Nanoparticle Interactions with Endothelial Cells
Jibanananda Mishra, Jiban Jyoti Panda
Nanoparticles (NPs) have earned significant attention for their prospective applications in various disciplines, including medicine. Discerning the interactions between NPs and biological systems is critical for the development of safe and effective nanomedicines. The interactions between NPs and endothelial cells play a pivotal role in drug delivery, diagnostics, and therapeutic interventions. This article aims on the complex interaction between NPs and endothelial cells, which configure the inner lining of the blood vessels. This chapter also discusses various mechanisms of NP-endothelial cell interactions, their implications in vascular biology, and the potential applications of these interactions in nanomedicine.
Keywords
Nanoparticles, Endothelial Cells, Interactions, Uptake, Therapeutic Applications
Published online 12/15/2024, 34 pages
Citation: Jibanananda Mishra, Jiban Jyoti Panda, Nanoparticle Interactions with Endothelial Cells, Materials Research Foundations, Vol. 171, pp 217-250, 2024
DOI: https://doi.org/10.21741/9781644903339-8
Part of the book on Advances in Healthcare and Nanoparticle Toxicology
References
[1] K. Lin, P.-P. Hsu, B.P. Chen, S. Yuan, S. Usami, J.Y.-J. Shyy, Y.-S. Li, S. Chien, Molecular mechanism of endothelial growth arrest by laminar shear stress, Proc. Natl. Acad. Sci. 97 (2000) 9385–9389. https://doi.org/10.1073/pnas.170282597.
[2] D. Gospodarowicz, J. Moran, D. Braun, C. Birdwell, Clonal growth of bovine vascular endothelial cells: fibroblast growth factor as a survival agent., Proc. Natl. Acad. Sci. 73 (1976) 4120–4124. https://doi.org/10.1073/pnas.73.11.4120.
[3] M.A. Gimbrone, G. García-Cardeña, Endothelial Cell Dysfunction and the Pathobiology of Atherosclerosis, Circ. Res. 118 (2016) 620–636. https://doi.org/10.1161/CIRCRESAHA.115.306301.
[4] B.T. Luk, L. Zhang, Cell membrane-camouflaged nanoparticles for drug delivery, J. Controlled Release 220 (2015) 600–607. https://doi.org/10.1016/j.jconrel.2015.07.019.
[5] J.-I. Koga, T. Matoba, K. Egashira, Anti-inflammatory Nanoparticle for Prevention of Atherosclerotic Vascular Diseases, J. Atheroscler. Thromb. 23 (2016) 757–765. https://doi.org/10.5551/jat.35113.
[6] A. Jayagopal, P.K. Russ, F.R. Haselton, Surface Engineering of Quantum Dots for In Vivo Vascular Imaging, Bioconjug. Chem. 18 (2007) 1424–1433. https://doi.org/10.1021/bc070020r.
[7] Y. Zhao, Y. Zhang, G. Qin, J. Cheng, W. Zeng, S. Liu, H. Kong, X. Wang, Q. Wang, H. Qu, In vivo biodistribution and behavior of CdTe/ZnS quantum dots, Int. J. Nanomedicine Volume 12 (2017) 1927–1939. https://doi.org/10.2147/IJN.S121075.
[8] Y. Yu, J. Gao, L. Jiang, J. Wang, Antidiabetic nephropathy effects of synthesized gold nanoparticles through mitigation of oxidative stress, Arab. J. Chem. 14 (2021) 103007. https://doi.org/10.1016/j.arabjc.2021.103007.
[9] Y. Pan, S. Neuss, A. Leifert, M. Fischler, F. Wen, U. Simon, G. Schmid, W. Brandau, W. Jahnen‐Dechent, Size‐Dependent Cytotoxicity of Gold Nanoparticles, Small 3 (2007) 1941–1949. https://doi.org/10.1002/smll.200700378.
[10] M.H. Sarfraz, M. Zubair, B. Aslam, A. Ashraf, M.H. Siddique, S. Hayat, J.N. Cruz, S. Muzammil, M. Khurshid, M.F. Sarfraz, A. Hashem, T.M. Dawoud, G.D. Avila-Quezada, E.F. Abd_Allah, Comparative analysis of phyto-fabricated chitosan, copper oxide, and chitosan-based CuO nanoparticles: antibacterial potential against Acinetobacter baumannii isolates and anticancer activity against HepG2 cell lines, Front. Microbiol. 14 (2023) 1188743. https://doi.org/10.3389/fmicb.2023.1188743.
[11] P. Gupta, E. Garcia, A. Sarkar, S. Kapoor, K. Rafiq, H.S. Chand, R.D. Jayant, Nanoparticle Based Treatment for Cardiovascular Diseases, Cardiovasc. Hematol. Disord.-Drug Targets 19 (2019) 33–44. https://doi.org/10.2174/1871529X18666180508113253.
[12] F. Li, H. Shao, G. Zhou, B. Wang, Y. Xu, W. Liang, L. Chen, The recent applications of nanotechnology in the diagnosis and treatment of common cardiovascular diseases, Vascul. Pharmacol. 152 (2023) 107200. https://doi.org/10.1016/j.vph.2023.107200.
[13] P. Mancuso, A. Calleri, G. Gregato, V. Labanca, J. Quarna, P. Antoniotti, L. Cuppini, G. Finocchiaro, M. Eoli, V. Rosti, F. Bertolini, A Subpopulation of Circulating Endothelial Cells Express CD109 and is Enriched in the Blood of Cancer Patients, PLoS ONE 9 (2014) e114713. https://doi.org/10.1371/journal.pone.0114713.
[14] Y.-J. Chiu, K. Kusano, T.N. Thomas, K. Fujiwara, Endothelial Cell-Cell Adhesion and Mechanosignal Transduction, Endothelium 11 (2004) 59–73. https://doi.org/10.1080/10623320490432489.
[15] C. Cerutti, A.J. Ridley, Endothelial cell-cell adhesion and signaling, Exp. Cell Res. 358 (2017) 31–38. https://doi.org/10.1016/j.yexcr.2017.06.003.
[16] D. Mehta, A.B. Malik, Signaling Mechanisms Regulating Endothelial Permeability, Physiol. Rev. 86 (2006) 279–367. https://doi.org/10.1152/physrev.00012.2005.
[17] F.H. Epstein, S. Moncada, A. Higgs, The L-Arginine-Nitric Oxide Pathway, N. Engl. J. Med. 329 (1993) 2002–2012. https://doi.org/10.1056/NEJM199312303292706.
[18] K. Ley, C. Laudanna, M.I. Cybulsky, S. Nourshargh, Getting to the site of inflammation: the leukocyte adhesion cascade updated, Nat. Rev. Immunol. 7 (2007) 678–689. https://doi.org/10.1038/nri2156.
[19] P. Carmeliet, R.K. Jain, Molecular mechanisms and clinical applications of angiogenesis, Nature 473 (2011) 298–307. https://doi.org/10.1038/nature10144.
[20] N. Ferrara, K. Alitalo, Clinical applications of angiogenic growth factors and their inhibitors, Nat. Med. 5 (1999) 1359–1364. https://doi.org/10.1038/70928.
[21] T.M. Kiio, S. Park, Physical properties of nanoparticles do matter, J. Pharm. Investig. 51 (2021) 35–51. https://doi.org/10.1007/s40005-020-00504-w.
[22] X. Duan, Y. Li, Physicochemical Characteristics of Nanoparticles Affect Circulation, Biodistribution, Cellular Internalization, and Trafficking, Small 9 (2013) 1521–1532. https://doi.org/10.1002/smll.201201390.
[23] Y. Zhao, Y. Wang, F. Ran, Y. Cui, C. Liu, Q. Zhao, Y. Gao, D. Wang, S. Wang, A comparison between sphere and rod nanoparticles regarding their in vivo biological behavior and pharmacokinetics, Sci. Rep. 7 (2017) 4131. https://doi.org/10.1038/s41598-017-03834-2.
[24] P. Foroozandeh, A.A. Aziz, Insight into Cellular Uptake and Intracellular Trafficking of Nanoparticles, Nanoscale Res. Lett. 13 (2018) 339. https://doi.org/10.1186/s11671-018-2728-6.
[25] S. Behzadi, V. Serpooshan, W. Tao, M.A. Hamaly, M.Y. Alkawareek, E.C. Dreaden, D. Brown, A.M. Alkilany, O.C. Farokhzad, M. Mahmoudi, Cellular uptake of nanoparticles: journey inside the cell, Chem. Soc. Rev. 46 (2017) 4218–4244. https://doi.org/10.1039/C6CS00636A.
[26] E. Blanco, H. Shen, M. Ferrari, Principles of nanoparticle design for overcoming biological barriers to drug delivery, Nat. Biotechnol. 33 (2015) 941–951. https://doi.org/10.1038/nbt.3330.
[27] A. Amruta, D. Iannotta, S.W. Cheetham, T. Lammers, J. Wolfram, Vasculature organotropism in drug delivery, Adv. Drug Deliv. Rev. 201 (2023) 115054. https://doi.org/10.1016/j.addr.2023.115054.
[28] M.D. Howard, E.D. Hood, C.F. Greineder, I.S. Alferiev, M. Chorny, V. Muzykantov, Targeting to Endothelial Cells Augments the Protective Effect of Novel Dual Bioactive Antioxidant/Anti-Inflammatory Nanoparticles, Mol. Pharm. 11 (2014) 2262–2270. https://doi.org/10.1021/mp400677y.
[29] S.H. Anastasiadis, K. Chrissopoulou, E. Stratakis, P. Kavatzikidou, G. Kaklamani, A. Ranella, How the Physicochemical Properties of Manufactured Nanomaterials Affect Their Performance in Dispersion and Their Applications in Biomedicine: A Review, Nanomaterials 12 (2022) 552. https://doi.org/10.3390/nano12030552.
[30] S. Gelperina, O. Maksimenko, A. Khalansky, L. Vanchugova, E. Shipulo, K. Abbasova, R. Berdiev, S. Wohlfart, N. Chepurnova, J. Kreuter, Drug delivery to the brain using surfactant-coated poly(lactide-co-glycolide) nanoparticles: Influence of the formulation parameters, Eur. J. Pharm. Biopharm. 74 (2010) 157–163. https://doi.org/10.1016/j.ejpb.2009.09.003.
[31] M.P. Monopoli, D. Walczyk, A. Campbell, G. Elia, I. Lynch, F. Baldelli Bombelli, K.A. Dawson, Physical−Chemical Aspects of Protein Corona: Relevance to in Vitro and in Vivo Biological Impacts of Nanoparticles, J. Am. Chem. Soc. 133 (2011) 2525–2534. https://doi.org/10.1021/ja107583h.
[32] M. Pacurari, Y. Qian, W. Fu, D. Schwegler-Berry, M. Ding, V. Castranova, N.L. Guo, Cell Permeability, Migration, and Reactive Oxygen Species Induced by Multiwalled Carbon Nanotubes in Human Microvascular Endothelial Cells, J. Toxicol. Environ. Health A 75 (2012) 112–128. https://doi.org/10.1080/15287394.2011.615110.
[33] B. Dehouck, M.P. Dehouck, J.C. Fruchart, R. Cecchelli, Upregulation of the low density lipoprotein receptor at the blood-brain barrier: intercommunications between brain capillary endothelial cells and astrocytes., J. Cell Biol. 126 (1994) 465–473. https://doi.org/10.1083/jcb.126.2.465.
[34] R.E. Serda, J. Gu, J.K. Burks, K. Ferrari, C. Ferrari, M. Ferrari, Quantitative mechanics of endothelial phagocytosis of silicon microparticles, Cytometry A 75A (2009) 752–760. https://doi.org/10.1002/cyto.a.20769.
[35] S. Muro, ed., Drug Delivery Systems that Fuse with Plasmalemma, in: Drug Deliv. Physiol. Barriers, 0 ed., Jenny Stanford Publishing, 2016: pp. 309–330. https://doi.org/10.1201/b19907-16.
[36] S. Xu, B.Z. Olenyuk, C.T. Okamoto, S.F. Hamm-Alvarez, Targeting receptor-mediated endocytotic pathways with nanoparticles: Rationale and advances, Adv. Drug Deliv. Rev. 65 (2013) 121–138. https://doi.org/10.1016/j.addr.2012.09.041.
[37] Z. Wang, C. Tiruppathi, R.D. Minshall, A.B. Malik, Size and Dynamics of Caveolae Studied Using Nanoparticles in Living Endothelial Cells, ACS Nano 3 (2009) 4110–4116. https://doi.org/10.1021/nn9012274.
[38] S. Mayor, R.E. Pagano, Pathways of clathrin-independent endocytosis, Nat. Rev. Mol. Cell Biol. 8 (2007) 603–612. https://doi.org/10.1038/nrm2216.
[39] J. Yoo, C. Park, G. Yi, D. Lee, H. Koo, Active Targeting Strategies Using Biological Ligands for Nanoparticle Drug Delivery Systems, Cancers 11 (2019) 640. https://doi.org/10.3390/cancers11050640.
[40] A.K. Pearce, R.K. O’Reilly, Insights into Active Targeting of Nanoparticles in Drug Delivery: Advances in Clinical Studies and Design Considerations for Cancer Nanomedicine, Bioconjug. Chem. 30 (2019) 2300–2311. https://doi.org/10.1021/acs.bioconjchem.9b00456.
[41] T. Dos Santos, J. Varela, I. Lynch, A. Salvati, K.A. Dawson, Quantitative Assessment of the Comparative Nanoparticle‐Uptake Efficiency of a Range of Cell Lines, Small 7 (2011) 3341–3349. https://doi.org/10.1002/smll.201101076.
[42] C. Guo, M. Yang, L. Jing, J. Wang, Y. Yu, Y. Li, J. Duan, X. Zhou, Y. Li, Z. Zwsun@Ccmu.Edu.Cn, Amorphous silica nanoparticles trigger vascular endothelial cell injury through apoptosis and autophagy via reactive oxygen species-mediated MAPK/Bcl-2 and PI3K/Akt/mTOR signaling, Int. J. Nanomedicine Volume 11 (2016) 5257–5276. https://doi.org/10.2147/IJN.S112030.
[43] P. Laux, C. Riebeling, A.M. Booth, J.D. Brain, J. Brunner, C. Cerrillo, O. Creutzenberg, I. Estrela-Lopis, T. Gebel, G. Johanson, H. Jungnickel, H. Kock, J. Tentschert, A. Tlili, A. Schäffer, A.J.A.M. Sips, R.A. Yokel, A. Luch, Biokinetics of nanomaterials: The role of biopersistence, NanoImpact 6 (2017) 69–80. https://doi.org/10.1016/j.impact.2017.03.003.
[44] B. Bahrami, M. Hojjat-Farsangi, H. Mohammadi, E. Anvari, G. Ghalamfarsa, M. Yousefi, F. Jadidi-Niaragh, Nanoparticles and targeted drug delivery in cancer therapy, Immunol. Lett. 190 (2017) 64–83. https://doi.org/10.1016/j.imlet.2017.07.015.
[45] S. Raj, S. Khurana, R. Choudhari, K.K. Kesari, M.A. Kamal, N. Garg, J. Ruokolainen, B.C. Das, D. Kumar, Specific targeting cancer cells with nanoparticles and drug delivery in cancer therapy, Semin. Cancer Biol. 69 (2021) 166–177. https://doi.org/10.1016/j.semcancer.2019.11.002.
[46] L. Bareford, P. Swaan, Endocytic mechanisms for targeted drug delivery☆, Adv. Drug Deliv. Rev. 59 (2007) 748–758. https://doi.org/10.1016/j.addr.2007.06.008.
[47] R.V. Stan, Endothelial stomatal and fenestral diaphragms in normal vessels and angiogenesis, J. Cell. Mol. Med. 11 (2007) 621–643. https://doi.org/10.1111/j.1582-4934.2007.00075.x.
[48] R. Bawa, Nanoparticle-based therapeutics in humans: A survey, Nanotechnol. Law Bus. 5 (2008) 135–155.
[49] N.D. Donahue, H. Acar, S. Wilhelm, Concepts of nanoparticle cellular uptake, intracellular trafficking, and kinetics in nanomedicine, Adv. Drug Deliv. Rev. 143 (2019) 68–96. https://doi.org/10.1016/j.addr.2019.04.008.
[50] S.A. Smith, L.I. Selby, A.P.R. Johnston, G.K. Such, The Endosomal Escape of Nanoparticles: Toward More Efficient Cellular Delivery, Bioconjug. Chem. 30 (2019) 263–272. https://doi.org/10.1021/acs.bioconjchem.8b00732.
[51] G. Sahay, W. Querbes, C. Alabi, A. Eltoukhy, S. Sarkar, C. Zurenko, E. Karagiannis, K. Love, D. Chen, R. Zoncu, Y. Buganim, A. Schroeder, R. Langer, D.G. Anderson, Efficiency of siRNA delivery by lipid nanoparticles is limited by endocytic recycling, Nat. Biotechnol. 31 (2013) 653–658. https://doi.org/10.1038/nbt.2614.
[52] P. Vader, E.A. Mol, G. Pasterkamp, R.M. Schiffelers, Extracellular vesicles for drug delivery, Adv. Drug Deliv. Rev. 106 (2016) 148–156. https://doi.org/10.1016/j.addr.2016.02.006.
[53] O.M. Elsharkasy, J.Z. Nordin, D.W. Hagey, O.G. De Jong, R.M. Schiffelers, S.E. Andaloussi, P. Vader, Extracellular vesicles as drug delivery systems: Why and how?, Adv. Drug Deliv. Rev. 159 (2020) 332–343. https://doi.org/10.1016/j.addr.2020.04.004.
[54] J.A. Champion, S. Mitragotri, Role of target geometry in phagocytosis, Proc. Natl. Acad. Sci. 103 (2006) 4930–4934. https://doi.org/10.1073/pnas.0600997103.
[55] S.G. Han, B. Newsome, B. Hennig, Titanium dioxide nanoparticles increase inflammatory responses in vascular endothelial cells, Toxicology 306 (2013) 1–8. https://doi.org/10.1016/j.tox.2013.01.014.
[56] T.-C. Tsou, S.-C. Yeh, F.-Y. Tsai, H.-J. Lin, T.-J. Cheng, H.-R. Chao, L.-A. Tai, Zinc oxide particles induce inflammatory responses in vascular endothelial cells via NF-κB signaling, J. Hazard. Mater. 183 (2010) 182–188. https://doi.org/10.1016/j.jhazmat.2010.07.010.
[57] K. Peters, R.E. Unger, A.M. Gatti, E. Sabbioni, R. Tsaryk, C.J. Kirkpatrick, Metallic Nanoparticles Exhibit Paradoxical Effects on Oxidative Stress and Pro-Inflammatory Response in Endothelial Cells in Vitro, Int. J. Immunopathol. Pharmacol. 20 (2007) 685–695. https://doi.org/10.1177/039463200702000404.
[58] M.D. Mauricio, S. Guerra-Ojeda, P. Marchio, S.L. Valles, M. Aldasoro, I. Escribano-Lopez, J.R. Herance, M. Rocha, J.M. Vila, V.M. Victor, Nanoparticles in Medicine: A Focus on Vascular Oxidative Stress, Oxid. Med. Cell. Longev. 2018 (2018) 1–20. https://doi.org/10.1155/2018/6231482.
[59] G. Taneja, A. Sud, N. Pendse, B. Panigrahi, A. Kumar, A.K. Sharma, Nano-medicine and Vascular Endothelial Dysfunction: Options and Delivery Strategies, Cardiovasc. Toxicol. 19 (2019) 1–12. https://doi.org/10.1007/s12012-018-9491-x.
[60] M.L. Carmo Bastos, J.V. Silva-Silva, J. Neves Cruz, A.R. Palheta da Silva, A.A. Bentaberry-Rosa, G. da Costa Ramos, J.E. de Sousa Siqueira, M.R. Coelho-Ferreira, S. Percário, P. Santana Barbosa Marinho, A.M. do R. Marinho, M. de Oliveira Bahia, M.F. Dolabela, Alkaloid from Geissospermum sericeum Benth. & Hook.f. ex Miers (Apocynaceae) Induce Apoptosis by Caspase Pathway in Human Gastric Cancer Cells, Pharmaceuticals 16 (2023) 765. https://doi.org/10.3390/ph16050765.
[61] Y. Cao, J. Long, L. Liu, T. He, L. Jiang, C. Zhao, Z. Li, A review of endoplasmic reticulum (ER) stress and nanoparticle (NP) exposure, Life Sci. 186 (2017) 33–42. https://doi.org/10.1016/j.lfs.2017.08.003.
[62] Q. Li, Y. Feng, R. Wang, R. Liu, Y. Ba, H. Huang, Recent insights into autophagy and metals/nanoparticles exposure, Toxicol. Res. 39 (2023) 355–372. https://doi.org/10.1007/s43188-023-00184-2.
[63] L. Jia, S.-L. Hao, W.-X. Yang, Nanoparticles induce autophagy via mTOR pathway inhibition and reactive oxygen species generation, Nanomed. 15 (2020) 1419–1435. https://doi.org/10.2217/nnm-2019-0387.
[64] W. Osburn, T. Kensler, Nrf2 signaling: An adaptive response pathway for protection against environmental toxic insults, Mutat. Res. Mutat. Res. 659 (2008) 31–39. https://doi.org/10.1016/j.mrrev.2007.11.006.
[65] E. Dejana, Endothelial cell–cell junctions: happy together, Nat. Rev. Mol. Cell Biol. 5 (2004) 261–270. https://doi.org/10.1038/nrm1357.
[66] C.-H. Li, M.-K. Shyu, C. Jhan, Y.-W. Cheng, C.-H. Tsai, C.-W. Liu, C.-C. Lee, R.-M. Chen, J.-J. Kang, Gold Nanoparticles Increase Endothelial Paracellular Permeability by Altering Components of Endothelial Tight Junctions, and Increase Blood-Brain Barrier Permeability in Mice, Toxicol. Sci. 148 (2015) 192–203. https://doi.org/10.1093/toxsci/kfv176.
[67] S. Tenzer, D. Docter, J. Kuharev, A. Musyanovych, V. Fetz, R. Hecht, F. Schlenk, D. Fischer, K. Kiouptsi, C. Reinhardt, K. Landfester, H. Schild, M. Maskos, S.K. Knauer, R.H. Stauber, Rapid formation of plasma protein corona critically affects nanoparticle pathophysiology, Nat. Nanotechnol. 8 (2013) 772–781. https://doi.org/10.1038/nnano.2013.181.
[68] A. Aliyandi, C. Reker-Smit, R. Bron, I.S. Zuhorn, A. Salvati, Correlating Corona Composition and Cell Uptake to Identify Proteins Affecting Nanoparticle Entry into Endothelial Cells, ACS Biomater. Sci. Eng. 7 (2021) 5573–5584. https://doi.org/10.1021/acsbiomaterials.1c00804.
[69] A. Nel, T. Xia, L. Mädler, N. Li, Toxic Potential of Materials at the Nanolevel, Science 311 (2006) 622–627. https://doi.org/10.1126/science.1114397.
[70] U. Förstermann, Nitric oxide and oxidative stress in vascular disease, Pflüg. Arch. – Eur. J. Physiol. 459 (2010) 923–939. https://doi.org/10.1007/s00424-010-0808-2.
[71] Y. Cao, The Toxicity of Nanoparticles to Human Endothelial Cells, in: Q. Saquib, M. Faisal, A.A. Al-Khedhairy, A.A. Alatar (Eds.), Cell. Mol. Toxicol. Nanoparticles, Springer International Publishing, Cham, 2018: pp. 59–69. https://doi.org/10.1007/978-3-319-72041-8_4.
[72] M. Shilo, A. Sharon, K. Baranes, M. Motiei, J.-P.M. Lellouche, R. Popovtzer, The effect of nanoparticle size on the probability to cross the blood-brain barrier: an in-vitro endothelial cell model, J. Nanobiotechnology 13 (2015) 19. https://doi.org/10.1186/s12951-015-0075-7.
[73] A. Aliyandi, S. Satchell, R.E. Unger, B. Bartosch, R. Parent, I.S. Zuhorn, A. Salvati, Effect of endothelial cell heterogeneity on nanoparticle uptake, Int. J. Pharm. 587 (2020) 119699. https://doi.org/10.1016/j.ijpharm.2020.119699.
[74] I. Rahman, S.K. Biswas, P.A. Kirkham, Regulation of inflammation and redox signaling by dietary polyphenols, Biochem. Pharmacol. 72 (2006) 1439–1452. https://doi.org/10.1016/j.bcp.2006.07.004.
[75] B. Li, M. Tang, Research progress of nanoparticle toxicity signaling pathway, Life Sci. 263 (2020) 118542. https://doi.org/10.1016/j.lfs.2020.118542.
[76] M. Valko, D. Leibfritz, J. Moncol, M.T.D. Cronin, M. Mazur, J. Telser, Free radicals and antioxidants in normal physiological functions and human disease, Int. J. Biochem. Cell Biol. 39 (2007) 44–84. https://doi.org/10.1016/j.biocel.2006.07.001.
[77] T.A. Springer, Adhesion receptors of the immune system, Nature 346 (1990) 425–434. https://doi.org/10.1038/346425a0.
[78] I.F. Charo, R.M. Ransohoff, The Many Roles of Chemokines and Chemokine Receptors in Inflammation, N. Engl. J. Med. 354 (2006) 610–621. https://doi.org/10.1056/NEJMra052723.
[79] A. Sukhanova, S. Bozrova, P. Sokolov, M. Berestovoy, A. Karaulov, I. Nabiev, Dependence of Nanoparticle Toxicity on Their Physical and Chemical Properties, Nanoscale Res. Lett. 13 (2018) 44. https://doi.org/10.1186/s11671-018-2457-x.
[80] V. Lenders, X. Koutsoumpou, A. Sargsian, B.B. Manshian, Biomedical nanomaterials for immunological applications: ongoing research and clinical trials, Nanoscale Adv. 2 (2020) 5046–5089. https://doi.org/10.1039/D0NA00478B.
[81] M.A. Dobrovolskaia, S.E. McNeil, Immunological properties of engineered nanomaterials, Nat. Nanotechnol. 2 (2007) 469–478. https://doi.org/10.1038/nnano.2007.223.
[82] T. Heitzer, T. Schlinzig, K. Krohn, T. Meinertz, T. Münzel, Endothelial Dysfunction, Oxidative Stress, and Risk of Cardiovascular Events in Patients With Coronary Artery Disease, Circulation 104 (2001) 2673–2678. https://doi.org/10.1161/hc4601.099485.
[83] A. Abdal Dayem, M. Hossain, S. Lee, K. Kim, S. Saha, G.-M. Yang, H. Choi, S.-G. Cho, The Role of Reactive Oxygen Species (ROS) in the Biological Activities of Metallic Nanoparticles, Int. J. Mol. Sci. 18 (2017) 120. https://doi.org/10.3390/ijms18010120.
[84] Z. Wang, M. Tang, Research progress on toxicity, function, and mechanism of metal oxide nanoparticles on vascular endothelial cells, J. Appl. Toxicol. 41 (2021) 683–700. https://doi.org/10.1002/jat.4121.
[85] J.N. Cruz, S.G. Silva, D.S. Pereira, A.P. da S. Souza Filho, M.S. de Oliveira, R.R. Lima, E.H. de A. Andrade, In Silico Evaluation of the Antimicrobial Activity of Thymol—Major Compounds in the Essential Oil of Lippia thymoides Mart. & Schauer (Verbenaceae), Molecules 27 (2022). https://doi.org/10.3390/molecules27154768.
[86] J. Duan, Y. Yu, Y. Li, Y. Yu, Y. Li, X. Zhou, P. Huang, Z. Sun, Toxic Effect of Silica Nanoparticles on Endothelial Cells through DNA Damage Response via Chk1-Dependent G2/M Checkpoint, PLoS ONE 8 (2013) e62087. https://doi.org/10.1371/journal.pone.0062087.
[87] M. Zhu, L. Du, R. Zhao, H.Y. Wang, Y. Zhao, G. Nie, R.-F. Wang, Cell-Penetrating Nanoparticles Activate the Inflammasome to Enhance Antibody Production by Targeting Microtubule-Associated Protein 1-Light Chain 3 for Degradation, ACS Nano 14 (2020) 3703–3717. https://doi.org/10.1021/acsnano.0c00962.
[88] J. Wu, Z. Zhu, W. Liu, Y. Zhang, Y. Kang, J. Liu, C. Hu, R. Wang, M. Zhang, L. Chen, L. Shao, How Nanoparticles Open the Paracellular Route of Biological Barriers: Mechanisms, Applications, and Prospects, ACS Nano 16 (2022) 15627–15652. https://doi.org/10.1021/acsnano.2c05317.
[89] J.K. Tee, L.X. Yip, E.S. Tan, S. Santitewagun, A. Prasath, P.C. Ke, H.K. Ho, D.T. Leong, Nanoparticles’ interactions with vasculature in diseases, Chem. Soc. Rev. 48 (2019) 5381–5407. https://doi.org/10.1039/C9CS00309F.
[90] Y. Liu, E. Yoo, C. Han, G.J. Mahler, A.L. Doiron, Endothelial barrier dysfunction induced by nanoparticle exposure through actin remodeling via caveolae/raft-regulated calcium signalling, NanoImpact 11 (2018) 82–91. https://doi.org/10.1016/j.impact.2018.02.007.
[91] Duan, Y. Yu, Y. Yu, Y. Li, J. Wang, W. Geng, L. Jiang, Q. Li, X. Zhou, Z. Sun, Silica nanoparticles induce autophagy and endothelial dysfunction via the PI3K/Akt/mTOR signaling pathway, Int. J. Nanomedicine (2014) 5131. https://doi.org/10.2147/IJN.S71074.
[92] Y. Cao, M. Roursgaard, P.H. Danielsen, P. Møller, S. Loft, Carbon Black Nanoparticles Promote Endothelial Activation and Lipid Accumulation in Macrophages Independently of Intracellular ROS Production, PLoS ONE 9 (2014) e106711. https://doi.org/10.1371/journal.pone.0106711.
[93] H. Ota, M. Eto, M.R. Kano, T. Kahyo, M. Setou, S. Ogawa, K. Iijima, M. Akishita, Y. Ouchi, Induction of Endothelial Nitric Oxide Synthase, SIRT1, and Catalase by Statins Inhibits Endothelial Senescence Through the Akt Pathway, Arterioscler. Thromb. Vasc. Biol. 30 (2010) 2205–2211. https://doi.org/10.1161/ATVBAHA.110.210500.
[94] M. Lasak, K. Ciepluch, Overview of mechanism and consequences of endothelial leakiness caused by metal and polymeric nanoparticles, Beilstein J. Nanotechnol. 14 (2023) 329–338. https://doi.org/10.3762/bjnano.14.28.
[95] F. Zhao, Y. Zhao, Y. Liu, X. Chang, C. Chen, Y. Zhao, Cellular Uptake, Intracellular Trafficking, and Cytotoxicity of Nanomaterials, Small 7 (2011) 1322–1337. https://doi.org/10.1002/smll.201100001.
[96] C.M. Beddoes, C.P. Case, W.H. Briscoe, Understanding nanoparticle cellular entry: A physicochemical perspective, Adv. Colloid Interface Sci. 218 (2015) 48–68. https://doi.org/10.1016/j.cis.2015.01.007.
[97] G. Wardani, J. Nugraha, R. Kurnijasanti, M.R. Mustafa, S.A. Sudjarwo, Molecular Mechanism of Fucoidan Nanoparticles as Protector on Endothelial Cell Dysfunction in Diabetic Rats’ Aortas, Nutrients 15 (2023) 568. https://doi.org/10.3390/nu15030568.
[98] S. Muzammil, J. Neves Cruz, R. Mumtaz, I. Rasul, S. Hayat, M.A. Khan, A.M. Khan, M.U. Ijaz, R.R. Lima, M. Zubair, Effects of Drying Temperature and Solvents on In Vitro Diabetic Wound Healing Potential of Moringa oleifera Leaf Extracts, Molecules 28 (2023). https://doi.org/10.3390/molecules28020710.
[99] J.N. Cruz, S. Muzammil, A. Ashraf, M.U. Ijaz, M.H. Siddique, R. Abbas, M. Sadia, Saba, S. Hayat, R.R. Lima, A review on mycogenic metallic nanoparticles and their potential role as antioxidant, antibiofilm and quorum quenching agents, Heliyon 10 (2024). https://doi.org/10.1016/j.heliyon.2024.e29500.
[100] S. Allen, Y.-G. Liu, E. Scott, Engineering Nanomaterials to Address Cell-Mediated Inflammation in Atherosclerosis, Regen. Eng. Transl. Med. 2 (2016) 37–50. https://doi.org/10.1007/s40883-016-0012-9.
[101] Q. Hu, Z. Fang, J. Ge, H. Li, Nanotechnology for cardiovascular diseases, Innov. Camb. Mass 3 (2022) 100214. https://doi.org/10.1016/j.xinn.2022.100214.
[102] E.S. Ali, S.Md. Sharker, M.T. Islam, I.N. Khan, S. Shaw, Md.A. Rahman, S.J. Uddin, M.C. Shill, S. Rehman, N. Das, S. Ahmad, J.A. Shilpi, S. Tripathi, S.K. Mishra, M.S. Mubarak, Targeting cancer cells with nanotherapeutics and nanodiagnostics: Current status and future perspectives, Semin. Cancer Biol. 69 (2021) 52–68. https://doi.org/10.1016/j.semcancer.2020.01.011.
[103] R.K. Jain, P. Au, J. Tam, D.G. Duda, D. Fukumura, Engineering vascularized tissue, Nat. Biotechnol. 23 (2005) 821–823. https://doi.org/10.1038/nbt0705-821.
[104] S.S. Katta, V. Nagati, A.S.V. Paturi, S.P. Murakonda, A.B. Murakonda, M.K. Pandey, S.C. Gupta, A.K. Pasupulati, K.B. Challagundla, Neuroblastoma: Emerging trends in pathogenesis, diagnosis, and therapeutic targets, J. Controlled Release 357 (2023) 444–459. https://doi.org/10.1016/j.jconrel.2023.04.001.
[105] J. Kim, H.S. Kim, N. Lee, T. Kim, H. Kim, T. Yu, I.C. Song, W.K. Moon, T. Hyeon, Multifunctional Uniform Nanoparticles Composed of a Magnetite Nanocrystal Core and a Mesoporous Silica Shell for Magnetic Resonance and Fluorescence Imaging and for Drug Delivery, Angew. Chem. Int. Ed. 47 (2008) 8438–8441. https://doi.org/10.1002/anie.200802469.
[106] A.M. Nyström, B. Fadeel, Safety assessment of nanomaterials: Implications for nanomedicine, J. Controlled Release 161 (2012) 403–408. https://doi.org/10.1016/j.jconrel.2012.01.027.
[107] M.R.C. Marques, Q. Choo, M. Ashtikar, T.C. Rocha, S. Bremer-Hoffmann, M.G. Wacker, Nanomedicines – Tiny particles and big challenges, Adv. Drug Deliv. Rev. 151–152 (2019) 23–43. https://doi.org/10.1016/j.addr.2019.06.003.
[108] A.E. Nel, L. Mädler, D. Velegol, T. Xia, E.M.V. Hoek, P. Somasundaran, F. Klaessig, V. Castranova, M. Thompson, Understanding biophysicochemical interactions at the nano–bio interface, Nat. Mater. 8 (2009) 543–557. https://doi.org/10.1038/nmat2442.
[109] Y. Liu, J. Hardie, X. Zhang, V.M. Rotello, Effects of engineered nanoparticles on the innate immune system, Semin. Immunol. 34 (2017) 25–32. https://doi.org/10.1016/j.smim.2017.09.011.
[110] Q. Muhammad, Y. Jang, S.H. Kang, J. Moon, W.J. Kim, H. Park, Modulation of immune responses with nanoparticles and reduction of their immunotoxicity, Biomater. Sci. 8 (2020) 1490–1501. https://doi.org/10.1039/C9BM01643K.
[111] J. Wolfram, M. Zhu, Y. Yang, J. Shen, E. Gentile, D. Paolino, M. Fresta, G. Nie, C. Chen, H. Shen, M. Ferrari, Y. Zhao, Safety of Nanoparticles in Medicine, Curr. Drug Targets 16 (2015) 1671–1681. https://doi.org/10.2174/1389450115666140804124808.
[112] S. Schöttler, G. Becker, S. Winzen, T. Steinbach, K. Mohr, K. Landfester, V. Mailänder, F.R. Wurm, Protein adsorption is required for stealth effect of poly(ethylene glycol)- and poly(phosphoester)-coated nanocarriers, Nat. Nanotechnol. 11 (2016) 372–377. https://doi.org/10.1038/nnano.2015.330.
[113] Z. Liu, C. Davis, W. Cai, L. He, X. Chen, H. Dai, Circulation and long-term fate of functionalized, biocompatible single-walled carbon nanotubes in mice probed by Raman spectroscopy, Proc. Natl. Acad. Sci. 105 (2008) 1410–1415. https://doi.org/10.1073/pnas.0707654105.
[114] S. Bremer‐Hoffmann, B. Halamoda‐Kenzaoui, S.E. Borgos, Identification of regulatory needs for nanomedicines, J. Interdiscip. Nanomedicine 3 (2018) 4–15. https://doi.org/10.1002/jin2.34.
[115] D. Van Der Zwaag, N. Vanparijs, S. Wijnands, R. De Rycke, B.G. De Geest, L. Albertazzi, Super Resolution Imaging of Nanoparticles Cellular Uptake and Trafficking, ACS Appl. Mater. Interfaces 8 (2016) 6391–6399. https://doi.org/10.1021/acsami.6b00811.
[116] X. Yao, X. Fan, N. Yan, Cryo-EM analysis of a membrane protein embedded in the liposome, Proc. Natl. Acad. Sci. 117 (2020) 18497–18503. https://doi.org/10.1073/pnas.2009385117.
[117] M. Piffoux, A. Nicolás-Boluda, V. Mulens-Arias, S. Richard, G. Rahmi, F. Gazeau, C. Wilhelm, A.K.A. Silva, Extracellular vesicles for personalized medicine: The input of physically triggered production, loading and theranostic properties, Adv. Drug Deliv. Rev. 138 (2019) 247–258. https://doi.org/10.1016/j.addr.2018.12.009.
[118] W.J.M. Mulder, G.J. Strijkers, G.A.F. Van Tilborg, D.P. Cormode, Z.A. Fayad, K. Nicolay, Nanoparticulate Assemblies of Amphiphiles and Diagnostically Active Materials for Multimodality Imaging, Acc. Chem. Res. 42 (2009) 904–914. https://doi.org/10.1021/ar800223c.
[119] J. Kim, Y. Piao, T. Hyeon, Multifunctional nanostructured materials for multimodal imaging, and simultaneous imaging and therapy, Chem Soc Rev 38 (2009) 372–390. https://doi.org/10.1039/B709883A.
