Magnetic-Assisted Treatment of Liver Fibrosis
Abstract
:1. Introduction
1.1. Liver Fibrosis
1.2. Roles of Different Hepatic Cell Types in Liver Fibrosis
1.3. Current Clinical Trials on Liver Fibrosis
2. Theoretical Background of Magnetism
2.1. Magnetic Nanomedicines
2.1.1. Methods for Synthesis of Magnetic Nanomedicines
2.1.2. Clinical Use and Further Perspectives Iron Oxide
2.1.3. Magnetic Hybrid Nanomaterials
2.2. Magnetic Materials in Drug Delivery
2.2.1. Magnetic-Assisted Medical Applications
2.2.2. Selective Targeting of Hepatic Stellate Cells—Mission Impossible?
Author Contributions
Funding
Conflicts of Interest
References
- Hodgson, H.J. Basic and clinical aspects of liver growth: Prometheus revisited. Humphry Davy Rolleston Lecture 1992. J. Roy. Coll. Phys. Lond. 1993, 27, 278–283. [Google Scholar]
- Zajicek, G.; Oren, R.; Weinreb, M., Jr. The streaming liver. Liver 1985, 5, 293–300. [Google Scholar] [CrossRef] [PubMed]
- Van Dijk, F.; Teekamp, N.; Beljaars, L.; Post, E.; Schuppan, D.; Kim, Y.; Poelstra, K.; Frijlink, E.; Hinrichs, W.; Olinga, P. Towards clinical use of targeted therapies for liver fibrosis: Development of a sustained release formulation for therapeutic proteins. J. Hepatol. 2017, 66, S44. [Google Scholar] [CrossRef]
- Lee, Y.A.; Wallace, M.C.; Friedman, S.L. Pathobiology of liver fibrosis: A translational success story. Gut 2015, 64, 830–841. [Google Scholar] [CrossRef] [PubMed]
- Weiskirchen, R.; Tacke, F. Liver Fibrosis: From Pathogenesis to Novel Therapies. Digest. Dis. 2016, 34, 410–422. [Google Scholar] [CrossRef]
- Pinzani, M. Pathophysiology of liver fibrosis. Digest. Dis. 2015, 33, 492–497. [Google Scholar] [CrossRef]
- Schuppan, D. Liver fibrosis: Common mechanisms and antifibrotic therapies. Clin. Res. Hepatol. Gastroenterol. 2015, 39, S51–S59. [Google Scholar] [CrossRef]
- Ng, M.; Fleming, T.; Robinson, M.; Thomson, B.; Graetz, N.; Margono, C.; Mullany, E.C.; Biryukov, S.; Abbafati, C.; Abera, S.F.; et al. Global, regional, and national prevalence of overweight and obesity in children and adults during 1980-2013: A systematic analysis for the Global Burden of Disease Study 2013. Lancet 2014, 384, 766–781. [Google Scholar] [CrossRef]
- Dulai, P.S.; Singh, S.; Patel, J.; Soni, M.; Prokop, L.J.; Younossi, Z.; Sebastiani, G.; Ekstedt, M.; Hagstrom, H.; Nasr, P.; et al. Increased risk of mortality by fibrosis stage in nonalcoholic fatty liver disease: Systematic review and meta-analysis. Hepatology 2017, 65, 1557–1565. [Google Scholar] [CrossRef]
- Siddiqui, M.S.; Harrison, S.A.; Abdelmalek, M.F.; Anstee, Q.M.; Bedossa, P.; Castera, L.; Dimick-Santos, L.; Friedman, S.L.; Greene, K.; Kleiner, D.E.; et al. Case definitions for inclusion and analysis of endpoints in clinical trials for nonalcoholic steatohepatitis through the lens of regulatory science. Hepatology 2018, 67, 2001–2012. [Google Scholar] [CrossRef] [Green Version]
- Tapper, E.B.; Lok, A.S. Use of Liver Imaging and Biopsy in Clinical Practice. N. Engl. J. Med. 2017, 377, 756–768. [Google Scholar] [CrossRef] [PubMed]
- Seki, E.; De Minicis, S.; Osterreicher, C.H.; Kluwe, J.; Osawa, Y.; Brenner, D.A.; Schwabe, R.F. TLR4 enhances TGF-beta signaling and hepatic fibrosis. Nat. Med. 2007, 13, 1324–1332. [Google Scholar] [CrossRef] [PubMed]
- Xiao, Y.; Liu, R.; Li, X.; Gurley, E.C.; Hylemon, P.B.; Lu, Y.; Zhou, H.; Cai, W. Long Noncoding RNA H19 Contributes to Cholangiocyte Proliferation and Cholestatic Liver Fibrosis in Biliary Atresia. Hepatology 2019. [Google Scholar] [CrossRef] [PubMed]
- Sato, K.; Meng, F.; Giang, T.; Glaser, S.; Alpini, G. Mechanisms of cholangiocyte responses to injury. Biochim. Biophys. Acta Mol. Basis Dis. 2018, 1864, 1262–1269. [Google Scholar] [CrossRef]
- Hargrove, L.; Kennedy, L.; Demieville, J.; Jones, H.; Meng, F.; DeMorrow, S.; Karstens, W.; Madeka, T.; Greene, J., Jr.; Francis, H. Bile duct ligation-induced biliary hyperplasia, hepatic injury, and fibrosis are reduced in mast cell-deficient Kit(W-sh) mice. Hepatology 2017, 65, 1991–2004. [Google Scholar] [CrossRef]
- Bradding, P.; Pejler, G. The controversial role of mast cells in fibrosis. Immunol. Rev. 2018, 282, 198–231. [Google Scholar] [CrossRef] [Green Version]
- Bartneck, M.; Ritz, T.; Keul, H.A.; Wambach, M.; Bornemann, J.; Gbureck, U.; Ehling, J.; Lammers, T.; Heymann, F.; Gassler, N.; et al. Peptide-functionalized gold nanorods increase liver injury in hepatitis. ACS Nano 2012, 6, 8767–8777. [Google Scholar] [CrossRef]
- Kupffer, K.W.v. Über Sternzellen der Leber. Arch Mikroskop Anat., 1876; Volume 12, pp. 353–358. Available online: http://www.springerlink.com/index/F7X6532P76172836.pdf (accessed on 17 October 2019).
- Metchnikof, E. Ueber die phagocytäre Rolle der Tuberkelriesenzellen. Archiv für pathologische Anatomie und Physiologie und für klinische Medecin, 1888; Volume 113, pp. 63–94. Available online: http://www.springerlink.com/index/70U3823357485325.pdf (accessed on 17 October 2019).
- Krenkel, O.; Puengel, T.; Govaere, O.; Abdallah, A.T.; Mossanen, J.C.; Kohlhepp, M.; Liepelt, A.; Lefebvre, E.; Luedde, T.; Hellerbrand, C.; et al. Therapeutic inhibition of inflammatory monocyte recruitment reduces steatohepatitis and liver fibrosis. Hepatology 2018, 67, 1270–1283. [Google Scholar] [CrossRef]
- Krenkel, O.; Hundertmark, J.; Ritz, T.P.; Weiskirchen, R.; Tacke, F. Single Cell RNA Sequencing Identifies Subsets of Hepatic Stellate Cells and Myofibroblasts in Liver Fibrosis. Cells 2019, 8, 503. [Google Scholar] [CrossRef]
- Trautwein, C.; Friedman, S.L.; Schuppan, D.; Pinzani, M. Hepatic fibrosis: Concept to treatment. J. Hepatol. 2015, 62, S15–S24. [Google Scholar] [CrossRef] [Green Version]
- Tsuchida, T.; Friedman, S.L. Mechanisms of hepatic stellate cell activation. Nat. Rev. Gastroenterol. Hepatol. 2017, 14, 397–411. [Google Scholar] [CrossRef] [PubMed]
- Campana, L.; Iredale, J.P. Regression of Liver Fibrosis. Semin. Liver Dis. 2017, 37, 1–10. [Google Scholar] [PubMed]
- Hutchinson, J.H.; Rowbottom, M.W.; Lonergan, D.; Darlington, J.; Prodanovich, P.; King, C.D.; Evans, J.F.; Bain, G. Small Molecule Lysyl Oxidase-like 2 (LOXL2) Inhibitors: The Identification of an Inhibitor Selective for LOXL2 over LOX. ACS Med. Chem. Lett. 2017, 8, 423–427. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bartneck, M.; Fech, V.; Ehling, J.; Govaere, O.; Warzecha, K.T.; Hittatiya, K.; Vucur, M.; Gautheron, J.; Luedde, T.; Trautwein, C.; et al. Histidine-rich glycoprotein promotes macrophage activation and inflammation in chronic liver disease. Hepatology 2016, 63, 1310–1324. [Google Scholar] [CrossRef] [PubMed]
- Jun, J.I.; Lau, L.F. Resolution of organ fibrosis. J. Clin. Invest. 2018, 128, 97–107. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Vilar-Gomez, E.; Martinez-Perez, Y.; Calzadilla-Bertot, L.; Torres-Gonzalez, A.; Gra-Oramas, B.; Gonzalez-Fabian, L.; Friedman, S.L.; Diago, M.; Romero-Gomez, M. Weight Loss Through Lifestyle Modification Significantly Reduces Features of Nonalcoholic Steatohepatitis. Gastroenterology 2015, 149, 367–378. [Google Scholar] [CrossRef] [PubMed]
- Marcellin, P.; Gane, E.; Buti, M.; Afdhal, N.; Sievert, W.; Jacobson, I.M.; Washington, M.K.; Germanidis, G.; Flaherty, J.F.; Aguilar Schall, R.; et al. Regression of cirrhosis during treatment with tenofovir disoproxil fumarate for chronic hepatitis B: A 5-year open-label follow-up study. Lancet 2013, 381, 468–475. [Google Scholar] [CrossRef]
- Ellis, E.L.; Mann, D.A. Clinical evidence for the regression of liver fibrosis. J. Hepatol. 2012, 56, 1171–1180. [Google Scholar] [CrossRef] [Green Version]
- Luedde, T.; Kaplowitz, N.; Schwabe, R.F. Cell death and cell death responses in liver disease: Mechanisms and clinical relevance. Gastroenterology 2014, 147, 765–783. [Google Scholar] [CrossRef]
- Wree, A.; Mehal, W.Z.; Feldstein, A.E. Targeting Cell Death and Sterile Inflammation Loop for the Treatment of Nonalcoholic Steatohepatitis. Semin. Liver Dis. 2016, 36, 27–36. [Google Scholar] [CrossRef] [Green Version]
- Vanden Berghe, T.; Linkermann, A.; Jouan-Lanhouet, S.; Walczak, H.; Vandenabeele, P. Regulated necrosis: The expanding network of non-apoptotic cell death pathways. Nat. Rev. Mol. Cell Biol. 2014, 15, 135–147. [Google Scholar] [CrossRef] [PubMed]
- Loomba, R.; Lawitz, E.; Mantry, P.S.; Jayakumar, S.; Caldwell, S.H.; Arnold, H.; Diehl, A.M.; Djedjos, C.S.; Han, L.; Myers, R.P.; et al. The ASK1 inhibitor selonsertib in patients with nonalcoholic steatohepatitis: A randomized, phase 2 trial. Hepatology 2018, 67, 549–559. [Google Scholar] [CrossRef] [PubMed]
- Fickert, P.; Fuchsbichler, A.; Moustafa, T.; Wagner, M.; Zollner, G.; Halilbasic, E.; Stoger, U.; Arrese, M.; Pizarro, M.; Solis, N.; et al. Farnesoid X receptor critically determines the fibrotic response in mice but is expressed to a low extent in human hepatic stellate cells and periductal myofibroblasts. Am. J. Pathol. 2009, 175, 2392–2405. [Google Scholar] [CrossRef] [PubMed]
- Roth, J.D.; Veidal, S.S.; Fensholdt, L.K.D.; Rigbolt, K.T.G.; Papazyan, R.; Nielsen, J.C.; Feigh, M.; Vrang, N.; Young, M.; Jelsing, J.; et al. Combined obeticholic acid and elafibranor treatment promotes additive liver histological improvements in a diet-induced ob/ob mouse model of biopsy-confirmed NASH. Sci. Rep. 2019, 9, 9046. [Google Scholar] [CrossRef]
- Lefebvre, E.; Moyle, G.; Reshef, R.; Richman, L.P.; Thompson, M.; Hong, F.; Chou, H.L.; Hashiguchi, T.; Plato, C.; Poulin, D.; et al. Antifibrotic Effects of the Dual CCR2/CCR5 Antagonist Cenicriviroc in Animal Models of Liver and Kidney Fibrosis. PLoS ONE 2016, 11, e0158156. [Google Scholar] [CrossRef]
- Friedman, S.; Sanyal, A.; Goodman, Z.; Lefebvre, E.; Gottwald, M.; Fischer, L.; Ratziu, V. Efficacy and safety study of cenicriviroc for the treatment of non-alcoholic steatohepatitis in adult subjects with liver fibrosis: CENTAUR Phase 2b study design. Contemp. Clin. Trials 2016, 47, 356–365. [Google Scholar] [CrossRef] [Green Version]
- Fisher, F.M.; Chui, P.C.; Nasser, I.A.; Popov, Y.; Cunniff, J.C.; Lundasen, T.; Kharitonenkov, A.; Schuppan, D.; Flier, J.S.; Maratos-Flier, E. Fibroblast growth factor 21 limits lipotoxicity by promoting hepatic fatty acid activation in mice on methionine and choline-deficient diets. Gastroenterology 2014, 147, 1073–1083. [Google Scholar] [CrossRef]
- Armstrong, M.J.; Gaunt, P.; Aithal, G.P.; Barton, D.; Hull, D.; Parker, R.; Hazlehurst, J.M.; Guo, K.; Abouda, G.; Aldersley, M.A.; et al. Liraglutide safety and efficacy in patients with non-alcoholic steatohepatitis (LEAN): A multicentre, double-blind, randomised, placebo-controlled phase 2 study. Lancet 2016, 387, 679–690. [Google Scholar] [CrossRef]
- Stiede, K.; Miao, W.; Blanchette, H.S.; Beysen, C.; Harriman, G.; Harwood, H.J., Jr.; Kelley, H.; Kapeller, R.; Schmalbach, T.; Westlin, W.F. Acetyl-coenzyme A carboxylase inhibition reduces de novo lipogenesis in overweight male subjects: A randomized, double-blind, crossover study. Hepatology 2017, 66, 324–334. [Google Scholar] [CrossRef]
- Harrison, S.A.; Rinella, M.E.; Abdelmalek, M.F.; Trotter, J.F.; Paredes, A.H.; Arnold, H.L.; Kugelmas, M.; Bashir, M.R.; Jaros, M.J.; Ling, L.; et al. NGM282 for treatment of non-alcoholic steatohepatitis: A multicentre, randomised, double-blind, placebo-controlled, phase 2 trial. Lancet 2018, 391, 1174–1185. [Google Scholar] [CrossRef]
- Gubin, S.P.; Koksharov, Y.A.; Khomutov, G.; Yurkov, G.Y. Magnetic nanoparticles: Preparation, structure and properties. Russ. Chem. Rev. 2005, 74, 489. [Google Scholar] [CrossRef]
- Krishnan, K.M. Fundamentals and Applications of Magnetic Materials; Oxford University Press: Oxford, UK, 2016. [Google Scholar]
- Cullity, B.D.; Graham, C.D. Introduction to Magnetic Materials; John Wiley & Sons: Hoboken, NJ, USA, 2011. [Google Scholar]
- Peddis, D.; Jönsson, P.E.; Laureti, S.; Varvaro, G. Magnetic interactions: A tool to modify the magnetic properties of materials based on nanoparticles. In Frontiers of Nanoscience; Elsevier: Amsterdam, The Netherlands, 2014; pp. 129–188. [Google Scholar]
- Liu, J.P.; Fullerton, E.; Gutfleisch, O.; Sellmyer, D.J. Nanoscale Magnetic Materials and Applications; Springer: Berlin, Germany, 2009. [Google Scholar]
- Pankhurst, Q.; Thanh, N.; Jones, S.; Dobson, J. Progress in applications of magnetic nanoparticles in biomedicine. J. Phys. D Appl. Phys. 2009, 42, 224001. [Google Scholar] [CrossRef]
- Pankhurst, Q.A.; Connolly, J.; Jones, S.; Dobson, J. Applications of magnetic nanoparticles in biomedicine. J. Phys. D Appl. Phys. 2003, 36, R167. [Google Scholar] [CrossRef]
- De Crozals, G.; Bonnet, R.; Farre, C.; Chaix, C. Nanoparticles with multiple properties for biomedical applications: A strategic guide. Nano Today 2016, 11, 435–463. [Google Scholar] [CrossRef]
- Stoner, E.C.; Wohlfarth, E. A mechanism of magnetic hysteresis in heterogeneous alloys. Philos. Trans. R. Soc. Lond. Ser. A Math. Phys. Sci. 1948, 240, 599–642. [Google Scholar] [CrossRef] [Green Version]
- Dormann, J.L.; Fiorani, D.; Tronc, E. Magnetic relaxation in fine-particle systems. Adv. Chem. Phys. 1997, 283. [Google Scholar] [CrossRef]
- Angelakeris, M. Magnetic nanoparticles: A multifunctional vehicle for modern theranostics. Biochim. Biophys. Acta 2017, 1861, 1642–1651. [Google Scholar] [CrossRef]
- Knobel, M.; Nunes, W.; Socolovsky, L.; De Biasi, E.; Vargas, J.; Denardin, J. Superparamagnetism and other magnetic features in granular materials: A review on ideal and real systems. J. Nanosci. Nanotechnol. 2008, 8, 2836–2857. [Google Scholar] [CrossRef]
- Di Corato, R.; Espinosa, A.; Lartigue, L.; Tharaud, M.; Chat, S.; Pellegrino, T.; Ménager, C.; Gazeau, F.; Wilhelm, C. Magnetic hyperthermia efficiency in the cellular environment for different nanoparticle designs. Biomaterials 2014, 35, 6400–6411. [Google Scholar] [CrossRef]
- Bartneck, M. Immunomodulatory Nanomedicine. Macromol. Biosci. 2017. Published online on 6 April. [Google Scholar] [CrossRef]
- Salas, G.; Veintemillas-Verdaguer, S.; Morales, M.d.P. Relationship between physico-chemical properties of magnetic fluids and their heating capacity. Int. J. Hyperthermia 2013, 29, 768–776. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Weissleder, R.; Bogdanov, A.; Neuwelt, E.A.; Papisov, M. Long-circulating iron oxides for MR imaging. Adv. Drug Deliv. Rev. 1995, 16, 321–334. [Google Scholar] [CrossRef]
- Peer, D.; Karp, J.M.; Hong, S.; Farokhzad, O.C.; Margalit, R.; Langer, R. Nanocarriers as an emerging platform for cancer therapy. Nat. Nanotechnol. 2007, 2, 751. [Google Scholar] [CrossRef] [PubMed]
- Arami, H.; Khandhar, A.; Liggitt, D.; Krishnan, K.M. In vivo delivery, pharmacokinetics, biodistribution and toxicity of iron oxide nanoparticles. Chem. Soc. Rev. 2015, 44, 8576–8607. [Google Scholar] [CrossRef] [PubMed]
- Thomas, C.R.; Ferris, D.P.; Lee, J.-H.; Choi, E.; Cho, M.H.; Kim, E.S.; Stoddart, J.F.; Shin, J.-S.; Cheon, J.; Zink, J.I. Noninvasive remote-controlled release of drug molecules in vitro using magnetic actuation of mechanized nanoparticles. J. Am. Chem. Soc. 2010, 132, 10623–10625. [Google Scholar] [CrossRef] [PubMed]
- Cheon, J.; Lee, J.-H. Synergistically integrated nanoparticles as multimodal probes for nanobiotechnology. Acc. Chem. Res. 2008, 41, 1630–1640. [Google Scholar] [CrossRef] [PubMed]
- McCarthy, J.R.; Weissleder, R. Multifunctional magnetic nanoparticles for targeted imaging and therapy. Adv. Drug Deliv. Rev. 2008, 60, 1241–1251. [Google Scholar] [CrossRef] [Green Version]
- Batlle, X.; Pérez, N.; Guardia, P.; Iglesias, O.; Labarta, A.; Bartolomé, F.; García, L.; Bartolomé, J.; Roca, A.; Morales, M. Magnetic nanoparticles with bulklike properties. J. Appl. Phys. 2011, 109, 07B524. [Google Scholar] [CrossRef]
- Lacroix, L.-M.; Lachaize, S.; Falqui, A.; Blon, T.; Carrey, J.; Respaud, M.; Dumestre, F.; Amiens, C.; Margeat, O.; Chaudret, B. Ultrasmall iron nanoparticles: Effect of size reduction on anisotropy and magnetization. J. Appl. Phys. 2008, 103, 07D521. [Google Scholar] [CrossRef]
- Iv, M.; Telischak, N.; Feng, D.; Holdsworth, S.J.; Yeom, K.W.; Daldrup-Link, H.E. Clinical applications of iron oxide nanoparticles for magnetic resonance imaging of brain tumors. Nanomedicine 2015, 10, 993–1018. [Google Scholar] [CrossRef]
- Weissleder, R.; Elizondo, G.; Wittenberg, J.; Rabito, C.; Bengele, H.; Josephson, L. Ultrasmall superparamagnetic iron oxide: Characterization of a new class of contrast agents for MR imaging. Radiology 1990, 175, 489–493. [Google Scholar] [CrossRef] [PubMed]
- Laurent, S.; Vander Elst, L.; Muller, R.N. Superparamagnetic iron oxide nanoparticles for MRI. In The Chemistry of Contrast Agents in Medical Magmetic Resonance Imaging; John Wiley & Sons, Ltd.: Hoboken, NJ, USA, 2013; pp. 427–447. [Google Scholar]
- Morales, I.; Costo, R.; Mille, N.; Silva, G.B.d.; Carrey, J.; Hernando, A.; Presa, P.d.l. High Frequency Hysteresis Losses on γ-Fe2O3 and Fe3O4: Susceptibility as a Magnetic Stamp for Chain Formation. Nanomaterials 2018, 8, 970. [Google Scholar] [CrossRef]
- Carrey, J.; Mehdaoui, B.; Respaud, M. Simple models for dynamic hysteresis loop calculations of magnetic single-domain nanoparticles: Application to magnetic hyperthermia optimization. J. Appl. Phys. 2011, 109, 083921. [Google Scholar] [CrossRef]
- da Silva, F.; Depeyrot, J.; Campos, A.; Aquino, R.; Fiorani, D.; Peddis, D. Structural and Magnetic Properties of Spinel Ferrite Nanoparticles. J. Nanosci. Nanotechnol. 2019, 19, 4888–4902. [Google Scholar] [CrossRef] [PubMed]
- Wagener, P.; Jakobi, J.; Rehbock, C.; Chakravadhanula, V.S.K.; Thede, C.; Wiedwald, U.; Bartsch, M.; Kienle, L.; Barcikowski, S. Solvent-surface interactions control the phase structure in laser-generated iron-gold core-shell nanoparticles. Sci. Rep. 2016, 6, 23352. [Google Scholar] [CrossRef] [PubMed]
- Maneeratanasarn, P.; Khai, T.V.; Kim, S.Y.; Choi, B.G.; Shim, K.B. Synthesis of phase-controlled iron oxide nanoparticles by pulsed laser ablation in different liquid media. Phys. Status Solidi A 2013, 210, 563–569. [Google Scholar] [CrossRef]
- Fazio, E.; Santoro, M.; Lentini, G.; Franco, D.; Guglielmino, S.P.P.; Neri, F. Iron oxide nanoparticles prepared by laser ablation: Synthesis, structural properties and antimicrobial activity. Colloids Surf. A 2016, 490, 98–103. [Google Scholar] [CrossRef]
- Xiao, J.; Liu, P.; Wang, C.; Yang, G. External field-assisted laser ablation in liquid: An efficient strategy for nanocrystal synthesis and nanostructure assembly. Prog. Mater. Sci. 2017, 87, 140–220. [Google Scholar] [CrossRef]
- Amendola, V.; Meneghetti, M.; Granozzi, G.; Agnoli, S.; Polizzi, S.; Riello, P.; Boscaini, A.; Anselmi, C.; Fracasso, G.; Colombatti, M. Top-down synthesis of multifunctional iron oxide nanoparticles for macrophage labelling and manipulation. J. Mater. Chem. 2011, 21, 3803–3813. [Google Scholar] [CrossRef]
- Vitol, E.A.; Novosad, V.; Rozhkova, E.A. Microfabricated magnetic structures for future medicine: From sensors to cell actuators. Nanomedicine 2012, 7, 1611–1624. [Google Scholar] [CrossRef]
- Kim, D.-H.; Rozhkova, E.A.; Ulasov, I.V.; Bader, S.D.; Rajh, T.; Lesniak, M.S.; Novosad, V. Biofunctionalized magnetic-vortex microdiscs for targeted cancer-cell destruction. Nat. Mater. 2010, 9, 165. [Google Scholar] [CrossRef] [PubMed]
- Litvinov, J.; Nasrullah, A.; Sherlock, T.; Wang, Y.-J.; Ruchhoeft, P.; Willson, R.C. High-throughput top-down fabrication of uniform magnetic particles. PLoS ONE 2012, 7, e37440. [Google Scholar] [CrossRef] [PubMed]
- Kosiorek, A.; Kandulski, W.; Glaczynska, H.; Giersig, M. Fabrication of nanoscale rings, dots, and rods by combining shadow nanosphere lithography and annealed polystyrene nanosphere masks. Small 2005, 1, 439–444. [Google Scholar] [CrossRef] [PubMed]
- del Campo, A.; Arzt, E. Fabrication approaches for generating complex micro-and nanopatterns on polymeric surfaces. Chem. Rev. 2008, 108, 911–945. [Google Scholar] [CrossRef] [PubMed]
- Svetlichnyi, V.; Shabalina, A.; Lapin, I.; Goncharova, D.; Velikanov, D.; Sokolov, A. Characterization and magnetic properties study for magnetite nanoparticles obtained by pulsed laser ablation in water. Appl. Phys. A 2017, 123, 763. [Google Scholar] [CrossRef]
- Yue, M.; Zhang, X.; Liu, J.P. Fabrication of bulk nanostructured permanent magnets with high energy density: Challenges and approaches. Nanoscale 2017, 9, 3674–3697. [Google Scholar] [CrossRef] [PubMed]
- Bellusci, M.; Guglielmi, P.; Masi, A.; Padella, F.; Singh, G.; Yaacoub, N.; Peddis, D.; Secci, D. Magnetic Metal–Organic Framework Composite by Fast and Facile Mechanochemical Process. Inorg. Chem. 2018, 57, 1806–1814. [Google Scholar] [CrossRef]
- Thanh, N.T.; Maclean, N.; Mahiddine, S. Mechanisms of nucleation and growth of nanoparticles in solution. Chem. Rev. 2014, 114, 7610–7630. [Google Scholar] [CrossRef]
- Vayssieres, L.; Chanéac, C.; Tronc, E.; Jolivet, J.P. Size tailoring of magnetite particles formed by aqueous precipitation: An example of thermodynamic stability of nanometric oxide particles. J. Colloid Interface Sci. 1998, 205, 205–212. [Google Scholar] [CrossRef]
- Roca, A.G.; Gutierrez, L.; Gavilán, H.; Brollo, M.E.F.; Veintemillas-Verdaguer, S.; del Puerto Morales, M. Design strategies for shape-controlled magnetic iron oxide nanoparticles. Adv. Drug Deliv. Rev. 2018, 138, 68–104. [Google Scholar] [CrossRef]
- Salvador, M.; Moyano, A.; Martínez-García, J.C.; Blanco-López, M.C.; Rivas, M. Synthesis of Superparamagnetic Iron Oxide Nanoparticles: SWOT Analysis Towards Their Conjugation to Biomolecules for Molecular Recognition Applications. J. Nanosci. Nanotechnol. 2019, 19, 4839–4856. [Google Scholar] [CrossRef] [PubMed]
- Massart, R. Preparation of aqueous magnetic liquids in alkaline and acidic media. IEEE Trans. Magn. 1981, 17, 1247–1248. [Google Scholar] [CrossRef]
- Daffé, N.; Choueikani, F.; Neveu, S.; Arrio, M.-A.; Juhin, A.; Ohresser, P.; Dupuis, V.; Sainctavit, P. Magnetic anisotropies and cationic distribution in CoFe2O4 nanoparticles prepared by co-precipitation route: Influence of particle size and stoichiometry. J. Magn. Magn. Mater. 2018, 460, 243–252. [Google Scholar] [CrossRef]
- Yelenich, O.; Solopan, S.; Kolodiazhnyi, T.; Tykhonenko, Y.; Tovstolytkin, A.; Belous, A. Magnetic properties and AC losses in AFe2O4 (A= Mn, Co, Ni, Zn) nanoparticles synthesized from nonaqueous solution. J. Chem. 2015, 2015, 532198. [Google Scholar] [CrossRef]
- Nedelkoski, Z.; Kepaptsoglou, D.; Lari, L.; Wen, T.; Booth, R.A.; Oberdick, S.D.; Galindo, P.L.; Ramasse, Q.M.; Evans, R.F.; Majetich, S. Origin of reduced magnetization and domain formation in small magnetite nanoparticles. Sci. Rep. 2017, 7, 45997. [Google Scholar] [CrossRef]
- Jovanović, S.; Spreitzer, M.; Otoničar, M.; Jeon, J.-H.; Suvorov, D. pH control of magnetic properties in precipitation-hydrothermal-derived CoFe2O4. J. Alloys Compd. 2014, 589, 271–277. [Google Scholar] [CrossRef]
- Gomes, J.d.A.; Sousa, M.H.; Tourinho, F.A.; Aquino, R.; da Silva, G.J.; Depeyrot, J.; Dubois, E.; Perzynski, R. Synthesis of core− shell ferrite nanoparticles for ferrofluids: Chemical and magnetic analysis. J. Phys. Chem. C 2008, 112, 6220–6227. [Google Scholar] [CrossRef]
- Pilati, V.; Cabreira Gomes, R.; Gomide, G.; Coppola, P.; Silva, F.G.; Paula, F.b.L.; Perzynski, R.G.; Goya, G.F.; Aquino, R.; Depeyrot, J. Core/shell nanoparticles of non-stoichiometric Zn–Mn and Zn–Co ferrites as thermosensitive heat sources for magnetic fluid hyperthermia. J. Phys. Chem. C 2018, 122, 3028–3038. [Google Scholar] [CrossRef]
- Sanna Angotzi, M.; Musinu, A.; Mameli, V.; Ardu, A.; Cara, C.; Niznansky, D.; Xin, H.L.; Cannas, C. Spinel ferrite core–shell nanostructures by a versatile solvothermal seed-mediated growth approach and study of their nanointerfaces. ACS Nano 2017, 11, 7889–7900. [Google Scholar] [CrossRef]
- Liu, X.; Liu, J.; Zhang, S.; Nan, Z.; Shi, Q. Structural, magnetic, and thermodynamic evolutions of Zn-doped Fe3O4 nanoparticles synthesized using a one-step solvothermal method. J. Phys. Chem. C 2016, 120, 1328–1341. [Google Scholar] [CrossRef]
- Grabs, I.-M.; Bradtmöller, C.; Menzel, D.; Garnweitner, G. Formation mechanisms of iron oxide nanoparticles in different nonaqueous media. Cryst. Growth Des. 2012, 12, 1469–1475. [Google Scholar] [CrossRef]
- Muscas, G.; Yaacoub, N.; Concas, G.; Sayed, F.; Hassan, R.S.; Greneche, J.; Cannas, C.; Musinu, A.; Foglietti, V.; Casciardi, S. Evolution of the magnetic structure with chemical composition in spinel iron oxide nanoparticles. Nanoscale 2015, 7, 13576–13585. [Google Scholar] [CrossRef] [PubMed]
- Hemery, G.; Keyes, A.C., Jr.; Garaio, E.; Rodrigo, I.; Garcia, J.A.; Plazaola, F.; Garanger, E.; Sandre, O. Tuning sizes, morphologies, and magnetic properties of monocore versus multicore iron oxide nanoparticles through the controlled addition of water in the polyol synthesis. Inorg. Chem. 2017, 56, 8232–8243. [Google Scholar] [CrossRef] [PubMed]
- Franceschin, G.; Gaudisson, T.; Menguy, N.; Dodrill, B.C.; Yaacoub, N.; Grenèche, J.M.; Valenzuela, R.; Ammar, S. Exchange-Biased Fe3− xO4-CoO Granular Composites of Different Morphologies Prepared by Seed-Mediated Growth in Polyol: From Core–Shell to Multicore Embedded Structures. Part. Part. Syst. Charact. 2018, 35, 1800104. [Google Scholar] [CrossRef]
- William, W.Y.; Falkner, J.C.; Yavuz, C.T.; Colvin, V.L. Synthesis of monodisperse iron oxide nanocrystals by thermal decomposition of iron carboxylate salts. Chem. Commun. 2004, 2306–2307. [Google Scholar]
- Sun, S.; Zeng, H.; Robinson, D.B.; Raoux, S.; Rice, P.M.; Wang, S.X.; Li, G. Monodisperse mfe2o4 (m= fe, co, mn) nanoparticles. J. Am. Chem. Soc. 2004, 126, 273–279. [Google Scholar] [CrossRef]
- Park, J.; An, K.; Hwang, Y.; Park, J.-G.; Noh, H.-J.; Kim, J.-Y.; Park, J.-H.; Hwang, N.-M.; Hyeon, T. Ultra-large-scale syntheses of monodisperse nanocrystals. Nat. Mater. 2004, 3, 891. [Google Scholar] [CrossRef]
- Kolhatkar, A.; Jamison, A.; Litvinov, D.; Willson, R.; Lee, T. Tuning the magnetic properties of nanoparticles. Int. J. Mol. Sci. 2013, 14, 15977–16009. [Google Scholar] [CrossRef]
- Yoo, D.; Lee, J.-H.; Shin, T.-H.; Cheon, J. Theranostic magnetic nanoparticles. Acc. Chem. Res. 2011, 44, 863–874. [Google Scholar] [CrossRef]
- Cotin, G.; Blanco-Andujar, C.; Nguyen, D.V.; Affolter-Zbaraszczuk, C.; Boutry, S.; Anne, B.; Ronot, P.; Uring, B.; Choquet, P.; Zorn, P.E. Dendron based antifouling, MRI and magnetic hyperthermia properties of different shaped iron oxide nanoparticles. Nanotechnology 2019, 30, 37. [Google Scholar] [CrossRef]
- Noh, S.-H.; Na, W.; Jang, J.-T.; Lee, J.-H.; Lee, E.J.; Moon, S.H.; Lim, Y.; Shin, J.-S.; Cheon, J. Nanoscale magnetism control via surface and exchange anisotropy for optimized ferrimagnetic hysteresis. Nano Lett. 2012, 12, 3716–3721. [Google Scholar] [CrossRef] [PubMed]
- Toth, G.B.; Varallyay, C.G.; Horvath, A.; Bashir, M.R.; Choyke, P.L.; Daldrup-Link, H.E.; Dosa, E.; Finn, J.P.; Gahramanov, S.; Harisinghani, M.; et al. Current and potential imaging applications of ferumoxytol for magnetic resonance imaging. Kidney Int. 2017, 92, 47–66. [Google Scholar] [CrossRef] [PubMed]
- Hood, M.N.; Blankholm, A.D.; Stolpen, A. The Rise of Off-Label Iron-Based Agents in Magnetic Resonance Imaging. J. Radiol. Nurs. 2019, 38, 38–41. [Google Scholar] [CrossRef]
- Gaglia, J.L.; Harisinghani, M.; Aganj, I.; Wojtkiewicz, G.R.; Hedgire, S.; Benoist, C.; Mathis, D.; Weissleder, R. Noninvasive mapping of pancreatic inflammation in recent-onset type-1 diabetes patients. Proc. Natl. Acad. Sci. USA 2015, 112, 2139–2144. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Trujillo-Alonso, V.; Pratt, E.C.; Zong, H.; Lara-Martinez, A.; Kaittanis, C.; Rabie, M.O.; Longo, V.; Becker, M.W.; Roboz, G.J.; Grimm, J. FDA-approved ferumoxytol displays anti-leukaemia efficacy against cells with low ferroportin levels. Nat. Nanotechnol. 2019, 14, 616. [Google Scholar] [CrossRef] [PubMed]
- Huang, J.; Shu, Q.; Wang, L.; Wu, H.; Wang, A.Y.; Mao, H. Layer-by-layer assembled milk protein coated magnetic nanoparticle enabled oral drug delivery with high stability in stomach and enzyme-responsive release in small intestine. Biomaterials 2015, 39, 105–113. [Google Scholar] [CrossRef] [PubMed]
- Shah, K. Mesenchymal stem cells engineered for cancer therapy. Adv. Drug Deliv. Rev. 2012, 64, 739–748. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Qiao, L.; Xu, Z.; Zhao, T.; Zhao, Z.; Shi, M.; Zhao, R.C.; Ye, L.; Zhang, X. Suppression of tumorigenesis by human mesenchymal stem cells in a hepatoma model. Cell Res. 2008, 18, 500. [Google Scholar] [CrossRef]
- Long, X.; Matsumoto, R.; Yang, P.; Uemura, T. Effect of human mesenchymal stem cells on the growth of HepG2 and Hela cells. Cell Struct. Funct. 2013. [Google Scholar] [CrossRef]
- Yu, Y.; Lu, L.; Qian, X.; Chen, N.; Yao, A.; Pu, L.; Zhang, F.; Li, X.; Kong, L.; Sun, B. Antifibrotic effect of hepatocyte growth factor-expressing mesenchymal stem cells in small-for-size liver transplant rats. Stem Cells Dev. 2009, 19, 903–914. [Google Scholar] [CrossRef]
- Hu, C.; Zhao, L.; Duan, J.; Li, L. Strategies to improve the efficiency of mesenchymal stem cell transplantation for reversal of liver fibrosis. J. Cell. Mol. Med. 2019, 23, 1657–1670. [Google Scholar] [CrossRef] [PubMed]
- Faidah, M.; Noorwali, A.; Atta, H.; Ahmed, N.; Habib, H.; Damiati, L.; Filimban, N.; Al-qriqri, M.; Mahfouz, S.; Khabaz, M.N. Mesenchymal stem cell therapy of hepatocellular carcinoma in rats: Detection of cell homing and tumor mass by magnetic resonance imaging using iron oxide nanoparticles. Adv. Clin. Exp. Med. 2017, 26, 1171–1178. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lai, L.; Chen, J.; Wei, X.; Huang, M.; Hu, X.; Yang, R.; Jiang, X.; Shan, H. Transplantation of MSCs overexpressing HGF into a rat model of liver fibrosis. Mol. Imaging Biol. 2016, 18, 43–51. [Google Scholar] [CrossRef] [PubMed]
- Guimaraes, A.R.; Siqueira, L.; Uppal, R.; Alford, J.; Fuchs, B.C.; Yamada, S.; Tanabe, K.; Chung, R.T.; Lauwers, G.; Chew, M.L. T2 relaxation time is related to liver fibrosis severity. Quant. Imaging Med. Surg. 2016, 6, 103. [Google Scholar] [CrossRef] [PubMed]
- Wu, W.; Wu, Z.; Yu, T.; Jiang, C.; Kim, W.-S. Recent progress on magnetic iron oxide nanoparticles: Synthesis, surface functional strategies and biomedical applications. Sci. Technol. Adv. Mater. 2015, 16, 023501. [Google Scholar] [CrossRef]
- Li, Y.; Shang, W.; Liang, X.; Zeng, C.; Liu, M.; Wang, S.; Li, H.; Tian, J. The diagnosis of hepatic fibrosis by magnetic resonance and near-infrared imaging using dual-modality nanoparticles. RSC Adv. 2018, 8, 6699–6708. [Google Scholar] [CrossRef] [Green Version]
- Zhang, C.; Liu, H.; Cui, Y.; Li, X.; Zhang, Z.; Zhang, Y.; Wang, D. Molecular magnetic resonance imaging of activated hepatic stellate cells with ultrasmall superparamagnetic iron oxide targeting integrin αvβ3 for staging liver fibrosis in rat model. Int. J. Nanomed. 2016, 11, 1097. [Google Scholar]
- Wei, Y.; Zhao, M.; Yang, F.; Mao, Y.; Xie, H.; Zhou, Q. Iron overload by superparamagnetic iron oxide nanoparticles is a high risk factor in cirrhosis by a systems toxicology assessment. Sci. Rep. 2016, 6, 29110. [Google Scholar] [CrossRef]
- Lunov, O.; Syrovets, T.; Büchele, B.; Jiang, X.; Röcker, C.; Tron, K.; Nienhaus, G.U.; Walther, P.; Mailänder, V.; Landfester, K. The effect of carboxydextran-coated superparamagnetic iron oxide nanoparticles on c-Jun N-terminal kinase-mediated apoptosis in human macrophages. Biomaterials 2010, 31, 5063–5071. [Google Scholar] [CrossRef]
- Kolosnjaj-Tabi, J.; Lartigue, L.; Javed, Y.; Luciani, N.; Pellegrino, T.; Wilhelm, C.; Alloyeau, D.; Gazeau, F. Biotransformations of magnetic nanoparticles in the body. Nano Today 2016, 11, 280–284. [Google Scholar] [CrossRef]
- Yu, M.; Huang, S.; Yu, K.J.; Clyne, A.M. Dextran and polymer polyethylene glycol (PEG) coating reduce both 5 and 30 nm iron oxide nanoparticle cytotoxicity in 2D and 3D cell culture. Int. J. Mol. Sci. 2012, 13, 5554–5570. [Google Scholar] [CrossRef] [PubMed]
- Efremova, M.V.; Naumenko, V.A.; Spasova, M.; Garanina, A.S.; Abakumov, M.A.; Blokhina, A.D.; Melnikov, P.A.; Prelovskaya, A.O.; Heidelmann, M.; Li, Z.A. Magnetite-Gold nanohybrids as ideal all-in-one platforms for theranostics. Sci. Rep. 2018, 8, 11295. [Google Scholar] [CrossRef] [PubMed]
- Nguyen, T.; Mammeri, F.; Ammar, S. Iron oxide and gold based magneto-plasmonic nanostructures for medical applications: A review. Nanomaterials 2018, 8, 149. [Google Scholar] [CrossRef] [PubMed]
- Martinez-Boubeta, C.; Simeonidis, K.; Serantes, D.; Conde-Leborán, I.; Kazakis, I.; Stefanou, G.; Peña, L.; Galceran, R.; Balcells, L.; Monty, C. Adjustable Hyperthermia Response of Self-Assembled Ferromagnetic Fe-MgO Core–Shell Nanoparticles by Tuning Dipole–Dipole Interactions. Adv. Funct. Mater. 2012, 22, 3737–3744. [Google Scholar] [CrossRef]
- Lavorato, G.; Lima, E., Jr.; Vasquez Mansilla, M.; Troiani, H.; Zysler, R.; Winkler, E. Bifunctional CoFe2O4/ZnO core/shell nanoparticles for magnetic fluid hyperthermia with controlled optical response. J. Phys. Chem. C 2018, 122, 3047–3057. [Google Scholar] [CrossRef]
- Baeza, A.; Guisasola, E.; Ruiz-Hernandez, E.; Vallet-Regí, M. Magnetically triggered multidrug release by hybrid mesoporous silica nanoparticles. Chem. Mater. 2012, 24, 517–524. [Google Scholar] [CrossRef]
- El-Boubbou, K. Magnetic iron oxide nanoparticles as drug carriers: Clinical relevance. Nanomedicine 2018, 13, 953–971. [Google Scholar] [CrossRef]
- Kolosnjaj-Tabi, J.; Wilhelm, C. Magnetic nanoparticles in cancer therapy: How can thermal approaches help? Future Med. 2017. [Google Scholar] [CrossRef]
- Omelyanchik, A.; Efremova, M.; Myslitskaya, N.; Zybin, A.; Carey, B.J.; Sickel, J.; Kohl, H.; Bratschitsch, R.; Abakumov, M.; Majouga, A. Magnetic and Optical Properties of Gold-Coated Iron Oxide Nanoparticles. J. Nanosci. Nanotechnol. 2019, 19, 4987–4993. [Google Scholar] [CrossRef]
- Salvatore, A.; Montis, C.; Berti, D.; Baglioni, P. Multifunctional Magnetoliposomes for Sequential Controlled Release. ACS Nano 2016, 10, 7749–7760. [Google Scholar] [CrossRef]
- Illés, E.; Tombácz, E. The effect of humic acid adsorption on pH-dependent surface charging and aggregation of magnetite nanoparticles. J. Colloid Interface Sci. 2006, 295, 115–123. [Google Scholar] [CrossRef] [PubMed]
- Ungureanu, B.S.; Teodorescuv, C.-M.; Săftoiu, A. Magnetic Nanoparticles for Hepatocellular Carcinoma Diagnosis and Therapy. J. Gastrointest. Liver Dis. 2016, 25. [Google Scholar] [CrossRef]
- Ferrucci, J.; Stark, D. Iron oxide-enhanced MR imaging of the liver and spleen: Review of the first 5 years. AJR. Am. J. Roentgenol. 1990, 155, 943–950. [Google Scholar] [CrossRef] [PubMed]
- Giavridis, T.; van der Stegen, S.J.C.; Eyquem, J.; Hamieh, M.; Piersigilli, A.; Sadelain, M. CAR T cell-induced cytokine release syndrome is mediated by macrophages and abated by IL-1 blockade. Nat. Med. 2018, 24, 731–738. [Google Scholar] [CrossRef] [PubMed]
- Rezvani, K.; Rouce, R.; Liu, E.; Shpall, E. Engineering Natural Killer Cells for Cancer Immunotherapy. Molecular therapy. J. Am. Soc. Gene Ther. 2017, 25, 1769–1781. [Google Scholar] [CrossRef] [PubMed]
- Kang, J.H.; Krause, S.; Tobin, H.; Mammoto, A.; Kanapathipillai, M.; Ingber, D.E. A combined micromagnetic-microfluidic device for rapid capture and culture of rare circulating tumor cells. Lab Chip 2012, 12, 2175–2181. [Google Scholar] [CrossRef] [PubMed]
- Liu, F.; KC, P.; Zhang, G.; Zhe, J. Microfluidic magnetic bead assay for cell detection. Anal. Chem. 2015, 88, 711–717. [Google Scholar] [CrossRef]
- Shields, C.W., IV; Reyes, C.D.; López, G.P. Microfluidic cell sorting: A review of the advances in the separation of cells from debulking to rare cell isolation. Lab Chip 2015, 15, 1230–1249. [Google Scholar] [CrossRef]
- Ito, A.; Takizawa, Y.; Honda, H.; Hata, K.-I.; Kagami, H.; Ueda, M.; Kobayashi, T. Tissue engineering using magnetite nanoparticles and magnetic force: Heterotypic layers of cocultured hepatocytes and endothelial cells. Tissue Eng. 2004, 10, 833–840. [Google Scholar] [CrossRef]
- Ito, A.; Hibino, E.; Kobayashi, C.; Terasaki, H.; Kagami, H.; Ueda, M.; Kobayashi, T.; Honda, H. Construction and delivery of tissue-engineered human retinal pigment epithelial cell sheets, using magnetite nanoparticles and magnetic force. Tissue Eng. 2005, 11, 489–496. [Google Scholar] [CrossRef]
- Omelyanchik, A.; Levada, E.; Ding, J.; Lendinez, S.; Pearson, J.; Efremova, M.; Bessalova, V.; Karpenkov, D.; Semenova, E.; Khlusov, I. Design of Conductive Microwire Systems for Manipulation of Biological Cells. IEEE Trans. Magn. 2018, 54, 1–5. [Google Scholar] [CrossRef]
- Okochi, M.; Matsumura, T.; Honda, H. Magnetic force-based cell patterning for evaluation of the effect of stromal fibroblasts on invasive capacity in 3Dcultures. Biosens. Bioelectron. 2013, 42, 300–307. [Google Scholar] [CrossRef] [PubMed]
- Okochi, M.; Matsumura, T.; Yamamoto, S.; Nakayama, E.; Jimbow, K.; Honda, H. Cell behavior observation and gene expression analysis of melanoma associated with stromal fibroblasts in a three-dimensional magnetic cell culture array. Biotechnol. Prog. 2013, 29, 135–142. [Google Scholar] [CrossRef] [PubMed]
- Tanase, M.; Felton, E.J.; Gray, D.S.; Hultgren, A.; Chen, C.S.; Reich, D.H. Assembly of multicellular constructs and microarrays of cells using magnetic nanowires. Lab Chip 2005, 5, 598–605. [Google Scholar] [PubMed] [Green Version]
- Rieck, S.; Heun, Y.; Heidsieck, A.; Mykhaylyk, O.; Pfeifer, A.; Gleich, B.; Mannell, H.; Wenzel, D. Local anti-angiogenic therapy by magnet-assisted downregulation of SHP2 phosphatase. J. Controll. Release 2019, 305, 155–164. [Google Scholar] [CrossRef]
- Muthana, M.; Kennerley, A.J.; Hughes, R.; Fagnano, E.; Richardson, J.; Paul, M.; Murdoch, C.; Wright, F.; Payne, C.; Lythgoe, M.F.; et al. Directing cell therapy to anatomic target sites in vivo with magnetic resonance targeting. Nat. Commun. 2015, 6, 8009. [Google Scholar] [CrossRef] [Green Version]
- Wang, X.; Ho, C.; Tsatskis, Y.; Law, J.; Zhang, Z.; Zhu, M.; Dai, C.; Wang, F.; Tan, M.; Hopyan, S. Intracellular manipulation and measurement with multipole magnetic tweezers. Sci. Robot. 2019, 4, eaav6180. [Google Scholar] [CrossRef]
- Zamay, T.N.; Zamay, G.S.; Belyanina, I.V.; Zamay, S.S.; Denisenko, V.V.; Kolovskaya, O.S.; Ivanchenko, T.I.; Grigorieva, V.L.; Garanzha, I.V.; Veprintsev, D.V. Noninvasive Microsurgery Using Aptamer-Functionalized Magnetic Microdisks for Tumor Cell Eradication. Nucleic Acid Ther. 2017, 27, 105–114. [Google Scholar] [CrossRef]
- Golovin, Y.I.; Gribanovsky, S.L.; Golovin, D.Y.; Klyachko, N.L.; Majouga, A.G.; Master, A.M.; Sokolsky, M.; Kabanov, A.V. Towards nanomedicines of the future: Remote magneto-mechanical actuation of nanomedicines by alternating magnetic fields. J. Controll. Release 2015, 219, 43–60. [Google Scholar] [CrossRef] [Green Version]
- Du, V.; Luciani, N.; Richard, S.; Mary, G.; Gay, C.; Mazuel, F.; Reffay, M.; Menasche, P.; Agbulut, O.; Wilhelm, C. A 3D magnetic tissue stretcher for remote mechanical control of embryonic stem cell differentiation. Nat. Commun. 2017, 8, 400. [Google Scholar] [CrossRef]
- Sun, J.; Liu, X.; Huang, J.; Song, L.; Chen, Z.; Liu, H.; Li, Y.; Zhang, Y.; Gu, N. Magnetic assembly-mediated enhancement of differentiation of mouse bone marrow cells cultured on magnetic colloidal assemblies. Sci. Rep. 2014, 4, 5125. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tseng, P.; Judy, J.W.; Di Carlo, D. Magnetic nanoparticle–mediated massively parallel mechanical modulation of single-cell behavior. Nat. Methods 2012, 9, 1113. [Google Scholar] [CrossRef] [PubMed]
- Kollmannsberger, P.; Fabry, B. BaHigh-force magnetic tweezers with force feedback for biological applications. Rev. Sci. Instrum. 2007, 78, 114301. [Google Scholar] [CrossRef] [PubMed]
- Lipfert, J.; Kerssemakers, J.W.; Jager, T.; Dekker, N.H. Magnetic torque tweezers: Measuring torsional stiffness in DNA and RecA-DNA filaments. Nat. Methods 2010, 7, 977. [Google Scholar] [CrossRef] [PubMed]
- Noh, S.-H.; Moon, S.H.; Shin, T.-H.; Lim, Y.; Cheon, J. Recent advances of magneto-thermal capabilities of nanoparticles: From design principles to biomedical applications. Nano Today 2017, 13, 61–76. [Google Scholar] [CrossRef]
- He, S.; Zhang, H.; Liu, Y.; Sun, F.; Yu, X.; Li, X.; Zhang, L.; Wang, L.; Mao, K.; Wang, G. Maximizing specific loss power for magnetic hyperthermia by hard–soft mixed ferrites. Small 2018, 14, 1800135. [Google Scholar] [CrossRef] [PubMed]
- Riedinger, A.; Guardia, P.; Curcio, A.; Garcia, M.A.; Cingolani, R.; Manna, L.; Pellegrino, T. Subnanometer local temperature probing and remotely controlled drug release based on azo-functionalized iron oxide nanoparticles. Nano Lett. 2013, 13, 2399–2406. [Google Scholar] [CrossRef]
- Fuller, E.G.; Sun, H.; Dhavalikar, R.D.; Unni, M.; Scheutz, G.M.; Sumerlin, B.S.; Rinaldi, C. Externally Triggered Heat and Drug Release from Magnetically Controlled Nanocarriers. ACS Appl. Polym. Mater. 2019, 1, 211–220. [Google Scholar] [CrossRef]
- Chen, W.; Cheng, C.-A.; Zink, J.I. Spatial, Temporal, and Dose Control of Drug Delivery using Noninvasive Magnetic Stimulation. ACS Nano 2019, 13, 1292–1308. [Google Scholar] [CrossRef]
- Tietze, R.; Zaloga, J.; Unterweger, H.; Lyer, S.; Friedrich, R.P.; Janko, C.; Pöttler, M.; Dürr, S.; Alexiou, C. Magnetic nanoparticle-based drug delivery for cancer therapy. Biochem. Biophys. Res. Commun. 2015, 468, 463–470. [Google Scholar] [CrossRef]
- Stimphil, E.; Nagesetti, A.; Guduru, R.; Stewart, T.; Rodzinski, A.; Liang, P.; Khizroev, S. Physics considerations in targeted anticancer drug delivery by magnetoelectric nanoparticles. Appl. Phys. Rev. 2017, 4, 021101. [Google Scholar] [CrossRef] [Green Version]
- Mulens, V.; Morales, M.d.P.; Barber, D.F. Development of magnetic nanoparticles for cancer gene therapy: A comprehensive review. ISRN Nanomat. 2013, 2013, 646284. [Google Scholar] [CrossRef]
- Scialabba, C.; Puleio, R.; Peddis, D.; Varvaro, G.; Calandra, P.; Cassata, G.; Cicero, L.; Licciardi, M.; Giammona, G. Folate targeted coated SPIONs as efficient tool for MRI. Nano Res. 2017, 10, 3212–3227. [Google Scholar] [CrossRef]
- Nielsen, M.J.; Veidal, S.S.; Karsdal, M.A.; Orsnes-Leeming, D.J.; Vainer, B.; Gardner, S.D.; Hamatake, R.; Goodman, Z.D.; Schuppan, D.; Patel, K. Plasma Pro-C3 (N-terminal type III collagen propeptide) predicts fibrosis progression in patients with chronic hepatitis C. Liver Int. 2015, 35, 429–437. [Google Scholar] [CrossRef] [PubMed]
- Bauer, L.M.; Situ, S.F.; Griswold, M.A.; Samia, A.C.S. Magnetic particle imaging tracers: State-of-the-art and future directions. J. Phys. Chem. Lett. 2015, 6, 2509–2517. [Google Scholar] [CrossRef] [PubMed]
- Nikitin, M.P.; Orlov, A.; Sokolov, I.; Minakov, A.; Nikitin, P.; Ding, J.; Bader, S.; Rozhkova, E.; Novosad, V. Ultrasensitive detection enabled by nonlinear magnetization of nanomagnetic labels. Nanoscale 2018, 10, 11642–11650. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Haun, J.B.; Yoon, T.J.; Lee, H.; Weissleder, R. Magnetic nanoparticle biosensors. Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol. 2010, 2, 291–304. [Google Scholar] [CrossRef]
- Ehling, J.; Bartneck, M.; Fech, V.; Butzbach, B.; Cesati, R.; Botnar, R.; Lammers, T.; Tacke, F. Elastin-based molecular MRI of liver fibrosis. Hepatology 2013, 58, 1517–1518. [Google Scholar] [CrossRef]
- Nagórniewicz, B.; Mardhian, D.F.; Booijink, R.; Storm, G.; Prakash, J.; Bansal, R. Engineered Relaxin as theranostic nanomedicine to diagnose and ameliorate liver cirrhosis. Nanomedicine 2019, 17, 106–118. [Google Scholar] [CrossRef]
- Mardhian, D.F.; Storm, G.; Bansal, R.; Prakash, J. Nano-targeted relaxin impairs fibrosis and tumor growth in pancreatic cancer and improves the efficacy of gemcitabine in vivo. J. Controll. Release 2018, 290, 1–10. [Google Scholar] [CrossRef]
- Tan, S.Y.; Grimes, S. Paul Ehrlich (1854-1915): Man with the magic bullet. Singap. Med. J. 2010, 51, 842–843. [Google Scholar]
- Ledford, H. Bankruptcy filing worries developers of nanoparticle cancer drugs. Nature 2016, 533, 304–305. [Google Scholar] [CrossRef] [PubMed]
- Autio, K.A.; Dreicer, R.; Anderson, J.; Garcia, J.A.; Alva, A.; Hart, L.L.; Milowsky, M.I.; Posadas, E.M.; Ryan, C.J.; Graf, R.P.; et al. Safety and Efficacy of BIND-014, a Docetaxel Nanoparticle Targeting Prostate-Specific Membrane Antigen for Patients With Metastatic Castration-Resistant Prostate Cancer: A Phase 2 Clinical Trial. JAMA Oncol. 2018, 4, 1344–1351. [Google Scholar] [CrossRef] [PubMed]
- Josan, S.; Billingsley, K.; Orduna, J.; Park, J.M.; Luong, R.; Yu, L.; Hurd, R.; Pfefferbaum, A.; Spielman, D.; Mayer, D. Assessing inflammatory liver injury in an acute CCl4 model using dynamic 3D metabolic imaging of hyperpolarized [1-13C] pyruvate. NMR Biomed. 2015, 28, 1671–1677. [Google Scholar] [CrossRef] [PubMed]
- Kanai, A.J.; Konieczko, E.M.; Bennett, R.G.; Samuel, C.S.; Royce, S.G. Relaxin and fibrosis: Emerging targets, challenges, and future directions. Mol. Cell. Endocrinol. 2019, 487, 66–74. [Google Scholar] [CrossRef]
- Li, D.; He, L.; Guo, H.; Chen, H.; Shan, H. Targeting activated hepatic stellate cells (aHSCs) for liver fibrosis imaging. EJNMMI Res. 2015, 5, 71. [Google Scholar] [CrossRef]
- Mederacke, I.; Hsu, C.C.; Troeger, J.S.; Huebener, P.; Mu, X.; Dapito, D.H.; Pradere, J.-P.; Schwabe, R.F. Fate tracing reveals hepatic stellate cells as dominant contributors to liver fibrosis independent of its aetiology. Nat. Commun. 2013, 4, 2823. [Google Scholar] [CrossRef]
- Luangmonkong, T.; Suriguga, S.; Mutsaers, H.A.; Groothuis, G.M.; Olinga, P.; Boersema, M. Targeting oxidative stress for the treatment of liver fibrosis. In Reviews of Physiology, Biochemistry and Pharmacology, Vol. 175; Springer: Berlin, Germany, 2018; pp. 71–102. [Google Scholar]
- Schon, H.-T.; Bartneck, M.; Borkham-Kamphorst, E.; Nattermann, J.; Lammers, T.; Tacke, F.; Weiskirchen, R. Pharmacological intervention in hepatic stellate cell activation and hepatic fibrosis. Front. Pharmacol. 2016, 7, 33. [Google Scholar] [CrossRef]
- Ungefroren, H.; Gieseler, F.; Kaufmann, R.; Settmacher, U.; Lehnert, H.; Rauch, B. Signaling crosstalk of TGF-β/ALK5 and PAR2/PAR1: A Complex regulatory network controlling fibrosis and cancer. Int. J. Mol. Sci. 2018, 19, 1568. [Google Scholar] [CrossRef]
- Palomer, X.; Barroso, E.; Pizarro-Delgado, J.; Peña, L.; Botteri, G.; Zarei, M.; Aguilar, D.; Montori-Grau, M.; Vázquez-Carrera, M. PPARβ/δ: A key therapeutic target in metabolic disorders. Int. J. Mol. Sci. 2018, 19, 913. [Google Scholar] [CrossRef]
- Peng, Z.W.; Ikenaga, N.; Liu, S.B.; Sverdlov, D.Y.; Vaid, K.A.; Dixit, R.; Weinreb, P.H.; Violette, S.; Sheppard, D.; Schuppan, D. Integrin αvβ6 critically regulates hepatic progenitor cell function and promotes ductular reaction, fibrosis, and tumorigenesis. Hepatology 2016, 63, 217–232. [Google Scholar] [CrossRef] [PubMed]
- Greupink, R.; Bakker, H.I.; van Goor, H.; de Borst, M.H.; Beljaars, L.; Poelstra, K. Mannose-6-phosphate/insulin-Like growth factor-II receptors may represent a target for the selective delivery of mycophenolic acid to fibrogenic cells. Pharm. Res. 2006, 23, 1827–1834. [Google Scholar] [CrossRef] [PubMed]
- Bonner, J.C. Regulation of PDGF and its receptors in fibrotic diseases. Cytokine Growth Factor Rev. 2004, 15, 255–273. [Google Scholar] [CrossRef] [PubMed]
- Bansal, R.; Prakash, J.; De Ruiter, M.; Poelstra, K. Targeted recombinant fusion proteins of IFNgamma and mimetic IFNgamma with PDGFbetaR bicyclic peptide inhibits liver fibrogenesis in vivo. PLoS ONE 2014, 9, e89878. [Google Scholar] [CrossRef]
- van Dijk, F.; Teekamp, N.; Beljaars, L.; Post, E.; Zuidema, J.; Steendam, R.; Kim, Y.O.; Frijlink, H.W.; Schuppan, D.; Poelstra, K.; et al. Pharmacokinetics of a sustained release formulation of PDGFbeta-receptor directed carrier proteins to target the fibrotic liver. J. Controll. Release 2018, 269, 258–265. [Google Scholar] [CrossRef]
- Gressner, A.M.; Weiskirchen, R.; Breitkopf, K.; Dooley, S. Roles of TGF-beta in hepatic fibrosis. Front. Biosci. 2002, 7, d793–d807. [Google Scholar] [CrossRef]
- Henderson, N.C.; Arnold, T.D.; Katamura, Y.; Giacomini, M.M.; Rodriguez, J.D.; McCarty, J.H.; Pellicoro, A.; Raschperger, E.; Betsholtz, C.; Ruminski, P.G.; et al. Targeting of alphav integrin identifies a core molecular pathway that regulates fibrosis in several organs. Nat. Med. 2013, 19, 1617–1624. [Google Scholar] [CrossRef]
- Bansal, R.; Nakagawa, S.; Yazdani, S.; van Baarlen, J.; Venkatesh, A.; Koh, A.P.; Song, W.M.; Goossens, N.; Watanabe, H.; Beasley, M.B.; et al. Integrin alpha 11 in the regulation of the myofibroblast phenotype: Implications for fibrotic diseases. Exp. Mol. Med. 2017, 49, e396. [Google Scholar] [CrossRef]
- Samuel, C.; Royce, S.; Hewitson, T.; Denton, K.; Cooney, T.; Bennett, R. Anti-fibrotic actions of relaxin. Br. J. Pharmacol. 2017, 174, 962–976. [Google Scholar] [CrossRef]
- Bennett, R.G.; Simpson, R.L.; Hamel, F.G. Serelaxin increases the antifibrotic action of rosiglitazone in a model of hepatic fibrosis. World J. Gastroenterol. 2017, 23, 3999. [Google Scholar] [CrossRef]
- Feijóo-Bandín, S.; Aragón-Herrera, A.; Rodríguez-Penas, D.; Portolés, M.; Roselló-Lletí, E.; Rivera, M.; González-Juanatey, J.R.; Lago, F. Relaxin-2 in cardiometabolic diseases: Mechanisms of action and future perspectives. Front. Physiol. 2017, 8, 599. [Google Scholar] [CrossRef] [PubMed]
- Gracia-Sancho, J.; Maeso-Diaz, R.; Fernández-Iglesias, A.; Navarro-Zornoza, M.; Bosch, J. New cellular and molecular targets for the treatment of portal hypertension. Hepatol. Int. 2015, 9, 183–191. [Google Scholar] [CrossRef] [PubMed]
- Ng, H.H.; Leo, C.H.; Parry, L.J.; Ritchie, R.H. Relaxin as a Therapeutic Target for the Cardiovascular Complications of Diabetes. Front. Pharmacol. 2018, 9, 501. [Google Scholar] [CrossRef] [PubMed]
- Hoy, S.M. Patisiran: First Global Approval. Drugs 2018, 78, 1625–1631. [Google Scholar] [CrossRef]
- Bangen, J.M.; Hammerich, L.; Sonntag, R.; Baues, M.; Haas, U.; Lambertz, D.; Longerich, T.; Lammers, T.; Tacke, F.; Trautwein, C.; et al. Targeting CCl4 -induced liver fibrosis by RNA interference-mediated inhibition of cyclin E1 in mice. Hepatology 2017, 66, 1242–1257. [Google Scholar] [CrossRef]
- Roy, S.; Benz, F.; Luedde, T.; Roderburg, C. The role of miRNAs in the regulation of inflammatory processes during hepatofibrogenesis. Hepatobiliary Surg. Nutr. 2015, 4, 24–33. [Google Scholar]
Molecular Target | Compound | Effect |
---|---|---|
Apoptosis signal-regulating kinase 1 (ASK1) | Selonsertib (GS-4997) | oral bioavailable inhibitor of ASK1, thereby preventing the production of inflammatory and fibrotic acting cytokines |
Hepatic metabolism | Obeticholic acid | synthetically modified bile acid and potent agonist of the farnesoid X nuclear receptor (FXR) |
Elafibranor | Orally administered drug acting on the 3 sub-types of PPAR (PPARα, PPARγ, PPARδ) | |
Tropifexor | Investigational drug which acts as an agonist of the farnesoid X nuclear receptor (FXR) | |
Cilofexor (GS-9674) | agonist of the farnesoid X nuclear receptor (FXR) which improves cholestasis and liver injury | |
AKN-083 | farnesoid X receptor (FXR) agonist | |
INT-767 | a dual agonist targeting the farnesoid X receptor (FXR) and the G protein-coupled bile acid receptor 1 (GPBAR1) | |
Aramchol | An orally active fatty acid bile acid conjugate that inhibits stearoyl coenzyme A desaturase 1 (SCD1) | |
Saroglitazar | Agonist of PPARα (and PPARγ) | |
Lanifibranor | Orally administered drug acting on the 3 sub-types of PPAR (PPARα, PPARγ, PPARδ) | |
Firsocostat (GS-0976) | Liver-targeted acetyl-CoA carboxylase (ACC) inhibitor | |
PF-05221304 | Liver-targeted acetyl-CoA carboxylase (ACC) inhibitor | |
Chemokine receptors | Cenicriviroc | blocks the chemokine receptors CC chemokine receptor 2 (CCR2) and CCR5 |
Caspases | Emricasan | Prevents cells death by inhibition of caspases |
VX-166 | The drug has anti-apoptotic activity and prevents release of interleukins | |
Nivocasan (GS-9450) | hepatoprotective activity preventing fibrosis and apoptosis | |
Fibroblast growth factor 21 (FGF21) | Pegbelfermin (BMS-986036) | PEGylated FGF21 analogue that improves metabolic parameters |
Fibroblast growth factor 19 (FGF19) | Aldafermin (NGM282) | Synthetic FGF19 analogue preventing hepatic fat accumulation and liver damage |
Glucagon-like peptide-1 receptor | Liraglutide | GLP-1 receptor agonist triggering insulin synthesis |
Semaglutide | GLP-1 receptor agonist triggering insulin synthesis |
Role of MNP1 | Area of Biomedical Application | Literature |
---|---|---|
Binding-mediated cell capturing | Cell isolation and separation | [141,143,144,145] |
Cell and tissue engineering | [146,147,148] | |
Cell patterning and concentration | [149,150,151,152,153] | |
Mechanical cell control | Low-frequency magnetic field for cell destruction and induction of apoptosis | [78,155,156] |
Differentiation of stem cells, modulation of cell division and motility | [157,158,159] | |
Fundamental study of macromolecules and cell‘s mechanical properties | [160,161] | |
Drug delivery | Magnetic fluid hyperthermia of cancer | [135,162,163] |
On-demand release of drugs via thermosensitive polymers or azo molecules from hybrid nanoplatforms | [133,164,165] | |
Targeting or delivery of drug or genes immobilized on surfaces | [166,167,168,169] | |
Imaging applications | Reduction of T1 and T2 relaxation time of the water protons for the MRI-contrast | [66,124,170] |
Imaging and detection via a non-linear magnetic signal | [172,173] | |
Improved detection of magnetic signals, imaging of liver fibrosis | [174,175] |
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Levada, K.; Omelyanchik, A.; Rodionova, V.; Weiskirchen, R.; Bartneck, M. Magnetic-Assisted Treatment of Liver Fibrosis. Cells 2019, 8, 1279. https://doi.org/10.3390/cells8101279
Levada K, Omelyanchik A, Rodionova V, Weiskirchen R, Bartneck M. Magnetic-Assisted Treatment of Liver Fibrosis. Cells. 2019; 8(10):1279. https://doi.org/10.3390/cells8101279
Chicago/Turabian StyleLevada, Kateryna, Alexander Omelyanchik, Valeria Rodionova, Ralf Weiskirchen, and Matthias Bartneck. 2019. "Magnetic-Assisted Treatment of Liver Fibrosis" Cells 8, no. 10: 1279. https://doi.org/10.3390/cells8101279