v.97, n.3, p.448-458, 2006.
30. LIU, B.; CHEN, Y.; CLAIR, D.K.S. ROS and p53: versatile partnership. Free Radic. Biol. Med., v.44, n.8, p.1529-1535, 2008.
31. MACGREGOR, J.T.; HEDDLE, J.A.; HITE, M.; MARGOLIN, B.H.; RAMEL, C.; SALAMONE, M.F.; TICE, R.R.; WILD, D. Guidelines for the conduct of micronucleus assay in mammalian bone marrow erythrocytes. Mutat. Res., v.189, n.2, p.103-112, 1987.
32. MANOHARAN, K.; BANERJEE, M.R. ß-carotene reduces sister chromatid exchange induce chemical carcinogens in mouse mammary cells in organ culture. Cell Biol. Int. Rep., v.9, n.9, p.783-789, 1985.
33. MENEZES, S.M.; CORDEIRO, L.N.; VIANA, G.S. Punica granatum (pomegranate) extract is active against dental plaque. J. Herb. Pharmacother., v.6, n.2, p.79-92, 2006.
34. Molina-Jijón, E.; TAPIA, E.; ZAZUETA, C.; HAFIDI, M.E.; Zatarain-Barrón, Z.L.; Hernández-Pando, R.; Medina-Campos, O.N.; Zarco-Márquez, G.; Torres, I.; Pedraza-Chaverri, J. Curcumin prevents Cr(VI)-induced renal oxidant damage by a mitochondrial pathway. Free Radic. Biol. Med., v.51, n.8, p.1543-1557, 2011.
35. MONEIM, A.E.A.; El-Khadragy, M.F. The potential effects of pomegranate (Punica granatum) juice on carbon tetrachloride-induced nephrotoxicity in rats. J. Physiol. Biochem., v.69, n.3, p.359-370, 2012.
36. NEMR, A.E. Potential of pomegranate husk carbon for Cr(VI) removal from wastewater: kinetic and isotherm studies. J. Hazard. Mater., v.161, n.1, p.132-141, 2009.
37. NICKENS, K.P.; PATIERNO, S.R.; CERYAK, S. Chromium genotoxicity: a double-edged sword. Chem. Biol. Interact., v.188, n.2, p.276-288, 2010.
38. O'brien, T.J.; Ceryak, S.; Patierno, S.R. Complexities of chromium carcinogenesis: role of cellular response, repair and recovery mechanisms. Mutat. Res., v.533, n.1-2, p.3-36, 2003.
39. OKELLO, V.A.; MWILU, S.; NOAH, N.; ZHOU, A.; CHONG, J.; KNIPFING, M.; DOETSCHMAN, D.; SADIK, O. Reduction of hexavalent chromium using naturally-derived flavonoids. Environ. Sci. Technol., v.46, n.19, p.10743-10751, 2012.
40. OLFERT, E.D.; CROSS, B.M.; Mcwilliam, A.A. Guide to the care and use of experimental animals. 2.ed. Ottawa: Canadian Council on Animal Care, 1993. 298 p.
41. OLIVEIRA, L.P.; PINHEIRO, R.C.; VIEIRA, M.S.; PAULA, J.R.; BARA, M.T.F.; VALADARES, M.C. Cytotoxic and antiangiogenic activities of Punica granatum L., Punicaceae. Rev. Bras. Farmacogn., v.20, n.2, p.201-207, 2010.
42. OZGEN, M.; DURGAC, C.; SERC, S.; KAYA C. Chemical and antioxidant properties of pomegranate cultivars grown in the mediterranean region of Turkey. Food Chem., v.111, n.3, p.703-706, 2008.
43. Pedraza-Chaverri, J.; Yam-Canul, P.; Chirino, Y.I.; Sánchez-González, D.J.; Martínez-Martínez, C.M.; Cruz, C.; Medina-Campos, O.N. Protective effects of garlic powder against potassium dichromate-induced oxidative stress and nephrotoxicity. Food Chem. Toxicol., v.46, n.2, p.619-627, 2008.
44. Pirinccioglu, M.; Kizil, G.; Kizil, M.; Kanay, Z.; Ketani, A. The protective role of pomegranate juice against carbon tetrachloride-induced oxidative stress in rats. Toxicol. Ind. Health, DOI: 10.1177/0748233712464809, 2012.
45. PRASHANTH, D.; ASHA, M.K.; AMIT, A. Antibacterial activity of Punica granatum. Fitoterapia, v.72, n.2, p.171-173, 2001.
46. RAFAEL, A.I.; ALMEIDA, A.; SANTOS, P.; PARREIRA, I.; MADEIRA, V.M.; ALVES, R.; CABRITA, A.M.; ALPOIM, M.C. A role for transforming growth factor-beta apoptotic signaling pathway in liver injury induced by ingestion of water contaminated with high levels of Cr(VI). Toxicol. Appl. Pharmacol., v.224, n.2, p.163-173, 2007.
47. RICCI, D.; GIAMPERI, L.; BUCCHINI, A.; FRATERNALE, D. Antioxidant activity of Punica granatum fruits. Fitoterapia, v.77, n.4, p.310-312, 2006.
48. RODRIGUEZ, E.; AZEVEDO R.; FERNANDES P.; SANTOS C. Cr(VI) induces DNA damage, cell cycle arrest and polyploidization: a flow cytometric and comet assay study in Pisum sativum. Chem. Res. Toxicol., v.24, n.7, p.1040-1047, 2011.
49. RUSSO, P.; CATASSI, A.; CESARIO, A.; IMPERATORI, A.; ROTOLO, N.; FINI, M.; GRANONE, P.; DOMINIONI, L. Molecular mechanisms of hexavalent chromium-induced apoptosis in human broncoalveolar cells. Am. J. Respir. Cell Mol. Biol., v.33, n.6, p.489-600, 2005.
50. Sánchez-Lamar, A.; FONSECA, G.; FUENTES, J.L.; COZZI, R.; CUNDARI, E.; FIORE, M.; RICORDY, R.; PERTICONE, P.; DEGRASSI, F.; SALVIA, R. Assessment of the genotoxic risk of Punica granatum L. (Punicaceae) whole fruit extracts. J. Ethnopharmacol., v.115, n.3, p.416-422, 2008.
51. SEERAM, N.; AVIRAM, M.; ZHANG, Y.; HENNING, S.M.; FENG, L.; DREHER, M.; HEBER, D. Comparison of antioxidant potency of commonly consumed polyphenol-rich beverages in the United States. J. Agric. Food. Chem., v.56, n.4, p.1415-1422, 2008.
52. SHRIVASTAVA, R.; UPRETI, R.; SETH, P.; CHATURVEDI, U. Effects of chromium on the imune system. FEMS Immunol. Med. Microbiol., v.34, n.1, p.1-7, 2002.
53. SUDHEESH, S.; VIJAYALAKSHMI, N.R. Flavonoids from Punica granatum: potential antiperoxidative agents. Fitoterapia, v.76, n.2, p.181-186, 2005.
54. SUTHERLAND, J.E.; ZHITKOVICH, A.; KLUZ, T.; COSTA, M. Rats retain chromium in tissues following chronic ingestion of drinking water containing hexavalent chromium. Biol. Trace Elem. Res., v.74, n.1, p.41-53, 2000.
55. SYED, D.N.; AFAQ, F.; MUKHTAR, H. Pomegranate derived products for cancer chemoprevention. Semin. Cancer Biol., v.17, n.5, p.377-385, 2007.
56. URQUIAGA, I.; LEIGHTON, F. Plant polyphenols antioxidants and oxidative stress. Biol. Res., v.33, n.2, p.55-64, 2000.
57. VASCONCELOS, L.C.; SAMPAIO, F.C.; SAMPAIO, M.C.; PEREIRA, M.S.; HIGINO, J.S.; PEIXOTO, M.H. Minimum inhibitory concentration of adherence of Punica granatum Linn (pomegranate) gel against S. mutans, S. mitis and C. albicans. Braz. Dent. J., v.17, n.3, p.223-227, 2006.
58. VALADARES, M.C.; PEREIRA, E.R.T.; BENFICA, P.L.; PAULA, J.R. Assessment of mutagenic and antimutagenic effects of Punica granatum in mice. Braz. J. Pharm. Sci., v.46, n.1, p.121-127, 2010.
59. VALKO, M.; LEIBFRITZ, D.; MONCOL, J.; CRONIN, M.; MAZUR, M.; TELSER, J. Free radicals and antioxidants in normal physiological functions and human disease. Int. J. Biochem. Cell Biol., v.39, n.1, p.44-48, 2007.
60. WANG, R.; DING, Y.; LIU, R.; XIANG, L.; DU, L. Pomegranate: constituents, bioactivities and pharmacokinetics. Fruit, Veg. Cereal Sci. Biotech., v.4, n.2, p.77-87, 2010.
61. WU, F.; SUN, H.; KLUZ, T.; CLANCY, H.A.; KIOK, K.; COSTA, M. Epigallocatechin-3-gallate (EGCG) protects against chromate-induced toxicity in vitro. Toxicol. Appl. Pharmacol., v.258, n.2, p.166-175, 2012.
62. YAN, M.; WANG, X.; ZHU, X. Mitochondrial defects and oxidative stress in Alzheimer disease and Parkinson disease. Free Radic. Biol. Med., v.62, p.30-101, 2012.
63. YE, J.; LEONARD, S.S.; SUN, Y.; BUTTERWORTH, L.; ANTONINI, J.; DING, M.; ROJANASAKUL, Y.; VALLYATHAN, V.; CASTRANOVA, V.; SHI, X. Role of reactive oxygen species and p53 in chromium (VI)-induced apoptosis. J. Biol. Chem., v.274, n.49, p.34974-34980, 1999.
64. ZAGRODZKI, P.; Debecki, L.; Radkowski, A.; Bartoń, H.; Fołta, M.; Wójcik, E.; KULPA, J. Association of occupational exposure to chromium with tumour markers and selected biochemical parameters. Pol. J. Environ. Stud., v.16, n.2, p.275-281, 2007.