Protective effects of Salvia officinalis extract against cyclophosphamide-induced genotoxicity and oxidative stress in rats

Turkish Journal of Veterinary and Animal Sciences

Volumn 36, Issue 6, 2012, Pages 646-654

  Üstün Alkan, Fulya ^a   Esen Gürsel, Feraye ^a   Ateş, Atila ^a   Özyürek, Mustafa ^a   Güçlü, Kubilay ^a   Altun, Mehmet ^a  

^a ISTANBUL UNIVERSITY   (Turkey)

Author keywords

Antioxidant capacity; Cyclophosphamide; Micronucleus; Oxidative stress; Salvia officinalis

Indexed keywords

ANIMALIA; RATTUS; SALVIA OFFICINALIS;

EID: 84871596920     PISSN: 13000128     EISSN: 13036181     Source Type: Journal    
DOI: 10.3906/vet-1105-36     Document Type: Article

References (63)

1. Withrow, S.J., MacEwen, E.G. Small Animal Clinical Oncology. 3rd edn., W.B. Saunders, Philadelphia, Pennsylvania, USA. 2001.
2. Kopecna, L. Late effects of anticancer therapy on kidney function in children with acute lymphoblastic leukemia. Bratisl. Lek. Listy., 2001; 102: 357-360.
3. Gustafsson, L.L, Eriksson, L.S., Dahl, M.L., Eleborg, L., Ericzon, B.G., Nyberg, A. Cyclophosphamide-induced acute liver failure requiring transplantation in a patient with genetically deficient debrisoquine metabolism: a causal relationship? J. Intern. Med., 1996; 240: 311-314.
4. Hales, B.F. Comparison of the mutagenicity and teratogenicity of cyclophosphamide and its active metabolites, 4-hydroxycyclophosphamide, phosphoramide mustard, and acrolein. Cancer Res., 1982; 42: 3016-3021.
5. Madle, E., Korte, A., Beek, B. Species differences in mutagenicity testing. II. Sister-chromatid exchange and micronucleus induction in rats, mice and Chinese hamsters treated with cyclophosphamide. Mutagenesis, 1986; 1: 419- 422.
6. Moore, F.R., Urda, G.A., Krishna, G., Theiss, J.C. An in vivo/in vitro method for assessing micronucleus and chromosome aberration induction in rat bone marrow and spleen. 1. Studies with cyclophosphamide. Mutat. Res., 1995; 335: 191-199.
7. Manda, K., Bhatia, A.L. Prophylactic action of melatonin against cyclophosphamide-induced oxidative stress in mice. Cell Biol. Toxicol., 2003; 19: 367-372.
8. Li, M., Zhu, Q., Hu, C., Giesy, J.P., Kong, Z., Cui, Y. Protective effects of eicosapentaenoic acid on genotoxicity and oxidative stress of cyclophosphamide in mice. Environ. Toxicol., 2011; 26: 217-223.
9. Oboh, G., Henle, T. Antioxidant and inhibitory effects of aqueous extracts of Salvia officinalis leaves on pro-oxidantinduced lipid peroxidation in brain and liver in vitro. J. Med. Food, 2009; 12: 77-84.
10. Todorova, V., Vanderpool, D., Blossom, S., Nwokedi, E., Hennings, L., Mrak, R., Klimberg, V.S. Oral glutamine protects against cyclophosphamide-induced cardiotoxicity in experimental rats through increase of cardiac glutathione. Nutrition, 2009; 25: 812-817.
11. Grzegorczyk, I., Matkowski, A., Wysokinska, H. Antioxidant activity of extracts from in vitro cultures of Salvia officinalis L. Food Chem., 2007; 104: 536-541.
12. Subapriya, R., Kumaragurupan, R., Abraham, S.K., Nagini, S. Protective effects of ethanolic neem leaf extract on N-methyl-N'-nitro-N-nitrosoguanidine-induced genotoxicity and oxidative stress in mice. Drug Chem. Toxicol., 2004; 27: 15-26.
13. Weisburger, J.H. Antimutagenesis and anticarcinogenesis, from the past to the future. Mutat. Res., 2001; 480-481: 23-35.
14. Gurib-Fakim, A. Medicinal plants: traditions of yesterday and drugs of tomorrow. Mol. Aspects Med., 2006; 27: 1-93.
15. Hedge, I.C. Flora of Turkey and the East Aegean Islands. Edinburgh University Press, Edinburgh. 1982.
16. Mitić-Ćulafić, D., Vuković-Gačić, B., Knežević-Vukčević, J., Stanković, S., Simić, D. Comparative study on the antibacterial activity of volatiles from sage (Salvia officinalis L.). Arch. Biol. Sci., 2005; 57: 173-178.
17. Longaray, A.P.D., Moschen-Pistorello, I.T., Artico, L., Atti-Serafini, L., Echeverrigaray, S. Antibacterial activity of the essential oils of Salvia officinalis L. and Salvia triloba L. cultivated in South Brazil. Food Chem., 2007; 100: 603-608.
18. Šmidling, D., Mitić-Ćulafić, D., Vuković-Gačić, B., Simić, D., Knežević-Vukčević, J. Evaluation of antiviral activity of fractionated extracts of sage Salvia officinalis L. Arch. Biol. Sci., 2008; 60: 421-429.
19. Baricevic, D., Sosa, S., Della, L.R., Tubaro, A., Simonovska, B., Krasna, A., Zupancic, A. Topical anti-infl ammatory activity of Salvia officinalis L. leaves: the relevance of ursalic acid. J. Ethnopharmacol., 2001; 75: 125-132.
20. Eidi, M., Eidi, A., Zamanizadeh, H. Effect of Salvia officinalis L. leaves on serum glucose and insulin in healthy and streptozotocin-induced diabetic rats. J. Ethnopharmacol., 2005; 100: 310-313.
21. Bouaziz, M., Yangui, T., Sayadi, S., Dhouib, A. Disinfectant properties of essential oils from Salvia officinalis L. cultivated in Tunisia. Food Chem. Toxicol., 2009; 47: 2755- 2760.
22. Vuković-Gačić, B., Nikčević, S., Berić-Bjedov, T., Knežević-Vukčević, J., Simić, D. Antimutagenic effect of essential oil of sage (Salvia officinalis L.) and its monoterpenes against UV-induced mutations in Escherichia coli and Saccharomyces cerevisiae. Food Chem. Toxicol., 2006; 44: 1730-1738.
23. Xavier, C.P, Lima, C.F, Fernandes-Ferreira, M., Pereira-Wilson, C. Salvia fruticosa, Salvia officinalis, and rosmarinic acid induce apoptosis and inhibit proliferation of human colorectal cell lines: the role in MAPK/ERK pathway. Nutr. Cancer, 2009; 61: 564-571.
24. Zupko, I., Hohmann, J., Redei, D., Falkay, G., Janicsak, G., Mathe, I. Antioxidant activity of leaves of Salvia species in enzyme-dependent and enzyme-independent systems of lipid peroxidation and their phenolic constituents. Planta Med., 2001; 97: 383-389.
25. Cuvelier, M.E., Berset, C., Richard, H. Antioxidant constituents in sage (Salvia officinalis). J. Agr. Food Chem., 1994; 42: 665-669.
26. Lima, C.F., Carvalho, F., Fernandes, E., Bastos, M.L., Santos-Gomes, P.C., Fernandes-Ferreira, M., Pereira-Wilson, C. Evaluation of toxic/protective effects of the essential oil of Salvia officinalis on freshly isolated rat hepatocytes. Toxicol. in Vitro, 2004; 18: 457-465.
27. Lu, Y., Foo, L.Y. Antioxidant activities of polyphenols from sage (Salvia officinalis). Food Chem., 2001; 75: 197-202.
28. Then, M., Lemberkovics, E., Marczal, G., Szentmihályi, K., Szöke, E.: Plant anatomical and phytochemical evaluation of Salvia species. Acta Pharm. Hung., 1998; 68: 163-174.
29. Capek, P., Machová, E., Turjan, J. Scavenging and antioxidant activities of immunomodulating polysaccharides isolated from Salvia officinalis L. Int. J. Biol. Macromol., 2009; 44: 75-80.
30. Lima, C.F., Valentao, P.C., Andrade, P.B., Seabra, R.M., Fernandes-Ferreira, M., Pereira-Wilson, C. Water and methanolic extracts of Salvia officinalis protect HepG2 cells from t-BHP induced oxidative damage. Chem. Biol. Interact., 2007; 167: 107-115.
31. Krishna, G., Kropko, M.L., Ciaravino, V., Theiss, J.C. Simultaneous micronucleus and chromosome aberration assessment in the rat. Mutat. Res., 1991; 264: 29-35.
32. Özyürek, M., Bektaşoǧlu, B., Güçlü, K., Güngör, N., Apak, R. Simultaneous total antioxidant capacity assay of lipophilic and hydrophilic antioxidants in the same acetone-water solution containing 2% methyl-β-cyclodextrin using the cupric reducing antioxidant capacity (CUPRAC) method. Anal. Chim. Acta, 2008; 630: 28-39.
33. Dweck, C.A. The folklore and cosmetic use of various Salvia species.. In: Kintzios, S.E., Ed. Sage: The Genus Salvia. Harwood Academic Publishers, Amsterdam. 2000; 1-25.
34. Schmid, W. The micronucleus test. Mutat. Res., 1975; 31: 9-15.
35. MacGregor, T.J., Heddle, A.J., Hite, M., Margolin, H.B., Ramel, C., Salamone, F.M. Guidelines for the conduct of micronucleus assays in mammalian bone marrow erythrocytes. Mutat. Res., 1987; 189: 103-112.
36. Yoshoiko, T., Kawada, K., Shimada, T. Lipid peroxidation in maternal and cord blood and protective mechanism against active-oxygen toxicity in the blood. Am. J. Obstet. Gynecol., 1979; 135: 372-376.
37. Sun, Y., Oberley, L.W., Li, Y. A simple method for clinical assay of superoxide dismutase. Clin. Chem., 1988; 34: 497- 500.
38. Durak, I., Yurtarslani, Z., Canbolat, O., Akyol, O. A methodological approach to superoxide dismutase (SOD) activity assay based on inhibition of nitroblue tetrazolium (NBT) reduction. Clin. Chim. Acta, 1993; 31: 103-104.
39. Aebi, H. Catalase. In: Bergmeyer, H.U., Ed. Methods in Enzymatic Analysis. Academic Press, New York. 1983; 276-286.
40. Lowry, O.H, Rosebrough, N.J., Farr, A.L. Protein measurement with the Folin phenol reagent. J. Biol. Chem., 1951; 193: 265-275.
41. Apak, R., Güçlü, K., Özyürek, M., Karademir, S.E. Novel total antioxidant capacity index for dietary polyphenols and vitamins C and E, using their cupric ion reducing capability in the presence of neocuproine: CUPRAC method. J. Agric. Food Chem., 2004; 52: 7970-7981.
42. Elhajouji, A., Santos, A.P., Van Hummelen, P., Kirsch-Volders, M. Metabolic differences between whole blood and isolated lymphocyte cultures for micronucleus (MN) induction by cyclophosphamide and benzo[a]pyrene. Mutagenesis, 1994; 9: 307-313.
43. Sorsa, M., Pyy, L., Salomaa, S., Nylund, L., Yager, J.W. Biological and environmental monitoring of occupational exposure to cyclophosphamide in industry and hospitals. Mutat. Res., 1988; 204: 465-479.
44. Crook, T.R., Souhami, R.L., McLean, A.E. Cytotoxicity, DNA cross-linking, and single strand breaks induced by activated cyclophosphamide and acrolein in human leukemia cells. Cancer Res., 1986; 46: 5029-5034.
45. Bryce, S.M., Shi, J., Nicolette, J., Diehl, M., Sonders, P., Avlasevich, S., Raja, S., Bemis, J.C., Dertinger, S.D. High content flow cytometric micronucleus scoring method is applicable to attachment cell lines. Environ. Mol. Mutagen., 2010; 51: 260-266.
46. Tripathi, D.N., Jena, G.B. Intervention of astaxanthin against cyclophosphamide-induced oxidative stress and DNA damage: a study in mice. Chem. Biol. Interact., 2009; 180: 398-406.
47. Patel, J.M., Block, E.R. Cyclophosphamide-induced depression of the antioxidant defense mechanisms of the lung. Exp. Lung Res., 1985; 8: 153-165.
48. Zhang, Q.H., Wu, C.F., Duan, L., Yang, J.Y. Protective effects of ginsenoside Rg3 against cyclophosphamideinduced DNA damage and cell apoptosis in mice. Arch. Toxicol., 2008; 82: 117-123.
49. Aardema, M.J., Kirsch-Volders, M. The in vitro micronucleus assay. In: Choy, W.N., Ed. Genetic Toxicology and Cancer Risk Assessment. Informa Healthcare, New York. 2001; 163-186.
50. Hayashi, M., Tice, R.R., MacGregor, J.T., Anderson, D., Blakey, D.H., Kirsh-Volders, M., Oleson, F.B., Pacchierotti, F., Romagna, F., Shimada, H., Sutou, S., Vannier, B. In vivo rodent erythrocyte micronucleus assay. Mutat. Res., 1994; 312: 293-304.
51. Suzuki, Y., Nagae, Y., Li, J., Sakaba, H., Mozawa, K., Takahashi, A., Shimizu, H. The micronucleus test and erythropoiesis. Effects of erythropoietin and a mutagen on the ratio of polychromatic to normochromatic erythrocytes (P/N ratio). Mutagenesis, 1989; 4: 420-424.
52. Chandrasekar, M.J.N., Bommu, P., Nanjan, M.J., Suresh, B. Chemoprotective effect of Phyllanthus maderaspatensis in modulating cisplatin-induced nephrotoxicity and genotoxicity. Pharm. Biol., 2006; 44: 100-106.
53. SivaKumar, V., Niranjali Devaraj, S. Protective effect of Plumbago zeylanica against cyclophosphamide-induced genotoxicity and oxidative stress in Swiss albino mice. Drug Chem. Toxicol., 2006; 29: 279-288.
54. El-Ashmawy1, I.M., El-Nahas, A.F., Salama, O.M. Grape seed extract prevents gentamicin-induced nephrotoxicity and genotoxicity in bone marrow cells of mice. Basic Clin. Pharmacol., 2006; 99: 230-236.
55. Jahangir, T., Khan, T.H., Prasad, L., Sultana, S. Alleviation of free radical mediated oxidative and genotoxic effects of cadmium by farnesol in Swiss albino mice. Redox Rep., 2005; 10: 303-310.
56. Kehrer, J.P. Free radicals as mediators of tissue injury and disease. Crit. Rev. Toxicol., 1993; 23: 21-48.
57. Selvakumar, E., Prahalathan, C., Mythili, Y., Varalakshmi, P. Protective effect of DL-α-lipoic acid in cyclophosphamide induced oxidative injury in rat testis. Reprod. Toxicol., 2004; 19: 163-167.
58. Lin, H.M., Yen, F.L., Ng, L.T., Lin, C.C. Protective effects of Ligustrum lucidum fruit extract on acute butylated hydroxytoluene-induced oxidative stress in rats. J. Ethnopharmacol., 2007; 111: 129-136.
59. Senthilkumar, S., Yogeeta, S.K., Subashini, R., Devaki, T. Attenuation of cyclophosphamide induced toxicity by squalene in experimental rats. Chem-Biol. Interact., 2006; 160: 252-260.
60. Premkumar, K., Abraham, S.K., Santhiya, S.T., Ramesh, A. Protective effect of Spirulina fusiformis on chemicalinduced genotoxicity in mice. Fitoterapia, 2004; 75: 24-31.
61. Santos-Gomes, P.C., Seabra, R.M., Andrade, P.B., Fernandes-Ferreira, M. Phenolic antioxidant compounds produced by in vitro shoots of sage (Salvia officinalis L.). Plant Sci., 2002; 162: 981-987.
62. Roman, G.P., Neagu, E., Radu, G.L. Antiradical activities of Salvia officinalis and Viscum album L. extracts concentrated by ultrafi ltration process. Acta Sci. Pol. Technol. Aliment., 2009; 8: 47-58.
63. Patenkovic, A., Stamenkovic-Radak, M., Banjanac, T., Andjelkovic, M. Antimutagenic effect of sage tea in the wing spot test of Drosophila melanogaster. Food Chem. Tox., 2009; 47: 180-183.