Systemically delivered antibody-labeled magnetic iron oxide nanoparticles are less toxic than plain nanoparticles when activated by alternating magnetic fields

References

• Gilchrist R, Medal R, Shorey WD, et al. Selective inductive heating of lymph nodes. Ann Surg. 1957;146(4):596–606.
   PubMed Web of Science ®Google Scholar
• Weinstein JS, Varallyay CG, Dosa E, et al. Superparamagnetic iron oxide nanoparticles: diagnostic magnetic resonance imaging and potential therapeutic applications in neurooncology and central nervous system inflammatory pathologies, a review. J Cereb Blood Flow Metab. 2010;30(1):15–35.
   PubMed Web of Science ®Google Scholar
• Ivkov R. Magnetic nanoparticle hyperthermia: a new frontier in biology and medicine? Int J Hyperthermia. 2013;29(8):703–705.
   PubMed Web of Science ®Google Scholar
• Kandasamy G, Maity D. Recent advances in superparamagnetic iron oxide nanoparticles (SPIONs) for in vitro and in vivo cancer nanotheranostics. Int J Pharm. 2015;496(2):191–218.
   PubMed Web of Science ®Google Scholar
• Theil EC. Iron, ferritin, and nutrition. Annu Rev Nutr. 2004;24:327–343.
   PubMed Web of Science ®Google Scholar
• Auerbach M, Ballard H. Clinical use of intravenous iron: administration, efficacy, and safety. Hematology Am Soc Hematol Educ Program. 2010;2010:338–347.
   PubMed Web of Science ®Google Scholar
• Danielson BG. Structure, chemistry, and pharmacokinetics of intravenous iron agents. J Am Soc Nephrol. 2004;15(Suppl. 5):S93–S98.
   PubMed Web of Science ®Google Scholar
• Auerbach M, Coyne D, Ballard H. Intravenous iron: from anathema to standard of care. Am J Hematol. 2008;83(7):580–588.
   PubMed Web of Science ®Google Scholar
• Lebrun F, Klastersky J, Levacq D, et al. Intravenous iron therapy for anemic cancer patients: a review of recently published clinical studies. Support Care Cancer. 2017;25(7):2313–2319.
   PubMed Web of Science ®Google Scholar
• Coricovac D-E, Moacă E-A, Pinzaru I, et al. Biocompatible colloidal suspensions based on magnetic iron oxide nanoparticles: synthesis, characterization and toxicological profile. Front Pharmacol. 2017;8:154.
   PubMed Web of Science ®Google Scholar
• Mahmoudi K, Bouras A, Bozec D, et al. Magnetic hyperthermia therapy for the treatment of glioblastoma: a review of the therapy's history, efficacy and application in humans. Int J Hyperthermia. 2018;34(8):1316–1328.
   PubMed Web of Science ®Google Scholar
• Dennis CL, Ivkov R. Physics of heat generation using magnetic nanoparticles for hyperthermia. Int J Hyperthermia. 2013;29(8):715–729.
   PubMed Web of Science ®Google Scholar
• Soetaert F, Kandala SK, Bakuzis A, et al. Experimental estimation and analysis of variance of the measured loss power of magnetic nanoparticles. Sci Rep. 2017;7(1):6661.
   PubMed Web of Science ®Google Scholar
• Niculaes D, Lak A, Anyfantis GC, et al. Asymmetric assembling of iron oxide nanocubes for improving magnetic hyperthermia performance. ACS Nano. 2017;11(12):12121–12133.
   PubMed Web of Science ®Google Scholar
• Tong S, Quinto CA, Zhang L, et al. Size-dependent heating of magnetic iron oxide nanoparticles. ACS Nano. 2017;11(7):6808–6816.
   PubMed Web of Science ®Google Scholar
• He S, Zhang H, Liu Y, et al. Magnetic nanoparticle hyperthermia: maximizing specific loss power for magnetic hyperthermia by hard–soft mixed ferrites. Small. 2018;14(29):1870133.
   Web of Science ®Google Scholar
• Attaluri A, Kandala K, Wabler M, et al. Magnetic nanoparticle hyperthermia enhances radiation therapy: a study in mouse models of human prostate cancer. Int J Hyperthermia. 2015;31(4):359–374.
   PubMed Web of Science ®Google Scholar
• Shetake NG, Kumar A, Gaikwad S, et al. Magnetic nanoparticle-mediated hyperthermia therapy induces tumour growth inhibition by apoptosis and Hsp90/AKT modulation. Int J Hyperthermia. 2015;31(8):909–919.
   PubMed Web of Science ®Google Scholar
• Kut C, Zhang Y, Hedayati M, et al. Preliminary study of injury from heating systemically delivered, nontargeted dextran-superparamagnetic iron oxide nanoparticles in mice. Nanomedicine (Lond). 2012;7(11):1697–1711.
   PubMed Web of Science ®Google Scholar
• Janib SM, Moses AS, Mackay JA. Imaging and drug delivery using theranostic nanoparticles. Adv Drug Deliv Rev. 2010;62(11):1052–1063.
   PubMed Web of Science ®Google Scholar
• Lee DE, Koo H, Sun IC, et al. Multifunctional nanoparticles for multimodal imaging and theragnosis. Chem Soc Rev. 2012;41(7):2656–2672.
   PubMed Web of Science ®Google Scholar
• Denardo SJ, Denardo GL, Miers LA, et al. Development of tumor targeting bioprobes ((111)In-chimeric L6 monoclonal antibody nanoparticles) for alternating magnetic field cancer therapy. Clin Cancer Res. 2005;11(19 Pt 2):7087s–7092s.
   PubMed Web of Science ®Google Scholar
• Denardo SJ, Denardo GL, Natarajan A, et al. Thermal dosimetry predictive of efficacy of 111In-ChL6 nanoparticle AMF-induced thermoablative therapy for human breast cancer in mice. J Nucl Med. 2007;48(3):437–444.
   PubMed Web of Science ®Google Scholar
• Schroeder A, Heller DA, Winslow MM, et al. Treating metastatic cancer with nanotechnology. Nat Rev Cancer. 2011;12(1):39–50.
   PubMed Web of Science ®Google Scholar
• Blanco E, Shen H, Ferrari M. Principles of nanoparticle design for overcoming biological barriers to drug delivery. Nat Biotechnol. 2015;33(9):941–951.
   PubMed Web of Science ®Google Scholar
• Eifler AC, Thaxton CS. Nanoparticle therapeutics: FDA approval, clinical trials, regulatory pathways, and case study. Methods Mol Biol. 2011;726:325–338.
   PubMedGoogle Scholar
• Wilhelm S, Tavares S, Dai AJ, et al. Analysis of nanoparticle delivery to tumours. Nat Rev Mater. 2016;1:1–12.
   Web of Science ®Google Scholar
• Parivar K, Malekvand Fard F, Bayat M, et al. Evaluation of iron oxide nanoparticles toxicity on liver cells of BALB/c rats. Iran Red Crescent Med J. 2016;18(1):e28939.
   PubMed Web of Science ®Google Scholar
• Zhang YN, Poon W, Tavares AJ, et al. Nanoparticle–liver interactions: cellular uptake and hepatobiliary elimination. J Control Release. 2016;240:332–348.
   PubMed Web of Science ®Google Scholar
• Patil RM, Thorat ND, Shete PB, et al. Comprehensive cytotoxicity studies of superparamagnetic iron oxide nanoparticles. Biochem Biophys Rep. 2018;13:63–72.
   PubMedGoogle Scholar
• Cardoso MM, Peca IN, Roque AC. Antibody-conjugated nanoparticles for therapeutic applications. Curr Med Chem. 2012;19:3103–3127.
   PubMed Web of Science ®Google Scholar
• Grüttner C, Müller K, Teller J, et al. Synthesis and antibody conjugation of magnetic nanoparticles with improved specific power absorption rates for alternating magnetic field cancer therapy. J Magn Magn Mater. 2007;311(1):181–186.
   Web of Science ®Google Scholar
• Dennis C, Jackson A, Borchers J, et al. The influence of collective behavior on the magnetic and heating properties of iron oxide nanoparticles. J Appl Phys. 2008;103(7):07A319.
   Web of Science ®Google Scholar
• Dennis C, Jackson A, Borchers J, et al. Nearly complete regression of tumors via collective behavior of magnetic nanoparticles in hyperthermia. Nanotechnology. 2009;20(39):395103.
   PubMed Web of Science ®Google Scholar
• Bordelon DE, Cornejo C, Gruttner C, et al. Magnetic nanoparticle heating efficiency reveals magneto-structural differences when characterized with wide ranging and high amplitude alternating magnetic fields. J Appl Phys. 2011;109(12):124904.
   Web of Science ®Google Scholar
• Branquinho LC, Carrião MS, Costa AS, et al. Effect of magnetic dipolar interactions on nanoparticle heating efficiency: implications for cancer hyperthermia. Sci Rep. 2013;3:2887.
   PubMed Web of Science ®Google Scholar
• Dennis CL, Krycka KL, Borchers JA, et al. Internal magnetic structure of nanoparticles dominates time-dependent relaxation processes in a magnetic field. Adv Funct Mater. 2015;25(27):4300–4311.
   Web of Science ®Google Scholar
• Natarajan A, Gruettner C, Ivkov R, et al. NanoFerrite particle based radioimmunonanoparticles: binding affinity and in vivo pharmacokinetics. Bioconjug Chem. 2008;19(6):1211–1218.
   PubMed Web of Science ®Google Scholar
• Behnam Azad B, Banerjee SR, Pullambhatla M, et al. Evaluation of a PSMA-targeted BNF nanoparticle construct. Nanoscale. 2015;7(10):4432–4442.
   PubMed Web of Science ®Google Scholar
• Korangath P, Barnett JD, Sharma A, et al. Nanoparticle interactions with immune cells dominate tumor retention and induce T cell-mediated tumor suppression in models of breast cancer. Sci Adv. 2020;6(13):eaay1601.
   PubMed Web of Science ®Google Scholar
• Bordelon DE, Goldstein RC, Nemkov VS, et al. Modified solenoid coil that efficiently produces high amplitude AC magnetic fields with enhanced uniformity for biomedical applications. IEEE Trans Magn. 2012;48(1):47–52.
   Web of Science ®Google Scholar
• Nemkov V, Ruffini R, Goldstein R, et al. Magnetic field generating inductor for cancer hyperthermia research. COMPEL. 2011;30(5):1626–1636.
   Web of Science ®Google Scholar
• Kumar A, Attaluri A, Mallipudi R, et al. Method to reduce non-specific tissue heating of small animals in solenoid coils. Int J Hyperthermia. 2013;29(2):106–120.
   PubMed Web of Science ®Google Scholar
• Landi GT, Bakuzis AF. On the energy conversion efficiency in magnetic hyperthermia applications: a new perspective to analyze the departure from the linear regime. J Appl Phys. 2012;111(8):83915.
   Web of Science ®Google Scholar
• Alleva E, Santucci D. Guide for the care and use of laboratory animals. Ethology. 1997;103:1072–1073.
   Web of Science ®Google Scholar
• Jordan A, Scholz R, Maier-Hauff K, et al. The effect of thermotherapy using magnetic nanoparticles on rat malignant glioma. J Neurooncol. 2006;78(1):7–14.
   PubMed Web of Science ®Google Scholar
• Wilhelm C, Fortin JP, Gazeau F. Tumour cell toxicity of intracellular hyperthermia mediated by magnetic nanoparticles. J Nanosci Nanotechnol. 2007;7(8):2933–2937.
   PubMed Web of Science ®Google Scholar
• Giustini AJ, Perreard I, Rauwerdink AM, et al. Noninvasive assessment of magnetic nanoparticle-cancer cell interactions. Integr Biol (Camb). 2012;4(10):1283–1288.
   PubMed Web of Science ®Google Scholar
• Zhao Q, Wang L, Cheng R, et al. Magnetic nanoparticle-based hyperthermia for head & neck cancer in mouse models. Theranostics. 2012;2:113–121.
   PubMed Web of Science ®Google Scholar
• Sanz B, Calatayud MP, Torres TE, et al. Magnetic hyperthermia enhances cell toxicity with respect to exogenous heating. Biomaterials. 2017;114:62–70.
   PubMed Web of Science ®Google Scholar
• Rodrigues HF, Capistrano G, Mello FM, et al. Precise determination of the heat delivery during in vivo magnetic nanoparticle hyperthermia with infrared thermography. Phys Med Biol. 2017;62(10):4062–4082.
   PubMed Web of Science ®Google Scholar
• Balivada S, Rachakatla RS, Wang H, et al. A/C magnetic hyperthermia of melanoma mediated by iron(0)/iron oxide core/shell magnetic nanoparticles: a mouse study. BMC Cancer. 2010;10:119.
   PubMed Web of Science ®Google Scholar
• Kim J-E, Shin J-Y, Cho M-H. Magnetic nanoparticles: an update of application for drug delivery and possible toxic effects. Arch Toxicol. 2012;86(5):685–700.
   PubMed Web of Science ®Google Scholar
• Hoopes PJ, Wagner RJ, Duval K, et al. Treatment of canine oral melanoma with nanotechnology-based immunotherapy and radiation. Mol Pharm. 2018;15(9):3717–3722.
   PubMed Web of Science ®Google Scholar
• Chao Y, Chen G, Liang C, et al. Iron nanoparticles for low-power local magnetic hyperthermia in combination with immune checkpoint blockade for systemic antitumor therapy. Nano Lett. 2019;19(7):4287–4296.
   PubMed Web of Science ®Google Scholar
• Acharya S, Sahoo SK. PLGA nanoparticles containing various anticancer agents and tumour delivery by EPR effect. Adv Drug Deliv Rev. 2011;63(3):170–183.
   PubMed Web of Science ®Google Scholar
• Yarbrough BE, Hubbard RW. Heat-related illnesses. In: Auerbach PS, Geehr EC, editors. Management of wilderness and environmental emergencies. 2nd ed. St. Louis: C. V. Mosby; 1988. p. 119–143.
   Google Scholar
• Lambert GP. Role of gastrointestinal permeability in exertional heatstroke. Exerc Sport Sci Rev. 2004;32(4):185–190.
   PubMed Web of Science ®Google Scholar
• Adair ER, Black DR. Thermoregulatory responses to RF energy absorption. Bioelectromagnetics. 2003;24(S6):S17–S38.
   Web of Science ®Google Scholar
• Ivkov R, DeNardo SJ, Daum W, et al. Application of high amplitude alternating magnetic fields for heat induction of nanoparticles localized in cancer. Clin Cancer Res. 2005;11(19):7093s–7103s.
   PubMed Web of Science ®Google Scholar
• Soetaert F, Dupré L, Ivkov R, et al. Computational evaluation of amplitude modulation for enhanced magnetic nanoparticle hyperthermia. Biomed Eng/Biomed Techn. 2015;60:491–504.
   PubMed Web of Science ®Google Scholar
• Kandala SK, Liapi E, Whitcomb LL, et al. Temperature-controlled power modulation compensates for heterogeneous nanoparticle distributions: a computational optimization analysis for magnetic hyperthermia. Int J Hyperthermia. 2019;36(1):115–129.
   PubMed Web of Science ®Google Scholar
• Tay ZW, Chandrasekharan P, Chiu-Lam A, et al. Magnetic particle imaging-guided heating in vivo using gradient fields for arbitrary localization of magnetic hyperthermia therapy. ACS Nano. 2018;12(4):3699–3713.
   PubMed Web of Science ®Google Scholar