Superparamagnetic iron oxide nanoparticles for delivery of therapeutic agents: Opportunities and challenges

Expert Opinion on Drug Delivery

Volumn 11, Issue 9, 2014, Pages 1449-1470

  Laurent, Sophie ^a   Saei, Amir Ata ^b,c   Behzadi, Shahed ^d   Panahifar, Arash ^e   Mahmoudi, Morteza ^c,f  

^a UNIVERSITY OF MONS   (Belgium)

^b TABRIZ UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^c TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^d MAX PLANCK INSTITUTE FOR POLYMER RESEARCH   (Germany)

^e UNIVERSITY OF ALBERTA   (Canada)

^f STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Biomedical; Biomedicine; Coating; Controlled release; Functionalization; Nanocarrier; Surface targeting; Toxicity

Indexed keywords

NANOPARTICLE; SUPERPARAMAGNETIC IRON OXIDE;

BIOCOMPATIBILITY; CELL LABELING; CHEMICAL MODIFICATION; DIARRHEA; DRUG DELIVERY SYSTEM; DRUG FORMULATION; DRUG STABILITY; DRUG TARGETING; GENE EXPRESSION; HOMEOSTASIS; HUMAN; MAGNETIC FIELD; NAUSEA; OXIDATIVE STRESS; REVIEW; SIGNAL TRANSDUCTION; SURFACE PROPERTY; URTICARIA;

BIOMEDICAL; BIOMEDICINE; COATING; CONTROLLED RELEASE; FUNCTIONALIZATION; NANOCARRIER; SURFACE TARGETING; TOXICITY;

ANIMALS; DEXTRANS; DIAGNOSTIC IMAGING; DRUG CARRIERS; DRUG DELIVERY SYSTEMS; HUMANS; MAGNETIC FIELDS; MAGNETITE NANOPARTICLES; NANOMEDICINE;

EID: 84905989428     PISSN: 17425247     EISSN: 17447593     Source Type: Journal    
DOI: 10.1517/17425247.2014.924501     Document Type: Review

References (162)

1. Kelkar SS, Reineke TM. Theranostics: Combining imaging and therapy. Bioconjug Chem 2011;22(10):1879-903
2. Mahmoudi M, Sant S, Wang B, et al. Superparamagnetic iron oxide nanoparticles (SPIONs): Development, surface modification and applications in chemotherapy. Adv Drug Deliv Rev 2011;63(1-2):24-46
3. Yen SK, Padmanabhan P, Selvan ST. Multifunctional iron oxide nanoparticles for diagnostics, therapy and macromolecule delivery. Theranostics 2013;3(12):986
4. Anzai Y, Piccoli CW, Outwater EK, et al. Evaluation of neck and body metastases to nodes with ferumoxtran 10-enhanced MR imaging: Phase III safety and efficacy study 1. Radiology 2003;228(3):777-88
5. Sakhtianchi R, Minchin RF, Lee K-B, et al. Exocytosis of nanoparticles from cells: Role in cellular retention and toxicity. Adv Colloid Interface Sci 2013;201-202:18-29
6. Arruebo M, Galán M, Navascués N, et al. Development of magnetic nanostructured silica-based materials as potential vectors for drug-delivery applications. Chem Mater 2006;18(7):1911-19
7. Durán J, Arias J, Gallardo V, Delgado A. Magnetic colloids as drug vehicles. J Pharm Sci 2008;97(8):2948-83
8. Corot C, Robert P, Idée J-M, Port M. Recent advances in iron oxide nanocrystal technology for medical imaging. Adv Drug Deliv Rev 2006;58(14):1471-504
9. Saei AA, NazhadDolatabadi JE, Najafi-Marandi P, et al. Electrchemical biosensors for glucose based on metal nanoparticles. TrAC Trends Anal Chem 2013;42:216-27
10. Mahmoudi M, Hosseinkhani H, Hosseinkhani M, et al. Magnetic resonance imaging tracking of stem cells in vivo using iron oxide nanoparticles as a tool for the advancement of clinical regenerative medicine. Chem Rev 2010;111(2):253-80
11. Laurent S, Dutz S, Häfeli UO, Mahmoudi M. Magnetic fluid hyperthermia: Focus on superparamagnetic iron oxide nanoparticles. Adv Colloid Interface Sci 2011;166(1):8-23
12. Larson TA, Joshi PP, Sokolov K. Preventing protein adsorption and macrophage uptake of gold nanoparticles via a hydrophobic shield. ACS Nano 2012;6(10):9182-90
13. Larsen EKU, Nielsen T, Wittenborn T, et al. Accumulation of magnetic iron oxide nanoparticles coated with variably sized polyethylene glycol in murine tumors. Nanoscale 2012;4(7):2352-61
14. Koffie RM, Farrar CT, Saidi LJ, et al. Nanoparticles enhance brain Delivery of blood-brain barrier-impermeable probes for in vivo optical and magnetic resonance imaging. Proc Natl Acad Sci USA 2011;108(46):18837-42
15. Roca A, Costo R, Rebolledo A, et al. Progress in the preparation of magnetic nanoparticles for applications in biomedicine. J Phys D Appl Phys 2009;42(22):224002
16. Lee H, Yu MK, Park S, et al. Thermally cross-linked superparamagnetic iron oxide nanoparticles: Synthesis and application as a dual imaging probe for cancer in vivo. J Am Chem Soc 2007;129(42):12739-45
17. Larsen EK, Nielsen T, Wittenborn T, et al. Size-dependent accumulation of PEGylated silane-coated magnetic iron oxide nanoparticles in murine tumors. ACS Nano 2009;3(7):1947-51
18. Zhu XM, Wang YXJ, Leung KCF, et al. Enhanced cellular uptake of aminosilanecoated superparamagnetic iron oxide nanoparticles in mammalian cell lines. Int J Nanomed 2012;7:953
19. Maleki H, Simchi A, Imani M, Costa BFO. Size-controlled synthesis of superparamagnetic iron oxide nanoparticles and their surface coating by gold for biomedical applications. J Magn Magn Mater 2012;324(23):3997-4005
20. Laurent S, Forge D, Port M, et al. Magnetic iron oxide nanoparticles: Synthesis, stabilization, vectorization, physicochemical characterizations, and biological applications. Chem Rev 2008;108(6):2064-110
21. Fauconnier N, Pons J, Roger J, Bee A. Thiolation of maghemite nanoparticles by dimercaptosuccinic acid. J Colloid Interface Sci 1997;194(2):427-33
22. Racuciu M, Creanga D, Airinei A. Citric-Acid-coated magnetite nanoparticles for biological applications. Euro Phys J E Soft Matter 2006;21(2):117-21
23. Park J, Lee JJ, Kim IS, et al. Magnetic and MR relaxation properties of avidin-biotin conjugated superparamagnetic nanoparticles. Colloids Surf A 2008;313:288-91
24. Quan Q, Xie J, Gao H, et al. HSA coated iron oxide nanoparticles as drug delivery vehicles for cancer therapy. Mol Pharm 2011;8(5):1669-76
25. Lee YT, Woo K, Choi KS. Preparation of water-dispersible and biocompatible iron oxide nanoparticles for MRI agent. IEEE Trans Nanotechol 2008;7(2):111-14
26. Easo SL, Mohanan PV. Dextran stabilized iron oxide nanoparticles: Synthesis, characterization and in vitro studies. Carbohydr Polym 2013;92(1):726-32
27. Rosen JE, Chan L, Shieh DB, Gu FX. Iron oxide nanoparticles for targeted cancer imaging and diagnostics. Nanomedicine 2012;8(3):275-90
28. Lee SJ, Jeong JR, Shin SC, et al. Nanoparticles of magnetic ferric oxides encapsulated with poly (D, L latide-coglycolide) and their applications to magnetic resonance imaging contrast agent. J Magn Magn Mater 2004;272:2432-3
29. Prashant C, Dipak M, Yang CT, et al. Superparamagnetic iron oxide-Loaded poly (lactic acid)-d-A-Tocopherol polyethylene glycol 1000 succinate copolymer nanoparticles as MRI contrast agent. Biomaterials 2010;31(21):5588-97
30. Ai H, Flask C, Weinberg B, et al. Magnetite loaded polymeric micelles as ultrasensitive magnetic resonance probes. Adv Mater 2005;17(16):1949-52
31. Mahmoudi M, Simchi A, Imani M, et al. Optimal design and characterization of superparamagnetic iron oxide nanoparticles coated with polyvinyl alcohol for targeted delivery and imaging. J Phys Chem B 2008;112(46):14470-81
32. Wang Y, Teng X, Wang JS, Yang H. Solvent-free atom transfer radical polymerization in the synthesis of Fe2O3 polystyrene core-shell nanoparticles. Nano Lett 2003;3(6):789-93
33. Lee HY, Lim NH, Seo JA, et al. Preparation and magnetic resonance imaging effect of polyvinylpyrrolidone coated iron oxide nanoparticles. J Biomed Mater Res B Appl Biomater 2006;79(1):142-50
34. Xu Y-Y, Zhou M, Geng H-J, et al. A simplified method for synthesis of Fe3O4 PAA nanoparticles and its application for the removal of basic dyes. Appl Surf Sci 2012;258(8):3897-902
35. McBain S, Yiu H, El Haj A, Dobson J. Polyethyleneimine functionalized iron oxide nanoparticles as agents for DNA delivery and transfection. J Mater Chem 2007;17(24):2561-5
36. Wu W, He Q, Jiang C. Magnetic iron oxide nanoparticles: Synthesis and surface functionalization strategies. Nanoscale Res Lett 2008;3(11):397-415
37. Gomez-Lopera S, Plaza R, Delgado A. Synthesis and characterization of spherical magnetite/biodegradable polymer composite particles. J Colloid Interface Sci 2001;240(1):40-7
38. Schweiger C, Pietzonka C, Heverhagen J, Kissel T. Novel magnetic iron oxide nanoparticles coated with poly (ethylene imine)-g-poly (ethylene glycol) for potential biomedical application: Synthesis, stability, cytotoxicity and MR imaging. Int J Pharm 2011;408(1):130-7
39. Al-Deen FN, Selomulya C, Williams T. On Designing stable magnetic vectors as carriers for malaria DNA vaccine. Colloids Surf B 2013;102:492-503
40. Tombácz E, Szekeres M, Toth IY, et al. Colloidal stability of carboxylated iron oxide nanomagnets for biomedical use. Chem Eng 2014;58:3-10
41. Sun X, Ma P, Cao X, et al. Positive hyaluronan/PEI/DNA complexes as a target-specific intracellular delivery to malignant breast cancer. Drug Deliv 2009;16(7):357-62
42. Hofmann-Amtenbrink M, von Rechenberg B, Hofmann H. Superparamagnetic nanoparticles for biomedical applications. Transworld Research Network, Kerala, India, 2009
43. Viali WR, da Silva Nunes E, dos Santos CC, et al. PEGylation of SPIONs by polycondensation reactions: A new strategy to improve colloidal stability in biological media. J Nanoparticle Res 2013;15(8):1-14
44. Huh YM, Jun YW, Song HT, et al. In vivo magnetic resonance detection of cancer by using multifunctional magnetic nanocrystals. J Am Chem Soc 2005;127(35):12387-91
45. Zhang C, Jugold M, Woenne EC, et al. Specific targeting of tumor angiogenesis by RGD-conjugated ultrasmall superparamagnetic iron oxide particles using a clinical 1.5-T magnetic resonance scanner. Cancer Res 2007;67(4):1555-62
46. Bae YH, Park K. Targeted drug delivery to tumors: Myths, reality and possibility. J Controlled Release 2011;153(3):198
47. Koo YEL, Reddy GR, Bhojani M, et al. Brain cancer diagnosis and therapy with nanoplatforms. Adv Drug Deliv Rev 2006;58(14):1556-77
48. Longmire M, Choyke PL, Kobayashi H. Clearance properties of nano-sized particles and molecules as imaging agents: Considerations and caveats. Nanomedicine 2008;3(5):703-17
49. Choi HS, Liu W, Misra P, et al. Renal clearance of quantum dots. Nat Biotechnol 2007;25(10):1165-70
50. Gupta AK, Gupta M. Synthesis and surface engineering of iron oxide nanoparticles for biomedical applications. Biomaterials 2005;26(18):3995-4021
51. Saito S, Tsugeno M, Koto D, et al. Impact of surface coating and particle size on the uptake of small and ultrasmall superparamagnetic iron oxide nanoparticles by macrophages. Int J Nanomed 2012;7:5415
52. Chouly C, Pouliquen D, Lucet I, et al. Development of superparamagnetic nanoparticles for MRI: Effect of particle size, charge and surface nature on biodistribution. J. Microencapsulation 1996;13(3):245-55
53. Osaka T, Nakanishi T, Shanmugam S, et al. Effect of surface charge of magnetite nanoparticles on their internalization into breast cancer and umbilical vein endothelial cells. Colloids Surf B 2009;71(2):325-30
54. Kenzaoui BH, Vilá MR, Miquel JM, et al. Evaluation of uptake and transport of cationic and anionic ultrasmall iron oxide nanoparticles by human colon cells. Int J Nanomed 2012;7:1275
55. Mahmoudi M, Simchi A, Imani M, HaIfeli UO. Superparamagnetic iron oxide nanoparticles with rigid crosslinked polyethylene glycol fumarate coating for application in imaging and drug delivery. J Phys Chem C 2009;113(19):8124-31
56. Karlsson HL, Cronholm P, Gustafsson J, Moller L. Copper oxide nanoparticles are highly toxic: A comparison between metal oxide nanoparticles and carbon nanotubes. Chem Res Toxicol 2008;21(9):1726-32
57. Ankamwar B, Lai T, Huang J, et al. Biocompatibility of Fe3O4 nanoparticles evaluated by in vitro cytotoxicity assays using normal, glia and breast cancer cells. Nanotechnology 2010;21(7):075102
58. Thoeny HC, Triantafyllou M, Birkhaeuser FD, et al. Combined ultrasmall superparamagnetic particles of iron oxide-enhanced and diffusionweighted magnetic resonance imaging reliably detect pelvic lymph node metastases in normal-sized nodes of bladder and prostate cancer patients. Eur Urol 2009;55(4):761-9
59. Mahmoudi M, Simchi A, Imani M. Cytotoxicity of uncoated and polyvinyl alcohol coated superparamagnetic iron oxide nanoparticles. J Phys Chem C 2009;113(22):9573-80
60. Mahmoudi M, Simchi A, Vali H, et al. Cytotoxicity and cell cycle effects of bare and poly (vinyl alcohol) coated iron oxide nanoparticles in mouse fibroblasts. Adv Eng Mater 2009;11(12):B243-B50
61. Mahmoudi M, Simchi A, Imani M, et al. A new approach for the in vitro identification of the cytotoxicity of superparamagnetic iron oxide nanoparticles. Colloids Surf B 2010;75(1):300-9
62. Mahmoudi M, Laurent S, Shokrgozar MA, Hosseinkhani M. Toxicity evaluations of superparamagnetic iron oxide nanoparticles: Cell visionversus physicochemical properties of nanoparticles. ACS Nano 2011;5(9):7263-76
63. Yang WJ, Lee JH, Hong SC, et al. Difference between toxicities of iron oxide magnetic nanoparticles with various surface-functional groups against human normal fibroblasts and fibrosarcoma cells. Materials 2013;6(10):4689-706
64. Jain TK, Reddy MK, Morales MA, et al. Biodistribution, clearance, and biocompatibility of iron oxide magnetic nanoparticles in rats. Mol Pharm 2008;5(2):316-27
65. Weissleder RA, Stark D, Engelstad B, et al. Superparamagnetic iron oxide: Pharmacokinetics and toxicity. Am J Roentgenol 1989;152(1):167-73
66. Gaasch JA, Lockman PR, Geldenhuys WJ, et al. Brain iron toxicity: Differential responses of astrocytes, neurons, and endothelial cells. Neurochem Res 2007;32(7):1196-208
67. Walczyk D, Bombelli FB, Monopoli MP, et al. What the cell seesin bionanoscience. J Am Chem Soc 2010;132(16):5761-8
68. Mahmoudi M, Lohse SE, Murphy CJ, et al. Variation of protein corona composition of gold nanoparticles following plasmonic heating. Nano Lett 2014;14(1):6-12
69. Krol S, Macrez R, Docagne F, et al. Therapeutic benefits from nanoparticles: The potential significance of nanoscience in Diseases with compromise to the blood brain barrier. Chem Rev 2013;113(3):1877-903
70. Monopoli MP, Walczyk D, Campbell A, et al. Physical- chemical aspects of protein corona: Relevance to in vitro and in vivo biological impacts of nanoparticles. J Am Chem Soc 2011;133(8):2525-34
71. Ghavami M, Saffar S, Emamy BA, et al. Plasma concentration gradient influences the protein corona decoration on nanoparticles. RSC Adv 2013;3(4):1119-26
72. Salvati A, Pitek AS, Monopoli MP, et al. Transferrin-functionalized nanoparticles lose their targeting capabilities when a biomolecule corona adsorbs on the surface. Nat Nanotechnol 2013;8(2):137-43
73. Mirshafiee V, Mahmoudi M, Lou K, et al. Protein corona significantly reduces active targeting yield. Chem Commun 2013;49(25):2557-9
74. Xie J, Xu C, Kohler N, et al. Controlled PEGylation of monodisperse Fe3O4 nanoparticles for reduced non specific uptake by macrophage cells. Adv Mater 2007;19(20):3163-6
75. Ni F, Jiang L, Yang R, et al. Effects of PEG length and iron oxide nanoparticles size on reduced protein adsorption and non-specific uptake by macrophage cells. J Nanosci Nanotechnol 2012;12(3):2094-100
76. Ehrenberg MS, Friedman AE, Finkelstein JN, et al. The influence of protein adsorption on nanoparticle association with cultured endothelial cells. Biomaterials 2009;30(4):603-10
77. Mahmoudi M, Sheibani S, Milani A, et al. Crucial role of protein corona for specific targeting of nanoparticles. Nanomedicine 2014 In press
78. Mahmoudi M, Sheibani S, Milani A, et al. Crucial role of protein corona for specific targeting of nanoparticles. Nanomedicine 2014;In press 78. Amiri H, Bordonali L, Lascialfari A, et al. Protein corona affects the relaxivity and MRI contrast efficiency of magnetic nanoparticles. Nanoscale 2013;5(18):8656-65
79. Mahmoudi M, Shokrgozar MA, Sardari S, et al. Irreversible changes in protein conformation Due to interaction with superparamagnetic iron oxide nanoparticles. Nanoscale 2011;3(3):1127-38
80. Zhang D, Neumann O, Wang H, et al. Gold nanoparticles can induce the formation of protein-based aggregates at physiological pH. Nano Lett 2009;9(2):666-71
81. Gref R, Lück M, Quellec P, et al. Stealthcorona-core nanoparticles surface modified by polyethylene glycol (PEG): Influences of the corona (PEG chain length and surface density) and of the core composition on phagocytic uptake and plasma protein adsorption. Colloids Surf B 2000;18(3):301-13
82. Lee H, Lee E, Kim DK, et al. Antibiofouling polymer-coated superparamagnetic iron oxide nanoparticles as potential magnetic resonance contrast agents for in vivo cancer imaging. J Am Chem Soc 2006;128(22):7383-9
83. García KP, Zarschler K, Barbaro L, et al. Zwitterionic-coated stealthnanoparticles for biomedical applications: Recent advances in countering biomolecular corona formation and uptake by the mononuclear phagocyte system. Small 2014. [Epub ahead of print
84. Ge C, Du J, Zhao L, et al. Binding of blood proteins to carbon nanotubes reduces cytotoxicity. Proc Natl Acad Sci USA 2011;108(41):16968-73
85. Dominguez-Medina S, Blankenburg J, Olson J, et al. Adsorption of a protein monolayer via hydrophobic interactions prevents nanoparticle aggregation under harsh environmental conditions. ACS Sustain Chem Eng 2013;1(7):833-42
86. Kah JCY, Chen J, Zubieta A, Hamad-Schifferli K. Exploiting the protein corona around gold nanorods for loading and triggered release. ACS Nano 2012;6(8):6730-40
87. Cifuentes-Rius A, de Puig H, Kah JCY, et al. Optimizing the properties of the protein corona surrounding nanoparticles for tuning payload release. ACS Nano 2013;7(11):10066-74
88. Caracciolo G, Cardarelli F, Pozzi D, et al. Selective targeting capability acquired with a protein corona adsorbed on the surface of DOTAP/ DNA nanoparticles. ACS Appl Mater Interfaces 2013;5(24):13171-9
89. Nagayama S, Ogawara KI, Fukuoka Y, et al. Time-dependent changes in opsonin amount associated on nanoparticles alter their hepatic uptake characteristics. Int J Pharm 2007;342(1):215-21
90. Ogawara KI, Furumoto K, Nagayama S, et al. Pre-coating with serum albumin reduces receptor-mediated hepatic disposition of polystyrene nanosphere: Implications for rational design of nanoparticles. J Controlled Release 2004;100(3):451-5
91. Kubo T, Sugita T, Shimose S, et al. Targeted delivery of anticancer drugs with intravenously administered magnetic liposomes in osteosarcoma-bearing hamsters. Inter J Oncol 2000;17(2):309-24
92. Widder KJ, Senyei AE, Ranney DF. Magnetically responsive microspheres and other carriers for the biophysical targeting of antitumor agents. Adv Pharmacol Chemother 1979;16:213-71
93. Lübbe AS, Bergemann C, Huhnt W, et al. Preclinical experiences with magnetic drug targeting: Tolerance and efficacy. Cancer Res 1996;56(20):4694-701
94. Lübbe AS, Bergemann C, Riess H, et al. Clinical experiences with magnetic drug targeting: A phase I study with 4¢-epidoxorubicin in 14 patients with advanced solid tumors. Cancer Res 1996;56(20):4686-93
95. Widder KJ, Morris RM, Poore G, et al. Tumor remission in Yoshida sarcomabearing rts by selective targeting of magnetic albumin microspheres containing doxorubicin. Proc Natl Acad Sci USA 1981;78(1):579-81
96. Landfester K, Mailänder V. Nanocapsules with specific targeting and release properties using miniemulsion polymerization. Expert Opin Drug Deliv 2013;10(5):593-609
97. Kong SD, Zhang W, Lee JH, et al. Magnetically vectored nanocapsules for tumor penetration and remotely switchable on-demand drug release. Nano Lett 2010;10(12):5088-92
98. Kong SD, Choi C, Khamwannah J, Jin S. Magnetically vectored delivery of cancer drug using remotely on-off switchable nanocapsules. IEEE Trans Magnet 2013;49(1):349-52
99. Tan H, Wang M, Yang CT, et al. Silica nanocapsules of fluorescent conjugated polymers and superparamagnetic nanocrystals for dual mode cellular imaging. Chem A Eur J 2011;17(24):6696-706
100. Kim TH, Jiang HL, Jere D, et al. Chemical modification of chitosan as a gene carrier in vitro and in vivo. Prog Polym Sci 2007;32(7):726-53
101. Bae KH, Ha YJ, Kim C, et al. Pluronic/ chitosan shell cross-linked nanocapsules encapsulating magnetic nanoparticles. J Biomater Sci Polym Ed 2008;19(12):1571-83
102. Kumar A, Jena PK, Behera S, et al. Multifunctional magnetic nanoparticles for targeted delivery. Nanomedicine 2010;6(1):64-9
103. Zhang J, Misra R. Magnetic drugtargeting carrier encapsulated with thermosensitive smart polymer: Core-shell nanoparticle carrier and drug release response. Acta Biomater 2007;3(6):838-50
104. Purushotham S, Chang P, Rumpel H, et al. Thermoresponsive core-shell magnetic nanoparticles for combined modalities of cancer therapy. Nanotechnology 2009;20(30):305101
105. Yang X, Grailer JJ, Rowland IJ, et al. Multifunctional stable and pH-responsive polymer vesicles formed by heterofunctional triblock copolymer for targeted anticancer drug delivery and ultrasensitive MR imaging. ACS Nano 2010;4(11):6805-17
106. Yang X, Grailer JJ, Rowland IJ, et al. Multifunctional SPIO/DOX-loaded wormlike polymer vesicles for cancer therapy and MR imaging. Biomaterials 2010;31(34):9065-73
107. Wang CH, Kang ST, Yeh CK. Superparamagnetic iron oxide and drug complex-embedded acoustic droplets for ultrasound targeted theranosis. Biomaterials 2013;34(7):1852-61
108. Ketkar-Atre A, Struys T, Dresselaers T, et al. In vivo hepatocyte MR imaging using lactose functionalized magnetoliposomes. Biomaterials 2014;35(3):1015-24
109. Lamanna G, Kueny-Stotz M, Mamlouk-Chaouachi H, et al. Dendronized iron oxide nanoparticles for multimodal imaging. Biomaterials 2011;32(33):8562-73
110. Walter GA, Cahill KS, Huard J, et al. Noninvasive monitoring of stem cell transfer for muscle disorders. Magn Reson Med 2004;51(2):273-7
111. Yallapu MM, Othman SF, Curtis ET, et al. Multi-functional magnetic nanoparticles for magnetic resonance imaging and cancer therapy. Biomaterials 2011;32(7):1890-905
112. Matsuoka F, Shinkai M, Honda H, et al. Hyperthermia using magnetite cationic liposomes for hamster osteosarcoma. Biomagn Res Technol 2004;2(1):3
113. Qiang Y, Antony J, Sharma A, et al. Iron/iron oxide core-shell nanoclusters for biomedical applications. J Nanopart Res 2006;8(3-4):489-96
114. Hua MY, Yang HW, Liu HL, et al. Superhigh-magnetization nanocarrier as a doxorubicin Delivery platform for magnetic targeting therapy. Biomaterials 2011;32(34):8999-9010
115. Rosengart AJ, Kaminski MD. Decorporation of biohazards utilizing nanoscale magnetic carrier systems. Nanofabricat Towards Biomed Appl 2005;343-63
116. Goodwin S, Peterson C, Hoh C, Bittner C. Targeting and retention of magnetic targeted carriers (MTCs) enhancing intra-Arterial chemotherapy. J Magn Magn Mater 1999;194(1):132-9
117. Grief AD, Richardson G. Mathematical modelling of magnetically targeted drug delivery. J Magn Magn Mater 2005;293(1):455-63
118. Takeda SI, Mishima F, Fujimoto S, et al. Development of magnetically targeted drug delivery system using superconducting magnet. J Magn Magn Mater 2007;311(1):367-71
119. Forbes ZG, Yellen BB, Halverson DS, et al. Validation of high gradient magnetic field based drug delivery to magnetizable implants under flow. IEEE Trans Biomed Eng 2008;55(2):643-9
120. Chen H, Ebner AD, Kaminski MD, et al. Analysis of magnetic drug carrier particle capture by a magnetizable intravascular stent-2: Parametric study with multi-wire two-dimensional model. J Magn Magn Mater 2005;293(1):616-32
121. Mahmoudi M, Meng J, Xue X, et al. Interaction of stable colloidal nanoparticles with cellular membranes. Biotechnol Adv 2013. [Epub ahead of print
122. Mahmoudi M, Lohse SE, Murphy CJ, et al. Variation of protein corona composition of gold nanoparticles following plasmonic heating. Nano Lett 2014;14(1):6-12
123. Li H, El-Dakdouki MH, Zhu DC, et al. Synthesis of b-cyclodextrin conjugated superparamagnetic iron oxide nanoparticles for selective binding and detection of cholesterol crystals. Chem Commun 2012;48(28):3385-7
124. Grootendorst DJ, Fratila RM, Visscher M, et al. Intra operative ex vivo photoacoustic nodal staging in a rat model using a clinical superparamagnetic iron oxide nanoparticle dispersion. J Biophotonics 2013;6(6-7):493-504
125. Huang G, Chen H, Dong Y, et al. Superparamagnetic iron oxide nanoparticles: Amplifying ROS stress to improve anticancer drug efficacy. Theranostics 2013;3(2):116
126. Sharifi S, Daghighi S, Motazacker M, et al. Superparamagnetic iron oxide nanoparticles alter expression of obesity and T2D-Associated risk genes in human adipocytes. Sci Rep 2013;3:2173
127. Bhattacharya D, Das M, Mishra D, et al. Folate receptor targeted, carboxymethyl chitosan functionalized iron oxide nanoparticles: A novel ultradispersed nanoconjugates for bimodal imaging. Nanoscale 2011;3(4):1653-62
128. Das M, Mishra D, Maiti T, et al. Bio-functionalization of magnetite nanoparticles using an aminophosphonic acid coupling agent: New, ultradispersed, iron-oxide folate nanoconjugates for cancer-specific targeting. Nanotechnology 2008;19(41):415101
129. Sonvico F, Mornet S, Vasseur S, et al. Folate-conjugated iron oxide nanoparticles for solid tumor targeting as potential specific magnetic hyperthermia mediators: Synthesis, physicochemical characterization, and in vitro experiments. Bioconjug Chem 2005;16(5):1181-8
130. Mahajan S, Koul V, Choudhary V, et al. Preparation and in vitro evaluation of folate-receptor-Targeted SPION-polymer micelle hybrids for MRI contrast enhancement in cancer imaging. Nanotechnology 2013;24(1):015603
131. Zhang L, Gong F, Zhang F, et al. Targeted therapy for human hepatic carcinoma cells using folatefunctionalized polymeric micelles loaded with superparamagnetic iron oxide and sorafenib in vitro. Int J Nanomed 2013;8:1517
132. Kaaki K, HerveÌ-Aubert K, Chiper M, et al. Magnetic nanocarriers of doxorubicin coated with poly (ethylene glycol) and folic acid: Relation between coating structure, surface properties, colloidal stability, and cancer cell targeting. Langmuir 2011;28(2):1496-505
133. Maeng JH, Lee DH, Jung KH, et al. Multifunctional doxorubicin loaded superparamagnetic iron oxide nanoparticles for chemotherapy and magnetic resonance imaging in liver cancer. Biomaterials 2010;31(18):4995-5006
134. Guo M, Que C, Wang C, et al. Multifunctional superparamagnetic nanocarriers with folate-mediated and pH-responsive targeting properties for anticancer drug delivery. Biomaterials 2011;32(1):185-94
135. Lin JJ, Chen JS, Huang SJ, et al. Folic acid-Pluronic F127 magnetic nanoparticle clusters for combined targeting, diagnosis, and therapy applications. Biomaterials 2009;30(28):5114-24
136. Kohler N, Sun C, Wang J, Zhang M. Methotrexate-modified superparamagnetic nanoparticles and their intracellular uptake into human cancer cells. Langmuir 2005;21(19):8858-64
137. Kohler N, Sun C, Fichtenholtz A, et al. Methotrexate immobilized poly (ethylene glycol) magnetic nanoparticles for MR imaging and drug delivery. Small 2006;2(6):785-92
138. Taratula O, Garbuzenko O, Savla R, et al. Multifunctional nanomedicine platform for cancer specific delivery of siRNA by superparamagnetic iron oxide nanoparticles-dendrimer complexes. Curr Drug Deliv 2011;8(1):59-69
139. Leuschner C, Kumar CS, Hansel W, Hormes J. Targeting breast cancer cells and their metastases through luteinizing hormone releasing hormone (LHRH) receptors using magnetic nanoparticles. J Biomed Nanotechol 2005;1(2):229-33
140. Kim DK, Chang JH, Kang YJ. Efficient internalization of peptide-conjugated SPIONs in Dendritic cells for tumor targeting. J Nanosci Nanotechnol 2012;12(7):5191-8
141. Cho H-S, Dong Z, Pauletti GM, et al. Fluorescent, superparamagnetic nanospheres for drug storage, targeting, and imaging: A multifunctional nanocarrier system for cancer diagnosis and treatment. ACS Nano 2010;4(9):5398-404
142. El-Dakdouki MH, Zhu DC, El-Boubbou K, et al. Development of multifunctional hyaluronan-coated nanoparticles for imaging and drug delivery to cancer cells. Biomacromolecules 2012;13(4):1144-51
143. Yu MK, Park J, Jeong YY, et al. Integrin-Targeting thermally cross-linked superparamagnetic iron oxide nanoparticles for combined cancer imaging and drug delivery. Nanotechnology 2010;21(41):415102
144. Wu C, Gong F, Pang P, et al. An RGDmodified MRI-visible polymeric vector for targeted siRNA delivery to hepatocellular carcinoma in nude mice. PLoS One 2013;8(6):e66416
145. Yang X, Hong H, Grailer JJ, et al. cRGD-functionalized, DOX-conjugated, and 64Cu-labeled superparamagnetic iron oxide nanoparticles for targeted anticancer drug delivery and PET/MR imaging. Biomaterials 2011;32(17):4151-60
146. Cavalli S, Carbajo D, Acosta M, et al. Efficient gamma-Amino-proline- derived cell penetrating peptide-superparamagnetic iron oxide nanoparticle conjugates via anilinecatalyzed oxime chemistry as bimodal imaging nanoagents. Chem Commun 2012;48(43):5322-4
147. Sun C, Fang C, Stephen Z, et al. Tumor-Targeted drug delivery and MRI contrast enhancement by chlorotoxin-conjugated iron oxide nanoparticles. Nanomedicine (Lond) 2008;3(4):495-505
148. Veiseh O, Gunn JW, Kievit FM, et al. Inhibition of tumor cell invasion with chlorotoxin bound superparamagnetic nanoparticles. Small 2009;5(2):256-64
149. Veiseh O, Kievit FM, Fang C, et al. Chlorotoxin bound magnetic nanovector tailored for cancer cell targeting, imaging, and siRNA delivery. Biomaterials 2010;31(31):8032-42
150. Kievit FM, Veiseh O, Fang C, et al. Chlorotoxin labeled magnetic nanovectors for targeted gene delivery to glioma. ACS Nano 2010;4(8):4587-94
151. Kumar M, Yigit M, Dai G, et al. Image-guided breast tumor therapy using a small interfering RNA nanodrug. Cancer Res 2010;70(19):7553-61
152. Yu MK, Kim D, Lee IH, et al. Image guided prostate cancer therapy using aptamer functionalized thermally cross linked superparamagnetic iron oxide nanoparticles. Small 2011;7(15):2241-9
153. Wang AZ, Bagalkot V, Vasilliou CC, et al. Superparamagnetic iron oxide nanoparticle-Aptamer bioconjugates for combined prostate cancer imaging and therapy. ChemMedChem 2008;3(9):1311-15
154. Min K, Jo H, Song K, et al. Dual-Aptamer-based delivery vehicle of doxorubicin to both PSMA (+) and PSMA (-) prostate cancers. Biomaterials 2011;32(8):2124-32
155. Chen W, Cao Y, Liu M, et al. Rotavirus capsid surface protein VP4-coated Fe3O4 nanoparticles as a theranostic platform for cellular imaging and drug delivery. Biomaterials 2012;33(31):7895-902
156. Chen G, Chen W, Wu Z, et al. MRI-visible polymeric vector bearing CD3 single chain antibody for gene delivery to T cells for immunosuppression. Biomaterials 2009;30(10):1962-70
157. Yang C, Rait A, Pirollo KF, et al. Nanoimmunoliposome delivery of superparamagnetic iron oxide markedly enhances targeting and uptake in human cancer cells in vitro and in vivo. Nanomedicine 2008;4(4):318-29
158. Jiang W, Xie H, Ghoorah D, et al. Conjugation of functionalized SPIONs with transferrin for targeting and imaging brain glial tumors in rat model. PLoS One 2012;7(5):e37376
159. Liang S, Wang Y, Yu J, et al. Surface modified superparamagnetic iron oxide nanoparticles: As a new carrier for biomagnetically targeted therapy. J Mater Sci Mater Med 2007;18(12):2297-302
160. Zou P, Yu Y, Wang YA, et al. Superparamagnetic iron oxide nanotheranostics for targeted cancer cell imaging and pH-dependent intracellular drug release. Mol Pharm 2010;7(6):1974-84
161. Kievit FM, Stephen ZR, Veiseh O, et al. Targeting of primary breast cancers and metastases in a transgenic mouse model using rationally designed multifunctional SPIONs. ACS Nano 2012;6(3):2591-601
162. Hadjipanayis CG, Machaidze R, Kaluzova M, et al. EGFRvIII antibody-conjugated iron oxide nanoparticles for magnetic resonance imaging-guided convection-enhanced delivery and targeted therapy of glioblastoma. Cancer Res 2010;70(15):6303-12.