Multifunctional modification of Fe₃O₄ nanoparticles for diagnosis and treatment of diseases: A review

Abstract

With the rapid improvements in nanomaterials and imaging technology, great progresses have been made in diagnosis and treatment of diseases during the past decades. Fe₃O₄ magnetic nanoparticles (MNPs) with good biocompatibility and superparamagnetic property are usually used as contrast agent for diagnosis of diseases in magnetic resonance imaging (MRI). Currently, the combination of multiple imaging technologies has been considered as new tendency in diagnosis and treatment of diseases, which could enhance the accuracy and reliability of disease diagnosis and provide new strategies for disease treatment. Therefore, novel contrast agents used for multifunctional imaging are urgently needed. Fe₃O₄ MNPs are believed to be a potential candidate for construction of multifunctional platform in diagnosis and treatment of diseases. In recent years, there are a plethora of studies concerning the construction of multifunctional platform presented based on Fe₃O₄ MNPs. In this review, we introduce fabrication methods and modification strategies of Fe₃O₄ MNPs, expecting great improvements for diagnosis and treatment of diseases in the future.

Keywords

Fe₃O₄ MNPs / preparation methods / modification strategy / multifunctional platform

References

[1] Lewinski N, Colvin V, Drezek R. Cytotoxicity of nanoparticles. Small, 2008, 4(1): 26–49

[2] Formoso P, Muzzalupo R, Tavano L, . Nanotechnology for the environment and medicine. Mini-Reviews in Medicinal Chemistry, 2016, 16(8): 668–675

[3] Hoshyar N, Gray S, Han H B, . The effect of nanoparticle size on in vivo pharmacokinetics and cellular interaction. Nanomedicine, 2016, 11(6): 673–692

[4] Farokhzad O C, Langer R. Impact of nanotechnology on drug delivery. ACS Nano, 2009, 3(1): 16–20

[5] Baetke S C, Lammers T, Kiessling F. Applications of nanoparticles for diagnosis and therapy of cancer. The British Journal of Radiology, 2015, 88(1054): 20150207

[6] Gupta J. Nanotechnology applications in medicine and dentistry. Journal of Investigative and Clinical Dentistry, 2011, 2(2): 81–88

[7] Zhang A, Lieber C M. Nano-bioelectronics. Chemical Reviews, 2016, 116(1): 215–257

[8] Angle M R, Cui B, Melosh N A. Nanotechnology and neurophysiology. Current Opinion in Neurobiology, 2015, 32: 132–140

[9] Noy A. Bionanoelectronics. Advanced Materials, 2011, 23(7): 807–820

[10] Guerra F D, Attia M F, Whitehead D C, . Nanotechnology for environmental remediation: Materials and applications. Molecules, 2018, 23(7): 1760

[11] Hu X, Xu J, Wu C, . Ethylenediamine grafted to graphene oxide@Fe₃O₄ for chromium(VI) decontamination: Performance, modelling, and fractional factorial design. PLoS One, 2017, 12(10): e0187166

[12] Ma S, Zhan S, Jia Y, . Superior antibacterial activity of Fe₃O₄–TiO₂ nanosheets under solar light. ACS Applied Materials & Interfaces, 2015, 7(39): 21875–21883

[13] Sadeghi R, Rodriguez R J, Yao Y, . Advances in nanotechnology as they pertain to food and agriculture: Benefits and risks. Annual Review of Food Science and Technology, 2017, 8(1): 467–492

[14] Iavicoli I, Leso V, Beezhold D H, . Nanotechnology in agriculture: Opportunities, toxicological implications, and occupational risks. Toxicology and Applied Pharmacology, 2017, 329: 96–111

[15] Das G, Patra J K, Paramithiotis S, . The sustainability challenge of food and environmental nanotechnology: Current status and imminent perceptions. International Journal of Environmental Research and Public Health, 2019, 16(23): 4848

[16] Rossi M, Passeri D, Sinibaldi A, . Nanotechnology for food packaging and food quality assessment. Advances in Food and Nutrition Research, 2017, 82: 149–204

[17] Wei M, Le W D. The role of nanomaterials in autophagy. Advances in Experimental Medicine and Biology, 2019, 1206: 273–286

[18] Mohammadinejad R, Moosavi M A, Tavakol S, . Necrotic, apoptotic and autophagic cell fates triggered by nanoparticles. Autophagy, 2019, 15(1): 4–33

[19] El-Boubbou K. Magnetic iron oxide nanoparticles as drug carriers: Preparation, conjugation and delivery. Nanomedicine, 2018, 13(8): 929–952

[20] Song C, Sun W, Xiao Y, . Ultrasmall iron oxide nanoparticles: Synthesis, surface modification, assembly, and biomedical applications. Drug Discovery Today, 2019, 24(3): 835–844

[21] Gupta A K, Gupta M. Synthesis and surface engineering of iron oxide nanoparticles for biomedical applications. Biomaterials, 2005, 26(18): 3995–4021

[22] Yuan Y, Ding Z, Qian J, . Casp3/7-instructed intracellular aggregation of Fe₃O₄ nanoparticles enhances T₂ MR imaging of tumor apoptosis. Nano Letters, 2016, 16(4): 2686–2691

[23] Chen Y, Zhou Q, Li X, . Ultrasmall paramagnetic iron oxide nanoprobe targeting epidermal growth factor receptor for in vivo magnetic resonance imaging of hepatocellular carcinoma. Bioconjugate Chemistry, 2017, 28(11): 2794–2803

[24] Huang J, Wang L, Zhong X, . Facile non-hydrothermal synthesis of oligosaccharides coated sub-5 nm magnetic iron oxide nanoparticles with dual MRI contrast enhancement effect. Journal of Materials Chemistry B: Materials for Biology and Medicine, 2014, 2(33): 5344–5351

[25] Martinkova P, Brtnicky M, Kynicky J, . Iron oxide nanoparticles: Innovative tool in cancer diagnosis and therapy. Advanced Healthcare Materials, 2018, 7(5): 1700932

[26] Qiao R, Jia Q, Zeng J, . Magnetic iron oxide nanoparticles and their applications in magnetic resonance imaging. Acta Biophysica Sinica, 2011, 27(4): 272–288 (in Chinese)

[27] Das R, Rinaldi-Montes N, Alonso J, . Boosted hyperthermia therapy by combined ac magnetic and photothermal exposures in Ag/Fe₃O₄ nanoflowers. ACS Applied Materials & Interfaces, 2016, 8(38): 25162–25169

[28] Nielsen O S, Horsman M, Overgaard J. A future for hyperthermia in cancer treatment? European Journal of Cancer, 2001, 37(13): 1587–1589

[29] Vangijzegem T, Stanicki D, Laurent S. Magnetic iron oxide nanoparticles for drug delivery: Applications and characteristics. Expert Opinion on Drug Delivery, 2019, 16(1): 69–78

[30] Tietze R, Zaloga J, Unterweger H, . Magnetic nanoparticle-based drug delivery for cancer therapy. Biochemical and Biophysical Research Communications, 2015, 468(3): 463–470

[31] Hu X, Ma M, Zeng M, . Supercritical carbon dioxide anchored Fe₃O₄ nanoparticles on graphene foam and lithium battery performance. ACS Applied Materials & Interfaces, 2014, 6(24): 22527–22533

[32] Harnchana V, Chaiyachad S, Pimanpang S, . Hierarchical Fe₃O₄-reduced graphene oxide nanocomposite grown on NaCl crystals for triiodide reduction in dye-sensitized solar cells. Scientific Reports, 2019, 9: 1494

[33] Niemiec T, Dudek M, Dziekan N, . The method of coating Fe₃O₄ with carbon nanoparticles to modify biological properties of oxide measured in vitro. Journal of AOAC International, 2017, 100(4): 905–915

[34] Chen S S, Xu H, Xu H J, . A facile ultrasonication assisted method for Fe₃O₄@SiO₂–Ag nanospheres with excellent antibacterial activity. Dalton Transactions, 2015, 44(19): 9140–9148

[35] Jiao Z, Zhang Y, Fan H. Ultrasonic-microwave method in preparation of polypyrrole-coated magnetic particles for vitamin D extraction in milk. Journal of Chromatography A, 2016, 1457: 7–13

[36] Montaseri H, Alipour S, Vakilinezhad M A. Development, evaluation and optimization of superparamagnetite nanoparticles prepared by co-precipitation method. Research in Pharmaceutical Sciences, 2017, 12(4): 274–282

[37] Park J, An K, Hwang Y, . Ultra-large-scale syntheses of monodisperse nanocrystals. Nature Materials, 2004, 3(12): 891–895

[38] Yu X, Cheng G, Zhou M D, . On-demand one-step synthesis of monodisperse functional polymeric microspheres with droplet microfluidics. Langmuir, 2015, 31(13): 3982–3992

[39] Li P, Li L, Zhao Y, . Selective binding and magnetic separation of histidine-tagged proteins using Fe₃O₄/Cu-apatite nanoparticles. Journal of Inorganic Biochemistry, 2016, 156: 49–54

[40] Lu A H, Salabas E L, Schüth F. Magnetic nanoparticles: Synthesis, protection, functionalization, and application. Angewandte Chemie International Edition in English, 2007, 46(8): 1222–1244

[41] Ling D, Lee N, Hyeon T. Chemical synthesis and assembly of uniformly sized iron oxide nanoparticles for medical applications. Accounts of Chemical Research, 2015, 48(5): 1276– 1285

[42] Park J, Kadasala N R, Abouelmagd S A, . Polymer–iron oxide composite nanoparticles for EPR-independent drug delivery. Biomaterials, 2016, 101: 285–295

[43] Syu W J, Huang C C, Hsiao J K, . Co-precipitation synthesis of near-infrared iron oxide nanocrystals on magnetically targeted imaging and photothermal cancer therapy via photoablative protein denature. Nanotheranostics, 2019, 3(3): 236–254

[44] Gan L, Lu Z, Cao D, . Effects of cetyltrimethylammonium bromide on the morphology of green synthesized Fe₃O₄ nanoparticles used to remove phosphate. Materials Science and Engineering C, 2018, 82: 41–45

[45] Wang H, Zhao X, Meng W, . Cetyltrimethylammonium bromide-coated Fe₃O₄ magnetic nanoparticles for analysis of 15 trace polycyclic aromatic hydrocarbons in aquatic environments by ultraperformance, liquid chromatography with fluorescence detection. Analytical Chemistry, 2015, 87(15): 7667–7675

[46] Nosrati H, Salehiabar M, Manjili H K, . Preparation of magnetic albumin nanoparticles via a simple and one-pot desolvation and co-precipitation method for medical and pharmaceutical applications. International Journal of Biological Macromolecules, 2018, 108: 909–915

[47] Anbarasu M, Anandan M, Chinnasamy E, . Synthesis and characterization of polyethylene glycol (PEG) coated Fe₃O₄ nanoparticles by chemical co-precipitation method for biomedical applications. Spectrochimica Acta Part A: Molecular Spectroscopy, 2015, 135: 536–539

[48] Li C. A targeted approach to cancer imaging and therapy. Nature Materials, 2014, 13(2): 110–115

[49] LaGrow A P, Besenhard M O, Hodzic A, . Unravelling the growth mechanism of the co-precipitation of iron oxide nanoparticles with the aid of synchrotron X-ray diffraction in solution. Nanoscale, 2019, 11(14): 6620–6628

[50] Jun Y W, Huh Y M, Choi J S, . Nanoscale size effect of magnetic nanocrystals and their utilization for cancer diagnosis via magnetic resonance imaging. Journal of the American Chemical Society, 2005, 127(16): 5732–5733

[51] Hufschmid R, Arami H, Ferguson R M, . Synthesis of phase-pure and monodisperse iron oxide nanoparticles by thermal decomposition. Nanoscale, 2015, 7(25): 11142–11154

[52] Guo H, Zhang Y, Liang W, . An inorganic magnetic fluorescent nanoprobe with favorable biocompatibility for dual-modality bioimaging and drug delivery. Journal of Inorganic Biochemistry, 2019, 192: 72–81

[53] Effenberger F B, Couto R A, Kiyohara P K, . Economically attractive route for the preparation of high quality magnetic nanoparticles by the thermal decomposition of iron(III) acetylacetonate. Nanotechnology, 2017, 28(11): 115603

[54] Patsula V, Kosinová L, Lovrić M, . Superparamagnetic Fe₃O₄ nanoparticles: synthesis by thermal decomposition of iron(III) glucuronate and application in magnetic resonance imaging. ACS Applied Materials & Interfaces, 2016, 8(11): 7238–7247

[55] Barbosa I A, de Sousa Filho P C, da Silva D L, . Metalloporphyrins immobilized in Fe₃O₄@SiO₂ mesoporous submicrospheres: Reusable biomimetic catalysts for hydrocarbon oxidation. Journal of Colloid and Interface Science, 2016, 469: 296–309

[56] Mumtaz S, Wang S, Hussain S Z, . Dopamine coated Fe₃O₄ nanoparticles as enzyme mimics for the sensitive detection of bacteria. Chemical Communications, 2017, 53(91): 12306–12308

[57] Liu Y, Purich D L, Wu C, . Ionic functionalization of hydrophobic colloidal nanoparticles to form ionic nanoparticles with enzyme like properties. Journal of the American Chemical Society, 2015, 137(47): 14952–14958

[58] Wang X, Zhuang J, Peng Q, . A general strategy for nanocrystal synthesis. Nature, 2005, 437(7055): 121–124

[59] Cai H, An X, Cui J, . Facile hydrothermal synthesis and surface functionalization of polyethyleneimine-coated iron oxide nanoparticles for biomedical applications. ACS Applied Materials & Interfaces, 2013, 5(5): 1722–1731

[60] Bagwe R P, Kanicky J R, Palla B J, . Improved drug delivery using microemulsions: rationale, recent progress, and new horizons. Critical Reviews in Therapeutic Drug Carrier Systems, 2001, 18(1): 77–140

[61] Bai F, Wang D, Huo Z, . A versatile bottom-up assembly approach to colloidal spheres from nanocrystals. Angewandte Chemie International Edition, 2007, 46(35): 6650–6653

[62] Liu Z L, Wang X, Yao K, . Synthesis of magnetite nanoparticles in W/O microemulsion. Journal of Materials Science, 2004, 39(7): 2633–2636

[63] Zhuang L, Zhang W, Zhao Y, . Preparation and characterization of Fe₃O₄ particles with novel nanosheets morphology and magnetochromatic property by a modified solvothermal method. Scientific Reports, 2015, 5(1): 9320

[64] Lastovina T A, Budnyk A P, Kudryavtsev E A, . Solvothermal synthesis of Sm³⁺-doped Fe₃O₄ nanoparticles. Materials Science and Engineering C, 2017, 80: 110–116

[65] Gao L, Tang Y, Wang C, . Highly-efficient amphiphilic magnetic nanocomposites based on a simple sol–gel modification for adsorption of phthalate esters. Journal of Colloid and Interface Science, 2019, 552: 142–152

[66] Zeng Y, Hao R, Xing B, . One-pot synthesis of Fe₃O₄ nanoprisms with controlled electrochemical properties. Chemical Communications, 2010, 46(22): 3920–3922

[67] Carenza E, Barceló V, Morancho A, . Rapid synthesis of water-dispersible superparamagnetic iron oxide nanoparticles by a microwave-assisted route for safe labeling of endothelial progenitor cells. Acta Biomaterialia, 2014, 10(8): 3775–3785

[68] Shan D, Deng S, Zhao T, . Preparation of ultrafine magnetic biochar and activated carbon for pharmaceutical adsorption and subsequent degradation by ball milling. Journal of Hazardous Materials, 2016, 305: 156–163

[69] Chang M, Chang Y J, Chao P Y, . Exosome purification based on PEG-coated Fe₃O₄ nanoparticles. PLoS One, 2018, 13(6): e0199438

[70] Shahabadi N, Falsafi M, Mansouri K. Improving antiproliferative effect of the anticancer drug cytarabine on human promyelocytic leukemia cells by coating on Fe₃O₄@SiO₂ nanoparticles. Colloids and Surfaces B: Biointerfaces, 2016, 141: 213–222

[71] Achilli C, Grandi S, Guidetti G F, . Fe₃O₄@SiO₂ core–shell nanoparticles for biomedical purposes: Adverse effects on blood cells. Biomaterials Science, 2016, 4(10): 1417–1421

[72] Wei Y, Yin G, Ma C, . Synthesis and cellular compatibility of biomineralized Fe₃O₄ nanoparticles in tumor cells targeting peptides. Colloids and Surfaces B: Biointerfaces, 2013, 107: 180–188

[73] Wang G, Gao W, Zhang X, . Au nanocage functionalized with ultra-small Fe₃O₄ nanoparticles for targeting T₁–T₂ dual MRI and CT imaging of tumor. Scientific Reports, 2016, 6: 28258

[74] Felber M, Alberto R. 99mTc radiolabelling of Fe₃O₄–Au core–shell and Au–Fe₃O₄ dumbbell-like nanoparticles. Nanoscale, 2015, 7(15): 6653–6660

[75] Gou M, Li S, Zhang L, . Facile one-pot synthesis of carbon/calcium phosphate/Fe₃O₄ composite nanoparticles for simultaneous imaging and pH/NIR-responsive drug delivery. Chemical Communications, 2016, 52(74): 11068–11071

[76] Shen S, Ding B, Zhang S, . Near-infrared light-responsive nanoparticles with thermosensitive yolk–shell structure for multimodal imaging and chemo-photothermal therapy of tumor. Nanomedicine, 2017, 13(5): 1607–1616

[77] Nayak S, Lyon L A. Soft nanotechnology with soft nanoparticles. Angewandte Chemie International Edition, 2005, 44(47): 7686–7708

[78] Tang Z, Zhao X, Zhao T, . Magnetic nanoparticles interaction with humic acid: In the presence of surfactants. Environmental Science & Technology, 2016, 50(16): 8640– 8648

[79] Dutta B, Shetake N G, Barick B K, . pH sensitive surfactant-stabilized Fe₃O₄ magnetic nanocarriers for dual drug delivery. Colloids and Surfaces B: Biointerfaces, 2018, 162: 163–171

[80] Justin C, Samrot A V, Sruthi D P, . Preparation, characterization and utilization of core/shell super paramagnetic iron oxide nanoparticles for curcumin delivery. PLoS One, 2018, 13(7): e0200440

[81] Can H K, Kavlak S, ParviziKhosroshahi S, . Preparation, characterization and dynamical mechanical properties of dextran-coated iron oxide nanoparticles (DIONPs). Artificial Cells Nanomedicine and Biotechnology, 2018, 46(2): 421–431

[82] Barrow M, Taylor A, Carrión J C, . Co-precipitation of DEAE-dextran coated SPIONs: How synthesis conditions affect particle properties, stem cell labelling and MR contrast. Contrast Media & Molecular Imaging, 2016, 11(5): 362–370

[83] Wu D, Zhu L, Li Y, . Superparamagnetic chitosan nanocomplexes for colorectal tumor-targeted delivery of irinotecan. International Journal of Pharmaceutics, 2020, 584: 119394

[84] Soares P I P, Machado D, Laia C, . Thermal and magnetic properties of chitosan–iron oxide nanoparticles. Carbohydrate Polymers, 2016, 149: 382–390

[85] Zhang X, Wang Y, Yang S. Simultaneous removal of Co(II) and 1-naphthol by core–shell structured Fe₃O₄@cyclodextrin magnetic nanoparticles. Carbohydrate Polymers, 2014, 114: 521–529

[86] Xie J, Huang J, Li X, . Iron oxide nanoparticle platform for biomedical applications. Current Medicinal Chemistry, 2009, 16(10): 1278–1294

[87] Wang F, Li X, Li W, . Dextran coated Fe₃O₄ nanoparticles as a near-infrared laser-driven photothermal agent for efficient ablation of cancer cells in vitro and in vivo. Materials Science and Engineering C, 2018, 90: 46–56

[88] Assa F, Jafarizadeh-Malmiri H, Ajamein H, . Chitosan magnetic nanoparticles for drug delivery systems. Critical Reviews in Biotechnology, 2017, 37(4): 492–509

[89] Xing H, Zhang S, Bu W, . Ultrasmall NaGdF₄ nanodots for efficient MR angiography and atherosclerotic plaque imaging. Advanced Materials, 2014, 26(23): 3867–3872

[90] Gupta A K, Wells S. Surface-modified superparamagnetic nanoparticles for drug delivery: Preparation, characterization, and cytotoxicity studies. IEEE Transactions on Nanobioscience, 2004, 3(1): 66–73

[91] Yang G, Ma W, Zhang B, . The labeling of stem cells by superparamagnetic iron oxide nanoparticles modified with PEG/PVP or PEG/PEI. Materials Science and Engineering C, 2016, 62: 384–390

[92] Chen Y, Zhang F, Wang Q, . The synthesis of LA-Fe₃O₄@PDA-PEG-DOX for photothermal therapy-chemotherapy. Dalton Transactions, 2018, 47(7): 2435–2443

[93] Wang L, Wang M, Zhou B, . PEGylated reduced-graphene oxide hybridized with Fe₃O₄ nanoparticles for cancer photothermal-immunotherapy. Journal of Materials Chemistry B: Materials for Biology and Medicine, 2019, 7(46): 7406–7414

[94] Yang C, Guo W, Cui L, . pH-responsive magnetic core–shell nanocomposites for drug delivery. Langmuir, 2014, 30(32): 9819–9827

[95] Wei H, Insin N, Lee J, . Compact zwitterion-coated iron oxide nanoparticles for biological applications. Nano Letters, 2012, 12(1): 22–25

[96] Liu Y, Chen T, Wu C, . Facile surface functionalization of hydrophobic magnetic nanoparticles. Journal of the American Chemical Society, 2014, 136(36): 12552–12555

[97] Wang J J, Lei K F, Han F. Tumor microenvironment: Recent advances in various cancer treatments. European Review for Medical and Pharmacological Sciences, 2018, 22(12): 3855–3864

[98] Zaimy M A, Saffarzadeh N, Mohammadi A, . New methods in the diagnosis of cancer and gene therapy of cancer based on nanoparticles. Cancer Gene Therapy, 2017, 24(6): 233–243

[99] Li L, Gao F, Jiang W, . Folic acid-conjugated superparamagnetic iron oxide nanoparticles for tumor-targeting MR imaging. Drug Delivery, 2016, 23(5): 1726–1733

[100] Choi H, Choi S R, Zhou R, . Iron oxide nanoparticles as magnetic resonance contrast agent for tumor imaging via folate receptor-targeted delivery. Academic Radiology, 2004, 11(9): 996–1004

[101] Yang J, Luo Y, Xu Y, . Conjugation of iron oxide nanoparticles with RGD-modified dendrimers for targeted tumor MR imaging. ACS Applied Materials & Interfaces, 2015, 7(9): 5420–5428

[102] Luo Y, Yang J, Yan Y, . RGD-functionalized ultrasmall iron oxide nanoparticles for targeted T₁-weighted MR imaging of gliomas. Nanoscale, 2015, 7(34): 14538–14546

[103] Zhang H, Li J, Hu Y, . Folic acid-targeted iron oxide nanoparticles as contrast agents for magnetic resonance imaging of human ovarian cancer. Journal of Ovarian Research, 2016, 9(1): 19

[104] Cui Y, Zhang C, Luo R, . Noninvasive monitoring of early antiangiogenic therapy response in human nasopharyngeal carcinoma xenograft model using MRI with RGD-conjugated ultrasmall superparamagnetic iron oxide nanoparticles. International Journal of Nanomedicine, 2016, 11: 5671–5682

[105] Hirata E, Sahai E. Tumor microenvironment and differential responses to therapy. Cold Spring Harbor Perspectives in Medicine, 2017, 7(7): a026781

[106] Wu T, Dai Y. Tumor microenvironment and therapeutic response. Cancer Letters, 2017, 387: 61–68

[107] Li H, Zhao Y, Jia Y, . Covalently assembled dopamine nanoparticle as an intrinsic photosensitizer and pH-responsive nanocarrier for potential application in anticancer therapy. Chemical Communications, 2019, 55(100): 15057–15060

[108] Li E, Yang Y, Hao G, . Multifunctional magnetic mesoporous silica nanoagents for in vivo enzyme-responsive drug delivery and MR imaging. Nanotheranostics, 2018, 2(3): 233–242

[109] Yang T, Niu D, Chen J, . Biodegradable organosilica magnetic micelles for magnetically targeted MRI and GSH-triggered tumor chemotherapy. Biomaterials Science, 2019, 7(7): 2951–2960

[110] Gao Z, Hou Y, Zeng J, . Tumor microenvironment-triggered aggregation of antiphagocytosis ^99mTc-labeled Fe₃O₄ nanoprobes for enhanced tumor imaging in vivo. Advanced Materials, 2017, 29(24): 1701095

[111] Lu J, Sun J, Li F, . Highly sensitive diagnosis of small hepatocellular carcinoma using pH-responsive iron oxide nanocluster assemblies. Journal of the American Chemical Society, 2018, 140(32): 10071–10074

[112] Ma T, Hou Y, Zeng J, . Dual-ratiometric target-triggered fluorescent probe for simultaneous quantitative visualization of tumor microenvironment protease activity and pH in vivo. Journal of the American Chemical Society, 2018, 140(1): 211–218

[113] Qin M, Peng Y, Xu M, . Uniform Fe₃O₄/Gd₂O₃-DHCA nanocubes for dual-mode magnetic resonance imaging. Beilstein Journal of Nanotechnology, 2020, 11: 1000–1009

[114] Zhou Z, Huang D, Bao J, . A synergistically enhanced T₁–T₂ dual-modal contrast agent. Advanced Materials, 2012, 24(46): 6223–6228

[115] Lu C, Dong P, Pi L, . Hydroxyl-PEG-phosphonic acid-stabilized superparamagnetic manganese oxide-doped iron oxide nanoparticles with synergistic effects for dual-mode MR imaging. Langmuir, 2019, 35(29): 9474–9482

[116] Xu S, Yang F, Zhou X, . Uniform PEGylated PLGA microcapsules with embedded Fe₃O₄ nanoparticles for US/MR dual-modality imaging. ACS Applied Materials & Interfaces, 2015, 7(36): 20460–20468

[117] Cui X, Mathe D, Kovács N, . Synthesis, characterization, and application of core–shell Co_0.16Fe_2.84O₄@NaYF₄(Yb, Er) and Fe₃O₄@NaYF₄(Yb, Tm) nanoparticle as trimodal (MRI, PET/SPECT, and optical) imaging agents. Bioconjugate Chemistry, 2016, 27(2): 319–328

[118] Sánchez A, Ovejero Paredes K, Ruiz-Cabello J, . Hybrid decorated core@shell Janus nanoparticles as a flexible platform for targeted multimodal molecular bioimaging of cancer. ACS Applied Materials & Interfaces, 2018, 10(37): 31032–31043

[119] Cai W, Guo M, Weng X, . Modified green synthesis of Fe₃O₄@SiO₂ nanoparticles for pH responsive drug release. Materials Science and Engineering C, 2020, 112: 110900

[120] Zhang T Y, Li F Y, Xu Q H, . Ferrimagnetic nanochains-based mesenchymal stem cell engineering for highly efficient post-stroke recovery. Advanced Functional Materials, 2019, 29(24): 1900603

[121] Huh Y M, Lee E S, Lee J H, . Hybrid nanoparticles for magnetic resonance imaging of target-specific viral gene delivery. Advanced Materials, 2007, 19(20): 3109–3112

[122] Arriortua O K, Insausti M, Lezama L, . RGD-functionalized Fe₃O₄ nanoparticles for magnetic hyperthermia. Colloids and Surfaces B: Biointerfaces, 2018, 165: 315–324

[123] Xu C, Zheng Y, Gao W, . Magnetic hyperthermia ablation of tumors using injectable Fe₃O₄/calcium phosphate cement. ACS Applied Materials & Interfaces, 2015, 7(25): 13866–13875

[124] Li L, Fu S, Chen C, . Microenvironment-driven bioelimination of magnetoplasmonic nanoassemblies and their multimodal imaging-guided tumor photothermal therapy. ACS Nano, 2016, 10(7): 7094–7105

[125] Liu Y, Yang Z, Huang X, . Glutathione-responsive self-assembled magnetic gold nanowreath for enhanced tumor imaging and imaging-guided photothermal therapy. ACS Nano, 2018, 12(8): 8129–8137

Acknowledgements

This work was supported by the National Natural Science Foundation of China (Grant Nos. 11502158, 11632013 and 11802197). The support of the Shanxi Provincial Key Research and Development Project, China (Grant Nos. 201803D421060, 201903D421064 and 201803D421076), the Natural Science Foundation of Shanxi Province, China (201901D111078 and 201901D111077), and the Shanxi Scholarship Council of China (No. HGKY2019037) are also acknowledged with gratitude.

RIGHTS & PERMISSIONS

2021 Higher Education Press