Abstract
Low-toxic colloidal superparamagnetic iron oxide nanoparticles (SPIONs) for theranostic applications were obtained by microwave-assisted technique. Nanoparticles were synthesized by the hydrothermal method under different conditions. XANES, XRD, and XPS studies support the maghemite (γ-Fe2O3) atomic and electronic structure of the nanoparticles. XANES data analysis reveals that nanoparticles have the structure reminiscent of the macroscopic maghemite. Mossbauer spectroscopy supports the γ-Fe2O3 phase of the nanoparticles and vibration magnetometry study shows that the nanoparticles appear to be superparamagnetic. Nanoparticle shape and size were studied by TEM and DLS methods. It was shown that the nanoparticles do not exceed 20 nm. Also, the nanoparticles are found to be low-toxic and did not have significant effects on the viability of the HeLa cell culture. The obtained nanoparticles generated heat with the highest ILP value of 2.56 nHm2/kg and can be considered potential candidates as heat mediators for local magnetic hyperthermia in oncology.
Graphical abstract
Similar content being viewed by others
References
Atefeh Zarepour AZ, Khosravi A (2017) SPIONs as nano-theranostics agents. Springer
Blanco-Andujar C, Ortega D, Southern P, Pankhurst QA, Thanh NT (2015) High performance multi-core iron oxide nanoparticles for magnetic hyperthermia: microwave synthesis, and the role of core-to-core interactions. Nanoscale 7:1768–1775. https://doi.org/10.1039/c4nr06239f
Bruniaux J, A-V E, Aubrey N, Lakhrif Z, Djemaa SB, Eljack S, Marchais H, Hervé-Aubert K, Chourpa I, David S (2019) Magnetic nanocarriers for the specifc delivery of siRNA: contribution of breast cancer cells active targeting for down-regulation effciency. Int J Pharm https://doi.org/10.1016/j.ijpharm.2019.118572
Chuev MA (2013) On the shape of gammaresonance spectra of ferrimagnetic nanoparticles under conditions of metamagnetism. JETP Lett 98:465–470
Dadfar SM, Roemhild K, Drude NI, von Stillfried S, Knüchel R, Kiessling F, Lammers T (2019) Iron oxide nanoparticles: diagnostic, therapeutic and theranostic applications. Adv Drug Deliv Rev 138:302–325. https://doi.org/10.1016/j.addr.2019.01.005
Daniel Hofmann ST, Bannwarth MB, Messerschmidt C, Glaser S-F, Schild H, Landfester K, Mailander V (2014) Mass spectrometry and imaging analysis of nanoparticle-containing vesicles provide a mechanistic insight into cellular trafficking. ACS Nano 8:10077–10088
Deatsch AE, E BA (2014) Heating efficiency in magnetic nanoparticle hyperthermia. J Magn Magn Mater 354:163–172. https://doi.org/10.1016/j.jmmm.2013.11.006
Della Longa S, Pin S, Cortès R, Soldatov AV, Alpert B (1998) Fe-heme conformations in ferric myoglobin. Biophys J 75:3154–3162
Elena Kuchma SK, Soldatov A (2018) The local atomic structure of colloidal superparamagnetic iron oxide nanoparticles for theranostics in oncology. Biomedicines, 78, https://doi.org/10.3390/biomedicines6030078
Ferraz FS, L JLP, Lacerda SMSN, Procópio MS, Figueiredo AFA, Martins EMN, Guimarães PPG, Ladeira LO, Kitten GT, Dias FF, Domingues RZ, Costa GMJ (2020) Biotechnological approach to induce human fibroblast apoptosis using superparamagnetic iron oxide nanoparticles. J Inorg Biochem 206:111017
Haneda K, M AH (1977) Vacancy ordering in γ-Fe2O3 small particles 22
Hohnholt MC, Dringen R (2013) Uptake and metabolism of iron and iron oxide nanoparticles in brain astrocytes. Biochem Soc Trans 41:1588–1592. https://doi.org/10.1042/BST20130114
Ingle AP, Duran N, Rai M (2014) Bioactivity, mechanism of action, and cytotoxicity of copper-based nanoparticles: a review. Appl Microbiol Biotechnol 98:1001–1009. https://doi.org/10.1007/s00253-013-5422-8
Jafari S, M C, Tavakoli MB, Zarrabi A, Ghazikhanlu Sani K, Afzalipour R (2020) Investigation of combination effect between 6 MV X-ray radiation and polyglycerol coated superparamagnetic iron oxide nanoparticles on U87-MG cancer cells. J Biomed Phys Eng, 1
Joanna Dulińska-Litewka AŁ, Hałubiec P, Szafrański O, Karnas K, Karewicz A (2019) Superparamagnetic iron oxide nanoparticles— current and prospective medical applications. Materials, 12, https://doi.org/10.3390/ma12040617
Justine Wallyn NA, Vandamme TF (2019) Synthesis, principles, and properties of magnetite nanoparticles for in vivo imaging applications—a review. Pharmaceutics, 601, https://doi.org/10.3390/pharmaceutics11110601
Kang MungSoo, J S, Lee DK, Cho HJ (2020) MRI visualization of whole brain macro- and microvascular remodeling in a rat model of ischemic stroke: a pilot study
Kosman DJ (2013) Iron metabolism in aerobes: managing ferric iron hydrolysis and ferrous iron autoxidation. Coord Chem Rev 257:210–217. https://doi.org/10.1016/j.ccr.2012.06.030
Kozakov AT, G KA, Googlev KA, Nikolsky AV, Raevski IP, Smotrakov VG, Eremkin VV (2011) X-ray photoelectron study of the valence state of iron in iron – containing single – crystal (BiFeO3, PbFe1/2Nb1/2O3), and ceramic (BaFe1/2Nb1/2O3) multiferroics. J Electron Spectrosc Relat Phenom 184:16–23
Kuchma EA, Zolotukhin PV, Belanova AA, Soldatov MA, Lastovina TA, Kubrin SP, Nikolsky AV, Mirmikova LI, Soldatov AV (2017) Low toxic maghemite nanoparticles for theranostic applications. Int J Nanomedicine 12:6365–6371. https://doi.org/10.2147/IJN.S140368
Lastovina TA, B AP, Kubrin SP, Soldatov AV (2018) Microwave-assisted synthesis of ultra-small iron oxide nanoparticles for biomedicine. Mendeleev Commun 28:167–169
Laurent S, Bridot J-L, Elst LV, Muller RN (2010) Magnetic iron oxide nanoparticles for biomedical applications. Future Med Chem 2(3):427–449. https://doi.org/10.4155/fmc.09.164
Laurent S, Dutz S, Häfeli UO, Mahmoudi M (2011) Magnetic fluid hyperthermia: focus on superparamagnetic iron oxide nanoparticles. Adv Colloid Interf Sci 166(1–2):8–23. https://doi.org/10.1016/j.cis.2011.04.003
Magnetic nanoparticles: from fabrication to clinical applications CRC Press: Boca Raton, 2012
Marina Llenas SS, Costa PM, Oró-Solé J, Lope-Piedrafita S, Ballesteros B, Al-Jamal KT, Tobias G (2019) Microwave-assisted synthesis of SPION-reduced graphene oxide hybrids for magnetic resonance imaging (MRI). Nanomaterials 9:1364. https://doi.org/10.3390/nano9101364
Matsnev ME, Rusakov VS SpectrRelax: an application for Mössbauer spectra modeling and fitting. 178–185
Menil F (1985) Systematic trends of the 57Fe Mossbauer isomer shifts in (FeOn) and (FeFn) polyhedra. Evidence of a new correlation between the isomer shift and the inductive effect of the competing bond T-X (*Fe) (where X is O or F and T any element with a formal positive charge). J Phys Chem Solids 46:763–789
Moghimi SM, Hunter AC, Murray JC (2005) Nanomedicine: current status and future prospects. FASEB J 19(3):311–330
Namita Saxena ND, Akkireddy S, Singh A, Yadav UCS, Dube CL (2020) Efficient microwave synthesis, functionalisation and biocompatibility studies of SPION based potential nano-drug carriers. Applied Nanoscience, https://doi.org/10.1007/s13204-019-01153-8, 649–660
Nazanin Talebloo MG, Robertson N, Wang P (2019) Magnetic particle imaging: current applications in biomedical research. J Magn Reson Imagine, https://doi.org/10.1002/jmri.26875
Ortega D, A PQ (2013) Magnetic hyperthermia, in nanoscience. Nanostructures through chemistry, vol 1. Royal Society of Chemistry, Cambridge
Perigo EA, Hemery G, Sandre O, Ortega D, Garaio E, Plazaola F, Teran FJ (2015) Fundamentals and advances in magnetic hyperthermia. Appl Phys Rev 2:041302. https://doi.org/10.1063/1.4935688
Pieter Glatzela AJ (2013) X-ray absorption and emission spectroscopy. Walton, D.W.B.D.O.H.R.I., Ed
Roghayyeh Vakili-Ghartavol AAM-B, Vakili-Ghartavol Z, Aiyelabegan HT, Jaafari MR, Rezayat SM, Bidgoli SA (2020) Toxicity assessment of superparamagnetic iron oxide nanoparticles in different tissues. Artificial Cells, Nanomedicine, And Biotechnology 48:443–451
Rongrong Jin LL, Zhu W, Li D, Yang L, Duan J, Cai Z, Nie Y, Zhang Y, Gong Q, Song B, Wen L, Anderson JM, Aia H (2019) Iron oxide nanoparticles promote macrophage autophagy and inflammatory response through activation of toll-like Receptor-4 signaling. Biomaterials 203:20123–20130. https://doi.org/10.1016/j.biomaterials.2019.02.026
Schellenberger EA, Reynolds F, Weissleder R, Josephson L (2004) Surface functionalized nanoparticle library yields probes for apoptotic cells. Chembiochem 5(3):275–279
Seyed Mohammadali Dadfar DC, Darguzyte M, Roemhild K, Varvarà P, Metselaar J, Banala S, Straub M, Güvener N, Engelmann U, Slabu I, Buhl M, van Leusen J, Kögerler P, Hermanns-Sachweh B, Schulz V, Kiessling F, Lammers T (2020) Size-isolation of superparamagnetic iron oxide nanoparticles improves MRI, MPI and hyperthermia performance. J Nanobiotechnol, 18
Soldatov MA, T JG, Kubrin SP, Guda AA, Lastovina TA, Bugaev AL, Rusalev YV, Soldatov AV, Lamberti C (2018) Insight from X ray absorption spectroscopy to octahedral/ tetrahedral site distribution in Sm-doped iron oxide magnetic nanoparticles. J Phys Chem:8543–8552
Soldatov MA, Gottlicher J, Kubrin SP, Guda AA, Lastovina TA, Bugaev AL, Rusalev YV, Soldatov AV, Lamberti C (2018) Insight from X-ray absorption spectroscopy to octahedral/tetrahedral site distribution in Sm-doped iron oxide magnetic nanoparticles. J Phys Chem C 122:8543–8552. https://doi.org/10.1021/acs.jpcc.7b12797
Tao Liu RB, Zhou H, Wang R, Liu J, Zhao Y, Chen C (2020) The effect of size and surface ligands of iron oxide nanoparticles on blood compatibility. RSC Adv 10:7559
Tronc EJ, P J (1996) Dispersions of γ-Fe2O3 nanoparticles. Mossbauer spectroscopic studies of the superparamagnetic relaxation. Mater Sci Forum 235-238:659–668
Vega-Villa KR, Takemoto JK, Yáñez JA, Remsberg CM, Forrest ML, Davies NM (2008) Clinical toxicities of nanocarrier systems. Adv Drug Deliv Rev 60(8):929–938
Viviana Frantellizzi MC, Pontico M, Pani A, Pani R, De Vincentis G. New frontiers in molecular imaging with superparamagnetic iron oxide nanoparticles (SPIONs): efficacy, toxicity, and future applications Nucl Med Mol Imaging
Vogel CF, Charrier JG, Wu D, McFall AS, Li W, Abid A, Kennedy IM, Anastasio C (2016) Physicochemical properties of iron oxide nanoparticles that contribute to cellular ROS-dependent signaling and acellular production of hydroxyl radical. Free Radic Res 50:1153–1164. https://doi.org/10.3109/10715762.2016.1152360
Wang Y, Zi XY, Su J, Zhang HX, Zhang XR, Zhu HY, Li JX, Yin M, Yang F, Hu YP (2012) Cuprous oxide nanoparticles selectively induce apoptosis of tumor cells. Int J Nanomedicine 7:2641–2652. https://doi.org/10.2147/IJN.S31133
Yamashita T, P.H. (2008) Analysis of XPS spectra of Fe2+ and Fe3+ ions in oxide materials. Appl Surf Sci:2441–2449
Yufen Xiao JD Superparamagnetic nanoparticles for biomedical applications. Journal of Materials Chemistry B, https://doi.org/10.1039/c9tb01955c
Zhang ZQ, Song SC (2016) Thermosensitive/superparamagnetic iron oxide nanoparticle-loaded nanocapsule hydrogels for multiple cancer hyperthermia. Biomaterials 106:13–23. https://doi.org/10.1016/j.biomaterials.2016.08.015
Zhao S, Yu X, Qian Y, Chen W, Shen J (2020) Multifunctional magnetic iron oxide nanoparticles: an advanced platform for cancer theranostics. Theranostics 10(14):6278–6309. https://doi.org/10.7150/thno.42564
Zolotukhin P, Kozlova Y, Dovzhik A, Kovalenko K, Kutsyn K, Aleksandrova A, Shkurat T (2013) Oxidative status interactome map: towards novel approaches in experiment planning, data analysis, diagnostics and therapy. Mol BioSyst 9:2085–2096. https://doi.org/10.1039/c3mb70096h
Acknowledgements
The XANES experiments were performed at beamline ID26 of European Synchrotron Radiation Facility (ESRF), Grenoble, France.
Funding
This research was financially supported by the Ministry of Science and Higher Education of the Russian Federation (state assignment in the field of scientific activity, № 0852–2020-0019).
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare no competing interests.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Kuchma, E.A., Zolotukhin, P.V., Belanova, A.A. et al. Effect of synthesis conditions on local atomic structure and properties of low-toxic maghemite nanoparticles for local magnetic hyperthermia in oncology. J Nanopart Res 24, 25 (2022). https://doi.org/10.1007/s11051-021-05393-0
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11051-021-05393-0