Doxorubicin induces an increase of nitric oxide synthesis in rat cardiac cells that is inhibited by iron supplementation

Toxicology and Applied Pharmacology

Volumn 185, Issue 2, 2002, Pages 85-90

  Aldieri, Elisabetta ^a   Bergandi, Loredana ^a   Riganti, Chiara ^a   Costamagna, Costanzo ^a   Bosia, Amalia ^a   Ghigo, Dario ^a  

^a UNIVERSITY OF TURIN   (Italy)

Author keywords

Desferrioxamine; Ferric nitrilotri acetate; Hypoxia responsive enhancer; Iron regulatory protein; Iron responsive element; Nitric oxide; Nitric oxide synthase; Nitrilotriacetate; Nuclear factor interleukin 6; Reverse transcription polymerase chain reaction

Indexed keywords

DOXORUBICIN; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NITRILOTRIACETATE IRON; NITRITE;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DOSE RESPONSE; DRUG EFFECT; ENZYME ACTIVITY; GENE EXPRESSION; HEART MUSCLE CELL; HOMEOSTASIS; NONHUMAN; RAT; RNA TRANSCRIPTION; SUPPLEMENTATION; SYNTHESIS;

EID: 0036939363     PISSN: 0041008X     EISSN: None     Source Type: Journal    
DOI: 10.1006/taap.2002.9527     Document Type: Article

References (42)

1. Aldieri, E., Ghigo, D., Tomatis, M., Prandi, L., Fenoglio, I., Costamagna, C., Pescarmona, G., Bosia, A., and Fubini, B. (2001). Iron inhibits the nitric oxide synthesis elicited by asbestos in murine macrophages. Free Radical Biol. Med. 31, 412-417.
2. Bani, D., Masini, E., Bello, M. G., Bigazzi, M., and Bani Sacchi, T. (1995). Relaxin activates the L-arginine-nitric oxide pathway in human breast cancer cells. Cancer Res. 55, 5272-5275.
3. Brown, G. C. (1999). Nitric oxide and mitochondrial respiration. Biochim. Biophys. Acta 1411, 351-369.
4. Byrd, T. F., and Horwitz, M. A. (1991). Chloroquine inhibits the intracellular multiplication of Legionella pneumophila by limiting the availability of iron: A potential new mechanism for the therapeutic effect of chloroquine against intracellular pathogens. J. Clin. Invest. 88, 351-357.
5. Chomczynski, P., and Sacchi, N. (1987). Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162, 156-159.
6. Di Marco, A. (1975). Adriamycin (NSC-123127): Mode and mechanism of action. Cancer Chemother. Rep. 6, 91-106.
7. Dinapoli, M. R., Calderon, C. L., and Lopez, D. M. (1996). The altered tumoricidal capacity of macrophages isolated from tumor-bearing mice is related to reduce expression of the inducible nitric oxide synthase gene. J. Exp. Med. 183, 1323-1329.
8. Dlaska, M., and Weiss, G. (1999). Central role of transcription factor NF-IL6 for cytokine and iron-mediated regulation of murine inducible nitric oxide synthase expression. J. Immunol. 162, 6171-6177.
9. Dong, Z., Staroselsky, A. H., Qi, X., Xie, K., and Fidler, I. J. (1994). Inverse correlation between expression of inducible nitric oxide synthase activity and production of metastasis in K-1735 murine melanoma cells. Cancer. Res. 54, 789-793.
10. Doroshow, J. H. (1983). Effect of antracycline antibiotics on oxygen radical formation in rat heart. Cancer Res. 43, 460-472.
11. Dorr, R. T. (1996). Cytoprotective agents for anthracyclines. Semin. Oncol. 23, 23-34.
12. Ghigo, D., Aldieri, E., Todde, R., Costamagna, C., Garbarino, G., Pescarmona, G., and Bosia, A. (1998). Chloroquine stimulates nitric oxide synthesis in murine, porcine, and human endothelial cells. J. Clin. Invest. 102, 595-605.
13. Haywood, G. A., Tsao, P. S., von der Leyen, H. E., Mann, M. J., Keeling, P. J., Trindade, P. T., Lewis, N. P., Byrne, C. D., Rickenbacher, P. R., Bishopric, N. H., Cooke, J. P., McKenna, W. J., and Fowler, M. B. (1996). Expression of inducible nitric oxide synthase in human heart failure. Circulation 15, 1087-1094.
14. Igarashi, J., Nishida, M., Hoshida, S., Yamashita, N., Kosaka, H., Hori, M., Kuzuya, T., and Tada, M. (1998). Inducible nitric oxide synthase augments injury elicited by oxidative stress in rat cardiac myocytes. Am. J. Physiol. 274, 245-252.
15. Joshi, P., Vig, P. J. S., Veerisetty, V., Cameron, J. A., Sekhon, B. S., and Desaiah, D. (1996). Increase in brain nitric oxide synthase activity in daunorubicin-treated rats. Pharmacol. Toxicol. 78, 99-103.
16. Kalivendi, S. V., Kotamraju, S., Zhao, H., Joseph, J., and Kalyanaraman, B. (2001). Doxorubicin-induced apoptosis is associated with increased transcription of endothelial nitric-oxide synthase: Effect of antiapoptotic antioxidants and calcium. J. Biol. Chem. 276, 47266-47276.
17. Kelm, M. (1999). Nitric oxide metabolism and breakdown. Biochim. Biophys. Acta 1411, 273-289.
18. Krogstad, D. J., and Schlesinger, P. H. (1987). Acid-vesicle function, intracellular pathogens, and the action of chloroquine against Plasmodium falciparum. N. Engl. J. Med. 317, 542-549.
19. Lind, D. S., Kontaridis, M. I., Edwards, P. D., Josephs, M. D., Moldawer, L. L., and Copeland III E. M. (1997). Nitric oxide contributes to adriamycin's antitumor effect. J. Surg. Res. 69, 283-287, doi: 10.1006/jsre.1997.5015.
20. Magrinat, G., Mason, S. N., Shami, P. J., and Weinberg, J. B. (1992). Nitric oxide modulation of human leukemia cell differentiation and gene expression. Blood 80, 1880-1884.
21. Mayer, L. D., Bally, M. B., and Culli, P. R. (1986). Uptake of adriamycin into large unilamellar vesicles in response to a pH gradient. Biochim. Biophys. Acta 857, 123-126.
22. Melillo, G., Taylor, L. S., Brooks, A., Musso, T., Cox, G. W., and Varesio, L. (1997). Functional requirement of the hypoxia-responsive element in the activation of the inducible nitric oxide synthase promoter by the iron chelator desferrioxamine. J. Biol. Chem. 272, 12236-12243.
23. Minotti, G., Cavaliere, A. F., Mordente, A., Rossi, M., Schiavello, R., Zamparelli, R., and Possati, G. F. (1995). Secondary alcohol metabolites mediate iron delocalization in cytosolic fractions of myocardial biopsies exposed to anticancer anthracyclines. J. Clin. Invest. 95, 1595-1605.
24. Molina y Vedia, L., McDonald, B., Reep, B., Brüne, B., Di Silvio, M., Billiar, T. R., and Lapetina, E. (1992). Nitric oxide-induced S-nitrosylation of glyceraldehyde-3-phosphate dehydrogenase inhibits enzymatic activity and increases endogenous ADP-ribosylation. J. Biol. Chem. 267, 24929-24932.
25. Mostafa, A. M., Nagi, M. N., Al Rikabi, A. C., Al-Shabanah, O. A., and El-Kashef, H. A. (1999). Protective effect of aminoguanidine against cardiovascular toxicity of chronic doxorubicin treatment in rats. Res. Commun. Mol. Pathol. Pharmacol. 106, 193-202.
26. Murphy, M. P. (1999). Nitric oxide and cell death. Biochim. Biophys. Acta 1411, 401-414.
27. Myers, C. (1998). The role of iron in doxorubicin-induced cardiomyopathy. Semin. Oncol. 25, 10-14.
28. Nathan, C. (1997). Inducible nitric oxide synthase: What difference does it make? J. Clin. Invest. 100, 2417-2423.
29. Olson, R. D., and Mushlin, P. S. (1990). Doxorubicin cardiotoxicity: Analysis of prevailing hypotheses. FASEB J. 4, 3076-3086.
30. Palmer, R. M. J., Ashton, D. S., and Moncada, S. (1988). Vascular endothelial cells synthesize nitric oxide from L-arginine. Nature 333, 664-666.
31. Riganti, C., Aldieri, E., Bergandi, L., Fenoglio, I., Costamagna, C., Fubini, B., Bosia, A., and Ghigo, D. (2002). Crocidolite asbestos inhibits pentose phosphate oxidative pathway and glucose 6-phosphate dehydrogenase activity in human lung epithelial cells. Free Radical Biol. Med. 32, 938-949.
32. Singal, P. K., and Iliskovic, N. (1998). Doxorubicin-induced cardiomyopathy. N. Engl. J. Med. 339, 900-905.
33. Stamler, J. S. (1994). Redox signaling: Nitrosylation and related target interactions of nitric oxide. Cell 78, 931-936.
34. Son, K., and Kim, Y. M. (1995). In vivo cisplatin-exposed macrophages increase immunostimulant-induced nitric oxide synthesis for tumor cell killing. Cancer Res. 55, 5524-5527.
35. Stefanelli, C., Pignatti, C., Tantini, B., Stanic, I., Bonavita, F., Muscari, C., Guarnieri, C., Clo, C., and Caldarera, C. M. (1999). Nitric oxide can function as either a killer molecule or an antiapoptotic effector in cardiomyocytes. Biocim. Biophys. Acta 1450, 406-413.
36. Stuehr, D. J. (1999). Mammalian nitric oxide synthases. Biochim. Biophys. Acta 1411, 217-230.
37. Swain, S. M. (1998). Adult multicenter trials using dexrazoxane to protect against cardiac toxicity. Semin. Oncol. 25, 43-47.
38. Tamir, S., and Tannenbaum, S. R. (1996). The role of nitric oxide (NO) in the carcinogenic process. Biochim. Biophys. Acta 1288, F31-F36.
39. Varin, R., Mulder, P., Richard, V., Tamion, F., Devaux, C., Henry, J. P., Lallemand, F., Lerebours, G., and Thuillez, C. (1999). Exercise improves flow-mediated vasodilatation of skeletal muscle arteries in rats with chronic heart failure: Role of nitric oxide, prostanoids, and oxidant stress. Circulation 99, 2951-2957.
40. Vàsquez-Vivar, J., Martasek, P., Hogg, N., Siler Masters, B. S., Pritchard, K. A., Jr., and Kalyanaraman, B. (1997). Endothelial nitric oxide synthase-dependent superoxide generation from adriamycin. Biochemistry 36, 11293-11297.
41. Weinstein, D. M., Mihm, M. J., and Bauer, J. A. (2000). Cardiac peroxynitrite formation and left ventricular dysfunction following doxorubicin treatment in mice. J. Pharmacol. Exp. Ther. 294, 396-401.
42. Weiss, G., Werner-Felmayer, G., Werner, E. R., Grünewald, K., Wachter, H., and Hentze, M. W. (1994). Iron regulates nitric oxide synthase activity by controlling nuclear transcription. J. Exp. Med. 180, 969-976.