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BioMed Research International
Volume 2014, Article ID 240642, 8 pages
http://dx.doi.org/10.1155/2014/240642
Review Article

Animal Models in Studies of Cardiotoxicity Side Effects from Antiblastic Drugs in Patients and Occupational Exposed Workers

1Department of Experimental Medicine, Section of Hygiene, Occupational Medicine and Forensic Medicine, Area of Occupational Medicine, Second University of Naples, Via L. De Crecchio 7, 80138 Naples, Italy
2National Institute for the Study and Treatment of Cancer, Foundation “G. Pascale”, Via Mariano Semmola, 80131 Napoli, Italy
3Department of Biochemistry, Biophysics and General Pathology, Second University of Naples, Via L. De Crecchio 7, 80138 Naples, Italy
4Department of Radiology, Oncology and Pathological Anatomy Sciences, University of Rome, “La Sapienza”, Piazzale Aldo Moro 5, 00185 Rome, Italy
5Spencer-Lorillard Foundation, University of Rome, “La Sapienza”, Piazzale Aldo Moro 5, 00185 Rome, Italy
6Sbarro Institute for Cancer Research and Molecular Medicine, Center for Biotechnology, Building Suite 431, 1900 North 12th Street, Philadelphia, PA 19122, USA

Received 31 July 2013; Revised 29 October 2013; Accepted 7 November 2013; Published 19 February 2014

Academic Editor: Monica Fedele

Copyright © 2014 Monica Lamberti et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. T. H. Connor, G. DeBord, J. R. Pretty et al., “Evaluation of antineoplastic drug exposure of health care workers at three university-based US cancer centers,” Journal of Occupational and Environmental Medicine, vol. 52, no. 10, pp. 1019–1027, 2010. View at Publisher · View at Google Scholar · View at Scopus
  2. M. Pieri, L. Castiglia, P. Basilicata, N. Sannolo, A. Acampora, and N. Miraglia, “Biological monitoring of nurses exposed to doxorubicin and epirubicin by a validated liquid chromatography/fluorescence detection method,” The Annals of Occupational Hygiene, vol. 54, no. 4, pp. 368–376, 2010. View at Publisher · View at Google Scholar · View at Scopus
  3. K. J. Schimmel, D. J. Richel, R. B. van den Brink, and H. J. Guchelaar, “Cardiotoxicity of cytotoxic drugs,” Cancer Treatment Reviews, vol. 30, no. 2, pp. 181–191, 2004. View at Publisher · View at Google Scholar · View at Scopus
  4. Y. J. Kang, “Molecular and cellular mechanisms of cardiotoxicity,” Environmental Health Perspectives, vol. 109, supplement 1, pp. 27–34, 2001. View at Google Scholar · View at Scopus
  5. H. Broder, R. A. Gottlieb, and N. E. Lepor, “Chemotherapy and cardiotoxicity,” Reviews in Cardiovascular Medicine, vol. 9, no. 2, pp. 75–83, 2008. View at Google Scholar · View at Scopus
  6. C. Dechant, M. Baur, R. Bock et al., “Acute reversible heart failure caused by coronary vasoconstriction due to continuous 5-fluorouracil combination chemotherapy,” Case Reports in Oncology, vol. 5, no. 2, pp. 296–301, 2012. View at Publisher · View at Google Scholar
  7. L. Montella, M. Caraglia, R. Addeo et al., “Atrial fibrillation following chemotherapy for stage IIIE diffuse large B-cell gastric lymphoma in a patient with myotonic dystrophy (Steinert's disease),” Annals of Hematology, vol. 84, no. 3, pp. 192–193, 2005. View at Publisher · View at Google Scholar · View at Scopus
  8. F. S. Carvalho, A. Burgeiro, R. Garcia, A. J. Moreno, R. A. Carvalho, and P. J. Oliveira, “Doxorubicin-induced cardiotoxicity: from bioenergetic failure and cell death to cardiomyopathy,” Medicinal Research Reviews, vol. 34, no. 1, pp. 106–135, 2014. View at Publisher · View at Google Scholar
  9. J. B. Vermorken, “The integration of paclitaxel and new platinum compounds in the treatment of advanced ovarian cancer,” International Journal of Gynecological Cancer, vol. 11, supplement s1, pp. 21–30, 2001. View at Publisher · View at Google Scholar · View at Scopus
  10. S. Y. Saad, T. A. Najjar, and M. Alashari, “Cardiotoxicity of doxorubicin/paclitaxel combination in rats: effect of sequence and timing of administration,” Journal of Biochemical and Molecular Toxicology, vol. 18, no. 2, pp. 78–86, 2004. View at Publisher · View at Google Scholar · View at Scopus
  11. M. Lamberti, M. Caraglia, S. Zappavigna et al., “Evaluation in vitro of the cardiotoxic effects of 5-fluorouracil for the prevention of cardiovascular damage in health workers occupationally exposed,” Giornale Italiano di Medicina del Lavoro ed Ergonomia, vol. 33, no. 3, supplement, pp. 298–302, 2011. View at Google Scholar
  12. M. Lamberti, S. Porto, M. Marra et al., “5-Fluorouracil induces apoptosis in rat cardiocytes through intracellular oxidative stress,” Journal of Experimental & Clinical Cancer Research, vol. 31, article 60, 2012. View at Publisher · View at Google Scholar
  13. B. B. Hasinoff, “The cardiotoxicity and myocyte damage caused by small molecule anticancer tyrosine kinase inhibitors is correlated with lack of target specificity,” Toxicology and Applied Pharmacology, vol. 244, no. 2, pp. 190–195, 2010. View at Publisher · View at Google Scholar · View at Scopus
  14. M. Indinnimeo, A. Impagnatiello, G. D’Ettorre et al., “Buschke-Löwenstein tumor with squamous cell carcinoma treated with chemo-radiation therapy and local surgical excision: report of three cases,” World Journal of Surgical Oncology, vol. 11, article 231, 2013. View at Publisher · View at Google Scholar
  15. M. Lotrionte, G. Biondi-Zoccai, A. Abbate et al., “Review and meta-analysis of incidence and clinical predictors of anthracycline cardiotoxicity,” The American Journal of Cardiology, vol. 112, no. 12, pp. 1980–1984, 2013. View at Publisher · View at Google Scholar
  16. V. Brower, “Cardiotoxicity debated for anthracyclines and trastuzumab in breast cancer,” Journal of the National Cancer Institute, vol. 105, no. 12, pp. 835–836, 2013. View at Publisher · View at Google Scholar
  17. V. Chintalgattu, M. L. Rees, J. C. Culver et al., “Coronary microvascular pericytes are the cellular target of sunitinib malate-induced cardiotoxicity,” Science Translational Medicine, vol. 5, no. 187, p. 187ra69, 2013. View at Publisher · View at Google Scholar
  18. M. Wasowska, I. Oszczapowicz, J. Wietrzyk et al., “Influence of the structure of new anthracycline antibiotics on their biological properties,” Anticancer Research, vol. 25, no. 3, pp. 2043–2048, 2005. View at Google Scholar
  19. R. Danesi, S. Fogli, A. Gennari, P. Conte, and M. Del Tacca, “Pharmacokinetic-pharmacodynamic relationships of the anthracycline anticancer drugs,” Clinical Pharmacokinetics, vol. 41, no. 6, pp. 431–444, 2002. View at Publisher · View at Google Scholar · View at Scopus
  20. E. Jirkovský, O. Lenčová-Popelová, M. Hroch et al., “Early and delayed cardioprotective intervention with dexrazoxane each show different potential for prevention of chronic anthracycline cardiotoxicity in rabbits,” Toxicology, vol. 311, no. 3, pp. 191–204, 2013. View at Publisher · View at Google Scholar
  21. S. Gillings, J. Johnson, A. Fulmer, and M. Hauck, “Effect of a 1-hour IV infusion of doxorubicin on the development of cardiotoxicity in dogs as evaluated by electrocardiography and echocardiography,” Veterinary Therapeutics, vol. 10, no. 1-2, pp. 46–58, 2009. View at Google Scholar · View at Scopus
  22. D. Beulz-Riche, J. Robert, C. Menard, and D. Ratanasavanh, “Metabolism of methoxymorpholino-doxorubicin in rat, dog and monkey liver microsomes: comparison with human microsomes,” Fundamental and Clinical Pharmacology, vol. 15, no. 6, pp. 373–378, 2001. View at Publisher · View at Google Scholar · View at Scopus
  23. M. Tokarska-Schlattner, M. Dolder, I. Gerber, O. Speer, T. Wallimann, and U. Schlattner, “Reduced creatine-stimulated respiration in doxorubicin challenged mitochondria: particular sensitivity of the heart,” Biochimica et Biophysica Acta, vol. 1767, no. 11, pp. 1276–1284, 2007. View at Publisher · View at Google Scholar · View at Scopus
  24. M. A. Parker, V. King, and K. P. Howard, “Nuclear magnetic resonance study of doxorubicin binding to cardiolipin containing magnetically oriented phospholipid bilayers,” Biochimica et Biophysica Acta, vol. 1514, no. 2, pp. 206–216, 2001. View at Publisher · View at Google Scholar · View at Scopus
  25. J. Vásquez-Vivar, P. Martasek, N. Hogg, B. S. Masters, K. A. Pritchard Jr., and B. Kalyanaraman, “Endothelial nitric oxide synthase-dependent superoxide generation from adriamycin,” Biochemistry, vol. 36, no. 38, pp. 11293–11297, 1997. View at Publisher · View at Google Scholar · View at Scopus
  26. K. A. Sauter, L. J. Wood, J. Wong, M. Iordanov, and B. E. Magun, “Doxorubicin and daunorubicin induce processing and release of interleukin-1β through activation of the NLRP3 inflammasome,” Cancer Biology and Therapy, vol. 11, no. 12, pp. 1008–1016, 2011. View at Publisher · View at Google Scholar · View at Scopus
  27. Y. Ma, T. Yamazaki, H. Yang et al., “Tumor necrosis factor is dispensable for the success of immunogenic anticancer chemotherapy,” Oncoimmunology, vol. 2, no. 6, Article ID e24786, 2013. View at Publisher · View at Google Scholar
  28. C. D. Aluise, S. Miriyala, T. Noel et al., “2-Mercaptoethane sulfonate prevents doxorubicin-induced plasma protein oxidation and TNF-α release: implications for the reactive oxygen species-mediated mechanisms of chemobrain,” Free Radical Biology and Medicine, vol. 50, no. 11, pp. 1630–1638, 2011. View at Publisher · View at Google Scholar · View at Scopus
  29. E. Chiosi, A. Spina, A. Sorrentino et al., “Change in TNF-α receptor expression is a relevant event in doxorubicin-induced H9c2 cardiomyocyte cell death,” Journal of Interferon and Cytokine Research, vol. 27, no. 7, pp. 589–597, 2007. View at Publisher · View at Google Scholar · View at Scopus
  30. H. A. Gambliel, B. E. Burke, B. J. Cusack et al., “Doxorubicin and C-13 deoxydoxorubicin effects on ryanodine receptor gene expression,” Biochemical and Biophysical Research Communications, vol. 291, no. 3, pp. 433–438, 2002. View at Publisher · View at Google Scholar · View at Scopus
  31. M. Verma, N. Shulga, and J. G. Pastorino, “Sirtuin-4 modulates sensitivity to induction of the mitochondrial permeability transition pore,” Biochimica et Biophysica Acta, vol. 1827, no. 1, pp. 38–49, 2013. View at Publisher · View at Google Scholar
  32. A. Ascensão, J. Lumini-Oliveira, N. G. Machado et al., “Acute exercise protects against calcium-induced cardiac mitochondrial permeability transition pore opening in doxorubicin-treated rats,” Clinical Science, vol. 120, no. 1, pp. 37–49, 2011. View at Publisher · View at Google Scholar · View at Scopus
  33. C. Richard, S. Ghibu, S. Delemasure-Chalumeau et al., “Oxidative stress and myocardial gene alterations associated with doxorubicin-induced cardiotoxicity in rats persist for 2 months after treatment cessation,” The Journal of Pharmacology and Experimental Therapeutics, vol. 339, no. 3, pp. 807–814, 2011. View at Publisher · View at Google Scholar · View at Scopus
  34. F. Rossi, W. Filippelli, S. Russo, A. Filippelli, and L. Berrino, “Cardiotoxicity of doxorubicin: effects of drugs inhibiting the release of vasoactive substances,” Pharmacology and Toxicology, vol. 75, no. 2, pp. 99–107, 1994. View at Google Scholar · View at Scopus
  35. T. Budde, J. Haney, S. Bien et al., “Acute exposure to doxorubicin results in increased cardiac P-glycoprotein expression,” Journal of Pharmaceutical Sciences, vol. 100, no. 9, pp. 3951–3958, 2011. View at Publisher · View at Google Scholar · View at Scopus
  36. H. Akimoto, N. A. Bruno, D. L. Slate, M. E. Billingham, S. V. Torti, and F. M. Torti, “Effect of verapamil on doxorubicin cardiotoxicity: altered muscle gene expression in cultured neonatal rat cardiomyocytes,” Cancer Research, vol. 53, no. 19, pp. 4658–4664, 1993. View at Google Scholar · View at Scopus
  37. P. Tagliaferri, P. Correale, M. Mottola et al., “Cardiovascular monitoring of drug-resistant lymphoma patients treated with epoch chemotherapy plus high dose verapamil in continuous-infusion,” Oncology Reports, vol. 1, no. 2, pp. 341–344, 1994. View at Google Scholar · View at Scopus
  38. H. Jacobs, R. Peters, G. J. den Hartog, W. J. van der Vijgh, A. Bast, and G. R. Haenen, “Identification of the metabolites of the antioxidant flavonoid 7-mono-O-(β-hydroxyethyl)-rutoside in mice,” Drug Metabolism and Disposition, vol. 39, no. 5, pp. 750–756, 2011. View at Publisher · View at Google Scholar · View at Scopus
  39. S. Arunachalam, S. Y. Kim, S. H. Lee et al., “Davallialactone protects against adriamycin-induced cardiotoxicity in vitro and in vivo,” Journal of Natural Medicines, vol. 66, no. 1, pp. 149–157, 2012. View at Publisher · View at Google Scholar · View at Scopus
  40. A. M. Osman, S. E. Al-Harthi, O. M. Alarabi et al., “Chemosensetizing and cardioprotective effects of resveratrol in doxorubicin-treated animals,” Cancer Cell International, vol. 13, article 52, 2013. View at Publisher · View at Google Scholar
  41. E. H. Herman, V. J. Ferrans, C. E. Myers, and J. F. Van Vleet, “Comparison of the effectiveness of (+/-)-1,2-bis(3,5-dioxopiperazinyl-1-yl)propane (ICRF-187) and N-acetylcysteine in preventing chronic doxorubicin cardiotoxicity in beagles,” Cancer Research, vol. 45, no. 1, pp. 276–281, 1985. View at Google Scholar · View at Scopus
  42. A. Carbone, P. J. Psaltis, A. J. Nelson et al., “Dietary omega-3 supplementation exacerbates left ventricular dysfunction in an ovine model of anthracycline-induced cardiotoxicity,” Journal of Cardiac Failure, vol. 18, no. 6, pp. 502–511, 2012. View at Publisher · View at Google Scholar
  43. A. Bast, G. R. Haenen, A. M. Bruynzeel, and W. J. van der Vijgh, “Protection by flavonoids against anthracycline cardiotoxicity: from chemistry to clinical trials,” Cardiovascular Toxicology, vol. 7, no. 2, pp. 154–159, 2007. View at Publisher · View at Google Scholar · View at Scopus
  44. C. D. Aluise, D. St Clair, M. Vore, and D. A. Butterfield, “In vivo amelioration of adriamycin induced oxidative stress in plasma by gamma-glutamylcysteine ethyl ester (GCEE),” Cancer Letters, vol. 282, no. 1, pp. 25–29, 2009. View at Publisher · View at Google Scholar · View at Scopus
  45. C. Myers, R. Bonow, S. Palmeri et al., “A randomized controlled trial assessing the prevention of doxorubicin cardiomyopathy by N-acetylcysteine,” Seminars in Oncology, vol. 10, no. 1, supplement 1, pp. 53–55, 1983. View at Google Scholar · View at Scopus
  46. G. Minotti, S. Licata, A. Saponiero et al., “Anthracycline metabolism and toxicity in human myocardium: comparisons between doxorubicin, epirubicin, and a novel disaccharide analogue with a reduced level of formation and [4Fe-4S] reactivity of its secondary alcohol metabolite,” Chemical Research in Toxicology, vol. 13, no. 12, pp. 1336–1341, 2000. View at Publisher · View at Google Scholar · View at Scopus
  47. O. S. Bains, M. J. Karkling, T. A. Grigliatti, R. E. Reid, and K. W. Riggs, “Two nonsynonymous single nucleotide polymorphisms of human carbonyl reductase 1 demonstrate reduced in vitro metabolism of daunorubicin and doxorubicin,” Drug Metabolism and Disposition, vol. 37, no. 5, pp. 1107–1114, 2009. View at Publisher · View at Google Scholar · View at Scopus
  48. P. S. Mushlin, B. J. Cusack, R. J. Boucek Jr., T. Andrejuk, X. Li, and R. D. Olson, “Time-related increases in cardiac concentrations of doxorubicin could interact with doxorubicin to depress myocardial contractile function,” British Journal of Pharmacology, vol. 110, no. 3, pp. 975–982, 1993. View at Google Scholar · View at Scopus
  49. G. L. Forrest, B. Gonzalez, W. Tseng, X. Li, and J. Mann, “Human carbonyl reductase overexpression in the heart advances the development of doxorubicin-induced cardiotoxicity in transgenic mice,” Cancer Research, vol. 60, no. 18, pp. 5158–5164, 2000. View at Google Scholar · View at Scopus
  50. R. Cirillo, G. Sacco, S. Venturella, J. Brightwell, A. Giachetti, and S. Manzini, “Comparison of doxorubicin-and MEN 10755-induced long-term progressive cardiotoxicity in the rat,” Journal of Cardiovascular Pharmacology, vol. 35, no. 1, pp. 100–108, 2000. View at Publisher · View at Google Scholar · View at Scopus
  51. P. G. Gervasi, M. R. Agrillo, A. Lippi, N. Bernardini, R. Danesi, and M. Del Tacca, “Superoxide anion production by doxorubicin analogs in heart sarcosomes and by mitochondrial NADH dehydrogenase,” Research Communications in Chemical Pathology and Pharmacology, vol. 67, no. 1, pp. 101–115, 1990. View at Google Scholar · View at Scopus
  52. R. J. Boucek Jr., R. D. Olson, D. E. Brenner, E. M. Ogunbunmi, M. Inui, and S. Fleischer, “The major metabolite of doxorubicin is a potent inhibitor of membrane-associated ion pumps: a correlative study of cardiac muscle with isolated membrane fractions,” The Journal of Biological Chemistry, vol. 262, no. 33, pp. 15851–15856, 1987. View at Google Scholar · View at Scopus
  53. G. Minotti, R. Ronchi, E. Salvatorelli, P. Menna, and G. Cairo, “Doxorubicin irreversibly inactivates iron regulatory proteins 1 and 2 in cardiomyocytes: evidence for distinct metabolic pathways and implications for iron-mediated cardiotoxicity of antitumor therapy,” Cancer Research, vol. 61, no. 23, pp. 8422–8428, 2001. View at Google Scholar · View at Scopus
  54. K. Gaurav, R. K. Goel, M. Shukla, and M. Pandey, “Glutamine: a novel approach to chemotherapy-induced toxicity,” Indian Journal of Medical and Paediatric Oncology, vol. 33, no. 1, pp. 13–20, 2012. View at Publisher · View at Google Scholar
  55. S. I. Glushkov, S. A. Kutsenko, T. M. Novikova, and V. V. Axenov, “Glutathione metabolism in rat cardiac tissues in acute doxorubicin-induced intoxication,” Voprosy Onkologii, vol. 51, no. 1, pp. 108–112, 2005. View at Google Scholar · View at Scopus
  56. H. Xue, D. Slavov, and P. E. Wischmeyer, “Glutamine-mediated dual regulation of heat shock transcription factor-1 activation and expression,” The Journal of Biological Chemistry, vol. 287, no. 48, pp. 40400–40413, 2012. View at Publisher · View at Google Scholar
  57. L. Liu, X.-J. Zhang, B. Qian, X.-Y. Min, and Y.-L. Cheng, “Heat shock protein 27 attenuated doxorubicin-induced myocardial damage by reducing cardiomyocyte apoptosis, mitochondria damage and protein carbonylation,” Zhonghua Xin Xue Guan Bing Za Zhi, vol. 36, no. 11, pp. 1021–1026, 2008. View at Google Scholar · View at Scopus
  58. P. E. Wischmeyer, D. Jayakar, U. Williams et al., “Single dose of glutamine enhances myocardial tissue metabolism, glutathione content, and improves myocardial function after ischemia-reperfusion injury,” Journal of Parenteral and Enteral Nutrition, vol. 27, no. 6, pp. 396–403, 2003. View at Google Scholar · View at Scopus
  59. R. A. Forrest, L. P. Swift, B. J. Evison et al., “The hydroxyl epimer of doxorubicin controls the rate of formation of cytotoxic anthracycline-DNA adducts,” Cancer Chemotherapy and Pharmacology, vol. 71, no. 3, pp. 809–816, 2013. View at Google Scholar
  60. O. Tacar, P. Sriamornsak, and C. R. Dass, “Doxorubicin: an update on anticancer molecular action, toxicity and novel drug delivery systems,” Journal of Pharmacy and Pharmacology, vol. 65, no. 2, pp. 157–170, 2013. View at Publisher · View at Google Scholar
  61. N. Ashley and J. Poulton, “Mitochondrial DNA is a direct target of anti-cancer anthracycline drugs,” Biochemical and Biophysical Research Communications, vol. 378, no. 3, pp. 450–455, 2009. View at Publisher · View at Google Scholar · View at Scopus
  62. C. F. Greineder, S. Kohnstamm, and B. Ky, “Heart failure associated with sunitinib: lessons learned from animal models,” Current Hypertension Reports, vol. 13, no. 6, pp. 436–441, 2011. View at Publisher · View at Google Scholar · View at Scopus
  63. M. Caraglia, G. Giuberti, M. Marra et al., “Oxidative stress and ERK1/2 phosphorylation as predictors of outcome in hepatocellular carcinoma patients treated with sorafenib plus octreotide LAR,” Cell Death and Disease, vol. 2, no. 4, article e150, 2011. View at Publisher · View at Google Scholar · View at Scopus
  64. A. Y. Khakoo, P. P. Liu, T. Force et al., “Cardiotoxicity due to cancer therapy,” Texas Heart Institute Journal, vol. 38, no. 3, pp. 253–256, 2011. View at Google Scholar · View at Scopus
  65. T. Force, D. S. Krause, and R. A. Van Etten, “Molecular mechanisms of cardiotoxicity of tyrosine kinase inhibition,” Nature Reviews Cancer, vol. 7, no. 5, pp. 332–344, 2007. View at Publisher · View at Google Scholar · View at Scopus
  66. R. Kerkela, K. C. Woulfe, J.-B. Durand et al., “Sunitinib-induced cardiotoxicity is mediated by off-target inhibition of AMP-activated protein kinase,” Clinical and Translational Science, vol. 2, no. 1, pp. 15–25, 2009. View at Publisher · View at Google Scholar · View at Scopus
  67. B. Yang and T. Papoian, “Tyrosine kinase inhibitor (TKI)-induced cardiotoxicity: approaches to narrow the gaps between preclinical safety evaluation and clinical outcome,” Journal of Applied Toxicology, vol. 32, no. 12, pp. 945–951, 2012. View at Publisher · View at Google Scholar
  68. D. Hannani, C. Locher, T. Yamazaki et al., “Contribution of humoral immune responses to the antitumor effects mediated by anthracyclines,” Cell Death and Differentiation, vol. 21, no. 1, pp. 50–58, 2014. View at Publisher · View at Google Scholar
  69. E. Senkus and J. Jassem, “Cardiovascular effects of systemic cancer treatment,” Cancer Treatment Reviews, vol. 37, no. 4, pp. 300–311, 2011. View at Publisher · View at Google Scholar · View at Scopus
  70. A. Pieniążek, J. Czepas, J. Piasecka-Zelga, K. Gwoździński, and A. Koceva-Chyła, “Oxidative stress induced in rat liver by anticancer drugs doxorubicin, paclitaxel and docetaxel,” Advances in Medical Sciences, vol. 58, no. 1, pp. 104–111, 2013. View at Publisher · View at Google Scholar
  71. K. Kandylis, M. Vassilomanolakis, S. Tsoussis, and A. P. Efremidis, “Ifosfamide cardiotoxicity in humans,” Cancer Chemotherapy and Pharmacology, vol. 24, no. 6, pp. 395–396, 1989. View at Google Scholar · View at Scopus
  72. J. Nuver, E. C. De Haas, Z. M. Van, J. A. Gietema, and C. Meijer, “Vascular damage in testicular cancer patients: a study on endothelial activation by bleomycin and cisplatin in vitro,” Oncology Reports, vol. 23, no. 1, pp. 247–253, 2010. View at Publisher · View at Google Scholar · View at Scopus
  73. F. Zhang, G. Suarez, J. Sha, J. C. Sierra, J. W. Peterson, and A. K. Chopra, “Phospholipase A2-activating protein (PLAA) enhances cisplatin-induced apoptosis in HeLa cells,” Cellular Signalling, vol. 21, no. 7, pp. 1085–1099, 2009. View at Publisher · View at Google Scholar · View at Scopus
  74. M. Bonifazi, M. Franchi, M. Rossi et al., “Trastuzumab-related cardiotoxicity in early breast cancer: a cohort study,” The Oncologist, vol. 18, no. 7, pp. 795–801, 2013. View at Publisher · View at Google Scholar