Superparamagnetic iron oxide nanoparticles (SPIONs) modulate hERG ion channel activity

References

• Andrews, N. C. 1999. “Disorders of Iron Metabolism.” The New England Journal of Medicine 341(26): 1986–1995. doi:10.1056/NEJM199912233412607.
   PubMed Web of Science ®Google Scholar
• Ankamwar, B., T. C. Lai, J. H. Huang, R. S. Liu, M. Hsiao, C. H. Chen, and Y. K. Hwu. 2010. “Biocompatibility of Fe3O4 Nanoparticles Evaluated by in Vitro Cytotoxicity Assays Using Normal, Glia and Breast Cancer Cells.” Nanotechnology 21(7): 075102–0759. doi:10.1088/0957-4484/21/7/075102.
   PubMed Web of Science ®Google Scholar
• Armstrong, C. M., R. P. Swenson, and S. R. Jr Taylor. 1982. “Block of Squid Axon K Channels by Internally and Externally Applied Barium Ions.” The Journal of General Physiology 80(5): 663–682. doi:10.1085/jgp.80.5.663.
   PubMed Web of Science ®Google Scholar
• Beedle, A. M., J. Hamid, and G. W. Zamponi. 2002. “Inhibition of Transiently Expressed Low- and High-Voltage-Activated Calcium Channels by Trivalent Metal Cations.” The Journal of Membrane Biology 187: 225–238. doi:10.1007/s00232-001-0166-2.
   PubMed Web of Science ®Google Scholar
• Bérubé, J., D. Caouette, and P. Daleau. 2001. “Hydrogen Peroxide Modifies the Kinetics of hERG Channel Expressed in a Mammalian Cell Line.” Journal of Pharmacology and Experimental Therapeutics 297: 96–102. http://jpet.aspetjournals.org/content/297/1/96.long.
   PubMed Web of Science ®Google Scholar
• Bulte, J. W. M., T. Douglas, B. Witwer, S. C. Zhang, E. Strable, B. K. Lewis, H. Zywicke, B. Miller, P. van Gelderen, and B. M. Moskowitz. 2001. “Magnetodendrimers Allow Endosomal Magnetic Labeling and in Vivo Tracking of Stem Cells.” Nature Biotechnology 19(12): 1141–1147. doi:10.1038/nbt1201-1141.
   PubMed Web of Science ®Google Scholar
• Chen, M. X., R. M. Helliwell, and J. J. Clare. 2009. “In Vitro Profiling against Ion Channels beyond hERG as an Early Indicator of Cardiac Risk.” Current Opinion in Molecular Therapeutics 11: 269–281. https://www.ncbi.nlm.nih.gov/pubmed/19479660.
   PubMed Web of Science ®Google Scholar
• Colombo, M., S. Carregal-Romero, M. F. Casula, L. Gutiérrez, M. P. Morales, I. B. Böhm, J. T. Heverhagen, D. Prosperi, and W. J. Parak. 2012. “Biological Applications of Magnetic Nanoparticles.” Chemical Society Reviews 41(11): 4306–4334. doi:10.1039/c2cs15337h.
   PubMed Web of Science ®Google Scholar
• Dissanayake, N. M., K. M. Current, and S. O. Obare. 2015. “Mutagenic Effects of Iron Oxide Nanoparticles on Biological Cells.” International Journal of Molecular Sciences 16(10): 23482–23516. doi:10.3390/ijms161023482.
   PubMed Web of Science ®Google Scholar
• Duguet, E., S. Vasseur, S. Mornet, and J. M. Devoisselle. 2006. “Magnetic Nanoparticles and Their Applications in Medicine.” Nanomedicine 1(2): 157–168. doi:10.2217/17435889.1.2.157.
   PubMed Web of Science ®Google Scholar
• Elinder, F., and P. Arhem. 2003. “Metal Ion Effects on Ion Channel Gating.” Quarterly Reviews of Biophysics 36(4): 373–427. doi:10.1017/S0033583504003932.
   PubMed Web of Science ®Google Scholar
• Fermini, B., and A. A. Fossa. 2003. “The Impact of Drug-Induced QT Interval Prolongation on Drug Discovery and Development.” Nature Reviews Drug Discovery 2(6): 439–447. doi:10.1038/nrd1108.
   PubMed Web of Science ®Google Scholar
• Fernandez, D., A. Ghanta, K. I. Kinard, and M. C. Sanguinetti. 2005. “Molecular Mapping of a Site for Cd2+-Induced Modification of Human Ether-à-Go-Go-Related Gene (hERG) Channel Activation.” The Journal of Physiology 567(3): 737–755. doi:10.1113/jphysiol.2005.089094.
   PubMed Web of Science ®Google Scholar
• Ficker, E., W. Jarolimek, and A. M. Brown. 2001. “Molecular Determinants of Inactivation and Dofetilide Block in Ether a-Go-Go (EAG) Channels and EAG-Related K(+) Channels.” Molecular Pharmacology 60(6): 1343–1348. doi:10.1124/mol.60.6.1343.
   PubMed Web of Science ®Google Scholar
• Food and Drug Administration, HHS. 2005. “International Conference on Harmonisation (ICH) Guidance on S7B Nonclinical Evaluation of the Potential for Delayed Ventricular Repolarization (QT Interval Prolongation). Human Pharmaceuticals Availability. Notice. Federal Register 70: 61133–61134. http://www.ich.org/fileadmin/Public_Web_Site/ICH_Products/Guidelines/Safety/S7B/Step4/S7B_Guideline.pdf.
   Google Scholar
• Gu, Z., L. D. Plant, X. Y. Meng, J. M. Perez-Aguilar, Z. Wang, M. Dong, D. E. Logothetis, and R. Zhou. 2018. “Exploring the Nanotoxicology of MoS2: A Study on the Interaction of MoS2 Nanoflakes and K+ Channels.” ACS Nano 12(1): 705–717. doi:10.1021/acsnano.7b07871.
   PubMed Web of Science ®Google Scholar
• Gualdani, R., M. M. Cavalluzzi, F. Tadini-Buoninsegni, M. Convertino, P. Gailly, A. Stary-Weinzinger, and G. Lentini. 2018. “Molecular Insights into hERG Potassium Channel Blockade by Lubeluzole.” Cellular Physiology and Biochemistry 45(6): 2233–2245. doi:10.1159/000488169.
   PubMedGoogle Scholar
• Gualdani, R., F. Tadini-Buoninsegni, M. Roselli, I. Defrenza, M. Contino, N. A. Colabufo, and G. Lentini. 2015. “Inhibition of hERG Potassium Channel by the Antiarrhythmic Agent Mexiletine and its Metabolite m-Hydroxymexiletine.” Pharmacology Research & Perspectives 3: E 00160. doi:10.1002/prp2.160.
   Web of Science ®Google Scholar
• Gupta, A. K., and M. Gupta. 2005. “Synthesis and Surface Engineering of Iron Oxide Nanoparticles for Biomedical Applications.” Biomaterials 26(18): 3995–4021. doi:10.1016/j.biomaterials.2004.10.012.
   PubMed Web of Science ®Google Scholar
• Hafeli, U. O., J. S. Riffle, L. Harris-Shekhawat, A. Carmichael-Baranauskas, F. Mark, J. P. Dailey, and D. Bardenstein. 2009. “Cell Uptake and in Vitro Toxicity of Magnetic Nanoparticles Suitable for Drug Delivery.” Molecular Pharmaceutics 6: 1417–1428. doi:10.1021/mp900083m.
   PubMed Web of Science ®Google Scholar
• Horwitz, L. D., and E. A. Rosenthal. 1999. “Iron-Mediated Cardiovascular Injury.” Vascular Medicine 4(2): 93–99. doi:10.1191/135886399676588477.
   PubMed Web of Science ®Google Scholar
• Huber, D.L. 2005. “Synthesis, Properties, and Applications of Iron Nanoparticles.” Small 1(5): 482–501. doi:10.1002/smll.200500006.
   PubMed Web of Science ®Google Scholar
• Hussain, S. M., K. L. Hess, J. M. Gearhart, K. T. Geiss, and J. J. Schlager. 2005. “In Vitro Toxicity of Nanoparticles in BRL 3A Rat Liver Cells.” Toxicology in Vitro: An International Journal Published in Association with Bibra 19(7): 975–983. doi:10.1016/j.tiv.2005.06.034.
   PubMed Web of Science ®Google Scholar
• Iancu, T. C., H. Shiloh, G. Link, E. R. Bauminger, A. Pinson, and C. Hershko. 1987. “Ultrastructural Pathology of Iron-Loaded Rat Myocardial Cells in Culture.” British Journal of Experimental Pathology 68: 53–65. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2012992/.
   PubMedGoogle Scholar
• Jeng, H. A., and J. Swanson. 2006. “Toxicity of Metal Oxide Nanoparticles in Mammalian Cells.” Journal of Environmental Science and Health. Part A, Toxic/Hazardous Substances & Environmental Engineering 41: 2699–2711. doi:10.1080/10934520600966177.
   PubMed Web of Science ®Google Scholar
• Johannsen, M., U. Gneveckow, K. Taymoorian, B. Thiesen, N. Waldöfner, R. Scholz, K. Jung, A. Jordan, P. Wust, and S. A. Loening. 2007. “Morbidity and Quality of Life During Thermotherapy Using Magnetic Nanoparticles in Locally Recurrent Prostate Cancer: Results of a Prospective Phase I Trial.” International Journal of Hyperthermia 23(3): 315–323. doi:10.1080/02656730601175479.
   PubMed Web of Science ®Google Scholar
• Johnson, J. P., J. R. Balser, and P. B. Bennett. 2001. “A Novel Extracellular Calcium Sensing Mechanism in Voltage-Gated Potassium Ion Channels.” The Journal of Neuroscience 21(12): 4143–4153. doi:10.1523/JNEUROSCI.21-12-04143.2001.
   PubMed Web of Science ®Google Scholar
• Johnson, J. P., F. M. Mullins, and P. B. Bennett. 1999. “Human Ether-à-Go-Go-Related Gene K+ Channel Gating Probed with Extracellular Ca2+: Evidence for Two Distinct Voltage Sensors.” The Journal of General Physiology 113(4): 565–580. doi:10.1085/jgp.113.4.565.
   PubMed Web of Science ®Google Scholar
• Kremastinos, D. T., and D. Farmakis. 2011. “Iron Overload Cardiomyopathy in Clinical Practice.” Circulation 124(20): 2253–2263. doi:10.1161/CIRCULATIONAHA.111.050773.
   PubMed Web of Science ®Google Scholar
• Kudaibergenova, M., L. L. Perissinotti, and S. Y. Noskov. 2018. “Lipid Roles in hERG Function and Interactions with Drugs.” Neuroscience Letters 700:70–77. doi:10.1016/j.neulet.2018.05.019.
   PubMed Web of Science ®Google Scholar
• Kuryshev, Y. A., G. M. Brittenham, H. Fujioka, P. Kannan, C. C. Shieh, S. A. Cohen, and A. M. Brown. 1999. “Decreased Sodium and Increased Transient Outward Potassium Currents in Iron-Loaded Cardiac Myocytes.” Circulation 100: 675–683. doi:10.1161/01.CIR.100.6.675.
   PubMed Web of Science ®Google Scholar
• Leifert, A., Y. Pan, A. Kinkeldey, F. Schiefer, J. Setzler, O. Scheel, H. Lichtenbeld, et al. 2013. “Differential hERG Ion Channel Activity of Ultrasmall Gold Nanoparticles.” Proceedings of the National Academy of Sciences of Sciences 110(20): 8004–8009. doi:10.1073/pnas.1220143110. .
   PubMed Web of Science ®Google Scholar
• Lin, M. C., and D. M. Papazian. 2007. “Differences between Ion Binding to Eag and HERG Voltage Sensors Contribute to Differential Regulation of Activation and Deactivation Gating.” Channels (Austin) 1(6): 429–437. doi:10.4161/chan.1.6.5760.
   PubMed Web of Science ®Google Scholar
• Maier-Hauff, K., F. Ulrich, D. Nestler, H. Niehoff, P. Wust, B. Thiesen, H. Orawa, V. Budach, and A. Jordan. 2011. “Jordan, Efficacy and Safety of Intratumoral Thermotherapy Using Magnetic Iron-Oxide Nanoparticles Combined with External Beam Radiotherapy on Patients with Recurrent Glioblastoma Multiforme.” Journal of Neuro-Oncology 103(2): 317–324. doi:10.1007/s11060-010-0389-0.
   PubMed Web of Science ®Google Scholar
• McLaughlin, S. 1989. “The Electrostatic Properties of Membranes.” Annual Review of Biophysics and Biophysical Chemistry 18: 113–136. doi:10.1146/annurev.bb.18.060189.000553.
   PubMedGoogle Scholar
• Mitcheson, J. S., J. Chen, M. Lin, C. Culberson, and M. C. Sanguinetti. 2000. “A Structural Basis for Drug-Induced Long QT Syndrome.” Proceedings of the National Academy of Sciences of Sciences 97(22): 12329–12333. doi:10.1073/pnas.210244497.
   PubMed Web of Science ®Google Scholar
• Moore, T. L., L. Rodriguez-Lorenzo, V. Hirsch, S. Balog, D. Urban, C. Jud, B. Rothen-Rutishauser, M. Lattuada, and A. Petri-Fink. 2015. “Nanoparticle Colloidal Stability in Cell Culture Media and Impact on Cellular Interactions.” Chemical Society Reviews 44(17): 6287–6305. doi:10.1039/C4CS00487F.
   PubMed Web of Science ®Google Scholar
• Oshiro, S., M. S. Morioka, and M. Kikuchi. 2011. “Dysregulation of Iron Metabolism in Alzheimer’s Disease, Parkinson’s Disease, and Amyotrophic Lateral Sclerosis.” Advances in Pharmacological Sciences 2011: 1. doi:10.1155/2011/378278.
   Google Scholar
• Parkes, J. G., Y. Liu, J. B. Sirna, and D. M. Templeton. 2000. “Changes in Gene Expression with Iron Loading and Chelation in Cardiac Myocytes and Non-Myocytic Fibroblasts.” Journal of Molecular and Cellular Cardiology 32(2): 233–246. doi:10.1006/jmcc.1999.1068.
   PubMed Web of Science ®Google Scholar
• Piscopo, S., and E. R. Brown. 2018. “Zinc Oxide Nanoparticles and Voltage-Gated Human KV11.1 Potassium Channels Interact Though a Novel Mechanism.” Small 14(15): 1703403. doi:10.1002/smll.201703403.
   Web of Science ®Google Scholar
• Po, S. S., D. W. Wang, I. C. Yang, J. P. Jr Johnson, L. Nie, and P. B. Bennett. 1999. “Modulation of hERG Potassium Channels by Extracellular Magnesium and Quinidine.” Journal of Cardiovascular Pharmacology 33(2): 181–185. doi:10.1097/00005344-199902000-00002.
   PubMed Web of Science ®Google Scholar
• Sanguinetti, M. C., M. E. Curran, A. Zou, J. Shen, P. S. Spector, D. L. Atkinson, and M. T. Keating. 1996. “Coassembly of K(V)LQT1 and minK (IsK) Proteins to Form Cardiac I(Ks) Potassium Channel.” Nature 384(6604): 80–83. doi:10.1038/384080a0.
   PubMed Web of Science ®Google Scholar
• Sanguinetti, M. C., C. Jiang, M. E. Curran, and M. T. Keating. 1995. “A Mechanistic Link between an Inherited and an Acquired Cardiac Arrhythmia: hERG Encodes the IKr Potassium Channel.” Cell 81(2): 299–307. doi:10.1016/0092-8674(95)90340-2.
   PubMed Web of Science ®Google Scholar
• Singh, N., G. J. S. Jenkins, R. Asadi, and S. H. Doaka. 2010. “Potential Toxicity of Superparamagnetic Iron Oxide Nanoparticles (SPION).” Nano Reviews 1: 5358. doi:10.3402/nano.v1i0.5358.
   PubMedGoogle Scholar
• Stankiewicz, J. M., and S. D. Brass. 2009. “Role of Iron in Neurotoxicity: A Cause for Concern in the Elderly?” Current Opinion in Clinical Nutrition and Metabolic Care 12: 22–29. doi:10.1097/MCO.0b013e32831ba07c.
   PubMed Web of Science ®Google Scholar
• Stroh, A., C. Zimmer, C. Gutzeit, M. Jakstadt, F. Marschinke, T. Jung, H. Pilgrimm, and T. Grune. 2004. “Iron Oxide Particles for Molecular Magnetic Resonance Imaging Cause Transient Oxidative Stress in Rat Macrophages.” Free Radical Biology and Medicine 36(8): 976–984. doi:10.1016/j.freeradbiomed.2004.01.016.
   PubMed Web of Science ®Google Scholar
• Taglialatela, M., P. Castaldo, S. Iossa, A. Pannaccione, A. Fresi, E. Ficker, and L. Annunziato. 1997. “Regulation of the Human Ether-a-Gogo Related Gene (HERG) K+ Channels by Reactive Oxygen Species.” Proceedings of the National Academy of Sciences of Sciences 94(21): 11698–11703. doi:10.1073/pnas.94.21.11698.
   PubMed Web of Science ®Google Scholar
• Tsushima, R. G., A. D. Wickenden, R. A. Bouchard, G. Y. Oudit, P. P. Liu, and P. H. Backx. 1999. “Modulation of Iron Uptake in Heart by L-Type Ca2+ Channel Modifiers: Possible Implications in Iron Overload.” Circulation Research 84(11): 1302–1309. doi:10.1161/01.RES.84.11.1302.
   PubMed Web of Science ®Google Scholar
• Veranth, J. M., E. G. Kaser, M. M. Veranth, M. Koch, and G. S. Yost. 2007. “Cytokine Responses of Human Lung Cells (BEAS-2B) Treated with Micron-Sized and Nanoparticles of Metal Oxides Compared to Soil Dusts.” Particle and Fibre Toxicology 4(1): 2. doi:10.1186/1743-8977-4-2.
   PubMedGoogle Scholar
• Winegar, R. D., R. Kelly, and J. B. Lansman. 1991. “Block of Current through Single Calcium Channels by Fe, Co, and Ni. Location of the Transition Metal Binding Site in the Pore.” The Journal of General Physiology 97(2): 351–367. doi:10.1085/jgp.97.2.351.
   PubMed Web of Science ®Google Scholar
• Zhang, A. S., and C. A. Enns. 2009. “Molecular Mechanisms of Normal Iron Homeostasis.” Hematology 2009: 207–214. doi:10.1182/asheducation-2009.1.207.
   Google Scholar
• Zhou, Z., Q. Gong, B. Ye, Z. Fan, J.C. Makielski, G. A. Robertson, and C. T. January. 1998. “Properties of HERG Channels Stably Expressed in HEK 293 Cells Studied at Physiological Temperature.” Biophysical Journal 74(1): 230–241. doi:10.1016/S0006-3495(98)77782-3.
   PubMed Web of Science ®Google Scholar