Effect of lycopene on doxorubicin-induced cardiotoxicity: An echocardiographic, histological and morphometrical assessment

Basic and Clinical Pharmacology and Toxicology

Volumn 101, Issue 1, 2007, Pages 16-24

  Anjos Ferreira, Ana Lucia ^a   Russell, Robert Mitchell ^b   Rocha, Noeme ^a   Placido Ladeira, Marcelo Sady ^a   Favero Salvadori, Daisy Maria ^a   Oliveira Nascimento, Maria Carolina Munhoz ^a   Matsui, Mirna ^a   Carvalho, Flavio Augusto ^a   Tang, Guangwen ^b   Matsubara, Luiz Shiguero ^a   Matsubara, Beatriz Bojikian ^a  

^a SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

^b TUFTS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CAROTENE; COLLAGEN; DOXORUBICIN; LYCOPENE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARDIOTOXICITY; CELL DAMAGE; CONTROLLED STUDY; DRUG BLOOD LEVEL; ECHOCARDIOGRAPHY; FEEDING; HEART; HEART DISEASE; HEART LEFT VENTRICLE CONTRACTION; HEART PROTECTION; HISTOLOGY; LEYDIG CELL; LIVER; MALE; MORPHOMETRICS; MUSCLE CELL; NONHUMAN; PLASMA; PRIORITY JOURNAL; RANDOMIZATION; RAT; SYSTOLIC DYSFUNCTION;

ANIMALS; ANTIBIOTICS, ANTINEOPLASTIC; ANTIOXIDANTS; CAROTENOIDS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; DOXORUBICIN; ELECTROCARDIOGRAPHY; HEART; MALE; MYOCARDIUM; MYOCYTES, CARDIAC; RANDOM ALLOCATION; RATS; RATS, WISTAR;

ANIMALIA; RATTUS; RATTUS NORVEGICUS; ZEA MAYS;

EID: 34250652557     PISSN: 17427835     EISSN: 17427843     Source Type: Journal    
DOI: 10.1111/j.1742-7843.2007.00070.x     Document Type: Article

References (66)

1. Buja LM, Ferrans VJ, Mayer RJ, Roberts WC, Henderson ES. Cardiac ultraestructural changes induced by daunorubicin therapy. Cancer 1973 32: 771 88.
2. Li T, Danelisen I, Singal PK. Early changes in myocardial antioxidant enzymes in rats treated with adriamycin. Mol Cell Biochem 2002 232: 19 26.
3. Van Vleet JF, Ferrans VJ, Weirich WE. Cardiac disease induced by chronic adriamycin administration in dogs and an evaluation of vitamin E and selenium as cardioprotectants. Am J Pathol 1980 99: 13 42.
4. Breed JG, Zimmerman AN, Dormans JA, Pinedo HM. Failure of the antioxidant vitamin E to protect against adriamycin-induced cardiotoxicity in the rabbit. Cancer Res 1980 40: 2033 8.
5. Legha SS, Wang YM, Mackay B et al. Clinical and pharmacologic investigation of the effects of alpha-tocopherol on adriamycin cardiotoxicity. Ann N Y Acad Sci 1982 393: 411 8.
6. Myers C, Bonow R, Palmeri S et al. A randomized controlled trial assessing the prevention of doxorubicin cardiomyopathy by N-acetylcysteine. Semin Oncol 1983 10: 53 5.
7. Wahab MHA, Akoul EEMS, Abdelaziz AH. Modulatory effects of melatonin and vitamin-E on doxorubicin-induced cardiotoxicity in Ehrlich ascites carcinoma bearing mice. Tumori 2000 86: 157 62.
8. Danelisen I, Palace V, Lou H, Singal PK. Maintenance of myocardial levels of vitamin A in heart failure due to adriamycin. J Mol Cell Cardiol 2002 34: 789 95.
9. Wattanapitayakul SK, Chularojmontri L, Herunsalee A, Charuchongkolwongse S, Niumsakul S, Bauer JA. Screening of antioxidants from medicinal plants for cardioprotective effect against doxorubicin toxicity. Basic Clin Pharmacol Toxicol 2005 96: 80 7.
10. Stahl W, Sies H. Physical quenching of singlet oxygen and cis-trans isomerization of carotenoids. Ann N Y Acad Sci 1993 691: 10 9.
11. Di Mascio P, Kaiser S, Sies H. Lycopene as the most efficient biological carotenoid singlet oxygen quencher. Arch Biochem Biophys 1989 274: 532 8.
12. Agarwal S, Rao VA. Tomato lycopene and its role in human health and chronic diseases. Can Med Assoc J 2000 163: 739 44.
13. Stahl W, Sies H. Antioxidant activity of carotenoids. Mol Aspects Med 2003 24: 345 51.
14. Wang S, Konorev EA, Kotamraju S, Joseph J, Kalivendi S, Kalyanaraman B. Doxorubicin induces apoptosis in normal and tumor cells via distinctly different mechanisms. Intermediacy of H2O2- and p53-dependent pathways. J Biol Chem 2004 279: 25535 43.
15. Lu Y, Etoh H, Watanabe N et al. A new carotenoid, hydrogen peroxide oxidation products from lycopene. Biosci Biotech Biochem 1995 59: 2153 5.
16. Wu K, Schwartz SJ, Platz EA et al. Variations in plasma lycopene and specific isomers over time in a cohort of U.S. men. J Nutr 2003 133: 1930 6.
17. Kardinaal AF, Kok FJ, Ringstad J et al. Antioxidants in adipose tissue and risk of myocardial infarction: the EURAMIC Study. Lancet 1993 342: 1379 84.
18. Kohlmeier L, Kark JD, Gomez-Gracia E et al. Lycopene and myocardial infarction risk in the EURAMIC Study. Am J Epidemiol 1997 146: 618 26.
19. Kristenson M, Zieden B, Kucinskiene Z et al. Antioxidant state and mortality from coronary heart disease in Lithuanian and Swedish men: concomitant cross sectional study of men aged 50. Br Med J 1997 314: 629 33.
20. Karimi G, Ramezani M, Abdi A. Protective effects of lycopene and tomato extract against doxorubicin-induced cardiotoxicity. Phytother Res 2005 19: 912 4.
21. Yilmaz S, Atessahin A, Sahna E, Karahan I, Ozer S. Protective effect of lycopene on adriamycin-induced cardiotoxicity and nephrotoxicity. Toxicology 2006 218: 164 71.
22. Paiva SA, Novo R, Matsubara BB et al. Beta-carotene attenuates the paradoxical effect of tobacco smoke on the mortality of rats after experimental myocardial infarction. J Nutr 2005 135: 2109 13.
23. Siveski-Iliskovic N, Hill M, Chow DA, Singal PK. Probucol protects against adriamycin cardiomyopathy without interfering with its antitumor effect. Circulation 1995 91: 10 5.
24. Cohen LA. A review of animal model studies of tomato carotenoids, lycopene, and cancer chemoprevention. Exp Biol Med 2002 227: 864 8.
25. Abdel-aleem S, el-Merzabani MM, Sayed-Ahmed M, Taylor DA, Lowe JE. Acute and chronic effects of adriamycin on fatty acid oxidation in isolated cardiac myocytes. J Mol Cell Cardiol 1997 29: 789 97.
26. Matos HR, Capelozzi VL, Gomes OF, Di Mascio P, Medeiros MHG. Lycopene inhibits DNA damage and liver necrosis in rats treated with ferric nitrilotriacetate. Arch Biochem Biophys 2001 396: 171 7.
27. Yeum KJ, Lee-Kim YC, Yoon S et al. Similar metabolites formed from β-carotene by either human gastric mucosal homogenates, lipoxygenase or linoleic acid hydroperoxide. Arch Biochem Biophys 1995 321: 167 74.
28. Ferreira ALA, Yeum KJ, Liu C et al. Tissue distribution of lycopene in ferrets and rats after lycopene supplementation. J Nutr 2000 130: 1256 60.
29. Sahn DJ, DeMaria A, Kisslo J, Weyman AE. The Committee on M-mode standardization of the American Society of Echocardiography. Recommendations regarding quantitation in M-mode echocardiography: results of a survey of echocardiographic measurements. Circulation 1978 58: 1072 83.
30. Matsubara LS, Matsubara BB, Okoshi MP, Cicogna AC, Janicki JS. Alterations in myocardial collagen content affect rat papillary muscle function. Am Physiol Heart Circ Physiol 2000 279: H1534 9.
31. Hiroe M, Ohta Y, Fujita N et al. Myocardial uptake of 111 In monoclonal antimyosin Fab in detecting doxorubicin cardiotoxicity in rats. Morphological and hemodynamic findings. Circulation 1992 86: 1965 72.
32. Deepa PR, Varalakshmi P. The cytoprotective role of a low-molecular-weight heparin fragment studied in an experimental model of glomerulotoxicity. Eur J Pharmacol 2003 478: 199 205.
33. Cusack BJ, Muslin PS, Johnson CJ, Vestal RE, Olson RD. Aging increases the cardiotoxicity of daunorubicin and daunorubicinol in the rat. J Gerontol A Biol Sci Med Sci 1996 51: B376 84.
34. Stahl W, Sies H. Uptake of lycopene and its geometrical isomers is greater from heat-processed than from unprocessed tomato juice in humans. J Nutr 1992 122: 2161 6.
35. Jain CK, Agarwal S, Rao AV. The effect of dietary lycopene on bioavailability, tissue distribution, in vivoantioxidant properties and colonic preneoplasia in rats. Nutr Res 1999 19: 1383 91.
36. Kaplan LA, Lau JM, Stein EA. Carotenoid composition, concentrations, and relationships in various human organs. Clin Physiol Biochem 1990 8: 1 10.
37. Narisawa T, Fukaura Y, Hasebe M et al. Prevention of N-methylnitrosourea- induced colon carcinogenesis in F344 rats by lycopene and tomato juice rich in lycopene. Jpn J Cancer Res 1998 89: 1003 8.
38. Clinton SK, Emenhiser C, Schwartz SJ et al. cis-trans lycopene isomers, carotenoids, and retinol in the human prostate. Cancer Epidemiol Biomarkers Prev 1996 5: 823 33.
39. Osono Y, Woollett LA, Herz J, Dietschy JM. Role of the low density lipoprotein receptor in the flux of cholesterol through the plasma and across the tissues of the mouse. J Clin Invest 1995 95: 1124 32.
40. Quiles JL, Ramirez-Tortosa MC, Huertas JR et al. Olive oil supplemented with vitamin E affects mitochondrial coenzyme Q levels in liver of rats after an oxidative stress induced by adriamycin. Biofactors 1999 9: 331 6.
41. Minotti G, Mancuso C, Frustaci A et al. Paradoxical inhibition of cardiac lipid peroxidation in cancer patients treated with doxorubicin. Pharmacologic and molecular reappraisal of anthracycline cardiotoxicity. J Clin Invest 1996 98: 650 61.
42. Deepa PR, Varalakshmi P. Protective effect of low molecular weight heparin on oxidative injury and cellular abnormalities in adriamycin-induced cardiac and hepatic toxicity. Chem Biol Interact 2003 146: 201 10.
43. Dziegiel P, Murawska-Cialowicz E, Jethon Z et al. Melatonin stimulates the activity of protective antioxidative enzymes in myocardial cells of rats in the course of doxorubicin intoxication. J Pineal Res 2003 35: 183 7.
44. Li T, Danelisen I, Belló-Klein A, Singal PK. Effects of probucol on changes of antioxidant enzymes in adriamycin-induced cardiomyopathy in rats. Cardiovasc Res 2000 46: 523 30.
45. Siveski-Iliskovic N, Singal PK. Lipid lowering: an important factor in preventing adriamycin-induced heart failure. Am J Pathol 1997 150: 727 34.
46. Neely JR, Morgan HE. Relationship between carbohydrate and lipid metabolism and the energy balance of heart muscle. Annu Rev Physiol 1974 36: 413 59.
47. Corr PB, Gross RS, Sobel BE. Amphipathic metabolites and membrane dysfunction in ischemic myocardium. Circ Res 1985 55: 135 54.
48. Krinsky NI, Cornewell DG, Oncley JL. The transport of vitamin A and carotenoids in human plasma. Arch Biochem Biophys 1958 73: 233 46.
49. Esterbauer H, Jurgens G, Quehenberger O, Koller E. Autoxidation of human low density lipoprotein: loss of polyunsaturated fatty acids and vitamin E and generation of aldehydes. J Lipid Res 1987 28: 495 509.
50. Saad SY, Najjar TA, Al-Rikabi AC. The preventive role of deferoxamine against acute doxorubicin-induced cardiac, renal and hepatic toxicity in rats. Pharmacol Res 2001 43: 211 8.
51. Yagmurca M, Fadillioglu E, Erdogan H, Ucar M, Sogut S, Irmak MK. Erdosteine prevents doxorubicin-induced cardiotoxicity in rats. Pharmacol Res 2003 48: 377 82.
52. Billingham ME, Mason JW, Bristow MR, Daniels JR. Anthracycline cardiomyopathy monitored by morphologic changes. Cancer Treat Rep 1978 62: 865 72.
53. Richelle M, Bortlik K, Liardet S et al. A food-based formulation provides lycopene with the same bioavailability to humans as that from tomato paste. J Nutr 2002 132: 404 8.
54. Tokudome T, Mizushige K, Noma T et al. Prevention of doxorubicin (adriamycin)-induced cardiomyopathy by simultaneous administration of angiotensin-converting enzyme inhibitor assessed by acoustic densitometry. J Cardiovasc Pharmacol 2000 36: 361 8.
55. Caulfield JB, Bittner V. Cardiac matrix alterations induced by adriamycin. Am J Pathol 1988 133: 298 305.
56. Jalil JE, Doering CW, Janicki JS, Pick R, Shroff SG, Weber KT. Fibrillar collagen and myocardial stiffness in the intact hypertrophied rat left ventricle. Circ Res 1989 64: 1041 50.
57. Brilla CG, Weber KT. Reactive and reparative myocardial fibrosis in arterial hypertension in the rat. Cardiovasc Res 1992 26: 671 7.
58. Delgado RM, Nawar MA, Zewail AM et al. Cyclooxygenase-2 inhibitor treatment improves left ventricular function and mortality in a murine model of doxorubicin-induced heart failure. Circulation 2004 109: 1428 33.
59. Ha JW, Kang SM, Pyun WB et al. Serial assessment of myocardial properties using cyclic variation of integrated backscatter in an adriamycin-induced cardiomyopathy rat model. Yonsei Med J 2005 46: 73 7.
60. de Andrade JN, Camacho AA, Santos PS, Fantinatti AP, Nunes N, Stopiglia AJ. Plication of the free wall of the left ventricle in dogs with doxorubicin-induced cardiomyopathy. Am J Vet Res 2005 66: 238 43.
61. Katona M, Boros K, Santha P, Ferdinandy P, Dux M, Jancso G. Selective sensory denervation by capsaicin aggravates adriamycin-induced cardiomyopathy in rats. Naunyn Schmiedebergs Arch Pharmacol 2004 370: 436 43.
62. Koh E, Nakamura T, Takahashi H. Troponin-T and brain natriuretic peptide as predictors for adriamycin-induced cardiomyopathy in rats. Circ J 2004 68: 163 7.
63. Sung RY, Huang GY, Shing MK et al. Echocardiographic evaluation of cardiac function in paediatric oncology patients treated with or without anthracycline. Int J Cardiol 1997 60: 239 48.
64. Marchandise B, Schroeder E, Bosly A et al. Early detection of doxorubicin cardiotoxicity: interest of Doppler echocardiographic analysis of left ventricular filling dynamics. Am Heart J 1989 118: 92 8.
65. Lipshultz SE, Lipsitz SR, Mone SM et al. Female sex and drug dose as risk factors for late cardiotoxic effects of doxorubicin therapy for childhood cancer. N Engl J Med 1995 332: 1738 43.
66. Paiva MG, Petrilli AS, Moises VA, Macedo CR, Tanaka C, Campos O. Cardioprotective effect of dexrazoxane during treatment with doxorubicin: a study using low-dose dobutamine stress echocardiography. Pediatr Blood Cancer 2005 45: 902 8.