Abstract
With cardiovascular disease has remained a leading cause of death and treatment modalities for myocardial tissue repair have provided promise and life to damaged heart tissue patients. Biomaterials, including natural and synthetic polymers, have shown effectiveness towards cell differentiation and proliferation. Small amounts of collagen in the matrix increase the biocompatibility and biodegradability, and thus the matrix employed in the study utilized a composition consisting of chitosan (CNPs) and collagen (Coll). In this study, gold nanoparticles (GNP) were added to the matrix to enhance the electrical conductivity to improve the heart function. 5-Azacitidine (5-Aza) was incorporated into the matrix to induce myogenic differentiation. The prepared matrix of GNP-5-Aza@CNPs@Coll thus had a hydrodynamic diameter of 382 nm and an electrical conductivity of 120.2 μs/cm. Loading of 5-Aza and gold nanoparticles in the matrix has been confirmed through HPLC and ICP-OES analyses, while FTIR bands confirmed the fingerprint of each component of composite. Biocompatibility of the matrix has been established through hemolysis assays. Animal studies revealed promising application of the matrix as injectable formulations for myocardial tissue engineering. In essence, the study opens a promise for otherwise challenged myocardial tissue engineering, through appropriate combination of chitosan, collagen, 5-Aza, and gold nanoparticles, leading to a biocompatible and potentially biodegradable matrix.
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The datasets generated during and/or analyzed during the study are available on reasonable request.
References
A.E. Azab, Acute myocardial infarction risk factors and correlation of its markers with serum lipids. J. Appl. Biotechnol. Bioeng. 3(4), 00075 (2017)
J. Qin, S. Zhou, Z. Li, Y. Chen, Q. Qin, T. Ai, Combination of magnetic resonance imaging and targeted contrast agent for the diagnosis of myocardial infarction. Exp. Ther. Med. 16(4), 3303–3308 (2018). https://doi.org/10.3892/etm.2018.6600
J. Bejarano, M. Navarro-Marquez, F. Morales-Zavala, J.O. Morales, I. Garcia-Carvajal, E. Araya-Fuentes, Y. Flores, H.E. Verdejo, P.F. Castro, S. Lavandero, M.J. Kogan, Nanoparticles for diagnosis and therapy of atherosclerosis and myocardial infarction: evolution toward prospective theranostic approaches. Theranostics 8(17), 4710–4732 (2018). https://doi.org/10.7150/thno.26284
P.-M. Boarescu, I. Chirilă, A.E. Bulboacă, I.C. Bocșan, R.M. Pop, D. Gheban, S.D. Bolboacă, Effects of curcumin nanoparticles in isoproterenol-induced myocardial infarction. Oxid. Med. Cell. Longev. 2019, 7847142 (2019). https://doi.org/10.1155/2019/7847142
D.J. Lundy, K.-H. Chen, E.K.-W. Toh, P.C.-H. Hsieh, Distribution of systemically administered nanoparticles reveals a size-dependent effect immediately following cardiac ischaemia-reperfusion injury. Sci. Rep. 6(1), 1–10 (2016)
Qian Q, Qian H, Zhang X, Zhu W, Yan Y, Ye S, Peng X, Li W, Xu Z, Lingyun Sun, Wenrong Xu, 5-Azacytidine induces cardiac differentiation of human umbilical cord-derived mesenchymal stem cells by activating extracellular regulated kinase. Stem Cells Dev. 21(1), 67–75 (2012)
Perea-Gil I, Prat-Vidal C, Bayes-Genis A, In vivo experience with natural scaffolds for myocardial infarction: the times they are a-changin, Stem Cell Res. Ther. 6(1), 1-25 (2015)
S. Farzamfar, M. Aleahmad, S. Gholamreza, S. Majid, N. Niloofar, Polycaprolactone/gelatin nanofibrous scaffolds for tissue engineering. Biointerface Res Appl Chem 11, 11104–11115 (2020)
Muzzarelli RAA, Biomedical exploitation of chitin and chitosan via mechano-chemical disassembly, electrospinning, dissolution in imidazolium ionic liquids, and supercritical drying. Mar. Drugs 9(9), 1510–1533 (2011)
Best C, Fukunishi T, Drews J, Khosravi R, Hor K, Mahler N, Yi T, Humphrey JD, Johnson J, Christopher K. Breuer, Narutoshi Hibino, Oversized biodegradable arterial grafts promote enhanced neointimal tissue formation. Tissue Eng. Part A 24(15-16), 1251–1261 (2018)
M. Abudhahir, A. Saleem, P. Paramita, S.D. Kumar, C. Tze-Wen, N. Selvamurugan, A. Moorthi, Polycaprolactone fibrous electrospun scaffolds reinforced with copper doped wollastonite for bone tissue engineering applications. J. Biomed. Mater. Res. B Appl. Biomater. 109(5), 654–664 (2021). https://doi.org/10.1002/jbm.b.34729
K. Mohamed Abudhahir, R. Murugesan, R. Vijayashree, N. Selvamurugan, T.-W. Chung, A. Moorthi, Metal doped calcium silicate biomaterial for skin tissue regeneration in vitro. J. Biomater. Appl. 36(1), 140–151 (2021)
Pestov A, Bratskaya SJM, Chitosan and its derivatives as highly efficient polymer ligands. Molecules 21(3), 330 (2016)
Kravanja G, Primožič M, Knez Ž, Leitgeb MJM, Chitosan-based (nano) materials for novel biomedical applications. Molecules 24(10), 960 (2019)
B. Beleño Acosta, R.C. Advincula, C.D. Grande-Tovar, Chitosan-based scaffolds for the treatment of myocardial infarction: a systematic review. Molecules 28(4), 1920 (2023)
S. Kazemi Asl, M. Rahimzadegan, R. Ostadrahimi, The recent advancement in the chitosan hybrid-based scaffolds for cardiac regeneration after myocardial infarction. Carbohydr. Polym. 300, 120266 (2023). https://doi.org/10.1016/j.carbpol.2022.120266
V. Sharma, A. Manhas, S. Gupta, M. Dikshit, K. Jagavelu, R.S. Verma, Fabrication, characterization and in vivo assessment of cardiogel loaded chitosan patch for myocardial regeneration. Int. J. Biol. Macromol. 222, 3045–3056 (2022). https://doi.org/10.1016/j.ijbiomac.2022.10.079
P. Singh, S. Pandit, V. Mokkapati, A. Garg, V. Ravikumar, I. Mijakovic, Gold nanoparticles in diagnostics and therapeutics for human cancer. Int. J. Mol. Sci. 19(7) (2018). https://doi.org/10.3390/ijms19071979
R.S. Darweesh, N.M. Ayoub, S. Nazzal, Gold nanoparticles and angiogenesis: molecular mechanisms and biomedical applications. Int. J. Nanomedicine 14, 7643–7663 (2019). https://doi.org/10.2147/IJN.S223941
M. Meyer, Processing of collagen based biomaterials and the resulting materials properties. Biomed. Eng. Online 18(1), 24 (2019). https://doi.org/10.1186/s12938-019-0647-0
H. Mohammadi, P.D. Arora, C.A. Simmons, P.A. Janmey, C.A. McCulloch, Inelastic behaviour of collagen networks in cell-matrix interactions and mechanosensation. J. R. Soc. Interface 12(102), 20141074 (2015). https://doi.org/10.1098/rsif.2014.1074
K.A. Jansen, A.J. Licup, A. Sharma, R. Rens, F.C. MacKintosh, G.H. Koenderink, The role of network architecture in collagen mechanics. Biophys. J. 114(11), 2665–2678 (2018). https://doi.org/10.1016/j.bpj.2018.04.043
W.-q. Wu, S. Peng, Z.-y. Song, S. Lin, Collagen biomaterial for the treatment of myocardial infarction: an update on cardiac tissue engineering and myocardial regeneration. Drug Deliv. Transl. Res. 9(5), 920–934 (2019). https://doi.org/10.1007/s13346-019-00627-0
L.A. Reis, L.L.Y. Chiu, Y. Liang, K. Hyunh, A. Momen, M. Radisic, A peptide-modified chitosan–collagen hydrogel for cardiac cell culture and delivery. Acta Biomater. 8(3), 1022–1036 (2012). https://doi.org/10.1016/j.actbio.2011.11.030
Y. Wang, Z. Fan, Q. Li, J. Lu, X. Wang, J. Zhang, Z. Wu, Construction of a myocardial patch with mesenchymal stem cells and poly(CL-co-TOSUO)/collagen scaffolds for myocardial infarction repair by coaxial electrospinning. J. Mater. Chem. B (2023). https://doi.org/10.1039/D3TB00174A
S. Cesur, S. Ulag, L. Ozak, A. Gumussoy, S. Arslan, B.K. Yilmaz, N. Ekren, M. Agirbasli, D.M. Kalaskar, O. Gunduz, Production and characterization of elastomeric cardiac tissue-like patches for myocardial tissue engineering. Polymer Testing 90, 106613 (2020). https://doi.org/10.1016/j.polymertesting.2020.106613
J.H. Fu, M. Zhao, Y.R. Lin, X.D. Tian, Y.D. Wang, Z.X. Wang, L.X. Wang, Degradable chitosan-collagen composites seeded with cells as tissue engineered heart valves. Heart Lung Circ. 26(1), 94–100 (2017). https://doi.org/10.1016/j.hlc.2016.05.116
S. Narayan, A. Rajagopalan, J.S. Reddy, A. Chadha, BSA binding to silica capped gold nanostructures: effect of surface cap and conjugation design on nanostructure-BSA interface. RSC Adv. 4(3), 1412–1420 (2014). https://doi.org/10.1039/C3RA45887C
W. Fan, W. Yan, Z. Xu, H. Ni, Formation mechanism of monodisperse, low molecular weight chitosan nanoparticles by ionic gelation technique. Colloids Surf. B Biointerfaces 90, 21–27 (2012). https://doi.org/10.1016/j.colsurfb.2011.09.042
L. Ding, C. Hao, Y. Xue, H. Ju, A bio-inspired support of gold nanoparticles−chitosan nanocomposites gel for immobilization and electrochemical study of K562 leukemia cells. Biomacromolecules 8(4), 1341–1346 (2007). https://doi.org/10.1021/bm061224y
V.V.S.R. Karri, G. Kuppusamy, S.V. Talluri, S.S. Mannemala, R. Kollipara, A.D. Wadhwani, S. Mulukutla, K.R.S. Raju, R. Malayandi, Curcumin loaded chitosan nanoparticles impregnated into collagen-alginate scaffolds for diabetic wound healing. Int. J. Biol. Macromol. 93, 1519–1529 (2016). https://doi.org/10.1016/j.ijbiomac.2016.05.038
A. Tasatargil, N. Kuscu, S. Dalaklioglu, D. Adiguzel, C. Celik-Ozenci, S. Ozdem, A. Barutcigil, S. Ozdem, Cardioprotective effect of nesfatin-1 against isoproterenol-induced myocardial infarction in rats: role of the Akt/GSK-3β pathway. Peptides 95, 1–9 (2017). https://doi.org/10.1016/j.peptides.2017.07.003
M. Rajadurai, P. Stanely Mainzen Prince, Preventive effect of naringin on isoproterenol-induced cardiotoxicity in Wistar rats: an in vivo and in vitro study. Toxicology 232(3), 216–225 (2007). https://doi.org/10.1016/j.tox.2007.01.006
S.M. Ahmed, S.A. Abdelrahman, A.E. Salama, Efficacy of gold nanoparticles against isoproterenol induced acute myocardial infarction in adult male albino rats. Ultrastruct. Pathol. 41(2), 168–185 (2017). https://doi.org/10.1080/01913123.2017.1281367
Y.S. Kim, W.S. Kang, J.S. Kwon, M.H. Hong, H.Y. Jeong, H.C. Jeong, M.H. Jeong, Y. Ahn, Protective role of 5-azacytidine on myocardial infarction is associated with modulation of macrophage phenotype and inhibition of fibrosis. J. Cell. Mol. Med. 18(6), 1018–1027 (2014). https://doi.org/10.1111/jcmm.12248
M.Y. Spivak, R.V. Bubnov, I.M. Yemets, L.M. Lazarenko, N.O. Tymoshok, Z.R. Ulberg, Development and testing of gold nanoparticles for drug delivery and treatment of heart failure: a theranostic potential for PPP cardiology. The EPMA Journal 4(1), 20–20 (2013). https://doi.org/10.1186/1878-5085-4-20
S. Fleischer, M. Shevach, R. Feiner, T. Dvir, Coiled fiber scaffolds embedded with gold nanoparticles improve the performance of engineered cardiac tissues. Nanoscale 6(16), 9410–9414 (2014). https://doi.org/10.1039/c4nr00300d
P. Baei, S. Jalili-Firoozinezhad, S. Rajabi-Zeleti, M. Tafazzoli-Shadpour, H. Baharvand, N. Aghdami, Electrically conductive gold nanoparticle-chitosan thermosensitive hydrogels for cardiac tissue engineering. Mater. Sci. Eng. C 63, 131–141 (2016). https://doi.org/10.1016/j.msec.2016.02.056
A. Ahmadi, B. Vulesevic, N.J.R. Blackburn, J.J.M. Ruel, E.J. Suuronen, A collagen-chitosan injectable hydrogel improves cardiac remodeling in a mouse model of myocardial infarction. J. Biomater. Tissue. Eng. 4(11), 886–894 (2014). https://doi.org/10.1166/jbt.2014.1264
W. Dai, L.E. Wold, J.S. Dow, R.A. Kloner, Thickening of the infarcted wall by collagen injection improves left ventricular function in rats. J. Am. Coll. Cardiol. 46(4), 714 (2005)
Z. Cui, B. Yang, R.-K. Li, Application of biomaterials in cardiac repair and regeneration. Engineering 2(1), 141–148 (2016). https://doi.org/10.1016/J.ENG.2016.01.028
Y. Deng, J. Ren, G. Chen, G. Li, X. Wu, G. Wang, G. Gu, J. Li, Injectable in situ cross-linking chitosan-hyaluronic acid based hydrogels for abdominal tissue regeneration. Sci. Rep. 7(1), 2699 (2017). https://doi.org/10.1038/s41598-017-02962-z
A. Hasan, A. Khattab, M.A. Islam, K.A. Hweij, J. Zeitouny, R. Waters, M. Sayegh, M.M. Hossain, A. Paul, Injectable hydrogels for cardiac tissue repair after myocardial infarction. Adv. Sci. 2(11), 1500122 (2015). https://doi.org/10.1002/advs.201500122
T. Banerjee, S. Mitra, A. Kumar Singh, R. Kumar Sharma, A. Maitra, Preparation, characterization and biodistribution of ultrafine chitosan nanoparticles. Int. J. Pharm. 243(1), 93–105 (2002). https://doi.org/10.1016/S0378-5173(02)00267-3
M. Ashokkumar, K.M. Sumukh, R. Murali, N.T. Narayanan, P.M. Ajayan, P. Thanikaivelan, Collagen–chitosan biocomposites produced using nanocarbons derived from goatskin waste. Carbon 50(15), 5574–5582 (2012). https://doi.org/10.1016/j.carbon.2012.08.006
L. Thi Lanh, D. Quang Khieu, T. Thai Hoa, N. Hai Phong, H. Thi Le Hien, N. Quoc Hien, Synthesis of water soluble chitosan stabilized gold nanoparticles and determination of uric acid. Adv. Nat. Sci. Nanosci. Nanotechnol. 5(2), 025014 (2014)
R.P. Ramasamy, S.M. Maliyekkal, Formation of gold nanoparticles upon chitosan leading to formation and collapse of gels. New J. Chem. 38(1), 63–69 (2014). https://doi.org/10.1039/C3NJ00603D
A. Alagha, A. Nourallah, S. Hariri, Characterization of dexamethasone loaded collagen-chitosan sponge and in vitro release study. J. Drug Deliv. Sci. Technol. 55, 101449 (2020). https://doi.org/10.1016/j.jddst.2019.101449
S. Unser, S. Holcomb, R. Cary, L. Sagle, Collagen-gold nanoparticle conjugates for versatile biosensing. Sensors 17(2), 378 (2017). https://doi.org/10.3390/s17020378
D.R. Bhumkar, H.M. Joshi, M. Sastry, V.B. Pokharkar, Chitosan reduced gold nanoparticles as novel carriers for transmucosal delivery of insulin. Pharm. Res. 24(8), 1415–1426 (2007). https://doi.org/10.1007/s11095-007-9257-9
Y.J. Lee, E.-Y. Ahn, Y. Park, Shape-dependent cytotoxicity and cellular uptake of gold nanoparticles synthesized using green tea extract. Nanoscale Res. Lett. 14(1), 129 (2019). https://doi.org/10.1186/s11671-019-2967-1
J. Hwang, B.H. San, N.J. Turner, L.J. White, D.M. Faulk, S.F. Badylak, Y. Li, S.M. Yu, Molecular assessment of collagen denaturation in decellularized tissues using a collagen hybridizing peptide. Acta Biomater. 53, 268–278 (2017). https://doi.org/10.1016/j.actbio.2017.01.079
M. Tashakori-Miyanroudi, K. Rakhshan, M. Ramez, S. Asgarian, A. Janzadeh, Y. Azizi, A. Seifalian, F. Ramezani, Conductive carbon nanofibers incorporated into collagen bio-scaffold assists myocardial injury repair. Int. J. Biol. Macromol. 163, 1136–1146 (2020). https://doi.org/10.1016/j.ijbiomac.2020.06.259
K. Kalishwaralal, S. Jeyabharathi, K. Sundar, S. Selvamani, M. Prasanna, A. Muthukumaran, A novel biocompatible chitosan–selenium nanoparticles (SeNPs) film with electrical conductivity for cardiac tissue engineering application. Mater. Sci. Eng. C 92, 151–160 (2018). https://doi.org/10.1016/j.msec.2018.06.036
A.M. Martins, G. Eng, S.G. Caridade, J.F. Mano, R.L. Reis, G. Vunjak-Novakovic, Electrically conductive chitosan/carbon scaffolds for cardiac tissue engineering. Biomacromolecules 15(2), 635–643 (2014). https://doi.org/10.1021/bm401679q
B.C. Dash, G. Réthoré, M. Monaghan, K. Fitzgerald, W. Gallagher, A. Pandit, The influence of size and charge of chitosan/polyglutamic acid hollow spheres on cellular internalization, viability and blood compatibility. Biomaterials 31(32), 8188–8197 (2010). https://doi.org/10.1016/j.biomaterials.2010.07.067
K.M. de la Harpe, P.P.D. Kondiah, Y.E. Choonara, T. Marimuthu, L.C. du Toit, V. Pillay, The hemocompatibility of nanoparticles: a review of cell-nanoparticle interactions and hemostasis. Cells 8(10), 1209 (2019). https://doi.org/10.3390/cells8101209
K. Ichikawa, N. Aritaka, K. Ogura, N. Komatsu, T. Hirano, Strongly suspicious hemolysis caused by azacitidine in a myelodysplastic syndrome patient. Geriatr. Gerontol. Int. 14(4), 1006–1007 (2014). https://doi.org/10.1111/ggi.12226
X. Sun, H. Li, Y. Zhu, P. Xu, Q. Zuo, B. Li, X. Gu, 5-Azacytidine-induced cardiomyocyte differentiation of very small embryonic-like stem cells. Stem Cells Int. 2020, 5162350 (2020). https://doi.org/10.1155/2020/5162350
M.-C. Yang, S.-S. Wang, N.-K. Chou, N.-H. Chi, Y.-Y. Huang, Y.-L. Chang, M.-J. Shieh, T.-W. Chung, The cardiomyogenic differentiation of rat mesenchymal stem cells on silk fibroin–polysaccharide cardiac patches in vitro. Biomaterials 30(22), 3757–3765 (2009). https://doi.org/10.1016/j.biomaterials.2009.03.057
J. Leibacher, K. Dauber, S. Ehser, V. Brixner, K. Kollar, A. Vogel, G. Spohn, R. Schäfer, E. Seifried, R. Henschler, Human mesenchymal stromal cells undergo apoptosis and fragmentation after intravenous application in immune-competent mice. Cytotherapy 19(1), 61–74 (2017). https://doi.org/10.1016/j.jcyt.2016.09.010
T. Satish Kumar, D. Vijaya Ramu, N.S. Sampath Kumar, Preparation and characterization of biodegradable collagen – chitosan scaffolds. Mater. Today: Proc. 19, 2587–2590 (2019). https://doi.org/10.1016/j.matpr.2019.10.091
J. Zhang, Y. Xue, Y. Ni, F. Ning, L. Shang, A. Ma, Size dependent effects of gold nanoparticles in ISO-induced hyperthyroid rats. Sci. Rep. 8(1), 10960 (2018). https://doi.org/10.1038/s41598-018-27934-9
P.-M. Boarescu, I. Boarescu, I.C. Bocșan, R.M. Pop, D. Gheban, A.E. Bulboacă, C. Nicula, R.-M. Râjnoveanu, S.D. Bolboacă, Curcumin nanoparticles protect against isoproterenol induced myocardial infarction by alleviating myocardial tissue oxidative stress, Electrocardiogram, and Biological Changes. Molecules 24(15), 2802 (2019)
W. Bei, L. Jing, N. Chen, Cardio protective role of wogonin loaded nanoparticle against isoproterenol induced myocardial infarction by moderating oxidative stress and inflammation. Colloids Surf. B Biointerfaces 185, 110635 (2020). https://doi.org/10.1016/j.colsurfb.2019.110635
S.R. Boovarahan, G.A. Kurian, Preconditioning the rat heart with 5-azacytidine attenuates myocardial ischemia/reperfusion injury via PI3K/GSK3β and mitochondrial KATP signaling axis. J. Biochem. Mol. Toxicol. 35(12), e22911 (2021). https://doi.org/10.1002/jbt.22911
A. Vinodhini, K. Govindaraju, G. Singaravelu, A. Mohamed Sadiq, V.G. Kumar, Cardioprotective potential of biobased gold nanoparticles. Colloids Surf. B Biointerfaces 117, 480–486 (2014). https://doi.org/10.1016/j.colsurfb.2014.01.006
L. Song, M. Srilakshmi, Y. Wu, T.S.M. Saleem, Sulforaphane attenuates isoproterenol-induced myocardial injury in mice. Biomed. Res. Int. 2020, 3610285 (2020). https://doi.org/10.1155/2020/3610285
M. Ibrar, M.A. Khan, I.M. Abdullah, Evaluation of Paeonia emodi and its gold nanoparticles for cardioprotective and antihyperlipidemic potentials. J. Photochem. Photobiol. B Biol. 189, 5–13 (2018). https://doi.org/10.1016/j.jphotobiol.2018.09.018
E.M. Bakir, N.S. Younis, M.E. Mohamed, N.A. El Semary, Cyanobacteria as nanogold factories: chemical and anti-myocardial infarction properties of gold nanoparticles synthesized by Lyngbya majuscula. Mar. Drugs 16(6), 217 (2018)
Z. Huang, H. Wang, C. Gao, H. Shen, F. Xe, Drug loaded gold nano-particulates for therapeutics of myocardial infarction in rat model. J. Biomater. Tissue. Eng. 8(2), 197–205 (2018)
D. Danila, E. Johnson, P. Kee, CT imaging of myocardial scars with collagen-targeting gold nanoparticles. Nanomed. Nanotechnol. Biol. Med. 9(7), 1067–1076 (2013). https://doi.org/10.1016/j.nano.2013.03.009
C.-E. Roată, Ș. Iacob, Ș. Morărașu, C. Livadaru, I. Tudorancea, S. Luncă, M.-G. Dimofte, Collagen-binding nanoparticles: a scoping review of methods and outcomes. Crystals 11(11), 1396 (2021)
C. Dong, A. Ma, L. Shang, Animal models used in the research of nanoparticles for cardiovascular diseases. J. Nanopart. Res. 23(8), 172 (2021). https://doi.org/10.1007/s11051-021-05289-z
D.R. Amin, E. Sink, S.P. Narayan, M. Abdel-Hafiz, L. Mestroni, B. Peña, Nanomaterials for cardiac tissue engineering. Molecules 25(21), 5189 (2020)
I.C. Pop, O. Grad, E. Pall, C. Pestean, M. Mircean, I.A. Mironiuc, The relationship between left ventricular fractional shortening and intravenous administration of stem cells in laboratory rabbits presenting chronic myocardial infarction. Clujul Med 88(1), 28–32 (2015). https://doi.org/10.15386/cjmed-267
W. Dai, S.L. Hale, G.L. Kay, A.J. Jyrala, R.A. Kloner, Delivering stem cells to the heart in a collagen matrix reduces relocation of cells to other organs as assessed by nanoparticle technology. Regen. Med. 4(3), 387–395 (2009). https://doi.org/10.2217/rme.09.2
L.C. Heather, A.F. Catchpole, D.J. Stuckey, M.A. Cole, C.A. Carr, K. Clarke, Isoproterenol induces in vivo functional and metabolic abnormalities: similar to those found in the infarcted rat heart. J. Physiol. Pharmacol. 60(3), 31–39 (2009)
R. Thangaiyan, S. Arjunan, K. Govindasamy, H.A. Khan, A.S. Alhomida, N.R. Prasad, Galangin attenuates isoproterenol-induced inflammation and fibrosis in the cardiac tissue of albino Wistar rats. Front. Pharmacol. 11 (2020). https://doi.org/10.3389/fphar.2020.585163
S.S. El Shaer, T.A. Salaheldin, N.M. Saied, S.M. Abdelazim, In vivo ameliorative effect of cerium oxide nanoparticles in isoproterenol-induced cardiac toxicity. Exp. Toxicol. Pathol. 69(7), 435–441 (2017). https://doi.org/10.1016/j.etp.2017.03.001
P.-M. Boarescu, I. Boarescu, A.E. Bulboacă, I.C. Bocșan, R.M. Pop, D. Gheban, R.-M. Râjnoveanu, A. Râjnoveanu, Ş.H. Roşian, A.D. Buzoianu, S.D. Bolboacă, Multi-organ protective effects of curcumin nanoparticles on drug-induced acute myocardial infarction in rats with type 1 diabetes mellitus. Appl. Sci. 11(12), 5497 (2021)
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The authors thank Chettinad Academy of Research and Education for funding student project. We thank CSIR-CLRI and IIT Madras for instrumentation facilities.
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Nikitha Shalom, R., Narayan, S., Sangamithra, N. et al. 5-Azacytidine incorporated chitosan/collagen/gold nanoparticle matrix preparation and characterization with potential to repair myocardial infarction. emergent mater. 6, 1563–1576 (2023). https://doi.org/10.1007/s42247-023-00534-8
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DOI: https://doi.org/10.1007/s42247-023-00534-8