Alleviation of doxorubicin-induced toxicities by anthocyanin-rich bilberry (Vaccinium myrtillus L.) extract in rats and mice

BioFactors

Volumn 36, Issue 4, 2010, Pages 319-327

  Choi, Eun Hye ^a   Park, Jae Hwan ^a   Kim, Mi Kyung ^b   Chun, Hyang Sook ^a  

^a Korea Food Research Institute   (South Korea)

^b Ewha Womans University   (South Korea)

Author keywords

Anthocyanin; Bilberry; Doxorubicin; Oxidative stress; Toxicity

Indexed keywords

ALANINE AMINOTRANSFERASE; ANTIOXIDANT; ASPARTATE AMINOTRANSFERASE; CREATINE KINASE; DOXORUBICIN; GLUTATHIONE; HEMOGLOBIN; VACCINIUM MYRTILLUS ANTHOCYANOSIDE; VACCINIUM MYRTILLUS EXTRACT;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; ASCITES; ASPARTATE AMINOTRANSFERASE BLOOD LEVEL; BONE MARROW CELL; BONE MARROW TOXICITY; CARDIOTOXICITY; CELL COUNT; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DIET SUPPLEMENTATION; ENZYME ACTIVITY; ERYTHROCYTE; HEART INFARCTION; HISTOPATHOLOGY; LEUKOCYTE; LIPID PEROXIDATION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; RAT; SPRAGUE DAWLEY RAT; VACCINIUM MYRTILLUS; WEIGHT REDUCTION;

ANIMALS; ANTHOCYANINS; DOXORUBICIN; HEART; LIPID PEROXIDATION; MALE; MICE; MICE, INBRED C57BL; RATS; RATS, SPRAGUE-DAWLEY;

MUS; RATTUS; VACCINIUM MYRTILLUS;

EID: 78149481647     PISSN: 09516433     EISSN: 18728081     Source Type: Journal    
DOI: 10.1002/biof.106     Document Type: Article

References (57)

1. Minotti, G., Menna, P., Salvatorelli, E., Cairo, G., and Gianni, L. (2004) Anthracyclines: molecular advances and pharmacologic developments in antitumor activity and cardiotoxicity. Pharmacol. Rev. 56, 185-229.
2. Weiss, R. B. (1992) The anthracyclines: will we ever find a better doxorubicin? Semin. Oncol. 19, 670-686.
3. Blum, R. H. and Carter, S. K. (1974) Adriamycin. A new anticancer drug with significant clinical activity. Ann. Intern. Med. 80, 249-259.
4. Von Hoff, D. D., Layard, M. W., Basa, P., Davis, H. L. Jr., Von Hoff, A. L., Rozencweig, M., and Muggia, F. M. (1979) Risk factors for doxorubicin-induced congestive heart failure. Ann. Intern. Med. 91, 710-717.
5. Doroshow, J. H. (1991) Doxorubicin-induced cardiac toxicity. N. Engl. J. Med. 324, 843-845.
6. Singal, P. K. and Iliskovic, N. (1998) Doxorubicin-induced cardiomyopathy. N. Engl. J. Med. 339, 900-905.
7. Minotti, G., Cairo, G., and Monti, E. (1999) Role of iron in anthracycline cardiotoxicity: new tunes for an old song? FASEB J. 13, 199-212.
8. Goodman, J. and Hochstein, P. (1977) Generation of free radicals and lipid peroxidation by redox cycling of adriamycin and daunomycin. Biochem. Biophys. Res. Commun. 77, 797-803.
9. Gille, L. and Nohl, H. (1997) Analyses of the molecular mechanism of adriamycin-induced cardiotoxicity. Free Radic. Biol. Med. 23, 775-782.
10. Simunek, T., Sterba, M., Popelova, O., Adamcova, M., Hrdina, R., and Gersl, V. (2009) Anthracycline-induced cardiotoxicity: overview of studies examining the roles of oxidative stress and free cellular iron. Pharmacol. Rep. 61, 154-171.
11. Granados-Principal, S., Quiles, J., Ramirez-Tortosa, C., Sanchez-Rovira, P., and Ramirez-Tortosa, M. (2010) New advances in molecular mechanisms and the prevention of adriamycin toxicity by antioxidant nutrients. Food Chem. Toxicol. 48, 1425-1438.
12. Zafra-Stone, S., Yasmin, T., Bagchi, M., Chatterjee, A., Vinson, J. A., and Bagchi, D. (2007) Berry anthocyanins as novel antioxidants in human health and disease prevention. Mol. Nutr. Food Res. 51, 675-683.
13. Matsumoto, H., Nakamura, Y., Tachibanaki, S., Kawamura, S., and Hirayama, M. (2003) Stimulatory effect of cyanidin 3-glycosides on the regeneration of rhodopsin. J. Agric. Food Chem. 51, 3560-3563.
14. Jang, Y. P., Zhou, J., Nakanishi, K., and Sparrow, J. R. (2005) Anthocyanins protect against A2E photooxidation and membrane permeabilization in retinal pigment epithelial cells. Photochem. Photobiol. 81, 529-536.
15. Dearing, M. D., Appel, H. M., and Schultz, J. C. (2002) Why do cranberries reduce incidence of urinary tract infections? J. Ethnopharmacol. 80, 211.
16. Ohnishi, R., Ito, H., Kasajima, N., Kaneda, M., Kariyama, R., Kumon, H., Hatano, T., and Yoshida, T. (2006) Urinary excretion of anthocyanins in humans after cranberry juice ingestion. Biosci. Biotechnol. Biochem. 70, 1681-1687.
17. Mullen, W., McGinn, J., Lean, M. E., MacLean, M. R., Gardner, P., Duthie, G. G., Yokota, T., and Crozier, A. (2002) Ellagitannins, flavonoids, and other phenolics in red raspberries and their contribution to antioxidant capacity and vasorelaxation properties. J. Agric. Food Chem. 50, 5191-5196.
18. Bagchi, D., Sen, C. K., Bagchi, M., and Atalay, M. (2004) Anti-angiogenic, antioxidant, and anti-carcinogenic properties of a novel anthocyanin-rich berry extract formula. Biochemistry (Mosc) 69, 75-80.
19. Zhao, C., Giusti, M. M., Malik, M., Moyer, M. P., and Magnuson, B. A. (2004) Effects of commercial anthocyanin-rich extracts on colonic cancer and nontumorigenic colonic cell growth. J. Agric. Food Chem. 52, 6122-6128.
20. Hou, D. X. (2003) Potential mechanisms of cancer chemoprevention by anthocyanins. Curr. Mol. Med. 3, 149-159.
21. Katsube, N., Iwashita, K., Tsushida, T., Yamaki, K., and Kobori, M. (2003) Induction of apoptosis in cancer cells by Bilberry (Vaccinium myrtillus) and the anthocyanins. J. Agric. Food Chem. 51, 68-75.
22. Meiers, S., Kemeny, M., Weyand, U., Gastpar, R., von Angerer, E., and Marko D. (2001) The anthocyanidins cyanidin and delphinidin are potent inhibitors of the epidermal growth-factor receptor. J. Agric. Food Chem. 49, 958-962.
23. Youdim, K. A., Shukitt-Hale, B., MacKinnon, S., Kalt, W., and Joseph J. A. (2000) Polyphenolics enhance red blood cell resistance to oxidative stress: in vitro and in vivo. Biochim. Biophys. Acta 1523, 117-122.
24. Galli, R. L., Shukitt-Hale, B., Youdim, K. A., and Joseph, J. A. (2002) Fruit polyphenolics and brain aging: nutritional interventions targeting age-related neuronal and behavioral deficits. Ann. N. Y. Acad. Sci. 959, 128-132.
25. Cignarella, A., Nastasi, M., Cavalli, E., and Puglisi, L. (1996) Novel lipid-lowering properties of Vaccinium myrtillus L. leaves, a traditional antidiabetic treatment, in several models of rat dyslipidaemia: a comparison with ciprofibrate. Thromb. Res. 84, 311-322.
26. Matsui, T., Ogunwande, I. A., Abesundara, K. J., and Matsumoto, K. (2006) Anti-hyperglycemic potential of natural products. Mini Rev. Med. Chem. 6, 349-356.
27. Choi, E. H., Chang, H. J., Cho, J. Y., and Chun, H. S. (2007) Cytoprotective effect of anthocyanins against doxorubicin-induced toxicity in H9c2 cardiomyocytes in relation to their antioxidant activities. Food Chem. Toxicol. 45, 1873-1881.
28. Lätti, A. K., Riihinen, K. R., and Kainulainen, P. S. (2008) Analysis of anthocyanin variation in wild populations of bilberry (Vaccinium myrtillus L.) in Finland. J. Agric. Food Chem. 56, 190-196.
29. Kähkönen, M. P., Hopia, A. I., Vuorela, H. J., Rauha, J. P., Pihlaja, K., Kujala, T. S., and Heinonen, M. (1999) Antioxidant activity of plant extracts containing phenolic compounds. J. Agric. Food Chem. 47, 3954-3962.
30. European Scientific Cooperative on Phytotherapy (ESCOP) Monographs (2003). In Myrtilli fructus, 2nd edn. pp. 345-350, Thieme Publishers, New York, NY.
31. 3-induced kidney damage in mice. J. Agric. Food Chem. 56, 420-425.
32. Heinonen, M. (2007) Antioxidant activity and antimicrobial effect of berry phenolics-a Finnish perspective. Mol. Nutr. Food Res. 51, 684-691.
33. Milbury, P. E., Graf, B., Curran-Celentano, J. M., and Blumberg, J. B. (2007) Bilberry (Vaccinium myrtillus) anthocyanins modulate heme oxygenase-1 and glutathione S-transferase-pi expression in ARPE-19 cells. Invest. Ophthalmol. Vis. Sci. 48, 2343-2249.
34. Choi, E. H., Ok, H. E., Yoon, Y., Magnuson, B. A., Kim, M. K., and Chun, H. S. (2007) Protective effect of anthocyanin-rich extract from bilberry (Vaccinium myrtillus L.) against myelotoxicity induced by 5-fluorouracil. Biofactors 29, 55-65.
35. Reeves, P. G. (1993) AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. J. Nutr. 123, 1939-1951.
36. Choi, E. H., Lee, N., Kim, H. J., Kim, M. K., Chi, S. G., Kwon, D. Y., and Chun, H. S. (2008) Schisandra fructus extract ameliorates doxorubicin-induced cytotoxicity in cardiomyocytes: altered gene expression for detoxification enzymes. Genes Nutr. 2, 337-345.
37. Shaik, I. H. and Mehvar, R. (2006) Rapid determination of reduced and oxidized glutathione levels using a new thiol-masking reagent and the enzymatic recycling method: application to the rat liver and bile samples. Anal. Bioanal. Chem. 385, 105-113.
38. Habig, W. H., Pabst, M. J., and Jakoby, W. B. (1974) Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. J. Biol. Chem. 249, 7130-7139.
39. Johansson, L. H. and Borg, L. A. (1988) A spectrophotometric method for determination of catalase activity in small tissue samples. Anal. Biochem. 174, 331-336.
40. Nandini, M., Rahiman, M. A., and Rao, S. N. (1999) Effect of dietary fish on antioxidant parameters of normal and cholesterol stressed rats. Indian J. Exp. Biol. 37, 1187-1191.
41. Marklund, S. and Marklund, G. (1974) Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. Eur. J. Biochem. 47, 469-474.
42. Anjos Ferreira, A. L., Russell, R. M., Rocha, N., Placido Ladeira, M. S., Favero Salvador, D. M., Oliveira Nascimento, M. C., Matsui, M., Carvalho, F. A., Tang, G., Matsubara, L. S., and Matsubara, B. B. (2007) Effect of lycopene on doxorubicin-induced cardiotoxicity: an echocardiographic, histological and morphometrical assessment. Basic Clin. Pharmacol. Toxicol. 101, 16-24.
43. Saad, S. Y., Najjar, T. A., and Arafah, M. M. (2006) Cardioprotective effects of subcutaneous ebselen against daunorubicin-induced cardiomyopathy in rats. Basic Clin. Pharmacol. Toxicol. 99, 412-417.
44. Mohamed, H. E., El-Swefy, S. E., and Hagar, H. H. (2000) The protective effect of glutathione administration on adriamycin-induced acute cardiac toxicity in rats. Pharmacol. Res. 42, 115-121.
45. Yin, X., Wu, H., Chen, Y., and Kang, Y. J. (1998) Induction of antioxidants by adriamycin in mouse heart. Biochem. Pharmacol. 56, 87-93.
46. Pritsos, C. A. and Ma, J. (2000) Basal and drug-induced antioxidant enzyme activities correlate with age-dependent doxorubicin oxidative toxicity. Chem. Biol. Interact. 127, 1-11.
47. Wallimann, T., Wyss, M., Brdiczka, D., Nicolay, K., and Eppenberger, H. M. (1992) Intracellular compartmentation, structure and function of creatine kinase isoenzymes in tissues with high and fluctuating energy demands: the 'phosphocreatine circuit' for cellular energy homeostasis. Biochem. J. 281, 21-40.
48. Muraoka, S. and Miura, T. (2004) Thiol oxidation induced by oxidative action of adriamycin. Free Radic. Res. 38, 963-968.
49. Tokarska-Schlattner, M., Wallimann, T., and Schlattner, U. (2002) Multiple interference of anthracyclines with mitochondrial creatine kinases: preferential damage of the cardiac isoenzyme and its implications for drug cardiotoxicity. Mol. Pharmacol. 61, 516-523.
50. Ferrans, V. J., Clark, J. R., Zhang, J., Yu, Z. X., and Herman, E. H. (1997) Pathogenesis and prevention of doxorubicin cardiomyopathy. Tsitologiia 39, 928-937.
51. Lazze, M. C., Pizzala, R., Savio, M., Stivala, L. A., Prosperi, E., and Bianchi, L. (2003) Anthocyanins protect against DNA damage induced by tert-butyl-hydroperoxide in rat smooth muscle and hepatoma cells. Mutat. Res. 535, 103-115.
52. Mas, T., Susperregui, J., Berke, B., Cheze, C., Moreau, S., Nuhrich, A., and Vercauteren, J. (2000) DNA triplex stabilization property of natural anthocyanins. Phytochemistry 53, 679-687.
53. Talavera, S., Felgines, C., Texier, O., Besson, C., Mazur, A., Lamaison, J., and Remesy, C. (2006) Bioavailability of a bilberry anthocyanin extract and its impact on plasma antioxidant capacity in rats. J. Sci. Food Agric. 86, 90-97.
54. Ichiyanagi, T., Shida, Y., Rahman, M. M., Hatano, Y., and Konishi, T. (2006) Bioavailability and tissue distribution of anthocyanins in bilberry (Vaccinium myrtillus L.) extract in rats. J. Agric. Food Chem. 54, 6578-6587.
55. Myers, C., Bonow, R., Palmeri, S., Jenkin, J., Corden, B., Locker, G, Doroshow, J., and Epstein, S. (1983) A randomized controlled trial assessing the prevention of doxorubicin cardiomyopathy by N-acetylcysteine. Semin. Oncol. 10, 53-55.
56. Bruynzeel, A. M., Vormer-Bonne, S., Bast, A., Niessen, H. W., and van der Vijgh, W. J. (2007) Long-term effects of 7-monohydroxyethylrutoside (monoHER) on DOX-induced cardiotoxicity in mice. Cancer Chemother. Pharmacol. 60, 509-514.
57. Iarussi, D., Auricchio, U., Murano, A., Giuliano, M., Di Tullio, M. T., and Iacono, A. (1994) Protective effect of coenzyme Q on anthracyclines cardiotoxicity: control study in children with acute lymphoblastic leukaemia or non-Hodgkin lymphoma. Mol. Asp. Med. 15, 207-212.