Progress in cancer therapy with functionalized Fe₃O₄ nanomaterials

Abstract

Malignant neoplasms represent a significant global health threat. To address the need for accurate diagnosis and effective treatment, research is underway to develop therapeutic nanoplatforms. Iron oxide nanoparticles (NPs), specifically Fe₃O₄ NPs have been extensively studied as potential therapeutic agents for cancer due to their unique properties including magnetic targeting, favorable biocompatibility, high magnetic response sensitivity, prolonged in vivo circulation time, stable performance, and high self-metabolism. Their ability to be integrated with magnetic hyperthermia, photodynamic therapy, and photothermal therapy has resulted in the widespread use of Fe₃O₄ NPs in cancer diagnosis and treatment, making them a popular choice for such applications. Various methods can be employed to synthesize magnetic Fe₃O₄ NPs, which can then be surface-modified with biocompatible materials or active targeting molecules. Multifunctional systems can be created by combining Fe₃O₄ NPs with polymers. By combining various therapeutic approaches, more effective biomedical materials can be developed. This paper discusses the synthesis of Fe₃O₄ NPs and the latest research advances in Fe₃O₄-based nanotherapeutic platforms, as well as their applications in the biomedical field.

Graphical abstract

Keywords

Fe₃O₄ NPs / cancer treatment / magnetic targeting / magnetic thermotherapy

References

[1] Siegel R L, Miller K D, Jemal A . Cancer statistics, 2020.CA: A Cancer Journal for Clinicians, 2020, 70(1): 7–30

[2] Veiseh O, Gunn J W, Zhang M . Design and fabrication of magnetic nanoparticles for targeted drug delivery and imaging.Advanced Drug Delivery Reviews, 2010, 62(3): 284–304

[3] Xie J, Liu G, Eden H S, . Surface-engineered magnetic nanoparticle platforms for cancer imaging and therapy.Accounts of Chemical Research, 2011, 44(10): 883–892

[4] Zhu K, Ju Y, Xu J, . Magnetic nanomaterials: chemical design, synthesis, and potential applications.Accounts of Chemical Research, 2018, 51(2): 404–413

[5] Zhou Z, Yang L, Gao J, . Structure–relaxivity relationships of magnetic nanoparticles for magnetic resonance imaging.Advanced Materials, 2019, 31(8): 1804567

[6] Xu C, Sun S . New forms of superparamagnetic nanoparticles for biomedical applications.Advanced Drug Delivery Reviews, 2013, 65(5): 732–743

[7] Qian X, Han X, Yu L, . Manganese-based functional nanoplatforms: nanosynthetic construction, physiochemical property, and theranostic applicability.Advanced Functional Materials, 2020, 30(3): 1907066

[8] Cardoso V F, Francesko A, Ribeiro C, . Advances in magnetic nanoparticles for biomedical applications.Advanced Healthcare Materials, 2018, 7(5): 1700845

[9] Babaei M, Ganjalikhani M . The potential effectiveness of nanoparticles as radio sensitizers for radiotherapy.BioImpacts, 2014, 4(1): 15–20

[10] Salunkhe A B, Khot V M, Pawar S H . Magnetic hyperthermia with magnetic nanoparticles: a status review.Current Topics in Medicinal Chemistry, 2014, 14(5): 572–594

[11] Klein S, Sommer A, Distel L V R, . Superparamagnetic iron oxide nanoparticles as radiosensitizer via enhanced reactive oxygen species formation.Biochemical and Biophysical Research Communications, 2012, 425(2): 393–397

[12] Lee N, Yoo D, Ling D, . Iron oxide based nanoparticles for multimodal imaging and magnetoresponsive therapy.Chemical Reviews, 2015, 115(19): 10637–10689

[13] Qin M, Xu M, Niu L, . Multifunctional modification of Fe₃O₄ nanoparticles for diagnosis and treatment of diseases: a review.Frontiers of Materials Science, 2021, 15(1): 36–53

[14] Muthiah M, Park I K, Cho C S . Surface modification of iron oxide nanoparticles by biocompatible polymers for tissue imaging and targeting.Biotechnology Advances, 2013, 31(8): 1224–1236

[15] Barrow M, Taylor A, Murray P, . Design considerations for the synthesis of polymer coated iron oxide nanoparticles for stem cell labelling and tracking using MRI.Chemical Society Reviews, 2015, 44(19): 6733–6748

[16] Hou Z, Liu Y, Xu J, . Surface engineering of magnetic iron oxide nanoparticles by polymer grafting: synthesis progress and biomedical applications.Nanoscale, 2020, 12(28): 14957–14975

[17] McNamara K, Tofail S A M . Nanoparticles in biomedical applications.Advances in Physics: X, 2017, 2(1): 54–88

[18] Mylkie K, Nowak P, Rybczynski P, . Polymer-coated magnetite nanoparticles for protein immobilization.Materials, 2021, 14(2): 248

[19] Campos I, Espindola A, Chagas C, . Biocompatible superparamagnetic nanoparticles with ibuprofen as potential drug carriers.SN Applied Sciences, 2020, 2(3): 456

[20] Zhang L, Xu H, Cheng Z, . Human cancer cell membrane-cloaked Fe₃O₄ nanocubes for homologous targeting improvement.The Journal of Physical Chemistry B, 2021, 125(27): 7417–7426

[21] Foroughi F, Hassanzadeh-Tabrizi S A, Bigham A . In situ microemulsion synthesis of hydroxyapatite–MgFe₂O₄ nanocomposite as a magnetic drug delivery system.Materials Science and Engineering C, 2016, 68: 774–779

[22] Stojanović Z, Otoničar M, Lee J, . The solvothermal synthesis of magnetic iron oxide nanocrystals and the preparation of hybrid poly(L-lactide)-polyethyleneimine magnetic particles.Colloids and Surfaces B: Biointerfaces, 2013, 109: 236–243

[23] Wu W, He Q, Jiang C . Magnetic iron oxide nanoparticles: synthesis and surface functionalization strategies.Nanoscale Research Letters, 2008, 3(11): 397–415

[24] 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

[25] Xu C, Xu K, Gu H, . Dopamine as a robust anchor to immobilize functional molecules on the iron oxide shell of magnetic nanoparticles.Journal of the American Chemical Society, 2004, 126(32): 9938–9939

[26] Gillich T, Acikgöz C, Isa L, . PEG-stabilized core–shell nanoparticles: impact of linear versus dendritic polymer shell architecture on colloidal properties and the reversibility of temperature-induced aggregation.ACS Nano, 2013, 7(1): 316–329

[27] Zhang T, Wang L, He X, . Cytocompatibility of pH-sensitive, chitosan-coated Fe₃O₄ nanoparticles in gynecological cells.Frontiers in Medicine, 2022, 9: 799145

[28] de Oliveira P N, Moussa A, Milhau N, . In situ synthesis of Fe₃O₄ nanoparticles coated by chito-oligosaccharides: physicochemical characterizations and cytotoxicity evaluation for biomedical applications.Nanotechnology, 2020, 31(17): 175602

[29] Haume K, Rosa S, Grellet S, . Gold nanoparticles for cancer radiotherapy: a review.Cancer Nanotechnology, 2016, 7(1): 8

[30] Anuje M, Pawaskar P N, Khot V, . Synthesis, characterization, and cytotoxicity evaluation of polyethylene glycol-coated iron oxide nanoparticles for radiotherapy application.Journal of Medical Physics, 2021, 46(3): 154–161

[31] Lin L, Li H, Su S, . Study on the structure and properties of Fe₃O₄@HMPDA@HA magnetic hollow mesoporous submicron drug-carrying system.Microporous and Mesoporous Materials, 2022, 330: 111582

[32] Wang Y, Ma S, Liu X, . Hyaluronic acid mediated Fe₃O₄ nanocubes reversing the EMT through targeted cancer stem cell.Colloids and Surfaces B: Biointerfaces, 2023, 222: 113071

[33] Liang Z, Wang Y, Wang J, . Multifunctional Fe₃O₄-PEI@HA nanoparticles in the ferroptosis treatment of hepatocellular carcinoma through modulating reactive oxygen species.Colloids and Surfaces B: Biointerfaces, 2023, 227: 113358

[34] Xing R, Zou Q, Yuan C, . Self-assembling endogenous biliverdin as a versatile near-infrared photothermal nanoagent for cancer theranostics.Advanced Materials, 2019, 31(16): 1900822

[35] Li H, Jiang B, Li J . Recent advances in dopamine-based materials constructed via one-pot co-assembly strategy.Advances in Colloid and Interface Science, 2021, 295: 102489

[36] Zhu M, Shi Y, Shan Y, . Recent developments in mesoporous polydopamine-derived nanoplatforms for cancer theranostics.Journal of Nanobiotechnology, 2021, 19(1): 387

[37] Li W, Cao Z, Yu L, . Hierarchical drug release designed Au@PDA-PEG-MTX NPs for targeted delivery to breast cancer with combined photothermal-chemotherapy.Journal of Nanobiotechnology, 2021, 19(1): 143

[38] Chen Y, Su M, Jia L, . Synergistic chemo-photothermal and ferroptosis therapy of polydopamine nanoparticles for esophageal cancer.Nanomedicine, 2022, 17(16): 1115–1130

[39] Zhou X, Yang A, Huang Z, . Enhancement of neurite adhesion, alignment and elongation on conductive polypyrrole-poly(lactide acid) fibers with cell-derived extracellular matrix.Colloids and Surfaces B: Biointerfaces, 2017, 149: 217–225

[40] Liang Y, Mitriashkin A, Lim T T, . Conductive polypyrrole-encapsulated silk fibroin fibers for cardiac tissue engineering.Biomaterials, 2021, 276: 121008

[41] Miar S, Ong J L, Bizios R, . Electrically stimulated tunable drug delivery from polypyrrole-coated polyvinylidene fluoride.Frontiers in Chemistry, 2021, 9: 599631

[42] Yu Z, Tong S, Wang C, . PPy@Fe₃O₄ nanoparticles inhibit the proliferation and metastasis of CRC via suppressing the NF-κB signaling pathway and promoting ferroptosis.Frontiers in Bioengineering and Biotechnology, 2022, 10: 1001994

[43] Huang H, Wang X, Wang W, . Injectable hydrogel for postoperative synergistic photothermal-chemodynamic tumor and anti-infection therapy.Biomaterials, 2022, 280: 121289

[44] Askari M, Afzali Naniz M, Kouhi M, . Recent progress in extrusion 3D bioprinting of hydrogel biomaterials for tissue regeneration: a comprehensive review with focus on advanced fabrication techniques.Biomaterials Science, 2021, 9(3): 535–573

[45] Liang Y, He J, Guo B . Functional hydrogels as wound dressing to enhance wound healing.ACS Nano, 2021, 15(8): 12687–12722

[46] Zhang D, Ouyang Q, Hu Z, . Catechol functionalized chitosan/active peptide microsphere hydrogel for skin wound healing.International Journal of Biological Macromolecules, 2021, 173: 591–606

[47] Tang Q, Lu B, He J, . Exosomes-loaded thermosensitive hydrogels for corneal epithelium and stroma regeneration.Biomaterials, 2022, 280: 121320

[48] Zhang L, Guan X, Xiao X, . Dual-phase injectable thermosensitive hydrogel incorporating Fe₃O₄@PDA with pH and NIR triggered drug release for synergistic tumor therapy.European Polymer Journal, 2022, 176: 111424

[49] Wang X, Niu D, Li P, . Dual-enzyme-loaded multifunctional hybrid nanogel system for pathological responsive ultrasound imaging and T₂-weighted magnetic resonance imaging.ACS Nano, 2015, 9(6): 5646–5656

[50] Abdollahi B B, Ghorbani M, Hamishehkar H, , . Synthesis and characterization of actively HER-2 targeted Fe₃O₄@Au nanoparticles for molecular radiosensitization of breast cancer. BioImpacts, 2022 (in press), doi:10.34172/bi.2022.23682

[51] Nassar M Y, El-Salhy H I, El-Shiwiny W H, . Composite nanoarchitectonics of magnetic silicon dioxide-modified chitosan for doxorubicin delivery and in vitro cytotoxicity assay.Journal of Inorganic and Organometallic Polymers and Materials, 2023, 33(1): 237–253

[52] Chen W, Yi P, Zhang Y, . Composites of aminodextran-coated Fe₃O₄ nanoparticles and graphene oxide for cellular magnetic resonance imaging.ACS Applied Materials & Interfaces, 2011, 3(10): 4085–4091

[53] Katifelis H, Mukha I, Bouziotis P, . Ag/Au bimetallic nanoparticles inhibit tumor growth and prevent metastasis in a mouse model.International Journal of Nanomedicine, 2020, 15: 6019–6032

[54] Yang Y, Li F, Chen J, . Single Au atoms anchored on amino-group-enriched graphitic carbon nitride for photocatalytic CO₂ reduction.ChemSusChem, 2020, 13(8): 1979–1985

[55] Zhang Y, Zhang X, Zhang L, . Green formulation, chemical characterization, and antioxidant, cytotoxicity, and anti-human cervical cancer effects of vanadium nanoparticles: a pre-clinical study.Arabian Journal of Chemistry, 2021, 14(6): 103147

[56] Wang D, Yin F X, Cheng B, . Enhanced photocatalytic activity and mechanism of CeO₂ hollow spheres for tetracycline degradation.Rare Metals, 2021, 40(9): 2369–2380

[57] Mai D N X, Danh L T X, Dang H D M, , . Study on adenosine loading capacity of porous nanosilica for application in drug delivery. Science and Technology Development, 2020, doi:10.32508/stdjns.v5i1.933

[58] Yuk S H, Oh K S, Cho S H, . Glycol chitosan/heparin immobilized iron oxide nanoparticles with a tumor-targeting characteristic for magnetic resonance imaging.Biomacromolecules, 2011, 12(6): 2335–2343

[59] Barinov A, Malcioǧlu O B, Fabris S, . Initial stages of oxidation on graphitic surfaces: photoemission study and density functional theory calculations.The Journal of Physical Chemistry C, 2009, 113(21): 9009–9013

[60] Hu W, Qi Q, Hu H, . Fe₃O₄ liposome for photothermal/chemo-synergistic inhibition of metastatic breast tumor.Colloids and Surfaces A: Physicochemical and Engineering Aspects, 2022, 634: 127921

[61] Rao L, Bu L L, Xu J H, . Red blood cell membrane as a biomimetic nanocoating for prolonged circulation time and reduced accelerated blood clearance.Small, 2015, 11(46): 6225–6236

[62] Bu L L, Rao L, Yu G T, . Cancer stem cell-platelet hybrid membrane-coated magnetic nanoparticles for enhanced photothermal therapy of head and neck squamous cell carcinoma.Advanced Functional Materials, 2019, 29(10): 1807733

[63] Malyutin A G, Cheng H, Sanchez-Felix O R, . Coat protein-dependent behavior of poly(ethylene glycol) tails in iron oxide core virus-like nanoparticles.ACS Applied Materials & Interfaces, 2015, 7(22): 12089–12098

[64] Felfoul O, Mohammadi M, Taherkhani S, . Magneto-aerotactic bacteria deliver drug-containing nanoliposomes to tumour hypoxic regions.Nature Nanotechnology, 2016, 11(11): 941–947

[65] Chen W, Wang Y, Qin M, . Bacteria-driven hypoxia targeting for combined biotherapy and photothermal therapy.ACS Nano, 2018, 12(6): 5995–6005

[66] Miller K D, Nogueira L, Mariotto A B, . Cancer treatment and survivorship statistics, 2019.CA: A Cancer Journal for Clinicians, 2019, 69(5): 363–385

[67] Shi M, Lan S, Zhang C, . Biocompatible zinc gallogermanate persistent luminescent nanoparticles for fast tumor drainage lymph node imaging in vivo.Colloids and Surfaces B: Biointerfaces, 2021, 205: 111887

[68] Hu H, Wang J, Wang H, . Cell-penetrating peptide-based nanovehicles potentiate lymph metastasis targeting and deep penetration for anti-metastasis therapy.Theranostics, 2018, 8(13): 3597–3610

[69] Zhang Y, Tian Z, Zhao X, . Dual-modified bufalin loaded liposomes for enhanced tumor targeting.Colloids and Surfaces A: Physicochemical and Engineering Aspects, 2019, 571: 72–79

[70] Meng T, Jiang R, Wang S, . Stem cell membrane-coated Au–Ag–PDA nanoparticle-guided photothermal acne therapy.Colloids and Surfaces B: Biointerfaces, 2020, 192: 111145

[71] Xu C H, Ye P J, Zhou Y C, . Cell membrane-camouflaged nanoparticles as drug carriers for cancer therapy.Acta Biomaterialia, 2020, 105: 1–14

[72] Wang C, Wu B, Wu Y, . Camouflaging nanoparticles with brain metastatic tumor cell membranes: a new strategy to traverse blood–brain barrier for imaging and therapy of brain tumors.Advanced Functional Materials, 2020, 30(14): 1909369

[73] Fan J X, Peng M Y, Wang H, . Engineered bacterial bioreactor for tumor therapy via fenton-like reaction with localized H₂O₂ generation.Advanced Materials, 2019, 31(16): 1808278

[74] Qin M, Xu M, Huang D, . Iron oxide nanoparticles in the application of magnetic resonance imaging.Progress in Chemistry, 2020, 32(9): 1264–1273

Disclosure of potential conflicts of interests

The authors declare no competing financial interest.

Acknowledgements

This work was supported by the National Natural Science Foundation of China (Grant Nos. 12272253, 82103147, 12202302, 31800684, and 11802197), the Natural Science Foundation of Shanxi Province, China (Grant Nos. 202203021221047, 20210302124007, and 20210302124405), the Shanxi Scholarship Council of China (HGKY2019037), the Shanxi-Zheda Institute of Advanced Materials and Chemical Engineering (2021SX-AT008 and 2021SX-AT009), the Central Guidance on Local Science and Technology Development Fund of Shanxi Province (YDZJSX2021A021), and the Fund Program for the Scientific Activities of Selected Returned Overseas Professionals in Shanxi Province (20220006) is also acknowledged with gratitude.

RIGHTS & PERMISSIONS

2023 Higher Education Press