The roles of resveratrol on cardiac mitochondrial function in cardiac diseases

European Journal of Nutrition volume 60, pages29–44(2021)Cite this article

Abstract

Left ventricular (LV) dysfunction is commonly associated with a variety of health conditions including acute myocardial infarction and obesity/diabetes. In addition, administration of several pharmacological agents such as anticancer, antiviral, and immunosuppressive drugs has been shown to be related with LV dysfunction. The molecular mechanism responsible for LV dysfunction has been extensively studied, and it has been proposed that the overproduction of reactive oxygen species (ROS) plays a crucial role in the regulation of this function. Mitochondria require the balance between ROS production and antioxidants to maintain their appropriate function and to prevent excessive ROS production. Thus, the excessive production of ROS and the reduced scavenging process under any pathological conditions could disrupt mitochondrial function, leading to energy depletion with subsequent cell death. Therefore, maintenance of the balance between oxidative stress and antioxidants is essential. Resveratrol, a stilbene, has been investigated extensively, and potentially used to treat or prevent various cardiovascular diseases. Resveratrol directly upregulates antioxidative capacity by increasing antioxidant genes such as heme oxygenase-1, superoxide dismutase, catalase, and glutathione. In this review, accumulated data from in vitro, ex vivo, and in vivo studies regarding the effects of resveratrol on cardiac mitochondrial function in cardiac pathologies are comprehensively summarized and discussed. Since there is no conclusive available clinical study regarding the effects of resveratrol on cardiac mitochondrial function, this review also aims to encourage more clinical investigations to confirm findings from basic research. This comprehensive review will provide insight regarding the potential mechanistic roles of resveratrol in preventing and/or treating patients with cardiovascular diseases to improve LV function and their health status.

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References

  1. 1.

    Kavarana MN, Pessin-Minsley MS, Urtecho J, Catanese KA, Flannery M, Oz MC, Naka Y (2002) Right ventricular dysfunction and organ failure in left ventricular assist device recipients: a continuing problem. Ann Thorac Surg 73(3):745–750. https://doi.org/10.1016/s0003-4975(01)03406-3

    Article  PubMed  Google Scholar 

  2. 2.

    Ribichini F, Wijns W (2002) Acute myocardial infarction: reperfusion treatment. Heart 88(3):298–305. https://doi.org/10.1136/heart.88.3.298

    Article  PubMed  PubMed Central  Google Scholar 

  3. 3.

    Mohseni J, Kazemi T, Maleki MH, Beydokhti H (2017) A systematic review on the prevalence of acute myocardial infarction in Iran. Heart Views 18(4):125–132. https://doi.org/10.4103/heartviews.Heartviews_71_17

    Article  PubMed  PubMed Central  Google Scholar 

  4. 4.

    Carden DL, Granger DN (2000) Pathophysiology of ischaemia-reperfusion injury. J Pathol 190(3):255–266. https://doi.org/10.1002/(sici)1096-9896(200002)190:3%3c255:Aid-path526%3e3.0.Co;2-6

    CAS  Article  PubMed  Google Scholar 

  5. 5.

    Rentrop KP, Feit F (2015) Reperfusion therapy for acute myocardial infarction: Concepts and controversies from inception to acceptance. Am Heart J 170(5):971–980. https://doi.org/10.1016/j.ahj.2015.08.005

    Article  PubMed  Google Scholar 

  6. 6.

    Bugger H, Abel ED (2008) Molecular mechanisms for myocardial mitochondrial dysfunction in the metabolic syndrome. Clin Sci (Lond) 114(3):195–210. https://doi.org/10.1042/cs20070166

    CAS  Article  Google Scholar 

  7. 7.

    Nicolson GL (2007) Metabolic syndrome and mitochondrial function: molecular replacement and antioxidant supplements to prevent membrane peroxidation and restore mitochondrial function. J Cell Biochem 100(6):1352–1369. https://doi.org/10.1002/jcb.21247

    CAS  Article  PubMed  Google Scholar 

  8. 8.

    Ott M, Gogvadze V, Orrenius S, Zhivotovsky B (2007) Mitochondria, oxidative stress and cell death. Apoptosis 12(5):913–922. https://doi.org/10.1007/s10495-007-0756-2

    CAS  Article  Google Scholar 

  9. 9.

    Lin KJ, Lengacher CA (2019) Anthracycline chemotherapy-induced cardiotoxicity in breast cancer survivors: a systematic review. Oncol Nurs Forum 46(5):E145–e158. https://doi.org/10.1188/19.Onf.E145-e158

    Article  PubMed  Google Scholar 

  10. 10.

    Lemieux H, Hoppel CL (2009) Mitochondria in the human heart. J Bioenerg Biomembr 41(2):99–106. https://doi.org/10.1007/s10863-009-9211-0

    CAS  Article  PubMed  Google Scholar 

  11. 11.

    Chen L, Knowlton AA (2010) Mitochondria and heart failure: New insights into an energetic problem. Minerva Cardioangiol 58(2):213–229

    CAS  PubMed  PubMed Central  Google Scholar 

  12. 12.

    Khanduja KL, Bhardwaj A (2003) Stable free radical scavenging and antiperoxidative properties of resveratrol compared in vitro with some other bioflavonoids. Indian J Biochem Biophys 40(6):416–422

    CAS  PubMed  Google Scholar 

  13. 13.

    Salehi B, Mishra AP, Nigam M, Sener B, Kilic M, Sharifi-Rad M, Fokou PVT, Martins N, Sharifi-Rad J (2018) Resveratrol: a double-edged sword in health benefits. Biomedicines. https://doi.org/10.3390/biomedicines6030091

    Article  PubMed  PubMed Central  Google Scholar 

  14. 14.

    Yu W, Fu YC, Wang W (2012) Cellular and molecular effects of resveratrol in health and disease. J Cell Biochem 113(3):752–759. https://doi.org/10.1002/jcb.23431

    CAS  Article  PubMed  Google Scholar 

  15. 15.

    Zhang Y, Li XR, Zhao L, Duan GL, Xiao L, Chen HP (2018) DJ-1 preserving mitochondrial complex I activity plays a critical role in resveratrol-mediated cardioprotection against hypoxia/reoxygenation-induced oxidative stress. Biomed Pharmacother 98:545–552. https://doi.org/10.1016/j.biopha.2017.12.094

    CAS  Article  PubMed  Google Scholar 

  16. 16.

    Danz ED, Skramsted J, Henry N, Bennett JA, Keller RS (2009) Resveratrol prevents doxorubicin cardiotoxicity through mitochondrial stabilization and the Sirt1 pathway. Free Radic Biol Med 46(12):1589–1597. https://doi.org/10.1016/j.freeradbiomed.2009.03.011

    CAS  Article  PubMed  Google Scholar 

  17. 17.

    Dong W, Yang R, Yang J, Yang J, Ding J, Wu H, Zhang J (2015) Resveratrol pretreatment protects rat hearts from ischemia/reperfusion injury partly via a NALP3 inflammasome pathway. Int J Clin Exp Pathol 8(8):8731–8741

    PubMed  PubMed Central  Google Scholar 

  18. 18.

    Bagul PK, Katare PB, Bugga P, Dinda AK, Banerjee SK (2018) SIRT-3 modulation by resveratrol improves mitochondrial oxidative phosphorylation in diabetic heart through deacetylation of TFAM. Cells. https://doi.org/10.3390/cells7120235

    Article  PubMed  PubMed Central  Google Scholar 

  19. 19.

    Nunes R, Baiao A, Monteiro D, Neves J, Sarmento B (2020) Zein nanoparticles as low-cost, safe, and effective carriers to improve the oral bioavailability of resveratrol. Drug Deliv Transl Res. https://doi.org/10.1007/s13346-020-00738-z

    Article  PubMed  Google Scholar 

  20. 20.

    de Ligt M, Bruls YMH, Hansen J, Habets MF, Havekes B, Nascimento EBM, Moonen-Kornips E, Schaart G, Schrauwen-Hinderling VB, van Marken LW, Schrauwen P (2018) Resveratrol improves ex vivo mitochondrial function but does not affect insulin sensitivity or brown adipose tissue in first degree relatives of patients with type 2 diabetes. Mol Metab 12:39–47. https://doi.org/10.1016/j.molmet.2018.04.004

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  21. 21.

    Chekalina NI (2017) Resveratrol has a positive effect on parameters of central hemodynamics and myocardial ischemia in patients with stable coronary heart disease. Wiad Lek 70(2 pt 2):286–291

    PubMed  Google Scholar 

  22. 22.

    Militaru C, Donoiu I, Craciun A, Scorei ID, Bulearca AM, Scorei RI (2013) Oral resveratrol and calcium fructoborate supplementation in subjects with stable angina pectoris: effects on lipid profiles, inflammation markers, and quality of life. Nutrition 29(1):178–183. https://doi.org/10.1016/j.nut.2012.07.006

    CAS  Article  PubMed  Google Scholar 

  23. 23.

    Marques B, Trindade M, Aquino JCF, Cunha AR, Gismondi RO, Neves MF, Oigman W (2018) Beneficial effects of acute trans-resveratrol supplementation in treated hypertensive patients with endothelial dysfunction. Clin Exp Hypertens 40(3):218–223. https://doi.org/10.1080/10641963.2017.1288741

    CAS  Article  PubMed  Google Scholar 

  24. 24.

    Rahman S, Islam R (2011) Mammalian Sirt 1: insights on its biological functions. Cell Commun Signal 9:11. https://doi.org/10.1186/1478-811x-9-11

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  25. 25.

    Khan MA, Chen HC, Wan XX, Tania M, Xu AH, Chen FZ, Zhang DZ (2013) Regulatory effects of resveratrol on antioxidant enzymes: a mechanism of growth inhibition and apoptosis induction in cancer cells. Mol Cells 35(3):219–225. https://doi.org/10.1007/s10059-013-2259-z

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  26. 26.

    Miller NJ, Rice-Evans CA (1995) Antioxidant activity of resveratrol in red wine. Clin Chem 41(12 Pt 1):1789

    CAS  Article  Google Scholar 

  27. 27.

    Kovacic P, Somanathan R (2010) Multifaceted approach to resveratrol bioactivity: Focus on antioxidant action, cell signaling and safety. Oxid Med Cell Longev 3(2):86–100. https://doi.org/10.4161/oxim.3.2.11147

    Article  PubMed  PubMed Central  Google Scholar 

  28. 28.

    Horio Y, Hayashi T, Kuno A, Kunimoto R (2011) Cellular and molecular effects of sirtuins in health and disease. Clin Sci (Lond) 121(5):191–203. https://doi.org/10.1042/cs20100587

    CAS  Article  Google Scholar 

  29. 29.

    Li YG, Zhu W, Tao JP, Xin P, Liu MY, Li JB, Wei M (2013) Resveratrol protects cardiomyocytes from oxidative stress through SIRT1 and mitochondrial biogenesis signaling pathways. Biochem Biophys Res Commun 438(2):270–276. https://doi.org/10.1016/j.bbrc.2013.07.042

    CAS  Article  PubMed  Google Scholar 

  30. 30.

    Guo Y, Zhang L, Li F, Hu CP, Zhang Z (2016) Restoration of SIRT1 function by pterostilbene attenuates hypoxia-reoxygenation injury in cardiomyocytes. Eur J Pharmacol 776:26–33. https://doi.org/10.1016/j.ejphar.2016.02.052

    CAS  Article  PubMed  Google Scholar 

  31. 31.

    Tong Z, Xie Y, He M, Ma W, Zhou Y, Lai S, Meng Y, Liao Z (2017) VDAC1 deacetylation is involved in the protective effects of resveratrol against mitochondria-mediated apoptosis in cardiomyocytes subjected to anoxia/reoxygenation injury. Biomed Pharmacother 95:77–83. https://doi.org/10.1016/j.biopha.2017.08.046

    CAS  Article  PubMed  Google Scholar 

  32. 32.

    Kerner J, Lee K, Tandler B (1818) Hoppel CL (2012) VDAC proteomics: Post-translation modifications. Biochim Biophys Acta 6:1520–1525. https://doi.org/10.1016/j.bbamem.2011.11.013

    CAS  Article  Google Scholar 

  33. 33.

    Noskov SY, Rostovtseva TK, Chamberlin AC, Teijido O, Jiang W, Bezrukov SM (2016) Current state of theoretical and experimental studies of the voltage-dependent anion channel (VDAC). Biochim Biophys Acta. https://doi.org/10.1016/j.bbamem.2016.02.026

    Article  PubMed  PubMed Central  Google Scholar 

  34. 34.

    Camara AKS, Zhou Y, Wen PC, Tajkhorshid E, Kwok WM (2017) Mitochondrial VDAC1: a key gatekeeper as potential therapeutic target. Front Physiol 8:460. https://doi.org/10.3389/fphys.2017.00460

    Article  PubMed  PubMed Central  Google Scholar 

  35. 35.

    Heo JY, Park JH, Kim SJ, Seo KS, Han JS, Lee SH, Kim JM, Park JI, Park SK, Lim K, Hwang BD, Shong M, Kweon GR (2012) DJ-1 null dopaminergic neuronal cells exhibit defects in mitochondrial function and structure: involvement of mitochondrial complex I assembly. PLoS ONE 7(3):e32629. https://doi.org/10.1371/journal.pone.0032629

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  36. 36.

    Nagakubo D, Taira T, Kitaura H, Ikeda M, Tamai K, Iguchi-Ariga SM, Ariga H (1997) DJ-1, a novel oncogene which transforms mouse NIH3T3 cells in cooperation with ras. Biochem Biophys Res Commun 231(2):509–513. https://doi.org/10.1006/bbrc.1997.6132

    CAS  Article  PubMed  Google Scholar 

  37. 37.

    Tang BL (2016) Sirt1 and the mitochondria. Mol Cells 39(2):87–95. https://doi.org/10.14348/molcells.2016.2318

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  38. 38.

    Li P, Liu Y, Burns N, Zhao KS, Song R (2017) SIRT1 is required for mitochondrial biogenesis reprogramming in hypoxic human pulmonary arteriolar smooth muscle cells. Int J Mol Med 39(5):1127–1136. https://doi.org/10.3892/ijmm.2017.2932

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  39. 39.

    Xi J, Wang H, Mueller RA, Norfleet EA, Xu Z (2009) Mechanism for resveratrol-induced cardioprotection against reperfusion injury involves glycogen synthase kinase 3beta and mitochondrial permeability transition pore. Eur J Pharmacol 604(1–3):111–116. https://doi.org/10.1016/j.ejphar.2008.12.024

    CAS  Article  PubMed  Google Scholar 

  40. 40.

    Beurel E, Grieco SF, Jope RS (2015) Glycogen synthase kinase-3 (GSK3): regulation, actions, and diseases. Pharmacol Ther 148:114–131. https://doi.org/10.1016/j.pharmthera.2014.11.016

    CAS  Article  PubMed  Google Scholar 

  41. 41.

    Nishihara M, Miura T, Miki T, Tanno M, Yano T, Naitoh K, Ohori K, Hotta H, Terashima Y, Shimamoto K (2007) Modulation of the mitochondrial permeability transition pore complex in GSK-3beta-mediated myocardial protection. J Mol Cell Cardiol 43(5):564–570. https://doi.org/10.1016/j.yjmcc.2007.08.010

    CAS  Article  PubMed  Google Scholar 

  42. 42.

    Watcharasit P, Bijur GN, Song L, Zhu J, Chen X, Jope RS (2003) Glycogen synthase kinase-3beta (GSK3beta) binds to and promotes the actions of p53. J Biol Chem 278(49):48872–48879. https://doi.org/10.1074/jbc.M305870200

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  43. 43.

    Liao Z, Liu D, Tang L, Yin D, Yin S, Lai S, Yao J, He M (2015) Long-term oral resveratrol intake provides nutritional preconditioning against myocardial ischemia/reperfusion injury: Involvement of VDAC1 downregulation. Mol Nutr Food Res 59(3):454–464. https://doi.org/10.1002/mnfr.201400730

    CAS  Article  PubMed  Google Scholar 

  44. 44.

    Torre-Amione G, Kapadia S, Benedict C, Oral H, Young JB, Mann DL (1996) Proinflammatory cytokine levels in patients with depressed left ventricular ejection fraction: a report from the Studies of Left Ventricular Dysfunction (SOLVD). J Am Coll Cardiol 27(5):1201–1206. https://doi.org/10.1016/0735-1097(95)00589-7

    CAS  Article  PubMed  Google Scholar 

  45. 45.

    Nakayama H, Otsu K (2018) Mitochondrial DNA as an inflammatory mediator in cardiovascular diseases. Biochem J 475(5):839–852. https://doi.org/10.1042/bcj20170714

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  46. 46.

    Moe GW, Marin-Garcia J, Konig A, Goldenthal M, Lu X, Feng Q (2004) In vivo TNF-alpha inhibition ameliorates cardiac mitochondrial dysfunction, oxidative stress, and apoptosis in experimental heart failure. Am J Physiol Heart Circ Physiol 287(4):H1813–1820. https://doi.org/10.1152/ajpheart.00036.2004

    CAS  Article  PubMed  Google Scholar 

  47. 47.

    Gao RY, Mukhopadhyay P, Mohanraj R, Wang H, Horvath B, Yin S, Pacher P (2011) Resveratrol attenuates azidothymidine-induced cardiotoxicity by decreasing mitochondrial reactive oxygen species generation in human cardiomyocytes. Mol Med Rep 4(1):151–155. https://doi.org/10.3892/mmr.2010.390

    CAS  Article  PubMed  Google Scholar 

  48. 48.

    Yang Y, Wang W, Xiong Z, Kong J, Qiu Y, Shen F, Huang Z (2016) Activation of SIRT3 attenuates triptolide-induced toxicity through closing mitochondrial permeability transition pore in cardiomyocytes. Toxicol In Vitro 34:128–137. https://doi.org/10.1016/j.tiv.2016.03.020

    CAS  Article  PubMed  Google Scholar 

  49. 49.

    Hao E, Lang F, Chen Y, Zhang H, Cong X, Shen X, Su G (2013) Resveratrol alleviates endotoxin-induced myocardial toxicity via the Nrf2 transcription factor. PLoS ONE 8(7):e69452. https://doi.org/10.1371/journal.pone.0069452

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  50. 50.

    Lewis W, Simpson JF, Meyer RR (1994) Cardiac mitochondrial DNA polymerase-gamma is inhibited competitively and noncompetitively by phosphorylated zidovudine. Circ Res 74(2):344–348. https://doi.org/10.1161/01.res.74.2.344

    CAS  Article  PubMed  Google Scholar 

  51. 51.

    Barile M, Valenti D, Passarella S, Quagliariello E (1997) 3'-Azido-3'-deoxythmidine uptake into isolated rat liver mitochondria and impairment of ADP/ATP translocator. Biochem Pharmacol 53(7):913–920. https://doi.org/10.1016/s0006-2952(96)00831-3

    CAS  Article  PubMed  Google Scholar 

  52. 52.

    Panaro MA, Acquafredda A, Cavallo P, Cianciulli A, Saponaro C, Mitolo V (2010) Inflammatory responses in embryonal cardiomyocytes exposed to LPS challenge: an in vitro model of deciphering the effects of LPS on the heart. Curr Pharm Des 16(7):754–765. https://doi.org/10.2174/138161210790883516

    CAS  Article  PubMed  Google Scholar 

  53. 53.

    Asgharzadeh F, Bargi R, Hosseini M, Farzadnia M, Khazaei M (2018) Cardiac and renal fibrosis and oxidative stress balance in lipopolysaccharide-induced inflammation in male rats. ARYA Atheroscler 14(2):71–77. https://doi.org/10.22122/arya.v14i2.1550

    Article  PubMed  PubMed Central  Google Scholar 

  54. 54.

    Andreyev AY, Kushnareva YE, Starkov AA (2005) Mitochondrial metabolism of reactive oxygen species. Biochemistry (Mosc) 70(2):200–214

    CAS  Article  Google Scholar 

  55. 55.

    Burton GJ, Jauniaux E (2011) Oxidative stress. Best Pract Res Clin Obstet Gynaecol 25(3):287–299. https://doi.org/10.1016/j.bpobgyn.2010.10.016

    Article  PubMed  PubMed Central  Google Scholar 

  56. 56.

    Zhou J, Xi C, Wang W, Fu X, Jinqiang L, Qiu Y, Jin J, Xu J, Huang Z (2014) Triptolide-induced oxidative stress involved with Nrf2 contribute to cardiomyocyte apoptosis through mitochondrial dependent pathways. Toxicol Lett 230(3):454–466. https://doi.org/10.1016/j.toxlet.2014.08.017

    CAS  Article  PubMed  Google Scholar 

  57. 57.

    Xi Y, Wang W, Wang L, Pan J, Cheng Y, Shen F, Huang Z (2018) Triptolide induces p53-dependent cardiotoxicity through mitochondrial membrane permeabilization in cardiomyocytes. Toxicol Appl Pharmacol 355:269–285. https://doi.org/10.1016/j.taap.2018.07.011

    CAS  Article  PubMed  Google Scholar 

  58. 58.

    Bo-Htay C, Palee S, Apaijai N, Chattipakorn SC, Chattipakorn N (2018) Effects of d-galactose-induced ageing on the heart and its potential interventions. J Cell Mol Med 22(3):1392–1410. https://doi.org/10.1111/jcmm.13472

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  59. 59.

    Chang L, Liu X, Liu J, Li H, Yang Y, Liu J, Guo Z, Xiao K, Zhang C, Liu J, Zhao-Wilson X, Long J (2014) D-galactose induces a mitochondrial complex I deficiency in mouse skeletal muscle: Potential benefits of nutrient combination in ameliorating muscle impairment. J Med Food 17(3):357–364. https://doi.org/10.1089/jmf.2013.2830

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  60. 60.

    Angebault C, Charif M, Guegen N, Piro-Megy C, Mousson de Camaret B, Procaccio V, Guichet PO, Hebrard M, Manes G, Leboucq N, Rivier F, Hamel CP, Lenaers G, Roubertie A (2015) Mutation in NDUFA13/GRIM19 leads to early onset hypotonia, dyskinesia and sensorial deficiencies, and mitochondrial complex I instability. Hum Mol Genet 24(14):3948–3955. https://doi.org/10.1093/hmg/ddv133

    CAS  Article  PubMed  Google Scholar 

  61. 61.

    Ren X, Chen L, Xie J, Zhang Z, Dong G, Liang J, Liu L, Zhou H, Luo P (2017) Resveratrol ameliorates mitochondrial elongation via Drp1/Parkin/PINK1 signaling in senescent-like cardiomyocytes. Oxid Med Cell Longev 2017:4175353. https://doi.org/10.1155/2017/4175353

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  62. 62.

    Liesa M, Shirihai OS (2013) Mitochondrial dynamics in the regulation of nutrient utilization and energy expenditure. Cell Metab 17(4):491–506. https://doi.org/10.1016/j.cmet.2013.03.002

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  63. 63.

    Nan J, Zhu W, Rahman MS, Liu M, Li D, Su S, Zhang N, Hu X, Yu H, Gupta MP (1864) Wang J (2017) Molecular regulation of mitochondrial dynamics in cardiac disease. Biochim Biophys Acta Mol Cell Res 7:1260–1273. https://doi.org/10.1016/j.bbamcr.2017.03.006

    CAS  Article  Google Scholar 

  64. 64.

    Ding WX, Yin XM (2012) Mitophagy: Mechanisms, pathophysiological roles, and analysis. Biol Chem 393(7):547–564. https://doi.org/10.1515/hsz-2012-0119

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  65. 65.

    Gewirtz DA (1999) A critical evaluation of the mechanisms of action proposed for the antitumor effects of the anthracycline antibiotics adriamycin and daunorubicin. Biochem Pharmacol 57(7):727–741

    CAS  Article  Google Scholar 

  66. 66.

    Minotti G, Menna P, Salvatorelli E, Cairo G, Gianni L (2004) Anthracyclines: Molecular advances and pharmacologic developments in antitumor activity and cardiotoxicity. Pharmacol Rev 56(2):185–229. https://doi.org/10.1124/pr.56.2.6

    CAS  Article  PubMed  Google Scholar 

  67. 67.

    Feng L, Ren J, Li Y, Yang G, Kang L, Zhang S, Ma C, Li J, Liu J, Yang L, Qi Z (2018) Resveratrol protects against isoproterenol induced myocardial infarction in rats through VEGF-B/AMPK/eNOS/NO signaling pathway. Free Radic Res. https://doi.org/10.1080/10715762.2018.1554901

    Article  PubMed  Google Scholar 

  68. 68.

    Al-Harthi SE, Alarabi OM, Ramadan WS, Alaama MN, Al-Kreathy HM, Damanhouri ZA, Khan LM, Osman AM (2014) Amelioration of doxorubicininduced cardiotoxicity by resveratrol. Mol Med Rep 10(3):1455–1460. https://doi.org/10.3892/mmr.2014.2384

    CAS  Article  PubMed  Google Scholar 

  69. 69.

    Ilkun O, Boudina S (2013) Cardiac dysfunction and oxidative stress in the metabolic syndrome: an update on antioxidant therapies. Curr Pharm Des 19(27):4806–4817. https://doi.org/10.2174/1381612811319270003

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  70. 70.

    Schmidt RE, Dorsey DA, Beaudet LN, Peterson RG (2003) Analysis of the Zucker Diabetic Fatty (ZDF) type 2 diabetic rat model suggests a neurotrophic role for insulin/IGF-I in diabetic autonomic neuropathy. Am J Pathol 163(1):21–28. https://doi.org/10.1016/s0002-9440(10)63626-7

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  71. 71.

    Wang P, Chatham JC (2004) Onset of diabetes in Zucker diabetic fatty (ZDF) rats leads to improved recovery of function after ischemia in the isolated perfused heart. Am J Physiol Endocrinol Metab 286(5):E725–736. https://doi.org/10.1152/ajpendo.00295.2003

    CAS  Article  PubMed  Google Scholar 

  72. 72.

    Duncan JG (2011) Mitochondrial dysfunction in diabetic cardiomyopathy. Biochim Biophys Acta 1813(7):1351–1359. https://doi.org/10.1016/j.bbamcr.2011.01.014

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  73. 73.

    Beaudoin MS, Perry CG, Arkell AM, Chabowski A, Simpson JA, Wright DC, Holloway GP (2014) Impairments in mitochondrial palmitoyl-CoA respiratory kinetics that precede development of diabetic cardiomyopathy are prevented by resveratrol in ZDF rats. J Physiol 592(12):2519–2533. https://doi.org/10.1113/jphysiol.2013.270538

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  74. 74.

    Lu Y, Lu X, Wang L, Yang W (2019) Resveratrol attenuates high fat diet-induced mouse cardiomyopathy through upregulation of estrogen related receptor-alpha. Eur J Pharmacol 843:88–95. https://doi.org/10.1016/j.ejphar.2018.10.018

    CAS  Article  PubMed  Google Scholar 

  75. 75.

    Giguere V, Yang N, Segui P, Evans RM (1988) Identification of a new class of steroid hormone receptors. Nature 331(6151):91–94. https://doi.org/10.1038/331091a0

    CAS  Article  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by Thailand Research Fund grants: RTA 6080003 (SCC), TRG6280005 (NA); the NSTDA Research Chair grant from the National Science and Technology Development Agency Thailand (NC), and the Chiang Mai University Center of Excellence Award (NC).

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  1. Cardiac Electrophysiology Research and Training Center, Faculty of Medicine, Chiang Mai University, Chiang Mai, 50200, Thailand

    Apiwan Arinno, Nattayaporn Apaijai, Siriporn C. Chattipakorn & Nipon Chattipakorn

  2. Center of Excellence in Cardiac Electrophysiology Research, Chiang Mai University, Chiang Mai, 50200, Thailand

    Apiwan Arinno, Nattayaporn Apaijai, Siriporn C. Chattipakorn & Nipon Chattipakorn

  3. Cardiac Electrophysiology Unit, Department of Physiology, Faculty of Medicine, Chiang Mai University, Chiang Mai, 50200, Thailand

    Apiwan Arinno & Nipon Chattipakorn

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  1. Apiwan Arinno
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Arinno, A., Apaijai, N., Chattipakorn, S.C. et al. The roles of resveratrol on cardiac mitochondrial function in cardiac diseases. Eur J Nutr 60, 29–44 (2021). https://doi.org/10.1007/s00394-020-02256-7

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Keywords

  • Resveratrol
  • Mitochondria
  • Cardiotoxicity
  • Cardiac ischemia–reperfusion injury
  • Chemotherapy