In vitro cytotoxicity and hyperthermia studies of superparamagnetic poly(urea-urethane) nanoparticles obtained by miniemulsion polymerization in human erythrocytes and NIH3T3 and HeLa cells

References

• Shokrollahi, H. Contrast Agents for MRI. Mater. Sci. Eng. C 2013, 33, 4485–4497. doi:10.1016/j.msec.2013.07.012.
   PubMed Web of Science ®Google Scholar
• Pour, S. A.; Shaterian, H. R. Design and Characterization of Lisinopril-Loaded Superparamagnetic Nanoparticles as a New Contrast Agent for in Vitro, in Vivo MRI Imaging, Diagnose the Tumors and Drug Delivery System. J. Mater. Sci. Mater. Med. 2017, 28, 1–11.
   PubMed Web of Science ®Google Scholar
• El-Kharrag, R.; Abdel Halim, S. S.; Amin, A.; Greish, Y. E. Synthesis and Characterization of Chitosan-Coated Magnetite Nanoparticles Using a Modified Wet Method for Drug Delivery Applications. Int. J. Polym. Mater. Polym. Biomater. 2019, 68, 73–82. doi:10.1080/00914037.2018.1525725.
   Web of Science ®Google Scholar
• Ulbrich, K.; Holá, K.; Šubr, V.; Bakandritsos, A.; Tuček, J.; Zbořil, R. Targeted Drug Delivery with Polymers and Magnetic Nanoparticles: Covalent and Noncovalent Approaches, Release Control, and Clinical Studies. Chem. Rev. 2016, 116, 5338–5431. doi:10.1021/acs.chemrev.5b00589.
   PubMed Web of Science ®Google Scholar
• Weissleder, R.; Bogdanov, A.; Neuwelt, E. A.; Papisov, M. Long-Circulating Iron Oxides for MR Imaging. Adv. Drug Deliv. Rev. 1995, 16, 321–334. doi:10.1016/0169-409X(95)00033-4.
   Web of Science ®Google Scholar
• Chouly, C.; Pouliquen, D.; Lucet, I.; Jeune, J. J.; Jallet, P. Development of Superparamagnetic Nanoparticles for MRI: Effect of Particle Size, Charge and Surface Nature on Biodistribution. J. Microencapsul. 1996, 13, 245–255. doi:10.3109/02652049609026013.
   PubMed Web of Science ®Google Scholar
• Sakellari, D.; Brintakis, K.; Kostopoulou, A.; Myrovali, E.; Simeonidis, K.; Lappas, A.; Angelakeris, M. Ferrimagnetic Nanocrystal Assemblies as Versatile Magnetic Particle Hyperthermia Mediators. Mater. Sci. Eng. C 2016, 58, 187–193. doi:10.1016/j.msec.2015.08.023.
   PubMed Web of Science ®Google Scholar
• Huang, H. S.; Hainfeld, J. F. Intravenous Magnetic Nanoparticle Cancer Hyperthermia. Int. J. Nanomed. 2013, 8, 2521–2532.
   PubMed Web of Science ®Google Scholar
• Mattos dos Santos, P. C.; Feuser, P. E.; Barreto, P.; Steiner, B. T.; Córneo, S.; Scussel, R.; Viegas, A. d C.; Machado-de-Ávila, R. A.; Sayer, C.; de Araújo, P. H. H. Evaluation of in Vitro Cytotoxicity of Nanoparticles on Erythrocytes, Non-Tumor (NIH3T3), Tumor (HeLa) Cells and Hyperthermia Studies. J. Biomater. Sci. Polym. Ed. 2018, 29, 1935–1948. doi:10.1080/09205063.2018.1564134.
   PubMed Web of Science ®Google Scholar
• Sabale, S.; Jadhav, V.; Khot, V.; Zhu, X.; Xin, M.; Chen, H. Superparamagnetic MFe2O4 (M = Ni, Co, Zn, Mn) Nanoparticles: Synthesis, Characterization, Induction Heating and Cell Viability Studies for Cancer Hyperthermia Applications. J. Mater. Sci. Mater. Med. 2015, 26, 127.
   PubMed Web of Science ®Google Scholar
• Kumar, C.; Mohammad, F. Magnetic Nanomaterials for Hyperthermia-Based Therapy and Controlled Drug Delivery. Adv. Drug Deliv. Rev. 2011, 63, 789–808. doi:10.1016/j.addr.2011.03.008.
   PubMed Web of Science ®Google Scholar
• Landfester, K.; Ram Rez, L. P. Encapsulated Magnetite Particles for Biomedical Application. J. Phys: Condens. Matter. 2003, 15, S1345–S1361. doi:10.1088/0953-8984/15/15/304.
   Web of Science ®Google Scholar
• Landfester, K.; Weiss, C. K. Encapsulation by Miniemulsion Polymerization. Adv. Polym. Sci. 2010, 229, 14–49.
   Web of Science ®Google Scholar
• Thammawong, C.; Sreearunothai, P.; Petchsuk, A.; Tangboriboonrat, P.; Pimpha, N.; Opaprakasit, P. Preparation and Characterizations of Naproxen-Loaded Magnetic Nanoparticles Coated with PLA-g-Chitosan Copolymer. J. Nanoparticle Res. 2012, 14, 1046–1047.
   Web of Science ®Google Scholar
• Shi, F.; Ding, J.; Xiao, C.; Zhuang, X.; He, C.; Chen, L.; Chen, X. Intracellular Microenvironment Responsive PEGylated Polypeptide Nanogels with Ionizable Cores for Efficient Doxorubicin Loading and Triggered Release. J. Mater. Chem. 2012, 22, 14168–14179. doi:10.1039/c2jm32033a.
   Web of Science ®Google Scholar
• Muela, A.; Muñoz, D.; Martín-Rodríguez, R.; Orue, I.; Garaio, E.; Abad Díaz de Cerio, A.; Alonso, J.; García, J. Á.; Fdez-Gubieda, M. L. Optimal Parameters for Hyperthermia Treatment Using Biomineralized Magnetite Nanoparticles: Theoretical and Experimental Approach. J. Phys. Chem. C 2016, 120, 24437–24448. doi:10.1021/acs.jpcc.6b07321.
   Web of Science ®Google Scholar
• Pourjavadi, A.; Mazaheri Tehrani, Z.; Dastanpour, L. Smart Magnetic Self-Assembled Micelle: An Effective Nanocarrier for Thermo-Triggered Paclitaxel Delivery. Int. J. Polym. Mater. Polym. Biomater. 2019, 68, 741–749. doi:10.1080/00914037.2018.1493687.
   Web of Science ®Google Scholar
• Feuser, P. E.; Bubniak, L. D. S.; Silva, M. C. D. S.; Viegas, A. D. C.; Castilho Fernandes, A.; Ricci-Junior, E.; Nele, M.; Tedesco, A. C.; Sayer, C.; de Araújo, P. H. H. Encapsulation of Magnetic Nanoparticles in Poly(Methyl Methacrylate) by Miniemulsion and Evaluation of Hyperthermia in U87MG Cells. Eur. Polym. J. 2015, 68, 355–365. doi:10.1016/j.eurpolymj.2015.04.029.
   Web of Science ®Google Scholar
• Hauser, A. K.; Wydra, R. J.; Stocke, N. A.; Anderson, K. W.; Hilt, J. Z. Magnetic Nanoparticles and Nanocomposites for Remote Controlled Therapies. J. Control. Release 2015, 219, 76–94. doi:10.1016/j.jconrel.2015.09.039.
   PubMed Web of Science ®Google Scholar
• Kumar, A.; Gupta, M. Synthesis and Surface Engineering of Iron Oxide Nanoparticles for Biomedical Applications. Biomaterials 2005, 26, 3995–4021. doi:10.1016/j.biomaterials.2004.10.012.
   PubMed Web of Science ®Google Scholar
• Basel, M. T.; Balivada, S.; Wang, H.; Shrestha, T. B.; Seo, G. M.; Pyle, M.; Abayaweera, G.; Dani, R.; Koper, O. B.; Tamura, M.; et al. Cell-Delivered Magnetic Nanoparticles Caused Hyperthermia-Mediated Increased Survival in a Murine Pancreatic Cancer Model. Int. J. Nanomed. 2012, 7, 297–306. doi:10.2147/IJN.S28344.
   PubMed Web of Science ®Google Scholar
• Yan, K.; Li, P.; Zhu, H.; Zhou, Y.; Ding, J.; Shen, J.; Li, Z.; Xu, Z.; Chu, P. K. Recent Advances in Multifunctional Magnetic Nanoparticles and Applications to Biomedical Diagnosis and Treatment. RSC Adv. 2013, 3, 10598. doi:10.1039/c3ra40348c.
   Web of Science ®Google Scholar
• Meenach, S. A.; Shapiro, J. M.; Hilt, J. Z.; Anderson, K. W. Characterization of PEG-Iron Oxide Hydrogel Nanocomposites for Dual Hyperthermia and Paclitaxel Delivery. J. Biomater. Sci. Polym. Ed. 2013, 24, 1112–1126. doi:10.1080/09205063.2012.741321.
   PubMed Web of Science ®Google Scholar
• Yanase, N.; Noguchi, H.; Asakura, H.; Suzuta, T. Preparation of Magnetic Latex-Particles by Emulsion Polymerization of Styrene in the Presence of a Ferrofluid. J. Appl. Polym. Sci. 1993, 50, 765–776. doi:10.1002/app.1993.070500504.
   Web of Science ®Google Scholar
• Pillai, J. J.; Thulasidasan, A. K. T.; Anto, R. J.; Chithralekha, D. N.; Narayanan, A.; Kumar, G. S. V. Folic Acid Conjugated Cross-Linked Acrylic Polymer (FA-CLAP) Hydrogel for Site Specific Delivery of Hydrophobic Drugs to Cancer Cells. J. Nanobiotechnol. 2014, 12, 1–9.
   PubMed Web of Science ®Google Scholar
• Rodrigues, H.; Peres, A.; Da, A.; Viegas, C.; Romio, A. P.; Kobitskaya, E.; Ziener, U.; Landfester, K.; Sayer, C.; Ara, P. H. H. Encapsulation of Magnetic Nickel Nanoparticles via Inverse Miniemulsion Polymerization. Appl. Polym. Sci. 2013, 129, 1426–1433. doi:10.1002/app.38840.
   Web of Science ®Google Scholar
• Xu, Z. Z.; Wang, C. C.; Yang, W. L.; Deng, Y. H.; Fu, S. K. Encapsulation of Nanosized Magnetic Iron Oxide by Polyacrylamide via Inverse Miniemulsion Polymerization. J. Magn. Magn. Mater. 2004, 277, 136–143. doi:10.1016/j.jmmm.2003.10.018.
   Web of Science ®Google Scholar
• Peres, L. B.; dos Anjos, R. S.; Tappertzhofen, L. C.; Feuser, P. E.; de Araújo, P. H. H.; Landfester, K.; Sayer, C.; Muñoz-Espí, R. pH-Responsive Physically and Chemically Cross-Linked Glutamic-Acid-Based Hydrogels and Nanogels. Eur. Polym. J. 2018, 101, 341–349. doi:10.1016/j.eurpolymj.2018.02.039.
   Web of Science ®Google Scholar
• Staudt, T.; Machado, T. O.; Vogel, N.; Weiss, C. K.; Araujo, P. H. H.; Sayer, C.; Landfester, K. Magnetic Polymer/Nickel Hybrid Nanoparticles via Miniemulsion Polymerization. Macromol. Chem. Phys. 2013, 214, 2213–2222. doi:10.1002/macp.201300329.
   Web of Science ®Google Scholar
• Chiaradia, V.; Valério, A.; Feuser, P. E.; De Oliveira, D.; Araújo, P. H. H.; Sayer, C. Incorporation of Superparamagnetic Nanoparticles into Poly(Urea-Urethane) Nanoparticles by Step Growth Interfacial Polymerization in Miniemulsion. Colloids Surf. A Physicochem. Eng. Asp. 2015, 482, 596–603. doi:10.1016/j.colsurfa.2015.06.035.
   Web of Science ®Google Scholar
• Feuser, P. E.; Arévalo, J. M. C.; Junior, E. L.; Rossi, G. R.; da Silva Trindade, E.; Rocha, M. E. M.; Jacques, A. V.; Ricci-Júnior, E.; Santos-Silva, M. C.; Sayer, C.; de Araújo, P. H. H. Increased Cellular Uptake of Lauryl Gallate Loaded in Superparamagnetic Poly(Methyl Methacrylate) Nanoparticles Due to Surface Modification with Folic Acid. J. Mater. Sci. Mater. Med. 2016, 27, 185. doi:10.1007/s10856-016-5796-0.
   PubMed Web of Science ®Google Scholar
• Asua, J. M. Miniemulsion Polymerization. Prog. Polym. Sci. 2002, 27, 1283–1346. doi:10.1016/S0079-6700(02)00010-2.
   Web of Science ®Google Scholar
• Rocas, P.; Cusco, C.; Rocas, J.; Albericio, F. On the Importance of Polyurethane and Polyurea Nanosystems for Future Drug Delivery. Curr. Drug Deliv. 2018, 15, 37–43. doi:10.2174/1567201814666171019102537.
   PubMed Web of Science ®Google Scholar
• Wang, A.; Gao, H.; Sun, Y.; Sun, Y.; Yang, Y.; Wu, G.; Wang, Y.; Fan, Y.; Ma, J. Temperature- and pH-Responsive Nanoparticles of Biocompatible Polyurethanes for Doxorubicin Delivery. Int. J. Pharm. 2013, 441, 30–39. doi:10.1016/j.ijpharm.2012.12.021.
   PubMed Web of Science ®Google Scholar
• Valério, A.; Feuser, P. E.; Dos Santos Bubniak, L.; Dos Santos-Silva, M. C.; De Araújo, P. H. H.; Sayer, C. In Vitro Biocompatibility and Macrophage Uptake Assays of Poly(Urea-Urethane) Nanoparticles Obtained by Miniemulsion Polymerization. J. Nanosci. Nanotechnol. 2017, 17, 4955–4960. doi:10.1166/jnn.2017.13434.
   Web of Science ®Google Scholar
• Pan, D.; Vargas-Morales, O.; Zern, B.; Anselmo, A. C.; Gupta, V.; Zakrewsky, M.; Mitragotri, S.; Muzykantov, V. The Effect of Polymeric Nanoparticles on Biocompatibility of Carrier Red Blood Cells. PLoS One 2016, 11, 1–17. doi:10.1371/journal.pone.0152074.
   Web of Science ®Google Scholar
• Fornaguera, C.; Calderó, G.; Mitjans, M.; Vinardell, M. P.; Solans, C.; Vauthier, C. Interactions of PLGA Nanoparticles with Blood Components: Protein Adsorption, Coagulation, Activation of the Complement System and Hemolysis Studies. Nanoscale 2015, 7, 6045–6058. doi:10.1039/C5NR00733J.
   PubMed Web of Science ®Google Scholar
• Cho, W. S.; Thielbeer, F.; Duffin, R.; Johansson, E. M. V.; Megson, I. L.; Macnee, W.; Bradley, M.; Donaldson, K. Surface Functionalization Affects the Zeta Potential, Coronal Stability and Membranolytic Activity of Polymeric Nanoparticles. Nanotoxicology 2014, 8, 202–211. doi:10.3109/17435390.2013.773465.
   PubMed Web of Science ®Google Scholar
• Feuser, P. E.; Jacques, A. V.; Arévalo, J. M. C.; Rocha, M. E. M.; dos Santos-Silva, M. C.; Sayer, C.; de Araújo, P. H. H. Superparamagnetic Poly(Methyl Methacrylate) Nanoparticles Surface Modified with Folic Acid Presenting Cell Uptake Mediated by Endocytosis. J. Nanoparticle Res. 2016, 18, 104.
   Web of Science ®Google Scholar
• Sahoo, B.; Devi, K. S. P.; Banerjee, R.; Maiti, T. K.; Pramanik, P.; Dhara, D. Thermal and pH Responsive Polymer-Tethered Multifunctional Magnetic Nanoparticles for Targeted Delivery of Anticancer Drug. ACS Appl. Mater. Interfaces 2013, 5, 3884–3893. doi:10.1021/am400572b.
   PubMed Web of Science ®Google Scholar
• Li, Z.; Zhang, J.; Guo, X.; Guo, X.; Zhang, Z. Multi-Functional Magnetic Nanoparticles as an Effective Drug Carrier for the Controlled anti-Tumor Treatment. J. Biomater. Appl. 2018, 32, 967–976. doi:10.1177/0885328217748023.
   PubMed Web of Science ®Google Scholar
• Soares, P. I. P.; Laia, C. A. T.; Carvalho, A.; Pereira, L. C. J.; Coutinho, J. T.; Ferreira, I. M. M.; Novo, C. M. M.; Borges, J. P. Iron Oxide Nanoparticles Stabilized with a Bilayer of Oleic Acid for Magnetic Hyperthermia and MRI Applications. Appl. Surf. Sci. 2016, 383, 240–247. doi:10.1016/j.apsusc.2016.04.181.
   Web of Science ®Google Scholar
• Ortega, G. A.; Pérez-Rodriguez, S.; Reguera, E. Magnetic Paper – Based ELISA for IgM-Dengue Detection. RSC Adv. 2017, 7, 4921–4932. doi:10.1039/C6RA25992H.
   Web of Science ®Google Scholar
• Li, H.; Yan, K.; Shang, Y.; Shrestha, L.; Liao, R.; Liu, F.; Li, P.; Xu, H.; Xu, Z.; Chu, P. K. Folate-Bovine Serum Albumin Functionalized Polymeric Micelles Loaded with Superparamagnetic Iron Oxide Nanoparticles for Tumor Targeting and Magnetic Resonance Imaging. Acta Biomater. 2015, 15, 117–126. doi:10.1016/j.actbio.2015.01.006.
   PubMed Web of Science ®Google Scholar
• Zheng, S. W.; Huang, M.; Hong, R. Y.; Deng, S. M.; Cheng, L. F.; Gao, B.; Badami, D. RGD-Conjugated Iron Oxide Magnetic Nanoparticles for Magnetic Resonance Imaging Contrast Enhancement and Hyperthermia. J. Biomater. Appl. 2014, 28, 1051–1059. doi:10.1177/0885328213493486.
   PubMed Web of Science ®Google Scholar
• Peddis, D.; Cannas, C.; Musinu, A.; Piccaluga, G. Coexistence of Superparmagnetism and Spin-Glass like Magnetic Ordering Phenomena in a CoFe2O4-SiO2 Nanocomposite. J. Phys. Chem. C 2008, 112, 5141–5147. doi:10.1021/jp076704d.
   Web of Science ®Google Scholar
• Li, J.; Hu, Y.; Hou, Y.; Shen, X.; Xu, G.; Dai, L.; Zhou, J.; Liu, Y.; Cai, K. Phase-Change Material Filled Hollow Magnetic Nanoparticles for Cancer Therapy and Dual Modal Bioimaging. Nanoscale 2015, 7, 9004–9012. doi:10.1039/C5NR01744K.
   PubMed Web of Science ®Google Scholar
• Sato, I.; Umemura, M.; Mitsudo, K.; Fukumura, H.; Kim, J.-H.; Hoshino, Y.; Nakashima, H.; Kioi, M.; Nakakaji, R.; Sato, M.; et al. Simultaneous Hyperthermia-Chemotherapy with Controlled Drug Delivery Using Single-Drug Nanoparticles. Sci. Rep. 2016, 6, 24629. doi:10.1038/srep24629.
   PubMed Web of Science ®Google Scholar
• McDonald, M.; Corde, S.; Lerch, M.; Rosenfeld, A.; Jackson, M.; Tehei, M. First in Vitro Evidence of Modulated Electro-Hyperthermia Treatment Performance in Combination with Megavoltage Radiation by Clonogenic Assay. Sci. Rep. 2018, 8, 1–13.
   PubMed Web of Science ®Google Scholar
• Mantso, T.; Vasileiadis, S.; Anestopoulos, I.; Voulgaridou, G. P.; Lampri, E.; Botaitis, S.; Kontomanolis, E. N.; Simopoulos, C.; Goussetis, G.; Franco, R.; et al. Hyperthermia Induces Therapeutic Effectiveness and Potentiates Adjuvant Therapy with Non-targeted and Targeted Drugs in an In Vitro Model of Human Malignant Melanoma. Sci. Rep. 2018, 8, 10724. doi:10.1038/s41598-018-29018-0.
   PubMed Web of Science ®Google Scholar
• Asín, L.; Ibarra, M. R.; Tres, A.; Goya, G. F. Controlled Cell Death by Magnetic Hyperthermia: Effects of Exposure Time, Field Amplitude, and Nanoparticle Concentration. Pharmaceut. Res. 2012, 29, 1319–1327. doi:10.1007/s11095-012-0710-z.
   PubMed Web of Science ®Google Scholar
• Roca, A. G.; Wiese, B.; Timmis, J.; Vallejo-Fernandez, G.; O’Grady, K. Effect of Frequency and Field Amplitude in Magnetic Hyperthermia. IEEE Trans. Magn. 2012, 48, 4054–4057. doi:10.1109/TMAG.2012.2201459.
   Web of Science ®Google Scholar
• He, M.; Potuck, A.; Kohn, J. C.; Fung, K.; Reinhart-King, C. A.; Chu, C. C. Self-Assembled Cationic Biodegradable Nanoparticles from pH-Responsive Amino-Acid-Based Poly(Ester Urea Urethane)s and Their Application as a Drug Delivery Vehicle. Biomacromolecules 2016, 17, 523–537. doi:10.1021/acs.biomac.5b01449.
   PubMed Web of Science ®Google Scholar
• Piagnerelli, M.; Zouaoui Boudjeltia, K.; Brohee, D.; Vereerstraeten, A.; Piro, P.; Vincent, J. L.; Vanhaeverbeek, M. Assessment of Erythrocyte Shape by Flow Cytometry Techniques. J. Clin. Pathol. 2006, 60, 549–554. doi:10.1136/jcp.2006.037523.
   PubMed Web of Science ®Google Scholar
• Rolfes-Curi, A.; Odgen, L. L.; Omann, M. G.; Aminoff, D. Flow Cytometric Analysis of Human Erythrocytes: Possible Identification of Senescent RBC with Fluorescently Labelled Wheat Germ Agglutinin. Exp. Gerontol. 1991, 26, 327–345. doi:10.1016/0531-5565(91)90045-N.
   PubMed Web of Science ®Google Scholar
• Ahlgrim, C.; Pottgiesser, T.; Sander, T.; Schumacher, Y. O.; Baumstark, M. W. Flow Cytometric Assessment of Erythrocyte Shape through Analysis of FSC Histograms: Use of Kurtosis and Implications for Longitudinal Evaluation. PLoS One 2013, 8, e59862. doi:10.1371/journal.pone.0059862.
   PubMed Web of Science ®Google Scholar
• Yamamoto, A.; Saito, N.; Yamauchi, Y.; Takeda, M.; Ueki, S.; Itoga, M.; Kojima, K.; Kayaba, H. Flow Cytometric Analysis of Red Blood Cell Osmotic Fragility. J. Lab. Autom. 2014, 19, 483–487. doi:10.1177/2211068214532254.
   PubMedGoogle Scholar