Moringa oleifera Leaves Extract Ameliorates Doxorubicin-Induced Cardiotoxicity via Its Mitochondrial Biogenesis Modulatory Activity in Rats

References

• Carvalho C, Santos RX, Cardoso S, et al. Doxorubicin: the good, the bad, and the ugly effect. Curr Med Chem. 2009;16(25):3267–3285. doi:10.2174/092986709788803312
   PubMed Web of Science ®Google Scholar
• Pugazhendhi A, Edison T, Velmurugan BK, Jacob JA, Karuppusamy I. Toxicity of Doxorubicin (Dox) to different experimental organ systems. Life Sci. 2018;200:26–30. doi:10.1016/j.lfs.2018.03.023
   PubMed Web of Science ®Google Scholar
• Murabito A, Hirsch E, Ghigo A. Mechanisms of anthracycline-induced cardiotoxicity: is mitochondrial dysfunction the answer? Front Cardiovasc Med. 2020;7:35. doi:10.3389/fcvm.2020.00035
   PubMed Web of Science ®Google Scholar
• Kalyanaraman B. Teaching the basics of the mechanism of doxorubicin-induced cardiotoxicity: have we been barking up the wrong tree? Redox Biol. 2020;29:101394. doi:10.1016/j.redox.2019.101394
   PubMed Web of Science ®Google Scholar
• Santos D, Goldenberg R. Doxorubicin-induced cardiotoxicity: from mechanisms to development of efficient therapy; 2018.
   Google Scholar
• Ichikawa Y, Ghanefar M, Bayeva M, et al. Cardiotoxicity of doxorubicin is mediated through mitochondrial iron accumulation. J Clin Invest. 2014;124(2):617–630. doi:10.1172/JCI72931
   PubMed Web of Science ®Google Scholar
• Wang S, Kotamraju S, Konorev E, Kalivendi S, Joseph J, Kalyanaraman B. Activation of nuclear factor-kappaB during doxorubicin-induced apoptosis in endothelial cells and myocytes are pro-apoptotic: the role of hydrogen peroxide. Biochem J. 2002;367(Pt 3):729–740. doi:10.1042/bj20020752
   PubMedGoogle Scholar
• Ferreira A, Cunha-Oliveira T, Simões RF, et al. Altered mitochondrial epigenetics associated with subchronic doxorubicin cardiotoxicity. Toxicology. 2017;390:63–73. doi:10.1016/j.tox.2017.08.011
   PubMed Web of Science ®Google Scholar
• Osataphan N, Phrommintikul A, Chattipakorn SC, Chattipakorn N. Effects of doxorubicin-induced cardiotoxicity on cardiac mitochondrial dynamics and mitochondrial function: insights for future interventions. J Cell Mol Med. 2020;24(12):6534–6557. doi:10.1111/jcmm.15305
   PubMed Web of Science ®Google Scholar
• Wei S, Ma W, Li X, et al. Involvement of ROS/NLRP3 Inflammasome Signaling Pathway in Doxorubicin-Induced Cardiotoxicity. Cardiovasc Toxicol. 2020;20(5):507–519. doi:10.1007/s12012-020-09576-4
   PubMed Web of Science ®Google Scholar
• Cappetta D, De Angelis A, Sapio L, et al. Oxidative stress and cellular response to doxorubicin: a common factor in the complex milieu of anthracycline cardiotoxicity. Oxid Med Cell Longev. 2017;2017:1521020. doi:10.1155/2017/1521020
   PubMed Web of Science ®Google Scholar
• Gorini S, De Angelis A, Berrino L, Malara N, Rosano G, Ferraro E. Chemotherapeutic drugs and mitochondrial dysfunction: focus on doxorubicin, trastuzumab, and sunitinib. Oxid Med Cell Longev. 2018;2018:7582730. doi:10.1155/2018/7582730
   PubMed Web of Science ®Google Scholar
• Wang DD, Cheng RK, Tian R. Combat doxorubicin cardiotoxicity with the power of mitochondria transfer. JACC CardioOncol. 2021;3(3):441–443. doi:10.1016/j.jaccao.2021.08.001
   PubMedGoogle Scholar
• Yue P, Jing S, Liu L, et al. Association between mitochondrial DNA copy number and cardiovascular disease: current evidence based on a systematic review and meta-analysis. PLoS One. 2018;13(11):e0206003. doi:10.1371/journal.pone.0206003
   PubMed Web of Science ®Google Scholar
• Cheung KG, Cole LK, Xiang B, et al. Sirtuin-3 (SIRT3) protein attenuates doxorubicin-induced oxidative stress and improves mitochondrial respiration in H9c2 cardiomyocytes. J Biol Chem. 2015;290(17):10981–10993. doi:10.1074/jbc.M114.607960
   PubMed Web of Science ®Google Scholar
• Lu Z, Xu X, Hu X, et al. PGC-1 alpha regulates expression of myocardial mitochondrial antioxidants and myocardial oxidative stress after chronic systolic overload. Antioxid Redox Signal. 2010;13(7):1011–1022. doi:10.1089/ars.2009.2940
   PubMed Web of Science ®Google Scholar
• Oseni O, Ogunmoyole T, Idowu K. Lipid profile and cardio-protective effects of aqueous extract of moringa oleifera (lam) leaf on bromate-induced cardiotoxicity on Wistar albino rats. Eur J Adv Res Biol Life Sci. 2015;3(2):1–15.
   Google Scholar
• Sailaja BS, Aita R, Maledatu S, Ribnicky D, Verzi MP, Raskin I. Moringa isothiocyanate-1 regulates Nrf2 and NF-κB pathway in response to LPS-driven sepsis and inflammation. PLoS One. 2021;16(4):e0248691. doi:10.1371/journal.pone.0248691
   PubMed Web of Science ®Google Scholar
• Quagliariello V, Basilicata MG, Pepe G, et al. Combination of spirulina platensis, ganoderma lucidum, and moringa oleifera improves cardiac functions and reduces pro-inflammatory biomarkers in preclinical models of short-term doxorubicin-mediated cardiotoxicity: new frontiers in cardiology? J Cardiovasc Dev Dis. 2022;9(12). doi:10.3390/jcdd9120423.
   PubMed Web of Science ®Google Scholar
• Cheraghi M, Namdari M, Daraee H, Negahdari B. Cardioprotective effect of magnetic hydrogel nanocomposite loaded N,α-L-rhamnopyranosyl vincosamide isolated from Moringa oleifera leaves against doxorubicin-induced cardiac toxicity in rats: in vitro and in vivo studies. J Microencapsul. 2017;34(4):335–341. doi:10.1080/02652048.2017.1311955
   PubMed Web of Science ®Google Scholar
• Arozal W, Purwoningsih E, Lee HJ, Barinda AJ, Munim A. Effects of moringa oleifera in two independents formulation and as neuroprotective agent against scopolamine-induced memory impairment in mice. Front Nutr. 2022;9. doi:10.3389/fnut.2022.799127
   PubMed Web of Science ®Google Scholar
• Gibson-Corley KN, Olivier AK, Meyerholz DK. Principles for valid histopathologic scoring in research. Vet Pathol. 2013;50(6):1007–1015. doi:10.1177/0300985813485099
   PubMed Web of Science ®Google Scholar
• Barinda AJ, Arozal W, Sandhiutami NMD, et al. Curcumin prevents epithelial-to-mesenchymal transition-mediated ovarian cancer progression through NRF2/ETBR/ET-1 axis and preserves mitochondria biogenesis in kidney after cisplatin administration. Adv Pharm Bull. 2022;12(1):128. doi:10.34172/apb.2022.014
   PubMed Web of Science ®Google Scholar
• Melva Louisa AMP, Sidqi AA, Kirana Mahaputra D, et al. Attenuation of cisplatin-induced hepatotoxicity by nanocurcumin through modulation of antioxidative and anti-inflammatory pathways. J Appl Pharm Sci. 2023;13:3.
   Google Scholar
• Zhao H, Liu J, Pan S, et al. SOD mRNA and MDA expression in rectus femoris muscle of rats with different eccentric exercise programs and time points. PLoS One. 2013;8(9):e73634. doi:10.1371/journal.pone.0073634
   PubMed Web of Science ®Google Scholar
• Khan V, Sharma S, Bhandari U, Sharma N, Rishi V, Haque SE. Suppression of isoproterenol-induced cardiotoxicity in rats by raspberry ketone via activation of peroxisome proliferator-activated receptor-α. Eur J Pharmacol. 2019;842:157–166. doi:10.1016/j.ejphar.2018.10.034
   PubMed Web of Science ®Google Scholar
• Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 2001;25(4):402–408. doi:10.1006/meth.2001.1262
   PubMed Web of Science ®Google Scholar
• Pomierny-Chamioło L, Moniczewski A, Wydra K, Suder A, Filip M. Oxidative stress biomarkers in some rat brain structures and peripheral organs underwent cocaine. Neurotox Res. 2013;23(1):92–102. doi:10.1007/s12640-012-9335-6
   PubMed Web of Science ®Google Scholar
• Nagata S. Apoptosis and clearance of apoptotic cells. Annu Rev Immunol. 2018;36(1):489–517. doi:10.1146/annurev-immunol-042617-053010
   PubMedGoogle Scholar
• Torres-Gonzalez M, Gawlowski T, Kocalis H, Scott BT, Dillmann WH. Mitochondrial 8-oxo guanine glycosylase decreases mitochondrial fragmentation and improves mitochondrial function in H9C2 cells under oxidative stress conditions. Am J Physiol Cell Physiol. 2014;306(3):C221–C229. doi:10.1152/ajpcell.00140.2013
   PubMed Web of Science ®Google Scholar
• Wallace KB, Sardão VA, Oliveira PJ. Mitochondrial determinants of doxorubicin-induced cardiomyopathy. Circ Res. 2020;126(7):926–941. doi:10.1161/CIRCRESAHA.119.314681
   PubMed Web of Science ®Google Scholar
• Yoshida M, Shiojima I, Ikeda H, Komuro I. Chronic doxorubicin cardiotoxicity is mediated by oxidative DNA damage-ATM-p53-apoptosis pathway and attenuated by pitavastatin through the inhibition of Rac1 activity. J Mol Cell Cardiol. 2009;47(5):698–705. doi:10.1016/j.yjmcc.2009.07.024
   PubMed Web of Science ®Google Scholar
• Hu C, Zhang X, Wei W, et al. Matrine attenuates oxidative stress and cardiomyocyte apoptosis in doxorubicin-induced cardiotoxicity via maintaining AMPKα/UCP2 pathway. Acta Pharm Sin B. 2019;9(4):690–701. doi:10.1016/j.apsb.2019.03.003
   PubMed Web of Science ®Google Scholar
• Sandoval-Acuña C, Ferreira J, Speisky H. Polyphenols and mitochondria: an update on their increasingly emerging ROS-scavenging independent actions. Arch Biochem Biophys. 2014;559:75–90. doi:10.1016/j.abb.2014.05.017
   PubMed Web of Science ®Google Scholar
• Warpe VS, Mali VR, A S, Bodhankar SL, Mahadik KR. Cardioprotective effect of ellagic acid on doxorubicin-induced cardiotoxicity in Wistar rats. J Acute Med. 2015;5(1):1–8. doi:10.1016/j.jacme.2015.02.003
   Web of Science ®Google Scholar
• Nandave M, Ojha SK, Joshi S, Kumari S, Arya DS. Moringa oleifera leaf extract prevents isoproterenol-induced myocardial damage in rats: evidence for an antioxidant, antiperoxidative, and cardioprotective intervention. J Med Food. 2009;12(1):47–55. doi:10.1089/jmf.2007.0563
   PubMed Web of Science ®Google Scholar
• Childs AC, Phaneuf SL, Dirks AJ, Phillips T, Leeuwenburgh C. Doxorubicin treatment in vivo causes cytochrome C release and cardiomyocyte apoptosis, as well as increased mitochondrial efficiency, superoxide dismutase activity, and Bcl-2: Bax ratio. Cancer Res. 2002;62(16):4592–4598.
   PubMed Web of Science ®Google Scholar
• Michihiko U, Yoshihiko K, Koh-ichi Y, et al. Doxorubicin induces apoptosis by activating caspase-3 in cultured cardiomyocytes in vitro and rat cardiac ventricles in vivo. J Pharmacol Sci. 2006;101(2):151–158. doi:10.1254/jphs.FP0050980
   PubMed Web of Science ®Google Scholar
• Vandaele L, Goossens K, Peelman L, Van Soom A. mRNA expression of Bcl-2, Bax, caspase-3, and −7 cannot be used as a marker for apoptosis in bovine blastocysts. Anim Reprod Sci. 2008;106(1–2):168–173. doi:10.1016/j.anireprosci.2007.12.016
   PubMed Web of Science ®Google Scholar
• Chen Q, Kao X, Gao Y, Chen J, Dong Z, Chen C. Increase in NO causes osteoarthritis, and chondrocyte apoptosis and chondrocyte ERK play a protective role in the process. Mol Biol Rep. 2021;48(11):7303–7312. doi:10.1007/s11033-021-06731-0
   PubMed Web of Science ®Google Scholar
• El-Agamy DS, El-Harbi KM, Khoshhal S, et al. Pristimerin protects against doxorubicin-induced cardiotoxicity and fibrosis through modulation of Nrf2 and MAPK/NF-kB signaling pathways. Cancer Manag Res. 2019;11:47–61. doi:10.2147/CMAR.S186696
   PubMed Web of Science ®Google Scholar
• Hassanien RT, Shoukry HS, Moataz MK, Rabab AR, Ibrahim HS, Ibrahim ER. Vitamin E improves doxorubicin induced nephrotoxicity; possible underlying mechanisms. Med J Cairo Univ. 2018;86:651–657. doi:10.21608/mjcu.2018.55380
   Google Scholar
• Chodari L, Dilsiz Aytemir M, Vahedi P, et al. Targeting mitochondrial biogenesis with polyphenol compounds. Oxid Med Cell Longev. 2021;2021:4946711. doi:10.1155/2021/4946711
   PubMed Web of Science ®Google Scholar
• Peoples JN, Saraf A, Ghazal N, Pham TT, Kwong JQ. Mitochondrial dysfunction and oxidative stress in heart disease. Exp Mol Med. 2019;51(12):1–13. doi:10.1038/s12276-019-0355-7
   PubMedGoogle Scholar
• Kong C-Y, Guo Z, Song P, et al. Underlying the mechanisms of doxorubicin-induced acute cardiotoxicity: oxidative stress and cell death. Int J Biol Sci. 2022;18(2):760–770. doi:10.7150/ijbs.65258
   PubMed Web of Science ®Google Scholar
• Liang H, Ward WF. PGC-1α: a key regulator of energy metabolism. Adv Physiol Educ. 2006;30(4):145–151. doi:10.1152/advan.00052.2006
   PubMed Web of Science ®Google Scholar
• S-i O, Sabry AD, Cawley KM, Warren JS. Multiple levels of PGC-1α dysregulation in heart failure. Front Cardiovasc Med. 2020;7:2. doi:10.3389/fcvm.2020.00002
   PubMed Web of Science ®Google Scholar
• Guo Q, Guo J, Yang R, et al. Cyclovirobuxine D attenuates doxorubicin-induced cardiomyopathy by suppression of oxidative damage and mitochondrial biogenesis impairment. Oxid Med Cell Longev. 2015;2015:151972. doi:10.1155/2015/151972
   PubMed Web of Science ®Google Scholar
• Monraz-Méndez CA, Escutia-Gutiérrez R, Rodriguez-Sanabria JS, et al. Moringa oleifera improves MAFLD by inducing epigenetic modifications. Nutrients. 2022;14(20):4225. doi:10.3390/nu14204225
   PubMed Web of Science ®Google Scholar
• Chaudhary S, Ganguly S, Palanichamy JK, et al. PGC1A driven enhanced mitochondrial DNA copy number predicts outcome in pediatric acute myeloid leukemia. Mitochondrion. 2021;58:246–254. doi:10.1016/j.mito.2021.03.013
   PubMed Web of Science ®Google Scholar
• Bam S, Buchanan E, Mahony C, O’Ryan C. DNA methylation of PGC-1α is associated with elevated mtDNA copy number and altered urinary metabolites in autism spectrum disorder. Front Cell Dev Biol. 2021;9. doi:10.3389/fcell.2021.696428
   PubMed Web of Science ®Google Scholar
• Popov LD. Mitochondrial biogenesis: an update. J Cell Mol Med. 2020;24(9):4892–4899. doi:10.1111/jcmm.15194
   PubMed Web of Science ®Google Scholar
• Muhammed RE, El-Desouky MA, Abo-Seda SB, Nahas A, Elhakim HK, Alkhalaf MI. The protecting role of Moringa oleifera in cypermethrin-induced mitochondrial dysfunction and apoptotic events in rats brain. J King Saud Univ Sci. 2020;32(6):2717–2722. doi:10.1016/j.jksus.2020.06.006
   Web of Science ®Google Scholar
• Sánchez-Muñoz M A, Valdez-Solana MA, Campos-Almazán MI, et al. Streptozotocin-induced adaptive modification of mitochondrial supercomplexes in the liver of Wistar rats and the protective effect of Moringa oleifera Lam. Biochem Res Int. 2018;2018. doi:10.1155/2018/5681081
   Web of Science ®Google Scholar