Curcumin-coated gold nanoparticles attenuate doxorubicin-induced cardiotoxicity via regulating apoptosis in a mouse model.
Animals
Apoptosis
/ drug effects
Cardiotoxicity
/ drug therapy
Cardiotoxins
/ antagonists & inhibitors
Curcumin
/ therapeutic use
Doxorubicin
/ antagonists & inhibitors
Gold
Male
Metal Nanoparticles
Mice
Mice, Inbred BALB C
Microscopy, Electron, Transmission
Photoelectron Spectroscopy
Spectroscopy, Fourier Transform Infrared
apoptosis
cardiotoxicity
curcumin
doxorubicin
gold nanoparticles
Journal
Clinical and experimental pharmacology & physiology
ISSN: 1440-1681
Titre abrégé: Clin Exp Pharmacol Physiol
Pays: Australia
ID NLM: 0425076
Informations de publication
Date de publication:
01 2022
01 2022
Historique:
revised:
21
08
2021
received:
25
11
2020
accepted:
24
08
2021
pubmed:
28
8
2021
medline:
30
3
2022
entrez:
27
8
2021
Statut:
ppublish
Résumé
Doxorubicin (DOX) is one of the most widely used chemotherapy agents; however, its nonselective effect causes cardiotoxicity. Curcumin (Cur), a well known dietary polyphenol, could exert a significant cardioprotective effect, but the biological application of this substance is limited by its chemical insolubility. To overcome this limitation, in this study, we synthesised gold nanoparticles based on Cur (Cur-AuNPs). Ultraviolet-visible (UV-Vis) absorbance spectroscopy and transmission electron microscopy (TEM) were performed for the characterisation of synthesised NPs, and Fourier transform infrared (FTIR) spectroscopy were applied to detect Cur on the surface of AuNPs. Its cytotoxicity effect on H9c2 cells was evaluated using 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide (MTT) assay. The biological efficacy of Cur-AuNPs was assessed after acute cardiotoxicity induction in BALB/c mice with DOX injection. The serum biomarkers, myocardial histological changes, and cardiomyocyte apoptosis were then measured. The results revealed that the heart protection by Cur-AuNPs is more effective than Cur alone. Heart protective effect of Cur-AuNPs was evident both in the short-term (24 hours) and long-term (14 days) study. The results of Cur-AuNPs400 after 24 hours of toxicity induction displayed the reduction of the cardiac injury serum biomarkers (LDH, CK-MB, cTnI, ADT, and ALT) and apoptotic proteins (Bax and Caspase-3), as well as increase of Bcl-2 anti-apoptotic proteins without any sign of interfibrillar haemorrhage and intercellular spaces in the heart tissue microscopic images. Our long-term study signifies that Cur-AuNPs400 in DOX-intoxicated mice could successfully inhibit body and heart weight loss in comparison to DOX group.
Identifiants
pubmed: 34449914
doi: 10.1111/1440-1681.13579
doi:
Substances chimiques
Cardiotoxins
0
Gold
7440-57-5
Doxorubicin
80168379AG
Curcumin
IT942ZTH98
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
70-83Subventions
Organisme : Iran University of Medical Sciences
Informations de copyright
© 2021 John Wiley & Sons Australia, Ltd.
Références
Zagar TM, Cardinale DM, Marks LB. Breast cancer therapy-associated cardiovascular disease. Nature Rev Clin Oncol. 2016;13(3):172.
Rochette L, Guenancia C, Gudjoncik A, et al. Anthracyclines/trastuzumab: new aspects of cardiotoxicity and molecular mechanisms. Trends Pharmacol Sci. 2015;36(6):326-348.
Raj S, Franco VI, Lipshultz SE. Anthracycline-induced cardiotoxicity: a review of pathophysiology, diagnosis, and treatment. Curr Treat Options Cardiovas Med. 2014;16(6):315.
Rharass T, Gbankoto A, Canal C, et al. Oxidative stress does not play a primary role in the toxicity induced with clinical doses of doxorubicin in myocardial H9c2 cells. Mol Cell Biochem. 2016;413(1-2):199-215.
Lipshultz SE. Anthracycline-induced cardiotoxicity in children and young adults. Crit Rev Oncol/Hematol. 1998;1(27):53-68.
Mihm MJ, Yu F, Weinstein DM, Reiser PJ, Bauer JA. Intracellular distribution of peroxynitrite during doxorubicin cardiomyopathy: evidence for selective impairment of myofibrillar creatine kinase. Br J Pharmacol. 2002;135(3):581-588.
Zhao L, Zhang B. Doxorubicin induces cardiotoxicity through upregulation of death receptors mediated apoptosis in cardiomyocytes. Sci Rep. 2017;7:44735.
Luo X, Evrovsky Y, Cole D, Trines J, Benson LN, Lehotay DC. Doxorubicin-induced acute changes in cytotoxic aldehydes, antioxidant status and cardiac function in the rat. Biochim et Biophys Acta (BBA)-Mol Basis Dis. 1997;1360(1):45-52.
Jm K, Marchetti P, Gallego M-A, et al. Mitochondrial proliferation during apoptosis induced by anticancer agents: effects of doxorubicin and mitoxantrone on cancer and cardiac cells. Oncogene. 2004;23(42):7018-7030.
Spinale FG. Matrix metalloproteinases: regulation and dysregulation in the failing heart. Circ Res. 2002;90(5):520-530.
Ammon H, Anazodo M. Curcumin: A potent inhibitor of leukotriene B4 formation in rat peritoneal polymorphonuclear neutrophils (PMNL). Planta Med. 1992;58:226.
Sindhu K, Indra R, Rajaram A, Sreeram K, Rajaram R. Investigations on the interaction of gold-curcumin nanoparticles with human peripheral blood lymphocytes. J Biomed Nanotechnol. 2011;7(1):56.
Trujillo J, Granados-Castro LF, Zazueta C, Andérica-Romero AC, Chirino YI, Pedraza-Chaverrí J. Mitochondria as a target in the therapeutic properties of curcumin. Arch Pharm (Weinheim). 2014;347(12):873-884.
Ganjali S, Sahebkar A, Mahdipour E, et al. Investigation of the effects of curcumin on serum cytokines in obese individuals: a randomized controlled trial. Sci World J. 2014;2014:1-6.
Priyadarsini KI, Maity DK, Naik G, et al. Role of phenolic OH and methylene hydrogen on the free radical reactions and antioxidant activity of curcumin. Free Radic Biol Med. 2003;35(5):475-484.
Namdari M, Eatemadi A. Cardioprotective effects of curcumin-loaded magnetic hydrogel nanocomposite (nanocurcumin) against doxorubicin-induced cardiac toxicity in rat cardiomyocyte cell lines. Art Cells, Nanomed Biotech. 2017;45(4):731-739.
Swamy AV, Gulliaya S, Thippeswamy A, Koti BC, Manjula DV. Cardioprotective effect of curcumin against doxorubicin-induced myocardial toxicity in albino rats. Indian J Pharmacol. 2012;44(1):73.
Wen C, Fu L, Huang J, et al. Curcumin reverses doxorubicin resistance via inhibition the efflux function of ABCB4 in doxorubicin-resistant breast cancer cells. Mol Med Rep. 2019;19(6):5162-5168.
Hosseinzadeh L, Behravan J, Mosaffa F, Bahrami G, Bahrami A, Karimi G. Curcumin potentiates doxorubicin-induced apoptosis in H9c2 cardiac muscle cells through generation of reactive oxygen species. Food Chem Toxicol. 2011;49(5):1102-1109.
Agashe H, Sahoo K, Lagisetty P, Awasthi V. Cyclodextrin-mediated entrapment of curcuminoid 4-[3, 5-bis (2-chlorobenzylidene-4-oxo-piperidine-1-yl)-4-oxo-2-butenoic acid] or CLEFMA in liposomes for treatment of xenograft lung tumor in rats. Colloids Surf, B. 2011;84(2):329-337.
Prasad M, Lambe UP, Brar B, et al. Nanotherapeutics: An insight into healthcare and multi-dimensional applications in medical sector of the modern world. Biomed Pharmacother. 2018;97:1521-1537.
Singh NA. Nanotechnology innovations, industrial applications and patents. Environ Chem Lett. 2017;15(2):185-191.
Guo R, Song Y, Wang G, Murray RW. Does core size matter in the kinetics of ligand exchanges of monolayer-protected Au clusters? J Am Chem Soc. 2005;127(8):2752-2757.
Lu H, Peng Y, Ye H, et al. Sensitization, energy transfer and infra-red emission decay modulation in Yb 3+-doped NaYF 4 nanoparticles with visible light through a perfluoroanthraquinone chromophore. Sci Rep. 2017;7(1):5066.
Ackerson CJ, Jadzinsky PD, Sexton JZ, Bushnell DA, Kornberg RD. Synthesis and bioconjugation of 2 and 3 nm-diameter gold nanoparticles. Bioconjug Chem. 2010;21(2):214-218.
Biswal J, Ramnani S, Shirolikar S, Sabharwal S. Synthesis of rectangular plate like gold nanoparticles by in situ generation of seeds by combining both radiation and chemical methods. Radiat Phys Chem. 2011;80(1):44-49.
Noruzi M, Zare D, Khoshnevisan K, Davoodi D. Rapid green synthesis of gold nanoparticles using Rosa hybrida petal extract at room temperature. Spectrochim Acta Part A Mol Biomol Spectrosc. 2011;79(5):1461-1465.
Nath D, Banerjee P. Green nanotechnology-a new hope for medical biology. Environ Toxicol Pharmacol. 2013;36(3):997-1014.
Sathishkumar M, Sneha K, Won S, Cho C-W, Kim S, Yun Y-S. Cinnamon zeylanicum bark extract and powder mediated green synthesis of nano-crystalline silver particles and its bactericidal activity. Colloids Surf, B. 2009;73(2):332-338.
Huang X, El-Sayed MA. Gold nanoparticles: Optical properties and implementations in cancer diagnosis and photothermal therapy. J Advan Res. 2010;1(1):13-28.
Krishnankutty K, Venugopalan P. Metal chelates of curcuminoids. Synth React Inorg Met-Org Chem. 1998;28(8):1313-1325.
Shaabani E, Amini SM, Kharrazi S, Tajerian R. Curcumin coated gold nanoparticles: synthesis, characterization, cytotoxicity, antioxidant activity and its comparison with citrate coated gold nanoparticles. Nanomedicine J. 2017;4(2):115-125.
McGowan JV, Chung R, Maulik A, Piotrowska I, Walker JM, Yellon DM. Anthracycline chemotherapy and cardiotoxicity. Cardiovasc Drugs Ther. 2017;31(1):63-75.
An L, Hu X-W, Zhang S, et al. UVRAG deficiency exacerbates doxorubicin-induced cardiotoxicity. Sci Rep. 2017;7:43251.
Sahu BD, Kumar JM, Kuncha M, Borkar RM, Srinivas R, Sistla R. Baicalein alleviates doxorubicin-induced cardiotoxicity via suppression of myocardial oxidative stress and apoptosis in mice. Life Sci. 2016;144:8-18.
Elberry AA, Abdel-Naim AB, Abdel-Sattar EA, et al. Cranberry (Vaccinium macrocarpon) protects against doxorubicin-induced cardiotoxicity in rats. Food Chem Toxicol. 2010;48(5):1178-1184.
Granados-Principal S, El-Azem N, Pamplona R, et al. Hydroxytyrosol ameliorates oxidative stress and mitochondrial dysfunction in doxorubicin-induced cardiotoxicity in rats with breast cancer. Biochem Pharmacol. 2014;90(1):25-33.
Emanuel K, Mackiewicz U, Pytkowski B, Lewartowski B. Properties of ventricular myocytes isolated from the hypertrophied and failing hearts of spontaneously hypertensive rats. J Physiol Pharmacol. 1999;50(2):243-258.
Hojo Y, Saito T, Kondo H. Role of apoptosis in left ventricular remodeling after acute myocardial infarction. J Cardiol. 2012;60(2):91-92.
Reeve JL, Szegezdi E, Logue SE, et al. Distinct mechanisms of cardiomyocyte apoptosis induced by doxorubicin and hypoxia converge on mitochondria and are inhibited by Bcl-xL. J Cell Mol Med. 2007;11(3):509-520.
Yu W, Sun H, Zha W, et al. Apigenin attenuates adriamycin-induced cardiomyocyte apoptosis via the PI3K/AKT/mTOR pathway. Evidence-Based Complement Alternat Med. 2017;2017.
Arola OJ, Saraste A, Pulkki K, Kallajoki M, Parvinen M, Voipio-Pulkki L-M. Acute doxorubicin cardiotoxicity involves cardiomyocyte apoptosis. Can Res. 2000;60(7):1789-1792.
Ghosh J, Das J, Manna P, Sil PC. The protective role of arjunolic acid against doxorubicin induced intracellular ROS dependent JNK-p38 and p53-mediated cardiac apoptosis. Biomaterials. 2011;32(21):4857-4866.
Zhu W, Soonpaa MH, Chen H, et al. Acute doxorubicin cardiotoxicity is associated with p53-induced inhibition of the mTOR pathway. Circulation. 2009;119(1):99.
Weinberg LE, Singal PK. Refractory heart failure and age-related differences in adriamycin-induced myocardial changes in rats. Can J Physiol Pharmacol. 1987;65(9):1957-1965.
Singla DK, Ahmed A, Singla R, Yan B. Embryonic stem cells improve cardiac function in doxorubicin-induced cardiomyopathy mediated through multiple mechanisms. Cell Transplant. 2012;21(9):1919-1930.
Feridooni T, Hotchkiss A, Remley-Carr S, Saga Y, Pasumarthi KB. Cardiomyocyte specific ablation of p53 is not sufficient to block doxorubicin induced cardiac fibrosis and associated cytoskeletal changes. PLoS One. 2011;6(7):e22801.
Mukhopadhyay P, Rajesh M, Batkai S, et al. CB1 cannabinoid receptors promote oxidative stress and cell death in murine models of doxorubicin-induced cardiomyopathy and in human cardiomyocytes. Cardiovasc Res. 2010;85(4):773-784.
Zhu W, Shou W, Payne RM, Caldwell R, Field LJ. A mouse model for juvenile doxorubicin-induced cardiac dysfunction. Pediatr Res. 2008;64(5):488-494.