Magnetic nanoparticles coated with dimercaptosuccinic acid: development, characterization, and application in biomedicine
Source abstract
Abstract
This review intends to summarize some of the results achieved in the development of magnetic nanoparticles coated with anionic ligands, specifically dimercaptosuccinic acid applied in the biomedical area. We describe synthetic routes used to produce iron oxide-based magnetic nanoparticles, subsequently coated with DMSA as well as functionalization strategies for specific purposes with polymers, antibodies, and cytokines. Finally, we have collected data on biological interactions of DMSA-coated nanoparticles in vitro and in vivo, in particular cell interaction process, pharmacokinetics, and biodistribution in different animal models and their promising applications in drug delivery, NMR imaging, hyperthermia, nanothermometry, magnetic separation, and bioremediation.
Source: openaire · Quality: candidate unverified · Source record ↗
Research context
OpenAlex topics: Nanoparticle-Based Drug Delivery · Characterization and Applications of Magnetic Nanoparticles · Iron oxide chemistry and applications
SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.
References (92)
Show source-provided references
1. Aposhian HV, Aposhian MM (1990) Meso-2,3-Dimercaptosuccinic acid: chemical, pharmacological and toxicological properties of an orally effective metal chelating agent. Annu Rev Pharmacol Toxicol 30:279–30610.1146/annurev.pa.30.040190.001431 ↗
2. Auffan M, Decome L, Rose J, Orsiere T, DeMeo M, Briois V, Chaneac C, Olivi L, Berge-lefranc JL, Botta A et al (2006) In vitro Interactions between DMSA-coated maghemite nanoparticles and human fibroblasts: a physicochemical and cyto-genotoxical study. Environ Sci Technol 40:4367–437310.1021/es060691k ↗
3. Bee A, Bouchami T, Brossel R, Cabuil V, Carpentier M, Fruchart JM, Massart R, Neveu S, Pons JN, Robineau M et al (1990) 9006484 (French Patent)
4. Berry CC (2009) Progress in functionalization of magnetic nanoparticles for applications in biomedicine. J Phys D Appl Phys 42:22400310.1088/0022-3727/42/22/224003 ↗
5. Calero M, Gutierrrez L, Salas G, Luengo Y, Lazaro A, Acedo P, Morales MP, Miranda R, Villanueva A (2013) Efficient and safe internalization of magnetic iron oxide Nanoparticles: two fundamental requirements for biomedical applications. Nanomed Nanotechnol Biol Med 10(4):733–74310.1016/j.nano.2013.11.010 ↗
6. Chaves SB, Lacava LM, Lacava ZGM, Silva O, Pelegrini F, Buske N, Gansau C, Morais PC, Azevedo RB (2002) Light microscopy and magnetic resonance characterization of a DMSA-coated magnetic fluid in mice. IEEE Trans Magn 38:3231–323310.1109/TMAG.2002.802495 ↗
7. Chaves SB, Silva LP, Lacava ZGM, Morais PC, Azevedo RB (2005) Interleukin-1 and interleukin-6 production in mice’s lungs induced by 2, 3 meso-dimercaptosuccinic-coated magnetic nanoparticles. J Appl Phys 97:10Q91510.1063/1.1854531 ↗
8. Chen ZP, Zhang Y, Zhang S, Xia JG, Liu JW, Xu K, Gu N (2008) Preparation and characterization of water-soluble monodisperse magnetic iron oxide nanoparticles via surface double-exchange with DMSA. Colloids Surf A 316:210–21610.1016/j.colsurfa.2007.09.017 ↗
9. Chen W, Cao Y, Liu M, Zhao Q, Huang J, Zhang H, Deng Z, Dai J, Williams DF, Zhang Z (2012) Rotavirus capsid surface protein VP4-coated Fe3O4 nanoparticles as a theranostic platform for cellular imaging and drug delivery. Biomaterials 33:7895–790210.1016/j.biomaterials.2012.07.016 ↗
10. Chouly C, Pouliquen D, Lucet I, Jeune JJ, Jallet P (1996) Development of superparamagnetic nanoparticles for MRI: effect of particle size, charge and surface nature on biodistribution. J Microencapsul 13:245–25510.3109/02652049609026013 ↗
11. Colombo M, Carregal-Romero S, Casula MF, Gutierrez L, Morales MP, Bohm IB, Heverhagen JT, Prosperi D, Parak WJ (2012) Biological applications of magnetic nanoparticles. Chem Soc Rev 41:4306–433410.1039/c2cs15337h ↗
12. da Paz MC, Santos Mde F, Santos CM, da Silva SW, de Souza LB, Lima EC, Silva RC, Lucci CM, Morais PC, Azevedo RB et al (2012) Anti-CEA loaded maghemite nanoparticles as a theragnostic device for colorectal cancer. Int J Nanomed 7:5271–5282
13. delaPresa P, Luengo Y, Multigner M, Costo R, Morales MP, Rivero G, Hernando A (2012) Study of heating efficiency as a function of concentration, size, and applied field in γ-Fe2O3 nanoparticles. J Phys Chem C 116:25602–2561010.1021/jp310771p ↗
14. Estevanato L, Cintra D, Baldini N, Portilho F, Barbosa L, Martins O, Lacava B, Miranda-Vilela AL, Tedesco AC, Bao S et al (2011) Preliminary biocompatibility investigation of magnetic albumin nanosphere designed as a potential versatile drug delivery system. Int J Nanomed 6:1709–171710.2217/nnm.11.62 ↗
15. Farquhar MG (1978) Recovery of surface membrane in anterior pituitary cells. Variations in traffic detected with anionic and cationic ferritin. J Cell Biol 77:R35–R4210.1083/jcb.77.3.R35 ↗
16. Fauconnier N, Pons JN, Roger J, Bee A (1997) Thiolation of maghemite nanoparticles by dimercaptosuccinic acid. J Colloid Interface Sci 194:427–43310.1006/jcis.1997.5125 ↗
17. Ferrari M (2005) Cancer nanotechnology: opportunities and challenges. Nat Rev Cancer 5:161–17110.1038/nrc1566 ↗
18. Flora SJS, Pande M, Mehta A (2003) Beneficial effect of combined administration of some naturally occurring antioxidants (vitamins) and thiol chelators in the treatment of chronic lead intoxication. Chem Biol Interact 145:267–28010.1016/S0009-2797(03)00025-5 ↗
19. Fortin JP, Wilhelm C, Servais J, Ménager C, Bacri JC, Gazeau F (2007) Size-sorted anionic iron oxide nanomagnets as colloidal mediators for magnetic hyperthermia. J Am Chem Soc 129:2628–263510.1021/ja067457e ↗
20. Freitas ERd, Soares PR, Santos RP, Santos RLd, Silva JRd, Porfirio EP, Báo SN, Lima EC, Morais PC, Guillo LA (2008) In vitro biological activities of anionic gamma-Fe2O3 nanoparticles on human melanoma cells. J Nanosci Nanotechnol 8:2385–239110.1166/jnn.2008.275 ↗
21. Galimard A, Safi M, Ould-Moussa N, Montero D, Conjeaud H, Berret JF (2012) Thirty-femtogram detection of iron in mammalian cells. Small 8:2036–204410.1002/smll.201102356 ↗
22. Garcia MP, Parca RM, Chaves SB, Silva LP, Santos AD, Lacava ZGM, Morais PC, Azevedo RB (2005) Morphological analysis of mouse lungs after treatment with magnetite-based magnetic fluid stabilized with DMSA. J Magn Magn Mater 293:277–28210.1016/j.jmmm.2005.02.053 ↗
23. Ge Y, Zhang Y, Xia J, Ma M, He S, Nieb F, Gu N (2009) Effect of surface charge and agglomerate degree of magnetic iron oxide nanoparticles on KB cellular uptake in vitro. Colloids Surf B 73:294–30110.1016/j.colsurfb.2009.05.031 ↗
24. Ge G, Wu H, Xiong F, Zhang Y, Guo Z, Bian Z, Xu J, Gu C, Gu N, Chen X et al (2013) The cytotoxicity evaluation of magnetic iron oxide nanoparticles on human aortic endothelial cells. Nanoscale Res Lett 8:21510.1186/1556-276X-8-215 ↗
25. Geppert M, Hohnholt MC, Thiel K, Nürnberger S, Grunwald I, Rezwan K, Dringen R (2011) Uptake of dimercaptosuccinate-coated magnetic iron oxide nanoparticles by cultured brain astrocytes. Nanotechnology 22:14510110.1088/0957-4484/22/14/145101 ↗
26. Gutiérrez L, Mejías R, Barber DF, Veintemillas-Verdaguer S, Serna CJ, Lázaro FJ, Morales MP (2011) Ac magnetic susceptibility study of in vivo nanoparticle biodistribution. J Phys D 44:25500210.1088/0022-3727/44/25/255002 ↗
27. Gutiérrez L, Mejías R, Lázaro FJ, Serna CJ, Barber DF, Morales MP (2013) Effect of anesthesia on magnetic nanoparticle biodistribution after intravenous injection. IEEE Trans Magn 49:398–40110.1109/TMAG.2012.2221162 ↗
28. Hohnholt MC, Dringen R (2011) Iron-dependent formation of reactive oxygen species and glutathione depletion after accumulation of magnetic iron oxide nanoparticles by oligodendroglial cells. J Nanopart Res 13:6761–677410.1007/s11051-011-0585-7 ↗
29. Hou Y, Liu Y, Chen Z, Gu N, Wang J (2010) Manufacture of IRDye800CW-coupled Fe3O4 nanoparticles and their applications in cell labeling and in vivo imaging. J Nanobiotechnol 8:2510.1186/1477-3155-8-25 ↗
30. Huh YM, Jun YW, Song HT, Kim S, Choi JS, Lee JH, Kim KS, Shin JS, Suh JS, Cheon J (2005) In vivo magnetic resonance detection of cancer by using multifunctional magnetic nanocrystals. J Am Chem Soc 127:12387–1239110.1021/ja052337c ↗
31. Hyeon T, Lee LL, Park J, Chung Y, Na HB (2001) Synthesis of highly crystalline and monodisperse maghemite nanocrystallites without a size-selection process. J Am Chem Soc 123:12798–1280110.1021/ja016812s ↗
32. Ikeda Y, Nagasaki Y (2011) PEGylation technology in nanomedicine. Adv Polym Sci 247:115–14010.1007/12_2011_154 ↗
33. Jun YW, Huh YM, Choi JS, Lee JH, Song HT, Kim S, Yoon S, Kim KS, Shin JS, Suh JS et al (2005) Nanoscale size effect of magnetic nanocrystals and their utilisation for cancer diagnosis via magnetic resonance imaging. J Am Chem Soc 127:5732–573310.1021/ja0422155 ↗
34. Kratz F (2008) Albumin as a drug carrier: design of prodrugs, drug conjugates and nanoparticles. J Control Rel 132:171–18310.1016/j.jconrel.2008.05.010 ↗
35. Lartigue L, Alloyeau D, Kolosnjaj-Tabi J, Javed Y, Guardia P, Riedinger A, Péchoux C, Pellegrino T, Wilhelm C, Gazeau F (2013) Biodegradation of iron oxide nanocubes: high-resolution in situ monitoring. ACS Nano 28:3939–395210.1021/nn305719y ↗
36. Laurent S, Mahmoudi M (2011) Superparamagnetic iron oxide nanoparticles: promises for diagnosis and treatment of cancer. Int J Mol Epidemiol Genet 2:367–390
37. Laurent S, Forge D, Port M, Roch A, Robic C, Elst LV, Muller RN (2008) Magnetic iron oxide nanoparticles: synthesis, stabilization, vectorization, physicochemical characterizations, and biological applications. Chem Rev 108:2064–211010.1021/cr068445e ↗
38. Laurent S, Burtea C, Thirifays C, Hafeli UO, Mahmoudi M (2012) Crucial ignored parameters on nanotoxicology: the importance of toxicity assay modifications and “cell vision”. PLoS One 7:e999710.1371/journal.pone.0029997 ↗
39. Lee J, Kotov NA (2007) Thermometer design at the nanoscale. Nano Today 2:48–5110.1016/S1748-0132(07)70019-1 ↗
40. Lee DC, Smith DK, Heitsch AT, Korgel BA (2007a) Colloidal magnetic nanocrystals: synthesis, properties and applications. Annu Rep Sect C 103:351–402
41. Lee JH, Huh YM, Jun YW, Seo JW, Jang JT, Song HT, Kim S, Cho EJ, Yoon HG, Suh JS et al (2007b) Artificially engineered magnetic nanoparticles for ultra-sensitive molecular imaging. Nat Med 13:95–9910.1038/nm1467 ↗
42. Levy M, Luciani N, Alloyeau D, Elgrabli D, Deveaux V, Pechoux C, Chat S, Wang G, Vats N, Gendron F et al (2011) Long term in vivo biotransformation of iron oxide nanoparticles. Biomaterials 32:3988–399910.1016/j.biomaterials.2011.02.031 ↗
43. Lewinski N, Colvin V, Drezek R (2008) Cytotoxicity of nanoparticles. Small 4:26–4910.1002/smll.200700595 ↗
44. Liu Y, Chen Z, Gu N, Wang J (2011) Effects of DMSA-coated Fe3O4 magnetic nanoparticles on global gene expression of mouse macrophage RAW264.7 cells. Toxicol Lett 205:130–13910.1016/j.toxlet.2011.05.1031 ↗
45. Luengo Y, Nardecchia S, Morales MP, Serrano MC (2013) Different cell responses induced by exposure to maghemite nanoparticles. Nanoscale 5:11428–1143710.1039/c3nr02148c ↗
46. Ma HL, Xu YF, Qi XR, Maitani Y, Nagai T (2008) Superparamagnetic iron oxide nanoparticles stabilized by alginate: pharmacokinetics, tissue distribution, and applications in detecting liver cancers. Int J Pharm 354:217–22610.1016/j.ijpharm.2007.11.036 ↗
47. Mahmoudi M, Simchi A, Imani M, Shokrgozar MA, Milani AS, Hafeli UO, Stroeve P (2010) A new approach for the in vitro identification of the cytotoxicity of superparamagnetic iron oxide nanoparticles. Colloids Surf B 75:300–30910.1016/j.colsurfb.2009.08.044 ↗
48. Markides H, Rotherham M, Haj AJE (2012) Biocompatibility and toxicity of magnetic nanoparticles in regenerative medicine. J Nanomater 2012:1–1110.1155/2012/614094 ↗
49. Massart R (1981) Preparation of aqueous magnetic liquids in alkaline and acidic media Magnetics. IEEE Trans 17:1247–1248
50. Massart R, Roger J, Cabuil V (1995) New trends in chemistry of magnetic colloids: Polar and non polar magnetic fluids, emulsions, capsules and vesicles. Braz J Phys 25:135–141
51. Mateo C, Moreno E, Amour K, Lombardero J, Harris W, Pérez R (1997) Humanization of a mouse monoclonal antibody that blocks the epidermal growth factor receptor: recovery of antagonistic activity. Immunotechnology 3:71–8110.1016/S1380-2933(97)00065-1 ↗
52. Mejias R, Costo R, Roca AG, Arias CF, Veintemillas-Verdaguer S, Gonzalez-Carreno T, del Puerto Morales M, Serna CJ, Manes S, Barber DF (2008) Cytokine adsorption/release on uniform magnetic nanoparticles for localized drug delivery. J Control Release 130:168–17410.1016/j.jconrel.2008.05.028 ↗
53. Mejias R, Perez-Yague S, Gutierrez L, Cabrera LI, Spada R, Acedo P, Serna CJ, Lazaro FJ, Villanueva A, Morales Mdel P et al (2011) Dimercaptosuccinic acid-coated magnetite nanoparticles for magnetically guided in vivo delivery of interferon gamma for cancer immunotherapy. Biomaterials 32:2938–295210.1016/j.biomaterials.2011.01.008 ↗
54. Mejías R, Pérez-Yagüe S, Roca AG, Pérez N, Villanueva A, Cañete M, Mañes S, Ruiz-Cabello J, Benito M, Labarta A et al (2010) Liver and brain imaging through dimercaptosuccinic acid-coated iron oxide nanoparticles. Nanomed Nanotechnol Biol Med 5:397–408
55. Mejías R, Gutiérrez L, Salas G, Pérez-Yagüe S, Zotes TM, Lázaro FJ, Morales MP, Barber DF (2013) Long term biotransformation and toxicity of dimercaptosuccinic acid-coated magnetic nanoparticles support their use in biomedical applications. J Control Release 171:225–23310.1016/j.jconrel.2013.07.019 ↗
56. Monge-Fuentes V, García MP, Tavares MC, Valois CR, Lima EC, Teixeira DS, Morais PC, Tomaz C, Azevedo RB (2011) Biodistribution and biocompatibility of DMSA-stabilized maghemite magnetic nanoparticles in nonhuman primates (Cebus spp.). Nanomed Nanotechnol Biol Med 6:1529–1544
57. Morais PC, Garg VK, Oliveira AC, Silva LP, Azevedo RB, Silva AML, Lima ECD (2001) Synthesis and characterization of size-controlled cobalt-ferrite-based ionic ferrofluids. J Magn Magn Mater 225:37–4010.1016/S0304-8853(00)01225-7 ↗
58. Pande M, Mehta A, Pant BP, Flora SJS (2001) Combined administration of a chelating agent and an antioxidant in the prevention and treatment of acute lead intoxication in rats. Environ Toxicol Pharmacol 9:173–18410.1016/S1382-6689(01)00064-3 ↗
59. Passos SK, de Souza PE, Soares PK, Eid DR, Primo FL, Tedesco AC, Lacava ZG, Morais PC (2013) Quantitative approach to skin field cancerization using a nanoencapsulated photodynamic therapy agent: a pilot study. Clin Cosmet Investig Dermatol 6:51–59
60. Qin J, Li K, Peng C, Li X, Lin J, Ye K, Yang X, Xie Q, Shen Z, Jin Y et al (2013) MRI of iron oxide nanoparticle-labeled ADSCs in a model of hindlimb ischemia. Biomaterials 34:4914–492510.1016/j.biomaterials.2013.03.014 ↗
61. Rahman M, Ahmad MZ, Kazmi I, Akhter S, Kumar Y, Ahmad FJ, Anwar F (2012) Novel approach for the treatment of cancer: theranostic nanomedicine. Pharmacologia 3:371–37610.5567/pharmacologia.2012.371.376 ↗
62. Roca AG, Morales MP, O’Grady K, Serna CJ (2006) Structural and magnetic properties of uniform magnetite nanoparticles prepared by high temperature decomposition of organic precursors. Nanotechnology 17:2783–278810.1088/0957-4484/17/11/010 ↗
63. Roca AG, Costo R, Rebolledo AF, Veintemillas-Verdaguer S, Tartaj P, González-Carreño T, Morales MP, Serna CJ (2009a) Progress in the preparation of magnetic nanoparticles for applications in biomedicine. J Phys D 42:22400210.1088/0022-3727/42/22/224002 ↗
64. Roca AG, Veintemillas-Verdaguer S, Port M, Robic C, Serna CJ, Morales MP (2009b) Effect of nanoparticle and aggregate size on the relaxometric properties of MR contrast agents based on high quality magnetite nanoparticles. J Phys Chem B 113:7033–703910.1021/jp807820s ↗
65. Ruiz A, Salas G, Calero M, Hernández Y, Villanueva A, Herranz F, Veintemillas-Verdaguer S, Martínez E, Barber DF, Morales MP (2013) Short-chain PEG molecules strongly bound to magnetic nanoparticle for MRI long circulating agents. Acta Biomater 9:6421–643010.1016/j.actbio.2012.12.032 ↗
66. Salas G, Casado C, Teran FJ, Miranda R, Serna CJ, Morales MP (2012) Controlled synthesis of uniform magnetite nanocrystals with high-quality properties for biomedical applications. J Mater Chem 22:2106510.1039/c2jm34402e ↗
67. Salas G, Veintemillas-Verdaguer S, Morales MP (2013) Relationship between physico-chemical properties of magnetic fluids and their heating capacity. Int J Hyperth 29:768–77610.3109/02656736.2013.826824 ↗
68. Shan XH, Hu H, Xiong F, Gu N, Geng XD, Zhu W, Lin J, Wang YF (2012) Targeting Glut1-overexpressing MDA-MB-231 cells with 2-deoxy-d-g1ucose modified SPIOs. Eur J Radiol 81:95–9910.1016/j.ejrad.2011.03.013 ↗
69. Shubayev VI, Pisanic TR, Jin S (2009) Magnetic nanoparticles for theragnostics. Adv Drug Deliv Rev 61:467–47710.1016/j.addr.2009.03.007 ↗
70. Si S, Kotal A, Mandal TK, Giri S, Nakamura H, Kohara T (2004) Size-controlled synthesis of magnetite nanoparticles in the presence of polyelectrolytes. Chem Mater 16:3489–349610.1021/cm049205n ↗
71. Silva LP, Kuckelhaus S, Guedes MHA, Lacava ZGM, Tedesco AC, Morais PC, Azevedo RB (2005) Kinetic of magnetic nanoparticles uptake evaluated by morphometry of mice peritoneal cells. J Magn Magn Mater 289:463–46510.1016/j.jmmm.2004.11.130 ↗
72. Simoni AR, Martins OP, Lacava ZG, Azevedo RB, Lima EC, Lacava BM, Morais PC, Tedesco AC (2006) Cell toxicity studies of albumin-based nanosized magnetic beads. J Nanosci Nanotechnol 6:2413–241510.1166/jnn.2006.511 ↗
73. Simoni AR, Garcia MP, Azevedo RB, Chaves SB, Lacava ZGM, Lima ECD, Morais PC, Tedesco AC (2008) Evaluation of the binding properties of maghemite nanoparticle surface-coated with meso-2-3-Dimercaptosuccinic acid to serum albumin. J Nanosci Nanotechnol 8:5813–581710.1166/jnn.2008.245 ↗
74. Singh A, Sahoo SK (2013) Magnetic nanoparticles: a novel platform for cancer theranostics. Drug Discov Today 19:474–48110.1016/j.drudis.2013.10.005 ↗
75. Soler MAG, Lima ECD, Nunes ES, Silva FLR, Oliveira AC, Azevedo RB, Morais PC (2011) Spectroscopic Study of Maghemite Nanoparticles Surface-Grafted with DMSA. J Phys Chem A 115:1003–100810.1021/jp1109916 ↗
76. Sun S, Zeng H (2002) Size-controlled synthesis of magnetite nanoparticles. J Am Chem Soc 124:8204–820510.1021/ja026501x ↗
77. Sun C, Sze R, Zhang M (2006) Folic acid-PEG conjugated superparamagnetic nanoparticles for targeted cellular uptake and detection by MRI. J Biomed Mater Res Part A 78:550–55710.1002/jbm.a.30781 ↗
78. Tang SC, Lo IM (2013) Magnetic nanoparticles: essential factors for sustainable environmental applications. Water Res 47:2613–263210.1016/j.watres.2013.02.039 ↗
79. Tartaj P, Morales MP, Veintemillas-Verdaguer S, González-Carreño T, Serna CJ (2003) The preparation of magnetic nanoparticles for applications in biomedicine. J Phys D 36:R182–R19710.1088/0022-3727/36/13/202 ↗
80. Tartaj P, Morales MP, González-Carreño T, Veintemillas-Verdaguer S, Serna CJ (2011) The iron oxides strike back: from biomedical applications to energy storage devices and photoelectrochemical water splitting. Adv Mater 23:5243–524910.1002/adma.201101368 ↗
81. Villanueva A, Canete M, Roca AG, Calero M, Veintemillas-Verdaguer S, Serna CJ, Morales MP, Miranda R (2009) The influence of surface functionalization on the enhanced internalization of magnetic nanoparticles in cancer cells. Nanotechnology 20:11510310.1088/0957-4484/20/11/115103 ↗
82. Wang R, Billone PS, Mullett WM (2013) Nanomedicine in action: An overview of cancer nanomedicine on the market and in clinical trials. J Nanomater 2013:62968110.1155/2013/629681 ↗
83. Wattendorf U, Merkle HP (2008) PEGylation as a tool for the biomedical engineering of surface modified microparticles. J Pharm Sci 97:4655–466910.1002/jps.21350 ↗
84. Wilhelm C, Gazeau F (2008) Universal cell labelling with anionic magnetic nanoparticles. Biomaterials 29:3161–317410.1016/j.biomaterials.2008.04.016 ↗
85. Wilhelm C, Gazeau F, Bacri JC (2002a) Magnetophoresis and ferromagnetic resonance of magnetically labeled cells. Eur Biophys J 2:118–12510.1007/s00249-001-0200-4 ↗
86. Wilhelm C, Gazeau F, Roger J, Pons JN, Bacri J-C (2002b) Interaction of anionic superparamagnetic nanoparticles with cells: kinetic analyses of membrane adsorption and subsequent internalization. Langmuir 18:8148–815510.1021/la0257337 ↗
87. Wilhelm C, Billotey C, Roger J, Pons JN, Bacri J-C, Gazeau F (2003) Intracellular uptake of anionic superparamagnetic nanoparticles as a function of their surface coating. Biomaterials 24:1001–101110.1016/S0142-9612(02)00440-4 ↗
88. Wu Y, Song M, Xin Z, Zhang X, Zhang Y, Wang C, Li S, Gu N (2011) Ultra-small particles of iron oxide as peroxidase for immunohistochemical detection. Nanotechnology 22:22570310.1088/0957-4484/22/22/225703 ↗
89. Xiong F, Zhu ZY, Xiong C, Hua XQ, Shan XH, Zhang Y, Gu N (2012) Preparation, characterization of 2-deoxy-d-glucose functionalized dimercaptosuccinic acid-coated maghemite nanoparticles for targeting tumor cells. Pharm Res 4:1087–109710.1007/s11095-011-0653-9 ↗
90. Yu S, Chowa GM (2004) Carboxyl group (–CO2H) functionalized ferrimagnetic iron oxide nanoparticles for potential bio-applications. J Mater Chem 14(2781–2782):2786
91. Zhang S, Bian Z, Gu C, Zhang Y, He S, Gu N, Zhang J (2007) Preparation of anti-human cardiac troponin I immunomagnetic nanoparticles and biological activity assays. Colloids Surf B 55:143–14810.1016/j.colsurfb.2006.11.041 ↗
92. Zhong J, Liu W, Du Z, Morais PC, Xiang Q, Xie Q (2012) A noninvasive, remote and precise method for temperature and concentration estimation using magnetic nanoparticles. Nanotechnology 23:07570310.1088/0957-4484/23/7/075703 ↗