Protective effects of ω-3 PUFA in anthracycline-induced cardiotoxicity: A critical review

Carregando...
Imagem de Miniatura
Citações na Scopus
19
Tipo de produção
article
Data de publicação
2017
Título da Revista
ISSN da Revista
Título do Volume
Editora
MDPI AG
Autores
SERINI, S.
GOMES, R. N.
CALVIELLO, G.
Citação
INTERNATIONAL JOURNAL OF MOLECULAR SCIENCES, v.18, n.12, article ID 2689, p, 2017
Projetos de Pesquisa
Unidades Organizacionais
Fascículo
Resumo
It has been demonstrated that ω-3 polyunsaturated fatty acids (ω-3 PUFA) may exert a beneficial role as adjuvants in the prevention and treatment of many disorders, including cardiovascular diseases and cancer. Particularly, several in vitro and in vivo preclinical studies have shown the antitumor activity of ω-3 PUFA in different kinds of cancers, and several human studies have shown that ω-3 PUFA are able to decrease the risk of a series of cardiovascular diseases. Several mechanisms have been proposed to explain their pleiotropic beneficial effects. ω-3 PUFA have also been shown to prevent harmful side-effects (including cardiotoxicity and heart failure) induced by conventional and innovative anti-cancer drugs in both animals and patients. The available literature regarding the possible protective effects of ω-3 PUFA against anthracycline-induced cardiotoxicity, as well as the mechanisms involved, will be critically discussed herein. The study will analyze the critical role of different levels of ω-3 PUFA intake in determining the results of the combinatory studies with anthracyclines. Suggestions for future research will also be considered. © 2017 by the authors. Licensee MDPI, Basel, Switzerland.
Palavras-chave
Anthracyclines, Cardioprotection, Cardiotoxicity, Chemotherapy, ω-3 PUFA
Referências
  1. Lee, J.Y., Sim, T.B., Lee, J.E., Na, H.K., Chemopreventive and chemotherapeutic effects of fish oil derived ω-3 polyunsaturated fatty acids on colon carcinogenesis (2017) Clin. Nutr. Res, 6, pp. 147-160. , [CrossRef] [PubMed]
  2. Liu, J., Ma, D.W., The role of n-3 polyunsaturated fatty acids in the prevention and treatment of breast cancer (2014) Nutrients, 6, pp. 5184-5223. , [CrossRef] [PubMed]
  3. Endo, J., Arita, M., Cardioprotective mechanism of ω-3 polyunsaturated fatty acids (2016) J. Cardiol, 67, pp. 22-27. , [CrossRef] [PubMed]
  4. Devassy, J.G., Leng, S., Gabbs, M., Monirujjaman, M., Aukema, H.M., Ω-3 polyunsaturated fatty acids and oxylipins in neuroinflammation and management of Alzheimer disease (2016) Adv. Nutr, 7, pp. 905-916. , [CrossRef] [PubMed]
  5. Calviello, G., Su, H.M., Weylandt, K.H., Fasano, E., Serini, S., Cittadini, A., Experimental evidence of ω-3 polyunsaturated fatty acid modulation of inflammatory cytokines and bioactive lipid mediators: Their potential role in inflammatory, neurodegenerative, and neoplastic diseases (2013) BioMed Res. Int, 2013, p. 743171. , [CrossRef] [PubMed]
  6. Ma, D.W., Seo, J., Davidson, L.A., Callaway, E.S., Fan, Y.Y., Lupton, J.R., Chapkin, R.S., n-3 PUFA alter caveolae lipid composition and resident protein localization in mouse colon (2004) FASEB J, 18, pp. 1040-1042. , [CrossRef] [PubMed]
  7. Serini, S., Ottes Vasconcelos, R., Fasano, E., Calviello, G., Epigenetic regulation of gene expression and M2 macrophage polarization as new potential ω-3 polyunsaturated fatty acid targets in colon inflammation and cancer (2016) Expert Opin. Ther. Targets, 20, pp. 843-858. , [CrossRef] [PubMed]
  8. Serini, S., Calviello, G., Reduction of oxidative/nitrosative stress in brain and its involvement in the neuroprotective effect of n-3 PUFA in Alzheimer’s disease (2016) Curr. Alzheimer Res, 13, pp. 123-134. , [CrossRef] [PubMed]
  9. Eltweri, A.M., Thomas, A.L., Metcalfe, M., Calder, P.C., Dennison, A.R., Bowrey, D.J., Potential applications of fish oils rich in ω-3 polyunsaturated fatty acids in the management of gastrointestinal cancer (2017) Clin. Nutr, 36, pp. 65-78. , [CrossRef] [PubMed]
  10. Calviello, G., Serini, S., Piccioni, E., n-3 polyunsaturated fatty acids and the prevention of colorectal cancer:Molecular mechanisms involved (2007) Curr. Med. Chem, 14, pp. 3059-3069. , [CrossRef] [PubMed]
  11. Serini, S., Calviello, G., Modulation of Ras/ERK and phosphoinositide signaling by long-chain n-3 PUFA in breast cancer and their potential complementary role in combination with targeted drugs (2017) Nutrients, 9, p. 185. , [CrossRef] [PubMed]
  12. Serini, S., Piccioni, E., Merendino, N., Calviello, G., Dietary polyunsaturated fatty acids as inducers of apoptosis: Implications for cancer (2009) Apoptosis, 14, pp. 135-152. , [CrossRef] [PubMed]
  13. Serini, S., Ottes Vasconcelos, R., Fasano, E., Calviello, G., How plausible is the use of dietary n-3 PUFA in the adjuvant therapy of cancer? (2016) Nutr. Res. Rev, 29, pp. 102-125. , [CrossRef] [PubMed]
  14. Merendino, N., Costantini, L., Manzi, L., Molinari, R., D’Eliseo, D., Velotti, F., Dietary ω-3 polyunsaturated fatty acid DHA: A potential adjuvant in the treatment of cancer (2013) BioMed Res. Int, 2013, p. 310186. , [CrossRef] [PubMed]
  15. Ghigo, A., Li, M., Hirsch, E., New signal transduction paradigms in anthracycline-induced cardiotoxicity (2016) Biochim. Biophys. Acta, 1863, pp. 1916-1925. , [CrossRef] [PubMed]
  16. World Health Organization, , http://www.who.int/mediacentre/factsheets/fs317/en/, Available online, (accessed on 7 November 2017)
  17. Ravera, A., Carubelli, V., Sciatti, E., Bonadei, I., Gorga, E., Cani, D., Vizzardi, E., Lombardi, C., Nutrition and cardiovascular disease: Finding the perfect recipe for cardiovascular health (2016) Nutrients, 8, p. 363. , [CrossRef] [PubMed]
  18. Spencer, R.M., Heidecker, B., Ganz, P., Behavioral cardiovascular risk factors-effect of physical activity and cardiorespiratory fitness on cardiovascular outcomes (2016) Circ. J, 80, pp. 34-43. , [CrossRef] [PubMed]
  19. Bowen, K.J., Harris, W.S., Kris-Etherton, P.M., Ω-3 fatty acids and cardiovascular disease: Are there benefits? (2016) Curr. Treat. Options Cardiovasc. Med, 18, p. 69. , [CrossRef] [PubMed]
  20. Calder, P.C., Ω-3 polyunsaturated fatty acids and inflammatory processes: Nutrition or pharmacology? (2013) Br. J. Clin. Pharmacol, 75, pp. 645-662. , [CrossRef] [PubMed]
  21. Yang, Z.H., Emma-Okon, B., Remaley, A.T., Dietary marine-derived long-chain monounsaturated fatty acids and cardiovascular disease risk: A mini review (2016) Lipids Health Dis, 15, p. 201. , [CrossRef] [PubMed]
  22. Chiesa, G., Busnelli, M., Manzini, S., Parolini, C., Nutraceuticals and bioactive components from fish for dyslipidemia and cardiovascular risk reduction (2016) Mar. Drugs, 14, p. 113. , [CrossRef] [PubMed]
  23. Weisman, D., Beinart, R., Erez, A., Koren-Morag, N., Goldenberg, I., Eldar, M., Glikson, M., Luria, D., Effect of supplemented intake of ω-3 fatty acids on arrhythmias in patients with ICD: Fish oil therapy may reduce ventricular arrhythmia (2017) J. Interv. Card. Electrophysiol, 49, pp. 255-261. , [CrossRef] [PubMed]
  24. Phang, M., Lincz, L.F., Garg, M.L., Eicosapentaenoic and docosahexaenoic acid supplementations reduce platelet aggregation and hemostatic markers differentially in men and women (2013) J. Nutr, 143, pp. 457-463. , [CrossRef] [PubMed]
  25. Li, X., Ballantyne, L.L., Che, X., Mewburn, J.D., Kang, J.X., Barkley, R.M., Murphy, R.C., Funk, C.D., Endogenously generated ω-3 fatty acids attenuate vascular inflammation and neointimal hyperplasia by interaction with free fatty acid receptor 4 in mice (2015) J. Am. Heart. Assoc, 4. , [CrossRef] [PubMed]
  26. Backes, J., Anzalone, D., Hilleman, D., Catini, J., The clinical relevance of ω-3 fatty acids in the management of hypertriglyceridemia (2016) Lipids Health Dis, 15, p. 118. , [CrossRef] [PubMed]
  27. Colussi, G., Catena, C., Novello, M., Bertin, N., Sechi, L.A., Impact of ω-3 polyunsaturated fatty acids on vascular function and blood pressure: Relevance for cardiovascular outcomes (2017) Nutr. Metab. Cardiovasc. Dis, 27, pp. 191-200. , [CrossRef] [PubMed]
  28. Sauder, K.A., Skulas-Ray, A.C., Campbell, T.S., Johnson, J.A., Kris-Etherton, P.M., West, S.G., Effects of ω-3 fatty acid supplementation on heart rate variability at rest and during acute stress in adults with moderate hypertriglyceridemia (2013) Psychosom. Med, 75, pp. 382-389. , [CrossRef] [PubMed]
  29. Hansen, A.L., Dahl, L., Olson, G., Thornton, D., Graff, I.E., Frøyland, L., Thayer, J.F., Pallesen, S., Fish consumption, sleep, daily functioning, and heart rate variability (2014) J. Clin. Sleep Med, 10, pp. 567-575. , [CrossRef] [PubMed]
  30. Biondo, P.D., Brindley, D.N., Sawyer, M.B., Field, C.J., The potential for treatment with dietary long-chain polyunsaturated n-3 fatty acids during chemotherapy (2008) J. Nutr. Biochem, 19, pp. 787-796. , [CrossRef] [PubMed]
  31. Serini, S., Piccioni, E., Calviello, G., ω-3 PUFAs and colon cancer: Experimental studies and human interventional trials (2010) Dietary Ω-3 Polyunsaturated Fatty Acids and Cancer, 1, pp. 67-89. , Calviello, G., Serini, S., Eds, Springer: New York, NY, USA, ISBN 978-90-481-3578-3
  32. Stillwell, W., Jenski, L.J., Crump, F.T., Ehringer, W., Effect of docosahexaenoic acid on mouse mitochondrial membrane properties (1997) Lipids, 32, pp. 497-506. , [CrossRef] [PubMed]
  33. Turk, H.F., Chapkin, R.S., Membrane lipid raft organization is uniquely modified by n-3 polyunsaturated fatty acids (2013) Prostaglandins Leukot. Essent. Fat. Acids, 88, pp. 43-47. , [CrossRef] [PubMed]
  34. Calviello, G., Serini, S., Palozza, P., n-3 polyunsaturated fatty acids as signal transduction modulators and therapeutical agents in cancer (2006) Curr. Signal Transdust. Ther, 1, pp. 255-271. , [CrossRef]
  35. Gillet, L., Roger, S., Bougnoux, P., Le Guennec, J.Y., Besson, P., Beneficial effects of ω-3 long-chain fatty acids in breast cancer and cardiovascular diseases: Voltage-gated sodium channels as a common feature? (2011) Biochimie, 93, pp. 4-6. , [CrossRef] [PubMed]
  36. Ferrier, G.R., Redondo, I., Zhu, J., Murphy, M.G., Differential effects of docosahexaenoic acid on contractions and L-type Ca2+ current in adult cardiac myocytes (2002) Cardiovasc. Res, 54, pp. 601-610. , [CrossRef]
  37. Sansbury, B.E., Spite, M., Resolution of acute inflammation and the role of resolvins in immunity, thrombosis, and vascular biology (2016) Circ. Res, 119, pp. 113-130. , [CrossRef] [PubMed]
  38. Wu, B., Mottola, G., Schaller, M., Upchurch, G.R., Jr., Conte, M.S., Resolution of vascular injury: Specialized lipid mediators and their evolving therapeutic implications (2017) Mol. Asp. Med, 58, pp. 72-82. , [CrossRef] [PubMed]
  39. Zivkovic, A.M., Telis, N., German, J.B., Hammock, B.D., Dietary ω-3 fatty acids aid in the modulation of inflammation and metabolic health (2011) Calif. Agric, 65, pp. 106-111. , [CrossRef] [PubMed]
  40. Russo, G.L., Dietary n-6 and n-3 polyunsaturated fatty acids: From biochemistry to clinical implications in cardiovascular prevention (2009) Biochem. Pharmacol, 77, pp. 937-946. , [CrossRef] [PubMed]
  41. Serhan, C.N., Treating inflammation and infection in the 21st century: New hints from decoding resolution mediators and mechanisms (2017) FASEB J, 31, pp. 1273-1288. , [CrossRef] [PubMed]
  42. Calder, P.C., The role of marine ω-3 (n-3) fatty acids in inflammatory processes, atherosclerosis and plaque stability (2012) Mol. Nutr. Food Res, 56, pp. 1073-1080. , [CrossRef] [PubMed]
  43. Wong, A.T., Chan, D.C., Ooi, E.M., Ng, T.W., Watts, G.F., Barrett, P.H., Ω-3 fatty acid ethyl ester supplementation decreases very-low-density lipoprotein triacylglycerol secretion in obese men (2013) Clin. Sci. Lond, 125, pp. 45-51. , [CrossRef] [PubMed]
  44. Sampath, H., Ntambi, J.M., Polyunsaturated fatty acid regulation of genes of lipid metabolism (2005) Annu. Rev. Nutr, 25, pp. 317-340. , [CrossRef] [PubMed]
  45. Kimura, R., Takahashi, N., Lin, S., Goto, T., Murota, K., Nakata, R., Inoue, H., Kawada, T., DHA attenuates postprandial hyperlipidemia via activating PPARα in intestinal epithelial cells (2013) J. Lipid Res, 54, pp. 3258-3268. , [CrossRef] [PubMed]
  46. Adkins, Y., Kelley, D.S., Mechanisms underlying the cardioprotective effects of ω-3 polyunsaturated fatty acids (2010) J. Nutr. Biochem, 21, pp. 781-792. , [CrossRef] [PubMed]
  47. Newell, M., Baker, K., Postovit, L.M., Field, C.J., A critical review on the effect of docosahexaenoic acid (DHA) on cancer cell cycle (2017) Int. J. Mol. Sci, 18, p. 1784. , [CrossRef] [PubMed]
  48. Song, E.A., Kim, H., Docosahexaenoic acid induces oxidative DNA damage and apoptosis, and enhances the chemosensitivity of cancer cells (2016) Int. J. Mol. Sci, 17, p. 1257. , [CrossRef] [PubMed]
  49. Spencer, L., Mann, C., Metcalfe, M., Webb, M., Pollard, C., Spencer, D., Berry, D., Dennison, A., The effect of ω-3 FAs on tumour angiogenesis and their therapeutic potential (2009) Eur. J. Cancer, 45, pp. 2077-2086. , [CrossRef] [PubMed]
  50. D’Eliseo, D., Velotti, F., Ω-3 fatty acids and cancer cell cytotoxicity: Implications for multi-targeted cancer therapy (2016) J. Clin. Med, 5, p. 15. , [CrossRef] [PubMed]
  51. Shaikh, S.R., Biophysical and biochemical mechanisms by which dietary N-3 polyunsaturated fatty acids from fish oil disrupt membrane lipid rafts (2012) J. Nutr. Biochem, 23, pp. 101-105. , [CrossRef] [PubMed]
  52. Schley, P.D., Brindley, D.N., Field, C.J., (n-3) PUFA alter raft lipid composition and decrease epidermal growth factor receptor levels in lipid rafts of human breast cancer cells (2007) J. Nutr, 137, pp. 548-553. , [PubMed]
  53. Schley, P.D., Jijon, H.B., Robinson, L.E., Field, C.J., Mechanisms of ω-3 fatty acid-induced growth inhibition in MDA-MB-231 human breast cancer cells (2005) Breast Cancer Res. Treat, 92, pp. 187-195. , [CrossRef] [PubMed]
  54. Ding, W.Q., Liu, B., Vaught, J.L., Palmiter, R.D., Lind, S.E., Clioquinol and docosahexaenoic acid act synergistically to kill tumor cells (2006) Mol. Cancer Ther, 5, pp. 1864-1872. , [CrossRef] [PubMed]
  55. Ghosh-Choudhury, T., Mandal, C.C., Woodruff, K., St Clair, P., Fernandes, G., Choudhury, G.G., Ghosh-Choudhury, N., Fish oil targets PTEN to regulate NFκB for downregulation of anti-apoptotic genes in breast tumor growth (2009) Breast Cancer Res. Treat, 118, pp. 213-228. , [CrossRef] [PubMed]
  56. Han, L., Zhang, Y., Meng, M., Cheng, D., Wang, C., Eicosapentaenoic acid induced SKOV-3 cell apoptosis through ERK1/2-mTOR-NF-κB pathways (2016) Anticancer Drugs, 27, pp. 635-642. , [CrossRef] [PubMed]
  57. Mazière, C., Conte, M.A., Degonville, J., Ali, D., Mazière, J.C., Cellular enrichment with polyunsaturated fatty acids induces an oxidative stress and activates the transcription factors AP1 and NFκB (1999) Biochem. Biophys. Res. Commun, 265, pp. 116-122. , [CrossRef] [PubMed]
  58. Chapkin, R.S., Hong, M.Y., Fan, Y.Y., Davidson, L.A., Sanders, L.M., Henderson, C.E., Barhoumi, R., Lupton, J.R., Dietary n-3 PUFA alter colonocyte mitochondrial membrane composition and function (2002) Lipids, 37, pp. 193-199. , [CrossRef] [PubMed]
  59. Erejuwa, O.O., Sulaiman, S.A., Ab Wahab, M.S., Evidence in support of potential applications of lipid peroxidation products in cancer treatment (2013) Oxid. Med. Cell Longev, 2013, p. 931251. , [CrossRef] [PubMed]
  60. Angeli, J.P., Garcia, C.C., Sena, F., Freitas, F.P., Miyamoto, S., Medeiros, M.H., Di Mascio, P., Lipid hydroperoxide-induced and hemoglobin-enhanced oxidative damage to colon cancer cells (2011) Free Radic. Biol. Med, 51, pp. 503-515. , [CrossRef] [PubMed]
  61. Falconer, J.S., Ross, J.A., Fearon, K.C., Hawkins, R.A., O’Riordain, M.G., Carter, D.C., Effect of eicosapentaenoic acid and other fatty acids on the growth in vitro of human pancreatic cancer cell lines (1994) Br. J. Cancer, 69, pp. 826-832. , [CrossRef] [PubMed]
  62. Bagga, D., Wang, L., Farias-Eisner, R., Glaspy, J.A., Reddy, S.T., Differential effects of prostaglandin derived from ω-6 and ω-3 polyunsaturated fatty acids on COX-2 expression and IL-6 secretion (2003) Proc. Natl. Acad. Sci. USA, 100, pp. 1751-1756. , [CrossRef] [PubMed]
  63. Vaughan, V.C., Hassing, M.R., Lewandowski, P.A., Marine polyunsaturated fatty acids and cancer therapy (2013) Br. J. Cancer, 108, pp. 486-492. , [CrossRef] [PubMed]
  64. Sunpaweravong, S., Puttawibul, P., Ruangsin, S., Laohawiriyakamol, S., Sunpaweravong, P., Sangthawan, D., Pradutkanchana, J., Geater, A., Randomized study of antiinflammatory and immune-modulatory effects of enteral immunonutrition during concurrent chemoradiotherapy for esophageal cancer (2014) Nutr. Cancer, 66, pp. 1-5. , [CrossRef] [PubMed]
  65. Zhelev, Z., Ivanova, D., Lazarova, D., Aoki, I., Bakalova, R., Saga, T., Docosahexaenoic acid sensitizes leukemia lymphocytes to Barasertib and Everolimus by ROS-dependent mechanism without affecting the level of ROS and viability of normal lymphocytes (2016) Anticancer Res, 36, pp. 1673-1682. , [PubMed]
  66. Siddiqui, R.A., Harvey, K.A., Xu, Z., Bammerlin, E.M., Walker, C., Altenburg, J.D., Docosahexaenoic acid:A natural powerful adjuvant that improves efficacy for anticancer treatment with no adverse effects (2011) Biofactors, 37, pp. 399-412. , [CrossRef] [PubMed]
  67. Gelsomino, G., Corsetto, P.A., Campia, I., Montorfano, G., Kopecka, J., Castella, B., Gazzano, E., Riganti, C., Omega 3 fatty acids chemosensitize multidrug resistant colon cancer cells by down-regulating cholesterol synthesis and altering detergent resistant membranes composition (2013) Mol. Cancer, 12, p. 137. , [CrossRef] [PubMed]
  68. Jiao, Y., Hannafon, B.N., Zhang, R.R., Fung, K.M., Ding, W.Q., Docosahexaenoic acid and disulfiram act in concert to kill cancer cells: A mutual enhancement of their anticancer actions (2017) Oncotarget, 8, pp. 17908-17920. , [CrossRef] [PubMed]
  69. Gao, K., Liang, Q., Zhao, Z.H., Li, Y.F., Wang, S.F., Synergistic anticancer properties of docosahexaenoic acid and 5-fluorouracil through interference with energy metabolism and cell cycle arrest in human gastric cancer cell line AGS cells (2016) World J. Gastroenterol, 22, pp. 2971-2980. , [CrossRef] [PubMed]
  70. Sheng, H., Chen, X., Liu, B., Li, P., Cao, W., Ω-3 polyunsaturated fatty acids enhance cisplatin efficacy in gastric cancer cells by inducing apoptosis via ADORA1 (2016) Anticancer Agents Med. Chem, 16, pp. 1085-1092. , [CrossRef] [PubMed]
  71. Chauvin, L., Goupille, C., Blanc, C., Pinault, M., Domingo, I., Guimaraes, C., Bougnoux, P., Mahéo, K., Long chain n-3 polyunsaturated fatty acids increase the efficacy of docetaxel in mammary cancer cells by downregulating Akt and PKCɛ/δ-induced ERK pathways (2016) Biochim. Biophys. Acta, 1861, pp. 380-390. , [CrossRef] [PubMed]
  72. Abdi, J., Garssen, J., Faber, J., Redegeld, F.A., Ω-3 fatty acids, EPA and DHA induce apoptosis and enhance drug sensitivity in multiple myeloma cells but not in normal peripheral mononuclear cells (2014) J. Nutr. Biochem, 25, pp. 1254-1262. , [CrossRef] [PubMed]
  73. Mason, J.K., Fu, M., Chen, J., Thompson, L.U., Flaxseed oil enhances the effectiveness of trastuzumab in reducing the growth of HER2-overexpressing human breast tumors (BT-474) (2015) J. Nutr. Biochem, 26, pp. 16-23. , [CrossRef] [PubMed]
  74. Bougnoux, P., Hajjaji, N., Ferrasson, M.N., Giraudeau, B., Couet, C., Le Floch, O., Improving outcome of chemotherapy of metastatic breast cancer by docosahexaenoic acid: A phase II trial (2009) Br. J. Cancer, 101, pp. 1978-1985. , [CrossRef] [PubMed]
  75. Murphy, R.A., Mourtzakis, M., Chu, Q.S., Baracos, V.E., Reiman, T., Mazurak, V.C., Supplementation with fish oil increases first-line chemotherapy efficacy in patients with advanced non-small cell lung cancer (2011) Cancer, 117, pp. 3774-3780. , [CrossRef] [PubMed]
  76. Miyata, H., Yano, M., Yasuda, T., Yamasaki, M., Murakami, K., Makino, T., Nishiki, K., Shiraishi, O., Randomized study of the clinical effects of ω-3 fatty acid-containing enteral nutrition support during neoadjuvant chemotherapy on chemotherapy-related toxicity in patients with esophageal cancer (2017) Nutrition, 33, pp. 204-210. , [CrossRef] [PubMed]
  77. Shirai, Y., Okugawa, Y., Hishida, A., Ogawa, A., Okamoto, K., Shintani, M., Morimoto, Y., Tanaka, K., Fish oil-enriched nutrition combined with systemic chemotherapy for gastrointestinal cancer patients with cancer cachexia (2017) Sci. Rep, 7, p. 4826. , [CrossRef] [PubMed]
  78. Teng, L.L., Shao, L., Zhao, Y.T., Yu, X., Zhang, D.F., Zhang, H., The beneficial effect of n-3 polyunsaturated fatty acids on doxorubicin-induced chronic heart failure in rats (2010) J. Int. Med. Res, 38, pp. 940-948. , [CrossRef] [PubMed]
  79. Uygur, R., Aktas, C., Tulubas, F., Alpsoy, S., Topcu, B., Ozen, O.A., Cardioprotective effects of fish ω-3 fatty acids on doxorubicin-induced cardiotoxicity in rats (2014) Hum. Exp. Toxicol, 33, pp. 435-445. , [CrossRef] [PubMed]
  80. Hsu, H.C., Chen, C.Y., Chen, M.F., N-3 polyunsaturated fatty acids decrease levels of doxorubicin-induced reactive oxygen species in cardiomyocytes-Involvement of uncoupling protein UCP2 (2014) J. Biomed. Sci, 21, p. 101. , [CrossRef] [PubMed]
  81. Xue, H., Ren, W., Denkinger, M., Schlotzer, E., Wischmeyer, P.E., Nutrition modulation of cardiotoxicity and anticancer efficacy related to Doxorubicin chemotherapy by glutamine and ω-3 polyunsaturated fatty acids (2016) J. Parenter. Enter. Nutr, 40, pp. 52-66. , [CrossRef] [PubMed]
  82. Wang, Z.Q., Chen, M.T., Zhang, R., Zhang, Y., Li, W., Li, Y.G., Docosahexaenoic acid attenuates doxorubicin-induced cytotoxicity and inflammation by suppressing NF-κB/iNOS/NO signaling pathway activation in H9C2 cardiac cells (2016) J. Cardiovasc. Pharmacol, 67, pp. 283-289. , [CrossRef] [PubMed]
  83. Vishnu, K.V., Ajeesh Kumar, K.K., Chatterjee, N.S., Lekshmi, R.G.K., Sreerekha, P.R., Mathew, S., Ravishankar, C.N., Sardine oil loaded vanillic acid grafted chitosan microparticles, a new functional food ingredient: Attenuates myocardial oxidative stress and apoptosis in cardiomyoblast cell lines (H9c2) (2017) Cell Stress Chaperones, , [CrossRef] [PubMed]
  84. Edwardson, D.W., Narendrula, R., Chewchuk, S., Mispel-Beyer, K., Mapletoft, J.P., Parissenti, A.M., Role of drug metabolism in the cytotoxicity and clinical efficacy of anthracyclines (2015) Curr. Drug Metab, 16, pp. 412-426. , [CrossRef] [PubMed]
  85. Arcamone, F.M., From the pigments of the actinomycetes to third generation antitumor anthracyclines (1998) Biochimie, 80, pp. 201-206. , [CrossRef]
  86. Preobrazhenskaya, M.N., Tevyashova, A.N., Olsufyeva, E.N., Huang, H.-F., Huang, H.S., Second generation drugs-Derivatives of natural anti-tumor anthracycline antibiotics Daunorubicin, Doxorubicin and Carminomycin (2006) J. Med. Sci, 26, pp. 119-128
  87. Cortes-Funes, H., Coronado, C., Role of anthracyclines in the era of targeted therapy (2007) Cardiovasc. Toxicol, 7, pp. 56-60. , [CrossRef] [PubMed]
  88. Fumoleau, P., Roche, H., Kerbrat, P., Bonneterre, J., Romestaing, P., Fargeot, P., Namer, M., Goudier, M.J., Long-term cardiac toxicity after adjuvant epirubicin-based chemotherapy in early breast cancer: French Adjuvant Study Group results (2006) Ann. Oncol, 17, pp. 85-92. , [CrossRef] [PubMed]
  89. Chien, A.J., Moasser, M.M., Cellular mechanisms of resistance to anthracyclines and taxanes in cancer:Intrinsic and acquired (2008) Semin. Oncol, 35, pp. S1-S14. , [CrossRef] [PubMed]
  90. Bartlett, J.J., Trivedi, P.C., Pulinilkunnil, T., Autophagic dysregulation in doxorubicin cardiomyopathy (2017) J. Mol. Cell. Cardiol, 104, pp. 1-8. , [CrossRef] [PubMed]
  91. Gammella, E., Maccarinelli, F., Buratti, P., Recalcati, S., Cairo, G., The role of iron in anthracycline cardiotoxicity (2014) Front. Pharmacol, 5, p. 25. , [CrossRef] [PubMed]
  92. Vejpongsa, P., Yeh, E.T., Prevention of anthracycline-induced cardiotoxicity: Challenges and opportunities (2014) J. Am. Coll. Cardiol, 64, pp. 938-945. , [CrossRef] [PubMed]
  93. Ichikawa, Y., Ghanefar, M., Bayeva, M., Wu, R., Khechaduri, A., Naga Prasad, S.V., Mutharasan, R.K., Ardehali, H., Cardiotoxicity of doxorubicin is mediated through mitochondrial iron accumulation (2014) J. Clin. Investig, 124, pp. 617-630. , [CrossRef] [PubMed]
  94. Link, G., Tirosh, R., Pinson, A., Hershko, C., Role of iron in the potentiation of anthracycline cardiotoxicity:Identification of heart cell mitochondria as a major site of iron-anthracycline interaction (1996) J. Lab. Clin. Med, 127, pp. 272-278. , [CrossRef]
  95. Van Dalen, E.C., Caron, H.N., Dickinson, H.O., Kremer, L.C., Cardioprotective interventions for cancer patients receiving anthracyclines (2011) Cochrane Database Syst. Rev, 6
  96. Dresdale, A.R., Barr, L.H., Bonow, R.O., Mathisen, D.J., Myers, C.E., Schwartz, D.E., D’Angelo, T., Rosenberg, S.A., Prospective randomized study of the role of N-acetyl cysteine in reversing doxorubicin-induced cardiomyopathy (1982) Am. J. Clin. Oncol, 5, pp. 657-663. , [CrossRef] [PubMed]
  97. Panjrath, G.S., Patel, V., Valdiviezo, C.I., Narula, N., Narula, J., Jain, D., Potentiation of Doxorubicin cardiotoxicity by iron loading in a rodent model (2007) J. Am. Coll. Cardiol, 49, pp. 2457-2464. , [CrossRef] [PubMed]
  98. Hasinoff, B.B., Schnabl, K.L., Marusak, R.A., Patel, D., Huebner, E., Dexrazoxane (ICRF-187) protects cardiac myocytes against doxorubicin by preventing damage to mitochondria (2003) Cardiovasc. Toxicol, 3, pp. 89-99. , [CrossRef] [PubMed]
  99. Martin, E., Thougaard, A.V., Grauslund, M., Jensen, P.B., Bjorkling, F., Hasinoff, B.B., Tjørnelund, J., Jensen, L.H., Evaluation of the topoisomerase II-inactive bisdioxopiperazine ICRF-161 as a protectant against doxorubicin-induced cardiomyopathy (2009) Toxicology, 255, pp. 72-79. , [CrossRef] [PubMed]
  100. Nitiss, K.C., Nitiss, J.L., Twisting and ironing: Doxorubicin cardiotoxicity by mitochondrial DNA damage (2014) Clin. Cancer Res, 20, pp. 4737-4739. , [CrossRef] [PubMed]
  101. Zhang, S., Liu, X., Bawa-Khalfe, T., Lu, L.S., Lyu, Y.L., Liu, L.F., Yeh, E.T., Identification of the molecular basis of doxorubicin-induced cardiotoxicity (2012) Nat. Med, 18, pp. 1639-1642. , [CrossRef] [PubMed]
  102. Abd El-Aziz, T.A., Mohamed, R.H., Pasha, H.F., Abdel-Aziz, H.R., Catechin protects against oxidative stress and inflammatory-mediated cardiotoxicity in adriamycin-treated rats (2012) Clin. Exp. Med, 12, pp. 233-240. , [CrossRef] [PubMed]
  103. Guo, R., Lin, J., Xu, W., Shen, N., Mo, L., Zhang, C., Feng, J., Hydrogen sulfide attenuates doxorubicin-induced cardiotoxicity by inhibition of the p38 MAPK pathway in H9c2 cells (2013) Int. J. Mol. Med, 31, pp. 644-650. , [CrossRef] [PubMed]
  104. Pecoraro, M., Del Pizzo, M., Marzocco, S., Sorrentino, R., Ciccarelli, M., Iaccarino, G., Pinto, A., Popolo, A., Inflammatory mediators in a short-time mouse model of doxorubicin-induced cardiotoxicity (2016) Toxicol. Appl. Pharmacol, 293, pp. 44-52. , [CrossRef] [PubMed]
  105. Holmgren, G., Synnergren, J., Andersson, C.X., Lindahl, A., Sartipy, P., MicroRNAs as potential biomarkers for doxorubicin-induced cardiotoxicity (2016) Toxicol. In Vitro, 34, pp. 26-34. , [CrossRef] [PubMed]
  106. Saddic, L.A., Muehlschlegel, J.D., Sarco “MiR” friend or foe: A perspective on the mechanisms of doxorubicin-induced cardiomyopathy (2016) Ann. Transl. Med, 4, p. 203. , [CrossRef] [PubMed]
  107. Fasano, E., Serini, S., Piccioni, E., Toesca, A., Monego, G., Cittadini, A.R., Ranelletti, F.O., Calviello, G., DHA induces apoptosis by altering the expression and cellular location of GRP78 in colon cancer cell lines (2012) Biochim. Biophys. Acta, 1822, pp. 1762-1772. , [CrossRef] [PubMed]
  108. Dirks-Naylor, A.J., Kouzi, S.A., Yang, S., Tran, N.T., Bero, J.D., Mabolo, R., Phan, D.T., Taylor, H.N., Can short-term fasting protect against doxorubicin-induced cardiotoxicity? (2014) World J. Biol. Chem, 5, pp. 269-274. , [CrossRef] [PubMed]
  109. Pizarro, M., Troncoso, R., Martinez, G.J., Chiong, M., Castro, P.F., Lavandero, S., Basal autophagy protects cardiomyocytes from doxorubicin-induced toxicity (2016) Toxicology, 370, pp. 41-48. , [CrossRef] [PubMed]
  110. Loos, B., du Toit, A., Hofmeyr, J.H., Defining and measuring autophagosome flux-concept and reality (2014) Autophagy, 10, pp. 2087-2096. , [CrossRef] [PubMed]
  111. Cappetta, D., Rossi, F., Piegari, E., Quaini, F., Berrino, L., Urbanek, K., De Angelis, A., Doxorubicin targets multiple players: A new view of an old problem (2017) Pharmacol. Res, , [CrossRef] [PubMed]
  112. Matsui, H., Morishima, I., Hayashi, K., Kamiya, H., Saburi, Y., Okumura, K., Dietary fish oil does not prevent doxorubicin-induced cardiomyopathy in rats (2002) Can. J. Cardiol, 18, pp. 279-286. , [PubMed]
  113. Carbone, A., Psaltis, P.J., Nelson, A.J., Metcalf, R., Richardson, J.D., Weightman, M., Thomas, A., Worthley, S.G., Dietary ω-3 supplementation exacerbates left ventricular dysfunction in an ovine model of anthracycline-induced cardiotoxicity (2012) J. Card. Fail, 18, pp. 502-511. , [CrossRef] [PubMed]
  114. Germain, E., Lavandier, F., Chajès, V., Schubnel, V., Bonnet, P., Lhuillery, C., Bougnoux, P., Dietary n-3 polyunsaturated fatty acids and oxidants increase rat mammary tumor sensitivity to epirubicin without change in cardiac toxicity (1999) Lipids, 34. , [CrossRef] [PubMed]
  115. Germain, E., Bonnet, P., Aubourg, L., Grangeponte, M.C., Chajès, V., Bougnoux, P., Anthracycline-induced cardiac toxicity is not increased by dietary ω-3 fatty acids (2003) Pharmacol. Res, 47, pp. 111-117. , [CrossRef]
  116. Schjøtt, J., Brurok, H., Jynge, P., Bjerve, K.S., Effects of eicosapentaenoic acid and docosahexaenoic acid diet supplement on tolerance to the cardiotoxicity of epirubicin and to ischaemia reperfusion in the isolated rat heart (1996) Pharmacol. Toxicol, 79, pp. 65-72. , [CrossRef] [PubMed]
  117. Yu, X., Cui, L., Zhang, Z., Zhao, Q., Li, S., α-Linolenic acid attenuates doxorubicin-induced cardiotoxicity in rats through suppression of oxidative stress and apoptosis (2013) Acta Biochim. Biophys. Sin, 45, pp. 817-826. , [CrossRef] [PubMed]
  118. Hajjaji, N., Besson, P., Bougnoux, P., Tumor and non-tumor tissues differential oxidative stress response to supplemental DHA and chemotherapy in rats (2012) Cancer Chemother. Pharmacol, 70, pp. 17-23. , [CrossRef] [PubMed]
  119. Vitelli, M.R., Filippelli, A., Rinaldi, B., Rossi, S., Palazzo, E., Rossi, F., Berrino, L., Effects of docosahexaenoic acid on [Ca2+]i increase induced by doxorubicin in ventricular rat cardiomyocytes (2002) Life Sci, 71, pp. 1905-1916. , [CrossRef]
  120. Lau, D.H., Psaltis, P.J., Carbone, A., Kelly, D.J., Mackenzie, L., Worthington, M., Metcalf, R.G., Zhang, Y., Atrial protective effects of n-3 polyunsaturated fatty acids: A long-term study in ovine chronic heart failure (2011) Heart Rhythm, 8, pp. 575-582. , [CrossRef] [PubMed]
  121. Fasano, E., Serini, S., Cittadini, A., Calviello, G., Long-chain n-3 PUFA against breast and prostate cancer:Which are the appropriate doses for intervention studies in animals and humans? (2017) Crit. Rev. Food Sci. Nutr, 57, pp. 2245-2262. , [CrossRef] [PubMed]
  122. Menna, P., Salvatorelli, E., Primary prevention strategies for anthracycline cardiotoxicity: A brief overview (2017) Chemotherapy, 62, pp. 159-168. , [CrossRef] [PubMed]
  123. Brenna, J.T., Efficiency of conversion of α-linolenic acid to long chain n-3 fatty acids in man (2002) Curr. Opin. Clin. Nutr. Metab. Care, 5, pp. 127-132. , [CrossRef] [PubMed]
  124. Colas, S., Mahéo, K., Denis, F., Goupille, C., Hoinard, C., Champeroux, P., Tranquart, F., Bougnoux, P., Sensitization by dietary docosahexaenoic acid of rat mammary carcinoma to anthracycline: A role for tumor vascularization (2006) Clin. Cancer Res, 12, pp. 5879-5886. , [CrossRef] [PubMed]
  125. Serini, S., Fasano, E., Piccioni, E., Cittadini, A.R., Calviello, G., Dietary n-3 polyunsaturated fatty acids and the paradox of their health benefits and potential harmful effects (2011) Chem. Res. Toxicol, 24, pp. 2093-2105. , [CrossRef] [PubMed]
  126. Cetrullo, S., Tantini, B., Flamigni, F., Pazzini, C., Facchini, A., Stefanelli, C., Caldarera, C.M., Pignatti, C., Antiapoptotic and antiautophagic effects of eicosapentaenoic acid in cardiac myoblasts exposed to palmitic acid (2012) Nutrients, 4, pp. 78-90. , [CrossRef] [PubMed]
  127. Hsu, H.C., Chen, C.Y., Chiang, C.H., Chen, M.F., Eicosapentaenoic acid attenuated oxidative stress-induced cardiomyoblast apoptosis by activating adaptive autophagy (2014) Eur. J. Nutr, 53, pp. 541-547. , [CrossRef] [PubMed]
  128. Gwon, D.H., Hwang, T.W., Ro, J.Y., Kang, Y.J., Jeong, J.Y., Kim, D.K., Lim, K., Kim, J.J., High endogenous accumulation of ω-3 polyunsaturated fatty acids protect against ischemia-reperfusion renal injury through AMPK-mediated autophagy in Fat-1 mice (2017) Int. J. Mol. Sci, 18, p. 2081. , [CrossRef] [PubMed]
  129. Pettersen, K., Monsen, V.T., Hakvåg Pettersen, C.H., Overland, H.B., Pettersen, G., Samdal, H., Tesfahun, A.N., Schønberg, S.A., DHA-induced stress response in human colon cancer cells-Focus on oxidative stress and autophagy (2016) Free Radic. Biol. Med, 90, pp. 158-172. , [CrossRef] [PubMed]
  130. Karimi, M., Vedin, I., Freund Levi, Y., Basun, H., Faxén Irving, G., Eriksdotter, M., Wahlund, L.O., Cederholm, T., DHA-rich n-3 fatty acid supplementation decreases DNA methylation in blood leukocytes: The WD study (2017) Am. J. Clin. Nutr, 106, pp. 1157-1165. , [CrossRef] [PubMed]
  131. Valenzuela, R., Rincón-Cervera, M.Á., Echeverría, F., Barrera, C., Espinosa, A., Hernández-Rodas, M.C., Ortiz, M., Videla, L.A., Iron-induced pro-oxidant and pro-lipogenic responses in relation to impaired synthesis and accretion of long-chain polyunsaturated fatty acids in rat hepatic and extrahepatic tissues (2018) Nutrition, 45, pp. 49-58. , [CrossRef] [PubMed]