C-phycocyanin ameliorates doxorubicin-induced oxidative stress and apoptosis in adult rat cardiomyocytes

Journal of Cardiovascular Pharmacology

Volumn 47, Issue 1, 2006, Pages 9-20

  Khan, Mahmood ^a,b   Varadharaj, Saradhadevi ^a   Shobha, Jagdish C ^b   Naidu, Madireddi U ^b   Parinandi, Narasimham L ^a   Kutala, Vijay Kumar ^a,b   Kuppusamy, Periannan ^a,c  

^a OHIO STATE UNIVERSITY   (United States)

^b NIZAM'S INSTITUTE OF MEDICAL SCIENCES   (India)

^c OHIO STATE UNIVERSITY   (United States)

Author keywords

Apoptosis; Biliprotein; C phycocyanin; Cardiotoxicity; Doxorubicin; Oxidative stress; Spirulina

Indexed keywords

ANTINEOPLASTIC AGENT; BROXURIDINE; C PHYCOCYANIN; CASPASE 3; CYTOCHROME C; DICHLORODIHYDROFLUORESCEIN DIACETATE; DNA FRAGMENT; DOXORUBICIN; FLUORESCEIN ISOTHIOCYANATE; HYDROETHIDINE; PHYCOCYANIN; PROPIDIUM IODIDE; PROTEIN BAX; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG; ANTINEOPLASTIC ANTIBIOTIC; BACTERIAL PROTEIN; CASP3 PROTEIN, RAT; CASPASE; PROTEIN BCL 2;

ADOLESCENT; ANIMAL CELL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; BLUE GREEN ALGA; CARDIOMYOPATHY; CARDIOTOXICITY; CONGESTIVE HEART FAILURE; FLOW CYTOMETRY; FLUORESCENCE; HEART MUSCLE CELL; HEART PROTECTION; MALE; NICK END LABELING; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT; SPIRULINA; ANIMAL; DRUG EFFECT; METABOLISM; PATHOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; ANTIBIOTICS, ANTINEOPLASTIC; APOPTOSIS; BACTERIAL PROTEINS; CASPASE 3; CASPASES; DOXORUBICIN; IN SITU NICK-END LABELING; MALE; MYOCYTES, CARDIAC; OXIDATIVE STRESS; PHYCOCYANIN; PROTO-ONCOGENE PROTEINS C-BCL-2; RATS; RATS, SPRAGUE-DAWLEY; SPIRULINA;

EID: 33646409207     PISSN: 01602446     EISSN: None     Source Type: Journal    
DOI: 10.1097/01.fjc.0000191520.48404.27     Document Type: Article

References (68)

1. Weiss RB. The anthracyclines: will we ever find a better doxorubicin? Semin Oncol. 1992;19:670-686.
2. Lefrak EA, Pitha J, Rosenheim S, et al. A clinicopathologic analysis of adriamycin cardiotoxicity. Cancer. 1973;32:302-314.
3. Singal PK, Iliskovic N. Doxorubicin-induced cardiomyopathy. N Engl J Med. 1998;339:900-905.
4. Bristow MR, Sageman WS, Scott RH, et al. Acute and chronic cardiovascular effects of doxorubicin in the dog: the cardiovascular pharmacology of drug-induced histamine release. J Cardiovasc Pharmacol. 1980;2:487-515.
5. Tong J, Ganguly PK, Singal PK. Myocardial adrenergic changes at two stages of heart failure due to adriamycin treatment in rats. Am J Physiol. 1991;260:H909-H916.
6. Doroshow JH, Davies KJ. Redox cycling of anthracyclines by cardiac mitochondria. II. Formation of superoxide anion, hydrogen peroxide, and hydroxyl radical. J Biol Chem. 1986;261:3068-3074.
7. Doroshow JH. Anthracycline antibiotic-stimulated superoxide, hydrogen peroxide, and hydroxyl radical production by NADH dehydrogenase. Cancer Res. 1983;43:4543-4551.
8. Olson RD, Mushlin PS. Doxorubicin cardiotoxicity: analysis of prevailing hypotheses. FASEB J. 1990;4:3076-3086.
9. Kotamraju S, Konorev EA, Joseph J, et al. Doxorubicin-induced apoptosis in endothelial cells and cardiomyocytes is ameliorated by nitrone spin traps and ebselen. Role of reactive oxygen and nitrogen species. J Biol Chem. 2000;275:33585-33592.
10. Li PF, Dietz R, von Harsdorf R. Superoxide induces apoptosis in cardiomyocytes, but proliferation and expression of transforming growth factor-beta1 in cardiac fibroblasts. FEBS Lett. 1999;448:206-210.
11. Slater AF, Nobel CS, Orrenius S. The role of intracellular oxidants in apoptosis. Biochim Biophys Acta. 1995;1271:59-62.
12. Stangel M, Zettl UK, Mix E, et al. H2O2 and nitric oxide-mediated oxidative stress induce apoptosis in rat skeletal muscle myoblasts. J Neuropathol Exp Neurol. 1996;55:36-43.
13. Wang S, Kotamraju S, Konorev E, et al. Activation of nuclear factor-kappaB during doxorubicin-induced apoptosis in endothelial cells and myocytes is pro-apoptotic: the role of hydrogen peroxide. Biochem J. 2002;367:729-740.
14. von Harsdorf R, Li PF, Dietz R. Signaling pathways in reactive oxygen species-induced cardiomyocyte apoptosis. Circulation. 1999;99:2934-2941.
15. Zhu W, Zou Y, Aikawa R, et al. MAPK superfamily plays an important role in daunomycin-induced apoptosis of cardiac myocytes. Circulation. 1999;100:2100-2107.
16. Aoki H, Kang PM, Hampe J, et al. Direct activation of mitochondrial apoptosis machinery by c-Jun N-terminal kinase in adult cardiac myocytes. J Biol Chem. 2002;277:10244-10250.
17. Akao M, O'Rourke B, Teshima Y, et al. Mechanistically distinct steps in the mitochondrial death pathway triggered by oxidative stress in cardiac myocytes. Circ Res. 2003;92:186-194.
18. Datta SR, Dudek H, Tao X, et al. Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell. 1997;91:231-241.
19. Nakamura T, Ueda Y, Juan Y, et al. Fas-mediated apoptosis in adriamycin-induced cardiomyopathy in rats: in vivo study. Circulation. 2000;102:572-578.
20. Narula J, Haider N, Virmani R, et al. Apoptosis in myocytes in end-stage heart failure. N Engl J Med. 1996;335:1182-1189.
21. Sawyer DB, Fukazawa R, Arstall MA, et al. Daunorubicin-induced apoptosis in rat cardiac myocytes is inhibited by dexrazoxane. Circ Res. 1999;84:257-265.
22. Yen HC, Oberley TD, Vichitbandha S, et al. The protective role of manganese superoxide dismutase against adriamycin-induced acute cardiac toxicity in transgenic mice. J Clin Invest. 1996;98:1253-1260.
23. Kang YJ, Chen Y, Epstein PN. Suppression of doxorubicin cardiotoxicity by overexpression of catalase in the heart of transgenic mice. J Biol Chem. 1996;271:12610-12616.
24. L'Ecuyer T, Allebban Z, Thomas R, et al. Glutathione S-transferase overexpression protects against anthracycline-induced H9C2 cell death. Am J Physiol Heart Circ Physiol. 2004;286:H2057-H2064.
25. DeAtley SM, Aksenov MY, Aksenova MV, et al. Antioxidants protect against reactive oxygen species associated with adriamycin-treated cardiomyocytes. Cancer Lett. 1999;136:41-46.
26. Dorr RT, Lagel K, McLean S. Cardioprotection of rat heart myocytes with amifostine (Ethyol) and its free thiol, WR-1065, in vitro. Eur J Cancer. 1996;32A(suppl 4):S21-S25.
27. Van Vleet JF, Ferrans VJ. Evaluation of vitamin E and selenium protection against chronic adriamycin toxicity in rabbits. Cancer Treat Rep. 1980;64:315-317.
28. Kumar D, Kirshenbaum L, Li T, et al. Apoptosis in isolated adult cardiomyocytes exposed to adriamycin. Ann N Y Acad Sci. 1999;874:156-168.
29. Kumar D, Kirshenbaum LA, Li T, et al. Apoptosis in adriamycin cardiomyopathy and its modulation by probucol. Antioxid Redox Signal. 2001;3:135-145.
30. Kang YJ, Chen Y, Yu A, et al. Overexpression of metallothionein in the heart of transgenic mice suppresses doxorubicin cardiotoxicity. J Clin Invest. 1997;100:1501-1506.
31. Speyer JL, Green MD, Kramer E, et al. Protective effect of the bispiperazinedione ICRF-187 against doxorubicin-induced cardiac toxicity in women with advanced breast cancer. N Engl J Med. 1988;319:745-752.
32. Naidu M, Vijay Kumar K, Mohan IK, et al. Protective effect of Gingko biloba extract against doxorubicin-induced cardiotoxicity in mice. Indian J Exp Biol. 2002;40:894-900.
33. Mohan IK, Kutala VK, Naidu MUR, et al. Protective effect of CardiPro against doxorubicin-induced cardiotoxicity in mice. Phytomedicine. 2005. (in press).
34. Duerring M, Schmidt GB, Huber R. Isolation, crystallization, crystal structure analysis and refinement of constitutive C-phycocyanin from the chromatically adapting cyanobacterium Fremyella diplosiphon at 1.66 A resolution. J Mol Biol. 1991;217:577-592.
35. Lissi EA, Pizarro M, Aspee A, et al. Kinetics of phycocyanin bilin groups destruction by peroxyl radicals. Free Radic Biol Med. 2000;28:1051-1055.
36. Miranda MS, Cintra RG, Barros SB, et al. Antioxidant activity of the microalga Spirulina maxima. Braz J Med Biol Res. 1998;31:1075-1079.
37. Romay C, Armesto J, Remirez D, et al. Antioxidant and anti-inflammatory properties of C-phycocyanin from blue-green algae. Inflamm Res. 1998;47:36-41.
38. Bhat VB, Madyastha KM. C-phycocyanin: a potent peroxyl radical scavenger in vivo and in vitro. Biochem Biophys Res Commun. 2000;275:20-25.
39. Romay C, Gonzalez R. Phycocyanin is an antioxidant protector of human erythrocytes against lysis by peroxyl radicals. J Pharm Pharmacol. 2000;52:367-368.
40. Bhat VB, Madyastha KM. Scavenging of peroxynitrite by phycocyanin and phycocyanobilin from Spirulina platensis: protection against oxidative damage to DNA. Biochem Biophys Res Commun. 2001;285:262-266.
41. Vadiraja BB, Gaikwad NW, Madyastha KM. Hepatoprotective effect of C-phycocyanin: protection for carbon tetrachloride and R-(+)-pulegone-mediated hepatotoxicty in rats. Biochem Biophys Res Commun. 1998;249:428-431.
42. Reddy MC, Subhashini J, Mahipal SV, et al. C-Phycocyanin, a selective cyclooxygenase-2 inhibitor, induces apoptosis in lipopolysaccharide-stimulated RAW 264.7 macrophages. Biochem Biophys Res Commun. 2003;304:385-392.
43. Farooq SM, Asokan D, Sakthivel R, et al. Salubrious effect of C-phycocyanin against oxalate-mediated renal cell injury. Clin Chim Acta. 2004;348:199-205.
44. Rimbau V, Camins A, Romay C, et al. Protective effects of C-phycocyanin against kainic acid-induced neuronal damage in rat hippocampus. Neurosci Lett. 1999;276:75-78.
45. Khan M, Shobha JC, Mohan IK, et al. Protective effect of Spirulina against Doxorubicin-induced cardiotoxicity. Phytother Res. 2005 (in press).
46. McDonough PM, Yasui K, Betto R, et al. Control of cardiac Ca2+ levels. Inhibitory actions of sphingosine on Ca2+ transients and L-type Ca2+ channel conductance. Circ Res. 1994;75:981-989.
47. Spallarossa P, Garibaldi S, Altieri P, et al. Carvedilol prevents doxorubicin-induced free radical release and apoptosis in cardiomyocytes in vitro. J Mol Cell Cardiol. 2004;37:837-846.
48. Yamanaka S, Tatsumi T, Shiraishi J, et al. Amlodipine inhibits doxorubicin-induced apoptosis in neonatal rat cardiac myocytes. J Am Coll Cardiol. 2003;41:870-878.
49. Kalyanaraman B, Perez-Reyes E, Mason RP. Spin-trapping and direct electron spin resonance investigations of the redox metabolism of quinone anticancer drugs. Biochim Biophys Acta. 1980;630:119-130.
50. Green PS, Leeuwenburgh C. Mitochondrial dysfunction is an early indicator of doxorubicin-induced apoptosis. Biochim Biophys Acta. 2002;1588:94-101.
51. Benedetti S, Benvenuti F, Pagliarani S, et al. Antioxidant properties of a novel phycocyanin extract from the blue-green alga Aphanizomenon flos-aquae. Life Sci. 2004;75:2353-2362.
52. Solem LE, Heller LJ, Wallace KB. Dose-dependent increase in sensitivity to calcium-induced mitochondrial dysfunction and cardiomyocyte cell injury by doxorubicin. J Mol Cell Cardiol. 1996;28:1023-1032.
53. Chao DT, Korsmeyer SJ. BCL-2 family: regulators of cell death. Annu Rev Immunol. 1998;16:395-419.
54. Wu S, Ko YS, Teng MS, et al. Adriamycin-induced cardiomyocyte and endothelial cell apoptosis: in vitro and in vivo studies. J Mol Cell Cardiol. 2002;34:1595-1607.
55. Wang L, Ma W, Markovich R, et al. Insulin-like growth factor I modulates induction of apoptotic signaling in H9C2 cardiac muscle cells. Endocrinology. 1998;139:1354-1360.
56. Bialik S, Cryns VL, Drincic A, et al. The mitochondrial apoptotic pathway is activated by serum and glucose deprivation in cardiac myocytes. Circ Res. 1999;85:403-414.
57. Green DR. Apoptotic pathways: paper wraps stone blunts scissors. Cell. 2000;102:1-4.
58. Pollack M, Leeuwenburgh C. Apoptosis and aging: role of the mitochondria. J Gerontol A Biol Sci Med Sci. 2001;56:B475-B482.
59. Kalyanaraman B, Joseph J, Kalivendi S, et al. Doxorubicin-induced apoptosis: implications in cardiotoxicity. Mol Cell Biochem. 2002;234-235:119-124.
60. Beere HM, Wolf BB, Cain K, et al. Heat-shock protein 70 inhibits apoptosis by preventing recruitment of procaspase-9 to the Apaf-1 apoptosome. Nat Cell Biol. 2000;2:469-475.
61. Upasani CD, Khera A, Balaraman R. Effect of lead with vitamin E, C, or Spirulina on malondialdehyde, conjugated dienes and hydroperoxides in rats. Indian J Exp Biol. 2001;39:70-74.
62. Konorev EA, Kotamraju S, Zhao H, et al. Paradoxical effects of metalloporphyrins on doxorubicin-induced apoptosis: scavenging of reactive oxygen species versus induction of heme oxygenase-1. Free Radic Biol Med. 2002;33:988.
63. Shioji K, Kishimoto C, Nakamura H, et al. Overexpression of thioredoxin-1 in transgenic mice attenuates adriamycin-induced cardiotoxicity. Circulation. 2002;106:1403-1409.
64. Yoshizumi M, Kogame T, Suzaki Y, et al. Ebselen attenuates oxidative stress-induced apoptosis via the inhibition of the c-Jun N-terminal kinase and activator protein-1 signalling pathway in PC12 cells. Br J Pharmacol. 2002;136:1023-1032.
65. Negoro S, Oh H, Tone E, et al. Glycoprotein 130 regulates cardiac myocyte survival in doxorubicin-induced apoptosis through phosphatidylinositol 3-kinase/Akt phosphorylation and Bcl-xL/caspase-3 interaction. Circulation. 2001;103:555-561.
66. Adderley SR, Fitzgerald DJ. Oxidative damage of cardiomyocytes is limited by extracellular regulated kinases 1/2-mediated induction of cyclooxygenase-2. J Biol Chem. 1999;274:5038-5046.
67. Cicconi S, Ventura N, Pastore D, et al. Characterization of apoptosis signal transduction pathways in HL-5 cardiomyocytes exposed to ischemia/reperfusion oxidative stress model. J Cell Physiol. 2003;195:27-37.
68. Ikeda S, Hamada M, Hiwada K. Cardiomyocyte apoptosis with enhanced expression of P53 and Bax in right ventricle after pulmonary arterial banding. Life Sci. 1999;65:925-933.