Influence of surface charge and polymer coating on internalization and biodistribution of polyethylene glycol-modified iron oxide nanoparticles

Journal of Biomedical Nanotechnology

Volumn 11, Issue 1, 2015, Pages 126-136

  Maurizi, Lionel ^a,d   Papa, Anne Laure ^a,e   Dumont, Laure ^b   Bouyer, Frédéric ^a   Walker, Paul ^c   Vandroux, David ^b   Millot, Nadine ^a  

^a UNIVERSITÉ DE BOURGOGNE   (France)

^b NVH Medicinal   (France)

^c DIJON UNIVERSITY HOSPITAL   (France)

^d EPFL   (Switzerland)

^e HARVARD UNIVERSITY   (United States)

Author keywords

In vivo assays; Macrophages; MRI (magnetic resonance imaging); Nanoparticles; Surface grafting

Indexed keywords

GRAFTING (CHEMICAL); MACROPHAGES; MAGNETIC RESONANCE IMAGING; METAL NANOPARTICLES; NANOMAGNETICS; NANOPARTICLES; PLASTIC COATINGS;

BIOLOGICAL INTERACTIONS; CELL INTERNALIZATION; IN-VIVO; IRON OXIDE NANOPARTICLE; MRI (MAGNETIC RESONANCE IMAGING); RETICULOENDOTHELIAL SYSTEMS; SUPERPARAMAGNETIC IRON OXIDE NANOPARTICLES; SURFACE GRAFTING;

IRON OXIDES;

FERUCARBOTRAN; IRON OXIDE; MACROGOL; NANOPARTICLE; POLYMER; SUPERPARAMAGNETIC IRON OXIDE NANOPARTICLE; BIOMATERIAL; DEXTRAN; FERUMOXTRAN-10; MACROGOL DERIVATIVE; MAGNETITE NANOPARTICLE; NANOCAPSULE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; CYTOTOXICITY; HUMAN; HUMAN CELL; INTERNALIZATION; LIVER; MATERIAL COATING; MOUSE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; RETICULOENDOTHELIAL SYSTEM; SURFACE CHARGE; ANIMAL; ANTIBODY SPECIFICITY; CELL LINE; CELL SURVIVAL; CHEMISTRY; DRUG EFFECTS; HEPG2 CELL LINE; MACROPHAGE; MATERIALS TESTING; PARTICLE SIZE; STATIC ELECTRICITY; STRUCTURE ACTIVITY RELATION; TISSUE DISTRIBUTION; ULTRASTRUCTURE;

ANIMALS; CELL LINE; CELL SURVIVAL; COATED MATERIALS, BIOCOMPATIBLE; DEXTRANS; HEP G2 CELLS; HUMANS; MACROPHAGES; MAGNETITE NANOPARTICLES; MATERIALS TESTING; MICE; NANOCAPSULES; ORGAN SPECIFICITY; PARTICLE SIZE; POLYETHYLENE GLYCOLS; STATIC ELECTRICITY; STRUCTURE-ACTIVITY RELATIONSHIP; TISSUE DISTRIBUTION;

EID: 84907845064     PISSN: 15507033     EISSN: 15507041     Source Type: Journal    
DOI: 10.1166/jbn.2015.1996     Document Type: Article

References (64)

1. Q. A. Pankhurst, N. T. K. Thanh, S. K. Jones, and J. Dobson, Progress in applications of magnetic nanoparticles in biomedicine. J. Phys.-Appl. Phys. 42, 22 (2009).
2. I. Hilger and W. A. Kaiser, Iron oxide-based nanostructures for MRI and magnetic hyperthermia. Nanomed. 7, 1443 (2012).
3. A. K. Gupta, R. R. Naregalkar, V. D. Vaidya, and M. Gupta, Recent advances on surface engineering of magnetic iron oxide nanoparticles and their biomedical applications. Nanomed. 2, 23 (2007).
4. Z. L. Zhang, R. Dharmakumar, N. Mascheri, Z. Y. Fan, S. Y. Wu, and D. B. Li, Comparison of superparamagnetic and ultrasmall superparamagnetic iron oxide cell labeling for tracking green fluorescent protein gene marker with negative and positive contrast magnetic resonance imaging. Mol. Imaging 8, 148 (2009).
5. F. Liu, S. Laurent, H. Fattahi, L. V. Elst, and R. N. Muller, Superparamagnetic nanosystems based on iron oxide nanoparticles for biomedical imaging. Nanomed. 6, 519 (2011).
6. R. Singh and H. S. Nalwa, Medical applications of nanoparticles in biological imaging, cell labeling, antimicrobial agents, and anticancer nanodrugs. J. Biomed. Nanotechnol. 7, 489 (2011).
7. Y. X. J. Wang, S. M. Hussain, and G. P. Krestin, Superparamagnetic iron oxide contrast agents: Physicochemical characteristics and applications in MR imaging. Eur. Radiol. 11, 2319 (2001).
8. P. Reimer and T. Balzer, Ferucarbotran (resovist): A new clinically approved RES-specific contrast agent for contrast-enhanced MRI of the liver: Properties, clinical development, and applications. Eur. Radiol. 13, 1266 (2003).
9. K.-J. Chen, S. M. Wolahan, H. Wang, C.-H. Hsu, H.-W. Chang, A. Durazo, L.-P. Hwang, M. A. Garcia, Z. K. Jiang, L. Wu, Y.-Y. Lin, and H.-R. Tseng, A small MRI contrast agent library of gadolinium(III)-encapsulated supramolecular nanoparticles for improved relaxivity and sensitivity. Biomaterials 32, 2160 (2011).
10. P. Poix, Sur une methode de determination des distances cationoxygene dans les oxydes mixtes a structure spinelle-application des valeurs a quelques cas particuliers. Bull. Soc. Chim. Fr. 4, 1085 (1965).
11. T. Belin, N. Millot, N. Bovet, and M. Gailhanou, In situ and time resolved study of the gamma/alpha-Fe2O3 transition in nanometric particles. J. Solid State Chem. 180, 2377 (2007).
12. J. L. Dormann, D. Fiorani, and E. Tronc, Magnetic relaxation in fine-particle systems. Adv. Chem. Phys. 98, 283 (1997).
13. S. Laurent, D. Forge, M. Port, A. Roch, C. Robic, L. V. Elst, and R. N. Muller, Magnetic iron oxide nanoparticles: Synthesis, stabilization, vectorization, physicochemical characterizations, and biological applications. Chem. Rev. 108, 2064 (2008).
14. H. Duan, M. Kuang, X. Wang, Y. A. Wang, H. Mao, and S. Nie, Reexamining the effects of particle size and surface chemistry on the magnetic properties of iron oxide nanocrystals: New insights into spin disorder and proton relaxivity. J. Phys. Chem. C 112, 8127 (2008).
15. U. I. Tromsdorf, N. C. Bigall, M. G. Kaul, O. T. Bruns, M. S. Nikolic, B. Mollwitz, R. A. Sperling, R. Reimer, H. Hohenberg, W. J. Parak, S. Forster, U. Beisiegel, G. Adam, and H. Weller, Size and surface effects on the MRI relaxivity of manganese ferrite nanoparticle contrast agents. Nano Lett. 7, 2422 (2007).
16. S. Campelj, D. Makovec, and M. Drofenik, Functionalization of magnetic nanoparticles with 3-aminopropyl silane. J. Magn. Magn. Mater. 321, 1346 (2009).
17. C. M. Cheng, G. Kou, X. L. Wang, S. H. Wang, H. C. Gu, and Y. J. Guo, Synthesis of carboxyl superparamagnetic ultrasmall iron oxide (USPIO) nanoparticles by a novel flocculation-redispersion process. J. Magn. Magn. Mater. 321, 2663 (2009).
18. T. J. Daou, S. Begin-Colin, J. M. Greneche, F. Thomas, A. Derory, P. Bernhardt, P. Legare, and G. Pourroy, Phosphate adsorption properties of magnetite-based nanoparticles. Chem. Mater. 19, 4494 (2007).
19. L. Maurizi, F. Bouyer, J. Paris, F. Demoisson, L. Saviot, and N. Millot, One step continuous hydrothermal synthesis of very fine stabilized superparamagnetic nanoparticles of magnetite. Chem. Commun. 47, 11706 (2011).
20. X. F. Xue, K. Hanna, C. Despas, F. Wu, and N. S. Deng, Effect of chelating agent on the oxidation rate of PCP in the magnetite/H2O2 system at neutral pH. J. Mol. Catal. Chem. 311, 29 (2009).
21. L. Maurizi, U. Sakulkhu, L. A. Crowe, V. M. Dao, N. Leclaire, J.-P. Vallée, and H. Hofmann, Syntheses of cross-linked polymeric superparamagnetic beads with tunable properties. RSC Adv. 4, 11142 (2014).
22. M. Chanana, Z. Mao, and D. Wang, Using polymers to make up magnetic nanoparticles for biomedicine. J. Biomed. Nanotechnol. 5, 652 (2009).
23. M. D. Butterworth, L. Illum, and S. S. Davis, Preparation of ultrafine silica- and PEG-coated magnetite particles. Colloids Surf.- Physicochem. Eng. Asp. 179, 93 (2001).
24. A. Petri-Fink, M. Chastellain, L. Juillerat-Jeanneret, A. Ferrari, and H. Hofmann, Development of functionalized superparamagnetic iron oxide nanoparticles for interaction with human cancer cells. Biomaterials 26, 2685 (2005).
25. S. Nayar and A. Guha, A novel biomimetic material-Glycine-PVA ferrofluid that crosses the blood-brain barrier. J. Biomed. Nanotechnol. 7, 78 (2011).
26. L. Kaufner, R. Cartier, R. Wuestneck, I. Fichtner, S. Pietschmann, H. Bruhn, D. Schuett, A. F. Thuenemann, and U. Pison, Poly(ethylene oxide)-block-poly(glutamic acid) coated maghemite nanoparticles: In vitro characterization and in vivo behaviour. Nanotechnology 18, 115710 (2007).
27. P. Reimer and B. Tombach, Hepatic MRI with SPIO: Detection and characterization of focal liver lesions. Eur. Radiol. 8, 1198 (1998).
28. V. Dousset, L. Ballarino, C. Delalande, M. Coussemacq, P. Canioni, K. G. Petry, and J. M. Caille, Comparison of ultrasmall particles of iron oxide (USPIO)-enhanced T2-Weighted, conventional T2- weighted, and gadolinium-enhanced T1-weighted MR images in rats with experimental autoimmune encephalomyelitis. Am. J. Neuroradiol. 20, 223 (1999).
29. A. Bjornerud and L. Johansson, The utility of superparamagnetic contrast agents in MRI: Theoretical consideration and applications in the cardiovascular system. Nmr. Biomed. 17, 465 (2004).
30. A. J. L. Villaraza, A. Bumb, and M. W. Brechbiel, Macromolecules, dendrimers, and nanomaterials in magnetic resonance imaging: The interplay between size, function, and pharmacokinetics. Chem. Rev. 110, 2921 (2010).
31. C. Sun, J. S. H. Lee, and M. Q. Zhang, Magnetic nanoparticles in MR imaging and drug delivery. Adv. Drug Deliv. Rev. 60, 1252 (2008).
32. E. Duguet, S. Vasseur, S. Mornet, and J. M. Devoisselle, Magnetic nanoparticles and their applications in medicine. Nanomed. 1, 157 (2006).
33. S. M. Moghimi, A. C. Hunter, and J. C. Murray, Long-circulating and target-specific nanoparticles: Theory to practice. Pharmacol. Rev. 53, 283 (2001).
34. C. Corot, P. Robert, J. M. Idee, and M. Port, Recent advances in iron oxide nanocrystal technology for medical imaging. Adv. Drug Deliv. Rev. 58, 1471-1504 (2006).
35. A. C. Faure, S. Dufort, V. Josserand, P. Perriat, J. L. Coll, S. Roux, and O. Tillement, Control of the in Vivo biodistribution of hybrid nanoparticles with different poly(ethylene glycol) coatings. Small 5, 2565 (2009).
36. G. Ge, H. Wu, F. Xiong, Y. Zhang, Z. Guo, Z. Bian, J. Xu, C. Gu, N. Gu, X. Chen, and D. Yang, The cytotoxicity evaluation of magnetic iron oxide nanoparticles on human aortic endothelial cells. Nanoscale Res. Lett. 8, 215 (2013).
37. C. Barrera, A. P. Herrera, and C. Rinaldi, Colloidal dispersions of monodisperse magnetite nanoparticles modified with poly(ethylene glycol). J. Colloid Interface Sci. 329, 107 (2009).
38. C. Oh, Y. G. Lee, T. S. Choi, C. U. Jon, and S. G. Oh, Facile synthesis of PEG-silica hybrid particles using one-step sol-gel reaction in aqueous solution. Colloids Surf.-Physicochem. Eng. Asp. 349, 145 (2009).
39. F. Bertorelle, C. Wilhelm, J. Roger, F. Gazeau, C. Menager, and V. Cabuil, Fluorescence-modified superparamagnetic nanoparticles: Intracellular uptake and use in cellular imaging. Langmuir 22, 5385 (2006).
40. L. Maurizi, H. Bisht, F. Bouyer, and N. Millot, Easy route to functionalize iron oxide nanoparticles via long-term stable thiol groups. Langmuir 25, 8857 ( 2009).
41. R. Massart, E. Dubois, V. Cabuil, and E. Hasmonay, Preparation and properties of monodisperse magnetic fluids. J. Magn. Magn. Mater. 149, 1 (1995).
42. J. Boudon, J. Paris, Y. Bernhard, E. Popova, R. A. Decreau, and N. Millot, Magneto-optical nanomaterial: A SPIO-phthalocyanine scaffold built step-by-step towards bimodal imaging. Chem. Commun. 49, 7394 (2013).
43. S. Jo and K. Park, Surface modification using silanated poly(ethylene glycol)s. Biomaterials 21, 605 (2000).
44. C. Flesch, M. Joubert, E. Bourgeat-Lami, S. Mornet, E. Duguet, C. Delaite, and P. Dumas, Organosilane-modified maghemite nanoparticles and their use as Co-initiator in the ring-opening polymerization of epsilon-caprolactone. Colloids Surf.-Physicochem. Eng. Asp. 262, 150 (2005).
45. R. Shen, P. H. C. Camargo, Y. Xia, and H. Yang, Silane-based poly(ethylene glycol) as a primer for surface modification of nonhydrolytically synthesized nanoparticles using the stober method. Langmuir 24, 11189 (2008).
46. P. Eyer, F. Worek, D. Kiderlen, G. Sinko, A. Stuglin, V. Simeon- Rudolf, and E. Reiner, Molar absorption coefficients for the reduced ellman reagent: Reassessment. Anal. Biochem. 312, 224 (2003).
47. A.-L. Papa, L. Maurizi, D. Vandroux, P. Walker, and N. Millot, Synthesis of titanate nanotubes directly coated with USPIO in hydrothermal conditions: A new detectable nanocarrier. J. Phys. Chem. C 115, 19012 (2011).
48. K. H. Diehl, R. Hull, D. Morton, R. Pfister, Y. Rabemampianina, D. Smith, J. M. Vidal, and C. van de Vorstenbosch, European federation of pharmaceutical industries association and european centre for the validation of alternative methods, A good practice guide to the administration of substances and removal of blood, including routes and volumes. J. Appl. Toxicol. JAT 21, 15 (2001).
49. D.W. Yang, Q. Ye, M. Williams, Y. Sun, T. C. C. Hu, D. S. Williams, J. M. F. Moura, and C. Ho, USPIO-enhanced dynamic MRI: Evaluation of normal and transplanted rat kidneys. Magn. Reson. Med. 46, 1152 (2001).
50. D. E. Sosnovik, M. Nahrendorf, and R. Weissleder, Magnetic nanoparticles for MR imaging: Agents, techniques and cardiovascular applications. Basic Res. Cardiol. 103, 122 (2008).
51. N. Fauconnier, A. Bee, J. Roger, and J. N. Pons, Synthesis of aqueous magnetic liquids by surface complexation of maghemite nanoparticles. J. Mol. Liq. 83, 233 (1999).
52. Y. W. Jun, Y. M. Huh, J. S. Choi, J. H. Lee, H. T. Song, S. Kim, S. Yoon, K. S. Kim, J. S. Shin, J. S. Suh, and J. Cheon, Nanoscale size effect of magnetic nanocrystals and their utilization for cancer diagnosis via magnetic resonance imaging. J. Am. Chem. Soc. 127, 5732 (2005).
53. Y. W. Jun, J. W. Seo, and A. Cheon, Nanoscaling laws of magnetic nanoparticles and their applicabilities in biomedical sciences. Acc. Chem. Res. 41, 179 (2008).
54. B. A. Larsen, M. A. Haag, N. J. Serkova, K. R. Shroyer, and C. R. Stoldt, Controlled aggregation of superparamagnetic iron oxide nanoparticles for the development of molecular magnetic resonance imaging probes. Nanotechnology 19, 265102 (2008).
55. A. Roch, Y. Gossuin, R. N. Muller, and P. Gillis, Superparamagnetic colloid suspensions: Water magnetic relaxation and clustering. J. Magn. Magn. Mater. 293, 532 (2005).
56. L. E. W. LaConte, N. Nitin, O. Zurkiya, D. Caruntu, C. J. O'Connor, X. P. Hu, and G. Bao, Coating thickness of magnetic iron oxide nanoparticles affects R2 relaxivity. J. Magn. Reson. Imaging 26, 1634 (2007).
57. T. Schlorf, M. Meincke, E. Kossel, C.-C. Glüer, O. Jansen, and R. Mentlein, Biological properties of iron oxide nanoparticles for cellular and molecular magnetic resonance imaging. Int. J. Mol. Sci. 12, 12 (2010).
58. A. P. Khandhar, R. M. Ferguson, J. A. Simon, and K. M. Krishnan, Tailored magnetic nanoparticles for optimizing magnetic fluid hyperthermia. J. Biomed. Mater. Res. A 100, 728 (2012).
59. A. P. Khandhar, R. M. Ferguson, H. Arami, and K. M. Krishnan, Monodisperse magnetite nanoparticle tracers for in vivo magnetic particle imaging. Biomaterials 34, 3837 (2013).
60. M. F. Calmon, A. T. de Souza, N. M. Candido, M. I. B. Raposo, S. Taboga, P. Rahal, and J. G. Nery, A systematic study of transfection efficiency and cytotoxicity in HeLa cells using iron oxide nanoparticles prepared with organic and inorganic bases. Colloids Surf. B Biointerfaces 100, 177 (2012).
61. M. Goutayer, S. Dufort, V. Josserand, A. Royere, E. Heinrich, F. Vinet, J. Bibette, J. L. Coll, and I. Texier, Tumor targeting of functionalized lipid nanoparticles: Assessment by in vivo fluorescence imaging. Eur. J. Pharm. Biopharm. 75, 137 (2010).
62. Y. Okuhata, Delivery of diagnostic agents for magnetic resonance imaging. Adv. Drug Deliv. Rev. 37, 121 (1999).
63. S. Mornet, S. Vasseur, F. Grasset, P. Veverka, G. Goglio, A. Demourgues, J. Portier, E. Pollert, and E. Duguet, Magnetic nanoparticle design for medical applications. Prog. Solid State Chem. 34, 237 (2006).
64. L. Maurizi, U. Sakulkhu, A. Gramoun, J.-P. Vallee, and H. Hofmann, A fast and reproducible method to quantify magnetic nanoparticle biodistribution. Analyst 139, 1184 (2014).