Amniotic membrane mesenchymal stem cells labeled by iron oxide nanoparticles exert cardioprotective effects against isoproterenol (ISO)-induced myocardial damage by targeting inflammatory MAPK/NF-κB pathway.


Journal

Drug delivery and translational research
ISSN: 2190-3948
Titre abrégé: Drug Deliv Transl Res
Pays: United States
ID NLM: 101540061

Informations de publication

Date de publication:
02 2021
Historique:
pubmed: 23 5 2020
medline: 26 11 2021
entrez: 23 5 2020
Statut: ppublish

Résumé

The aim of the present study is to investigate the protective effects of human amniotic membrane-derived mesenchymal stem cells (hAMSCs) labeled by superparamagnetic iron oxide nanoparticles (SPIONs) against isoproterenol (ISO)-induced myocardial injury in the presence and absence of a magnetic field. ISO was injected subcutaneously for 4 consecutive days to induce myocardial injury in male Wistar rats. The hAMSCs were incubated with 100 μg/ml SPIONs and injected to rats in magnet-dependent and magnet-independent groups via the tail vein. The size and shape of nanoparticles were determined by dynamic light scattering (DLS) and transmission electron microscopy (TEM). Prussian blue staining was used to determine cell uptake of nanoparticles. Myocardial fibrosis, heart function, characterization of hAMSCs, and histopathological changes were determined using Masson's trichrome, echocardiography, flow cytometry, and H&E staining, respectively. Enzyme-linked immunosorbent assay (ELISA) was used to the expression pro-inflammatory cytokines. Immunohistochemistry assay was used to determine the expression of nuclear factor-κB (NF-κB) and the Ras/mitogen-activated protein kinase (MAPK). SPION-labeled MSCs in the presence of magnetic field significantly improved cardiac function and reduced fibrosis and tissue damage by suppressing inflammation in a NF-κB/MAPK-dependent mechanism (p < 0. 05). Collectively, our findings demonstrate that SPION-labeled MSCs in the presence of magnetic field can be a good treatment option to reduce inflammation following myocardial injury. Graphical abstract.

Identifiants

pubmed: 32441012
doi: 10.1007/s13346-020-00788-3
pii: 10.1007/s13346-020-00788-3
doi:

Substances chimiques

NF-kappa B 0
Mitogen-Activated Protein Kinases EC 2.7.11.24
Isoproterenol L628TT009W

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

242-254

Références

Aizik G, Grad E, Golomb G. Monocyte-mediated drug delivery systems for the treatment of cardiovascular diseases. Drug Deliv Transl Res. 2018;8:868–82.
doi: 10.1007/s13346-017-0431-2
Saporito F, et al. In situ gelling scaffolds loaded with platelet growth factors to improve cardiomyocyte survival after ischemia. ACS Biomater Sci Eng. 2018;5:329–38.
Amani H, et al. Three-dimensional graphene foams: synthesis, properties, biocompatibility, biodegradability, and applications in tissue engineering. ACS Biomater Sci Eng. 2018;5:193–214.
Ramani GV, Uber PA, Mehra MR Chronic heart failure: contemporary diagnosis and management. In: Mayo Clinic Proceedings, 2010. vol 2. Elsevier, pp 180–195.
Afousi AG, Gaeini A, Rakhshan K, Naderi N, Azar AD, Aboutaleb N. Targeting necroptotic cell death pathway by high-intensity interval training (HIIT) decreases development of post-ischemic adverse remodelling after myocardial ischemia/reperfusion injury. J Cell Commun Signal. 2019;13:255–67.
doi: 10.1007/s12079-018-0481-3
Rakhshan K, Azizi Y, Naderi N, Afousi AG, Aboutaleb N. ELABELA (ELA) peptide exerts cardioprotection against myocardial infarction by targeting oxidative stress and the improvement of heart function. Int J Pept Res Ther. 2019;25:613–21.
doi: 10.1007/s10989-018-9707-8
Souri F, Rakhshan K, Erfani S, Azizi Y, Maleki SN, Aboutaleb N. Natural lavender oil (Lavandula angustifolia) exerts cardioprotective effects against myocardial infarction by targeting inflammation and oxidative stress. Inflammopharmacology. 2019;27:799–807.
doi: 10.1007/s10787-018-0520-y
Jin L, et al. Gallic acid improves cardiac dysfunction and fibrosis in pressure overload-induced heart failure. Sci Rep. 2018;8:9302.
doi: 10.1038/s41598-018-27599-4
Nguyen M-N, et al. Mechanisms responsible for increased circulating levels of galectin-3 in cardiomyopathy and heart failure. Sci Rep. 2018;8:8213.
doi: 10.1038/s41598-018-26115-y
Attalla DM, Ahmed LA, Zaki HF, Khattab MM. Paradoxical effects of atorvastatin in isoproterenol-induced cardiotoxicity in rats: role of oxidative stress and inflammation. Biomed Pharmacother. 2018;104:542–9.
doi: 10.1016/j.biopha.2018.05.005
Suchal K, Malik S, Gamad N, Malhotra RK, Goyal SN, Ojha S, et al. Mangiferin protect myocardial insults through modulation of MAPK/TGF-β pathways. Eur J Pharmacol. 2016;776:34–43.
Verma VK, Malik S, Narayanan SP, Mutneja E, Sahu AK, Bhatia J, et al. Role of MAPK/NF-κB pathway in cardioprotective effect of Morin in isoproterenol induced myocardial injury in rats. Mol Biol Rep. 2019;46:1139–48.
doi: 10.1007/s11033-018-04575-9
Amani H, Arzaghi H, Bayandori M, Dezfuli AS, Pazoki-Toroudi H, Shafiee A, et al. Controlling cell behavior through the design of biomaterial surfaces: a focus on surface modification techniques. Adv Mater Interfaces. 2019a:1900572.
Mueller P, Lemcke H, David R. Stem cell therapy in heart diseases–cell types, mechanisms and improvement strategies. Cell Physiol Biochem. 2018;48:2607–55.
doi: 10.1159/000492704
Kobayashi K, et al. Fibrin glue-aided, instant epicardial placement enhances the efficacy of mesenchymal stromal cell-based therapy for heart failure. Sci Rep. 2018;8:9448.
doi: 10.1038/s41598-018-27881-5
Nazarinia D, Aboutaleb N, Gholamzadeh R, Maleki SN, Mokhtari B, Nikougoftar M. Conditioned medium obtained from human amniotic mesenchymal stem cells attenuates focal cerebral ischemia/reperfusion injury in rats by targeting mTOR pathway. J Chem Neuroanat. 2019:101707.
Wobma HM, Liu D, Vunjak-Novakovic G. Paracrine effects of mesenchymal stromal cells cultured in three-dimensional settings on tissue repair. ACS Biomater Sci Eng. 2017;4:1162–75.
Liu S, et al. Strategies to optimize adult stem cell therapy for tissue regeneration. Int J Mol Sci. 2016;17:982.
doi: 10.3390/ijms17060982
Li X, et al. Iron oxide nanoparticles promote the migration of mesenchymal stem cells to injury sites. Int J Nanomedicine. 2019;14:573.
doi: 10.2147/IJN.S184920
Amani H, Habibey R, Shokri F, Hajmiresmail SJ, Akhavan O, Mashaghi A, et al. Selenium nanoparticles for targeted stroke therapy through modulation of inflammatory and metabolic signaling. Sci Rep. 2019b;9:1–15.
doi: 10.1038/s41598-019-42633-9
Amani H, Mostafavi E, Alebouyeh MR, Arzaghi H, Akbarzadeh A, Pazoki-Toroudi H, et al. Would colloidal gold nanocarriers present an effective diagnosis or treatment for ischemic stroke? Int J Nanomedicine. 2019d;14:8013–31.
doi: 10.2147/IJN.S210035
Ahn YJ, Kong TH, Choi JS, Yun WS, Key J, Seo YJ. Strategies to enhance efficacy of SPION-labeled stem cell homing by magnetic attraction: a systemic review with meta-analysis. Int J Nanomedicine. 2019;14:4849.
doi: 10.2147/IJN.S204910
Duan X, et al. The long-term fate of mesenchymal stem cells labeled with magnetic resonance imaging-visible polymersomes in cerebral ischemia. Int J Nanomedicine. 2017;12:6705.
doi: 10.2147/IJN.S146742
Amani H, Habibey R, Hajmiresmail S, Latifi S, Pazoki-Toroudi H, Akhavan O. Antioxidant nanomaterials in advanced diagnoses and treatments of ischemia reperfusion injuries. J Mater Chem B. 2017;5:9452–76.
doi: 10.1039/C7TB01689A
Bull E, Madani SY, Sheth R, Seifalian A, Green M, Seifalian AM. Stem cell tracking using iron oxide nanoparticles. Int J Nanomedicine. 2014;9:1641.
pubmed: 24729700 pmcid: 3976208
Li X-X, et al. In vivo MRI tracking of iron oxide nanoparticle-labeled human mesenchymal stem cells in limb ischemia. Int J Nanomedicine. 2013;8:1063.
pubmed: 23515426 pmcid: 3598527
Santoso MR, Yang PC. Magnetic nanoparticles for targeting and imaging of stem cells in myocardial infarction. Stem Cells Int. 2016, 2016.
Naseroleslami M, Aboutaleb N, Parivar K. The effects of superparamagnetic iron oxide nanoparticles-labeled mesenchymal stem cells in the presence of a magnetic field on attenuation of injury after heart failure. Drug Deliv Transl Res. 2018;8:1214–25.
Wu X, Li M, Chen SQ, Li S, Guo F. Pin1 facilitates isoproterenol-induced cardiac fibrosis and collagen deposition by promoting oxidative stress and activating the MEK1/2-ERK1/2 signal transduction pathway in rats. Int J Mol Med. 2018;41:1573–83.
pubmed: 29286102
Naseroleslami M, Parivar K, Khoei S, Aboutaleb N. Magnetic resonance imaging of human-derived amniotic membrane stem cells using PEGylated superparamagnetic iron oxide nanoparticles. Cell Journal (Yakhteh). 2016;18:332.
Ajami M, et al. Expression of Bcl-2 and Bax after hippocampal ischemia in DHA+ EPA treated rats. Neurol Sci. 2011;32:811.
doi: 10.1007/s10072-011-0621-5
Amani H, Kazerooni H, Hassanpoor H, Akbarzadeh A, Pazoki-Toroudi H. Tailoring synthetic polymeric biomaterials towards nerve tissue engineering: a review. Artif Cells Nanomed Biotechnol. 2019c;47:3524–39.
doi: 10.1080/21691401.2019.1639723
Habibey R, Ajami M, Ebrahimi SA, Hesami A, Babakoohi S, Pazoki-Toroudi H. Nitric oxide and renal protection in morphine-dependent rats. Free Radic Biol Med. 2010;49:1109–18.
doi: 10.1016/j.freeradbiomed.2010.06.024
Pazoki-Toroudi H, Nassiri-Kashani M, Tabatabaie H, Ajami M, Habibey R, Shizarpour M, et al. Combination of azelaic acid 5% and erythromycin 2% in the treatment of acne vulgaris. J Dermatol Treat. 2010;21:212–6.
doi: 10.3109/09546630903440064
dos Santos RB, de Almeida FM, Sales CM, De Lima S, Martinez AMB. Injection of bone marrow mesenchymal stem cells by intravenous or intraperitoneal routes is a viable alternative to spinal cord injury treatment in mice. Neural Regen Res. 2018;13:1046.
doi: 10.4103/1673-5374.233448
Traverse JH. Is there a role for intravenous stem cell delivery in nonischemic cardiomyopathy? Am Heart Assoc. 2017.
Hany E, Sobh MA, ElKhier MTA, ElSabaa HM, Zaher AR. The effect of different routes of injection of bone marrow mesenchymal stem cells on parotid glands of rats receiving cisplatin: a comparative study. Int J Stem Cell. 2017;10:169.
Mokhtari B, Aboutaleb N, Nazarinia D, Nikougoftar M, Razavi Tousi SMT, Molazem M, et al. Comparison of the effects of intramyocardial and intravenous injections of human mesenchymal stem cells on cardiac regeneration after heart failure. IJBMS. 2020.
Yanai A, et al. Focused magnetic stem cell targeting to the retina using superparamagnetic iron oxide nanoparticles. Cell Transplant. 2012;21:1137–48.
doi: 10.3727/096368911X627435
Vaněček V, et al. Highly efficient magnetic targeting of mesenchymal stem cells in spinal cord injury. Int J Nanomedicine. 2012;7:3719.
doi: 10.2147/IJN.S32824
Chaudeurge A, Wilhelm C, Chen-Tournoux A, Farahmand P, Bellamy V, Autret G, et al. Can magnetic targeting of magnetically labeled circulating cells optimize intramyocardial cell retention? Cell Transplant. 2012;21:679–91.
doi: 10.3727/096368911X612440
Shen W-B, et al. Cell-based therapy in TBI: magnetic retention of neural stem cells in vivo. Cell Transplant. 2016;25:1085–99.
doi: 10.3727/096368915X689550
Ryu Y, et al. Gallic acid prevents isoproterenol-induced cardiac hypertrophy and fibrosis through regulation of JNK2 signaling and Smad3 binding activity. Sci Rep. 2016;6:34790.
doi: 10.1038/srep34790
Kocak C, et al. Molecular and biochemical evidence on the protective effects of embelin and carnosic acid in isoproterenol-induced acute myocardial injury in rats. Life Sci. 2016;147:15–23.
doi: 10.1016/j.lfs.2016.01.038
Khan SI, et al. Febuxostat modulates MAPK/NF-κBp65/TNF-α signaling in cardiac ischemia-reperfusion injury. Oxidative Med Cell Longev. 2017;2017.
Muslin AJ. MAPK signalling in cardiovascular health and disease: molecular mechanisms and therapeutic targets. Clin Sci. 2008;115:203–18.
doi: 10.1042/CS20070430

Auteurs

Maryam Naseroleslami (M)

Department of Cellular and Molecular Biology, Faculty of Advanced Science and Technology, Tehran Medical Sciences, Islamic Azad University, Tehran, Iran. naseroleslami@gmail.com.

Nahid Aboutaleb (N)

Physiology Research Center, Iran University of Medical Sciences, Tehran, Iran. dr_nabo40@yahoo.com.
Department of Physiology, Faculty of Medicine, Iran University of Medical Sciences, Tehran, Iran. dr_nabo40@yahoo.com.

Behnaz Mokhtari (B)

Physiology Research Center, Iran University of Medical Sciences, Tehran, Iran.
Department of Physiology, Faculty of Medicine, Iran University of Medical Sciences, Tehran, Iran.

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