Intranasal Delivery of Endothelial Cell-Derived Extracellular Vesicles with Supramolecular Gel Attenuates Myocardial Ischemia-Reperfusion Injury

References

• Yeh RW, Sidney S, Chandra M, Sorel M, Selby JV, Go AS. Population trends in the incidence and outcomes of acute myocardial infarction. N Engl J Med. 2010;362(23):2155–2165. doi:10.1056/NEJMoa0908610
   PubMed Web of Science ®Google Scholar
• Davidson SM, Ferdinandy P, Andreadou I, et al. Multitarget Strategies to Reduce Myocardial Ischemia/Reperfusion Injury: JACC Review Topic of the Week. J Am Coll Cardiol. 2019;73(1):89–99. doi:10.1016/j.jacc.2018.09.086
   PubMed Web of Science ®Google Scholar
• Neri M, Riezzo I, Pascale N, Pomara C, Turillazzi E. Ischemia/Reperfusion Injury following Acute Myocardial Infarction: a Critical Issue for Clinicians and Forensic Pathologists. Mediators Inflamm. 2017;2017:7018393. doi:10.1155/2017/7018393
   PubMed Web of Science ®Google Scholar
• Prabhu SD, Frangogiannis NG. The Biological Basis for Cardiac Repair After Myocardial Infarction: from Inflammation to Fibrosis. Circ Res. 2016;119(1):91–112. doi:10.1161/CIRCRESAHA.116.303577
   PubMed Web of Science ®Google Scholar
• Kain V, Prabhu SD and Halade GV. Inflammation revisited: inflammation versus resolution of inflammation following myocardial infarction. Basic Res Cardiol. 2014;109(6):444. doi: 10.1007/s00395-014-0444-7
   PubMed Web of Science ®Google Scholar
• Timmers L, Pasterkamp G, de Hoog VC, Arslan F, Appelman Y, de Kleijn DP. The innate immune response in reperfused myocardium. Cardiovasc Res. 2012;94(2):276–283. doi:10.1093/cvr/cvs018
   PubMed Web of Science ®Google Scholar
• Ong SB, Hernandez-Resendiz S, Crespo-Avilan GE, et al. Inflammation following acute myocardial infarction: multiple players, dynamic roles, and novel therapeutic opportunities. Pharmacol Ther. 2018;186:73–87. doi:10.1016/j.pharmthera.2018.01.001
   PubMed Web of Science ®Google Scholar
• Wu X, Reboll MR, Korf-Klingebiel M, Wollert KC. Angiogenesis after acute myocardial infarction. Cardiovasc Res. 2021;117(5):1257–1273. doi:10.1093/cvr/cvaa287
   PubMed Web of Science ®Google Scholar
• Tombor LS, John D, Glaser SF, et al. Single cell sequencing reveals endothelial plasticity with transient mesenchymal activation after myocardial infarction. Nat Commun. 2021;12(1):681. doi:10.1038/s41467-021-20905-1
   PubMed Web of Science ®Google Scholar
• Godo S, Shimokawa H. Endothelial Functions. Arterioscler Thromb Vasc Biol. 2017;37(9):e108–e114. doi:10.1161/ATVBAHA.117.309813
   PubMed Web of Science ®Google Scholar
• Vancheri F, Longo G, Vancheri S, Henein M. Coronary Microvascular Dysfunction. J Clin Med. 2020;9(9):2880. doi:10.3390/jcm9092880
   PubMed Web of Science ®Google Scholar
• Hosseinkhani B, Kuypers S, van den Akker NMS, Molin DGM, Michiels L. Extracellular Vesicles Work as a Functional Inflammatory Mediator Between Vascular Endothelial Cells and Immune Cells. Front Immunol. 2018;9:1789. doi:10.3389/fimmu.2018.01789
   PubMed Web of Science ®Google Scholar
• Li M, Li S, Du C, et al. Exosomes from different cells: characteristics, modifications, and therapeutic applications. Eur J Med Chem. 2020;207:112784. doi:10.1016/j.ejmech.2020.112784
   PubMed Web of Science ®Google Scholar
• Hoshino A, Kim HS, Bojmar L, et al. Extracellular Vesicle and Particle Biomarkers Define Multiple Human Cancers. Cell. 2020;182(4):1044–1061 e18. doi:10.1016/j.cell.2020.07.009
   PubMed Web of Science ®Google Scholar
• Zhao J, Li X, Hu J, et al. Mesenchymal stromal cell-derived exosomes attenuate myocardial ischaemia-reperfusion injury through miR-182-regulated macrophage polarization. Cardiovasc Res. 2019;115(7):1205–1216. doi:10.1093/cvr/cvz040
   PubMed Web of Science ®Google Scholar
• Sadeghi S, Tehrani FR, Tahmasebi S, Shafiee A, Hashemi SM. Exosome engineering in cell therapy and drug delivery. Inflammopharmacology. 2023;31(1):145–169. doi:10.1007/s10787-022-01115-7
   PubMed Web of Science ®Google Scholar
• Njock MS, Cheng HS, Dang LT, et al. Endothelial cells suppress monocyte activation through secretion of extracellular vesicles containing antiinflammatory microRNAs. Blood. 2015;125(20):3202–3212. doi:10.1182/blood-2014-11-611046
   PubMed Web of Science ®Google Scholar
• Paone S, Baxter AA, Hulett MD, Poon IKH. Endothelial cell apoptosis and the role of endothelial cell-derived extracellular vesicles in the progression of atherosclerosis. Cell Mol Life Sci. 2019;76(6):1093–1106. doi:10.1007/s00018-018-2983-9
   PubMed Web of Science ®Google Scholar
• Togliatto G, Dentelli P, Rosso A, et al. PDGF-BB Carried by Endothelial Cell-Derived Extracellular Vesicles Reduces Vascular Smooth Muscle Cell Apoptosis in Diabetes. Diabetes. 2018;67(4):704–716. doi:10.2337/db17-0371
   PubMed Web of Science ®Google Scholar
• Todorova D, Simoncini S, Lacroix R, Sabatier F, Dignat-George F. Extracellular Vesicles in Angiogenesis. Circ Res. 2017;120(10):1658–1673. doi:10.1161/CIRCRESAHA.117.309681
   PubMed Web of Science ®Google Scholar
• Herman S, Fishel I, Offen D. Intranasal delivery of mesenchymal stem cells-derived extracellular vesicles for the treatment of neurological diseases. Stem Cells. 2021, 39(12):1589–1600. doi:10.1002/stem.3456
   PubMed Web of Science ®Google Scholar
• Tai J, Han M, Lee D, Park IH, Lee SH, Kim TH. Different Methods and Formulations of Drugs and Vaccines for Nasal Administration. Pharmaceutics. 2022;14(5):1073. doi:10.3390/pharmaceutics14051073
   PubMed Web of Science ®Google Scholar
• Du X, Zhou J, Shi J, Xu B. Supramolecular Hydrogelators and Hydrogels: from Soft Matter to Molecular Biomaterials. Chem Rev. 2015;115(24):13165–13307. doi:10.1021/acs.chemrev.5b00299
   PubMed Web of Science ®Google Scholar
• Wang JT, Rodrigo AC, Patterson AK, et al. Enhanced Delivery of Neuroactive Drugs via Nasal Delivery with a Self-Healing Supramolecular Gel. Adv Sci. 2021;8(14):e2101058. doi:10.1002/advs.202101058
   Web of Science ®Google Scholar
• Hawkins K, Patterson AK, Clarke PA, Smith DK. Catalytic Gels for a Prebiotically Relevant Asymmetric Aldol Reaction in Water: from Organocatalyst Design to Hydrogel Discovery and Back Again. J Am Chem Soc. 2020;142(9):4379–4389. doi:10.1021/jacs.9b13156
   PubMed Web of Science ®Google Scholar
• Hu H, Dong L, Bu Z, Shen Y, Liu Z. miR-23a-3p-abundant small extracellular vesicles released from Gelma/nanoclay hydrogel for cartilage regeneration. J Extracell Vesicles. 2020;9(1):1778883.
   PubMed Web of Science ®Google Scholar
• Laham S, Broxup B, Robinet M, Potvin M, Schrader K. Subacute inhalation toxicity of benzaldehyde in the Sprague-Dawley rat. Am Ind Hyg Assoc J. 1991;52(12):503–510. doi:10.1080/15298669191365126
   PubMed Web of Science ®Google Scholar
• Andersen A. Final report on the safety assessment of benzaldehyde. Int J Toxicol. 2006;25(Suppl 1):11–27. doi:10.1080/10915810600716612
   PubMedGoogle Scholar
• Wan Z, Zhao L, Lu F, et al. Mononuclear phagocyte system blockade improves therapeutic exosome delivery to the myocardium. Theranostics. 2020;10(1):218–230. doi:10.7150/thno.38198
   PubMed Web of Science ®Google Scholar
• Humeres C, Frangogiannis NG. Fibroblasts in the Infarcted, Remodeling, and Failing Heart. JACC Basic Translational Sci. 2019;4(3):449–467. doi:10.1016/j.jacbts.2019.02.006
   PubMedGoogle Scholar
• Qiao S, Zhang W, Yin Y, et al. Extracellular vesicles derived from Kruppel-Like Factor 2-overexpressing endothelial cells attenuate myocardial ischemia-reperfusion injury by preventing Ly6C(high) monocyte recruitment. Theranostics. 2020;10(25):11562–11579. doi:10.7150/thno.45459
   PubMed Web of Science ®Google Scholar
• Leuschner F, Panizzi P, Chico-Calero I, et al. Angiotensin-converting enzyme inhibition prevents the release of monocytes from their splenic reservoir in mice with myocardial infarction. Circ Res. 2010;107(11):1364–1373. doi:10.1161/CIRCRESAHA.110.227454
   PubMed Web of Science ®Google Scholar
• Shahidi M. Thrombosis and von Willebrand Factor. Adv Exp Med Biol. 2017;906:285–306. doi:10.1007/5584_2016_122
   PubMed Web of Science ®Google Scholar
• Zhang X, Gong P, Zhao Y, et al. Endothelial caveolin-1 regulates cerebral thrombo-inflammation in acute ischemia/reperfusion injury. EBioMedicine. 2022;84:104275. doi:10.1016/j.ebiom.2022.104275
   PubMed Web of Science ®Google Scholar
• Grassin-Delyle S, Buenestado A, Naline E, et al. Intranasal drug delivery: an efficient and non-invasive route for systemic administration: focus on opioids. Pharmacol Ther Jun. 2012;134(3):366–379. doi:10.1016/j.pharmthera.2012.03.003
   PubMed Web of Science ®Google Scholar
• Cone AS, Yuan X, Sun L, et al. Mesenchymal stem cell-derived extracellular vesicles ameliorate Alzheimer’s disease-like phenotypes in a preclinical mouse model. Theranostics. 2021;11(17):8129–8142. doi:10.7150/thno.62069
   PubMed Web of Science ®Google Scholar
• Narbute K, Pilipenko V, Pupure J, et al. Intranasal Administration of Extracellular Vesicles Derived from Human Teeth Stem Cells Improves Motor Symptoms and Normalizes Tyrosine Hydroxylase Expression in the Substantia Nigra and Striatum of the 6-Hydroxydopamine-Treated Rats. Stem Cells Transl Med. 2019;8(5):490–499. doi:10.1002/sctm.18-0162
   PubMed Web of Science ®Google Scholar
• Losurdo M, Pedrazzoli M, D’Agostino C, et al. Intranasal delivery of mesenchymal stem cell-derived extracellular vesicles exerts immunomodulatory and neuroprotective effects in a 3xTg model of Alzheimer’s disease. Stem Cells Transl Med. 2020;9(9):1068–1084. doi:10.1002/sctm.19-0327
   PubMed Web of Science ®Google Scholar
• Peng H, Li Y, Ji W, et al. Intranasal Administration of Self-Oriented Nanocarriers Based on Therapeutic Exosomes for Synergistic Treatment of Parkinson’s Disease. ACS Nano. 2022;16(1):869–884. doi:10.1021/acsnano.1c08473
   PubMed Web of Science ®Google Scholar
• Nguyen DV, Li F, Li H, et al. Drug permeation through skin is inversely correlated with carrier gel rigidity. Mol Pharm. 2015;12(2):444–452. doi:10.1021/mp500542a
   PubMedGoogle Scholar
• Frangogiannis NG. Regulation of the inflammatory response in cardiac repair. Circ Res. 2012;110(1):159–173. doi:10.1161/CIRCRESAHA.111.243162
   PubMed Web of Science ®Google Scholar
• Dewald O, Zymek P, Winkelmann K, et al. CCL2/Monocyte Chemoattractant Protein-1 regulates inflammatory responses critical to healing myocardial infarcts. Circ Res. 2005;96(8):881–889. doi:10.1161/01.RES.0000163017.13772.3a
   PubMed Web of Science ®Google Scholar
• Bujak M, Dobaczewski M, Chatila K, et al. Interleukin-1 receptor type I signaling critically regulates infarct healing and cardiac remodeling. Am J Pathol. 2008;173(1):57–67. doi:10.2353/ajpath.2008.070974
   PubMed Web of Science ®Google Scholar
• Hilfiker-Kleiner D, Shukla P, Klein G, et al. Continuous glycoprotein-130-mediated signal transducer and activator of transcription-3 activation promotes inflammation, left ventricular rupture, and adverse outcome in subacute myocardial infarction. Circulation. 2010;122(2):145–155. doi:10.1161/CIRCULATIONAHA.109.933127
   PubMed Web of Science ®Google Scholar
• Wan Q, Xu C, Zhu L, et al. Targeting PDE4B (Phosphodiesterase-4 Subtype B) for Cardioprotection in Acute Myocardial Infarction via Neutrophils and Microcirculation. Circ Res. 2022;131(5):442–455. doi:10.1161/CIRCRESAHA.122.321365
   PubMed Web of Science ®Google Scholar
• Cantaluppi V, Gatti S, Medica D, et al. Microvesicles derived from endothelial progenitor cells protect the kidney from ischemia-reperfusion injury by microRNA-dependent reprogramming of resident renal cells. Kidney Int. 2012;82(4):412–427. doi:10.1038/ki.2012.105
   PubMed Web of Science ®Google Scholar
• Deanfield JE, Halcox JP, Rabelink TJ. Endothelial function and dysfunction: testing and clinical relevance. Circulation. 2007;115(10):1285–1295. doi:10.1161/CIRCULATIONAHA.106.652859
   PubMed Web of Science ®Google Scholar
• Dube KN, Thomas TM, Munshaw S, Rohling M, Riley PR, Smart N. Recapitulation of developmental mechanisms to revascularize the ischemic heart. JCI Insight. 2017;2(22). doi:10.1172/jci.insight.96800
   PubMed Web of Science ®Google Scholar