aAPC: artificial antigen-presenting cell; APTES: 3-aminopropyl-triethoxysilane; CTL: cytotoxic T-lymphocyte; EMF: external magnetic field; MNCs: magnetic nanoclusters; MNP: magnetic nanoparticle; OVA: ovalbumin; PEI: poly(ethylenimine)
Declarations
Acknowledgments
The authors thank Dr. A. Omelyanchik from Research and Educational Centre “Smart Materials and Biomedical Applications”, Immanuel Kant Baltic Federal University for editing the text and fruitful discussion.
Author contributions
IC: Conceptualization, Writing—original draft, Writing—review & editing. PF, IS, and SP: Writing—original draft, Writing—review & editing. KL: Conceptualization, Writing—review & editing. VA and MK: Supervision. All authors read and approved the submitted version.
Conflicts of interest
The authors declare that they have no conflicts of interest.
Bharathala S, Sharma P. Biomedical Applications of Nanoparticles. In: Maurya PK, Singh S, editors. Nanotechnology in Modern Animal Biotechnology: Concepts and Applications. Elsevier; 2019. pp. 113–32.
Materón EM, Miyazaki CM, Carr O, Joshi N, Picciani PHS, Dalmaschio CJ, et al. Magnetic nanoparticles in biomedical applications: A review.Appl Surf Sci Adv. 2021;6:100163. [DOI]
Wu W, Yu X, Sun J, Han Y, Ma Y, Zhang G, et al. Zeolitic Imidazolate Framework (ZIF-8) Decorated Iron Oxide Nanoparticles Loaded Doxorubicin Hydrochloride for Osteosarcoma Treatment - in vitro and in vivo Preclinical Studies.Int J Nanomedicine. 2023;18:7985–99. [DOI] [PubMed] [PMC]
Kandasamy G, Maity D. Inorganic nanocarriers for siRNA delivery for cancer treatments.Biomed Mater. 2024;19. [DOI] [PubMed]
Liu XL, Chen S, Zhang H, Zhou J, Fan HM, Liang XJ. Magnetic Nanomaterials for Advanced Regenerative Medicine: The Promise and Challenges.Adv Mater. 2019;31:e1804922. [DOI] [PubMed]
Thorat ND, Lemine OM, Bohara RA, Omri K, El Mir L, Tofail SA. Superparamagnetic iron oxide nanocargoes for combined cancer thermotherapy and MRI applications.Phys Chem Chem Phys. 2016;18:21331–9. [DOI] [PubMed]
Salvador M, Moyano A, Martínez-García JC, Blanco-López MC, Rivas M. Synthesis of Superparamagnetic Iron Oxide Nanoparticles: SWOT Analysis Towards Their Conjugation to Biomolecules for Molecular Recognition Applications.J Nanosci Nanotechnol. 2019;19:4839–56. [DOI] [PubMed]
Guduri BR, Luyt AS. Structure and mechanical properties of polycarbonate modified clay nanocomposites.J Nanosci Nanotechnol. 2008;8:1880–5. [PubMed]
Socoliuc V, Peddis D, Petrenko VI, Avdeev MV, Susan-Resiga D, Szabó T, et al. Magnetic Nanoparticle Systems for Nanomedicine—A Materials Science Perspective.Magnetochemistry. 2020;6:2. [DOI]
Panina LV, Gurevich A, Beklemisheva A, Omelyanchik A, Levada K, Rodionova V. Spatial Manipulation of Particles and Cells at Micro- and Nanoscale via Magnetic Forces.Cells. 2022;11:950. [DOI] [PubMed] [PMC]
Omelyanchik A, da Silva FG, Gomide G, Kozenkov I, Depeyrot J, Aquino R, et al. Effect of citric acid on the morpho-structural and magnetic properties of ultrasmall iron oxide nanoparticles.J Alloys Compd. 2021;883:160779. [DOI]
Batlle X, Pérez N, Guardia P, Iglesias O, Labarta A, Bartolomé F, et al. Magnetic nanoparticles with bulklike properties.J Appl Phys. 2011;109:07B524. [DOI]
Maldonado ACM, Winkler EL, Raineri M, Córdova AT, Rodríguez LM, Troiani H, et al. Free-Radical Formation by the Peroxidase-Like Catalytic Activity of MFe2O4 (M = Fe, Ni, and Mn) Nanoparticles.J Phys Chem. 2019;123:20617–27. [DOI]
Frison R, Cernuto G, Cervellino A, Zaharko O, Colonna GM, Guagliardi A, et al. Magnetite–Maghemite Nanoparticles in the 5–15 nm Range: Correlating the Core–Shell Composition and the Surface Structure to the Magnetic Properties. A Total Scattering Study.Chem Mater. 2013;25:4820–7. [DOI]
Levy M, Luciani N, Alloyeau D, Elgrabli D, Deveaux V, Pechoux C, et al. Long term in vivo biotransformation of iron oxide nanoparticles.Biomaterials. 2011;32:3988–99. [DOI] [PubMed]
Feng Q, Liu Y, Huang J, Chen K, Huang J, Xiao K. Uptake, distribution, clearance, and toxicity of iron oxide nanoparticles with different sizes and coatings.Sci Rep. 2018;8:2082. [DOI] [PubMed] [PMC]
Elbialy NS, Fathy MM, Khalil WM. Preparation and characterization of magnetic gold nanoparticles to be used as doxorubicin nanocarriers.Phys Med. 2014;30:843–8. [DOI] [PubMed]
Andreas K, Georgieva R, Ladwig M, Mueller S, Notter M, Sittinger M, et al. Highly efficient magnetic stem cell labeling with citrate-coated superparamagnetic iron oxide nanoparticles for MRI tracking.Biomaterials. 2012;33:4515–25. [DOI] [PubMed]
Sanz-Ortega L, Rojas JM, Marcos A, Portilla Y, Stein JV, Barber DF. T cells loaded with magnetic nanoparticles are retained in peripheral lymph nodes by the application of a magnetic field.J Nanobiotechnology. 2019;17:14. [DOI] [PubMed] [PMC]
Jin H, Qian Y, Dai Y, Qiao S, Huang C, Lu L, et al. Magnetic Enrichment of Dendritic Cell Vaccine in Lymph Node with Fluorescent-Magnetic Nanoparticles Enhanced Cancer Immunotherapy.Theranostics. 2016;6:2000–14. [DOI] [PubMed] [PMC]
Tukmachev D, Lunov O, Zablotskii V, Dejneka A, Babic M, Syková E, et al. An effective strategy of magnetic stem cell delivery for spinal cord injury therapy.Nanoscale. 2015;7:3954–8. [DOI] [PubMed]
Su H, Mou Y, An Y, Han W, Huang X, Xia G, et al. The migration of synthetic magnetic nanoparticle labeled dendritic cells into lymph nodes with optical imaging.Int J Nanomedicine. 2013;8:3737–44. [DOI] [PubMed] [PMC]
de Chickera SN, Snir J, Willert C, Rohani R, Foley R, Foster PJ, et al. Labelling dendritic cells with SPIO has implications for their subsequent in vivo migration as assessed with cellular MRI.Contrast Media Mol Imaging. 2011;6:314–27. [DOI] [PubMed]
Polyak B, Fishbein I, Chorny M, Alferiev I, Williams D, Yellen B, et al. High field gradient targeting of magnetic nanoparticle-loaded endothelial cells to the surfaces of steel stents.Proc Natl Acad Sci U S A. 2008;105:698–703. [DOI] [PubMed] [PMC]
Sanz-Ortega L, Rojas JM, Barber DF. Improving Tumor Retention of Effector Cells in Adoptive Cell Transfer Therapies by Magnetic Targeting.Pharmaceutics. 2020;12:812. [DOI] [PubMed] [PMC]
Mühlberger M, Janko C, Unterweger H, Friedrich RP, Friedrich B, Band J, et al. Functionalization Of T Lymphocytes With Citrate-Coated Superparamagnetic Iron Oxide Nanoparticles For Magnetically Controlled Immune Therapy.Int J Nanomedicine. 2019;14:8421–32. [DOI] [PubMed] [PMC]
Mühlberger M, Unterweger H, Band J, Lehmann C, Heger L, Dudziak D, et al. Loading of Primary Human T Lymphocytes with Citrate-Coated Superparamagnetic Iron Oxide Nanoparticles Does Not Impair Their Activation after Polyclonal Stimulation.Cells. 2020;9:342. [DOI] [PubMed] [PMC]
Boosz P, Pfister F, Stein R, Friedrich B, Fester L, Band J, et al. Citrate-Coated Superparamagnetic Iron Oxide Nanoparticles Enable a Stable Non-Spilling Loading of T Cells and Their Magnetic Accumulation.Cancers (Basel). 2021;13:4143. [DOI] [PubMed] [PMC]
Pfister F, Dörrie J, Schaft N, Buchele V, Unterweger H, Carnell LR, et al. Human T cells loaded with superparamagnetic iron oxide nanoparticles retain antigen-specific TCR functionality.Front Immunol. 2023;14:1223695. [DOI] [PubMed] [PMC]
Wilhelm S, Tavares AJ, Dai Q, Ohta S, Audet J, Dvorak HF, et al. Analysis of nanoparticle delivery to tumours.Nat Rev Mater. 2016;1:16014. [DOI]
Wu J. The Enhanced Permeability and Retention (EPR) Effect: The Significance of the Concept and Methods to Enhance Its Application.J Pers Med. 2021;11:771. [DOI] [PubMed] [PMC]
Golombek SK, May JN, Theek B, Appold L, Drude N, Kiessling F, et al. Tumor targeting via EPR: Strategies to enhance patient responses.Adv Drug Deliv Rev. 2018;130:17–38. [DOI] [PubMed] [PMC]
Wang X, Hua P, He C, Chen M. Non-apoptotic cell death-based cancer therapy: Molecular mechanism, pharmacological modulators, and nanomedicine.Acta Pharm Sin B. 2022;12:3567–93. [DOI] [PubMed] [PMC]
Nikzamir M, Akbarzadeh A, Panahi Y. An overview on nanoparticles used in biomedicine and their cytotoxicity.J Drug Deliv Sci Technol. 2021;61:102316. [DOI]
Frtús A, Smolková B, Uzhytchak M, Lunova M, Jirsa M, Kubinová Š, et al. Analyzing the mechanisms of iron oxide nanoparticles interactions with cells: A road from failure to success in clinical applications.J Control Release. 2020;328:59–77. [DOI] [PubMed]
Jang ES, Shin JH, Ren G, Park MJ, Cheng K, Chen X, et al. The manipulation of natural killer cells to target tumor sites using magnetic nanoparticles.Biomaterials. 2012;33:5584–92. [DOI] [PubMed] [PMC]
Sanz-Ortega L, Portilla Y, Pérez-Yagüe S, Barber DF. Magnetic targeting of adoptively transferred tumour-specific nanoparticle-loaded CD8+ T cells does not improve their tumour infiltration in a mouse model of cancer but promotes the retention of these cells in tumour-draining lymph nodes.J Nanobiotechnology. 2019;17:87. [DOI] [PubMed] [PMC]
Sanz-Ortega L, Rojas JM, Portilla Y, Pérez-Yagüe S, Barber DF. Magnetic Nanoparticles Attached to the NK Cell Surface for Tumor Targeting in Adoptive Transfer Therapies Does Not Affect Cellular Effector Functions.Front Immunol. 2019;10:2073. [DOI] [PubMed] [PMC]
Zhang Q, Wei W, Wang P, Zuo L, Li F, Xu J, et al. Biomimetic Magnetosomes as Versatile Artificial Antigen-Presenting Cells to Potentiate T-Cell-Based Anticancer Therapy.ACS Nano. 2017;11:10724–32. [DOI] [PubMed]
Zhang F, Zhao LJ, Wang SM, Yang J, Lu GH, Luo NN, et al. Construction of a Biomimetic Magnetosome and Its Application as a SiRNA Carrier for High-Performance Anticancer Therapy.Adv Funct Mater. 2018;28:1703326. [DOI]
Nie W, Wei W, Zuo L, Lv C, Zhang F, Lu GH, et al. Magnetic Nanoclusters Armed with Responsive PD-1 Antibody Synergistically Improved Adoptive T-Cell Therapy for Solid Tumors.ACS Nano. 2019;13:1469–78. [DOI] [PubMed]
Lee JH, Lee K, Moon SH, Lee Y, Park TG, Cheon J. All-in-one target-cell-specific magnetic nanoparticles for simultaneous molecular imaging and siRNA delivery.Angew Chem Int Ed Engl. 2009;48:4174–9. [DOI] [PubMed]
Luo Z, Luo L, Lu Y, Zhu C, Qin B, Jiang M, et al. Dual-binding nanoparticles improve the killing effect of T cells on solid tumor.J Nanobiotechnology. 2022;20:261. [DOI] [PubMed] [PMC]
Hunter AC. Molecular hurdles in polyfectin design and mechanistic background to polycation induced cytotoxicity.Adv Drug Deliv Rev. 2006;58:1523–31. [DOI] [PubMed]
Moghimi SM, Symonds P, Murray JC, Hunter AC, Debska G, Szewczyk A. A two-stage poly(ethylenimine)-mediated cytotoxicity: implications for gene transfer/therapy.Mol Ther. 2005;11:990–5. [DOI] [PubMed]
Hwang YS, So D, Lee M, Yoon J, Reipa V, Tona A, et al. Polyethyleneimine/polyethylene glycol-conjugated gold nanoparticles as nanoscale positive/negative controls in nanotoxicology: testing in frog embryo teratogenesis assay-Xenopus and mammalian tissue culture system.Nanotoxicology. 2023;17:94–115. [DOI] [PubMed] [PMC]
Natarajan A, Chun C, Hickman JJ, Molnar P. Growth and electrophysiological properties of rat embryonic cardiomyocytes on hydroxyl- and carboxyl-modified surfaces.J Biomater Sci Polym Ed. 2008;19:1319–31. [DOI] [PubMed] [PMC]
Puerari RC, Ferrari E, Oscar BV, Simioni C, Ouriques LC, Vicentini DS, et al. Acute and chronic toxicity of amine-functionalized SiO2 nanostructures toward Daphnia magna.Ecotoxicol Environ Saf. 2021;212:111979. [DOI] [PubMed]
Li B, Zhang XY, Yang JZ, Zhang YJ, Li WX, Fan CH, et al. Influence of polyethylene glycol coating on biodistribution and toxicity of nanoscale graphene oxide in mice after intravenous injection.Int J Nanomedicine. 2014;9:4697–707. [DOI] [PubMed] [PMC]
Chen TY, Chen MR, Liu SW, Lin JY, Yang YT, Huang HY, et al. Assessment of Polyethylene Glycol-Coated Gold Nanoparticle Toxicity and Inflammation In Vivo Using NF-κB Reporter Mice.Int J Mol Sci. 2020;21:8158. [DOI] [PubMed] [PMC]
Wenande E, Garvey LH. Immediate-type hypersensitivity to polyethylene glycols: a review.Clin Exp Allergy. 2016;46:907–22. [DOI] [PubMed]
Stone CA Jr, Liu Y, Relling MV, Krantz MS, Pratt AL, Abreo A, et al. Immediate Hypersensitivity to Polyethylene Glycols and Polysorbates: More Common Than We Have Recognized.J Allergy Clin Immunol Pract. 2019;7:1533–40, e8. [DOI] [PubMed] [PMC]
Rocha JMV, de Souza VB, Panunto PC, Nicolosi JS, da Silva EDN, Cadore S, et al. In vitro and in vivo acute toxicity of a novel citrate-coated magnetite nanoparticle.PLoS One. 2022;17:e0277396. [DOI] [PubMed] [PMC]